Leptin treatment confers clinical benefit at multiple stages of virally induced type 1 diabetes in BB rats

References

• Giarratana N, Penna G, Adorini L. Animal models of spontaneous autoimmune disease: Type 1 diabetes in the nonobese diabetic mouse. Methods Mol Biol. 2007; 380:285–311.
   PubMedGoogle Scholar
• Zipris D. Epidemiology of type 1 diabetes and what animal models teach us about the role of viruses in disease mechanisms. Clin Immunol. 2009; 131:11–23.
   PubMed Web of Science ®Google Scholar
• Mordes JP, Serreze DV, Greiner DL, Rossini AA. 2004. Animal models of autoimmune diabetes mellitus. In: LeRoith D, Taylor SI, Olefski JM. editors. Diabetes Mellitus: A Fundamental and Clinical Text. Philadelphia, PA: Lippincott Williams & Wilkins. p 591–604.
   Google Scholar
• Mordes JP, Bortell R, Blankenhorn EP, Rossini AA, Greiner DL. Rat models of type 1 diabetes: Genetics, environment, and autoimmunity. ILAR J. 2004; 45:278–291.
   PubMed Web of Science ®Google Scholar
• Ramanathan S, Bihoreau M-T, Paterson AD, Marandi L, Gauguier D, Poussier P. Thymectomy and radiation-induced type 1 diabetes in nonlymphopenic BB rats. Diabetes. 2002; 51:2975–2981.
   PubMed Web of Science ®Google Scholar
• Zipris D, Lien E, Xie JX, Greiner DL, Mordes JP, Rossini AA. TLR activation synergizes with Kilham rat virus infection to induce diabetes in BBDR rats. J Immunol. 2005; 174:131–142.
   PubMed Web of Science ®Google Scholar
• Mordes JP, Bortell R, Doukas J, Rigby M, Whalen B, Zipris D, Greiner DL, Rossini AA. The BB/Wor rat and the balance hypothesis of autoimmunity. Diabetes Metab Rev. 1996; 12:103–109.
   PubMed Web of Science ®Google Scholar
• Anderson MS, Bluestone JA. The NOD mouse: A model of immune dysregulation. Annu Rev Immunol. 2005; 23:447–485.
   PubMed Web of Science ®Google Scholar
• Yu X, Park BH, Wang MY, Wang ZV, Unger RH. Making insulin-deficient type 1 diabetic rodents thrive without insulin. Proc Natl Acad Sci USA. 2008; 105:14070–14075.
   PubMed Web of Science ®Google Scholar
• Havel PJ. Control of energy homeostasis and insulin action by adipocyte hormones: Leptin, acylation stimulation protein, and adiponectin. Curr Opin Lipidol. 2008; 13:51–59.
   Google Scholar
• Kapica M, Puzio I, Kato I, Kuwahara A, Zabielski R. Role of feed-regulating peptides on pancreatic exocrine secretion. J Physiol Pharmacol. 2008; 2:145–159 59 Suppl.
   Google Scholar
• Lam QL, Lu L. Role of leptin in immunity. Cell Mol Immunol. 2007; 4:1–13.
   PubMed Web of Science ®Google Scholar
• La Cava A, Matarese G. The weight of leptin in immunity. Nat Rev Immunol. 2004; 4:371–379.
   PubMed Web of Science ®Google Scholar
• Okuya S, Tanabe K, Tanizawa Y, Oka Y. Leptin increases the viability of isolated rat pancreatic islets by suppressing apoptosis. Endocrinology. 2001; 142:4827–4830.
   PubMed Web of Science ®Google Scholar
• Roduit R, Thorens B. Inhibition of glucose-induced insulin secretion by long-term preexposure of pancreatic islets to leptin. FEBS Lett. 1997; 415:179–182.
   PubMed Web of Science ®Google Scholar
• Shimabukuro M, Wang MY, Zhou YT, Newgard CB, Unger RH. Protection against lipoapoptosis of beta cells through leptin-dependent maintenance of Bcl-2 expression. Proc Natl Acad Sci USA. 1998; 95:9558–9561.
   PubMed Web of Science ®Google Scholar
• Unger RH, Zhou YT, Orci L. Regulation of fatty acid homeostasis in cells: Novel role of leptin. Proc Natl Acad Sci USA. 1999; 96:2327–2332.
   PubMed Web of Science ®Google Scholar
• Bernotiene E, Palmer G, Gabay C. The role of leptin in innate and adaptive immune responses. Arthritis Res Ther. 2006; 8:217–226.
   PubMed Web of Science ®Google Scholar
• Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998; 394:897–901.
   PubMed Web of Science ®Google Scholar
• Matarese G, Sanna V, Lechler RI, Sarvetnick N, Fontana S, Zappacosta S, La Cava A. Leptin accelerates autoimmune diabetes in female NOD mice. Diabetes. 2002; 51:1356–1361.
   PubMed Web of Science ®Google Scholar
• Keystone EC, Schorlemmer HU, Pope C, Allison AC. Zymosan-induced arthritis: A model of chronic proliferative arthritis following activation of the alternative pathway of complement. Arthritis Rheum. 1977; 20:1396–1401.
   PubMed Web of Science ®Google Scholar
• Bernotiene E, Palmer G, Talabot-Ayer D, Szalay-Quinodoz I, Aubert ML, Gabay C. Delayed resolution of acute inflammation during zymosan-induced arthritis in leptin-deficient mice. Arthritis Res Ther. 2004; 6:R256–R263.
   Web of Science ®Google Scholar
• Hultgren OH, Tarkowski A. Leptin in septic arthritis: Decreased levels during infection and amelioration of disease activity upon its administration. Arthritis Res. 2001; 3:389–394.
   PubMedGoogle Scholar
• Chen G, Koyama K, Yuan X, Lee Y, Zhou YT, O'Doherty R, Newgard CB, Unger RH. Disappearance of body fat in normal rats induced by adenovirus-mediated leptin gene therapy. Proc Natl Acad Sci USA. 1996; 93:14795–14799.
   PubMed Web of Science ®Google Scholar
• Gottlieb PA, Berrios JP, Mariani G, Handler ES, Greiner D, Mordes JP. Autoimmune destruction of islets transplanted into RT6-depleted diabetes-resistant BB/Wor rats. Diabetes. 1990; 39:643–645etal.
   PubMed Web of Science ®Google Scholar
• Lacy PE, Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes. 1967; 16:35–39.
   PubMed Web of Science ®Google Scholar
• Shimizu H, Inoue K, Mori M. The leptin-dependent and – independent melanocortin signaling system: Regulation of feeding and energy expenditure. J Endocrinol. 2007; 193:1–9.
   PubMed Web of Science ®Google Scholar
• Kieffer TJ, Heller RS, Leech CA, Holz GG, Habener JF. Leptin suppression of insulin secretion by the activation of ATP-sensitive K+channels in pancreatic beta-cells. Diabetes. 1997; 46:1087–1093.
   PubMed Web of Science ®Google Scholar
• Seufert J, Kieffer TJ, Habener JF. Leptin inhibits insulin gene transcription and reverses hyperinsulinemia in leptin-deficient ob/ob mice. Proc Natl Acad Sci USA. 1999; 96:674–679.
   PubMed Web of Science ®Google Scholar
• Matarese G, Carrieri PB, La Cava A, Perna F, Sanna V, De Rosa V, Aufiero D, Fontana S, Zappacosta S. Leptin increase in multiple sclerosis associates with reduced number of CD4(+)CD25+regulatory T cells. Proc Natl Acad Sci USA. 2005; 102:5150–5155.
   PubMed Web of Science ®Google Scholar
• Matarese G, Di Giacomo A, Sanna V, Lord GM, Howard JK, Di Tuoro A, Bloom SR, Lechler RI, Zappacosta S, Fontana S. Requirement for leptin in the induction and progression of autoimmune encephalomyelitis. J Immunol. 2001; 166:5909–5916.
   PubMed Web of Science ®Google Scholar
• Matarese G, Sanna V, Di Giacomo A, Lord GM, Howard JK, Bloom SR, Lechler RI, Fontana S, Zappacosta S. Leptin potentiates experimental autoimmune encephalomyelitis in SJL female mice and confers susceptibility to males. Eur J Immunol. 2001; 31:1324–1332.
   PubMed Web of Science ®Google Scholar
• Tuzun A, Uygun A, Yesilova Z, Ozel AM, Erdil A, Yaman H, Bagci S, Gulsen M, Karaeren N, Dagalp K. Leptin levels in the acute stage of ulcerative colitis. J Gastroenterol Hepatol. 2004; 19:429–432.
   PubMed Web of Science ®Google Scholar
• Lee Y, Ravazzola M, Park BH, Bashmakov YK, Orci L, Unger RH. Metabolic mechanisms of failure of intraportally transplanted pancreatic beta-cells in rats: Role of lipotoxicity and prevention by leptin. Diabetes. 2007; 56:2295–2301.
   PubMed Web of Science ®Google Scholar
• Muller WA, Faloona GR, Unger RH. The effect of experimental insulin deficiency on glucagon secretion. J Clin Invest. 197; 50: 19921999.
   PubMed Web of Science ®Google Scholar
• Sakurai H, Dobbs RE, Unger RH. The role of glucagon in the pathogenesis of the endogenous hyperglycemia of diabetes mellitus. Metabolism. 1975; 24:1287–1297.
   PubMed Web of Science ®Google Scholar
• Dobbs R, Sakurai H, Sasaki H, Faloona G, Valverde I, Baetens D, Orci L, Unger R. Glucagon: Role in the hyperglycemia of diabetes mellitus. Science. 1975; 187:544–547.
   PubMed Web of Science ®Google Scholar
• Filippi C, von Herrath M. How viral infections affect the autoimmune process leading to type 1 diabetes. Cell Immunol. 2005; 233:125–132.
   PubMed Web of Science ®Google Scholar
• van der Werf N, Kroese FG, Rozing J, Hillebrands JL. Viral infections as potential triggers of type 1 diabetes. Diabetes Metab Res Rev. 2007; 23:169–183.
   Google Scholar
• von Herrath M. Can we learn from viruses how to prevent type 1 diabetes? The role of viral infections in the pathogenesis of type 1 diabetes and the development of novel combination therapies. Diabetes. 2009; 58:2–11.
   PubMed Web of Science ®Google Scholar
• Andréoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyglem MC, Lefebvre J, Wattré P. Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of type I diabetes mellitus. J Med Virol. 1997; 52:121–127.
   PubMedGoogle Scholar
• Clements GB, Galbraith DN, Taylor KW, Coxsackie B. virus infection and onset of childhood diabetes. Lancet. 1995; 346:221–223.
   PubMed Web of Science ®Google Scholar
• Hyo¨ty H, Hiltunen M, Knip M, Laakkonen M, Va¨ha¨salo P, Karjalainen J, Koskela P, Roivainen M, Leinikki P, Hovi T. A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. Childhood Diabetes in Finland (DiMe) Study Group. Diabetes. 1995; 44:652–657.
   PubMed Web of Science ®Google Scholar
• Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia. 2009; 52:1143–1151.
   PubMed Web of Science ®Google Scholar