Leptin deficiency in rats results in hyperinsulinemia and impaired glucose homeostasis

Endocrinology

Volumn 155, Issue 4, 2014, Pages 1268-1279

  D'Souza, Anna M ^a   Asadi, Ali ^a   Johnson, James D ^a   Covey, Scott D ^a   Kieffer, Timothy J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; LEPTIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEPTIN DEFICIENCY; MALE; NONHUMAN; OBESITY; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; WEIGHT GAIN;

ANIMALS; BLOOD GLUCOSE; BODY COMPOSITION; BODY WEIGHT; DISEASE MODELS, ANIMAL; FEMALE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HYPERINSULINISM; INSULIN; INSULIN RESISTANCE; ISLETS OF LANGERHANS; LEPTIN; LIVER; MALE; MUSCLES; OBESITY; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC;

EID: 84897876072     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1523     Document Type: Article

References (61)

1. Hardie LJ, Rayner DV, Holmes S, Trayhurn P. Circulating leptin levels are modulated by fasting, cold exposure and insulin administration in lean but not Zucker (fa/fa) rats as measured by ELISA. Biochem Biophys Res Commun. 1996;223:660-665. (Pubitemid 26246129)
2. Halaas JL, Gajiwala KS, Maffei M, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 1995;269: 543-546.
3. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature. 1998;395:763-770. (Pubitemid 28485436)
4. Coleman DL, Hummel KP. The influence of genetic background on the expression of the obese (Ob) gene in the mouse. Diabetologia. 1973;9:287-293.
5. Duncan JG. Lipotoxicity: what is the fate of fatty acids? J Lipid Res. 2008;49:1375-1376.
6. Coleman DL. Obese and diabetes: two mutant genes causing diabetes-obesity syndromes in mice. Diabetologia. 1978;14:141-148. (Pubitemid 8286141)
7. Dubuc PU. The development of obesity, hyperinsulinemia, and hyperglycemia in ob/ob mice. Metab Clin Exp. 1976;25:1567-1574. (Pubitemid 8002401)
8. Chen H, Charlat O, Tartaglia LA, et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell. 1996;84:491-495. (Pubitemid 26060722)
9. Argilés JM. The obese Zucker rat: a choice for fat metabolism 1968-1988: twenty years of research on the insights of the Zucker mutation. Prog Lipid Res. 1989;28:53-66.
10. Kawasaki F, MatsudaM,Kanda Y, Inoue H, Kaku K. Structural and functional analysis of pancreatic islets preserved by pioglitazone in db/db mice. Am J Physiol Endocrinol Metab. 2005;288:E510-E518. (Pubitemid 40250545)
11. Pick A, Clark J, Kubstrup C, et al. Role of apoptosis in failure of β-cell mass compensation for insulin resistance and β-cell defects in the male Zucker diabetic fatty rat. Diabetes. 1998;47:358-364. (Pubitemid 28104196)
12. Kjørholt C, Akerfeldt MC, Biden TJ, Laybutt DR. Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of β-cell differentiation and secretory function in the db/db mouse model of diabetes. Diabetes. 2005;54:2755-2763. (Pubitemid 41233599)
13. Coleman DL, Hummel KP. The influence of genetic background on the expression of the obese (Ob) gene in the mouse. Diabetologia. 1973;9:287-293.
14. Hedbacker K, Birsoy K, Wysocki RW, et al. Antidiabetic effects of IGFBP2, a leptin-regulated gene. Cell Metab. 2010;11:11-22.
15. Pelleymounter MA, Cullen MJ, Baker MB, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 1995;269:540-543.
16. Koch C, Augustine RA, Steger J, et al. Leptin rapidly improves glucose homeostasis in obese mice by increasing hypothalamic insulin sensitivity. J Neurosci. 2010;30:16180-16187.
17. Khan A, Narangoda S, Ahren B, Holm C, Sundler F, Efendic S. Long-term leptin treatment of ob/ob mice improves glucose-induced insulin secretion. Int J Obes Relat Metab Disord. 2001;25:816-821. (Pubitemid 32601374)
18. Cummings BP, Bettaieb A, Graham JL, et al. Subcutaneous administration of leptin normalizes fasting plasma glucose in obese type 2 diabetic UCD-T2DM rats. Proc Natl Acad Sci USA. 2011;108: 14670-14675.
19. Farooqi IS, Jebb SA, Langmack G, et al. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. N Engl J Med. 1999;341:879-884. (Pubitemid 29427050)
20. Gibson WT, Farooqi IS, Moreau M, et al. Congenital leptin deficiency due to homozygosity for the Δ133G mutation: report of another case and evaluation of response to four years of leptin therapy. J Clin Endocrinol Metab. 2004;89:4821-4826. (Pubitemid 39391413)
21. Schwartz MW, Baskin DG, Bukowski TR, et al. Specificity of leptin action on elevated blood glucose levels and hypothalamic neuropeptide Y gene expression in ob/ob mice. Diabetes. 1996;45:531-535. (Pubitemid 26111317)
22. Vaira S, Yang C, McCoy A, et al. Creation and preliminary characterization of a leptin knockout rat. Endocrinology. 2012;153: 5622-5628.
23. Chehab FF, Lim ME, Lu R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet. 1996;12:318-320. (Pubitemid 26080094)
24. Levi J, Gray SL, Speck M, et al. Acute disruption of leptin signaling in vivo leads to increased insulin levels and insulin resistance. Endocrinology. 2011;152:3385-3395.
25. Wideman RD, Gray SL, Covey SD, Webb GC, Kieffer TJ. Transplantation of PC1/3-Expressing α-cells improves glucose handling and cold tolerance in leptin-resistant mice. Mol Ther. 2009;17:191-198.
26. Briaud I, Harmon JS, Kelpe CL, Segu VB, Poitout V. Lipotoxicity of the pancreatic β-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids. Diabetes. 2001;50:315-321. (Pubitemid 32127288)
27. Huynh FK, Levi J, Denroche HC, et al. Disruption of hepatic leptin signaling protects mice from age- and diet-related glucose intolerance. Diabetes. 2010;59:3032-3040.
28. Lacy PE, Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes. 1967;16:35-39.
29. Salvalaggio PR, Deng S, Ariyan CE, et al. Islet filtration: a simple and rapid new purification procedure that avoids Ficoll and improves islet mass and function. Transplantation. 2002;74:877-879.
30. Denroche HC, Levi J, Wideman RD, et al. Leptin therapy reverses hyperglycemia in mice with streptozotocin-induced diabetes, independent of hepatic leptin signaling. Diabetes. 2011;60:1414-1423.
31. Haluzik M, Colombo C, Gavrilova O, et al. Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology. 2004;145: 3258-3264. (Pubitemid 38829998)
32. Alemzadeh R, Tushaus KM. Modulation of adipoinsular axis in prediabetic Zucker diabetic fatty rats by diazoxide. Endocrinology. 2004;145:5476-5484. (Pubitemid 39564587)
33. Turpin SM, Ryall JG, Southgate R, et al. Examination of 'lipotoxicity' in skeletal muscle of high-fat fed and ob/ob mice. J Physiol. 2009;587:1593-1605.
34. Shimabukuro M, Zhou YT, Levi M, Unger RH. Fatty acid-induced β cell apoptosis: a link between obesity and diabetes. Proc Natl Acad Sci USA. 1998;95:2498-2502. (Pubitemid 28145970)
35. Billington CJ, Briggs JE, Grace M, Levine AS. Effects of intracere-broventricular injection of neuropeptide Y on energy metabolism. Am J Physiol. 1991;260:R321-R327.
36. Weigle DS, Bukowski TR, Foster DC, et al. Recombinant ob protein reduces feeding and body weight in the ob/ob mouse. J Clin Invest. 1995;96:2065-2070.
37. Bryzgalova G, Lundholm L, Portwood N, et al. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am J Physiol Endocrinol Metab. 2008;295: E904-E912.
38. Riant E, Waget A, Cogo H, Arnal JF, Burcelin R, Gourdy P. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology. 2009;150:2109-2117.
39. Karakash C, Assimacopoulos-Jeannet F, Jeanrenaud B. An anomaly of insulin removal in perfused livers of obese-hyperglycemic (ob/ob) mice. J Clin Invest. 1976;57:1117-1124.
40. German JP, Wisse BE, Thaler JP, et al. Leptin deficiency causes insulin resistance induced by uncontrolled diabetes. Diabetes. 2010; 59:1626-1634.
41. Mehran AE, Templeman NM, Brigidi GS, et al. Hyperinsulinemia drives diet-induced obesity independently of brain insulin production. Cell Metab. 2012;16:723-737.
42. Thorens B, Sarkar HK, Kaback HR, Lodish HF. Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and β-pancreatic islet cells. Cell. 1988; 55:281-290.
43. Kieffer TJ, Habener JF. The adipoinsular axis: effects of leptin on pancreatic β-cells. Am J Physiol Endocrinol Metab. 2000;278:E1-E14. (Pubitemid 30101914)
44. Anini Y, Brubaker PL. Role of leptin in the regulation of glucagon-like peptide-1 secretion. Diabetes. 2003;52:252-259. (Pubitemid 36173176)
45. Wideman RD, Kieffer TJ. Mining incretin hormone pathways for novel therapies. Trends Endocrinol Metab. 2009;20:280-286.
46. Aizawa-Abe M, Ebihara K, Ebihara C, et al. Generation of leptin-deficient Lepmkyo/Lepmkyo rats and identification of leptin-responsive genes in the liver. Physiol Genomics. 2013;45:786-793.
47. Jonkers RA, van Loon LJ, Nicolay K, Prompers JJ. In vivo post-prandial lipid partitioning in liver and skeletal muscle in prediabetic and diabetic rats. Diabetologia. 2013;56:618-626.
48. Shimomura I, Bashmakov Y, Horton JD. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J Biol Chem. 1999;274:30028-30032.
49. Greenbaum CJ, Havel PJ, Taborsky GJ Jr, Klaff LJ. Intra-islet insulin permits glucose to directly suppress pancreatic A cell function. J Clin Invest. 1991;88:767-773.
50. Tudurí E, Marroquí L, Soriano S, et al. Inhibitory effects of leptin on pancreatic α-cell function. Diabetes. 2009;58:1616-1624.
51. Shiota M, Printz RL. Diabetes in Zucker diabetic fatty rat. Methods Mol Biol. 2012;933:103-123.
52. Harris RB, Zhou J, Redmann SM Jr, et al. A leptin dose-response study in obese (ob/ob) and lean (+/?) mice. Endocrinology. 1998;139:8-19. (Pubitemid 28166285)
53. Trayhurn P, James WP. Thermoregulation and non-shivering thermogenesis in the genetically obese (ob/ob) mouse. Pflugers Arch. 1978;373:189-193. (Pubitemid 8308043)
54. Seufert J, Kieffer TJ, Leech CA, et al. Leptin suppression of insulin secretion and gene expression in human pancreatic islets: implications for the development of adipogenic diabetes mellitus. J Clin Endocrinol Metab. 1999;84:670-676. (Pubitemid 29075704)
55. Ahrén B, Havel PJ. Leptin inhibits insulin secretion induced by cellular cAMP in a pancreatic B cell line (INS-1 cells). Am J Physiol. 1999;277:R959-R966. (Pubitemid 29525947)
56. Huynh FK, Neumann UH, Wang Y, Rodrigues B, Kieffer TJ, Covey SD. Arole for hepatic leptin signaling in lipid metabolism via altered very low density lipoprotein composition and liver lipase activity in mice. Hepatology. 2013;57:543-554.
57. Picard F, Richard D, Huang Q, Deshaies Y. Effects of leptin adipose tissue lipoprotein lipase in the obese ob/ob mouse. Int J Obes Relat Metab Disord. 1998;22:1088-1095. (Pubitemid 28486600)
58. Toyoshima Y, Gavrilova O, Yakar S, et al. Leptin improves insulin resistance and hyperglycemia in a mouse model of type 2 diabetes. Endocrinology. 2005;146:4024-4035. (Pubitemid 41175774)
59. Sivitz WI, Walsh SA, Morgan DA, Thomas MJ, Haynes WG. Effects of leptin on insulin sensitivity in normal rats. Endocrinology. 1997; 138:3395-3401. (Pubitemid 27345694)
60. Iannaccone PM, Jacob HJ. Rats! Dis Model Mech. 2009;2:206-210.
61. Enriori PJ, Evans AE, Sinnayah P, Cowley MA. Leptin resistance and obesity. Obesity (Silver Spring). 2006;14(suppl 5):254S-258S.