Kv7.1 surface expression is regulated by epithelial cell polarization

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 4, 2011, Pages

  Andersen, Martin N ^a   Olesen, Søren Peter ^a   Rasmussen, Hanne B ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Basolateral targeting; Calcium switch; Madin darby canine kidney cell; Trafficking

Indexed keywords

CALCIUM; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV7.1; POTASSIUM CHANNEL KCNQ1;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CELL POLARITY; CELL SURFACE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EPITHELIUM CELL; GENE; GENE MUTATION; HEARING IMPAIRMENT; HEART REPOLARIZATION; KCNQ1 GENE; LONG QT SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WATER TRANSPORT; ANIMAL; CELL JUNCTION; CELL LINE; CYTOLOGY; DESMOSOME; DOG; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TIGHT JUNCTION;

ADHERENS JUNCTIONS; ANIMALS; CALCIUM; CELL LINE; CELL MEMBRANE; CELL POLARITY; DESMOSOMES; DOGS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EPITHELIAL CELLS; HUMANS; KCNQ1 POTASSIUM CHANNEL; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE C; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

EID: 79955129911     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00390.2010     Document Type: Article

References (51)

1. Amar LS, Shabana AHM, Oboeuf M, Martin N, Forest N. Desmosomes are regulated by protein kinase C in primary rat epithelial cells. Cell Commun Adhes 5: 1-12, 1998.
2. Arthur WT, Noren NK, Burridge K. Regulation of Rho family GTPases by cell-cell and cell-matrix adhesion. Biol Res 35: 239-246, 2002.
3. Barhanin J, Lesage F, Guillemare E, Fink M, Lazdunski M, Romey G. KvLQT1 and IsK (minK) proteins associate to form the IKs cardiac potassium current. Nature 384: 78-80, 1996.
4. Bennett V, Healy J. Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol Med 14: 28-36, 2008.
5. Boucherot A, Schreiber R, Kunzelmann K. Regulation and properties of KCNQ1 (K V LQT1) and impact of the cystic fibrosis transmembrane conductance regulator. J Membr Biol 182: 39-47, 2001.
6. Cannon JL, Burkhardt JK. The regulation of actin remodeling during T-cellûAPC conjugate formation. Immunol Rev 186: 90-99, 2002.
7. Dahimene S, Alcolea S, Naud P, Jourdon P, Escande D, Brasseur R, Thomas A, Baro I, Merot J. The N-terminal juxtamembranous domain of KCNQ1 is critical for channel surface expression. Implications in the Romano-Ward LQT1 syndrome. Circ Res 99: 1076-1083, 2006.
8. Dedek K, Waldegger S. Colocalization of KCNQ1/KCNE channel subunits in the mouse gastrointestinal tract. Pflügers Arch 442: 896-902, 2001.
9. Denisenko N, Burighel P, Citi S. Different effects of protein kinase inhibitors on the localization of junctional proteins at cell-cell contact sites. J Cell Sci 107: 969-981, 1994.
10. Garrard SM, Capaldo CT, Gao L, Rosen MK, Macara IG, Tomchick DR. Structure of Cdc42 in a complex with the GTPase-binding domain of the cell polarity protein, Par6. EMBO J 22: 1125-1133, 2003.
11. Gassama-Diagne A, Yu W, Ter Beest M, Martin-Belmonte F, Kierbel A, Engel J, Mostov K. Phosphatidylinositol-3, 4, 5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nature Cell Biol 8: 963-970, 2006.
12. Gonzalez-Mariscal L, Chavez de Ramirez B, Cereijido M. Tight junction formation in cultured epithelial cells (MDCK). J Membr Biol 86: 113-125, 1985.
13. Gouas L, Bellocq C, Berthet M, Potet F, Demolombe S, Forhan A, Lescasse R, Simon F, Balkau B, Denjoy I. New KCNQ1 mutations leading to haploinsufficiency in a general population: defective trafficking of a KvLQT1 mutant. Cardiovasc Res 63: 60-68, 2004.
14. Grunnet M, Jespersen T, Rasmussen HB, Ljungstrøm T, Jorgensen NK, Olesen SP, Klaerke DA. KCNE4 is an inhibitory subunit to the KCNQ1 channel. J Physiol 542: 119-130, 2002.
15. Gumbiner B, Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulinlike polypeptide. J Cell Biol 102: 457-468, 1986.
16. Gumbiner B, Stevenson B, Grimaldi A. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol 107: 1575-1587, 1988.
17. Gusarova GA, Dada LA, Kelly AM, Brodie C, Witters LA, Chandel NS, Sznajder JI. 1-AMP-activated protein kinase regulates hypoxiainduced Na, K-ATPase endocytosis via direct phosphorylation of protein kinase Cζ. Mol Cell Biol 29: 3455-3464, 2009.
18. Hu K, Huang CS, Jan YN, Jan LY. ATP-sensitive potassium channel traffic regulation by adenosine and protein kinase C. Neuron 38: 417-432, 2003.
19. Jespersen T, Rasmussen HB, Grunnet M, Jensen HS, Angelo K, Dupuis DS, Vogel LK, Jorgensen NK, Klaerke DA, Olesen SP. Basolateral localisation of KCNQ1 potassium channels in MDCK cells: molecular identification of an N-terminal targeting motif. J Cell Sci 117: 4517-4526, 2004.
20. Kizhatil K, Bennett V. Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J Biol Chem 279: 16706-16714, 2004.
21. Kizhatil K, Davis JQ, Davis L, Hoffman J, Hogan BLM, Bennett V. Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J Biol Chem 282: 26552-26561, 2007.
22. Kizhatil K, Yoon W, Mohler PJ, Davis LH, Hoffman JA, Bennett V. Ankyrin-G and 2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J Biol Chem 282: 2029-2037, 2007.
23. Laprise P, Chailler P, Houde M, Beaulieu JF, Boucher MJ, Rivard N. Phosphatidylinositol 3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J Biol Chem 277: 8226-8324, 2002.
24. Laprise P, Langlois MJ, Boucher MJ, Jobin C, Rivard N. Downregulation of MEK/ERK signaling by E-cadherin-dependent PI3K/Akt pathway in differentiating intestinal epithelial cells. J Cell Physiol 199: 32-39, 2003.
25. Lhuillier L, Dryer SE. Developmental regulation of neuronal KCa Channels by TGFbeta 1: an essential role for PI3 kinase signaling and membrane insertion. J Neurophysiol 88: 954-964, 2002.
26. Nejsum LN, Nelson WJ. A molecular mechanism directly linking Ecadherin adhesion to initiation of epithelial cell surface polarity. J Cell Biol 178: 323-335, 2007.
27. Neyroud N, Tesson F, Denjoy I, Leibovici M, Donger C, Barhanin J, Faurq S, Gary F, Coumel P, Petit C. A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange-Nielsen cardioauditory syndrome. Nat Genetics 15: 186-189, 1997.
28. Nigam SK, Rodriguez-Boulan E, Silver RB. Changes in intracellular calcium during the development of epithelial polarity and junctions. Proc Natl Acad Sci USA 89: 162-166, 1992.
29. O'Mahony F, Alzamora R, Betts V, LaPaix F, Carter D, Irnaten M, Harvey BJ. Female gender-specific inhibition of KCNQ1 channels and chloride secretion by 17-estradiol in rat distal colonic crypts. J Biol Chem 282: 24563-24573, 2007.
30. Ozaki M, Ogita H, Takai Y. Involvement of integrin-induced activation of protein kinase C in the formation of adherens junctions. Genes Cells 12: 651-662, 2007.
31. Pasdar M, Li Z, Chan H. Desmosome assembly and disassembly are regulated by reversible protein phosphorylation in cultured epithelial cells. Cell Mot Cytoskel 30: 108-121, 1995.
32. Pasdar M, Nelson WJ. Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell-cell contact. I Biochemical analysis. J Cell Biol 106: 677-685, 1988.
33. Pece S, Chiariello M, Murga C, Gutkind JS. Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. J Biol Chem 274: 19347-19351, 1999.
34. Sanguinetti MC, Curran ME, Zou A, Shen J, Specter PS, Atkinson DL, Keating MT. Coassembly of KvLQT1 and minK (IsK) proteins to form cardiac IKs potassium channel. Nature 384: 80-83, 1996.
35. Schmitt N, Calloe K, Nielsen NH, Buschmann M, Speckmann EJ, Schulze-Bahr E, Schwarz M. The novel C-terminal KCNQ1 mutation M520R alters protein trafficking. Biochem Biophys Res Commun 358: 304-310, 2007.
36. Shamgar L, Ma L, Schmitt N, Haitin Y, Peretz A, Wiener R, Hirsch J, Pongs O, Attali B. Calmodulin is essential for cardiac IKS channel gating and assembly: impaired function in long-QT mutations. Circ Res 98: 1055-1063, 2006.
37. Sheu HM, Kitajima Y, Yaoita H. Involvement of protein kinase C in translocation of desmoplakins from cytosol to plasma membrane during desmosome formation in human squamous cell carcinoma cells grown in low to normal calcium concentration. Exp Cell Res 185: 176-190, 1989.
38. Stuart RO, Nigam SK. Regulated assembly of tight junctions by protein kinase C. Proc Natl Acad Sci USA 92: 6072-6076, 1995.
39. Tengholm A, Meyer T. A PI3-kinase signaling code for insulin-triggered insertion of glucose transporters into the plasma membrane. Current Biol 12: 1871-1876, 2002.
40. Vadász I, Morty RE, Olschewski A. Thrombin impairs alveolar fluid clearance by promoting endocytosis of Na+, K+-ATPase. Am J Respir Cell Mol Biol 33: 343-354, 2005.
41. Vallon V, Grahammer F, Volkl H, Sandu CD, Richter K, Rexhepaj R, Gerlach U, Rong Q, Pfeifer K, Lang F. KCNQ1-dependent transport in renal and gastrointestinal epithelia. Proc Natl Acad Sci USA 102: 17864-17869, 2005.
42. Viard P, Butcher AJ, Halet G, Davies A, Nrnberg B, Heblich F, Dolphin AC. PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nature Neurosci 7: 939-946, 2004.
43. Wang Q, Curran ME, Splawski I, Burn TC, Millholland JM, Van- Raay TJ, Shen J, Timothy KW, Vincent GM, de Jager T, Schwartz PJ, Towbin JA, Moss AJ, Atkinson DL, Landes GM, Connors TD, Keating MT. Positional cloning of a novel potassium channel gene: KVLQT1 mutations cause cardiac arrhythmias. Nat Genet 12: 17-23, 1996.
44. Wangemann P, Liu J, Marcus DC. Ion transport mechanisms responsible for K+ secretion and the transepithelial voltage across marginal cells of stria vascularis in vitro. Hear Res 4: 19-29, 1995.
45. Wieman HL, Wofford JA, Rathmell JC. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol Biol Cell 18: 1437-1446, 2007.
46. Wiener R, Haitin Y, Shamgar L, Fernbndez-Alonso MC, Martos A, Chomsky-Hecht O, Rivas G, Attali B, Hirsch JA. The KCNQ1 (Kv71) COOH terminus, a multitiered scaffold for subunit assembly and protein interaction. J Biol Chem 283: 5815-51830, 2008.
47. Wilson AJ, Quinn KV, Graves FM, Bitner-Glindzicz M, Tinker A. Abnormal KCNQ1 trafficking influences disease pathogenesis in hereditary long QT syndromes (LQT1). Cardiovasc Res 67: 476-486, 2005.
48. Wollner DA, Krzeminski KA, Nelson WJ. Remodeling the cell surface distribution of membrane proteins during the development of epithelial cell polarity. J Cell Biol 116: 889-899, 1992.
49. Yamanaka T, Horikoshi Y, Suzuki A, Sugiyama Y, Kitamura K, Maniwa R, Nagai Y, Yamashita A, Hirose T, Ishikawa H. PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contactinduced formation of the epithelial junctional complex. Genes Cells 6: 721-731, 2001.
50. Yap AS, Brieher WM, Gumbiner BM. Molecular and functional analysis of cadherin-based adherens junctions. Ann Rev Cell Develop Biol 13: 119-146, 1997.
51. Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci USA 104: 819-822, 2007.