Artículos de revistas
Duodenal-jejunal Bypass Restores Insulin Action And Βeta-cell Function In Hypothalamic-obese Rats
Registro en:
Obesity Surgery. Springer New York Llc, v. 25, n. 4, p. 656 - 665, 2015.
9608923
10.1007/s11695-014-1427-3
2-s2.0-84925873589
Institución
Resumen
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Background: Bariatric operations are frequently used to improve metabolic profile and comorbidities in obese subjects, but the effects of this procedure in hypothalamic-obese (HyO) patients are controversial. Here, using HyO rats, we investigate the effects of duodenal-jejunal bypass (DJB) upon obesity, serum lipid levels, glucose tolerance, and insulin action and secretion. Methods: Hypothalamic obesity was induced in male rats by the administration of monosodium glutamate [4 g/kg body weight (BW), HyO group] during the first 5 days of life. Control (CTL) group received saline (1.25 g/kg BW). At 90 days of age, HyO rats were submitted to DJB (HyO DJB group) or sham surgery. After 2 months, lipid levels, glucose tolerance, obesity parameters, and insulin sensitivity and secretion were verified. Results: HyO rats displayed obesity, hypertriglyceridemia, hypercholesterolemia, glucose intolerance, and hyperinsulinemia. A higher HOMA-IR and no alteration in the ratio of phospho (p)-Akt related to Akt protein content in the liver, after insulin stimulus, demonstrated that HyO rats were insulin resistant. Islets isolated from HyO rats hypersecreted insulin in response to glucose and carbachol (Cch). At 2 months after DJB, HyO rats still displayed higher fat stores, but showed normal serum lipids and insulin levels. The HyO DJB group displayed better glucose tolerance, associated with a normal hepatic insulin activation of Akt. Normal glucose and Cch-induced insulin secretion was observed in HyO DJB islets. Conclusions: DJB ameliorated glucose homeostasis, restored hepatic insulin action, and normalized islet function in HyO rats, indicating that this surgery may be useful for the treatment of hypothalamic obesity. © 2014, Springer Science+Business Media New York. 25 4 656 665 CAPES, Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Serra-Majem, L., Bautista-Castano, I., Etiology of obesity: two “key issues” and other emerging factors (2013) Nutr Hosp, 28, pp. 32-43. , PID: 2401074 Hochberg, I., Hochberg, Z., Expanding the definition of hypothalamic obesity. Obesity ereviews (2010) Off J Int Assoc Study Obes, 11, pp. 709-721. , COI: 1:CAS:528:DC%2BC3cXhsVagtLv Lee, M., Korner, J., Review of physiology, clinical manifestations, and management of hypothalamic obesity in humans (2009) Pituitary, 12, pp. 87-95. , COI: 1:CAS:528:DC%2BD1MXjslWmu70%3D, PID: 1832764 Bingham, N.C., Rose, S.R., Inge, T.H., Bariatric surgery in hypothalamic obesity (2012) Front Endocrinol, 3, p. 23 Muller, H.L., Gebhardt, U., Wessel, V., Schroder, S., Kolb, R., Sorensen, N., First experiences with laparoscopic adjustable gastric banding (LAGB) in the treatment of patients with childhood craniopharyngioma and morbid obesity (2007) Klin Padiatr, 219, pp. 323-325. , COI: 1:STN:280:DC%2BD2sjhtFCmuw%3D%3D, PID: 1805004 Inge, T.H., Pfluger, P., Zeller, M., Rose, S.R., Burget, L., Sundararajan, S., Gastric bypass surgery for treatment of hypothalamic obesity after craniopharyngioma therapy. Nature clinical practice (2007) Endocrinol Metab, 3, pp. 606-609 Schultes, B., Ernst, B., Schmid, F., Thurnheer, M., Distal gastric bypass surgery for the treatment of hypothalamic obesity after childhood craniopharyngioma (2009) Eur J EndocrinolEur Fed Endocr Soc, 161, pp. 201-206. , COI: 1:CAS:528:DC%2BD1MXovVKkuro%3 Bretault, M., Boillot, A., Muzard, L., Poitou, C., Oppert, J.M., Barsamian, C., Bariatric surgery following treatment for craniopharyngioma: a systematic review and individual-level data meta-analysis (2013) J Clin Endocrinol Metab, 98, pp. 2239-2246. , COI: 1:CAS:528:DC%2BC3sXptlKmt7Y%3D, PID: 2353323 Weismann, D., Pelka, T., Bender, G., Jurowich, C., Fassnacht, M., Thalheimer, A., Bariatric surgery for morbid obesity in craniopharyngioma (2013) Clin Endocrinol (Oxf), 78, pp. 385-390 Panchal, S.K., Brown, L., Rodent models for metabolic syndrome research (2011) J Biomed Biotechnol, 2011, p. 351982. , PID: 2125358 Olney, J.W., Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate (1969) Science, 164, pp. 719-721. , COI: 1:CAS:528:DyaF1MXktFWhurw%3D, PID: 577802 Arees, E.A., Mayer, J., Monosodium glutamate-induced brain lesions: electron microscopic examination (1970) Science, 170, pp. 549-550. , COI: 1:CAS:528:DyaE3MXitFGltA%3D%3D, PID: 550720 Balbo, S.L., Mathias, P.C., Bonfleur, M.L., Alves, H.F., Siroti, F.J., Monteiro, O.G., Vagotomy reduces obesity in MSG-treated rats (2000) Res Commun Mol Pathol Pharmacol, 108, pp. 291-296. , COI: 1:CAS:528:DC%2BD38XislGjsbg%3D, PID: 1195828 Maiter, D., Underwood, L.E., Martin, J.B., Koenig, J.I., Neonatal treatment with monosodium glutamate: effects of prolonged growth hormone (GH)-releasing hormone deficiency on pulsatile GH secretion and growth in female rats (1991) Endocrinology, 128, pp. 1100-1106. , COI: 1:CAS:528:DyaK3MXpvFentg%3D%3D, PID: 198984 Nagata, M., Suzuki, W., Iizuka, S., Tabuchi, M., Maruyama, H., Takeda, S., Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate (2006) Exp Anim Japan Assoc Lab Anim Sci, 55, pp. 109-115. , COI: 1:CAS:528:DC%2BD28XlsVOjtbo%3 Balbo, S.L., Grassiolli, S., Ribeiro, R.A., Bonfleur, M.L., Gravena, C., Brito, M.O.N., Fat storage is partially dependent on vagal activity and insulin secretion of hypothalamic obese rat (2007) Endocrine, 31, pp. 142-148. , COI: 1:CAS:528:DC%2BD2sXhtVSgtb%2FO, PID: 1787332 Nardelli, T.R., Ribeiro, R.A., Balbo, S.L., Vanzela, E.C., Carneiro, E.M., Boschero, A.C., Taurine prevents fat deposition and ameliorates plasma lipid profile in monosodium glutamate-obese rats (2011) Amino Acids, 41, pp. 901-908. , COI: 1:CAS:528:DC%2BC3MXhtFKitLbK, PID: 2104281 Ribeiro, R.A., Balbo, S.L., Roma, L.P., Camargo, R.L., Barella, L.F., Vanzela, E.C., Impaired muscarinic type 3 (M3) receptor/PKC and PKA pathways in islets from MSG-obese rats (2013) Mol Biol Rep, 40, pp. 4521-4528. , COI: 1:CAS:528:DC%2BC3sXps1Cnurs%3D, PID: 2365299 Ribeiro, R.A., Bonfleur, M.L., Vanzela, E.C., Zotti, A.I., Scomparin, D.X., Boschero, A.C., Balbo, S.L., Physical exercise introduced after weaning enhances pancreatic islet responsiveness to glucose and potentiating agents in adult msg-obese rats (2014) Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme Hirata, A.E., Andrade, I.S., Vaskevicius, P., Dolnikoff, M.S., Monosodium glutamate (MSG)-obese rats develop glucose intolerance and insulin resistance to peripheral glucose uptake. Brazilian journal of medical and biological research (1997) Revista Bras Pesquisas Med Biologicas Soc Bras Biofisica, 30, pp. 671-674. , COI: 1:CAS:528:DyaK2sXjvVCmtb0%3 Hirata, A.E., Alvarez-Rojas, F., Carvalheira, J.B., Carvalho, C.R., Dolnikoff, M.S., Abdalla Saad, M.J., Modulation of IR/PTP1B interaction and downstream signaling in insulin sensitive tissues of MSG-rats (2003) Life Sci, 73, pp. 1369-1381. , COI: 1:CAS:528:DC%2BD3sXltF2nt74%3D, PID: 1285049 Dawson, R., Pelleymounter, M.A., Millard, W.J., Liu, S., Eppler, B., Attenuation of leptin-mediated effects by monosodium glutamate-induced arcuate nucleus damage (1997) Am J Physiol, 273, pp. 202-206. , COI: 1:CAS:528:DyaK2sXlt1Srsbc%3D, PID: 925249 Oida, K., Nakai, T., Hayashi, T., Miyabo, S., Takeda, R., Plasma lipoproteins of monosodium glutamate-induced obese rats (1984) Int J Obes (Lond), 8, pp. 385-391. , COI: 1:CAS:528:DyaL2MXhs1CrtL8%3 Meguid, M.M., Ramos, E.J., Suzuki, S., Xu, Y., George, Z.M., Das, U.N., A surgical rat model of human Roux-en-Y gastric bypass (2004) J Gastrointest Surg Off J Soc Surg Aliment Tract, 8, pp. 621-630 Jurowich, C.F., Rikkala, P.R., Thalheimer, A., Wichelmann, C., Seyfried, F., Sander, V., Duodenal-jejunal bypass improves glycemia and decreases SGLT1-mediated glucose absorption in rats with streptozotocin-induced type 2 diabetes (2013) Ann Surg, 258, pp. 89-97. , PID: 2347852 Batista, T.M., da Silva, P.M., Amaral, A.G., Ribeiro, R.A., Boschero, A.C., Carneiro, E.M., Taurine supplementation restores insulin secretion and reduces ER stress markers in protein-malnourished mice (2013) Adv Exp Med Biol, 776, pp. 129-139. , COI: 1:CAS:528:DC%2BC3sXhvVSnu7rJ, PID: 2339287 Bernardis, L.L., Patterson, B.D., Correlation between ‘Lee index’ and carcass fat content in weanling and adult female rats with hypothalamic lesions (1968) J Endocrinol, 40, pp. 527-528. , COI: 1:STN:280:DyaF1c7ptFWgsg%3D%3D, PID: 486841 Ribeiro, R.A., Vanzela, E.C., Oliveira, C.A., Bonfleur, M.L., Boschero, A.C., Carneiro, E.M., Taurine supplementation: involvement of cholinergic/phospholipase C and protein kinase A pathways in potentiation of insulin secretion and Ca2+ handling in mouse pancreatic islets (2010) Br J Nutr, 104, pp. 1148-1155. , COI: 1:CAS:528:DC%2BC3cXht1Oms7fP, PID: 2059120 Bonora, E., Targher, G., Alberiche, M., Bonadonna, R.C., Saggiani, F., Zenere, M.B., Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subjects with various degrees of glucose tolerance and insulin sensitivity (2000) Diabetes Care, 23, pp. 57-63. , COI: 1:STN:280:DC%2BD3czpsVyisA%3D%3D, PID: 1085796 Matthews, D.R., Hosker, J.P., Rudenski, A.S., Naylor, B.A., Treacher, D.F., Turner, R.C., Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man (1985) Diabetologia, 28, pp. 412-419. , COI: 1:CAS:528:DyaL2MXlslKnu7k%3D, PID: 389982 Folch, J., Lees, M., Sloane Stanley, G.H., A simple method for the isolation and purification of total lipides from animal tissues (1957) J Biol Chem, 226, pp. 497-509. , COI: 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D, PID: 1342878 Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal Biochem, 72, pp. 248-254. , COI: 1:CAS:528:DyaE28XksVehtrY%3D, PID: 94205 Rubino, F., Marescaux, J., Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease (2004) Ann Surg, 239, pp. 1-11. , PID: 1468509 Rubino, F., Bariatric surgery: effects on glucose homeostasis (2006) Curr Opin Clin Nutr Metab Care, 9, pp. 497-507. , COI: 1:CAS:528:DC%2BD28Xot1aht74%3D, PID: 1677858 Araujo, A.C., Bonfleur, M.L., Balbo, S.L., Ribeiro, R.A., de Freitas, A.C., Duodenal-jejunal bypass surgery enhances glucose tolerance and beta-cell function in Western diet obese rats (2012) Obes Surg, 22, pp. 819-826. , PID: 2241157 Zechner, J.F., Mirshahi, U.L., Satapati, S., Berglund, E.D., Rossi, J., Scott, M.M., Weight-independent effects of roux-en-Y gastric bypass on glucose homeostasis via melanocortin-4 receptors in mice and humans (2013) Gastroenterology, 144, p. 580. , COI: 1:CAS:528:DC%2BC3sXhslCms7Y%3D, PID: 2315944 Strader, A.D., Vahl, T.P., Jandacek, R.J., Woods, S.C., D’Alessio, D.A., Seeley, R.J., Weight loss through ileal transposition is accompanied by increased ileal hormone secretion and synthesis in rats (2005) Am J Physiol Endocrinol Metab, 288, pp. 447-453. , COI: 1:CAS:528:DC%2BD2MXhsVCktLo%3D, PID: 1545439 Speck, M., Cho, Y.M., Asadi, A., Rubino, F., Kieffer, T.J., Duodenal-jejunal bypass protects GK rats from {beta}-cell loss and aggravation of hyperglycemia and increases enteroendocrine cells coexpressing GIP and GLP-1 (2011) Am J Physiol Endocrinol Metab, 300, pp. 923-932. , COI: 1:CAS:528:DC%2BC3MXmsFClsb4%3D, PID: 2130406 Salinari, S., le Roux, C.W., Bertuzzi, A., Rubino, F., Mingrone, G., Duodenal-jejunal bypass and jejunectomy improve insulin sensitivity in Goto-Kakizaki diabetic rats without changes in incretins or insulin secretion (2014) Diabetes, 63, pp. 1069-1078. , PID: 2424153 Gatta, B., Nunes, M.L., Bailacq-Auder, C., Etchechoury, L., Collet, D., Tabarin, A., Is bariatric surgery really inefficient in hypothalamic obesity? (2013) Clin Endocrinol (Oxf), 78, pp. 636-638 Rottembourg, D., O’Gorman, C.S., Urbach, S., Garneau, P.Y., Langer, J.C., Van Vliet, G., Outcome after bariatric surgery in two adolescents with hypothalamic obesity following treatment of craniopharyngioma (2009) J Pediatr Endocrinol Metab, 22, pp. 867-872. , PID: 1996089 Zhang, S.Y., Sun, X.J., Zheng, J.B., Wang, W., Liu, D., Chen, N.Z., Preserve common limb in duodenal-jejunal bypass surgery benefits rats with type 2-like diabetes (2014) Obes Surg, 24, pp. 405-411. , PID: 2419043 Geloneze, B., Geloneze, S.R., Fiori, C., Stabe, C., Tambascia, M.A., Chaim, E.A., Surgery for nonobese type 2 diabetic patients: an interventional study with duodenal-jejunal exclusion (2009) Obes Surg, 19, pp. 1077-1083. , PID: 1947546 Rubino, F., Gagner, M., Gentileschi, P., Kini, S., Fukuyama, S., Feng, J., The early effect of the Roux-en-Y gastric bypass on hormones involved in body weight regulation and glucose metabolism (2004) Ann Surg, 240, pp. 236-242. , PID: 1527354 Sun, D., Wang, K., Yan, Z., Zhang, G., Liu, S., Liu, F., Duodenal-jejunal bypass surgery up-regulates the expression of the hepatic insulin signaling proteins and the key regulatory enzymes of intestinal gluconeogenesis in diabetic Goto-Kakizaki rats (2013) Obes Surg, 23, pp. 1734-1742. , PID: 2370023 Strader, A.D., Clausen, T.R., Goodin, S.Z., Wendt, D., Ileal interposition improves glucose tolerance in low dose streptozotocin-treated diabetic and euglycemic rats (2009) Obes Surg, 19, pp. 96-104. , PID: 1898972 Pacheco, D., de Luis, D.A., Romero, A., Gonzalez Sagrado, M., Conde, R., Izaola, O., The effects of duodenal-jejunal exclusion on hormonal regulation of glucose metabolism in Goto-Kakizaki rats (2007) Am J Surg, 194, pp. 221-224. , COI: 1:CAS:528:DC%2BD2sXnsFWmtbY%3D, PID: 1761880 Mackenzie, R.W., Elliott, B.T., Akt/PKB activation and insulin signaling: a novel insulin signaling pathway in the treatment of type 2 diabetes (2014) Diabetes Metab Syndrome Obes Targets Ther, 7, pp. 55-64. , COI: 1:CAS:528:DC%2BC2cXhs1Gjsrf Boucher, J., Kleinridders, A., and Kahn, C. R. Insulin receptor signaling in normal and insulin-resistant states. Cold spring harbor perspectives in biology. 2014;6Seely, B.L., Staubs, P.A., Reichart, D.R., Berhanu, P., Milarski, K.L., Saltiel, A.R., Protein tyrosine phosphatase 1B interacts with the activated insulin receptor (1996) Diabetes, 45, pp. 1379-1385. , COI: 1:CAS:528:DyaK28XmtFCntrg%3D, PID: 882697 Bell, G.I., Kayano, T., Buse, J.B., Burant, C.F., Takeda, J., Lin, D., Molecular biology of mammalian glucose transporters (1990) Diabetes Care, 13, pp. 198-208. , COI: 1:STN:280:DyaK3c7mvVGktw%3D%3D, PID: 240747 Manna, P., Jain, S.K., Decreased hepatic phosphatidylinositol-3,4,5-triphosphate (PIP3) levels and impaired glucose homeostasis in type 1 and type 2 diabetic rats. Cellular physiology and biochemistry (2012) Int J Exp Cell. Physiol Biochem Pharmacol, 30, pp. 1363-1370. , COI: 1:CAS:528:DC%2BC3sXhslWisbg%3 David-Silva, A., Freitas, H.S., Okamoto, M.M., Sabino-Silva, R., Schaan, B.D., Machado, U.F., Hepatocyte nuclear factors 1α/4α and forkhead box A2 regulate the solute carrier 2A2 (Slc2a2) gene expression in the liver and kidney of diabetic rats (2013) Life Sci, 93, pp. 805-813. , COI: 1:CAS:528:DC%2BC3sXhs12ksrzK, PID: 2415745 Yamamoto, T., Fukumoto, H., Koh, G., Yano, H., Yasuda, K., Masuda, K., Liver and muscle-fat type glucose transporter gene expression in obese and diabetic rats (1991) Biochem Biophys Res Commun, 175, pp. 995-1002. , COI: 1:CAS:528:DyaK3MXhvVehtro%3D, PID: 202526 Donglei, Z., Liesheng, L., Xun, J., Chenzhu, Z., Weixing, D., Effects and mechanism of duodenal-jejunal bypass and sleeve gastrectomy on GLUT2 and glucokinase in diabetic Goto-Kakizaki rats (2012) Eur J Med Res, 17, p. 15. , PID: 2268670 Rubino, F., Forgione, A., Cummings, D.E., Vix, M., Gnuli, D., Mingrone, G., The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes (2006) Ann Surg, 244, pp. 741-749. , PID: 1706076 Woods, M., Lan, Z., Li, J., Wheeler, M.B., Wang, H., Wang, R., Antidiabetic effects of duodenojejunal bypass in an experimental model of diabetes induced by a high-fat diet (2011) Br J Surg, 98, pp. 686-696. , COI: 1:STN:280:DC%2BC3Mvgtlygug%3D%3D, PID: 2138100 Salinari, S., Bertuzzi, A., Asnaghi, S., Guidone, C., Manco, M., Mingrone, G., First-phase insulin secretion restoration and differential response to glucose load depending on the route of administration in type 2 diabetic subjects after bariatric surgery (2009) Diabetes Care, 32, pp. 375-380. , COI: 1:CAS:528:DC%2BD1MXjvVyqsbs%3D, PID: 1903340 Villanueva-Penacarrillo, M.L., Marquez, L., Gonzalez, N., Diaz-Miguel, M., Valverde, I., Effect of GLP-1 on lipid metabolism in human adipocytes (2001) Horm Metab Res, 33, pp. 73-77. , COI: 1:CAS:528:DC%2BD3MXjtVahu78%3D, PID: 1129449 MacAulay, K., Doble, B.W., Patel, S., Hansotia, T., Sinclair, E.M., Drucker, D.J., Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism (2007) Cell Metab, 6, pp. 329-337. , COI: 1:CAS:528:DC%2BD2sXht1Sjsr3F, PID: 1790856 Kaidanovich-Beilin, O., Eldar-Finkelman, H., Long-term treatment with novel glycogen synthase kinase-3 inhibitor improves glucose homeostasis in ob/ob mice: molecular characterization in liver and muscle (2006) J Pharmacol Exp Ther, 316, pp. 17-24. , COI: 1:CAS:528:DC%2BD28XhsleksA%3D%3D, PID: 1616993 Rao, R., Hao, C.M., Redha, R., Wasserman, D.H., McGuinness, O.P., Breyer, M.D., Glycogen synthase kinase 3 inhibition improves insulin-stimulated glucose metabolism but not hypertension in high-fat-fed C57BL/6J mice (2007) Diabetologia, 50, pp. 452-460. , COI: 1:CAS:528:DC%2BD2sXitlSksg%3D%3D, PID: 1715186 Lochhead, P.A., Coghlan, M., Rice, S.Q., Sutherland, C., Inhibition of GSK-3 selectively reduces glucose-6-phosphatase and phosphatase and phosphoenolypyruvate carboxykinase gene expression (2001) Diabetes, 50, pp. 937-946. , COI: 1:CAS:528:DC%2BD3MXkvFSgtb0%3D, PID: 1133443 Scomparin, D.X., Gomes, R.M., Grassiolli, S., Rinaldi, W., Martins, A.G., de Oliveira, J.C., Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice (2009) Endocrine, 36, pp. 510-517. , COI: 1:CAS:528:DC%2BD1MXhsVaksrbE, PID: 1985613 Balbo, S.L., Bonfleur, M.L., Carneiro, E.M., Amaral, M.E., Filiputti, E., Mathias, P.C., Parasympathetic activity changes insulin response to glucose and neurotransmitters (2002) Diabetes Metab, 28, pp. 313-317. , COI: 1:CAS:528:DC%2BD3sXhs1ykt7Y%3D, PID: 12688628, discussion 13S108-11 Mari, A., Manco, M., Guidone, C., Nanni, G., Castagneto, M., Mingrone, G., Restoration of normal glucose tolerance in severely obese patients after bilio-pancreatic diversion: role of insulin sensitivity and beta cell function (2006) Diabetologia, 49, pp. 2136-2143. , COI: 1:CAS:528:DC%2BD28XnslSitbg%3D, PID: 1681961