L-Carnitine supplementation during vitrification of mouse germinal vesicle stage-oocytes and their subsequent in vitro maturation improves meiotic spindle configuration and mitochondrial distribution in metaphase II oocytes

Human Reproduction

Volumn 29, Issue 10, 2014, Pages 2256-2268

  Moawad, Adel R ^a,b,c   Xu, Baozeng ^a,b   Tan, Seang Lin ^a,b   Taketo, Teruko ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b University Health Centre   (Canada)

^c Cairo University   (Egypt)

Author keywords

IVM; L carnitine; Mitochondria; Oocyte; Vitrification

Indexed keywords

CARNITINE; ADENOSINE TRIPHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GERMINAL VESICLE; IN VITRO OOCYTE MATURATION; MEIOTIC SPINDLE; METAPHASE; METAPHASE CHROMOSOME; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OOCYTE MATURATION; SUPPLEMENTATION; VITRIFICATION; WARMING; ANIMAL; CULTURE TECHNIQUE; DBA MOUSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; OOCYTE; SPINDLE APPARATUS; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARNITINE; CELL CULTURE TECHNIQUES; FEMALE; IN VITRO OOCYTE MATURATION TECHNIQUES; MALE; METAPHASE; MICE; MICE, INBRED DBA; MITOCHONDRIA; OOCYTES; SPINDLE APPARATUS; VITRIFICATION;

EID: 84929458070     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu201     Document Type: Article

References (105)

1. Abdelhafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapidfreezingofhuman embryos:asystematic review and meta-analysis. Reprod Biomed Online 2010;20:209-222.
2. Abdelrazik H, Sharma R, Mahfouz R, Agarwal A. L-carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil Steril 2009;91:589-596.
3. Agca Y, Liu J, Peter AT, Critser ES, Critser JK. Effect of developmental stage on bovine oocyte plasma membrane water and cryoprotectant permeability characteristics. Mol Reprod Dev 1998;49:408-415.
4. Aono N, Naganuma T, Abe H, Hara K, Sasada H, Sato E, Yoshida H. Successful production of blastocysts following ultrarapid vitrification with step-wise equilibration of germinal vesicle-stage mouse oocytes. J Reprod Dev 2003;49:501-506.
5. Aono N, Abe H, Hara K, Sasada H, Sato E, Yoshida H. Production of live offspring from mouse germinal vesicle-stage oocytes vitrified by modified stepwise method, SWEID. Fertil Steril 2005;84:1078-1082.
6. Apparicio M, Ruggeri E, Luvoni GC. Vitrification of immature feline oocytes with a commercial kit for bovine embryo vitrification. Reprod Dom Anim 2013;48:240-244.
7. Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 1996;11:2217-2222.
8. Bavister B, Squirrell JM. Mitochondrial distribution and function in oocytes and early embryos. Hum Reprod 2000;15:189-198.
9. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 2007;22:1506-1512.
10. Cha SK, Kim BY, Kim MK, Lee WS, Yoon TK, Lee DR. Effects of various combinations of cryoprotectants and cooling speed on the survival and further development of mouse oocytes after vitrification. Clin Exp Reprod Med 2011;38:24-30.
11. Chang CC, Elliott TA, Wright G, Shapiro DB, Toledo AA, Nagy ZP. Prospective controlled study to evaluate laboratory and clinical outcomes of oocytes vitrification obtained in in vitro fertilization patients aged 30-39 years. Fertil Steril 2013;99:1891-1897.
12. Chankitisakul V, Somfai T, Inaba Y, Techakumphu M, Nagai T. Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology 2013;79:590-598.
13. Chen C. Pregnancy after human oocyte cryopreservation. Lancet 1986;1:884-886.
14. Chen SU, Lien YR, Chao KH, Ho HN, Yang YS, Lee TY. Effects of cryopreservation on meiotic spindles of oocytes and its dynamics after thawing: clinical implications in oocyte freezing-a review article. Mol Cell Endocrinol 2003;202:101-107.
15. Chen C, Han S, Liu W, Wang Y, Huang G. Effect of vitrification on mitochondrial membrane potential in human metaphase II oocytes. J Assist Reprod Genet 2012;29:1045-1050.
16. Chian RC, Gulekli B, Buckett WM, Tan SL. Priming with human chorionic gonadotropin before retrieval of immature oocytes in women with infertility due to the polycystic ovary syndrome. N Engl J Med 1999;341:1624-1626.
17. Chian RC, Gilbert L, Huang JYJ, Demirtas E, Holzer H, Benjamin A, Buckett WM, Tulandi T, Tan SL. Live birth after vitrification of in vitro matured human oocytes. Fertil Steril 2009;91:372-376.
18. Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril 2011;96:277-285.
19. Cobo A, Pérez S, Delos Santos MJ, Zulategui J, Domingo J, RemohíJ. Effect of different cryopreservation protocolson the metaphaseII spindleinhuman oocytes. Reprod Biomed Online 2008;17:350-359.
20. Cobo A, Remohi J, Chang CC, Nagy ZP. Oocyte cryopreservation for donor egg banking. Reprod Biomed Online 2011;23:341-346.
21. Cooper A, Paynter SJ, Fuller BJ, Shaw RW. Differential effects of cryopreservation on nuclear maturation or cytoplasmic maturation in vitro in immature mouse oocytes from stimulated ovaries. Hum Reprod 1998;13:971-978.
22. Dalton CM, Carroll J. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci 2013;126:2955-2964.
23. Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. β-oxidationis essential for mouse oocyte developmental competence and early embryo development. Biol Reprod 2010;83:909-918.
24. Dunning KR, Akison LK, Russell DL, Norman RJ, Robker RL. Increased β-oxidation oxidation and improved oocyte developmental competence in response to L-carnitine during ovarian in vitro follicle development in mice. Biol Reprod 2011;85:548-555.
25. Eroglu A, Toner M, Leykin L, Toth L. Cytoskeleton and polyploidy after maturation and fertilization of cryopreserved germinal vesicle-stage mouse oocytes. J Assist Reprod Genet 1998;15:447-454.
26. Frydman N, Selva J, Bergere M, Auroux M, Maro B. Cryopreserved immature mouse oocytes: a chromosomal and spindle study. J Assist Reprod Genet 1997;14:617-623.
27. Ghetler Y, Skutelsky E, Ben Nun I, Ben Dor L, Amihai D, Shalgi R. Human oocyte cryopreservation and the fate of cortical granules. Fertil Steril 2006;86:210-216.
28. Gomes CM, Silva CA, Acevedo N, Baracat N, Baracat E, Serafini P, Smith GD. Influence of vitrification on mouse metaphase II oocyte spindle dynamics and chromatin alignment. Fertil Steril 2008;90:1396-1404.
29. Heggeness MH, Simon M, Singer SI. Association of mitochondria with microtubules in cultured cells. Proc Natl Acad Sci USA 1978;75:3863-3866.
30. Huang JYJ, Buckett WM, Gilbert L, Tan SL, Chian RC. Retrieval of immature oocytes followed by in vitro maturation and vitrification: a case reporton a new strategy of fertility preservation in women with borderline ovarian malignancy. Gynecol Oncol 2007;105:542-544.
31. Huang JY, Chen HY, Park J, Tan SL, Chian RC. Comparison of spindle and chromosome configuration in in vitro- and in vivo-matured mouse oocytes after vitrification. Fertil Steril 2008;90:1424-1432.
32. Huang JY, Chian RC, Gilbert L, Fleiszer D, Holzer H, Dermitas E, Elizur SE, Gidoni Y, Levin D, Son WY et al. Retrieval of immature oocytes from unstimulated ovaries followed by in vitro maturation and vitrification: a novel strategy of fertility preservation for breast cancer patient. Am J Surg 2010;200:177-183.
33. Isachenko EF, Nayudu PL. Vitrification of mouse germinal vesicle oocytes: effect of treatment temperature and egg yolk on chromatin and spindle normality and cumulus integrity. Hum Reprod 1999;14:400-408.
34. Isachenko V, Soler C, Isachenko E, Perez-Sanchez F, Grishchenko V. Vitrification of immature porcine oocytes: effects of lipid droplets, temperature, cytoskeleton and addition and removal of cryoprotectants. Cryobiology 1998;36:250-253.
35. Isachenko V, Montag M, Isachenko E, Dessole S, Nawroth F, van der Ven H. Aseptic vitrification of human germinal vesicle oocytes using dimethyl sulphoxide as a cryoprotectant. Fertil Steril 2006;85:741-747.
36. Johnson MH, Pickering SJ, George MA. The influence of cooling on the properties of the zona pellucida of the mouse oocyte. Hum Reprod 1988;3:383-387.
37. Jones A, Van Blerkom J, Davis P, Toledo AT. Cryopreservation ofmetaphase II human oocytes effects mitochondrial membrane potential: implications for developmental competence. Hum Reprod 2004;19:1861-1866.
38. Keefe D, Liu L, Wang W, Silva C. Imaging meiotic spindlesbypolarization light microscopy: principles and applications to IVF. Reprod Biomed Online 2003;7:24-29.
39. Kharche SD, Sharma GT, Majumdar AC. In vitro maturation and fertilization of goat oocytes vitrified at the germinal vesicle stage. Small Rum Res 2005;57:81-84.
40. Kim DH, Park HS, Kim SW, Hwang IS, Yang BC, Im GS, Chung HJ, Seong HW, Moon SJ, Yang BS. Vitrification of immature bovine oocytes by microdrop method. J Reprod Dev 2007;53:843-851.
41. Kim SS, Klemp J, Fabian C. Breast cancer and fertility preservation. Fertil Steril 2011;95:1535-1543.
42. Kuleshova L, Lopata A. Vitrification can be more favourable than slow cooling. Fertil Steril 2002;78:449-454.
43. Kuleshova L, Gianaroli L, Magli C, Ferraretti A, Trounson A. Birth following vitrification of small number of human oocytes: case report. Hum Reprod 1999;14:3077-3079.
44. Le Du A, Kadoch IJ, Bourcigaux N, Doumerc S, Bourrier MC, Chevalier N, Fanchin R, Chian RC, Tachdjian G, Frydman R et al. In vitro oocyte maturation for the treatment of infertility associated with polycystic ovarian syndrome: the French experience. Hum Reprod 2005;20:420-424.
45. Leibo SP. Water permeability and its activation energy of fertilized and unfertilized mouse ova. J Membr Biol 1980;53:179-188.
46. Loutradi KE, Kolibianakis EM, Venetis CA, Papanikolaou EG, Pados G, Bontis I, Tarlatzis BC. Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil Steril 2008;90:186-193.
47. Mandelbaum J, Anastasious O, Levy R, Guerin JF, de Larouziere V, Antonine JM. Effect of cryopreservation on meiotic spindle of human oocytes. Eur J Obstet Gynecol Reprod Biol 2004;113S:S17-S23.
48. Manipalviratn S, Tong ZB, Stegmann B, Widra J, Carter J, DeCherney J. Effect of vitrification and thawingonhuman oocyte ATPconcentration. Fertil Steril 2011;95:1839-1841.
49. Mansour G, Abdelrazik H, Sharma RK, Radwan E, Falcone T, Argarwal A. L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil Steril 2009;91:2079-2086.
50. Marei WF, Wathes DC, Fouladi-Nashta AA. Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reprod Fertil Dev 2012;24:679-690.
51. Melegh B, Sumegi B, Sherry AD. Preferential elimination of pivalate with supplemental carnitine via formation of pivaloylcarnitine in man. Xenobiotica 1993;23:1255-1261.
52. Melegh B, Pap M, Morava E, Molnar D, Dani M, Kurucz J. Carnitine dependent changes of metabolic fuel consumption during long-term treatment with valproic acid. J Pediatr 1994;125:317-321.
53. Mikkelsen AL. Strategies in human in-vitro maturation and their clinical outcome. Reprod Biomed Online 2005;10:593-609.
54. Miyamoto K, Sato EF, Kasahara E, Jikumaru M, Hiramoto K, Tabata H, Katsuragi M, Odo S, Utsumi K, Inoue M. Effect of oxidative stress during repeated ovulation on structure and functions of the ovary, oocytes, and their mitochondria. Free Radical Biol Med 2010;49:647-681.
55. Moawad AR, Choi I, Zhu J, Campbell KHS. Ovine oocytes vitrifiedatgerminal vesicle stage as cytoplast recipients for somatic cell nuclear transfer (SCNT). Cell Reprogram 2011;13:289-296.
56. Moawad AR, Fisher P, Zhu J, Choi I, Polgar Z, Dinnyes A, Campbell KHS. In vitro fertilization of ovine oocytes vitrified by solid surface vitrification at germinal vesicle stage. Cryobiology 2012;65:139-144.
57. Moawad AR, Zhu J, Choi I, Amarnath D, Campbell KHS. Effect of cytochalasin B pre-treatmentonviability, frequencies of invitro fertilizationand subsequent development of ovine oocytes vitrified at germinal vesicle stage. Cryo Letters 2013a; 34:634-644.
58. Moawad AR, Zhu J, Choi I, Amarnath D, Chen W, Campbell KHS. Production of good-quality blastocyst embryos following IVFofovine oocytes vitrified at the germinal vesicle stage using a cryoloop. Reprod Fertil Dev 2013b; 25:1204-1215.
59. Moawad AR, Tan SL, Xu B, Chen HY, Taketo T. L-carnitine supplementation during vitrification of mouse oocytesatthe germinal vesicle stage improves pre-Implantation development following maturation and fertilization in vitro. Biol Reprod 2013c; 88:104.
60. Muggleton-Harris AL, Brown JJ. Cytoplasmic factors influence mitochondrial reorganization and resumption of cleavage during culture of early mouse embryos. Hum Reprod 1988;3:1020-1028.
61. Nagai S, Mabuchi T, Hirata S, Shoda T, Kasai T, Yokota S, Shitara H, Yonekawa H, Hoshi K. Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J Exp Med 2006;210:137-144.
62. Nagy ZP, Chang CC, Shapiro DB, Bernal DP, Elsner CW, Mitchell-Leef D, Toledo AA, Kort HI. Clinical evaluation of the efficiency of an oocyte donation program using egg cryo-banking. Fertil Steril 2009;92:520-526.
63. Nangaku M, Sato-Yoshitake R, Okada Y, Noda Y, Takemura R, Yamazaki H, Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 1994;79:1209-1220.
64. Navarro-Costa P, Correia SC, Gouveia-Oliveria A, Negreiro F, Jorge S, Cidadao AJ, Carvalho MJ, Plancha CE. Effects of mouse ovarian tissue cryopreservation on granulose cell-oocyte interaction. Hum Reprod 2005;20:1607-1614.
65. Noyes N, Boldt J, Nagy ZP. Oocyte cryopreservation: is it time to remove its experimental label? J Assist Reprod Genet 2010a; 27:69-74.
66. Noyes N, Knopman J, Labella P, McCaffrey C, Clark-Williams M, Grifo J. Oocyte cryopreservation outcomes including pre-cryopreservation and post-thaw meiotic spindle evaluation following slow cooling and vitrification of human oocytes. Fertil Steril 2010b; 94:2078-2082.
67. Ou XH, Li S, Wang ZB, Li M, Quan S, Xing F, Guo L, Chao SB, Chen Z, Liang XW et al. Maternal insulin resistance causes oxidative stress and mitochondrial dysfunction in mouse oocytes. Hum Reprod 2012;27:2130-2145.
68. Park SE, Lee KA, Son WY, Ko JJ, Lee SH, Cha KY. Chromosome and spindle configurationsofhuman oocytes maturedinvitro after cryopreservation at the germinal vesicle stage. Fertil Steril 1997;68:920-926.
69. Pickering SJ, Braude PR, Johnson MH, Cant A, Curri J. Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil Steril 1990;54:102-108.
70. Potdar N, Gelbay TA, Nardo LG. Oocyte vitrification in the 21st century and post-warming fertility outcomes: a systematic review and meta-analysis. Reprod Biomed Online 2014 (in press).
71. Rao GD, Chian RC, Son WS, Gilbert L, Tan SL. Fertility preservation in women undergoing cancer treatment. The Lancet 2004;363:1829-1830.
72. Rho GJ, Kim S, Yoo JG, Balasubramanian S, Lee HJ, Choe S. Microtubulin configuration and mitochondrial distribution after ultra-rapid cooling of bovine oocytes. Mol Reprod Dev 2002;63:464-470.
73. Rojas C, Palomo MJ, Albarracin JL, Mogas T. Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules, and actin microfilaments. Cryobiology 2004;49:211-220.
74. Ruffing NA, Steponkus PL, Pitt RE, Parks JE. Osmometric behaviour, hydraulic conductivity, and incidenceofintracellular ice formationinbovine oocytesat different developmental stages. Cryobiology 1993;30:562-580.
75. Ruppert-Lingham CJ, Paynter SJ, Godfrey J, Fuller BJ, Shaw RW. Developmental potential of murine germinal vesicle stage cumulus-oocyte complexes following exposure to dimethylsulphoxide or cryopreservation: loss of membrane integrity of cumulus cells after thawing. Hum Reprod 2003;18:392-398.
76. Salehnia M, Töhönen V, Zavareh S, Inzunza J. Does cryopreservation of ovarian tissue affect the distribution and function of germinal vesicle oocytes mitochondria? Biomed Res Int 2013;2013:Article ID 89032.
77. Schon EA, Kim SH, Ferreira J, Magalhaes P, Grace M, Warburton D, Gross SJ. Chromosomal non-disjunction in human oocytes: isthere a mitochondrial connection? Hum Reprod 2000;15:160-172.
78. Shahedi A, Hosseini A, Khalili MA, Norouzian M, Salehi M, Piriaei A, Nottola SA. The effect of vitrification on ultrastructure of human in vitro matured germinal vesicle oocytes. Eur J Obstet Gynecol Reprod Biol 2013;167:69-75.
79. Shi LY, Jin HF, Kim JG, Mohana Kumar B, Balasubramanian S, Choe SY, Rho GJ. Ultra-structural changes and developmental potential of porcine oocytes following vitrification. Anim Reprod Sci 2007;100:128-140.
80. Somfai T, Noguchi J, Kaneko H, Nakai M, Ozawa M, Kashiwazaki N, Egerszegi I, Ratky J, Nagai T, Kikuchi K. Production of good-quality porcine blastocysts by in vitro fertilization of follicular oocytes vitrified at the germinal vesicle stage. Theriogenology 2010;73:147-156.
81. Somfai T, Kaneda M, Akagi S, Watanabe S, Haraguchi S, Mizutani E, Dang-Nguyen TQ, Geshi M, Kikuchi K, Nagai T. Enhancement of lipid metabolism with L-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod Fertil Dev 2011;23:912-920.
82. Son WY, Tan SL. Comparison between slow freezing and vitrification for human embryos. Expert Rev Med Devices 2009;6:1-7.
83. Stojkovic M, Macado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, Wolf E. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol Reprod 2001;64:904-909.
84. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998;93:1147-1158.
85. Tharasanit T, Colenbrander B, Stout TAE. Effect of maturation stage at cryopreservation on post-thaw cytoskeleton quality and fertilizability of equine oocytes. Mol Reprod Dev 2006;73:627-637.
86. Tharasanit T, Colleoni S, Galli C, Colenbrander B, Stout TAE. Protective effects of cumulus-corona radiata complex during vitrification of horse oocytes. Reproduction 2009;137:391-401.
87. Toth TL, Hassen WA, Lanzendorf SE, Hansen K, Sandow BA, Hodgen GD. Cryopreservation of human prophase I oocytes collected from unstimulated follicles. Fertil Steril 1994;61:1077-1082.
88. Tucker MJ, Wright G, Morton PC, Massey JB. Birth after cryopreservation of immature oocytes with subsequent in vitro maturation. Fertil steril 1998;70:578-579.
89. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism ionic regulation and developmental competence. Reproduction 2004;128:269-280.
90. Vandevoort CA, Shirley CR, Hill DL, Leibo SP. Effects of cryoprotectants and cryopreservation on germinal vesicle-stage cumulus-oocyte complexes of rhesus monkeys. Fertil Steril 2008;90:805-816.
91. Vaz FM, Melegh B, Bene J, Cuebas D, Gage DA, Bootsma A, Vreken P, van Gennip AH, Bieber LL, Wanders RJ. Analysis of carnitine biosynthesis metabolites in urine by HPLC-electrospray tandem mass spectrometry. Clin Chem 2002;48:826-834.
92. Vieira AD, Mazzalira A, Barbieri DP, Lehmkuhl RC, Rubin MIB, Vajta G. Calves born after open pulled straw vitrification of immature bovine oocytes. Cryobiology 2002;45:91-94.
93. Vincent C, Pickering SJ, Johnson MH. The hardening effect of dimethylsulphoxide on the mouse zona pellucida requires the presence of an oocyte and is associated with a reduction in the number of cortical granules present. J Reprod Fertil 1990;89:253-259.
94. Wang W, Keefe D. Spindle observation in living mammalian oocytes with the polarization microscope and its practical use. Cloning Stem Cells 2002;4:269-276.
95. Wang Q, Ratchford AM, Chi MMY, Schoeller E, Frolova A, Schedl T, Moley KH. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol Endocrinol 2009;23:1603-1612.
96. Whittingham DG. Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at - 1968C. J Reprod Fertil 1977;49:89-94.
97. Wilding M, Dale B, Marino M, diMotteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 2001;16:909-917.
98. Wilding M, Coppola G, Dale B, Di Matteo L Mitochondria and human preimplantation embryo development. Reproduction 2009;137:619-624.
99. Wu J, Zhang L, Wang X. In vitro maturation, fertilization and embryo development after ultra-rapid freezing of immature human oocytes. Reproduction 2001;121:389-393.
100. Wu LL, Russell DL, Norman RJ, Robker RL. Endoplasmic reticulum (ER) stress in cumulus-oocyte complexes impairs pentraxin-3 secretion, mitochondrial membrane potential (DCm) and embryo development. Mol Endocrinol 2012;26:562-573.
101. Xu B, Noohi S, Shin JS, Tan SL, Taketo T. Bi-directional communication with the cumulus cells is involved in the deficiency of XY oocytes in the components essential for proper second meiotic spindle assembly. Dev Biol 2014;385:242-252.
102. Yan CL, Fu XW, Zhou GB, Zhao XM, Suo L, Zhu SE. Mitochondrialbehaviors in the vitrified mouse oocyte and its parthenogenetic embryo: effect of taxol pretreatment and relationship to competence. Fertil Steril 2010;93:959-966.
103. Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol 2010;224:672-680.
104. Zander-Fox D, Cashman KS, Lane M. The presence of 1 mM glycine in vitrification solutions protects oocyte mitochondrial homeostasis and improves blastocyst development. J Assist Reprod Genet 2013;30:107-116.
105. Zhang X, Wu XY, Lu S, Guo YL, Ma XU. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res 2006;16:841-850.