Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening
Abstract
New secondary mesenchyme specific genes, expressed exclusively in pigment cells, were isolated from sea urchin embryos using a differential screening of a macroarray cDNA library. The comparison was performed between mRNA populations of embryos having an expansion of the endo-mesodermal territory and embryos blocked in secondary mesenchyme specification. To be able to isolate transcripts with a prevalence down to five copies per cell, a subtractive hybridization procedure was employed. About 400 putative positive clones were identified and sequenced from the 5′ end. Gene expression analysis was carried out on a subset of 66 clones with real time quantitative PCR and 40 clones were positive. This group of clones contained sequences highly similar to: the transcription factor glial cells missing(gcm); the polyketide synthase gene cluster (pks-gc); three different members of the flavin-containing monooxygenase gene family(fmo); and a sulfotransferase gene (sult). Using whole mount in situ hybridization, it was shown that these genes are specifically expressed in pigment cells. A functional analysis of the S. purpuratus pks and of one S. purpuratus fmo was carried out using antisense technology and it was shown that their expression is necessary for the biosynthesis of the sea urchin pigment echinochrome. The results suggest that S. purpuratus pks, fmo and sult could belong to a differentiation gene battery of pigment cells.
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The whole echinoid GRN subcircuit from Delta-N signaling to gcm to downstream pigment cell differentiation genes is novel with respect to sea stars.
“Thus, with respect to sea stars, the whole of the echinoid GRN subcircuit from Delta-N signaling to gcm to downstream pigment cell differentiation genes (15) is novel.”
From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [15]
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Evolutionary plasticity of developmental gene regulatory network architecture
Hinman, V. F., & Davidson, E. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709994104 · Cited by 154 · see citing works
Self-citationRansick, A., & Davidson, E. H. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.05.037 · Cited by 153 · see citing works
Self-citationGene regulatory network controlling embryonic specification in the sea urchin
Oliveri, P., & Davidson, E. H. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.06.004 · Cited by 149 · see citing works
Self-citationGene Regulation: Gene Control Network in Development
de‐Leon, S. B., & Davidson, E. H. (2007) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.35.040405.102002 · Cited by 147 · see citing works
Self-citationSmith, L. C., Rast, J. P., Brockton, V., Terwilliger, D. P., Nair, S. V., Buckley, K. M., & Majeske, A. J. (2006) · Invertebrate survival journal · Cited by 135 · see citing works
Self-citationEchinodermata: The Complex Immune System in Echinoderms
Smith, L. C., Arizza, V., Hudgell, M. A. B., Barone, G., Bodnar, A. G., Buckley, K. M., Cunsolo, V., Dheilly, N. M., Franchi, N., Fugmann, S. D., et al. (2018) · Springer eBooks · doi:10.1007/978-3-319-76768-0_13 · Cited by 131 · see citing works
“Together, SpGcm and SpGata4/5/6 activate downstream differentiation gene batteries (Calestani et al. 2003; Calestani and Rogers 2010), and perturbation of either factor results in “albino” larvae that lack pigment cells.”
BackgroundSelf-citationGenetic Mapping and Biochemical Basis of Yellow Feather Pigmentation in Budgerigars
Cooke, T. F., Fischer, C. R., Wu, P., Jiang, T., Xie, K. T., Kuo, J., Doctorov, E., Zehnder, A. M., Khosla, C., Chuong, C., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.016 · Cited by 126 · see citing works
Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo
Duboc, V., Lapraz, F., Saudemont, A., Bessodes, N., Mekpoh, F., Haillot, E., Quirin, M., & Lepage, T. (2009) · Development · doi:10.1242/dev.042531 · Cited by 108 · see citing works
“…rise to a heterogeneous population of nonskeletogenic mesodermal cells that comprises muscles cells, precursors of the coelomic pouches (Ettensohn, 1992; Ruffins and Ettensohn, 1993), pigment cells (Calestani et al., 2003; Gibson and Burke, 1985) and blastocoelar cells (Tamboline and Burke, 1992).”
BackgroundHo, E. C. H., Buckley, K. M., Schrankel, C. S., Schuh, N. W., Hibino, T., Solek, C. M., Bae, K., Wang, G., & Rast, J. P. (2016) · Immunology and Cell Biology · doi:10.1038/icb.2016.51 · Cited by 90 · see citing works
Self-citationPoustka, A. J., Kühn, A., Groth, D., Weise, V., Yaguchi, S., Burke, R. D., Herwig, R., Lehrach, H. R., & Panopoulou, G. (2007) · Genome biology · doi:10.1186/gb-2007-8-5-r85 · Cited by 89 · see citing works
“These genes were uncovered in part through three array screens: a subtractive screen, in which RNA from lithiumtreated embryos was subtracted with RNA isolated from cadherin injected embryos [3]; a Brachyury target gene screen [4]; and a screen for pigment cell-specific genes [5].”
Ettensohn, C. A. (2008) · Development · doi:10.1242/dev.023564 · Cited by 86 · see citing works
A comprehensive analysis of Delta signaling in pre-gastrular sea urchin embryos
Materna, S. C., & Davidson, E. H. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.01.017 · Cited by 84 · see citing works
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript downstream pigment cell differentiation genes is lost, i.e., those encoding Bpnt, Dopt, Fmo, Papps, Pks, and Sult (Calestani et al., 2003).”
BackgroundSelf-citationRohrer, B., Pinto, F. R., Hulse, K. E., Lohr, H. R., Zhang, L., & Almeida, J. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405085200 · Cited by 83 · see citing works
Garfield, D. A., Runcie, D. E., Babbitt, C. C., Haygood, R., Nielsen, W., & Wray, G. A. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001696 · Cited by 78 · see citing works
“One exception was the node annotated as ‘‘FvMo1,2,3,’’ which represents three members of the flavin-containing monooxygenase gene family that are co-expressed in developing pigment cells and are strongly suspected to be co-regulated [96].”
BackgroundDiversification of oral and aboral mesodermal regulatory states in pregastrular sea urchin embryos
Materna, S. C., Ransick, A., Li, E., & Davidson, E. H. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.11.033 · Cited by 72 · see citing works
“Gcm provides a direct input into pigment cell differentiation genes, which begin to be expressed even before gastrulation (Calestani et al., 2003; Calestani and Rogers, 2010).”
Self-citationSolek, C. M., Oliveri, P., Loza‐Coll, M., Schrankel, C. S., Ho, E. C. H., Wang, G., & Rast, J. P. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.06.019 · Cited by 72 · see citing works
“The pigment cell differentiation gene polyketide synthase (SpPKS; Calestani et al., 2003) is sometimes elevated in SpGatac MASO injected embryos (Table S2), which is consistent with non-quantitative observations from WMISH where expression of pigment cell genes is enhanced relative to control injected embryos (see bel…”
InfluentialSelf-citationFernandez-Serra, M., Consales, C., Livigni, A., & Arnone, M. I. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2003.12.029 · Cited by 72 · see citing works
A novel group of type I polyketide synthases (PKS) in animals and the complex phylogenomics of PKSs
Castoe, T. A., Stephens, T., Noonan, B. P., & Calestani, C. (2006) · Gene · doi:10.1016/j.gene.2006.11.005 · Cited by 70 · see citing works
“Early indications, during the first characterization of this gene (Calestani et al., 2003), suggested a complex evolutionary origin and a lack of animal orthologs.”
BackgroundInfluentialSelf-citationSpHnf6, a transcription factor that executes multiple functions in sea urchin embryogenesis
Otim, O., Amore, G., Minokawa, T., McClay, D. R., & Davidson, E. H. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.05.033 · Cited by 68 · see citing works
Self-citationPankewitz, F., & Hilker, M. (2008) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2008.00040.x · Cited by 67 · see citing works
The biosynthetic diversity of the animal world
Torres, J. P., & Schmidt, E. W. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.006130 · Cited by 58 · see citing works
“In 2003, the first animal PKS (Pks1) was reported in a sea urchin, Strongylocentrus purpuratus, where its knockdown led to loss of color, whereas urchin Pks2 is involved in skeletogenesis and immune defense in embryos (31).”
BackgroundCis-regulatory logic driving glial cells missing: Self-sustaining circuitry in later embryogenesis
Ransick, A., & Davidson, E. H. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.02.003 · Cited by 54 · see citing works
“Finally, gcm promotes differentiation of pigment cells by driving genes in the echinochrome synthesis pathway, such as polyketide synthases and flavin-monooxygenases (Calestani et al., 2003; Calestani and Rogers, 2010).”
BackgroundSelf-citationHou, Y., Васильева, Е. А., Carne, A., McConnell, M. A., Bekhit, A. E. A., & Mishchenko, N. P. (2018) · RSC Advances · doi:10.1039/c8ra04777d · Cited by 53 · see citing works
Regulation of dynamic pigment cell states at single-cell resolution
Perillo, M., Oulhen, N., Foster, S., Spurrell, M., Calestani, C., & Wessel, G. M. (2020) · eLife · doi:10.7554/elife.60388 · Cited by 50 · see citing works
“…in a ring of NSM precursors surrounding the skeletogenic mesenchyme (SM) and later during blastula stage they become restricted to the aboral NSM ( Calestani et al., 2003 ; Duboc et al., 2010 ; Gibson and Burke, 1987 ; Gustafson and Wolpert, 1967 ; Kominami et al., 2001 ; Materna et al., 2013 ;…”
InfluentialSelf-citationInnate immune complexity in the purple sea urchin: diversity of the Sp185/333 system
Smith, L. C. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00070 · Cited by 47 · see citing works
“The spherule cells include cells with colorless inclusions and cells with red spherules that contain echinochrome A, which has antibacterial and antifungal activity (Johnson and Chapman, 1970; Messer and Wardlaw, 1980; Service and Wardlaw, 1984; Calestani et al., 2003).”
BackgroundLogic of gene regulatory networks
Materna, S. C., & Davidson, E. H. (2007) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2007.07.008 · Cited by 45 · see citing works
Self-citationCole, A. G., Rizzo, F. M., Martı́nez, P., Fernandez-Serra, M., & Arnone, M. I. (2009) · Development · doi:10.1242/dev.029959 · Cited by 44 · see citing works
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“Each QRT-PCR was performed in quadruplicate in 25 µl volume in iCycler (Bio-Rad, Hercules, CA) using SYBR Green PCR Core Reagents (Applied Biosystems, Foster City, CA).”
InfluentialHedgehog signaling patterns mesoderm in the sea urchin
Walton, K. D., Warner, J. F., Hertzler, P. L., & McClay, D. R. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.04.018 · Cited by 43 · see citing works
“The NSM later differentiates into to four different cell types: pigment cells (Calestani et al., 2003), blastocoelar cells (Hibino et al.”
BackgroundAlbinism as a visual, in vivo guide for CRISPR/Cas9 functionality in the sea urchin embryo
Oulhen, N., & Wessel, G. M. (2016) · Molecular Reproduction and Development · doi:10.1002/mrd.22757 · Cited by 42 · see citing works
“Echinoderms produce a variety of pigments referred to as echinochromes, with key enzymes in the synthetic pathways recently documented (Calestani et al., 2003; Barsi et al., 2015).”
BackgroundThe Axial Organ and the Pharynx Are Sites of Hematopoiesis in the Sea Urchin
Golconda, P., Buckley, K. M., Reynolds, C. R., Romanello, J. P., & Smith, L. C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00870 · Cited by 42 · see citing works
“Pigment cell precursor specification begins with the expression of SpGcm which, along with other factors, activates a gene battery involved in immune response and pigment synthesis (62, 63).”
BackgroundWessel, G. M., Kiyomoto, M., Shen, T., & Yajima, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-58584-5 · Cited by 40 · see citing works
A protocol for unraveling gene regulatory networks
Materna, S. C., & Oliveri, P. (2008) · Nature Protocols · doi:10.1038/nprot.2008.187 · Cited by 37 · see citing works
“For example, in the sea urchin, genes for skeletal matrix proteins and enzymes of the pigment synthesis pathway have been successfully used as markers for skeletogenic and pigment cell specification, respectivel”
MethodRegulative deployment of the skeletogenic gene regulatory network during sea urchin development
Sharma, T., & Ettensohn, C. A. (2011) · Development · doi:10.1242/dev.065193 · Cited by 35 · see citing works
“We confirmed this pattern of migration in L. variegatus by F-WMISH with pks, a gene specifically expressed by pigment cells (Calestani et al., 2003) (see Fig.”
BackgroundHinman, V. F., Yankura, K. A., & McCauley, B. S. (2009) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2009.01.004 · Cited by 32 · see citing works
“These factors are required to specify various mesodermal cells types, including pigment and blastocoelar cells [63,64].”
Establishment of knockout adult sea urchins by using a CRISPR‐Cas9 system
Liu, D., Awazu, A., Sakuma, T., Yamamoto, T., & Sakamoto, N. (2019) · Development Growth & Differentiation · doi:10.1111/dgd.12624 · Cited by 30 · see citing works
“Knockdown of Pks1 by MASO resulted in albino embryos (Calestani et al., 2003).”
BackgroundA Computational Screen for Type I Polyketide Synthases in Metagenomics Shotgun Data
Förstner, K. U., Doerks, T., Creevey, C. J., Doerks, A., & Peer Bork, B. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003515 · Cited by 33 · see citing works
“[10,11].”
Cis-regulatory analysis of the sea urchin pigment cell gene polyketide synthase
Calestani, C., & Rogers, D. J. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.01.026 · Cited by 33 · see citing works
“Previous studies have identified a set of SpPks upstream transcriptional regulators specifically expressed in pigment cells: glial cells missing (SpGcm; Ransick et al., 2002; Davidson et al., 2002b; Calestani et al., 2003); SpGatae (Pancer et al.”
BackgroundInfluentialSelf-citationUnexpected link between polyketide synthase and calcium carbonate biomineralization
Hojo, M., Omi, A., Hamanaka, G., Shindo, K., Shimada, A., Kondo, M., Narita, T., Kiyomoto, M., Katsuyama, Y., Ohnishi, Y., et al. (2015) · Zoological Letters · doi:10.1186/s40851-014-0001-0 · Cited by 32 · see citing works
“Another echinoderm pks gene, hppks-1 was found to contribute to pigmentation as previously reported [39] (Figure 4B Upper Panel and C, and Additional file 7C).”
BackgroundResultEmbryonic hematopoiesis modulates the inflammatory response and larval hematopoiesis in Drosophila
Bazzi, W., Cattenoz, P. B., Delaporte, C., Dasari, V., Sakr, R., Yuasa, Y., & Giangrande, A. (2018) · eLife · doi:10.7554/elife.34890 · Cited by 32 · see citing works
Impacts of a new transcription factor family
Hashemolhosseini, S., & Wegner, M. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200406097 · Cited by 30 · see citing works
“In the sea urchin Strongylocentrotus purpuratus , SpGcm was identified as a Notch-dependent factor (Calestani et al., 2003).”
BackgroundMeyer, A., Ku, C. J., Hatleberg, W. L., Telmer, C. A., & Hinman, V. F. (2023) · eLife · doi:10.7554/elife.80090 · Cited by 29 · see citing works
“These clusters shared 107 markers including known 432 markers of pigment cells in sea urchins, including gcml, polyketide synthase 1 (pks1), 433 dimethylaniline monooxygenase [N-oxide-forming] 2 (fmo3), and sulfotransferase (sult) 434 (Calestani et al. 2003).”
BackgroundNickel toxicity in P. lividus embryos: Dose dependent effects and gene expression analysis
Bonaventura, R., Zito, F., Chiaramonte, M., Costa, C., & Russo, R. (2018) · Marine Environmental Research · doi:10.1016/j.marenvres.2018.05.002 · Cited by 28 · see citing works
de‐Leon, S. B., & Davidson, E. H. (2006) · Science s STKE · doi:10.1126/stke.3612006pe47 · Cited by 28 · see citing works
Self-citationPigment Cell Differentiation in Sea Urchin Blastula-Derived Primary Cell Cultures
Ageenko, N. V., Kiselev, K. V., Dmitrenok, P. S., & Odintsova, N. A. (2014) · Marine Drugs · doi:10.3390/md12073874 · Cited by 27 · see citing works
“[13] revealed three groups of genes expressed in sea urchin pigment cells that play key roles in the biosynthesis of naphthoquinone pigments [14].”
BackgroundGene Regulatory Network Analysis in Sea Urchin Embryos
Oliveri, P., & Davidson, E. H. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74032-7 · Cited by 27 · see citing works
Self-citationSala, G. D., Hochmuth, T., Costantino, V., Teta, R., Gerwick, W. H., Gerwick, L. G., Piel, J., & Mangoni, A. (2013) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12081 · Cited by 26 · see citing works
“Among animals, iterative type I PKSs have been discovered in sea urchins (Calestani et al., 2003), while putative non-FAS iterative type I PKS with unknown functions are present in the genomes of chickens and fish (Castoe et al.”
BackgroundThese Colors Don’t Run: Regulation of Pigment—Biosynthesis in Echinoderms
Calestani, C., & Wessel, G. M. (2018) · Results and problems in cell differentiation · doi:10.1007/978-3-319-92486-1_22 · Cited by 25 · see citing works
“The sea urchin SpPks1 belongs to the type I class of PKSs (Castoe et al., 2007) and it is required for the larval echinochrome biosynthesis (Calestani et al., 2003).”
BackgroundInfluentialSelf-citationThe gene regulatory control of sea urchin gastrulation
Ettensohn, C. A. (2020) · Mechanisms of Development · doi:10.1016/j.mod.2020.103599 · Cited by 23 · see citing works
“Many pigment cell-specific mRNAs have been identified, including those that encode enzymes involved in pigment biosynthesis (Calestani et al., 2003; Barsi et al., 2015).”
Zito, F., Koop, D., Byrne, M., & Matranga, V. (2015) · Development Growth & Differentiation · doi:10.1111/dgd.12229 · Cited by 23 · see citing works
“Although CA has not been identified in the gene repertoire of larval immune pigment cells (Calestani et al. 2003), it is possible that one of the 19 genes encoding for CAs in the S. purpuratus genome (Livingston et al. 2006) may be associated with these cells, the nature of which has yet to be…”
BackgroundSynthetic in vivo validation of gene network circuitry
Damle, S. S., & Davidson, E. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119905109 · Cited by 23 · see citing works
“Thus, gcm is both a pigment cell specification gene and a driver of a pigment synthesis gene battery (14).”
BackgroundSelf-citationKiselev, K. V., Ageenko, N. V., & Kurilenko, V. V. (2012) · Diseases of Aquatic Organisms · doi:10.3354/dao02570 · Cited by 23 · see citing works
“Sea urchin embryos of Strongylo - cen trotus purpuratus lacking pks (via knock-down) develop pigment cells but appear unpigmented; these individuals are referred to as the albino phenotype (Calestani et al. 2003).”
BackgroundLee, S. H., Zhao, S., Recknor, J. C., Nettleton, D. S., Orley, S., Kang, S., Lee, B.-C., Hwang, W. S., & Tuggle, C. K. (2005) · Molecular Reproduction and Development · doi:10.1002/mrd.20291 · Cited by 23 · see citing works
“With these advantages, gene expression patterns using membrane array techniques have been reported (Rast et al., 2002; Calestani et al., 2003; Zhao et al., 2003).”
BackgroundAgeenko, N. V., Kiselev, K. V., & Odintsova, N. A. (2011) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2011/730356 · Cited by 22 · see citing works
“Our results agree with the data of Calestani with colleagues that showed that the pks genes are expressed in sea urchin pigment cells beginning from the blastula stage and that this expression is maintained throughout the pluteus stage [21].”
BackgroundResultInfluentialSchrankel, C. S., Solek, C. M., Buckley, K. M., Anderson, M. K., & Rast, J. P. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.05.034 · Cited by 22 · see citing works
Self-citationBringmann, G., & Irmer, A. (2008) · Phytochemistry Reviews · doi:10.1007/s11101-008-9090-8 · Cited by 22 · see citing works
“The knowledge about polyketide synthases from animals, by contrast, is as yet rather marginal, thus making it impossible to predict the structure of the respective PKS, which might constitute another member of the novel group of animal-derived type I polyketide synthases (Calestani et al. 2003), whose origin is, howev…”
BackgroundExpression pattern of polyketide synthase-2 during sea urchin development
Beeble, A., & Calestani, C. (2011) · Gene Expression Patterns · doi:10.1016/j.gep.2011.09.004 · Cited by 21 · see citing works
“Pks1 expression continues throughout development, to the pluteus stage in pigment cells embedded in the aboral ectoderm (Calestani et al., 2003). bCorresponding Author: Cristina Calestani, Valdosta State University, 1500 N. Patterson St., Valdosta, GA 31698, ccalestani@valdosta.edu,Phone:…”
BackgroundInfluentialSelf-citationCRISPR/Cas9-mediated genome editing in sea urchins
Lin, C.-Y., Oulhen, N., Wessel, G. M., & Su, Y. (2018) · Methods in cell biology · doi:10.1016/bs.mcb.2018.10.004 · Cited by 21 · see citing works
Sea Urchin Polyketide Synthase SpPks1 Produces the Naphthalene Precursor to Echinoderm Pigments
Li, F., Lin, Z., Torres, J. P., Hill, E. A., Li, D., Townsend, C. A., & Schmidt, E. W. (2022) · Journal of the American Chemical Society · doi:10.1021/jacs.2c01416 · Cited by 20 · see citing works
Ageenko, N. V., Kiselev, K. V., & Odintsova, N. A. (2022) · Marine Drugs · doi:10.3390/md20100611 · Cited by 20 · see citing works
“It is possible that the biosynthesis of sea urchin spinochromes occurs with the participation of their own enzyme complex without the participation of endosymbionts [68].”
BackgroundFrançois, R. M. M., Massicard, J.-M., & Weissman, K. J. (2024) · Natural Product Reports · doi:10.1039/d4np00046c · Cited by 18 · see citing works
Chang, Y.-C., Pai, C.-Y., Chen, Y., Ting, H.-C., Martı́nez, P., Telford, M. J., Yu, J., & Su, Y. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.12.015 · Cited by 16 · see citing works
Aiswarya, G., Vijayanathan, M., Sreekumar, S., Jasim, B., Menon, T. G., Radhakrishnan, E. K., & Soniya, E. V. (2021) · Current Molecular Pharmacology · doi:10.2174/1874467214666210319145816 · Cited by 18 · see citing works
Comparative studies on the skeletogenic mesenchyme of echinoids
Minokawa, T. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.11.011 · Cited by 17 · see citing works
“…antisense oligonucleotide (MASO) into S. purpuratus eggs results in transcriptional activation of NSM specification genes, including gcm (glial cells missing; Ransick et al., 2002) and pks (polyketide synthase; Calestani et al., 2003) in descendants of the micromere (Oliveri et al., 2008).”
BackgroundSingle-cell RNA-sequencing analysis of early sea star development
Foster, S., Oulhen, N., Fresques, T., Zaki, H. A., & Wessel, G. M. (2022) · Development · doi:10.1242/dev.200982 · Cited by 16 · see citing works
“At blastula stage, the transcription factor glial cells missing ( gcm ; gcml ), which marks the pigment cells in the related purple sea urchin, shows no localized expression; gcm -positive cells are present throughout the ectoderm (Calestani et al., 2003; McCauley et al., 2010).”
BackgroundThe polyketide to fatty acid transition in the evolution of animal lipid metabolism
Lin, Z., Li, F., Krug, P. J., & Schmidt, E. W. (2024) · Nature Communications · doi:10.1038/s41467-023-44497-0 · Cited by 16 · see citing works
Cutignano, A., Villani, G., & Fontana, A. (2012) · Organic Letters · doi:10.1021/ol2032653 · Cited by 16 · see citing works
Mechanisms of the epithelial-to-mesenchymal transition in sea urchin embryos
Katow, H. (2015) · Tissue Barriers · doi:10.1080/21688370.2015.1059004 · Cited by 15 · see citing works
“Pks and sult are pigment cellspecific genes along with gcm, which are 3 different members of the fmo gene family.(132) The number of pigment cells increases considerably in vitro when embryos are incubated in the coelomic fluids of injured sea urchins, suggesting the involvement of the cells in some pathological situa…”
BackgroundOdintsova, N. A., Ageenko, N. V., Kipryushina, Y. O., Maiorova, M. A., & Boroda, A. V. (2015) · Cryobiology · doi:10.1016/j.cryobiol.2015.06.002 · Cited by 14 · see citing works
“We suppose that an expression analysis of genes involved in pigment differentiation in sea urchins [4,9,15] may help to identify changes in pigment differentiation that occur in sea urchin cells after freezing–thawing.”
BackgroundExpression of Exogenous mRNAs to Study Gene Function in the Sea Urchin Embryo
Lepage, T., & Gache, C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74027-3 · Cited by 13 · see citing works
Genomic Resources for the Study of Sea Urchin Development
Cameron, R. A., Rast, J. P., & Brown, C. T. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74030-3 · Cited by 13 · see citing works
Self-citationXing, L., Wang, L., Liu, S., Sun, L., Wessel, G. M., & Yang, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512213 · Cited by 12 · see citing works
Wang, Z., Hu, H., Wang, H., Yan, L., Zhang, Y., Wang, H., Lv, X., Li, J., & Bai, Z. (2024) · Aquaculture · doi:10.1016/j.aquaculture.2024.741658 · Cited by 12 · see citing works
Wound repair in sea urchin larvae involves pigment cells and blastocoelar cells
Allen, R. L., George, A. N., Miranda, E., Phillips, T. M., Crawford, J. M., Kiehart, D. P., & McClay, D. R. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.08.005 · Cited by 12 · see citing works
Spurrell, M., Oulhen, N., Foster, S., Perillo, M., & Wessel, G. M. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.11.008 · Cited by 12 · see citing works
“Previous studies have identi fi ed an extensive suite of genes specifically expressed in pigment cells and include SpPks1 and SpFmo3, which are responsible for larval pigment production (Wessel et al., 2020), (Calestani et al., 2003), (Oulhen and Wessel, 2016), (Perillo et al., 2020).”
BackgroundInfluentialChiaramonte, M., Russo, R., Costa, C., Bonaventura, R., & Zito, F. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.118558 · Cited by 12 · see citing works
Barca, A., Vacca, F., Vizioli, J., Drago, F., Vetrugno, C., Verri, T., & Pagliara, P. (2017) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2017.09.078 · Cited by 11 · see citing works
Cutignano, A., Cimino, G., Villani, G., & Fontana, A. (2009) · Tetrahedron · doi:10.1016/j.tet.2009.07.078 · Cited by 11 · see citing works
Xing, L., Sun, L., Liu, S., Li, X., Zhang, L., & Yang, H. (2017) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2017.05.004 · Cited by 11 · see citing works
Global patterns of enhancer activity during sea urchin embryogenesis assessed by eRNA profilingPreprint
Khor, J. M., Guerrero‐Santoro, J., Douglas, W. A., & Ettensohn, C. A. (2021) · Genome Research · doi:10.1101/gr.275684.121 · Cited by 11 · see citing works
“We examined enhancers located within 20 kb of genes shown previ-ouslytobedifferentiallyexpressedbyPMCs(Rafiq etal.2014),pigment cells (Calestani et al. 2003; Barsi et al. 2015), and ciliated band cells (Barsi et al. 2015).”
Echinoderm immunity: is the larval immune system immature?
Hirano, M. (2016) · Immunology and Cell Biology · doi:10.1038/icb.2016.67 · Cited by 10 · see citing works
CRISPR/Cas9 knockin methodology for the sea urchin embryo
Oulhen, N., Morita, S., Warner, J. F., & Wessel, G. M. (2023) · Molecular Reproduction and Development · doi:10.1002/mrd.23672 · Cited by 9 · see citing works
“Sea urchin larvae produce echinochrome pigments that require several gene functions including the enzyme polyketide synthase 1 (PKS1) (Barsi et al., 2015; Calestani & Wessel, 2018; Calestani et al., 2003; Perillo et al., 2020; Wessel et al., 2020).”
BackgroundLiu, B., Xing, L., Liu, S., Sun, L., Su, F., Cui, W., & Jiang, C. (2024) · Frontiers in Marine Science · doi:10.3389/fmars.2024.1334761 · Cited by 9 · see citing works
Wakayama, N., Katow, T., & Katow, H. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00112 · Cited by 9 · see citing works
“SMC-specific genes, such as glial cells missing (gcm), the polyketide synthase gene cluster (pks-gc), the flavin-containing monooxygenases multigene family (fmo), and sulfotransferase (sult ), are isolated from the pigment cell lineage, and they are downstream of the Notch signaling pathway (78).”
BackgroundHigh-resolution, three-dimensional mapping of gene expression using GeneExpressMap (GEM)
Flynn, C., Sharma, T., Ruffins, S. W., Guerra, S. L., Crowley, J. C., & Ettensohn, C. A. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.06.033 · Cited by 9 · see citing works
“Pks is a terminal differentiation gene in the pigment cell GRN and encodes an enzyme complex that is required for the accumulation of echinochrome (Calestani et al., 2003).”
BackgroundHardin, J. D., & Illingworth, C. A. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20941 · Cited by 9 · see citing works
“, 2006) and most SMC markers identified using macroarray approaches (Calestani et al., 2003) suggests that Lv-snail is only expressed in a subset of SMCs.”
BackgroundLinking Genes to Molecules in Eukaryotic Sources: An Endeavor to Expand Our Biosynthetic Repertoire
Ganley, J. G., & Derbyshire, E. R. (2020) · Molecules · doi:10.3390/molecules25030625 · Cited by 8 · see citing works
“While many of these natural products are indeed produced by associated microbiome members [50], de novo production has also been illustrated in marine animals [92], including sea slugs [51], nudibranchs [52], sponges [93], corals [62,94], sea urchins [91], and bryozoans [95], to give some examples.”
BackgroundThe Cell States of Sea Urchin During Metamorphosis Revealed by Single-Cell RNA Sequencing
Ge, H. M., Huang, Y., Zhang, L., Huang, S., & Wang, G. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031059 · Cited by 7 · see citing works
More than a colour; how pigment influences colourblind microbes
Wessel, G. M., Xing, L., & Oulhen, N. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0077 · Cited by 7 · see citing works
“Of those, sequences encoding metabolic enzymes, transcription factors, extracellular matrix proteins, and others, as well as orthologues of PKS, Fmo3 and a sulfo-transferase, were found repeatedly [39].”
BackgroundMethodTyunin, A. P., Ageenko, N. V., & Kiselev, K. V. (2016) · Biotechnology Letters · doi:10.1007/s10529-016-2191-3 · Cited by 7 · see citing works
“purpuratus and ensure opportune expression of SpPks and subsequent biosynthesis of echinochrome (Calestani et al. 2003).”
BackgroundInfluentialTakata, H., & Kominami, T. (2011) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01278.x · Cited by 7 · see citing works
“In the pigment cell lineage, the glial cells missing, GataE and Krüppellike genes positively regulate polyketide synthase, which is important for the synthesis of larval echinochrome (Calestani et al. 2003; Calestani & Rogers 2010).”
BackgroundA molecular basis for spine color morphs in the sea urchin Lytechinus variegatus
Wise, M., Silvia, M., Reyes, G., Dunn, R., Onorato, T. M., Pieplow, C. A., Furze, A. R., Hebert, E., Oulhen, N., Ritschoff, D., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-79312-3 · Cited by 6 · see citing works
Echinoderm Antimicrobial Peptides
Arizza, V., & Schillaci, D. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803252-7.00012-6 · Cited by 6 · see citing works
- Authors
- Calestani, C., Rast, J. P., & Davidson, E. H.
- Affiliations
- California Institute of Technology (US)
- Corresponding author
- Calestani, Cristina
- Davidson, Eric H.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2003-10-01
- Volume
- 130
- Issue
- 19
- Pages
- 4587-4596
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2074040006
- Cited by
- 137
- References
- 95
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 15 · 2023: 4 · 2022: 7 · 2021: 2 · 2020: 4 · 2019: 8 · 2018: 6 · 2017: 4 · 2016: 9 · 2015: 5 · 2014: 3 · 2013: 5 · 2012: 7
- FWCI
- 2.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Institutes of Health (5r01rr006591-13, 5p01hd037105-20)
- National Center for Research Resources (RR 06591, P40RR015044, RR15044)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD37105)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Echinoderm biology and ecology
- Keywords
- secondary mesenchyme, subtractive hybridization, gene isolation, polyketide synthase, flavin-containing monooxygenase, sulfotransferase, endomesoderm specification
- MeSH terms
- Animals, Embryo, Nonmammalian, Mesoderm, Multienzyme Complexes, Neuropeptides, Oxygenases, Sea Urchins, Sulfotransferases, Trans-Activators, Oligonucleotides, Antisense, In Situ Hybridization, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling
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