Arginase inhibition: A new treatment for preventing progression of established diabetic nephropathy

American Journal of Physiology - Renal Physiology

Volumn 309, Issue 5, 2015, Pages F447-F455

  You, Hanning ^a   Gao, Ting ^a   Cooper, Timothy K ^a   Morris, Sidney M ^b   Awad, Alaa S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

ACEi; Arginase; Established diabetic nephropathy; Nitric oxide

Indexed keywords

(2 BORONOETHYL) CYSTEINE; ALBUMIN; ARGINASE; CAPTOPRIL; CREATININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENZYME INHIBITOR; NEPHRIN; NITRATE; NITRITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG; (2-BORONOETHYL)-CYSTEINE; BORONIC ACID DERIVATIVE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IMMUNOHISTOCHEMISTRY; KIDNEY BLOOD FLOW; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RENAL PROTECTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; DIABETIC NEPHROPATHIES; DISEASE COURSE; DRUG EFFECTS; KIDNEY; METABOLISM; PHOSPHORYLATION; TREATMENT OUTCOME;

ALBUMINURIA; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; ARGINASE; BORONIC ACIDS; CAPTOPRIL; DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; KIDNEY; MICE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; TREATMENT OUTCOME;

EID: 84940869104     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00137.2015     Document Type: Article

References (47)

1. Abdel-Rahman EM, Saadulla L, Reeves WB, Awad AS. Therapeutic modalities in diabetic nephropathy: standard and emerging approaches. J Gen Intern Med 27: 458–468, 2012.
2. Awad AS, Kinsey GR, Khutsishvili K, Gao T, Bolton WK, Okusa MD. Monocyte/macrophage chemokine receptor CCR2 mediates diabetic renal injury. Am J Physiol Renal Physiol 301: F1358–F1366, 2011.
3. Balakumar P, Chakkarwar VA, Krishan P, Singh M. Vascular endothelial dysfunction: a tug of war in diabetic nephropathy? Biomed Pharmacother 63: 171–179, 2009.
4. Bartosz M, Kedziora J, Bartosz G. Antioxidant and prooxidant properties of captopril and enalapril. Free Radic Biol Med 23: 729–735, 1997.
5. Baylis C. Nitric oxide deficiency in chronic kidney disease. Am J Physiol Renal Physiol 294: F1–F9, 2008.
6. Breyer MD, Bottinger E, Brosius FC, 3rd, Coffman TM, Harris RC, Heilig CW, Sharma K. Mouse models of diabetic nephropathy. J Am Soc Nephrol 16: 27–45, 2005.
7. Brosius FC, 3rd, Alpers CE, Bottinger EP, Breyer MD, Coffman TM, Gurley SB, Harris RC, Kakoki M, Kretzler M, Leiter EH, Levi M, McIndoe RA, Sharma K, Smithies O, Susztak K, Takahashi N, Takahashi T. Mouse models of diabetic nephropathy. J Am Soc Nephrol 20: 2503–2512, 2009.
8. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443: 285–289, 1999.
9. Cheng H, Harris RC. Renal endothelial dysfunction in diabetic nephropathy. Cardiovasc Hematol Disord Drug Targets 14: 22–33, 2014.
10. Cheng H, Wang H, Fan X, Paueksakon P, Harris RC. Improvement of endothelial nitric oxide synthase activity retards the progression of diabetic nephropathy in db/db mice. Kidney Int 82: 1176–1183, 2012.
11. Cheung CW, Cohen NS, Raijman L. Channeling of urea cycle intermediates in situ in permeabilized hepatocytes. J Biol Chem 264: 4038–4044, 1989.
12. Choi KC, Kim NH, An MR, Kang DG, Kim SW, Lee J. Alterations of intrarenal renin-angiotensin and nitric oxide systems in streptozotocininduced diabetic rats. Kidney Int Suppl 60: S23–S27, 1997.
13. Collins AJ, Foley RN, Herzog C, Chavers B, Gilbertson D, Ishani A, Johansen K, Kasiske B, Kutner N, Liu J, St Peter W, Ding S, Guo H, Kats A, Lamb K, Li S, Roberts T, Skeans M, Snyder J, Solid C, Thompson B, Weinhandl E, Xiong H, Yusuf A, Zaun D, Arko C, Chen SC, Daniels F, Ebben J, Frazier E, Hanzlik C, Johnson R, Sheets D, Wang X, Forrest B, Constantini E, Everson S, Eggers P, Agodoa L. US Renal Data System 2012 Annual Data Report. Am J Kidney Dis 61: A7, e1–476, 2013.
14. Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev 93: 137–188, 2013.
15. Giunti S, Barutta F, Perin PC, Gruden G. Targeting the MCP-1/CCR2 system in diabetic kidney disease. Curr Vasc Pharmacol 8: 849–860, 2010.
16. Gotoh T, Sonoki T, Nagasaki A, Terada K, Takiguchi M, Mori M. Molecular cloning of cDNA for nonhepatic mitochondrial arginase (arginase II) and comparison of its induction with nitric oxide synthase in a murine macrophage-like cell line. FEBS Lett 395: 119–122, 1996.
17. Hyndman KA, Boesen EI, Elmarakby AA, Brands MW, Huang P, Kohan DE, Pollock DM, Pollock JS. Renal collecting duct NOS1 maintains fluid-electrolyte homeostasis and blood pressure. Hypertension 62: 91–98, 2013.
18. Igarashi K, Ueda S, Yoshida K, Kashiwagi K. Polyamines in renal failure. Amino Acids 31: 477–483, 2006.
19. Kanetsuna Y, Takahashi K, Nagata M, Gannon MA, Breyer MD, Harris RC, Takahashi T. Deficiency of endothelial nitric oxide synthase confers susceptibility to diabetic nephropathy in nephropathy-resistant inbred mice. Am J Pathol 170: 1473–1484, 2007.
20. Keynan S, Hirshberg B, Levin-Iaina N, Wexler ID, Dahan R, Reinhartz E, Ovadia H, Wollman Y, Chernihovskey T, Iaina A, Raz I. Renal nitric oxide production during the early phase of experimental diabetes mellitus. Kidney Int 58: 740–747, 2000.
21. Komers R, Anderson S. Paradoxes of nitric oxide in the diabetic kidney. Am J Physiol Renal Physiol 284: F1121–F1137, 2003.
22. Lapenna D, Ciofani G, Pierdomenico SD, Giamberardino MA, Cuccurullo F. Reaction conditions affecting the relationship between thiobarbituric acid reactivity and lipid peroxides in human plasma. Free Radic Biol Med 31: 331–335, 2001.
23. Lovell HG. Angiotensin converting enzyme inhibitors in normotensive diabetic patients with microalbuminuria. Cochrane Database Syst Rev 1: CD002183, 2001.
24. Lu D, Fu Y, Lopez-Ruiz A, Zhang R, Juncos R, Liu H, Manning RD, Juncos LA, Liu R. Salt-sensitive splice variant of nNOS expressed in the macula densa cells. Am J Physiol Renal Physiol 298: F1465–F1471, 2010.
25. Martin MF, Surrall KE, McKenna F, Dixon JS, Bird HA, Wright V. Captopril: a new treatment for rheumatoid arthritis? Lancet 1: 1325–1328, 1984.
26. Morris SM Jr. Arginine metabolism: boundaries of our knowledge. J Nutr 137: 1602S–1609S, 2007.
27. Morris SM Jr, Bhamidipati D, Kepka-Lenhart D. Human type II arginase: sequence analysis and tissue-specific expression. Gene 193: 157–161, 1997.
28. Morris SM Jr, Gao T, Cooper TK, Kepka-Lenhart D, Awad AS. Arginase-2 mediates diabetic renal injury. Diabetes 60: 3015–3022, 2011.
29. Nakagawa T, Sato W, Glushakova O, Heinig M, Clarke T, Campbell-Thompson M, Yuzawa Y, Atkinson MA, Johnson RJ, Croker B. Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. J Am Soc Nephrol 18: 539–550, 2007.
30. Nakagawa T, Tanabe K, Croker BP, Johnson RJ, Grant MB, Kosugi T, Li Q. Endothelial dysfunction as a potential contributor in diabetic nephropathy. Nat Rev Nephrol 7: 36–44, 2011.
31. Shin SJ, Lai FJ, Wen JD, Hsiao PJ, Hsieh MC, Tzeng TF, Chen HC, Guh JY, Tsai JH. Neuronal and endothelial nitric oxide synthase expressionin outer medulla of streptozotocin-induced diabetic rat kidney. Diabetologia 43: 649–659, 2000.
32. Takahashi T, Harris RC. Role of endothelial nitric oxide synthase indiabetic nephropathy: lessons from diabetic eNOS knockout mice. JDiabetes Res 2014: 590541, 2014.
33. Tang WW, Qi M, Warren JS. Monocyte chemoattractant protein 1mediates glomerular macrophage infiltration in anti-GBM Ab GN. Kidney Int 50: 665–671, 1996.
34. Tipping PG, Leong TW, Holdsworth SR. Tumor necrosis factor production by glomerular macrophages in anti-glomerular basement membrane glomerulonephritis in rabbits. Lab Invest 65: 272–279, 1991.
35. Tipping PG, Lowe MG, Holdsworth SR. Glomerular interleukin 1 production is dependent on macrophage infiltration in anti-GBM glomerulonephritis. Kidney Int 39: 103–110, 1991.
36. Vockley JG, Jenkinson CP, Shukla H, Kern RM, Grody WW, Cederbaum SD. Cloning and characterization of the human type II arginase gene. Genomics 38: 118–123, 1996.
37. Wada T, Furuichi K, Sakai N, Iwata Y, Yoshimoto K, Shimizu M, Takeda SI, Takasawa K, Yoshimura M, Kida H, Kobayashi KI, Mukaida N, Naito T, Matsushima K, Yokoyama H. Up-regulation of monocyte chemoattractant protein-1 in tubulointerstitial lesions of humandiabetic nephropathy. Kidney Int 58: 1492–1499, 2000.
38. Wang CH, Li F, Hiller S, Kim HS, Maeda N, Smithies O, Takahashi N. A modest decrease in endothelial NOS in mice comparable to that associated with human NOS3 variants exacerbates diabetic nephropathy. Proc Natl Acad Sci USA 108: 2070–2075, 2011.
39. Wu G, Morris SM Jr. Arginine metabolism: nitric oxide and beyond. Biochem J 336: 1–17, 1998.
40. Yagihashi N, Nishida N, Seo HG, Taniguchi N, Yagihashi S. Expression of nitric oxide synthase in macula densa in streptozotocin diabetic rats. Diabetologia 39: 793–799, 1996.
41. You H, Gao T, Cooper TK, Brian Reeves W, Awad AS. Macrophages directly mediate diabetic renal injury. Am J Physiol Renal Physiol 305: F1719–F1727, 2013.
42. You H, Gao T, Cooper TK, Morris SM Jr, Awad AS. Arginase inhibition mediates renal tissue protection in diabetic nephropathy by a nitric oxide synthase 3-dependent mechanism. Kidney Int 84: 1189–1197, 2013.
43. You H, Gao T, Cooper TK, Morris SM Jr, Awad AS. Diabetic nephropathy is resistant to oral L-arginine or L-citrulline supplementation. Am J Physiol Renal Physiol 307: F1292–F1301, 2014.
44. Yuen DA, Stead BE, Zhang Y, White KE, Kabir MG, Thai K, Advani SL, Connelly KA, Takano T, Zhu L, Cox AJ, Kelly DJ, Gibson IW, Takahashi T, Harris RC, Advani A. eNOS deficiency predisposes podocytes to injury in diabetes. J Am Soc Nephrol 23: 1810–1823, 2012.
45. Zhang A, Huang S. Progress in pathogenesis of proteinuria. Int J Nephrol 2012: 314251, 2012.
46. Zhang MZ, Wang S, Yang S, Yang H, Fan X, Takahashi T, Harris RC. Role of blood pressure and the renin-angiotensin system in development of diabetic nephropathy (DN) in eNOS-/- db/db mice. Am J Physiol Renal Physiol 302: F433–F438, 2012.
47. Zhao HJ, Wang S, Cheng H, Zhang MZ, Takahashi T, Fogo AB, Breyer MD, Harris RC. Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice. J Am Soc Nephrol 17: 2664–2669, 2006.