Endocytic trafficking routes of wild type and ΔF508 cystic fibrosis transmembrane conductance regulator

Molecular Biology of the Cell

Volumn 15, Issue 6, 2004, Pages 2684-2696

  Gentzsch, Martina ^a   Chang, Xiu Bao ^a   Cui, Liying ^a   Wu, Yufeng ^a   Ozols, Victor V ^a   Choudhury, Amit ^a   Pagano, Richard E ^a   Riordan, John R ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROTEINASE INHIBITOR; RAB PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYSTIC FIBROSIS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE;

ANIMALS; CELL LINE; CELL MEMBRANE; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOCYTOSIS; EPITOPES; HUMANS; PROTEASE INHIBITORS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; TEMPERATURE;

ANIMALIA;

EID: 2542480784     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-03-0176     Document Type: Article

References (58)

1. Benharouga, M., Haardt, M., Kartner, N., and Lukacs, G.L. (2001). COOH-terminal truncations promote proteasome-dependent degradation of mature cystic fibrosis transmembrane conductance regulator from post-Golgi compartments. J. Cell Biol. 153, 957-970.
2. Bonifacino, J.S., and Traub, L.M. (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447.
3. Bradbury, N.A., Clark, J.A., Watkins, S.C., Widnell, C.C., Smith, H.S.T., and Bridges, R.J. (1999). Characterization of the internalization pathways for the cystic fibrosis transmembrane conductance regulator. Am. J. Physiol. 276, L659-L668.
4. Bradbury, N.A., Jilling, T., Berta, G., Sorscher, E.J., Bridges, R.J., and Kirk, K.L. (1992). Regulation of plasma membrane recycling by CFTR. Science 256, 530-532.
5. Brown, C.R., Hong-Brown, L.Q., and Welch, W.J. (1997). Strategies for correcting the delta F508 CFTR protein-folding defect. J. Bioenerg. Biomembr. 29, 491-502.
6. Chang, X.-B., Cui, L., Hou, Y., Jensen, T.J., Aleksandrov, A.A., Mengos, A., and Riordan, J.R. (1999). Removal of multiple arginine-framed trafficking signals overcomes misprocessing of delta F508 CFTR present in most patients with cystic fibrosis. Mol. Cell 4, 137-142.
7. Chang, X.-B., Hou, Y.-X., Jensen, T., and Riordan, J.R. (1994). Mapping of the cystic fibrosis transmembrane conductance regulator membrane topology by glycosylation site insertion. J. Biol. Chem. 269, 18572-18575.
8. Chang, X.-B., Tabcharani, J.A., Hou, Y.-X., Jensen, T.J., Kartner, N., Alon, N., Hanrahan, J.W., and Riordan, J.R. (1993). Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all ten PKA consensus phosphorylation sites. J. Biol. Chem. 268, 11304-11311.
9. Choudhury, A., Dominguez, M., Puri, V., Sharma, D.K., Narita, K., Wheatley, C.L., Marks, D.L., and Pagano, R.E. (2002). Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Investig. 109, 1541-1550.
10. Denning, G.M., Anderson, M.P., Amara, J.F., Marshall, J., Smith, A.E., and Welsh, M.J. (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764.
11. Dunn, W.A., Hubbard, A.L., and Aronson, N.N., Jr. (1980). Low temperature selectively inhibits fusion between pinocytic vesicles and lysosomes during heterophagy of 125I-asialofetuin by the perfused rat liver. J. Biol. Chem. 255, 5971-5978.
12. Gelman, M.S., and Kopito, R.R. (2002). Rescuing protein conformation: prospects for pharmacological therapy in cystic fibrosis. J. Clin. Investig. 110, 1591-1597.
13. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Paolo Di Fiore, P., and Dikic, I. (2003). Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466.
14. Hämmerle, M.M., Aleksandrov, A.A., and Riordan, J.R. (2001). Disease-associated mutations in the extracytoplasmic loops of cystic fibrosis transmembrane conductance regulator do not impede biosynthetic processing but impair chloride channel stability. J. Biol. Chem. 276, 14848-14854.
15. Hanrahan, J.H., Gentzsch, M., and Riordan, J.R. (2003). The cystic fibrosis transmembrane conductance regulator (ABCC7). In: ABC Proteins: From Bacteria to Man, ed. B. Holland, C.F. Higgins, K. Kuchler, and S.P.C. Cole, New York: Elsevier Science, 589-618.
16. Heda, G.D., Tanwani, M., and Marino, C.R. (2001). The Delta F508 mutation shortens the biochemical half-life of plasma membrane CFTR in polarized epithelial cells. Am. J. Physiol. 280, C166-C174.
17. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport to ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell. Dev. Biol. 19, 141-172.
18. Howard, M., DuVall, M.D., Devor, D.C., Dong, J.Y., Henze, K., and Frizzell, R.A. (1995). Epitope tagging permits cell surface detection of functional CFTR. Am. J. Physiol. 269, C1565-C1576.
19. Howard, M., Jiang, X., Stolz, D.B., Hill, W.G., Johnson, J.A., Watkins, S.C., Frizzell, R.A., Bruton, C.M., Robbins, P.D., and Weisz, O.A. (2000). Forskolin-induced apical membrane insertion of virally expressed, epitope-tagged CFTR in polarized MDCK cells. Am. J. Physiol. 279, C375-C382.
20. Hu, W., Howard, M., and Lukacs, G.L. (2001). Multiple endocytic signals in the C-terminal tail of the cystic fibrosis transmembrane conductance regulator. Biochem. J. 354, 561-572.
21. Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol. 3, 893-905.
22. Kauppi, M., Simonsen, A., Bremnes, B., Vieira, A., Callaghan, J., Stenmark, H., and Olkkonen, V.M. (2002). The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J. Cell Sci. 115, 899-911.
23. Kopito, R.R. (1999). Biosynthesis and degradation of CFTR. Physiol. Rev. 79, S167-S173.
24. Longva, K.E., Blystad, F.D., Stang, E., Larsen, A.M., Johannessen, L.E., and Madshus, I.H. (2002). Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156, 843-854.
25. Lukacs, G.L., Chang, X.-B., Bear, C., Kartner, N., Mohamed, A., Riordan, J.R., and Grinstein, S. (1993). The DF508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J. Biol. Chem. 268, 21592-21598.
26. Lukacs, G.L., Chang, X.-B., Kartner, N., Rotstein, O.D., Riordan, J.R., and Grinstein, S. (1992). The cystic fibrosis transmembrane regulator is present and functional in endosomes. Role as a determinant of endosomal pH. J. Biol. Chem. 267, 14568-14572.
27. Lukacs, G.L., Segal, G., Kartner, N., Grinstein, S., and Zhang, F. (1997). Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation. Biochem. J. 328, 353-361.
28. Marsh, M., Bolzau, E., and Helenius, A. (1983). Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32, 931-940.
29. Melman, L., Geuze, H.J., Li, Y., McCormick, L.M., Van Kerkhof, P., Strous, G.J., Schwartz, A.L., and Bu, G. (2002). Proteasome regulates the delivery of LDL receptor-related protein into the degradation pathway. Mol. Biol. Cell 13, 3325-3335.
30. Mohrmann, K., Leijendekker, R., Gerez, L., and van Der Sluijs, P. (2002). rab4 regulates transport to the apical plasma membrane in Madin-Darby canine kidney cells. J. Biol. Chem. 277, 10474-10481.
31. Parton, R.G., Prydz, K., Bomsel, M., Simons, K., and Griffiths, G. (1989). Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J. Cell Biol. 109, 3259-3272.
32. Pfeffer, S.R. (2001). Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol. 11, 487-491.
33. Picciano, J.A., Ameen, N., Grant, B., and Bradbury, N.A. (2003). Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator. Am. J. Physiol. 285, C1009-C1018.
34. Prince, L.S., Workman, R.B., Jr., and Marchase, R.B. (1994). Rapid endocytosis of the cystic fibrosis transmembrane conductance regulator chloride channel. Proc. Natl. Acad. Sci. USA 91, 5192-5196.
35. Riordan, J.R. (1999). Cystic fibrosis as a disease of misprocessing of the cystic fibrosis transmembrane conductance regulator glycoprotein. Am. J. Hum. Genet. 64, 1499-1504.
36. Roberts, M., Barry, S., Woods, A., van der Sluijs, P., and Norman, J. (2001). PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402.
37. Roberts, R.L., Barbieri, M.A., Pryse, K.M., Chua, M., Morisaki, J.H., and Stahl, P.D. (1999). Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112, 3667-3675.
38. Rocca, A., Lamaze, C., Subtil, A., and Dautry-Varsat, A. (2001). Involvement of the ubiquitin/proteasome system in sorting of the interleukin 2 receptor beta chain to late endocytic compartments. Mol. Biol. Cell 12, 1293-1301.
39. Rohn, W.M., Rouille, Y., Waguri, S., and Hoflack, B. (2000). Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J. Cell Sci. 113, 2093-2101.
40. Setiadi, H., Sedgewick, G., Erlandsen, S.L., and McEver, R.P. (1998). Interactions of the cytoplasmic domain of P-selectin with clathrin-coated pits enhance leukocyte adhesion under flow. J. Cell Biol. 142, 859-871.
41. Sharma, D.K., Choudhury, A., Singh, R.D., Wheatley, C.L., Marks, D.L., and Pagano, R.E. (2003). Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem. 278, 7564-7572.
42. Sharma, M., Benharouga, M., Hu, W., and Lukacs, G.L. (2001). Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J. Biol. Chem. 276, 8942-8950.
43. Sheff, D., Pelletier, L., O'Connell, C.B., Warren, G., and Mellman, I. (2002). Transferrin receptor recycling in the absence of perinuclear recycling endosomes. J. Cell Biol. 156, 797-804.
44. Sheff, D.R., Daro, E.A., Hull, M., and Mellman, I. (1999). The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145, 123-139.
45. Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.M., Brech, A., Callaghan, J., Toh, B.H., Murphy, C., Zerial, M., and Stenmark, H. (1998). EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498.
46. Sonnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
47. Stenmark, H., Parton, R.G., Steele-Mortimer, O., Lutcke, A., Gruenberg, J., and Zerial, M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296.
48. Swiatecka-Urban, A., Duhaime, M., Coutermarsh, B., Karlson, K.H., Collawn, J., Milewski, M., Cutting, G.R., Guggino, W.B., Langford, G., and Stanton, B.A. (2002). PDZ domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 40099-40105.
49. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M., and Parton, R.G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
50. van der Sluijs, P., Hull, M., Webster, P., Male, P., Goud, B., and Mellman, I. (1992). The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70, 729-740.
51. van Kerkhof, P., Alves dos Santos, C.M., Sachse, M., Klumperman, J., Bu, G., and Strous, G.J. (2001). Proteasome inhibitors block a late step in lysosomal transport of selected membrane but not soluble proteins. Mol. Biol. Cell 12, 2556-2566.
52. Vollenweider, P., Martin, S.S., Haruta, T., Morris, A.J., Nelson, J.G., Cormont, M., Le Marchand-Brustel, Y., Rose, D.W., and Olefsky, J.M. (1997). The small guanosine triphosphate-binding protein Rab4 is involved in insulin-induced GLUT4 translocation and actin filament rearrangement in 3T3-L1 cells. Endocrinology 138, 4941-4949.
53. Ward, C.L., Omura, S., and Kopito, R.R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
54. Weixel, K.M., and Bradbury, N.A. (2001). Mu 2 binding directs the cystic fibrosis transmembrane conductance regulator to the clathrin-mediated endocytic pathway. J. Biol. Chem. 276, 46251-46259.
55. Yamashiro, D.J., Tycko, B., Fluss, S.R., and Maxfield, F.R. (1984). Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37, 789-800.
56. Yoo, J.S., Moyer, B.D., Bannykh, S., Yoo, H.M., Riordan, J.R., and Balch, W.E. (2002). Non-conventional trafficking of the cystic fibrosis transmembrane conductance regulator through the early secretory pathway. J. Biol. Chem. 277, 11401-11409.
57. Yu, A., and Malek, T.R. (2001). The proteasome regulates receptor-mediated endocytosis of interleukin-2. J. Biol. Chem. 276, 381-385.
58. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2, 107-117.