Abstract
Marine invertebrates employ external fertilization to take the advantages of sexual reproduction as one of excellent survival strategies. To prevent mismatching, successful fertilization can be made only after going though strictly defined steps in the fertilization. In sea stars, the fertilization process starts with the chemotaxis of sperm followed by hyperactivation of sperm upon arriving onto the egg coat, and then sperm penetrate to the egg coat before achieving the fusion. To investigate whether the initiation of chemotaxis and the following signaling has species specificity, we conducted comparative studies in the protein level among sea stars, Asterias amurensis, A. forbesi, and Asterina pectinifera. Since transcription of messenger ribonucleic acid (mRNA) has been suppressed in gamete, the roles of sperm proteins during the fertilization cannot be investigated by examining the mRNA profile. Therefore, proteomics analysis by mass spectrometry was used in this study. In sea stars, upon receiving asteroidal sperm-activating peptide (asterosap), the receptor membrane-bound guanylate cyclases in the sperm tail trigger sperm chemotaxis. We confirmed the presence of membrane-bound guanylate cyclases in the three sea star species, and they all had the same structural domains including the extracellular domain, kinase-like domain, and guanylate cyclase domain. The majority of peptides recovered were from α-helices distributed on the solvent side of the protein. More peptides were recovered from the intracellular domains. The transmembrane domain has not been recovered. The functions of the receptors seemed to be conserved among the species. Furthermore, we identified proteins that may be involved in the guanylate cyclase-triggered signaling pathway.
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References
Afzelius BA (1992) Section staining for electron microscopy using tannic acid as a mordant: a simple method for visualization of glycogen and collagen. Microsc Res Technol 21:65–72
Baccetti B, Afzelius BA (1976) The biology of the sperm cell. Monogr Dev Biol 10:1–254
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2007) GenBank. Nucleic Acids Res 35:D21–D25
Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, Gasteiger E, Martin MJ, Michoud K, O’Donovan C, Phan I, Pilbout S, Schneider M (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31:365–370
Bohmer M, Van Q, Weyand I, Hagen V, Beyermann M, Matsumoto M, Hoshi M, Hildebrand E, Kaupp UB (2005) Ca2+ spikes in the flagellum control chemotactic behavior of sperm. Embo J 24:2741–2752
Fitzpatrick DA, O’Halloran DM, Burnell AM (2006) Multiple lineage specific expansions within the guanylyl cyclase gene family. BMC Evol Biol 6:26
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723
Hempel LU, Rathke C, Raja SJ, Renkawitz-Pohl R (2006) In Drosophila, don juan and don juan like encode proteins of the spermatid nucleus and the flagellum and both are regulated at the transcriptional level by the TAF II80 cannonball while translational repression is achieved by distinct elements. Dev Dyn 235:1053–1064
Inaba K, Padma P, Satouh Y, Shin IT, Kohara Y, Satoh N, Satou Y (2002) EST analysis of gene expression in testis of the ascidian Ciona intestinalis. Mol Reprod Dev 62:431–445
Islam MS, Kawase O, Hase S, Minakata H, Hoshi M, Matsumoto M (2006) Na(+)/Ca(2+) exchanger contributes to asterosap-induced elevation of intracellular Ca(2+) concentration in starfish spermatozoa. Zygote 14:133–141
Kawase O, Minakata H, Hoshi M, Matsumoto M (2005) Asterosap-induced elevation in intracellular pH is indispensable for ARIS-induced sustained increase in intracellular Ca2+ and following acrosome reaction in starfish spermatozoa. Zygote 13:63–71
Kelley LA, MacCallum RM, Sternberg MJ (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 299:499–520
Kopp J, Schwede T (2006) The SWISS-MODEL Repository: new features and functionalities. Nucleic Acids Res 34:D315–D318
Martinez-Heredia J, Estanyol JM, Ballesca JL, Oliva R (2006) Proteomic identification of human sperm proteins. Proteomics 6:4356–4369
Matsui T, Nishiyama I, Hino A, Hoshi M (1986) Induction of the acrosome reaction in starfish. Develop Growth Differ 28:339–348
Matsumoto M, Briones AV, Nishigaki T, Hoshi M (1999) Sequence analysis of cDNAs encoding precursors of starfish asterosaps. Dev Genet 25:130–136
Matsumoto M, Solzin J, Helbig A, Hagen V, Ueno S, Kawase O, Maruyama Y, Ogiso M, Godde M, Minakata H, Kaupp UB, Hoshi M, Weyand I (2003) A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm. Dev Biol 260:314–324
Matsumura K, Aketa K (1991) Proteasome (multicatalytic proteinase) of sea urchin sperm and its possible participation in the acrosome reaction. Mol Reprod Dev 29:189–199
Morales P, Kong M, Pizarro E, Pasten C (2003) Participation of the sperm proteasome in human fertilization. Hum Reprod 18:1010–1017
Nakachi M, Moriyama H, Hoshi M, Matsumoto M (2006) Acrosome reaction is subfamily specific in sea star fertilization. Dev Biol 298:597–604
Nishigaki T, Chiba K, Hoshi M (2000) A 130-kDa membrane protein of sperm flagella is the receptor for asterosaps, sperm-activating peptides of starfish Asterias amurensis. Dev Biol 219:154–162
Ogawa H, Qiu Y, Ogata CM, Misono KS (2004) Crystal structure of hormone-bound atrial natriuretic peptide receptor extracellular domain: rotation mechanism for transmembrane signal transduction. J Biol Chem 279:28625–28631
Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
Rohila JS, Chen M, Chen S, Chen J, Cerny R, Dardick C, Canlas P, Xu X, Gribskov M, Kanrar S, Zhu JK, Ronald P, Fromm ME (2006) Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J 46:1–13
Sawada H (2002) Ascidian sperm lysin system. Zool Sci 19:139–151
Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H (2002) Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci USA 99:1223–1228
Shiba K, Tagata T, Ohmuro J, Mogami Y, Matsumoto M, Hoshi M, Baba SA (2006) Peptide-induced hyperactivation-like vigorous flagellar movement in starfish sperm. Zygote 14:23–32
Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE, Day BN (2004) Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod 71:1625–1637
Takizawa S, Sawada H, Someno T, Saitoh Y, Yokosawa H, Hoshi M (1993) Effects of protease inhibitors on binding of sperm to the vitelline coat of ascidian eggs: implications for participation of a proteasome (multicatalytic proteinase complex). J Exp Zool 267:86–91
Tesmer JJ, Dessauer CW, Sunahara RK, Murray LD, Johnson RA, Gilman AG, Sprang SR (2000) Molecular basis for P-site inhibition of adenylyl cyclase. Biochemistry 39:14464–14471
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Vacquier VD (1998) Evolution of gamete recognition proteins. Science 281:1995–1998
Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, Jones CM, Marshall CJ, Springer CJ, Barford D, Marais R (2004) Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116:855–867
Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Mazumder R, O’Donovan C, Redaschi N, Suzek B (2006) The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res 34:D187–D191
Acknowledgments
We thank Dr. Kohei Homma and Ms. Brittney Schirber for their technical assistance. The mass spectrometry facility is supported in part by NIH Grant P20 RR15635 from the COBRE Program of the National Center for Research Resources, NCI Cancer Center Support Grant P30 CA36727, NIH grant RR015468-01, and the Nebraska Research Initiative.
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Nakachi, M., Matsumoto, M., Terry, P.M. et al. Identification of Guanylate Cyclases and Related Signaling Proteins in Sperm Tail from Sea Stars by Mass Spectrometry. Mar Biotechnol 10, 564–571 (2008). https://doi.org/10.1007/s10126-008-9096-7
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DOI: https://doi.org/10.1007/s10126-008-9096-7