The spatial and mechanical challenges of female meiosis

Molecular Reproduction and Development

Volumn 78, Issue 10-11, 2011, Pages 769-777

  Evans, Janice P ^a   Robinson, Douglas N ^b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALCIUM; MYOSIN II;

ANAPHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL SHAPE; CELL STRUCTURE; CHROMATIN; CHROMOSOME; CYTOKINESIS; CYTOSKELETON; DAUGHTER CELL; FEEDBACK SYSTEM; FERTILIZATION; GAMETE; HAPLOID SPORE; MECHANICAL STRESS; MEIOSIS; MEIOTIC PROPHASE I; METAPHASE; MITOSIS SPINDLE; MORPHOGENESIS; NONHUMAN; OOCYTE; POLYSPERMY; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SPERMATOCYTE; TELOPHASE; XENOPUS; ZYGOTE;

ANIMALS; BIOMECHANICS; CELL POLARITY; CELL SHAPE; FEMALE; HUMANS; MAMMALS; MEIOSIS; MITOSIS; MODELS, BIOLOGICAL; OOCYTES; POLAR BODIES;

MAMMALIA;

EID: 80054726341     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21358     Document Type: Review

References (78)

1. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, Verlhac MH. 2008. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 18: 1514-1519.
2. Barrett SL, Albertini DF. 2007. Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol Reprod 76: 949-957.
3. Bretscher A, Edwards K, Fehon RG. 2002. ERM proteins and merlin: Integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599.
4. Brunet S, Maro B. 2005. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: Integrating time and space. Reproduction 130: 801-811.
5. Carreno S, Kouranti I, Glusman ES, Fuller MT, Echard A, Payre F. 2008. Moesin and its activating kinase slik are required for cortical stability and microtubule organization in mitotic cells. J Cell Biol 180: 739-746.
6. Cho WK, Stern S, Biggers JD. 1974. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 187: 383-386.
7. Cole KS. 1932. Surface forces of the Arbacia egg. J Cell Comp Physiol 1: 1-9.
8. Cole KS, Michaelis EM. 1932. Surface forces of fertilized Arbacia eggs. J Cell Comp Physiol 2: 121-126.
9. D'Avino PP, Savoian MS, Glover DM. 2005. Cleavage furrow formation and ingression during animal cytokinesis: A microtubule legacy. J Cell Sci 118: 1549-1558.
10. De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Boroni A, Coticchio G. 2005. Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod Biomed Online 11: 36-42.
11. Deng M, Suraneni P, Schultz RM, Li R. 2007. The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes. Dev Cell 12: 301-308.
12. Derganc J, Božic B, Sventina S, Žekš B. 2000. Stability analysis of micropipette aspriation of neutrophils. Biophys J 79: 153-162.
13. Doi Y, Itoh M, Yonemura S, Ishihara S, Takano H, Noda T, Tsukita S. 1999. Normal development of mice and unimpaired cell adhesion/cell motility/actin-based cytoskeleton without compensatory up-regulation of ezrin or radixin in moesin gene knockout. J Biol Chem 274: 2315-2321.
14. Ducibella T. 1998. Biochemical and cellular insights into the temporal window of normal fertilization. Theriogenology 49: 53-65.
15. 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: 254-265.
16. Effler JC, Kee YS, Berk JM, Tran MN, Iglesias PA, Robinson DN. 2006. Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr Biol 16: 1962-1967.
17. Effler JC, Iglesias PA, Robinson DN. 2007. A mechanosensory system controls cell shape changes during mitosis. Cell Cycle 6: 30-35.
18. Evans E, Yeung A. 1989. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J 56: 151-160.
19. Evsikov AV, Graber JH, Brockman JM, Hampl A, Holbrook AE, Singh P, Eppig JJ, Solter D, Knowles BB. 2006. Cracking the egg: Molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes Dev 20: 2713-2727.
20. Fehon RG, McClatchey AI, Bretscher A. 2010. Organizing the cell cortex: The role of ERM proteins. Nat Rev Mol Cell Biol 11: 276-287.
21. Gardner AJ, Evans JP. 2006. Mammalian membrane block to polyspermy: New insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod Fertil Dev 18: 53-61.
22. Geiger B, Spatz JP, Bershadsky AD. 2009. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 10: 21-33.
23. Giansanti MG, Bonaccorsi S, Williams B, Williams EV, Santolamazza C, Goldberg ML, Gatti M. 1998. Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev 12: 396-410.
24. Gibson WT, Veldhuis JH, Rubinstein B, Cartwright HN, Perrimon N, Brodland GW, Nagpal R, Gibson MC. 2011. Control of the mitotic cleavage plane by local epithelial topology. Cell 144: 427-428.
25. Gönczy P. 2008. Mechanisms of asymmetric cell division: Flies and worms pave the way. Nat Rev Mol Cell Biol 9: 355-366.
26. Grill SW. 2010. Cell biology: Forced to be unequal. Science 330: 597-598.
27. Halet G, Carroll J. 2007. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 12: 309-317.
28. Hiramoto Y. 1976. Mechanical properties of starfish oocytes. Dev Growth Differ 18: 205-209.
29. Hochmuth RM. 2000. Micropipet aspiration of living cells. J Biomech 33: 15-22.
30. Horner VL, Wolfner MF. 2008. Mechanical stimulation by osmotic and hydrostatic pressure activates Drosophila oocytes in vitro in a calcium-dependent manner. Dev Biol 316: 100-109.
31. Ikeda M, Nemoto S, Yoneda M. 1976. Periodic changes in the content of protein bound sulfhydryl groups and tension at the surface of starfish oocyts in correlation with the meiotic division cycle. Dev Growth Differ 18: 221-225.
32. Jankovics F, Sinka R, Lukacsovich T, Erdelyi M. 2002. MOESIN crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr Biol 12: 2060-2065.
33. Kee YS, Robinson DN. 2008. Motor proteins: Myosin mechanosensors. Curr Biol 18: R860-R862.
34. Kikuchi S, Hata M, Fukumoto K, Yamane Y, Matsui T, Tamura A, Yonemura S, Yamagishi H, Keppler D, Tsukita S. 2002. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat Genet 31: 320-325.
35. Kunda P, Pelling AE, Liu T, Baum B. 2008. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 18: 91-101.
36. Larson SM, Lee HJ, Hung PH, Matthews LM, Robinson DN, Evans JP. 2010. Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and Ezrin-Radixin-Moesin (ERM) proteins. Mol Biol Cell 21: 3182-3192.
37. Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, Maas R, Leder P. 2002. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4: 921-928.
38. Levi M, Maro B, Shalgi R. 2010. The involvement of Fyn kinase in resumption of the first meiotic division in mouse oocytes. Cell Cycle 9: 1577-1589.
39. Longo FJ, Chen DY. 1984. Development of surface polarity in mouse eggs. Scan Electron Microsc 703-716.
40. Longo FJ, Chen DY. 1985. Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus. Dev Biol 107: 382-394.
41. Lucero A, Stack C, Bresnick AR, Shuster CB. 2006. A global, myosin light chain kinase-dependent increase in myosin II contractility accompanies the metaphase-anaphase transition in sea urchin eggs. Mol Biol Cell 17: 4093-4104.
42. Luo J, McGinnis LK, Kinsey WH. 2010. Role of Fyn kinase in oocyte developmental potential. Reprod Fertil Dev 22: 966-976.
43. Ma C, Benink HA, Cheng D, Montplaisir V, Wang L, Xi Y, Zheng PP, Bement WM, Liu XJ. 2006. Cdc42 activation couples spindle positioning to first polar body formation in oocyte maturation. Curr Biol 16: 214-220.
44. Martinac B. 2004. Mechanosensitive ion channels: Molecules of mechanotransduction. J Cell Sci 117: 2449-2460.
45. Matzke R, Jacobson K, Radmacher M. 2001. Direct, high-resolution measurement of furrow stiffening during division of adherent cells. Nat Cell Biol 3: 607-610.
46. Minc N, Burgess DR, Chang F. 2011. Influence of cell geometry on division-plan positioning. Cell 144: 414-426.
47. Mitchison JM, Swann MM. 1954. The mechanical properties of the cell surface: II. The unfertilized sea-urchin egg. J Exp Biol 31: 461-472.
48. Mitchison JM, Swann MM. 1955. The mechanical properties of the cell surface: III. The sea-urchin egg from fertilization to cleavage. J Exp Biol 32: 734-750.
49. Moore SW, Roca-Cusachs P, Sheetz MP. 2010. Stretchy proteins on stretchy substrates: The important elements of integrin-mediated rigidity sensing. Dev Cell 19: 194-206.
50. Na J, Zernicka-Goetz M. 2006. Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr Biol 16: 1249-1254.
51. Nicosia SV, Wolf DP, Inoue M. 1977. Cortical granule distribution and cell surface characteristics in mouse eggs. Dev Biol 57: 56-74.
52. Octtaviani E, Effler JC, Robinson DN. 2006. Enlazin, a natural fusion of two classes of canonical cytoskeletal proteins, contributes to cytokinesis dynamics. Mol Biol Cell 17: 5275-5286.
53. Pasternak C, Elson EL. 1985. Lymphocyte mechanical response triggered by cross-linking surface receptors. J Cell Biol 100: 860-872.
54. Pasternak C, Spudich JA, Elson EL. 1989. Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341: 549-551.
55. Pielak RM, Gaysinskaya VA, Cohen WD. 2004. Formation and function of the polar body contractile ring in Spisula. Dev Biol 269: 421-432.
56. Polesello C, Delon I, Valenti P, Ferrer P, Payre F. 2002. Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat Cell Biol 4: 782-789.
57. Reichl EM, Effler JC, Robinson DN. 2005. The stress and strain of cytokinesis. Trends Cell Biol 15: 200-206.
58. Reichl EM, Ren Y, Morphew MK, Delannoy M, Effler JC, Girard KD, Divi S, Iglesias PA, Kuo SC, Robinson DN. 2008. Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr Biol 18: 471-480.
59. Ren Y, Effler JC, Norstrome M, Luo T, Firtel RA, Iglesias PA, Rock RS, Robinson DN. 2009. Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin. Curr Biol 19: 1421-1428.
60. Rosenblatt J, Cramer LP, Baum B, McGee KM. 2004. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117: 361-372.
61. Sanfins A, Lee GY, Plancha CE, Overstrom EW, Albertini DF. 2003. Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol Reprod 69: 2059-2067.
62. Sanfins A, Plancha CE, Overstrom EW, Albertini DF. 2004. Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: Insights into the relationship between nuclear and cytoplasmic quality. Hum Reprod 19: 2889-2899.
63. Saotome I, Curto M, McClatchey AI. 2004. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell 6: 855-864.
64. Schmerler S, Wessel GM. 2011. Polar bodies - More a lack of understanding than a lack of respect. Mol Reprod Dev 78: 3-8.
65. Selman GG, Waddington CH. 1955. The mechanism of cell division in the cleavage of the newt's egg. J Exp Biol 32: 700-733.
66. Sharan SK, Pyle A, Coppola V, Babus J, Swaminathan S, Bendict J, Swing D, Martin BK, Tessarollo L, Evans JP, Flaws JA, Handel MA. 2004. BRCA2 deficiency in mice leads to meiotic impairment and infertility. Development 131: 131-142.
67. Shôji Y, Hamaguchi MS, Hiramoto Y. 1978. Mechanical properties of the endoplasm in starfish oocytes. Exp Cell Res 117: 79-87.
68. Simerly C, Nowak G, de Lanerolle P, Schatten G. 1998. Differential expression and functions of cortical myosin IIA and IIB isotypes during meiotic maturation, fertilization, and mitosis in mouse oocytes and embryos. Mol Biol Cell 9: 2509-2525.
69. Stewart MP, Helenius J, Toyoda Y, Ramanathan SP, Muller DJ, Hyman AA. 2011. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469: 226-230.
70. Surcel A, Kee YS, Luo T, Robinson DN. 2010. Cytokinesis through biochemical-mechanical feedback loops. Semin Cell Dev Biol 21: 866-873.
71. Swain JE, Pool TB. 2008. ART failure: Oocyte contributions to unsuccessful fertilization. Human Reprod Update 14: 431-446.
72. Ubaldi FM, Rienzi L. 2008. Morphological selection of gametes. Placenta 29: 115-120.
73. Verlhac MH, Lefebvre C, Guillaud P, Rassinier P, Maro B. 2000. Asymmetric division in mouse oocytes: With or without Mos. Curr Biol 10: 1303-1306.
74. Yanagamachi R. 1978. Sperm-egg association in mammals. Curr Top Dev Biol 12: 83-105.
75. Yanagimachi R. 1988. Sperm-egg fusion. Curr Top Membr Transp 32: 3-43.
76. Zhang W, Robinson DN. 2005. Balance of actively generated contractile and resistive forces controls cytokinesis dynamics. Proc Natl Acad Sci USA 102: 7186-7191.
77. Zhang X, Ma C, Miller AL, Katbi HA, Bement WM, Liu XJ. 2008. Polar body emission requries a RhoA contractile ring and Cdc42-mediated membrane protrusion. Dev Cell 15: 386-400.
78. Zhou Q, Kee YS, Poirier CC, Jelinek C, Osborne J, Divi S, Surcel A, Will ME, Eggert US, Muller-Taudenberger A, Iglesias PA, Cotter RJ, Robinson DN. 2010. 14-3-3 coordinates microtubules, Rac, and myosin-II to control cell mechanics and cytokinesis. Curr Biol 20: 1881-1889.