Fertilization and the oocyte-to-embryo transition in C. elegans

BMB Reports

Volumn 43, Issue 6, 2010, Pages 389-399

  Marcello, Matthew R ^a   Singson, Andrew ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

C. elegans; Egg activation; Fertilization; Oocyte to embryo transition; Sperm egg fusion

Indexed keywords

ANIMAL; ANIMAL EMBRYO; CAENORHABDITIS ELEGANS; CYTOLOGY; EMBRYOLOGY; FERTILIZATION; OOCYTE; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; EMBRYO, NONMAMMALIAN; FERTILIZATION; OOCYTES;

EID: 77955812816     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2010.43.6.389     Document Type: Review

References (100)

1. Stitzel, M. L. and Seydoux, G. (2007) Regulation of the oocyte-to-zygote transition. Science 316, 407-408.
2. de Kretser, D. M. (1997) Male infertility. Lancet 349, 787-790.
3. O'Flynn O'Brien, K. L., Varghese, A. C. and Agarwal, A. (2010) The genetic causes of male factor infertility: a review. Fertil Steril 93, 1-12.
4. Manetti, G. J. and Honig, S. C. (2010) Update on male hormonal contraception: is the vasectomy in jeopardy? Int. J. Impot. Res. 22, 159-170.
5. Laprise, S. L. (2009) Implications of epigenetics and genomic imprinting in assisted reproductive technologies. Mol. Reprod. Dev. 76, 1006-1018.
6. Grace, K. S. and Sinclair, K. D. (2009) Assisted reproductive technology, epigenetics, and long-term health: a developmental time bomb still ticking. Semin. Reprod. Med. 27, 409-416.
7. Florman, H. M. and Ducibella, T. (2006) Fertilization in Mammals; in Knobil and Neill's Physiology of Reproduction. Neill, J. D. (ed.), Elsevier, San Diego, USA.
8. Singson, A., Hang, J. S. and Parry, J. M. (2008) Genes required for the common miracle of fertilization in Caenorhabditis elegans. Int. J. Dev. Biol. 52, 647-656.
9. L'Hernault, S. W. (2006) Spermatogenesis; in Worm-Book: online review of C. elegans biology. Community, T. C. e. R. (ed.), http://www.wormbook.org.
10. Consortium, T. C. e. S. (1998) Genome sequence of the nematode C. elegans a platform for investigating biology. Science 282, 2012-2018.
11. Sulston, J. E. and Horvitz, H. R. (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
12. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R. (1997) C. elegans II, pp. 1222, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
13. Horner, V. L. and Wolfner, M. F. (2008) Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev. Dyn. 237, 527-544.
14. Govindan, J. A. and Greenstein, D. (2007) Embryogenesis: anchors away! Curr. Biol. 17, R890-892.
15. Yamamoto, I., Kosinski, M. E. and Greenstein, D. (2006) Start me up: cell signaling and the journey from oocyte to embryo in C. elegans. Dev. Dyn. 235, 571-585.
16. Ikawa, M., Inoue, N., Benham, A. M. and Okabe, M. (2010) Fertilization: a sperm's journey to and interaction with the oocyte. J. Clin. Invest. 120, 984-994.
17. Ward, S. and Carrel, J. S. (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 73, 304-321.
18. Singson, A. (2001) Every sperm is sacred: fertilization in Caenorhabditis elegans. Dev. Biol. 230, 101-109.
19. Bembenek, J. N., Richie, C. T., Squirrell, J. M., Campbell, J. M., Eliceiri, K. W., Poteryaev, D., Spang, A., Golden, A. and White, J. G. (2007) Cortical granule exocytosis in C. elegans is regulated by cell cycle components including separase. Development 134, 3837-3848.
20. L'Hernault S, W. (1997) Spermatogenesis; in C. Elegans II. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R. (eds.), pp. 271-294, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
21. Nelson, G. A. and Ward, S. (1980) Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19, 457-464.
22. Ward, S., Hogan, E. and Nelson, G. A. (1983) The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev. Biol. 98, 70-79.
23. Bandyopadhyay, J., Lee, J., Lee, J. I., Yu, J. R., Jee, C., Cho, J. H., Jung, S., Lee, M. H., Zannoni, S., Singson, A., Kim, D., H., Koo, H. S. and Ahnn, J. (2002) Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in caenorhabditis elegans. Mol. Biol. Cell 13, 3281- 3293.
24. Washington, N. L. and Ward, S. (2006) FER-1 regulates Ca2+ -mediated membrane fusion during C. elegans spermatogenesis. J. Cell Sci. 119, 2552-2562.
25. Kubagawa, H. M., Watts, J. L., Corrigan, C., Edmonds, J. W., Sztul, E., Browse, J. and Miller, M. A. (2006) Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat. Cell Biol. 8, 1143-1148.
26. Miller, M. A., Nguyen, V. Q., Lee, M. H., Kosinski, M., Schedl, T., Caprioli, R. M. and Greenstein, D. (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291, 2144-2147.
27. Samuel, A. D., Murthy, V. N. and Hengartner, M. O. (2001) Calcium dynamics during fertilization in C. elegans. BMC Dev. Biol. 1, 8.
28. Zannoni, S., L'Hernault, S. W. and Singson, A. W. (2003) Dynamic localization of SPE-9 in sperm: a protein required for sperm-oocyte interactions in Caenorhabditis elegans. BMC Dev. Biol. 3, 10.
29. Goldstein, B. and Hird, S. N. (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467-1474.
30. Jorgensen, E. M. and Mango, S. E. (2002) The art and design of genetic screens: caenorhabditis elegans. Nat. Rev. Genet. 3, 356-369.
31. Nishimura, H. and L'Hernault, S. W. (2010) Spermatogenesisdefective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction. Dev. Dyn. 239, 1502-1514.
32. L'Hernault, S. W., Shakes, D. C. and Ward, S. (1988) Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120, 435-452.
33. Kadandale, P., Stewart-Michaelis, A., Gordon, S., Rubin, J., Klancer, R., Schweinsberg, P., Grant, B. D. and Singson, A. (2005) The egg surface LDL receptor repeatcontaining proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans. Curr. Biol. 15, 2222-2229.
34. Singson, A., Mercer, K. B. and L'Hernault, S. W. (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.
35. Putiri, E., Zannoni, S., Kadandale, P. and 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.
36. Chatterjee, I., Richmond, A., Putiri, E., Shakes, D. C. and 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.
37. Roberts, T. M., Pavalko, F. M. and Ward, S. (1986) Membrane and cytoplasmic proteins are transported in the same organell complex during nematode spermatogenesis. J. Cell Biology 102, 1787-1796.
38. Shakes, D. and Ward, S. (1989) Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Developmental Biology 134, 307-316.
39. Xu, X. Z. and Sternberg, P. W. (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114, 285-297.
40. Castellano, L. E., Trevino, C. L., Rodriguez, D., Serrano, C. J., Pacheco, J., Tsutsumi, V., Felix, R. and Darszon, A. (2003) Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility. FEBS Lett. 541, 69-74.
41. Jungnickel, M. K., Marrero, H., Birnbaumer, L., Lemos, J. R. and Florman, H. M. (2001) Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat. Cell. Biol. 3, 499-502.
42. Schindl, R. and Romanin, C. (2007) Assembly domains in TRP channels. Biochem. Soc. Trans. 35, 84-85.
43. Beech, D. J., Bahnasi, Y. M., Dedman, A. M. and Al-Shawaf, E. (2009) TRPC channel lipid specificity and mechanisms of lipid regulation. Cell Calcium 45, 583-588.
44. Kroft, T. L., Gleason, E. J. and L'Hernault S, W. (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.
45. Miyamoto, T. (2006) The dendritic cell-specific transmembrane protein DC-STAMP is essential for osteoclast fusion and osteoclast bone-resorbing activity. Mod. Rheumatol. 16, 341-342.
46. Albert, T. K., Hanzawa, H., Legtenberg, Y. I., de Ruwe, M. J., van den Heuvel, F. A., Collart, M. A., Boelens, R. and Timmers, H. T. (2002) Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J. 21, 355-364.
47. Hanzawa, H., de Ruwe, M. J., Albert, T. K., van Der Vliet, P. C., Timmers, H. T. and Boelens, R. (2001) The structure of the C4C4 ring finger of human NOT4 reveals features distinct from those of C3HC4 RING fingers. J. Biol. Chem. 276, 10185-10190.
48. Deshaies, R. J. and Joazeiro, C. A. (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
49. Nykjaer, A. and Willnow, T. E. (2002) The low-density lipoprotein receptor gene family: a cellular Swiss army knife? Trends. Cell Biol. 12, 273-280.
50. Vjugina, U. and Evans, J. P. (2008) New insights into the molecular basis of mammalian sperm-egg membrane interactions. Front. Biosci. 13, 462-476.
51. Okabe, M., Adachi, T., Takada, K., Oda, H., Yagasaki, M., Kohama, Y. and Mimura, T. (1987) Capacitation-related changes in antigen distribution on mouse sperm heads and its relation to fertilization rate in vitro. J. Reprod. Immunol. 11, 91-100.
52. Okabe, M., Yagasaki, M., Oda, H., Matzno, S., Kohama, Y. and Mimura, T. (1988) Effect of a monoclonal anti-mouse sperm antibody (OBF13) on the interaction of mouse sperm with zona-free mouse and hamster eggs. J. Reprod. Immunol. 13, 211-219.
53. Inoue, N., Ikawa, M., Isotani, A. and Okabe, M. (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434, 234-238.
54. Inoue, N., Ikawa, M. and Okabe, M. (2008) Putative sperm fusion protein IZUMO and the role of N-glycosylation. Biochem. Biophys. Res. Commun. 377, 910-914.
55. Sosnik, J., Miranda, P. V., Spiridonov, N. A., Yoon, S. Y., Fissore, R. A., Johnson, G. R. and Visconti, P. E. (2009) Tssk6 is required for Izumo relocalization and gamete fusion in the mouse. J. Cell Sci. 122, 2741-2749.
56. Gadella, B. M., Tsai, P. S., Boerke, A. and Brewis, I. A. (2008) Sperm head membrane reorganisation during capacitation. Int. J. Dev. Biol. 52, 473-480.
57. Toshimori, K., Saxena, D. K., Tanii, I. and Yoshinaga, K. (1998) An MN9 antigenic molecule, equatorin, is required for successful sperm-oocyte fusion in mice. Biol. Reprod. 59, 22-29.
58. Ellerman, D. A., Pei, J., Gupta, S., Snell, W. J., Myles, D. and Primakoff, P. (2009) Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm. Mol. Reprod. Dev. 76, 1188-1199.
59. Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M. and Boucheix, C. (2000) Severely reduced female fertility in CD9-deficient mice. Science 287, 319-321.
60. Miyado, K., Yamada, G., Yamada, S., Hasuwa, H., Nakamura, Y., Ryu, F., Suzuki, K., Kosai, K., Inoue, K., Ogura, A., Okabe, M. and Mekada, E. (2000) Requirement of CD9 on the egg plasma membrane for fertilization.Science 287, 321-324.
61. Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sakagami, J., Tada, N., Miyazaki, S. and Kudo, A. (2000) The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat. Genet. 24, 279-282.
62. Miyado, K., Yoshida, K., Yamagata, K., Sakakibara, K., Okabe, M., Wang, X., Miyamoto, K., Akutsu, H., Kondo, T., Takahashi, Y., Ban, T., Ito, C., Toshimori, K., Nakamura, A., Ito, M., Miyado, M., Mekada, E. and Umezawa, A. (2008) The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc. Natl. Acad. Sci. U.S.A. 105, 12921-12926.
63. Barraud-Lange, V., Naud-Barriant, N., Bomsel, M., Wolf, J. P. and Ziyyat, A. (2007) Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J. 21, 3446-3449.
64. Gupta, S., Primakoff, P. and Myles, D. G. (2009) Can the presence of wild-type oocytes during insemination rescue the fusion defect of CD9 null oocytes? Mol. Reprod. Dev. 76, 602.
65. Ito, C., Yamatoya, K., Yoshida, K., Maekawa, M., Miyado, K. and Toshimori, K. (2010) Tetraspanin family protein CD9 in the mouse sperm: unique localization, appearance, behavior and fate during fertilization. Cell Tissue Res. 340, 583-594.
66. McNally, K. L. and McNally, F. J. (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev. Biol. 282, 218-230.
67. Golden, A., Sadler, P. L., Wallenfang, M. R., Schumacher, J. M., Hamill, D. R., Bates, G., Bowerman, B., Seydoux, G. and Shakes, D. C. (2000) Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J. Cell Biol. 151, 1469-1482.
68. Browning, H. and Strome, S. (1996) A sperm-supplied factor required for embryogenesis in C. elegans. Development 122, 391-404.
69. Hill, D. P., Shakes, D. C., Ward, S. and Strome, S. (1989) A sperm-supplied product essential for initiation of normal embryogenesis in Caenorhabditis elegans is encoded by the paternal-effect embryonic-lethal gene, spe-11 [published erratum appears in Dev Biol 1990 May;139(1):230]. Dev. Biol. 136, 154-166.
70. Jantsch-Plunger, V., Gonczy, P., Romano, A., Schnabel, H., Hamill, D., Schnabel, R., Hyman, A. A. and Glotzer, M. (2000) CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149, 1391-1404.
71. Jenkins, N., Saam, J. R. and Mango, S. E. (2006) CYK-4/ GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 313, 1298-1301.
72. Maruyama, R., Velarde, N. V., Klancer, R., Gordon, S., Kadandale, P., Parry, J. M., Hang, J. S., Rubin, J., Stewart-Michaelis, A., Schweinsberg, P., Grant, B. D., Piano, F., Sugimoto, A. and Singson, A. (2007) EGG-3 regulates cell-surface and cortex rearrangements during egg activation in Caenorhabditis elegans. Curr. Biol. 17, 1555-1560.
73. Parry, J. M., Velarde, N. V., Lefkovith, A. J., Zegarek, M. H., Hang, J. S., Ohm, J., Klancer, R., Maruyama, R., Druzhinina, M. K., Grant, B. D., Piano, F. and Singson, A. (2009) EGG-4 and EGG-5 Link Events of the Oocyte-to-Embryo Transition with Meiotic Progression in C. elegans. Curr. Biol. 19, 1752-1757.
74. Stitzel, M. L., Cheng, K. C. and Seydoux, G. (2007) Regulation of MBK-2/Dyrk kinase by dynamic cortical anchoring during the oocyte-to-zygote transition. Curr. Biol. 17, 1545-1554.
75. Cheng, K. C., Klancer, R., Singson, A. and Seydoux, G. (2009) Regulation of MBK-2/DYRK by CDK-1 and the pseudophosphatases EGG-4 and EGG-5 during the oocyte-to-embryo transition. Cell 139, 560-572.
76. Tonks, N. K. (2009) Pseudophosphatases: grab and hold on. Cell 139, 464-465.
77. Pils, B. and Schultz, J. (2004) Evolution of the multifunctional protein tyrosine phosphatase family. Mol. Biol. Evol. 21, 625-631.
78. Tonks, N. K. (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell. Biol. 7, 833-846.
79. Harris, M. T., Lai, K., Arnold, K., Martinez, H. F., Specht, C. A. and Fuhrman, J. A. (2000) Chitin synthase in the filarial parasite, Brugia malayi. Mol. Biochem. Parasitol. 111, 351-362.
80. Veronico, P., Gray, L. J., Jones, J. T., Bazzicalupo, P., Arbucci, S., Cortese, M. R., Di Vito, M. and De Giorgi, C. (2001) Nematode chitin synthases: gene structure, expression and function in Caenorhabditis elegans and the plant parasitic nematode Meloidogyne artiellia. Mol. Genet. Genomics. 266, 28-34.
81. Zhang, Y., Foster, J. M., Nelson, L. S., Ma, D. and Carlow, C. K. (2005) The chitin synthase genes chs-1 and chs-2 are essential for C. elegans development and responsible for chitin deposition in the eggshell and pharynx, respectively. Dev. Biol. 285, 330-339.
82. Guven-Ozkan, T., Nishi, Y., Robertson, S. M. and Lin, R. (2008) Global transcriptional repression in C. elegans germline precursors by regulated sequestration of TAF-4. Cell 135, 149-160.
83. Nishi, Y., Rogers, E., Robertson, S. M. and Lin, R. (2008) Polo kinases regulate C. elegans embryonic polarity via binding to DYRK2-primed MEX-5 and MEX-6. Development 135, 687-697.
84. Pang, K. M., Ishidate, T., Nakamura, K., Shirayama, M., Trzepacz, C., Schubert, C. M., Priess, J. R. and Mello, C. C. (2004) The minibrain kinase homolog, mbk-2, is required for spindle positioning and asymmetric cell division in early C. elegans embryos. Dev. Biol. 265, 127-139.
85. Pellettieri, J., Reinke, V., Kim, S. K. and Seydoux, G. (2003) Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 5, 451-462.
86. Quintin, S., Mains, P. E., Zinke, A. and Hyman, A. A. (2003) The mbk-2 kinase is required for inactivation of MEI-1/katanin in the one-cell Caenorhabditis elegans embryo. EMBO Rep. 4, 1175-1181.
87. Srayko, M., Buster, D. W., Bazirgan, O. A., McNally, F. J. and Mains, P. E. (2000) MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes. Dev. 14, 1072-1084.
88. Saunders, C. M., Larman, M. G., Parrington, J., Cox, L. J., Royse, J., Blayney, L. M., Swann, K. and Lai, F. A. (2002) PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 129, 3533-3544.
89. Swann, K., Saunders, C. M., Rogers, N. T. and Lai, F. A. (2006) PLCzeta (zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin. Cell Dev. Biol. 17, 264-273.
90. Ducibella, T. and Fissore, R. (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev. Biol. 315, 257-279.
91. Liu, J. and Maller, J. L. (2005) Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol. 15, 1458-1468.
92. Rauh, N. R., Schmidt, A., Bormann, J., Nigg, E. A. and Mayer, T. U. (2005) Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature 437, 1048-1052.
93. Hansen, D. V., Tung, J. J. and Jackson, P. K. (2006) CaMKII and polo-like kinase 1 sequentially phosphorylate the cytostatic factor Emi2/XErp1 to trigger its destruction and meiotic exit. Proc. Natl. Acad. Sci. U.S.A. 103, 608-613.
94. Wessel, G. M., Brooks, J. M., Green, E., Haley, S., Voronina, E., Wong, J., Zaydfudim, V. and Conner, S. (2001) The biology of cortical granules. Int. Rev. Cytol. 209, 117-206.
95. Matson, S., Markoulaki, S. and Ducibella, T. (2006) Antagonists of myosin light chain kinase and of myosin II inhibit specific events of egg activation in fertilized mouse eggs. Biol. Reprod. 74, 169-176.
96. Sato, M., Grant, B. D., Harada, A. and Sato, K. (2008) Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J. Cell Sci. 121, 3177-3186.
97. Gardner, A. J., Williams, C. J. and Evans, J. P. (2007) Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation. Reproduction 133, 383-393.
98. Gardner, A. J., Knott, J. G., Jones, K. T. and Evans, J. P. (2007) CaMKII can participate in but is not sufficient for the establishment of the membrane block to polyspermy in mouse eggs. J. Cell Physiol. 212, 275-280.
99. Wortzman-Show, G. B., Kurokawa, M., Fissore, R. A. and Evans, J. P. (2007) Calcium and sperm components in the establishment of the membrane block to polyspermy: studies of ICSI and activation with sperm factor. Mol. Hum. Reprod. 13, 557-565.
100. Gardner, A. J. and Evans, J. P. (2006) Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod. Fertil. Dev. 18, 53-61.