Myosin Ia is Required for CFTR Brush Border Membrane Trafficking and Ion Transport in the Mouse Small Intestine

Traffic

Volumn 13, Issue 8, 2012, Pages 1072-1082

  Kravtsov, Dmitri V ^a   Caputo, Christina ^a   Collaco, Anne ^a   Hoekstra, Nadia ^a   Egan, Marie E ^a   Mooseker, Mark S ^a   Ameen, Nadia A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brush border; CFTR; Intestine; Myosin Ia; Traffic; Villus

Indexed keywords

CYCLIC AMP; MYOSIN VI; SUCRASE ISOMALTASE; SYNTAXIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL EXPERIMENT; ARTICLE; BRUSH BORDER; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; IMMUNOPRECIPITATION; INTESTINE CELL; INTESTINE VILLUS; ION TRANSPORT; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE; WILD TYPE;

ANIMALS; CACO-2 CELLS; CHLORIDES; COLON; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ELECTRIC STIMULATION; ENDOCYTOSIS; ENTEROCYTES; EXOCYTOSIS; HUMANS; INTESTINE, SMALL; ION TRANSPORT; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROVILLI; MYOSIN HEAVY CHAINS; ORGAN SPECIFICITY; TRANSPORT VESICLES;

EID: 84863865683     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2012.01368.x     Document Type: Article

References (55)

1. Coluccio LM, Myosin I. In: Coluccio LM, editor. Myosins A Superfamily of Molecular Motors. Dordrecht: Springer; 1998, pp. 95-124.
2. Tyska MJ, Mooseker MS. A role for myosin-1A in the localization of a brush border disaccharidase. J Cell Biol 2004;165:395-405.
3. Tyska MJ, Mackey AT, Huang JD, Copeland NG, Jenkins NA, Mooseker MS. Myosin-1a is critical for normal brush border structure and composition. Mol Biol Cell 2005;16:2443-2457.
4. McConnell RE, Tyska MJ. Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J Cell Biol 2007;177:671-681.
5. McConnell RE, Higginbotham JN, Shifrin DA Jr, Tabb DL, Coffey RJ, Tyska MJ. The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 2009;185:1285-1298.
6. Buss F, Spudich G, Kendrick-Jones J. Myosin VI: cellular functions and motor properties. Annu Rev Cell Dev Biol 2004;20:649-676.
7. Krendel M, Osterweil EK, Mooseker M. Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 2007;581:644-650.
8. Nambiar R, McConnell RE, Tyska MJ. Control of cell membrane tension by myosin-I. Proc Natl Acad Sci USA 2009;106:11972-11977.
9. Fath KR, Burgess DR. Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J Cell Biol 1993;120:117-127.
10. Ameen N, Apodaca G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 2007;8:998-1006.
11. Hegan PS, Giral H, Levi M, Mooseker MS. Myosin VI is required for maintenance of brush border structure, composition, and membrane trafficking functions in the intestinal epithelial cell. Cytoskeleton 2012;69:235-251.
12. 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.
13. 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 2009;20:2337-2350.
14. Golin-Bisello F, Bradbury NA, Ameen NA. Heat Stable Enterotoxin (STa) and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G. Am J Physiol Cell Physiol 2005;289:C708-C716.
15. O'Loughlin EV, Hunt DM, Gaskin KJ, Steil D, Bruzuszcak IM, Martin HCO, 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.
16. Pratha VS, Hogan DL, Martensson BA, Bernard J, Zhou R, Isenberg JI. Identification of transport abnormalities in duodenal mucosa and duodenal enterocytes from patients with cystic fibrosis. Gastroenterology 2000;118:1051-1060.
17. Gabriel SE, Brigman KN, Koller BV, Boucher RC, Stutts MJ. Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 1994;266:107-109.
18. Park R, Grand R. Gastrointestinal manifestations of cystic fibrosis: a review. Gastroenterology 1981;81:1143-1161.
19. Field M, Semrad CE. Toxigenic diarrheas, congenital diarrheas and cystic fibrosis: disorders of intestinal ion transport. Annu Rev Physiol 1993;55:631-655.
20. 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.
21. Heintzelman MB, Mooseker MS. Assembly of the brush border cytoskeleton: changes in the distribution of microvillar core proteins during enterocyte differentiation in adult chicken intestine. Cell Motil Cytoskeleton 1990;15:12-22.
22. Skowron JF, Mooseker MS. Cloning and characterization of mouse brush border myosin-I in adult and embryonic intestine. J Exp Zool 1999;283:242-257.
23. Jakab RL, Collaco AM, Ameen NA. 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.
24. Wang Z, Petrovic S, Mann E, Soleimani M. Identification of an apical Cl(-)/HCO3(-) exchanger in the small intestine. Am J Physiol Gastrointest Liver Physiol 2002;282:G573-G579.
25. Singh AK, Sjoblom M, Zheng W, Krabbenhoft A, Riederer B, Rausch B, Manns MP, Soleimani M, Seidler U. CFTR and its key role in in vivo resting and luminal acid-induced duodenal HCO3-secretion. Acta Physiol (Oxf) 2008;193:357-365.
26. Singh AK, Riederer B, Chen M, Xiao F, Krabbenhoft A, Engelhardt R, Nylander O, Soleimani M, Seidler U. The switch of intestinal Slc26 exchangers from anion absorptive to HCOFormula secretory mode is dependent on CFTR anion channel function. Am J Physiol Cell Physiol 2010;298:C1057-C1065.
27. Lalles JP. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 2010;68:323-332.
28. Finn AL, Kuzhikandathil EV, Oxford GS, Itoh-Lindstrom Y. Sucrase-isomaltase is an adenosine 3', 5'-cyclic monophosphate-dependent epithelial chloride channel. Gastroenterology 2001;120:117-125.
29. Barrett KE, Kelly S. Integrative physiology and pathophysiology of intestinal electrolyte transport, 4th edn. In: Johnson LR, editor. Physiology of the Gastrointestinal Tract. New York: Elsevier; 2006. p. 1931-1951.
30. Benesh AE, Nambiar R, McConnell RE, Mao S, Tabb DL, Tyska MJ. Differential localization and dynamics of class I myosins in the enterocyte microvillus. Mol Biol Cell 2010;21:970-978.
31. Mooseker MS, Pollard TD, Fujiwara K. Characterization and localization of myosin in the brush border of intestinal epithelial cells. J Cell Biol 1978;79:444-453.
32. Heintzelman MB, Hasson T, Mooseker MS. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J Cell Sci 1994;107:3535-3543.
33. Bement WM, Hasson T, Wirth JA, Cheney RE, Mooseker MS. Identification and overlapping expression of multiple unconventional myosin genes in vertebrate cell types. Proc Natl Acad Sci USA 1994;91:6549-6553.
34. Wolfrum U, Liu X, Schmitt A, Udovichenko IP, Williams DS. Myosin VIIa as a common component of cilia and microvilli. Cell Motil Cytoskeleton 1998;40:261-271.
35. Chen ZY, Hasson T, Zhang DS, Schwender BJ, Derfler BH, Mooseker MS, Corey DP. Myosin-VIIb, a novel unconventional myosin, is a constituent of microvilli in transporting epithelia. Genomics 2001;72:285-296.
36. Muller T, Hess MW, Schiefermeier N, Pfaller K, Ebner HL, Heinz-Erian P, Ponstingl H, Partsch J, Rollinghoff B, Kohler H, Berger T, Lenhartz H, Schlenck B, Houwen RJ, Taylor CJ, et al. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat Genet 2008;40:1163-1165.
37. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111-136.
38. Dudez T, Borot F, Huang S, Kwak BR, Bacchetta M, Ollero M, Stanton BA, Chanson M. CFTR in a lipid raft-TNFR1 complex modulates gap junctional intercellular communication and IL-8 secretion. Biochim Biophys Acta 2008;1783:779-788.
39. Spudich G, Chibalina MV, Au JS, Arden SD, Buss F, Kendrick-Jones J. Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns(4, 5)P2. Nat Cell Biol 2007;9:176-183.
40. Collaco A, Jakab R, Hegan P, Mooseker M, Ameen N. Alpha-AP-2 directs myosin VI-dependent endocytosis of cystic fibrosis transmembrane conductance regulator chloride channels in the intestine. J Biol Chem 2010;285:17177-17187.
41. Self T, Sobe T, Copeland NG, Jenkins NA, Avraham KB, Steel KP. Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol 1999;214:331-341.
42. Mooseker MS. Brush border motility. Microvillar contraction in triton-treated brush borders isolated from intestinal epithelium. J Cell Biol 1976;71:417-433.
43. Bretscher A, Weber K. Tropomyosin from bovine brain contains two polypeptide chains of slightly different molecular weights. FEBS Lett 1978;85:145-148.
44. Tang N, Ostap EM. Motor domain-dependent localization of myo1b (myr-1). Curr Biol 2001;11:1131-1135.
45. Fanning AS, Wolenski JS, Mooseker MS, Izant JG. Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil Cytoskeleton 1994;29:29-45.
46. Hirokawa N, Keller TC 3rd, Chasan R, Mooseker MS. Mechanism of brush border contractility studied by the quick-freeze, deep-etch method. J Cell Biol 1983;96:1325-1336.
47. Mooseker MS, Bonder EM, Conzelman KA, Fishkind DJ, Howe CL, Keller TC 3rd. Brush border cytoskeleton and integration of cellular functions. J Cell Biol 1984;99:104s-112s.
48. De La Cruz EM, Ostap EM, Sweeney HL. Kinetic mechanism and regulation of myosin VI. J Biol Chem 2001;276:32373-32381.
49. Jontes JD, Milligan RA, Pollard TD, Ostap EM. Kinetic characterization of brush border myosin-I ATPase. Proc Natl Acad Sci USA 1997;94:14332-14337.
50. Hagen SJ, Allan CH, Trier JS. Demonstration of microtubules in the terminal web of mature absorptive cells from the small intestine of the rat. Cell Tissue Res 1987;248:709-711.
51. Skowron JF, Bement WM, Mooseker MS. Human brush border myosin-I and myosin-Ic expression in human intestine and Caco-2BBe cells. Cell Motil Cytoskeleton 1998;41:308-324.
52. Kirkeby S, Thomsen CE. Quantitative immunohistochemistry of fluorescence labelled probes using low-cost software. J Immunol Methods 2005;301:102-113.
53. Grubb BR. Bioelectric measurement of CFTR function in mice. Methods Mol Med 2002;70:525-535.
54. Weiner SA, Caputo C, Bruscia E, Ferreira EC, Price JE, Krause DS, Egan ME. Rectal potential difference and the functional expression of CFTR in the gastrointestinal epithelia in cystic fibrosis mouse models. Pediatr Res 2008;63:73-78.
55. Bruscia EM, Price JE, Cheng EC, Weiner S, Caputo C, Ferreira EC, Egan ME, Krause DS. Assessment of cystic fibrosis transmembrane conductance regulator (CFTR) activity in CFTR-null mice after bone marrow transplantation. Proc Natl Acad Sci USA 2006;103:2965-2970.