Mechanism and clinical evidence of lipocalin-2 and adipocyte fatty acid-binding protein linking obesity and atherosclerosis

Diabetes/Metabolism Research and Reviews

Volumn 30, Issue 6, 2014, Pages 447-456

  Wu, Guangyu ^a,b   Li, Huating ^a   Zhou, Mi ^a   Fang, Qichen ^a   Bao, Yuqian ^a   Xu, Aimin ^c,d   Jia, Weiping ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Adipocyte fatty acid binding protein; Atherosclerosis; Lipocalin 2; Obesity

Indexed keywords

FATTY ACID BINDING PROTEIN 4; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ACUTE PHASE PROTEIN; ADIPOCYTOKINE; BIOLOGICAL MARKER; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; LCN2 PROTEIN, HUMAN; LIPOCALIN; ONCOPROTEIN;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CHRONIC INFLAMMATION; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; FOAM CELL; GLUCOSE METABOLISM; HUMAN; INSULIN SENSITIVITY; NONHUMAN; OBESITY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; ADIPOSE TISSUE; ANIMAL; BIOLOGICAL MODEL; BLOOD; EVIDENCE BASED MEDICINE; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; SECRETION (PROCESS); VASCULAR ENDOTHELIUM;

ACUTE-PHASE PROTEINS; ADIPOKINES; ADIPOSE TISSUE; ANIMALS; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; ENDOTHELIUM, VASCULAR; EVIDENCE-BASED MEDICINE; FATTY ACID-BINDING PROTEINS; HUMANS; LIPOCALINS; MODELS, BIOLOGICAL; OBESITY; PROTO-ONCOGENE PROTEINS;

EID: 84899428263     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.2493     Document Type: Review

References (89)

1. Whitlock G, Lewington S, Sherliker P, et al. Body-mass index and cause-specific mortality in 900000 adults: collaborative analyses of 57 prospective studies. Lancet 2009; 373: 1083-1096.
2. Ferroni P, Basili S, Falco A, Davi G. Inflammation, insulin resistance, and obesity. Curr Atheroscler Rep 2004; 6: 424-431.
3. Shoelson SE, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007; 132: 2169-2180.
4. Li FY, Cheng KK, Lam KS, Vanhoutte PM, Xu A. Cross-talk between adipose tissue and vasculature: role of adiponectin. Acta Physiol (Oxf) 2011; 203: 167-180.
5. Tso AW, Xu A, Chow WS, Lam KS. Adipose tissue and the metabolic syndrome: focusing on adiponectin and several novel adipokines. Biomarkers Med 2008; 2: 239-252.
6. Zhang J, Wu Y, Zhang Y, et al. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol Endocrinol 2008; 22: 1416-1426.
7. Giasson J, Li GH, Chen Y. Neutrophil gelatinase-associated lipocalin (NGAL) as a new biomarker for non-acute kidney injury (AKI) diseases. Inflamm Allergy Drug Targets 2011; 10: 272-282.
8. Kjeldsen L, Johnsen AH, Sengeløv H, Borregaard N. Isolation and primary structure of NGAL: a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993; 268: 10425-10432.
9. Goetz DH, Willie ST, Armen RS, et al. Ligand preference inferred from the structure of neutrophil gelatinase associated lipocalin. Biochemistry 2000; 39: 1935-1941.
10. Bratt T, Ohlson S, Borregaard N. Interactions between neutrophil gelatinase-associated lipocalin and natural lipophilic ligands. Biochim Biophys Acta 1999; 1472: 262.
11. Flo TH, Smith KD, Sato S, et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432: 917-921.
12. Devireddy LR, Teodoro JG, Richard FA, Green MR. Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by interleukin-3 deprivation. Science 2001; 293: 829-834.
13. Melino M, Gadd VL, Walker GV, et al. Macrophage secretory products induce an inflammatory phenotype in hepatocytes. World J Gastroenterol 2012; 18: 1732-1744.
14. Pawluczyk IZ, Furness PN, Harris KP. Macrophage-induced rat mesangial cell expression of the 24p3-like protein α2-microglobulin-related protein. Biochim Biophys Acta 2003; 1645: 218-227.
15. Yan QW, Yang Q, Mody N, et al. The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 2007; 56: 2533-2540.
16. Bu DX, Hemdahl AL, Gabrielsen A, et al. Induction of neutrophil gelatinase-associated lipocalin in vascular injury via activation of nuclear factor-κB. Am J Pathol 2006; 169: 2245-2253.
17. Glaros T, Fu Y, Xing J, Li L. Molecular mechanism underlying persistent induction of LCN2 by lipopolysaccharide in kidney fibroblasts. PLoS One 2012; 7: e34633.
18. Guo H, Jin D, Zhang Y, et al. Lipocalin-2 deficiency impairs thermogenesis and potentiates diet-induced insulin resistance in mice. Diabetes 2010; 59: 1376-1385.
19. Law IK, Xu A, Lam KS, et al. Lipocalin-2 deficiency attenuates insulin resistance associated with aging and obesity. Diabetes 2010; 59: 872-882.
20. Jun LS, Siddall CP, Rosen ED. A minor role for lipocalin 2 in high-fat diet-induced glucose intolerance. Am J Physiol Endocrinol Metab 2011; 301: E825-E835.
21. Aigner F, Maier HT, Schwelberger HG, et al. Lipocalin-2 regulates the inflammatory response during ischemia and reperfusion of the transplanted heart. Am J Transpl 2007; 7: 779-788.
22. Jin D, Guo H, Bu SY, et al. Lipocalin 2 is a selective modulator of peroxisome proliferator-activated receptor-gamma activation and function in lipid homeostasis and energy expenditure. FASEB J 2011; 25: 754-764.
23. Hemdahl AL, Gabrielsen A, Zhu C, et al. Expression of neutrophil gelatinase-associated lipocalin in atherosclerosis and myocardial infarction. Arterioscler Thromb Vasc Biol 2006; 26: 136-142.
24. Yndestad A, Landro L, Ueland T, et al. Increased systemic and myocardial expression of neutrophil gelatinase-associated lipocalin in clinical and experimental heart failure. Eur Heart J 2009; 30: 1229-1236.
25. Abel ED, Litwin SE, Sweeney G. Cardiac remodeling in obesity. Physiol Rev 2008; 88: 389-419.
26. te Boekhorst BC, Bovens SM, Hellings WE, et al. Molecular MRI of murine atherosclerotic plaque targeting NGAL: a protein associated with unstable human plaque characteristics. Cardiovasc Res 2011; 89: 680-688.
27. Van den Steen PE, Dubois B, Nelissen I, et al. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002; 37: 375-536.
28. Yan L, Borregaard N, Kjeldsen L, Moses MA. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001; 276: 37258-37265.
29. Hutchinson KR, Stewart JA Jr, Lucchesi PA. Extracellular matrix remodeling during the progression of volume overload-induced heart failure. J Mol Cell Cardiol 2010; 48: 564-569.
30. Liu JT, Song E, Xu A, et al. Lipocalin-2 deficiency prevents endothelial dysfunction associated with dietary obesity: role of cytochrome P450 2C inhibition. Br J Pharmacol 2012; 165: 520-531.
31. Hamzic N, Blomqvist A, Nilsberth C. Immune-induced expression of lipocalin-2 in brain endothelial cells: relationship with interleukin-6, cyclooxygenase-2 and the febrile response. J Neuroendocrinol 2013; 25: 271-280.
32. Latouche C, El Moghrabi S, Messaoudi S, et al. Neutrophil gelatinase-associated lipocalin is a novel mineralocorticoid target in the cardiovascular system. Hypertension 2012; 59: 966-972.
33. Xu G, Ahn J, Chang S, et al. Lipocalin-2 induces cardiomyocyte apoptosis by increasing intracellular iron accumulation. J Biol Chem 2012; 287: 4808-4817.
34. Lee YH, Lee SH, Jung ES, et al. Visceral adiposity and the severity of coronary artery disease in middle-aged subjects with normal waist circumference and its relation with lipocalin-2 and MCP-1. Atherosclerosis 2010; 213: 592-597.
35. Corripio R, Gonzalez-Clemente JM, Perez-Sanchez J, et al. Weight loss in prepubertal obese children is associated with a decrease in adipocyte fatty acid-binding protein without changes in lipocalin-2: a 2-year longitudinal study. Eur J Endocrinol 2010; 163: 887-893.
36. Wang Y, Lam KS, Kraegen EW, et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 2007; 53: 34-41.
37. Moreno-Navarrete JM, Manco M, Ibanez J, et al. Metabolic endotoxemia and saturated fat contribute to circulating NGAL concentrations in subjects with insulin resistance. Int J Obes (Lond) 2010; 34: 240-249.
38. Huang Y, Yang Z, Ye Z, et al. Lipocalin-2, glucose metabolism and chronic low-grade systemic inflammation in Chinese people. Cardiovasc Diabetol 2012; 11: 11.
39. El-Mesallamy HO, Hamdy NM, Sallam AA. Effect of obesity and glycemic control on serum lipocalins and insulin-like growth factor axis in type 2 diabetic patients. Acta Diabetol 2012 Feb 4. [Epub ahead of print] doi:10.1007/s00592-012-0373-6.
40. Xiao Y, Xu A, Hui X, et al. Circulating lipocalin-2 and retinol-binding protein 4 are associated with intima-media thickness and subclinical atherosclerosis in patients with type 2 diabetes. PLoS One 2013; 8: e66607.
41. Choi KM, Lee JS, Kim EJ, et al. Implication of lipocalin-2 and visfatin levels in patients with coronary heart disease. Eur J Endocrinol 2008; 158: 203-207.
42. Ding L, Hanawa H, Ota Y, et al. Lipocalin-2/neutrophil gelatinase-B associated lipocalin is strongly induced in hearts of rats with autoimmune myocarditis and in human myocarditis. Circ J 2010; 74: 523-530.
43. Falke P, Elneihoum AM, Ohlsson K. Leukocyte activation: relation to cardiovascular mortality after cerebrovascular ischemia. Cerebrovasc Dis 2000; 10: 97-101.
44. Bolignano D, Basile G, Parisi P, et al. Increased plasma neutrophil gelatinase-associated lipocalin levels predict mortality in elderly patients with chronic heart failure. Rejuv Res 2009; 12: 7-14.
45. Makowski L, Hotamisligil GS. Fatty acid binding proteins-the evolutionary crossroads of inflammatory and metabolic responses. J Nutrit 2004; 134: 2464-2468S.
46. Pelton PD, Zhou L, Demarest KT, Burris TP. PPARγ activation induces the expression of the adipocyte fatty acid binding protein gene in human monocytes. Biochem Biophys Res Commun 1999; 261: 456-458.
47. Bernlohr DA, Simpson MA, Hertzel AV, Banaszak LJ. Intracellular lipid-binding proteins and their genes. Annu Rev Nutrit 1997; 17: 277-303.
48. Hoo RL, Yeung DC, Lam KS, Xu A. Inflammatory biomarkers associated with obesity and insulin resistance: a focus on lipocalin-2 and adipocyte fatty acid-binding protein. Expert Rev Endocrinol Metab 2008; 3: 29-41.
49. Amri EZ, Bertrand B, Ailhaud G, Grimaldi P. Regulation of adipose cell differentiation. I. Fatty acids are inducers of the aP2 gene expression. J Lipid Res 1991; 32: 1449-1456.
50. Kletzien RF, Foellmi LA, Harris PK, Wyse BM, Clarke SD. Adipocyte fatty acid-binding protein: regulation of gene expression in vivo and in vitro by an insulin-sensitizing agent. Mol Pharmacol 1992; 42: 558-562.
51. Perera RJ, Marcusson EG, Koo S, et al. Identification of novel PPARγ target genes in primary human adipocytes. Gene 2006; 369: 90-99.
52. Fu Y, Luo N, Lopes-Virella MF. Oxidized LDL induces the expression of ALBP/aP2 mRNA and protein in human THP-1 macrophages. J Lipid Res 2000; 41: 2017-2023.
53. Kazemi MR, McDonald CM, Shigenaga JK, Grunfeld C, Feingold KR. Adipocyte fatty acid-binding protein expression and lipid accumulation are increased during activation of murine macrophages by toll-like receptor agonists. Arterioscler Thromb Vasc Biol 2005; 25: 1220-1224.
54. Spiegelman BM, Frank M, Green H. Molecular cloning of mRNA from 3T3 adipocytes. Regulation of mRNA content for glycerophosphate dehydrogenase and other differentiation-dependent proteins during adipocyte development. J Biol Chem 1983; 258: 10083-10089.
55. Makowski L, Boord JB, Maeda K, et al. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med 2001; 7: 699-705.
56. Hotamisligil GS, Johnson RS, Distel RJ, et al. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science 1996; 274: 1377-1379.
57. Uysal KT, Scheja L, Wiesbrock SM, Bonner-Weir S, Hotamisligil GS. Improved glucose and lipid metabolism in genetically obese mice lacking aP2. Endocrinology 2000; 141: 3388-3396.
58. -/- mice. Diabetes 1999; 48: 1987-1994.
59. Hertzel AV, Smith LA, Berg AH, et al. Lipid metabolism and adipokine levels in fatty acid-binding protein null and transgenic mice. Am J Physiol Endocrinol Metab 2006; 290: E814-E823.
60. Makowski L, Brittingham KC, Reynolds JM, Suttles J, Hotamisligil GS. The fatty acid-binding protein, aP2, coordinates macrophage cholesterol trafficking and inflammatory activity. Macrophage expression of aP2 impacts peroxisome proliferator-activated receptor-γ and IκB kinase activities. J Biol Chem 2005; 280: 12888-12895.
61. Hui X, Li H, Zhou Z, et al. Adipocyte fatty acid-binding protein modulates inflammatory responses in macrophages through a positive feedback loop involving c-Jun NH2-terminal kinases and activator protein-1. J Biol Chem 2010; 285: 10273-10280.
62. Furuhashi M, Tuncman G, Gorgun CZ, et al. Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature 2007; 447: 959-965.
63. Erbay E, Babaev VR, Mayers JR, et al. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat Med 2009; 15: 1383-1391.
64. Boord JB, Maeda K, Makowski L, et al. Adipocyte fatty acid-binding protein, aP2, alters late atherosclerotic lesion formation in severe hypercholesterolemia. Arterioscler Thromb Vasc Biol 2002; 22: 1686-1691.
65. Boord JB, Fazio S, Linton MF. Cytoplasmic fatty acid-binding proteins: emerging roles in metabolism and atherosclerosis. Curr Opin Lipidol 2002; 13: 141-147.
66. Layne MD, Patel A, Chen YH, et al. Role of macrophage-expressed adipocyte fatty acid binding protein in the development of accelerated atherosclerosis in hypercholesterolemic mice. FASEB J 2001; 15: 2733-2735.
67. Fu Y, Luo N, Lopes-Virella MF, Garvey WT. The adipocyte lipid binding protein (ALBP/aP2) gene facilitates foam cell formation in human THP-1 macrophages. Atherosclerosis 2002; 165: 259-269.
68. Lee MY, Li H, Xiao Y, et al. Chronic administration of BMS309403 improves endothelial function in apolipoprotein E-deficient mice and in cultured human endothelial cells. Br J Pharmacol 2011; 162: 1564-1576.
69. Chan CK, Zhao Y, Liao SY, et al. A-FABP and oxidative stress underlie the impairment of endothelium-dependent relaxations to serotonin and the intima-medial thickening in the porcine coronary artery with regenerated endothelium. ACS Chem Neurosci 2013; 4: 122-129.
70. Hsu BG, Chen YC, Lee RP, et al. Fasting serum level of fatty-acid-binding protein 4 positively correlates with metabolic syndrome in patients with coronary artery disease. Circ J 2010; 74: 327-331.
71. Mohlig M, Weickert MO, Ghadamgadai E, et al. Adipocyte fatty acid-binding protein is associated with markers of obesity, but is an unlikely link between obesity, insulin resistance, and hyperandrogenism in polycystic ovary syndrome women. Eur J Endocrinol 2007; 157: 195-200.
72. Stejskal D, Karpisek M. Adipocyte fatty acid binding protein in a Caucasian population: a new marker of metabolic syndrome? Eur J Clin Invest 2006; 36: 621-625.
73. Xu A, Tso AW, Cheung BM, et al. Circulating adipocyte-fatty acid binding protein levels predict the development of the metabolic syndrome: a 5-year prospective study. Circulation 2007; 115: 1537-1543.
74. Tso AW, Xu A, Sham PC, et al. Serum adipocyte fatty acid binding protein as a new biomarker predicting the development of type 2 diabetes: a 10-year prospective study in a Chinese cohort. Diabetes Care 2007; 30: 2667-2672.
75. Milner KL, van der Poorten D, Xu A, et al. Adipocyte fatty acid binding protein levels relate to inflammation and fibrosis in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1926-1934.
76. Fisher RM, Thorne A, Hamsten A, Arner P. Fatty acid binding protein expression in different human adipose tissue depots in relation to rates of lipolysis and insulin concentration in obese individuals. Mol Cell Biochem 2002; 239: 95-100.
77. Haider DG, Schindler K, Bohdjalian A, et al. Plasma adipocyte and epidermal fatty acid binding protein is reduced after weight loss in obesity. Diabetes Obesity Metab 2007; 9: 761-763.
78. Karpisek M, Stejskal D, Kotolova H, et al. Treatment with atorvastatin reduces serum adipocyte-fatty acid binding protein value in patients with hyperlipidaemia. Eur J Clin Invest 2007; 37: 637-642.
79. Yeung DC, Xu A, Cheung CW, et al. Serum adipocyte fatty acid-binding protein levels were independently associated with carotid atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27: 1796-1802.
80. Bao Y, Lu Z, Zhou M, et al. Serum levels of adipocyte fatty acid-binding protein are associated with the severity of coronary artery disease in Chinese women. PLoS One 2011; 6: e19115.
81. Huang CL, Wu YW, Wu CC, et al. Association between serum adipocyte fatty-acid binding protein concentrations, left ventricular function and myocardial perfusion abnormalities in patients with coronary artery disease. Cardiovasc Diabetol 2013; 12: 105.
82. Rhee EJ, Lee WY, Park CY, et al. The association of serum adipocyte fatty acid-binding protein with coronary artery disease in Korean adults. Eur J Endocrinol 2009; 160: 165-172.
83. Tuncman G, Erbay E, Hom X, et al. A genetic variant at the fatty acid-binding protein aP2 locus reduces the risk for hypertriglyceridemia, type 2 diabetes, and cardiovascular disease. Proc Natl Acad Sci U S A 2006; 103: 6970-6975.
84. Lovren F, Pan Y, Quan A, et al. Adiponectin primes human monocytes into alternative anti-inflammatory M2 macrophages. Am J Physiol Heart Circ Physiol 2010; 299: H656-H663.
85. Cabre A, Lazaro I, Girona J, et al. Fatty acid binding protein 4 is increased in metabolic syndrome and with thiazolidinedione treatment in diabetic patients. Atherosclerosis 2007; 195: e150-e158.
86. Trujillo ME, Scherer PE. Adiponectin - journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med 2005; 257: 167-175.
87. 18F-fluorodeoxyglucose positron emission tomography. J Clin Endocrinol Metab 2011; 96: E488-E492.
88. von Eynatten M, Breitling LP, Roos M, et al. Circulating adipocyte fatty acid-binding protein levels and cardiovascular morbidity and mortality in patients with coronary heart disease: a 10-year prospective study. Arterioscler Thromb Vasc Biol 2012; 32: 2327-2335.
89. Chow WS, Tso AW, Xu A, et al. Elevated circulating adipocyte-fatty acid binding protein levels predict incident cardiovascular events in a community-based cohort: a 12-year prospective study. J Am Heart Assoc 2013; 2: e004176.