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Abstract:

Obesity constitutes a health problem of increasing worldwide prevalence related to many reproductive problems such as infertility, ovulation dysfunction, preterm delivery, fetal growth disorders, etc. The mechanisms linking obesity to these pathologies are not fully understood. Cafeteria diet (CAF) is the animal model used for the study of obesity that more closely reflects western diet habits. Previously we described that CAF induces obesity associated to hyperglycemia, reduced ovarian reserve, presence of follicular cysts and ovulatory impairments. The aim of the present study was to contribute in the understanding of the physiological mechanisms altered as consequence of obesity. For that purpose, female Wistar rats were fed ad libitum with a standard diet (control group) or CAF (Obese group). We found that CAF fed-rats developed obesity, glucose intolerance and insulin resistance. Ovaries from obese rats showed decreased glucose uptake and became insulin resistant, showing decreased ovarian expression of glucotransporter type 4 and insulin receptor gene expression respect to controls. These animals showed an increased follicular nitric oxyde synthase expression that may be responsible for the ovulatory disruptions and for inflammation, a common feature in obesity. Obese rats resulted subfertile and their pups were macrosomic. We conclude that obesity alters the systemic and the ovarian glucidic homeostasis impairing the reproductive outcome. Since macrosomia is a risk factor for metabolic and obstetric disorders in adult life, we suggest that obesity is impacting not only on health and reproduction but it is also impacting on health and reproduction of the offspring. © 2017

Registro:

Documento: Artículo
Título:Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats
Autor:Bazzano, M.V.; Paz, D.A.; Elia, E.M.
Filiación:Laboratorio de Biología del Desarrollo, Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-CONICET-UBA), Pabellón 2, Cdad. Universitaria, Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón 2. Cdad. Universitaria, Buenos Aires, Argentina
Palabras clave:Fertility; Glucose; Glut-4; Insulin; Obesity; Ovary; Reproductive outcome; glucose; glucose transporter 4; insulin; insulin receptor; glucose transporter 4; insulin receptor; nitric oxide synthase; Slc2a4 protein, rat; animal experiment; animal tissue; Article; body fat distribution; cafeteria diet; controlled study; diet; diet induced obesity; female; gene expression; glucose intolerance; glucose tolerance test; glucose transport; homeostasis; hyperglycemia; immunohistochemistry; insulin resistance; insulin tolerance test; macrosomia; nonhuman; obesity; ovarian glucidic homeostasis; ovary; rat; reproduction; reproductive success; animal; complication; genetics; homeostasis; metabolism; obesity; ovary follicle; pathology; pathophysiology; pregnancy; Wistar rat; Animals; Body Fat Distribution; Diet; Female; Glucose Tolerance Test; Glucose Transporter Type 4; Homeostasis; Insulin Resistance; Nitric Oxide Synthase; Obesity; Ovarian Follicle; Ovary; Pregnancy; Rats, Wistar; Receptor, Insulin
Año:2017
Volumen:42
Página de inicio:194
Página de fin:202
DOI: http://dx.doi.org/10.1016/j.jnutbio.2017.01.003
Título revista:Journal of Nutritional Biochemistry
Título revista abreviado:J. Nutr. Biochem.
ISSN:09552863
CODEN:JNBIE
CAS:glucose, 50-99-7, 84778-64-3; glucose transporter 4, 188071-24-1; insulin, 9004-10-8; nitric oxide synthase, 125978-95-2; Glucose Transporter Type 4; Nitric Oxide Synthase; Receptor, Insulin; Slc2a4 protein, rat
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09552863_v42_n_p194_Bazzano

Referencias:

  • Fullston, T., Shehadeh, H., Sandeman, L.Y., Kang, W.X., Wu, L.L., Robker, R.L., Female offspring sired by diet induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells (2015) J Assist Reprod Genet, 32 (5), pp. 725-735
  • Grindler, N.M., Moley, K.H., Maternal obesity, infertility and mitochondrial dysfunction: Potential mechanisms emerging from mouse model systems (2013) Mol Hum Reprod, 19 (8), pp. 487-494
  • Elia, E., Bazzano, M., Paz, D., Reproductive disorders in obesity (2015) Integr Obes Diabetes, 1 (1), pp. 20-25
  • Campbell, B.K., Kendall, N.R., Onions, V., Scaramuzzi, R.J., The effect of systemic and ovarian infusion of glucose, galactose and fructose on ovarian function in sheep (2010) Reproduction, 140 (5), pp. 721-732
  • Katz, M.G., Vollenhoven, B., The reproductive endocrine consequences of anorexia nervosa (2000) BJOG Int J Obstet Gynaecol, 107 (6), pp. 707-713
  • Butler, W.R., Nutritional interactions with reproductive performance in dairy cattle (2000) Anim Reprod Sci, 60-61, pp. 449-457
  • de Vries, M.J., Veerkamp, R.F., Energy Balance of Dairy Cattle in Relation to Milk Production Variables and Fertility (2000) J Dairy Sci, 83 (1), pp. 62-69
  • Norman, R.J., Clark, A.M., Obesity and reproductive disorders: a review (1998) Reprod Fertil Dev, 10 (1), pp. 55-63
  • Crosignani, P.G., Vegetti, W., Colombo, M., Ragni, G., Resumption of fertility with diet in overweight women (2002) Reprod BioMed Online, 5 (1), pp. 60-64
  • Biddinger, S.B., Kahn, C.R., From mice to men: Insights into the insulin resistance syndromes (2006) Journal, 68 (Issue), pp. 123-158
  • Kitamura, Y., Accili, D., New insights into the integrated physiology of insulin action (2004) Rev Endocr Metab Disord, 5 (2), pp. 143-149
  • Ozbilgin, K., Kuscu, N.K., Two oestrous cycles. Ten days insulin treatment reduced ovarian leptin expression of rat (2005) Saudi Med J, 26 (6), pp. 923-927
  • Poretsky, L., Kalin, M.F., The gonadotropic function of insulin (1987) Endocr Rev, 8 (2), pp. 132-141
  • Louet, J.F., LeMay, C., Mauvais-Jarvis, F., Antidiabetic actions of estrogen: Insight from human and genetic mouse models (2004) Curr Atheroscler Rep, 6 (3), pp. 180-185
  • Carr, M.C., The emergence of the metabolic syndrome with menopause (2003) J Clin Endocrinol Metab, 88 (6), pp. 2404-2411
  • Kanaya, A.M., Herrington, D., Vittinghoff, E., Lin, F., Grady, D., Bittner, V., Glycemic effects of postmenopausal hormone therapy: The heart and estrogen/progestin replacement study: A randomized, double-blind, placebo-controlled trial (2003) Ann Intern Med, 138 (1), pp. 1-9
  • Margolis, K.L., Bonds, D.E., Rodabough, R.J., Tinker, L., Phillips, L.S., Allen, C., Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: Results from the Women's Health Initiative Hormone Trial (2004) Diabetologia, 47 (7), pp. 1175-1187
  • Wagner, J.D., Thomas, M.J., Williams, J.K., Zhang, L., Greaves, K.A., Cefalu, W.T., Insulin sensitivity and cardiovascular risk factors in ovariectomized monkeys with estradiol alone or combined with nomegestrol acetate (1998) J Clin Endocrinol Metab, 83 (3), pp. 896-901
  • Kumagai, S., Holmang, A., Bjorntorp, P., The effects of oestrogen and progesterone on insulin sensitivity in female rats (1993) Acta Physiol Scand, 149 (1), pp. 91-97
  • Riant, E., Waget, A., Cogo, H., Arnal, J.F., Burcelin, R., Gourdy, P., Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice (2009) Endocrinology, 150 (5), pp. 2109-2117
  • Buettner, R., Parhofer, K.G., Woenckhaus, M., Wrede, C.E., Kunz-Schughart, L.A., Scholmerich, J., Defining high-fat-diet rat models: metabolic and molecular effects of different fat types (2006) J Mol Endocrinol, 36 (3), pp. 485-501
  • Cesaretti, M.L., Kohlmann Junior, O., Experimental models of insulin resistance and obesity: lessons learned (2006) Arq Bras Endocrinol Metabol, 50 (2), pp. 190-197
  • Kim, S., Jin, Y., Choi, Y., Park, T., Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice (2011) Biochem Pharmacol, 81 (11), pp. 1343-1351
  • Kohli, R., Kirby, M., Xanthakos, S.A., Softic, S., Feldstein, A.E., Saxena, V., High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis (2010) Hepatology, 52 (3), pp. 934-944
  • Cunha, T.S., Farah, V., Paulini, J., Pazzine, M., Elased, K.M., Marcondes, F.K., Relationship between renal and cardiovascular changes in a murine model of glucose intolerance (2007) Regul Pept, 139 (1-3), pp. 1-4
  • Calligaris, S.D., Lecanda, M., Solis, F., Ezquer, M., Gutierrez, J., Brandan, E., Mice long-term high-fat diet feeding recapitulates human cardiovascular alterations: an animal model to study the early phases of diabetic cardiomyopathy (2013) PLoS One, 8 (4)
  • Bazzano, M.V., Torelli, C., Pustovrh, M.C., Paz, D.A., Elia, E.M., Obesity induced by cafeteria diet disrupts fertility in the rat by affecting multiple ovarian targets (2015) Reprod BioMed Online, 31 (5), pp. 655-667
  • Akyol, A., Langley-Evans, S.C., McMullen, S., Obesity induced by cafeteria feeding and pregnancy outcome in the rat (2009) Br J Nutr, 102 (11), pp. 1601-1610
  • Hsieh, C.H., Wang, T.Y., Hung, C.C., Chen, M.C., Hsu, K.C., Improvement of glycemic control in streptozotocin-induced diabetic rats by Atlantic salmon skin gelatin hydrolysate as the dipeptidyl-peptidase IV inhibitor (2015) Food Funct, 6 (6), pp. 1887-1892
  • Yao, X.H., Nguyen, K.H., Nyomba, B.L., Reversal of glucose intolerance in rat offspring exposed to ethanol before birth through reduction of nuclear skeletal muscle HDAC expression by the bile acid TUDCA (2014) Physiol Rep, 2 (12)
  • Chen, S., Wasserman, D.H., MacKintosh, C., Sakamoto, K., Mice with AS160/TBC1D4-Thr649Ala knockin mutation are glucose intolerant with reduced insulin sensitivity and altered GLUT4 trafficking (2011) Cell Metab, 13 (1), pp. 68-79
  • Sakamoto, K., McCarthy, A., Smith, D., Green, K.A., Grahame Hardie, D., Ashworth, A., Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction (2005) EMBO J, 24 (10), pp. 1810-1820
  • Elia, E.M., Quintana, R., Carrere, C., Bazzano, M.V., Rey-Valzacchi, G., Paz, D.A., Metformin decreases the incidence of ovarian hyperstimulation syndrome: an experimental study (2013) J Ovarian Res, 6 (1), p. 62
  • Myers, M., Britt, K.L., Wreford, N.G., Ebling, F.J., Kerr, J.B., Methods for quantifying follicular numbers within the mouse ovary (2004) Reproduction, 127 (5), pp. 569-580
  • Supriya, C., Reddy, P.S., Prenatal exposure to aflatoxin B1: developmental, behavioral, and reproductive alterations in male rats (2015) Naturwissenschaften, 102 (5-6), p. 26
  • Brothers, K.J., Wu, S., DiVall, S.A., Messmer, M.R., Kahn, C.R., Miller, R.S., Rescue of obesity-induced infertility in female mice due to a pituitary-specific knockout of the insulin receptor (2010) Cell Metab, 12 (3), pp. 295-305
  • Algenstaedt, P., Rosenblatt, N., Kolb, I., Krutzelmann, A., Schwarzloh, B., Bottcher, A., A new model of primary human adipocytes reveals reduced early insulin signalling in type 2 diabetes (2004) Horm Metab Res, 36 (8), pp. 531-537
  • Hussey, S.E., McGee, S.L., Garnham, A., Wentworth, J.M., Jeukendrup, A.E., Hargreaves, M., Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes (2011) Diabetes Obes Metab, 13 (10), pp. 959-962
  • Higa, T.S., Spinola, A.V., Fonseca-Alaniz, M.H., Evangelista, F.S.A., Comparison between cafeteria and high-fat diets in the induction of metabolic dysfunction in mice (2014) Int J Physiol Pathophysiol Pharmacol, 6 (1), pp. 47-54
  • Bispo, K., Amusquivar, E., Garcia-Seco, D., Ramos-Solano, B., Gutierrez-Manero, J., Herrera, E., Supplementing diet with blackberry extract causes a catabolic response with increments in insulin sensitivity in rats (2015) Plant Foods Hum Nutr, 70 (2), pp. 170-175
  • Nishimoto, H., Matsutani, R., Yamamoto, S., Takahashi, T., Hayashi, K.G., Miyamoto, A., Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum (2006) J Endocrinol, 188 (1), pp. 111-119
  • Frolova, A.I., Moley, K.H., Glucose transporters in the uterus: an analysis of tissue distribution and proposed physiological roles (2011) Reproduction, 142 (2), pp. 211-220
  • Zhang, C., Niu, W., Wang, Z., Wang, X., Xia, G., The effect of gonadotropin on glucose transport and apoptosis in rat ovary (2012) PLoS One, 7 (8)
  • Kuo, C.H., Hwang, H., Lee, M.C., Castle, A.L., Ivy, J.L., Role of insulin on exercise-induced GLUT-4 protein expression and glycogen supercompensation in rat skeletal muscle (2004) J Appl Physiol (1985), 96 (2), pp. 621-627
  • Peyron-Caso, E., Fluteau-Nadler, S., Kabir, M., Guerre-Millo, M., Quignard-Boulange, A., Slama, G., Regulation of glucose transport and transporter 4 (GLUT-4) in muscle and adipocytes of sucrose-fed rats: effects of N-3 poly- and monounsaturated fatty acids (2002) Horm Metab Res, 34 (7), pp. 360-366
  • MacLean, P.S., Zheng, D., Jones, J.P., Olson, A.L., Dohm, G.L., Exercise-induced transcription of the muscle glucose transporter (GLUT 4) gene (2002) Biochem Biophys Res Commun, 292 (2), pp. 409-414
  • Steinberg, H.O., Chaker, H., Leaming, R., Johnson, A., Brechtel, G., Baron, A.D., Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance (1996) J Clin Invest, 97 (11), pp. 2601-2610
  • Petrie, J.R., Ueda, S., Webb, D.J., Elliott, H.L., Connell, J.M.C., Endothelial Nitric Oxide Production and Insulin Sensitivity: A Physiological Link With Implications for Pathogenesis of Cardiovascular Disease (1996) Circulation, 93 (7), pp. 1331-1333
  • Zackrisson, U., Mikuni, M., Wallin, A., Delbro, D., Hedin, L., Brannstrom, M., Cell-specific localization of nitric oxide synthases (NOS) in the rat ovary during follicular development, ovulation and luteal formation (1996) Hum Reprod, 11 (12), pp. 2667-2673
  • Hassani, F., Karami, M., Jalali Nadoushan, M.R., Yazdi, P.E., Nitric Oxide-Induced Polycystic Ovaries in The Wistar Rat (2012) Int J Fertil Steril, 6 (2), pp. 111-116
  • Sen, S., Simmons, R.A., Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats (2010) Diabetes, 59 (12), pp. 3058-3065
  • Surkan, P.J., Hsieh, C.C., Johansson, A.L.V., Dickman, P.W., Cnattingius, S., Reasons for increasing trends in large for gestational age births (2004) Obstet Gynecol, 104 (4), pp. 720-726
  • Bao, C., Zhou, Y., Jiang, L., Sun, C., Wang, F., Xia, W., Reasons for the increasing incidence of macrosomia in Harbin, China (2011) BJOG, 118 (1), pp. 93-98
  • Koyanagi, A., Zhang, J., Dagvadorj, A., Hirayama, F., Shibuya, K., Souza, J.P., Macrosomia in 23 developing countries: An analysis of a multicountry, facility-based, cross-sectional survey (2013) Lancet, 381 (9865), pp. 476-483
  • Shapiro, C., Sutija, V.G., Bush, J., Effect of maternal weight gain on infant birth weight (2000) J Perinat Med, 28 (6), pp. 428-431
  • Boulet, S.L., Alexander, G.R., Salihu, H.M., Pass, M., Macrosomic births in the United States: Determinants, outcomes, and proposed grades of risk (2003) Am J Obstet Gynecol, 188 (5), pp. 1372-1378
  • Ehrenberg, H.M., Mercer, B.M., Catalano, P.M., The influence of obesity and diabetes on the prevalence of macrosomia (2004) Am J Obstet Gynecol, 191 (3), pp. 964-968
  • Tavares, M., Rodrigues, T., Cardoso, F., Barros, H., Leite, L.P., Independent effect of maternal birth weight on infant birth weight (1996) J Perinat Med, 24 (4), pp. 391-396
  • Ahlsson, F., Gustafsson, J., Tuvemo, T., Lundgren, M., Females born large for gestational age have a doubled risk of giving birth to large for gestational age infants (2007) Acta Paediatr Int J Paediatr, 96 (3), pp. 358-362
  • de Wilde, J., van Buuren, S., Middelkoop, B., Trends in birth weight and the prevalence of low birth weight and small-for-gestational-age in Surinamese South Asian babies since 1974: cross-sectional study of three birth cohorts (2013) BMC Public Health, 13 (1), p. 931
  • Tsai, P.J., Roberson, E., Dye, T., Gestational diabetes and macrosomia by race/ethnicity in Hawaii (2013) BMC Res Notes, 6, p. 395
  • Ogonowski, J., Miazgowski, T., Intergenerational transmission of macrosomia in women with gestational diabetes and normal glucose tolerance (2015) Eur J Obstet Gynecol Reprod Biol, 195, pp. 113-116
  • Hermann, G.M., Dallas, L.M., Haskell, S.E., Roghair, R.D., Neonatal macrosomia is an independent risk factor for adult metabolic syndrome (2010) Neonatology, 98 (3), pp. 238-244
  • Wei, J.N., Sung, F.C., Li, C.Y., Chang, C.H., Lin, R.S., Lin, C.C., Low birth weight and high birth weight infants are both at an increased risk to have type 2 diabetes among schoolchildren in Taiwan (2003) Diabetes Care, 26 (2), pp. 343-348
  • Sorensen, H.T., Sabroe, S., Rothman, K.J., Gillman, M., Fischer, P., Sorensen, T.I., Relation between weight and length at birth and body mass index in young adulthood: cohort study (1997) BMJ, 315 (7116), p. 1137
  • Feuer, S., Rinaudo, P., From Embryos to Adults: A DOHaD Perspective on In Vitro Fertilization and Other Assisted Reproductive Technologies (2016) Healthcare (Basel), 4 (3)
  • Zambrano, E., Guzman, C., Rodriguez-Gonzalez, G.L., Durand-Carbajal, M., Nathanielsz, P.W., Fetal programming of sexual development and reproductive function (2014) Mol Cell Endocrinol, 382 (1), pp. 538-549

Citas:

---------- APA ----------
Bazzano, M.V., Paz, D.A. & Elia, E.M. (2017) . Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats. Journal of Nutritional Biochemistry, 42, 194-202.
http://dx.doi.org/10.1016/j.jnutbio.2017.01.003
---------- CHICAGO ----------
Bazzano, M.V., Paz, D.A., Elia, E.M. "Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats" . Journal of Nutritional Biochemistry 42 (2017) : 194-202.
http://dx.doi.org/10.1016/j.jnutbio.2017.01.003
---------- MLA ----------
Bazzano, M.V., Paz, D.A., Elia, E.M. "Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats" . Journal of Nutritional Biochemistry, vol. 42, 2017, pp. 194-202.
http://dx.doi.org/10.1016/j.jnutbio.2017.01.003
---------- VANCOUVER ----------
Bazzano, M.V., Paz, D.A., Elia, E.M. Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats. J. Nutr. Biochem. 2017;42:194-202.
http://dx.doi.org/10.1016/j.jnutbio.2017.01.003