Developmental programming: intrauterine caloric restriction promotes upregulation of mitochondrial sirtuin with mild effects on oxidative parameters in the ovaries and testes of offspring
B. M. Dal Magro A , V. Stone B , C. P. Klein B , R. M. Maurmann A , A. B. Saccomori A , B. G. dos Santos B , P. M. August B , K. S. Rodrigues B , L. Conrado A , F. A. B. de Sousa C , D. Dreimeier D , F. Mello E and C. Matté
A B F G
+ Author Affiliations
- Author Affiliations
A Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos, 2600-Prédio Anexo, Floresta, Porto Alegre, RS, 90035-003, Brazil.
B Programa de Pós-graduação em Ciências Biológicas: Bioquímica, Instituto de Ciências, Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos, 2600-Prédio Anexo, Floresta, Porto Alegre, RS, 90035-003, Brazil.
C Hospital de Clínicas Veterinárias, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, Agronomia, Porto Alegre, RS, 90650-001, Brazil.
D Setor de Anatomia Patológica Veterinária, Departamento de Patologia Clínica Veterinária, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, Agronomia, Porto Alegre, RS, 90650-001, Brazil.
E Centro de Reprodução e Experimentação Animal, Universidade Federal do Rio Grande do Sul, Campus do Vale, Prédio 43.300, Agronomia, RS, 91509-900, Brazil.
F Programa de Pós-graduação em Ciências Biológicas: Fisiologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, R. Sarmento Leite, n° 500, Farroupilha, Porto Alegre, RS, 90050-170, Brazil.
G Corresponding author. Email: matte@ufrgs.br
Reproduction, Fertility and Development 32(8) 763-773 https://doi.org/10.1071/RD19384
Submitted: 5 October 2019 Accepted: 20 January 2020 Published: 22 April 2020
Abstract
According to the developmental origins of health and disease (DOHaD) hypothesis, changes in the maternal environment are known to reprogram the metabolic response of offspring. Known for its redox modulation, caloric restriction extends the lifespan of some species, which contributes to diminished cellular damage. Little is known about the effects of gestational caloric restriction, in terms of antioxidant parameters and molecular mechanisms of action, on the reproductive organs of offspring. This study assessed the effects of moderate (20%) caloric restriction on redox status parameters, molecular expression of sirtuin (SIRT) 1 and SIRT3 and histopathological markers in the ovaries and testes of adult rats that were subjected to gestational caloric restriction. Although enzyme activity was increased, ovaries from female pups contained high levels of oxidants, whereas testes from male pups had decreased antioxidant enzyme defences, as evidenced by diminished glyoxalase I activity and reduced glutathione content. Expression of SIRT3, a deacetylase enzyme related to cellular bioenergetics, was increased in both ovaries and testes. Previous studies have suggested that, in ovaries, diminished antioxidant metabolism can lead to premature ovarian failure. Unfortunately, there is little information regarding the redox profile in the testis. This study is the first to assess the redox network in both ovaries and testes, suggesting that, although intrauterine caloric restriction improves molecular mechanisms, it has a negative effect on the antioxidant network and redox status of reproductive organs of young adult rats.
Additional keywords: early development, environment, mitochondria, nutrition, oxidative stress, pregnancy.
References
Aebi, H. (1984). Catalase in vitro. Methods Enzymol. 105, 121–126.| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |
Agale, S., Kulkarni, A., Ranjekar, P., and Joshi, S. (2010). Maternal caloric restriction spares fetal brain polyunsaturated fatty acids in Wistar rats. Brain Dev. 32, 123–129.
| Maternal caloric restriction spares fetal brain polyunsaturated fatty acids in Wistar rats.Crossref | GoogleScholarGoogle Scholar | 19128907PubMed |
Agarwal, A., Gupta, S., and Sharma, R. K. (2005). Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 3, 28.
| Role of oxidative stress in female reproduction.Crossref | GoogleScholarGoogle Scholar | 16018814PubMed |
Agarwal, A., Aponte-Mellado, A., Premkumar, B. J., Shaman, A., and Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reprod. Biol. Endocrinol. 10, 49.
| The effects of oxidative stress on female reproduction: a review.Crossref | GoogleScholarGoogle Scholar | 22748101PubMed |
Aitken, R. J., Gibb, Z., Baker, M. A., Drevet, J., and Gharagozloo, P. (2016). Causes and consequences of oxidative stress in spermatozoa. Reprod. Fertil. Dev. 28, 1–10.
| Causes and consequences of oxidative stress in spermatozoa.Crossref | GoogleScholarGoogle Scholar | 27062870PubMed |
Aksenov, M. Y., and Markesbery, W. R. (2001). Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci. Lett. 302, 141–145.
| Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease.Crossref | GoogleScholarGoogle Scholar | 11290407PubMed |
Allaman, I., Bélanger, M., and Magistretti, P. J. (2015). Methylglyoxal, the dark side of glycolysis. Front. Neurosci. 9, 23.
| Methylglyoxal, the dark side of glycolysis.Crossref | GoogleScholarGoogle Scholar | 25709564PubMed |
Allard, J. S., Perez, E., Zou, S., and De Cabo, R. (2009). Dietary activators of Sirt1. Mol. Cell. Endocrinol. 299, 58–63.
| Dietary activators of Sirt1.Crossref | GoogleScholarGoogle Scholar | 19010386PubMed |
Bansal, A. K., and Bilaspuri, G. (2010). Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 2011, 686137.
| Impacts of oxidative stress and antioxidants on semen functions.Crossref | GoogleScholarGoogle Scholar |
Behrman, H. R., Kodaman, P. H., Preston, S. L., and Gao, S. (2001). Oxidative stress and the ovary. J. Soc. Gynecol. Investig. 8, S40.
| 11223371PubMed |
Birben, E., Sahiner, U. M., Sackesen, C., Erzurum, S., and Kalayci, O. (2012). Oxidative stress and antioxidant defense. World Allergy Organ J. 5, 9–19.
| Oxidative stress and antioxidant defense.Crossref | GoogleScholarGoogle Scholar | 23268465PubMed |
Bordone, L., Cohen, D., Robinson, A., Motta, M. C., van Veen, E., Czopik, A., Steele, A. D., Crowe, H., Marmor, S., Luo, J., Gu, W., and Guarente, L. (2007). SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6, 759–767.
| SIRT1 transgenic mice show phenotypes resembling calorie restriction.Crossref | GoogleScholarGoogle Scholar | 17877786PubMed |
Browne, R. W., and Armstrong, D. (1998). Reduced glutathione and glutathione disulfide. Methods Mol. Biol. 108, 347–352.
| 9921543PubMed |
Buffenstein, R., Edrey, Y. H., Yang, T., and Mele, J. (2008). The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age (Dordr.) 30, 99–109.
| The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms.Crossref | GoogleScholarGoogle Scholar | 19424860PubMed |
Burger, H. G., Dudley, E. C., Robertson, D. M., and Dennerstein, L. (2002). Hormonal changes in the menopause transition. Recent Prog. Horm. Res. 57, 257–275.
| Hormonal changes in the menopause transition.Crossref | GoogleScholarGoogle Scholar | 12017547PubMed |
Canadian Council on Animal Care (1993) ‘Guide to the care and use of experimental animals.’ (Canadian Council on Animal Care: Ontario.)
Cerqueira, F. M., Cunha, F. M., Laurindo, F. R., and Kowaltowski, A. J. (2012). Calorie restriction increases cerebral mitochondrial respiratory capacity in a NO•-mediated mechanism: impact on neuronal survival. Free Radic. Biol. Med. 52, 1236–1241.
| Calorie restriction increases cerebral mitochondrial respiratory capacity in a NO•-mediated mechanism: impact on neuronal survival.Crossref | GoogleScholarGoogle Scholar | 22310960PubMed |
Colman, R. J., Beasley, T. M., Kemnitz, J. W., Johnson, S. C., Weindruch, R., and Anderson, R. M. (2014). Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat. Commun. 5, 3557.
| Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 24691430PubMed |
National Research Council (2010) ‘Guide for the care and use of laboratory animals.’ (National Academies Press)
Coussens, M., Maresh, J. G., Yanagimachi, R., Maeda, G., and Allsopp, R. (2008). Sirt1 deficiency attenuates spermatogenesis and germ cell function. PLoS One 3, e1571.
| Sirt1 deficiency attenuates spermatogenesis and germ cell function.Crossref | GoogleScholarGoogle Scholar | 18270565PubMed |
Crain, D. A., Janssen, S. J., Edwards, T. M., Heindel, J., Ho, S. M., Hunt, P., Iguchi, T., Juul, A., McLachlan, J. A., Schwartz, J., Skakkebaek, N., Soto, A. M., Swan, S., Walker, C., Woodruff, T. K., Woodruff, T. J., Giudice, L. C., and Guillette, L. J. (2008). Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil. Steril. 90, 911–940.
| Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing.Crossref | GoogleScholarGoogle Scholar | 18929049PubMed |
Currais, A., and Maher, P. (2013). Functional consequences of age-dependent changes in glutathione status in the brain. Antioxid. Redox Signal. 19, 813–822.
| Functional consequences of age-dependent changes in glutathione status in the brain.Crossref | GoogleScholarGoogle Scholar | 23249101PubMed |
Dang, W. (2014). The controversial world of sirtuins. Drug Discov. Today. Technol. 12, e9–e17.
| The controversial world of sirtuins.Crossref | GoogleScholarGoogle Scholar | 25027380PubMed |
de Bruin, J., Dorland, M., Spek, E., Posthuma, G., Van Haaften, M., Looman, C., and Te Velde, E. (2002). Ultrastructure of the resting ovarian follicle pool in healthy young women. Biol. Reprod. 66, 1151–1160.
| Ultrastructure of the resting ovarian follicle pool in healthy young women.Crossref | GoogleScholarGoogle Scholar | 11906936PubMed |
Ettinger, B., Pressman, A., Sklarin, P., Bauer, D. C., Cauley, J. A., and Cummings, S. R. (1998). Associations between low levels of serum estradiol, bone density, and fractures among elderly women: the study of osteoporotic fractures. J. Clin. Endocrinol. Metab. 83, 2239–2243.
| 9661589PubMed |
Eyre, H., Kahn, R., and Robertson, R. M. (2004). Preventing cancer, cardiovascular disease, and diabetes: a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association. CA Cancer J. Clin. 54, 190–207.
| Preventing cancer, cardiovascular disease, and diabetes: a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association.Crossref | GoogleScholarGoogle Scholar | 15253917PubMed |
Fleury, C., Mignotte, B., and Vayssiere, J. L. (2002). Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84, 131–141.
| Mitochondrial reactive oxygen species in cell death signaling.Crossref | GoogleScholarGoogle Scholar | 12022944PubMed |
Gedik, C. M., Grant, G., Morrice, P. C., Wood, S. G., and Collins, A. R. (2005). Effects of age and dietary restriction on oxidative DNA damage, antioxidant protection and DNA repair in rats. Eur. J. Nutr. 44, 263–272.
| Effects of age and dietary restriction on oxidative DNA damage, antioxidant protection and DNA repair in rats.Crossref | GoogleScholarGoogle Scholar | 15278370PubMed |
Hanson, M. A., and Gluckman, P. (2014). Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol. Rev. 94, 1027–1076.
| Early developmental conditioning of later health and disease: physiology or pathophysiology?Crossref | GoogleScholarGoogle Scholar | 25287859PubMed |
Harman, D. (1956). Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298–300.
| Aging: a theory based on free radical and radiation chemistry.Crossref | GoogleScholarGoogle Scholar | 13332224PubMed |
He, W., Wang, Y., Zhang, M. Z., You, L., Davis, L. S., Fan, H., Yang, H. C., Fogo, A. B., Zent, R., Harris, R. C., Breyer, M. D., and Hao, C. M. (2010). Sirt1 activation protects the mouse renal medulla from oxidative injury. J. Clin. Invest. 120, 1056–1068.
| Sirt1 activation protects the mouse renal medulla from oxidative injury.Crossref | GoogleScholarGoogle Scholar | 20335659PubMed |
Heindel, J. J., Balbus, J., Birnbaum, L., Brune-Drisse, M. N., Grandjean, P., Gray, K., Landrigan, P. J., Sly, P. D., Suk, W., and Slechta, D. C. (2015). Developmental origins of health and disease: integrating environmental influences. Endocrinology 156, 3416–3421.
| Developmental origins of health and disease: integrating environmental influences.Crossref | GoogleScholarGoogle Scholar | 26241070PubMed |
Hirschey, M. D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D. B., Grueter, C. A., Harris, C., Biddinger, S., and Ilkayeva, O. R. (2010). SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464, 121–125.
| SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation.Crossref | GoogleScholarGoogle Scholar | 20203611PubMed |
Hoppe, J. B., Frozza, R. L., Horn, A. P., Comiran, R. A., Bernardi, A., Campos, M. M., Battastini, A. M., and Salbego, C. (2010). Amyloid-beta neurotoxicity in organotypic culture is attenuated by melatonin: involvement of GSK-3beta, tau and neuroinflammation. J. Pineal Res. 48, 230–238.
| Amyloid-beta neurotoxicity in organotypic culture is attenuated by melatonin: involvement of GSK-3beta, tau and neuroinflammation.Crossref | GoogleScholarGoogle Scholar | 20136701PubMed |
Houtkooper, R. H., Canto, C., Wanders, R. J., and Auwerx, J. (2010). The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr. Rev. 31, 194–223.
| The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways.Crossref | GoogleScholarGoogle Scholar | 20007326PubMed |
Imai, S., Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000). Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795–800.
| Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase.Crossref | GoogleScholarGoogle Scholar | 10693811PubMed |
Johansson, H. K. L., Svingen, T., Fowler, P. A., Vinggaard, A. M., and Boberg, J. (2017). Environmental influences on ovarian dysgenesis – developmental windows sensitive to chemical exposures. Nat. Rev. Endocrinol. 13, 400–414.
| Environmental influences on ovarian dysgenesis – developmental windows sensitive to chemical exposures.Crossref | GoogleScholarGoogle Scholar |
Kaneko, T., Iuchi, Y., Kawachiya, S., Fujii, T., Saito, H., Kurachi, H., and Fujii, J. (2001). Alteration of glutathione reductase expression in the female reproductive organs during the estrous cycle. Biol. Reprod. 65, 1410–1416.
| Alteration of glutathione reductase expression in the female reproductive organs during the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 11673257PubMed |
Kanfi, Y., Peshti, V., Gozlan, Y. M., Rathaus, M., Gil, R., and Cohen, H. Y. (2008). Regulation of SIRT1 protein levels by nutrient availability. FEBS Lett. 582, 2417–2423.
| Regulation of SIRT1 protein levels by nutrient availability.Crossref | GoogleScholarGoogle Scholar | 18544345PubMed |
Kim, H. J., Jung, K. J., Yu, B. P., Cho, C. G., Choi, J. S., and Chung, H. Y. (2002). Modulation of redox-sensitive transcription factors by calorie restriction during aging. Mech. Ageing Dev. 123, 1589–1595.
| Modulation of redox-sensitive transcription factors by calorie restriction during aging.Crossref | GoogleScholarGoogle Scholar | 12470896PubMed |
Laloraya, M., and Laloraya, M. M. (1988). Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle of Rattus norvegicus and induction of superoxide dismutase in rat ovary by lutropin. Biochem. Biophys. Res. Commun. 157, 146–153.
| Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle of Rattus norvegicus and induction of superoxide dismutase in rat ovary by lutropin.Crossref | GoogleScholarGoogle Scholar | 2848516PubMed |
Laloraya, M., Kumar, G., and Laloraya, M. (1989). Histochemical study of superoxide dismutase in the ovary of the rat during the oestrous cycle. J. Reprod. Fertil. 86, 583–587.
| Histochemical study of superoxide dismutase in the ovary of the rat during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 2760887PubMed |
LeBel, C. P., Ischiropoulos, H., and Bondy, S. C. (1992). Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5, 227–231.
| Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1322737PubMed |
Lee, C., and Longo, V. (2016). Dietary restriction with and without caloric restriction for healthy aging. F1000Res. 5, 117.
| Dietary restriction with and without caloric restriction for healthy aging.Crossref | GoogleScholarGoogle Scholar |
Lim, J., and Luderer, U. (2011a). Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol. Reprod. 84, 775–782.
| Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 21148108PubMed |
Lim, J., and Luderer, U. (2011b). Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol. Reprod. 84, 775–782.
| Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 21148108PubMed |
Liu, C., Song, Z., Wang, L., Yu, H., Liu, W., Shang, Y., Xu, Z., Zhao, H., Gao, F., Wen, J., Zhao, L., Gui, Y., Jiao, J., Gao, F., and Li, W. (2017). Sirt1 regulates acrosome biogenesis by modulating autophagic flux during spermiogenesis in mice. Development 144, 441–451.
| Sirt1 regulates acrosome biogenesis by modulating autophagic flux during spermiogenesis in mice.Crossref | GoogleScholarGoogle Scholar | 28003215PubMed |
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
| 14907713PubMed |
Lucas, A. (1991). Programming by early nutrition in man. Ciba Found. Symp. 156, 38–50.
| 1855415PubMed |
Luderer, U., Kavanagh, T. J., White, C. C., and Faustman, E. M. (2001). Gonadotropin regulation of glutathione synthesis in the rat ovary. Reprod Toxicol. 15, 495–504.
| 11780957PubMed |
Mann, T., and Lutwak-Mann, C. (2012). ‘Male Reproductive Function and Semen: Themes and Trends in Physiology, Biochemistry and Investigative Andrology.’ (Springer Science & Business Media: New York.)
Marcelino, T. B., Longoni, A., Kudo, K. Y., Stone, V., Rech, A., de Assis, A. M., Scherer, E. B., da Cunha, M. J., Wyse, A. T., Pettenuzzo, L. F., Leipnitz, G., and Matte, 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.
| Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats.Crossref | GoogleScholarGoogle Scholar | 23639877PubMed |
McCay, C. M., Crowell, M. F., and Maynard, L. A. (1989). The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935. Nutrition 5, 155–171, discussion 172.
| 2520283PubMed |
Meema, S., and Meema, H. E. (1976). Menopausal bone loss and estrogen replacement. Isr. J. Med. Sci. 12, 601–606.
| 972014PubMed |
Michan, S., and Sinclair, D. (2007). Sirtuins in mammals: insights into their biological function. Biochem. J. 404, 1–13.
| Sirtuins in mammals: insights into their biological function.Crossref | GoogleScholarGoogle Scholar | 17447894PubMed |
Misra, H. P., and Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247, 3170–3175.
| 4623845PubMed |
NHS Digital. (2017). Statistics on obesity, physical activity and diet – England 2017. Available at https://digital.nhs.uk/data-and-information/publications/statistical/statistics-on-obesity-physical-activity-and-diet/statistics-on-obesity-physical-activity-and-diet-england-2017 [verified 18 March 2020].
Osborne, T. B., Mendel, L. B., and Ferry, E. L. (1917). The effect of retardation of growth upon the breeding period and duration of life of rats. Science 45, 294–295.
| The effect of retardation of growth upon the breeding period and duration of life of rats.Crossref | GoogleScholarGoogle Scholar | 17760202PubMed |
Palacios, O. M., Carmona, J. J., Michan, S., Chen, K. Y., Manabe, Y., Ward Iii, J. L., Goodyear, L. J., and Tong, Q. (2009). Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle. Aging (Albany NY) 1, 771–783.
| Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 20157566PubMed |
Qiu, X., Brown, K., Hirschey, M. D., Verdin, E., and Chen, D. (2010). Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 12, 662–667.
| Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation.Crossref | GoogleScholarGoogle Scholar | 21109198PubMed |
Rebrin, I., Kamzalov, S., and Sohal, R. S. (2003). Effects of age and caloric restriction on glutathione redox state in mice. Free Radic. Biol. Med. 35, 626–635.
| Effects of age and caloric restriction on glutathione redox state in mice.Crossref | GoogleScholarGoogle Scholar | 12957655PubMed |
Reznick, A. Z., and Packer, L. (1994). Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 233, 357–363.
| Oxidative damage to proteins: spectrophotometric method for carbonyl assay.Crossref | GoogleScholarGoogle Scholar | 8015470PubMed |
Rodríguez-González, G. L., Reyes-Castro, L. A., Vega, C. C., Boeck, L., Ibáñez, C., Nathanielsz, P. W., Larrea, F., and Zambrano, E. (2014). Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress. Age (Dordr.) 36, 9721.
| Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress.Crossref | GoogleScholarGoogle Scholar | 25354645PubMed |
Selesniemi, K., Lee, H.-J., Muhlhauser, A., and Tilly, J. L. (2011). Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc. Natl Acad. Sci. USA 108, 12319–12324.
| Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies.Crossref | GoogleScholarGoogle Scholar | 21730149PubMed |
Shadyab, A. H., Macera, C. A., Shaffer, R. A., Jain, S., Gallo, L. C., Gass, M. L., Waring, M. E., Stefanick, M. L., and LaCroix, A. Z. (2017). Ages at menarche and menopause and reproductive lifespan as predictors of exceptional longevity in women: the Women’s Health Initiative. Menopause 24, 35–44.
| Ages at menarche and menopause and reproductive lifespan as predictors of exceptional longevity in women: the Women’s Health Initiative.Crossref | GoogleScholarGoogle Scholar | 27465713PubMed |
Sies, H. (2013). ‘Oxidative Stress.’ (Elsevier: Cambridge.)
Singh, D., and Pandey, R. (1998). Changes in catalase activity and hydrogen peroxide level in rat ovary during estrous cycle and induction of catalase in rat ovary by estradiol-17 beta. Indian J. Exp. Biol. 36, 421–423.
| 9717456PubMed |
Sitzmann, B. D., Brown, D. I., Garyfallou, V. T., Kohama, S. G., Mattison, J. A., Ingram, D. K., Roth, G. S., Ottinger, M. A., and Urbanski, H. F. (2014). Impact of moderate calorie restriction on testicular morphology and endocrine function in adult rhesus macaques (Macaca mulatta). Age (Dordr.) 36, 183–197.
| Impact of moderate calorie restriction on testicular morphology and endocrine function in adult rhesus macaques (Macaca mulatta).Crossref | GoogleScholarGoogle Scholar | 23881606PubMed |
Skakkebaek, N. E., Rajpert-De Meyts, E., Buck Louis, G. M., Toppari, J., Andersson, A.-M., Eisenberg, M. L., Jensen, T. K., Jørgensen, N., Swan, S. H., and Sapra, K. J. (2015). Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol. Rev. 96, 55–97.
| Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility.Crossref | GoogleScholarGoogle Scholar |
Sohal, R. S., and Forster, M. J. (2014). Caloric restriction and the aging process: a critique. Free Radic. Biol. Med. 73, 366–382.
| Caloric restriction and the aging process: a critique.Crossref | GoogleScholarGoogle Scholar | 24941891PubMed |
Stone, V., Crestani, M. S., Saccomori, A. B., dal Magro, B. M., Maurmann, R. M., August, P. M., Dos Santos, B. G., Klein, C. P., Hackenhaar, F. S., and da Silveira Benfato, M. (2019a). Gestational caloric restriction improves redox homeostasis parameters in the brain of Wistar rats: a screening from birth to adulthood. J Nutr Biochem. 67, 138–148.
| 30903960PubMed |
Stone, V., Maurmann, R. M., dal Magro, B. M., Crestani, M. S., Hozer, R. M., Klein, C. P., and Matté, C. (2019b). Gestational caloric restriction with micronutrients supplementation does not delay development and promotes feeding behavior benefits. Nutr Neurosci. , 1–11.
| 31610769PubMed |
Tatone, C., and Amicarelli, F. (2013). The aging ovary – the poor granulosa cells. Fertil. Steril. 99, 12–17.
| The aging ovary – the poor granulosa cells.Crossref | GoogleScholarGoogle Scholar | 23273984PubMed |
Tatone, C., Di Emidio, G., Vitti, M., Di Carlo, M., Santini, S., D’Alessandro, A. M., Falone, S., and Amicarelli, F. (2015). Sirtuin functions in female fertility: possible role in oxidative stress and aging. Oxid. Med. Cell. Longev. 2015, 659687.
| Sirtuin functions in female fertility: possible role in oxidative stress and aging.Crossref | GoogleScholarGoogle Scholar | 26075037PubMed |
Thornalley, P J., and Tisdale, M. (1988). Inhibition of proliferation of human promyelocytic leukaemia HL60 cells by SD-lactoylglutathione in vitro. Leuk. Res. 12, 897–904.
| Inhibition of proliferation of human promyelocytic leukaemia HL60 cells by SD-lactoylglutathione in vitro.Crossref | GoogleScholarGoogle Scholar | 2905755PubMed |
US Department of Agriculture, and US Department of Health and Human Services. (2010). Dietary guidelines for Americans 2010. Available at https://health.gov/sites/default/files/2020-01/DietaryGuidelines2010.pdf [verified 18 March 2020].
Wendel, A. (1981). Glutathione peroxidase. Methods Enzymol. 77, 325–333.
| Glutathione peroxidase.Crossref | GoogleScholarGoogle Scholar | 7329310PubMed |
Yamada, T., Ohsawa, K., and Ohno, H. (1988). The usefulness of alkaline solutions for clearing the uterus and staining implantation sites in rats. Exp. Anim. 37, 325–331.
| The usefulness of alkaline solutions for clearing the uterus and staining implantation sites in rats.Crossref | GoogleScholarGoogle Scholar |
Yang, H., Yang, T., Baur, J. A., Perez, E., Matsui, T., Carmona, J. J., Lamming, D. W., Souza-Pinto, N. C., Bohr, V. A., and Rosenzweig, A. (2007). Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 130, 1095–1107.
| Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival.Crossref | GoogleScholarGoogle Scholar | 17889652PubMed |
Yu, B. P. (1996). Aging and oxidative stress: modulation by dietary restriction. Free Radic. Biol. Med. 21, 651–668.
| Aging and oxidative stress: modulation by dietary restriction.Crossref | GoogleScholarGoogle Scholar | 8891668PubMed |
Zhang, J., Fang, L., Lu, Z., Xiong, J., Wu, M., Shi, L., Luo, A., and Wang, S. (2016). Are sirtuins markers of ovarian aging? Gene 575, 680–686.
| Are sirtuins markers of ovarian aging?Crossref | GoogleScholarGoogle Scholar | 26403315PubMed |
Zhong, L., and Mostoslavsky, R. (2011). Fine tuning our cellular factories: sirtuins in mitochondrial biology. Cell Metab. 13, 621–626.
| Fine tuning our cellular factories: sirtuins in mitochondrial biology.Crossref | GoogleScholarGoogle Scholar | 21641544PubMed |
