Maternal obesity, infertility and mitochondrial dysfunction: Potential mechanisms emerging from mouse model systems

Molecular Human Reproduction

Volumn 19, Issue 8, 2013, Pages 487-494

  Grindler, Natalia M ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Infertility; Mitochondria; Obesity; Oocyte

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AGING; ARTICLE; CALORIC RESTRICTION; CHROMOSOME ABERRATION; EMBRYO DEVELOPMENT; HUMAN; HYPERGLYCEMIA; INFERTILITY; LIPID DIET; MATERNAL OBESITY; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRION; MOUSE STRAIN; NONHUMAN; OOCYTE MATURATION; PATHOGENESIS; PRIORITY JOURNAL; RISK FACTOR; SMOKING; ANIMAL; DISEASE MODEL; FEMALE; FEMALE INFERTILITY; METABOLISM; MOUSE; OBESITY; OOCYTE; PATHOLOGY; PREGNANCY; REPRODUCTIVE HEALTH;

NICOTIANA TABACUM;

AGING; ANIMALS; CALORIC RESTRICTION; DISEASE MODELS, ANIMAL; FEMALE; HYPERGLYCEMIA; INFERTILITY, FEMALE; MICE; MITOCHONDRIA; OBESITY; OOCYTES; PREGNANCY; REPRODUCTIVE HEALTH; SMOKING;

EID: 84880729455     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat026     Document Type: Article

References (82)

1. Acton BM, Jurisicova A, Jurisica I, Casper RF. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod 2004;10:23-32.
2. Amaral S, Oliveira PJ, Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev 2008;4:46-54.
3. Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J et al. Fertility and ageing. Hum Reprod Update 2005;11:261-276.
4. Ballinger SW, Bouder TG, Davis GS, Judice SA, Nicklas JA, Albertini RJ. Mitochondrial genome damage associated with cigarette smoking. Cancer Res. 1996;56:5692-5697.
5. Barja G. Endogenous oxidative stress: relationship to aging, longevity and caloric restriction. Ageing Res Rev. 2002;1:397-411.
6. Barnett DK, Kimura J, Bavister BD. Translocation of active mitochondria during hamster preimplantation embryo development studied by confocal laser scanning microscopy. Dev Dyn 1996;205:64-72.
7. Bentov Y, Esfandiari N, Burstein E, Casper RF. The use of mitochondrial nutrients to improve the outcome of infertility treatment in older patients. Fertil Steril 2010;93:272-275.
8. Bolumar F, Olsen J, Rebagliato M, Saez-Lloret I, Bisanti L. Body mass index and delayed conception: a European Multicenter Study on Infertility and Subfecundity. Am J Epidemiol 2000;151:1072-1079.
9. Bratic I, Hench J, Henriksson J, Antebi A, Burglin TR, Trifunovic A. Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res 2009; 37:1817-1828.
10. Brenner CA, Wolny YM, Barritt JA, Matt DW, Munne S, Cohen J. Mitochondrial DNA deletion in human oocytes and embryos. Mol Hum Reprod 1998;4:887-892.
11. Cao L, Shitara H, Horii T, Nagao Y, Imai H, Abe K, Hara T, Hayashi J, Yonekawa H. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet 2007; 39:386-390.
12. Castillo-Martinez L, Lopez-Alvarenga JC, Villa AR, Gonzalez-Barranco J. Menstrual cycle length disorders in 18-to 40-y-old obese women. Nutrition 2003;19:317-320.
13. Chehab FF, Lim ME, Lu R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet 1996;12:318-320.
14. Chen X, Prosser R, Simonetti S, Sadlock J, Jagiello G, Schon EA. Rearranged mitochondrial genomes are present in human oocytes. Am J Hum Genet 1995;57:239-247.
15. Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996;84:491-495.
16. Cummins JM. The role of maternal mitochondria during oogenesis, fertilization and embryogenesis. Reprod Biomed Online 2002;4:176-182.
17. Depalo R, Garruti G, Totaro I, Panzarino M, Vacca MP, Giorgino F, Selvaggi LE. Oocyte morphological abnormalities in overweight women undergoing in vitro fertilization cycles. Gynecol Endocrinol 2011; 27:880-884.
18. Dokras A, Baredziak L, Blaine J, Syrop C, VanVoorhis BJ, Sparks A. Obstetric outcomes after in vitro fertilization in obese and morbidly obese women. Obstet Gynecol 2006;108:61-69.
19. Douchi T, Kuwahata R, Yamamoto S, Oki T, Yamasaki H, Nagata Y. Relationship of upper body obesity to menstrual disorders. Acta Obstet Gynecol Scand. 2002;81:147-150.
20. Duchen MR. Mitochondria and calcium: from cell signalling to cell death. J Physiol 2000;529(Pt 1):57-68.
21. Duran HE, Simsek-Duran F, Oehninger SC, Jones HW Jr, Castora FJ. The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation. Fertil Steril 2011;96:384-388.
22. Dvorak M, Tesarik J, Pilka L, Travnik P. Fine structure of human two-cell ova fertilized and cleaved in vitro. Fertil Steril 1982;37:661-667.
23. Ebert KM, Liem H, Hecht NB. Mitochondrial DNA in the mouse preimplantation embryo. J Reprod Fertil 1988;82:145-149.
24. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 2004;13:935-944.
25. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001;122:829-838.
26. Fontanesi F, Soto IC, Horn D, Barrientos A. Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 2006;291:C1129-C1147.
27. Ge H, TollnerTL, HuZ, DaiM, LiX, GuanH, ShanD, ZhangX, LvJ, Huang C et al. The importance of mitochondrial metabolic activity and mitochondrial DNA replication during oocyte maturation in vitro on oocyte quality and subsequent embryo developmental competence. Mol Reprod Dev 2012;79:392-401.
28. Hewitson LC, Leese HJ. Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst. J Exp Zool 1993;267:337-343.
29. Houghton FD. Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 2006;74:11-18.
30. Hummel KP. Transplantation of ovaries in the obese mouse. Anat Rec 1957; 128:569.
31. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 2010;5:e10074.
32. Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K, Kuwayama T, Monji Y. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev 2011; 23:424-432.
33. Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH. Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 2010;151:4039-4046.
34. Jurisicova A, Taniuchi A, Li H, Shang Y, Antenos M, Detmar J, Xu J, Matikainen T, Benito Hernandez A, Nunez G et al. Maternal exposure to polycyclic aromatic hydrocarbons diminishes murine ovarian reserve via induction of Harakiri. J Clin Invest 2007;117:3971-3978.
35. Kaufman BA, Durisic N, Mativetsky JM, Costantino S, Hancock MA, Grutter P, Shoubridge EA. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol Biol Cell 2007;18:3225-3236.
36. Kogo N, Tazaki A, Kashino Y, Morichika K, Orii H, Mochii M, Watanabe K. Germ-line mitochondria exhibit suppressed respiratory activity to support their accurate transmission to the next generation. Dev Biol 2011;349:462-469.
37. Kushnir VA, Ludaway T, Russ RB, Fields EJ, KoczorC, Lewis W. Reproductive aging is associated with decreased mitochondrial abundance and altered structure in murine oocytes. J Assist Reprod Genet 2012;29:637-642.
38. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005;1:361-370.
39. Liu X, Fernandes R, Gertsenstein M, Perumalsamy A, Lai I, Chi M, Moley KH, Greenblatt E, Jurisica I, Casper RF et al. Automated microinjection of recombinant BCL-X into mouse zygotes enhances embryo development. PLoS One 2011;6:e21687.
40. Luke B, Brown MB, Stern JE, Missmer SA, Fujimoto VY, Leach R. Female obesity adversely affects assisted reproductive technology (ART) pregnancy and live birth rates. Hum Reprod 2011;26:245-252.
41. Luoma P, Melberg A, Rinne JO, KaukonenJA, Nupponen NN, Chalmers RM, Oldfors A, Rautakorpi I, Peltonen L, Majamaa K et al. Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet 2004; 364:875-882.
42. Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One 2012;7:e49217.
43. Machtinger R, Combelles CM, Missmer SA, Correia KF, Fox JH, Racowsky C. The association between severe obesity and characteristics of failed fertilized oocytes. Hum Reprod 2012;27:3198-3207.
44. Mahrous E, Yang Q, Clarke HJ. Regulation of mitochondrial DNA accumulation during oocyte growth and meiotic maturation in the mouse. Reproduction 2012;144:177-185.
45. Mair W, Dillin A. Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 2008;77:727-754.
46. Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev 2005; 126:913-922.
47. Sakai T, Korsmeyer SJ, Casper RF et al. Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat Genet 2001;28:355-360.
48. Mattison DR, Shiromizu K, Nightingale MS. Oocyte destruction by polycyclic aromatic hydrocarbons. Am J Ind Med 1983;4:191-202.
49. Mattison DR, Singh H, Takizawa K, Thomford PJ. Ovarian toxicity of benzo(a)pyrene and metabolites in mice. Reprod Toxicol 1989;3:115-125.
50. Mick DU, Vukotic M, Piechura H, Meyer HE, Warscheid B, Deckers M, Rehling P. Coa3 and Cox14 are essential for negative feedback regulation of COX1 translation in mitochondria. J Cell Biol 2010; 191:141-154.
51. Motta PM, Nottola SA, Makabe S, Heyn R. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod 2000;15(Suppl. 2):129-147.
52. Muller-Hocker J, Schafer S, Weis S, Munscher C, Strowitzki T. Morphological-cytochemical and molecular genetic analyses of mitochondria in isolated human oocytes in the reproductive age. Mol Hum Reprod 1996;2:951-958.
53. Nagano M, Katagiri S, Takahashi Y. Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 2006;14:53-61.
54. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993;74:609-619.
55. Paszkowski T, Clarke RN, Hornstein MD. Smoking induces oxidative stress inside the Graafian follicle. Hum Reprod 2002;17:921-925.
56. Paula-Lopes FF, Boelhauve M, Habermann FA, Sinowatz F, Wolf E. Leptin promotes meiotic progression and developmental capacity of bovine oocytes via cumulus cell-independent and -dependent mechanisms. Biol. Reprod 2007;76:532-541.
57. Perez GI, Jurisicova A, Wise L, Lipina T, Kanisek M, Bechard A, Takai Y, Hunt P, Roder J, Grynpas M et al. Absence of the proapoptotic Bax protein extends fertility and alleviates age-related health complications in female mice. Proc Natl Acad Sci USA 2007;104:5229-5234.
58. Practice Committee of American Society for Reproductive M. Obesity and reproduction: an educational bulletin. Fertil Steril 2008;90:S21-S29.
59. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 2009; 15:553-572.
60. Ratchford AM, Chang AS, Chi MM, Sheridan R, Moley KH. Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am J Physiol Endocrinol Metab 2007; 293:E1198-E1206.
61. Reers M, Smith TW, Chen LB. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 1991;30:4480-4486.
62. Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425-429.
63. Rich-Edwards JW, Goldman MB, Willett WC, Hunter DJ, Stampfer MJ, Colditz GA, Manson JE. Adolescent body mass index and infertility caused by ovulatory disorder. Am J Obstet Gynecol 1994;171:171-177.
64. Rodgers JT, Lerin C, Gerhart-Hines Z, Puigserver P. Metabolic adaptations through thePGC-1alpha and SIRT1 pathways. FEBS Lett 2008;582:46-53.
65. Santos TA, El Shourbagy S, St John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril 2006;85:584-591.
66. Selesniemi K, Lee HJ, Muhlhauser A, Tilly JL. Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci USA 2011;108:12319-12324.
67. Senoo-Matsuda N, Igaki T, Miura M. Bax-like protein Drob-1 protects neurons from expanded polyglutamine-induced toxicity in Drosophila. EMBO J 2005;24:2700-2713.
68. Smithberg M, Runner MN. Pregnancy induced in genetically sterile mice. J Heredity 1957;48:97-100.
69. Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech Ageing Dev 1994;74:121-133.
70. Stojkovic M, Machado 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.
71. Sussman NB, Mazumdar S, Mattison DR. Modeling adverse environmental impacts on the reproductive system. JWomens Health 1999;8:217-226.
72. Tamer Erel C, Senturk LM. The impact of body mass index on assisted reproduction. Curr Opin Obstet Gynecol 2009;21:228-235.
73. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 2004;128:269-280.
74. Van Blerkom J. Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod Biomed Online 2008;16:553-569.
75. Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 2011; 11:797-813.
76. Van Blerkom J, Davis P. Mitochondrial signaling and fertilization. Mol Hum Reprod 2007;13:759-770.
77. Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reproduct 2010;83:52-62.
78. Wang JX, Davies MJ, Norman RJ. Obesity increases the risk of spontaneous abortion during infertility treatment. Obes Res 2002;10:551-554.
79. Wang Q, Ratchford AM, Chi MM, 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.
80. WHO. World Health Organization. Obesity and overweight: fact sheet N311, 2012.
81. Wu LL, Dunning KR, Yang X, Russell DL, Lane M, Norman RJ, Robker RL. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexesc and decreased fertilization rates. Endocrinology 2010;151:5438-5445.
82. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 1994; 372:425-432.