Obesity alters the uterine environment before pregnancy

Obesity is a metabolic disorder that predisposes to numerous diseases and has become a major global public health concern. 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 administration for 60 da...

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Autor principal: Bazzano, M.V
Otros Autores: Sarrible, G.B, Martinez, N., Berón de Astrada, M., Elia, E.M
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: Elsevier Inc. 2018
Acceso en línea:Registro en Scopus
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Sumario:Obesity is a metabolic disorder that predisposes to numerous diseases and has become a major global public health concern. 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 administration for 60 days induces obesity in female rats and their fetuses develop macrosomia. Given that, in our model, rats are not genetically modified and that obese mothers were fed standard chow during pregnancy, the aim of the current study was to test the hypothesis that obesity alters the intrauterine environment prior to pregnancy, and this may explain the exacerbated fetal weight gain. We found that uteri from obese rats during the estrous phase developed insulin resistance through mechanisms that involve the induction of uterine hypoxia and the down-regulation of the insulin receptor gene. Moreover, uterine cell proliferation was induced by obesity concomitantly with the reduction in the uterine contractile response to a β2 AR agonist, salbutamol, and this may be consequence of the down-regulation in the uterine β2 AR expression. We conclude that CAF-induced obesity alters the uterine environment in rats during the estrous phase and may cause the fetal macrosomia previously described by us in obese animals. The lower sensitivity of the uterus to a relaxation stimulus (salbutamol) is not a minor fact given that for implantation to occur the uterus must be relaxed for embryo nidation. Thus, the alteration in the uterine quiescence may impair implantation and, consequently, the foregoing pregnancy. © 2018 Elsevier Inc.
Bibliografía:Yamaguchi, M., Sakata, M., Ogura, K., Miyake, A., Gestational changes of glucose transporter gene expression in the mouse placenta and decidua (1996) J Endocrinol Invest, 19 (8), pp. 567-569
Bryant, N.J., Govers, R., James, D.E., Regulated transport of the glucose transporter GLUT4 (2002) Nat Rev Mol Cell Biol, 3, p. 267
Scheepers, A., Joost, H.G., Schurmann, A., The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function (2004) JPEN J Parenter Enteral Nutr, 28 (5), pp. 364-371
Wang, J.X., Davies, M., Norman, R.J., Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study (2000) BMJ, 321 (7272), pp. 1320-1321
Fedorcsak, P., Dale, P.O., Storeng, R., Ertzeid, G., Bjercke, S., Oldereid, N., Impact of overweight and underweight on assisted reproduction treatment (2004) Hum Reprod, 19 (11), pp. 2523-2528
Lintsen, A.M.E., Pasker-de Jong, P.C.M., de Boer, E.J., Burger, C.W., Jansen, C.A.M., Braat, D.D.M., Effects of subfertility cause, smoking and body weight on the success rate of IVF (2005) Hum Reprod, 20 (7), pp. 1867-1875
Maheshwari, A., Stofberg, L., Bhattacharya, S., Effect of overweight and obesity on assisted reproductive technology — a systematic review (2007) Hum Reprod Update, 13 (5), pp. 433-444
Straus, D.S., Growth-stimulatory actions of insulin in vitro and in vivo* (1984) Endocr Rev, 5 (2), pp. 356-369
Strowitzki, T., von Eye, H.C., Kellerer, M., Ulrich Häring, H., Tyrosine kinase activity of insulin-like growth factor I and insulin receptors in human endometrium during the menstrual cycle: cyclic variation of insulin receptor expression (1993) Fertil Steril, 59 (2), pp. 315-322
Rosenbaum, D., Haber, R.S., Dunaif, A., Insulin resistance in polycystic ovary syndrome: Decreased expression of GLUT-4 glucose transporters in adipocytes (1993) Am J Physiol, 264 (2 27–2), pp. E197-E202
Wong, B.W., Kuchnio, A., Bruning, U., Carmeliet, P., Emerging novel functions of the oxygen-sensing prolyl hydroxylase domain enzymes (2013) Trends Biochem Sci, 38 (1), pp. 3-11
Kim, J.W., Tchernyshyov, I., Semenza, G.L., Dang, C.V., HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia (2006) Cell Metab, 3 (3), pp. 177-185
Halberg, N., Khan, T., Trujillo, M.E., Wernstedt-Asterholm, I., Attie, A.D., Sherwani, S., Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue (2009) Mol Cell Biol, 29 (16), pp. 4467-4483
Zhang, H., Zhang, G., Gonzalez, F.J., Park, S.M., Cai, D., Hypoxia-inducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation (2011) PLoS Biol, 9 (7)
Quaegebeur, A., Segura, I., Schmieder, R., Verdegem, D., Decimo, I., Bifari, F., Deletion or inhibition of the oxygen sensor PHD1 protects against ischemic stroke via reprogramming of neuronal metabolism (2016) Cell Metab, 23 (2), pp. 280-291
Semenza, G.L., Hydroxylation of HIF-1: oxygen sensing at the molecular level (2004) Phys Ther, 19, pp. 176-182
Corrales, P., Vidal-Puig, A., Medina-Gomez, G., PPARs and metabolic disorders associated with challenged adipose tissue plasticity (2018) Int J Mol Sci, 19 (7)
Tontonoz, P., Spiegelman, B.M., Fat and beyond: the diverse biology of PPARgamma (2008) Annu Rev Biochem, 77, pp. 289-312
DeFronzo, R.A., Pharmacologic therapy for type 2 diabetes mellitus (1999) Ann Intern Med, 131 (4), pp. 281-303
Bazzano, M.V., Paz, D.A., Elia, E.M., Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats (2017) J Nutr Biochem, 42, pp. 194-202
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
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
Elia, E.M., Pustovrh, C., Amalfi, S., Devoto, L., Motta, A.B., Link between metformin and the peroxisome proliferator-activated receptor gamma pathway in the uterine tissue of hyperandrogenized prepubertal mice (2011) Fertil Steril, 95 (8), pp. 2534-2537. , [e1]
Lopez Merlo, M., Faya, M., Priotto, M., Barbeito, C., Gobello, C., Development and proliferation of feline endometrial glands from fetal life to ovarian cyclicity (2017) Theriogenology, 99, pp. 119-123
Chen, Q., Zhang, Y., Peng, H., Lei, L., Kuang, H., Zhang, L., Transient {beta}2-adrenoceptor activation confers pregnancy loss by disrupting embryo spacing at implantation (2011) J Biol Chem, 286 (6), pp. 4349-4356
Chaud, M.A., Franchi, A.M., Beron de Astrada, M., Gimeno, M.F., Role of nitric oxide on oxytocin-evoked contractions and prostaglandin synthesis in isolated pregnant rat uterus (1997) Prostaglandins Leukot Essent Fatty Acids, 57 (3), pp. 323-329
Parida, S., Uttam Singh, T., Ravi Prakash, V., Mishra, S.K., Molecular and functional characteristics of beta3-adrenoceptors in late pregnant mouse uterus: a comparison with beta2-adrenoceptors (2013) Eur J Pharmacol, 700 (1-3), pp. 74-79
Srdic, B., Stokic, E., Korac, A., Ukropina, M., Velickovic, K., Breberina, M., Morphological characteristics of abdominal adipose tissue in normal-weight and obese women of different metabolic profiles (2010) Exp Clin Endocrinol Diabetes, 118 (10), pp. 713-718
Armoni, M., Harel, C., Karnieli, E., Transcriptional regulation of the GLUT4 gene: from PPAR-gamma and FOXO1 to FFA and inflammation (2007) Trends Endocrinol Metab, 18 (3), pp. 100-107
Zelzer, E., Levy, Y., Kahana, C., Shilo, B.Z., Rubinstein, M., Cohen, B., Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT (1998) EMBO J, 17 (17), pp. 5085-5094
Xie, B.-Y., Lv, Q.-Y., Ning, C.-C., Yang, B.-Y., Shan, W.-W., Cheng, Y.-L., TET1-GPER-PI3K/AKT pathway is involved in insulin-driven endometrial cancer cell proliferation (2017) Biochem Biophys Res Commun, 482 (4), pp. 857-862
Setiawan, V.W., Yang, H.P., Pike, M.C., McCann, S.E., Yu, H., Xiang, Y.B., Type I and II endometrial cancers: have they different risk factors? (2013) J Clin Oncol, 31 (20), pp. 2607-2618
Rosato, V., Zucchetto, A., Bosetti, C., Dal Maso, L., Montella, M., Pelucchi, C., Metabolic syndrome and endometrial cancer risk (2011) Ann Oncol, 22 (4), pp. 884-889
Jawerbaum, A., Catafau, J.R., Gonzalez, E.T., Novaro, V., Gomez, G., Gelpi, E., Eicosanoid production, metabolism and contractile activity in the isolated uterus from non-insulin-dependent diabetic rats during late pregnancy (1996) Prostaglandins, 51 (5), pp. 307-320
Markiewicz, W., Jaroszewski, J.J., β2- and β3-adrenergic receptors stimulation relaxes porcine myometrium in the peri-implantation period1,2 (2016) J Anim Sci, 94 (11), pp. 4611-4618
Engstrom, T., Bratholm, P., Vilhardt, H., Christensen, N.J., Effect of pregnancy on rat myometrial beta 2-adrenoceptor mRNA and isoproterenol-induced relaxation of isolated uterine strips (1997) J Endocrinol, 153 (3), pp. 393-399
Liu, Y.L., Nwosu, U.C., Rice, P.J., Relaxation of isolated human myometrial muscle by beta2-adrenergic receptors but not beta1-adrenergic receptors (1998) Am J Obstet Gynecol, 179 (4), pp. 895-898
Coatmellec-Taglioni, G., Dausse, J.P., Ribiere, C., Giudicelli, Y., Hypertension in cafeteria-fed rats: alterations in renal alpha2-adrenoceptor subtypes (2000) Am J Hypertens, 13 (5), pp. 529-534
Llado, I., Rodriguez-Cuenca, S., Pujol, E., Monjo, M., Estrany, M.E., Roca, P., Gender effects on adrenergic receptor expression and lipolysis in white adipose tissue of rats (2002) Obes Res, 10 (4), pp. 296-305
Plut, C., Ribiere, C., Giudicelli, Y., Dausse, J.P., Gender differences in hypothalamic tyrosine hydroxylase and alpha(2)-adrenoceptor subtype gene expression in cafeteria diet-induced hypertension and consequences of neonatal androgenization (2002) J Pharmacol Exp Ther, 302 (2), pp. 525-531
Wu, S., Divall, S., Wondisford, F., Wolfe, A., Reproductive tissues maintain insulin sensitivity in diet-induced obesity (2012) Diabetes, 61 (1), pp. 114-123
Sasson, I.E., Vitins, A.P., Mainigi, M.A., Moley, K.H., Simmons, R.A., Pre-gestational vs gestational exposure to maternal obesity differentially programs the offspring in mice (2015) Diabetologia, 58 (3), pp. 615-624
Kim, N.S., Kang, Y.J., Jo, J.O., Kim, H.Y., Oh, Y.R., Kim, Y.O., Elevated expression of thymosin beta4, vascular endothelial growth factor (VEGF), and hypoxia inducible factor (HIF)-1alpha in early-stage cervical cancers (2011) Pathol Oncol Res, 17 (3), pp. 493-502
Yu, C.X., Song, J.H., Li, Y.F., Tuo, Y., Zheng, J.J., Miao, R.J., Correlation between replicative senescence of endometrial gland epithelial cells in shedding and non-shedding endometria and endometriosis cyst during menstruation (2018) Gynecol Endocrinol, pp. 1-6
Comstock, I.A., Diaz-Gimeno, P., Cabanillas, S., Bellver, J., Sebastian-Leon, P., Shah, M., Does an increased body mass index affect endometrial gene expression patterns in infertile patients? A functional genomics analysis (2017) Fertil Steril, 107 (3), pp. 740-748.e2
Provost, M.P., Acharya, K.S., Acharya, C.R., Yeh, J.S., Steward, R.G., Eaton, J.L., Pregnancy outcomes decline with increasing recipient body mass index: an analysis of 22,317 fresh donor/recipient cycles from the 2008–2010 Society for Assisted Reproductive Technology Clinic Outcome Reporting System registry (2016) Fertil Steril, 105 (2), pp. 364-368
Bulletti, C., de Ziegler, D., Uterine contractility and embryo implantation (2005) Curr Opin Obstet Gynecol, 17 (3), pp. 265-276
Khairy, M., Dhillon, R.K., Chu, J., Rajkhowa, M., Coomarasamy, A., The effect of peri-implantation administration of uterine relaxing agents in assisted reproduction treatment cycles: a systematic review and meta-analysis (2016) Reprod Biomed Online, 32 (4), pp. 362-376
MM, I.J., Evers, J.L., Dunselman, G.A., Volovics, L., Hoogland, H.J., Relation between endometrial wavelike activity and fecundability in spontaneous cycles (1997) Fertil Steril, 67 (3), pp. 492-496
ISSN:09552863
DOI:10.1016/j.jnutbio.2018.09.009