Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging

Aging Cell

Volumn 14, Issue 5, 2015, Pages 887-895

  Ben Meir, Assaf ^a,b   Burstein, Eliezer ^a,b   Borrego Alvarez, Aluet ^a   Chong, Jasmine ^a   Wong, Ellen ^a,c   Yavorska, Tetyana ^a,c   Naranian, Taline ^a,c   Chi, Maggie ^d   Wang, Ying ^e   Bentov, Yaakov ^b,c   Alexis, Jennifer ^f   Meriano, James ^f   Sung, Hoon Ki ^a   Gasser, David L ^g   Moley, Kelle H ^d   Hekimi, Siegfried ^e   Casper, Robert F ^a,b,c   Jurisicova, Andrea ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b Toronto Centre for Advanced Reproductive Technology   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f Lifequest Centre for Reproductive Medicine   (Canada)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Anti aging; Fecundity; Individual; Mitochondria; Molecular biology of aging; Mouse models

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHORIONIC GONADOTROPIN; COENZYME Q 6; DECAPRENYL DIPHOSPHATE SYNTHASE SUBUNIT 2; QUINONE DERIVATIVE; RESVERATROL; SERIC GONADOTROPIN; SYNTHETASE; THIOCTIC ACID; UBIDECARENONE; UNCLASSIFIED DRUG; UBIQUINONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL FUNCTION; CONTROLLED STUDY; ENZYME SUBUNIT; ENZYME SYNTHESIS; FEMALE; FEMALE FERTILITY; FEMALE INFERTILITY; GENE EXPRESSION; GENOTYPE; GERM LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MEIOTIC SPINDLE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OOCYTE; OVARIAN PRESERVATION; OVARIAN RESERVE; OVULATION INDUCTION; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; AGING; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; DRUG EFFECTS; FERTILITY; METABOLISM; TRANSGENIC MOUSE;

AGING; ANIMALS; FEMALE; FERTILITY; MICE; MICE, TRANSGENIC; MITOCHONDRIA; OOCYTES; REPRODUCTION; UBIQUINONE;

EID: 84940892038     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12368     Document Type: Article

References (43)

1. Battaglia DE, Goodwin P, Klein NA, Soules MR (1996) Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 11, 2217-2222.
2. Bentov Y, Yavorska T, Esfandiari N, Jurisicova A, Casper RF (2011) The contribution of mitochondrial function to reproductive aging. J. Assist. Reprod. Genet. 28, 773-783.
3. Chi MM, Hoehn A, Moley KH (2002) Metabolic changes in the glucose-induced apoptotic blastocyst suggest alterations in mitochondrial physiology. Am. J. Physiol. Endocrinol. Metab. 283, E226-E232.
4. Chiang T, Schultz RM, Lampson MA (2011) Age-dependent susceptibility of chromosome cohesion to premature separase activation in mouse oocytes. Biol. Reprod. 85, 1279-1283.
5. Crane FL (2001) Biochemical functions of coenzyme Q10. J. Am. Coll. Nutr. 20, 591-598.
6. Dalton CM, Szabadkai G, Carroll J (2014) Measurement of ATP in single oocytes: impact of maturation and cumulus cells on levels and consumption. J. Cell. Physiol. 229, 353-361.
7. Dumollard R, Ward Z, Carroll J, Duchen MR (2007) Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455-465.
8. Faddy MJ (2000) Follicle dynamics during ovarian ageing. Mol. Cell. Endocrinol. 163, 43-48.
9. Faddy MJ, Gosden RG, Edwards RG (1983) Ovarian follicle dynamics in mice: a comparative study of three inbred strains and an F1 hybrid. J. Endocrinol. 96, 23-33.
10. Fernandes R, Tsuda C, Perumalsamy AL, Naranian T, Chong J, Acton BM, Tong ZB, Nelson LM, Jurisicova A (2012) NLRP5 mediates mitochondrial function in mouse oocytes and embryos. Biol. Reprod. 86, 138, 1-10.
11. Garcia-Corzo L, Luna-Sanchez M, Doerrier C, Garcia JA, Guaras A, Acin-Perez R, Bullejos-Peregrin J, Lopez A, Escames G, Enriquez JA, Acuna-Castroviejo D, Lopez LC (2013) Dysfunctional Coq9 protein causes predominant encephalomyopathy associated with CoQ deficiency. Hum. Mol. Genet. 22, 1233-1248.
12. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS (2004) Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 13, 2263-2278.
13. Heeringa SF, Chernin G, Chaki M, Zhou W, Sloan AJ, Ji Z, Xie LX, Salviati L, Hurd TW, Vega-Warner V, Killen PD, Raphael Y, Ashraf S, Ovunc B, Schoeb DS, McLaughlin HM, Airik R, Vlangos CN, Gbadegesin R, Hinkes B, Saisawat P, Trevisson E, Doimo M, Casarin A, Pertegato V, Giorgi G, Prokisch H, Rotig A, Nurnberg G, Becker C, Wang S, Ozaltin F, Topaloglu R, Bakkaloglu A, Bakkaloglu SA, Muller D, Beissert A, Mir S, Berdeli A, Varpizen S, Zenker M, Matejas V, Santos-Ocana C, Navas P, Kusakabe T, Kispert A, Akman S, Soliman NA, Krick S, Mundel P, Reiser J, Nurnberg P, Clarke CF, Wiggins RC, Faul C, Hildebrandt F (2011) COQ6 mutations in human patients produce nephrotic syndrome with sensorineural deafness. J. Clin. Invest. 121, 2013-2024.
14. Kalen A, Appelkvist EL, Dallner G (1989) Age-related changes in the lipid compositions of rat and human tissues. Lipids 24, 579-584.
15. Kujjo LL, Acton BM, Perkins GA, Ellisman MH, D'Estaing SG, Casper RF, Jurisicova A, Perez GI (2013) Ceramide and its transport protein (CERT) contribute to deterioration of mitochondrial structure and function in aging oocytes. Mech. Ageing Dev. 134, 43-52.
16. Leese HJ, Barton AM (1984) Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J. Reprod. Fertil. 72, 9-13.
17. Lewandoski M, Wassarman KM, Martin GR (1997) Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr. Biol. 7, 148-151.
18. Liu L, Keefe DL (2002) Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum. Reprod. 17, 2678-2685.
19. Lobe CG, Koop KE, Kreppner W, Lomeli H, Gertsenstein M, Nagy A (1999) Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208, 281-292.
20. Lopez LC, Schuelke M, Quinzii CM, Kanki T, Rodenburg RJ, Naini A, Dimauro S, Hirano M (2006) Leigh syndrome with nephropathy and CoQ10 deficiency due to decaprenyl diphosphate synthase subunit 2 (PDSS2) mutations. Am. J. Hum. Genet. 79, 1125-1129.
21. Lu S, Lu LY, Liu MF, Yuan QJ, Sham MH, Guan XY, Huang JD (2012) Cerebellar defects in Pdss2 conditional knockout mice during embryonic development and in adulthood. Neurobiol. Dis. 45, 219-233.
22. Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH (2012) High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE 7, e49217.
23. Miles MV, Horn PS, Tang PH, Morrison JA, Miles L, DeGrauw T, Pesce AJ (2004) Age-related changes in plasma coenzyme Q10 concentrations and redox state in apparently healthy children and adults. Clin. Chim. Acta 347, 139-144.
24. Morre DM, Guo F, Morre DJ (2003) An aging-related cell surface NADH oxidase (arNOX) generates superoxide and is inhibited by coenzyme Q. Mol. Cell. Biochem. 254, 101-109.
25. Noia G, Littarru GP, De Santis M, Oradei A, Mactromarino C, Trivellini C, Caruso A (1996) Coenzyme Q10 in pregnancy. Fetal Diagn. Ther. 11, 264-270.
26. O'Connor KA, Holman DJ, Wood JW (1998) Declining fecundity and ovarian ageing in natural fertility populations. Maturitas 30, 127-136.
27. Pan H, Ma P, Zhu W, Schultz RM (2008) Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 316, 397-407.
28. Peng M, Falk MJ, Haase VH, King R, Polyak E, Selak M, Yudkoff M, Hancock WW, Meade R, Saiki R, Lunceford AL, Clarke CF, Gasser DL (2008) Primary coenzyme Q deficiency in Pdss2 mutant mice causes isolated renal disease. PLoS Genet. 4, e1000061.
29. Perumalsamy A, Fernandes R, Lai I, Detmar J, Varmuza S, Casper RF, Jurisicova A (2010) Developmental consequences of alternative Bcl-x splicing during preimplantation embryo development. FEBS J. 277, 1219-1233.
30. Quinzii CM, Lopez LC, Gilkerson RW, Dorado B, Coku J, Naini AB, Lagier-Tourenne C, Schuelke M, Salviati L, Carrozzo R, Santorelli F, Rahman S, Tazir M, Koenig M, DiMauro S, Hirano M (2010) Reactive oxygen species, oxidative stress, and cell death correlate with level of CoQ10 deficiency. FASEB J. 24, 3733-3743.
31. Saiki R, Lunceford AL, Shi Y, Marbois B, King R, Pachuski J, Kawamukai M, Gasser DL, Clarke CF (2008) Coenzyme Q10 supplementation rescues renal disease in Pdss2kd/kd mice with mutations in prenyl diphosphate synthase subunit 2. Am. J. Physiol. Renal. Physiol. 295, F1535-F1544.
32. Takeuchi T, Neri QV, Katagiri Y, Rosenwaks Z, Palermo GD (2005) Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol. Reprod. 72, 584-592.
33. Thouas GA, Trounson AO, Jones GM (2006) Developmental effects of sublethal mitochondrial injury in mouse oocytes. Biol. Reprod. 74, 969-977.
34. Titus S, Li F, Stobezki R, Akula K, Unsal E, Jeong K, Dickler M, Robson M, Moy F, Goswami S, Oktay K (2013) Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci. Transl. Med. 5, 172ra121.
35. Tran UC, Clarke CF (2007) Endogenous synthesis of coenzyme Q in eukaryotes. Mitochondrion 7(Suppl), S62-S71.
36. Turi A, Giannubilo SR, Bruge F, Principi F, Battistoni S, Santoni F, Tranquilli AL, Littarru G, Tiano L (2012) Coenzyme Q10 content in follicular fluid and its relationship with oocyte fertilization and embryo grading. Arch. Gynecol. Obstet. 285, 1173-1176.
37. Van Blerkom J, Davis PW, Lee J (1995) ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10, 415-424.
38. te Velde ER, Pearson PL (2002) The variability of female reproductive ageing. Hum. Reprod. Update 8, 141-154.
39. Wang Y, Hekimi S (2013) Molecular genetics of ubiquinone biosynthesis in animals. Crit. Rev. Biochem. Mol. Biol. 48, 69-88.
40. Wang Q, Ratchford AM, Chi MM, Schoeller E, Frolova A, Schedl T, Moley KH (2009) Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol. Endocrinol. 23, 1603-1612.
41. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G (2001) Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909-917.
42. Wyman A, Pinto AB, Sheridan R, Moley KH (2008) One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring. Endocrinology 149, 466-469.
43. Ziegler CG, Peng M, Falk MJ, Polyak E, Tsika E, Ischiropoulos H, Bakalar D, Blendy JA, Gasser DL (2012) Parkinson's disease-like neuromuscular defects occur in prenyl diphosphate synthase subunit 2 (Pdss2) mutant mice. Mitochondrion 12, 248-257.