Regulation of asymmetrical cytokinesis by cAMP during meiosis I in mouse oocytes

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Chen, Dawei ^a   Zhang, Yuanwei ^a   Yi, Qiyi ^a   Huang, Yun ^a   Hou, Heli ^a   Zhang, Yingyin ^a,b   Hao, Qiaomei ^a   Cooke, Howard J ^a,b,c   Li, Lei ^d   Sun, Qingyuan ^d   Shi, Qinghua ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; MYOSIN II; PROTEIN ANTIBODY; BUCLADESINE; ISOBUTYLMETHYLXANTHINE; ISOQUINOLINE DERIVATIVE; N (2 (4 BROMOCINNAMYLAMINO)ETHYL) 5 ISOQUINOLINESULFONAMIDE; N-(2-(4-BROMOCINNAMYLAMINO)ETHYL)-5-ISOQUINOLINESULFONAMIDE; SULFONAMIDE;

ANAPHASE; ANIMAL CELL; ARTICLE; ASSYMETRICAL CYTOKINESIS; CELL DIVISION; CHROMOSOME; CONTROLLED STUDY; CYTOKINESIS; DAUGHTER CELL; ENZYME INHIBITION; FEMALE; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; PROTEIN FUNCTION; REGULATORY MECHANISM; ANIMAL; ASYMMETRIC CELL DIVISION; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG EFFECT; INSTITUTE FOR CANCER RESEARCH MOUSE; INTRACELLULAR SPACE; METABOLISM; MICROINJECTION;

MAMMALIA;

1-METHYL-3-ISOBUTYLXANTHINE; ANAPHASE; ANIMALS; ASYMMETRIC CELL DIVISION; BUCLADESINE; CELL MOVEMENT; CELLS, CULTURED; CHROMOSOMES, MAMMALIAN; CYCLIC AMP; CYTOKINESIS; FEMALE; INTRACELLULAR SPACE; ISOQUINOLINES; MEIOSIS; MICE; MICE, INBRED ICR; MICROINJECTIONS; MYOSIN TYPE II; OOCYTES; SULFONAMIDES;

EID: 84855656014     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029735     Document Type: Article

References (73)

1. Carmena A, (2008) Signaling networks during development: the case of asymmetric cell division in the Drosophila nervous system. Dev Biol 321: 1-17.
2. Hawkins ED, Russell SM, (2008) Upsides and downsides to polarity and asymmetric cell division in leukemia. Oncogene 27: 7003-7017.
3. Azoury J, Verlhac MH, Dumont J, (2009) Actin filaments: key players in the control of asymmetric divisions in mouse oocytes. Biol Cell 101: 69-76.
4. Menke FL, Scheres B, (2009) Plant asymmetric cell division, vive la difference! Cell 137: 1189-1192.
5. Siller KH, Doe CQ, (2009) Spindle orientation during asymmetric cell division. Nat Cell Biol 11: 365-374.
6. Morrison SJ, Kimble J, (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441: 1068-1074.
7. Halet G, Carroll J, (2007) Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 12: 309-317.
8. Longo FJ, Chen DY, (1985) Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev Biol 107: 382-394.
9. Maro B, Johnson MH, Webb M, Flach G, (1986) Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J Embryol Exp Morphol 92: 11-32.
10. Wang L, Wang ZB, Zhang X, FitzHarris G, Baltz JM, et al. (2008) Brefeldin A disrupts asymmetric spindle positioning in mouse oocytes. Dev Biol 313: 155-166.
11. Edwards RG, (1965) Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208: 349-351.
12. 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.
13. Fabritius AS, Ellefson ML, McNally FJ, (2010) Nuclear and spindle positioning during oocyte meiosis. Curr Opin Cell Biol.
14. Gonczy P, (2008) Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9: 355-366.
15. Schuh M, Ellenberg J, (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130: 484-498.
16. Kubiak J, Paldi A, Weber M, Maro B, (1991) Genetically identical parthenogenetic mouse embryos produced by inhibition of the first meiotic cleavage with cytochalasin D. Development 111: 763-769.
17. Dumont J, Million K, Sunderland K, Rassinier P, Lim H, et al. (2007) Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 301: 254-265.
18. Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, et al. (2002) Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4: 921-928.
19. 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: 1301-1308.
20. Bezanilla M, Wadsworth P, (2009) Spindle positioning: actin mediates pushing and pulling. Curr Biol 19: R168-169.
21. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, et al. (2008) Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 18: 1514-1519.
22. Wu Q, Sahasrabudhe RM, Luo LZ, Lewis DW, Gollin SM, et al. (2010) Deficiency in myosin light-chain phosphorylation causes cytokinesis failure and multipolarity in cancer cells. Oncogene.
23. Larson SM, Lee HJ, Hung PH, Matthews LM, Robinson DN, et al. (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.
24. Schuh M, Ellenberg J, (2008) A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18: 1986-1992.
25. Johnson MH, Maro B, (1984) The distribution of cytoplasmic actin in mouse 8-cell blastomeres. J Embryol Exp Morphol 82: 97-117.
26. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, et al. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299: 1743-1747.
27. Asano S, Hamao K, Hosoya H, (2009) Direct evidence for roles of phosphorylated regulatory light chain of myosin II in furrow ingression during cytokinesis in HeLa cells. Genes Cells 14: 555-568.
28. Robinson DN, Spudich JA, (2004) Mechanics and regulation of cytokinesis. Curr Opin Cell Biol 16: 182-188.
29. Meijer L, Dostmann W, Genieser HG, Butt E, Jastorff B, (1989) Starfish oocyte maturation: evidence for a cyclic AMP-dependent inhibitory pathway. Dev Biol 133: 58-66.
30. Tsafriri A, Dekel N, (1994) Molecular mechanisms in ovulation. In: Findlay JD, editors. Molecular Biology of the Female Reproductive System San Diego Academic Press Inc pp. 207-258.
31. Tornell J, Brannstrom M, Magnusson C, Billig H, (1990) Effects of follicle stimulating hormone and purines on rat oocyte maturation. Mol Reprod Dev 27: 254-260.
32. Conti M, (2002) Specificity of the cyclic adenosine 3′,5′-monophosphate signal in granulosa cell function. Biol Reprod 67: 1653-1661.
33. Mehlmann LM, (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130: 791-799.
34. Cho WK, Stern S, Biggers JD, (1974) Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 187: 383-386.
35. Dekel N, Lawrence TS, Gilula NB, Beers WH, (1981) Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Dev Biol 86: 356-362.
36. Schultz RM, Montgomery RR, Belanoff JR, (1983) Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 97: 264-273.
37. Vivarelli E, Conti M, De Felici M, Siracusa G, (1983) Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differ 12: 271-276.
38. Bornslaeger EA, Mattei P, Schultz RM, (1986) Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev Biol 114: 453-462.
39. 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.
40. Dekel N, (2005) Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol Cell Endocrinol 234: 19-25.
41. LaRosa C, Downs SM, (2006) Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol Reprod 74: 585-592.
42. Sun QY, Miao YL, Schatten H, (2009) Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8: 2741-2747.
43. Seamon KB, Padgett W, Daly JW, (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc Natl Acad Sci U S A 78: 3363-3367.
44. Chen J, Chi MM, Moley KH, Downs SM, (2009) cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138: 759-770.
45. Urner F, Herrmann WL, Baulieu EE, Schorderet-Slatkine S, (1983) Inhibition of denuded mouse oocyte meiotic maturation by forskolin, an activator of adenylate cyclase. Endocrinology 113: 1170-1172.
46. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, et al. (1990) Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265: 5267-5272.
47. Han D, Cao XY, Wang HL, Li JJ, Wang YB, et al. (2010) Effects of puberty and gonadotropins on the molecular events controlling meiotic resumption of mouse oocytes. Reproduction 139: 959-969.
48. Deng M, Kishikawa H, Yanagimachi R, Kopf GS, Schultz RM, et al. (2003) Chromatin-mediated cortical granule redistribution is responsible for the formation of the cortical granule-free domain in mouse eggs. Dev Biol 257: 166-176.
49. Murthy KS, (2006) Signaling for contraction and relaxation in smooth muscle of the gut. Annu Rev Physiol 68: 345-374.
50. Bosgraaf L, van Haastert PJ, (2006) The regulation of myosin II in Dictyostelium. Eur J Cell Biol 85: 969-979.
51. Yuan W, Lopez Bernal A, (2007) Cyclic AMP signalling pathways in the regulation of uterine relaxation. BMC Pregnancy Childbirth 7 (Suppl 1): S10.
52. Moussavi RS, Kelley CA, Adelstein RS, (1993) Phosphorylation of vertebrate nonmuscle and smooth muscle myosin heavy chains and light chains. Mol Cell Biochem 127-128: 219-227.
53. Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers JR, (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279: 35557-35563.
54. Glotzer M, (2005) The molecular requirements for cytokinesis. Science 307: 1735-1739.
55. McCollum D, (2004) Cytokinesis: the central spindle takes center stage. Curr Biol 14: R953-955.
56. Wang Q, Racowsky C, Deng M, (2011) Mechanism of the chromosome-induced polar body extrusion in mouse eggs. Cell Div 6: 17.
57. Mullins JM, Biesele JJ, (1977) Terminal phase of cytokinesis in D-98s cells. J Cell Biol 73: 672-684.
58. Shi Q, King RW, (2005) Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 437: 1038-1042.
59. D'Avino PP, (2009) How to scaffold the contractile ring for a safe cytokinesis- lessons from Anillin-related proteins. J Cell Sci 122: 1071-1079.
60. 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.
61. Maruoka H, Sasaya H, Shimamura Y, Nakatani Y, Shimoke K, et al. (2010) Dibutyryl-cAMP up-regulates nur77 expression via histone modification during neurite outgrowth in PC12 cells. J Biochem 148: 93-101.
62. Conti M, Beavo J, (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
63. Wang J, Cao WL, Liu XJ, (2006) Protein kinase A(PKA)-restrictive and PKA-permissive phases of oocyte maturation. Cell Cycle 5: 213-217.
64. Feliciello A, Gottesman ME, Avvedimento EV, (2001) The biological functions of A-kinase anchor proteins. J Mol Biol 308: 99-114.
65. Diviani D, Baisamy L, Appert-Collin A, (2006) AKAP-Lbc: a molecular scaffold for the integration of cyclic AMP and Rho transduction pathways. Eur J Cell Biol 85: 603-610.
66. Kirschner LS, Yin Z, Jones GN, Mahoney E, (2009) Mouse models of altered protein kinase A signaling. Endocr Relat Cancer 16: 773-793.
67. Newhall KJ, Criniti AR, Cheah CS, Smith KC, Kafer KE, et al. (2006) Dynamic anchoring of PKA is essential during oocyte maturation. Curr Biol 16: 321-327.
68. Kovo M, Kandli-Cohen M, Ben-Haim M, Galiani D, Carr DW, et al. (2006) An active protein kinase A (PKA) is involved in meiotic arrest of rat growing oocytes. Reproduction 132: 33-43.
69. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, et al. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15: 510-519.
70. Andersson M, Usiello A, Borgkvist A, Pozzi L, Dominguez C, et al. (2005) Cannabinoid action depends on phosphorylation of dopamine- and cAMP-regulated phosphoprotein of 32 kDa at the protein kinase A site in striatal projection neurons. J Neurosci 25: 8432-8438.
71. Yang JX, Lin Y, (2005) The action of PKA on smooth muscle myosin phosphorylation. Life Sci 77: 2669-2675.
72. Garcia JG, Lazar V, Gilbert-McClain LI, Gallagher PJ, Verin AD, (1997) Myosin light chain kinase in endothelium: molecular cloning and regulation. Am J Respir Cell Mol Biol 16: 489-494.
73. Xu B, Hua J, Zhang Y, Jiang X, Zhang H, et al. (2011) Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. PLoS One 6: e16046.