Implications of crosstalk between leptin and insulin signaling during the development of diet-induced obesity

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 5, 2009, Pages 409-416

  Morrison, Christopher D ^a   Huypens, Peter ^a   Stewart, Laura K ^a,b   Gettys, Thomas W ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Arcuate nuclei; Diet induced obesity; High fat diet; Hyperinsulinemic euglycemic clamp; Hypothalamus; Insulin resistance; Leptin resistance

Indexed keywords

INSULIN; LEPTIN; SATURATED FATTY ACID;

DIABETES MELLITUS; DIET; DIET SUPPLEMENTATION; DISEASE COURSE; FOOD INTAKE; HYPOTHALAMUS; INSULIN RESISTANCE; LIPID DIET; MOLECULAR MECHANICS; NERVE CELL; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW;

ADIPOSITY; ANIMALS; DIETARY FATS; ENERGY INTAKE; HUMANS; INSULIN; INSULIN RESISTANCE; LEPTIN; MICE; OBESITY; RATS; SIGNAL TRANSDUCTION;

MUS; RATTUS;

EID: 64249147779     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2008.09.005     Document Type: Review

References (98)

1. Surwit R.S., Seldin M.F., Kuhn C.M., Cochrane C., and Feinglos M.N. Control of expression of insulin resistance and hyperglycemia by different genetic factors in diabetic C57BL/6J mice. Diabetes 40 (1991) 82-87
2. Surwit R.S., Kuhn C.M., Cochrane C., McCubbin J.A., and Feinglos M.N. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37 (1988) 1163-1167
3. Myers M.G., Cowley M.A., and Munzberg H. Mechanisms of leptin action and leptin resistance. Annu. Rev. Physiol. 70 (2008) 537-556
4. Park S.Y., Cho Y.R., Kim H.J., Higashimori T., Danton C., Lee M.K., Dey A., Rothermel B., Kim Y.B., Kalinowski A., Russell K.S., and Kim J.K. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 54 (2005) 3530-3540
5. Storlien L.H., James D.E., Burleigh K.M., Chisholm D.J., and Kraegen E.W. Fat feeding causes widespread in vivo insulin resistance, decreased energy expenditure, and obesity in rats. Am. J. Physiol. 251 (1986) E576-E583
6. Kraegen E.W., James D.E., Storlien L.H., Burleigh K.M., and Chisholm D.J. In vivo insulin resistance in individual peripheral tissues of the high fat fed rat: assessment by euglycaemic clamp plus deoxyglucose administration. Diabetologia 29 (1986) 192-198
7. Oakes N.D., Cooney G.J., Camilleri S., Chisholm D.J., and Kraegen E.W. Mechanisms of liver and muscle insulin resistance induced by chronic high-fat feeding. Diabetes 46 (1997) 1768-1774
8. Pagliassotti M.J., Horton T.J., Gayles E.C., Koppenhafer T.A., Rosenzweig T.D., and Hill J.O. Reduced insulin suppression of glucose appearance is related to susceptibility to dietary obesity in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 272 (1997) R1264-R1270
9. Commerford S.R., Bizeau M.E., McRae H., Jampolis A., Thresher J.S., and Pagliassotti M.J. Hyperglycemia compensates for diet-induced insulin resistance in liver and skeletal muscle of rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281 (2001) R1380-R1389
10. Dhalla A.K., Wong M.Y., Voshol P.J., Belardinelli L., and Reaven G.M. A1 adenosine receptor partial agonist lowers plasma FFA and improves insulin resistance induced by high-fat diet in rodents. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E1358-E1363
11. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., and Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 372 (1994) 425-432
12. Friedman J.M. The function of leptin in nutrition, weight, and physiology. Nutr. Rev. 60 (2002) S1-S14
13. Gettys T.W. Leptin. In: William J., and Lennarz M.D.L. (Eds). Encylopedia of Biological Chemistry (2004), Elsevier, San Diego 541-545
14. Maffei M., Halaas J., Ravussin E., Pratley R.E., Lee G.H., Zhang Y., Fei H., Kim S., Lallone R., and Ranganathan S. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. 1 (1995) 1155-1161
15. Considine R.V., Sinha M.K., Heiman M.L., Kriauciunas A., Stephens T.W., Nyce M.R., Ohannesian J.P., Marco C.C., McKee L.J., and Bauer T.L. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N. Engl. J. Med. 334 (1996) 292-295
16. Halaas J.L., Boozer C., Blair-West J., Fidahusein N., Denton D.A., and Friedman J.M. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8878-8883
17. Commins S.P., Marsh D.J., Thomas S.A., Watson P.M., Padgett M.A., Palmiter R.D., and Gettys T.W. Norepinephrine is required for leptin effects on gene expression in brown and white adipose tissue. Endocrinology 140 (1999) 4772-4776
18. Collins S., Kuhn C.M., Petro A.E., Swick A.G., Chrunyk B.A., and Surwit R.S. Role of leptin in fat regulation. Nature 380 (1996) 677
19. Haynes W.G., Morgan D.A., Walsh S.A., Mark A.L., and Sivitz W.I. Receptor-mediated regional sympathetic nerve activation by leptin. J. Clin. Invest. 100 (1997) 270-278
20. Scarpace P.J., and Matheny M. Leptin induction of UCP1 gene expression is dependent on sympathetic innervation. Am. J. Physiol. Endocrinol. Metab. 275 (1998) E259-E264
21. Hwa J.J., Ghibaudi L., Compton D., Fawzi A.B., and Strader C.D. Intracerebroventricular injection of leptin increases thermogenesis and mobilizes fat metabolism in ob/ob mice. Horm. Metab. Res. 28 (1996) 659-663
22. Hwa J.J., Fawzi A.B., Graziano M.P., Ghibaudi L., Williams P., Van Heek M., Davis H., Rudinski M., Sybertz E., and Strader C.D. Leptin increases energy expenditure and selectively promotes fat metabolism in ob/ob mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 272 (1997) R1204-R1209
23. Vaisse C., Halaas J.L., Horvath C.M., Darnell Jr. J.E., Stoffel M., and Friedman J.M. Leptin activation of Stat3 in the hypothalamus of wildtype and ob/ob mice but not db/db mice. Nature Genet. 14 (1996) 95-97
24. Tartaglia L.A., Dembski M., Weng X., Deng N., Culpepper J., Devos R., Richards G.J., Campfield L.A., Clark F.T., Deeds J., Muir C., Sanker S., Moriarty A., Moore K.J., Smutko J.S., Mays G.G., Woolf E.A., Monroe C.A., and Tepper R.I. Identification and expression cloning of a leptin receptor, OB-R. Cell 83 (1995) 1263-1271
25. Cowley M.A., Smart J.L., Rubinstein M., Cerdan M.G., Diano S., Horvath T.L., Cone R.D., and Low M.J. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411 (2001) 480-483
26. Bjorbaek C., Uotani S., Da Silva B., and Flier J.S. Divergent signaling capacities of the long and short isoforms of the leptin receptor. J. Biol. Chem. 272 (1997) 32686-32695
27. Faouzi M., Leshan R., Bjornholm M., Hennessey T., Jones J., and Munzberg H. Differential accessibility of circulating leptin to individual hypothalamic sites. Endocrinology 148 (2007) 5414-5423
28. Van Heek M., Compton D.S., France C.F., Tedesco R.P., Fawzi A.B., Graziano M.P., Sybertz E.J., Strader C.D., and Davis Jr. H.R. Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J. Clin. Invest. 99 (1997) 385-390
29. El-Haschimi K., Pierroz D.D., Hileman S., Bjorbæk C., and Flier J.S. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J. Clin. Invest. 105 (2000) 1827-1832
30. Prpic V., Watson P.M., Frampton I.C., Sabol M.A., Jezek G.E., and Gettys T.W. Differential mechanisms and development of leptin resistance in A/J vs C57BL/6J mice during diet-induced obesity. Endocrinology 144 (2003) 1155-1163
31. Banks W.A., and Farrell C.L. Impaired transport of leptin across the blood-brain barrier in obesity is acquired and reversible. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E10-E15
32. Banks W.A., Coon A.B., Robinson S.M., Moinuddin A., Shultz J.M., Nakaoke R., and Morley J.E. Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 53 (2004) 1253-1260
33. 3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology 138 (1997) 405-413
34. Commins S.P., Watson P.M., Levin N., Beiler R.J., and Gettys T.W. Central leptin regulates the UCP1 and ob genes in brown and white adipose tissue via different β-adrenoceptor subtypes. J. Biol. Chem. 275 (2000) 33059-33067
35. Munzberg H., Flier J.S., and Bjorbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 145 (2004) 4880-4889
36. Munzberg H. Differential leptin access into the brain - a hierarchical organization of hypothalamic leptin target sites?. Physiol. Behav. 94 (2008) 664-669
37. Rasouli N., Molavi B., Elbein S.C., and Kern P.A. Ectopic fat accumulation and metabolic syndrome. Diabetes Obes. Metab. 9 (2007) 1-10
38. Pagliassotti M.J., Prach P.A., Koppenhafer T.A., and Pan D.A. Changes in insulin action, triglycerides, and lipid composition during sucrose feeding in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271 (1996) R1319-R1326
39. Kim J.K., Gavrilova O., Chen Y., Reitman M.L., and Shulman G.I. Mechanism of insulin resistance in A-ZIP/F-1 fatless mice. J. Biol. Chem. 275 (2000) 8456-8460
40. Yu C., Chen Y., Cline G.W., Zhang D., Zong H., Wang Y., Bergeron R., Kim J.K., Cushman S.W., Cooney G.J., Atcheson B., White M.F., Kraegen E.W., and Shulman G.I. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277 (2002) 50230-50236
41. An J., Muoio D.M., Shiota M., Fujimoto Y., Cline G.W., Shulman G.I., Koves T.R., Stevens R., Millington D., and Newgard C.B. Hepatic expression of malonyl-CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance. Nat. Med. 10 (2004) 268-274
42. Koves T.R., Ussher J.R., Noland R.C., Slentz D., Mosedale M., Ilkayeva O., Bain J., Stevens R., Dyck J.R., Newgard C.B., Lopaschuk G.D., and Muoio D.M. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7 (2008) 45-56
43. Koves T.R., Li P., An J., Akimoto T., Slentz D., Ilkayeva O., Dohm G.L., Yan Z., Newgard C.B., and Muoio D.M. PPARgamma coactivator-1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J. Biol. Chem. 280 (2005) 33588-33598
44. Kastin A.J., and Pan W. Dynamic regulation of leptin entry into brain by the blood-brain barrier. Regul. Pept. 92 (2000) 37-43
45. Ayala J.E., Bracy D.P., McGuinness O.P., and Wasserman D.H. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55 (2006) 390-397
46. Enriori P.J., Evans A.E., Sinnayah P., Jobst E.E., Tonelli-Lemos L., Billes S.K., Glavas M.M., Grayson B.E., Perello M., Nillni E.A., Grove K.L., and Cowley M.A. Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab. 5 (2007) 181-194
47. Metlakunta A.S., Sahu M., and Sahu A. Hypothalamic phosphatidylinositol 3-kinase pathway of leptin signaling is impaired during the development of diet-induced obesity in FVB/N mice. Endocrinology 149 (2008) 1121-1128
48. Sahu A., and Metlakunta A.S. Hypothalamic phosphatidylinositol 3-kinase-phosphodiesterase 3B-cyclic AMP pathway of leptin signalling is impaired following chronic central leptin infusion. J. Neuroendocrinol. 17 (2005) 720-726
49. Chandler P.C., Viana J.B., Oswald K.D., Wauford P.K., and Boggiano M.M. Feeding response to melanocortin agonist predicts preference for and obesity from a high-fat diet. Physiol. Behav. 85 (2005) 221-230
50. Clegg D.J., Benoit S.C., Air E.L., Jackman A., Tso P., D'Alessio D., Woods S.C., and Seeley R.J. Increased dietary fat attenuates the anorexic effects of intracerebroventricular injections of MTII. Endocrinology 144 (2003) 2941-2946
51. Lu H.Q., Buison A., Jen K.L.C., and Dunbar J.C. Leptin resistance in obesity is characterized by decreased sensitivity to proopiomelanocortin products. Peptides 21 (2000) 1479-1485
52. Pierroz D.D., Ziotopoulou M., Ungsunan L., Moschos S., Flier J.S., and Mantzoros C.S. Effects of acute and chronic administration of the melanocortin agonist MTII in mice with diet-induced obesity. Diabetes 51 (2002) 1337-1345
53. Carreia M.L., Haynes W.G., Rahmouni K., Morgan D.A., Sivitz W.I., and Mark A.L. The concept of selective leptin resistance: evidence from agouti yellow obese mice. Diabetes 51 (2002) 439-442
54. Rahmouni K., Morgan D.A., Morgan G.M., Mark A.L., and Haynes W.G. Role of selective leptin resistance in diet-induced obesity hypertension. Diabetes 54 (2005) 2012-2018
55. Howard J.K., and Flier J.S. Attenuation of leptin and insulin signaling by SOCS proteins. Trends Endocrinol. Metab. 17 (2006) 365-371
56. Bjorbaek C., Elmquist J.K., Frantz J.D., Shoelson S.E., and Flier J.S. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell 1 (1999) 819-825
57. Bjorbaek C., El-Haschimi K., Frantz J.D., and Flier J.S. The role of SOCS-3 in leptin signaling and leptin resistance. J. Biol. Chem. 274 (1999) 30059-30065
58. Bjornholm M., Munzberg H., Leshan R.L., Villanueva E.C., Bates S.H., Louis G.W., Jones J.C., Ishida-Takahashi R., Bjorbaek C., and Myers Jr. M.G. Mice lacking inhibitory leptin receptor signals are lean with normal endocrine function. J. Clin. Invest. 117 (2007) 1354-1360
59. Howard J.K., Cave B.J., Oksanen L.J., Tzameli I., Bjorbaek C., and Flier J.S. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat. Med. 10 (2004) 734-738
60. Mori H., Hanada R., Hanada T., Aki D., Mashima R., Nishinakamura H., Torisu T., Chien K.R., Yasukawa H., and Yoshimura A. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 10 (2004) 739-743
61. Zabolotny J.M., Bence-Hanulec K.K., Stricker-Krongrad A., Haj F., Wang Y., Minokoshi Y., Kim Y.B., Elmquist J.K., Tartaglia L.A., Kahn B.B., and Neel B.G. PTP1B regulates leptin signal transduction in vivo. Dev. Cell. 2 (2002) 489-495
62. Cheng A., Uetani N., Simoncic P.D., Chaubey V.P., Lee-Loy A., McGlade C.J., Kennedy B.P., and Tremblay M.L. Attenuation of leptin action and regulation of obesity by protein tyrosine phosphatase 1B. Dev. Cell. 2 (2002) 497-503
63. Kaszubska W., Falls H.D., Schaefer V.G., Haasch D., Frost L., Hessler P., Kroeger P.E., White D.W., Jirousek M.R., and Trevillyan J.M. Protein tyrosine phosphatase 1B negatively regulates leptin signaling in a hypothalamic cell line. Mol. Cell Endocrinol. 195 (2002) 109-118
64. Bence K.K., Delibegovic M., Xue B., Gorgun C.Z., Hotamisligil G.S., Neel B.G., and Kahn B.B. Neuronal PTP1B regulates body weight, adiposity and leptin action. Nat. Med. 12 (2006) 917-924
65. Morrison C.D., White C.L., Wang Z., Lee S.Y., Lawrence D.S., Cefalu W.T., Zhang Z.Y., and Gettys T.W. Increased hypothalamic protein tyrosine phosphatase 1B contributes to leptin resistance with age. Endocrinology 148 (2007) 433-440
66. Picardi P.K., Calegari V.C., Prada P.O., Moraes J.C., Araujo E., Marcondes M.C., Ueno M., Carvalheira J.B., Velloso L.A., and Saad M.J. Reduction of hypothalamic protein tyrosine phosphatase improves insulin and leptin resistance in diet-induced obese rats. Endocrinology 149 (2008) 3870-3880
67. Elchebly M., Payette P., Michaliszyn E., Cromlish W., Collins S., Loy A.L., Normandin D., Cheng A., Himms-Hagen J., Chan C.C., Ramachandran C., Gresser M.J., Tremblay M.L., and Kennedy B.P. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283 (1999) 1544-1548
68. Emanuelli B., Peraldi P., Filloux C., Sawka-Verhelhe D., Hilton D.J., and Van Obberghen E. SOCS-3 is an insulin-induced negative regulator of insulin signaling. J. Biol. Chem. 275 (2000) 15985-15991
69. Shi H., Tzameli I., Bjorbaek C., and Flier J.S. Suppressor of cytokine signaling 3 is a physiological regulator of adipocyte insulin signaling. J Biol.Chem. 279 (2004) 34733-34740
70. Niswender K.D., and Schwartz M.W. Insulin and leptin revisited: adiposity signals with overlapping physiological and intracellular signaling capabilities. Front. Neuroendocrinol. 24 (2003) 1-10
71. Wang J., Obici S., Morgan K., Barzilai N., Feng Z., and Rossetti L. Overfeeding rapidly induces leptin and insulin resistance. Diabetes 50 (2001) 2786-2791
72. Woods S.C., D'Alessio D.A., Tso P., Rushing P.A., Clegg D.J., Benoit S.C., Gotoh K., Liu M., and Seeley R.J. Consumption of a high-fat diet alters the homeostatic regulation of energy balance. Physiol. Behav. 83 (2004) 573-578
73. Clegg D.J., Benoit S.C., Reed J.A., Woods S.C., Dunn-Meynell A., and Levin B.E. Reduced anorexic effects of insulin in obesity-prone rats fed a moderate-fat diet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005) R981-R986
74. Levin B.E., Dunn-Meynell A.A., and Banks W.A. Obesity-prone rats have normal blood-brain barrier transport but defective central leptin signaling before obesity onset. Am. J. Physiol. Regul. Integr.Comp. Physiol. 286 (2004) R143-R150
75. Levin B.E., Magnan C., Migrenne S., Chua Jr. S.C., and Dunn-Meynell A.A. F-DIO obesity-prone rat is insulin resistant before obesity onset. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 (2005) R704-R711
76. C.L. White, A. Whittington, M.J. Barnes, Z. Wang, G.A. Bray, C.D. Morrison, Increased hypothalamic PTP1B in response to diet-induced obesity and chronic hyperleptinemia. Am. J. Physiol. Endocrinol. Metab. Submitted (2008).
77. Lam T.K., Pocai A., Gutierrez-Juarez R., Obici S., Bryan J., guilar-Bryan L., Schwartz G.J., and Rossetti L. Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat. Med. 11 (2005) 320-327
78. Morgan K., Obici S., and Rossetti L. Hypothalamic responses to long-chain fatty acids are nutritionally regulated. J. Biol. Chem. 279 (2004) 31139-31148
79. Maness L.M., Banks W.A., and Kastin A.J. Persistence of blood-to-brain transport of leptin in obese leptin-deficient and leptin receptor-deficient mice. Brain Res. 873 (2000) 165-167
80. Harris R.B.S., Zhou J., Redmann Jr. S.M., Smagin G.N., Smith S.R., Rodgers E., and Zachwieja J.J. A leptin dose-response study in obese (ob/ob) and lean (+/?) mice. Endocrinology 139 (1998) 8-19
81. Boston B.A., Blaydon K.M., Varnerin J., and Cone R.D. Independent and additive effects of central POMC and leptin pathways on murine obesity. Science 278 (1997) 1641-1644
82. Benomar Y., Wetzler S., Larue-Achagiotis C., Djiane J., Tome D., and Taouis M. In vivo leptin infusion impairs insulin and leptin signalling in liver and hypothalamus. Mol. Cell Endocrinol. 242 (2005) 59-66
83. Shapiro A., Matheny M., Zhang Y., Tumer N., Cheng K.Y., Rogrigues E., Zolotukhin S., and Scarpace P.J. Synergy between leptin therapy and a seemingly negligible amount of voluntary wheel running prevents progression of dietary obesity in leptin-resistant rats. Diabetes 57 (2008) 614-622
84. Scarpace P.J., Matheny M., Tumer N., Cheng K.Y., and Zhang Y. Leptin resistance exacerbates diet-induced obesity and is associated with diminished maximal leptin signalling capacity in rats. Diabetologia 48 (2005) 1075-1083
85. Scarpace P.J., and Zhang Y. Elevated leptin: consequence or cause of obesity?. Front Biosci. 12 (2007) 3531-3544
86. Obici S., Feng Z., Morgan K., Stein D., Karkanias G., and Rossetti L. Central administration of oleic acid inhibits glucose production and food intake. Diabetes 51 (2002) 271-275
87. Obici S., Feng Z., Arduini A., Conti R., and Rossetti L. Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat. Med. 9 (2003) 756-761
88. Pocai A., Obici S., Schwartz G.J., and Rossetti L. A brain-liver circuit regulates glucose homeostasis. Cell Metab. 1 (2005) 53-61
89. Lam T.K., van de W.G., and Giacca A. Free fatty acids increase basal hepatic glucose production and induce hepatic insulin resistance at different sites. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E281-E290
90. Watson P.M., Commins S.P., Beiler R.J., Hatcher H.C., and Gettys T.W. Differential regulation of leptin release and function in A/J versus C57BL/6J mice during diet-induced obesity. Am. J. Physiol. 279 (2000) E356-E365
91. Harris R.B.S., Mitchell T.D., and Hebert S. Leptin-induced changes in body composition in high fat-fed mice. Exp. Biol. Med. 228 (2003) 24-32
92. Bowen H., Mitchell T.D., and Harris R.B.S. Method of leptin dosing, strain, and group housing influence leptin sensitivity in high-fat-fed weanling mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 (2003) R87-R100
93. Haltiner A.L., Mitchell T.D., and Harris R.B. Leptin action is modified by an interaction between dietary fat content and ambient temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 (2004) R1250-R1255
94. L.K. Stewart, Z. Wang, D. Ribnicky, J.L. Soileau, W.T. Cefalu, T.W. Gettys, Failure of dietary quercetin to alter the temporal progression of insulin resistance among tissues of C57BL/6J mice during the development of diet-induced obesity, Diabetologia (submitted for publication).
95. Beebe S.J., Redmon J.B., Blackmore P.F., and Corbin J.D. Discriminative insulin antagonism of stimulatory effects of various cAMP analogs on adipocyte lipolysis and hepatocyte glycogenolysis. J. Biol. Chem. 260 (1985) 15781-15788
96. Corbin J.D., Beebe S.J., Blackmore P.F., Redmon J.B., Sheorain V.S., and Gettys T.W. Discriminative insulin antagonism of effects of different cAMP analogs in intact mammalian cells. In: Belfrage P., Donner J., and Stralfors P. (Eds). Mechanisms of Insulin Action (1986), Elsevier Science Publishers, Amsterdam 167-174
97. Loten E.G., Assimacopoulos-Jeannet F.D., Exton J.H., and Park C.R. Stimulation of a low Km phosphodiesterase from liver by insulin and glucagon. J. Biol. Chem. 253 (1978) 746-757
98. 3-adrenergic receptor inhibits insulin-stimulated leptin secretion from isolated rat adipocytes. Endocrinology 137 (1996) 4054-4057