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Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra

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Abstract

From an evolutionary point of view, Hydra has one of the most primitive nervous systems among metazoans. Two different groups of peptides that affect neuron differentiation were identified in a systematic screening of peptide signaling molecules in Hydra. Within the first group of peptides, a neuropeptide, Hym-355, was previously shown to positively regulate neuron differentiation. The second group of peptides encompasses the PW family of peptides that negatively regulate neuron differentiation. In this study, we identified the gene encoding PW peptide preprohormone. Moreover, we made the antibody that specifically recognizes LPW. In situ hybridization and immunohistochemical analyses showed that the PW peptides and the gene encoding them were expressed in ectodermal epithelial cells throughout the body except for the basal disk. The PW peptides are produced by epithelial cells and are therefore termed “epitheliopeptides.” Together with Hym-355, the PW family peptides mediate communication between neurons and epithelial cells and thereby maintain a specific density of neurons in Hydra.

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References

  • Bode HR, Berking S, David CN, Gierer A, Schaller HC, Trenkner E (1973) Quantitative analysis of cell types during growth and regeneration in hydra. Wilhelm Roux’s Arch Entwicklungsmech Org 117:269–285

    Article  Google Scholar 

  • Bode HR, Heimfeld S, Chow M, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122:577–585

    Article  PubMed  CAS  Google Scholar 

  • Bode HR, Gee LW, Chow MA (1990) Neuron differentiation in hydra involves dividing intermediates. Dev Biol 139:231–243

    Article  PubMed  CAS  Google Scholar 

  • Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191

    Article  Google Scholar 

  • Campbell RD (1967a) Tissue dynamics of steady-state growth in Hydra litoralis. I. Patterns of cell division. Dev Biol 15:487–502

    Article  PubMed  CAS  Google Scholar 

  • Campbell RD (1967b) Tissue dynamics of steady-state growth in Hydra litoralis. II. Patterns of tissue movement. J Morphol 121:19–28

    Article  PubMed  CAS  Google Scholar 

  • Campbell RD (1973) Vital marking of single cells in developing tissues: India ink injection to trace tissue movements in Hydra. J Cell Sci 23:651–661

    Google Scholar 

  • Campbell RD (1976) Elimination of Hydra interstitial and nerve cells by means of colchicines. J Cell Sci 21:1–13

    PubMed  CAS  Google Scholar 

  • David CN (1973) A quantitative method for maceration of hydra tissue. Wilhelm Roux’s Arch Entwickl.mech. Org 171:259–268

    Article  Google Scholar 

  • David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359–375

    PubMed  CAS  Google Scholar 

  • Dunne J, Javois LC, Huang LW, Bode HR (1985) A subset of cells in the nerve net of Hydra oligactis defined by a monoclonal antibody: its arrangement and development. Dev Biol 109:41–53

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa T (1989) Role of interstitial cell migration in generating position-dependent patterns of nerve cell differentiation in Hydra. Dev Biol 133:77–82

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa T (2008) Hydra peptide project 1993–2007. Dev Growth Differ 50(Suppl 1):S257–268

    PubMed  CAS  Google Scholar 

  • Grens A, Gee L, Fisher DA, Bode HR (1996) CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in Hydra. Dev Biol 180:473–488

    Article  PubMed  CAS  Google Scholar 

  • Grimmelikhuijzen CJP, Dockray GJ, Schot LPC (1982a) FMRFamide-like immunoreactivity in the nervous system of hydra. Histochemistry 73:499–508

    Article  PubMed  CAS  Google Scholar 

  • Grimmelikhuijzen CJP, Dierickx K, Boer GJ (1982b) Oxytocin/vasopression-like immunoreactivity in the nervous system of hydra. Neuroscience 7:3191–3199

    Article  PubMed  CAS  Google Scholar 

  • Hager G, David CN (1997) Pattern of differentiated nerve cells in hydra is determined by precursor migration. Development 124:569–576

    PubMed  CAS  Google Scholar 

  • Hansen GN, Williamson M, Grimmelikhuijzen CJP (2002) A new case of neuropeptide coexpression (RGamide and LWamides) in Hydra, found by whole-mount, two-color double-labeling in situ hybridization. Cell Tissue Res 308(1):157–165

    Article  PubMed  CAS  Google Scholar 

  • Harafuji N, Takahashi T, Hatta M, Tezuka H, Morishita F, Matsushima O, Fujisawa T (2001) Enhancement of foot formation in Hydra by a novel epitheliopeptide, Hym-323. Development 128:437–446

    PubMed  CAS  Google Scholar 

  • Hayakawa E, Fujisawa C, Fujisawa T (2004) Involvement of Hydra achaete-scute gene, CnASH in the differentiation pathway of sensory neurons in the tentacles. Dev Genes Evol 214:486–492

    PubMed  CAS  Google Scholar 

  • Hayakawa E, Takahashi T, Nishimiya-Fujisawa T, Fujisawa T (2007) A novel neuropeptide (FRamide) family identified by a peptidomic approach in Hydra magnipapillata. FEBS J 274:5438–5448

    Article  PubMed  CAS  Google Scholar 

  • Heimfeld S, Bode HR (1984) Interstitial cell migration in Hydra attenuata. I. Selective migration of nerve cell precursors as the basis for position-dependent nerve cell differentiation. Dev Biol 105:10–17

    Article  PubMed  CAS  Google Scholar 

  • Holstein TW, Mala C, Kurz E, Bauer K, Greber M, David CN (1992) The primitive metazoan Hydra expresses antistasin, a serine protease inhibitor of vertebrate blood coagulation: cDNA cloning, cellular localization and developmental regulation. FEBS Lett 309:288–292

    Article  PubMed  CAS  Google Scholar 

  • Javois LC, Wood RD, Bode HR (1986) Patterning of the head in hydra as visualized by a monoclonal antibody. I. Budding and regeneration. Dev Biol 117:607–618

    Article  PubMed  CAS  Google Scholar 

  • Khalturin K, Anton-Erxleben F, Sassmann S, Wittlieb J, Hemmrich G, Bosch TCG (2008) A novel gene family controls species-specific morphological traits in Hydra. PLoS Biol 6:2436–2449

    Article  CAS  Google Scholar 

  • Koizumi O, Heimfeld S, Bode HR (1988) Plasticity in the nervous system of adult hydra. II. Conversion of ganglion cells of the body column into epidermal sensory cells of the hypostome. Dev Biol 129:358–371

    Article  PubMed  CAS  Google Scholar 

  • Leviev I, Williamson M, Grimmelikhuijzen CJP (1997) Molecular cloning of a preprohormone from Hydra magnipapillata containing multiple copies of Hydra-LWamide (Leu-Trp-NH2) neuropeptides: Evidence for processing at Ser and Asn residues. J Neurochem 68:1319–1325

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971

    Article  PubMed  CAS  Google Scholar 

  • Marcum BA, Campbell RD (1978) Development of hydra lacking nerve and interstitial cells. J Cell Sci 29:17–33

    PubMed  CAS  Google Scholar 

  • Minobe S, Koizumi O, Sugiyama T (1995) Nerve cell differentiation in nerve-free tissue of epithelial hydra from precursor cells introduced by grafting I. Tentacles and hypostome. Dev Biol 172:170–181

    Article  PubMed  CAS  Google Scholar 

  • Nishimiya-Fujisawa C, Sugiyama T (1993) Genetic analysis of developmental mechanisms in Hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. Dev Biol 157:1–9

    Article  PubMed  CAS  Google Scholar 

  • Peerters JM, Hazendonk TG, Beuvery EC, Tesser GI (1989) Comparison of four bifunctional reagents for coupling peptides to proteins and the effect of the three moieties on the immunogenicity of the conjugates. J Immunol Meth 120:133–143

    Article  Google Scholar 

  • Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci 85:197–215

    PubMed  CAS  Google Scholar 

  • Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in hydra. I. Sexual reproduction of Hydra magnipapillata and isolation of mutants. Dev Growth Differ 19:187–200

    Article  Google Scholar 

  • Sugiyama T, Fujisawa T (1978) Genetic analysis of developmental mechanisms in hydra. II. Isolation and characterization of an interstitial cell-deficient strain. J Cell Sci 29:35–52

    PubMed  CAS  Google Scholar 

  • Sugiyama T, Fujisawa T (1979) Genetic analysis of developmental mechanisms in hydra VI. Cellular composition of chimera hydra. J Cell Sci 35:1–15

    PubMed  CAS  Google Scholar 

  • Takahashi T, Muneoka Y, Lohmann J, deHaro LM, Solleder G, Bosch TCG, David CN, Bode HR, Koizumi O, Shimizu H, Hatta M, Fujisawa T, Sugiyama T (1997) Systematic isolation of peptide signal molecules regulating development in hydra: Lwamide and PW families. Proc Natl Acad Sci USA 94:1241–1246

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TCG, Kobayakawa Y, Mohri S, Bode HR, Yum S, Hatta M, Fujisawa T (2000) A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development 127:997–1005

    PubMed  CAS  Google Scholar 

  • Takahashi T, Kobayakawa Y, Muneoka Y, Fujisawa Y, Mohri S, Hatta M, Shimizu H, Fujisawa T, Sugiyama T, Takahara M, Yanagi K, Koizumi O (2003) Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps. Comp Biochem Physiol Part B 135:309–324

    Article  CAS  Google Scholar 

  • Takahashi T, Hatta M, Yum S, Gee L, Ohtani M, Fujisawa T, Bode HR (2005) Hym-301, a novel peptide, regulates the number of tentacles formed in hydra. Development 132:2225–2234

    Article  PubMed  CAS  Google Scholar 

  • Technau U, Holstein TW (1996) Phenotypic maturation of neurons and continuous precursor migration in the formation of the peduncle nerve net in Hydra. Dev Biol 177:599–615

    Article  PubMed  CAS  Google Scholar 

  • Teragawa CK, Bode HR (1990) Special and temporal patterns of interstitial cell migration in Hydra vulgaris. Dev Biol 138:63–81

    Article  PubMed  CAS  Google Scholar 

  • Teragawa CK, Bode HR (1995) Migrating interstitial cells differentiate into neurons in hydra. Dev Biol 171:286–293

    Article  PubMed  CAS  Google Scholar 

  • von Heijne G (1983) Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133:17–21

    Article  Google Scholar 

  • Yum S, Takahashi T, Koizumi O, Ariura Y, Kobayakawa Y, Mohri S, Fujisawa T (1998) A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Commun 248:584–590

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We greatly appreciated the excellent technical assistance of the late Mr. Norio Sugimoto. This work was supported in part by grants from the Ministry of Education, Science, Sport and Culture of Japan (to T.F., O.K., Y.K., and T.S.), the Sumitomo Foundation and Japan Space Forum (Ground Research Announcement for Space Utilization) (to T.F.), and Deutche Forschungsgemeinschaft (DFG) (to T.C.G.B. and C.N.D). This work was also supported in part by a Grant-in-Aid for young Scientists (T.T.). T.F. was a Mercator Professor at University of Heidelberg from 2007~2008 funded by DFG and would express his appreciation for the kind hospitality of Prof. Thomas Holstein.

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Correspondence to Toshitaka Fujisawa.

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Communicated by: M.Q. Martindale

Toshio Takahashi, Osamu Koizumi equally contributed to this study.

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Fig. S1

Nucleotide and deduced amino acid sequence of the gene encoding the PW family peptides. The predicted signal sequence (Von Heijne 1983) is thickly underlined. Known PW peptides (Takahashi Et Al. 1997) are thinly underlined, and putative PW peptides are underlined with a dotted line. Hym-1397 (TPALHW) is underlined with a double line. The asterisk indicates a stop codon. A possible polyadenylation signal is highlighted in red (GIF 247 KB).

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Takahashi, T., Koizumi, O., Hayakawa, E. et al. Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra . Dev Genes Evol 219, 119–129 (2009). https://doi.org/10.1007/s00427-009-0272-1

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