Renal collectrin protects against salt-sensitive hypertension and is downregulated by angiotensin II

Journal of the American Society of Nephrology

Volumn 28, Issue 6, 2017, Pages 1826-1837

  Chu, Pei Lun ^a   Gigliotti, Joseph C ^a,d   Cechova, Sylvia ^a   Bodonyi Kovacs, Gabor ^a   Chan, Fang ^a   Ralph, Donna Lee ^d   Howell, Nancy ^c   Kalantari, Kambiz ^a   Klibanov, Alexander L ^b   Carey, Robert M ^c   Mcdonough, Alicia A ^d   Le, Thu H ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c Liberty University College of Osteopathic Medicine   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR; COLLECTRIN; EPITHELIAL SODIUM CHANNEL; GLYCOPROTEIN; LITHIUM; MEMBRANE PROTEIN; MESSENGER RNA; NEURONAL NITRIC OXIDE SYNTHASE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM PROTON EXCHANGE PROTEIN 3; UNCLASSIFIED DRUG; SALT INTAKE; TMEM27 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MONITORING; BLOOD PRESSURE REGULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DIMERIZATION; DOWN REGULATION; EXPERIMENTAL HYPERTENSION; GENE EXPRESSION; HEART RATE; IN VIVO STUDY; KIDNEY BLOOD FLOW; KIDNEY PROXIMAL TUBULE; KIDNEY TISSUE; KIDNEY TRANSPLANTATION; KNOCKOUT MOUSE; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RENAL CLEARANCE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SALT INTAKE; SALT SENSITIVITY; SALT TOLERANCE; SODIUM TRANSPORT; SODIUM URINE LEVEL; SYSTOLIC BLOOD PRESSURE; WILD TYPE MOUSE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; HYPERTENSION; KIDNEY; MALE; METABOLISM; PHYSIOLOGY;

ANGIOTENSIN II; ANIMALS; DOWN-REGULATION; HYPERTENSION; KIDNEY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; SODIUM CHLORIDE, DIETARY;

EID: 85020193316     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2016060675     Document Type: Article

References (48)

1. Zhang H, Wada J, Hida K, Tsuchiyama Y, Hiragushi K, Shikata K, Wang H, Lin S, Kanwar YS, Makino H: Collectrin, a collecting duct-specific transmembrane glycoprotein, is a novel homolog of ACE2 and is developmentally regulated in embryonic kidneys. J Biol Chem 276: 17132-17139, 2001.
2. Akpinar P, Kuwajima S, Krützfeldt J, Stoffel M: Tmem27: A cleaved and shed plasma membrane protein that stimulates pancreatic beta cell proliferation. Cell Metab 2: 385-397, 2005.
3. Danilczyk U, Sarao R, Remy C, Benabbas C, Stange G, Richter A, Arya S, Pospisilik JA, Singer D, Camargo SM, Makrides V, Ramadan T, Verrey F, Wagner CA, Penninger JM: Essential role for collectrin in renal amino acid transport. Nature 444: 1088-1091, 2006.
4. Fukui K, Yang Q, Cao Y, Takahashi N, Hatakeyama H, Wang H, Wada J, Zhang Y, Marselli L, Nammo T, Yoneda K, Onishi M, Higashiyama S, Matsuzawa Y, Gonzalez FJ, Weir GC, Kasai H, Shimomura I, Miyagawa J, Wollheim CB, Yamagata K: The HNF-1 target collectrin controls insulin exocytosis by SNARE complex formation. Cell Metab 2: 373-384, 2005.
5. Gu X, Neric NJ, Crabb JS, Crabb JW, Bhattacharya SK, Rayborn ME, Hollyfield JG, Bonilha VL: Age-related changes in the retinal pigment epithelium (RPE). PLoS One 7: E38673, 2012.
6. Malakauskas SM, Kourany WM, Zhang XY, Lu D, Stevens RD, Koves TR, Hohmeier HE, Muoio DM, Newgard CB, Le TH: Increased insulin sensitivity in mice lacking collectrin, a downstream target of HNF-1alpha. Mol Endocrinol 23: 881-892, 2009.
7. Malakauskas SM, Quan H, Fields TA, McCall SJ, Yu MJ, Kourany WM, Frey CW, Le TH: Aminoaciduria and altered renal expression of luminal amino acid transporters in mice lacking novel gene collectrin. Am J Physiol Renal Physiol 292: F533-F544, 2007.
8. Cechova S, Zeng Q, Billaud M, Mutchler S, Rudy CK, Straub AC, Chi L, Chan FR, Hu J, Griffiths R, Howell NL, Madsen K, Jensen BL, Palmer LA, Carey RM, Sung SS, Malakauskas SM, Isakson BE, Le TH: Loss of collectrin, an angiotensin-converting enzyme 2 homolog, uncouples endothelial nitric oxide synthase and causes hypertension and vascular dysfunction. Circulation 128: 1770-1780, 2013.
9. Fairweather SJ, Bröer A, Subramanian N, Tumer E, Cheng Q, Schmoll D, O'Mara ML, Bröer S: Molecular basis for the interaction of the mammalian amino acid transporters B0AT1 and B0AT3 with their ancillary protein collectrin. J Biol Chem 290: 24308-24325, 2015.
10. Zhang H, Wada J, Kanwar YS, Tsuchiyama Y, Hiragushi K, Hida K, Shikata K, Makino H: Screening for genes up-regulated in 5/6 nephrectomized mouse kidney. Kidney Int 56: 549-558, 1999.
11. Yasuhara A, Wada J, Malakauskas SM, Zhang Y, Eguchi J, Nakatsuka A, Murakami K, Kanzaki M, Teshigawara S, Yamagata K, Le TH, Makino H: Collectrin is involved in the development of salt-sensitive hypertension by facilitating the membrane trafficking of apical membrane proteins via interaction with soluble N-ethylmaleiamide-sensitive factor attachment protein receptor complex. Circulation 118: 2146-2155, 2008.
12. Hecker M, Sessa WC, Harris HJ, Anggård EE, Vane JR: The metabolism of L-Arginine and its significance for the biosynthesis of endotheliumderived relaxing factor: Cultured endothelial cells recycle L-citrulline to L-Arginine. Proc Natl Acad Sci U S A 87: 8612-8616, 1990.
13. Pallone TL, Mattson DL: Role of nitric oxide in regulation of the renal medulla in normal and hypertensive kidneys. Curr Opin Nephrol Hypertens 11: 93-98, 2002.
14. Roczniak A, Zimpelmann J, Burns KD: Effect of dietary salt on neuronal nitric oxide synthase in the inner medullary collecting duct. Am J Physiol 275: F46-F54, 1998.
15. Kogan P, Johnson KA, Feingold S, Garrett N, Guracar I, Arendshorst WJ, Dayton PA: Validation of dynamic contrast-enhanced ultrasound in rodent kidneys as an absolute quantitative method for measuring blood perfusion. Ultrasound Med Biol 37: 900-908, 2011.
16. Dukacz SA, Adams MA, Kline RL: Short-And long-Term enalapril affect renal medullary hemodynamics in the spontaneously hypertensive rat. Am J Physiol 276: R10-R16, 1999.
17. Dixit MP, Xu L, Xu H, Bai L, Collins JF, Ghishan FK: Effect of angiotensin- II on renal Na+/H+ exchanger-NHE3 and NHE2. BiochimBiophys Acta 1664: 38-44, 2004.
18. He P, Klein J, Yun CC: Activation of Na+/H+ exchanger NHE3 by angiotensin II is mediated by inositol 1, 4, 5-Triphosphate (IP3) receptor- binding protein released with IP3 (IRBIT) and Ca2+/calmodulindependent protein kinase II. J Biol Chem 285: 27869-27878, 2010.
19. Kamat NV, Thabet SR, Xiao L, Saleh MA, Kirabo A, Madhur MS, Delpire E, Harrison DG, McDonough AA: Renal transporter activation during angiotensin-II hypertension is blunted in interferon-g-/-And interleukin- 17A-/- mice. Hypertension 65: 569-576, 2015.
20. Weinberger MH, Fineberg NS, Fineberg SE, Weinberger M: Salt sensitivity, pulse pressure, and death in normal and hypertensive humans. Hypertension 37: 429-432, 2001.
21. Dahl LK, Heine M: Primary role of renal homografts in setting chronic blood pressure levels in rats. Circ Res 36: 692-696, 1975.
22. Ni Z, Oveisi F, Vaziri ND: Nitric oxide synthase isotype expression in saltsensitive and salt-resistant Dahl rats. Hypertension 34: 552-557, 1999.
23. Francois H, Athirakul K, Howell D, Dash R, Mao L, Kim HS, Rockman HA, Fitzgerald GA, Koller BH, Coffman TM: Prostacyclin protects against elevated blood pressure and cardiac fibrosis. Cell Metab 2: 201-207, 2005.
24. Ryan MJ, Didion SP, Davis DR, Faraci FM, Sigmund CD: Endothelial dysfunction and blood pressure variability in selected inbred mouse strains. Arterioscler Thromb Vasc Biol 22: 42-48, 2002.
25. Wang Q, Hummler E, Nussberger J, Clément S, Gabbiani G, Brunner HR, Burnier M: Blood pressure, cardiac, and renal responses to salt and deoxycorticosterone acetate in mice: Role of Renin genes. J Am Soc Nephrol 13: 1509-1516, 2002.
26. Campese VM, Parise M, Karubian F, Bigazzi R: Abnormal renal hemodynamics in black salt-sensitive patients with hypertension. Hypertension 18: 805-812, 1991.
27. Chiolero A, Würzner G, Burnier M: Renal determinants of the salt sensitivity of blood pressure. Nephrol Dial Transplant 16: 452-458, 2001.
28. van Paassen P, de Zeeuw D, Navis G, de Jong PE: Does the reninangiotensin system determine the renal and systemic hemodynamic response to sodium in patients with essential hypertension? Hypertension 27: 202-208, 1996.
29. Williams GH, Hollenberg NK: Non-modulating hypertension. A subset of sodium-sensitive hypertension. Hypertension 17[Suppl]: I81-I85, 1991.
30. Closs EI, Scheld JS, Sharafi M, Förstermann U: Substrate supply for nitric-oxide synthase in macrophages and endothelial cells: Role of cationic amino acid transporters. Mol Pharmacol 57: 68-74, 2000.
31. Simon A, Plies L, Habermeier A, Martiné U, Reining M, Closs EI: Role of neutral amino acid transport and protein breakdown for substrate supply of nitric oxide synthase in human endothelial cells. Circ Res 93: 813-820, 2003.
32. Arendshorst WJ, Navar LG: Renal Circulation and Glomerular Hemodynamics, Philadelphia, PA, Lipincott Williams and Wilkins, 2007.
33. Navar LG, Inscho EW, Majid SA, Imig JD, Harrison-Bernard LM, Mitchell KD: Paracrine regulation of the renal microcirculation. Physiol Rev 76: 425-536, 1996.
34. Just A, Olson AJ, Whitten CL, Arendshorst WJ: Superoxide mediates acute renal vasoconstriction produced by angiotensin II and catecholamines by amechanismindependent of nitric oxide.Am J Physiol Heart Circ Physiol 292: H83-H92, 2007.
35. Mattson DL, Meister CJ: Renal cortical and medullary blood flow responses to L-NAME and ANG II in wild-Type, nNOS null mutant, and eNOS null mutant mice. Am J Physiol Regul Integr Comp Physiol 289: R991-R997, 2005.
36. Berthold H, Just A, Kirchheim HR, Ehmke H: Interaction between nitric oxide and endogenous vasoconstrictors in control of renal blood flow. Hypertension 34: 1254-1258, 1999.
37. Roman RJ, Zou AP: Influence of the renal medullary circulation on the control of sodium excretion. Am J Physiol 265: R963-R973, 1993.
38. Kakoki M, Kim HS, Arendshorst WJ, Mattson DL: L-Arginine uptake affects nitric oxide production and blood flow in the renal medulla. Am J Physiol Regul Integr Comp Physiol 287: R1478-R1485, 2004.
39. Kakoki M, Wang W, Mattson DL: Cationic amino acid transport in the renal medulla and blood pressure regulation. Hypertension 39: 287- 292, 2002.
40. Balligand JL, Feron O, Dessy C: ENOS activation by physical forces: From short-Term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89: 481-534, 2009.
41. Nguyen MT, Han J, Ralph DL, Veiras LC, McDonough AA: Short-Term nonpressor angiotensin II infusion stimulates sodium transporters in proximal tubule and distal nephron. Physiol Rep 3: E12496 2015.
42. McDonough AA, Nguyen MT: Maintaining balance under pressure: Integrated regulation of renal transporters during hypertension. Hypertension 66: 450-455, 2015.
43. Nguyen MT, Lee DH, Delpire E, McDonough AA: Differential regulation of Na+ transporters along nephron during ANG II-dependent hypertension: Distal stimulation counteracted by proximal inhibition. Am J Physiol Renal Physiol 305: F510-F519, 2013.
44. Gurley SB, Riquier-Brison AD, Schnermann J, Sparks MA, Allen AM, Haase VH, Snouwaert JN, Le TH, McDonough AA, Koller BH, Coffman TM: AT1A angiotensin receptors in the renal proximal tubule regulate blood pressure. Cell Metab 13: 469-475, 2011.
45. Crowley SD, Gurley SB, Oliverio MI, Pazmino AK, Griffiths R, Flannery PJ, Spurney RF, Kim HS, Smithies O, Le TH, Coffman TM: Distinct roles for the kidney and systemic tissues in blood pressure regulation by the renin-Angiotensin system. J Clin Invest 115: 1092-1099, 2005.
46. Sorensen MV, Grossmann S, Roesinger M, Gresko N, Todkar AP, Barmettler G, Ziegler U, Odermatt A, Loffing-Cueni D, Loffing J: Rapid dephosphorylation of the renal sodium chloride cotransporter in response to oral potassium intake in mice. Kidney Int 83: 811-824, 2013.
47. McDonough AA, Veiras LC, Minas JN, Ralph DL: Considerations when quantitating protein abundance by immunoblot. Am J Physiol Cell Physiol 308: C426-C433, 2015.
48. Salzler HR, Griffiths R, Ruiz P, Chi L, Frey C, Marchuk DA, Rockman HA, Le TH: Hypertension and albuminuria in chronic kidney disease mapped to a mouse chromosome 11 locus. Kidney Int 72: 1226-1232, 2007.