The Cap1-claudin-4 regulatory pathway is important for renal chloride reabsorption and blood pressure regulation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 36, 2014, Pages E3766-E3774

  Gong, Yongfeng ^a,b   Yu, Miao ^c   Yang, Jing ^a   Gonzales, Ernie ^a   Perez, Ronaldo ^a   Hou, Mingli ^d   Tripathi, Piyush ^a   Hering Smith, Kathleen S ^c   Hamm, L Lee ^c   Hou, Jianghui ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BINZHOU MEDICAL UNIVERSITY   (China)

^c TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Chloride channel; Epithelium; Hypertension

Indexed keywords

CHLORIDE; CLAUDIN 4; ELECTROLYTE; PROSTASIN; PROTEIN BINDING; RECOMBINANT PROTEIN; SERINE PROTEINASE; TRYPSIN;

ANIMAL; ANTIBODY SPECIFICITY; BLOOD; BLOOD PRESSURE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; HEK293 CELL LINE; HUMAN; KIDNEY; KIDNEY COLLECTING TUBULE; KIDNEY TUBULE ABSORPTION; KNOCKOUT MOUSE; METABOLISM; PROTEIN TRANSPORT; RNA INTERFERENCE; TELEMETRY; URINE;

ANIMALS; BLOOD PRESSURE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHLORIDES; CLAUDIN-4; ELECTROLYTES; HEK293 CELLS; HUMANS; KIDNEY; KIDNEY TUBULES, COLLECTING; MICE, KNOCKOUT; ORGAN SPECIFICITY; PROTEIN BINDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; RENAL REABSORPTION; RNA INTERFERENCE; SERINE ENDOPEPTIDASES; TELEMETRY; TRYPSIN;

EID: 84907000462     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406741111     Document Type: Article

References (51)

1. Kurtz TW, Morris RC, Jr (1983) Dietary chloride as a determinant of "sodium-dependent" hypertension. Science 222(4628):1139- 1141.
2. Whitescarver SA, Ott CE, Jackson BA, Guthrie GP, Jr, Kotchen TA (1984) Salt-sensitive hypertension: Contribution of chloride. Science 223(4643):1430-1432.
3. Guyton AC (1991) Blood pressure control-Special role of the kidneys and body fluids. Science 252(5014):1813-1816.
4. Lifton RP, Gharavi AG, Geller DS (2001) Molecular mechanisms of human hypertension. Cell 104(4):545-556.
5. Reilly RF, Ellison DH (2000) Mammalian distal tubule: Physiology, pathophysiology, and molecular anatomy. Physiol Rev 80(1):277-313.
6. Royaux IE, et al. (2001) Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci USA 98(7):4221-4226.
7. Leviel F, et al. (2010) The Na+-dependent chloride-bicarbonate exchanger SLC4A8 mediates an electroneutral Na+ reabsorption process in the renal cortical collecting ducts of mice. J Clin Invest 120(5):1627-1635.
8. Canessa CM, et al. (1994) Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367(6462):463-467.
9. Kim YH, et al. (2007) Reduced ENaC protein abundance contributes to the lower blood pressure observed in pendrin-null mice. Am J Physiol Renal Physiol 293(4):F1314-F1324.
10. Pech V, et al. (2010) Pendrin modulates ENaC function by changing luminal HCO3-. J Am Soc Nephrol 21(11):1928-1941.
11. Hou J, Renigunta A, Yang J, Waldegger S (2010) Claudin-4 forms paracellular chloride channel in the kidney and requires claudin-8 for tight junction localization. Proc Natl Acad Sci USA 107(42):18010-18015.
12. Sansom SC, Weinman EJ, O'Neil RG (1984) Microelectrode assessment of chloride-conductive properties of cortical collecting duct. Am J Physiol 247(2 Pt 2):F291-F302.
13. Hou J, Rajagopal M, Yu AS (2013) Claudins and the kidney. Annu Rev Physiol 75:479-501.
14. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC (1997) An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389(6651):607-610.
15. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC (2002) Synergistic activation of ENaC by three membrane-bound channel-activating serine proteases (mCAP1, mCAP2, and mCAP3) and serum- and glucocorticoid-regulated kinase (Sgk1) in Xenopus oocytes. J Gen Physiol 120(2):191-201.
16. Narikiyo T, et al. (2002) Regulation of prostasin by aldosterone in the kidney. J Clin Invest 109(3):401-408.
17. Furuse M, et al. (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J Cell Biol 156(6):1099-1111.
18. Katahira J, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N (1997) Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J Cell Biol 136(6):1239-1247.
19. Mitchell LA, Overgaard CE, Ward C, Margulies SS, Koval M (2011) Differential effects of claudin-3 and claudin-4 on alveolar epithelial barrier function. Am J Physiol Lung Cell Mol Physiol 301(1):L40-L49.
20. Fujita H, Hamazaki Y, Noda Y, Oshima M, Minato N (2012) Claudin-4 deficiency results in urothelial hyperplasia and lethal hydronephrosis. PLoS ONE 7(12):e52272.
21. Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW (1993) Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90(24):11663-11667.
22. Christensen BM, et al. (2010) Sodium and potassium balance depends on αENaC expression in connecting tubule. J Am Soc Nephrol 21(11):1942-1951.
23. Ronzaud C, et al. (2007) Impairment of sodium balance in mice deficient in renal principal cell mineralocorticoid receptor. J Am Soc Nephrol 18(6):1679-1687.
24. Hansen PB, et al. (2004) Plasma renin in mice with one or two renin genes. Acta Physiol Scand 181(4):431-437.
25. Liu L, Hering-Smith KS, Schiro FR, Hamm LL (2002) Serine protease activity in m-1 cortical collecting duct cells. Hypertension 39(4):860-864.
26. Vuagniaux G, et al. (2000) Activation of the amiloride-sensitive epithelial sodium channel by the serine protease mCAP1 expressed in a mouse cortical collecting duct cell line. J Am Soc Nephrol 11(5):828-834.
27. Hou J, Paul DL, Goodenough DA (2005) Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 118(Pt 21):5109-5118.
28. Chen M, Chen LM, Lin CY, Chai KX (2010) Hepsin activates prostasin and cleaves the extracellular domain of the epidermal growth factor receptor. Mol Cell Biochem 337(1-2):259-266.
29. Verghese GM, Gutknecht MF, Caughey GH (2006) Prostasin regulates epithelial monolayer function: Cell-specific Gpld1-mediated secretion and functional role for GPI anchor. Am J Physiol Cell Physiol 291(6):C1258-C1270.
30. Déry O, Corvera CU, Steinhoff M, Bunnett NW (1998) Proteinase-activated receptors: Novel mechanisms of signaling by serine proteases. Am J Physiol 274(6 Pt 1):C1429-C1452.
31. Hou J, et al. (2008) Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest 118(2):619-628.
32. Hou J, et al. (2009) Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci USA 106(36):15350-15355.
33. Furuse M, Sasaki H, Tsukita S (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cell Biol 147(4):891-903.
34. Daugherty BL, Ward C, Smith T, Ritzenthaler JD, Koval M (2007) Regulation of heterotypic claudin compatibility. J Biol Chem 282(41):30005-30013.
35. Piontek J, et al. (2008) Formation of tight junction: Determinants of homophilic interaction between classic claudins. FASEB J 22(1):146-158.
36. Kausalya PJ, et al. (2006) Disease-associated mutations affect intracellular traffic and paracellular Mg2+ transport function of Claudin-16. J Clin Invest 116(4):878-891.
37. Shipway A, et al. (2004) Biochemical characterization of prostasin, a channel activating protease. Biochem Biophys Res Commun 324(2):953-963.
38. Naguro I, et al. (2012) ASK3 responds to osmotic stress and regulates blood pressure by suppressing WNK1-SPAK/OSR1 signaling in the kidney. Nat Commun 3:1285.
39. Hadchouel J, et al. (2010) Decreased ENaC expression compensates the increased NCC activity following inactivation of the kidney-specific isoform of WNK1 and prevents hypertension. Proc Natl Acad Sci USA 107(42):18109-18114.
40. Doi M, et al. (2010) Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nat Med 16(1):67-74.
41. Garella S, Cohen JJ, Northrup TE (1991) Chloride-depletion metabolic alkalosis induces ECF volume depletion via internal fluid shifts in nephrectomized dogs. Eur J Clin Invest 21(3):273 - 279.
42. Galla JH (2000) Metabolic alkalosis. J Am Soc Nephrol 11(2):369-375.
43. Ring AM, et al. (2007) WNK4 regulates activity of the epithelial Na+ channel in vitro and in vivo. Proc Natl Acad Sci USA 104(10):4020-4024.
44. Kahle KT, et al. (2004) Paracellular Cl- permeability is regulated by WNK4 kinase: Insight into normal physiology and hypertension. Proc Natl Acad Sci USA 101(41):14877-14882.
45. Le Moellic C, et al. (2005) Aldosterone and tight junctions: Modulation of claudin-4 phosphorylation in renal collecting duct cells. Am J Physiol Cell Physiol 289(6):C1513-C1521.
46. Swystun VA, et al. (2009) Serine proteases decrease intestinal epithelial ion permeability by activation of protein kinase Czeta. Am J Physiol Gastrointest Liver Physiol 297(1):G60-G70.
47. Buzza MS, et al. (2013) Prostasin is required for matriptase activation in intestinal epithelial cells to regulate closure of the paracellular pathway. J Biol Chem 288(15):10328-10337.
48. Buzza MS, et al. (2010) Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc Natl Acad Sci USA 107(9):4200-4205.
49. Leyvraz C, et al. (2005) The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 170(3):487-496.
50. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: A dynamic duo. Annu Rev Physiol 73:283-309.
51. Veshnyakova A, et al. (2012) Mechanism of Clostridium perfringens enterotoxin interaction with claudin-3/-4 protein suggests structural modifications of the toxin to target specific claudins. J Biol Chem 287(3):1698-1708.