MicroRNA-324-3p promotes renal fibrosis and is a target of ACE inhibition

Journal of the American Society of Nephrology

Volumn 23, Issue 9, 2012, Pages 1496-1505

  Macconi, Daniela ^a   Tomasoni, Susanna ^a   Romagnani, Paola ^b   Trionfini, Piera ^a   Sangalli, Fabio ^a   Mazzinghi, Benedetta ^b   Rizzo, Paola ^a   Lazzeri, Elena ^b   Abbate, Mauro ^a   Remuzzi, Giuseppe ^a,c   Benigni, Ariela ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; MICRORNA; MICRORNA 10B; MICRORNA 134; MICRORNA 135B; MICRORNA 187; MICRORNA 189; MICRORNA 324 3P; MICRORNA 330; MICRORNA 337; MICRORNA 34C; MICRORNA 381; MICRORNA 9; MICRORNA 98; N ACETYL SERYLASPARTYL LYSYL PROLINE; PROLYL ENDOPEPTIDASE; PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOWMAN CAPSULE; COMPUTER MODEL; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; FIBROSING ALVEOLITIS; GLOMERULUS; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; IN VITRO STUDY; KIDNEY CORTEX; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY TUBULE; MALE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEINURIA; RAT; RENAL PROTECTION; UPREGULATION;

EID: 84865963313     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2011121144     Document Type: Article

References (46)

1. Rovira-Halbach G, Alt JM, Brunkhorst R, Frei U, Kühn K, Stolte H: Single nephron hyperfiltration and proteinuria in a newly selected rat strain with superficial glomeruli. Ren Physiol 9: 317-325, 1986 (Pubitemid 17057363)
2. Fassi A, Sangalli F, Maffi R, Colombi F, Mohamed EI, Brenner BM, Remuzzi G, Remuzzi A: Progressive glomerular injury in the MWF rat is predicted by inborn nephron deficit. J Am Soc Nephrol 9: 1399-1406, 1998 (Pubitemid 28354549)
3. Remuzzi A, Puntorieri S, Mazzoleni A, Remuzzi G: Sex related differences in glomerular ultrafiltration and proteinuria in Munich-Wistar rats. Kidney Int 34: 481-486, 1988
4. Remuzzi A, Puntorieri S, Alfano M, Macconi D, Abbate M, Bertani T, Remuzzi G: Pathophysiologic implications of proteinuria in a rat model of progressive glomerular injury. Lab Invest 67: 572-579, 1992
5. Macconi D, Abbate M, Morigi M, Angioletti S, Mister M, Buelli S, Bonomelli M, Mundel P, Endlich K, Remuzzi A, Remuzzi G: Permselective dysfunction of podocyte-podocyte contact upon angiotensin II unravels the molecular target for renoprotective intervention. Am J Pathol 168: 1073-1085, 2006
6. Lapinski R, Perico N, Remuzzi A, Sangalli F, Benigni A, Remuzzi G: Angiotensin II modulates glomerular capillary permselectivity in rat isolated perfused kidney. J Am Soc Nephrol 7: 653-660, 1996 (Pubitemid 27465996)
7. Remuzzi A, Gagliardini E, Sangalli F, Bonomelli M, Piccinelli M, Benigni A, Remuzzi G: ACE inhibition reduces glomerulosclerosis and regenerates glomerular tissue in amodel of progressive renal disease. Kidney Int 69: 1124-1130, 2006
8. Macconi D, Sangalli F, Bonomelli M, Conti S, Condorelli L, Gagliardini E, Remuzzi G, Remuzzi A: Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition. Am J Pathol 174: 797-807, 2009
9. Remuzzi G, Benigni A, Remuzzi A: Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J Clin Invest 116: 288-296, 2006 (Pubitemid 43228342)
10. Macconi D: Targeting the renin angiotensin system for remission/regression of chronic kidney disease. Histol Histopathol 25: 655-668, 2010
11. Remuzzi A, Gagliardini E, Donadoni C, Fassi A, Sangalli F, Lepre MS, Remuzzi G, Benigni A: Effect of angiotensin II antagonism on the regression of kidney disease in the rat. Kidney Int 62: 885-894, 2002 (Pubitemid 35316717)
12. Farris AB, Adams CD, Brousaides N, Della Pelle PA, Collins AB, Moradi E, Smith RN, Grimm PC, Colvin RB: Morphometric and visual evaluation of fibrosis in renal biopsies. J Am Soc Nephrol 22: 176-186, 2011
13. Schulz A, Standke D, Kovacevic L, Mostler M, Kossmehl P, Stoll M, Kreutz R: A major gene locus links early onset albuminuria with renal interstitial fibrosis in the MWF rat with polygenetic albuminuria. J Am Soc Nephrol 14: 3081-3089, 2003 (Pubitemid 37509286)
14. van Es N, Schulz A, Ijpelaar D, van der Wal A, Kuhn K, Schütten S, Kossmehl P, Nyengaard JR, de Heer E, Kreutz R: Elimination of severe albuminuria in aging hypertensive rats by exchange of 2 chromosomes in double-consomic rats. Hypertension 58: 219-224, 2011
15. Pillai RS, Bhattacharyya SN, Filipowicz W: Repression of protein synthesis by miRNAs: How many mechanisms? Trends Cell Biol 17: 118-126, 2007 (Pubitemid 46357525)
16. Nilsen TW: Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 23: 243-249, 2007
17. Kloosterman WP, Plasterk RH: The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-450, 2006 (Pubitemid 44430905)
18. Kato M, Arce L, Natarajan R: MicroRNAs and their role in progressive kidney diseases. Clin J Am Soc Nephrol 4: 1255-1266, 2009
19. Oba S, Kumano S, Suzuki E, Nishimatsu H, Takahashi M, Takamori H, Kasuya M, Ogawa Y, Sato K, Kimura K, Homma Y, Hirata Y, Fujita T: miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS One 5: e13614, 2010
20. Lorenzen JM, Haller H, Thum T: MicroRNAs as mediators and therapeutic targets in chronic kidney disease. Nat Rev Nephrol 7: 286-294, 2011
21. Rea D, Fülöp V: Structure-function properties of prolyl oligopeptidase family enzymes. Cell Biochem Biophys 44: 349-365, 2006 (Pubitemid 43780391)
22. García-Horsman JA, Männistö PT, Venäläinen JI: On the role of prolyl oligopeptidase in health and disease. Neuropeptides 41: 1-24, 2007
23. Szeltner Z, Polgár L: Structure, function and biological relevance of prolyl oligopeptidase. Curr Protein Pept Sci 9: 96-107, 2008
24. Cavasin MA, Rhaleb NE, Yang XP, Carretero OA: Prolyl oligopeptidase is involved in release of the antifibrotic peptide Ac-SDKP. Hypertension 43: 1140-1145, 2004 (Pubitemid 38579927)
25. Iwamoto N, Xano HJ, Yoshioka T, Shiraga H, Nitta K, Muraki T, Ito K: Acetyl-seryl-aspartyl-lysyl-proline is a novel natural cell cycle regulator of renal cells. Life Sci 66: PL221-PL226, 2000 (Pubitemid 30152320)
26. Rousseau A, Michaud A, Chauvet MT, Lenfant M, Corvol P: The hemoregulatory peptide N-acetyl-Ser-Asp-Lys-Pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J Biol Chem 270: 3656-3661, 1995
27. Fuchs S, Xiao HD, Cole JM, Adams JW, Frenzel K, Michaud A, Zhao H, Keshelava G, Capecchi MR, Corvol P, Bernstein KE: Role of the N-terminal catalytic domain of angiotensin-converting enzyme investigated by targeted inactivation in mice. J Biol Chem279: 15946-15953, 2004 (Pubitemid 38509282)
28. Shi S, Yu L, Chiu C, Sun Y, Chen J, Khitrov G, Merkenschlager M, Holzman LB, Zhang W, Mundel P, Bottinger EP: Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 19: 2159-2169, 2008
29. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, McManus MT, Benzing T, Miner JH: Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 19: 2150-2158, 2008
30. Zhdanova O, Srivastava S, Di L, Li Z, Tchelebi L, Dworkin S, Johnstone DB, Zavadil J, Chong MM, Littman DR, Holzman LB, Barisoni L, Skolnik EY: The inducible deletion of Drosha and microRNAs in mature podocytes results in a collapsing glomerulopathy. Kidney Int 80: 719-730, 2011
31. Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, Natarajan R: MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 104: 3432-3437, 2007 (Pubitemid 46364176)
32. Chung AC, Huang XR, Meng X, Lan HY: miR-192 mediates TGF-beta/Smad3- driven renal fibrosis. J Am Soc Nephrol 21: 1317-1325, 2010
33. Benigni A, Morigi M, Rizzo P, Gagliardini E, Rota C, Abbate M, Ghezzi S, Remuzzi A, Remuzzi G: Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol 179: 628-638, 2011
34. Myöhänen TT, García-Horsman JA, Tenorio-Laranga J, Männistö PT: Issues about the physiological functions of prolyl oligopeptidase based on its discordant spatial association with substrates and inconsistencies among mRNA, protein levels, and enzymatic activity. J Histochem Cytochem 57: 831-848, 2009
35. Fuse Y, Polk DH, Lam RW, Reviczky AL, Fisher DA: Distribution and ontogeny of thyrotropin-releasing hormone degrading enzymes in rats. Am J Physiol 259: E787-E791, 1990
36. Goossens F, De Meester I, Vanhoof G, Scharpé S: Distribution of prolyl oligopeptidase in human peripheral tissues and body fluids. Eur J Clin Chem Clin Biochem 34: 17-22, 1996 (Pubitemid 26053038)
37. Welches WR, Brosnihan KB, Ferrario CM: A comparison of the properties and enzymatic activities of three angiotensin processing enzymes: Angiotensin converting enzyme, prolyl endopeptidase and neutral endopeptidase 24.11. Life Sci 52: 1461-1480, 1993
38. Dilauro M, Burns KD: Angiotensin-(1-7) and its effects in the kidney. Scientific World Journal 9: 522-535, 2009
39. Cavasin MA, Liao TD, Yang XP, Yang JJ, Carretero OA: Decreased endogenous levels of Ac-SDKP promote organ fibrosis. Hypertension 50: 130-136, 2007 (Pubitemid 46986021)
40. Casarini DE, Alves KB, Araújo MS, Stella RC: Endopeptidase and carboxypeptidase activities in human urine which hydrolyze bradykinin. Braz J Med Biol Res 25: 219-229, 1992
41. Casarini DE, Boim MA, Stella RC, Schor N: Endopeptidases (kininases) are able to hydrolyze kinins in tubular fluid along the rat nephron. Am J Physiol 277: F66-F74, 1999 (Pubitemid 29352676)
42. Peng H, Carretero OA, Liao TD, Peterson EL, Rhaleb NE: Role of N-acetyl-seryl-aspartyl-lysyl-proline in the antifibrotic and anti-inflammatory effects of the angiotensin-converting enzyme inhibitor captopril in hypertension. Hypertension 49: 695-703, 2007
43. Anglicheau D, Sharma VK, Ding R, Hummel A, Snopkowski C, Dadhania D, Seshan SV, Suthanthiran M: MicroRNA expression profiles predictive of human renal allograft status. Proc Natl Acad Sci U S A 106: 5330-5335, 2009
44. Lasagni L, Francalanci M, Annunziato F, Lazzeri E, Giannini S, Cosmi L, Sagrinati C, Mazzinghi B, Orlando C, Maggi E, Marra F, Romagnani S, Serio M, Romagnani P: An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med 197: 1537-1549, 2003 (Pubitemid 36682550)
45. Weibel ER: Practical Methods for Biological Morphometry. Stereological Methods, London, Academic Press, 1979
46. Myöhänen TT, Venäläinen JI, García-Horsman JA, Piltonen M, MännistöPT: Distribution of prolyl oligopeptidase in the mouse whole-body sections and peripheral tissues. Histochem Cell Biol 130: 993-1003, 2008