Maternal swimming with overload allied to postnatal high-fat, high-sugar diet induce subtle impairment on rat offspring’s ovarian redox homeostasis
Bárbara Mariño Dal Magro A , Bernardo Gindri dos Santos A , Pauline Maciel August B , Manuela Zeferino Menegotto A , David Driemeier C and Cristiane Matté A B *A
B
C
Abstract
The Developmental Origins of Health and Disease (DOHaD) concept suggests that early-life interventions significantly influence the long-term health outcomes of offspring. Emerging evidence supports that maternal physical exercise and balanced nutrition can positively impact the health of the next generation.
This study investigated the effects of maternal swimming combined with postnatal high-fat, high-sugar (HFHS) diet on the ovarian health of adult female Wistar rat offspring.
Adult female Wistar rats performed swimming exercise in a controlled temperature environment (32°C, 2% bodyweight overload adjusted daily) during 4 weeks, starting 1 week prior mating. The female offspring received a control or HFHS diet from postnatal day (PND) 21 to PND 90. We analyzed offspring’s body weight, ovarian histomorphology, redox status, and associated molecular pathways 5′ adenosine monophosphate-activated protein kinase (AMPKα), forkhead box O3 (FoxO3), and mitofusin 1 (Mfn-1).
Our findings reveal that maternal swimming exerted an effect on offspring body weight gain, delaying it. Individually, maternal exercise reduced superoxide dismutase (SOD) activity and mitofusin-1 levels, while the postnatal HFHS diet alone decreased both SOD and glutathione peroxidase (GPx) activities and increased the pFOXO3a/FOXO3a ratio in the ovaries.
We showed that combination of maternal swimming with a 2% overload and a postnatal HFHS diet can negatively affect the ovarian redox balance in offspring.
Prenatal and postnatal lifestyle might affect reproductive function in females.
Keywords: antioxidant, DOHaD, high fat high sugar diet, maternal exercise, ovary, rat, redox signalling, redox status.
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121-126.
| Crossref | Google Scholar | PubMed |
Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S (2012) The effects of oxidative stress on female reproduction: a review. Reproductive Biology and Endocrinology 10, 49.
| Crossref | Google Scholar |
Akamine EH, Marçal AC, Camporez JP, Hoshida MS, Caperuto LC, Bevilacqua E, Carvalho CR (2010) Obesity induced by high-fat diet promotes insulin resistance in the ovary. Journal of Endocrinology 206(1), 65.
| Crossref | Google Scholar | PubMed |
Amstad P, Peskin A, Shah G, Mirault ME, Moret R, Zbinden I, Cerutti P (1991) The balance between copper-zinc superoxide dismutase and catalase affects the sensitivity of mouse epidermal cells to oxidative stress. Biochemistry 30(38), 9305-9313.
| Crossref | Google Scholar | PubMed |
August PM, Hözer R, Rodrigues KS, Dos Santos BG, Maurmann RM, Scortegagna MC, Matté C (2020) Effect of maternal exercise on diet-induced redox imbalance in hippocampus of adult offspring. Neuroscience 437, 196-206.
| Crossref | Google Scholar | PubMed |
Barker DJP (2007) The origins of the developmental origins theory. Journal of Internal Medicine 261(5), 412-417.
| Crossref | Google Scholar | PubMed |
Barker DJ, Osmond C (1986a) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. The Lancet 327(8489), 1077-1081.
| Crossref | Google Scholar |
Barker DJ, Osmond C (1986b) Diet and coronary heart disease in England and Wales during and after the second world war. Journal of Epidemiology & Community Health 40(1), 37-44.
| Crossref | Google Scholar | PubMed |
Barker DJP, Osmond C, Winter PD, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. The Lancet 334(8663), 577-580.
| Crossref | Google Scholar |
Bianchi C, Battini L, Aragona M, Lencioni C, Ottanelli S, Romano M, Calabrese M, Cuccuru I, De Bellis A, Mori ML, Leopardi A, Sabbatini G, Bottone P, Miccoli R, Trojano G, Salerno MG, Del Prato S, Bertolotto A, on behalf of Tuscany working group on “Diabetes, Pregnancy and Exercise”* (2017) Prescribing exercise for prevention and treatment of gestational diabetes: review of suggested recommendations. Gynecological Endocrinology 33(4), 254-260.
| Crossref | Google Scholar |
Browne RW, Armstrong D (1998) Reduced glutathione and glutathione disulfide. Methods in Molecular Biology (Clifton, N.J.) 108, 347-352.
| Crossref | Google Scholar |
Carbone MC, Tatone C, Delle Monache S, Marci R, Caserta D, Colonna R, Amicarelli F (2003) Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Molecular Human Reproduction 9(11), 639-643.
| Crossref | Google Scholar | PubMed |
Carrera-Bastos P, Fontes-Villalba M, O’Keefe JH, Lindeberg S, Cordain L (2011) The western diet and lifestyle and diseases of civilization. Research Reports in Clinical Cardiology 2, 15-35.
| Google Scholar |
Chiang JL, Shukla P, Pagidas K, Ahmed NS, Karri S, Gunn DD, Hurd WW, Singh KK (2020) Mitochondria in ovarian aging and reproductive longevity. Ageing Research Reviews 63, 101168.
| Crossref | Google Scholar | PubMed |
Chinkin AS (2013) The effects of various swimming training protocols on cardiac capacity and ventricular fibrillation threshold in rats. Central European Journal of Sport Sciences and Medicine 2, 9-14.
| Google Scholar |
Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, Watkins BA, O’Keefe JH, Brand-Miller J (2005) Origins and evolution of the western diet: health implications for the 21st century1,2. The American Journal of Clinical Nutrition 81(2), 341-354.
| Crossref | Google Scholar | PubMed |
Coughlan KA, Valentine RJ, Ruderman NB, Saha AK (2014) AMPK activation: a therapeutic target for type 2 diabetes? Diabetes, Metabolic Syndrome and Obesity : Targets and Therapy 7, 241-253.
| Crossref | Google Scholar |
Cristiano F, de Haan JB, Iannello RC, Kola I (1995) Changes in the levels of enzymes which modulate the antioxidant balance occur during aging and correlate with cellular damage. Mechanisms of Ageing and Development 80(2), 93-105.
| Crossref | Google Scholar | PubMed |
Dal Magro BM, Stone V, Klein CP, Maurmann RM, Saccomori AB, Dos Santos BG, August PM, Rodrigues KS, Conrado L, de Sousa FAB, Dreimeier D, Mello F, Matté C (2020) Developmental programming: intrauterine caloric restriction promotes upregulation of mitochondrial sirtuin with mild effects on oxidative parameters in the ovaries and testes of offspring. Reproduction, Fertility and Development 32(8), 763-773.
| Crossref | Google Scholar | PubMed |
de Haan JB, Cristiano F, Iannello R, Bladier C, Kelner MJ, Kola I (1996) Elevation in the ratio of Cu/Zn-superoxide dismutase to glutathione peroxidase activity induces features of cellular senescence and this effect is mediated by hydrogen peroxide. Human Molecular Genetics 5(2), 283-292.
| Crossref | Google Scholar | PubMed |
de Melo GB, Soares JF, Costa TCL, Benevides ROA, Vale CC, Paes AMdA, Gaspar RS (2021) Early exposure to high-sucrose diet leads to deteriorated ovarian health. Frontiers in Endocrinology 12, 656831.
| Crossref | Google Scholar |
Falone S, Santini S, Jr, Cordone V, Grannonico M, Cacchio M, Di Emidio G, Tatone C, Amicarelli F (2016) Regular and moderate exercise counteracts the decline of antioxidant protection but not methylglyoxal-dependent glycative burden in the ovary of reproductively aging mice. Oxidative Medicine and Cellular Longevity 2016, 3837623.
| Crossref | Google Scholar | PubMed |
Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M (1997) A maternal diet high in n - 6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proceedings of the National Academy of Sciences of the United States of America 94(17), 9372-9377.
| Crossref | Google Scholar |
Hsueh AJW, Kawamura K, Cheng Y, Fauser BCJM (2015) Intraovarian control of early folliculogenesis. Endocrine Reviews 36(1), 1-24.
| Crossref | Google Scholar | PubMed |
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine 54(4), 287-293.
| Crossref | Google Scholar |
Jang H, Lee O-H, Lee Y, Yoon H, Chang EM, Park M, Lee J-W, Hong K, Kim JO, Kim NK, Ko JJ, Lee DR, Yoon TK, Lee WS, Choi Y (2016) Melatonin prevents cisplatin-induced primordial follicle loss via suppression of PTEN/AKT/FOXO3a pathway activation in the mouse ovary. Journal of Pineal Research 60(3), 336-347.
| Crossref | Google Scholar | PubMed |
Jazwiec PA, Sloboda DM (2019) Nutritional adversity, sex and reproduction: 30 years of DOHaD and what have we learned? Journal of Endocrinology 242(1), T51-T68.
| Crossref | Google Scholar | PubMed |
Kaminski SL, Grazul-Bilska AT, Harris EK, Berg EP, Vonnahme KA (2014) Impact of maternal physical activity during gestation on porcine fetal, neonatal, and adolescent ovarian development. Domestic Animal Endocrinology 48, 56-61.
| Crossref | Google Scholar | PubMed |
Klein CP, Dos Santos Rodrigues K, Hözer RM, de Sá Couto-Pereira N, Saccomori AB, Dal Magro BM, Crestani MS, Hoppe JB, Salbego CG, Dalmaz C, Matté C (2018) Swimming exercise before and during pregnancy: promising preventive approach to impact offspring’s health. International Journal of Developmental Neuroscience 71(1), 83-93.
| Crossref | Google Scholar |
Kopp W (2019) How western diet and lifestyle drive the pandemic of obesity and civilization diseases. Diabetes, Metabolic Syndrome and Obesity : Targets and Therapy 12, 2221-2236.
| Crossref | Google Scholar |
Liu K, Rajareddy S, Liu L, Jagarlamudi K, Boman K, Selstam G, Reddy P (2006) Control of mammalian oocyte growth and early follicular development by the oocyte PI3 kinase pathway: new roles for an old timer. Developmental Biology 299(1), 1-11.
| Crossref | Google Scholar | PubMed |
Liu H, Luo L-L, Qian Y-S, Fu Y-C, Sui X-X, Geng Y-J, Huang D-N, Gao S-T, Zhang R-L (2009) FOXO3a is involved in the apoptosis of naked oocytes and oocytes of primordial follicles from neonatal rat ovaries. Biochemical and Biophysical Research Communications 381(4), 722-727.
| Crossref | Google Scholar | PubMed |
Marcelino TB, Longoni A, Kudo KY, Stone V, Rech A, de Assis AM, Scherer EBS, da Cunha MJ, Wyse ATS, Pettenuzzo LF, Leipnitz G, Matté C (2013) Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats. Neuroscience 246, 28-39.
| Crossref | Google Scholar | PubMed |
Marcelino TB, de Lemos Rodrigues PI, Klein CP, Santos BGD, Miguel PM, Netto CA, Silva LOP, Matté C (2016) Behavioral benefits of maternal swimming are counteracted by neonatal hypoxia-ischemia in the offspring. Behavioural Brain Research 312, 30-38.
| Crossref | Google Scholar | PubMed |
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. The Journal of Biological Chemistry 247(10), 3170-3175.
| Crossref | Google Scholar | PubMed |
Mittendorfer B (2011) Origins of metabolic complications in obesity: adipose tissue and free fatty acid trafficking. Current Opinion in Clinical Nutrition and Metabolic Care 14(6), 535-541.
| Crossref | Google Scholar | PubMed |
National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011) ‘Guide for the care and use of laboratory animals.’ (National Academies Press (US): Washington (DC)) Available at http://www.ncbi.nlm.nih.gov/books/NBK54050/
OECD (2009) ‘Guidance document for histologic evaluation of endocrine and reproductive tests in rodents.’ (OECD) 10.1787/cd68c07d-en
Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ (1993) Early growth and death from cardiovascular disease in women. British Medical Journal 307, 1519.
| Crossref | Google Scholar |
Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Analytical Biochemistry 83(2), 346-356.
| Crossref | Google Scholar |
Prather H, Spitznagle T, Hunt D (2012) Benefits of exercise during pregnancy. PM & R : The Journal of Injury, Function, and Rehabilitation 4(11), 845-850.
| Crossref | Google Scholar | PubMed |
Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293(5532), 1089-1093.
| Crossref | Google Scholar | PubMed |
Reynolds KA, Boudoures AL, Chi MM-Y, Wang Q, Moley KH (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. Reproduction, Fertility and Development 27(4), 716-724.
| Crossref | Google Scholar | PubMed |
Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in Enzymology 233, 357-363.
| Crossref | Google Scholar | PubMed |
Roberts JS, Perets RA, Sarfert KS, Bowman JJ, Ozark PA, Whitworth GB, Blythe SN, Toporikova N (2017) High-fat high-sugar diet induces polycystic ovary syndrome in a rodent model. Biology of Reproduction 96(3), 551-562.
| Crossref | Google Scholar | PubMed |
Ruderman NB, Carling D, Prentki M, Cacicedo JM (2013) AMPK, insulin resistance, and the metabolic syndrome. The Journal of Clinical Investigation 123(7), 2764-2772.
| Crossref | Google Scholar | PubMed |
Sadowska J, Dudzińska W, Skotnicka E, Sielatycka K, Daniel I (2019) The impact of a diet containing sucrose and systematically repeated starvation on the oxidative status of the uterus and ovary of rats. Nutrients 11(7), 1544.
| Crossref | Google Scholar | PubMed |
Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N (2011) Reactive oxygen species are indispensable in ovulation. Proceedings of the National Academy of Sciences 108(4), 1462-1467.
| Crossref | Google Scholar |
Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends in Endocrinology & Metabolism 21(4), 214-222.
| Crossref | Google Scholar | PubMed |
Sonigo C, Beau I, Grynberg M, Binart N (2019) AMH prevents primordial ovarian follicle loss and fertility alteration in cyclophosphamide-treated mice. The FASEB Journal 33, 1278-1287.
| Crossref | Google Scholar |
Stone V, Kudo KY, Marcelino TB, August PM, Matté C (2015) Swimming exercise enhances the hippocampal antioxidant status of female wistar rats. Redox Report 20(3), 133-138.
| Crossref | Google Scholar |
Stone V, August PM, Stocher DP, Klein CP, Couto PRG, Silva YD, Sagini JP, Salomon TB, Benfato MS, Matté C (2016) Food restriction during pregnancy alters brain’s antioxidant network in dams and their offspring. Free Radical Research 50(5), 530-541.
| Crossref | Google Scholar | PubMed |
Stone V, Crestani MS, Saccomori AB, Mariño Dal Magro B, Maurmann RM, August PM, Dos Santos BG, Klein CP, Hackenhaar FS, da Silveira Benfato M, Matté C (2019) Gestational caloric restriction improves redox homeostasis parameters in the brain of Wistar rats: a screening from birth to adulthood. The Journal of Nutritional Biochemistry 67, 138-148.
| Crossref | Google Scholar | PubMed |
Stone V, Maurmann RM, Dal Magro BM, Crestani MS, Hozer RM, Klein CP, Matté C (2021) Gestational caloric restriction with micronutrients supplementation does not delay development and promotes feeding behavior benefits. Nutritional Neuroscience 24(10), 770-780.
| Crossref | Google Scholar | PubMed |
Şükür YE, Kıvançlı İB, Özmen B (2014) Ovarian aging and premature ovarian failure. Journal of the Turkish German Gynecological Association 15(3), 190-196.
| Crossref | Google Scholar | PubMed |
Sun C, Velazquez MA, Fleming TP (2016) DOHaD and the periconceptional period, a critical window in time. In ‘The epigenome and developmental origins of health and disease’. (Ed. CS Rosenfeld) pp. 33–47. (Elsevier) 10.1016/B978-0-12-801383-0.00003-7
Suzuki K (2018) The developing world of DOHaD. Journal of Developmental Origins of Health and Disease 9(3), 266-269.
| Crossref | Google Scholar | PubMed |
Thornalley PJ, Tisdale MJ (1988) Inhibition of proliferation of human promyelocytic leukaemia HL60 cells by S-d-lactoylglutathione in vitro. Leukemia Research 12, 897-904.
| Crossref | Google Scholar | PubMed |
Udagawa O, Ishihara T, Maeda M, Matsunaga Y, Tsukamoto S, Kawano N, Miyado K, Shitara H, Yokota S, Nomura M, Mihara K, Mizushima N, Ishihara N (2014) Mitochondrial fission factor Drp1 maintains oocyte quality via dynamic rearrangement of multiple organelles. Current Biology 24(20), 2451-2458.
| Crossref | Google Scholar | PubMed |
Vega CC, Reyes-Castro LA, Bautista CJ, Larrea F, Nathanielsz PW, Zambrano E (2015) Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. International Journal of Obesity 39, 712-719.
| Crossref | Google Scholar |
Volk KM, Pogrebna VV, Roberts JA, Zachry JE, Blythe SN, Toporikova N (2017) High-fat, high-sugar diet disrupts the preovulatory hormone surge and induces cystic ovaries in cycling female rats. Journal of the Endocrine Society 1(12), 1488-1505.
| Crossref | Google Scholar | PubMed |
Wallack L, Thornburg K (2016) Developmental origins, epigenetics, and equity: moving upstream. Maternal and Child Health Journal 20(5), 935-940.
| Crossref | Google Scholar | PubMed |
Wasinski F, Bacurau RFP, Estrela GR, Klempin F, Arakaki AM, Batista RO, Mafra FFP, do Nascimento LFR, Hiyane MI, Velloso LA, Câmara NOS, Araujo RC (2015) Exercise during pregnancy protects adult mouse offspring from diet-induced obesity. Nutrition & Metabolism 12, 56.
| Crossref | Google Scholar |
Wendel A (1981) Glutathione peroxidase. Methods in Enzymology 77, 325-333.
| Crossref | Google Scholar | PubMed |
Willows R, Sanders MJ, Xiao B, Patel BR, Martin SR, Read J, Wilson JR, Hubbard J, Gamblin SJ, Carling D (2017) Phosphorylation of AMPK by upstream kinases is required for activity in mammalian cells. Biochemical Journal 474(17), 3059-3073.
| Crossref | Google Scholar | PubMed |
Yan S, Wang F, Shi Q (2020) The effect of maternal high-fat-diet mediated oxidative stress on ovarian function in mice offspring. Experimental and Therapeutic Medicine 20(6), 135.
| Crossref | Google Scholar | PubMed |
Zhang M, Bener MB, Jiang Z, Wang T, Esencan E, Scott III R, Horvath T, Seli E (2019) Mitofusin 1 is required for female fertility and to maintain ovarian follicular reserve. Cell Death & Disease 10, 560.
| Crossref | Google Scholar | PubMed |