Plasminogen activator inhibitor-1 modulates adipocyte differentiation

American Journal of Physiology - Endocrinology and Metabolism

Volumn 290, Issue 1, 2006, Pages

  Liang, Xiubin ^a   Kanjanabuch, Talerngsak ^a   Mao, Su Li ^a   Hao, Chuan Ming ^a   Tang, Yi Wei ^a   Declerck, Paul J ^b   Hasty, Alyssa H ^a   Wasserman, David H ^a   Fogo, Agnes B ^a   Ma, Li Jun ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adipocyte differentiation; Glucose uptake; Insulin resistance; Peroxisome proliferator activated receptor ; Plasminogen activator inhibitor 1

Indexed keywords

ADIPONECTIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; COLLAGEN TYPE 1; FATTY ACID BINDING PROTEIN; GLUCOSE TRANSPORTER 4; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLASMIN; PLASMINOGEN ACTIVATOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; RESISTIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; UROKINASE; GLUCOSE; INSULIN; MONOCLONAL ANTIBODY; SERPINE1 PROTEIN, HUMAN; SLC2A4 PROTEIN, MOUSE;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GENE TRANSFER; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; IMMUNOFLUORESCENCE MICROSCOPY; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; ANIMAL; C57BL MOUSE; CELL STRAIN 3T3; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; ANIMALS; ANTIBODIES, MONOCLONAL; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELL DIFFERENTIATION; COLLAGEN TYPE I; FATTY ACID-BINDING PROTEINS; GENE EXPRESSION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PPAR GAMMA; RESISTIN; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; URINARY PLASMINOGEN ACTIVATOR;

EID: 33644873563     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00605.2004     Document Type: Article

References (67)

1. Alessi MC, Peiretti F, Morange P, Henry M, Nalbone G, and Juhan-Vague I. Production of plasminogen activator inhibitor 1 by human adipose tissue: possible link between visceral fat accumulation and vascular disease. Diabetes 46: 860-867, 1997.
2. Asplund-Carlson A, Hamsten A, Wiman B, and Carlson LA. Relationship between plasma plasminogen activator inhibitor-1 activity and VLDL triglyceride concentration, insulin levels and insulin sensitivity: studies in randomly selected normal and hypertriglyceridaemic men. Diabetologia 36: 817-825, 1993.
3. Banerjee RR, Rangwala SM, Shapiro JS, Rich AS, Rhoades B, Qi Y, Wang J, Rajala MW, Pocai A, Scherer PE, Steppan CM, Ahima RS, Obici S, Rossetti L, and Lazar MA. Regulation of fasted blood glucose by resistin. Science 303: 1195-1198, 2004.
4. Barroso I, Gurnell M, Crowley VE, Agostini M, Schwabe JW, Soos MA, Maslen GL, Williams TD, Lewis H, Schafer AJ, Chatterjee VK, and O'Rahilly S. Dominant negative mutations in human PPARgamma associated with severe insulin resistance, diabetes mellitus and hypertension. Nature 402: 880-883, 1999.
5. Bastard JP, Pieroni L, and Hainque B. Relationship between plasma plasminogen activator inhibitor 1 and insulin resistance. Diabetes Metab Res Rev 16: 192-201, 2000.
6. Berry CN, Lunven C, Lechaire I, Girardot C, and O'Connor SE. Antithrombotic activity of a monoclonal antibody inducing the substrate form of plasminogen activator inhibitor type 1 in rat models of venous and arterial thrombosis. Br J Pharmacol 125: 29-34, 1998.
7. Bijnens AP, Gils A, Knockaert I, Stassen JM, and Declerck PJ. Importance of the hinge region between alpha-helix F and the main part of serpins, based upon identification of the epitope of plasminogen activator inhibitor type 1 neutralizing antibodies. J Biol Chem 275: 6375-6380, 2000.
8. Bjorntorp P, Karlsson M, Pertoft H, Pettersson P, Sjostrom L, and Smith U. Isolation and characterization of cells from rat adipose tissue developing into adipocytes. J Lipid Res 19: 316-324, 1978.
9. Bouloumie A, Sengenes C, Portolan G, Galitzky J, and Lafontan M. Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50: 2080-2086, 2001.
10. Carmeliet P, Moons L, Lijnen R, Janssens S, Lupu F, Collen D, and Gerard RD. Inhibitory role of plasminogen activator inhibitor-1 in arterial wound healing and neointima formation: a gene targeting and gene transfer study in mice. Circulation 96: 3180-3191, 1997.
11. Chavey C, Mari B, Monthouel MN, Bonnafous S, Anglard P, Van Obberghen E, and Tartare-Deckert S. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J Biol Chem 278: 11888-11896, 2003.
12. Cigolini M, Targher G, Seidell JC, Schiavon R, Manara F, Zenti MG, Mattioli C, and De Sandre G. Relationships of plasminogen activator inhibitor-1 to anthropometry, serum insulin, triglycerides and adipose tissue fatty acids in healthy men. Atherosclerosis 106: 139-147, 1994.
13. Cigolini M, Tonoli M, Borgato L, Frigotto L, Manzato F, Zeminian S, Cardinale C, Camin M, Chiaramonte E, De Sandre G, and Lunardi C. Expression of plasminogen activator inhibitor-1 in human adipose tissue: a role for TNF-alpha? Atherosclerosis 143: 81-90, 1999.
14. Combs TP, Pajvani UB, Berg AH, Lin Y, Jelicks LA, Laplante M, Nawrocki AR, Rajala MW, Parlow AF, Cheeseboro L, Ding YY, Russell RG, Lindemann D, Hartley A, Baker GR, Obici S, Deshaies Y, Ludgate M, Rossetti L, and Scherer PE. A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 145: 367-383, 2004.
15. Debrock S and Declerck PJ. Neutralization of plasminogen activator inhibitor-1 inhibitory properties: identification of two different mechanisms. Biochim Biophys Acta 1337: 257-266, 1997.
16. Declerck PJ, De Mol M, Vaughan DE, and Collen D. Identification of a conformationally distinct form of plasminogen activator inhibitor-1, acting as a noninhibitory substrate for tissue-type plasminogen activator. J Biol Chem 267: 11693-11696, 1992.
17. Deng X, Li H, and Tang YW. Cytokine expression in respiratory syncytial virus-infected mice as measured by quantitative reverse-transcriptase PCR. J Virol Methods 107: 141-146, 2003.
18. Engelman JA, Berg AH, Lewis RY, Lisanti MP, and Scherer PE. Tumor necrosis fcator-a mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3T3-L1 adipocytes. Mol Endocrinol 14: 1557-1569, 2000.
19. Evans RM, Barish GD, and Wang YX. PPARs and the complex journey to obesity. Nat Med 10: 355-361, 2004.
20. Fogo AB. The potential for regression of renal scarring. Curr Opin Nephrol Hypertens 12: 223-225, 2003.
21. Fogo AB. Renal fibrosis: not just PAI-1 in the sky. J Clin Invest 112: 326-328, 2003.
22. Gurlek A, Bayraktar M, and Kirazli S. Increased plasminogen activator inhibitor-1 activity in offspring of type 2 diabetic patients: lack of association with plasma insulin levels. Diabetes Care 23: 88-92, 2000.
23. Haffner SM, D'Agostino R Jr, Mykkanen L, Tracy R, Howard B, Rewers M, Selby J, Savage PJ, and Saad MF. Insulin sensitivity in subjects with type 2 diabetes relationship to cardiovascular risk factors: the Insulin Resistance Atherosclerosis Study. Diabetes Care 22: 562-568, 1999.
24. Hauner H, Entenmann G, Wabitsch M, Gaillard D, Ailhaud G, Negrel R, and Pfeiffer EF. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 84: 1663-1670, 1989.
25. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, and Evans RM. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100: 15712-15717, 2003.
26. Hotamisligil GS, Budavari A, Murray D, and Spiegelman BM. Reduced tyrosine kinase activity of the insulin receptor in obesity-diabetes. Central role of tumor necrosis factor-alpha. J Clin Invest 94: 1543-1549, 1994.
27. Hotamisligil GS, Shargill NS, and Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91, 1993.
28. Huang Y, Haraguchi M, Lawrence DA, Border WA, Yu L, and Noble NA. A mutant, noninhibitory plasminogen activator inhibitor type 1 decreases matrix accumulation in experimental glomerulonephritis. J Clin Invest 112: 379-388, 2003.
29. Juhan-Vague I and Alessi MC. PAI-1, obesity, insulin resistance and risk of cardiovascular events. Thromb Haemost 78: 656-660, 1997.
30. Juhan-Vague I, Alessi MC, and Vague P. Thrombogenic and fibrinolytic factors and cardiovascular risk in non-insulin-dependent diabetes mellitus. Ann Med 28: 371-380, 1996.
31. Kockx M, Leenen R, Seidell J, Princen HM, and Kooistra T. Relationship between visceral fat and PAI-1 in overweight men and women before and after weight loss. Thromb Haemost 82: 1490-1496, 1999.
32. Kudo M, Sugawara A, Uruno A, Takeuchi K, and Ito S. Transcription suppression of peroxisome proliferator-activated receptor gamma2 gene expression by tumor necrosis factor alpha via an inhibition of CCAAT/enhancer-binding protein delta during the early stage of adipocyte differentiation. Endocrinology 145: 4948-4956, 2004.
33. Lambert V, Munaut C, Noel A, Frankenne F, Bajou K, Gerard R, Carmeliet P, Defresne MP, Foidart JM, and Rakic JM. Influence of plasminogen activator inhibitor type 1 on choroidal neovascularization. FASEB J 15: 1021-1027, 2001.
34. Landin K, Stigendahl L, Eriksson E, Krotkiewski M, Risberg B, Tengborn L, and Smith U. Abdominal obesity is associated with an impaired fibrinolytic activity and elevated plasminogen activator inhibitor-1. Metabolism 39: 1044-1048, 1990.
35. Lin FT and Lane MD. CCAAT/enhancer binding protein alpha is sufficient to initiate the 3T3-L1 adipocyte differentiation program. Proc Natl Acad Sci USA 91: 8757-8761, 1994.
36. Livak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] method. Methods 25: 402-408, 2001.
37. Loskutoff DJ. Regulation of PAI-1 gene expression. Fibrinolysis 5: 197-206, 1991.
38. Lyon CJ and Hsueh WA. Effect of plasminogen activator inhibitor-1 in diabetes mellitus and cardiovascular disease. Am J Med 115, Suppl 8A: 62S-68S, 2003.
39. Ma LJ and Fogo AB. Angiotensin as inducer of plasminogen activator inhibitor-1 and fibrosis. Contrib Nephrol 135: 161-170, 2001.
40. Ma LJ, Mao SL, Taylor KL, Kanjanabuch T, Guan Y, Zhang Y, Brown NJ, Swift LL, McGuinness OP, Wasserman DH, Vaughan DE, and Fogo AB. Prevention of obesity and insulin resistance in mice lacking plasminogen activator inhibitor 1. Diabetes 53: 336-346, 2004.
41. Ma LJ, Marcantoni C, Linton MF, Fazio S, and Fogo AB. Peroxisome proliferator-activated receptor-gamma agonist troglitazone protects against nondiabetic glomerulosclerosis in rats. Kidney Int 59: 1899-1910, 2001.
42. Mavri A, Alessi MC, and Juhan-Vague I. Hypofibrinolysis in the insulin resistance syndrome: implication in cardiovascular diseases. J Intern Med 255: 448-456, 2004.
43. Mur C, Arribas M, Benito M, and Valverde AM. Essential role of insulin-like growth factor I receptor in insulin-induced fetal brown adipocyte differentiation. Endocrinology 144: 581-593, 2003.
44. Picard F and Auwerx J. PPAR(gamma) and glucose homeostasis. Annu Rev Nutr 22: 167-197, 2002.
45. Primrose JN, Davies JA, Prentice CR, Hughes R, and Johnston D. Reduction in factor VII, fibrinogen and plasminogen activator inhibitor-1 activity after surgical treatment of morbid obesity. Thromb Haemost 68: 396-399, 1992.
46. Roca C, Primo L, Valdembri D, Cividalli A, Declerck P, Carmeliet P, Gabriele P, and Bussolino F. Hyperthermia inhibits angiogenesis by a plasminogen activator inhibitor 1-dependent mechanism. Cancer Res 63: 1500-1507, 2003.
47. Ron D, Brasier AR, McGehee RE Jr, and Habener JF. Tumor necrosis factor-induced reversal of adipocytic phenotype of 3T3-L1 cells is preceded by a loss of nuclear CCAAT/enhancer binding protein (C/EBP). J Clin Invest 89: 223-233, 1992.
48. Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, Gonzalez FJ, and Spiegelman BM. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev 16: 22-26, 2002.
49. Rosen ED, Walkey CJ, Puigserver P, and Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev 14: 1293-1307, 2000.
50. Saltiel AR. You are what you secrete. Nat Med 7: 887-888, 2001.
51. Samad F and Loskutoff DJ. Tissue distribution and regulation of plasminogen activator inhibitor-1 in obese mice. Mol Med 2: 568-582, 1996.
52. Sartipy P and Loskutoff DJ. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci USA 100: 7265-7270, 2003.
53. Sawdey MS and Loskutoff DJ. Regulation of murine type 1 plasminogen activator inhibitor gene expression in vivo. Tissue specificity and induction by lipopolysaccharide, tumor necrosis factor-alpha, and transforming growth factor-beta. J Clin Invest 88: 1346-1353, 1991.
54. Schafer K, Fujisawa K, Konstantinides S, and Loskutoff DJ. Disruption of the plasminogen activator inhibitor 1 gene reduces the adiposity and improves the metabolic profile of genetically obese and diabetic ob/ob mice. FASEB J 15: 1840-1842, 2001.
55. Seki T, Miyasu T, Noguchi T, Hamasaki A, Sasaki R, Ozawa Y, Okukita K, Declerck PJ, and Ariga T. Reciprocal regulation of tissue-type and urokinase-type plasminogen activators in the differentiation of murine preadipocyte line 3T3-L1 and the hormonal regulation of fibrinolytic factors in the mature adipocytes. J Cell Physiol 189: 72-78, 2001.
56. Selvarajan S, Lund LR, Takeuchi T, Craik CS, and Werb Z. A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat Cell Biol 3: 267-275, 2001.
57. Smith U, Axelsen M, Carvalho E, Eliasson B, Jansson PA, and Wesslau C. Insulin signaling and action in fat cells: associations with insulin resistance and type 2 diabetes. Ann NY Acad Sci 892: 119-126, 1999.
58. Stephens JM and Pekala PH. Transcriptional repression of the GLUT4 and C/EBP genes in 3T3-L1 adipocytes by tumor necrosis factor-alpha. J Biol Chem 266: 21839-21845, 1991.
59. Tontonoz P, Hu E, and Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79: 1147-1156, 1994.
60. Uysal KT, Wiesbrock SM, Marino MW, and Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614, 1997.
61. Vague P, Juhan-Vague I, Aillaud MF, Badier C, Viard R, Alessi MC, and Collen D. Correlation between blood fibrinolytic activity, plasminogen activator inhibitor level, plasma insulin level, ans relative body weight in normal and obese subjects. Metabolism 35: 250-253, 1996.
62. Vaughan DE. Angiotensin and vascular fibrinolytic balance. Am J Hypertens 15: 3S-8S, 2002.
63. Warne JP. Tumour necrosis factor alpha: a key regulator of adipose tissue mass. J Endocrinol 177: 351-355, 2003.
64. Weiner FR, Shah A, Smith PJ, Rubin CS, and Zern MA. Regulation of collagen gene expression in 3T3-L1 cells. Effects of adipocyte differentiation and tumor necrosis factor alpha. Biochemistry 28: 4094-4099, 1989.
65. Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, McKeon C, Darlington GJ, and Spiegelman BM. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 3: 151-158, 1999.
66. Yi T, Choi HM, Park RW, Sohn KY, and Kim IS. Transcriptional repression of type I procollagen genes during adipocyte differentiation. Exp Mol Med 33: 269-275, 2001.
67. Zhang B, Berger J, Hu E, Szalkowski D, White-Carrington S, Spiegelman BM, and Moller DE. Negative regulation of peroxisome proliferator-activated receptor-gamma gene expression contributes to the antiadipogenic effects of tumor necrosis factor-alpha. Mol Endocrinol 10: 1457-1466, 1996.