Skip to main content
Top
Published in: European Journal of Medical Research 1/2015

Open Access 01-12-2015 | Research

Calorie restriction inhibits ovarian follicle development and follicle loss through activating SIRT1 signaling in mice

Authors: Wei-Juan Liu, Xing-Mei Zhang, Na Wang, Xiao-Ling Zhou, Yu-Cai Fu, Li-Li Luo

Published in: European Journal of Medical Research | Issue 1/2015

Login to get access

Abstract

Background

Silent information regulator 2 related enzyme 1 (SIRT1) is one of the key factors in the mechanism of calorie restriction (CR) extending lifespan of animals. The aim of the study is to investigate if CR prolongs ovarian lifespan in mice through activating SIRT1 signaling.

Methods

In the present study, 21 female C57BL/6 mice were divided into three groups: the control (n = 7), CR (n = 7), and SRT1720 (n = 7) groups. After the 26-week treatment, the number of ovarian follicles at each stage was counted, and Western blot was performed.

Results

The number of surviving follicles in ovaries of the SRT1720 group was less than that of the CR group but more than that of the normal control (NC) group. The number of atretic follicles in the ovaries of the SRT1720 group was similar to that of the CR group but less than that of the NC group. The number of primordial follicles in the ovaries of the SRT1720 group was less than that of the CR group but more than that of the NC group. The numbers of primary follicles, secondary follicles, antral follicles, and corpora lutea in the SRT1720 group were similar to those in the CR group. Western blot analysis showed that the expression of SIRT1, SIRT6, FOXO3a, and NRF1 proteins was upregulated, and p53 was downregulated in both the CR group and the SRT1720 group compared to the control group.

Conclusions

Our results indicate that CR inhibits the activation of primordial follicles and development of follicles at different stages, thus preserving the reserve of follicle pool (at least partly) through activating SIRT1 signaling.
Literature
1.
go back to reference Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11:461–71.CrossRefPubMed Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11:461–71.CrossRefPubMed
5.
go back to reference Osborne TB, Mendel LB, Ferry EL. The effect of retardation of growth upon the breeding period and duration of life of rats. Science. 1917;45:294–5.CrossRefPubMed Osborne TB, Mendel LB, Ferry EL. The effect of retardation of growth upon the breeding period and duration of life of rats. Science. 1917;45:294–5.CrossRefPubMed
6.
go back to reference Nelson JF, Gosden RG, Felicio LS. Effect of dietary restriction on estrous cyclicity and follicular reserves in aging C57BL/6 J mice. Biol Reprod. 1985;32:515–22.CrossRefPubMed Nelson JF, Gosden RG, Felicio LS. Effect of dietary restriction on estrous cyclicity and follicular reserves in aging C57BL/6 J mice. Biol Reprod. 1985;32:515–22.CrossRefPubMed
7.
go back to reference Selesniemi K, Lee HJ, Tilly JL. Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell. 2008;7:622–9.CrossRefPubMedCentralPubMed Selesniemi K, Lee HJ, Tilly JL. Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell. 2008;7:622–9.CrossRefPubMedCentralPubMed
8.
go back to reference Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, Estey C, et al. SIRT1 regulates energy metabolism and response to caloric restriction in mice. PLoS One. 2008;3:e1759.CrossRefPubMedCentralPubMed Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, Estey C, et al. SIRT1 regulates energy metabolism and response to caloric restriction in mice. PLoS One. 2008;3:e1759.CrossRefPubMedCentralPubMed
9.
go back to reference Chen D, Steele AD, Lindquist S, Guarente L. Increase in activity during calorie restriction requires SIRT1. Science. 2005;310:1641.CrossRefPubMed Chen D, Steele AD, Lindquist S, Guarente L. Increase in activity during calorie restriction requires SIRT1. Science. 2005;310:1641.CrossRefPubMed
10.
go back to reference Luo LL, Chen XC, Fu YC, Xu JJ, Li L, Lin XH, et al. The effects of caloric restriction and a high-fat diet on ovarian lifespan and the expression of SIRT1 and SIRT6 proteins in rats. Aging Clin Exp Res. 2012;24:125–33.PubMed Luo LL, Chen XC, Fu YC, Xu JJ, Li L, Lin XH, et al. The effects of caloric restriction and a high-fat diet on ovarian lifespan and the expression of SIRT1 and SIRT6 proteins in rats. Aging Clin Exp Res. 2012;24:125–33.PubMed
11.
go back to reference Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell. 2007;6:759–67.CrossRefPubMed Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell. 2007;6:759–67.CrossRefPubMed
12.
13.
go back to reference Mitchell SJ, Martin-Montalvo A, Mercken EM, Palacios HH, Ward TM, Abulwerdi G, et al. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep. 2014;6(5):836–43.CrossRefPubMedCentralPubMed Mitchell SJ, Martin-Montalvo A, Mercken EM, Palacios HH, Ward TM, Abulwerdi G, et al. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep. 2014;6(5):836–43.CrossRefPubMedCentralPubMed
14.
go back to reference Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor FOXO3a. Science. 2003;301:215–8.CrossRefPubMed Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor FOXO3a. Science. 2003;301:215–8.CrossRefPubMed
15.
go back to reference Liu L, Rajareddy S, Reddy P, Du C, Jagarlamudi K, Shen Y, et al. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of FOXO3a. Development. 2007;134:199–209.CrossRefPubMed Liu L, Rajareddy S, Reddy P, Du C, Jagarlamudi K, Shen Y, et al. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of FOXO3a. Development. 2007;134:199–209.CrossRefPubMed
16.
go back to reference Larsson NG, Oldfors A, Holme E, Clayton DA. Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochem Biophys Res Commun. 1994;200:1374–81.CrossRefPubMed Larsson NG, Oldfors A, Holme E, Clayton DA. Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochem Biophys Res Commun. 1994;200:1374–81.CrossRefPubMed
17.
go back to reference Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 1990;4:1023–34.CrossRefPubMed Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 1990;4:1023–34.CrossRefPubMed
18.
go back to reference Wang N, Luo LL, Xu JJ, Xu MY, Zhang XM, Zhou XL, et al. Obesity accelerates ovarian follicle development and follicle loss in rats. Metabolism. 2013;S0026–0495(13):00280–1. Wang N, Luo LL, Xu JJ, Xu MY, Zhang XM, Zhou XL, et al. Obesity accelerates ovarian follicle development and follicle loss in rats. Metabolism. 2013;S0026–0495(13):00280–1.
19.
go back to reference Kim HS, Xiao C, Wang RH, Lahusen T, Xu X, Vassilopoulos A, et al. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell Metab. 2010;12:224–36.CrossRefPubMedCentralPubMed Kim HS, Xiao C, Wang RH, Lahusen T, Xu X, Vassilopoulos A, et al. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell Metab. 2010;12:224–36.CrossRefPubMedCentralPubMed
20.
go back to reference Kim JM, Yoon YD, Tsang BK. Involvement of the Fas/Fas ligand system in p53-mediated granulosa cell apoptosis during follicular development and atresia. Endocrinology. 1999;140:2307–17.PubMed Kim JM, Yoon YD, Tsang BK. Involvement of the Fas/Fas ligand system in p53-mediated granulosa cell apoptosis during follicular development and atresia. Endocrinology. 1999;140:2307–17.PubMed
21.
22.
go back to reference Tilly JL, Tilly KI, Kenton ML, Johnson AL. Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology. 1995;136:232–41.PubMed Tilly JL, Tilly KI, Kenton ML, Johnson AL. Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology. 1995;136:232–41.PubMed
23.
go back to reference Depalo R, Nappi L, Loverro G, Bettocchi S, Caruso ML, Valentini AM, et al. Evidence of apoptosis in human primordial and primary follicles. Hum Reprod. 2003;18:2678–82.CrossRefPubMed Depalo R, Nappi L, Loverro G, Bettocchi S, Caruso ML, Valentini AM, et al. Evidence of apoptosis in human primordial and primary follicles. Hum Reprod. 2003;18:2678–82.CrossRefPubMed
24.
go back to reference Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology. 1996;137:3717–28.PubMed Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology. 1996;137:3717–28.PubMed
25.
go back to reference Schedin P, Mitrenga T, Kaeck M. Estrous cycle regulation of mammary epithelial cell proliferation, differentiation, and death in the Sprague-Dawley rat: a model for investigating the role of estrous cycling in mammary carcinogenesis. J Mammary Gland Biol Neoplasia. 2000;5:211–25.CrossRefPubMed Schedin P, Mitrenga T, Kaeck M. Estrous cycle regulation of mammary epithelial cell proliferation, differentiation, and death in the Sprague-Dawley rat: a model for investigating the role of estrous cycling in mammary carcinogenesis. J Mammary Gland Biol Neoplasia. 2000;5:211–25.CrossRefPubMed
26.
go back to reference Luo LL, Huang J, Fu YC, Xu JJ, Qian YS. Effects of tea polyphenols on ovarian development in rats. J Endocrinol Invest. 2008;31:1110–8.CrossRefPubMed Luo LL, Huang J, Fu YC, Xu JJ, Qian YS. Effects of tea polyphenols on ovarian development in rats. J Endocrinol Invest. 2008;31:1110–8.CrossRefPubMed
27.
go back to reference Juliani CC, Silva-Zacarin EC, Santos DC, Boer PA. Effects of atrazine on female Wistar rats: morphological alterations in ovarian follicles and immunocytoch emical labeling of 90 kDa heat shock protein. Micron. 2008;39:607–16.CrossRefPubMed Juliani CC, Silva-Zacarin EC, Santos DC, Boer PA. Effects of atrazine on female Wistar rats: morphological alterations in ovarian follicles and immunocytoch emical labeling of 90 kDa heat shock protein. Micron. 2008;39:607–16.CrossRefPubMed
28.
go back to reference Wise PM, Smith MJ, Dubal DB, Wilson ME, Krajnak KM, Rosewell KL. Neuroendocrine influences and repercussions of the menopause. Endocr Rev. 1999;20:243–8.CrossRefPubMed Wise PM, Smith MJ, Dubal DB, Wilson ME, Krajnak KM, Rosewell KL. Neuroendocrine influences and repercussions of the menopause. Endocr Rev. 1999;20:243–8.CrossRefPubMed
29.
go back to reference Lamberts SW, van den Beld AW, van der Lely AJ. The endocrinology of aging. Science. 1997;278:419–24.CrossRefPubMed Lamberts SW, van den Beld AW, van der Lely AJ. The endocrinology of aging. Science. 1997;278:419–24.CrossRefPubMed
30.
go back to reference Anzalone CR, Hong LS, Lu JK, LaPolt PS. Influences of age and ovarian follicular reserve on estrous cycle patterns, ovulation, and hormone secretion in the Long-Evans rat. Biol Reprod. 2001;64:1056–62.CrossRefPubMed Anzalone CR, Hong LS, Lu JK, LaPolt PS. Influences of age and ovarian follicular reserve on estrous cycle patterns, ovulation, and hormone secretion in the Long-Evans rat. Biol Reprod. 2001;64:1056–62.CrossRefPubMed
31.
go back to reference Lu JK, Anzalone CR, LaPolt PS. Relation of neuroendocrine function to reproductive decline during aging in the female rat. Neurobiol Aging. 1994;15:541–4.CrossRefPubMed Lu JK, Anzalone CR, LaPolt PS. Relation of neuroendocrine function to reproductive decline during aging in the female rat. Neurobiol Aging. 1994;15:541–4.CrossRefPubMed
32.
go back to reference Moallem SA, Hales BF. The role of p53 and cell death by apoptosis and necrosis in 4-hydroperoxycyclophosphamide-induced limb malformations. Development. 1998;125:3225–34.PubMed Moallem SA, Hales BF. The role of p53 and cell death by apoptosis and necrosis in 4-hydroperoxycyclophosphamide-induced limb malformations. Development. 1998;125:3225–34.PubMed
33.
go back to reference Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, et al. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A. 2003;100:10794–9.CrossRefPubMedCentralPubMed Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, et al. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A. 2003;100:10794–9.CrossRefPubMedCentralPubMed
34.
go back to reference Ghafari F, Pelengaris S, Walters E, Hartshorne GM. Influence of p53 and genetic background on prenatal oogenesis and oocyte attrition in mice. Hum Reprod. 2009;24:1460–72.CrossRefPubMed Ghafari F, Pelengaris S, Walters E, Hartshorne GM. Influence of p53 and genetic background on prenatal oogenesis and oocyte attrition in mice. Hum Reprod. 2009;24:1460–72.CrossRefPubMed
Metadata
Title
Calorie restriction inhibits ovarian follicle development and follicle loss through activating SIRT1 signaling in mice
Authors
Wei-Juan Liu
Xing-Mei Zhang
Na Wang
Xiao-Ling Zhou
Yu-Cai Fu
Li-Li Luo
Publication date
01-12-2015
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2015
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-015-0114-8

Other articles of this Issue 1/2015

European Journal of Medical Research 1/2015 Go to the issue