TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis
Open accessAbstract
Non-bilaterian phyla represent key lineages for exploring the evolutionary history of early animals. However, despite an increasing number of sequenced genomes from early-branching metazoans, efficient and reproducible methodologies for analysis of gene function remain a major challenge. Here we report the utilization of the TALEN and CRISPR/Cas9 systems to induce targeted mutations and homologous recombination-mediated transgenesis in the sea anemone Nematostella vectensis. We also present a new method to isolate genetically modified animals using engineered selection cassettes introduced by homologous recombination. Taken together, these methods will permit sophisticated gain- and loss-of-function analyses in Nematostella and perhaps other early metazoan species that allow for zygotic injection.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
0 of 9 cited sources checked · 0 supported · 0 flagged
- Findingown data
Mutagenesis at the expected NvFP-7R site was confirmed in each of three mosaic 12-tentacle polyps analysed.
“We confirmed mutagenesis of the expected site in NvFP-7R in each of three mosaic 12-tentacle polyps analysed (Fig. 4c).”
Quote in the paperSubstantial claim - Findingown data
Five candidate Nematostella HSP70 coding genes were found by BLAST search of the Nematostella genome using zebrafish HSP70 as the query.
“We identified five potential Nematostella HSP70 coding genes using a BLAST search against the Nematostella genome (Joint Genome Institute) and zebrafish HSP70 as a query.”
Quote in the paperSubstantial claim - Findingown data
After CRISPR/Cas9-mediated homologous recombination, NvFP-7R::eGFP was expressed at ectopic positions around the oral pole.
“Intriguingly, NvFP-7R::eGFP expression was once again detected at ectopic positions around the oral pole (Fig. 4d), similar to the effect we observed following TALEN-mediated homologous recombination at a different position in exon 2 (Supplementary Fig. 5).”
Quote in the paperSubstantial claim - Findingown data
Polyp #1 showed substitution of NvFP-7R by NvFP-7R::eGFP in one domain.
“Polyp #1 displays a substitution of NvFP-7R by NvFP-7R::eGFP in one domain, while polyp #2 shows two domains of NvFP-7R::eGFP expression (white arrowheads).”
Quote in the paperNot a substantial claim - Findingown data
NvFP-7R is not needed for normal development or homeostasis of Nematostella under laboratory conditions.
“Together, these results suggest that NvFP-7R is not required for normal development or homeostasis of Nematostella under laboratory conditions.”
Quote in the paperSubstantial claim
- Findingown data
The hs-eGFP cassette integrated at the expected TALEN-exon2 target site.
“Amplification and sequencing of the DNA regions flanking the insertion confirmed that genomic integration occurred at the expected TALEN-exon2 target site (Fig. 3d).”
Quote in the paperSubstantial claim - Findingown data
Co-injection of nls-eGFP-2A-Cas9 mRNA, gRNA-Exon2 and the NvFP-7R::eGFP-MHC1-mCherry plasmid produced mosaic mCherry expression in 16.8% of primary polyps (n=434).
“Following co-injection of nls-eGPF-2A-Cas9 mRNA, gRNA-Exon2 and the NvFP-7R::eGFP-MHC1-mCherry plasmid into Nematostella eggs, 16.8% of primary polyps exhibited mosaic expression of mCherry (n ¼ 434).”
Quote in the paperSubstantial claim - Findingown data
Integration of the cassette at the expected target site was molecularly confirmed in two primary polyps after Cas9 mRNA injection.
“We molecularly confirmed the integration of the cassette at the expected target site in two primary polyps (Supplementary Fig. 6d).”
Quote in the paperSubstantial claim - Findingown data
The Nematostella HSP70 promoter drove strong eGFP expression in injected embryos after 30 min at 37 °C.
“Confirming its function, this promoter induced robust expression of eGFP in injected embryos that were incubated for 30 min at 37 °C (Fig. 3b).”
Quote in the paperSubstantial claim - Findingown data
In independent spawnings, 1/20 and 1/8 red-less adults showed germline transmission of the hs-eGFP cassette.
“In independent spawning of the same animals, 1/20 and 1/8 red-less adults exhibited germline transmission of the hs-eGFP selection cassette.”
Quote in the paperSubstantial claim - Findingreasoning
eGFP expression was stronger in F0 injected embryos than in F1 progeny.
“Notice that the expression level of eGFP in the F0 injected-embryos is stronger than that observed in the F1 progeny.”
Quote in the paperNot a substantial claim - Findingown data
At 6-8 hours after heat shock, the hs1 promoter drove strong eGFP expression.
“After 6-8 h post heat-shock treatment, the hs1 and hs2 promoters showed a strong and weak induction of eGFP expression, respectively.”
Quote in the paperSubstantial claim - Findingown data
At 6-8 hours after heat shock, the hs2 promoter drove weak eGFP expression.
“After 6-8 h post heat-shock treatment, the hs1 and hs2 promoters showed a strong and weak induction of eGFP expression, respectively.”
Quote in the paperNot a substantial claim - Findingown data
F1 embryos from red-less females co-injected with NvFP-7R-TALENs and the hs-eGFP donor vector included eGFP-positive embryos.
“Three F1 embryos spawned by red-less females co-injected with NvFP-7R-TALENs and the hs-eGFP donor vector.Yellow arrowhead indicates a representative F1 eGFP-positive embryo.”
Quote in the paperSubstantial claim - Findingown data
In that polyp, only one domain with normal NvFP-7R expression remained.
“Only one domain displaying normal expression of NvFP-7R is maintained in this polyp (white arrow).”
Quote in the paperNot a substantial claim - Findingown data
Mutations induced by gRNA-NvFP-7R Exon2/Cas9 were recovered from a single polyp with mosaic NvFP-7R expression.
“gRNA-NvFP-7R Exon2/Cas9-induced mutations recovered from a single polyp that exhibited mosaic expression of NvFP-7R.The back line indicates the target site of gRNA-NvFP-7R Exon2 with its PAM sequence.”
Quote in the paperNot a substantial claim- Rests on an assumption: Mutations recovered from injected Nematostella were caused by the injected TALENs or CRISPR/Cas9 rather than by spontaneous mutations or other factors.
- Findingown data
In an in vitro cleavage assay with recombinant Cas9 and gRNAs, both gRNA/Cas9 complexes produced the expected DNA fragments.
“In vitro DNA cleavage assay using recombinant Cas9 with gRNAs.Negative controls are the linearized plasmid alone or with Cas9 protein.Both gRNA/Cas9 complexes generated the expected DNA fragments (black arrowheads).”
Quote in the paperSubstantial claim - Findingown data
An F1 transgenic polyp showed replacement of NvFP-7R by the eGFP fusion cassette in all cells that express NvFP-7R.
“A F1 transgenic polyp exhibiting a replacement of NvFP-7R by the eGFP fusion cassette in all NvFP-7R-expressing cells.Scale bar, 1 mm.”
Quote in the paperSubstantial claim - Findingown data
Mutations in NvFP-7R induced by TALENs were recovered from an F0 animal with the red-less phenotype.
“Molecular characterization of NvFP-7R-TALEN-induced mutations recovered from a phenotypically Red-less F0 animal.”
Quote in the paperSubstantial claim- Rests on an assumption: Mutations recovered from injected Nematostella were caused by the injected TALENs or CRISPR/Cas9 rather than by spontaneous mutations or other factors.
- Findingown data
Both gRNA-Cas9 complexes cleaved their corresponding target sites in vitro.
“Both gRNA-Cas9 complexes produced the expected DNA fragments from a linearized plasmid, indicating that they successfully cleaved their corresponding target sites (Fig. 4b).”
Quote in the paperSubstantial claim - Findingown data
In a representative eGFP/mCherry-positive animal co-injected with TALENs and the NvFP-7R::eGFP-MHC-mCherry donor plasmid, a large clone of mCherry-positive cells also showed replacement of NvFP-7R by eGFP.
“Confocal image of a representative eGFP/mCherry-positive animal co-injected with TALENs and the NvFP-7R::eGFP-MHC-mCherry donor plasmid.Notice that the large clone of mCherry-positive cells (white arrowhead) also exhibits a replacement of NvFP-7R by eGFP (yellow arrowhead).”
Quote in the paperSubstantial claim - Findingown data
Injection of the gRNA-Exon2/Cas9 complex into unfertilized eggs produced mosaic red fluorescent protein expression in 10% of adult polyps (n=532).
“Strikingly, 10% of the resulting adult polyps exhibited mosaic red fluorescent protein expression (n ¼ 532; Supplementary Table 3).”
Quote in the paperSubstantial claim - Findingown data
The hs-eGFP selection cassette was transmitted through the germline to F1 progeny after heat shock.
“After a 30-min heat shock at 37 °C, we observed numerous eGFP-positive embryos in the F1 progeny, demonstrating germline transmission of the selection cassette (Fig. 3c).”
Quote in the paperSubstantial claim - Findingreasoning
mCherry-positive clones were generally smaller after Cas9 mRNA injection than after recombinant Cas9 protein injection.
“Although the frequency of mCherry-positive polyps was higher after the injection of Cas9 mRNA, it is noteworthy that the sizes of the mCherry-positive clones were generally smaller than those recovered in recombinant Cas9 protein-injected animals.”
Quote in the paperNot a substantial claim - Findingown data
Polyp #1 also showed ectopic expression of NvFP-7R::eGFP.
“Polyp #1 also exhibits ectopic expression of NvFP-7R::eGFP (yellow arrowhead).”
Quote in the paperNot a substantial claim - Interpretationreasoning
Integrated selection cassettes allow rapid isolation of somatic and germline mutations using visible markers.
“This approach, which should be widely applicable, allows for the rapid isolation of both somatic and germline mutations based on visible markers.”
Quote in the paperSubstantial claim - Interpretationreasoning
These methods will enable sophisticated gain- and loss-of-function analyses in Nematostella and perhaps other early metazoan species that permit zygotic injection.
“Taken together, these methods will permit sophisticated gain-and loss-of-function analyses in Nematostella and perhaps other early metazoan species that allow for zygotic injection.”
Quote in the paperSubstantial claim - Interpretationown data
CRISPR/Cas9 mediates editing of NvFP-7R.
“Figure 4 | CRISPR/Cas9-mediated editing of NvFP-7R.”
Quote in the paperSubstantial claim - Premisecitation
NvFP-7R encodes a red fluorescent protein specifically expressed in the oral pole of adult polyps.
“We previously reported that NvFP-7R encodes a red fluorescent protein that is specifically expressed in the oral pole of adult polyps 17 (Fig. 1a).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17] Ikmi, A. & Gibson, M. C. Identification and in vivo characterization of NvFP-7R, a developmentally regulated red fluorescent protein of Nematostella vectensis. PLoS ONE 5, e11807 (2010). source
Not checked in the free run.
- Interpretationown data
TALENs can tolerate two mismatches in vivo.
“Consistent with a previous report 19 , this suggests that TALENs can tolerate two mismatches in vivo.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [19] Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833–838 (2013). source
Not checked in the free run.
- Interpretationown data
Cassette-mediated conversion of NvFP-7R into NvFP-7R::eGFP allows efficient isolation of precise genomic integration events.
“As a visible readout of transgene insertion, cassette-mediated conversion of NvFP-7R into NvFP-7R::eGFP allows for efficient isolation of precise genomic integration events (Fig. 4e).”
Quote in the paperSubstantial claim - Premisecitation
The MHC1 promoter drives expression in muscle cells.
“The first selection marker comprised the coding sequence for mCherry under the control of the myosin heavy chain1 (MHC1) promoter, which drives expression in muscle cells 16 (MHC1-mCherry).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [16] Renfer, E., Amon-Hassenzahl, A., Steinmetz, P. R. & Technau, U. A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc. Natl Acad. Sci. USA 107, 104–108 (2010). source
Not checked in the free run.
- Interpretationown data
TALENs mediate homologous recombination at the NvFP-7R locus when using the hs-eGFP donor vector.
“Figure 3 | TALEN-mediated homologous recombination at the NvFP-7R locus using the hs-eGFPdonor vector.”
Quote in the paperSubstantial claim - Interpretationreasoning
TALEN tolerance of two mismatches could help disrupt multiple members of a gene family simultaneously to reveal phenotypes masked by functional redundancy.
“This could be advantageous for simultaneous disruption of multiple members of a gene family to examine phenotypes obscured by functional redundancy.”
Quote in the paperSubstantial claim - Interpretationown data
Insertion of the cassette interferes with how the NvFP-7R locus is transcriptionally regulated.
“This reinforces the hypothesis that cassette integration disrupts transcriptional regulation of the NvFP-7R locus.”
Quote in the paperSubstantial claim - Interpretationown data
These methods open the door to a wide range of functional manipulations in vivo.
“While additional analysis would be required to characterize potential off-target effects of the CRISPR/Cas9 system, these methods open the door to a wide range of functional manipulations in vivo.”
Quote in the paperNot a substantial claim - Interpretationreasoning
The genetic tools described in this study enable functional investigation of the ancestral molecular toolkit involved in early animal body plan diversification.
“While sequencing projects have produced an abundance of information about the genomic foundations of animal evolution 32 , emerging genetic tools of the kind described herein now permit functional interrogation of the ancestral molecular toolkit employed in the diversification of early animal body plans.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [32] Richter, D. J. & King, N. The genomic and cellular foundations of animal origins. Annu. Rev. Genet. 47, 509–537 (2013). source
Not checked in the free run.
- Premisecitation
The CRISPR/Cas9 system is a more flexible and cost-effective genome-editing method based on RNA-guided endonuclease activity than TALENs.
“As an alternative, the CRISPR/Cas9 system is a more flexible and cost-effective method for genome editing based on RNA-guided endonuclease activity 20 .”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [20] Hsu, P. D., Lander, E. S. & Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262–1278 (2014). source
Not checked in the free run.
- Interpretationreasoning
Using this general strategy, any target sequence in the Nematostella genome should be mutable, taggable or otherwise modifiable.
“Using this general strategy, it should be possible to mutate, tag or otherwise modify any target sequence in the Nematostella genome.”
Quote in the paperSubstantial claim - Premiseown data
At the 12-tentacle stage (about 1.5 months), Nematostella expresses NvFP-7R specifically at the oral pole.
“At the 12-tentacle stage (B1.5 months), Nematostella specifically express NvFP-7R at the oral pole (inset box).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [17] Ikmi, A. & Gibson, M. C. Identification and in vivo characterization of NvFP-7R, a developmentally regulated red fluorescent protein of Nematostella vectensis. PLoS ONE 5, e11807 (2010). source
Not checked in the free run.
- Interpretationown data
A visible marker can substantially raise the chance of finding founder animals.
“Importantly, they also illustrate how the presence of a visible marker can significantly increase the probability of identifying founder animals.”
Quote in the paperSubstantial claim - Interpretationreasoning
The stronger eGFP expression in F0 embryos is most likely explained by F1 embryos carrying a single copy of hs-eGFP.
“This is most likely due to the presence of a single copy of hs-eGFP in F1 embryos.”
Quote in the paperNot a substantial claim - Interpretationown data
Analysis of two independent loci shows that the CRISPR/Cas9 system can induce and select for site-specific DNA modifications in Nematostella.
“On the basis of the analysis of two independent loci, our results demonstrate a specific methodology by which the CRISPR/Cas9 system can be used to induce and select for site-specific DNA modifications in Nematostella.”
Quote in the paperSubstantial claim - Interpretationown data
TALENs mediate homologous recombination at the NvFP-7R locus.
“Figure 2 | TALEN-mediated homologous recombination at the NvFP-7R locus.”
Quote in the paperSubstantial claim - Interpretationown data
The off-target results suggest a minimal guideline for avoiding undesired TALEN cleavage in Nematostella.
“Further, it also suggests a minimal guideline for avoiding undesired off-target cleavage events in Nematostella.”
Quote in the paperSubstantial claim
- May combine two claims. 9
- Classified as probably not a substantial claim. 4
May combine two claims.
Findingown datahs-eGFP-injected embryos showed strong eGFP expression after a 30-minute heat shock at 37 °C, but not when kept at room temperature.
“hs-eGFP-injected embryos show strong expression of eGFP after heat-shock treatment (30 min at 37 °C), but not those incubated at room temperature.Scale bar, 600 mm.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataPolyp #2 showed two domains of NvFP-7R::eGFP expression.
“Polyp #1 displays a substitution of NvFP-7R by NvFP-7R::eGFP in one domain, while polyp #2 shows two domains of NvFP-7R::eGFP expression (white arrowheads).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataCRISPR/Cas9-mediated homologous recombination with the NvFP-7R::eGFP-MHC1-mCherry cassette gave mCherry expression in 6.4% of surviving 12-tentacle polyps, and 18.7% of those were also NvFP-7R::eGFP-positive, consistent with correct integration.
“Here, 6.4% of surviving 12-tentacle polyps displayed the expression of mCherry, and 18.7% of these animals were also NvFP-7R::eGFP-positive, consistent with integration at the correct genomic site (Supplementary Table 2).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataTALEN-induced mutations are transmitted through the germline of injected F0 females; transmission was seen in 50% of red-less F0 females, with mutation frequency up to 80%.
“In contrast, we documented germline transmission of induced mutations in unfertilized eggs from 50% of red-less F0 females (n ¼ 12; Supplementary Fig. 4a,b), with a frequency of NvFP-7R mutation up to 80% (Supplementary Fig. 4c).”
- Also stated in: § Germline transmission of TALEN-induced mutations. · boosted
“These results demonstrate efficient TALEN-induced mutations of the Nematostella germline.”
Quote in the paperSubstantial claim- Also stated in: § Germline transmission of TALEN-induced mutations. · boosted
May combine two claims.
Findingown dataTALEN-mediated homologous recombination works in both somatic and germline cells and can insert exogenous sequences at target sites in Nematostella.
“Taken together, these results show that TALENmediated homologous recombination functions in both somatic and germline cells and can be used to introduce exogenous sequences into target sites in the Nematostella genome.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataTALENs produce targeted DNA lesions in the Nematostella genome and often disrupt both alleles in many somatic cells.
“Collectively, these findings demonstrate that TALENs can efficiently generate targeted lesions in the Nematostella genome, frequently disrupting both alleles in a large number of somatic cells.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataIn red-less animals with strong NvFP-7R disruption, the NvFP5 off-target site with two mismatches was mutated in all three analysed animals, while the NvFP4 site with six mismatches was not mutated.
“Intriguingly, the NvFP5 site containing two mismatches was mutated in all analysed animals (n ¼ 3), but we did not detect any mutations in the NvFP4 site, which includes six mismatches (Supplementary Fig. 1b).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataCo-injection of the Nvanthox6 donor vector with gRNA-hox6/Cas9 protein complex gave mCherry-positive polyps in 4.5% of recovered polyps (n=440), and disruption of Nvanthox6 exon 1 by the MHC1-mCherry cassette was molecularly validated in a pool of five F0 primary polyps.
“Following coinjection of this donor vector with gRNA-hox6/Cas9 protein complex, 4.5% of recovered polyps were mCherry-positive (n ¼ 440), and we molecularly validated the disruption of Nvanthox6 exon 1 by the MHC1-mCherry cassette in a pool of five F0 primary polyps (Supplementary Fig. 7b).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataTALEN-injected animals displayed three NvFP-7R expression phenotypes: normal, mosaic with loss in some domains, and red-less with no detectable expression; the phenotype percentages were based on n=312.
“TALEN-injected animals exhibit three phenotypes of NvFP-7R expression.The first phenotype appears normal (wild type).The second phenotype (mosaic) displays loss of NvFP-7R expression in one or more domains and normal expression in others (white arrowheads).The third phenotype lacks any detectable expression of NvFP-7R (red-less).The percentages of each phenotype are indicated (n ¼ 312).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataInjection of nls-eGFP-2A-Cas9 mRNA into unfertilized eggs produced nuclear eGFP at 4 h post fertilization, with expression rising 30-fold and plateauing around 19 h post fertilization.
“After injection of the nls-eGPF-2A-Cas9 mRNA (250 ng ml À 1 ) into unfertilized eggs, we detected nuclear eGFP at 4 h post fertilization (h.p.f.) and its expression level increased 30-fold reaching a plateau around 19 h.p.f.(Supplementary Fig. 6b,c; Supplementary Movie 3).”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
InterpretationreasoningThis approach removes concern about position effects and multicopy insertions that can occur with traditional meganuclease-mediated transgenesis.
“Besides the ease of visual screening, this approach eliminates concern over position effects and multicopy insertions that could occur in the traditional meganuclease-mediated transgenesis method.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationTALEN-mediated homologous recombination has been used to insert exogenous DNA into the genomes of Drosophila, zebrafish and mouse.
“In a limited number of cases, TALEN-mediated homologous recombination has been used to insert exogenous DNA into the genomes of Drosophila 11 , zebrafish 8 and mouse 18 .”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [11] Katsuyama, T. et al. An efficient strategy for TALEN-mediated genome engineering in Drosophila. Nucleic Acids Res. 41, e163 (2013). source
Not checked in the free run.
- cites [8] Zu, Y. et al. TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat. Methods. 10, 329–331 (2013). source
Not checked in the free run.
- cites [18] Sommer, D. et al. Efficient genome engineering by targeted homologous recombination in mouse embryos using transcription activator-like effector nucleases. Nat. Commun. 5, 3045 (2014). source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
InterpretationreasoningThe same experimental approach has the potential to work in any nonbilaterian system with accessible eggs.
“Following from this proof of principle, the same experimental approach has the potential to succeed in any nonbilaterian system with accessible eggs.”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Efficient and reproducible methods for studying gene function in early-branching metazoans are still a major challenge.
“However, despite an increasing number of sequenced genomes from early-branching metazoans, efficient and reproducible methodologies for analysis of gene function remain a major challenge.”
The paper relies on this without support.
In non-bilaterian animals, experimental tools are a limiting factor for functional studies, so available approaches are restricted to partial and imprecise gene disruption.
“Among the non-bilaterians (Cnidaria, Placozoa, Porifera and Ctenophora), experimental tools remain a limiting factor for functional studies, restricting the available approaches to partial and imprecise gene disruption via morpholinos, RNA interference, pharmacological inhibitor experiments and correlative analyses of gene expression patterns.”
The paper relies on this without support.
Constructing functional TALEN pairs can be difficult and slow.
“The construction of functional TALEN pairs can be challenging and time-consuming.”
The paper relies on this without support.
Mutations recovered from injected Nematostella were caused by the injected TALENs or CRISPR/Cas9 rather than by spontaneous mutations or other factors.
“Molecular characterization of NvFP-7R-TALEN-induced mutations recovered from a phenotypically Red-less F0 animal.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Genome-editing technologies such as TALENs and CRISPR/Cas9 are now available in some cnidarian model systems.
“In addition to well-established transient knockdown strategies (dsRNA, morpholinos), genome-editing technologies like TALENs or CRISPR/Cas9 are now available in some cnidarian model systems [105,106].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [105]
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
Development and Applications of CRISPR-Cas9 for Genome Engineering
Hsu, P. D., Lander, E. S., & Zhang, F. (2014) · Cell · doi:10.1016/j.cell.2014.05.010 · Cited by 5,762 · see citing works
Genome-scale CRISPR-Cas9 knockout screening in human cells
Shalem, O., Sanjana, N. E., Hartenian, E., Shi, X., Scott, D. A., Mikkelsen, T. S., Heckl, D., Ebert, B. L., Root, D. E., Doench, J. G., et al. (2014) · Science · doi:10.1126/science.1247005 · Cited by 5,234 · see citing works
Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.04.025 · Cited by 3,495 · see citing works
Efficient genome editing in zebrafish using a CRISPR-Cas system
Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J.-R. J., & Joung, J. K. (2013) · Nature Biotechnology · doi:10.1038/nbt.2501 · Cited by 2,937 · see citing works
Genetic screens in human cells using the CRISPR-Cas9 system
Wang, T., Wei, J. J., Sabatini, D. M., & Lander, E. S. (2014) · Science · doi:10.1126/science.1246981 · Cited by 2,856 · see citing works
Breaking the Code of DNA Binding Specificity of TAL-Type III Effectors
Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., & Bonas, U. (2009) · Science · doi:10.1126/science.1178811 · Cited by 2,707 · see citing works
Čermák, T., Doyle, E., Christian, M. L., Wang, L., Zhang, Y., Schmidt, C. L., Baller, J. A., Somia, N. V., Bogdanove, A. J., & Voytas, D. F. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr218 · Cited by 2,034 · see citing works
A Simple Cipher Governs DNA Recognition by TAL Effectors
Moscou, M., & Bogdanove, A. J. (2009) · Science · doi:10.1126/science.1178817 · Cited by 1,992 · see citing works
RNA-guided genetic silencing systems in bacteria and archaea
Wiedenheft, B., Sternberg, S. H., & Doudna, J. A. (2012) · Nature · doi:10.1038/nature10886 · Cited by 1,851 · see citing works
Mali, P., Aach, J., Stranges, P. B., Esvelt, K. M., Moosburner, M., Kosuri, S., Yang, L., & Church, G. M. (2013) · Nature Biotechnology · doi:10.1038/nbt.2675 · Cited by 1,752 · see citing works
Computer Control of Microscopes Using µManager
Edelstein, A., Amodaj, N., Hoover, K., Vale, R. D., & Stuurman, N. (2010) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb1420s92 · Cited by 1,678 · see citing works
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
Kim, J. H., Lee, S. R., Li, L.-H., Park, H., Park, J.-H., Lee, K. Y., Kim, M., Shin, B. A., & Choi, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018556 · Cited by 1,340 · see citing works
Genetic engineering of human pluripotent cells using TALE nucleases
Hockemeyer, D. F., Wang, H., Kiani, S., Lai, C. S., Gao, Q., Cassady, J. P., Cost, G. J., Zhang, L., Santiago, Y., Miller, J. C., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1927 · Cited by 1,129 · see citing works
The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
Heritable genome editing in C. elegans via a CRISPR-Cas9 system
Friedland, A. E., Tzur, Y. B., Esvelt, K. M., Colaiácovo, M. P., Church, G. M., & Calarco, J. A. (2013) · Nature Methods · doi:10.1038/nmeth.2532 · Cited by 899 · see citing works
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
The ctenophore genome and the evolutionary origins of neural systems
Moroz, L. L., Kocot, K. M., Citarella, M. R., Dosung, S., Norekian, T. P., Povolotskaya, I. S., Grigorenko, A. P., Dailey, C., Berezikov, E., Buckley, K. M., et al. (2014) · Nature · doi:10.1038/nature13400 · Cited by 716 · see citing works
The Genome of the Ctenophore <i>Mnemiopsis leidyi</i> and Its Implications for Cell Type Evolution
Ryan, J. F., Pang, K., Schnitzler, C. E., Nguyen, A.-D., Moreland, R. T., Simmons, D. K., Koch, B. J., Francis, W. R., Havlak, P., Program, N. C. S., et al. (2013) · Science · doi:10.1126/science.1242592 · Cited by 702 · see citing works
TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction
Doyle, E., Booher, N. J., Standage, D., Voytas, D. F., Brendel, V., VanDyk, J. K., & Bogdanove, A. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks608 · Cited by 587 · see citing works
Ryan, M. D., King, A. M. Q., & Thomas, G. P. (1991) · Journal of General Virology · doi:10.1099/0022-1317-72-11-2727 · Cited by 496 · see citing works
Dahlem, T. J., Hoshijima, K., Jurynec, M. J., Gunther, D., Starker, C. G., Locke, A. S., Weis, A. M., Voytas, D. F., & Grunwald, D. J. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002861 · Cited by 453 · see citing works
TALEN-mediated precise genome modification by homologous recombination in zebrafish
Zu, Y., Tong, X., Wang, Z., Liu, D., Pan, R., Li, Z., Hu, Y., Luo, Z., Huang, P., Wu, Q., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2374 · Cited by 328 · see citing works
An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation
Wikramanayake, A. H., Hong, M., Lee, P. N., Pang, K., Byrum, C. A., Bince, J. M., Xu, R., & Martindale, M. Q. (2003) · Nature · doi:10.1038/nature02113 · Cited by 324 · see citing works
Evolutionary crossroads in developmental biology: Cnidaria
Technau, U., & Steele, R. E. (2011) · Development · doi:10.1242/dev.048959 · Cited by 274 · see citing works
Smith, C. L., Varoqueaux, F., Kittelmann, M., Azzam, R. N., Cooper, B., Winters, C. A., Eitel, M., Fasshauer, D., & Reese, T. S. (2014) · Current Biology · doi:10.1016/j.cub.2014.05.046 · Cited by 254 · see citing works
Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa)
Fritzenwanker, J. H., & Technau, U. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0214-7 · Cited by 218 · see citing works
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
Evolutionary conservation of the eumetazoan gene regulatory landscapePreprint
Schwaiger, M., Schönauer, A., Rendeiro, A. F., Pribitzer, C., Schauer, A., Gilles, A. F., Schinko, J. B., Renfer, E., Fredman, D., & Technau, U. (2014) · Genome Research · doi:10.1101/gr.162529.113 · Cited by 188 · see citing works
The Bilaterian Head Patterning Gene six3/6 Controls Aboral Domain Development in a Cnidarian
Sinigaglia, C., Busengdal, H., Leclère, L., Technau, U., & Rentzsch, F. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001488 · Cited by 169 · see citing works
FGF signalling controls formation of the apical sensory organ in the cnidarianNematostella vectensis
Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B., & Technau, U. (2008) · Development · doi:10.1242/dev.020784 · Cited by 166 · see citing works
A muscle-specific transgenic reporter line of the sea anemone, <i>Nematostella vectensis</i>
Renfer, E., Amon-Hassenzahl, A., Steinmetz, P. R. H., & Technau, U. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909148107 · Cited by 164 · see citing works
Röttinger, E., Dahlin, P., & Martindale, M. Q. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003164 · Cited by 140 · see citing works
Leininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136 · see citing works
Evolutionary crossroads in developmental biology
Patel, N. H. (2012) · Development · doi:10.1242/dev.085464 · Cited by 74 · see citing works
An efficient strategy for TALEN-mediated genome engineering in Drosophila
Katsuyama, T., Akmammedov, A., Seimiya, M., Hess, S. C., Sievers, C. M., & Paro, R. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt638 · Cited by 58 · see citing works
Mechanisms of tentacle morphogenesis in the sea anemone Nematostella vectensis
Fritz, A. E., Ikmi, A., Seidel, C. W., Paulson, A., & Gibson, M. C. (2013) · Development · doi:10.1242/dev.088260 · Cited by 45 · see citing works
Self-citationSommer, D. D., Peters, A. E., Wirtz, T., Mai, M., Ackermann, J. P., Thabet, Y., Schmidt, J., Weighardt, H., Wunderlich, F. T., Degen, J., et al. (2014) · Nature Communications · doi:10.1038/ncomms4045 · Cited by 44 · see citing works
Ikmi, A., & Gibson, M. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011807 · Cited by 26 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes
Liang, P., Xu, Y., Zhang, X., Ding, C., Huang, R., Zhang, Z., Lv, J., Xie, X., Chen, Y., Li, Y., et al. (2015) · Protein & Cell · doi:10.1007/s13238-015-0153-5 · Cited by 1,135 · see citing works
Review of CRISPR/Cas9 sgRNA Design Tools
Cui, Y., Xu, J., Cheng, M., Liao, X., & Peng, S. (2018) · Interdisciplinary Sciences Computational Life Sciences · doi:10.1007/s12539-018-0298-z · Cited by 243 · see citing works
Russell, J. J., Theriot, J. A., Sood, P., Marshall, W. F., Landweber, L. F., Fritz‐Laylin, L. K., Polka, J., Oliferenko, S., Gerbich, T. M., Gladfelter, A. S., et al. (2017) · BMC Biology · doi:10.1186/s12915-017-0391-5 · Cited by 224 · see citing works
Self-citationInsert, remove or replace: A highly advanced genome editing system using CRISPR/Cas9
Ceasar, S. A., Rajan, V., Prykhozhij, S. V., Berman, J. N., & Savarimuthu Ignacimuthu, S. J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.06.009 · Cited by 185 · see citing works
CRISPR/Cas9-mediated genome editing in a reef-building coral
Cleves, P. A., Strader, M. E., Bay, L. K., Pringle, J. R., & Matz, M. V. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722151115 · Cited by 154 · see citing works
Layden, M. J., Rentzsch, F., & Röttinger, É. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.222 · Cited by 148 · see citing works
An axial Hox code controls tissue segmentation and body patterning in Nematostella vectensis
He, S., Viso, F. D., Chen, C., Ikmi, A., Kroesen, A. E., & Gibson, M. C. (2018) · Science · doi:10.1126/science.aar8384 · Cited by 148 · see citing works
Self-citationBack to the Basics: Cnidarians Start to Fire
Bosch, T. C. G., Klimovich, A., Domazet-Lošo, T., Gründer, S., Holstein, T. W., Jékely, G., Miller, D. J., Murillo-Rincon, A. P., Rentzsch, F., Richards, G. S., et al. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2016.11.005 · Cited by 144 · see citing works
Pre-bilaterian origin of the blastoporal axial organizer
Kraus, Y., Aman, A., Technau, U., & Genikhovich, G. (2016) · Nature Communications · doi:10.1038/ncomms11694 · Cited by 143 · see citing works
The Molecular Language of the Cnidarian–Dinoflagellate Symbiosis
Rosset, S. L., Oakley, C. A., Ferrier‐Pagès, C., Suggett, D. J., Weis, V. M., & Davy, S. K. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.08.005 · Cited by 132 · see citing works
CRISPR / C as9‐mediated genome modification in the mollusc, Crepidula fornicata
Perry, K. J., & Henry, J. J. (2014) · genesis · doi:10.1002/dvg.22843 · Cited by 104 · see citing works
Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration
Leclère, L., & Röttinger, É. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00157 · Cited by 100 · see citing works
The cellular and molecular basis of cnidarian neurogenesis
Rentzsch, F., Layden, M. J., & Manuel, M. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.257 · Cited by 95 · see citing works
Brennan, J. J., Messerschmidt, J. L., Williams, L. M., Matthews, B. J., Reynoso, M., & Gilmore, T. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711530114 · Cited by 93 · see citing works
Amiel, A., Johnston, H. T., Nedoncelle, K., Warner, J. F., Ferreira, S., & Röttinger, É. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226100 · Cited by 80 · see citing works
Tournière, O., Dolan, D., Richards, G. S., Sunagar, K., Columbus-Shenkar, Y. Y., Moran, Y., & Rentzsch, F. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.031 · Cited by 74 · see citing works
Square, T. A., Romášek, M., Jandzík, D., Cattell, M. V., Klymkowsky, M. W., & Medeiros, D. M. (2015) · Development · doi:10.1242/dev.125609 · Cited by 74 · see citing works
β-Catenin–dependent mechanotransduction dates back to the common ancestor of Cnidaria and Bilateria
Pukhlyakova, E., Aman, A. J., Elsayad, K., & Technau, U. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713682115 · Cited by 74 · see citing works
Marine metagenomics as a source for bioprospecting
Kodzius, R., & Gojobori, T. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.07.001 · Cited by 73 · see citing works
Sunagar, K., Columbus-Shenkar, Y. Y., Fridrich, A., Gutkovich, N., Aharoni, R., & Moran, Y. (2018) · BMC Biology · doi:10.1186/s12915-018-0578-4 · Cited by 71 · see citing works
Emerging Sponge Models of Animal-Microbe Symbioses
Pita, L., Fraune, S., & Hentschel, U. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02102 · Cited by 70 · see citing works
Induction of Gametogenesis in the Cnidarian Endosymbiosis Model Aiptasia sp.
Grawunder, D., Hambleton, E. A., Bucher, M., Wolfowicz, I., Bechtoldt, N., & Guse, A. (2015) · Scientific Reports · doi:10.1038/srep15677 · Cited by 69 · see citing works
Transcription factor AP2 controls cnidarian germ cell induction
DuBuc, T. Q., Schnitzler, C. E., Chrysostomou, E., McMahon, E. T., Febrimarsa, F., Gahan, J. M., Buggie, T., Gornik, S. G., Hanley, S. A., Barreira, S. N., et al. (2020) · Science · doi:10.1126/science.aay6782 · Cited by 67 · see citing works
Symbiont transmission in marine sponges: reproduction, development, and metamorphosis
Carrier, T. J., Maldonado, M., Schmittmann, L., Pita, L., Bosch, T. C. G., & Hentschel, U. (2022) · BMC Biology · doi:10.1186/s12915-022-01291-6 · Cited by 58 · see citing works
Karabulut, A., He, S., Chen, C., McKinney, S., & Gibson, M. C. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.01.005 · Cited by 58 · see citing works
Self-citationAn adaptable chromosome preparation methodology for use in invertebrate research organisms
Guo, L., Accorsi, A., He, S., Guerrero‐Hernández, C., Sivagnanam, S., McKinney, S., Gibson, M. C., & Alvarado, A. S. (2018) · BMC Biology · doi:10.1186/s12915-018-0497-4 · Cited by 53 · see citing works
Self-citationCRISPR/Cas9-mediated gene knockin in the hydroid Hydractinia symbiolongicarpus
Sanders, S. M., Ma, Z., Hughes, J. M., Riscoe, B. M., Gibson, G. A., Watson, A. M., Flici, H., Uri Frank, A., Schnitzler, C. E., Baxevanis, A. D., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-5032-z · Cited by 52 · see citing works
Muscular hydraulics drive larva-polyp morphogenesis
Stokkermans, A., Chakrabarti, A., Subramanian, K., Wang, L., Yin, S., Moghe, P., Steenbergen, P. J., Mönke, G., Hiiragi, T., Prevedel, R., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.08.065 · Cited by 49 · see citing works
Self-citationNakanishi, N., & Martindale, M. Q. (2018) · eLife · doi:10.7554/elife.39742 · Cited by 48 · see citing works
CRISPR in Animals and Animal Models
Shrock, E. L., & Güell, M. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.07.010 · Cited by 47 · see citing works
Meganuclease-assisted generation of stable transgenics in the sea anemone Nematostella vectensis
Renfer, E., & Technau, U. (2017) · Nature Protocols · doi:10.1038/nprot.2017.075 · Cited by 46 · see citing works
Servetnick, M. D., Steinworth, B. M., Babonis, L. S., Simmons, D., Salinas‐Saavedra, M., & Martindale, M. Q. (2017) · Development · doi:10.1242/dev.145839 · Cited by 45 · see citing works
Feeding-dependent tentacle development in the sea anemone Nematostella vectensis
Ikmi, A., Steenbergen, P. J., Anzo, M., McMullen, M. R., Stokkermans, A., Ellington, L. R., & Gibson, M. C. (2020) · Nature Communications · doi:10.1038/s41467-020-18133-0 · Cited by 42 · see citing works
Self-citationOld questions, new models: unraveling complex organ regeneration with new experimental approaches
Grillo, M., Konstantinides, N., & Averof, M. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.006 · Cited by 40 · see citing works
Diving into marine genomics with CRISPR/Cas9 systems
Momose, T., & Concordet, J. (2016) · Marine Genomics · doi:10.1016/j.margen.2016.10.003 · Cited by 39 · see citing works
Overview of guide RNA design tools for CRISPR-Cas9 genome editing technology
Zhu, L. J. (2015) · Frontiers in Biology · doi:10.1007/s11515-015-1366-y · Cited by 38 · see citing works
Li, J., Wu, S., Zhang, K., Sun, X., Lin, W., Wang, C., & Lin, S. (2024) · Microorganisms · doi:10.3390/microorganisms12010118 · Cited by 37 · see citing works
Kamran, Z., Zellner, K., Kyriazes, H., Kraus, C. M., Reynier, J.-B., & Malamy, J. E. (2017) · BMC Developmental Biology · doi:10.1186/s12861-017-0160-2 · Cited by 37 · see citing works
Salinas‐Saavedra, M., Rock, A. Q., & Martindale, M. Q. (2018) · eLife · doi:10.7554/elife.36740 · Cited by 37 · see citing works
Sex, polyps, and medusae: Determination and maintenance of sex in cnidarians
Siebert, S., & Juliano, C. E. (2016) · Molecular Reproduction and Development · doi:10.1002/mrd.22690 · Cited by 37 · see citing works
Modern genomic tools reveal the structural and cellular diversity of cnidarian nervous systems
Rentzsch, F., Juliano, C. E., & Galliot, B. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.12.004 · Cited by 36 · see citing works
Jones, V. A. S., Bucher, M., Hambleton, E. A., & Guse, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-34773-1 · Cited by 36 · see citing works
Insights into how development and life-history dynamics shape the evolution of venom
Surm, J. M., & Moran, Y. (2021) · EvoDevo · doi:10.1186/s13227-020-00171-w · Cited by 36 · see citing works
Röttinger, É. (2021) · Cells · doi:10.3390/cells10102692 · Cited by 36 · see citing works
Fraune, S., Forêt, S., & Reitzel, A. M. (2016) · Frontiers in Marine Science · doi:10.3389/fmars.2016.00148 · Cited by 35 · see citing works
Recent advances in genomics and transcriptomics of cnidarians
Technau, U., & Schwaiger, M. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.09.007 · Cited by 35 · see citing works
Single-cell atavism reveals an ancient mechanism of cell type diversification in a sea anemone
Babonis, L. S., Enjolras, C., Reft, A., Foster, B. M., Hugosson, F., Ryan, J. F., Daly, M., & Martindale, M. Q. (2023) · Nature Communications · doi:10.1038/s41467-023-36615-9 · Cited by 34 · see citing works
Thiel, D. J., Yáñez-Guerra, L. A., Kieswetter, A., Cole, A. G., Temmerman, L., Technau, U., & Jékely, G. (2023) · eLife · doi:10.7554/elife.90674 · Cited by 32 · see citing works
A population of Vasa2 and Piwi1 expressing cells generates germ cells and neurons in a sea anemone
Miramón-Puértolas, P., Pascual-Carreras, E., & Steinmetz, P. R. H. (2024) · Nature Communications · doi:10.1038/s41467-024-52806-4 · Cited by 32 · see citing works
Genomics and development of Nematostella vectensis and other anthozoans
Rentzsch, F., & Technau, U. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.024 · Cited by 32 · see citing works
Transgenesis in the acoel worm Hofstenia miamia
Ricci, L., & Srivastava, M. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.10.012 · Cited by 30 · see citing works
Staal, J., Driege, Y., Haegman, M., Borghi, A., Hulpiau, P., Lievens, L., Gül, I. S., Sundararaman, S., Gonçalves, A. C., Dhondt, I., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01136 · Cited by 29 · see citing works
Ferrier, D. E. K. (2016) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv056 · Cited by 28 · see citing works
The genetic basis for PRC1 complex diversity emerged early in animal evolution
Gahan, J. M., Rentzsch, F., & Schnitzler, C. E. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2005136117 · Cited by 27 · see citing works
Chen, C., McKinney, S., Ellington, L. R., & Gibson, M. C. (2020) · eLife · doi:10.7554/elife.54573 · Cited by 27 · see citing works
Self-citationAmiel, A., Foucher, K., Ferreira, S., & Röttinger, É. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.31.891804 · Cited by 27 · see citing works
Amiel, A., Johnston, H. T., Chock, T., Dahlin, P., Iglesias, M., Layden, M. J., Röttinger, É., & Martindale, M. Q. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.08.015 · Cited by 26 · see citing works
Aguilar-Camacho, J. M., Foreman, K., Jaimes‐Becerra, A., Aharoni, R., Gründer, S., & Moran, Y. (2023) · Communications Biology · doi:10.1038/s42003-022-04399-1 · Cited by 25 · see citing works
Endogenous tagging of multiple cellular components in the sea anemone Nematostella vectensis
Paix, A., Basu, S., Steenbergen, P. J., Singh, R., Prevedel, R., & Ikmi, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2215958120 · Cited by 24 · see citing works
Self-citationDenner, A., Steger, J., Ries, A., Morozova-Link, E., Ritter, J., Haas, F., Cole, A. G., & Technau, U. (2024) · Science Advances · doi:10.1126/sciadv.ado0424 · Cited by 23 · see citing works
Ozment, E., Tamvacakis, A. N., Zhou, J., Rosiles-Loeza, P. Y., Escobar-Hernández, E. E., Fernández-Valverde, S. L., & Nakanishi, N. (2021) · eLife · doi:10.7554/elife.74336 · Cited by 23 · see citing works
Clonal analysis by tunable CRISPR-mediated excision
Gilles, A. F., Schinko, J. B., Schacht, M. I., Enjolras, C., & Averof, M. (2018) · Development · doi:10.1242/dev.170969 · Cited by 21 · see citing works
Finding genes and pathways that underlie coral adaptation
Selmoni, O. M., Bay, L. K., Expósito‐Alonso, M., & Cleves, P. A. (2024) · Trends in Genetics · doi:10.1016/j.tig.2024.01.003 · Cited by 21 · see citing works
Zang, H., & Nakanishi, N. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00063 · Cited by 20 · see citing works
Spatial transcriptomics reveals a cnidarian segment polarity program in Nematostella vectensis
He, S., Shao, W., Chen, S., Wang, T., & Gibson, M. C. (2023) · Current Biology · doi:10.1016/j.cub.2023.05.044 · Cited by 19 · see citing works
Self-citationGahan, J. M., Kouzel, I. U., Jansen, K. O., Burkhardt, P., & Rentzsch, F. (2022) · Nature Communications · doi:10.1038/s41467-022-28107-z · Cited by 19 · see citing works
β-catenin-driven endomesoderm specification is a Bilateria-specific novelty
Lebedeva, T. S., Boström, J., Kremnyov, S. V., Mörsdorf, D., Niedermoser, I., Genikhovich, E., Hejnol, A., Adameyko, I. I., & Genikhovich, G. (2025) · Nature Communications · doi:10.1038/s41467-025-57109-w · Cited by 18 · see citing works
The Diversity of Muscles and Their Regenerative Potential across Animals
Zullo, L., Bozzo, M., Daya, A., Clemente, A. D., Mancini, F. P., Megighian, A., Nesher, N., Röttinger, É., Shomrat, T., Tiozzo, S., et al. (2020) · Cells · doi:10.3390/cells9091925 · Cited by 17 · see citing works
Comparative genomics and the diversity of life
Dunn, C. W., & Munro, C. (2016) · Zoologica Scripta · doi:10.1111/zsc.12211 · Cited by 17 · see citing works
Extracellular matrix and morphogenesis in cnidarians: a tightly knit relationship
Bergheim, B. G., & Özbek, S. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190021 · Cited by 16 · see citing works
Admoni, Y., Kozlovski, I., Lewandowska, M., & Moran, Y. (2020) · Genes · doi:10.3390/genes11091081 · Cited by 16 · see citing works
Versatile Cell Penetrating Peptide for Multimodal CRISPR Gene Editing in Primary Stem Cells
Graham, J. P., Castro, J. G., Werba, L. C., Amitrano, J., Fardone, L. C., Francis, K. P., Ramamurthi, A., Layden, M. J., McCarthy, H. O., & Gonzalez‐Fernandez, T. (2025) · Advanced Functional Materials · doi:10.1002/adfm.202501532 · Cited by 15 · see citing works
Quiroga-Artigas, G., de Jong, D., & Schnitzler, C. E. (2022) · Open Biology · doi:10.1098/rsob.220120 · Cited by 15 · see citing works
Dynamic remodeling of the interactomes of Nematostella vectensis Hsp70 isoforms under heat shock
Knighton, L. E., Nitika, N., Waller, S. J., Strom, O. R., Wolfgeher, D. J., Reitzel, A. M., & Truman, A. W. (2019) · Journal of Proteomics · doi:10.1016/j.jprot.2019.103416 · Cited by 15 · see citing works
Systemic coordination of whole-body tissue remodeling during local regeneration in sea anemones
Cheung, S., Bredikhin, D., Gerber, T., Steenbergen, P. J., Basu, S., Bailleul, R., Hansen, P., Paix, A., Benton, M. A., Korswagen, H. C., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.11.001 · Cited by 14 · see citing works
Self-citationA genetically tractable non-vertebrate system to study complete camera-type eye regeneration
Accorsi, A., Pardo, B., Ross, E., Corbin, T. J., McClain, M., Weaver, K., Delventhal, K., Gattamraju, A., Morrison, J. A., McKinney, M. C., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-61681-6 · Cited by 14 · see citing works
Self-citationGuzman, C., Mohri, K., Nakamura, R., Miyake, M., Tsuchiya, Y., Tomii, K., & Watanabe, H. (2024) · Nature Communications · doi:10.1038/s41467-024-50818-8 · Cited by 13 · see citing works
The cellular basis of feeding-dependent body size plasticity in sea anemones
Garschall, K., Pascual-Carreras, E., Pascual, B. G., Filimonova, D., Guse, A., Johnston, I. G., & Steinmetz, P. R. H. (2024) · Development · doi:10.1242/dev.202926 · Cited by 12 · see citing works
A developmental biologist’s “outside-the-cell” thinking
Sherwood, D. R. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201501083 · Cited by 12 · see citing works
CLOCK evolved in cnidaria to synchronize internal rhythms with diel environmental cues
Aguillon, R., Rinsky, M., Simon‐Blecher, N., Doniger, T., Appelbaum, L., & Levy, O. (2023) · eLife · doi:10.7554/elife.89499 · Cited by 12 · see citing works
Fernández-Valverde, S. L., Aguilera, F., & Ramos-Díaz, R. A. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy061 · Cited by 12 · see citing works
Nematostella vectensis as a Model System
Al‐Shaer, L., Havrilak, J. A., & Layden, M. J. (2021) · CRC Press eBooks · doi:10.1201/9781003217503-7 · Cited by 12 · see citing works
A Need for Reverse Genetics to Study Coral Biology and Inform Conservation Efforts
Cleves, P. A. (2022) · Coral reefs of the world · doi:10.1007/978-3-031-07055-6_11 · Cited by 11 · see citing works
Cnidofest 2018: the future is bright for cnidarian research
He, S., Grasis, J. A., Nicotra, M. L., Juliano, C. E., & Schnitzler, C. E. (2019) · EvoDevo · doi:10.1186/s13227-019-0134-5 · Cited by 11 · see citing works
Exploring marine endosymbiosis systems with omics techniques
Hu, Y., Sun, S., Fan, H., Zhou, W., & Wei, F. (2021) · Science China Life Sciences · doi:10.1007/s11427-021-1925-1 · Cited by 11 · see citing works
Stevens, L. M., Kim, G., Koromila, T., Steele, J., McGehee, J. M., Stathopoulos, A., & Stein, D. S. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009544 · Cited by 11 · see citing works
Concepts and tools for gene editing
Josa, S., Seruggia, D., Fernández, A., & Montoliu, L. (2016) · Reproduction Fertility and Development · doi:10.1071/rd16396 · Cited by 11 · see citing works
Wang, R., Zhang, J., Ke-huan, L., Lu, S., & Zhu, X. (2019) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-019-00397-6 · Cited by 11 · see citing works
Warner, J. F., Besemer, R. M., Schickle, A., Borbee, E. M., Changsut, I. V., Sharp, K. H., & Babonis, L. S. (2025) · EvoDevo · doi:10.1186/s13227-025-00243-9 · Cited by 10 · see citing works
A “Numerical Evo-Devo” Synthesis for the Identification of Pattern-Forming Factors
Bailleul, R., Manceau, M., & Touboul, J. D. (2020) · Cells · doi:10.3390/cells9081840 · Cited by 10 · see citing works
Molecular techniques and their limitations shape our view of the holobiont
Cooke, I., Mead, O., Whalen, C., Boote, C., Moya, A., Ying, H., Robbins, S. J., Strugnell, J. M., Darling, A. E., Miller, D. J., et al. (2019) · Zoology · doi:10.1016/j.zool.2019.125695 · Cited by 9 · see citing works
Extraordinary model systems for regeneration
Accorsi, A., Guo, L., Marshall, W. F., Mommersteeg, M. T. M., & Nakajima, Y.-I. (2024) · Development · doi:10.1242/dev.203083 · Cited by 8 · see citing works
Baranyk, J., Malir, K., Silva, M. A. P., Rieck, S., Scheve, G., & Nakanishi, N. (2025) · Nature Communications · doi:10.1038/s41467-025-56115-2 · Cited by 8 · see citing works
Transcriptomic Analysis in the Sea Anemone Nematostella vectensis
Warner, J. F., & Röttinger, É. (2020) · Methods in molecular biology · doi:10.1007/978-1-0716-0974-3_14 · Cited by 8 · see citing works
Marine animal evolutionary developmental biology—Advances through technology development
Stracke, K., & Hejnol, A. (2022) · Evolutionary Applications · doi:10.1111/eva.13456 · Cited by 8 · see citing works
Foster, B. M., Hugosson, F., Scucchia, F., Enjolras, C., Babonis, L. S., Hoaen, W., & Martindale, M. Q. (2024) · iScience · doi:10.1016/j.isci.2024.109131 · Cited by 7 · see citing works
Optimized husbandry and targeted gene-editing for the cnidarian Nematostella vectensis
Carvalho, J. E., Burtin, M., Detournay, O., Amiel, A., & Röttinger, É. (2025) · Development · doi:10.1242/dev.204387 · Cited by 7 · see citing works
The evolutionary foundations of transcriptional regulation in animals
Coyle, M. C., & King, N. (2025) · Nature Reviews Genetics · doi:10.1038/s41576-025-00864-9 · Cited by 7 · see citing works
Basics and Roots of Synthetic Biology
Singh, S. P., Bansal, S., & Pandey, A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-444-64085-7.00001-0 · Cited by 7 · see citing works
L’anémone de merNematostella vectensis
Amiel, A., Michel, V., Carvalho, J. E., Shkreli, M., Petit, C., & Röttinger, É. (2021) · médecine/sciences · doi:10.1051/medsci/2020282 · Cited by 7 · see citing works
- Authors
- Ikmi, A., McKinney, S. A., Delventhal, K. M., & Gibson, M. C.
- Affiliations
- Stowers Institute for Medical Research (US)
- Corresponding author
- Gibson, Matthew C.
- Venue
- Nature Communications
- Published
- 2014-11-24
- Volume
- 5
- Issue
- 1
- Pages
- 5486-5486
- ISSN
- 2041-1723 (ISSN-L)
- OpenAlex
- W2121260094
- Semantic Scholar
- 128a4508034c3358353d8927a7036ce6e3f07ad7
- Cited by
- 165
- References
- 41
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 21 · 2023: 12 · 2022: 26 · 2021: 12 · 2020: 12 · 2019: 12 · 2018: 14 · 2017: 11 · 2016: 15 · 2015: 10 · 2014: 1
- FWCI
- 5.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Stowers Institute for Medical Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Animal Genetics and Reproduction
- Keywords
- Nematostella vectensis, TALEN, CRISPR/Cas9, genome editing, gene function analysis, sea anemone
- MeSH terms
- Animals, Base Sequence, Deoxyribonucleases, Endonucleases, Molecular Sequence Data, Sea Anemones, Mutagenesis, Genome, Homologous Recombination, Clustered Regularly Interspaced Short Palindromic Repeats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
