The PDZ-interaction of the intestinal anion exchanger downregulated in adenoma (DRA; SLC26A3) facilitates its movement into Rab11a-positive recycling endosomes

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 11, 2013, Pages

  Lissner, S ^a   Hsieh, C J ^a   Nold, L ^a   Bannert, K ^b   Bodammer, P ^b   Sultan, A ^c   Seidler, U ^c   Graeve, L ^d   Lamprecht, G ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF ROSTOCK   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Endocytosis; Endosomes; Rab5a

Indexed keywords

CELL PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; PDZ PROTEIN; RAB11A PROTEIN; SLC26A3 PROTEIN; UNCLASSIFIED DRUG;

ADENOMA; ANION EXCHANGE; ARTICLE; CELL MEMBRANE; CELL STRAIN HEK293; CELL SURFACE; DOWN REGULATION; ENDOSOME; HALF LIFE TIME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TRANSIENT EXPRESSION; TRANSIENT TRANSFECTION;

ENDOCYTOSIS; ENDOSOMES; RAB5A;

CELL MEMBRANE; CHLORIDE-BICARBONATE ANTIPORTERS; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; MUTATION; PDZ DOMAINS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS;

EID: 84878665429     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00132.2012     Document Type: Article

References (51)

1. Balse E, El Haou S, Dillanian G, Dauphin A, Eldstrom J, Fedida D, Coulombe A, Hatem SN. Cholesterol modulates the recruitment of Kv1.5 channels from Rab11-associated recycling endosome in native atrial myocytes. Proc Natl Acad Sci USA 106: 14681-14686, 2009.
2. + exchanger regulatory factor in the functional expression of cystic fibrosis transmembrane conductance regulator in nonpolarized cells and epithelia. J Biol Chem 278: 22079-22089, 2003.
3. Butterworth MB. Regulation of the epithelial sodium channel (ENaC) by membrane trafficking. Biochim Biophys Acta 1802: 1166-1177, 2010.
4. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401: 286-290, 1999.
5. Cormont M, Marchand-Brustel Y. The role of small G-proteins in the regulation of glucose transport. Mol Membr Biol 18: 213-220, 2001.
6. Corvera S, Czech MP. Direct targets of phosphoinositide 3-kinase products in membrane traffic and signal transduction. Trends Cell Biol 8: 442-446, 1998.
7. Ding W, Zhang LN, Yeaman C, Engelhardt JF. rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 13: 671-682, 2006.
8. Eggers CT, Schafer JC, Goldenring JR, Taylor SS. D-AKAP2 interacts with Rab4 and Rab11 through its RGS domains and regulates transferrin receptor recycling. J Biol Chem 284: 32869-32880, 2009.
9. Enyedi A, Strehler EE. Regulation of apical membrane enrichment and retention of plasma membrane Ca ATPase splice variants by the PDZdomain protein NHERF2. Commun Integr Biol 4: 340-343, 2011.
10. Fan GH, Lapierre LA, Goldenring JR, Sai J, Richmond A. Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol Biol Cell 15: 2456-2469, 2004.
11. Gagescu R, Demaurex N, Parton RG, Hunziker W, Huber LA, Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 11: 2775-2791, 2000.
12. Gorvel JP, Chavrier P, Zerial M, Gruenberg J. rab5 controls early endosome fusion in vitro. Cell 64: 915-925, 1991.
13. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10: 597-608, 2009.
14. Hoglund P, Haila S, Socha J, Tomaszewski L, Saarialho-Kere U, Karjalainen-Lindsberg ML, Airola K, Holmberg C, de la Chapelle A, Kere. Mutations of the Down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat Genet 14: 316-319, 1996.
15. Joubert L, Hanson B, Barthet G, Sebben M, Claeysen S, Hong W, Marin P, Dumuis A, Bockaert J. New sorting nexin (SNX27) and NHERF specifically interact with the 5-HT4a receptor splice variant: roles in receptor targeting. J Cell Sci 117: 5367-5379, 2004.
16. Karpushev AV, Levchenko V, Pavlov TS, Lam V, Vinnakota KC, Vandewalle A, Wakatsuki T, Staruschenko A. Regulation of ENaC expression at the cell surface by Rab11. Biochem Biophys Res Commun 377: 521-525, 2008.
17. Kato A, Romero MF. Regulation of electroneutral NaCl absorption by the small intestine. Annu Rev Physiol 73: 261-281, 2011.
18. + exchanger 3 (NHE3) requires an NHE3-E3KARP-alpha-actinin-4 complex for oligomerization and endocytosis. J Biol Chem 277: 23714-23724, 2002.
19. + exchanger NHE3 isoform is regulated by the phosphatidylinositol 3-kinase pathway. J Biol Chem 273: 20828-20836, 1998.
20. Lahuna O, Quellari M, Achard C, Nola S, Meduri G, Navarro C, Vitale N, Borg JP, Misrahi M. Thyrotropin receptor trafficking relies on the hScrib-[beta]PIX-GIT1-ARF6 pathway. EMBO J 24: 1364-1374, 2005.
21. Lamprecht G, Baisch S, Schoenleber E, Gregor M. Transport properties of the human intestinal anion exchanger DRA (down regulated in adenoma) in transfected HEK293 cells. Pflugers Arch 449: 479-490, 2005.
22. + exchange. Biochemistry 41: 12336-12342, 2002.
23. Lamprecht G, Seidler U. The emerging role of PDZ adapter proteins for regulation of intestinal ion transport. Am J Physiol Gastrointest Liver Physiol 291: G766-G777, 2006.
24. Lamprecht G, Hsieh CJ, Lissner S, Nold L, Heil A, Gaco V, Schafer J, Turner JR, Gregor M. The intestinal anion exchanger down regulated in adenoma (DRA) is inhibited by intracellular calcium. J Biol Chem 284: 19744-19753, 2009.
25. Lamprecht G, Schaefer J, Dietz K, Gregor M. Chloride and bicarbonate have similar affinities to the intestinal anion exchanger DRA (down regulated in adenoma). Pflugers Arch 452: 307-315, 2006.
26. Lauffer BE, Melero C, Temkin P, Lei C, Hong W, Kortemme T, von Zastrow M. SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J Cell Biol 190: 565-574, 2010.
27. 2+-dependent inhibition of NHE3 requires PKCα which binds to E3KARP to decrease surface NHE3 containing plasma membrane complexes. Am J Physiol Cell Physiol 285: C1527-C1536, 2003.
28. Li G, D'Souza-Schorey C, Barbieri MA, Roberts RL, Klippel A, Williams LT, Stahl PD. Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc Natl Acad Sci USA 92: 10207-10211, 1995.
29. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 119: 605-614, 2006.
30. Lissner S, Nold L, Hsieh CJ, Turner JR, Gregor M, Graeve L, Lamprecht G. Activity and PI3-kinase dependent trafficking of the intestinal anion exchanger downregulated in adenoma depend on its PDZ interaction and on lipid rafts. Am J Physiol Gastrointest Liver Physiol 299: G907-G920, 2010.
31. Lunn ML, Nassirpour R, Arrabit C, Tan J, McLeod I, Arias CM, Sawchenko PE, Yates JR, III, Slesinger PA. A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat Neurosci 10: 1249-1259, 2007.
32. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 5: 121-132, 2004.
33. Mertz J. Optical sectioning microscopy with planar or structured illumination. Nat Methods 8: 811-819, 2011.
34. Mohrmann K, van der SP. Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol Membr Biol 16: 81-87, 1999.
35. + exchanger NHE3 activity and trafficking are lipid raft-dependent. J Biol Chem 281: 17845-17855, 2006.
36. Nisar S, Daly ME, Federici AB, Artoni A, Mumford AD, Watson SP, Mundell SJ. An intact PDZ motif is essential for correct P2Y12 purinoceptor traffic in human platelets. Blood 118: 5641-5651, 2011.
37. Ostedgaard LS, Randak C, Rokhlina T, Karp P, Vermeer D, Ashbourne E, Welsh MJ. Effects of C-terminal deletions on cystic fibrosis transmembrane conductance regulator function in cystic fibrosis airway epithelia. Proc Natl Acad Sci USA 100: 1937-1942, 2003.
38. + exchanger. Nat Genet 19: 282-285, 1998.
39. Schweinfest CW, Spyropoulos DD, Henderson KW, Kim JH, Chapman JM, Barone S, Worrell RT, Wang Z, Soleimani M. slc26a3 (dra)-deficient mice display chloride-losing diarrhea, enhanced colonic proliferation, and distinct up-regulation of ion transporters in the colon. J Biol Chem 281: 37962-37971, 2006.
40. Scriven DRL, Lynch RM, Moore EDW. Image acquisition for colocalization using optical microscopy. Am J Physiol Cell Physiol 294: C1119-C1122, 2008.
41. Silvis MR, Bertrand CA, Ameen N, Golin-Bisello F, Butterworth MB, Frizzell RA, Bradbury NA. Rab11b regulates the apical recycling of the cystic fibrosis transmembrane conductance regulator in polarized intestinal epithelial cells. Mol Biol Cell 20: 2337-2350, 2009.
42. + exchange. Am J Physiol Gastrointest Liver Physiol 298: G182-G189, 2010.
43. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149: 901-914, 2000.
44. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525, 2009.
45. Swiatecka-Urban A, Duhaime M, Coutermarsh B, Karlson KH, Collawn J, Milewski M, Cutting GR, Guggino WB, Langford G, Stanton BA. PDZ Domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 277: 40099-40105, 2002.
46. Takata K, Tajika Y, Matsuzaki T, Aoki T, Suzuki T, Abduxukur A, Hagiwara H. Molecular mechanisms and drug development in aquaporin water channel diseases: water channel aquaporin-2 of kidney collecting duct cells. J Pharmacol Sci 96: 255-259, 2004.
47. Trischler M, Stoorvogel W, Ullrich O. Biochemical analysis of distinct Rab5-and Rab11-positive endosomes along the transferrin pathway. J Cell Sci 112: 4773-4783, 1999.
48. Wente W, Stroh T, Beaudet A, Richter D, Kreienkamp HJ. Interactions with PDZ domain proteins PIST/GOPC and PDZK1 regulate intracellular sorting of the somatostatin receptor subtype 5. J Biol Chem 280: 32419-32425, 2005.
49. + exchanger 3 via apical epidermal growth factor receptor in intestinal epithelial cells. Am J Physiol Cell Physiol 301: C1008-C1016, 2011.
50. Zachos NC, Hodson C, Kovbasnjuk O, Li X, Thelin WR, Cha B, Milgram S, Donowitz M. Elevated intracellular calcium stimulates NHE3 activity by an IKEPP (NHERF4) dependent mechanism. Cell Physiol Biochem 22: 693-704, 2008.
51. Zachos NC, Li X, Kovbasnjuk O, Hogema B, Sarker R, Lee LJ, Li M, de Jonge H, Donowitz M. NHERF3 (PDZK1) contributes to basal and calcium inhibition of NHE3 activity in Caco-2BBe cells. J Biol Chem 284: 23708-23718, 2009.