Keratin K18 increases cystic fibrosis transmembrane conductance regulator (CFTR) surface expression by binding to its C-terminal hydrophobic patch

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40547-40559

  Duan, Yuanyuan ^a,d   Sun, Ying ^a   Zhang, Fan ^a,e   Zhang, Wei Kevin ^a,f   Wang, Dong ^a,g   Wang, Yan ^a,h   Cao, Xu ^a   Hu, Wenbao ^a   Xie, Changyan ^a   Cuppoletti, John ^b   Magin, Thomas M ^c   Wang, Haixia ^a   Wu, Zhenguo ^a   Li, Ning ^a   Huang, Pingbo ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d Biothera Solutions Ltd   (China)

^e ZHEJIANG UNIVERSITY   (China)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g STANFORD UNIVERSITY   (United States)

^h CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL TAIL; C-TERMINUS; CELL SURFACE EXPRESSION; CRITICAL DETERMINANT; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATORS; HYDROPHOBIC PATCH; INTERMEDIATE FILAMENTS; OVER-EXPRESSION; RECYCLING RATE; RNA INTERFERENCE; SURFACE EXPRESSION; WILD TYPES;

BIOCHEMISTRY; CELL MEMBRANES; RNA;

PROTEINS;

CYTOKERATIN 18; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; BINDING SITE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DIMERIZATION; DUODENUM; GALLBLADDER; HUMAN; HUMAN CELL; HYDROPHOBICITY; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS;

ANIMALS; CELL LINE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KERATIN-18; MICE; MICE, KNOCKOUT; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TWO-HYBRID SYSTEM TECHNIQUES;

MUS;

EID: 84870002085     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.403584     Document Type: Article

References (54)

1. Hallows, K. R., Raghuram, V., Kemp, B. E., Witters, L. A., and Foskett, J. K. (2000) Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J. Clin. Invest. 105, 1711-1721 (Pubitemid 30421752)
2. Thelin, W. R., Kesimer, M., Tarran, R., Kreda, S. M., Grubb, B. R., Sheehan, J. K., Stutts, M. J., and Milgram, S. L. (2005) The cystic fibrosis transmembrane conductance regulator is regulated by a direct interaction with the protein phosphatase 2A. J. Biol. Chem. 280, 41512-41520 (Pubitemid 41832212)
3. Weixel, K. M., and Bradbury, N. A. (2000) The carboxyl terminus of the cystic fibrosis transmembrane conductance regulator binds to AP-2 clathrin adaptors. J. Biol. Chem. 275, 3655-3660 (Pubitemid 30083076)
4. 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
5. Guggino, W. B., and Stanton, B. A. (2006) New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat. Rev. Mol. Cell Biol. 7, 426-436 (Pubitemid 44050096)
6. Short, D. B., Trotter, K. W., Reczek, D., Kreda, S. M., Bretscher, A., Boucher, R. C., Stutts, M. J., and Milgram, S. L. (1998) An apical PDZ protein anchors the cystic fibrosis transmembrane conductance regulator to the cytoskeleton. J. Biol. Chem. 273, 19797-19801 (Pubitemid 28367041)
7. Wang, S., Yue, H., Derin, R. B., Guggino, W. B., and Li, M. (2000) Accessory protein-facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103, 169-179
8. Ostedgaard, L. S., Randak, C., Rokhlina, T., Karp, P., Vermeer, D., Ashbourne Excoffon, K. J., and Welsh, M. J. (2003) Effects of C-terminal deletions on cystic fibrosis transmembrane conductance regulator function in cystic fibrosis airway epithelia. Proc. Natl. Acad. Sci. U.S.A. 100, 1937-1942 (Pubitemid 36254552)
9. Haardt, M., Benharouga, M., Lechardeur, D., Kartner, N., and Lukacs, G. L. (1999) C-terminal truncations destabilize the cystic fibrosis transmembrane conductance regulator without impairing its biogenesis. A novel class of mutation. J. Biol. Chem. 274, 21873-21877
10. Mickle, J. E., Macek, M., Jr., Fulmer-Smentek, S. B., Egan, M. M., Schwiebert, E., Guggino, W., Moss, R., and Cutting, G. R. (1998) A mutation in the cystic fibrosis transmembrane conductance regulator gene associated with elevated sweat chloride concentrations in the absence of cystic fibrosis. Hum. Mol. Genet. 7, 729-735 (Pubitemid 28152272)
11. Gentzsch, M., and Riordan, J. R. (2001) Localization of sequences within the C-terminal domain of the cystic fibrosis transmembrane conductance regulator which impact maturation and stability. J. Biol. Chem. 276, 1291-1298 (Pubitemid 32096558)
12. Paramio, J. M., and Jorcano, J. L. (2002) Beyond structure: do intermediate filaments modulate cell signalling? Bioessays 24, 836-844 (Pubitemid 35022189)
13. Magin, T. M., Reichelt, J., and Hatzfeld, M. (2004) Emerging functions: diseases and animal models reshape our view of the cytoskeleton. Exp. Cell Res. 301, 91-102 (Pubitemid 39388901)
14. Vijayaraj, P., Söhl, G., and Magin, T. M. (2007) Keratin transgenic and knockout mice: functional analysis and validation of disease-causing mutations. Methods Mol. Biol. 360, 203-251
15. Magin, T. M., Schröder, R., Leitgeb, S., Wanninger, F., Zatloukal, K., Grund, C., and Melton, D. W. (1998) Lessons from keratin 18 knockout mice: formation of novel keratin filaments, secondary loss of keratin 7 and accumulation of liver-specific keratin 8-positive aggregates. J. Cell Biol. 140, 1441-1451 (Pubitemid 28152992)
16. Caulin, C., Ware, C. F., Magin, T. M., and Oshima, R. G. (2000) Keratin-dependent epithelial resistance to tumor necrosis factor-induced apoptosis. J. Cell Biol. 149, 17-22 (Pubitemid 30196695)
17. Inada, H., Izawa, I., Nishizawa, M., Fujita, E., Kiyono, T., Takahashi, T., Momoi, T., and Inagaki, M. (2001) Keratin attenuates tumor necrosis factor-induced cytotoxicity through association with TRADD. J. Cell Biol. 155, 415-426
18. Gilbert, S., Loranger, A., Daigle, N., and Marceau, N. (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J. Cell Biol. 154, 763-773 (Pubitemid 34292958)
19. Wald, F. A., Oriolo, A. S., Casanova, M. L., and Salas, P. J. (2005) Intermediate filaments interact with dormant ezrin in intestinal epithelial cells. Mol. Biol. Cell 16, 4096-4107 (Pubitemid 41262881)
20. Vijayaraj, P., Kroeger, C., Reuter, U., Hartmann, D., and Magin, T. M. (2010) Keratins regulate yolk sac hematopoiesis and vasculogenesis through reduced BMP-4 signaling. Eur J. Cell Biol. 89, 299-306
21. Vijayaraj, P., Kröger, C., Reuter, U., Windoffer, R., Leube, R. E., and Magin, T. M. (2009) Keratins regulate protein biosynthesis through localization of GLUT1 and -3 upstream of AMP kinase and Raptor. J. Cell Biol. 187, 175-184
22. Davezac, N., Tondelier, D., Lipecka, J., Fanen, P., Demaugre, F., Debski, J., Dadlez, M., Schrattenholz, A., Cahill, M. A., and Edelman, A. (2004) Global proteomic approach unmasks involvement of keratins 8 and 18 in the delivery of cystic fibrosis transmembrane conductance regulator (CFTR)/ΔF508-CFTR to the plasma membrane. Proteomics 4, 3833-3844 (Pubitemid 39657460)
23. Stanke, F., Hedtfeld, S., Becker, T., and Tümmler, B. (2011) An association study on contrasting cystic fibrosis endophenotypes recognizes KRT8 but not KRT18 as a modifier of cystic fibrosis disease severity and CFTRmediated residual chloride secretion. BMC Med. Genet. 12, 62
24. 2+-activated potassium channels in human airway Calu-3 epithelial cells. Am. J. Physiol. Cell Physiol. 294, C1443-C1453
25. Izawa, I., Nishizawa, M., Ohtakara, K., Ohtsuka, K., Inada, H., and Inagaki, M. (2000) Identification of Mrj, a DnaJ/Hsp40 family protein, as a keratin 8/18 filament regulatory protein. J. Biol. Chem. 275, 34521-34527
26. Lisanti, M. P., Le Bivic, A., Sargiacomo, M., and Rodriguez-Boulan, E. (1989) Steady-state distribution and biogenesis of endogenous Madin-Darby canine kidney glycoproteins: evidence for intracellular sorting and polarized cell surface delivery. J. Cell Biol. 109, 2117-2127 (Pubitemid 19282600)
27. Turvy, D. N., and Blum, J. S. (2001) Biotin labeling and quantitation of cell-surface proteins. Curr. Protoc. Immunol. Chapter 18, Unit 18.7
28. Li, C., and Naren, A. P. (2005) Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol. Ther. 108, 208-223 (Pubitemid 41527085)
29. Sun, F., Hug, M. J., Lewarchik, C. M., Yun, C. H., Bradbury, N. A., and Frizzell, R. A. (2000) E3KARP mediates the association of ezrin and protein kinase A with the cystic fibrosis transmembrane conductance regulator in airway cells. J. Biol. Chem. 275, 29539-29546 (Pubitemid 32043831)
30. Swiatecka-Urban, A., Boyd, C., Coutermarsh, B., Karlson, K. H., Barnaby, R., Aschenbrenner, L., Langford, G. M., Hasson, T., and Stanton, B. A. (2004) Myosin VI regulates endocytosis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 279, 38025-38031 (Pubitemid 39195518)
31. Salas, P. J. (1999) Insoluble γ-tubulin-containing structures are anchored to the apical network of intermediate filaments in polarized CACO-2 epithelial cells. J. Cell Biol. 146, 645-658
32. Toivola, D. M., Strnad, P., Habtezion, A., and Omary, M. B. (2010) Intermediate filaments take the heat as stress proteins. Trends Cell Biol. 20, 79-91
33. Desclozeaux, M., Venturato, J., Wylie, F. G., Kay, J. G., Joseph, S. R., Le, H. T., and Stow, J. L. (2008) Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am. J. Physiol. Cell Physiol. 295, C545-C556 (Pubitemid 352755787)
34. Silvis, M. R., Bertrand, C. A., Ameen, N., Golin-Bisello, F., Butterworth, M. B., Frizzell, R. A., and Bradbury, N. A. (2009) Rab11b regulates the apical recycling of the cystic fibrosis transmembrane conductance regulator in polarized intestinal epithelial cells. Mol. Biol. Cell 20, 2337-2350
35. Cantiello, H. F. (2001) Role of actin filament organization in CFTR activation. Pflugers Arch. 443, Suppl. 1, S75-S80
36. Thelin, W. R., Chen, Y., Gentzsch, M., Kreda, S. M., Sallee, J. L., Scarlett, C. O., Borchers, C. H., Jacobson, K., Stutts, M. J., and Milgram, S. L. (2007) Direct interaction with filamins modulates the stability and plasma membrane expression of CFTR. J. Clin. Invest. 117, 364-374 (Pubitemid 46203965)
37. Li, J., Dai, Z., Jana, D., Callaway, D. J., and Bu, Z. (2005) Ezrin controls the macromolecular complexes formed between an adapter protein Na+/H+exchanger regulatory factor and the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 280, 37634-37643 (Pubitemid 41643895)
38. Swiatecka-Urban, A., Talebian, L., Kanno, E., Moreau-Marquis, S., Coutermarsh, B., Hansen, K., Karlson, K. H., Barnaby, R., Cheney, R. E., Langford, G. M., Fukuda, M., and Stanton, B. A. (2007) Myosin Vb is required for trafficking of the cystic fibrosis transmembrane conductance regulator in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells. J. Biol. Chem. 282, 23725-23736 (Pubitemid 47311948)
39. Lipecka, J., Norez, C., Bensalem, N., Baudouin-Legros, M., Planelles, G., Becq, F., Edelman, A., and Davezac, N. (2006) Rescue of ΔF508-CFTR (cystic fibrosis transmembrane conductance regulator) by curcumin: involvement of the keratin 18 network. J. Pharmacol. Exp. Ther. 317, 500-505
40. Styers, M. L., Salazar, G., Love, R., Peden, A. A., Kowalczyk, A. P., and Faundez, V. (2004) The endo-lysosomal sorting machinery interacts with the intermediate filament cytoskeleton. Mol. Biol. Cell 15, 5369-5382 (Pubitemid 39564731)
41. Haggie, P. M., Stanton, B. A., and Verkman, A. S. (2004) Increased diffusional mobility of CFTR at the plasma membrane after deletion of its C-terminal PDZ binding motif. J. Biol. Chem. 279, 5494-5500 (Pubitemid 38220574)
42. Haggie, P. M., Kim, J. K., Lukacs, G. L., and Verkman, A. S. (2006) Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. Mol. Biol. Cell 17, 4937-4945 (Pubitemid 44907340)
43. Moyer, B. D., Denton, J., Karlson, K. H., Reynolds, D., Wang, S., Mickle, J. E., Milewski, M., Cutting, G. R., Guggino, W. B., Li, M., and Stanton, B. A. (1999) A PDZ-interacting domain in CFTR is an apical membrane polarization signal. J. Clin. Invest. 104, 1353-1361
44. Milewski, M. I., Mickle, J. E., Forrest, J. K., Stafford, D. M., Moyer, B. D., Cheng, J., Guggino, W. B., Stanton, B. A., and Cutting, G. R. (2001) A PDZ-binding motif is essential but not sufficient to localize theCterminus of CFTR to the apical membrane. J. Cell Sci. 114, 719-726 (Pubitemid 32237144)
45. Milewski, M. I., Lopez, A., Jurkowska, M., Larusch, J., and Cutting, G. R. (2005) PDZ-binding motifs are unable to ensure correct polarized protein distribution in the absence of additional localization signals. FEBS Lett. 579, 483-487 (Pubitemid 40092431)
46. Gentzsch, M., Aleksandrov, A., Aleksandrov, L., and Riordan, J. R. (2002) Functional analysis of the C-terminal boundary of the second nucleotide binding domain of the cystic fibrosis transmembrane conductance regulator and structural implications. Biochem. J. 366, 541-548 (Pubitemid 35001698)
47. Guilbault, C., Saeed, Z., Downey, G. P., and Radzioch, D. (2007) Cystic fibrosis mouse models. Am. J. Respir. Cell Mol. Biol. 36, 1-7 (Pubitemid 46067701)
48. Baribault, H., Penner, J., Iozzo, R. V., and Wilson-Heiner, M. (1994) Colorectal hyperplasia and inflammation in keratin 8-deficient FVB/N mice. Genes Dev. 8, 2964-2973
49. Toivola, D. M., Krishnan, S., Binder, H. J., Singh, S. K., and Omary, M. B. (2004) Keratins modulate colonocyte electrolyte transport via protein mistargeting. J. Cell Biol. 164, 911-921 (Pubitemid 38366902)
50. Ameen, N. A., Figueroa, Y., and Salas, P. J. (2001) Anomalous apical plasma membrane phenotype in CK8-deficient mice indicates a novel role for intermediate filaments in the polarization of simple epithelia. J. Cell Sci. 114, 563-575 (Pubitemid 32186113)
51. Davidson, D. J., and Dorin, J. R. (2001) The CF mouse: an important tool for studying cystic fibrosis. Expert Rev. Mol. Med. 3, 1-27
52. Dorin, J. R., Dickinson, P., Alton, E. W., Smith, S. N., Geddes, D. M., Stevenson, B. J., Kimber, W. L., Fleming, S., Clarke, A. R., Hooper, M. L., et al. (1992) Cystic fibrosis in the mouse by targeted insertional mutagenesis. Nature 359, 211-215
53. Dickinson, P., Smith, S. N., Webb, S., Kilanowski, F. M., Campbell, I. J., Taylor, M. S., Porteous, D. J., Willemsen, R., de Jonge, H. R., Farley, R., Alton, E. W., and Dorin, J. R. (2002) The severe G480C cystic fibrosis mutation, when replicated in the mouse, demonstrates mistrafficking, normal survival, and organ-specific bioelectrics. Hum. Mol. Genet. 11, 243-251 (Pubitemid 34173353)
54. van Doorninck, J. H., French, P. J., Verbeek, E., Peters, R. H., Morreau, H., Bijman, J., and Scholte, B. J. (1995) A mouse model for the cystic fibrosis ΔF508 mutation. EMBO J. 14, 4403-4411