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Immunoglobulin-Like Domains Have an Evolutionarily Conserved Role During Gamete Fusion in C. elegans and Mouse

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Origin and Evolution of Biodiversity

Abstract

The spe-9 class genes are predominantly or exclusively expressed in the C. elegans male germline and play critical roles during gamete fusion. However, it is a challenge to identify mammalian orthologs that exhibit similar functions to those of the spe-9 class, since reproductive genes evolve much faster than somatic genes. In the mouse, Izumo1 gene encodes a sperm-specific transmembrane (TM) protein with the immunoglobulin (Ig)-like domain that indispensably acts during gamete fusion. The C. elegans gene spe-45 was recently identified by forward and reverse genetic approaches. It shows male germline-enriched expression and encodes an Ig-like TM protein like IZUMO1. Worms lacking spe-45 produce otherwise normal spermatozoa that are incapable of fusing with oocytes. Thus, spe-45 is a new member of the spe-9 class, and the phenotype of spe-45 mutant worms is essentially the same as that of Izumo1-knockout mice. Moreover, the Ig-like domains of SPE-45 and IZUMO1 possess similar roles to each other during gamete fusion. This indicates that C. elegans spe-45 is functionally equivalent to mouse Izumo1 and that their roles during gamete fusion have been conserved for ~1 billion years. Intriguingly, diverged organisms also have TM proteins with Ig-like domains that are involved during gamete interactions. This suggests the evolutionarily conserved roles of the Ig-like domains during fertilization, which are presumably related to associating with cis- and/or trans-partners.

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References

  • Argon Y, Ward S (1980) Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics 96(2):413–433

    PubMed  PubMed Central  CAS  Google Scholar 

  • Aydin H, Sultana A, Li S, Thavalingam A, Lee JE (2016) Molecular architecture of the human sperm IZUMO1 and egg JUNO fertilization complex. Nature 534(7608):562–565. https://doi.org/10.1038/nature18595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beech DJ, Bahnasi YM, Dedman AM, Al-Shawaf E (2009) TRPC channel lipid specificity and mechanisms of lipid regulation. Cell Calcium 45(6):583–588

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bianchi E, Doe B, Goulding D, Wright GJ (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508(7497):483–487. https://doi.org/10.1038/nature13203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borden KL (2000) RING domains: master builders of molecular scaffolds? J Mol Biol 295(5):1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chatterjee I, Richmond A, Putiri E, Shakes DC, Singson A (2005) The Caenorhabditis elegans spe-38 gene encodes a novel four-pass integral membrane protein required for sperm function at fertilization. Development 132:2795–2808

    Article  CAS  PubMed  Google Scholar 

  • Cordle J, Johnson S, Tay JZ, Roversi P, Wilkin MB, de Madrid BH, Shimizu H, Jensen S, Whiteman P, Jin B, Redfield C, Baron M, Lea SM, Handford PA (2008) A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition. Nat Struct Mol Biol 15(8):849–857

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doniach T, Hodgkin J (1984) A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 106(1):223–235

    Article  CAS  PubMed  Google Scholar 

  • Ferris PJ, Woessner JP, Goodenough UW (1996) A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol Biol Cell 7(8):1235–1248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Florman HM, Fissore RA (2014) Fertilization in mammals. In: Plant TM, Zeleznik AJ (eds) Knobil and Neill’s physiology of reproduction, 4th edn. Elsevier Academic Press, Amsterdam (Netherlands), pp 149–196

    Google Scholar 

  • Grayson P (2015) Izumo1 and Juno: the evolutionary origins and coevolution of essential sperm-egg binding partners. R Soc Open Sci 2(12):150296. https://doi.org/10.1098/rsos.150296

    Article  PubMed  PubMed Central  Google Scholar 

  • Grzmil P, Kim Y, Shamsadin R, Neesen J, Adham IM, Heinlein UA, Schwarzer UJ, Engel W (2001) Human cyritestin genes (CYRN1 and CYRN2) are non-functional. Biochem J 357(Pt 2):551–556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, Singh RS (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177(3):1321–1335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49(1):200–219

    Article  CAS  PubMed  Google Scholar 

  • Igakura T, Kadomatsu K, Kaname T, Muramatsu H, Fan QW, Miyauchi T, Toyama Y, Kuno N, Yuasa S, Takahashi M, Senda T, Taguchi O, Yamamura K, Arimura K, Muramatsu T (1998) A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev Biol 194(2):152–165

    Article  CAS  PubMed  Google Scholar 

  • Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434(7030):234–238

    Article  CAS  PubMed  Google Scholar 

  • Inoue N, Nishikawa T, Ikawa M, Okabe M (2012) Tetraspanin-interacting protein IGSF8 is dispensable for mouse fertility. Fertil Steril 98(2):465–470. https://doi.org/10.1016/j.fertnstert

    Article  PubMed  CAS  Google Scholar 

  • Inoue N, Hamada D, Kamikubo H, Hirata K, Kataoka M, Yamamoto M, Ikawa M, Okabe M, Hagihara Y (2013) Molecular dissection of IZUMO1, a sperm protein essential for sperm-egg fusion. Development 140(15):3221–3229. https://doi.org/10.1242/dev.094854

    Article  PubMed  CAS  Google Scholar 

  • Inoue N, Hagihara Y, Wright D, Suzuki T, Wada I (2015) Oocyte-triggered dimerization of sperm IZUMO1 promotes sperm-egg fusion in mice. Nat Commun 6:8858. https://doi.org/10.1038/ncomms9858

    Article  PubMed  CAS  Google Scholar 

  • Jury JA, Frayne J, Hall L (1997) The human fertilin alpha gene is non-functional: implications for its proposed role in fertilization. Biochem J 321(Pt 3):577–581

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karadge UB, Gosto M, Nicotra ML (2015) Allorecognition proteins in an invertebrate exhibit homophilic interactions. Curr Biol 25(21):2845–2850. https://doi.org/10.1016/j.cub.2015.09.030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato K, Satouh Y, Nishimasu H, Kurabayashi A, Morita J, Fujihara Y, Oji A, Ishitani R, Ikawa M, Nureki O (2016) Structural and functional insights into IZUMO1 recognition by JUNO in mammalian fertilization. Nat Commun 7:12198. https://doi.org/10.1038/ncomms12198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kimble J, Ward S (1988) Germ-line development and fertilization. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 191–213

    Google Scholar 

  • Krauchunas AR, Singson A (2016) Marriage shrines and worms impacting our understanding of mammalian fertilization. Worm 5(3):e1184389

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krauchunas AR, Marcello MR, Singson A (2016) The molecular complexity of fertilization: introducing the concept of a fertilization synapse. Mol Reprod Dev 83(5):376–386. https://doi.org/10.1002/mrd.22634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kroft TL, Gleason EJ, L’Hernault SW (2005) The spe-42 gene is required for sperm-egg interactions during C. elegans fertilization and encodes a sperm-specific transmembrane protein. Dev Biol 286:169–181

    Article  CAS  PubMed  Google Scholar 

  • L’Hernault SW (1997) Male germline. In: Riddle D, Blumenthal R, Meyer BJ, Priess J (eds) C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 271–294

    Google Scholar 

  • L’Hernault SW (2009) The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol 306(1–2):59–65. https://doi.org/10.1016/j.mce.2009.01.008

    Article  PubMed  CAS  Google Scholar 

  • L’Hernault SW, Singson AW (2000) Developmental genetics of spermatogenesis in the nematode Caenorhabditis elegans. In: Goldberg E (ed) The testes: from stem cell to sperm function, Serono Symposium USA. Springer, New York, pp 109–119

    Google Scholar 

  • L’Hernault SW, Shakes DC, Ward S (1988) Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120(2):435–452

    PubMed  PubMed Central  Google Scholar 

  • Lorenzetti D, Poirier C, Zhao M, Overbeek PA, Harrison W, Bishop CE (2014) A transgenic insertion on mouse chromosome 17 inactivates a novel immunoglobulin superfamily gene potentially involved in sperm-egg fusion. Mamm Genome 25(3–4):141–148. https://doi.org/10.1007/s00335-013-9491-x

    Article  PubMed  CAS  Google Scholar 

  • Machaca K, DeFelice LJ, L’Hernault SW (1996) A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol 176(1):1–16

    Article  CAS  PubMed  Google Scholar 

  • McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205(1):111–128

    Article  CAS  PubMed  Google Scholar 

  • Misamore MJ, Gupta S, Snell WJ (2003) The Chlamydomonas Fus1 protein is present on the mating type plus fusion organelle and required for a critical membrane adhesion event during fusion with minus gametes. Mol Biol Cell 14(6):2530–2542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miyamoto T (2006) The dendritic cell-specific transmembrane protein DC-STAMP is essential for osteoclast fusion and osteoclast bone-resorbing activity. Mod Rheumatol 16(6):341–342

    Article  CAS  PubMed  Google Scholar 

  • Mori T, Igawa T (2014) Gamete attachment process revealed in flowering plant fertilization. Plant Signal Behav 9(12):e977715. https://doi.org/10.4161/15592324.2014.977715

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mori T, Igawa T, Tamiya G, Miyagishima SY, Berger F (2014) Gamete attachment requires GEX2 for successful fertilization in Arabidopsis. Curr Biol 24(2):170–175. https://doi.org/10.1016/j.cub.2013.11.030

    Article  PubMed  CAS  Google Scholar 

  • Nelson GA, Ward S (1980) Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19(2):457–464

    Article  CAS  PubMed  Google Scholar 

  • Nishimura H, L’Hernault SW (2010) Spermatogenesis-defective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction. Dev Dyn 239(5):1502–1514. https://doi.org/10.1002/dvdy.22271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura H, L’Hernault SW (2016) Gamete interactions require transmembranous immunoglobulin-like proteins with conserved roles during evolution. Worm 5(3):e1197485

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nishimura H, L’Hernault SW (2017) Spermatogenesis. Curr Biol 27(18):R988–R994. https://doi.org/10.1016/j.cub.2017.07.067

    Article  PubMed  CAS  Google Scholar 

  • Nishimura H, Cho C, Branciforte DR, Myles DG, Primakoff P (2001) Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta. Dev Biol 233(1):204–213

    Article  CAS  PubMed  Google Scholar 

  • Nishimura H, Kim E, Nakanishi T, Baba T (2004) Possible function of the ADAM1a/ADAM2 Fertilin complex in the appearance of ADAM3 on the sperm surface. J Biol Chem 279(33):34957–34962

    Google Scholar 

  • Nishimura H, Tajima T, Comstra HS, Gleason EJ, L’Hernault SW (2015) The immunoglobulin-like gene spe-45 acts during fertilization in Caenorhabditis elegans like the mouse Izumo1 gene. Curr Biol 25(24):3225–3231. https://doi.org/10.1016/j.cub.2015.10.056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura K, Han L, Bianchi E, Wright GJ, de Sanctis D, Jovine L (2016) The structure of sperm Izumo1 reveals unexpected similarities with Plasmodium invasion proteins. Curr Biol 26(14):R661–R662. https://doi.org/10.1016/j.cub.2016.06.028

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ohto U, Ishida H, Krayukhina E, Uchiyama S, Inoue N, Shimizu T (2016) Structure of IZUMO1-JUNO reveals sperm-oocyte recognition during mammalian fertilization. Nature 534(7608):566–569. https://doi.org/10.1038/nature18596

    Article  PubMed  CAS  Google Scholar 

  • Putiri E, Zannoni S, Kadandale P, Singson A (2004) Functional domains and temperature-sensitive mutations in SPE-9, an EGF repeat-containing protein required for fertility in Caenorhabditis elegans. Dev Biol 272:448–459

    Article  CAS  PubMed  Google Scholar 

  • Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, Kim SK (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6(3):605–616

    Article  CAS  PubMed  Google Scholar 

  • Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131(2):311–323

    Article  CAS  PubMed  Google Scholar 

  • Satouh Y, Inoue N, Ikawa M, Okabe M (2012) Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. J Cell Sci 125(Pt 21):4985–4990. https://doi.org/10.1242/jcs.100867

    Article  PubMed  CAS  Google Scholar 

  • Saxena DK, Oh-Oka T, Kadomatsu K, Muramatsu T, Toshimori K (2002) Behaviour of a sperm surface transmembrane glycoprotein basigin during epididymal maturation and its role in fertilization in mice. Reproduction 123(3):435–444

    Article  CAS  PubMed  Google Scholar 

  • Schindl R, Romanin C (2007) Assembly domains in TRP channels. Biochem Soc Trans 35(Pt 1):84–85

    Article  CAS  PubMed  Google Scholar 

  • Shamsadin R, Adham IM, Nayernia K, Heinlein UA, Oberwinkler H, Engel W (1999) Male mice deficient for germ-cell cyritestin are infertile. Biol Reprod 61(6):1445–1451

    Article  CAS  PubMed  Google Scholar 

  • Singaravelu G, Chatterjee I, Rahimi S, Druzhinina MK, Kang L, Xu XZ, Singson A (2012) The sperm surface localization of the TRP-3/SPE-41 Ca2+-permeable channel depends on SPE-38 function in Caenorhabditis elegans. Dev Biol 365(2):376–383. https://doi.org/10.1016/j.ydbio.2012.02.037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singaravelu G, Rahimi S, Krauchunas A, Rizvi A, Dharia S, Shakes D, Smith H, Golden A, Singson A (2015) Forward genetics identifies a requirement for the Izumo-like immunoglobulin superfamily spe-45 gene in Caenorhabditis elegans fertilization. Curr Biol 25(24):3220–3224. https://doi.org/10.1016/j.cub.2015.10.055

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singson A, Mercer KB, L’Hernault SW (1998) The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell 93:71–79

    Article  CAS  PubMed  Google Scholar 

  • Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3(2):137–144

    Article  CAS  PubMed  Google Scholar 

  • Takayama J, Onami S (2016) The sperm TRP-3 channel mediates the onset of a Ca2+ wave in the fertilized C. elegans oocyte. Cell Rep 15(3):625–637. https://doi.org/10.1016/j.celrep.2016.03.040

  • Ward S (1986) Asymmetric localization of gene products during the development of Caenorhaditis elegans spermatozoa. In: Gall JG (ed) Gametogenesis and the early embryo. Alan R. Liss, Inc., New York, pp 55–75

    Google Scholar 

  • Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73(2):304–321

    Article  CAS  PubMed  Google Scholar 

  • Ward S, Argon Y, Nelson GA (1981) Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91(1):26–44

    Article  CAS  PubMed  Google Scholar 

  • Wilson KL, Fitch KR, Bafus BT, Wakimoto BT (2006) Sperm plasma membrane breakdown during Drosophila fertilization requires sneaky, an acrosomal membrane protein. Development 133(24):4871–4879

    Article  CAS  PubMed  Google Scholar 

  • Wilson LD, Obakpolor OA, Jones AM, Richie AL, Mieczkowski BD, Fall GT, Hall RW, Rumbley JN, Kroft TL (2018) The C. elegans spe-49 gene is required for fertilization and encodes a sperm-Specific transmembrane protein homologous to SPE-42. Mol Reprod Dev. https://doi.org/10.1002/mrd.22992

  • Wolf N, Hirsh D, McIntosh JR (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63(2):155–169

    Article  CAS  PubMed  Google Scholar 

  • Wyckoff GJ, Wang W, Wu CI (2000) Rapid evolution of male reproductive genes in the descent of man. Nature 403(6767):304–309

    Article  CAS  PubMed  Google Scholar 

  • Xu XZ, Sternberg PM (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114(3):285–297

    Google Scholar 

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  1. Department of Life Science, Setsunan University, Osaka, 572-8508, Japan

    Tatsuya Tajima & Hitoshi Nishimura

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  1. Tatsuya Tajima
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  2. Hitoshi Nishimura
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Correspondence to Hitoshi Nishimura .

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  1. Aix-Marseille Université IRD, APHM, Microbe, Evolution, Phylogénie, Infection, IHU Méditerranée Infection, Marseille, France

    Pierre Pontarotti

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Tajima, T., Nishimura, H. (2018). Immunoglobulin-Like Domains Have an Evolutionarily Conserved Role During Gamete Fusion in C. elegans and Mouse. In: Pontarotti, P. (eds) Origin and Evolution of Biodiversity. Springer, Cham. https://doi.org/10.1007/978-3-319-95954-2_10

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