ERp29 regulates epithelial sodium channel functional expression by promoting channel cleavage

American Journal of Physiology - Cell Physiology

Volumn 307, Issue 8, 2014, Pages C701-C709

  Grumbach, Yael ^a   Bikard, Yann ^a   Suaud, Laurence ^a   Chanoux, Rebecca A ^a   Rubenstein, Ronald C ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biogenesis; Chaperone; Endoplasmic reticulum; Epithelium; Trafficking

Indexed keywords

CELL PROTEIN; CYSTEINE; EPITHELIAL SODIUM CHANNEL; ERP29 PROTEIN; SMALL INTERFERING RNA; TRYPSIN; UNCLASSIFIED DRUG; ERP29 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; SEC24D PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL LYSATE; CELL SURFACE; CONTROLLED STUDY; EPITHELIUM CELL; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SHORT CIRCUIT CURRENT; ANIMAL; CELL MEMBRANE; DOG; GENE EXPRESSION; HUMAN; MDCK CELL LINE; MEMBRANE POTENTIAL; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; XENOPUS LAEVIS;

ANIMALS; CELL MEMBRANE; DOGS; EPITHELIAL SODIUM CHANNELS; GENE EXPRESSION; HEAT-SHOCK PROTEINS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE POTENTIALS; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; VESICULAR TRANSPORT PROTEINS; XENOPUS LAEVIS;

EID: 84908051692     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00134.2014     Document Type: Article

References (39)

1. Adebamiro A, Cheng Y, Johnson JP, Bridges RJ. Endogenous protease activation of ENaC: effect of serine protease inhibition on ENaC single channel properties. J Gen Physiol 126: 339-352, 2005.
2. Barak NN, Neumann P, Sevvana M, Schutkowski M, Naumann K, Malesevic M, Reichardt H, Fischer G, Stubbs MT, Ferrari DM. Crystal structure and functional analysis of the protein disulfide isomeraserelated protein ERp29. J Mol Biol 385: 1630-1642, 2009.
3. + channels are fully activated by furin-and prostasin-dependent release of an inhibitory peptide from the γ-subunit. J Biol Chem 282: 6153-6160, 2007.
4. + transport. Am J Physiol Lung Cell Mol Physiol 288: L813-L819, 2005.
5. + channels. Am J Physiol Cell Physiol 286: C190-C194, 2004.
6. Canessa CM, Merillat AM, Rossier BC. Membrane topology of the epithelial sodium channel in intact cells. Am J Physiol Cell Physiol 267: C1682-C1690, 1994.
7. + channel is made of three homologous subunits. Nature 367: 463-467, 1994.
8. Chanoux RA, Robay A, Shubin CB, Kebler C, Suaud L, Rubenstein RC. Hsp70 promotes epithelial sodium channel functional expression by increasing its association with coat complex II and its exit from endoplasmic reticulum. J Biol Chem 287: 19255-19265, 2012.
9. Chanoux RA, Shubin CB, Robay A, Suaud L, Rubenstein RC. Hsc70 negatively regulates epithelial sodium channel trafficking at multiple sites in epithelial cells. Am J Physiol Cell Physiol 305: C776-C787, 2013.
10. Das S, Smith TD, Sarma JD, Ritzenthaler JD, Maza J, Kaplan BE, Cunningham LA, Suaud L, Hubbard MJ, Rubenstein RC, Koval M. ERp29 restricts connexin43 oligomerization in the endoplasmic reticulum. Mol Biol Cell 20: 2593-2604, 2009.
11. Hansson JH, Nelson-Williams C, Suzuki H, Schild L, Shimkets R, Lu Y, Canessa C, Iwasaki T, Rossier B, Lifton RP. Hypertension caused by a truncated epithelial sodium channel γ-subunit: genetic heterogeneity of Liddle syndrome. Nat Genet 11: 76-82, 1995.
12. Hansson JH, Schild L, Lu Y, Wilson TA, Gautschi I, Shimkets R, Nelson-Williams C, Rossier BC, Lifton RP. A de novo missense mutation of the β-subunit of the epithelial sodium channel causes hypertension and Liddle syndrome, identifying a proline-rich segment critical for regulation of channel activity. Proc Natl Acad Sci USA 92: 11495-11499, 1995.
13. + channel expressed in epithelial Madin-Darby canine kidney cells. J Biol Chem 277: 9772-9779, 2002.
14. Helms MN, Trac P. ERp29, a chaperone protein ushering in new insights on ion transport regulation. Focus on "ERp29 regulates epithelial sodium channel functional expression by promoting channel cleavage." Am J Physiol Cell Physiol (July 9, 2014). doi:10.1152/ajpcell.00217.2014.
15. Holbrook LM, Watkins NA, Simmonds AD, Jones CI, Ouwehand WH, Gibbins JM. Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. Br J Haematol 148: 627-637, 2010.
16. Hubbard MJ, Mangum JE, McHugh NJ. Purification and biochemical characterization of native ERp29 from rat liver. Biochem J 383: 589-597, 2004.
17. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong Q, Carattino MD, Johnson JP, Stockand JD, Kleyman TR. Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279: 18111-18114, 2004.
18. Hughey RP, Bruns JB, Kinlough CL, Kleyman TR. Distinct pools of epithelial sodium channels are expressed at the plasma membrane. J Biol Chem 279: 48491-48494, 2004.
19. Hummler E, Barker P, Talbot C, Wang Q, Verdumo C, Grubb B, Gatzy J, Burnier M, Horisberger JD, Beermann F, Boucher R, Rossier BC. A mouse model for the renal salt-wasting syndrome pseudohypoaldosteronism. Proc Natl Acad Sci USA 94: 11710-11715, 1997.
20. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449: 316-323, 2007.
21. Jiang Q, Li J, Dubroff R, Ahn YJ, Foskett JK, Engelhardt J, Kleyman TR. Epithelial sodium channels regulate cystic fibrosis transmembrane conductance regulator chloride channels in Xenopus oocytes. J Biol Chem 275: 13266-13274, 2000.
22. + absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10: 487-493, 2004.
23. Pruliere-Escabasse V, Planes C, Escudier E, Fanen P, Coste A, Clerici C. Modulation of epithelial sodium channel trafficking and function by sodium 4-phenylbutyrate in human nasal epithelial cells. J Biol Chem 282: 34048-34057, 2007.
24. Rainey-Barger EK, Mkrtchian S, Tsai B. Dimerization of ERp29, a PDI-like protein, is essential for its diverse functions. Mol Biol Cell 18: 1253-1260, 2007.
25. Rubenstein RC, Egan ME, Zeitlin PL. In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing ΔF508-CFTR. J Clin Invest 100: 2457-2465, 1997.
26. Rubenstein RC, Lockwood SR, Lide E, Bauer R, Suaud L, Grumbach Y. Regulation of endogenous ENaC functional expression by CFTR and ΔF508-CFTR in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 300: L88-L101, 2011.
27. Samaha FF, Rubenstein RC, Yan W, Ramkumar M, Levy DI, Ahn YJ, Sheng S, Kleyman TR. Functional polymorphism in the carboxyl terminus of the α-subunit of the human epithelial sodium channel. J Biol Chem 279: 23900-23907, 2004.
28. Sargsyan E, Baryshev M, Szekely L, Sharipo A, Mkrtchian S. Identification of ERp29, an endoplasmic reticulum lumenal protein, as a new member of the thyroglobulin folding complex. J Biol Chem 277: 17009-17015, 2002.
29. Schild L, Lu Y, Gautschi I, Schneeberger E, Lifton RP, Rossier BC. Identification of a PY motif in the epithelial Na channel subunits as a target sequence for mutations causing channel activation found in Liddle syndrome. EMBO J 15: 2381-2387, 1996.
30. Sen J, Goltz JS, Konsolaki M, Schupbach T, Stein D. Windbeutel is required for function and correct subcellular localization of the Drosophila patterning protein Pipe. Development 127: 5541-5550, 2000.
31. Shnyder SD, Hubbard MJ. ERp29 is a ubiquitous resident of the endoplasmic reticulum with a distinct role in secretory protein production. J Histochem Cytochem 50: 557-566, 2002.
32. Stewart AP, Haerteis S, Diakov A, Korbmacher C, Edwardson JM. Atomic force microscopy reveals the architecture of the epithelial sodium channel (ENaC). J Biol Chem 286: 31944-31952, 2011.
33. Suaud L, Carattino M, Kleyman TR, Rubenstein RC. Genistein improves regulatory interactions between G551D-cystic fibrosis transmembrane conductance regulator and the epithelial sodium channel in Xenopus oocytes. J Biol Chem 277: 50341-50347, 2002.
34. Suaud L, Li J, Jiang Q, Rubenstein RC, Kleyman TR. Genistein restores functional interactions between ΔF508-CFTR and ENaC in Xenopus oocytes. J Biol Chem 277: 8928-8933, 2002.
35. Suaud L, Miller K, Alvey L, Yan W, Robay A, Kebler C, Kreindler JL, Guttentag S, Hubbard MJ, Rubenstein RC. ERp29 regulates ΔF508 and wild-type cystic fibrosis transmembrane conductance regulator (CFTR) trafficking to the plasma membrane in cystic fibrosis (CF) and non-CF epithelial cells. J Biol Chem 286: 21239-21253, 2011.
36. Valentijn JA, Fyfe GK, Canessa CM. Biosynthesis and processing of epithelial sodium channels in Xenopus oocytes. J Biol Chem 273: 30344-30351, 1998.
37. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC. An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389: 607-610, 1997.
38. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC. 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: 191-201, 2002.
39. Yan W, Samaha FF, Ramkumar M, Kleyman TR, Rubenstein RC. Cystic fibrosis transmembrane conductance regulator differentially regulates human and mouse epithelial sodium channels in Xenopus oocytes. J Biol Chem 279: 23183-23192, 2004.