Genetic deficiency of Smad3 protects the kidneys from atrophy and interstitial fibrosis in 2K1C hypertension

American Journal of Physiology - Renal Physiology

Volumn 302, Issue 11, 2012, Pages

  Warner, Gina M ^a   Cheng, Jingfei ^a   Knudsen, Bruce E ^a   Gray, Catherine E ^a   Deibel, Ansgar ^a   Juskewitch, Justin E ^a   Lerman, Lilach O ^a   Textor, Stephen C ^a   Nath, Karl A ^a   Grande, Joseph P ^a  

^a MAYO CLINIC   (United States)

Author keywords

Renal artery stenosis; TGF signaling

Indexed keywords

RENIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ARTICLE; ATROPHY; CONTROLLED STUDY; GENE DISRUPTION; GENE SILENCING; HYPERTENSION; KIDNEY ARTERY STENOSIS; KIDNEY ATROPHY; KIDNEY DISEASE; KIDNEY FIBROSIS; MALE; MOUSE; NONHUMAN; PLASMA RENIN ACTIVITY; PRIORITY JOURNAL; RENAL PROTECTION; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE;

EID: 84861899027     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00645.2011     Document Type: Article

References (62)

1. Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE, Anzano M, Greenwell-Wild T, Wahl SM, Deng C, Roberts AB. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1: 260-266, 1999.
2. Attisano L, Lee-Hoeflich ST. The Smads. Genome Biol 2: REVIEWS3010, 2001.
3. Banh A, Deschamps PA, Gauldie J, Overbeek PA, Sivak JG, West-Mays J. Lens-specific expression of TGF-beta induces anterior subcapsular cataract formation in the absence of Smad3. Invest Ophthalmol Vis Sci 47: 3450-3460, 2006.
4. Boivin GP, O'Toole BA, Orsmby IE, Diebold RJ, Eis MJ, Doetschman T, Kier AB. Onset and progression of pathological lesions in transforming growth factor-beta 1-deficient mice. Am J Pathol 146: 276-288, 1995.
5. Bonniaud P, Margetts PJ, Ask K, Flanders K, Gauldie J, Kolb M. TGF-beta and Smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 175: 5390-5395, 2005.
6. Bottinger EP, Bitzer M. TGF-beta signaling in renal disease. J Am Soc Nephrol 13: 2600-2610, 2002.
7. Cambien F, Ricard S, Troesch A, Mallet C, Generenaz L, Evans A, Arveiler D, Luc G, Ruidavets JB, Poirier O. Polymorphisms of the transforming growth factor-beta 1 gene in relation to myocardial infarction and blood pressure. The Etude Cas-Temoin de l'Infarctus du Myocarde (ECTIM) Study. Hypertension 28: 881-887, 1996.
8. Chade AR, Zhu XY, Grande JP, Krier JD, Lerman A, Lerman LO. Simvastatin abates development of renal fibrosis in experimental renovascular disease. J Hypertens 26: 1651-1660, 2008.
9. Cheng J, Grande JP. Transforming growth factor-beta and kidney dysfunction. J Organ Dysfunct 5: 182-192, 2009.
10. Cheng J, Grande JP. Transforming growth factor-beta signal transduction and progressive renal disease. Exp Biol Med (Maywood) 227: 943-956, 2002.
11. Cheng J, Zhou W, Warner GM, Knudsen BE, Garovic VD, Gray CE, Lerman LO, Platt JL, Romero JC, Textor SC, Nath KA, Grande JP. Temporal analysis of signaling pathways activated in a murine model of 2-kidney, 1-clip hypertension. Am J Physiol Renal Physiol 297: F1055-F1068, 2009.
12. Dahly AJ, Hoagland KM, Flasch AK, Jha S, Ledbetter SR, Roman RJ. Antihypertensive effects of chronic anti-TGF-β antibody therapy in Dahl S rats. Am J Physiol Regul Integr Comp Physiol 283: R757-R767, 2002.
13. Derynck R, Zhang Y, Feng XH. Smads: transcriptional activators of TGF-beta responses. Cell 95: 737-740, 1998.
14. Diaz Encarnacion M, Griffin M, Slezak J, Bergstralh E, Stegall M, Velosa J, Grande J. Correlation of quantitative digital image analysis with glomerular filtration rate in CAN. Am J Transplant 4: 248-256, 2004.
15. Divakaran V, Adrogue J, Ishiyama M, Entman ML, Haudek S, Sivasubramanian N, Mann DL. Adaptive and maladaptive effects of SMAD3 signaling in the adult heart after hemodynamic pressure overloading. Circ Heart Fail 2: 633-642, 2009.
16. Favreau F, Zhu XY, Krier JD, Lin J, Warner L, Textor SC, Lerman LO. Revascularization of swine renal artery stenosis improves renal function but not the changes in vascular structure. Kidney Int 78: 1110-1118, 2010.
17. Feng M, Whitesall S, Zhang Y, Beibel M, D'Alecy L, DiPetrillo K. Validation of volume-pressure recording tail-cuff blood pressure measurements. Am J Hypertens 21: 1288-1291, 2008.
18. Flanders KC. Smad3 as a mediator of the fibrotic response. Int J Exp Pathol 85: 47-64, 2004.
19. Flanders KC, Major CD, Arabshahi A, Aburime EE, Okada MH, Fujii M, Blalock TD, Schultz GS, Sowers A, Anzano MA, Mitchell JB, Russo A, Roberts AB. Interference with transforming growth factor-beta/ Smad3 signaling results in accelerated healing of wounds in previously irradiated skin. Am J Pathol 163: 2247-2257, 2003.
20. Fujimoto M, Maezawa Y, Yokote K, Joh K, Kobayashi K, Kawamura H, Nishimura M, Roberts AB, Saito Y, Mori S. Mice lacking Smad3 are protected against streptozotocin-induced diabetic glomerulopathy. Biochem Biophys Res Commun 305: 1002-1007, 2003.
21. Garovic VD, Textor SC. Renovascular hypertension and ischemic nephropathy. Circulation 112: 1362-1374, 2005.
22. Gloviczki ML, Glockner JF, Lerman LO, McKusick MA, Misra S, Grande JP, Textor SC. Preserved oxygenation despite reduced blood flow in poststenotic kidneys in human atherosclerotic renal artery stenosis. Hypertension 55: 961-966, 2010.
23. Grande JP, Melder DC, Zinsmeister AR. Modulation of collagen gene expression by cytokines: stimulatory effect of transforming growth factorbeta1, with divergent effects of epidermal growth factor and tumor necrosis factor-alpha on collagen type I and collagen type IV. J Lab Clin Med 130: 476-486, 1997.
24. Grande JP, Warner GM, Walker HJ, Yusufi AN, Cheng J, Gray CE, Kopp JB, Nath KA. TGF-beta1 is an autocrine mediator of renal tubular epithelial cell growth and collagen IV production. Exp Biol Med (Maywood) 227: 171-181, 2002.
25. Hansen KJ, Edwards MS, Craven TE, Cherr GS, Jackson SA, Appel RG, Burke GL, Dean RH. Prevalence of renovascular disease in the elderly: a population-based study. J Vasc Surg 36: 443-451, 2002.
26. Huang XR, Chung AC, Yang F, Yue W, Deng C, Lau CP, Tse HF, Lan HY. Smad3 mediates cardiac inflammation and fibrosis in angiotensin II-induced hypertensive cardiac remodeling. Hypertension 55: 1165-1171, 2010.
27. Iglesias JI, Hamburger RJ, Feldman L, Kaufman JS. The natural history of incidental renal artery stenosis in patients with aortoiliac vascular disease. Am J Med 109: 642-647, 2000.
28. Inazaki K, Kanamaru Y, Kojima Y, Sueyoshi N, Okumura K, Kaneko K, Yamashiro Y, Ogawa H, Nakao A. Smad3 deficiency attenuates renal fibrosis, inflammation, and apoptosis after unilateral ureteral obstruction. Kidney Int 66: 597-604, 2004.
29. Jinno K, Takahashi T, Tsuchida K, Tanaka E, Moriyama K. Acceleration of palatal wound healing in Smad3-deficient mice. J Dent Res 88: 757-761, 2009.
30. Keddis MT, Garovic VD, Bailey KR, Wood CM, Raissian Y, Grande JP. Ischaemic nephropathy secondary to atherosclerotic renal artery stenosis: clinical and histopathological correlates. Nephrol Dial Transplant 25: 3615-3622, 2010.
31. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90: 770-774, 1993.
32. Kulkarni AB, Karlsson S. Transforming growth factor-beta 1 knockout mice. A mutation in one cytokine gene causes a dramatic inflammatory disease. Am J Pathol 143: 3-9, 1993.
33. Lavoie P, Robitaille G, Agharazii M, Ledbetter S, Lebel M, Lariviere R. Neutralization of transforming growth factor-beta attenuates hypertension and prevents renal injury in uremic rats. J Hypertens 23: 1895-1903, 2005.
34. Letterio JJ, Geiser AG, Kulkarni AB, Roche NS, Sporn MB, Roberts AB. Maternal rescue of transforming growth factor-beta 1 null mice. Science 264: 1936-1938, 1994.
35. Lin HM, Lee JH, Yadav H, Kamaraju AK, Liu E, Zhigang D, Vieira A, Kim SJ, Collins H, Matschinsky F, Harlan DM, Roberts AB, Rane SG. Transforming growth factor-beta/Smad3 signaling regulates insulin gene transcription and pancreatic islet beta-cell function. J Biol Chem 284: 12246-12257, 2009.
36. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12, 2004.
37. Liu Y. Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69: 213-217, 2006.
38. Lucas JA, Zhang Y, Li P, Gong K, Miller AP, Hassan E, Hage F, Xing D, Wells B, Oparil S, Chen YF. Inhibition of transforming growth factor-β signaling induces left ventricular dilation and dysfunction in the pressure-overloaded heart. Am J Physiol Heart Circ Physiol 298: H424-H432, 2010.
39. Martin JS, Dickson MC, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Analysis of homozygous TGF beta 1 null mouse embryos demonstrates defects in yolk sac vasculogenesis and hematopoiesis. Ann NY Acad Sci 752: 300-308, 1995.
40. Massague J. Receptors for the TGF-beta family. Cell 69: 1067-1070, 1992.
41. Massague J. TGF-beta signal transduction. Annu Rev Biochem 67: 753-791, 1998.
42. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 19: 2783-2810, 2005.
43. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19: 1745-1754, 2000.
44. Nath KA, Croatt AJ, Warner GM, Grande JP. Genetic deficiency of Smad3 protects against murine ischemic acute kidney injury. Am J Physiol Renal Physiol 301: F436-F442, 2011.
45. Rihal CS, Textor SC, Breen JF, McKusick MA, Grill DE, Hallett JW, Holmes DR Jr. Incidental renal artery stenosis among a prospective cohort of hypertensive patients undergoing coronary angiography. Mayo Clin Proc 77: 309-316, 2002.
46. Rodriguez-Vita J, Sanchez-Lopez E, Esteban V, Ruperez M, Egido J, Ruiz-Ortega M. Angiotensin II activates the Smad pathway in vascular smooth muscle cells by a transforming growth factor-beta-independent mechanism. Circulation 111: 2509-2517, 2005.
47. Safian RD, Textor SC. Renal-artery stenosis. N Engl J Med 344: 431-442, 2001.
48. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494, 2003.
49. Scaglione R, Argano C, Parrinello G, Colomba D, Di Chiara T, Ferrante A, Di Garbo V, Avellone G, Licata G. Relationship between transforming growth factor beta1 and progression of hypertensive renal disease. J Hum Hypertens 16: 641-645, 2002.
50. Suthanthiran M, Li B, Song JO, Ding R, Sharma VK, Schwartz JE, August P. Transforming growth factor-beta 1 hyperexpression in African-American hypertensives: a novel mediator of hypertension and/or target organ damage. Proc Natl Acad Sci USA 97: 3479-3484, 2000.
51. Textor SC. Ischemic nephropathy: where are we now? J Am Soc Nephrol 15: 1974-1982, 2004.
52. Textor SC. Managing renal arterial disease and hypertension. Curr Opin Cardiol 18: 260-267, 2003.
53. Textor SC. Pathophysiology of renal failure in renovascular disease. Am J Kidney Dis 24: 642-651, 1994.
54. Textor SC, Wilcox CS. Renal artery stenosis: a common, treatable cause of renal failure? Annu Rev Med 52: 421-442, 2001.
55. Weber-Mzell D, Kotanko P, Schumacher M, Klein W, Skrabal F. Coronary anatomy predicts presence or absence of renal artery stenosis. A prospective study in patients undergoing cardiac catheterization for suspected coronary artery disease. Eur Heart J 23: 1684-1691, 2002.
56. Wheatley K, Ives N, Gray R, Kalra PA, Moss JG, Baigent C, Carr S, Chalmers N, Eadington D, Hamilton G, Lipkin G, Nicholson A, Scoble J. Revascularization versus medical therapy for renal-artery stenosis. N Engl J Med 361: 1953-1962, 2009.
57. Wiesel P, Mazzolai L, Nussberger J, Pedrazzini T. Two-kidney, one clip and one-kidney, one clip hypertension in mice. Hypertension 29: 1025-1030, 1997.
58. Wright JR, Duggal A, Thomas R, Reeve R, Roberts IS, Kalra PA. Clinicopathological correlation in biopsy-proven atherosclerotic nephropathy: implications for renal functional outcome in atherosclerotic renovascular disease. Nephrol Dial Transplant 16: 765-770, 2001.
59. Yang F, Chung AC, Huang XR, Lan HY. Angiotensin II induces connective tissue growth factor and collagen I expression via transforming growth factor-beta-dependent and-independent Smad pathways: the role of Smad3. Hypertension 54: 877-884, 2009.
60. Yang YC, Piek E, Zavadil J, Liang D, Xie D, Heyer J, Pavlidis P, Kucherlapati R, Roberts AB, Bottinger EP. Hierarchical model of gene regulation by transforming growth factor beta. Proc Natl Acad Sci USA 100: 10269-10274, 2003.
61. Zacchigna L, Vecchione C, Notte A, Cordenonsi M, Dupont S, Maretto S, Cifelli G, Ferrari A, Maffei A, Fabbro C, Braghetta P, Marino G, Selvetella G, Aretini A, Colonnese C, Bettarini U, Russo G, Soligo S, Adorno M, Bonaldo P, Volpin D, Piccolo S, Lembo G, Bressan GM. Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell 124: 929-942, 2006.
62. Zhu Y, Richardson JA, Parada LF, Graff JM. Smad3 mutant mice develop metastatic colorectal cancer. Cell 94: 703-714, 1998.