Activation of ENaC in collecting duct cells by prorenin and its receptor PRR: Involvement of Nox4-derived hydrogen peroxide

American Journal of Physiology - Renal Physiology

Volumn 310, Issue 11, 2016, Pages F1243-F1250

  Lu, Xiaohan ^a,b   Wang, Fei ^a,b   Liu, Mi ^a,b   Yang, Kevin T ^a   Nau, Adam ^a   Kohan, Donald E ^a   Van Reese, ^a   Richardson, Russell S ^a   Yang, Tianxin ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

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

Author keywords

(pro)renin receptor; Epithelial sodium channel; Hydrogen peroxide; Inner medullary collecting duct; Renin activity

Indexed keywords

AMILORIDE; APOCYNIN; CATALASE; EPITHELIAL SODIUM CHANNEL; GKT 137892; HYDROGEN PEROXIDE; OXIDOREDUCTASE INHIBITOR; PRO 20; PRORENIN; PRORENIN RECEPTOR; REACTIVE OXYGEN METABOLITE; RECEPTOR BLOCKING AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; TEMPOL; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; EPITHELIAL SODIUM CHANNEL BLOCKING AGENT; NOX4 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN;

ARTICLE; CONTROLLED STUDY; GENE SILENCING; IN VITRO STUDY; INTRACELLULAR SIGNALING; KIDNEY COLLECTING TUBULE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SODIUM CELL LEVEL; SODIUM TRANSPORT; SPIN TRAPPING; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION;

AMILORIDE; ANIMALS; CELL LINE; EPITHELIAL SODIUM CHANNEL BLOCKERS; EPITHELIAL SODIUM CHANNELS; HYDROGEN PEROXIDE; KIDNEY TUBULES, COLLECTING; MICE; NADPH OXIDASE; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RECEPTORS, CELL SURFACE; RENIN; RNA, SMALL INTERFERING;

EID: 84984659023     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00492.2015     Document Type: Article

References (42)

1. Advani A, Kelly DJ, Cox AJ, White KE, Advani SL, Thai K, Connelly KA, Yuen D, Trogadis J, Herzenberg AM, Kuliszewski MA, Leong-Poi H, Gilbert RE. The (Pro)renin receptor: site-specific and functional linkage to the vacuolar H<-ATPase in the kidney. Hypertension 54: 261–269, 2009.
2. Batenburg WW, Krop M, Garrelds IM, de Vries R, de Bruin RJ, Burckle CA, Muller DN, Bader M, Nguyen G, Danser AH. Prorenin is the endogenous agonist of the (pro)renin receptor. Binding kinetics of renin and prorenin in rat vascular smooth muscle cells overexpressing the human (pro)renin receptor. J Hypertens 25: 2441–2453, 2007.
3. Bens M, Vallet V, Cluzeaud F, Pascual-Letallec L, Kahn A, RafestinOblin ME, Rossier BC, Vandewalle A. Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. J Am Soc Nephrol 10: 923–934, 1999.
4. Burckle C, Bader M. Prorenin and its ancient receptor. Hypertension 48: 549–551, 2006.
5. Clavreul N, Sansilvestri-Morel P, Magard D, Verbeuren TJ, Rupin A. (Pro)renin promotes fibrosis gene expression in HEK cells through a Nox4dependent mechanism. Am J Physiol Renal Physiol 300: F1310–F1318, 2011.
6. Gonzalez AA, Lara LS, Luffman C, Seth DM, Prieto MC. Soluble form of the (pro)renin receptor is augmented in the collecting duct and urine of chronic angiotensin II-dependent hypertensive rats. Hypertension 57: 859–864, 2011.
7. Gonzalez AA, Liu L, Lara LS, Seth DM, Navar LG, Prieto MC. Angiotensin II stimulates renin in inner medullary collecting duct cells via protein kinase C and independent of epithelial sodium channel and mineralocorticoid receptor activity. Hypertension 57: 594–599, 2011.
8. Gonzalez AA, Luffman C, Bourgeois CR, Vio CP, Prieto MC. Angiotensin II-independent upregulation of cyclooxygenase-2 by activation of the (Pro)renin receptor in rat renal inner medullary cells. Hypertension 61: 443–449, 2013.
9. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, Pennathur S, Martinez FJ, Thannickal VJ. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 15: 1077–1081, 2009.
10. Ilatovskaya DV, Pavlov TS, Levchenko V, Staruschenko A. ROS production as a common mechanism of ENaC regulation by EGF, insulin, and IGF-1. Am J Physiol Cell Physiol 304: C102–C111, 2013.
11. Kang JJ, Toma I, Sipos A, Meer EJ, Vargas SL, Peti-Peterdi J. The collecting duct is the major source of prorenin in diabetes. Hypertension 51: 1597–1604, 2008.
12. Lee DY, Kim HS, Won KJ, Lee KP, Jung SH, Park ES, Choi WS, Lee HM, Kim B. DJ-1 regulates the expression of renal (pro)renin receptor via reactive oxygen species-mediated epigenetic modification. Biochim Biophys Acta 1850: 426–434, 2015.
13. Li W, Sullivan MN, Zhang S, Worker CJ, Xiong Z, Speth RC, Feng Y. Intracerebroventricular infusion of the (Pro)renin receptor antagonist PRO20 attenuates deoxycorticosterone acetate-salt-induced hypertension. Hypertension 65: 352–361, 2015.
14. Ludwig J, Kerscher S, Brandt U, Pfeiffer K, Getlawi F, Apps DK, Schagger H. Identification and characterization of a novel 9.2-kDa membrane sector-associated protein of vacuolar proton-ATPase from chromaffin granules. J Biol Chem 273: 10939–10947, 1998.
15. + channel (ENaC) in distal nephron additively to aldosterone. J Biol Chem 287: 660–671, 2012.
16. McCormick JA, Bhalla V, Pao AC, Pearce D. SGK1: a rapid aldosterone-induced regulator of renal sodium reabsorption. Physiology 20: 134–139, 2005.
17. Montezano AC, Burger D, Ceravolo GS, Yusuf H, Montero M, Touyz RM. Novel Nox homologues in the vasculature: focusing on Nox4 and Nox5. Clin Sci 120: 131–141, 2011.
18. Nabi AH, Kageshima A, Uddin MN, Nakagawa T, Park EY, Suzuki F. Binding properties of rat prorenin and renin to the recombinant rat renin/prorenin receptor prepared by a baculovirus expression system. Int J Mol Med 18: 483–488, 2006.
19. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109: 1417–1427, 2002.
20. Nishimoto M, Fujita T. Renal mechanisms of salt-sensitive hypertension: contribution of two steroid receptor-associated pathways. Am J Physiol Renal Physiol 308: F377–F387, 2015.
21. Peng H, Li W, Seth DM, Nair AR, Francis J, Feng Y. (Pro)renin receptor mediates both angiotensin II-dependent and -independent oxidative stress in neuronal cells. PLoS One 8: e58339, 2013.
22. Prieto-Carrasquero MC, Botros FT, Pagan J, Kobori H, Seth DM, Casarini DE, Navar LG. Collecting duct renin is upregulated in both kidneys of 2-kidney, 1-clip goldblatt hypertensive rats. Hypertension 51: 1590–1596, 2008.
23. Prieto-Carrasquero MC, Harrison-Bernard LM, Kobori H, Ozawa Y, Hering-Smith KS, Hamm LL, Navar LG. Enhancement of collecting duct renin in angiotensin II-dependent hypertensive rats. Hypertension 44: 223–229, 2004.
24. Ramkumar N, Stuart D, Rees S, Hoek AV, Sigmund CD, Kohan DE. Collecting duct-specific knockout of renin attenuates angiotensin II-induced hypertension. Am J Physiol Renal Physiol 307: F931–F938, 2014.
25. Ramkumar N, Ying J, Stuart D, Kohan DE. Overexpression of Renin in the collecting duct causes elevated blood pressure. Am J Hypertens 26: 965–972, 2013.
26. Ringholm L, Pedersen-Bjergaard U, Thorsteinsson B, Boomsma F, Damm P, Mathiesen ER. A high concentration of prorenin in early pregnancy is associated with development of pre-eclampsia in women with type 1 diabetes. Diabetologia 54: 1615–1619, 2011.
27. Rohrwasser A, Morgan T, Dillon HF, Zhao L, Callaway CW, Hillas E, Zhang S, Cheng T, Inagami T, Ward K, Terreros DA, Lalouel JM. Elements of a paracrine tubular renin-angiotensin system along the entire nephron. Hypertension 34: 1265–1274, 1999.
28. Rossier BC, Baker ME, Studer RA. Epithelial sodium transport and its control by aldosterone: the story of our internal environment revisited. Physiol Rev 95: 297–340, 2015.
29. Rossman MJ, Groot HJ, Reese V, Zhao J, Amann M, Richardson RS. Oxidative stress and COPD: the effect of oral antioxidants on skeletal muscle fatigue. Med Sci Sports Exerc 45: 1235–1243, 2013.
30. Sealey JE, McCord D, Taufield PA, Ales KA, Druzin ML, Atlas SA, Laragh JH. Plasma prorenin in first-trimester pregnancy: relationship to changes in human chorionic gonadotropin. Am J Obstet Gynecol 153: 514–519, 1985.
31. Shi P, Grobe JL, Desland FA, Zhou G, Shen XZ, Shan Z, Liu M, Raizada MK, Sumners C. Direct pro-inflammatory effects of prorenin on microglia. PLoS One 9: e92937, 2014.
32. Sousa T, Pinho D, Morato M, Marques-Lopes J, Fernandes E, Afonso J, Oliveira S, Carvalho F, Albino-Teixeira A. Role of superoxide and hydrogen peroxide in hypertension induced by an antagonist of adenosine receptors. Eur J Pharmacol 588: 267–276, 2008.
33. Sun P, Yue P, Wang WH. Angiotensin II stimulates epithelial sodium channels in the cortical collecting duct of the rat kidney. Am J Physiol Renal Physiol 302: F679–F687, 2012.
34. 2 on saltinduced hypertension and renal injury. Am J Physiol Regul Integr Comp Physiol 289: R1573–R1579, 2005.
35. Thomas CP, Itani OA. New insights into epithelial sodium channel function in the kidney: site of action, regulation by ubiquitin ligases, serum- and glucocorticoid-inducible kinase and proteolysis. Curr Opin Nephrol Hypertens 13: 541–548, 2004.
36. Thomason J, Reyes M, Allen SR, Jones RO, Beeram MR, Kuehl TJ, Suzuki F, Uddin MN. Elevation of (pro)renin and (pro)renin receptor in preeclampsia. Am J Hypertens 28: 1277–1284, 2015.
37. Verrey F, Fakitsas P, Adam G, Staub O. Early transcriptional control of ENaC (de)ubiquitylation by aldosterone. Kidney Int 73: 691–696, 2008.
38. Wang F, Lu X, Peng K, Du Y, Zhou SF, Zhang A, Yang T. Prostaglandin E-prostanoid4 receptor mediates angiotensin II-induced (pro)renin receptor expression in the rat renal medulla. Hypertension 64: 369–377, 2014.
39. Wang F, Lu X, Peng K, Zhou L, Li C, Wang W, Yu X, Kohan DE, Zhou SF, Yang T. COX-2 mediates angiotensin II-induced (pro)renin receptor expression in the rat renal medulla. Am J Physiol Renal Physiol 307: F25–F32, 2014.
40. Yokota H, Nagaoka T, Tani T, Takahashi A, Sato E, Kato Y, Yoshida A. Higher levels of prorenin predict development of diabetic retinopathy in patients with type 2 diabetes. J Renin Angiotensin Aldosterone Syst 12: 290–294, 2011.
41. Zhang J, Chen S, Liu H, Zhang B, Zhao Y, Ma K, Zhao D, Wang Q, Ma H, Zhang Z. Hydrogen sulfide prevents hydrogen peroxide-induced activation of epithelial sodium channel through a PTEN/PI(3, 4,5)P3 dependent pathway. PLoS One 8: e64304, 2013.
42. Zhang J, Wu J, Gu C, Noble NA, Border WA, Huang Y. Receptormediated nonproteolytic activation of prorenin and induction of TGF-β1 and PAI-1 expression in renal mesangial cells. Am J Physiol Renal Physiol 303: F11–F20, 2012.