Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions

Cell

Volumn 124, Issue 1, 2006, Pages 119-131

  Coyne, Carolyn B ^a,b   Bergelson, Jeffrey M ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; CAVEOLIN; DECAY ACCELERATING FACTOR; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; VIRUS RNA;

ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COXSACKIE VIRUS; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; VIRUS ADSORPTION;

ADENOVIRIDAE; COXSACKIEVIRUS; MIRIDAE; RNA VIRUSES;

EID: 30344475861     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.10.035     Document Type: Article

References (55)

1. T. Aoki, R. Nomura, and T. Fujimoto Tyrosine phosphorylation of caveolin-1 in the endothelium Exp. Cell Res. 253 1999 629 636
2. E.S. Barton, J.C. Forrest, J.L. Connolly, J.D. Chappell, Y. Liu, F.J. Schnell, A. Nusrat, C.A. Parkos, and T.S. Dermody Junction adhesion molecule is a receptor for reovirus Cell 104 2001 441 451
3. A. Benmerah, C. Lamaze, B. Begue, S.L. Schmid, A. Dautry-Varsat, and N. Cerf-Bensussan AP-2/Eps15 interaction is required for receptor-mediated endocytosis J. Cell Biol. 140 1998 1055 1062
4. J.M. Bergelson Receptors for Coxsackieviruses and Echoviruses B.L. Semler E. Wimmer Molecular Biology of Picornaviruses 2002 ASM Press Washington, DC 107 113
5. J.M. Bergelson, J.A. Cunningham, G. Droguett, E.A. Kurt-Jones, A. Krithivas, J.S. Hong, M.S. Horwitz, R.L. Crowell, and R.W. Finberg Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5 Science 275 1997 1320 1323
6. B.B. Brasher, and R.A. Van Etten c-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the Src homology 3 domain and by autophosphorylation at two distinct regulatory tyrosines J. Biol. Chem. 275 2000 35631 35637
7. D.A. Brown, and E. London Functions of lipid rafts in biological membranes Annu. Rev. Cell Dev. Biol. 14 1998 111 136
8. Y. Chen, and L.C. Norkin Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae Exp. Cell Res. 246 1999 83 90
9. C.J. Cohen, J.T. Shieh, R.J. Pickles, T. Okegawa, J.T. Hsieh, and J.M. Bergelson The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction Proc. Natl. Acad. Sci. USA 98 2001 15191 15196
10. C.B. Coyne, and J.M. Bergelson CAR: a virus receptor within the tight junction Adv. Drug Deliv. Rev. 57 2005 869 882
11. C.B. Coyne, T. Voelker, S.L. Pichla, and J.M. Bergelson The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction J. Biol. Chem. 279 2004 48079 48084
12. H. Damke, T. Baba, D.E. Warnock, and S.L. Schmid Induction of mutant dynamin specifically blocks endocytic coated vesicle formation J. Cell Biol. 127 1994 915 934
13. R. Feuer, I. Mena, R. Pagarigan, M.K. Slifka, and J.L. Whitton Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro J. Virol. 76 2002 4430 4440
14. T. Friedrichson, and T.V. Kurzchalia Microdomains of GPI-anchored proteins in living cells revealed by crosslinking Nature 394 1998 802 805
15. Y. Gao, J.B. Dickerson, F. Guo, J. Zheng, and Y. Zheng Rational design and characterization of a Rac GTPase-specific small molecule inhibitor Proc. Natl. Acad. Sci. USA 101 2004 7618 7623
16. R.J. Geraghty, C. Krummenacher, G.H. Cohen, R.J. Eisenberg, and P.G. Spear Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor Science 280 1998 1618 1620
17. J.R. Glenney Jr. Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus J. Biol. Chem. 264 1989 20163 20166
18. J.H. Hanke, J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation J. Biol. Chem. 271 1996 695 701
19. J.R. Henley, E.W. Krueger, B.J. Oswald, and M.A. McNiven Dynamin-mediated internalization of caveolae J. Cell Biol. 141 1998 85 99
20. J.M. Hogle Poliovirus cell entry: common structural themes in viral cell entry pathways Annu. Rev. Microbiol. 56 2002 677 702
21. R.M. Horton, Z.L. Cai, S.N. Ho, and L.R. Pease Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction Biotechniques 8 1990 528 535
22. P. Liu, K. Aitken, Y.Y. Kong, M.A. Opavsky, T. Martino, F. Dawood, W.H. Wen, I. Kozieradzki, K. Bachmaier, and D. Straus The tyrosine kinase p56lck is essential in coxsackievirus B3-mediated heart disease Nat. Med. 6 2000 429 434
23. J.V. Melo The diversity of BCR-ABL fusion proteins and their relationship to leukemia phenotype Blood 88 1996 2375 2384
24. A.M. Milstone, J. Petrella, M.D. Sanchez, M. Mahmud, J.C. Whitbeck, and J.M. Bergelson Interaction with coxsackievirus and adenovirus receptor, but not with decay-accelerating factor (DAF), induces A particle formation in a DAF-binding coxsackievirus B3 isolate J. Virol. 79 2005 655 660
25. A. Nusrat, C.A. Parkos, P. Verkade, C.S. Foley, T.W. Liang, W. Innis-Whitehouse, K.K. Eastburn, and J.L. Madara Tight junctions are membrane microdomains J. Cell Sci. 113 2000 1771 1781
26. P. Oh, D.P. McIntosh, and J.E. Schnitzer Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium J. Cell Biol. 141 1998 101 114
27. P.A. Orlandi, and P.H. Fishman Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains J. Cell Biol. 141 1998 905 915
28. G.E. Palade An electron microscope study of the mitochondrial structure J. Histochem. Cytochem. 1 1953 188 211
29. M.A. Pallansch, and R.P. Roos Enteroviruses: Polioviruses, Coxsackieviruses, Echoviruses, and Newer Enteroviruses, 5 Edition 2001 Lippincott Williams & Wilkins Philadelphia
30. L. Pelkmans, and M. Zerial Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae Nature 436 2005 128 133
31. L. Pelkmans, J. Kartenbeck, and A. Helenius Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER Nat. Cell Biol. 3 2001 473 483
32. L. Pelkmans, D. Puntener, and A. Helenius Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae Science 296 2002 535 539
33. L. Pelkmans, E. Fava, H. Grabner, M. Hannus, B. Habermann, E. Krausz, and M. Zerial Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis Nature 436 2005 78 86
34. R.J. Pickles, D. McCarty, H. Matsui, P.J. Hart, S.H. Randell, and R.C. Boucher Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer J. Virol. 72 1998 6014 6023
35. K.J. Reagan, B. Goldberg, and R.L. Crowell Altered receptor specificity of coxsackievirus B3 after growth in rhabdomyosarcoma cells J. Virol. 49 1984 635 640
36. M.W. Renshaw, E. Lea-Chou, and J.Y. Wang Rac is required for v-Abl tyrosine kinase to activate mitogenesis Curr. Biol. 6 1996 76 83
37. R.R. Rueckert Picornaviridae: the viruses and their replication B.N. Fields D.M. Knipe P.M. Howley Fields Virology 1996 Lippincott-Raven Philadelphia 609 654
38. A.R. Sanguinetti, H. Cao, and C. Corley Mastick Fyn is required for oxidative- and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1 Biochem. J. 376 2003 159 168
39. M.D. Schaller, J.D. Hildebrand, and J.T. Parsons Complex formation with focal adhesion kinase: a mechanism to regulate activity and subcellular localization of Src kinases Mol. Biol. Cell 10 1999 3489 3505
40. T. Schindler, W. Bornmann, P. Pellicena, W.T. Miller, B. Clarkson, and J. Kuriyan Structural mechanism for STI-571 inhibition of abelson tyrosine kinase Science 289 2000 1938 1942
41. E.E. Schneeberger, and R.D. Lynch The tight junction: a multifunctional complex Am. J. Physiol. Cell Physiol. 286 2004 C1213 C1228
42. A.M. Shenoy-Scaria, J. Kwong, T. Fujita, M.W. Olszowy, A.S. Shaw, and D.M. Lublin Signal transduction through decay-accelerating factor. Interaction of glycosyl-phosphatidylinositol anchor and protein tyrosine kinases p56lck and p59fyn 1 J. Immunol. 149 1992 3535 3541
43. J.T. Shieh, and J.M. Bergelson Interaction with decay-accelerating factor facilitates coxsackievirus B infection of polarized epithelial cells J. Virol. 76 2002 9474 9480
44. T. Skorski, M. Nieborowska-Skorska, P. Wlodarski, M. Wasik, R. Trotta, P. Kanakaraj, P. Salomoni, M. Antonyak, R. Martinez, and M. Majewski The SH3 domain contributes to BCR/ABL-dependent leukemogenesis in vivo: role in adhesion, invasion, and homing Blood 91 1998 406 418
45. M.J. Stutts, R.C. Boucher, P.A. Bromberg, and J.T. Gatzy Effects of ammonium and nitrate salts on lon transport across the excised canine trachea Toxicol. Appl. Pharmacol. 60 1981 91 105
46. R.P. Tomko, R. Xu, and L. Philipson HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses Proc. Natl. Acad. Sci. USA 94 1997 3352 3356
47. M.T. Tosteson, and M. Chow Characterization of the ion channels formed by poliovirus in planar lipid membranes J. Virol. 71 1997 507 511
48. A.M. van der Bliek, T.E. Redelmeier, H. Damke, E.J. Tisdale, E.M. Meyerowitz, and S.L. Schmid Mutations in human dynamin block an intermediate stage in coated vesicle formation J. Cell Biol. 122 1993 553 563
49. D. Volonte, F. Galbiati, R.G. Pestell, and M.P. Lisanti Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress J. Biol. Chem. 276 2001 8094 8103
50. R.W. Walters, P. Freimuth, T.O. Moninger, I. Ganske, J. Zabner, and M.J. Welsh Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape Cell 110 2002 789 799
51. P.J. Woodring, T. Hunter, and J.Y. Wang Inhibition of c-Abl tyrosine kinase activity by filamentous actin J. Biol. Chem. 276 2001 27104 27110
52. P.J. Woodring, E.D. Litwack, D.D. O'Leary, G.R. Lucero, J.Y. Wang, and T. Hunter Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension J. Cell Biol. 156 2002 879 892
53. P.J. Woodring, T. Hunter, and J.Y. Wang Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases J. Cell Sci. 116 2003 2613 2626
54. E. Yamada The fine structure of the gall bladder epithelium of the mouse J. Biophys. Biochem. Cytol. 1 1955 445 458
55. K. Zen, Y. Liu, I.C. McCall, T. Wu, W. Lee, B.A. Babbin, A. Nusrat, and C.A. Parkos Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils Mol. Biol. Cell 16 2005 2694 2703