Mitochondrial dysfunction in the offspring of obese mothers and it's transmission through damaged oocyte mitochondria: Integration of mechanisms

WHO, 2022, Obesity and over weight [Internet], News Room Brewer, 2010, The adverse effects of obesity on conception and implantation. Reproduction, 140, 347 Lisonkova, 2017, Association between prepregnancy body mass index and severe maternal morbidity, JAMA, 318, 1777, 10.1001/jama.2017.16191 Platner, 2021, Severe maternal morbidity and mortality during delivery hospitalization of class I, II, III, and super obese women, Am. J. Obstet. Gynecol. MFM, 3, 10.1016/j.ajogmf.2021.100420 Zheng, 2018, Increased maternal Body Mass Index is associated with congenital heart defects: an updated meta-analysis of observational studies, Int. J. Cardiol., 273, 112, 10.1016/j.ijcard.2018.09.116 Vena, 2022, Risk of neural tube defects according to maternal body mass index: a systematic review and meta-analysis, J. Matern.-Fetal Neonatal Med., 35, 7296, 10.1080/14767058.2021.1946789 Crozier, 2010, Weight gain in pregnancy and childhood body composition: findings from the Southampton Women’s Survey, Am. J. Clin. Nutr., 91, 1745, 10.3945/ajcn.2009.29128 Catalano, 2009, Perinatal risk factors for childhood obesity and metabolic dysregulation, Am. J. Clin. Nutr., 90, 1303, 10.3945/ajcn.2008.27416 Robker, 2009, Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women, J. Clin. Endocrinol. Metab., 94, 1533, 10.1210/jc.2008-2648 Jungheim, 2010, Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring, Endocrinology, 151, 4039, 10.1210/en.2010-0098 Catteau, 2016, Leptin and its potential interest in assisted reproduction cycles, Hum. Reprod. Update, 22, 320, 10.1093/humupd/dmv057 Phy, 2004, Insulin and messenger ribonucleic acid expression of insulin receptor isoforms in ovarian follicles from nonhirsute ovulatory women and polycystic ovary syndrome patients, J. Clin. Endocrinol. Metab., 89, 3561, 10.1210/jc.2003-031888 Wyman, 2008, One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring, Endocrinology, 149, 466, 10.1210/en.2007-1273 Wallace, 2016, Genetics: mitochondrial DNA in evolution and disease, Nature, 535, 498, 10.1038/nature18902 Duchen, 2003, Imaging mitochondrial function in intact cells, Methods Enzymol., 361, 353, 10.1016/S0076-6879(03)61019-0 Igosheva, 2010, Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes, PLoS One, 5, 10.1371/journal.pone.0010074 Turner, 2015, Developmental programming of obesity and insulin resistance: does mitochondrial dysfunction in oocytes play a role?, Mol. Hum. Reprod., 21, 23, 10.1093/molehr/gau042 Luzzo, 2012, High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects, PLoS One, 7, 10.1371/journal.pone.0049217 Wang, 2015, Fruit and vegetable consumption and risk of lung cancer: a dose-response meta-analysis of prospective cohort studies, Lung Cancer, 88, 124, 10.1016/j.lungcan.2015.02.015 Boudoures, 2017, Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy, Dev. Biol., 426, 126, 10.1016/j.ydbio.2017.04.005 Wrottesley, 2018, Maternal traditional dietary pattern and antiretroviral treatment exposure are associated with neonatal size and adiposity in urban, black South Africans, Br. J. Nutr., 120, 557, 10.1017/S0007114518001708 English, 2021, Evaluation of dietary patterns and all-cause mortality: a systematic review, JAMA Netw. Open, 4, 1, 10.1001/jamanetworkopen.2021.22277 Bach-Faig, 2011, Mediterranean diet pyramid today. Science and cultural updates, Public Health Nutr., 14, 2274, 10.1017/S1368980011002515 Valerino-Perea, 2022, Adherence to a traditional Mexican diet and non-communicable disease-related outcomes: secondary data analysis of the cross-sectional Mexican National Health and Nutrition Survey, Br. J. Nutr, 129, 1 Wathes, 2007, Polyunsaturated fatty acids in male and female reproduction, Biol. Reprod., 77, 190, 10.1095/biolreprod.107.060558 Saini, 2018, Omega-3 and omega-6 polyunsaturated fatty acids: dietary sources, metabolism, and significance - a review, Life Sci., 203, 255, 10.1016/j.lfs.2018.04.049 Bentov, 2014, Coenzyme Q10 supplementation and oocyte aneuploidy in women undergoing IVF-ICSI treatment, Clin. Med. Insights Reprod. Health, 8, 10.4137/CMRH.S14681 Ochiai, 2019, Influence of resveratrol supplementation on IVF-embryo transfer cycle outcomes, Reprod. Biomed. Online, 39, 205, 10.1016/j.rbmo.2019.03.205 Takeo, 2014, Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes, J. Reprod. Dev., 60, 92, 10.1262/jrd.2013-102 Del Gobbo, 2016, ω-3 polyunsaturated fatty acid biomarkers and coronary heart disease: pooling project of 19 cohort studies, JAMA Intern. Med., 176, 1155, 10.1001/jamainternmed.2016.2925 Zhang, 2017, Efficacy of Omega-3 polyunsaturated fatty acids supplementation in managing overweight and obesity: a meta-analysis of randomized clinical trials, J. Nutr. Health Aging, 21, 187, 10.1007/s12603-016-0755-5 Yao, 2015, Resveratrol relieves gestational diabetes mellitus in mice through activating AMPK, Reprod. Biol. Endocrinol., 13, 10.1186/s12958-015-0114-0 Picard, 2022, Mitochondrial signal transduction, Cell Metab., 34, 1620, 10.1016/j.cmet.2022.10.008 Adebayo, 2021, Mitochondrial fusion and fission: the fine-tune balance for cellular homeostasis, FASEB J., 35, 10.1096/fj.202100067R Adebayo, 2021, Mitochondrial fusion and fission: the fine-tune balance for cellular homeostasis, FASEB J., 35, 10.1096/fj.202100067R Gyllenhammer, 2020, Developmental programming of mitochondrial biology: a conceptual framework and review, Proc. Biol. Sci., 287 Kasahara, 2014, Mitochondria: from cell death executioners to regulators of cell differentiation, Trends Cell Biol., 24, 761, 10.1016/j.tcb.2014.08.005 Herst, 2017, Functional mitochondria in health and disease, Front. Endocrinol. (Lausanne), 8 Calvo, 2010, The mitochondrial proteome and human disease, Annu. Rev. Genomics Hum. Genet., 11, 25, 10.1146/annurev-genom-082509-141720 Sharma, 2019, Mitochondrial DNA integrity: role in health and disease, Cells, 8, 10.3390/cells8020100 Wang, 2006, Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane, J. Biol. Chem., 281, 25791, 10.1074/jbc.M604501200 Brüser, 2021, The TFAM-to-mtDNA ratio defines inner-cellular nucleoid populations with distinct activity levels, Cell Rep., 37, 10.1016/j.celrep.2021.110000 Curth, 1994, Single-stranded-DNA-binding proteins from human mitochondria and Escherichia coli have analogous physicochemical properties, Eur. J. Biochem., 221, 435, 10.1111/j.1432-1033.1994.tb18756.x Alam, 2003, Human mitochondrial DNA is packaged with TFAM, Nucleic Acids Res., 31, 1640, 10.1093/nar/gkg251 Wei, 2019, Germline selection shapes human mitochondrial DNA diversity, Science, 364, 10.1126/science.aau6520 Shukla, 2023, Molecular characterization of variants in mitochondrial DNA encoded genes using next generation sequencing analysis and mitochondrial dysfunction in women with PCOS, Gene, 855, 10.1016/j.gene.2022.147126 Young, 2022, Identification of somatic mitochondrial DNA mutations, heteroplasmy, and increased levels of catenanes in tumor specimens obtained from three endometrial cancer patients, Life (Basel), 12 Ye, 2014, Extensive pathogenicity of mitochondrial heteroplasmy in healthy human individuals, Proc. Natl. Acad. Sci. U.S.A., 111, 10654, 10.1073/pnas.1403521111 Payne, 2013, Universal heteroplasmy of human mitochondrial DNA, Hum. Mol. Genet., 22, 384, 10.1093/hmg/dds435 Arbeithuber, 2020, Age-related accumulation of de novo mitochondrial mutations in mammalian oocytes and somatic tissues, PLoS Biol., 18, 10.1371/journal.pbio.3000745 Arbeithuber, 2022, Advanced age increases frequencies of de novo mitochondrial mutations in macaque oocytes and somatic tissues, Proc. Natl. Acad. Sci. U.S.A., 119, 10.1073/pnas.2118740119 Zaidi, 2019, Bottleneck and selection in the germline and maternal age influence transmission of mitochondrial DNA in human pedigrees, Proc. Natl. Acad. Sci. U.S.A., 116, 25172, 10.1073/pnas.1906331116 Sesaki, 2003, Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane, Mol. Biol. Cell, 14, 2342, 10.1091/mbc.e02-12-0788 Westermann, 2012, Bioenergetic role of mitochondrial fusion and fission, Biochim. Biophys. Acta, 1817, 1833, 10.1016/j.bbabio.2012.02.033 Chan, 2012, Fusion and fission: interlinked processes critical for mitochondrial health, Annu Rev Genet, 46, 265, 10.1146/annurev-genet-110410-132529 Bogenhagen, 2012, Mitochondrial DNA nucleoid structure, Biochim. Biophys. Acta - Gene Regul. Mech., 1819, 10.1016/j.bbagrm.2011.11.005 Valle, 2005, PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells, Cardiovasc. Res., 66, 562, 10.1016/j.cardiores.2005.01.026 Martínez-Reyes, 2020, Mitochondrial TCA cycle metabolites control physiology and disease, Nat. Commun., 11, 10.1038/s41467-019-13668-3 Xie, 2020, NAD+ metabolism: pathophysiologic mechanisms and therapeutic potential, Signal Transduct. Target. Ther., 5 Dai, 2020, The evolving metabolic landscape of chromatin biology and epigenetics, Nat. Rev. Genet., 21, 737, 10.1038/s41576-020-0270-8 Barile, 2000, The riboflavin/FAD cycle in rat liver mitochondria, Eur. J. Biochem., 267, 4888, 10.1046/j.1432-1327.2000.01552.x Nagaraj, 2017, Nuclear localization of mitochondrial TCA Cycle enzymes as a critical step in mammalian zygotic genome activation, Cell, 168, 210, 10.1016/j.cell.2016.12.026 Zhang, 2019, Mitofusin 1 is required for female fertility and to maintain ovarian follicular reserve, Cell Death Dis., 10, 10.1038/s41419-019-1799-3 Carvalho, 2020, Mitofusin 1 is required for oocyte growth and communication with follicular somatic cells, FASEB J., 34, 7644, 10.1096/fj.201901761R Partridge, 1996, Consumption of amino acids by bovine preimplantation embryos, Reprod. Fertil. Dev., 8, 945, 10.1071/RD9960945 Booth, 2005, Amino acid depletion and appearance during porcine preimplantation embryo development in vitro, Reproduction, 130, 655, 10.1530/rep.1.00727 Houghton, 2004, Metabolism and developmental competence of the preimplantation embryo, Eur. J. Obstet. Gynecol. Reprod. Biol., 115 Houghton, 2006, Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst, Differentiation, 74, 11, 10.1111/j.1432-0436.2006.00052.x Hewitson, 1993, Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst, J. Exp. Zool., 267, 337, 10.1002/jez.1402670310 Aizawa, 2019, Synthesis and maintenance of lipid droplets are essential for mouse preimplantation embryonic development, Development, 146, 10.1242/dev.181925 Seidler, 2015, Metabolic determinants of mitochondrial function in oocytes, Semin. Reprod. Med., 33, 396, 10.1055/s-0035-1567822 Dumollard, 2008, Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes, Dev. Biol., 316, 431, 10.1016/j.ydbio.2008.02.004 Kirillova, 2021, Mazunin I. The role of mitochondria in oocyte maturation, Cells, 10, 10.3390/cells10092484 Rojansky, 2016, Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1, Elife, 5 Dumollard, 2009, Mitochondrial function and redox state in mammalian embryos, Semin. Cell Dev. Biol., 20, 346, 10.1016/j.semcdb.2008.12.013 de Paula, 2013, Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template, Philos. Trans. R. Soc. Lond., B, Biol. Sci., 368, 10.1098/rstb.2012.0263 Rodríguez-Nuevo, 2022, Oocytes maintain ROS-free mitochondrial metabolism by suppressing complex I, Nature, 607, 756, 10.1038/s41586-022-04979-5 Aitken, 2020, Impact of oxidative stress on male and female germ cells: implications for fertility, Reproduction, 159, R189, 10.1530/REP-19-0452 Leese, 2002, Quiet please, do not disturb: a hypothesis of embryo metabolism and viability, Bioessays, 24, 845, 10.1002/bies.10137 Leese, 2016, Biological optimization, the Goldilocks principle, and how much is lagom in the preimplantation embryo, Mol. Reprod. Dev., 83, 748, 10.1002/mrd.22684 Gardner, 1990, Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro, J. Reprod. Fertil., 88, 361, 10.1530/jrf.0.0880361 Gupta, 2011, Fluctuations in total antioxidant capacity, catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis, Reprod. Fertil. Dev., 23, 673, 10.1071/RD10270 El Mouatassim, 2000, Mammalian oviduct and protection against free oxygen radicals: expression of genes encoding antioxidant enzymes in human and mouse, Eur. J. Obstet. Gynecol. Reprod. Biol., 89, 1, 10.1016/S0301-2115(99)00169-4 Freitas, 2017, Follicular fluid redox involvement for ovarian follicle growth, J. Ovarian Res., 10, 10.1186/s13048-017-0342-3 Fischer, 1993, Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits, J. Reprod. Fertil., 99, 673, 10.1530/jrf.0.0990673 Xiao, 2012, Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors, Genes Dev., 26, 1326, 10.1101/gad.191056.112 Constantopoulos, 1984, Nonenzymatic decarboxylation of pyruvate, Anal. Biochem., 139, 353, 10.1016/0003-2697(84)90016-2 Biggers, 1967, The pattern of energy metabolism in the mouse oöcyte and zygote, Proc. Natl. Acad. Sci. U.S.A., 58, 560, 10.1073/pnas.58.2.560 Leese, 1995, Metabolic control during preimplantation mammalian development, Hum. Reprod. Update, 1, 63, 10.1093/humupd/1.1.63 Summers, 2003, Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues, Hum. Reprod. Update, 9, 557, 10.1093/humupd/dmg039 Dumollard, 2007, Regulation of redox metabolism in the mouse oocyte and embryo, Development, 134, 455, 10.1242/dev.02744 Van Winkle, 2001, Amino acid transport regulation and early embryo development, Biol. Reprod., 64, 1, 10.1095/biolreprod64.1.1 Leese, 2008, Metabolism of the viable mammalian embryo: quietness revisited, Mol. Hum. Reprod., 14, 667, 10.1093/molehr/gan065 Pelland, 2009, Amino acid transport mechanisms in mouse oocytes during growth and meiotic maturation, Biol. Reprod., 81, 1041, 10.1095/biolreprod.109.079046 Hemmings, 2012, Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro, Biol. Reprod., 86, 10.1095/biolreprod.111.092585 Harris, 2007, Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro, Reproduction, 134, 415, 10.1530/REP-07-0061 Hugentobler, 2007, Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine, Mol. Reprod. Dev., 74, 445, 10.1002/mrd.20607 Picton, 1998, The molecular basis of oocyte growth and development, Mol. Cell. Endocrinol., 145, 27, 10.1016/S0303-7207(98)00166-X Tomek, 2002, Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro, Reprod. Domest. Anim., 37, 86, 10.1046/j.1439-0531.2002.00336.x Schultz, 1979, Program of early development in the mammal: changes in the patterns and absolute rates of tubulin and total protein synthesis during oocyte growth in the mouse, Dev. Biol., 73, 120, 10.1016/0012-1606(79)90142-8 Sternlicht, 1981, Biochemical studies of mammalian oogenesis: kinetics of accumulation of total and poly(A)-containing RNA during growth of the mouse oocyte, J. Exp. Zool., 215, 191, 10.1002/jez.1402150209 Zuelke, 1993, Increased glutamine metabolism in bovine cumulus cell-enclosed and denuded oocytes after in vitro maturation with luteinizing hormone, Biol. Reprod., 48, 815, 10.1095/biolreprod48.4.815 Rieger, 1994, Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro, J. Reprod. Fertil., 100, 257, 10.1530/jrf.0.1000257 Chand, 2011, Amino acid transport system L activity in developing mouse ovarian follicles, Hum. Reprod., 26, 3102, 10.1093/humrep/der298 Luberda, 2005, The role of glutathione in mammalian gametes, Reprod. Biol., 5 Sturmey, 2003, Energy metabolism in pig oocytes and early embryos, Reproduction, 126, 197, 10.1530/rep.0.1260197 Fujimoto, 2011, Not just fat: the structure and function of the lipid droplet, Cold Spring Harb. Perspect. Biol., 3, 1, 10.1101/cshperspect.a004838 Walther, 2012, Lipid droplets and cellular lipid metabolism, Annu. Rev. Biochem., 81, 687, 10.1146/annurev-biochem-061009-102430 Downs, 2009, Fatty acid oxidation and meiotic resumption in mouse oocytes, Mol. Reprod. Dev., 76, 844, 10.1002/mrd.21047 Dunning, 2010, Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development, Biol. Reprod., 83, 909, 10.1095/biolreprod.110.084145 Bradley, 2016, Quantitative imaging of lipids in live mouse oocytes and early embryos using CARS microscopy, Development, 143, 2238 Sieber, 2016, Electron transport chain remodeling by GSK3 during oogenesis connects nutrient state to reproduction, Cell, 164, 420, 10.1016/j.cell.2015.12.020 Valckx, 2014, Elevated non-esterified fatty acid concentrations during in vitro murine follicle growth alter follicular physiology and reduce oocyte developmental competence, Fertil. Steril., 102, 1769, 10.1016/j.fertnstert.2014.08.018 Zeron, 2002, Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes, Mol. Reprod. Dev., 61, 271, 10.1002/mrd.1156 Fouladi-Nashta, 2007, Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows, Biol. Reprod., 77, 9, 10.1095/biolreprod.106.058578 Jungheim, 2011, Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization, Fertil. Steril., 95, 1970, 10.1016/j.fertnstert.2011.01.154 Creanga, 2022, Obesity in pregnancy. Longo DL, editor, N. Engl. J. Med., 387, 248, 10.1056/NEJMra1801040 Vats, 2021, Impact of maternal pre-pregnancy body mass index on maternal, fetal and neonatal adverse outcomes in the worldwide populations: a systematic review and meta-analysis, Obes. Res. Clin. Pract., 15, 536, 10.1016/j.orcp.2021.10.005 D’Souza, 2019, Maternal body mass index and pregnancy outcomes: a systematic review and metaanalysis, Am. J. Obstet. Gynecol. MFM, 1, 1(4), 10.1016/j.ajogmf.2019.100041 Williams, 2015, Overweight and obesity: prevalence, consequences, and causes of a growing public health problem, Curr. Obes. Rep., 4, 363, 10.1007/s13679-015-0169-4 Pallares, 2010, Substantiation of ovarian effects of leptin by challenging a mouse model of obesity/type 2 diabetes, Theriogenology, 73, 1088, 10.1016/j.theriogenology.2010.01.008 Wu, 2010, High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates, Endocrinology, 151, 5438, 10.1210/en.2010-0551 Fleming, 2004, The embryo and its future, Biol. Reprod., 71, 1046, 10.1095/biolreprod.104.030957 Marei, 2020, Differential effects of high fat diet-induced obesity on oocyte mitochondrial functions in inbred and outbred mice, Sci. Rep., 10, 10.1038/s41598-020-66702-6 Reers, 1991, J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential, Biochemistry, 30, 4480, 10.1021/bi00232a015 Wang, 2021, NAMPT reduction-induced NAD+ insufficiency contributes to the compromised oocyte quality from obese mice, Aging Cell, 20, 10.1111/acel.13496 Bausenwein, 2010, Elevated levels of oxidized low-density lipoprotein and of catalase activity in follicular fluid of obese women, Mol. Hum. Reprod., 16, 117, 10.1093/molehr/gap078 Nonogaki, 1994, Developmental blockage of mouse embryos caused by fatty acids, J. Assist. Reprod. Genet., 11, 482, 10.1007/BF02215713 Shaaker, 2012, Fatty acid composition of human follicular fluid phospholipids and fertilization rate in assisted reproductive techniques, Iran. Biomed. J., 16, 1 Haggarty, 2006, Fatty acid metabolism in human preimplantation embryos, Hum. Reprod., 21, 766, 10.1093/humrep/dei385 Aardema, 2011, Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence, Biol. Reprod., 85, 62, 10.1095/biolreprod.110.088815 Jungheim, 2013, Weighing the impact of obesity on female reproductive function and fertility, Nutr. Rev., 71 Hammiche, 2011, Increased preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology, Fertil. Steril., 95, 1820, 10.1016/j.fertnstert.2010.11.021 Wu, 2015, Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors, Development, 142, 681, 10.1242/dev.114850 Malhotra, 2007, Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?, Antioxid. Redox Signal., 9, 2277, 10.1089/ars.2007.1782 Zhao, 2017, The ER-localized transmembrane protein EPG-3/VMP1 regulates SERCA activity to control ER-isolation membrane contacts for autophagosome formation, Mol. Cell, 67, 974, 10.1016/j.molcel.2017.08.005 Borradaile, 2006, Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death, J. Lipid Res., 47, 2726, 10.1194/jlr.M600299-JLR200 Garcia, 2020, Mice born to females with oocyte-specific deletion of mitofusin 2 have increased weight gain and impaired glucose homeostasis, Mol. Hum. Reprod., 26, 938, 10.1093/molehr/gaaa071 Hanson, 2021, Developmental origins of health and disease: towards a combined bio-social life-course perspective, Acta Paediatr., 110, 2306, 10.1111/apa.15905 Smith, 2022, Maternal fructose intake causes developmental reprogramming of hepatic mitochondrial catalytic activity and lipid metabolism in weanling and young adult offspring, Int. J. Mol. Sci., 23, 10.3390/ijms23020999 Shelley, 2009, Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice, Am. J. Physiol. Regul. Integr. Comp. Physiol., 297, 10.1152/ajpregu.00146.2009 Turdi, 2013, Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects, J. Mol. Cell. Cardiol., 55, 117, 10.1016/j.yjmcc.2012.12.007 Murrin, 2012, Body mass index and height over three generations: evidence from the Lifeways cross-generational cohort study, BMC Public Health, 12, 10.1186/1471-2458-12-81 Ponzio, 2012, Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1-F3 offspring, Life Sci., 90, 571, 10.1016/j.lfs.2012.01.017 Rodríguez-Nuevo, 2022, Oocytes maintain ROS-free mitochondrial metabolism by suppressing complex I, Nature, 607, 756, 10.1038/s41586-022-04979-5 Andreas, 2019, The effect of maternal high-fat/high-sugar diet on offspring oocytes and early embryo development, Mol. Hum. Reprod., 25, 717, 10.1093/molehr/gaz049 Boudoures, 2016, The effects of voluntary exercise on oocyte quality in a diet-induced obese murine model, Reproduction, 151, 261, 10.1530/REP-15-0419 Marei, 2019, Mitochondria-targeted therapy rescues development and quality of embryos derived from oocytes matured under oxidative stress conditions: a bovine in vitro model, Hum. Reprod., 34, 1984, 10.1093/humrep/dez161 Christoforou, 2020, Molecular mechanisms governing offspring metabolic programming in rodent models of in utero stress, Cell. Mol. Life Sci., 77, 4861, 10.1007/s00018-020-03566-z Saben, 2016, Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations, Cell Rep., 16, 1, 10.1016/j.celrep.2016.05.065 Hancock, 2021, Mammalian primordial germ cell specification, Development, 148, 10.1242/dev.189217 Wai, 2010, The role of mitochondrial DNA copy number in mammalian fertility, Biol. Reprod., 83, 52, 10.1095/biolreprod.109.080887 Borengasser, 2014, In utero exposure to prepregnancy maternal obesity and postweaning high-fat diet impair regulators of mitochondrial dynamics in rat placenta and offspring, Physiol. Genom., 46, 841, 10.1152/physiolgenomics.00059.2014 Borengasser, 2011, Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning, PLoS One, 6, 10.1371/journal.pone.0024068 Mdaki, 2016, Call for papers cardiovascular mitochondria and redox control in health and disease, Am. J. Physiol. Heart Circ. Physiol., 310, 681, 10.1152/ajpheart.00795.2015 Wang, 2019, Maternal obesity impairs fetal mitochondriogenesis and brown adipose tissue development partially via upregulation of miR-204-5p HHS public access, Biochim. Biophys. Acta Mol. basis Dis., 1865, 2706, 10.1016/j.bbadis.2019.07.012 Lu, 2021, Placental mitochondrial function in response to gestational exposures, Placenta, 104, 124, 10.1016/j.placenta.2020.11.012 Sferruzzi-Perri, 2023, Placental adaptations supporting fetal growth during normal and adverse gestational environments, Exp. Physiol., 108, 10.1113/EP090442 Napso, 2022, Diet-induced maternal obesity impacts feto-placental growth and induces sex-specific alterations in placental morphology, mitochondrial bioenergetics, dynamics, lipid metabolism and oxidative stress in mice, Acta Physiol. (Oxf.), 234, 10.1111/apha.13795 Woods, 2018, Influence of maternal aging on mitochondrial heterogeneity, inheritance, and function in oocytes and preimplantation embryos, Genes (Basel), 9, 10.3390/genes9050265 Fecher, 2019, Cell-type-specific profiling of brain mitochondria reveals functional and molecular diversity, Nat. Neurosci., 22, 1731, 10.1038/s41593-019-0479-z Picard, 2012, Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function, Am. J. Physiol. Cell Physiol., 302, 10.1152/ajpcell.00368.2011 Pagliarini, 2008, A mitochondrial protein compendium elucidates complex I disease biology, Cell, 134, 112, 10.1016/j.cell.2008.06.016 Yang, 2010, Eaten alive: a history of macroautophagy, Nat. Cell Biol., 12, 814, 10.1038/ncb0910-814 Nakatogawa, 2009, Dynamics and diversity in autophagy mechanisms: lessons from yeast, Nat. Rev. Mol. Cell Biol., 10, 458, 10.1038/nrm2708 Zhang, 2013, Autophagy and mitophagy in cellular damage control, Redox. Biol., 1, 19, 10.1016/j.redox.2012.11.008 Lemasters, 2005, Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging, Rejuvenation Res., 8, 3, 10.1089/rej.2005.8.3 Roberts, 2016, Defending the mitochondria: The pathways of mitophagy and mitochondrial-derived vesicles, Int. J. Biochem. Cell Biol., 79, 427, 10.1016/j.biocel.2016.07.020 Cummins, 2000, Fertilization and elimination of the paternal mitochondrial genome, Hum. Reprod., 2, 92, 10.1093/humrep/15.suppl_2.92 Al Rawi, 2011, Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission, Science, 334, 1144, 10.1126/science.1211878 Song, 2016, Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization, Proc. Natl. Acad. Sci. U.S.A., 113, E5261, 10.1073/pnas.1605844113 Sutovsky, 1999, Ubiquitin tag for sperm mitochondria, Nature, 402, 371, 10.1038/46466 Tsukamoto, 2008, Autophagy is essential for preimplantation development of mouse embryos, Science, 321, 117, 10.1126/science.1154822 Tsukamoto, 2008, The role of autophagy during the oocyte-to-embryo transition, Autophagy, 4, 1076, 10.4161/auto.7065 Kim, 2016, The role of Rad51 in safeguarding mitochondrial activity during the meiotic cell cycle in mammalian oocytes, Sci. Rep., 6 Rojas-Ríos, 2015, Translational control of autophagy by orb in the drosophila germline, Dev. Cell, 35, 622, 10.1016/j.devcel.2015.11.003 Vilser, 2010, The variable expression of lectin-like oxidized low-density lipoprotein receptor (LOX-1) and signs of autophagy and apoptosis in freshly harvested human granulosa cells depend on gonadotropin dose, age, and body weight, Fertil. Steril., 93, 2706, 10.1016/j.fertnstert.2009.02.038 Pikó, 1987, Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos, Dev. Biol., 123, 364, 10.1016/0012-1606(87)90395-2 Van Blerkom, 2002, Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos, Hum. Reprod., 17, 393, 10.1093/humrep/17.2.393 Van Blerkom, 2003, Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes, Hum. Reprod., 18, 2429, 10.1093/humrep/deg466 Van Blerkom, 2006, High-polarized (Delta Psi m(HIGH)) mitochondria are spatially polarized in human oocytes and early embryos in stable subplasmalemmal domains: developmental significance and the concept of vanguard mitochondria, Reprod. Biomed. Online, 13, 246, 10.1016/S1472-6483(10)60622-0 Peral-Sanchez, 2021, Epigenetics in the uterine environment: how maternal diet and ART may influence the epigenome in the offspring with long-term health consequences, Genes (Basel), 13, 10.3390/genes13010031 Hou, 2016, Both diet and gene mutation induced obesity affect oocyte quality in mice, Sci. Rep., 6 Han, 2018, Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes - PubMed, Nat. Genet., 432, 10.1038/s41588-018-0055-6 Penn, 2023, Maternal high-fat diet changes DNA methylation in the early embryo by disrupting the TCA cycle intermediary alpha ketoglutarate, Reproduction, 165, 347, 10.1530/REP-22-0302 Ou, 2019, Effects of obesity and diabetes on the epigenetic modification of mammalian gametes, J. Cell Physiol., 234, 7847, 10.1002/jcp.27847 McRorie, 2017, Understanding the physics of functional fibers in the gastrointestinal tract: an evidence-based approach to resolving enduring misconceptions about insoluble and soluble fiber, J. Acad. Nutr. Diet., 117, 251, 10.1016/j.jand.2016.09.021 Probst, 2017, Dietary phytochemical intake from foods and health outcomes: a systematic review protocol and preliminary scoping, BMJ Open, 7, 10.1136/bmjopen-2016-013337 Fraga, 2019, The effects of polyphenols and other bioactives on human health, Food Funct., 10, 514, 10.1039/C8FO01997E Li, 2016, Fruit and vegetables consumption and risk of hypertension: a meta-analysis, J. Clin. Hypertens. (Greenwich), 18, 468, 10.1111/jch.12777 Zhan, 2017, Fruit and vegetable consumption and risk of cardiovascular disease: a meta-analysis of prospective cohort studies, Crit. Rev. Food Sci. Nutr., 57, 1650, 10.1080/10408398.2015.1008980 Kaluza, 2017, Fruit and vegetable consumption and risk of COPD: a prospective cohort study of men, Thorax, 72, 500, 10.1136/thoraxjnl-2015-207851 Appel, 1997, A clinical trial of the effects of dietary patterns on blood pressure. DASH Collaborative Research Group, N. Engl. J. Med., 336, 1117, 10.1056/NEJM199704173361601 Marcason, 2015, What are the components to the MIND diet?, J. Acad. Nutr. Diet., 115, 1744, 10.1016/j.jand.2015.08.002 Price, 2019, Preconception management of women with obesity: a systematic review, Obes. Rev, 20, 510, 10.1111/obr.12804 Lassi, 2014, Preconception care: delivery strategies and packages for care, Reprod. Health, 11 J, 2014, 2013 AHA/ACC/TOS guideline for the management of overweight and obesity in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society, Circulation, 129 Reynolds, 2015, Adverse effects of obesity and/or high-fat diet on oocyte quality and metabolism are not reversible with resumption of regular diet in mice, Reprod. Fertil. Dev., 27, 716, 10.1071/RD14251 Smits, 2022, Obese outbred mice only partially benefit from diet normalization or calorie restriction as preconception care interventions to improve metabolic health and oocyte quality, Hum. Reprod., 37, 2867, 10.1093/humrep/deac226 Jia, 2018, Resveratrol reverses the adverse effects of a diet-induced obese murine model on oocyte quality and zona pellucida softening, Food Funct., 9, 2623, 10.1039/C8FO00149A Mutsaerts, 2013, Dropout is a problem in lifestyle intervention programs for overweight and obese infertile women: a systematic review, Hum. Reprod., 28, 979, 10.1093/humrep/det026 Smits, 2021, Diet normalization or caloric restriction as a preconception care strategy to improve metabolic health and oocyte quality in obese outbred mice, Reprod. Biol. Endocrinol., 19, 10.1186/s12958-021-00848-4 Eryilmaz, 2011, Melatonin improves the oocyte and the embryo in IVF patients with sleep disturbances, but does not improve the sleeping problems, J. Assist. Reprod. Genet., 28, 815, 10.1007/s10815-011-9604-y Zhao, 2019, Benefits of vitamins in the treatment of Parkinson’s disease, Oxid. Med. Cell. Longev., 2019, 10.1155/2019/9426867 Reiter, 2018, Mitochondria: central organelles for melatonin’s antioxidant and anti-aging actions, Molecules, 23, 10.3390/molecules23020509 Yeung, 2015, Coenzyme Q10 dose-escalation study in hemodialysis patients: safety, tolerability, and effect on oxidative stress, BMC Nephrol., 16, 10.1186/s12882-015-0178-2 Showell, 2017, Antioxidants for female subfertility, Cochrane Database Syst. Rev., 7, 1 Showell, 2020, Antioxidants for female subfertility, Cochrane Database Syst. Rev., 8 Sasaki, 2019, Impact of oxidative stress on age-associated decline in oocyte developmental competence, Front. Endocrinol. (Lausanne), 10, 10.3389/fendo.2019.00811 Florou, 2020, Does coenzyme Q10 supplementation improve fertility outcomes in women undergoing assisted reproductive technology procedures? A systematic review and meta-analysis of randomized-controlled trials, J. Assist. Reprod. Genet., 37, 2377, 10.1007/s10815-020-01906-3 Boots, 2016, Obesity-induced oocyte mitochondrial defects are partially prevented and rescued by supplementation with co-enzyme Q10 in a mouse model, Hum. Reprod., 31, 2090, 10.1093/humrep/dew181 Price, 2012, SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function, Cell Metab., 15, 675, 10.1016/j.cmet.2012.04.003 Liu, 2013, Resveratrol protects against age-associated infertility in mice, Hum. Reprod., 28, 707, 10.1093/humrep/des437 Chastang, 2018, Resveratrol production by grapevine cells in fed-batch bioreactor: Experiments and modelling, Biochem. Eng. J., 131, 9, 10.1016/j.bej.2017.12.009 Cabello, 2015, Effects of resveratrol on ovarian response to controlled ovarian hyperstimulation in ob/ob mice, Fertil. Steril., 103, 570, 10.1016/j.fertnstert.2014.10.034 Schube, 2014, Resveratrol and desferoxamine protect human OxLDL-treated granulosa cell subtypes from degeneration, J. Clin. Endocrinol. Metab., 99, 229, 10.1210/jc.2013-2692 Codd, 2018, Advances in the chemical biology of Desferrioxamine B, ACS Chem. Biol., 13, 11, 10.1021/acschembio.7b00851 Lan, 2018, Melatonin protects against defects induced by deoxynivalenol during mouse oocyte maturation, J. Pineal. Res., 65, 10.1111/jpi.12477 Li, 2020, Melatonin ameliorates the advanced maternal age-associated meiotic defects in oocytes through the SIRT2-dependent H4K16 deacetylation pathway, Aging, 12, 1610, 10.18632/aging.102703 Manchester, 2015, Melatonin: an ancient molecule that makes oxygen metabolically tolerable, J. Pineal. Res., 59, 403, 10.1111/jpi.12267 Zhang, 2014, Melatonin: a well-documented antioxidant with conditional pro-oxidant actions, J. Pineal. Res., 57, 131, 10.1111/jpi.12162 Han, 2017, Melatonin protects against maternal obesity-associated oxidative stress and meiotic defects in oocytes via the SIRT3-SOD2-dependent pathway, J. Pineal. Res., 63, 10.1111/jpi.12431 Wen, 2020, Phycocyanin improves reproductive ability in obese female mice by restoring ovary and oocyte quality, Front. Cell Dev. Biol., 8, 10.3389/fcell.2020.595373 Wang, 2021, NAMPT reduction-induced NAD+ insufficiency contributes to the compromised oocyte quality from obese mice, Aging Cell, 20, 10.1111/acel.13496 Wang, 2022, Administration of nicotinamide mononucleotide improves oocyte quality of obese mice, Cell Prolif., 55, 10.1111/cpr.13303 Hohos, 2020, High-fat diet-induced dysregulation of ovarian gene expression is restored with chronic omega-3 fatty acid supplementation, Mol. Cell. Endocrinol., 499, 10.1016/j.mce.2019.110615 Kala, 2016, Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation, Reprod. Med. Biol., 16, 28, 10.1002/rmb2.12013 Bradley, 2008, Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice, Am. J. Physiol. - Endocrinol. Metab., 295, 10.1152/ajpendo.00309.2007 Carter, 2013, Maternal exercise improves insulin sensitivity in mature rat offspring, Med. Sci. Sports Exerc., 45, 832, 10.1249/MSS.0b013e31827de953 Wagener, 2012, Early and late onset of voluntary exercise have differential effects on the metabolic syndrome in an obese mouse model, Exp. Clin. Endocrinol. Diabetes, 120, 591, 10.1055/s-0032-1321727 Evenson, 2014, Association of physical activity in the past year and immediately after in vitro fertilization on pregnancy, Fertil. Steril., 101, 10.1016/j.fertnstert.2013.12.041 McKinnon, 2016, Body mass index, physical activity and fecundability in a North American preconception cohort study, Fertil. Steril., 106, 451, 10.1016/j.fertnstert.2016.04.011 Wise, 2012, A prospective cohort study of physical activity and time to pregnancy, Fertil. Steril., 97, 10.1016/j.fertnstert.2012.02.025 Warren, 2001, The effects of intense exercise on the female reproductive system, J. Endocrinol., 170, 3, 10.1677/joe.0.1700003 Lee, 2020, Determining the association between physical activity prior to conception and pregnancy rate: a systematic review and meta-analysis of prospective cohort studies, Health Care Women Int., 41, 38, 10.1080/07399332.2019.1640701 Sloboda, 2009, Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat, PLoS One, 4, 10.1371/journal.pone.0006744 Bertoldo, 2018, Multigenerational obesity-induced perturbations in oocyte-secreted factor signalling can be ameliorated by exercise and nicotinamide mononucleotide, Hum. Reprod. Open, 2018, 10.1093/hropen/hoy010 Dunning, 2014, Regulation of fatty acid oxidation in mouse cumulus-oocyte complexes during maturation and modulation by PPAR agonists, PLoS One, 9, 10.1371/journal.pone.0087327 Minge, 2008, Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality, Endocrinology, 149, 2646, 10.1210/en.2007-1570