Skip to main content
SpringerLink
Log in

Neuropeptides, Peptide Hormones, and Their Receptors of a Tunicate, Ciona intestinalis

  • Chapter
  • First Online:
Evo-Devo: Non-model Species in Cell and Developmental Biology

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 68))

Abstract

The critical phylogenetic position of the ascidian, Ciona intestinalis, as the closest relative of vertebrates, suggested its potential applicability as a model organism in a wide variety of biological events including the nervous, neuroendocrine, and endocrine regulation. To date, approximately 40 neuropeptides and/or peptide hormones and several cognate receptors have been identified. These peptides are categorized into two types: (1) orthologs of vertebrate peptides, such as cholecystokinin, GnRH, tachykinin, vasopressin, and calcitonin, and (2) novel family peptides such as LF peptides and YFL/V peptides. Ciona GnRH receptors (Ci-GnRHR) were found to be multiplicated in the Ciona-specific lineages and to form unique heterodimers between Ci-GnRHR1 and R4 and between Ci-GnRHR2 and R4, leading to fine-tuning of the generation of second messengers. Furthermore, Ciona tachykinin was shown to regulate a novel protease-associated follicle growth pathway. These findings will pave the way for the exploration of both conserved and diversified endocrine, neuroendocrine, and nervous systems in the evolutionary lineage of invertebrate deuterostomes and/or chordates. In this chapter, we provide an overview of primary sequences, functions, and evolutionary aspects of neuropeptides, peptide hormones, and their receptors in C. intestinalis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 189.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AM:

Adrenomedullin

AMY:

Amylin

CCK:

Cholecystokinin

CGRP:

CT gene-related peptide

Ci:

Ciona intestinalis

CRSP:

CT receptor-stimulating peptide

CT:

Calcitonin

GnRH:

Gonadotropin-releasing hormone

OT:

Oxytocin

TK:

Tachykinin

TKRP:

TK-related peptide

VP:

Vasopressin

References

  • Adams BA, Tello JA, Erchegyi J, Warby C, Hong DJ, Akinsanya KO, Mackie GO, Vale W, Rivier JE, Sherwood NM (2003) Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology 144:1907–1919

    Article  CAS  Google Scholar 

  • Aikins MJ, Schooley DA, Begum K, Detheux M, Beeman RW, Park Y (2008) Vasopressin-like peptide and its receptor function in an indirect diuretic signaling pathway in the red flour beetle. Insect Biochem Mol Biol 38:740–748

    Article  CAS  Google Scholar 

  • Aoyama M, Kawada T, Fujie M, Hotta K, Sakai T, Sekiguchi T, Oka K, Satoh N, Satake H (2008) A novel biological role of tachykinins as an up-regulator of oocyte growth: identification of an evolutionary origin of tachykininergic functions in the ovary of the ascidian, Ciona intestinalis. Endocrinology 149:4346–4356

    Article  CAS  Google Scholar 

  • Aoyama M, Kawada T, Satake H (2012) Localization and enzymatic activity profiles of the proteases responsible for tachykinin-directed oocyte growth in the protochordate, Ciona intestinalis. Peptides 34:186–192

    Article  CAS  Google Scholar 

  • Beets I, Janssen T, Meelkop E, Temmerman L, Suetens N, Rademakers S, Jansen G, Schoofs L (2012) Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science 338:543–545

    Article  CAS  Google Scholar 

  • Cai W, Kim CH, Go HJ, Egertová M, Zampronio CG, Jones AM, Park NG, Elphick MR (2018) Biochemical, anatomical, and pharmacological characterization of calcitonin-type neuropeptides in starfish: discovery of an ancient role as muscle relaxants. Front Neurosci 12:382

    Article  Google Scholar 

  • Conner AC, Simms J, Hay DL, Mahmoud K, Howitt SG, Wheatley M, Poyner DR (2004) Heterodimers and family-B GPCRs: RAMPs, CGRP and adrenomedullin. Biochem Soc Trans 32:843–846

    Article  CAS  Google Scholar 

  • Elphick MR, Rowe ML (2009) NGFFFamide and echinotocin: structurally unrelated myoactive neuropeptides derived from neurophysin-containing precursors in sea urchins. J Exp Biol 212:1067–1077

    Article  CAS  Google Scholar 

  • Frank E, Landgraf R (2008) The vasopressin system—from antidiuresis to psychopathology. Eur J Pharmacol 583:226–242

    Article  CAS  Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683

    Article  CAS  Google Scholar 

  • Hasunuma I, Terakado K (2013) Two novel gonadotropin-releasing hormones (GnRHs) from the urochordate ascidian, Halocynthia roretzi: implications for the origin of vertebrate GnRH isoforms. Zool Sci 30:311–318

    Article  CAS  Google Scholar 

  • Horie T, Horie R, Chen K, Cao C, Nakagawa M, Kusakabe TG, Satoh N, Sasakura Y, Levine M (2018) Regulatory cocktail for dopaminergic neurons in a protovertebrate identified by whole-embryo single-cell transcriptomics. Genes Dev 32:1297–1302

    Article  CAS  Google Scholar 

  • Hoyle CHV (1998) Neuropeptide families: evolutionary perspectives. Regul Pept 73:1–33

    Article  CAS  Google Scholar 

  • Janssen T, Meelkop E, Lindemans M, Verstraelen K, Husson SJ, Temmerman L, Nachman RJ, Schoofs L (2008) Discovery of a cholecystokinin-gastrin-like signaling system in nematodes. Endocrinology 149:2826–2839

    Article  CAS  Google Scholar 

  • Jiang H, Lkhagva A, Daubnerová I, Chae HS, Å imo L, Jung SH, Yoon YK, Lee NR, Seong JY, Žitňan D, Park Y, Kim YJ (2013) Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects. Proc Natl Acad Sci USA 110:E3526–E3534

    Article  CAS  Google Scholar 

  • Johnsen AH (1998) Phylogeny of the cholecystokinin/gastrin family. Front Neuroendocrinol 19:73–99

    Article  CAS  Google Scholar 

  • Johnsen AH, Rehfeld JF (1990) Cionin: a disulfotyrosyl hybrid of cholecystokinin and gastrin from the neural ganglion of the protochordate Ciona intestinalis. J Biol Chem 265:3054–3058

    CAS  PubMed  Google Scholar 

  • Kah O, Lethimonier C, Somoza G, Guilgur LG, Vaillant C, Lareyre JJ (2007) GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol 153:346–364

    Article  CAS  Google Scholar 

  • Kamiya C, Ohta N, Ogura Y, Yoshida K, Horie T, Kusakabe TG, Satake H, Sasakura Y (2014) Nonreproductive role of gonadotropin-releasing hormone in the control of ascidian metamorphosis. Dev Dyn 243:1524–1535

    Article  CAS  Google Scholar 

  • Kanda A, Takahashi T, Satake H, Minakata H (2006) Molecular and functional characterization of a novel gonadotropin-releasing-hormone receptor isolated from the common octopus (Octopus vulgaris). Biochem J 395:125–135

    Article  CAS  Google Scholar 

  • Katafuchi T, Kikumoto K, Hamano K, Kangawa K, Matsuo H, Minamino N (2003) Calcitonin receptor-stimulating peptide, a new member of the calcitonin gene-related peptide family. Its isolation from porcine brain, structure, tissue distribution, and biological activity. J Biol Chem 278:12046–12054

    Article  CAS  Google Scholar 

  • Katafuchi T, Yasue H, Osaki T, Minamino N (2009) Calcitonin receptor-stimulating peptide: its evolutionary and functional relationship with calcitonin/calcitonin gene-related peptide based on gene structure. Peptides 30:1753–1762

    Article  CAS  Google Scholar 

  • Kavanaugh SI, Nozaki M, Sower SA (2008) Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey. Endocrinology 149:3860–3869

    Article  CAS  Google Scholar 

  • Kawada T, Sekiguchi T, Itoh Y, Ogasawara M, Satake H (2008) Characterization of a novel vasopressin/oxytocin superfamily peptide and its receptor from an ascidian, Ciona intestinalis. Peptides 29:1672–1678

    Article  CAS  Google Scholar 

  • Kawada T, Aoyama M, Okada I, Sakai T, Sekiguchi T, Ogasawara M, Satake H (2009a) A novel inhibitory gonadotropin-releasing hormone-related neuropeptide in the ascidian, Ciona intestinalis. Peptides 30:2200–2205

    Article  CAS  Google Scholar 

  • Kawada T, Sekiguchi T, Sugase K, Satake H (2009b) Evolutionary aspects of molecular forms and biological functions of oxytocin family peptides. In: Jastrow H, Feuerbach D (eds) Handbook of oxytocin research: synthesis, storage and release, actions and drug forms. Nova Science, Hauppage, NY, pp 59–85

    Google Scholar 

  • Kawada T, Sekiguchi T, Sakai T, Aoyama M, Satake H (2010) Neuropeptides, hormone peptides, and their receptors in Ciona intestinalis: an update. Zool Sci 27:134–153

    Article  CAS  Google Scholar 

  • Kawada T, Ogasawara M, Sekiguchi T, Aoyama M, Hotta K, Oka K, Satake H (2011) Peptidomic analysis of the central nervous system of the protochordate, Ciona intestinalis: homologs and prototypes of vertebrate peptides and novel peptides. Endocrinology 152:2416–2427

    Article  CAS  Google Scholar 

  • Kawada T, Aoyama M, Sakai T, Satake H (2013) Structure, function, and evolutionary aspects of invertebrate GnRHs and their receptors. In: Scott-Sills E (ed) Gonadotropin-releasing hormone (GnRH): production, structure and functions. Nova Science, New York, pp 1–16

    Google Scholar 

  • Kusakabe T, Mishima S, Shimada I, Kitajima Y, Tsuda M (2003) Structure, expression, and cluster organization of genes encoding gonadotropin-releasing hormone receptors found in the neural complex of the ascidian Ciona intestinalis. Gene 322:77–84

    Article  CAS  Google Scholar 

  • Matsubara S, Kawada T, Sakai T, Aoyama M, Osugi T, Shiraishi A, Satake H (2016) The significance of Ciona intestinalis as a stem organism in integrative studies of functional evolution of the chordate endocrine, neuroendocrine, and nervous systems. Gen Comp Endocrinol 227:101–108

    Article  CAS  Google Scholar 

  • Millar RP (2005) GnRHs and GnRH receptors. Anim Reprod Sci 88:5–28

    Article  CAS  Google Scholar 

  • Millar RP, Newton CL (2013) Current and future applications of GnRH, kisspeptin and neurokinin B analogues. Nat Rev Endocrinol 9:451–466

    Article  CAS  Google Scholar 

  • Millar RP, Lu ZL, Pawson AJ, Flanagan CA, Morgan K, Maudsley SR (2004) Gonadotropin-releasing hormone receptors. Endocr Rev 25:235–275

    Article  CAS  Google Scholar 

  • Nilsson IB, Svensson SP, Monstein HJ (2003) Molecular cloning of a putative Ciona intestinalis cionin receptor, a new member of the CCK/gastrin receptor family. Gene 323:79–88

    Article  CAS  Google Scholar 

  • Osugi T, Sasakura Y, Satake H (2017) The nervous system of the adult ascidian Ciona intestinalis Type A (Ciona robusta): insights from transgenic animal models. PLoS One 12:e0180227

    Article  Google Scholar 

  • Page NM (2006) Characterization of the gene structures, precursor processing and pharmacology of the endokinin peptides. Vasc Pharmacol 45:200–208

    Article  CAS  Google Scholar 

  • Powell JF, Reska-Skinner SM, Prakash MO, Fischer WH, Park M, Rivier JE, Craig AG, Mackie GO, Sherwood NM (1996) Two new forms of gonadotropin-releasing hormone in a protochordate and the evolutionary implications. Proc Natl Acad Sci USA 93:10461–10464

    Article  CAS  Google Scholar 

  • Roch GJ, Tello JA, Sherwood NM (2014) At the transition from invertebrates to vertebrates, a novel GnRH-like peptide emerges in amphioxus. Mol Biol Evol 31:765–778

    Article  CAS  Google Scholar 

  • Rowe ML, Elphick MR (2012) The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus. Gen Comp Endocrinol 179:331–344

    Article  CAS  Google Scholar 

  • Rowe ML, Achhala S, Elphick MR (2014) Neuropeptides and polypeptide hormones in echinoderms: new insights from analysis of the transcriptome of the sea cucumber Apostichopus japonicus. Gen Comp Endocrinol 197:43–55

    Article  CAS  Google Scholar 

  • Sakai T, Aoyama M, Kusakabe T, Tsuda M, Satake H (2010) Functional diversity of signaling pathways through G protein-coupled receptor heterodimerization with a species-specific orphan receptor subtype. Mol Biol Evol 27:1097–1106

    Article  CAS  Google Scholar 

  • Sakai T, Aoyama M, Kawada T, Kusakabe T, Tsuda M, Satake H (2012) Evidence for differential regulation of GnRH signaling via heterodimerization among GnRH receptor paralogs in the protochordate, Ciona intestinalis. Endocrinology 153:1841–1849

    Article  CAS  Google Scholar 

  • Sakai T, Shiraishi A, Kawada T, Matsubara S, Aoyama M, Satake H (2017) Invertebrate gonadotropin-releasing hormone-related peptides and their receptors: an update. Front Endocrinol (Lausanne) 8:217

    Article  Google Scholar 

  • Satake H, Kawada T (2006a) Neuropeptides, hormones, and their receptors in ascidians: emerging model animals. In: Satake H (ed) Invertebrate neuropeptides and hormones: basic knowledge and recent advances. Transworld Research Network, Trivandrum, pp 253–276

    Google Scholar 

  • Satake H, Kawada T (2006b) Overview of the primary structure, tissue-distribution, and functions of tachykinins and their receptors. Curr Drug Targets 7:963–974

    Article  CAS  Google Scholar 

  • Satake H, Takuwa K, Minakata H, Matsushima O (1999) Evidence for conservation of the vasopressin/oxytocin superfamily in Annelida. J Biol Chem 274:5605–5611

    Article  CAS  Google Scholar 

  • Satake H, Kawada T, Nomoto K, Minakata H (2003) Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: a review. Zool Sci 20:533–549

    Article  CAS  Google Scholar 

  • Satake H, Ogasawara M, Kawada T, Masuda K, Aoyama M, Minakata H, Chiba T, Metoki H, Satou Y, Satoh N (2004) Tachykinin and tachykinin receptor of an ascidian, Ciona intestinalis: evolutionary origin of the vertebrate tachykinin family. J Biol Chem 279:53798–53805

    Article  CAS  Google Scholar 

  • Satake H, Matsubara S, Aoyama M, Kawada T, Sakai T (2013) GPCR heterodimerization in the reproductive system: functional regulation and implication for biodiversity. Front Endocrinol (Lausanne) 4:100

    Article  Google Scholar 

  • Satoh N (2015) Two decades of ascidian developmental biology: a personal research story. Curr Top Dev Biol 117:289–300

    Article  Google Scholar 

  • Sekiguchi T (2018) The calcitonin/calcitonin gene-related peptide family in invertebrate deuterostomes. Front Endocrinol (Lausanne) 9:695

    Article  Google Scholar 

  • Sekiguchi T, Suzuki N, Fujiwara N, Aoyama M, Kawada T, Sugase K, Murata Y, Sasayama Y, Ogasawara M, Satake H (2009) Calcitonin in a protochordate, Ciona intestinalis—the prototype of the vertebrate calcitonin/calcitonin gene-related peptide superfamily. FEBS J 276:4437–4447

    Article  CAS  Google Scholar 

  • Sekiguchi T, Ogasawara M, Satake H (2012) Molecular and functional characterization of cionin receptors in the ascidian, Ciona intestinalis: the evolutionary origin of the vertebrate cholecystokinin/gastrin family. J Endocrinol 213:99–106

    Article  CAS  Google Scholar 

  • Sekiguchi T, Kuwasako K, Ogasawara M, Takahashi H, Matsubara S, Osugi T, Muramatsu I, Sasayama Y, Suzuki N, Satake H (2016) Evidence for conservation of the calcitonin superfamily and activity-regulating mechanisms in the basal chordate Branchiostoma floridae: insights into the molecular and functional evolution in chordates. J Biol Chem 291:2345–2356

    Article  CAS  Google Scholar 

  • Sekiguchi T, Shiraishi A, Satake H, Kuwasako K, Takahashi H, Sato M, Urata M, Wada S, Endo M, Ikari T, Hattori A, Srivastav AK, Suzuki N (2017) Calcitonin-typical suppression of osteoclastic activity by amphioxus calcitonin superfamily peptides and insights into the evolutionary conservation and diversity of their structures. Gen Comp Endocrinol 246:294–300

    Article  CAS  Google Scholar 

  • Semmens DC, Mirabeau O, Moghul I, Pancholi MR, Wurm Y, Elphick MR (2016) Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution. Open Biol 6:150224

    Article  Google Scholar 

  • Sherwood NM, Tello JA, Roch GJ (2006) Neuroendocrinology of protochordates: insights from Ciona genomics. Comp Biochem Physiol A Mol Integr Physiol 144:254–271

    Article  Google Scholar 

  • Stafflinger E, Hansen KK, Hauser F, Schneider M, Cazzamali G, Williamson M, Grimmelikhuijzen CJ (2008) Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects. Proc Natl Acad Sci USA 105:3262–3267

    Article  CAS  Google Scholar 

  • Steinhoff MS, von Mentzer B, Geppetti P, Pothoulakis C, Bunnett NW (2014) Tachykinins and their receptors: contributions to physiological control and the mechanisms of disease. Physiol Rev 94:265–301

    Article  CAS  Google Scholar 

  • Suwansa-Ard S, Chaiyamoon A, Talarovicova A, Tinikul R, Tinikul Y, Poomtong T, Elphick MR, Cummins SF, Sobhon P (2018) Transcriptomic discovery and comparative analysis of neuropeptide precursors in sea cucumbers (Holothuroidea). Peptides 99:231–240

    Article  CAS  Google Scholar 

  • Tello JA, Sherwood NM (2009) Amphioxus: beginning of vertebrate and end of invertebrate type GnRH receptor lineage. Endocrinology 150:2847–2856

    Article  CAS  Google Scholar 

  • Tello JA, Rivier JE, Sherwood NM (2005) Tunicate gonadotropin-releasing hormone (GnRH) peptides selectively activate Ciona intestinalis GnRH receptors and the green monkey type II GnRH receptor. Endocrinology 146:4061–4073

    Article  CAS  Google Scholar 

  • Tian S, Zandawala M, Beets I, Baytemur E, Slade SE, Scrivens JH, Elphick MR (2016) Urbilaterian origin of paralogous GnRH and corazonin neuropeptide signaling pathways. Sci Rep 6:28788

    Article  CAS  Google Scholar 

  • Ukena K, Iwakoshi-Ukena E, Hikosaka A (2008) Unique form and osmoregulatory function of a neurohypophysial hormone in a urochordate. Endocrinology 149:5254–5261

    Article  CAS  Google Scholar 

Download references

Acknowledgments

All ascidians were provided by Kyoto University through the National Bio-Resource Project of the MEXT, Japan. This study was funded by the Japan Society for the Promotion of Sciences, grant 16K07430 to H.S.

Author information

Authors and Affiliations

  1. Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan

    Honoo Satake, Shin Matsubara, Akira Shiraishi, Tatsuya Yamamoto, Tomohiro Osugi, Tsubasa Sakai & Tsuyoshi Kawada

Authors
  1. Honoo Satake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shin Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akira Shiraishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tatsuya Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomohiro Osugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tsubasa Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tsuyoshi Kawada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Honoo Satake .

Editor information

Editors and Affiliations

  1. Institute of Zoology and Biomedical Research, Jagiellonian University, Krakow, Poland

    Waclaw Tworzydlo

  2. Institute of Zoology and Biomedical Research, Jagiellonian University, Krakow, Poland

    Szczepan M. Bilinski

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Satake, H. et al. (2019). Neuropeptides, Peptide Hormones, and Their Receptors of a Tunicate, Ciona intestinalis . In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_5

Download citation

Publish with us

Policies and ethics

Search

Navigation