Elevation of the antifibrotic peptide N-acetyl-seryl-aspartyl-lysyl-proline: a blood pressure-independent beneficial effect of angiotensin I-converting enzyme inhibitors

Fibrogenesis and Tissue Repair

Volumn 4, Issue 1, 2011, Pages

  Kanasaki, Megumi ^a   Nagai, Takako ^a   Kitada, Munehiro ^a   Koya, Daisuke ^a   Kanasaki, Keizo ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II [3-8]; ANGIOTENSIN[1-7]; BRADYKININ; BRADYKININ B2 RECEPTOR; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GELATINASE A; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LOSARTAN; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOGENIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; SERASPENIDE; SMAD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA;

AMINO ACID BLOOD LEVEL; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ANGIOTENSIN BLOOD LEVEL; ANTIANGIOGENIC ACTIVITY; ANTIHYPERTENSIVE ACTIVITY; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; BIOSYNTHESIS; BLOOD PRESSURE MEASUREMENT; CARBOXY TERMINAL SEQUENCE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; DIABETIC RETINOPATHY; HUMAN; KIDNEY FIBROSIS; MICROALBUMINURIA; MOLECULAR MECHANICS; NONHUMAN; PHARMACOLOGICAL BLOCKING; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

EID: 84855511123     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-4-25     Document Type: Review

References (165)

1. Cushman DW, Ondetti MA. History of the design of captopril and related inhibitors of angiotensin converting enzyme. Hypertension 1991, 17:589-592.
2. Smith CG, Vane JR. The discovery of captopril. FASEB J 2003, 17:788-789.
3. Aulakh GK, Sodhi RK, Singh M. An update on non-peptide angiotensin receptor antagonists and related RAAS modulators. Life Sci 2007, 81:615-639.
4. Wood JM, Maibaum J, Rahuel J, Grütter MG, Cohen NC, Rasetti V, Rüger H, Göschke R, Stutz S, Fuhrer W, Schilling W, Rigollier P, Yamaguchi Y, Cumin F, Baum HP, Schnell CR, Herold P, Mah R, Jensen C, O'Brien E, Stanton A, Bedigian MP. Structure-based design of aliskiren, a novel orally effective renin inhibitor. Biochem Biophys Res Commun 2003, 308:698-705.
5. Parving HH, Persson F, Lewis JB, Lewis EJ, Hollenberg NK. Aliskiren combined with losartan in type 2 diabetes and nephropathy. New Engl J Med 2008, 358:2433-2446.
6. Solomon SD, Appelbaum E, Manning WJ, Verma A, Berglund T, Lukashevich V, Cherif Papst C, Smith BA, Dahlof B. Effect of the direct Renin inhibitor aliskiren, the Angiotensin receptor blocker losartan, or both on left ventricular mass in patients with hypertension and left ventricular hypertrophy. Circulation 2009, 119:530-537.
7. Padwal R, Laupacis A. Antihypertensive therapy and incidence of type 2 diabetes: a systematic review. Diabetes Care 2004, 27:247-255.
8. Scheen AJ. Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 1. A meta-analysis of randomised clinical trials. Diabetes Metabol 2004, 30:487-496.
9. Scheen AJ. Prevention of type 2 diabetes mellitus through inhibition of the Renin-Angiotensin system. Drugs 2004, 64:2537-2565.
10. Deelman L, Sharma K. Mechanisms of kidney fibrosis and the role of antifibrotic therapies. Curr Opin Nephrol Hypertens 2009, 18:85-90.
11. de Cavanagh EM, Inserra F, Ferder L. Angiotensin II blockade: a strategy to slow ageing by protecting mitochondria?. Cardiovasc Res 2011, 89:31-40.
12. Phillips MI, de Oliveira EM. Brain renin angiotensin in disease. J Mol Med 2008, 86:715-722.
13. Tigerstedt R, Bergman P. Niere und kreislauf. Scand Arch Physio 1898, 8:223-271.
14. Campbell DJ. Extrarenal renin and blood pressure regulation. An alternative viewpoint. Am J Hypertens 1989, 2:266-275.
15. Bernstein KE, Sayeski PP, Doan T, Farmer PK, Ali MS. Signal transduction pathways of angiotensin II in the kidney. Contrib Nephrol 2001, 135:16-33.
16. Wolf G, Ritz E. Combination therapy with ACE inhibitors and angiotensin II receptor blockers to halt progression of chronic renal disease: pathophysiology and indications. Kidney Int 2005, 67:799-812.
17. Gallinat S, Busche S, Raizada MK, Sumners C. The angiotensin II type 2 receptor: an enigma with multiple variations. Am J Physiol Endocrinol Metab 2000, 278:E357-374.
18. Gimonet V, Bussieres L, Medjebeur AA, Gasser B, Lelongt B, Laborde K. Nephrogenesis and angiotensin II receptor subtypes gene expression in the fetal lamb. Am J Physiol 1998, 274:F1062-1069.
19. Wolf G, Butzmann U, Wenzel UO. The renin-angiotensin system and progression of renal disease: from hemodynamics to cell biology. Nephron Physiol 2003, 93:P3-13.
20. Horiuchi M, Akishita M, Dzau VJ. Recent progress in angiotensin II type 2 receptor research in the cardiovascular system. Hypertension 1999, 33:613-621.
21. Opie LH, Sack MN. Enhanced angiotensin II activity in heart failure: reevaluation of the counterregulatory hypothesis of receptor subtypes. Circulation Res 2001, 88:654-658.
22. Naito T, Ma LJ, Yang H, Zuo Y, Tang Y, Han JY, Kon V, Fogo AB. Angiotensin type 2 receptor actions contribute to angiotensin type 1 receptor blocker effects on kidney fibrosis. Am J Physiol Renal Physiol 2010, 298:F683-691.
23. Regitz-Zagrosek V, Friedel N, Heymann A, Bauer P, Neuss M, Rolfs A, Steffen C, Hildebrandt A, Hetzer R, Fleck E. Regulation, chamber localization, and subtype distribution of angiotensin II receptors in human hearts. Circulation 1995, 91:1461-1471.
24. Asano K, Dutcher DL, Port JD, Minobe WA, Tremmel KD, Roden RL, Bohlmeyer TJ, Bush EW, Jenkin MJ, Abraham WT, Raynolds MV, Zisman LS, Perryman MB, Bristow MR. Selective downregulation of the angiotensin II AT1-receptor subtype in failing human ventricular myocardium. Circulation 1997, 95:1193-1200.
25. Ruiz-Ortega M, Lorenzo O, Ruperez M, Blanco J, Egido J. Systemic infusion of angiotensin II into normal rats activates nuclear factor-kappaB and AP-1 in the kidney: role of AT(1) and AT(2) receptors. Am J Pathol 2001, 158:1743-1756.
26. Wolf G, Wenzel U, Burns KD, Harris RC, Stahl RA, Thaiss F. Angiotensin II activates nuclear transcription factor-kappaB through AT1 and AT2 receptors. Kidney Int 2002, 61:1986-1995.
27. Cao Z, Bonnet F, Candido R, Nesteroff SP, Burns WC, Kawachi H, Shimizu F, Carey RM, De Gasparo M, Cooper ME. Angiotensin type 2 receptor antagonism confers renal protection in a rat model of progressive renal injury. J Am Soc Nephrol 2002, 13:1773-1787.
28. Wolf G, Wenzel U, Assmann KJ, Stahl RA. Renal expression of aminopeptidase A in rats with two-kidney, one-clip hypertension. Nephrol Dial Transplant 2000, 15:1935-1942.
29. Handa RK, Krebs LT, Harding JW, Handa SE. Angiotensin IV AT4-receptor system in the rat kidney. Am J Physiol 1998, 274:F290-299.
30. Albiston AL, McDowall SG, Matsacos D, Sim P, Clune E, Mustafa T, Lee J, Mendelsohn FA, Simpson RJ, Connolly LM, Chai SY. Evidence that the angiotensin IV (AT(4)) receptor is the enzyme insulin-regulated aminopeptidase. J Biol Chem 2001, 276:48623-48626.
31. Gesualdo L, Ranieri E, Monno R, Rossiello MR, Colucci M, Semeraro N, Grandaliano G, Schena FP, Ursi M, Cerullo G. Angiotensin IV stimulates plasminogen activator inhibitor-1 expression in proximal tubular epithelial cells. Kidney Int 1999, 56:461-470.
32. Ma LJ, Fogo AB. PAI-1 and kidney fibrosis. Front Biosci 2009, 14:2028-2041.
33. Hill-Kapturczak N, Kapturczak MH, Block ER, Patel JM, Malinski T, Madsen KM, Tisher CC. Angiotensin II-stimulated nitric oxide release from porcine pulmonary endothelium is mediated by angiotensin IV. J Am Soc Nephrol 1999, 10:481-491.
34. Chen JK, Zimpelmann J, Harris RC, Burns KD. Angiotensin IV induces tyrosine phosphorylation of focal adhesion kinase and paxillin in proximal tubule cells. Am J Physiol Renal Physiol 2001, 280:F980-988.
35. Wong YC, Sim MK, Lee KO. Des-aspartate-angiotensin-I and angiotensin IV improve glucose tolerance and insulin signalling in diet-induced hyperglycaemic mice. Biochem Pharmacol 2011,
36. Siebelmann M, Wensing J, Verspohl EJ. The impact of ANG II and IV on INS-1 cells and on blood glucose and plasma insulin. J Recept Signal Transduct Res 2010, 30:234-245.
37. Gard PR. Cognitive-enhancing effects of angiotensin IV. BMC Neurosci 2008, 9(Suppl 2):S15.
38. Kohara K, Brosnihan KB, Chappell MC, Khosla MC, Ferrario CM. Angiotensin-(1-7). A member of circulating angiotensin peptides. Hypertension 1991, 17:131-138.
39. Freeman EJ, Chisolm GM, Ferrario CM, Tallant EA. Angiotensin-(1-7) inhibits vascular smooth muscle cell growth. Hypertension 1996, 28:104-108.
40. Strawn WB, Ferrario CM, Tallant EA. Angiotensin-(1-7) reduces smooth muscle growth after vascular injury. Hypertension 1999, 33:207-211.
41. Benter IF, Ferrario CM, Morris M, Diz DI. Antihypertensive actions of angiotensin-(1-7) in spontaneously hypertensive rats. Am J Physiol 1995, 269:H313-319.
42. Clark MA, Diz DI, Tallant EA. Angiotensin-(1-7) downregulates the angiotensin II type 1 receptor in vascular smooth muscle cells. Hypertension 2001, 37:1141-1146.
43. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci USA 2003, 100:8258-8263.
44. Walther T, Wessel N, Kang N, Sander A, Tschope C, Malberg H, Bader M, Voss A. Altered heart rate and blood pressure variability in mice lacking the Mas protooncogene. Braz J Med Biol Res 2000, 33:1-9.
45. Peiro C, Vallejo S, Gembardt F, Azcutia V, Heringer-Walther S, Rodriguez-Manas L, Schultheiss HP, Sanchez-Ferrer CF, Walther T. Endothelial dysfunction through genetic deletion or inhibition of the G protein-coupled receptor Mas: a new target to improve endothelial function. J Hypertens 2007, 25:2421-2425.
46. Xu P, Santos RA, Bader M, Alenina N. Alterations in gene expression in the testis of angiotensin-(1-7)-receptor Mas-deficient mice. Regul Pept 2007, 138:51-55.
47. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J, Ferrario CM, Manoukian AS, Chappell MC, Backx PH, Yagil Y, Penninger JM. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 2002, 417:822-828.
48. Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, Godbout K, Parsons T, Baronas E, Hsieh F, Acton S, Patane M, Nichols A, Tummino P. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem 2002, 277:14838-14843.
49. Tikellis C, Johnston CI, Forbes JM, Burns WC, Burrell LM, Risvanis J, Cooper ME. Characterization of renal angiotensin-converting enzyme 2 in diabetic nephropathy. Hypertension 2003, 41:392-397.
50. Ferreira AJ, Santos RA, Bradford CN, Mecca AP, Sumners C, Katovich MJ, Raizada MK. Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases. Hypertension 2010, 55:207-213.
51. Perret-Guillaume C, Joly L, Jankowski P, Benetos A. Benefits of the RAS blockade: clinical evidence before the ONTARGET study. J Hypertens Suppl 2009, 27:S3-7.
52. Pereira RM, dos Santos RA, da Costa Dias FL, Teixeira MM, Simoes e Silva AC. Renin-angiotensin system in the pathogenesis of liver fibrosis. World J Gastroenterol 2009, 15:2579-2586.
53. Tharaux PL, Chatziantoniou C, Fakhouri F, Dussaule JC. Angiotensin II activates collagen I gene through a mechanism involving the MAP/ER kinase pathway. Hypertension 2000, 36:330-336.
54. Yaghini FA, Song CY, Lavrentyev EN, Ghafoor HU, Fang XR, Estes AM, Campbell WB, Malik KU. Angiotensin II-induced vascular smooth muscle cell migration and growth are mediated by cytochrome P450 1B1-dependent superoxide generation. Hypertension 2010, 55:1461-1467.
55. Xie Z, Singh M, Singh K. ERK1/2 and JNKs, but not p38 kinase, are involved in reactive oxygen species-mediated induction of osteopontin gene expression by angiotensin II and interleukin-1beta in adult rat cardiac fibroblasts. J Cell Physiol 2004, 198:399-407.
56. Li L, Fan D, Wang C, Wang JY, Cui XB, Wu D, Zhou Y, Wu LL. Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-β1 pathways in cardiac fibroblasts. Cardiovasc Res 2011, 91:80-89.
57. 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 2009, 54:877-884.
58. Zeng W, Chen W, Leng X, He JG, Ma H. Chronic angiotensin-(1-7) administration improves vascular remodeling after angioplasty through the regulation of the TGF-beta/Smad signaling pathway in rabbits. Biochem Biophys Res Commun 2009, 389:138-144.
59. Carvajal G, Rodriguez-Vita J, Rodrigues-Diez R, Sanchez-Lopez E, Ruperez M, Cartier C, Esteban V, Ortiz A, Egido J, Mezzano SA, Ruiz-Ortega M. Angiotensin II activates the Smad pathway during epithelial mesenchymal transdifferentiation. Kidney Int 2008, 74:585-595.
60. 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 2005, 111:2509-2517.
61. Liou JY, Hong HJ, Sung LC, Chao HH, Chen PY, Cheng TH, Chan P, Liu JC. Nicorandil Inhibits Angiotensin-II-Induced Proliferation of Cultured Rat Cardiac Fibroblasts. Pharmacology 2011, 87:144-151.
62. Wilmer WA, Hebert LA, Lewis EJ, Rohde RD, Whittier F, Cattran D, Levey AS, Lewis JB, Spitalewitz S, Blumenthal S, Bain RP. Remission of nephrotic syndrome in type 1 diabetes: long-term follow-up of patients in the Captopril Study. Am J Kidney Dis 1999, 34:308-314.
63. Group TG. Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia). Lancet 1997, 349:1857-1863.
64. Maschio G, Alberti D, Locatelli F, Mann JF, Motolese M, Ponticelli C, Ritz E, Janin G, Zucchelli P. Angiotensin-converting enzyme inhibitors and kidney protection: the AIPRI trial. The ACE Inhibition in Progressive Renal Insufficiency (AIPRI) Study Group. J Cardiovasc Pharmacol 1999, 33(Suppl 1):S16-20.
65. Ruggenenti P, Perna A, Gherardi G, Gaspari F, Benini R, Remuzzi G. Renal function and requirement for dialysis in chronic nephropathy patients on long-term ramipril: REIN follow-up trial. Gruppo Italiano di Studi Epidemiologici in Nefrologia (GISEN). Ramipril Efficacy in Nephropathy. Lancet 1998, 352:1252-1256.
66. Tyralla K, Adamczak M, Benz K, Campean V, Gross ML, Hilgers KF, Ritz E, Amann K. High-dose enalapril treatment reverses myocardial fibrosis in experimental uremic cardiomyopathy. PLoS ONE 2011, 6:e15287.
67. Gross O, Schulze-Lohoff E, Koepke ML, Beirowski B, Addicks K, Bloch W, Smyth N, Weber M. Antifibrotic, nephroprotective potential of ACE inhibitor vs AT1 antagonist in a murine model of renal fibrosis. Nephrol Dial Transplant 2004, 19:1716-1723.
68. Tang SC, Leung JC, Chan LY, Eddy AA, Lai KN. Angiotensin converting enzyme inhibitor but not angiotensin receptor blockade or statin ameliorates murine adriamycin nephropathy. Kidney Int 2008, 73:288-299.
69. Li Q, Wang Y, Sun SZ, Tian YJ, Liu MH. Effects of benazepril on cardiac fibrosis in STZ-induced diabetic rats. Acta Cardiol 2010, 65:431-439.
70. Imig JD, Navar GL, Zou LX, O'Reilly KC, Allen PL, Kaysen JH, Hammond TG, Navar LG. Renal endosomes contain angiotensin peptides, converting enzyme, and AT(1A) receptors. Am J Physiol 1999, 277:F303-311.
71. Lenfant M, Wdzieczak-Bakala J, Guittet E, Prome JC, Sotty D, Frindel E. Inhibitor of hematopoietic pluripotent stem cell proliferation: purification and determination of its structure. Proc Natl Acad Sci USA 1989, 86:779-782.
72. Grillon C, Rieger K, Bakala J, Schott D, Morgat JL, Hannappel E, Voelter W, Lenfant M. Involvement of thymosin beta 4 and endoproteinase Asp-N in the biosynthesis of the tetrapeptide AcSerAspLysPro a regulator of the hematopoietic system. FEBS Lett 1990, 274:30-34.
73. Liu JM, Garcia-Alvarez MC, Bignon J, Kusinski M, Kuzdak K, Riches A, Wdzieczak-Bakala J. Overexpression of the natural tetrapeptide acetyl-N-ser-asp-lys-pro derived from thymosin beta4 in neoplastic diseases. Ann NY Acad Sci 2010, 1194:53-59.
74. Cavasin MA, Rhaleb NE, Yang XP, Carretero OA. Prolyl oligopeptidase is involved in release of the antifibrotic peptide Ac-SDKP. Hypertension 2004, 43:1140-1145.
75. Huff T, Muller CS, Otto AM, Netzker R, Hannappel E. beta-Thymosins, small acidic peptides with multiple functions. Int J Biochem Cell Biol 2001, 33:205-220.
76. Hannappel E. Thymosin beta4 and its posttranslational modifications. Ann NY Acad Sci 2010, 1194:27-35.
77. Bock-Marquette I, Saxena A, White MD, Dimaio JM, Srivastava D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 2004, 432:466-472.
78. Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 2007, 445:177-182.
79. Wdzieczak-Bakala J, Fache MP, Lenfant M, Frindel E, Sainteny F. AcSDKP, an inhibitor of CFU-S proliferation, is synthesized in mice under steady-state conditions and secreted by bone marrow in long-term culture. Leukemia 1990, 4:235-237.
80. Azizi M, Rousseau A, Ezan E, Guyene TT, Michelet S, Grognet JM, Lenfant M, Corvol P, Menard J. Acute angiotensin-converting enzyme inhibition increases the plasma level of the natural stem cell regulator N-acetyl-seryl-aspartyl-lysyl-proline. J Clin Invest 1996, 97:839-844.
81. Kanasaki K, Haneda M, Sugimoto T, Shibuya K, Isono M, Isshiki K, Araki S, Uzu T, Kashiwagi A, Koya D. N-acetyl-seryl-aspartyl-lysyl-proline inhibits DNA synthesis in human mesangial cells via up-regulation of cell cycle modulators. Biochem Biophys Res Commun 2006, 342:758-765.
82. 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 2000, 66:PL221-226.
83. Rhaleb NE, Peng H, Harding P, Tayeh M, LaPointe MC, Carretero OA. Effect of N-acetyl-seryl-aspartyl-lysyl-proline on DNA and collagen synthesis in rat cardiac fibroblasts. Hypertension 2001, 37:827-832.
84. Rhaleb NE, Peng H, Yang XP, Liu YH, Mehta D, Ezan E, Carretero OA. Long-term effect of N-acetyl-seryl-aspartyl-lysyl-proline on left ventricular collagen deposition in rats with 2-kidney, 1-clip hypertension. Circulation 2001, 103:3136-3141.
85. Peng H, Carretero OA, Raij L, Yang F, Kapke A, Rhaleb NE. Antifibrotic effects of N-acetyl-seryl-aspartyl-lysyl-proline on the heart and kidney in aldosterone-salt hypertensive rats. Hypertension 2001, 37:794-800.
86. Pokharel S, Rasoul S, Roks AJ, van Leeuwen RE, van Luyn MJ, Deelman LE, Smits JF, Carretero O, van Gilst WH, Pinto YM. N-acetyl-Ser-Asp-Lys-Pro inhibits phosphorylation of Smad2 in cardiac fibroblasts. Hypertension 2002, 40:155-161.
87. Kanasaki K, Koya D, Sugimoto T, Isono M, Kashiwagi A, Haneda M. N-Acetyl-seryl-aspartyl-lysyl-proline inhibits TGF-beta-mediated plasminogen activator inhibitor-1 expression via inhibition of Smad pathway in human mesangial cells. J Am Soc Nephrol 2003, 14:863-872.
88. Border WA, Noble NA. Transforming growth factor beta in tissue fibrosis. New Engl J Med 1994, 331:1286-1292.
89. Miyazono K. TGF-beta signaling by Smad proteins. Cytokine Growth Factor Rev 2000, 11:15-22.
90. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang XF, Massague J. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992, 71:1003-1014.
91. Xiao Z, Liu X, Lodish HF. Importin beta mediates nuclear translocation of Smad 3. J Biol Chem 2000, 275:23425-23428.
92. Kurisaki A, Kose S, Yoneda Y, Heldin CH, Moustakas A. Transforming growth factor-beta induces nuclear import of Smad3 in an importin-beta1 and Ran-dependent manner. Mol Biol Cell 2001, 12:1079-1091.
93. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 1997, 389:631-635.
94. Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T, Miyazono K. Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem 2001, 276:12477-12480.
95. Suzuki C, Murakami G, Fukuchi M, Shimanuki T, Shikauchi Y, Imamura T, Miyazono K. Smurf1 regulates the inhibitory activity of Smad7 by targeting Smad7 to the plasma membrane. J Biol Chem 2002, 277:39919-39925.
96. Gronroos E, Hellman U, Heldin CH, Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol Cell 2002, 10:483-493.
97. Omata M, Taniguchi H, Koya D, Kanasaki K, Sho R, Kato Y, Kojima R, Haneda M, Inomata N. N-acetyl-seryl-aspartyl-lysyl-proline ameliorates the progression of renal dysfunction and fibrosis in WKY rats with established anti-glomerular basement membrane nephritis. J Am Soc Nephrol 2006, 17:674-685.
98. Lin CX, Rhaleb NE, Yang XP, Liao TD, D'Ambrosio MA, Carretero OA. Prevention of aortic fibrosis by N-acetyl-seryl-aspartyl-lysyl-proline in angiotensin II-induced hypertension. Am J Physiol Heart Circ Physiol 2008, 295:H1253-H1261.
99. Shah SA, Potter MW, Callery MP. Ubiquitin proteasome pathway: implications and advances in cancer therapy. Surg Oncol 2001, 10:43-52.
100. Bernstein KE, Shen XZ, Gonzalez-Villalobos RA, Billet S, Okwan-Duodu D, Ong FS, Fuchs S. Different in vivo functions of the two catalytic domains of angiotensin-converting enzyme (ACE). Curr Opin Pharmacol 2011, 11:105-111.
101. Wei L, Alhenc-Gelas F, Corvol P, Clauser E. The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J Biol Chem 1991, 266:9002-9008.
102. 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 1995, 270:3656-3661.
103. Zisman LS. Inhibiting tissue angiotensin-converting enzyme: a pound of flesh without the blood?. Circulation 1998, 98:2788-2790.
104. Li P, Xiao HD, Xu J, Ong FS, Kwon M, Roman J, Gal A, Bernstein KE, Fuchs S. Angiotensin-converting enzyme N-terminal inactivation alleviates bleomycin-induced lung injury. Am J Pathol 2010, 177:1113-1121.
105. Stephan J, Melaine N, Ezan E, Hakovirta H, Maddocks S, Toppari J, Garnier D, Wdzieczak-Bakala J, Jegou B. Source, catabolism and role of the tetrapeptide N-acetyl-ser-asp-lys-Pro within the testis. J Cell Sci 2000, 113:113-121.
106. 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 Chem 2004, 279:15946-15953.
107. Junot C, Gonzales MF, Ezan E, Cotton J, Vazeux G, Michaud A, Azizi M, Vassiliou S, Yiotakis A, Corvol P, Dive V. RXP 407, a selective inhibitor of the N-domain of angiotensin I-converting enzyme, blocks in vivo the degradation of hemoregulatory peptide acetyl-Ser-Asp-Lys-Pro with no effect on angiotensin I hydrolysis. J Pharmacol Exp Ther 2001, 297:606-611.
108. Vazeux G, Cotton J, Cuniasse P, Dive V. Potency and selectivity of RXP407 on human, rat, and mouse angiotensin-converting enzyme. Biochem Pharmacol 2001, 61:835-841.
109. Kroger WL, Douglas RG, O'Neill HG, Dive V, Sturrock ED. Investigating the domain specificity of phosphinic inhibitors RXPA380 and RXP407 in angiotensin-converting enzyme. Biochemistry 2009, 48:8405-8412.
110. Anthony CS, Corradi HR, Schwager SL, Redelinghuys P, Georgiadis D, Dive V, Acharya KR, Sturrock ED. The N domain of human angiotensin-I-converting enzyme: the role of N-glycosylation and the crystal structure in complex with an N domain-specific phosphinic inhibitor, RXP407. J Biol Chem 2010, 285:35685-35693.
111. Bomback AS, Klemmer PJ. The incidence and implications of aldosterone breakthrough. Nat Clin Pract Nephrol 2007, 3:486-492.
112. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. New Engl J Med 2001, 345:861-869.
113. Erdos EG, Tan F, Skidgel RA. Angiotensin I-converting enzyme inhibitors are allosteric enhancers of kinin B1 and B2 receptor function. Hypertension 2010, 55:214-220.
114. Schanstra JP, Neau E, Drogoz P, Arevalo Gomez MA, Lopez Novoa JM, Calise D, Pecher C, Bader M, Girolami JP, Bascands JL. In vivo bradykinin B2 receptor activation reduces renal fibrosis. J Clin Invest 2002, 110:371-379.
115. Kakoki M, Takahashi N, Jennette JC, Smithies O. Diabetic nephropathy is markedly enhanced in mice lacking the bradykinin B2 receptor. Proc Natl Acad Sci USA 2004, 101:13302-13305.
116. Schanstra JP, Duchene J, Desmond L, Neau E, Calise D, Estaque S, Girolami JP, Bascands JL. The protective effect of angiotensin converting enzyme inhibition in experimental renal fibrosis in mice is not mediated by bradykinin B2 receptor activation. Thromb Haemost 2003, 89:735-740.
117. Pawluczyk IZ, Patel SR, Harris KP. The role of bradykinin in the antifibrotic actions of perindoprilat on human mesangial cells. Kidney Int 2004, 65:1240-1251.
118. Mogensen CE, Neldam S, Tikkanen I, Oren S, Viskoper R, Watts RW, Cooper ME. Randomised controlled trial of dual blockade of renin-angiotensin system in patients with hypertension, microalbuminuria, and non-insulin dependent diabetes: the candesartan and lisinopril microalbuminuria (CALM) study. Br Med J 2000, 321:1440-1444.
119. Russo D, Minutolo R, Pisani A, Esposito R, Signoriello G, Andreucci M, Balletta MM. Coadministration of losartan and enalapril exerts additive antiproteinuric effect in IgA nephropathy. Am J Kidney Dis 2001, 38:18-25.
120. Kunz R, Friedrich C, Wolbers M, Mann JF. Meta-analysis: effect of monotherapy and combination therapy with inhibitors of the renin angiotensin system on proteinuria in renal disease. Ann Intern Med 2008, 148:30-48.
121. Granger CB, McMurray JJ, Yusuf S, Held P, Michelson EL, Olofsson B, Ostergren J, Pfeffer MA, Swedberg K. Effects of candesartan in patients with chronic heart failure and reduced left-ventricular systolic function intolerant to angiotensin-converting-enzyme inhibitors: the CHARM-Alternative trial. Lancet 2003, 362:772-776.
122. McMurray JJ, Ostergren J, Swedberg K, Granger CB, Held P, Michelson EL, Olofsson B, Yusuf S, Pfeffer MA. Effects of candesartan in patients with chronic heart failure and reduced left-ventricular systolic function taking angiotensin-converting-enzyme inhibitors: the CHARM-Added trial. Lancet 2003, 362:767-771.
123. Yusuf S, Pfeffer MA, Swedberg K, Granger CB, Held P, McMurray JJ, Michelson EL, Olofsson B, Ostergren J. Effects of candesartan in patients with chronic heart failure and preserved left-ventricular ejection fraction: the CHARM-Preserved Trial. Lancet 2003, 362:777-781.
124. Mann JF, Schmieder RE, McQueen M, Dyal L, Schumacher H, Pogue J, Wang X, Maggioni A, Budaj A, Chaithiraphan S, Dickstein K, Keltai M, Metsärinne K, Oto A, Parkhomenko A, Piegas LS, Svendsen TL, Teo KK, Yusuf S, . ONTARGET investigators Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial. Lancet 2008, 372:547-553. ONTARGET investigators.
125. Mauer M, Zinman B, Gardiner R, Suissa S, Sinaiko A, Strand T, Drummond K, Donnelly S, Goodyer P, Gubler MC, Klein R. Renal and retinal effects of enalapril and losartan in type 1 diabetes. New Engl J Med 2009, 361:40-51.
126. Metsarinne KP, Helin KH, Saijonmaa O, Stewen P, Sirvio ML, Fyhrquist FY. Tissue-specific regulation of angiotensin-converting enzyme by angiotensin II and losartan in the rat. Blood Press 1996, 5:363-370.
127. Pradelles P, Frobert Y, Creminon C, Ivonine H, Frindel E. Distribution of a negative regulator of haematopoietic stem cell proliferation (AcSDKP) and thymosin beta 4 in mouse tissues. FEBS Lett 1991, 289:171-175.
128. Pradelles P, Frobert Y, Creminon C, Liozon E, Masse A, Frindel E. Negative regulator of pluripotent hematopoietic stem cell proliferation in human white blood cells and plasma as analysed by enzyme immunoassay. Biochem Biophys Res Commun 1990, 170:986-993.
129. Bogden AE, Carde P, de Paillette ED, Moreau JP, Tubiana M, Frindel E. Amelioration of chemotherapy-induced toxicity by cotreatment with AcSDKP, a tetrapeptide inhibitor of hematopoietic stem cell proliferation. Ann N Y Acad Sci 1991, 628:126-139.
130. Grillon C, Bonnet D, Mary JY, Lenfant M, Najman A, Guigon M. The tetrapeptide AcSerAspLysPro (Seraspenide), a hematopoietic inhibitor, may reduce the in vitro toxicity of 3'-azido-3'-deoxythymidine to human hematopoietic progenitors. Stem Cells 1993, 11:455-464.
131. Deeg HJ, Seidel K, Hong DS, Yu C, Huss R, Schuening FG, Ewel CH, Storb R. In vivo radioprotective effect of AcSDKP on canine myelopoiesis. Ann Hematol 1997, 74:117-122.
132. Watanabe T, Brown GS, Kelsey LS, Yan Y, Jackson JD, Ewel C, Kessinger A, Talmadge JE. In vivo protective effects of tetrapeptide AcSDKP, with or without granulocyte colony-stimulation factor, on murine progenitor cells after sublethal irradiation. Exp Hematol 1996, 24:713-721.
133. Wierenga PK, Brenner MK, Konings AW. Enhanced selectivity of hyperthermic purging of human progenitor cells using Goralatide, an inhibitor of cell cycle progression. Bone Marrow Transplant 1998, 21:73-78.
134. Wierenga PK, Konings AW. Seraspenide (AcSDKP) mediated protection of hematopoietic stem cells in a hyperthermic purging protocol. Prog Clin Biol Res 1994, 389:189-195.
135. Wierenga PK, Setroikromo R, Vellenga E, Kampinga HH. Purging of acute myeloid leukaemia cells from stem cell grafts by hyperthermia: enhancement of the therapeutic index by the tetrapeptide AcSDKP and the alkyl-lysophospholipid ET-18-OCH(3). Br J Haematol 2000, 111:1145-1152.
136. Coutton C, Guigon M, Bohbot A, Ferrani K, Oberling F. Photoprotection of normal human hematopoietic progenitors by the tetrapeptide N-AcSDKP. Exp Hematol 1994, 22:1076-1080.
137. Coward WR, Saini G, Jenkins G. The pathogenesis of idiopathic pulmonary fibrosis. Ther Adv Respir Dis 2010, 4:367-388.
138. Rodriguez-Iturbe B, Garcia Garcia G. The role of tubulointerstitial inflammation in the progression of chronic renal failure. Nephron Clin Pract 2010, 116:c81-88.
139. Gieling RG, Burt AD, Mann DA. Fibrosis and cirrhosis reversibility-molecular mechanisms. Clin Liver Dis 2008, 12:915-937, xi.
140. Dooley R, Harvey BJ, Thomas W. The regulation of cell growth and survival by aldosterone. Front Biosci 2011, 16:440-457.
141. Chen YW, Liu BW, Zhang YJ, Chen YW, Dong GF, Ding XD, Xu LM, Pat B, Fan JG, Li DG. Preservation of basal AcSDKP attenuates carbon tetrachloride-induced fibrosis in the rat liver. J Hepatol 2010, 53:528-536.
142. Liu YH, D'Ambrosio M, Liao TD, Peng H, Rhaleb NE, Sharma U, Andre S, Gabius HJ, Carretero OA. N-acetyl-seryl-aspartyl-lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am J Physiol Heart Circ Physiol 2009, 296:H404-412.
143. Sharma U, Rhaleb NE, Pokharel S, Harding P, Rasoul S, Peng H, Carretero OA. Novel anti-inflammatory mechanisms of N-acetyl-Ser-Asp-Lys-Pro in hypertension-induced target organ damage. Am J Physiol Heart Circ Physiol 2008, 294:H1226-1232.
144. 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 2007, 49:695-703.
145. Yang F, Yang XP, Liu YH, Xu J, Cingolani O, Rhaleb NE, Carretero OA. Ac-SDKP reverses inflammation and fibrosis in rats with heart failure after myocardial infarction. Hypertension 2004, 43:229-236.
146. Wang M, Liu R, Jia X, Mu S, Xie R. N-acetyl-seryl-aspartyl-lysyl-proline attenuates renal inflammation and tubulointerstitial fibrosis in rats. Int J Mol Med 2010, 26:795-801.
147. Sun Y, Yang F, Yan J, Li Q, Wei Z, Feng H, Wang R, Zhang L, Zhang X. New anti-fibrotic mechanisms of n-acetyl-seryl-aspartyl-lysyl-proline in silicon dioxide-induced silicosis. Life Sci 2010, 87:232-239.
148. Peng H, Carretero OA, Peterson EL, Rhaleb NE. Ac-SDKP inhibits transforming growth factor-beta1-induced differentiation of human cardiac fibroblasts into myofibroblasts. Am J Physiol Heart Circ Physiol 2010, 298:H1357-1364.
149. Liu JM, Lawrence F, Kovacevic M, Bignon J, Papadimitriou E, Lallemand JY, Katsoris P, Potier P, Fromes Y, Wdzieczak-Bakala J. The tetrapeptide AcSDKP, an inhibitor of primitive hematopoietic cell proliferation, induces angiogenesis in vitro and in vivo. Blood 2003, 101:3014-3020.
150. Wang D, Carretero OA, Yang XY, Rhaleb NE, Liu YH, Liao TD, Yang XP. N-acetyl-seryl-aspartyl-lysyl-proline stimulates angiogenesis in vitro and in vivo. Am J Physiol Heart Circ Physiol 2004, 287:H2099-2105.
151. Fromes Y, Liu JM, Kovacevic M, Bignon J, Wdzieczak-Bakala J. The tetrapeptide acetyl-serine-aspartyl-lysine-proline improves skin flap survival and accelerates wound healing. Wound Repair Regen 2006, 14:306-312.
152. Koutrafouri V, Leondiadis L, Avgoustakis K, Livaniou E, Czarnecki J, Ithakissios DS, Evangelatos GP. Effect of thymosin peptides on the chick chorioallantoic membrane angiogenesis model. Biochim Biophys Acta 2001, 1568:60-66.
153. Philp D, Huff T, Gho YS, Hannappel E, Kleinman HK. The actin binding site on thymosin beta4 promotes angiogenesis. FASEB J 2003, 17:2103-2105.
154. Malinda KM, Goldstein AL, Kleinman HK. Thymosin beta 4 stimulates directional migration of human umbilical vein endothelial cells. FASEB J 1997, 11:474-481.
155. Liu JM, Bignon J, Ilic V, Briscoe C, Lallemand JY, Riches A, Wdzieczak-Bakala J. Evidence for an association of high levels of endogenous Acetyl-Ser-Asp-Lys-Pro, a potent mediator of angiogenesis, with acute myeloid leukemia development. Leuk Lymphoma 2006, 47:1915-1920.
156. Liu JM, Kusinski M, Ilic V, Bignon J, Hajem N, Komorowski J, Kuzdak K, Stepien H, Wdzieczak-Bakala J. Overexpression of the angiogenic tetrapeptide AcSDKP in human malignant tumors. Anticancer Res 2008, 28:2813-2817.
157. Liu JM, Gora-Tybor J, Grzybowska-Izydorczyk O, Bignon J, Robak T, Wdzieczak-Bakala J. Elevated plasma levels of the angiogenic tetrapeptide acetyl-ser-asp-lys-pro are found in some patients with hematologic malignancies. Leuk Lymphoma 2009, 50:2096-2097.
158. Folkman J. Angiogenesis: an organizing principle for drug discovery?. Nat Rev Drug Discov 2007, 6:273-286.
159. Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res 2005, 65:3967-3979.
160. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, Chandraker A, Yuan X, Pu WT, Roberts AB, Neilson EG, Sayegh MH, Izumo S, Kalluri R. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007, 13:952-961.
161. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003, 9:964-968.
162. Rieger KJ, Saez-Servent N, Papet MP, Wdzieczak-Bakala J, Morgat JL, Thierry J, Voelter W, Lenfant M. Involvement of human plasma angiotensin I-converting enzyme in the degradation of the haemoregulatory peptide N-acetyl-seryl-aspartyl-lysyl-proline. Biochem J 1993, 296:373-378.
163. Ezan E, Carde P, Le Kerneau J, Ardouin T, Thomas F, Isnard F, Deschamps de Paillette E, Grognet JM. Pharmcokinetics in healthy volunteers and patients of NAc-SDKP (seraspenide), a negative regulator of hematopoiesis. Drug Metab Dispos 1994, 22:843-848.
164. Robinson S, Lenfant M, Wdzieczak-Bakala J, Riches A. The molecular specificity of action of the tetrapeptide acetyl-N-Ser-Asp-Lys-Pro (AcSDKP) in the control of hematopoietic stem cell proliferation. Stem Cells 1993, 11:422-427.
165. Zhuo JL, Carretero OA, Peng H, Li XC, Regoli D, Neugebauer W, Rhaleb NE. Characterization and localization of Ac-SDKP receptor binding sites using 125I-labeled Hpp-Aca-SDKP in rat cardiac fibroblasts. Am J Physiol Heart Circ Physiol 2007, 292:H984-993.