Among the components of the female reproductive tract, the ovarian pool of follicles and their enclosed oocytes are highly sensitive to hyperthermia. Heat-induced alterations in small antral follicles can be expressed later as compromised maturation and developmental capacity of the ovulating oocyte. This review summarizes the most up-to-date information on the effects of heat stress on the oocyte with an emphasis on unclear points and open questions, some of which might involve new research directions, for instance, whether preantral follicles are heat resistant. The review focuses on the follicle-enclosed oocytes, provides new insights into the cellular and molecular responses of the oocyte to elevated temperature, points out the role of the follicle microenvironment, and discusses some mechanisms that might underlie oocyte impairment. Mechanisms include nuclear and cytoplasmic maturation, mitochondrial function, apoptotic pathways, and oxidative stress. Understanding the mechanism by which heat stress compromises fertility might enable development of new strategies to mitigate its effects.


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Literature Cited

  1. Bernabucci U, Biffani S, Buggiotti L, Vitali A, Lacetera N, Nardone A. 1.  2014. The effects of heat stress in Italian Holstein dairy cattle. J. Dairy Sci. 97:471–86 [Google Scholar]
  2. Roth Z. 2.  2008. Heat stress, the follicle and its enclosed oocyte: mechanism and potential strategies to improve fertility in heat-stressed cows. Reprod. Domest. Anim. 43:Suppl. 2238–44 [Google Scholar]
  3. Argov-Argaman N, Mahgrefthe K, Zeron Y, Roth Z. 3.  2013. Season-induced variation in lipid composition is associated with semen quality in Holstein bulls. Reproduction 145:479–89 [Google Scholar]
  4. Orgal S, Zeron Y, Elior N, Biran D, Friedman E. 4.  et al. 2012. Season-induced changes in bovine sperm motility following freeze-thaw procedure. J. Reprod. Dev. 58:212–18 [Google Scholar]
  5. Monterroso VH, Drury KC, Ealy AD, Edwards JL, Hansen PJ. 5.  1995. Effect of heat shock on function of frozen/thawed bull spermatozoa. Theriogenology 44:947–61 [Google Scholar]
  6. Hendricks KE, Martins L, Hansen PJ. 6.  2009. Consequences for the bovine embryo of being derived from a spermatozoon subjected to post-ejaculatory aging and heat shock: development to the blastocyst stage and sex ratio. J. Reprod. Dev. 55:69–74 [Google Scholar]
  7. Sakatani M, Yamanaka K, Balboula AZ, Takenouchi N, Takahashi M. 7.  2015. Heat stress during in vitro fertilization decreases fertilization success by disrupting anti-polyspermy systems of the oocytes. Mol. Reprod. Dev. 82:36–47 [Google Scholar]
  8. Hansen PJ. 8.  2007. Exploitation of genetic and physiological determinants of embryonic resistance to elevated temperature to improve embryonic survival in dairy cattle during heat stress. Theriogenology 68:242–49 [Google Scholar]
  9. Sakatani M, Kobayashi S, Takahashi M. 9.  2004. Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol. Reprod. Dev. 67:77–82 [Google Scholar]
  10. Brad AM, Hendricks KEM, Hansen PJ. 10.  2007. The block to apoptosis in bovine two-cell embryos involves inhibition of caspase-9 activation and caspase-mediated DNA damage. Reproduction 134:789–97 [Google Scholar]
  11. Carambula S, Oliveira LJ, Hansen PJ. 11.  2009. Repression of induced apoptosis in the two-cell bovine embryo involves DNA methylation and histone deacetylation. Biochem. Biophys. Res. Commun. 388:418–21 [Google Scholar]
  12. Rivera RM, Kelley KL, Erdos GW, Hansen PJ. 12.  2003. Alterations in ultrastructural morphology of two-cell bovine embryos produced in vitro and in vivo following a physiologically relevant heat shock. Biol. Reprod. 69:2068–77 [Google Scholar]
  13. Lussier JG, Matton P, Dufour JJ. 13.  1987. Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil. 81:301–7 [Google Scholar]
  14. Orisaka M, Tajima K, Tsang BK, Kotsuji F. 14.  2009. Oocyte-granulosa-theca cell interactions during preantral follicular development. J. Ovarian Res. 2:19 [Google Scholar]
  15. Campbell BK. 15.  2009. The endocrine and local control of ovarian follicle development in the ewe. Anim. Reprod. 6:159–71 [Google Scholar]
  16. Nilsson EE, Skinner MK. 16.  2009. Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Mol. Cell. Endocrinol. 313:9–16 [Google Scholar]
  17. Kim JY. 17.  2012. Control of ovarian primordial follicle activation. Clin. Exp. Reprod. Med. 39:10–14 [Google Scholar]
  18. Silva JRV, van den Hurk R, Figueiredo JR. 18.  2016. Ovarian follicle development in vitro and oocyte competence: advances and challenges for farm animals. Domest. Anim. Endocrinol. 55:123–35 [Google Scholar]
  19. Paes VM, Vieira LA, Correia HHV, Sa NAR, Moura AAA. 19.  et al. 2016. Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus-oocyte complex. Theriogenology 86:994–1003 [Google Scholar]
  20. Hyttel P, Fair T, Callesen H, Greve T. 20.  1997. Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47:23–32 [Google Scholar]
  21. Cortvrindt R, Smitz J. 21.  2001. In vitro follicle growth: achievements in mammalian species. Reprod. Domest. Anim. 36:3–9 [Google Scholar]
  22. Roth Z, Meidan R, Braw-Tal R, Wolfenson D. 22.  2000. Immediate and delayed effect of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J. Reprod. Fertil. 120:83–90 [Google Scholar]
  23. Roth Z, Meidan R, Shahan-Albalancy A, Braw-Tal R, Wolfenson D. 23.  2001. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction 121:745–51 [Google Scholar]
  24. Hojman D, Malul Y. 24.  2012. The Israeli Herd Book Caesarea, Isr.: Isr. Cattle Breed. Assoc. http://www.icba-israel.com/cbase/2012.pdf
  25. Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A. 25.  2001. Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121:447–54 [Google Scholar]
  26. Al-Katanani YM, Rivera RM, Hansen PJ. 26.  2002. Seasonal variation in development of in vitro produced bovine embryos. Vet. Rec. 150:486–87 [Google Scholar]
  27. Roth Z, Bor A, Braw-Tal R, Wolfenson D. 27.  2004. Carry-over effect of summer thermal stress on characteristics of the preovulatory follicle of lactating cows. J. Therm. Biol. 29:681–85 [Google Scholar]
  28. Friedman E, Voet H, Reznikov D, Dagoni I, Roth Z. 28.  2011. Induction of successive follicular waves by gonadotropin-releasing hormone and prostaglandin F to improve fertility of lactating cows during the summer and autumn. J. Dairy Sci. 94:2393–402 [Google Scholar]
  29. Roth Z. 29.  2015. Cellular and molecular mechanisms of heat stress related to bovine ovarian function. J. Anim. Sci. 93:2034–44 [Google Scholar]
  30. Ginther OJ, Knopf L, Kastelic JP. 30.  1989. Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J. Reprod. Fertil. 87:223–30 [Google Scholar]
  31. Savio JD, Keenan L, Boland MP, Roche JF. 31.  1988. Pattern of growth of dominant follicles during the oestrous cycle of heifers. J. Reprod. Fertil. 83:663–71 [Google Scholar]
  32. Sirois J, Fortune JE. 32.  1988. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biol. Reprod. 39:308–17 [Google Scholar]
  33. Ginther OJ, Wiltbank MC, Fricke PM, Gibbons JR, Kot K. 33.  1996. Selection of the dominant follicle in cattle. Biol. Reprod. 55:1187–94 [Google Scholar]
  34. Kastelic JP, Ko JC, Ginther OJ. 34.  1990. Suppression of dominant and subordinate ovarian follicles by a proteinaceous fraction of follicular fluid in heifers. Theriogenology 34:499–509 [Google Scholar]
  35. Badinga L, Thatcher WW, Diaz T, Drost M, Wolfenson D. 35.  1993. Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows. Theriogenology 39:797–810 [Google Scholar]
  36. Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. 36.  1998. Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J. Dairy Sci. 81:2124–31 [Google Scholar]
  37. Wilson SJ, Kirby CJ, Koenigsfeld AT, Keisler DH, Lucy MC. 37.  1998. Effects of controlled heat stress on ovarian function of dairy cattle. 2. Heifers. J. Dairy Sci. 81:2132–38 [Google Scholar]
  38. Wolfenson D, Roth Z, Meidan R. 38.  2000. Impaired reproduction in heat stressed cattle: basic and applied aspects. Anim. Reprod. Sci. 60–61:535–47 [Google Scholar]
  39. Roth Z. 39.  2008. Heat stress, the follicle, and its enclosed oocyte: mechanisms and potential strategies to improve fertility in dairy cows. Reprod. Domest. Anim. 43:Suppl. 2238–44 [Google Scholar]
  40. Shehab-El-Deen MA, Leroy JL, Fadel MS, Saleh SY, Maes D, Van Soom A. 40.  2010. Biochemical changes in the follicular fluid of the dominant follicle of high producing dairy cows exposed to heat stress early post-partum. Anim. Reprod. Sci. 117:189–200 [Google Scholar]
  41. Bridges PJ, Brusie MA, Fortune JE. 41.  2005. Elevated temperature (heat stress) in vitro reduces androstenedione and estradiol and increases progesterone secretion by follicular cells from bovine dominant follicles. Domest. Anim. Endocrinol. 29:508–22 [Google Scholar]
  42. Wise ME, Armstrong DV, Huber JT, Hunter R, Wiersma F. 42.  1988. Hormonal alterations in the lactating dairy cow in response to thermal stress. J. Dairy Sci. 71:2480–85 [Google Scholar]
  43. Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. 43.  1993. Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of estradiol in plasma of cyclic cows. J. Reprod. Fertil. 99:315–21 [Google Scholar]
  44. Lodde V, Modina S, Galbusera C, Franciosi F, Luciano AM. 44.  2007. Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74:740–49 [Google Scholar]
  45. Liu Y, Sui HS, Wang HL, Yuan JH, Luo MJ. 45.  et al. 2006. Germinal vesicle chromatin configuration of bovine oocytes. Microsc. Res. Tech. 69:799–807 [Google Scholar]
  46. Rocha A, Randel RD, Broussard JR, Lim JM, Blair RM. 46.  et al. 1998. High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology 49:657–65 [Google Scholar]
  47. Al-Katanani YM, Paula-Lopes FF, Hansen PJ. 47.  2002. Effect of season and exposure to heat stress on oocyte competence in Holstein cows. J. Dairy Sci. 85:390–96 [Google Scholar]
  48. Gendelman M, Aroyo A, Yavin S, Roth Z. 48.  2010. Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction 140:73–82 [Google Scholar]
  49. Friedman E, Voet H, Reznikov D, Wolfenson D, Roth Z. 49.  2014. Hormonal treatment before and after artificial insemination differentially improves fertility in subpopulations of dairy cows during the summer and autumn. J. Dairy Sci. 97:127465–75 [Google Scholar]
  50. Roth Z, Arav A, Bor A, Zeron Y, Braw-Tal R, Wolfenson D. 50.  2001. Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction 122:737–44 [Google Scholar]
  51. Torres-Júnior JR de S, Pires M de FA, de Sá WF, Ferreira A de M, Viana JHM. 51.  et al. 2008. Effect of maternal heat stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 15:155–66 [Google Scholar]
  52. Mermillod P, Marchal R. 52.  1999. Oocyte of domestic mammals: a model for the study of in vitro maturation. Contracept. Fertil. Sex. 27:440–48 [Google Scholar]
  53. Payton RR, Romar R, Coy P, Saxton AM, Lawrence JL, Edwards JL. 53.  2004. Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol. Reprod. 71:1303–8 [Google Scholar]
  54. Paula-Lopes FF, Lima RS, Risolia PHB, Ispada J, Assumpção MEOA, Visintin JA. 54.  2012. Heat stress induced alteration in bovine oocytes: functional and cellular aspects. Anim. Reprod. 9:395–403 [Google Scholar]
  55. Gendelman M, Roth Z. 55.  2012. In vivo versus in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression. Anim. Reprod. Sci. 134:125–34 [Google Scholar]
  56. Ferreira RM, Chiaratti MR, Macabelli CH, Rodrigues CA, Ferraza ML. 56.  et al. 2016. The infertility of repeat-breeder cows during summer is associated with decreased mitochondrial DNA and increased expression of mitochondrial and apoptotic genes in oocytes. Biol. Reprod. 94:66 [Google Scholar]
  57. Brevini-Gandolfi TA, Favetta LA, Mauri L, Luciano AM, Cillo F, Gandolfi F. 57.  1999. Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52:427–33 [Google Scholar]
  58. Brevini-Gandolfi TAL, Gandolfi F. 58.  2001. The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55:1255–76 [Google Scholar]
  59. Piccioni F, Zappavigna V, Verrotti AC. 59.  2005. Translational regulation during oogenesis and early development: the cap-poly(A) tail relationship. C. R. Biol. 328:863–81 [Google Scholar]
  60. Flemr M, Ma J, Richard M, Schultz RM, Svoboda P. 60.  2010. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes. Biol. Reprod. 82:1008–17 [Google Scholar]
  61. Memili E, Dominko T, First NL. 61.  1998. Onset of transcription in bovine oocytes and preimplantation embryos. Mol. Reprod. Dev. 51:36–41 [Google Scholar]
  62. Gendelman M, Roth Z. 62.  2012. Seasonal effect on germinal vesicle-stage bovine oocytes is further expressed by alterations in transcript levels in the developing embryos associated with reduced developmental competence. Biol. Reprod. 86:1–9 [Google Scholar]
  63. Chambers I, Tomlinson SR. 63.  2009. The transcriptional foundation of pluripotency. Development 36:2311–22 [Google Scholar]
  64. Cummings A, Sommerville J. 64.  1988. Protein kinase activity associated with stored protein kinase activity associated with stored messenger ribonucleoprotein particles of Xenopus oocytes. J. Cell Biol. 107:45–56 [Google Scholar]
  65. Marello K, LaRovere J, Sommerville J. 65.  1992. Binding of Xenopus oocyte masking proteins to mRNA sequences. Nucleic Acids Res 20:5593–600 [Google Scholar]
  66. Oh B, Hwang S, McLaughlin J, Solter D, Knowles BB. 66.  2000. Timely translation during the mouse oocyte-to-embryo transition. Development 127:3795–803 [Google Scholar]
  67. Richter JD. 67.  2007. CPEB: a life in translation. Trends Biochem. Sci. 32:279–85 [Google Scholar]
  68. Eppig JJ. 68.  1996. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8:485–89 [Google Scholar]
  69. Tripathi A, Kumar KV, Chaube SK. 69.  2010. Meiotic cell cycle arrest in mammalian oocytes. J. Cell. Physiol. 223:592–600 [Google Scholar]
  70. Ferreira EM, Vireque AA, Adona PR, Meirelles FV, Ferriani RA, Navarro PA. 70.  2009. Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71:836–48 [Google Scholar]
  71. Hyttel P, Viuff D, Fair T, Laurincik J, Thomsen PD. 71.  et al. 2001. Ribosomal RNA gene expression and chromosome aberrations in bovine oocytes and preimplantation embryos. Reproduction 122:21–30 [Google Scholar]
  72. Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P. 72.  et al. 2001. 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. 64:904–9 [Google Scholar]
  73. Ju JC, Tseng JK. 73.  2004. Nuclear and cytoskeletal alterations of in vitro matured porcine oocytes under hyperthermia. Mol. Reprod. Dev. 68:125–33 [Google Scholar]
  74. Tseng JK, Chen CH, Chou PC, Yeh SP, Ju JC. 74.  2004. Influences of follicular size on parthenogenetic activation and in vitro heat shock on the cytoskeleton in cattle oocytes. Reprod. Domest. Anim. 39:146–53 [Google Scholar]
  75. Ju JC, Jiang S, Tseng JK, Parks JE, Yang X. 75.  2005. Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64:1677–89 [Google Scholar]
  76. Roth Z, Hansen PJ. 76.  2005. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129:235–44 [Google Scholar]
  77. Pavani KC, Baron E, Correia P, Lourenço J, Bettencourt BF. 77.  et al. 2016. Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock. Zygote 28:1–12 [Google Scholar]
  78. Edwards JL, Saxton AM, Lawrence JL, Payton RR, Dunlap JR. 78.  2005. Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J. Dairy Sci. 88:4326–33 [Google Scholar]
  79. Schrock GE, Saxton AM, Schrick FN, Edwards JL. 79.  2007. Early in vitro fertilization improves development of bovine ova heat stressed during in vitro maturation. J. Dairy Sci. 90:4297–303 [Google Scholar]
  80. Gendelman M, Roth Z. 80.  2012. Incorporation of coenzyme Q10 into bovine oocytes improves mitochondrial features and alleviates the effects of summer thermal stress on developmental competence. Biol. Reprod. 87:1–12 [Google Scholar]
  81. Eppig JJ, Wigglesworth K, Pendola FL. 81.  2002. The mammalian oocyte orchestrates the rate of ovarian follicular development. PNAS 99:2890–94 [Google Scholar]
  82. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. 82.  2002. Intercellular communication in the mammalian ovary: Oocytes carry the conversation. Science 296:2178–80 [Google Scholar]
  83. Fair T, Hyttel P, Greve T. 83.  1995. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42:437–42 [Google Scholar]
  84. Assey RJ, Hyttel P, Greve T, Purwantara B. 84.  1994. Oocyte morphology in dominant and subordinate follicles. Mol. Reprod. Dev. 37:335–44 [Google Scholar]
  85. Paula-Lopes FF, Lima RS, Satrapa RA, Barros CMJ. 85.  2013. Influence of cattle genotype (Bos indicus versus Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature. Anim. Sci 91:1143–53 [Google Scholar]
  86. Kalo D, Roth Z. 86.  2011. Involvement of the sphingolipid ceramide in heat-shock induced apoptosis of bovine oocytes. Reprod. Fertil. Dev. 23:876–88 [Google Scholar]
  87. Ozawa M, Hirabayashi M, Kanai Y. 87.  2002. Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction 124:683–89 [Google Scholar]
  88. Ferreira RM, Ayres H, Chiaratti MR, Ferraz ML, Araújo AB. 88.  et al. 2011. The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. J. Dairy Sci. 94:2383–92 [Google Scholar]
  89. Liu L, Hammar K, Smith PJS, Inoue S, Keefe DL. 89.  2001. Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium 30:423–33 [Google Scholar]
  90. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD. 90.  2004. Calcium and mitochondria. FEBS Lett 567:96–102 [Google Scholar]
  91. Chappel S. 91.  2013. The role of mitochondria from mature oocyte to viable blastocyst. Obstet. Gynecol. Int 2013:183024 [Google Scholar]
  92. Smith LC, Alcivar AA. 92.  1993. Cytoplasmic inheritance and its effects on development and performance. J. Reprod. Fertil. 48:S31–S43 [Google Scholar]
  93. Michaels GS, Hauswirth WW, Laipis PJ. 93.  1982. Mitochondrial DNA copy number in bovine oocytes and somatic cells. Dev. Biol. 94:246–51 [Google Scholar]
  94. Dumollard R, Duchen M, Carroll J. 94.  2007. The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77:21–49 [Google Scholar]
  95. Thouas GA, Trounson AO, Wolvetang EJ, Jones GM. 95.  2004. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod. 71:1936–42 [Google Scholar]
  96. Ebert KM, Liem H, Hecht NB. 96.  1988. Mitochondrial DNA in the mouse preimplantation embryo. J. Reprod. Fertil. 82:145–49 [Google Scholar]
  97. Sathananthan AH, Trounson AO. 97.  2000. Mitochondrial morphology during preimplantational human embryogenesis. Hum. Reprod. 15:148–59 [Google Scholar]
  98. Motta PM, Nottola SA, Makabe S, Heyn R. 98.  2000. Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod. 15:129–47 [Google Scholar]
  99. Sherratt HS. 99.  1991. Mitochondria: structure and function. Rev. Neurol. 147:417–30 [Google Scholar]
  100. St. John JC, Facucho-Oliveira J, Jiang Y, Kelly R, Salah R. 100.  2010. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum. Reprod. Update 16:488–509 [Google Scholar]
  101. Andersson SG, Karlberg O, Canback B, Kurland CG. 101.  2003. On the origin of mitochondria: a genomics perspective. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:165–77 [Google Scholar]
  102. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR. 102.  et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:457–65 [Google Scholar]
  103. Jansen RPS. 103.  2000. Origin and persistence of the mitochondrial genome. Hum. Reprod. 15:1–10 [Google Scholar]
  104. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA. 104.  1981. Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–80 [Google Scholar]
  105. Clayton DA. 105.  1984. Transcription of the mammalian mitochondrial genome. Annu. Rev. Biochem. 53:573–94 [Google Scholar]
  106. Poyton RO, McEwen JE. 106.  1996. Crosstalk between nuclear and mitochondrial genomes. Annu. Rev. Biochem. 65:563–607 [Google Scholar]
  107. Cannino G, Di Liegro CM, Rinaldi AM. 107.  2007. Nuclear-mitochondrial interaction. Mitochondrion 7:359–66 [Google Scholar]
  108. Sazer S, Sherwood SW. 108.  1990. Mitochondrial growth and DNA synthesis occur in the absence of nuclear DNA replication in fission yeast. J. Cell Sci. 97:509–16 [Google Scholar]
  109. Spinazzola A, Zeviani M. 109.  2009. Mitochondrial diseases: a cross-talk between mitochondrial and nuclear genomes. Adv. Exp. Med. Biol 52:69–84 [Google Scholar]
  110. Piko L, Taylor KD. 110.  1987. Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev. Biol. 123:364–74 [Google Scholar]
  111. Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M. 111.  et al. 2001. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7:425–29 [Google Scholar]
  112. Van Blerkom J, Davis PW, Lee J. 112.  1995. Fertilization and early embryology: ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10:415–24 [Google Scholar]
  113. Zeng HT, Ren Z, Yeung WSB, Shu YM, Xu YW. 113.  et al. 2007. Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum. Reprod. 22:1681–86 [Google Scholar]
  114. Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. 114.  2010. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224:672–80 [Google Scholar]
  115. Bavister BD, Squirrell JM. 115.  2000. Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 2:189–98 [Google Scholar]
  116. Nagai S, Mabuchi T, Hirata S, Shoda T, Kasai T. 116.  et al. 2006. Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210:137–44 [Google Scholar]
  117. Boldogh IR, Pon LA. 117.  2007. Mitochondria on the move. Trends. Cell Biol. 17:502–10 [Google Scholar]
  118. Zampolla T, Spikings E, Rawson D, Zhang T. 118.  2011. Cytoskeleton proteins F-actin and tubulin distribution and interaction with mitochondria in the granulosa cells surrounding stage III zebrafish (Danio rerio) oocytes. Theriogenology 76:1110–19 [Google Scholar]
  119. Spikings EC, Alderson J, St. John JC. 119.  2006. Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer. Hum. Reprod. Update 12:401–15 [Google Scholar]
  120. Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K. 120.  et al. 2011. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23:424–32 [Google Scholar]
  121. May-Panloup P, Vignon X, Chrétien MF, Heyman Y, Tamassia M. 121.  et al. 2005. Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod. Biol. Endocrinol. 14:65–73 [Google Scholar]
  122. Horowitz S. 122.  2003. CoQ10: one antioxidant, many promising applications. Altern. Complement. Ther. 9:111–16 [Google Scholar]
  123. Van Blerkom J. 123.  2011. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11:797–813 [Google Scholar]
  124. Roth Z, Hansen PJ. 124.  2004. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71:1898–906 [Google Scholar]
  125. Roth Z, Hansen PJ. 125.  2004. Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol. Reprod. 71:2072–78 [Google Scholar]
  126. Soto P, Smith LC. 126.  2009. BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses ap-optotic mitochondrial changes in heat stressed bovine oocytes. Mol. Reprod. Dev. 76:637–46 [Google Scholar]
  127. Jenkins GM, Cowart LA, Signorelli P, Pettus BJ, Chalfant CE, Hannun YA. 127.  2002. Acute activation of de novo sphingolipid biosynthesis upon heat shock causes an accumulation of ceramide and subsequent dephosphorylation of SR proteins. J. Biol. Chem. 277:42572–78 [Google Scholar]
  128. Fouladi-Nashta AA, Gutierrez CG, Gong JG, Garnsworthy PC, Webb R. 128.  2007. Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biol. Reprod. 77:9–17 [Google Scholar]
  129. Matsuzuka T, Ozawa M, Hirabayashi M, Ushitani A, Kanai Y. 129.  2004. Developmental competence and glutathione content of maternally heat-stressed mouse oocytes and zygotes. Anim. Sci. J. 75:117–24 [Google Scholar]
  130. Nabenishi H, Takagi S, Kamata H, Nishimoto T, Morita T. 130.  et al. 2012. The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Mol. Reprod. Dev. 79:31–40 [Google Scholar]
  131. Takami M, Preston SL, Toyloy VA, Behrman HR. 131.  1999. Antioxidants reversibly inhibit the spontaneous resumption of meiosis. Am. J. Physiol. 276:684–88 [Google Scholar]
  132. Van Blerkom J, Antczak M, Schrader R. 132.  1997. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 12:1047–55 [Google Scholar]
  133. Ealy AD, Arechiga CF, Bray DR, Risco CA, Hansen PJ. 133.  1994. Effectiveness of short-term cooling and vitamin E for alleviation of infertility induced by heat stress in dairy cows. J. Dairy Sci. 77:3601–7 [Google Scholar]
  134. Aréchiga CF, Staples CR, McDowell LR, Hansen PJ. 134.  1998. Effects of timed insemination and supplemental β-carotene on reproduction and milk yield of dairy cows under heat stress. J. Dairy Sci. 81:390–402 [Google Scholar]
  135. Paula-Lopes FF, Al-Katanani YM, Majewski AC, McDowell LR, Hansen PJ. 135.  2003. Manipulation of antioxidant status fails to improve fertility of lactating cows or survival of heat-shocked embryos. J. Dairy Sci. 86:2343–51 [Google Scholar]
  136. Ealy AD, Howell JL, Monterroso VH, Arechiga CF, Hansen PJ. 136.  1995. Developmental changes in sensitivity of bovine embryos to heat shock and use of antioxidants as thermoprotectants. J. Dairy Sci. 73:1401–7 [Google Scholar]
  137. Sakatani M, Suda I, Oki T, Kobayashi S, Kobayashi S, Takahashi M. 137.  2007. Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock. J. Reprod. Dev. 53:605–14 [Google Scholar]
  138. Castro e Paula LA, Hansen PJ. 138.  2008. Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol. Mol. Reprod. Dev. 75:1338–50 [Google Scholar]
  139. Roth Z, Aroyo A, Yavin S, Arav A. 139.  2008. The antioxidant epigallocatechin gallate (EGCG) moderates the deleterious effects of maternal hyperthermia on follicle-enclosed oocytes in mice. Theriogenology 70:887–97 [Google Scholar]
  140. Matsuzuka T, Sakamoto N, Ozawa M, Ushitani A, Hirabayashi M, Kanai Y. 140.  2005. Alleviation of maternal hyperthermia-induced early embryonic death by administration of melatonin to mice. J. Pineal Res. 39:217–23 [Google Scholar]
  141. Garcia-Ispierto I, Abdelfatah A, López-Gatius F. 141.  2013. Melatonin treatment at dry-off improves reproductive performance postpartum in high-producing dairy cows under heat stress conditions. Reprod. Domest. Anim. 48:577–83 [Google Scholar]

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