Molecular motors and apical CFTR traffic in epithelia

International Journal of Molecular Sciences

Volumn 14, Issue 5, 2013, Pages 9628-9642

  Kravtsov, Dmitri V ^a   Ameen, Nadia A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin transport; CFTR; Microtubules; Myosins; Trafficking

Indexed keywords

ACTIN; ADAPTOR PROTEIN; CHLORIDE ION; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MOLECULAR MOTOR; MYOSIN I; MYOSIN IA; MYOSIN V; MYOSIN VI; REGULATOR PROTEIN; SODIUM ION; UNCLASSIFIED DRUG; MYOSIN;

CELL SPECIFICITY; CELL TYPE; CHANNEL GATING; CHLORIDE CURRENT; ENDOCYTOSIS; EPITHELIUM; EXOCYTOSIS; HUMAN; INTESTINE BRUSH BORDER; INTESTINE EPITHELIUM; KIDNEY EPITHELIUM; MICROTUBULE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RESPIRATORY EPITHELIUM; REVIEW; SODIUM TRANSPORT; ANIMAL; METABOLISM;

ACTINS; ANIMALS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIUM; HUMANS; MICROTUBULES; MYOSINS; PROTEIN TRANSPORT;

EID: 84877717945     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14059628     Document Type: Review

References (63)

1. Gadsby, D.C.; Vergani, P.; Csanady, L. The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 2006, 440, 477-483.
2. Harris, A.; Charkley, G.; Goodman, S.; Coleman, L. Expression of the cystic fibrosis gene in human development. Development 1991, 113, 305-310.
3. O'Loughlin, E.V.; Hunt, D.M.; Gaskin, K.J.; Steil, D.; Bruzuszcak, I.M.; Martin, H.C.O.; Bambach, C.; Smith, R. X-ray microanalysis of cell elements in normal and cystic fibrosis Jejunum: Evidence for chloride secretion in villi. Gastroenterology 1996, 110, 411-418.
4. Pratha, V.S.; Hogan, D.L.; Martensson, B.A.; Bernard, J.; Zhou, R.; Isenberg, J.I. Identification of transport abnormalities in duodenal mucosa and duodenal enterocytes from patients with cystic fibrosis. Gastroenterology 2000, 118, 1051-1060.
5. Rowe, S.M.; Miller, S.; Sorscher, E.J. Cystic fibrosis. N. Engl. J. Med. 2005, 352, 1992-2001.
6. Pilewski, J.M.; Frizzell, R.A. Role of CFTR in airway disease. Physiol. Rev. 1999, 79, S215-S255.
7. Terheggen-Lagro, S.W.; Rijkers, G.T.; van der Ent, C.K. The role of airway epithelium and blood neutrophils in the inflammatory response in cystic fibrosis. J. Cyst. Fibros. 2005, 4, 15-23.
8. Machen, T.E. Innate immune response in CF airway epithelia: Hyperinflammatory? Am. J. Physiol. Cell Physiol. 2006, 291, C218-C230.
9. Bridges, R.J. Mechanisms of bicarbonate secretion: Lessons from the airways. Cold Spring Harb. Perspect. Med. 2012, 2, doi:10.1101/cshperspect.a015016.
10. Jakab, R.L.; Collaco, A.M.; Ameen, N.A. Physiological relevance of cell-specific distribution patterns of CFTR, NKCC1, NBCe1, and NHE3 along the crypt-villus axis in the intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300, G82-G98.
11. Ameen, N.; Silvis, M.; Bradbury, N.A. Endocytic trafficking of CFTR in health and disease. J. Cyst. Fibros. 2007, 6, 1-14.
12. Lukacs, G.L.; Chang, X.B.; Bear, C.; Kartner, N.; Mohamed, A.; Riordan, J.R.; Grinstein, S. The delta F508 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. 1993, 268, 21592-21598.
13. Thiagarajah, J.R.; Verkman, A.S. CFTR pharmacology and its role in intestinal fluid secretion. Curr. Opin. Pharmacol. 2003, 3, 594-599.
14. Ameen, N.; Alexis, J.; Salas, P. Cellular localization of the cystic fibrosis transmembrane conductance regulator in mouse intestinal tract. Histochem. Cell Biol. 2000, 114, 69-75.
15. Ameen, N.A.; van Donselaar, E.; Posthuma, G.; de Jonge, H.; McLaughlin, G.; Geuze, H.J.; Marino, C.; Peters, P.J. Subcellular distribution of CFTR in rat intestine supports a physiologic role for CFTR regulation by vesicle traffic. Histochem. Cell Biol. 2000, 114, 219-228.
16. Guggino, W.B.; Stanton, B.A. New insights into cystic fibrosis: Molecular switches that regulate CFTR. Nat. Rev. Mol. Cell Biol. 2006, 7, 426-436.
17. Collaco, A.; Marathe, J.; Kohnke, H.; Kravstov, D.; Ameen, N. Syntaxin 3 is necessary for cAMP- and cGMP-regulated exocytosis of CFTR: Implications for enterotoxigenic diarrhea. Am. J. Physiol. Cell Physiol. 2010, 299, C1450-C1460.
18. Kravtsov, D.V.; Caputo, C.; Collaco, A.; Hoekstra, N.; Egan, M.E.; Mooseker, M.S.; Ameen, N.A. Myosin Ia is required for CFTR brush border membrane trafficking and ion transport in the mouse small intestine. Traffic 2012, 13, 1072-1082.
19. Gentzsch, M.; Chang, X.B.; Cui, L.; Wu, Y.; Ozols, V.V.; Choudhury, A.; Pagano, R.E.; Riordan, J.R. Endocytic trafficking routes of wild type and DeltaF508 cystic fibrosis transmembrane conductance regulator. Mol. Biol. Cell 2004, 15, 2684-2696.
20. 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., et al. 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. 2007, 282, 23725-23736.
21. Silvis, M.R.; Bertrand, C.A.; Ameen, N.; Golin-Bisello, F.; Butterworth, M.B.; Frizzell, R.A.; Bradbury, N.A. Rab11b regulates the apical recycling of the cystic fibrosis transmembrane conductance regulator in polarized intestinal epithelial cells. Mol. Biol. Cell 2009, 20, 2337-2350.
22. Cheng, S.H.; Rich, D.P.; Marshall, J.; Gregory, R.J.; Welsh, M.J.; Smith, A.E. Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 1991, 66, 1027-1036.
23. Tien, X.-Y.; Brasitus, T.A.; Kaetzel, M.A.; Dedman, J.R.; Nelson, D.J. Activation of the cystic fibrosis transmembrane conductance regulator by cGMP in the human colonic cancer cell line, Caco-2. J. Biol. Chem. 1994, 269, 51-54.
24. - channels. Am. J. Physiol. 1994, 267, C272-C281.
25. Ameen, N.A.; Marino, C.; Salas, P.J. cAMP-dependent exocytosis and vesicle traffic regulate CFTR and fluid transport in rat jejunum in vivo. Am. J. Physiol. Cell Physiol. 2003, 284, C429-C438.
26. Rogan, M.P.; Stoltz, D.A.; Hornick, D.B. Cystic fibrosis transmembrane conductance regulator intracellular processing, trafficking, and opportunities for mutation-specific treatment. Chest 2011, 139, 1480-1490.
27. Vale, R.D. The molecular motor toolbox for intracellular transport. Cell 2003, 112, 467-480.
28. Grotmol, T.; Van Dyke, R.W. Prostaglandin- and theophylline-induced C1 secretion in rat distal colon is inhibited by microtubule inhibitors. Dig. Dis. Sci. 1992, 37, 1709-1717.
29. - secretion in epithelial cells. Am. J. Physiol. 1994, 266, C254-C268.
30. Tousson, A.; Fuller, C.M.; Benos, D.J. Apical recruitment of CFTR in T84 cells is dependent on cAMP and microtubules but not calcium or microfilaments. J. Cell Sci. 1996, 109, 1325-1334.
31. Hiebsch, R.R.; Raub, T.J.; Wattenberg, B.W. Primaquine blocks transport by inhibiting the formation of functional transport vesicles. Studies in a cell-free assay of protein transport through the Golgi apparatus. J. Biol. Chem. 1991, 266, 20323-20328.
32. -secretion via CFTR in Calu-3 airway epithelial cells. Am. J. Physiol. 1998, 275, C913-C920.
33. Jin, M.; Snider, M.D. Role of microtubules in transferrin receptor transport from the cell surface to endosomes and the Golgi complex. J. Biol. Chem. 1993, 268, 18390-18397.
34. + reabsorption in A6 cells. Am. J. Physiol. 1998, 274, F300-F314.
35. Moyer, B.D.; Loffing, J.; Schwiebert, E.M.; Loffing-Cueni, D.; Halpin, P.A.; Karlson, K.H.; Ismailov, I.L.; Guggino, W.B.; Langford, G.M.; Stanton, B.A. Membrane trafficking of the cystic fibrosis gene product,cystic fibrosis transmembrane conductance regulator,tagged with green fluorescent protein in madin-darby kidney cells. J. Biol. Chem. 1998, 21, 21759-21768.
36. Johnston, J.A.; Illing, M.E.; Kopito, R.R. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskeleton 2002, 53, 26-38.
37. Bannykh, S.I.; Bannykh, G.I.; Fish, K.N.; Moyer, B.D.; Riordan, J.R.; Balch, W.E. Traffic pattern of cystic fibrosis transmembrane regulator through the early exocytic pathway. Traffic 2000, 1, 852-870.
38. Burnett, B.G.; Pittman, R.N. The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc. Natl. Acad. Sci. USA 2005, 102, 4330-4335.
39. Prat, A.G.; Xiao, Y.F.; Ausiello, D.A.; Cantiello, H.F. cAMP-independent regulation of CFTR by the actin cytoskeleton. Am. J. Physiol. 1995, 268, C1552-C1561.
40. Hug, T.; Koslowsky, T.; Ecke, D.; Greger, R.; Kunzelmann, K. Actin-dependent activation of ion conductances in bronchial epithelial cells. Pflugers Arch. 1995, 429, 682-690.
41. Halm, D.R.; Halm, S.T.; DiBona, D.R.; Frizzell, R.A.; Johnson, R.D. Selective stimulation of epithelial cells in colonic crypts: Relation to active chloride secretion. Am. J. Physiol. 1995, 269, C929-C942.
42. Krendel, M.; Mooseker, M.S. Myosins: Tails (and heads) of functional diversity. Physiology 2005, 20, 239-251.
43. Heintzelman, M.B.; Hasson, T.; Mooseker, M.S. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J. Cell Sci. 1994, 107, 3535-3543.
44. Henn, A.; De La Cruz, E.M. Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension. J. Biol. Chem. 2005, 280, 39665-39676.
45. Mermall, V.; Post, P.L.; Mooseker, M.S. Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 1998, 279, 527-533.
46. Ameen, N.A.; Salas, P.J. Microvillus inclusion disease: A genetic defect affecting apical membrane protein traffic in intestinal epithelium. Traffic 2000, 1, 76-83.
47. Ukarapol, N.; Chotinaruemol, S.; Lertprasertsuk, N.; Wongsawasdi, L. Microvillus inclusion disease as a cause of severe protracted diarrhea in infants. J Med. Assoc. Thail. 2001, 84, 1356-1360.
48. Cutz, E.; Rhoads, J.M.; Drumm, B.; Sherman, P.M.; Durie, P.R.; Forstner, G.G. Microvillus inclusion disease: An inherited defect of brush-border assembly and differentiation. N. Engl. J. Med. 1989, 320, 646-651.
49. Muller, T.; Hess, M.W.; Schiefermeier, N.; Pfaller, K.; Ebner, H.L.; Heinz-Erian, P.; Ponstingl, H.; Partsch, J.; Rollinghoff, B.; Kohler, H.; et al. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 2008, 40, 1163-1165.
50. Ruemmele, F.M.; Muller, T.; Schiefermeier, N.; Ebner, H.L.; Lechner, S.; Pfaller, K.; Thoni, C.E.; Goulet, O.; Lacaille, F.; Schmitz, J.; et al. Loss-of-function of MYO5B is the main cause of microvillus inclusion disease: 15 novel mutations and a CaCo-2 RNAi cell model. Hum. Mutat. 2010, 31, 544-551.
51. Ameen, N.; Apodaca, G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 2007, 8, 998-1006.
52. Tyska, M.J.; Mackey, A.T.; Huang, J.D.; Copeland, N.G.; Jenkins, N.A.; Mooseker, M.S. Myosin-1a is critical for normal brush border structure and composition. Mol. Biol. Cell 2005, 16, 2443-2457.
53. Tyska, M.J.; Mooseker, M.S. A role for myosin-1A in the localization of a brush border disaccharidase. J. Cell Biol. 2004, 165, 395-405.
54. Buss, F.; Arden, S.D.; Lindsay, M.; Luzio, J.P.; Kendrick-Jones, J. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 2001, 20, 3676-3684.
55. Buss, F.; Luzio, J.P.; Kendrick-Jones, J. Myosin VI, a new force in clathrin mediated endocytosis. FEBS Lett. 2001, 508, 295-299.
56. Swiatecka-Urban, A.; Boyd, C.; Coutermarsh, B.; Karlson, K.H.; Barnaby, R.; Aschenbrenner, L.; Langford, G.M.; Hasson, T.; Stanton, B.A. Myosin VI regulates endocytosis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 2004, 279, 38025-38031.
57. Coluccio, L.M. Myosin I. In Myosins A Superfamily of Molecular Motors; Coluccio, L.M., Ed.; Springer: Dordrecht, The Netherlands, 1998; pp. 95-124.
58. Madden, D.R.; Swiatecka-Urban, A. Tissue-specific control of CFTR endocytosis by Dab2: Cargo recruitment as a therapeutic target. Commun. Integr. Biol. 2012, 5, 473-476.
59. Swiatecka-Urban, A.; Brown, A.; Moreau-Marquis, S.; Renuka, J.; Coutermarsh, B.; Barnaby, R.; Karlson, K.H.; Flotte, T.R.; Fukuda, M.; Langford, G.M.; et al. The short apical membrane half-life of rescued {Delta}F508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated endocytosis of {Delta}F508-CFTR in polarized human airway epithelial cells. J. Biol. Chem. 2005, 280, 36762-36772.
60. Tang, B.L.; Gee, H.Y.; Lee, M.G. The cystic fibrosis transmembrane conductance regulator's expanding SNARE interactome. Traffic 2011, 12, 364-371.
61. Kreda, S.M.; Mall, M.; Mengos, A.; Rochelle, L.; Yankaskas, J.; Riordan, J.R.; Boucher, R.C. Characterization of wild-type and deltaF508 cystic fibrosis transmembrane regulator in human respiratory epithelia. Mol. Biol. Cell 2005, 16, 2154-2167.
62. 2+, and transport of CFTR to the plasma membrane. J. Gen. Physiol. 2001, 118, 135-144.
63. Chang, S.Y.; Di, A.; Naren, A.P.; Palfrey, H.C.; Kirk, K.L.; Nelson, D.J. Mechanisms of CFTR regulation by syntaxin 1A and PKA. J. Cell Sci. 2002, 115, 783-791.