Matrix metalloproteinase 2 induces epithelial-mesenchymal transition in proximal tubules from the luminal side and progresses fibrosis in mineralocorticoid/salt-induced hypertensive rats

Journal of Hypertension

Volumn 29, Issue 12, 2011, Pages 2440-2453

  Iwazu, Yoshitaka ^a   Muto, Shigeaki ^a   Hirahara, Ichiro ^a   Fujisawa, Genro ^b   Takeda, Shin Ichi ^a   Kusano, Eiji ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b Fujisawa Medical Clinic   (Japan)

Author keywords

(2R) 2 5 4 ethyl methylamino phenyl thiophene 2 sulfonylamino 3 methylbutyric acid (TISAM); Claudin 2; E cadherin; epithelial mesenchymal transition; matrix metalloproteinase 2; proximal tubule cells; spironolactone

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CLAUDIN 2; DEOXYCORTICOSTERONE ACETATE; GELATINASE A; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE INHIBITOR; MINERALOCORTICOID; POTASSIUM CHLORIDE; SODIUM CHLORIDE; SPIRONOLACTONE; UVOMORULIN; VILLIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HYPERTENSION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY PROXIMAL TUBULE; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; UPREGULATION; URINALYSIS;

EID: 81355138104     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0b013e32834c31f5     Document Type: Article

References (46)

1. Rudolph AE, Rocha R, McMahon EG. Aldosterone target organ protection by eplerenone. Mol Cell Endocrinol 2004; 217:229-238.
2. Fujisawa G, Okada K, Muto S, Fujita N, Itabashi N, Kusano E, et al. Na/H exchange isoform 1 is involved in mineralocorticoid/salt-induced cardiac injury. Hypertension 2003; 41:493-498.
3. Blasi ER, Rocha R, Rudolph AE, Blomme AG, Polly ML, McMahon EG. Aldosterone/salt induced renal inflammation and fibrosis in hypertensive rats. Kidney Int 2003; 63:1791-1800.
4. Nishiyama A, Yao L, Nagai Y, Miyata K, Yoshizumi M, Kagami S, et al. Possible contributions of reactive oxygen species and mitogen-activated protein kinase to renal injury in aldosterone/salt-induced hypertensive rats. Hypertension 2003; 43:841-848.
5. Iwazu Y, Muto S, Fujisawa G, Nakazawa E, Okada K, Ishibashi S, et al. Spirololactone suppresses peritubular capillary loss and prevents eoxycorticosterone acetate/salt-induced tubulointerstitial fibrosis. Hypertension 2008; 51:749-754.
6. Catania JM, Parris AR. Role of matrix metalloproteinases in renal pathophysiologies. Am. J. Physiol 2007; 292:F905-F911.
7. Ronco P, Chatziantoniou C. Matrix metalloproteinases and matrix receptors in progression and reversal of kidney disease: Therapeutic perspectives. Kidney Int 2008; 74:873-878.
8. Basile DP, Fredrich K, Weihrauch D, Hattan N, Chilian WM. Angiostatin and matrix metalloprotease expression following ischemic acute renal failure. Am. J. Physiol 2004; 286:F893-F902.
9. Sharma AK, Mauer SM, Kim Y, Michael AF. Altered expression of matrix metalloproteinase-2, TIMP and TIMP-2 in obstructive nephropathy. J. Lab Clin Med 1995; 125:754-761.
10. Gonzalez-Avila G, Iturria C, Vadillo-Ortega F, Ovalle C, Montario M. Changes in matrix metalloproteinases during the evolution of interstitial renal fibrosis in a rat experimental model. Pathophysiology 1998; 66:196-204.
11. Inkinen KA, Soots AP, Krogerus LA, Lautenschlager IT, Ahonen JP. Fibrosis and matrix metalloproteinases in rat renal allografts. Transpl Int 2005; 18:506-512.
12. Ma J, Weisberg A, Griffin JP, Vaughan DE, Fogo AB, Brown NJ. Plasminogen activator inhibitor-1 deficiency protects against aldosteroneinduced glomerular injury. Kidney Int 2006; 69:1064-1072.
13. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin Invest 2003; 112:1776-1784.
14. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J. Am. Soc Nephrol 2004; 15:1-12.
15. Lee DB, Haung E, Ward HJ. Tight junction biology and kidney function. Am. J. Physiol 2006; 290:F20-F34.
16. Cheng S, Lovvett DH. Gelatinase A (MMP-2) is necessary and sufficient for renal tubular cell epithelial-mesenchymal transformation. Am. J. Pathol 2003; 162:1937-1949.
17. Cheng S, Pollock AS, Mahimkar R, Olson JL, Lovett DH. Matrix metalloproteinase 2 and basement membrane integrity: A unifying mechanism for progressive renal injury. FASEB J. 2006; 20:E1248-E1256.
18. Zhang A, Jia Z, Guo X, Yang T. Aldosterone induces epithelialmesenchymal transition via ROS of mitochondrial origin. Am. J. Physiol 2007; 293:F723-F731.
19. Zheng G, Lyons JG, Tan TK, Wang Y, Hsu TT, Min D, et al. Disruption of E-cadherin by matrix metalloproteinase directly mediated epithelial-mesenchymal transition downstreAm. of transforming growth factor-b1 in renal tubular epithelial cells. Am. J. Pathol 2009; 175:580-591.
20. Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol 1997; 139:1861-1872.
21. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb Blood Flow Metab 2007; 27:697-709.
22. Reijerkerk A, KooiJ. G, van der Pol SMA, Khazen S, Dijkstra CD, de Vries HE. Diapedesis of monocytes is associated with MMP-mediated occluding disappearance in brain endothelial cells. FASEB J. 2006; 20:E1901-E1909.
23. Fujisawa G, Okada K, Muto S, Fujita N, Itabashi N, Kusano E, et al. Spironolactone prevents early renal injury in streptozotocin-induced diabetic rats. Kidney Int 2004; 66:1493-1502.
24. Matsumura S, Iwanaga S, Mochizuki S, Okamoto H, Ogawa S, Okada Y. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J. Clin Invest 2005; 115:599-609.
25. Nishida M, Okumura Y, Ozawa S, Shiraishi I, Itoi T, Hamaoka K. MMP-2 inhibitor reduces renal macrophage infiltration with increased fibrosis in UUO. Biochem Biophys Res Commun 2007; 354:133-139.
26. Hirahara I, Kusano E, Yanagiba S, Miyata Y, Ando Y, Muto S, et al. Peritoneal injury by methylglyoxal in peritoneal dialysis. Perit Dial Int 2006; 26:380-392.
27. Bernardo MM, Fridman R. TIMP-2 (tissue inhibitor of metalloproteinase-2) regulates MMP-2 (matrix metalloproteinase-2) activity in the extracellular environment after pro-MMP-2 activation by MT1 (membrane type 1)-MMP. Biochem J. 2003; 374:739-745.
28. Butler GS, Butler MJ, Atkinson SJ, Will H, Tamura T, van Westrum SS, et al. The TIMP2 membrane type 1 metalloproteinase receptor regulates the concentration and efficient activation of progelatinase A: A kinetic study. J. Biol Chem 1998; 273:871-880
29. Jo Y, Yeon J, Kim H-J, Lee S. Analysis of tissue inhibitor of metalloproteinases-2 effect on pro-matrix metalloproteinase-2 activation by membrane-type 1 matrix metalloproteinase using baculovirus/insect-cell expression system. Biochem J. 2000; 345:511-519.
30. White P, Doctor RB, Dahl RH, Chen J. Coincident microvillar actin bundle disruption and perinuclear actin sequestration in anoxic proximal tubule. Am. J. Physiol 2000; 278:F886-F893.
31. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J. Am. Soc Nephrol 2002; 13:875-886.
32. Enck AH, Berger UV, Yu ASL. Claudin-2 is selectively expressed in proximal nephron in mouse kidney. Am. J. Physiol 2001; 281:F966-F974.
33. Gonzalez-Mariscal L, Namorado MC, Martin D, Luna J, Alarcon L, Islas S, et al. Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int 2000; 57:2386-2402.
34. Legallicier B, Trugnan G, Murphy G, Lelongt B, Ronco R. Expression of the type IV collagenase system during mouse kidney development and tubule segmentation. J. Am. Soc Nephrol 2001; 12:2358-2369.
35. Levi E, Friedman R, Miao HQ, Ma YS, Yayon A, Vlodavsky I. Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1. Proc Natl Acad Sci USA 1996; 93:7069-7074.
36. Ito A, Mukaiyama A, Itoh H, Nagase H, Thogersen IB, Enghild JJ, et al. Degradation of interleukin 1b by matrix metalloproteinases. J. Biol Chem 1996; 271:14657-14660.
37. McQuibban GA, Gong J-H, TAm. EM, McCulloch CA, Clark-Lewis I, Overall CM. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 2000; 289:1202-1206.
38. Grände M, Franzen A, Karlsson JO, Ericson LE, Heldin NE, Nilsson M. Transforming growth factor-b and epidermal growth factor synergistically timulate epithelial to mesenchymal transition (EMT) through a MEKdependent mechanism in primary cultured pig thyrocytes. J. Cell Sci 2002; 115:4227-4236.
39. Furuse M, Furuse K, Sasaki H, Tsukita S. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into MDCK I cells. J. Cell Biol 2001; 153:263-272.
40. Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, Schulzke JD, et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J. Cell Sci 2002; 115:4969-4976.
41. Hou J, Gomes AS, Paul DL, Goodenough DA. Study of claudin function by RNA interference. J. Biol Chem 2006; 281:36117-36123.
42. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, et al. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA 2010; 107:8011-8016.
43. Brown NJ, Nakamura S, Ma L, Nakamura I, Donnert E, Freeman M, et al. Aldosterone modulates plasminogen activator inhibitor-1 and glomerulosclerosis in vivo. Kidney Int 2000; 58:1219-1227.
44. Feria I, Pichardo I, Juarez P, Ramirez V, Gonzalez MA, Uribe N, et al. Therapeutic benefit of spironolactone in experimental chronic cyclosporine A nephrotoxicity. Kidney Int 2003; 63:43-52.
45. Patni H, Mathew JT, Luan L, Franki N, Chander PN, Singhal PC. Aldosterone promotes proximal tubular cell apoptosis: Role of oxidative stress. Am. J. Physiol Renal Physiol 2007; 293:F1065-F1071.
46. Fan Y, Kohno M, Hitomi H, Kitada K, Fujisawa Y, Yatabe J, et al. Aldosterone/mineralocorticoid receptor stimulation induces cellular senescence in the kidney. Endocrinology 2011; 152:680-688.