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Differential effects of a high-fat diet on serum lipid parameters and ovarian gene expression in young and aged female mice

Published online by Cambridge University Press:  17 February 2016

Driele Neske Garcia ,
Lígia Antunes Prietsch ,
Joao Alveiro Alvarado Rincón ,
Iraê de Lima Moreira ,
Sandra Costa Valle ,
Carlos Castilho Barros ,
Elizabete Helbig ,
Marcio Nunes Corrêa  and
Augusto Schneider
Driele Neske Garcia
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Lígia Antunes Prietsch
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Joao Alveiro Alvarado Rincón
Affiliation:
Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Iraê de Lima Moreira
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Sandra Costa Valle
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Carlos Castilho Barros
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Elizabete Helbig
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Marcio Nunes Corrêa
Affiliation:
Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas, RS, Brasil.
Augusto Schneider*
Affiliation:
Faculdade de Nutrição, Universidade Federal de Pelotas, Rua Gomes Carneiro, 1 Sala 239 CEP 96010–610 Pelotas–RS, Brazil.
*
All correspondence to: Augusto Schneider. Faculdade de Nutrição, Universidade Federal de Pelotas, Rua Gomes Carneiro, 1 Sala 239 CEP 96010–610 Pelotas–RS, Brazil. Tel: + 55 53 39211270. E-mail: [email protected]
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Summary

The aim of this study was to compare serum lipid profiles and ovarian gene expression between aged and younger female mice fed a control or a high-fat diet for 2 months. For this 16 female mice (C57BL/6) of 4 months (Young, n = 8) or 13 months (Old, n = 8) of age were used. The females were divided into four groups: (i) young females fed a normal diet; (ii) young females fed a high-fat diet; (iii) old females fed a normal diet; and (iv) old females fed a high-fat diet. Food intake was reduced (P < 0.05) in mice fed with a high-fat (2.9 ± 0.1 g) diet in comparison with control mice (3.9 ± 0.1 g). Body weight was higher for old females on the high-fat diet (35.1 ± 0.3 g) than for young females on the same diet (23.3 ± 0.4 g; P < 0.05). PON1 activity was lower in the high-fat than control diet group (114.3 ± 5.8 vs. 78.1 ± 6.0 kU/L, respectively) and was higher in older than younger females (85.9 ± 6.4 vs. 106.5 ± 5.3; P < 0.05, respectively). Females fed a high-fat diet had lower expression of Igf1 mRNA (P = 0.04). There was an interaction between age and diet for the expression of Gdf9 and Survivin, with lower expression in older females in both diets and young females that received the high-fat diet (P < 0.05). Concluding, the high-fat diet reduced the expression of ovarian Igf1 mRNA, and Gdf9 and Survivin mRNA in younger females, which can indicate lower fertility rates. High-density lipoprotein concentration and PON1 activity were higher in aged female mice.

Keywords

AMHFOXO3aIGF-1SIRT1
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 676 - 683
Copyright
Copyright © Cambridge University Press 2016 

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References

Abbott, R.D., Sharp, D.S., Burchfiel, C.M., Curb, J.D., Rodriguez, B.L., Hakim, A.A. & Yano, K. (1997). Cross-sectional and longitudinal changes in total and high-density-lipoprotein cholesterol levels over a 20-year period in elderly men: the Honolulu Heart Program. Ann. Epidemiol. 7, 417–24.Google Scholar
Brown, C., La Rocca, J., Pietruska, J., Ota, M., Anderson, L., Smith, S.D., Weston, P., Rasoulpour, T. & Hixon, M.L. (2010). Subfertility caused by altered follicular development and oocyte growth in female mice lacking PKB alpha/Akt1. Biol. Reprod. 82, 246–56.Google Scholar
Browne, R.W., Koury, S.T., Marion, S., Wilding, G., Muti, P. & Trevisan, M. (2007). Accuracy and biological variation of human serum paraoxonase 1 activity and polymorphism (Q192R) by kinetic enzyme assay. Clin. Chem. 53, 310–7.Google Scholar
Castrillon, D.H., Miao, L., Kollipara, R., Horner, J.W. & De Pinho, R.A. (2003). Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301, 215–8.Google Scholar
Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. & Matzuk, M.M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–5.Google Scholar
Durrington, P.N., Mackness, B. & Mackness, M.I. (2001). Paraoxonase and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 21, 473–80.Google Scholar
Dursun, P., Demirtas, E., Bayrak, A. & Yarali, H. (2006). Decreased serum paraoxonase 1 (PON1) activity: an additional risk factor for atherosclerotic heart disease in patients with PCOS? Hum. Reprod. 21, 104–8.Google Scholar
Faddy, M.J., Gosden, R.G., Gougeon, A., Richardson, S.J. & Nelson, J.F. (1992). Accelerated disappearance of ovarian follicles in mid-life implications for forecasting menopause. Hum. Reprod. 7, 1342–6.Google Scholar
Gao, J., Huang, Y., Li, M., Zhao, H., Zhao, Y., Li, R., Yan, J., Yu, Y. & Qiao, J. (2015). Effect of local basic fibroblast growth factor and vascular endothelial growth factor on subcutaneously allotransplanted ovarian tissue in ovariectomized mice. PLoS One 10, e0134035.Google Scholar
Gougeon, A., Ecochard, R. & Thalabard, J.C. (1994). Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol. Reprod. 50, 653–63.Google Scholar
Jeppesen, J.V., Anderson, R.A., Kelsey, T.W., Christiansen, S.L., Kristensen, S.G., Jayaprakasan, K., Raine-Fenning, N., Campbell, B.K. & Andersen, C.Y. (2013). Which follicles make the most anti-Mullerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol. Hum. Reprod. 19, 519–27.Google Scholar
John, G.B., Gallardo, T.D., Shirley, L.J. & Castrillon, D.H. (2008). Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev. Biol. 321, 197–204.Google Scholar
Kim, D.S., Burt, A.A., Ranchalis, J.E., Richter, R.J., Marshall, J.K., Nakayama, K.S., Jarvik, E.R., Eintracht, J.F., Rosenthal, E.A., Furlong, C.E. & Jarvik, G.P. (2012). Dietary cholesterol increases paraoxonase 1 enzyme activity. J. Lipid Res. 53, 2450–8.Google Scholar
Leroy, J.L., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M. & Bols, P.E. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–78.Google Scholar
Li, M., Chiu, J.F., Mossman, B.T. & Fukagawa, N.K. (2006). Down-regulation of manganese-superoxide dismutase through phosphorylation of FOXO3a by Akt in explanted vascular smooth muscle cells from old rats. J. Biol. Chem. 281, 40429–39.Google Scholar
Li, L., Fu, Y.C., Xu, J.J., Lin, X.H., Chen, X.C., Zhang, X.M. & Luo, L.L. (2015). Caloric restriction promotes the reserve of follicle pool in adult female rats by inhibiting the activation of mammalian target of rapamycin signaling. Reprod. Sci. 22, 60–7.Google Scholar
Lim, J. & Luderer, U. (2011). Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol. Reprod. 84, 775–82.Google Scholar
Liu, W.-J., Zhang, X.-M., Wang, N., Zhou, X.-L., Fu, Y.-C. & Luo, L.-L. (2015). Calorie restriction inhibits ovarian follicle development and follicle loss through activating SIRT1 signaling in mice. Eur. J. Med. Res. 20, 22.Google Scholar
Luo, C., Zuñiga, J., Edison, E., Palla, S., Dong, W. & Parker-Thornburg, J. (2011). Superovulation strategies for 6 commonly used mouse strains. J. Am. Assoc. Lab. Anim. Sci. 50, 471–8.Google Scholar
Masternak, M.M., Al-Regaiey, K.A., Del Rosario Lim, M.M., Bonkowski, M.S., Panici, J.A., Przybylski, G.K. & Bartke, A. (2005). Caloric restriction results in decreased expression of peroxisome proliferator-activated receptor superfamily in muscle of normal and long-lived growth hormone receptor/binding protein knockout mice. J. Gerontol. A Biol. Sci. Med. Sci. 60, 1238–45.CrossRefGoogle ScholarPubMed
Nteeba, J., Ross, J.W., Perfield, J.W., Keating, A.F. 2nd& (2013). High fat diet induced obesity alters ovarian phosphatidylinositol-3 kinase signaling gene expression. Reprod. Toxicol. 42, 68–77.Google Scholar
Pelosi, E., Omari, S., Michel, M., Ding, J., Amano, T., Forabosco, A., Schlessinger, D. & Ottolenghi, C. (2013). Constitutively active Foxo3 in oocytes preserves ovarian reserve in mice. Nat. Commun. 4, 1843.Google Scholar
Reeves, P.G., Nielsen, F.H. & Fahey, G.C. Jr. (1993). AIN-93 purified diets for laboratory rodents: final report of the american institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939–51.Google Scholar
Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., Du, C., Tang, W., Hamalainen, T., Peng, S.L., Lan, Z.J., Cooney, A.J., Huhtaniemi, I. & Liu, K. (2008). Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319, 611–3.Google Scholar
Rocha, J.S., Bonkowski, M.S., de Franca, L.R. & Bartke, A. (2007). Effects of mild calorie restriction on reproduction, plasma parameters and hepatic gene expression in mice with altered GH/IGF-I axis. Mech. Ageing Dev. 128, 317–31.Google Scholar
Rojas, J., Chávez, M., Olivar, L., Rojas, M., Morillo, J., Mejías, J., Calvo, M. & Bermúdez, V. (2014). Polycystic ovary syndrome, insulin resistance, and obesity: navigating the pathophysiologic labyrinth. Int. J. Reprod. Med. 2014, 719050.Google Scholar
Schneider, A., Zhi, X., Bartke, A., Kopchick, J.J. & Masternak, M.M. (2014a). Effect of growth hormone receptor gene disruption and PMA treatment on the expression of genes involved in primordial follicle activation in mice ovaries. Age (Dordr.) 36, 9701.CrossRefGoogle ScholarPubMed
Schneider, A., Zhi, X., Moreira, F., Lucia, T. Jr., Mondadori, R.G. & Masternak, M.M. (2014b). Primordial follicle activation in the ovary of Ames dwarf mice. J. Ovarian Res. 7, 120.Google Scholar
Suehiro, T., Nakamura, T., Inoue, M., Shiinoki, T., Ikeda, Y., Kumon, Y., Shindo, M., Tanaka, H. & Hashimoto, K. (2000). A polymorphism upstream from the human paraoxonase (PON1) gene and its association with PON1 expression. Atherosclerosis 150, 295–8.Google Scholar
Sutton-Tyrrell, K., Lassila, H.C., Meilahn, E., Bunker, C., Matthews, K.A. & Kuller, L.H. (1998). Carotid atherosclerosis in premenopausal and postmenopausal women and its association with risk factors measured after menopause. Stroke 29, 1116–21.Google Scholar
te Velde, E.R., Scheffer, G.J., Dorland, M., Broekmans, F.J. & Fauser, B.C. (1998). Developmental and endocrine aspects of normal ovarian aging. Mol. Cell. Endocrinol. 145, 67– 73.Google Scholar
van Noord-Zaadstra, B., Looman, C., Alsbach, H., Habbema, J., te Velde, E. & Karbaat, J. (1991). Delayed childbearing: effect of age on fecundity and outcome of pregnancy. Brit. Med. J. 302, 1361–5.Google Scholar
Wandji, S.A., Wood, T.L., Crawford, J., Levison, S.W. & Hammond, J.M. (1998). Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology 139, 5205–14.Google Scholar
Wild, S., Pierpoint, T., McKeigue, P. & Jacobs, H. (2000). Cardiovascular disease in women with polycystic ovary syndrome at long-term follow-up: a retrospective cohort study. Clin. Endocrinol. 52, 595–600.Google Scholar
Wolfgang, M.J. & Lane, M.D. (2006). Control of energy homeostasis: role of enzymes and intermediates of fatty acid metabolism in the central nervous system. Annu. Rev. Nutr. 26, 23–44.Google Scholar
Wu, L.L., Norman, R.J. & Robker, R.L. (2011). The impact of obesity on oocytes: evidence for lipotoxicity mechanisms. Reprod. Fertil. Dev. 24, 29–34.Google Scholar