Start me up: Cell signaling and the journey from oocyte to embryo in C. elegans

Developmental Dynamics

Volumn 235, Issue 3, 2006, Pages 571-585

  Yamamoto, Ikuko ^a   Kosinski, Mary E ^a   Greenstein, David ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caenorhabditis elegans; Fertilization; Major sperm protein; Meiosis; Meiotic maturation; MSP signaling

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL SURFACE PROTEIN; CULLIN; CYCLIN DEPENDENT KINASE; EPHRIN; EPIDERMAL GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; KATANIN; MATURATION PROMOTING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR POU; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UBIQUITIN; UNCLASSIFIED DRUG;

ANEUPLOIDY; CAENORHABDITIS ELEGANS; CELL COMMUNICATION; CHROMOSOME SEGREGATION; CYTOKINESIS; EMBRYO DEVELOPMENT; FERTILIZATION; GAMETE; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OVULATION; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENTIATION; SPERM;

ANIMALS; CAENORHABDITIS ELEGANS; EMBRYO, NONMAMMALIAN; FEMALE; FERTILIZATION; HUMANS; MALE; MEIOSIS; OOCYTES; OOGENESIS; SIGNAL TRANSDUCTION;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 33644778525     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20662     Document Type: Review

References (159)

1. Albertson DG, Thomson JN. 1993. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chrom Res 1:15-26.
2. Albertson DG, Rose AM, Villeneuve AM. 1997. Chromosome organization, mitosis and meiosis. In: Riddle DL, Blumentha T, Meyer BJ, Priess JR, editors. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, p 47-78.
3. Altafaj X, Dierssen M, Baamonde C, Marti E, Visa J, Guimera J, Oset M, Gonzalez JR, Florez J, Fillat C, Estivill X. 2001. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum Mol Genet 10:1915-1923.
4. Anderson E, Albertini DF. 1976. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 71:680-686.
5. Angell R. 1997. First-meiotic-division nondisjunction in human oocytes. Am J Hum Genet 61:23-32.
6. Baum JS, St George JP, McCall K. 2005. Programmed cell death in the germline. Semin Cell Dev Biol 16:245-259.
7. Bottino D, Mogilner A, Roberts T, Stewart M, Oster G. 2002. How nematode sperm crawl. J Cell Sci 115:367-384.
8. Boxem, M, Srinivasan DG, van den Heuvel S. 1999. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126:2227-2239.
9. Browning H, Strome S. 1996. A sperm-supplied factor required for embryogenesis in C. elegans. Development 122:391-404.
10. Bui YK, Sternberg PW. 2002. Caenorhabditis elegans inositol 5-phosphatase homolog negatively regulates inositol 1,4,5-triphosphate signaling in ovulation. Mol Biol Cell. 13:1641-1651.
11. Buttery SM, Ekman GC, Seavy M, Stewart M, Roberts TM. 2003. Dissection of the Ascaris sperm motility machinery identifies key proteins involved in major sperm protein-based amoeboid locomotion. Mol Biol Cell 14:5082-5088.
12. Castellano LE, Trevino CL, Rodriguez D, Serrano C J, Pacheco J, Tsutsumi V, Felix R, 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.
13. Chase D, Serafinas C, Ashcroft N, Kosinski M, Longo D, Ferris DK, Golden A. 2000. The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis in Caenorhabditis elegans. Genesis 26:26-41.
14. 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 132:2795-808.
15. Church DL, Guan K-L, Lambie EJ. 1995. Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121:2525-2535.
16. Clandinin TR, Mains PE. 1993. Genetic studies of mei-1 gene activity during the transition from meiosis to mitosis in Caenorhabditis elegans. Genetics 134:199-210.
17. Clark-Maguire S, Mains PE. 1994a. mei-1, a gene required for meiotic spindle formation in Caenorhabditis elegans, is a member of a family of ATPases. Genetics 136:533-546.
18. Clark-Maguire S, Mains PE. 1994b. Localization of the mei-1 gene product of Caenorhabditis elegans, a meiotic-specific spindle component. J Cell Biol 126:199-209.
19. 2+/calmodulin-dependent kinase II activation during C. elegans oocyte meiotic maturation. Development 132:5225-5237.
20. Cowan CR, Hyman AA. 2004. Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu Rev Cell Dev Biol 20:427-453.
21. Cuenca AA, Schetter A, Aceto D, Kemphues K, Seydoux G. 2003. Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130:1255-1265.
22. Davis ES, Wille L, Chestnut BA, Sadler PL, Shakes DC, Golden A. 2002. Multiple subunits of the Caenorhabditis elegans anaphase-promoting complex are required for chromosome segregation during meiosis I. Genetics 160:805-813.
23. DeRenzo C, Reese KJ, Seydoux G. 2003. Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424:685-689.
24. Detwiler, MR, Reuben M, Li X, Rogers E, Lin R. 2001. Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev Cell 1:187-199.
25. Dow MR, Mains PE. 1998. Genetic and molecular characterization of the Caenorhabditis elegans gene, mel-26, a postmeiotic negative regulator of mei-1, a meiotic-specific spindle component. Genetics 150:119-128.
26. Downs SM, Hunzicker-Dunn M. 1995. Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte-cumulus cell complex by site-selective analogs of cyclic adenosine monophosphate. Dev Biol 172:72-85.
27. Ducibella T, Duffy P, Reindollar R, Su B. 1990. Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo. Biol Reprod 43:870-876.
28. Dunphy WG, Brizuela L, Beach D, Newport J. 1988. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell 54:423-431.
29. Edwards RG. 1965. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208:349-351.
30. Ellis R, Schedl T. 2005. Sex-determination in the germ line. WormBook, ed. The C. elegans Research Community, WormBook, in press.
31. Eppig JJ. 1991. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13:569-574.
32. Eppig JJ. 2001. Oocyte control of ovarian follicular development and function in mammals. Reproduction 122:829-838.
33. Fan HY, Sun QY. 2004. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70:535-547.
34. Ferrell JE Jr. 1999a. Xenopus oocyte maturation: new lessons from a good egg. Bioessays 21:833-842.
35. Ferrell JE Jr. 1999b. Building a cellular switch: more lessons from a good egg. Bioessays 21:866-870.
36. Foor WE. 1968. Zygote formation in Ascaris lumbricoides (Nematoda). J Cell Biol 39:119-134.
37. Furukawa M, He YJ, Borchers C, Xiong Y. 2003. Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat Cell Biol 5:1001-1007.
38. Furuta T, Tuck S, Kirchner J, Koch B, Auty R, Kitagawa R, Rose AM, Greenstein D. 2000. EMB-30: an APC4 homologue required for metaphase-to-anaphase transitions during meiosis and mitosis in Caenorhabditis elegans. Mol Biol Cell 11:1401-1419.
39. Gao M, Karin M. 2005. Regulating the regulators: control of protein ubiquitination and ubiquitin-like modifications by extracellular stimuli. Mol Cell 19:581-593.
40. -. Cell 54:433-439.
41. Gautier J, Minshull J, Lohka M, Glotzer M, Hunt T, Maller JL. 1990. Cyclin is a component of maturation-promoting factor from Xenopus. Cell 60:487-494.
42. Gilliland WD, Hawley RS. 2005. Cohesin and the maternal age effect. Cell 123:371-373.
43. Gleason EJ, Lindsey WC, Kroft TL, Singson AW, L'Hernault SW. 2006. spe-10 encodes a DHHC-CRD zinc-finger membrane protein required for ER/Golgi membrane morphogenesis during Caenorhabditis elegans spermatogenesis. Genetics (in press).
44. Golden A, Sadler PL, Wallenfang MR, Schumacher JM, Hamill DR, Bates G, Bowerman B, Seydoux G, Shakes DC. 2000. Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J Cell Biol 151:1469-1482.
45. Goldstein B, Hird SN. 1996. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122:1467-1474.
46. Gönczy P, Rose L. 2005. Asymmetric cell division and axis formation in the embryo. WormBook, ed. The C. elegans Research Community, WormBook (in press).
47. Greenstein D. 2005. Control of oocyte meiotic maturation and fertilization. WormBook, ed. The C. elegans Research Community, WormBook (in press).
48. Greenstein D, Hird S, Plasterk RHA, Andachi Y, Kohara Y, Wang B, Finney M, Ruvkun G. 1994. Targeted mutations in the Caenorhabditis elegans POU homeo box gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. Genes Dev 8:1935-1948.
49. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. 1999. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126:1011-1022.
50. Hall DH, Winfrey VP, Blaeuer G, Hoffman LH, Furuta T, Rose KL, Hobert O, Greenstein D. 1999. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev Biol 212:101-123.
51. Handel MA, Eppig JJ. 1997. Sexual dimorphism in the regulation of mammalian meiosis. In: Handel MA, editor. Current topics in developmental biology: meiosis and gametogenesis. Orlando, FL: Academic Press, p 333-359.
52. Hardy DM, editor. 2002. Fertilization. San Diego, CA: Academic Press.
53. Hassold T, Hunt P. 2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280-291.
54. Hill DP, Shakes DC, Ward S, 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. Dev Biol 136:154-166.
55. Hill KL, L'Hernault SW. 2001. Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev Biol 232:105-114.
56. Himpel S, Tegge W, Frank R, Leder S, Joost HG, Becker W. 2000. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J Biol Chem 275:2431-2438.
57. Himpel S, Panzer P, Eirmbter K, Czajkowska H, Sayed M, Packman LC, Blundell T, Kentrup H, Grotzinger J, Joost HG, Becker W. 2001. Identification of the autophosphorylation sites and characterization of their effects in the protein kinase DYRK1A. Biochem J 359:497-505.
58. Hird SN, Paulsen JE, Strome S. 1996. Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 122:1303-1312.
59. Hodges CA, Ilagan A, Jeimings D, Keri R, Nilson J, Hunt PA. 2002. Experimental evidence that changes in oocyte growth influence meiotic chromosome segregation. Hum Reprod 17:1171-1180.
60. Hodges CA, Revenkova E, Jessberger, R, Hassold TJ, Hunt PA. 2005. SMC1β-deficient female mice provide evidence that cohesins are a missing-link in age-related nondisjunction. Nat Genet (in press).
61. Howe M, McDonald KL, Albertson DG, Meyer BJ. 2001. HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J Cell Biol 153:1227-1238.
62. Hubbard EJA, Greenstein D. 2000. The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 218:2-22.
63. Italiano JE Jr, Roberts TM, Stewart M, Fontana CA. 1996. Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell 84:105-114.
64. Iwamatsu T, Chang MC. 1972. Sperm penetration in vitro of mouse oocytes at various times during maturation. J. Reprod Fertil 31:237-247.
65. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. 2004. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428:145-150.
66. Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, Tschudy KS, Tilly JC, Cortes ML, Forkert R, Spitzer T, Iacomini J, Scadden DT, Tilly JL. 2005. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122:303-315.
67. 2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499-502.
68. Kadandale P, Stewart A, Gordon S, Rubin J, Klancer R, Schweinsberg P, Grant BD, Singson A. 2005. The egg surface LDL-receptor-repeat containing proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans. Curr Biol (in press).
69. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A. 2000. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 24:279-282.
70. S protein-mediated pathway. Dev Biol 267:1-13.
71. Kemphues KJ, Priess JR, Morton DG, Cheng NS. 1988. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311-320.
72. Kimble J, Crittenden SL. 2005. Germline proliferation and its control. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook. 1.13.1, http://www.wormbook.org.
73. Kishimoto T. 2004. More than G1 or G2 arrest: useful starfish oocyte system for investigating skillful MAP kinase. Biol Cell 96:241-244.
74. Kosinski M, McDonald K, Schwartz J, Yamamoto I, Greenstein D. 2005. C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132:3357-3369.
75. 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.
76. Kurz T, Pintard L, Willis JH, Hamill DR, Gonczy P, Peter M, Bowerman B. 2002. Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295:1294-1298.
77. Kurz T, Ozlu N, Rudolf F, O'Rourke SM, Luke B, Hofmann K, Hyman AA, Bowerman B, Peter M. 2005. The conserved protein DCN-1/Dcn1p is required for cullin neddylation in C. elegans and S. cerevisiae. Nature 435:1257-1261.
78. Kuwabara PE. 2003. The multifaceted C. elegans major sperm protein: an ephrin signaling antagonist in oocyte maturation. Genes Dev 17:155-161.
79. Lamb NE, Hassold TJ. 2004. Nondisjunction: a view from ringside. N Engl J Med 351:1931-1934.
80. Lamb NE, Feingold E, Savage A, Avramopoulos D, Freeman S, Gu Y, Hallberg A, Hersey J, Karadima G, Pettay D, Saker D, Shen J, Taft L, Mikkelsen M, Petersen MB, Hassold T, Sherman SL. 1997. Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum Mol Genet 6:1391-1399.
81. Lamb NE, Yu K, Shaffer J, Feingold E, Sherman SL. 2005. Association between maternal age and meiotic recombination for trisomy 21. Am J Hum Genet 76:91-99.
82. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C. 2000. Severely reduced female fertility in CD9-deficient mice. Science 287:319-321.
83. L'Hernault SW, Shakes DC, Ward S. 1988. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120:435-452.
84. Lin R. 2003. A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality. Dev Biol 258:226-239.
85. Liu J, Maller JL. 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.
86. Liu J, Vasudevan S, Kipreos ET. 2004. CUL-2 and ZYG-11 promote meiotic anaphase II and the proper placement of the anterior-posterior axis in C. elegans. Development 131:3513-3525.
87. Lochhead PA, Sibbet G, Morrice N, Cleghon V. 2005. Activation-loop autophosphorylation is mediated by a novel transitional intermediate form of DYRKs. Cell 121:925-936.
88. Lohka MJ, Hayes MK, Maller JL. 1988. Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc Natl Acad Sci USA 85:3009-3013.
89. Luke-Glaser S, Pintard L, Lu C, Mains PE, Peter M. 2005. The BTB protein MEL-26 promotes cytokinesis in C. elegans by a CUL-3-independent mechanism. Curr Biol 15:1605-1615.
90. Mains PE, Kemphues KJ, Sprunger SA, Sulston IA, Wood WB. 1990. Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics 126:593-605.
91. Maller JL, Krebs EG. 1977. Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3′:5′-monophosphate-dependent protein kinase. J Biol Chem 252:1712-1718.
92. Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422-125.
93. Masui Y. 1985. Meiotic arrest in animal oocytes. In: Monroy A, Metz CB, editors. Biology of fertilization. Orlando, FL: Academic Press. Vol. 1, p. 189-219.
94. Masui Y. 2001. From oocyte maturation to the in vitro cell cycle: the history of discoveries of maturation-promoting Factor (MPF) and cytostatic factor (CSF). Differentiation 69:1-17.
95. Masui Y, Clarke HJ. 1979. Oocyte maturation. Int Rev Cytol 57:185-282.
96. Masui Y, Markert CL. 1971. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129-145.
97. McCarter J, Bartlett B, Dang T, Schedl T. 1997. Soma-germ cell interactions in Caenorhabditis elegans: Multiple events in germline development require the somatic sheath and spermathecal lineages. Dev Biol 181:121-143.
98. McCarter J, Bartlett B, Dang T, Schedl T. 1999. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205:111-128.
99. McNally FJ, Vale RD. 1993. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75:419-429.
100. McNally KL, McNally FJ. 2005. Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282:218-230.
101. S protein in the oocyte. Science 297:1343-1345.
102. S-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947-1950.
103. Miller MA, Nguyen VQ, Lee M-H, Kosinski M, Schedl T, Caprioli RM, Greenstein D. 2001. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291:2144-2147.
104. Miller MA, Ruest PJ, Kosinski M, Hanks SK, Greenstein D. 2003. An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev 17:187-200.
105. Miller MA, Cutter AD, Yamamoto I, Ward S, Greenstein D. 2004. Clustered organization of reproductive genes in the C. elegans genome. Curr Biol 14:1284-1290.
106. Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E. 2000. Requirement of CD9 on the egg plasma membrane for fertilization. Science 287:321-324.
107. Murray AW. 2004. Recycling the cell cycle: cyclins revisited. Cell 116:221-234.
108. Nance J. 2005. PAR proteins and the establishment of cell polarity during C. elegans development. Bioessays 27:126-135.
109. Neill AT, Vacquier VD. 2004. Ligands and receptors mediating signal transduction in sea urchin spermatozoa. Reproduction 127:141-149.
110. Nishi Y, Lin R. 2005. DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. Dev Biol 288:139-149.
111. Nurse P. 1990. Universal control mechanism regulating onset of M-phase. Nature 344:503-508.
112. O'Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, Li Y, White JG. 2001. The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105:547-558.
113. Ogle BM, Cascalho M, Platt JL. 2005. Biological implications of cell fusion. Nat Rev Mol Cell Biol 6:567-575.
114. Page BD, Guedes S, Waring D, Priess JR. 2001. The C. elegans E2F- and DP-related proteins are required for embryonic asymmetry and negatively regulate Ras/MAPK signaling. Mol Cell 7:451-460.
115. Pang KM, Ishidate T, Nakamura K, Shirayama M, Trzepacz C, Schubert CM, Priess JR, Mello CC. 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.
116. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. 2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684.
117. Pellettieri J, Reinke V, Kim SK, Seydoux G. 2003. Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev Cell 5:451-462.
118. Peters J-M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 9:931-943.
119. Pincus G, Enzmann EV. 1935. The comparative behavior of mammalian eggs in vivo and in vitro. I. The activation of ovarian eggs. J Exp Med 62:655-675.
120. Pintard L, Kurz T, Glaser S, Willis JH, Peter M, Bowerman B. 2003a. Neddylation and deneddylation of CUL-3 is required to target MEI-1/Katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr Biol 13:911-921.
121. Pintard L, Willis JH, Willems A, Johnson JL, Srayko M, Kurz T, Glaser S, Mains PE, Tyers M, Bowerman B, Peter M. 2003b. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425:311-316.
122. 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.
123. Quintin S, Mains PE, Zinke A, Hyman AA. 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.
124. Raich WB, Moorman C, Lacefield CO, Lehrer J, Bartsch D, Plasterk RH, Kandel ER, Hobert O. 2003. Characterization of Caenorhabditis elegans homologs of the Down syndrome candidate gene DYRK1A. Genetics 163:571-580.
125. Rappleye CA, Paredez AR, Smith CW, McDonald KL, Aroian RV. 1999. The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode Caenorhabditis elegans. Genes Dev 13:2838-2851.
126. Rappleye CA, Tagawa A, Lyczak R, Bowerman B, Aroian RV. 2002. The anaphase-promoting complex and separin are required for embryonic anterior-posterior axis formation. Dev Cell 2:195-206.
127. Rauh NR, Schmidt A, Bormann J, Nigg EA, Mayer TU. 2005. Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature 437:1048-1052.
128. Reese KJ, Dunn MA, Waddle JA, Seydoux G. 2000. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol Cell 6:445-455.
129. Rose KL, Winfrey VP, Hoffman LH, Hall DH, Furuta T, Greenstein D. 1997. The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 192:59-77.
130. Runft LL, Jaffe LA, Mehlmann LM. 2002. Egg activation at fertilization: where it all begins. Dev Biol 245:237-254.
131. Samuel AD, Murthy VN, Hengartner MO. 2001. Calcium dynamics during fertilization in C. elegans. BMC Dev Biol 1:8.
132. Schatten G. 1994. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299-335.
133. Shakes DC, Ward S. 1989. Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 134:307-316.
134. Shakes DC, Sadler PL, Schumacher JM, Abdolrasulnia M, Golden A. 2003. Developmental defects observed in hypomorphic anaphase-promoting complex mutants are linked to cell cycle abnormalities. Development 130:1605-1620.
135. Shimada M, Kawahara H, Doi H. 2002. Novel family of CCCH-type zinc-finger proteins, MOE-1, -2 and -3, participates in C. elegans oocyte maturation. Genes Cells 7:933-947.
136. Singson A. 2001. Every sperm is sacred: fertilization in Caenorhabditis elegans. Dev Biol 230:101-109.
137. 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.
138. Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, Glotzer M, Nasmyth K. 2001. Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr Biol 11:1825-1835.
139. Sonneville R, Gönczy P. 2004. zyg-11 and cul-2 regulate progression through meiosis II and polarity establishment in C. elegans. Development 131:3527-3543.
140. Srayko M, Buster DW, Bazirgan OA, McNally FJ, Mains PE. 2000. MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev 14:1072-1084.
141. Stricker SA. 1999. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211:157-176.
142. Strome S, Wood WB. 1982. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc Natl Acad Sci USA 79:1558-1562.
143. Strome S, Wood WB. 1983. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35:15-25.
144. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet 3:137-144.
145. Telfer EE, Gosden RG, Byskov AG, Spears N, Albertini D, Andersen CY, Anderson R, Braw-Tal R, Clarke H, Gougeon A, McLaughlin E, McLaren A, McNatty K, Schatten G, Silber S, Tsafriri A. 2005. On regenerating the ovary and generating controversy. Cell 122:821-822.
146. Tsafriri A, Chun SY, Zhang R, Hsueh AJ, Conti M. 1996. Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biol 178:393-402.
147. Tunquist BJ, Maller JL. 2003. Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev 17:683-710.
148. Ward S, Carrel JS. 1979. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304-321.
149. Wassarman PM, Jovine L, Litscher ES. 2001. A profile of fertilization in mammals. Nat Cell Biol 3:E59-64.
150. Webb RJ, Bains H, Cruttwell C, Carroll J. 2002. Gap-junctional communication in mouse cumulus-oocyte complexes: implications for the mechanism of meiotic maturation. Reproduction 123:41-52.
151. Wickramasinghe D, Albertini DF. 1993. Cell cycle control during mammalian oogenesis. Curr Top Dev Biol 28:125-153.
152. Wilson EB. 1925. The cell in development and heredity, 3rd ed. New York: Macmillan.
153. Wolf N, Hirsh D, McIntosh JR. 1978. Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63:155-169.
154. Wolstenholme J, Angell RR. 2000. Maternal age and trisomy: a unifying mechanism of formation. Chromosoma 109:435-438.
155. Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M, Elledge SJ, Harper JW. 2003. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316-321.
156. Xu XZ, Sternberg PW. 2003. A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285-297.
157. Yagi M, Miyamoto T, Sawatani Y, Iwamoto K, Hosogane N, Fujita N, Morita K, Ninomiya K, Suzuki T, Miyamoto K, Oike Y, Takeya M, Toyama Y, Suda T. 2005. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J Exp Med 202:345-351.
158. Yang HY, McNally K, McNally FJ. 2003. MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev Biol 260:245-259.
159. Zannoni S, L'Hernault SW, Singson AW. 2003. Dynamic localization of SPE-9 in sperm: a protein required for sperm-oocyte interactions in Caenorhabditis elegans. BMC Dev Biol 3:10.