Adipokines: Inflammation and the pleiotropic role of white adipose tissue

British Journal of Nutrition

Volumn 92, Issue 3, 2004, Pages 347-355

  Trayhurn, Paul ^a   Wood, I Stuart ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Acute phase proteins; Adipokines; Cytokines; Hypoxia; Inflammation; Obesity; White adipose tissue

Indexed keywords

ACUTE PHASE PROTEIN; ADIPOCYTOKINE; ADIPONECTIN; AMYLOID A PROTEIN; CELL PROTEIN; CYTOKINE; FATTY ACID; HAPTOGLOBIN; HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; LIPID; NERVE GROWTH FACTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROSTAGLANDIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PROTEIN;

ACUTE PHASE RESPONSE; ADIPOCYTE; ANGIOGENESIS; ARTICLE; BLOOD PRESSURE REGULATION; CELL TYPE; COMPLEMENT SYSTEM; CYTOKINE PRODUCTION; ENDOCRINE FUNCTION; ENERGY BALANCE; HEMOSTASIS; HORMONE RELEASE; HYPOXIA; INFLAMMATION; INSULIN SENSITIVITY; LIPID METABOLISM; LIPID STORAGE; MACROPHAGE; METABOLIC SYNDROME X; OBESITY; PARSIMONY ANALYSIS; PROTEIN SECRETION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; ANOXIA; HUMAN; METABOLISM; NOMENCLATURE; REVIEW;

ACUTE-PHASE PROTEINS; ADIPOCYTES; ADIPOSE TISSUE; ANOXIA; CYTOKINES; HUMANS; INFLAMMATION; OBESITY; PROTEINS; TERMINOLOGY;

EID: 6944237757     PISSN: 00071145     EISSN: None     Source Type: Journal    
DOI: 10.1079/BJN20041213     Document Type: Article

References (85)

1. Ahima RS, Prabakaran D, Mantzoros C, Qu DQ, Lowell B, Maratos-Flier E & Flier JS (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382, 250-252.
2. Alessi MC, Bastelica D, Morange P, Berthet B, Leduc I, Verdier M, Geel O & Juhan-Vague I (2000) Plasminogen activator inhibitor 1, TGFβ1, and BMI are closely associated in human adipose tissue during morbid obesity. Diabetes 49, 1374-1380.
3. Ambrosini G, Nath AK, Sierra-Honigmann MR & Flores-Riveros J (2002) Transcriptional activation of the human leptin gene in response to hypoxia. Involvement of hypoxia-inducible factor 1. J Biol Chem 277, 34601-34609.
4. Arita Y, Kihara S, Ouchi N, et al. (1999) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257, 79-83.
5. Bastard JP, Jardel C, Bruckert E, Blondy P, Capeau J, Laville M, Vidal H & Hainque B (2000) Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J Clin Endocrinol Metab 85, 3338-3342.
6. Berg AH, Combs TP, Du X, Brownlee M & Scherer PE (2001) The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nature Med 7, 947-953.
7. Binley K, Kan O, White J & Naylor S (2003) Exploiting the hypoxia response. Curr Opin Mol Ther 5, 650-656.
8. Bruun JM, Pedersen SB & Richelsen B (2000) Interleukin-8 production in human adipose tissue. Inhibitory effects of anti-diabetic compounds, the thiazolidinedione ciglitazone and the biguanide metformin. Horm Metab Res 32, 537-541.
9. Bruun JM, Pedersen SB & Richelsen B (2001) Regulation of interleukin 8 production and gene expression in human adipose tissue in vitro. J Clin Endocrinol Metab 86, 1267-1273.
10. Bulló M, Garcia-Lorda P, Megias I & Salas-Salvado J (2003) Systemic inflammation, adipose tissue tumor necrosis factor, and leptin expression. Obesity Res 11, 525-531.
11. Chaldakov GN, Stankulov IS, Fiore M, Ghenev PI & Aloe L (2001) Nerve growth factor levels and mast cell distribution in human coronary atherosclerosis. Atherosclerosis 159, 57-66.
12. Chiellini C, Bertacca A, Novelli SE, et al. (2002) Obesity modulates the expression of haptoglobin in the white adipose tissue via TNFα. J Cell Physiol 190, 251-258.
13. Chinetti G, Fruchart JC & Staels B (2003) Peroxisome proliferator-activated receptors and inflammation: from basic science to clinical applications. Int J Obesity 27, Suppl. 3, S41-S45.
14. Cigolini M, Tonoli M, Borgato L, et al. (1999) Expression of plasminogen activator inhibitor-1 in human adipose tissue: a role for TNF-α? Atherosclerosis 143, 81-90.
15. Claffey KP, Wilkison WO & Spiegelman BM (1992) Vascular endothelial growth factor. Regulation by cell differentiation and activated second messenger pathways. J Biol Chem 267, 16317-16322.
16. Cook KS, Groves DL, Min HY & Spiegelman BM (1985) A developmentally regulated mRNA from 3T3 adipocytes encodes a novel serine protease homologue. Proc Natl Acad Sci USA 82, 6480-6484.
17. Cook KS, Min HY, Johnson D, Chaplinsky RJ, Flier JS, Hunt CR & Spiegelman BM (1987) Adipsin: a circulating serine protease homolog secreted by adipose tissue and sciatic nerve. Science 237, 402-405.
18. Coppack SW (2001) Pro-inflammatory cytokines and adipose tissue. Proc Nutr Soc 60, 349-356.
19. Das UN (2001) Is obesity an inflammatory condition? Nutrition 17, 953-966.
20. Dietze D, Koenen M, Rohrig K, Horikoshi H, Hauner H & Eckel J (2002) Impairment of insulin signaling in human skeletal muscle cells by co-culture with human adipocytes. Diabetes 51, 2369-2376.
21. Ehrhart-Bornstein M, Lamounier-Zepter V, Schraven A, Langenbach J, Willenberg HS, Barthel A, Hauner H, McCann SM, Scherbaum WA & Bornstein SR (2003) Human adipocytes secrete mineralocorticoid-releasing factors. Proc Natl Acad Sci USA 100 14211-14216.
22. Engeli S, Feldpausch M, Gorzelniak K, Hartwig F, Heintze U, Janke J, Mohlig M, Pfeiffer AFH, Luft FC & Sharma AM (2003) Association between adiponectin and mediators of inflammation in obese women. Diabetes 52, 942-947.
23. Engström G, Hedblad B, Stavenow L, Lind P, Janzon L & Lindgärde F (2003) Inflammation-sensitive plasma proteins are associated with future weight gain. Diabetes 52, 2097-2101.
24. Eriksson P, Reynisdottir S, Lonnqvist F, Stemme V, Hamsten A & Arner P (1998) Adipose tissue secretion of plasminogen activator inhibitor-1 in non-obese and obese individuals. Diabetologia 41 65-71.
25. Esposito K, Pontillo A, Ciotola M, Di Palo C, Grella E, Nicoletti G & Giugliano D (2002) Weight loss reduces interleukin-18 levels in obese women. J Clin Endocrinol Metab 87, 3864-3866.
26. Esposito K, Pontillo A, Giugliano F, Giugliano G, Marfella R, Nicoletti G & Giugliano D (2003) Association of low interleukin-10 levels with the metabolic syndrome in obese women. J Clin Endocrinol Metab 88, 1055-1058.
27. Fain JN, Bahouth SW & Madan AK (2004a) Haptoglobin release by human adipose tissue in primary culture. J Lipid Res 45, 536-542.
28. Fain JN, Madan AK, Hiler ML, Cheema P & Bahouth SW (2004b Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145, 2273-2282.
29. Festa A, D'Agostino R Jr, Williams K, Karter AJ, Mayer-Davis EJ, Tracy RP & Haffner SM (2001) The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obesity 25, 1407-1415.
30. Friedrichs WE, Navarijo-Ashbaugh AL, Bowman BH & Yang F (1995) Expression and inflammatory regulation of haptoglobin gene in adipocytes. Biochem Biophys Res Commun 209, 250-256.
31. Frühbeck G, Gómez-Ambrosi J, Muruzabal FJ & Burrell MA (2001) The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am J Physiol 280, E827-E847.
32. Funahashi T, Nakamura T, Shimomura I, Maeda K, Kuriyama H, Takahashi M, Arita Y, Kihara S & Matsuzawa Y (1999) Role of adipocytokines on the pathogenesis of atherosclerosis in visceral obesity. Intern Med 38, 202-206.
33. Gabay C & Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. New Engl J Med 340, 448-454.
34. Hasan W, Zhang R, Liu M, Warn JD & Smith PG (2000) Coordinate expression of NGF and alpha-smooth muscle actin mRNA and protein in cutaneous wound tissue of developing and adult rats. Cell Tissue Res 300, 97-109.
35. Heinrich PC, Castell JV & Andus T (1990) Interleukin-6 and the acute phase response. Biochem J 265, 621-636.
36. Hellwig-Bürgel T, Rutkowski K, Metzen E, Fandrey J & Jelkmann W (1999) Interleukin-1β and tumor necrosis factor-α stimulate DNA binding of hypoxia-inducible factor-1. Blood 94, 1561-1567.
37. Höpfl G, Ogunshola O & Gassmann M (2004) HIFs and tumors - causes and consequences. Am J Physiol 286, R608-R623.
38. Hotamisligil GS (2003) Inflammatory pathways and insulin action. Int J Obesity 27, Suppl. 3, S53-S55.
39. Hotamisligil GS, Shargill NS & Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha - direct role in obesity-linked insulin resistance. Science 259, 87-91.
40. Hotta K, Funahashi T, Arita Y, et al. (2000) Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscl Thromb Vasc Biol 20, 1595-1599.
41. Kersten S, Mandard S, Tan NS, Escher P, Metzger D, Chambon P, Gonzalez FJ, Desvergne B & Wahli W (2000) Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem 275, 28488-28493.
42. Klaus S (2004) Adipose tissue as a regulator of energy balance. Curr Drug Targets 4, 1-10.
43. Kratchmarova I, Kalume DE, Blagoev B, et al. (2002) A proteomic approach for identification of secreted proteins during the differentiation of 3T3-L1 preadipocytes to adipocytes. Mol Cell Proteomics 1, 213-222.
44. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L & Leon A (1996) Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19, 514-520.
45. Lin Y, Rajala MW, Berger JP, Moller DE, Barzilai N & Scherer PE (2001) Hyperglycemia-induced production of acute phase reactants in adipose tissue. J Biol Chem 276, 42077-42083.
46. Lolmede K, Durand de Saint Front V, Galitzky J, Lafontan M & Bouloumie A (2003) Effects of hypoxia on the expression of proangiogenic factors in differentiated 3T3-F442A adipocytes. Int J Obesity 27 1187-1195.
47. Lundgren CH, Brown SL, Nordt TK, Sobel BE & Fujii S (1996) Elaboration of type-1 plasminogen activator inhibitor from adipocytes - a potential pathogenetic link between obesity and cardiovascular disease. Circulation 93, 106-110.
48. Mohamed-Ali V, Goodrick S, Rawesh A, Katz DR, Miles JM, Yudkin JS, Klein S & Coppack SW (1997) Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 82, 4196-4200.
49. Mohamed-Ali V, Pinkney JH & Coppack SW (1998) Adipose tissue as an endocrine and paracrine organ. Int J Obesity 22, 1145-1158.
50. Moller DE & Berger JP (2003) Role of PPARs in the regulation of obesity-related insulin sensitivity and inflammation. Int J Obesity 27, Suppl. 3, S17-S21.
51. Mutch NJ, Wilson HM & Booth NA (2001) Plasminogen activator inhibitor-1 and haemostasis in obesity. Proc Nutr Soc 60, 341-347.
52. Oller do Nascimento C, Hunter L & Trayhurn P (2004) Regulation of haptoglobin gene expression in 3T3-L1 adipocytes by cytokines, catecholamines, and PPARγ. Biochem Biophys Res Commun 313, 702-708.
53. Ouchi N, Kihara S, Arita Y, et al. (1999) Novel modulator for endothelial adhesion molecules - adipocyte-derived plasma protein adiponectin. Circulation 100, 2473-2476.
54. Ouchi N, Kihara S, Funahashi T, et al. (2003) Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation 107, 671-674.
55. Pannacciulli N, Cantatore FP, Minenna A, Bellacicco M, Giorgino R & De Pergola G (2001) C-reactive protein is independently associated with total body fat, central fat, and insulin resistance in adult women. Int J Obesity 25, 1416-1420.
56. Peeraully MR, Jenkins JR & Trayhum P (2004) NGF gene expression and secretion in white adipose tissue: regulation in 3T3-L1 adipocytes by hormones and inflammatory cytokines. Am J Physiol 287 (In the Press).
57. Prins JB, Niesler CU, Winterford CM, Bright NA, Siddle K, Orahilly S, Walker NI & Cameron DP (1997) Tumor necrosis factor-alpha induces apoptosis of human adipose cells. Diabetes 46, 1939-1944.
58. Rajala MW & Scherer PE (2003) Minireview: the adipocyte - at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144, 3765-3773.
59. Rayner DV & Trayhurn P (2001) Regulation of leptin production: sympathetic nervous system interactions. J Mol Med 79, 8-20.
60. Rupnick MA, Panigrahy D, Zhang C-Y, Dallabrida SM, Lowell BB, Langer R & Folkman MJ (2002) Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA 99, 10730-10735.
61. Samad F, Yamamoto K & Loskutoff DJ (1996) Distribution and regulation of plasminogen activator inhibitor-1 in murine adipose tissue in vivo - induction by tumor necrosis factor-α and lipopolysaccharide. J Clin Invest 97, 37-46.
62. Semenza GL (2001) HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 13, 167-171.
63. Soukas A, Cohen P, Socci ND & Friedman JM (2000) Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev 14, 963-980.
64. Starnes T, Broxmeyer HE, Robertson MJ & Hromas R (2002) Cutting edge: IL-17D, a novel member of the IL-17 family, stimulates cytokine production and inhibits hemopoiesis. J Immunol 169, 642-646.
65. Straczkowski M, Dzienis-Straczkowska S, Stepien A, Kowalska I, Szelachowska M & Kinalska I (2002) Plasma interleukin-8 concentrations are increased in obese subjects and related to fat mass and tumor necrosis factor-α system. J Clin Endocrinol Metab 87, 4602-4606.
66. Tchernof A, Nolan A, Sites CK, Ades PA & Poehlman ET (2002) Weight loss reduces C-reactive protein levels in obese postmenopausal women. Circulation 105, 564-569.
67. Trayhurn P & Beattie JH (2001) Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc Nutr Soc 60, 329-339.
68. Uhlar CM & Whitehead AS (1999) Serum amyloid A, the major vertebrate acute-phase reactant. Eur J Biochem 265, 501-523.
69. Vega JA, Garcia-Suarez O, Hannestad J, Perez-Perez M & Germana A (2003) Neurotrophins and the immune system. J Anat 203 1-19.
70. Visser M, Bouter LM, McQuillan GM, Wener MH & Harris TB (1999) Elevated C-reactive protein levels in overweight and obese adults. J Am Med Assoc 282, 2131-2135.
71. Volanakis JE (2001) Human C-reactive protein: expression, structure, and function. Mol Immunol 38, 189-197.
72. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C & Pratley RE (2001) Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obesity Res 9, 414-417.
73. Wallenius K, Wallenius V, Sunter D, Dickson SL & Jansson JO (2002) Intracerebroventricular interleukin-6 treatment decreases body fat in rats. Biochem Biophys Res Commun 293, 560-565.
74. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL & Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 1796-1808.
75. 2-regulated gene expression. FASEB J 16, 1151-1162.
76. Wiesner G, Morash BA, Ur E & Wilkinson M (2004) Food restriction regulates adipose-specific cytokines in pituitary gland but not in hypothalamus. J Endocrinol 180, R1-R6.
77. Xu H, Barnes GT, Yang Q, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112, 1821-1830.
78. Yamauchi T, Kamon J, Waki H, et al. (2001) The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nature Med 7, 941-946.
79. Yang YS, Song HD, Li RY, Zhou LB, Zhu ZD, Hu RM, Han ZG & Chen JL (2003) The gene expression profiling of human visceral adipose tissue and its secretory functions. Biochem Biophys Res Commun 300, 839-846.
80. Yokota T, Oritani K, Takahashi I, et al. (2000) Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 96, 1723-1732.
81. Yoon JC, Chickering TW, Rosen ED, Dussault B, Qin Y, Soukas A, Friedman JM, Holmes WE & Spiegelman BM (2000) Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol Cell Biol 20, 5343-5349.
82. Yudkin JS (2003) Adipose tissue, insulin action and vascular disease: inflammatory signals. Int J Obesity 27, Suppl. 3, S25-S28.
83. Yudkin JS, Kumari M, Humphries SE & Mohamed-Ali V (2000) Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 148, 209-214.
84. Yudkin JS, Stehouwer CD, Emeis JJ & Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19, 972-978.
85. Zhang YY, Proenca R, Maffei M, Barone M, Leopold L & Friedman JM (1994) Positional cloning of the mouse obese gene and its human homolog. Nature 372, 425-432.