Recent insights into spindle function in mammalian oocytes and early embryos

Biology of Reproduction

Volumn 89, Issue 3, 2013, Pages

  Howe, Katie ^a   FitzHarris, Greg ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Aneuploidy; Chromosome segregation; Embryo; Meiosis; Spindle

Indexed keywords

AURORA B KINASE; COHESIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE; KINESIN 5; RAN PROTEIN;

ANAPHASE; ANEUPLOIDY; CAENORHABDITIS ELEGANS; CELL CYCLE REGULATION; CELL MEMBRANE; CENTROMERE; CENTROSOME; CHROMOSOME; CHROMOSOME ARM; CHROMOSOME SEGREGATION; DAUGHTER CELL; EMBRYO DEVELOPMENT; FIRST TRIMESTER PREGNANCY; GENE SILENCING; HUMAN; LUTEINIZING HORMONE RELEASE; M PHASE CELL CYCLE CHECKPOINT; MAMMAL CELL; METAPHASE; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MITOSIS; MITOSIS SPINDLE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVULATION; POLAR BODY; PRIORITY JOURNAL; REVIEW; SISTER CHROMATID; SOMATIC CELL; XENOPUS LAEVIS;

ANEUPLOIDY; CHROMOSOME SEGREGATION; EMBRYO; MEIOSIS; SPINDLE;

ANIMALS; CHROMOSOME SEGREGATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GESTATIONAL AGE; HUMANS; MICE; OOCYTES; PREGNANCY; SPINDLE APPARATUS;

EID: 84889580170     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.112151     Document Type: Review

References (115)

1. Ganem NJ, Storchova Z, Pellman D. Tetraploidy, aneuploidy and cancer. Curr Opin Genet Dev 2007; 17:157-162.
2. Weaver BA, Cleveland DW. Does aneuploidy cause cancer? Curr Opin Cell Biol 2006; 18:658-667.
3. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001; 2:280-291.
4. Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 2012; 13:493-504.
5. Navara CS, Wu GJ, Simerly C, Schatten G. Mammalian model systems for exploring cytoskeletal dynamics during fertilization. Curr Top Dev Biol 1995; 31:321-342.
6. Simerly C, Zoran SS, Payne C, Dominko T, Sutovsky P, Navara CS, Salisbury JL, Schatten G. Biparental inheritance of gamma-tubulin during human fertilization: molecular reconstitution of functional zygotic centrosomes in inseminated human oocytes and in cell-free extracts nucleated by human sperm. Mol Biol Cell 1999; 10:2955-2969.
7. Simerly C, Wu GJ, Zoran S, Ord T, Rawlins R, Jones J, Navara C, Gerrity M, Rinehart J, Binor Z, Asch R, Schatten G. The paternal inheritance of the centrosome, the cell"s microtubule-organizing center, in humans, and the implications for infertility. Nat Med 1995; 1:47-52.
8. Albertini DF. Regulation of meiotic maturation in the mammalian oocyte: interplay between exogenous cues and the microtubule cytoskeleton. Bioessays 1992; 14:97-103.
9. Albertini DF. Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res 1992; 296:57-68.
10. Mitchison T, Kirschner M. Dynamic instability of microtubule growth. Nature 1984; 312:237-242.
11. Santaguida S, Musacchio A. The life and miracles of kinetochores. EMBO J 2009; 28:2511-2531.
12. Maiato H, DeLuca J, Salmon ED, Earnshaw WC. The dynamic kinetochore-microtubule interface. J Cell Sci 2004; 117:5461-5477.
13. Hayden JH, Bowser SS, Rieder CL. Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells. J Cell Biol 1990; 111: 1039-1045.
14. Maiato H, Lince-Faria M. The perpetual movements of anaphase. Cell Mol Life Sci 2010; 67:2251-2269.
15. Compton DA. Spindle assembly in animal cells. Annu Rev Biochem 2000; 69:95-114.
16. Walczak CE, Cai S, Khodjakov A. Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 2010; 11:91-102.
17. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8:379-393.
18. Holt JE, Jones KT. Control of homologous chromosome division in the mammalian oocyte. Mol Hum Reprod 2009; 15:139-147.
19. Homer H. The APC/C in female mammalian meiosis I. Reproduction 2013; 146(2):R61-R71.
20. Chaigne A, Verlhac MH, Terret ME. Spindle positioning in mammalian oocytes. Exp Cell Res 2012; 318:1442-1447.
21. Schatten G. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 1994; 165:299-335.
22. Delattre M, Gonczy P. The arithmetic of centrosome biogenesis. J Cell Sci 2004; 117:1619-1630.
23. Dumont J, Desai A. Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends Cell Biol 2012; 22:241-249.
24. Liu XJ. Polar body emission. Cytoskeleton (Hoboken) 2012; 69: 670-685.
25. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 1996; 382:420-425.
26. Huchon D, Crozet N, Cantenot N, Ozon R. Germinal vesicle breakdown in the Xenopus laevis oocyte: description of a transient microtubular structure. Reprod Nutr Dev 1981; 21:135-148.
27. Szollosi D, Calarco P, Donahue RP. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci 1972; 11:521-541.
28. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005; 130:801-811.
29. Combelles CM, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol 2001; 239:281-294.
30. Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 2007; 130:484-498.
31. Kitajima TS, Ohsugi M, Ellenberg J. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 2011; 146:568-581.
32. Dumont J, Petri S, Pellegrin F, Terret ME, Bohnsack MT, Rassinier P, Georget V, Kalab P, Gruss OJ, Verlhac MH. A centriole- and RanGTPindependent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 2007; 176:295-305.
33. Breuer M, Kolano A, Kwon M, Li CC, Tsai TF, Pellman D, Brunet S, Verlhac MH. HURP permits MTOC sorting for robust meiotic spindle bipolarity, similar to extra centrosome clustering in cancer cells. J Cell Biol 2010; 191:1251-1260.
34. Rusan NM, Tulu US, Fagerstrom C, Wadsworth P. Reorganization of the microtubule array in prophase/prometaphase requires cytoplasmic dynein-dependent microtubule transport. J Cell Biol 2002; 158: 997-1003.
35. Fitzharris G, Marangos P, Carroll J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol 2007; 305(1):133-144.
36. Dalton CM, Carroll J. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci 2013; 126: 2955-2964.
37. Clarke PR, Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol 2008; 9:464-477.
38. Gruss OJ, Vernos I. The mechanism of spindle assembly: functions of Ran and its target TPX2. J Cell Biol 2004; 166:949-955.
39. Brunet S, Dumont J, Lee KW, Kinoshita K, Hikal P, Gruss OJ, Maro B, Verlhac MH. Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS One 2008; 3:e3338.
40. Kolano A, Brunet S, Silk AD, Cleveland DW, Verlhac MH. Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc Natl Acad Sci U S A 2012; 109:E1858-E1867.
41. Brunet S, Polanski Z, Verlhac MH, Kubiak JZ, Maro B. Bipolar meiotic spindle formation without chromatin. Curr Biol 1998; 8:1231-1234.
42. Terret ME, Lefebvre C, Djiane A, Rassinier P, Moreau J, Maro B, Verlhac MH. DOC1R: a MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development 2003; 130: 5169-5177.
43. Lefebvre C, Terret ME, Djiane A, Rassinier P, Maro B, Verlhac MH. Meiotic spindle stability depends on MAPK-interacting and spindlestabilizing protein (MISS), a new MAPK substrate. J Cell Biol 2002; 157:603-613.
44. 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.
45. Gui L, Homer H. Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 2012; 139: 1941-1946.
46. Gui L, Homer H. Hec1-dependent cyclin B2 stabilization regulates the G2-M transition and early prometaphase in mouse oocytes. Dev Cell 2013; 25:43-54.
47. Sun SC, Lee SE, Xu YN, Kim NH. Perturbation of Spc25 expression affects meiotic spindle organization, chromosome alignment and spindle assembly checkpoint in mouse oocytes. Cell Cycle 2010; 9:4552-4559.
48. Sun SC, Zhang DX, Lee SE, Xu YN, Kim NH. Ndc80 regulates meiotic spindle organization, chromosome alignment, and cell cycle progression in mouse oocytes. Microsc Microanal 2011; 17:431-439.
49. Joglekar AP, Bloom KS, Salmon ED. Mechanisms of force generation by end-on kinetochore-microtubule attachments. Curr Opin Cell Biol 2010; 22:57-67.
50. Dumont S, Mitchison TJ. Force and length in the mitotic spindle. Curr Biol 2009; 19:R749-R761.
51. Wuhr M, Chen Y, Dumont S, Groen AC, Needleman DJ, Salic A, Mitchison TJ. Evidence for an upper limit to mitotic spindle length. Curr Biol 2008; 18:1256-1261.
52. Goshima G, Scholey JM. Control of mitotic spindle length. Annu Rev Cell Dev Biol 2010; 26:21-57.
53. Choi SH, McCollum D. A role for metaphase spindle elongation forces in correction of merotelic kinetochore attachments. Curr Biol 2012; 22: 225-230.
54. Kashina AS, Baskin RJ, Cole DG, Wedaman KP, Saxton WM, Scholey JM. A bipolar kinesin. Nature 1996; 379:270-272.
55. van den Wildenberg SM, Tao L, Kapitein LC, Schmidt CF, Scholey JM, Peterman EJ. The homotetrameric kinesin-5 KLP61F preferentially crosslinks microtubules into antiparallel orientations. Curr Biol 2008; 18: 1860-1864.
56. Kapitein LC, Peterman EJ, Kwok BH, Kim JH, Kapoor TM, Schmidt CF. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 2005; 435:114-118.
57. Blangy A, Lane HA, d'Hérin P, Harper M, Kress M, Nigg EA. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 1995; 83:1159-1169.
58. Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ. Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 2000; 150:975-988.
59. Cameron LA, Yang G, Cimini D, Canman JC, Kisurina-Evgenieva O, Khodjakov A, Danuser G, Salmon ED. Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J Cell Biol 2006; 173: 173-179.
60. Duncan FE, Chiang T, Schultz RM, Lampson MA. Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol Reprod 2009; 81:768-776.
61. Fitzharris G. A shift from kinesin 5-dependent metaphase spindle function during preimplantation development in mouse. Development 2009; 136:2111-2119.
62. Illingworth C, Pirmadjid N, Serhal P, Howe K, Fitzharris G. MCAK regulates chromosome alignment but is not necessary for preventing aneuploidy in mouse oocyte meiosis I. Development 2010; 137: 2133-2138.
63. Mailhes JB, Mastromatteo C, Fuseler JW. Transient exposure to the Eg5 kinesin inhibitor monastrol leads to syntelic orientation of chromosomes and aneuploidy in mouse oocytes. Mutat Res 2004; 559:153-167.
64. Rogers GC, Rogers SL, Sharp DJ. Spindle microtubules in flux. J Cell Sci 2005; 118:1105-1116.
65. Miyamoto DT, Perlman ZE, Burbank KS, Groen AC, Mitchison TJ. The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J Cell Biol 2004; 167:813-818.
66. Shirasu-Hiza M, Perlman ZE, Wittmann T, Karsenti E, Mitchison TJ. Eg5 causes elongation of meiotic spindles when flux-associated microtubule depolymerization is blocked. Curr Biol 2004; 14: 1941-1945.
67. Gaetz J, Kapoor TM. Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J Cell Biol 2004; 166:465-471.
68. Burbank KS, Mitchison TJ, Fisher DS. Slide-and-cluster models for spindle assembly. Curr Biol 2007; 17:1373-1383.
69. Yang G, Cameron LA, Maddox PS, Salmon ED, Danuser G. Regional variation of microtubule flux reveals microtubule organization in the metaphase meiotic spindle. J Cell Biol 2008; 182(4):631-639.
70. Thompson SL, Compton DA. Chromosome missegregation in human cells arises through specific types of kinetochore-microtubule attachment errors. Proc Natl Acad Sci U S A 2011; 108:17974-17978.
71. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 2001; 153:517-527.
72. Salmon ED, Cimini D, Cameron LA, DeLuca JG. Merotelic kinetochores in mammalian tissue cells. Philos Trans R Soc Lond B Biol Sci 2005; 360:553-568.
73. Liu D, Lampson MA. Regulation of kinetochore-microtubule attachments by Aurora B kinase. Biochem Soc Trans 2009; 37:976-980.
74. LaFountain JR, Jr., Oldenbourg R. Maloriented bivalents have metaphase positions at the spindle equator with more kinetochore microtubules to one pole than to the other. Mol Biol Cell 2004; 15:5346-5355.
75. Yang KT, Li SK, Chang CC, Tang CJ, Lin YN, Lee SC, Tang TK. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 2010; 21: 2371-2383.
76. Homer HA, McDougall A, Levasseur M, Yallop K, Murdoch AP, Herbert M. Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 2005; 19:202-207.
77. Lane SI, Chang HY, Jennings PC, Jones KT. The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint. Reproduction 2010; 140:521-530.
78. Merriman JA, Lane SI, Holt JE, Jennings PC, Garcia-Higuera I, Moreno S, McLaughlin EA, Jones KT. Reduced chromosome cohesion measured by interkinetochore distance is associated with aneuploidy even in oocytes from young mice. Biol Reprod 2013; 88:31.
79. Schindler K, Davydenko O, Fram B, Lampson MA, Schultz RM. Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development. Proc Natl Acad Sci U S A 2012; 109:E2215-E2222.
80. Vogt E, Kipp A, Eichenlaub-Ritter U. Aurora kinase B, epigenetic state of centromeric heterochromatin and chiasma resolution in oocytes. Reprod Biomed Online 2009; 19:352-368.
81. Swain JE, Ding J, Wu J, Smith GD. Regulation of spindle and chromatin dynamics during early and late stages of oocyte maturation by aurora kinases. Mol Hum Reprod 2008; 14:291-299.
82. Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ. Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 2009; 76:1094-1105.
83. Nagaoka SI, Hodges CA, Albertini DF, Hunt PA. Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 2011; 21:651-657.
84. Lane SI, Yun Y, Jones KT. Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 2012; 139:1947-1955.
85. McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabe AM, Helmhart W, Kudo NR, Wuensche A, Taylor S, Hoog C, Novak B, Nasmyth K. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol 2009; 19:369-380.
86. Ma W, Baumann C, Viveiros MM. NEDD1 is crucial for meiotic spindle stability and accurate chromosome segregation in mammalian oocytes. Dev Biol 2010; 339:439-450.
87. Dumont J, Oegema K, Desai A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 2010; 12:894-901.
88. Fitzharris G. Anaphase B precedes anaphase A in the mouse egg. Curr Biol 2012; 22(5):437-444.
89. Pan H, Ma P, Zhu W, Schultz RM. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol 2008; 316:397-407.
90. Merriman JA, Jennings PC, McLaughlin EA, Jones KT. Effect of aging on superovulation efficiency, aneuploidy rates, and sister chromatid cohesion in mice aged up to 15 months. Biol Reprod 2012; 86(2):49.
91. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA. Evidence that weakened centromere cohesion is a leading cause of agerelated aneuploidy in oocytes. Curr Biol 2010; 20:1522-1528.
92. Nasmyth K, Haering CH. Cohesin: its roles and mechanisms. Annu Rev Genet 2009; 43:525-558.
93. Revenkova E, Jessberger R. Keeping sister chromatids together: cohesins in meiosis. Reproduction 2005; 130:783-790.
94. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, et al. Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 2010; 20: 1511-1521.
95. Chiang T, Schultz RM, Lampson MA. Age-dependent susceptibility of chromosome cohesion to premature separase activation in mouse oocytes. Biol Reprod 2011; 85:1279-1283.
96. Duncan FE, Hornick JE, Lampson MA, Schultz RM, Shea LD, Woodruff TK. Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell 2012; 11:1121-1124.
97. Liu L, Keefe DL. Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod Biomed Online 2008; 16: 103-112.
98. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R. Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 2004; 6:555-562.
99. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA. SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 2005; 37: 1351-1355.
100. Revenkova E, Herrmann K, Adelfalk C, Jessberger R. Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 2010; 20:1529-1533.
101. Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, Nasmyth K. Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 2010; 24:2505-2516.
102. Fragouli E, Wells D. Aneuploidy in the human blastocyst. Cytogenet Genome Res 2011; 133:149-159.
103. Coonen E, Harper JC, Ramaekers FC, Delhanty JD, Hopman AH, Geraedts JP, Handyside AH. Presence of chromosomal mosaicism in abnormal preimplantation embryos detected by fluorescence in situ hybridisation. Hum Genet 1994; 94:609-615.
104. Courtois A, Schuh M, Ellenberg J, Hiiragi T. The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J Cell Biol 2012; 198:357-370.
105. Yamagata K, Fitzharris G. 4D imaging reveals a shift in chromosome segregation dynamics during mouse pre-implantation development. Cell Cycle 2013; 12:157-165.
106. Sikora-Polaczek M, Hupalowska A, Polanski Z, Kubiak JZ, Ciemerych MA. The first mitosis of the mouse embryo is prolonged by transitional metaphase arrest. Biol Reprod 2006; 74:734-743.
107. Kubiak JZ, Chesnel F, Richard-Parpaillon L, Bazile F, Pascal A, Polanski Z, Sikora-Polaczek M, Maciejewska Z, Ciemerych MA. Temporal regulation of the first mitosis in Xenopus and mouse embryos. Mol Cell Endocrinol 2008; 282:63-69.
108. Yamagata K, Suetsugu R, Wakayama T. Assessment of chromosomal integrity using a novel live-cell imaging technique in mouse embryos produced by intracytoplasmic sperm injection. Hum Reprod 2009; 24: 2490-2499.
109. Manandhar G, Simerly C, Schatten G. Centrosome reduction during mammalian spermiogenesis. Curr Top Dev Biol 2000; 49:343-363.
110. Manandhar G, Schatten H, Sutovsky P. Centrosome reduction during gametogenesis and its significance. Biol Reprod 2005; 72:2-13.
111. Gueth-Hallonet C, Antony C, Aghion J, Santa-Maria A, Lajoie-Mazenc I, Wright M. Maro B. gamma-Tubulin is present in acentriolar MTOCs during early mouse development. J Cell Sci 1993; 105(Pt 1):157-166.
112. Abumuslimov SS, Nadezhdina ES, Chentsov I. [An electron microscopic study of centriole and centrosome morphogenesis in the early development of the mouse]. Tsitologiia 1994; 36:1054-1061.
113. Howe K, Fitzharris G. A non-canonical mode of microtubule organization operates throughout pre-implantation development in mouse. Cell Cycle 2013; 12:1616-1624.
114. Palacios MJ, Joshi HC, Simerly C, Schatten G. Gamma-tubulin reorganization during mouse fertilization and early development. J Cell Sci 1993; 104(Pt 2):383-389.
115. Chiang T, Schultz RM, Lampson M. Meiotic origins of maternal agerelated aneuploidy. Biol Reprod 2012; 86(1):1-7.