Paricalcitol modulates ACE2 shedding and renal ADAM17 in NOD mice beyond proteinuria

American Journal of Physiology - Renal Physiology

Volumn 310, Issue 6, 2016, Pages F534-F546

  Riera, Marta ^a,b   Anguiano, Lidia ^a   Clotet, Sergi ^a   Roca Ho, Heleia ^a   Rebull, Marta ^a   Pascual, Julio ^a,b   Soler, Maria Jose ^a,b  

^a HOSPITAL DEL MAR   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Angiotensin converting enzyme 2; Animal model; Diabetic nephropathy; Renin angiotensin system

Indexed keywords

3 NITROTYROSINE; ADAM PROTEIN; ADAM17 PROTEIN; ALBUMIN; ALISKIREN; ANGIOTENSIN CONVERTING ENZYME 2; HYDROGEN PEROXIDE; PARICALCITOL; UNCLASSIFIED DRUG; DIPEPTIDYL CARBOXYPEPTIDASE; ERGOCALCIFEROL; RENIN; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVITY; FEMALE; IMMUNOLOCALIZATION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CORTEX; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PLASMA RENIN ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; URINARY EXCRETION; ANIMAL; BLOOD; BLOOD PRESSURE; DIABETIC NEPHROPATHIES; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; KIDNEY; METABOLISM; NONOBESE DIABETIC MOUSE; PRECLINICAL STUDY; RANDOMIZATION;

ADAM PROTEINS; ANIMALS; BLOOD PRESSURE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; DRUG EVALUATION, PRECLINICAL; ERGOCALCIFEROLS; FEMALE; KIDNEY; MICE, INBRED NOD; OXIDATIVE STRESS; PEPTIDYL-DIPEPTIDASE A; PROTEINURIA; RANDOM ALLOCATION; RENIN;

EID: 84980350558     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00082.2015     Document Type: Article

References (54)

1. Andersen S, Tarnow L, Rossing P, Hansen BV, Parving HH. Renoprotective effects of angiotensin II receptor blockade in type 1 diabetic patients with diabetic nephropathy. Kidney Int 57: 601-606, 2000
2. Arcidiacono MV, Yang J, Fernandez E, Dusso A. Parathyroid-specific epidermal growth factor-receptor inactivation prevents uremia-induced parathyroid hyperplasia in mice. Nephrol Dial Transplant 30: 434-440, 2015.
3. Batlle D, Wysocki J, Soler MJ, Ranganath K. Angiotensin-converting enzyme 2: enhancing the degradation of angiotensin II as a potential therapy for diabetic nephropathy. Kidney Int 81: 520-528, 2012
4. 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. N Engl J Med 345: 861-869, 2001.
5. 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 417: 822-828, 2002.
6. Chan JC, Ko GT, Leung DH, Cheung RC, Cheung MY, So WY, Swaminathan R, Nicholls MG, Critchley JA, Cockram CS. Long-term effects of angiotensin-converting enzyme inhibition and metabolic control in hypertensive type 2 diabetic patients. Kidney Int 57: 590-600, 2000
7. Chen S, Gardner DG. Liganded vitamin D receptor displays antihypertrophic activity in the murine heart. J Steroid Biochem Mol Biol 136: 150-155, 2012.
8. Chodavarapu H, Grobe N, Somineni HK, Salem ES, Madhu M, Elased KM. Rosiglitazone treatment of type 2 diabetic db/db miceattenuates urinary albumin and angiotensin converting enzyme 2 excretion. PLoS One 8: e62833, 2013.
9. Choi DE, Jeong JY, Lim BJ, Chang YK, Na KR, Shin YT, Lee KW. Aliskiren ameliorates renal inflammation and fibrosis induced by unilateral ureteral obstruction in mice. J Urol 186: 694-701, 2011.
10. Choi JH, Ke Q, Bae S, Lee JY, Kim YJ, Kim UK, Arbeeny C, Thadhani R, Kang PM. Doxercalciferol, a pro-hormone of vitamin D, prevents the development of cardiac hypertrophy in rats. J Card Fail 17: 1051-1058, 2011.
11. de Zeeuw D, Agarwal R, Amdahl M, Audhya P, Coyne D, Garimella T, Parving HH, Pritchett Y, Remuzzi G, Ritz E, Andress D. Selective vitamin D receptor activation with paricalcitol for reduction of albumin-uria in patients with type 2 diabetes (VITAL study): a randomised controlled trial. Lancet 376: 1543-1551, 2010.
12. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87: E1-E9, 2000.
13. Dusso A, Arcidiacono MV, Yang J, Tokumoto M. Vitamin D inhibition of TACE and prevention of renal osteodystrophy and cardiovascular mortality. J Steroid Biochem Mol Biol 121: 193-198, 2010.
14. Finch JL, Suarez EB, Husain K, Ferder L, Cardema MC, Glenn DJ, Gardner DG, Liapis H, Slatopolsky E. Effect of combining an ACE inhibitor and a VDR activator on glomerulosclerosis, proteinuria, and renal oxidative stress in uremic rats. Am J Physiol Renal Physiol 302: F141-F149, 2012.
15. Haudek SB, Cheng J, Du J, Wang Y, Hermosillo-Rodriguez J, Trial J, Taffet GE, Entman ML. Monocytic fibroblast precursors mediate fibrosis in angiotensin-II-induced cardiac hypertrophy. J Mol Cell Cardiol 49: 499-507, 2010.
16. Izquierdo MJ, Cavia M, Muniz P, de Francisco AL, Arias M, Santos J, Abaigar P. Paricalcitol reduces oxidative stress and inflammation in hemodialysis patients. BMC Nephrol 13: 159, 2012.
17. Jia HP, Look DC, Tan P, Shi L, Hickey M, Gakhar L, Chappell MC, Wohlford-Lenane C, McCray PB Jr. Ectodomain shedding of angiotensin converting enzyme 2 in human airway epithelia. Am J Physiol Lung Cell Mol Physiol 297: L84-L96, 2009.
18. Kong J, Kim GH, Wei M, Sun T, Li G, Liu SQ, Li X, Bhan I, Zhao Q, Thadhani R, Li YC. Therapeutic effects of vitamin D analogs on cardiac hypertrophy in spontaneously hypertensive rats. Am J Pathol 177: 622-631, 2010.
19. Kong J, Li YC. Effect of ANG II type I receptor antagonist and ACE inhibitor on vitamin D receptor-null mice. Am J Physiol Regul Integr Comp Physiol 285: R255-R261, 2003.
20. Lambert DW, Lambert LA, Clarke NE, Hooper NM, Porter KE, Turner AJ. Angiotensin-converting enzyme 2 is subject to post-transcriptional regulation by miR-421. Clin Sci (Lond) 127: 243-249, 2014.
21. Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rohde R, Raz I. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 345: 851-860, 2001.
22. Li YC, Qiao G, Uskokovic M, Xiang W, Zheng W, Kong J. Vitamin D: a negative endocrine regulator of the renin-angiotensin system and blood pressure. J Steroid Biochem Mol Biol 89-90: 387-392, 2004.
23. Mancuso P, Rahman A, Hershey SD, Dandu L, Nibbelink KA, Simpson RU. 1,25-Dihydroxyvitamin-D3 treatment reduces cardiac hypertrophy and left ventricular diameter in spontaneously hypertensive heart failure-prone (cp/) rats independent of changes in serum leptin. J Cardiovasc Pharmacol 51: 559-564, 2008.
24. Marquez E, Riera M, Pascual J, Soler MJ. Albumin inhibits the insulin-mediated ACE2 increase in cultured podocytes. Am J Physiol Renal Physiol 306: F1327-F1334, 2014.
25. Márquez E, Riera M, Pascual J, Soler MJ. Renin-angiotensin system within the diabetic podocyte. Am J Physiol Renal Physiol 308: F1-F10, 2015.
26. Mizobuchi M, Nakamura H, Tokumoto M, Finch J, Morrissey J, Liapis H, Slatopolsky E. Myocardial effects of VDR activators in renal failure. J Steroid Biochem Mol Biol 121: 188-192, 2010.
27. Morgado-Pascual JL, Rayego-Mateos S, Valdivielso JM, Ortiz A, Egido J, Ruiz-Ortega M. Paricalcitol inhibits aldosterone-induced proinflammatory factors by modulating epidermal growth factor receptor pathway in cultured tubular epithelial cells. Biomed Res Int 2015: 783538, 2015.
28. Nakai K, Fujii H, Kono K, Goto S, Kitazawa R, Kitazawa S, Hirata M, Shinohara M, Fukagawa M, Nishi S. Vitamin D activates the Nrf2-Keap1 antioxidant pathway and ameliorates nephropathy in diabetic rats. Am J Hypertens 27: 586-595, 2014.
29. Oliveira EM, Santos RA, Krieger JE. Standardization of a fluorimetric assay for the determination of tissue angiotensin-converting enzyme activity in rats. Braz J Med Biol Res 33: 755-764, 2000.
30. Parajuli N, Marine A, Simmons S, Saba H, Mitchell T, Shimizu T, Shirasawa T, Macmillan-Crow LA. Generation and characterization of a novel kidney-specific manganese superoxide dismutase knockout mouse. Free Radic Biol Med 51: 406-416, 2011.
31. Parving HH, Lehnert H, Brochner-Mortensen J, Gomis R, Andersen S, Arner P. The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med 345: 870-878, 2001.
32. Price DA, Porter LE, Gordon M, Fisher ND, De’Oliveira JM, Laffel LM, Passan DR, Williams GH, Hollenberg NK. The paradox of the low-renin state in diabetic nephropathy. J Am Soc Nephrol 10: 2382-2391, 1999.
33. Riera M, Marquez E, Clotet S, Gimeno J, Roca-Ho H, Lloreta J, Juanpere N, Batlle D, Pascual J, Soler MJ. Effect of insulin on ACE2 activity and kidney function in the non-obese diabetic mouse. PLoS One 9: e84683, 2014.
34. Ritz E, Rychlik I, Locatelli F, Halimi S. End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions. Am J Kidney Dis 34: 795-808, 1999.
35. Rosmalen JG, Pigmans MJ, Kersseboom R, Drexhage HA, Leenen PJ, Homo-Delarche F. Sex steroids influence pancreatic islet hypertrophy and subsequent autoimmune infiltration in nonobese diabetic (NOD) and NODscid mice. Lab Invest 81: 231-239, 2001.
36. Salem ES, Grobe N, Elased KM. Insulin treatment attenuates renal ADAM17 and ACE2 shedding in diabetic Akita mice. Am J Physiol Renal Physiol 306: F629-F639, 2014.
37. Sanchez-Niño MD, Bozic M, Córdoba-Lanús E, Valcheva P, Gracia O, Ibarz M, Fernandez E, Navarro-Gonzalez JF, Ortiz A, Valdivielso JM. Beyond proteinuria: VDR activation reduces renal inflammation in experimental diabetic nephropathy. Am J Physiol Renal Physiol 302: F647-F657, 2012.
38. Schwager SL, Carmona AK, Sturrock ED. A high-throughput fluorimetric assay for angiotensin I-converting enzyme. Nat Protoc 1: 1961-1964, 2006.
39. Shaltout HA, Westwood BM, Averill DB, Ferrario CM, Figueroa JP, Diz DI, Rose JC, Chappell MC. Angiotensin metabolism in renal proximal tubules, urine, and serum of sheep: evidence for ACE2-depen-dent processing of angiotensin II. Am J Physiol Renal Physiol 292: F82-F91, 2007.
40. Soler MJ, Wysocki J, Batlle D. ACE2 alterations in kidney disease. Nephrol Dial Transplant 28: 2687-2697, 2013.
41. Soler MJ, Wysocki J, Ye M, Lloveras J, Kanwar Y, Batlle D. ACE2 inhibition worsens glomerular injury in association with increased ACE expression in streptozotocin-induced diabetic mice. Kidney Int 72: 614-623, 2007.
42. Somineni HK, Boivin GP, Elased KM. Daily exercise training protects against albuminuria and angiotensin converting enzyme 2 shedding in db/db diabetic mice. J Endocrinol 221: 235-251, 2014.
43. Sumitomo-Ueda Y, Aihara K, Ise T, Yoshida S, Ikeda Y, Uemoto R, Yagi S, Iwase T, Ishikawa K, Hirata Y, Akaike M, Sata M, Kato S, Matsumoto T. Heparin cofactor II protects against angiotensin II-induced cardiac remodeling via attenuation of oxidative stress in mice. Hyperten-sion 56: 430-436, 2010.
44. Tikellis C, Bialkowski K, Pete J, Sheehy K, Su Q, Johnston C, Cooper ME, Thomas MC. ACE2 deficiency modifies renoprotection afforded by ACE inhibition in experimental diabetes. Diabetes 57: 1018-1025, 2008.
45. Wang G, Lai FM, Lai KB, Chow KM, Kwan CH, Li KT, Szeto CC. Discrepancy between intrarenal messenger RNA and protein expression of ACE and ACE2 in human diabetic nephropathy. Am J Nephrol 29: 524-531, 2009.
46. Wu-Wong JR, Noonan W, Nakane M, Brooks KA, Segreti JA, Polakowski JS, Cox B. Vitamin d receptor activation mitigates the impact of uremia on endothelial function in the 5/6 nephrectomized rats. Int J Endocrinol 2010: 625852, 2010.
47. Wysocki J, Ye M, Soler MJ, Gurley SB, Xiao HD, Bernstein KE, Coffman TM, Chen S, Batlle D. ACE and ACE2 activity in diabetic mice. Diabetes 55: 2132-2139, 2006.
48. Xiang W, Kong J, Chen S, Cao LP, Qiao G, Zheng W, Liu W, Li X, Gardner DG, Li YC. Cardiac hypertrophy in vitamin D receptor knockout mice: role of the systemic and cardiac renin-angiotensin systems. Am J Physiol Endocrinol Metab 288: E125-E132, 2005.
49. Yamaleyeva LM, Gilliam-Davis S, Almeida I, Brosnihan KB, Lindsey SH, Chappell MC. Differential regulation of circulating and renal ACE2 and ACE in hypertensive mRen2.Lewis rats with early-onset diabetes. Am J Physiol Renal Physiol 302: F1374-F1384, 2012.
50. Ye M, Wysocki J, William J, Soler MJ, Cokic I, Batlle D. Glomerular localization and expression of angiotensin-converting enzyme 2 and angiotensin-converting enzyme: implications for albuminuria in diabetes. J Am Soc Nephrol 17: 3067-3075, 2006.
51. Yuan W, Pan W, Kong J, Zheng W, Szeto FL, Wong KE, Cohen R, Klopot A, Zhang Z, Li YC. 1,25-dihydroxyvitamin D3 suppresses renin gene transcription by blocking the activity of the cyclic AMP response element in the renin gene promoter. J Biol Chem 282: 29821-29830, 2007.
52. Zhang Z, Sun L, Wang Y, Ning G, Minto AW, Kong J, Quigg RJ, Li YC. Renoprotective role of the vitamin D receptor in diabetic nephropathy. Kidney Int 73: 163-171, 2008.
53. Zhang Z, Zhang Y, Ning G, Deb DK, Kong J, Li YC. Combination therapy with AT1 blocker and vitamin D analog markedly ameliorates diabetic nephropathy: blockade of compensatory renin increase. Proc Natl Acad Sci USA 105: 15896-15901, 2008.
54. Zoccali C, Curatola G, Panuccio V, Tripepi R, Pizzini P, Versace M, Bolignano D, Cutrupi S, Politi R, Tripepi G, Ghiadoni L, Thadhani R, Mallamaci F. Paricalcitol and endothelial function in chronic kidney disease trial. Hypertension 64: 1005-1011, 2014