The role of key adipokines in obesity and insulin resistance in cats

Angela L. Lusby Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Claudia A. Kirk Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Joseph W. Bartges Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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  • 1.

    Anderson R. Obesity in the dog and cat. Vet Annu 1974;1441:182186.

  • 2.

    Lund EM, Armstrong PJ, Kirk CA, et al. Prevalence and risk factors for obesity in adult cats from private US veterinary practices. Int J Appl Res Vet Med 2005;3:8896.

    • Search Google Scholar
    • Export Citation
  • 3.

    Prahl A, Guptill L, Glickman NW, et al. Time trends and risk factors for diabetes mellitus in cats presented to veterinary teaching hospitals. J Feline Med Surg 2007;9:351358.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Halberg N, Wernstedt-Asterholm I, Scherer PE. The adipocyte as an endocrine cell. Endocrinol Metab Clin North Am 2008;37:753768.

  • 5.

    Halaas JL, Gajiwala KS, Maffei M, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 1995;269:543546.

  • 6.

    Zhang F, Chen Y, Heiman M, et al. Leptin: structure, function and biology. In: Litwack G, ed. Vitamins and hormones. Vol 71. San Diego: Academic Press Inc, 2005;345372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Munzberg H, Myers MG Jr. Molecular and anatomical determinants of central leptin resistance. Nat Neurosci 2005;8:566570.

  • 8.

    Oswal A, Yeo GSH. The leptin melanocortin pathway and the control of body weight: lessons from human and murine genetics. Obes Rev 2007;8:293306.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Horvath TL. Synaptic plasticity in energy balance regulation. Obesity (Silver Spring) 2006;14:228S–233S.

  • 10.

    Anukulkitch C, Rao A, Dunshea F, et al. A test of the lipostat theory in a seasonal (ovine) model under natural conditions reveals a close relationship between adiposity and melanin concentrating hormone expression. Domest Anim Endocrinol 2009;36:138151.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Münzberg H, Björnholm M, Bates SH, et al. Leptin receptor action and mechanisms of leptin resistance. Cell Mol Life Sci 2005;62:642652.

  • 12.

    Shimizu H, Oh-I S, Okada S, et al. Leptin resistance and obesity. Endocr J 2007;54:1726.

  • 13.

    Heymsfield SB, Greenberg AS, Fujioka K, et al. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA 1999;282:15681575.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Appleton DJ, Rand JS, Sunvold GD. Plasma leptin concentrations in cats: reference range, effect of weight gain and relationship with adiposity as measured by dual energy x-ray absorptiometry. J Feline Med Surg 2000;2:191199.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Backus RC, Havel PJ, Gingerich RL, et al. Relationship between serum leptin immunoreactivity and body fat mass as estimated by use of a novel gas-phase Fourier transform infrared spectroscopy deuterium dilution method in cats. Am J Vet Res 2000;61:796801.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Park S, Hong SM, Sung SR, et al. Long-term effects of central leptin and resistin on body weight, insulin resistance, and B-cell function and mass by the modulation of hypothalamic leptin and insulin signaling. Endocrinology 2008;149:445454.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Griffin ME, Marcucci MJ, Cline GW, et al. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes 1999;48:12701274.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Boden G. Effects of free fatty acids (FFA) on glucose metabolism: significance for insulin resistance and type 2 diabetes. Exp Clin Endocrinol Diabetes 2003;111:121124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Dyck DJ, Heigenhauser GJF, Bruce CR. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol 2006;186:516.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Sell H, Dietze-Schroeder D, Eckel J. The adipocyte-myocyte axis in insulin resistance. Trends Endocrinol Metab 2006;17:416422.

  • 21.

    Benomar Y, Wetzler S, Larue-Achagiotis C, et al. In vivo leptin infusion impairs insulin and leptin signalling in liver and hypothalamus. Mol Cell Endocrinol 2005;242:5966.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Ceddia RB, Koistinen HA, Zierath JR, et al. Analysis of paradoxical observations on the association between leptin and insulin resistance. FASEB J 2002;16:11631176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Martin LJM, Siliart B, Dumon HJW, et al. Spontaneous hormonal variations in male cats following gonadectomy. J Feline Med Surg 2006;8:309314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Hoenig M, Thomaseth K, Waldron M, et al. Insulin sensitivity, fat distribution, and adipocytokine response to different diets in lean and obese cats before and after weight loss. Am J Physiol Regul Integr Comp Physiol 2007;292:R227–R234.

    • Search Google Scholar
    • Export Citation
  • 25.

    Appleton DJ, Rand JS, Sunvold GD. Plasma leptin concentrations are independently associated with insulin sensitivity in lean and overweight cats. J Feline Med Surg 2002;4:8393.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Backus RC, Cave NJ, Keisler DH. Gonadectomy and high dietary fat but not high dietary carbohydrate induce gains in body weight and fat of domestic cats. Br J Nutr 2007;98:641650.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Belsito KR, Vester BM, Keel T, et al. Impact of ovariohysterectomy and food intake on body composition, physical activity, and adipose gene expression in cats. J Anim Sci 2009;87:594602.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Kanchuk ML, Backus RC, Calvert CC, et al. Neutering induces changes in food intake, body weight, plasma insulin and leptin concentrations in normal and lipoprotein lipase-deficient male cats. J Nutr 2002;132:1730S–1732S.

    • Search Google Scholar
    • Export Citation
  • 29.

    Hoenig M, Ferguson DC. Effects of neutering on hormonal concentrations and energy requirements in male and female cats. Am J Vet Res 2002;63:634639.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Coenen KR, Gruen ML, Chait A, et al. Diet-induced increases in adiposity, but not plasma lipids, promote macrophage infiltration into white adipose tissue. Diabetes 2007;56:564573.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Weisberg SP, McCann D, Desai M, et al. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:17961808.

  • 32.

    Cinti S, Mitchell G, Barbatelli G, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005;46:23472355.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Cawthorn WP, Sethi JK. TNF-alpha and adipocyte biology. FEBS Lett 2008;582:117131.

  • 34.

    Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993;259:8791.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Ryden M, Arner P. Tumour necrosis factor-alpha in human adipose tissue—from signalling mechanisms to clinical implications. J Intern Med 2007;262:431438.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Mohamed-Ali V, Goodrick S, Rawesh A, et al. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 1997;82:41964200.

    • Search Google Scholar
    • Export Citation
  • 37.

    Miller C, Bartges J, Cornelius L, et al. Tumor necrosis factor-alpha levels in adipose tissue of lean and obese cats. J Nutr 1998;128:2751S–2752S.

    • Search Google Scholar
    • Export Citation
  • 38.

    Hoenig M, McGoldrick JB, deBeer M, et al. Activity and tissue-specific expression of lipases and tumor-necrosis factor alpha in lean and obese cats. Domest Anim Endocrinol 2006;30:333344.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Peraldi P, Xu M, Spiegelman BM. Thiazolidinediones block tumor necrosis factor-alpha induced inhibition of insulin signaling. J Clin Invest 1997;100:18631869.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Boden G. Obesity and free fatty acids. Endocrinol Metab Clin North Am 2008;37:635646.

  • 41.

    Kim KY, Kim JK, Jeon JH, et al. c-Jun N-terminal kinase is involved in the suppression of adiponectin expression by TNF-alpha in 3T3–L1 adipocytes. Biochem Biophys Res Commun 2005;327:460467.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Kita A, Yamasaki H, Kuwahara H, et al. Identification of the promoter region required for human adiponectin gene transcription: association with CCAAT/enhancer binding protein-beta and tumor necrosis factor-alpha. Biochem Biophys Res Commun 2005;331:484490.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Arita Y, Kihara S, Ouchi N, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999;257:7983.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Swarbrick MM, Havel PJ. Physiological, pharmacological, and nutritional regulation of circulating adiponectin concentrations in humans. Metab Syndr Relat Disord 2008;6:87102.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Iwaki M, Matsuda M, Maeda N, et al. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 2003;52:16551663.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Waki H, Yamauchi T, Kamon J, et al. Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology 2005;146:790796.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Pajvani UB, Hawkins M, Combs TP, et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem 2004;279:1215212162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48.

    Fisher FF, Trujillo ME, Hanif W, et al. Serum high molecular weight complex of adiponectin correlates better with glucose tolerance than total serum adiponectin in Indo-Asian males. Diabetologia 2005;48:10841087.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Matsuzawa Y. Adiponectin: identification, physiology and clinical relevance in metabolic and vascular disease. Atheroscler Suppl 2005;6:714.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50.

    Weyer C, Funahashi T, Tanaka S, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 2001;86:19301935.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51.

    Kantartzis K, Fritsche A, Tschritter O, et al. The association between plasma adiponectin and insulin sensitivity in humans depends on obesity. Obes Res 2005;13:16831691.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 52.

    Tschritter O, Fritsche A, Thamer C, et al. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes 2003;52:239243.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 53.

    Hotta K, Funahashi T, Bodkin NL, et al. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes 2001;50:11261133.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54.

    Lindsay RS, Funahashi T, Hanson RL, et al. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 2002;360:5758.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55.

    Yamamoto Y, Hirose H, Saito I, et al. Adiponectin, an adipocyte-derived protein, predicts future insulin resistance: two-year follow-up study in Japanese population. J Clin Endocrinol Metab 2004;89:8790.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56.

    Snehalatha C, Mukesh B, Simon M, et al. Plasma adiponectin is an independent predictor of type 2 diabetes in Asian Indians. Diabetes Care 2003;26:32263229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 57.

    Karbowska J, Kockan Z. Role of adiponectin in the regulation of carbohydrate and lipid metabolism. J Physiol Pharmacol 2006;57:103113.

    • Search Google Scholar
    • Export Citation
  • 58.

    Berg AH, Combs TP, Du X, et al. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 2001;7:947953.

  • 59.

    Combs TP, Berg AH, Obici S, et al. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest 2001;108:18751881.

  • 60.

    Deepa SS, Dong LQ. APPL1: role in adiponectin signaling and beyond. Am J Physiol Endocrinol Metab 2009;296:E22–E36.

  • 61.

    Rogers QR, Morris JG, Freedland RA. Lack of hepatic enzymatic adaptation to low and high levels of dietary protein in the adult cat. Enzyme 1977;22:348356.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62.

    Zoran DL. The carnivore connection to nutrition in cats. J Am Vet Med Assoc 2002;221:15591567.

  • 63.

    Ishioka K, Omachi A, Sasaki N, et al. Feline adiponectin: molecular structures and plasma concentrations in obese cats. J Vet Med Sci 2009;71:189194.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64.

    Zini E, Linscheid P, Franchini M, et al. Partial sequencing and expression of genes involved in glucose metabolism in adipose tissues and skeletal muscle of healthy cats. Vet J 2009;180:6670.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 65.

    Hernandez-Morante JJ, Milagro FI, Larque E, et al. Relationship among adiponectin, adiponectin gene expression and fatty acids composition in morbidly obese patients. Obes Surg 2007;17:516524.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66.

    Lihn AS, Bruun JM, He G, et al. Lower expression of adiponectin mRNA in visceral adipose tissue in lean and obese subjects. Mol Cell Endocrinol 2004;219:915.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 67.

    Fisher FM, McTernan PG, Valsamakis G, et al. Differences in adiponectin protein expression: effect of fat depots and type 2 diabetic status. Horm Metab Res 2002;34:650654.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 68.

    Claessens M, van Baak MA, Monsheimer S, et al. The effect of a low-fat, high-protein or high-carbohydrate ad libitum diet on weight loss maintenance and metabolic risk factors. Int J Obes 2009;33:296304.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 69.

    Riera-Guardia N, Rothenbacher D. The effect of thiazolidinediones on adiponectin serum level: a meta-analysis. Diabetes Obes Metab 2008;10:367375.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 70.

    Hoenig M, Ferguson DC. Effect of darglitazone on glucose clearance and lipid metabolism in obese cats. Am J Vet Res 2003;64:14091413.

  • 71.

    Lusby A, Kirk C. Obesity. In: Bonagura J, Twedt DC, eds. Kirk's current veterinary therapy XIV. Philadelphia: Saunders, 2008;191195.

  • 72.

    Scarlett JM, Donoghue S. Associations between body condition and disease in cats. J Am Vet Med Assoc 1998;212:17251731.

  • 73.

    Buffington CA. External and internal influences on disease risk in cats. J Am Vet Med Assoc 2002;220:9941002.

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