Skip to main content

Control of Oocyte Growth and Meiotic Maturation in Caenorhabditis elegans

  • Chapter
  • First Online:
Germ Cell Development in C. elegans

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 757))

Abstract

In sexually reproducing animals, oocytes arrest at diplotene or diakinesis and resume meiosis (meiotic maturation) in response to hormones. Chromosome segregation errors in female meiosis I are the leading cause of human birth defects, and age-related changes in the hormonal environment of the ovary are a suggested cause. Caenorhabditis elegans is emerging as a genetic paradigm for studying hormonal control of meiotic maturation. The meiotic maturation processes in C. elegans and mammals share a number of biological and molecular similarities. Major sperm protein (MSP) and luteinizing hormone (LH), though unrelated in sequence, both trigger meiotic resumption using somatic Gαs-adenylate cyclase pathways and soma–germline gap-junctional communication. At a molecular level, the oocyte responses apparently involve the control of conserved protein kinase pathways and post-transcriptional gene regulation in the oocyte. At a cellular level, the responses include cortical cytoskeletal rearrangement, nuclear envelope breakdown, assembly of the acentriolar meiotic spindle, chromosome segregation, and likely changes important for fertilization and the oocyte-to-embryo transition. This chapter focuses on signaling mechanisms required for oocyte growth and meiotic maturation in C. elegans and discusses how these mechanisms coordinate the completion of meiosis and the oocyte-to-embryo transition.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1(1):15–26

    PubMed  CAS  Google Scholar 

  • Allard P, Colaiacovo MP (2010) Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc Natl Acad Sci USA 107(47):20405–20410

    PubMed  CAS  Google Scholar 

  • Altun ZF, Chen B, Wang ZW, Hall DH (2009) High resolution map of Caenorhabditis elegans gap junction proteins. Dev Dyn 238(8):1936–1950

    PubMed  CAS  Google Scholar 

  • Andresson T, Ruderman JV (1998) The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway. EMBO J 17(19):5627–5637

    PubMed  CAS  Google Scholar 

  • Andux S, Ellis RE (2008) Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet 4(12):e1000295

    PubMed  Google Scholar 

  • Angelo G, Van Gilst MR (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326(5955):954–958

    PubMed  CAS  Google Scholar 

  • Aono S, Legouis R, Hoose WA, Kemphues KJ (2004) PAR-3 is required for epithelial cell polarity in the distal spermatheca of C. elegans. Development 131(12):2865–2874

    PubMed  CAS  Google Scholar 

  • Arur S, Ohmachi M, Nayak S, Hayes M, Miranda A, Hay A, Golden A, Schedl T (2009) Multiple ERK substrates execute single biological processes in Caenorhabditis elegans germ-line development. Proc Natl Acad Sci USA 106(12):4776–4781

    PubMed  CAS  Google Scholar 

  • Arur S, Ohmachi M, Berkseth M, Nayak S, Hansen D, Zarkower D, Schedl T (2011) MPK-1 ERK controls membrane organization in C. elegans oogenesis via a sex-determination module. Dev Cell 20(5):677–688

    PubMed  CAS  Google Scholar 

  • Bailly A, Gartner A (2012) Germ cell apoptosis and DNA damage responses. Advances in Experimental Medicine and Biology 757:249–276. (Chap. 9, this volume) Springer, New York

    PubMed  CAS  Google Scholar 

  • Bembenek JN, Richie CT, Squirrell JM, Campbell JM, Eliceiri KW, Poteryaev D, Spang A, Golden A, White JG (2007) Cortical granule exocytosis in C. elegans is regulated by cell cycle components including separase. Development 134(21):3837–3848

    PubMed  CAS  Google Scholar 

  • Bishop JD, Han Z, Schumacher JM (2005) The Caenorhabditis elegans Aurora B kinase AIR-2 phosphorylates and is required for the localization of a BimC kinesin to meiotic and mitotic spindles. Mol Biol Cell 16(2):742–756

    PubMed  CAS  Google Scholar 

  • Bottino D, Mogilner A, Roberts T, Stewart M, Oster G (2002) How nematode sperm crawl. J Cell Sci 115(Pt 2):367–384

    PubMed  CAS  Google Scholar 

  • 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(10):2227–2239

    PubMed  CAS  Google Scholar 

  • Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Mayo KE, Shea LD, Woodruff TK (2006) Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev Biol 298(1):149–154

    PubMed  CAS  Google Scholar 

  • Browning H, Strome S (1996) A sperm-supplied factor required for embryogenesis in C. elegans. Development 122(1):391–404

    PubMed  CAS  Google Scholar 

  • Buck SH, Chiu D, Saito RM (2009) The cyclin-dependent kinase inhibitors, cki-1 and cki-2, act in overlapping but distinct pathways to control cell cycle quiescence during C. elegans development. Cell Cycle 8(16):2613–2620

    PubMed  CAS  Google Scholar 

  • 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(5):1641–1651

    PubMed  CAS  Google Scholar 

  • Burke DJ, Ward S (1983) Identification of a large multigene family encoding the major sperm protein of Caenorhabditis elegans. J Mol Biol 171(1):1–29

    PubMed  CAS  Google Scholar 

  • Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, Schumacher JM, Golden A (2006) The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133(4):697–709

    PubMed  CAS  Google Scholar 

  • Castilho PV, Williams BC, Mochida S, Zhao Y, Goldberg ML (2009) The M phase kinase Greatwall (Gwl) promotes inactivation of PP2A/B55delta, a phosphatase directed against CDK phosphosites. Mol Biol Cell 20(22):4777–4789

    PubMed  CAS  Google Scholar 

  • 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(1):26–41

    PubMed  CAS  Google Scholar 

  • Cheng H, Govindan JA, Greenstein D (2008) Regulated trafficking of the MSP/Eph receptor during oocyte meiotic maturation in C. elegans. Curr Biol 18(10):705–714

    PubMed  CAS  Google Scholar 

  • Cheng KC, Klancer R, Singson A, 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(3):560–572

    PubMed  CAS  Google Scholar 

  • Chi W, Reinke V (2006) Promotion of oogenesis and embryogenesis in the C. elegans gonad by EFL-1/DPL-1 (E2F) does not require LIN-35 (pRB). Development 133(16):3147–3157

    PubMed  CAS  Google Scholar 

  • Chi W, Reinke V (2009) DPL-1 (DP) acts in the germ line to coordinate ovulation and fertilization in C. elegans. Mech Dev 126(5–6):406–416

    PubMed  CAS  Google Scholar 

  • Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20(17):1522–1528

    PubMed  CAS  Google Scholar 

  • Cho S, Jin SW, Cohen A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14(7):1207–1220

    PubMed  CAS  Google Scholar 

  • Chu DS, Shakes DC (2012) Spermatogenesis. Advances in Experimental Medicine and Biology 757:171–203. (Chap. 7, this volume) Springer, New York

    Google Scholar 

  • Church DL, Guan KL, 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(8):2525–2535

    PubMed  CAS  Google Scholar 

  • Clandinin TR, Mains PE (1993) Genetic studies of mei-1 gene activity during the transition from meiosis to mitosis in Caenorhabditis elegans. Genetics 134(1):199–210

    PubMed  CAS  Google Scholar 

  • Clandinin TR, DeModena JA, Sternberg PW (1998) Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92(4):523–533

    PubMed  CAS  Google Scholar 

  • 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(2):533–546

    PubMed  CAS  Google Scholar 

  • Clark-Maguire S, Mains PE (1994b) Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component. J Cell Biol 126(1):199–209

    PubMed  CAS  Google Scholar 

  • Clary LM, Okkema PG (2010) The EGR family gene egrh-1 functions non-autonomously in the control of oocyte meiotic maturation and ovulation in C. elegans. Development 137(18):3129–3137

    PubMed  CAS  Google Scholar 

  • Corrigan C, Subramanian R, Miller MA (2005) Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation. Development 132(23):5225–5237

    PubMed  CAS  Google Scholar 

  • 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(2):805–813

    PubMed  CAS  Google Scholar 

  • de Carvalho CE, Zaaijer S, Smolikov S, Gu Y, Schumacher JM, Colaiacovo MP (2008) LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev 22(20):2869–2885

    PubMed  Google Scholar 

  • 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(2):187–199

    PubMed  CAS  Google Scholar 

  • Deyter GM, Furuta T, Kurasawa Y, Schumacher JM (2010) Caenorhabditis elegans cyclin B3 is required for multiple mitotic processes including alleviation of a spindle checkpoint-dependent block in anaphase chromosome segregation. PLoS Genet 6(11):e1001218

    PubMed  Google Scholar 

  • Dorn JF, Zhang L, Paradis V, Edoh-Bedi D, Jusu S, Maddox PS, Maddox AS (2010) Actomyosin tube formation in polar body cytokinesis requires Anillin in C. elegans. Curr Biol 20(22):2046–2051

    PubMed  CAS  Google Scholar 

  • Dumont J, Million K, Sunderland K, Rassinier P, Lim H, Leader B, Verlhac MH (2007) Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 301(1):254–265

    PubMed  CAS  Google Scholar 

  • Dumont J, Oegema K, Desai A (2010) A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 12(9):894–901

    PubMed  CAS  Google Scholar 

  • 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(3):423–431

    PubMed  CAS  Google Scholar 

  • Dupre A, Jessus C, Ozon R, Haccard O (2002) Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. EMBO J 21(15):4026–4036

    PubMed  CAS  Google Scholar 

  • Edmonds JW, Prasain JK, Dorand D, Yang Y, Hoang HD, Vibbert J, Kubagawa HM, Miller MA (2010) Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev Cell 19(6):858–871

    PubMed  CAS  Google Scholar 

  • Eggan K, Jurga S, Gosden R, Min IM, Wagers AJ (2006) Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature 441(7097):1109–1114

    PubMed  CAS  Google Scholar 

  • Ellefson ML, McNally FJ (2009) Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans. Mol Biol Cell 20(11):2722–2730

    PubMed  CAS  Google Scholar 

  • Ellefson ML, McNally FJ (2011) CDK-1 inhibits meiotic spindle shortening and dynein-dependent spindle rotation in C. elegans. J Cell Biol 193(7):1229–1244

    PubMed  CAS  Google Scholar 

  • Fabritius AS, Ellefson ML, McNally FJ (2011) Nuclear and spindle positioning during oocyte meiosis. Curr Opin Cell Biol 23(1):78–84

    PubMed  CAS  Google Scholar 

  • Ferby I, Blazquez M, Palmer A, Eritja R, Nebreda AR (1999) A novel p34(cdc2)-binding and activating protein that is necessary and sufficient to trigger G(2)/M progression in Xenopus oocytes. Genes Dev 13(16):2177–2189

    PubMed  CAS  Google Scholar 

  • Ferrell JE Jr (1999a) Xenopus oocyte maturation: new lessons from a good egg. Bioessays 21(10):833–842

    PubMed  Google Scholar 

  • Ferrell JE Jr (1999b) Building a cellular switch: more lessons from a good egg. Bioessays 21(10):866–870

    PubMed  Google Scholar 

  • Francis R, Maine E, Schedl T (1995) Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 139(2):607–630

    PubMed  CAS  Google Scholar 

  • 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(4):1401–1419

    PubMed  CAS  Google Scholar 

  • Gautier J, Norbury C, Lohka M, Nurse P, Maller J (1988) Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell 54(3):433–439

    PubMed  CAS  Google Scholar 

  • 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(3):487–494

    PubMed  CAS  Google Scholar 

  • George SE, Simokat K, Hardin J, Chisholm AD (1998) The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans. Cell 92(5):633–643

    PubMed  CAS  Google Scholar 

  • Gibert MA, Starck J, Beguet B (1984) Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans. Biol Cell 50(1):77–85

    PubMed  CAS  Google Scholar 

  • Gissendanner CR, Kelley K, Nguyen TQ, Hoener MC, Sluder AE, Maina CV (2008) The Caenorhabditis elegans NR4A nuclear receptor is required for spermatheca morphogenesis. Dev Biol 313(2):767–786

    PubMed  CAS  Google Scholar 

  • 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(7):1469–1482

    PubMed  CAS  Google Scholar 

  • Goldstein B, Hird SN (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122(5):1467–1474

    PubMed  CAS  Google Scholar 

  • Govindan JA, Cheng H, Harris JE, Greenstein D (2006) Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr Biol 16(13):1257–1268

    PubMed  CAS  Google Scholar 

  • Govindan JA, Nadarajan S, Kim S, Starich TA, Greenstein D (2009) Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 136(13):2211–2221

    PubMed  CAS  Google Scholar 

  • Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10(12):4311–4326

    PubMed  CAS  Google Scholar 

  • Green RA, Kao HL, Audhya A, Arur S, Mayers JR, Fridolfsson HN, Schulman M, Schloissnig S, Niessen S, Laband K, Wang S, Starr DA, Hyman AA, Schedl T, Desai A, Piano F, Gunsalus KC, Oegema K (2011) A high-resolution C. elegans essential gene network based on phenotypic profiling of a complex tissue. Cell 145(3):470–482

    PubMed  CAS  Google Scholar 

  • Greenstein D, Hird S, Plasterk RH, 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(16):1935–1948

    PubMed  CAS  Google Scholar 

  • 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(5):1011–1022

    PubMed  CAS  Google Scholar 

  • Gutch MJ, Flint AJ, Keller J, Tonks NK, Hengartner MO (1998) The Caenorhabditis elegans SH2 domain-containing protein tyrosine phosphatase PTP-2 participates in signal transduction during oogenesis and vulval development. Genes Dev 12(4):571–585

    PubMed  CAS  Google Scholar 

  • Guven-Ozkan T, Nishi Y, Robertson SM, Lin R (2008) Global transcriptional repression in C. elegans germline precursors by regulated sequestration of TAF-4. Cell 135(1):149–160

    PubMed  CAS  Google Scholar 

  • Guven-Ozkan T, Robertson SM, Nishi Y, Lin R (2010) zif-1 translational repression defines a second, mutually exclusive OMA function in germline transcriptional repression. Development 137(20):3373–3382

    PubMed  CAS  Google Scholar 

  • Haccard O, Jessus C (2006) Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. EMBO Rep 7(3):321–325

    PubMed  CAS  Google Scholar 

  • Hall DH, Altun Z (2008) C. elegans atlas. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • 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(1):101–123

    PubMed  CAS  Google Scholar 

  • Hansen D, Schedl T (2012) Stem cell proliferation versus meiotic fate decision in C. elegans. Advances in Experimental Medicine and Biology 757:71–99. (Chap. 4, this volume) Springer, New York

    Google Scholar 

  • Harris JE, Govindan JA, Yamamoto I, Schwartz J, Kaverina I, Greenstein D (2006) Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev Biol 299(1):105–121

    PubMed  CAS  Google Scholar 

  • Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev 2(4):280–291

    CAS  Google Scholar 

  • Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382(6590):420–425

    PubMed  CAS  Google Scholar 

  • Henderson MA, Cronland E, Dunkelbarger S, Contreras V, Strome S, Keiper BD (2009) A germline-specific isoform of eIF4E (IFE-1) is required for efficient translation of stored mRNAs and maturation of both oocytes and sperm. J Cell Sci 122(Pt 10):1529–1539

    PubMed  CAS  Google Scholar 

  • Hiatt SM, Duren HM, Shyu YJ, Ellis RE, Hisamoto N, Matsumoto K, Kariya K, Kerppola TK, Hu CD (2009) Caenorhabditis elegans FOS-1 and JUN-1 regulate plc-1 expression in the spermatheca to control ovulation. Mol Biol Cell 20(17):3888–3895

    PubMed  CAS  Google Scholar 

  • 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(1):154–166

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hochegger H, Klotzbucher A, Kirk J, Howell M, le Guellec K, Fletcher K, Duncan T, Sohail M, Hunt T (2001) New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation. Development 128(19):3795–3807

    PubMed  CAS  Google Scholar 

  • Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37(12):1351–1355

    PubMed  CAS  Google Scholar 

  • Hopper NA, Lee J, Sternberg PW (2000) ARK-1 inhibits EGFR signaling in C. elegans. Mol Cell 6(1):65–75

    PubMed  CAS  Google Scholar 

  • Horner VL, Wolfner MF (2008) Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn 237(3):527–544

    PubMed  CAS  Google Scholar 

  • 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(6):1227–1238

    PubMed  CAS  Google Scholar 

  • Hubbard EJ, Greenstein D (2000) The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 218(1):2–22

    PubMed  CAS  Google Scholar 

  • Hughes SE, Evason K, Xiong C, Kornfeld K (2007) Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet 3(2):e25

    PubMed  Google Scholar 

  • Hughes SE, Huang C, Kornfeld K (2011) Identification of mutations that delay somatic or reproductive aging of Caenorhabditis elegans. Genetics 189(1):341–356

    Google Scholar 

  • Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ (2003) Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 13(7):546–553

    PubMed  CAS  Google Scholar 

  • Iwasaki K, McCarter J, Francis R, Schedl T (1996) emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. J Cell Biol 134(3):699–714

    PubMed  CAS  Google Scholar 

  • Jadhav S, Rana M, Subramaniam K (2008) Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos-2 to primordial germ cells. Development 135(10):1803–1812

    PubMed  CAS  Google Scholar 

  • Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J (2007) Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol 308(1):206–221

    PubMed  CAS  Google Scholar 

  • Johnston WL, Krizus A, Dennis JW (2006) The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. elegans embryo. BMC Biol 4:35

    PubMed  Google Scholar 

  • Johnston WL, Krizus A, Dennis JW (2010) Eggshell chitin and chitin-interacting proteins prevent polyspermy in C. elegans. Curr Biol 20(21):1932–1937

    PubMed  CAS  Google Scholar 

  • Jud M, Razelun J, Bickel J, Czerwinski M, Schisa JA (2007) Conservation of large foci formation in arrested oocytes of Caenorhabditis nematodes. Dev Genes Evol 217(3):221–226

    PubMed  Google Scholar 

  • Jud MC, Czerwinski MJ, Wood MP, Young RA, Gallo CM, Bickel JS, Petty EL, Mason JM, Little BA, Padilla PA, Schisa JA (2008) Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway. Dev Biol 318(1):38–51

    PubMed  CAS  Google Scholar 

  • Kadyk LC, Kimble J (1998) Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125(10):1803–1813

    PubMed  CAS  Google Scholar 

  • Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, Brunger AT (2005) Structural basis of FFAT motif-mediated ER targeting. Structure 13(7):1035–1045

    PubMed  CAS  Google Scholar 

  • Kaitna S, Mendoza M, Jantsch-Plunger V, Glotzer M (2000) Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr Biol 10(19):1172–1181

    PubMed  CAS  Google Scholar 

  • Kalab P, Solc P, Motlik J (2011) The role of RanGTP gradient in vertebrate oocyte maturation. Results Probl Cell Differ 53:235–267

    PubMed  CAS  Google Scholar 

  • Kaneda M, Tang F, O’Carroll D, Lao K, Surani MA (2009) Essential role for Argonaute2 protein in mouse oogenesis. Epigenetics Chromatin 2(1):9

    PubMed  Google Scholar 

  • Kariya K, Bui YK, Gao X, Sternberg PW, Kataoka T (2004) Phospholipase Cepsilon regulates ovulation in Caenorhabditis elegans. Dev Biol 274(1):201–210

    PubMed  CAS  Google Scholar 

  • Kashina AS, Rogers GC, Scholey JM (1997) The bimC family of kinesins: essential bipolar mitotic motors driving centrosome separation. Biochim Biophys Acta 1357(3):257–271

    PubMed  CAS  Google Scholar 

  • Kemphues KJ, Priess JR, Morton DG, Cheng NS (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52(3):311–320

    PubMed  CAS  Google Scholar 

  • Kim DY, Roy R (2006) Cell cycle regulators control centrosome elimination during oogenesis in Caenorhabditis elegans. J Cell Biol 174(6):751–757

    PubMed  CAS  Google Scholar 

  • Kimble J, Sharrock WJ (1983) Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev Biol 96(1):189–196

    PubMed  CAS  Google Scholar 

  • Kiontke K, Fitch DH (2005) The phylogenetic relationships of Caenorhabditis and other rhabditids. WormBook:1–11

    Google Scholar 

  • Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101(24):9003–9008

    PubMed  CAS  Google Scholar 

  • Klass MR, Kinsley S, Lopez LC (1984) Isolation and characterization of a sperm-specific gene family in the nematode Caenorhabditis elegans. Mol Cell Biol 4(3):529–537

    PubMed  CAS  Google Scholar 

  • Kornbluth S, Sebastian B, Hunter T, Newport J (1994) Membrane localization of the kinase which phosphorylates p34cdc2 on threonine 14. Mol Biol Cell 5(3):273–282

    PubMed  CAS  Google Scholar 

  • Korswagen HC, Park JH, Ohshima Y, Plasterk RH (1997) An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration. Genes Dev 11(12):1493–1503

    PubMed  CAS  Google Scholar 

  • 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(15):3357–3369

    PubMed  CAS  Google Scholar 

  • Kostic I, Li S, Roy R (2003) cki-1 links cell division and cell fate acquisition in the C. elegans somatic gonad. Dev Biol 263(2):242–252

    PubMed  CAS  Google Scholar 

  • Kovacevic I, Cram EJ (2010) FLN-1/filamin is required for maintenance of actin and exit of fertilized oocytes from the spermatheca in C. elegans. Dev Biol 347(2):247–257

    PubMed  CAS  Google Scholar 

  • Kubagawa HM, Watts JL, Corrigan C, Edmonds JW, Sztul E, Browse J, Miller MA (2006) Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat Cell Biol 8(10):1143–1148

    PubMed  CAS  Google Scholar 

  • Kumagai A, Dunphy WG (1991) The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 64(5):903–914

    PubMed  CAS  Google Scholar 

  • Kumagai A, Dunphy WG (1996) Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science 273(5280):1377–1380

    PubMed  CAS  Google Scholar 

  • Lee MH, Ohmachi M, Arur S, Nayak S, Francis R, Church D, Lambie E, Schedl T (2007) Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177(4):2039–2062

    PubMed  CAS  Google Scholar 

  • Lenormand JL, Dellinger RW, Knudsen KE, Subramani S, Donoghue DJ (1999) Speedy: a novel cell cycle regulator of the G2/M transition. EMBO J 18(7):1869–1877

    PubMed  CAS  Google Scholar 

  • Li H, Guo F, Rubinstein B, Li R (2008) Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nat Cell Biol 10(11):1301–1308

    PubMed  CAS  Google Scholar 

  • Liang CG, Su YQ, Fan HY, Schatten H, Sun QY (2007) Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol Endocrinol 21(9):2037–2055

    PubMed  CAS  Google Scholar 

  • Liang ZY, Hallen MA, Endow SA (2009) Mature Drosophila meiosis I spindles comprise microtubules of mixed polarity. Curr Biol 19(2):163–168

    PubMed  CAS  Google Scholar 

  • Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, Hoog C, Herbert M (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20(17):1511–1521

    PubMed  CAS  Google Scholar 

  • 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(16):1458–1468

    PubMed  CAS  Google Scholar 

  • 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(15):3513–3525

    PubMed  CAS  Google Scholar 

  • 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(9):3009–3013

    PubMed  CAS  Google Scholar 

  • Lorin-Nebel C, Xing J, Yan X, Strange K (2007) CRAC channel activity in C. elegans is mediated by Orai1 and STIM1 homologues and is essential for ovulation and fertility. J Physiol 580(Pt 1):67–85

    Google Scholar 

  • Lui DY, Colaiácovo MP (2012) Meiotic development in C. elegans. Advances in Experimental Medicine and Biology 757:133–170. (Chap. 6, this volume) Springer, New York

    Google Scholar 

  • Luo S, Shaw WM, Ashraf J, Murphy CT (2009) TGF-beta Sma/Mab signaling mutations uncouple reproductive aging from somatic aging. PLoS Genet 5(12):e1000789

    PubMed  Google Scholar 

  • Luo S, Kleemann GA, Ashraf JM, Shaw WM, Murphy CT (2010) TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143(2):299–312

    PubMed  CAS  Google Scholar 

  • Maddox PS, Oegema K, Desai A, Cheeseman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res 12(6):641–653

    PubMed  CAS  Google Scholar 

  • Maddox AS, Habermann B, Desai A, Oegema K (2005) Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132(12):2837–2848

    PubMed  CAS  Google Scholar 

  • 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(3):593–605

    PubMed  CAS  Google Scholar 

  • Marcello MR, Singaravelu G, Singson A (2012) Fertilization. Advances in Experimental Medicine and Biology 757:321–350. (Chap. 11, this volume) Springer, New York

    Google Scholar 

  • Maruyama R, Velarde NV, Klancer R, Gordon S, Kadandale P, Parry JM, Hang JS, Rubin J, Stewart-Michaelis A, Schweinsberg P, Grant BD, Piano F, Sugimoto A, Singson A (2007) EGG-3 regulates cell-surface and cortex rearrangements during egg activation in Caenorhabditis elegans. Curr Biol 17(18):1555–1560

    PubMed  CAS  Google Scholar 

  • 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):1–17

    PubMed  CAS  Google Scholar 

  • Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282

    PubMed  CAS  Google Scholar 

  • Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177(2):129–145

    PubMed  CAS  Google Scholar 

  • Matthies HJ, McDonald HB, Goldstein LS, Theurkauf WE (1996) Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein. J Cell Biol 134(2):455–464

    PubMed  CAS  Google Scholar 

  • Matyash V, Geier C, Henske A, Mukherjee S, Hirsh D, Thiele C, Grant B, Maxfield FR, Kurzchalia TV (2001) Distribution and transport of cholesterol in Caenorhabditis elegans. Mol Biol Cell 12(6):1725–1736

    PubMed  CAS  Google Scholar 

  • McCarter J (1998) The regulation of oocyte maturation and ovulation in Caenorhabditis elegans. PhD Thesis, Washington University

    Google Scholar 

  • McCarter J, Bartlett B, Dang T, Schedl T (1997) Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev Biol 181(2):121–143

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • McMullan R, Nurrish SJ (2011) The RHO-1 RhoGTPase modulates fertility and multiple behaviors in adult C. elegans. PLoS One 6(2):e17265

    PubMed  CAS  Google Scholar 

  • McNally KL, McNally FJ (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282(1):218–230

    PubMed  CAS  Google Scholar 

  • McNally KP, McNally FJ (2011) The spindle assembly function of Caenorhabditis elegans katanin does not require microtubule-severing activity. Mol Biol Cell 22(9):1550–1560

    PubMed  CAS  Google Scholar 

  • McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75(3):419–429

    PubMed  CAS  Google Scholar 

  • McNally K, Audhya A, Oegema K, McNally FJ (2006) Katanin controls mitotic and meiotic spindle length. J Cell Biol 175(6):881–891

    PubMed  CAS  Google Scholar 

  • McNally KL, Martin JL, Ellefson M, McNally FJ (2010) Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos. Dev Biol 339(1):126–140

    PubMed  CAS  Google Scholar 

  • Mendez R, Richter JD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2(7):521–529

    PubMed  CAS  Google Scholar 

  • Mendez R, Hake LE, Andresson T, Littlepage LE, Ruderman JV, Richter JD (2000) Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature 404(6775):302–307

    PubMed  CAS  Google Scholar 

  • Meyerzon M, Fridolfsson HN, Ly N, McNally FJ, Starr DA (2009) UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 136(16):2725–2733

    PubMed  CAS  Google Scholar 

  • Mikeladze-Dvali T, von Tobel L, Strnad P, Knott G, Leonhardt H, Schermelleh L, Gönczy P (2012) Analysis of centriole elimination during C. elegans oogenesis. Development 139(9):1670–1679

    PubMed  CAS  Google Scholar 

  • Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, Caprioli RM, Greenstein D (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291(5511):2144–2147

    PubMed  CAS  Google Scholar 

  • 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(2):187–200

    PubMed  CAS  Google Scholar 

  • Mochida S, Maslen SL, Skehel M, Hunt T (2010) Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330(6011):1670–1673

    PubMed  CAS  Google Scholar 

  • Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7(12):1248–1255

    PubMed  Google Scholar 

  • Morgan DO (2007) The cell cycle: principles of control. New Science Press, London

    Google Scholar 

  • Mueller PR, Coleman TR, Dunphy WG (1995) Cell cycle regulation of a Xenopus Wee1-like kinase. Mol Biol Cell 6(1):119–134

    PubMed  CAS  Google Scholar 

  • Muller-Reichert T, Greenan G, O’Toole E, Srayko M (2010) The elegans of spindle assembly. Cell Mol Life Sci 67(13):2195–2213

    PubMed  Google Scholar 

  • Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM, Hannon GJ (2007) Critical roles for Dicer in the female germline. Genes Dev 21(6):682–693

    PubMed  CAS  Google Scholar 

  • Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116(2):221–234

    PubMed  CAS  Google Scholar 

  • Myers CD, Goh PY, Allen TS, Bucher EA, Bogaert T (1996) Developmental genetic analysis of troponin T mutations in striated and nonstriated muscle cells of Caenorhabditis elegans. J Cell Biol 132(6):1061–1077

    PubMed  CAS  Google Scholar 

  • Na J, Zernicka-Goetz M (2006) Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr Biol 16(12):1249–1254

    PubMed  CAS  Google Scholar 

  • Nadarajan S, Govindan JA, McGovern M, Hubbard EJ, Greenstein D (2009) MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 136(13):2223–2234

    PubMed  CAS  Google Scholar 

  • Nance J, Zallen JA (2011) Elaborating polarity: PAR proteins and the cytoskeleton. Development 138(5):799–809

    PubMed  CAS  Google Scholar 

  • Noble SL, Allen BL, Goh LK, Nordick K, Evans TC (2008) Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development. J Cell Biol 182(3):559–572

    PubMed  CAS  Google Scholar 

  • Norman KR, Fazzio RT, Mellem JE, Espelt MV, Strange K, Beckerle MC, Maricq AV (2005) The Rho/Rac-family guanine nucleotide exchange factor VAV-1 regulates rhythmic behaviors in C. elegans. Cell 123(1):119–132

    PubMed  CAS  Google Scholar 

  • Nousch M, Eckmann CR (2012) Translational control in the C. elegans germ line. Advances in Experimental Medicine and Biology 757:205–247. (Chap. 8, this volume) Springer, New York

    Google Scholar 

  • Obinata T, Ono K, Ono S (2010) Troponin I controls ovulatory contraction of non-striated actomyosin networks in the C. elegans somatic gonad. J Cell Sci 123(Pt 9):1557–1566

    PubMed  CAS  Google Scholar 

  • 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(4):547–558

    PubMed  Google Scholar 

  • Ohmachi M, Rocheleau CE, Church D, Lambie E, Schedl T, Sundaram MV (2002) C. elegans ksr-1 and ksr-2 have both unique and redundant functions and are required for MPK-1 ERK phosphorylation. Curr Biol 12(5):427–433

    PubMed  CAS  Google Scholar 

  • Ono K, Ono S (2004) Tropomyosin and troponin are required for ovarian contraction in the Caenorhabditis elegans reproductive system. Mol Biol Cell 15(6):2782–2793

    PubMed  CAS  Google Scholar 

  • Ono K, Yu R, Ono S (2007) Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation. Dev Dyn 236(4):1093–1105

    PubMed  CAS  Google Scholar 

  • Ono K, Yamashiro S, Ono S (2008) Essential role of ADF/cofilin for assembly of contractile actin networks in the C elegans somatic gonad. J Cell Sci 121(Pt 16):2662–2670

    PubMed  CAS  Google Scholar 

  • Padmanabhan K, Richter JD (2006) Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 20(2):199–209

    PubMed  CAS  Google Scholar 

  • 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(3):451–460

    PubMed  CAS  Google Scholar 

  • Parry JM, Velarde NV, Lefkovith AJ, Zegarek MH, Hang JS, Ohm J, Klancer R, Maruyama R, Druzhinina MK, Grant BD, Piano F, 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(20):1752–1757

    PubMed  CAS  Google Scholar 

  • Patterson JR, Wood MP, Schisa JA (2011) Assembly of RNP granules in stressed and aging oocytes requires nucleoporins and is coordinated with nuclear membrane blebbing. Dev Biol 353(2):173–185

    PubMed  CAS  Google Scholar 

  • Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, Woglar A, Csaszar E, Pasierbek P, Ammerer G, Gruenbaum Y, Jantsch V (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139(5):920–933

    PubMed  CAS  Google Scholar 

  • Pepling ME, Spradling AC (1998) Female mouse germ cells form synchronously dividing cysts. Development 125(17):3323–3328

    PubMed  CAS  Google Scholar 

  • Peter M, Labbe JC, Doree M, Mandart E (2002) A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. Development 129(9):2129–2139

    PubMed  CAS  Google Scholar 

  • Peters JM (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 9(5):931–943

    PubMed  CAS  Google Scholar 

  • Peters H, Levy E, Crone M (1962) Deoxyribonucleic acid synthesis in oocytes of mouse embryos. Nature 195:915–916

    PubMed  CAS  Google Scholar 

  • Piekny AJ, Mains PE (2002) Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J Cell Sci 115(Pt 11):2271–2282

    PubMed  CAS  Google Scholar 

  • Pilipiuk J, Lefebvre C, Wiesenfahrt T, Legouis R, Bossinger O (2009) Increased IP3/Ca2+ signaling compensates depletion of LET-413/DLG-1 in C. elegans epithelial junction assembly. Dev Biol 327(1):34–47

    PubMed  CAS  Google Scholar 

  • Powers J, Rose DJ, Saunders A, Dunkelbarger S, Strome S, Saxton WM (2004) Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. J Cell Biol 166(7):991–1001

    PubMed  CAS  Google Scholar 

  • Racki WJ, Richter JD (2006) CPEB controls oocyte growth and follicle development in the mouse. Development 133(22):4527–4537

    PubMed  CAS  Google Scholar 

  • 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(2):195–206

    PubMed  CAS  Google Scholar 

  • 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(7061):1048–1052

    PubMed  CAS  Google Scholar 

  • Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6(6):555–562

    PubMed  CAS  Google Scholar 

  • Revenkova E, Herrmann K, Adelfalk C, Jessberger R (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20(17):1529–1533

    PubMed  CAS  Google Scholar 

  • Richter JD (2007) CPEB: a life in translation. Trends Biochem Sci 32(6):279–285

    PubMed  CAS  Google Scholar 

  • Robertson S, Lin R (2012) The oocyte-to-embryo transition. Advances in Experimental Medicine and Biology, 757:351–372. (Chap. 12, this volume) Springer, New York

    Google Scholar 

  • Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157(2):219–229

    PubMed  CAS  Google Scholar 

  • 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(1):59–77

    PubMed  CAS  Google Scholar 

  • Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254

    PubMed  CAS  Google Scholar 

  • Rutledge E, Bianchi L, Christensen M, Boehmer C, Morrison R, Broslat A, Beld AM, George AL, Greenstein D, Strange K (2001) CLH-3, a ClC-2 anion channel ortholog activated during meiotic maturation in C. elegans oocytes. Curr Biol 11(3):161–170

    PubMed  CAS  Google Scholar 

  • Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF (1988) Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335(6190):519–525

    PubMed  CAS  Google Scholar 

  • Samuel AD, Murthy VN, Hengartner MO (2001) Calcium dynamics during fertilization in C. elegans. BMC Dev Biol 1:8

    PubMed  CAS  Google Scholar 

  • Sato K, Sato M, Audhya A, Oegema K, Schweinsberg P, Grant BD (2006) Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol Biol Cell 17(7):3085–3094

    PubMed  CAS  Google Scholar 

  • Saunders AM, Powers J, Strome S, Saxton WM (2007) Kinesin-5 acts as a brake in anaphase spindle elongation. Curr Biol 17(12):R453–R454

    PubMed  CAS  Google Scholar 

  • Schisa JA, Pitt JN, Priess JR (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128(8):1287–1298

    PubMed  CAS  Google Scholar 

  • Schuh M, Ellenberg J (2008) A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18(24):1986–1992

    PubMed  CAS  Google Scholar 

  • Schumacher JM, Golden A, Donovan PJ (1998) AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 143(6):1635–1646

    PubMed  CAS  Google Scholar 

  • Segbert C, Barkus R, Powers J, Strome S, Saxton WM, Bossinger O (2003) KLP-18, a Klp2 kinesin, is required for assembly of acentrosomal meiotic spindles in Caenorhabditis elegans. Mol Biol Cell 14(11):4458–4469

    PubMed  CAS  Google Scholar 

  • Seidel HS, Kimble J (2011) The oogenic germline starvation response in C. elegans. PLoS One 6(12):e28074

    PubMed  CAS  Google Scholar 

  • Severson AF, Ling L, van Zuylen V, Meyer BJ (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23(15):1763–1778

    Google Scholar 

  • 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(8):1605–1620

    PubMed  CAS  Google Scholar 

  • Shakes DC, Allen AK, Albert KM, Golden A (2011) emb-1 encodes the APC16 subunit of the Caenorhabditis elegans anaphase-promoting complex. Genetics 189(2):549–560

    Google Scholar 

  • Shelton CA, Carter JC, Ellis GC, Bowerman B (1999) The nonmuscle myosin regulatory light chain gene mlc-4 is required for cytokinesis, anterior-posterior polarity, and body morphology during Caenorhabditis elegans embryogenesis. J Cell Biol 146(2):439–451

    PubMed  CAS  Google Scholar 

  • 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(9):933–947

    PubMed  CAS  Google Scholar 

  • 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(23):1825–1835

    PubMed  CAS  Google Scholar 

  • Skold HN, Komma DJ, Endow SA (2005) Assembly pathway of the anastral Drosophila oocyte meiosis I spindle. J Cell Sci 118(Pt 8):1745–1755

    PubMed  Google Scholar 

  • Smith LD, Ecker RE (1969) Role of the oocyte nucleus in physiological maturation in Rana pipiens. Dev Biol 19(3):281–309

    PubMed  CAS  Google Scholar 

  • Sonneville R, Gonczy P (2004) zyg-11 and cul-2 regulate progression through meiosis II and polarity establishment in C. elegans. Development 131(15):3527–3543

    PubMed  CAS  Google Scholar 

  • 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(9):1072–1084

    PubMed  CAS  Google Scholar 

  • Srayko M, O’Toole ET, Hyman AA, Muller-Reichert T (2006) Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol 16(19):1944–1949

    PubMed  CAS  Google Scholar 

  • St Johnston D, Ahringer J (2010) Cell polarity in eggs and epithelia: parallels and diversity. Cell 141(5):757–774

    PubMed  CAS  Google Scholar 

  • Starck J (1977) Radioautographic study of RNA synthesis in Caenorhabditis elegans (Bergerac Variety) oogenesis. Biol Cell 30:181–182

    Google Scholar 

  • Starich T, Sheehan M, Jadrich J, Shaw J (2001) Innexins in C. elegans. Cell Comm Adhesion 8(4–6):311–314

    Google Scholar 

  • Stitzel ML, Pellettieri J, Seydoux G (2006) The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr Biol 16(1):56–62

    PubMed  CAS  Google Scholar 

  • Strome S (1986) Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans. J Cell Biol 103(6 Pt 1):2241–2252

    PubMed  CAS  Google Scholar 

  • Sun QY, Liu K, Kikuchi K (2008) Oocyte-specific knockout: a novel in vivo approach for studying gene functions during folliculogenesis, oocyte maturation, fertilization, and embryogenesis. Biol Reprod 79(6):1014–1020

    PubMed  CAS  Google Scholar 

  • Susiarjo M, Hassold TJ, Freeman E, Hunt PA (2007) Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet 3(1):e5

    PubMed  Google Scholar 

  • Suzuki Y, Han M (2006) Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Genes Dev 20(4):423–428

    PubMed  CAS  Google Scholar 

  • Swan KA, Severson AF, Carter JC, Martin PR, Schnabel H, Schnabel R, Bowerman B (1998) cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. J Cell Sci 111(Pt 14):2017–2027

    PubMed  CAS  Google Scholar 

  • Tang F, Kaneda M, O’Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K, Surani MA (2007) Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21(6):644–648

    PubMed  CAS  Google Scholar 

  • Tarr DE, Scott AL (2005) MSP domain proteins. Trends Parasitol 21(5):224–231

    PubMed  CAS  Google Scholar 

  • 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(6):821–822

    PubMed  CAS  Google Scholar 

  • Tsuda H, Han SM, Yang Y, Tong C, Lin YQ, Mohan K, Haueter C, Zoghbi A, Harati Y, Kwan J, Miller MA, Bellen HJ (2008) The amyotrophic lateral sclerosis 8 protein VAPB is cleaved, secreted, and acts as a ligand for Eph receptors. Cell 133(6):963–977

    PubMed  CAS  Google Scholar 

  • Tunquist BJ, Maller JL (2003) Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev 17(6):683–710

    PubMed  CAS  Google Scholar 

  • van der Voet M, Berends CW, Perreault A, Nguyen-Ngoc T, Gonczy P, Vidal M, Boxem M, van den Heuvel S (2009) NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Galpha. Nat Cell Biol 11(3):269–277

    PubMed  Google Scholar 

  • Vazquez-Manrique RP, Nagy AI, Legg JC, Bales OA, Ly S, Baylis HA (2008) Phospholipase C-epsilon regulates epidermal morphogenesis in Caenorhabditis elegans. PLoS Genet 4(3):e1000043

    PubMed  Google Scholar 

  • Von Stetina JR, Tranguch S, Dey SK, Lee LA, Cha B, Drummond-Barbosa D (2008) alpha-Endosulfine is a conserved protein required for oocyte meiotic maturation in Drosophila. Development 135(22):3697–3706

    Google Scholar 

  • Walczak CE, Vernos I, Mitchison TJ, Karsenti E, Heald R (1998) A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr Biol 8(16):903–913

    PubMed  CAS  Google Scholar 

  • Walker AK, Boag PR, Blackwell TK (2007) Transcription reactivation steps stimulated by oocyte maturation in C. elegans. Dev Biol 304(1):382–393

    PubMed  CAS  Google Scholar 

  • Walter SA, Guadagno SN, Ferrell JE Jr (2000) Activation of Wee1 by p42 MAPK in vitro and in cycling Xenopus egg extracts. Mol Biol Cell 11(3):887–896

    PubMed  CAS  Google Scholar 

  • Wang R, He G, Nelman-Gonzalez M, Ashorn CL, Gallick GE, Stukenberg PT, Kirschner MW, Kuang J (2007) Regulation of Cdc25C by ERK-MAP kinases during the G2/M transition. Cell 128(6):1119–1132

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ward S, Burke DJ, Sulston JE, Coulson AR, Albertson DG, Ammons D, Klass M, Hogan E (1988) Genomic organization of major sperm protein genes and pseudogenes in the nematode Caenorhabditis elegans. J Mol Biol 199(1):1–13

    PubMed  CAS  Google Scholar 

  • Whitten SJ, Miller MA (2007) The role of gap junctions in Caenorhabditis elegans oocyte maturation and fertilization. Dev Biol 301(2):432–446

    PubMed  CAS  Google Scholar 

  • Wignall SM, Villeneuve AM (2009) Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11(7):839–844

    PubMed  CAS  Google Scholar 

  • Wilson EB (1925) The cell in development and heredity. Macmillan, New York

    Google Scholar 

  • Wissmann A, Ingles J, Mains PE (1999) The Caenorhabditis elegans mel-11 myosin phosphatase regulatory subunit affects tissue contraction in the somatic gonad and the embryonic epidermis and genetically interacts with the Rac signaling pathway. Dev Biol 209(1):111–127

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Wolke U, Jezuit EA, Priess JR (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134(12):2227–2236

    PubMed  CAS  Google Scholar 

  • Wolstenholme J, Angell RR (2000) Maternal age and trisomy–a unifying mechanism of formation. Chromosoma 109(7):435–438

    PubMed  CAS  Google Scholar 

  • Woodruff GC, Eke O, Baird SE, Felix MA, Haag ES (2010) Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186(3):997–1012

    PubMed  Google Scholar 

  • Xu X, Guo H, Wycuff DL, Lee M (2007) Role of phosphatidylinositol-4-phosphate 5′ kinase (ppk-1) in ovulation of Caenorhabditis elegans. Exp Cell Res 313(11):2465–2475

    PubMed  CAS  Google Scholar 

  • Yan X, Xing J, Lorin-Nebel C, Estevez AY, Nehrke K, Lamitina T, Strange K (2006) Function of a STIM1 homologue in C. elegans: evidence that store-operated Ca2+ entry is not essential for oscillatory Ca2+ signaling and ER Ca2+ homeostasis. J Gen Physiol 128(4):443–459

    PubMed  CAS  Google Scholar 

  • 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(1):245–259

    PubMed  CAS  Google Scholar 

  • Yang HY, Mains PE, McNally FJ (2005) Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter. J Cell Biol 169(3):447–457

    PubMed  CAS  Google Scholar 

  • Yang Y, Han SM, Miller MA (2010) MSP hormonal control of the oocyte MAP kinase cascade and reactive oxygen species signaling. Dev Biol 342(1):96–107

    PubMed  CAS  Google Scholar 

  • Yin X, Gower NJ, Baylis HA, Strange K (2004) Inositol 1,4,5-trisphosphate signaling regulates rhythmic contractile activity of myoepithelial sheath cells in Caenorhabditis elegans. Mol Biol Cell 15(8):3938–3949

    PubMed  CAS  Google Scholar 

  • Yu J, Zhao Y, Li Z, Galas S, Goldberg ML (2006) Greatwall kinase participates in the Cdc2 autoregulatory loop in Xenopus egg extracts. Mol Cell 22(1):83–91

    PubMed  CAS  Google Scholar 

  • Zetka M (2009) Homologue pairing, recombination and segregation in Caenorhabditis elegans. Genome Dyn 5:43–55

    PubMed  CAS  Google Scholar 

  • Zhao Y, Haccard O, Wang R, Yu J, Kuang J, Jessus C, Goldberg ML (2008) Roles of Greatwall kinase in the regulation of cdc25 phosphatase. Mol Biol Cell 19(4):1317–1327

    PubMed  CAS  Google Scholar 

  • Zhou K, Rolls MM, Hall DH, Malone CJ, Hanna-Rose W (2009) A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J Cell Biol 186(2):229–241

    PubMed  CAS  Google Scholar 

  • Zuckerman S (1951) The number of oocytes in the mature ovary. Recent Prog Horm Res 6:63–109

    Google Scholar 

Download references

Acknowledgments

We are grateful to Valerie Osterberg, Sara Christensen, and Bruce Bowerman for providing Fig. 10.6a. Thanks to Swathi Arur, Bruce Bowerman, Andy Golden, Frank McNally, Michael Miller, Martin Srayko, and Jennifer Schisa for providing comments on the manuscript. Thanks to Bruce Bowerman, Amaranath Govindan, Tim Schedl, Jennifer Schisa, and Todd Starich for communication of unpublished results. This work was supported by NIH grants GM65115 and GM57173 to D.G.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Greenstein .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Kim, S., Spike, C., Greenstein, D. (2013). Control of Oocyte Growth and Meiotic Maturation in Caenorhabditis elegans . In: Schedl, T. (eds) Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology, vol 757. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4015-4_10

Download citation

Publish with us

Policies and ethics