Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

Small GTPases and formins in mammalian oocyte maturation: cytoskeletal organizers

  • Kwon, So-Jung (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Research Center for Transcription Control, Konkuk University) ;
  • Lim, Hyun-Jung J. (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Research Center for Transcription Control, Konkuk University)
  • Received : 2011.02.01
  • Accepted : 2011.02.15
  • Published : 2011.03.02
Download PDF
⟨ Previous Next ⟩

Abstract

The maturation process of mammalian oocytes accompanies an extensive rearrangement of the cytoskeleton and associated proteins. As this process requires a delicate interplay between the cytoskeleton and its regulators, it is often targeted by various external and internal adversaries that affect the congression and/or segregation of chromosomes. Asymmetric cell division in oocytes also requires specific regulators of the cytoskeleton, including formin-2 and small GTPases. Recent literature providing clues regarding how actin filaments and microtubules interact during spindle migration in mouse oocytes are highlighted in this review.

Keywords

References

  1. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005;130:801-11. https://doi.org/10.1530/rep.1.00364
  2. Compton DA. Spindle assembly in animal cells. Annu Rev Biochem 2000;69:95-114. https://doi.org/10.1146/annurev.biochem.69.1.95
  3. Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 2007;130:484-98. https://doi.org/10.1016/j.cell.2007.06.025
  4. Carabatsos MJ, Combelles CM, Messinger SM, Albertini DF. Sorting and reorganization of centrosomes during oocyte maturation in the mouse. Microsc Res Tech 2000;49:435-44. https://doi.org/10.1002/(SICI)1097-0029(20000601)49:5<435::AID-JEMT5>3.0.CO;2-H
  5. Gueth-Hallonet C, Antony C, Aghion J, Santa-Maria A, Lajoie-Mazenc I, Wright M, et al. Gamma-tubulin is present in acentriolar MTOCs during early mouse development. J Cell Sci 1993;105: 157-66.
  6. Brunet S, Maria AS, Guillaud P, Dujardin D, Kubiak JZ, Maro B. Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 1999;146:1-12. https://doi.org/10.1083/jcb.146.3.1
  7. Lenart P, Bacher CP, Daigle N, Hand AR, Eils R, Terasaki M, et al. A contractile nuclear actin network drives chromosome congression in oocytes. Nature 2005;436:812-8. https://doi.org/10.1038/nature03810
  8. Verlhac MH, Dumont J. Interactions between chromosomes, microfilaments and microtubules revealed by the study of small GTPases in a big cell, the vertebrate oocyte. Mol Cell Endocrinol 2008;282:12-7. https://doi.org/10.1016/j.mce.2007.11.018
  9. Van Aelst L, D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev 1997;11:2295-322. https://doi.org/10.1101/gad.11.18.2295
  10. Bielak-Zmijewska A, Kolano A, Szczepanska K, Maleszewski M, Borsuk E. Cdc42 protein acts upstream of IQGAP1 and regulates cytokinesis in mouse oocytes and embryos. Dev Biol 2008;322: 21-32. https://doi.org/10.1016/j.ydbio.2008.06.039
  11. Na J, Zernicka-Goetz M. Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr Biol 2006;16:1249-54. https://doi.org/10.1016/j.cub.2006.05.023
  12. Cui XS, Li XY, Kim NH. Cdc42 is implicated in polarity during meiotic resumption and blastocyst formation in the mouse. Mol Reprod Dev 2007;74:785-94. https://doi.org/10.1002/mrd.20571
  13. Halet G, Carroll J. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 2007;12:309-17. https://doi.org/10.1016/j.devcel.2006.12.010
  14. Deng M, Suraneni P, Schultz RM, Li R. The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes. Dev Cell 2007;12:301-8. https://doi.org/10.1016/j.devcel.2006.11.008
  15. Dumont J, Petri S, Pellegrin F, Terret ME, Bohnsack MT, Rassinier P, et al. A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 2007;176: 295-305. https://doi.org/10.1083/jcb.200605199
  16. Chesarone MA, DuPage AG, Goode BL. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rev Mol Cell Biol 2010;11:62-74. https://doi.org/10.1038/nrm2816
  17. Faix J, Grosse R. Staying in shape with formins. Dev Cell 2006;10: 693-706. https://doi.org/10.1016/j.devcel.2006.05.001
  18. Manseau L, Calley J, Phan H. Profilin is required for posterior patterning of the Drosophila oocyte. Development 1996;122:2109-16
  19. Kwon S, Shin H, Lim HJ. Dynamic interaction of formin proteins and cytoskeleton in mouse oocytes during meiotic maturation. Mol Hum Reprod 2010 Oct 22 [Epub]. DOI: 10.1093/molehr/gaq088.
  20. Wood JR, Dumesic DA, Abbott DH, Strauss JF 3rd. Molecular abnormalities in oocytes from women with polycystic ovary syndrome revealed by microarray analysis. J Clin Endocrinol Metab 2007;92:705-13. https://doi.org/10.1210/jc.2006-2123
  21. Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, et al. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 2002;4:921-8. https://doi.org/10.1038/ncb880
  22. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, Verlhac MH. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 2008;18:1514-9. https://doi.org/10.1016/j.cub.2008.08.044
  23. Burkel BM, von Dassow G, Bement WM. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil Cytoskeleton 2007;64:822-32. https://doi.org/10.1002/cm.20226
  24. Schuh M, Ellenberg J. A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 2008;18:1986-92. https://doi.org/10.1016/j.cub.2008.11.022
  25. Li H, Guo F, Rubinstein B, Li R. Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nat Cell Biol 2008;10:1301-8. https://doi.org/10.1038/ncb1788
  26. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, et al. Lifeact: a versatile marker to visualize F-actin. Nat Methods 2008;5:605-7. https://doi.org/10.1038/nmeth.1220
  27. Lammers M, Rose R, Scrima A, Wittinghofer A. The regulation of mDia1 by autoinhibition and its release by Rho . GTP. EMBO J 2005; 24:4176-87. https://doi.org/10.1038/sj.emboj.7600879
  28. Kato T, Watanabe N, Morishima Y, Fujita A, Ishizaki T, Narumiya S. Localization of a mammalian homolog of diaphanous, mDia1, to the mitotic spindle in HeLa cells. J Cell Sci 2001;114:775-84.
  29. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 2008;181:523- 36. https://doi.org/10.1083/jcb.200709029
  30. Lammers M, Meyer S, Kuhlmann D, Wittinghofer A. Specificity of interactions between mDia isoforms and Rho proteins. J Biol Chem 2008;283:35236-46. https://doi.org/10.1074/jbc.M805634200
  31. Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad? Trends Genet 2008;24:86-93. https://doi.org/10.1016/j.tig.2007.11.010
  32. Hassold T, Hunt P. Maternal age and chromosomally abnormal pregnancies: what we know and what we wish we knew. Curr Opin Pediatr 2009;21:703-8. https://doi.org/10.1097/MOP.0b013e328332c6ab
  33. Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod 2008;23:1118-27. https://doi.org/10.1093/humrep/den048
  34. Hamel M, Dufort I, Robert C, Leveille MC, Leader A, Sirard MA. Genomic assessment of follicular marker genes as pregnancy predictors for human IVF. Mol Hum Reprod 2010;16:87-96. https://doi.org/10.1093/molehr/gap079
  35. Bione S, Sala C, Manzini C, Arrigo G, Zuffardi O, Banfi S, et al. A human homologue of the Drosophila melanogaster diaphanous gene is disrupted in a patient with premature ovarian failure: evidence for conserved function in oogenesis and implications for human sterility. Am J Hum Genet 1998;62:533-41. https://doi.org/10.1086/301761
  36. Lynch ED, Lee MK, Morrow JE, Welcsh PL, León PE, King MC. Nonsyndromic deafness DFNA1 associated with mutation of a human homolog of the Drosophila gene diaphanous. Science 1997;278: 1315-8. https://doi.org/10.1126/science.278.5341.1315

Cited by

  1. Blastocyst biopsy and vitrification are effective for preimplantation genetic diagnosis of monogenic diseases vol.28, pp.5, 2011, https://doi.org/10.1093/humrep/det048
  2. The Formin Protein mDia2 Serves as a Marker of Spindle Pole Dynamics in Vitrified-Warmed Mouse Oocytes vol.8, pp.9, 2011, https://doi.org/10.1371/journal.pone.0075729
  3. The Transcription Factor Egr3 Is a Putative Component of the Microtubule Organizing Center in Mouse Oocytes vol.9, pp.4, 2011, https://doi.org/10.1371/journal.pone.0094708
  4. Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida vol.23, pp.1, 2011, https://doi.org/10.1017/s0967199413000403
  5. The small GTPase RhoA regulates the LIMK1/2‐cofilin pathway to modulate cytoskeletal dynamics in oocyte meiosis vol.233, pp.8, 2018, https://doi.org/10.1002/jcp.26450