Skip to main content

Advertisement

SpringerLink
Log in

Effect of calorie restriction on redox status during chemically induced estropause in female mice

  • Original Article
  • Published:
GeroScience Aims and scope Submit manuscript

Abstract

In females, there is a continuous decline of the ovarian reserve with age, which results in menopause in women or estropause in mice. Loss of ovarian function results in metabolic alterations in mice and women. Based on this, we aimed to evaluate the effect of caloric restriction (CR) on redox status and metabolic changes in chemically induced estropause in mice. For this, mice were divided into four groups (n = 10): cyclic ad libitum (AL), cyclic 30% CR, AL estropause, and estropause 30% CR. Estropause was induced using 4-vinylcyclohexene diepoxide (VCD) for 20 consecutive days in 2-month-old females. The CR protocol started at 5 months of age and the treatments lasted for 4 months. The CR females gained less body weight than AL females (p < 0.001) and had lower glycemic curves in response to glucose tolerance test (GTT). The AL estropause females had the highest body weight and body fat, despite having lower food intake. However, the estropause females on 30% CR lost the most body weight and had the lowest amount of body fat compared to all groups. The effect of 30% CR on redox status in fat and liver tissue was similar for cyclic and estropause females. Interestingly, estropause decreased ROS in adipose tissue, while increasing it in the liver. No significant effects of CR on redox status were observed. Chemically induced estropause did not influence the response to 30% CR on glucose tolerance and redox status; however, weight loss was exarcebated compared to cyclic females.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data presented in the work are available from the corresponding author upon request.

References

  1. Te Velde ER, Scheffer GJ, Dorland M, Broekmans FJ, Fauser BC. Developmental and endocrine aspects of normal ovarian aging. Mol Cell Endocrinol. 1998;145(1-2):67–73. https://doi.org/10.1016/s0303-7207(98)00171-3.

    Article  Google Scholar 

  2. Neves MM, AD MARQUESJR. Senescência reprodutiva feminina em mamíferos. Rev Bras Reprod Anim. 2008;32(2):133–40.

    Google Scholar 

  3. Cavalcante MB, Sampaio OGM, Câmara FEA, Schneider A, de Ávila BM, Prosczek J, Masternak MM, Campos AR. Ovarian aging in humans: potential strategies for extending reproductive lifespan. Geroscience. 2023; https://doi.org/10.1007/s11357-023-00768-8.

  4. Ferreira VN, Chinelato RS, Castro MR, Ferreira ME. Menopausa: marco biopsicossocial do envelhecimento feminino. Psicol Soc. 2013;25(2):410–9.

    Article  Google Scholar 

  5. Finch CE. The menopause and aging, a comparative perspective. J Steroid Biochem Mol Biol. 2014;142:132–41. https://doi.org/10.1016/j.jsbmb.2013.03.010.

    Article  CAS  PubMed  Google Scholar 

  6. de Medeiros SF, Maitelli A, Nince APB. Efeitos da terapia hormonal na menopausa sobre o sistema imune. Rev Bras Ginecol Obstet. 2007;29(11):593–601.

    Article  Google Scholar 

  7. Bitto A, Altavilla D, Bonaiuto A, Polito F, Minutoli L, Di Stefano V, Giuliani D, Guarini S, Arcoraci V, Squadrito F. Effects of aglycone genistein in a rat experimental model of postmenopausal metabolic syndrome. J Endocrinol. 2009;200(3):367–76. https://doi.org/10.1677/JOE-08-0206.

    Article  CAS  PubMed  Google Scholar 

  8. Bourgonje AR, Abdulle AE, Al-Rawas AM, Al-Maqbali M, Al-Saleh M, Enriquez MB, Al-Siyabi S, Al-Hashmi K, Al-Lawati I, Bulthuis MLC, Mulder DJ, Gordijn SJ, van Goor H, Saleh J. Systemic oxidative stress is increased in postmenopausal women and independently associates with homocysteine levels. Int J Mol Sci. 2020;21(1):314. https://doi.org/10.3390/ijms21010314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Doshi SB, Agarwal A. The role of oxidative stress in menopause. J Midlife Health. 2013;4(3):140–6. https://doi.org/10.4103/0976-7800.118990.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Signorelli SS, Neri S, Sciacchitano S, Pino LD, Costa MP, Marchese G, Celotta G, Cassibba N, Pennisi G, Caschetto S. Behaviour of some indicators of oxidative stress in postmenopausal and fertile women. Maturitas. 2006;53(1):77–82. https://doi.org/10.1016/j.maturitas.2005.03.001.

    Article  CAS  PubMed  Google Scholar 

  11. McLean RR. Proinflammatory cytokines and osteoporosis. Curr Osteoporos Rep. 2009;7(4):134–9. https://doi.org/10.1007/s11914-009-0023-2.

    Article  PubMed  Google Scholar 

  12. Chen H, Perez JN, Constantopoulos E, McKee L, Regan J, Hoyer PB, Brooks HL, Konhilas J. A method to study the impact of chemically-induced ovarian failure on exercise capacity and cardiac adaptation in mice. J Vis Exp. 2014;86:51083. https://doi.org/10.3791/51083.

    Article  Google Scholar 

  13. Das M, Ellies LG, Kumar D, Sauceda C, Oberg A, Gross E, Mandt T, Newton IG, Kaur M, Sears DD, Webster NJG. Time-restricted feeding normalizes hyperinsulinemia to inhibit breast cancer in obese postmenopausal mouse models. Nat Commun. 2021;12(1):565. https://doi.org/10.1038/s41467-020-20743-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Romero-Aleshire MJ, Diamond-Stanic MK, Hasty AH, Hoyer PB, Brooks HL. Loss of ovarian function in the VCD mouse-model of menopause leads to insulin resistance and a rapid progression into the metabolic syndrome. Am J Physiol Regul Integr Comp Physiol. 2009;297(3):R587–92. https://doi.org/10.1152/ajpregu.90762.2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Brooks HL, Pollow DP, Hoyer PB. The VCD mouse model of menopause and perimenopause for the study of sex differences in cardiovascular disease and the metabolic syndrome. Physiology (Bethesda). 2016;31(4):250–7. https://doi.org/10.1152/physiol.00057.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Van Kempen TA, Milner TA, Waters EM. Accelerated ovarian failure: a novel, chemically induced animal model of menopause. Brain Res. 2011;1379:176–87. https://doi.org/10.1016/j.brainres.2010.12.064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rivera Z, Christian PJ, Marion SL, Brooks HL, Hoyer PB. Steroidogenic capacity of residual ovarian tissue in 4-vinylcyclohexene diepoxide-treated mice. Biol Reprod. 2009;80(2):328–36. https://doi.org/10.1095/biolreprod.108.070359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Acosta JI, Mayer L, Talboom JS, Tsang CW, Smith CJ, Enders CK, Bimonte-Nelson HA. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology. 2009;150(9):4248–59. https://doi.org/10.1210/en.2008-1802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rodrigues CM, Domingues TE, de Sousa SC, Costa-Pereira LV, Mendes BF, Dos Santos JM, Costa KB, Silva G, Cantuária VL, Rocha-Vieira E, Dias-Peixoto MF, Honorato-Sampaio K. Cardioprotective effects of severe calorie restriction from birth in adult ovariectomized rats. Life Sci. 2021;275:119411. https://doi.org/10.1016/j.lfs.2021.119411.

    Article  CAS  PubMed  Google Scholar 

  20. Normandin E, Sénéchal M, Prud’homme D, Rabasa-Lhoret R, Brochu M. Effects of caloric restriction with or without resistance training in dynapenic-overweight and obese menopausal women: a MONET study. J Frailty Aging. 2015;4(3):155–62. https://doi.org/10.14283/jfa.2015.54.

    Article  CAS  PubMed  Google Scholar 

  21. Salminen A, Kaarniranta K. SIRT1: regulation of longevity via autophagy. Cell Signal. 2009;21(9):1356–60. https://doi.org/10.1016/j.cellsig.2009.02.014.

    Article  CAS  PubMed  Google Scholar 

  22. Silva WJM da, Ferrari CKB. Metabolismo mitocondrial, radicais livres e envelhecimento. Rev Bras Geriatr Gerontol. 2011;14(3):441–451. https://doi.org/10.1590/S1809-98232011000300005

  23. Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev. 2005;126(9):913–22. https://doi.org/10.1016/j.mad.2005.03.012.

    Article  CAS  PubMed  Google Scholar 

  24. de Genaro PS, Sarkis KS, Martini LA. O efeito da restrição calórica na longevidade. Arq Bras Endocrinol Metab. 2009;53(5):667–72. https://doi.org/10.1590/S0004-27302009000500019.

    Article  Google Scholar 

  25. de Magalhães JP. Open-minded scepticism: inferring the causal mechanisms of human ageing from genetic perturbations. Ageing Res Rev. 2005;4(1):1–22. https://doi.org/10.1016/j.arr.2004.05.003.

    Article  PubMed  Google Scholar 

  26. Lohff JC, Christian PJ, Marion SL, Arrandale A, Hoyer PB. Characterization of cyclicity and hormonal profile with impending ovarian failure in a novel chemical-induced mouse model of perimenopause. Comp Med. 2005;55(6):523–7.

    CAS  PubMed  Google Scholar 

  27. McLean AC, Valenzuela N, Fai S, Bennett SA. Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. J Vis Exp. 2012;67:e4389. https://doi.org/10.3791/4389.

    Article  CAS  Google Scholar 

  28. Koebele SV, Bimonte-Nelson HA. The endocrine-brain-aging triad where many paths meet: female reproductive hormone changes at midlife and their influence on circuits important for learning and memory. Exp Gerontol. 2017;94:14–23. https://doi.org/10.1016/j.exger.2016.12.011.

    Article  CAS  PubMed  Google Scholar 

  29. Fang Y, Westbrook R, Hill C, Boparai RK, Arum O, Spong A, Wang F, Javors MA, Chen J, Sun LY, Bartke A. Duration of rapamycin treatment has differential effects on metabolism in mice. Cell Metab. 2013;17(3):456–62. https://doi.org/10.1016/j.cmet.2013.02.008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bennis MT, Schneider A, Victoria B, Do A, Wiesenborn DS, Spinel L, Gesing A, Kopchick JJ, Siddiqi SA, Masternak MM. The role of transplanted visceral fat from the long-lived growth hormone receptor knockout mice on insulin signaling. Geroscience. 2017;39(1):51–9. https://doi.org/10.1007/s11357-017-9957-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Myers M, Britt KL, Wreford NG, Ebling FJ, Kerr JB. Methods for quantifying follicular numbers within the mouse ovary. Reproduction. 2004;127(5):569–80. https://doi.org/10.1530/rep.1.00095.

    Article  CAS  PubMed  Google Scholar 

  32. Ali SF, LeBel CP, Bondy SC. Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology. 1992;13(3):637–48.

    CAS  PubMed  Google Scholar 

  33. Aksenov MY, Markesbery WR. Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett. 2001;302(2-3):141–5. https://doi.org/10.1016/s0304-3940(01)01636-6.

    Article  CAS  PubMed  Google Scholar 

  34. Esterbauer H, Cheeseman KH. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol. 1990;186:407–21. https://doi.org/10.1016/0076-6879(90)86134-h.

    Article  CAS  PubMed  Google Scholar 

  35. Stuehr DJ, Nathan CF. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med. 1989;169(5):1543–55. https://doi.org/10.1084/jem.169.5.1543.

    Article  CAS  PubMed  Google Scholar 

  36. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–6. https://doi.org/10.1016/s0076-6879(84)05016-3.

    Article  CAS  PubMed  Google Scholar 

  37. Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170–5.

    Article  CAS  PubMed  Google Scholar 

  38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265–75.

    Article  CAS  PubMed  Google Scholar 

  39. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54. https://doi.org/10.1006/abio.1976.9999.

    Article  CAS  PubMed  Google Scholar 

  40. Kao SW, Sipes IG, Hoyer PB. Early effects of ovotoxicity induced by 4-vinylcyclohexene diepoxide in rats and mice. Reprod Toxicol. 1999;13(1):67–75. https://doi.org/10.1016/s0890-6238(98)00061-6.

    Article  CAS  PubMed  Google Scholar 

  41. Mayer LP, Pearsall NA, Christian PJ, Devine PJ, Payne CM, McCuskey MK, Marion SL, Sipes IG, Hoyer PB. Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide. Reprod Toxicol. 2002;16(6):775–81. https://doi.org/10.1016/s0890-6238(02)00048-5.

    Article  CAS  PubMed  Google Scholar 

  42. Borman SM, VanDePol BJ, Kao S, Thompson KE, Sipes IG, Hoyer PB. A single dose of the ovotoxicant 4-vinylcyclohexene diepoxide is protective in rat primary ovarian follicles. Toxicol Appl Pharmacol. 1999;158(3):244–52. https://doi.org/10.1006/taap.1999.8702.

    Article  CAS  PubMed  Google Scholar 

  43. Rogers NH, Perfield JW 2nd, Strissel KJ, Obin MS, Greenberg AS. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology. 2009;150(5):2161–8. https://doi.org/10.1210/en.2008-1405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. de Vasconcellos LS, Sabino KR, Petroianu A. Relação entre ooforectomia e peso em modelo experimental. Rev Col Bras Cir. 2005;32(3):132–5. https://doi.org/10.1590/S0100-69912005000300006.

    Article  Google Scholar 

  45. Redman LM, Ravussin E. Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxid Redox Signal. 2011;14(2):275–87. https://doi.org/10.1089/ars.2010.3253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Garcia DN, Saccon TD, Pradiee J, Rincón JAA, Andrade KRS, Rovani MT, Mondadori RG, Cruz LAX, Barros CC, Masternak MM, Bartke A, Mason JB, Schneider A. Effect of caloric restriction and rapamycin on ovarian aging in mice. Geroscience. 2019;41(4):395–408. https://doi.org/10.1007/s11357-019-00087-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pósa A, Szabó R, Kupai K, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015;2015:787063. https://doi.org/10.1155/2015/787063.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Mason JB, Cargill SL, Anderson GB, Carey JR. Ovarian status influenced the rate of body-weight change but not the total amount of body-weight gained or lost in female CBA/J mice. Exp Gerontol. 2010;45(6):435–41. https://doi.org/10.1016/j.exger.2010.03.010.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Boldarine VT, Pedroso AP, Brandão-Teles C, LoTurco EG, Nascimento CMO, Oyama LM, Bueno AA, Martins-de-Souza D, Ribeiro EB. Ovariectomy modifies lipid metabolism of retroperitoneal white fat in rats: a proteomic approach. Am J Physiol Endocrinol Metab. 2020;319(2):E427–37. https://doi.org/10.1152/ajpendo.00094.2020.

    Article  CAS  PubMed  Google Scholar 

  50. Nishio E, Hayashi T, Nakatani M, Aida N, Suda R, Fujii T, Wakatsuki T, Honda S, Harada N, Shimono Y. Lack of association of ovariectomy-induced obesity with overeating and the reduction of physical activities. Biochem Biophys Rep. 2019;20:100671. https://doi.org/10.1016/j.bbrep.2019.100671.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Habermehl TL, Mason JB. Decreased sarcopenia in aged females with young ovary transplants was preserved in mice that received germ cell-depleted young ovaries. J Clin Med. 2019;8(1):40. https://doi.org/10.3390/jcm8010040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Margolis KL, Bonds DE, Rodabough RJ, Tinker L, Phillips LS, Allen C, Bassford T, Burke G, Torrens J. Howard BV; Women’s Health Initiative Investigators. Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women’s Health Initiative Hormone Trial. Diabetologia. 2004;47(7):1175–87. https://doi.org/10.1007/s00125-004-1448-x.

    Article  CAS  PubMed  Google Scholar 

  53. Kanaya AM, Herrington D, Vittinghoff E, Lin F, Grady D, Bittner V, Cauley JA, Barrett-Connor E, Heart and Estrogen/Progestin Replacement Study. Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/Progestin Replacement Study. A randomized, double-blind, placebo-controlled trial. Ann Intern Med. 2003;138(1):1–9. https://doi.org/10.7326/0003-4819-138-1-200301070-00005.

    Article  CAS  PubMed  Google Scholar 

  54. Salpeter SR, Walsh JM, Ormiston TM, Greyber E, Buckley NS, Salpeter EE. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes Metab. 2006;8(5):538–54. https://doi.org/10.1111/j.1463-1326.2005.00545.x.

    Article  CAS  PubMed  Google Scholar 

  55. Sapatini LRL, Calsa B, Marim LJ, Helaehil JV, Chiarotto GB, do Corezola Amaral ME. Caloric restriction prevents inflammation and insulin dysfunction in middle-aged ovariectomized mice. Mol Biol Rep. 2023;50(7):5675–85. https://doi.org/10.1007/s11033-023-08508-z.

    Article  CAS  PubMed  Google Scholar 

  56. Tyler KA, Habermehl TL, Mason JB. Manipulation of ovarian function influenced glucose metabolism in CBA/J mice. Exp Gerontol. 2019;126:110686. https://doi.org/10.1016/j.exger.2019.110686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Longo VD, Anderson RM. Nutrition, longevity and disease: from molecular mechanisms to interventions. Cell. 2022;185(9):1455–70. https://doi.org/10.1016/j.cell.2022.04.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Palmer AK, Jensen MD. Metabolic changes in aging humans: current evidence and therapeutic strategies. J Clin Invest. 2022;132(16):e158451. https://doi.org/10.1172/JCI158451.

    Article  PubMed  PubMed Central  Google Scholar 

  59. de Souza Nunes Faria MS, Pimentel VE, Helaehil JV, Bertolo MC, NTH S, da Silva-Neto PV, Thomazini BF, de Oliveira CA, do Amaral MEV. Caloric restriction overcomes pre-diabetes and hypertension induced by a high fat diet and renal artery stenosis. Mol Biol Rep. 2022;49(7):5883–95. https://doi.org/10.1007/s11033-022-07370-9.

    Article  CAS  PubMed  Google Scholar 

  60. Wu QJ, Zhang TN, Chen HH, Yu XF, Lv JL, Liu YY, Liu YS, Zheng G, Zhao JQ, Wei YF, Guo JY, Liu FH, Chang Q, Zhang YX, Liu CG, Zhao YH. The sirtuin family in health and disease. Signal Transduct Target Ther. 2022;7(1):402. https://doi.org/10.1038/s41392-022-01257-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kim JY, Mondaca-Ruff D, Singh S, Wang Y. SIRT1 and autophagy: implications in endocrine disorders. Front Endocrinol (Lausanne). 2022;13:930919. https://doi.org/10.3389/fendo.2022.930919.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Tozzi R, Cipriani F, Masi D, Basciani S, Watanabe M, Lubrano C, Gnessi L, Mariani S. Ketone bodies and SIRT1, synergic epigenetic regulators for metabolic health: a narrative review. Nutrients. 2022;14(15):3145. https://doi.org/10.3390/nu14153145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Walsh ME, Shi Y, Van Remmen H. The effects of dietary restriction on oxidative stress in rodents. Free Radic Biol Med. 2014;66:88–99. https://doi.org/10.1016/j.freeradbiomed.2013.05.037.

    Article  CAS  PubMed  Google Scholar 

  64. Fernández-Sánchez A, Madrigal-Santillán E, Bautista M, Esquivel-Soto J, Morales-González A, Esquivel-Chirino C, Durante-Montiel I, Sánchez-Rivera G, Valadez-Vega C, Morales-González JA. Inflammation, oxidative stress, and obesity. Int J Mol Sci. 2011;12(5):3117–32. https://doi.org/10.3390/ijms12053117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lissarassa YPS, Vincensi CF, Costa-Beber LC, Dos Santos AB, Goettems-Fiorin PB, Dos Santos JB, Donato YH, Wildner G, de Bittencourt H, Júnior PI, Frizzo MN, Heck TG, Ludwig MS. Chronic heat treatment positively impacts metabolic profile of ovariectomized rats: association with heat shock response pathways. Cell Stress Chaperones. 2020;25(3):467–79. https://doi.org/10.1007/s12192-020-01087-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. King TL, Underwood KB, Hansen KK, Kinter MT, Schneider A, Masternak MM, Mason JB. Chronological and reproductive aging-associated changes in resistance to oxidative stress in post-reproductive female mice. Geroscience. 2023; https://doi.org/10.1007/s11357-023-00865-8.

  67. Vuković R, Blažetić S, Oršolić I, Heffer M, Vari SG, Gajdoš M, Krivošíková Z, Kramárová P, Kebis A, Has-Schön E. Impact of ovariectomy, high fat diet, and lifestyle modifications on oxidative/antioxidative status in the rat liver. Croat Med J. 2014;55(3):218–27. https://doi.org/10.3325/cmj.2014.55.218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Research reported in this publication was supported by CAPES, CNPq, and FAPERGS.

Author information

Authors and Affiliations

  1. Faculdade de Nutrição, Universidade Federal de Pelotas, Rua Gomes Carneiro, 1 Sala 228 CEP, Pelotas, RS, 9601-610, Brazil

    Bianca M. Ávila, Bianka M. Zanini, Jéssica D. Hense, Driele N. Garcia, Juliane Prosczek & Augusto Schneider

  2. Centro de Ciências Quimicas, Farmacêutica e de Alimentos, Universidade Federal de Pelotas, Pelotas, RS, Brazil

    Karina P. Luduvico & Francielle M. Stefanello

  3. College of Veterinary Medicine, Department of Veterinary Clinical and Life Sciences, Center for Integrated BioSystems, Utah State University, Logan, UT, USA

    Jeffrey B. Mason

  4. College of Medicine, Burnett School of Biomedical Sciences, University of Central Florida, Orlando, FL, USA

    Michal M. Masternak

  5. Department of Head and Neck Surgery, Poznan University of Medical Sciences, Poznan, Poland

    Michal M. Masternak

Authors
  1. Bianca M. Ávila
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bianka M. Zanini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karina P. Luduvico
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jéssica D. Hense
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Driele N. Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juliane Prosczek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Francielle M. Stefanello
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jeffrey B. Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michal M. Masternak
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Augusto Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Augusto Schneider.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ávila, B.M., Zanini, B.M., Luduvico, K.P. et al. Effect of calorie restriction on redox status during chemically induced estropause in female mice. GeroScience 46, 2139–2151 (2024). https://doi.org/10.1007/s11357-023-00979-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-023-00979-z

Keywords

Search

Navigation