Lipid rafts mediate internalization of β1-integrin in migrating intestinal epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 5, 2008, Pages

  Vassilieva, Elena V ^a   Gerner Smidt, Kirsten ^a   Ivanov, Andrei I ^b   Nusrat, Asma ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Caveolin; Dynamin; Endocytosis; Flotillin; Mucosal restitution; Recycling

Indexed keywords

BETA1 INTEGRIN; CAVEOLIN 1; CHOLERA TOXIN; CLATHRIN; FLOTILLIN 1; FLOTILLIN 2; SMALL INTERFERING RNA;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; INTESTINE EPITHELIUM CELL; LIPID RAFT; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANTIGENS, CD29; CELL LINE, TUMOR; CELL MOVEMENT; CLATHRIN; DYNAMINS; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; INTESTINES; MEMBRANE MICRODOMAINS;

EID: 57349148152     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00082.2008     Document Type: Article

References (72)

1. Altankov G, Grinnell F. Depletion of intracellular potassium disrupts coated pits and reversibly inhibits cell polarization during fibroblast spreading. J Cell Biol 120: 1449-1459, 1993.
2. Altankov G, Grinnell F. Fibronectin receptor internalization and AP-2 complex reorganization in potassium-depleted fibroblasts. Exp Cell Res 216: 299-309, 1995.
3. Altschuler Y, Barbas SM, Terlecky LJ, Tang K, Hardy S, Mostov KE, Schmid SL. Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J Cell Biol 143: 1871-1881, 1998.
4. Boyd ND, Chan BM, Petersen NO. Beta1 integrins are distributed in adhesion structures with fibronectin and caveolin and in coated pits. Biochem Cell Biol 81: 335-348, 2003.
5. Bretscher MS. Circulating integrins: alpha 5 beta 1, alpha 6 beta 4 and Mac-1, but not alpha 3 beta 1, alpha 4 beta 1 or LFA-1. Embo J 11: 405-410, 1992.
6. Bretscher MS. Endocytosis and recycling of the fibronectin receptor in CHO cells. Embo J 8: 1341-1348, 1989.
7. Bruzzaniti A, Neff L, Sanjay A, Horne WC, De Camilli P, Baron R. Dynamin forms a Src kinase-sensitive complex with Cbl and regulates podosomes and osteoclast activity. Mol Biol Cell 16: 3301-3313, 2005.
8. Burridge K. Foot in mouth: do focal adhesions disassemble by endocytosis? Nat Cell Biol 7: 545-547, 2005.
9. Caswell PT, Norman JC. Integrin trafficking and the control of cell migration. Traffic 7: 14-21, 2006.
10. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 422: 37-44, 2003.
11. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934, 1994.
12. De Deyne PG, O'Neill A, Resneck WG, Dmytrenko GM, Pumplin DW, Bloch RJ. The vitronectin receptor associates with clathrin-coated membrane domains via the cytoplasmic domain of its beta5 subunit. J Cell Sci 111: 2729-2740, 1998.
13. Decker L, Baron W, Ffrench-Constant C. Lipid rafts: microenvironments for integrin-growth factor interactions in neural development. Biochem Soc Trans 32: 426-430, 2004.
14. Decker L, Ffrench-Constant C. Lipid rafts and integrin activation regulate oligodendrocyte survival. J Neurosci 24: 3816-3825, 2004.
15. Echarri A, Muriel O, Del Pozo MA. Intracellular trafficking of raft/caveolae domains: Insights from integrin signaling. Semin Cell Dev Biol 18: 627-637, 2007.
16. Ezratty EJ, Partridge MA, Gundersen GG. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7: 581-590, 2005.
17. Fenteany G, Janmey PA, Stossel TP. Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr Biol 10: 831-838, 2000.
18. Fernow I, Icking A, Tikkanen R. Reggie-1 and reggie-2 localize in non-caveolar rafts in epithelial cells: cellular localization is not dependent on the expression of caveolin proteins. Eur J Cell Biol 86: 345-352, 2007.
19. Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17: 1151-1156, 2007.
20. Gaus K, Le Lay S, Balasubramanian N, Schwartz MA. Integrin-mediated adhesion regulates membrane order. J Cell Biol 174: 725-734, 2006.
21. Gilcrease MZ. Integrin signaling in epithelial cells. Cancer Lett 247: 1-25, 2007.
22. Gonzalez E, Nagiel A, Lin AJ, Golan DE, Michel T. Small interfering RNA-mediated down-regulation of caveolin-1 differentially modulates signaling pathways in endothelial cells. J Biol Chem 279: 40659-40669, 2004.
23. Grose R, Hutter C, Bloch W, Thorey I, Watt FM, Fassler R, Brakebusch C, Werner S. A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129: 2303-2315, 2002.
24. Hinshaw JE. Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16: 483-519, 2000.
25. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687, 2002.
26. Imelli N, Meier O, Boucke K, Hemmi S, Greber UF. Cholesterol is required for endocytosis and endosomal escape of adenovirus type 2. J Virol 78: 3089-3098, 2004.
27. Irie T, Fukunaga K, Pitha J. Hydroxypropylcyclodextrins in parenteral use. I: Lipid dissolution and effects on lipid transfers in vitro. J Pharm Sci 81: 521-523, 1992.
28. Ivanov AI. Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol Biol 440: 15-33, 2008.
29. Ivanov AI, Bachar M, Babbin BA, Adelstein RS, Nusrat A, Parkos CA. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions (Abstract). PLoS ONE 2: e658, 2007.
30. Jones MC, Caswell PT, Norman JC. Endocytic recycling pathways: emerging regulators of cell migration. Curr Opin Cell Biol 18: 549-557, 2006.
31. Kilsdonk EP, Yancey PG, Stoudt GW, Bangerter FW, Johnson WJ, Phillips MC, Rothblat GH. Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 270: 17250-17256, 1995.
32. Kirkham M, Parton RG. Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 1746: 349-363, 2005.
33. Lajoie P, Nabi IR. Regulation of raft-dependent endocytosis. J Cell Mol Med 11: 644-653, 2007.
34. Laukaitis CM, Webb DJ, Donais K, Horwitz AF. Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J Cell Biol 153: 1427-1440, 2001.
35. Le Bivic A, Real FX, Rodriguez-Boulan E. Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc Natl Acad Sci USA 86: 9313-9317, 1989.
36. Le PU, Guay G, Altschuler Y, Nabi IR. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J Biol Chem 277: 3371-3379, 2002.
37. Li J, Peters PJ, Bai M, Dai J, Bos E, Kirchhausen T, Kandror KV, Hsu VW. An ACAP1-containing clathrin coat complex for endocytic recycling. J Cell Biol 178: 453-464, 2007.
38. Lotz MM, Nusrat A, Madara JL, Ezzell R, Wewer UM, Mercurio AM. Intestinal epithelial restitution. Involvement of specific laminin isoforms and integrin laminin receptors in wound closure of a transformed model epithelium. Am J Pathol 150: 747-760, 1997.
39. Lussier C, Basora N, Bouatrouss Y, Beaulieu JF. Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa. Microsc Res Tech 51: 169-178, 2000.
40. Marechal V, Prevost MC, Petit C, Perret E, Heard JM, Schwartz O. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J Virol 75: 11166-11177, 2001.
41. Mellgren RL. Detergent-resistant membrane subfractions containing proteins of plasma membrane, mitochondrial, and internal membrane origins. J Biochem Biophys Methods 70: 1029-1036, 2008.
42. Morgan MR, Humphries MJ, Bass MD. Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8: 957-969, 2007.
43. Mukoyama Y, Utani A, Matsui S, Zhou S, Miyachi Y, Matsuyoshi N. T-cadherin enhances cell-matrix adhesiveness by regulating beta1 integrin trafficking in cutaneous squamous carcinoma cells. Genes Cells 12: 787-796, 2007.
44. Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 161: 673-677, 2003.
45. Nakase I, Niwa M, Takeuchi T, Sonomura K, Kawabata N, Koike Y, Takehashi M, Tanaka S, Ueda K, Simpson JC, Jones AT, Sugiura Y, Futaki S. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther 10: 1011-1022, 2004.
46. Nakashima H, Hamamura K, Houjou T, Taguchi R, Yamamoto N, Mitsudo K, Tohnai I, Ueda M, Urano T, Furukawa K, Furukawa K. Overexpression of caveolin-1 in a human melanoma cell line results in dispersion of ganglioside GD3 from lipid rafts and alteration of leading edges, leading to attenuation of malignant properties. Cancer Sci 98: 512-520, 2007.
47. Ng T, Shima D, Squire A, Bastiaens PI, Gschmeissner S, Humphries MJ, Parker PJ. PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic. Embo J 18: 3909-3923, 1999.
48. Nishimura T, Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13: 15-28, 2007.
49. Panicker AK, Buhusi M, Erickson A, Maness PF. Endocytosis of beta1 integrins is an early event in migration promoted by the cell adhesion molecule L1. Exp Cell Res 312: 299-307, 2006.
50. Pankov R, Markovska T, Hazarosova R, Antonov P, Ivanova L, Momchilova A. Cholesterol distribution in plasma membranes of beta1 integrin-expressing and beta1 integrin-deficient fibroblasts. Arch Biochem Biophys 442: 160-168, 2005.
51. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 8: 185-194, 2007.
52. Partridge MA, Marcantonio EE. Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol Biol Cell 17: 4237-4248, 2006.
53. Pellinen T, Arjonen A, Vuoriluoto K, Kallio K, Fransen JA, Ivaska J. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J Cell Biol 173: 767-780, 2006.
54. Pietiainen V, Marjomaki V, Upla P, Pelkmans L, Helenius A, Hyypia T. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 15: 4911-4925, 2004.
55. Radel C, Carlile-Klusacek M, Rizzo V. Participation of caveolae in beta1 integrin-mediated mechanotransduction. Biochem Biophys Res Commun 358: 626-631, 2007.
56. Raub TJ, Kuentzel SL. Kinetic and morphological evidence for endocytosis of mammalian cell integrin receptors by using an anti-fibronectin receptor beta subunit monoclonal antibody. Exp Cell Res 184: 407-426, 1989.
57. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science 302: 1704-1709, 2003.
58. Runz S, Mierke CT, Joumaa S, Behrens J, Fabry B, Altevogt P. CD24 induces localization of beta1 integrin to lipid raft domains. Biochem Biophys Res Commun 365: 35-41, 2008.
59. Rutten MJ, Ito S. Morphology and electrophysiology of guinea pig gastric mucosal repair in vitro. Am J Physiol Gastrointest Liver Physiol 244: G171-G182, 1983.
60. Salanueva IJ, Cerezo A, Guadamillas MC, Del Pozo MA. Integrin regulation of caveolin function. J Cell Mol Med 11: 969-980, 2007.
61. Sharma DK, Brown JC, Cheng Z, Holicky EL, Marks DL, Pagano RE. The glycosphingolipid, lactosylceramide, regulates beta1-integrin clustering and endocytosis. Cancer Res 65: 8233-8241, 2005.
62. Smart EJ, Anderson RG. Alterations in membrane cholesterol that affect structure and function of caveolae. Methods Enzymol 353: 131-139, 2002.
63. Thorne RF, Marshall JF, Shafren DR, Gibson PG, Hart IR, Burns GF. The integrins alpha3beta1 and alpha6beta1 physically and functionally associate with CD36 in human melanoma cells. Requirement for the extracellular domain OF CD36. J Biol Chem 275: 35264-35275, 2000.
64. Tong Q, Vassilieva EV, Ivanov AI, Wang Z, Brown GT, Parkos CA, Nusrat A. Interferon-gamma inhibits T84 epithelial cell migration by redirecting transcytosis of beta1 integrin from the migrating leading edge. J Immunol 175: 4030-4038, 2005.
65. Upla P, Marjomaki V, Kankaanpaa P, Ivaska J, Hyypia T, Van Der Goot FG, Heino J. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol Biol Cell 15: 625-636, 2004.
66. von Delwig A, Bailey E, Gibbs DM, Robinson JH. The route of bacterial uptake by macrophages influences the repertoire of epitopes presented to CD4 T cells. Eur J Immunol 32: 3714-3719, 2002.
67. Wary KK, Mariotti A, Zurzolo C, Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634, 1998.
68. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 109: 2731-2739, 1989.
69. Wiseman PW, Brown CM, Webb DJ, Hebert B, Johnson NL, Squier JA, Ellisman MH, Horwitz AF. Spatial mapping of integrin interactions and dynamics during cell migration by image correlation microscopy. J Cell Sci 117: 5521-5534, 2004.
70. Yanagisawa M, Nakamura K, Taga T. Roles of lipid rafts in integrin-dependent adhesion and gp130 signalling pathway in mouse embryonic neural precursor cells. Genes Cells 9: 801-809, 2004.
71. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116: 4605-4613, 2003.
72. Zhang W, Razani B, Altschuler Y, Bouzahzah B, Mostov KE, Pestell RG, Lisanti MP. Caveolin-1 inhibits epidermal growth factor-stimulated lamellipod extension and cell migration in metastatic mammary adenocarcinoma cells (MTLn3). Transformation suppressor effects of adenovirus-mediated gene delivery of caveolin-1. J Biol Chem 275: 20717-20725, 2000.