Conserved MIP receptor–ligand pair regulates Platynereis larval settlement
Open accessAbstract
Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory–neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii . MIP is expressed in chemosensory–neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor–ligand pair in regulating marine annelid settlement.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Mutant sensory cilia in the nematode Caenorhabditis elegans
Perkins, L. A., Hedgecock, E. M., Thomson, J. N., & Culotti, J. G. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90314-3 · Cited by 907 · see citing works
Chemical ecology of the settlement of benthic marine invertebrates
Pawlik, J. R. (1992) · Oceanography and Marine Biology/Oceanography and marine biology - an annual review · doi:10.1016/0967-0653(93)91415-9 · Cited by 795 · see citing works
The Genome Portal of the Department of Energy Joint Genome Institute
Grigoriev, I. V., Nordberg, H. P., Shabalov, I., Aerts, A. L., Cantor, M., Goodstein, D. M., Kuo, A., Minovitsky, S., Nikitin, R., Ohm, R. A., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr947 · Cited by 546 · see citing works
The origins of insect metamorphosis
Truman, J. W., & Riddiford, L. M. (1999) · Nature · doi:10.1038/46737 · Cited by 544 · see citing works
Drosophila neuropeptides in regulation of physiology and behavior
Nässel, D. R., & Winther, Å. M. E. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.010 · Cited by 495 · see citing works
Phylogenomic analyses unravel annelid evolution
Struck, T. H., Paul, C., Hill, N., Hartmann, S. A., Hösel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G., et al. (2011) · Nature · doi:10.1038/nature09864 · Cited by 406 · see citing works
Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.04.041 · Cited by 384 · see citing works
Cardona, A., Saalfeld, S., Preibisch, S., Schmid, B., Cheng, A., Pulokas, J., Tomancak, P., & Hartenstein, V. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000502 · Cited by 372 · see citing works
Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry
Moroz, L. L., Edwards, J. R., Puthanveettil, S. V., Kohn, A. B., Ha, T. J., Heyland, A., Knudsen, B., Sahni, A., Yu, F., Liu, L., et al. (2006) · Cell · doi:10.1016/j.cell.2006.09.052 · Cited by 323 · see citing works
The Origins and Evolution of Vertebrate Metamorphosis
Laudet, V. (2011) · Current Biology · doi:10.1016/j.cub.2011.07.030 · Cited by 321 · see citing works
Tomer, R., Denes, A. S., Tessmar-Raible, K., & Arendt, D. (2010) · Cell · doi:10.1016/j.cell.2010.07.043 · Cited by 317 · see citing works
Atlas of Marine Invertebrate Larvae
Young, C. M., Sewell, M. A., & Rice, M. E. (2003) · Aquaculture Research · doi:10.1046/j.1365-2109.2003.00819.x · Cited by 312 · see citing works
Mechanism of phototaxis in marine zooplankton
Jékely, G., Colombelli, J., Hausen, H., Guy, K., Stelzer, E., Nédélec, F., & Arendt, D. (2008) · Nature · doi:10.1038/nature07590 · Cited by 298 · see citing works
Self-citationChemical signaling processes in the marine environment
Zimmer, R. K., & Butman, C. (2000) · Biological Bulletin · doi:10.2307/1542522 · Cited by 281 · see citing works
Stress hormones mediate environment-genotype interactions during amphibian development
Denver, R. J. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.04.016 · Cited by 276 · see citing works
Baubet, V., Mouellic, H. L., Campbell, A. K., Lucas-Meunier, E., Fossier, P., & Brûlet, P. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.13.7260 · Cited by 272 · see citing works
Ecological Developmental Biology
Gilbert, S. F. (2017) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0020479.pub2 · Cited by 247 · see citing works
The normal development of Platynereis dumerilii (Nereididae, Annelida)
Fischer, A., Henrich, T., & Arendt, D. (2010) · Frontiers in Zoology · doi:10.1186/1742-9994-7-31 · Cited by 235 · see citing works
Veenstra, J. A. (2010) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2010.02.010 · Cited by 228 · see citing works
Kim, Y., Žitňan, D., Galizia, C. G., Cho, K.-H., & Adams, M. E. (2006) · Current Biology · doi:10.1016/j.cub.2006.06.027 · Cited by 228 · see citing works
Lorenz, M. W., Kellner, R., & Hoffmann, K. H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.36.21103 · Cited by 210 · see citing works
Acampora, D., Postiglione, M. P., Avantaggiato, V., Bonito, M. D., Vaccarino, F. M., Michaud, J. L., & Simeone, A. (1999) · Genes & Development · doi:10.1101/gad.13.21.2787 · Cited by 198 · see citing works
MIPs are ancestral ligands for the sex peptide receptor
Kim, Y., Bartalska, K., Audsley, N., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914764107 · Cited by 190 · see citing works
Schoofs, L., Holman, G. M., Hayes, T. K., et al. (1991) · Regulatory Peptides · doi:10.1016/0167-0115(91)90199-q · Cited by 184 · see citing works
The apical sensory organ of a gastropod veliger is a receptor for settlement cues
Hadfield, M., Meleshkevitch, E., & Boudko, D. (2000) · The Biological Bulletin · doi:10.2307/1542804 · Cited by 176 · see citing works
Why and how marine-invertebrate larvae metamorphose so fast
Hadfield, M. G. . (2000) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0197 · Cited by 172 · see citing works
Six3 demarcates the anterior-most developing brain region in bilaterian animals
Steinmetz, P. R. H., Urbach, R., Posnien, N., Eriksson, J., Kostyuchenko, R. P., Brena, C., Guy, K., Akam, M. E., Bucher, G., & Arendt, D. (2010) · EvoDevo · doi:10.1186/2041-9139-1-14 · Cited by 172 · 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
Identification of a Prothoracicostatic Peptide in the Larval Brain of the Silkworm, Bombyx mori
Hua, Y., Tanaka, Y., Nakamura, K., Sakakibara, M., Nagata, S., & Kataoka, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.44.31169 · Cited by 163 · see citing works
Maldonado, M., & Young, C. M. (1996) · Marine Ecology Progress Series · doi:10.3354/meps138169 · Cited by 154 · see citing works
Larval settlement of polychaetes
Qian, P. (1999) · Springer eBooks · doi:10.1007/978-94-017-2887-4_14 · Cited by 153 · see citing works
Leitz, T., Morand, K. L., & Mann, M. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1160 · Cited by 145 · see citing works
Fischer, A., & Dorresteijn, A. W. C. (2004) · BioEssays · doi:10.1002/bies.10409 · Cited by 141 · see citing works
Williamson, M. P., Lenz, C., Winther, Å. M. E., Nässel, D. R., & Grimmelikhuijzen, C. J. P. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4565 · Cited by 137 · see citing works
Neuropeptides regulate swimming depth of Platynereis larvae
Conzelmann, M., Offenburger, S.-L., Asadulina, A., Keller, T., Münch, T. A., & Jékely, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109085108 · Cited by 136 · see citing works
Self-citationVeenstra, J. A. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.01.005 · Cited by 133 · see citing works
Larval settlement of polychaetes
Qian, P. (1999) · Hydrobiologia · doi:10.1023/a:1003704928668 · Cited by 132 · see citing works
Yamanaka, N., Hua, Y., Roller, L., Spalovská, I., Mizoguchi, A., Kataoka, H., & Tanaka, Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907471107 · Cited by 126 · see citing works
Tunaru, S., Lättig, J., Kero, J. T., Krause, G., & Offermanns, S. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.015750 · Cited by 125 · see citing works
Self-citationSignaling mechanisms underlying metamorphic transitions in animals.
Heyland, A., & Moroz, L. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icl023 · Cited by 121 · see citing works
Sense organs in polychaetes (Annelida)
Purschke, G. (2005) · Hydrobiologia · doi:10.1007/s10750-004-4358-5 · Cited by 115 · see citing works
Rapid Behavioral Responses of an Invertebrate Larva to Dissolved Settlement Cue
Hadfield, M. G. ., & Koehl, M. A. R. (2004) · Biological Bulletin · doi:10.2307/1543626 · Cited by 114 · see citing works
Williamson, M. P., Lenz, C., Winther, M. E., Nässel, D. R., & Grimmelikhuijzen, C. J. P. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4402 · Cited by 107 · see citing works
LWamides from Cnidaria constitute a novel family of neuropeptides with morphogenetic activity
Gajewski, M., Leitz, T., Schlo�herr, J., & Plickert, G. (1996) · Development Genes and Evolution · doi:10.1007/bf00365801 · Cited by 100 · see citing works
The Construction of a Bioactive Peptide Database in Metazoa
Liu, F., Baggerman, G., Schoofs, L., & Wets, G. (2008) · Journal of Proteome Research · doi:10.1021/pr800037n · Cited by 95 · see citing works
Nielsen, C. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05051.x · Cited by 95 · see citing works
Santagata, S., Resh, C., Hejnol, A., Martindale, M. Q., & Passamaneck, Y. J. (2012) · EvoDevo · doi:10.1186/2041-9139-3-3 · Cited by 92 · see citing works
Ecological developmental biology: environmental signals for normal animal development
Gilbert, S. F. (2012) · Evolution & Development · doi:10.1111/j.1525-142x.2011.00519.x · Cited by 90 · see citing works
The Biphasic Life Cycle—A Central Theme of Metazoan Evolution
Rieger, R. M. (1994) · American Zoologist · doi:10.1093/icb/34.4.484 · Cited by 90 · see citing works
Page, L. R., & Parries, S. C. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000320)418:4 · Cited by 85 · see citing works
Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide
Erwin, P. M., & Szmant, A. M. (2010) · Coral Reefs · doi:10.1007/s00338-010-0634-1 · Cited by 82 · see citing works
Endoscopic observations of invertebrate larval substratum exploration and settlement
Walters, L., Miron, G., & Bourget, E. (1999) · Marine Ecology Progress Series · doi:10.3354/meps182095 · Cited by 74 · see citing works
Conzelmann, M., & Jékely, G. (2012) · EvoDevo · doi:10.1186/2041-9139-3-23 · Cited by 67 · see citing works
Self-citationTranscriptional Orchestration of the Regulated Secretory Pathway in Neurons by the bHLH protein DIMM
Hamanaka, Y., Park, D., Yin, P., Annangudi, S. P., Edwards, T. N., Sweedler, J. V., Meinertzhagen, I. A., & Taghert, P. H. (2010) · Current Biology · doi:10.1016/j.cub.2009.11.065 · Cited by 61 · see citing works
Expanding networks: Signaling components in and a hypothesis for the evolution of metamorphosis
Hodin, J. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icl038 · Cited by 59 · see citing works
Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria)
Piraino, S., Zega, G., Di Benedetto, C., Leone, A., Dell'Anna, A., Pennati, R., Candia Carnevali, D., Schmid, V., & Reichert, H. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22614 · Cited by 56 · see citing works
Park, D., Shafer, O. T., Shepherd, S. P., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01104-07 · Cited by 56 · see citing works
Whole-body gene expression pattern registration in Platynereis larvae
Asadulina, A., Panzera, A., Verasztó, C., Liebig, C., & Jékely, G. (2012) · EvoDevo · doi:10.1186/2041-9139-3-27 · Cited by 52 · see citing works
Self-citationSchoofs, L., Veelaert, D., Broeck, J. V., et al. (1996) · Regulatory Peptides · doi:10.1016/0167-0115(96)00040-7 · Cited by 43 · see citing works
Caspers, H. (1971) · Internationale Revue der gesamten Hydrobiologie und Hydrographie · doi:10.1002/iroh.19710560213 · Cited by 36 · see citing works
Jackson, D. J., Meyer, N. P., Seaver, E. C., Pang, K., McDougall, C., Moy, V. N., Gordon, K. L., Degnan, B. M., Martindale, M. Q., Burke, R. D., et al. (2010) · Development Genes and Evolution · doi:10.1007/s00427-010-0343-3 · Cited by 36 · see citing works
Sense organs in polychaetes (Annelida)
Purschke, G. (2005) · Springer eBooks · doi:10.1007/1-4020-3240-4_5 · Cited by 32 · see citing works
Homology of insect corpora allata and vertebrate adenohypophysis?
Wirmer, A., Bradler, S., & Heinrich, R. (2012) · Arthropod Structure & Development · doi:10.1016/j.asd.2012.04.003 · Cited by 12 · see citing works
Schoofs, L. (1996) · Regulatory Peptides · doi:10.1016/s0167-0115(96)00040-7 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
High-throughput spatial mapping of single-cell RNA-seq data to tissue of origin
Achim, K., Pettit, J.-B., Saraiva, L. R., Gavriouchkina, D., Larsson, T., Arendt, D., & Marioni, J. C. (2015) · Nature Biotechnology · doi:10.1038/nbt.3209 · Cited by 395 · see citing works
From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system
Arendt, D., Tosches, M. A., & Marlow, H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.15 · Cited by 279 · see citing works
Phylogenomic Insights into Animal Evolution
Telford, M. J., Budd, G. E., & Philippe, H. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.060 · Cited by 213 · see citing works
The phylogenetic position of ctenophores and the origin(s) of nervous systems
Jákely, G., Paps, J., & Nielsen, C. (2015) · EvoDevo · doi:10.1186/2041-9139-6-1 · Cited by 189 · see citing works
Self-citationAn option space for early neural evolution
Jékely, G., Keijzer, F., & Godfrey-Smith, P. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0181 · Cited by 171 · see citing works
Self-citationThe neuropeptide complement of the marine annelid Platynereis dumerilii
Conzelmann, M., Williams, E. A., Krug, K., Franz-Wachtel, M., Macek, B., & Jékely, G. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-906 · Cited by 165 · see citing works
Self-citationSynaptic and peptidergic connectome of a neurosecretory center in the annelid brain
Williams, E. A., Verasztó, C., Jasek, S., Conzelmann, M., Shahidi, R., Bauknecht, P., Mirabeau, O., & Jékely, G. (2017) · eLife · doi:10.7554/elife.26349 · Cited by 119 · see citing works
Self-citationThe evolution and nomenclature of GnRH-type and corazonin-type neuropeptide signaling systems
Zandawala, M., Tian, S., & Elphick, M. R. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.06.007 · Cited by 105 · see citing works
Verasztó, C., Jasek, S., Gühmann, M., Shahidi, R., Ueda, N., Beard, J. D., Mendes, S., Heinz, K., Bezares-Calderón, L. A., Williams, E., et al. (2020) · doi:10.1101/2020.08.21.260984 · Cited by 54 · see citing works
Self-citationBannister, S., Antonova, O., Polo, A., Lohs, C., Hallay, N., Valinciute, A., Raible, F., & Tessmar-Raible, K. (2014) · Genetics · doi:10.1534/genetics.113.161091 · Cited by 56 · see citing works
“While useful for gaining spatio-temporal insight into protein activity, the penetration (i.e., effective dosage), affinity, and specificity of smallmolecule inhibitors (often developed for use in other systems) may limit the pathways and targets that can be investigated in vivo in Platynereis.”
BackgroundMethodNeuropeptides control life-phase transitions
Schoofs, L., & Beets, I. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305724110 · Cited by 27 · see citing works
- Authors
- Conzelmann, M., Williams, E. A., Tunaru, S., Randel, N., Shahidi, R., Asadulina, A., Berger, J., Offermanns, S., & Jékely, G.
- Affiliations
- Max Planck Institute for Developmental Biology (DE)
- Max Planck Institute for Heart and Lung Research (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-04-08
- Volume
- 110
- Issue
- 20
- Pages
- 8224-8229
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3657792
- OpenAlex
- W1983885633
- Cited by
- 155
- References
- 65
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 32 · 2023: 15 · 2022: 8 · 2021: 8 · 2020: 12 · 2019: 11 · 2018: 9 · 2017: 8 · 2016: 8 · 2015: 13 · 2014: 12 · 2013: 4
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Funders
- European Commission (2007–2013, FP7 2007-2013, 260821, FP7/2007)
- Max-Planck-Gesellschaft
- FP7 Ideas: European Research Council (260821)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- myoinhibitory peptides, neuropeptide signaling, larval settlement, Platynereis dumerilii, sex peptide receptor, life cycle transitions, Polychaeta, morpholino knockdown
- MeSH terms
- Animals, Annelida, Dose-Response Relationship, Drug, Image Processing, Computer-Assisted, Larva, Ligands, Microscopy, Electron, Scanning, Molecular Sequence Data, Neurons, Neuropeptides, Signal Transduction, Gene Library, Receptors, Neuropeptide, DNA, Complementary, Expressed Sequence Tags, Receptors, G-Protein-Coupled, Microscopy, Electron, Transmission, Gene Knockdown Techniques
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.
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