Thrombospondin 1 mediates renal dysfunction in a mouse model of high-fat diet-induced obesity

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 6, 2013, Pages

  Cui, Wenpeng ^a,b   Maimaitiyiming, Hasiyeti ^a   Qi, Xinyu ^a   Norman, Heather ^a   Wang, Shuxia ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

Kidney; Leptin; Obesity; Thrombospondin 1

Indexed keywords

COLLAGEN TYPE 4; FIBRONECTIN; LEPTIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL ISOLATION; CONTROLLED STUDY; DISEASE MODEL; IN VITRO STUDY; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; LIPID DIET; LIPID STORAGE; MALE; MESANGIUM; MESANGIUM CELL; MOUSE; NEPHRITIS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION;

EID: 84884232736     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00209.2013     Document Type: Article

References (57)

1. Alicic RZ, Patakoti R, Tuttle KR. Direct and indirect effects of obesity on the kidney. Adv Chronic Kidney Dis 20: 121-127, 2013.
2. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917, 1959.
3. Bornstein P. Thrombospondins as matricellular modulators of cell function. J Clin Invest 107: 929-934, 2001.
4. Chavez RJ, Haney RM, Cuadra RH, Ganguly R, Adapala RK, Thodeti CK, Raman P. Upregulation of thrombospondin-1 expression by leptin in vascular smooth muscle cells via JAK2-and MAPK-dependent pathways. Am J Physiol Cell Physiol 303: C179-C191, 2012.
5. Crawford SE, Stellmach V, Murphy-Ullrich JE, Ribeiro SM, Lawler J, Hynes RO, Boivin GP, Bouck N. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93: 1159-1170, 1998.
6. Daniel C, Schaub K, Amann K, Lawler J, Hugo C. Thrombospondin-1 is an endogenous activator of TGF-beta in experimental diabetic nephropathy in vivo. Diabetes 56: 2982-2989, 2007.
7. Daniel C, Schaub K, Amann K, Lawler J, Hugo C. Thrombospondin-1 is an endogenous activator of TGF-beta in experimental diabetic nephropathy in vivo. Diabetes 18: 2982-2989, 2007.
8. Daniel C, Wiede J, Krutzsch HC, Ribeiro SM, Roberts DD, Murphy-Ullrich JE, Hugo C. Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 65: 459-468, 2004.
9. Daugherty A, Rateri D, Hong L, Balakrishnan A. Measuring blood pressure in mice using volume pressure recording, a tail-cuff method. J Vis Exp 27: 1291, 2009.
10. Decleves AE, Mathew AV, Cunard R, Sharma K. AMPK mediates the initiation of kidney disease induced by a high-fat diet. J Am Soc Nephrol 22: 1846-1855, 2011.
11. Donoviel DB, Amacher SL, Judge KW, Bornstein P. Thrombospondin gene expression is associated with mitogenesis in 3T3 cells: induction by basic fibroblast growth factor. J Cell Physiol 145: 16-23, 1990.
12. Garcia-Diaz DF, Arellano AV, Milagro FI, Moreno-Aliaga MJ, Portillo MP, Martinez JA, Campion J. Glucose and insulin modify thrombospondin 1 expression and secretion in primary adipocytes from dietinduced obese rats. J Physiol Biochem 67: 453-461, 2011.
13. Han DC, Isono M, Chen S, Casaretto A, Hong SW, Wolf G, Ziyadeh FN. Leptin stimulates type I collagen production in db/db mesangial cells: glucose uptake and TGF-beta type II receptor expression. Kidney Int 59: 1315-1323, 2001.
14. Henegar JR, Bigler SA, Henegar LK, Tyagi SC, Hall JE. Functional and structural changes in the kidney in the early stages of obesity. J Am Soc Nephrol 12: 1211-1217, 2001.
15. Hida K, Wada J, Zhang H, Hiragushi K, Tsuchiyama Y, Shikata K, Makino H. Identification of genes specifically expressed in the accumulated visceral adipose tissue of OLETF rats. J Lipid Res 41: 1615-1622, 2000.
16. Hohenstein B, Daniel C, Hausknecht B, Boehmer K, Riess R, Amann KU, Hugo CP. Correlation of enhanced thrombospondin-1 expression, TGF-beta signalling and proteinuria in human type-2 diabetic nephropathy. Nephrol Dial Transplant 23: 3880-3887, 2008.
17. Hugo C, Pichler R, Meek R, Gordon K, Kyriakides T, Floege J, Bornstein P, Couser WG, Johnson RJ. Thrombospondin 1 is expressed by proliferating mesangial cells and is upregulated by PDGF and bFGF in vivo. Kidney Int 48: 1846-1856, 1995.
18. Kosugi T, Heinig M, Nakayama T, Connor T, Yuzawa Y, Li Q, Hauswirth WW, Grant MB, Croker BP, Campbell-Thompson M, Zhang L, Atkinson MA, Segal MS, Nakagawa T. Lowering blood pressure blocks mesangiolysis and mesangial nodules, but not tubulointerstitial injury, in diabetic eNOS knockout mice. Am J Pathol 174: 1221-1229, 2009.
19. Lee MP, Orlov D, Sweeney G. Leptin induces rat glomerular mesangial cell hypertrophy, but does not regulate hyperplasia or apoptosis. Int J Obes (Lond) 29: 1395-1401, 2005.
20. Lee W, Eom DW, Jung Y, Yamabe N, Lee S, Jeon Y, Hwang YR, Lee JH, Kim YK, Kang KS, Kim SN. Dendrobium moniliforme attenuates high-fat diet-induced renal damage in mice through the regulation of lipid-induced oxidative stress. Am J Chin Med 40: 1217-1228, 2012.
21. Li Y, Tong X, Rumala C, Clemons K, Wang S. Thrombospondin1 deficiency reduces obesity-associated inflammation and improves insulin sensitivity in a diet-induced obese mouse model. PLos One 6: e26656, 2011.
22. Lu A, Miao M, Schoeb TR, Agarwal A, Murphy-Ullrich JE. Blockade of TSP1-dependent TGF-beta activity reduces renal injury and proteinuria in a murine model of diabetic nephropathy. Am J Pathol 178: 2573-2586, 2011.
23. Ma LJ, Corsa BA, Zhou J, Yang H, Li H, Tang YW, Babaev VR, Major AS, Linton MF, Fazio S, Hunley TE, Kon V, Fogo AB. Angiotensin type 1 receptor modulates macrophage polarization and renal injury in obesity. Am J Physiol Renal Physiol 300: F1203-F1213, 2011.
24. Maier KG, Han X, Sadowitz B, Gentile KL, Middleton FA, Gahtan V. Thrombospondin-1: a proatherosclerotic protein augmented by hyperglycemia. J Vasc Surg 51: 1238-1247, 2010.
25. Maile LA, Allen LB, Hanzaker CF, Gollahon KA, Dunbar P, Clemmons DR. Glucose regulation of thrombospondin and its role in the modulation of smooth muscle cell proliferation. Exp Diabetes Res 2010: 1-12, 2010.
26. Mathew AV, Okada S, Sharma K. Obesity related kidney disease. Curr Diabetes Rev 7: 41-49, 2011.
27. Morandi V, Cherradi SE, Lambert S, Fauvel-Lafeve F, Legrand YJ, Legrand C. Proinflammatory cytokines (interleukin-1β and tumor necrosis factor-β) down regulate synthesis and secretion of thrombospondin by human endothelial cells. J Cell Physiol 160: 367-377, 1994.
28. Murphy-Ullrich JE, Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev 11: 59-69, 2000.
29. Nishida Y, Oda H, Yorioka N. Effect of lipoproteins on mesangial cell proliferation. Kidney Int Suppl 71: S51-S53, 1999.
30. Phelan MW, Forman LW, Perrine SP, Faller DV. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J Lab Clin Med 132: 519-529, 1998.
31. Poczatek MH, Hugo C, Darley-Usmar V, Murphy-Ullrich JE. Glucose stimulation of transforming growth factor-beta bioactivity in mesangial cells is mediated by thrombospondin-1. Am J Pathol 157: 1353-1363, 2000.
32. Ramis JM, Franssen-van Hal NL, Kramer E, Llado I, Bouillaud F, Palou A, Keijer J. Carboxypeptidase E and thrombospondin-1 are differently expressed in subcutaneous and visceral fat of obese subjects. Cell Mol Life Sci 59: 1960-1971, 2002.
33. Sarafidis PA. Obesity, insulin resistance and kidney disease risk: insights into the relationship. Curr Opin Nephrol Hypertens 17: 450-456, 2008.
34. Satirapoj B, Supasyndh O, Mayteedol N, Punpanich D, Chaiprasert A, Nata N, Ruangkanchanasetr P, Kanjanakul I, Choovichian P. Obesity and its relation to chronic kidney disease: a population-based, cross-sectional study of a Thai army population and relatives. Nephrology (Carlton) 18: 229-234, 2012.
35. Schultz-Cherry S, Lawler J, Murphy-Ullrich JE. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J Biol Chem 269: 26783-26788, 1994.
36. Schultz-Cherry S, Murphy-Ullrich JE. Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J Cell Biol 122: 923-932, 1993.
37. Shi L, Nikolic D, Liu S, Lu H, Wang S. Activation of renal reninangiotensin system in upstream stimulatory factor 2 transgenic mice. Am J Physiol Renal Physiol 296: F257-F265, 2009.
38. Spoto B, Mattace-Raso F, Sijbrands E, Mallamaci F, Leonardis D, Aucella F, Testa A, Gesuete A, Sanguedolce MC, D'Arrigo G, Parlongo RM, Pisano A, Torino C, Enia G, Tripepi G, Postorino M, Zoccali C. The fat-mass and obesity-associated gene (FTO) predicts mortality in chronic kidney disease of various severity. Nephrol Dial Transplant 27, Suppl 4: iv58-iv62, 2012.
39. Stemmer K, Perez-Tilve D, Ananthakrishnan G, Bort A, Seeley RJ, Tschop MH, Dietrich DR, Pfluger PT. High-fat-diet-induced obesity causes an inflammatory and tumor-promoting microenvironment in the rat kidney. Dis Model Mech 5: 627-635, 2012.
40. Varma V, Yao-Borengasser A, Bodles AM, Rasouli N, Phanavanh B, Nolen GT, Kern EM, Nagarajan R, Spencer HJ 3rd, Lee MJ, Fried SK, McGehee RE Jr, Peterson CA, Kern PA. Thrombospondin-1 is an adipokine associated with obesity, adipose inflammation, and insulin resistance. Diabetes 57: 432-439, 2008.
41. Veldink H, Faulhaber-Walter R, Park JK, Martens-Lobenhoffer J, Bode-Boger S, Schuett H, Haghikia A, Hilfiker-Kleiner D, Kielstein JT. Effects of chronic SDMA infusion on glomerular filtration rate, blood pressure, myocardial function and renal histology in C57BL6/J mice. Nephrol Dial Transplant 28: 1434-1439, 2013.
42. Voros G, Maquoi E, Demeulemeester D, Clerx N, Collen D, Lijnen HR. Modulation of angiogenesis during adipose tissue development in murine models of obesity. Endocrinology 146: 4545-4554, 2005.
43. Wahab NA, Schaefer L, Weston BS, Yiannikouris O, Wright A, Babelova A, Schaefer R, Mason RM. Glomerular expression of thrombospondin-1, transforming growth factor beta and connective tissue growth factor at different stages of diabetic nephropathy and their interdependent roles in mesangial response to diabetic stimuli. Diabetologia 4: 1-11, 2005.
44. Wang S, Shiva S, Poczatek MH, Darley-Usmar V, Murphy-Ullrich JE. Nitric oxide and cGMP-dependent protein kinase regulation of glucosemediated thrombospondin 1-dependent transforming growth factor-beta activation in mesangial cells. J Biol Chem 277: 9880-9888, 2002.
45. Wang S, Skorczewski J, Feng X, Mei L, Murphy-Ullrich JE. Glucose upregulates thrombospondin 1 gene transcription and transforming growth factor-beta activity through antagonism of cGMP-dependent protein kinase repression via upstream stimulatory factor 2. J Biol Chem 279: 34311-34322, 2004.
46. Wang S, Wu X, Lincoln TM, Murphy-Ullrich JE. Expression of constitutively active cGMP-dependent protein kinase prevents glucose stimulation of thrombospondin 1 expression and TGF-beta activity. Diabetes 52: 2144-2150, 2003.
47. Wang XX, Jiang T, Shen Y, Adorini L, Pruzanski M, Gonzalez FJ, Scherzer P, Lewis L, Miyazaki-Anzai S, Levi M. The farnesoid X receptor modulates renal lipid metabolism and diet-induced renal inflammation, fibrosis, and proteinuria. Am J Physiol Renal Physiol 297: F1587-F1596, 2009.
48. Weisinger JR, Kempson RL, Eldridge FL, Swenson RS. The nephrotic syndrome: a complication of massive obesity. Ann Intern Med 81: 440-447, 1974.
49. Whaley-Connell A, Pavey BS, Afroze A, Bakris GL. Obesity and insulin resistance as risk factors for chronic kidney disease. J Cardiometab Syndr 1: 209-214, 2006.
50. Wickman C, Kramer H. Obesity and kidney disease: potential mechanisms. Semin Nephrol 33: 14-22, 2013.
51. Wolf G, Hamann A, Han DC, Helmchen U, Thaiss F, Ziyadeh FN, Stahl RA. Leptin stimulates proliferation and TGF-beta expression in renal glomerular endothelial cells: potential role in glomerulosclerosis. Kidney Int 56: 860-872, 1999.
52. Wolf G, Ziyadeh FN. Leptin and renal fibrosis. Contrib Nephrol 151: 175-183, 2006.
53. Yevdokimova N, Wahab NA, Mason RM. Thrombospondin-1 is the key activator of TGF-beta1 in human mesangial cells exposed to high glucose. J Am Soc Nephrol 12: 703-712, 2001.
54. Young GD, Murphy-Ullrich JE. Molecular interactions that confer latency to transforming growth factor-beta. J Biol Chem 279: 38032-38039, 2004.
55. Yung S, Lee CY, Zhang Q, Lau SK, Tsang RC, Chan TM. Elevated glucose induction of thrombospondin-1 upregulates fibronectin synthesis in proximal renal tubular epithelial cells through TGF-beta1 dependent and TGF-beta1 independent pathways. Nephrol Dial Transplant 21: 1504-1513, 2006.
56. Zhang R, Reisin E. Obesity-hypertension: the effects on cardiovascular and renal systems. Am J Hypertens 13: 1308-1314, 2000.
57. Zoccali C, Torino C, Tripepiand G, Mallamaci F. Assessment of obesity in chronic kidney disease: what is the best measure? Curr Opin Nephrol Hypertens 21: 641-646, 2012.