Junctional Adhesion Molecule-A Is Required for Hematogenous Dissemination of Reovirus

Cell Host and Microbe

Volumn 5, Issue 1, 2009, Pages 59-71

  Antar, Annukka A R ^a   Konopka, Jennifer L ^a   Campbell, Jacquelyn A ^a   Henry, Rachel A ^a   Perdigoto, Ana L ^a   Carter, Bruce D ^a   Pozzi, Ambra ^a,b   Abel, Ty W ^a   Dermody, Terence S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Veterans Affairs   (United States)

Author keywords

CELLBIO; MICROBIO

Indexed keywords

IMMUNOGLOBULIN; JUNCTIONAL ADHESION MOLECULE A; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; HISTOLOGY; INOCULATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REOVIRUS; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS REPLICATION; WILD TYPE;

ANIMALS; BODY WEIGHT; BRAIN; CELL ADHESION MOLECULES; ENDOTHELIAL CELLS; HEART; INTESTINES; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; RECEPTORS, VIRUS; REOVIRIDAE; REOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; VIRUS REPLICATION;

MAMMALIA; MUS; ORTHOREOVIRUS;

EID: 58249094521     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2008.12.001     Document Type: Article

References (59)

1. Barton E.S., Connolly J.L., Forrest J.C., Chappell J.D., and Dermody T.S. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J. Biol. Chem. 276 (2001) 2200-2211
2. Barton E.S., Forrest J.C., Connolly J.L., Chappell J.D., Liu Y., Schnell F., Nusrat A., Parkos C.A., and Dermody T.S. Junction adhesion molecule is a receptor for reovirus. Cell 104 (2001) 441-451
3. Barton E.S., Youree B.E., Ebert D.H., Forrest J.C., Connolly J.L., Valyi-Nagy T., Washington K., Wetzel J.D., and Dermody T.S. Utilization of sialic acid as a coreceptor is required for reovirus-induced biliary disease. J. Clin. Invest. 111 (2003) 1823-1833
4. Bass D.M., Trier J.S., Dambrauskas R., and Wolf J.L. Reovirus type 1 infection of small intestinal epithelium in suckling mice and its effect on M cells. Lab. Invest. 58 (1988) 226-235
5. Becker M.M., Peters T.R., and Dermody T.S. Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J. Virol. 77 (2003) 5948-5963
6. Bodkin D.K., and Fields B.N. Growth and survival of reovirus in intestinal tissue: role of the L2 and S1 genes. J. Virol. 63 (1989) 1188-1193
7. Campbell J.A., Shelling P., Wetzel J.D., Johnson E.M., Wilson G.A.R., Forrest J.C., Aurrand-Lions M., Imhof B., Stehle T., and Dermody T.S. Junctional adhesion molecule-A serves as a receptor for prototype and field-isolate strains of mammalian reovirus. J. Virol. 79 (2005) 7967-7978
8. Cera M.R., Del Prete A., Vecchi A., Corada M., Martin-Padura I., Motoike T., Tonetti P., Bazzoni G., Vermi W., Gentili F., et al. Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J. Clin. Invest. 114 (2004) 729-738
9. Chappell J.D., Barton E.S., Smith T.H., Baer G.S., Duong D.T., Nibert M.L., and Dermody T.S. Cleavage susceptibility of reovirus attachment protein σ1 during proteolytic disassembly of virions is determined by a sequence polymorphism in the σ1 neck. J. Virol. 72 (1998) 8205-8213
10. Chappell J.D., Duong J.L., Wright B.W., and Dermody T.S. Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J. Virol. 74 (2000) 8472-8479
11. Chappell J.D., Prota A., Dermody T.S., and Stehle T. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 21 (2002) 1-11
12. Cocchi F., Lopez M., Menotti L., Aoubala M., Dubreuil P., and Campadelli-Fiume G. The V domain of herpesvirus Ig-like receptor (HIgR) contains a major functional region in herpes simplex virus-1 entry into cells and interacts physically with the viral glycoprotein D. Proc. Natl. Acad. Sci. USA 95 (1998) 15700-15705
13. Dermody T.S., Nibert M.L., Bassel-Duby R., and Fields B.N. A sigma 1 region important for hemagglutination by serotype 3 reovirus strains. J. Virol. 64 (1990) 5173-5176
14. Di Pasquale G., and Chiorini J.A. AAV transcytosis through barrier epithelia and endothelium. Mol. Ther. 13 (2006) 506-516
15. Dichter M.A., and Weiner H.L. Infection of neuronal cell cultures with reovirus mimics in vitro patterns of neurotropism. Ann. Neurol. 16 (1984) 603-610
16. Excoffon K.J.D.A., Guglielmi K.M., Wetzel J.D., Gansemer N.D., Campbell J.A., Dermody T.S., and Zabner J. Reovirus preferentially infects the basolateral surface and is released from the apical surface of polarized human respiratory epithelial cells. J. Infect. Dis. 197 (2008) 1189-1197
17. Forrest J.C., Campbell J.A., Schelling P., Stehle T., and Dermody T.S. Structure-function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J. Biol. Chem. 278 (2003) 48434-48444
18. Fraser R.D.B., Furlong D.B., Trus B.L., Nibert M.L., Fields B.N., and Steven A.C. Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J. Virol. 64 (1990) 2990-3000
19. Furlong D.B., Nibert M.L., and Fields B.N. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62 (1988) 246-256
20. Geraghty R.J., Krummenacher C., Cohen G.H., Eisenberg R.J., and Spear P.G. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280 (1998) 1618-1620
21. Guglielmi K.M., Kirchner E., Holm G.H., Stehle T., and Dermody T.S. Reovirus binding determinants in junctional adhesion molecule-A. J. Biol. Chem. 282 (2007) 17930-17940
22. Gujuluva C., Burns A.R., Pushkarsky T., Popik W., Berger O., Bukrinsky M., Graves M.C., and Fiala M. HIV-1 penetrates coronary artery endothelial cells by transcytosis. Mol. Med. 7 (2001) 169-176
23. Haarr L., Shukla D., Rodahl E., Dal Canto M.C., and Spear P.G. Transcription from the gene encoding the herpesvirus entry receptor nectin-1 (HveC) in nervous tissue of adult mouse. Virology 287 (2001) 301-309
24. Kauffman R.S., Wolf J.L., Finberg R., Trier J.S., and Fields B.N. The σ1 protein determines the extent of spread of reovirus from the gastrointestinal tract of mice. Virology 124 (1983) 403-410
25. Kornecki E., Walkowiak B., Naik U.P., and Ehrlich Y.H. Activation of human platelets by a stimulatory monoclonal antibody. J. Biol. Chem. 265 (1990) 10042-10048
26. Laukoetter M.G., Nava P., Lee W.Y., Severson E.A., Capaldo C.T., Babbin B.A., Williams I.R., Koval M., Peatman E., Campbell J.A., et al. JAM-A regulates permeability and inflammation in the intestine in vivo. J. Exp. Med. 204 (2007) 3067-3076
27. Lee P.W.K., Hayes E.C., and Joklik W.K. Protein σ1 is the reovirus cell attachment protein. Virology 108 (1981) 156-163
28. Makino A., Shimojima M., Miyazawa T., Kato K., Tohya Y., and Akashi H. Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J. Virol. 80 (2006) 4482-4490
29. Mandell K.J., Babbin B.A., Nusrat A., and Parkos C.A. Junctional adhesion molecule-1 (JAM1) regulates epithelial cell morphology through effects on β1 integrins and Rap1 activity. J. Biol. Chem. 280 (2005) 11665-11674
30. Mann M.A., Knipe D.M., Fischbach G.D., and Fields B.N. Type 3 reovirus neuroinvasion after intramuscular inoculation: direct invasion of nerve terminals and age-dependent pathogenesis. Virology 303 (2002) 222-231
31. Martin-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., Panzeri C., Stoppacciaro A., Ruco L., Villa A., et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142 (1998) 117-127
32. Matoba Y., Sherry B., Fields B.N., and Smith T.W. Identification of the viral genes responsible for growth of strains of reovirus in cultured mouse heart cells. J. Clin. Invest. 87 (1991) 1628-1633
33. Matoba Y., Colucci W.S., Fields B.N., and Smith T.W. The reovirus M1 gene determines the relative capacity of growth of reovirus in cultured bovine aortic endothelial cells. J. Clin. Invest. 92 (1993) 2883-2888
34. Morrison L.A., Sidman R.L., and Fields B.N. Direct spread of reovirus from the intestinal lumen to the central nervous system through vagal autonomic nerve fibers. Proc. Natl. Acad. Sci. USA 88 (1991) 3852-3856
35. Nathanson N., and Tyler K.L. Entry, dissemination, shedding, and transmission of viruses. In: Nathanson N. (Ed). Viral Pathogenesis (1997), Lippincott-Raven, Philadelphia 13-33
36. Newberry R.D. Intestinal lymphoid tissues: is variety an asset or a liability?. Curr. Opin. Gastroenterol. 24 (2008) 121-128
37. Predescu S.A., Predescu D.N., and Malik A.B. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 293 (2007) L823-L842
38. Raine C.S., and Fields B.N. Reovirus type 3 encephalitis-a virologic and ultrastructural study. J. Neuropathol. Exp. Neurol. 32 (1973) 19-33
39. Richardson-Burns S.M., and Tyler K.L. Regional differences in viral growth and central nervous system injury correlate with apoptosis. J. Virol. 78 (2004) 5466-5475
40. Rubin D.H., and Fields B.N. Molecular basis of reovirus virulence: role of the M2 gene. J. Exp. Med. 152 (1980) 853-868
41. Rubin D.H., Kornstein M.J., and Anderson A.O. Reovirus serotype 1 intestinal infection: a novel replicative cycle with ileal disease. J. Virol. 53 (1985) 391-398
42. Sacher T., Podlech J., Mohr C.A., Jordan S., Ruzsics Z., Reddehase M.J., and Koszinowski U.H. The major virus-producing cell type during murine cytomegalovirus infection, the hepatocyte, is not the source of virus dissemination in the host. Cell Host Microbe 3 (2008) 263-272
43. Schiff L.A., Nibert M.L., and Tyler K.L. Orthoreoviruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology (2007), Lippincott Williams & Wilkins, Philadelphia 1853-1915
44. Stoeckel J., and Hay J.G. Drug evaluation: Reolysin-wild-type reovirus as a cancer therapeutic. Curr. Opin. Mol. Ther. 8 (2006) 249-260
45. Taylor J.M., Lin E., Susmarski N., Yoon M., Zago A., Ware C.F., Pfeffer K., Miyoshi J., Takai Y., and Spear P.G. Alternative entry receptors for herpes simplex virus and their roles in disease. Cell Host Microbe 2 (2007) 19-28
46. Tsukita S., Furuse M., and Itoh M. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2 (2001) 285-293
47. Tyler K.L., Bronson R.T., Byers K.B., and Fields B.N. Molecular basis of viral neurotropism: experimental reovirus infection. Neurology 35 (1985) 88-92
48. Tyler K.L., McPhee D.A., and Fields B.N. Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science 233 (1986) 770-774
49. Tyler K.L., Barton E.S., Ibach M.L., Robinson C., Valyi-Nagy T., Campbell J.A., Clarke P., O'Donnell S.M., Wetzel J.D., and Dermody T.S. Isolation and molecular characterization of a novel type 3 reovirus from a child with meningitis. J. Infect. Dis. 189 (2004) 1664-1675
50. Van Itallie C.M., and Anderson J.M. Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68 (2006) 403-429
51. Virgin IV H.W., Bassel-Duby R., Fields B.N., and Tyler K.L. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62 (1988) 4594-4604
52. Virgin H.W., Tyler K.L., and Dermody T.S. Reovirus. In: Nathanson N. (Ed). Viral Pathogenesis (1997), Lippincott-Raven, New York 669-699
53. Vogelmann R., Amieva M.R., Falkow S., and Nelson W.J. Breaking into the epithelial apical-junctional complex-news from pathogen hackers. Curr. Opin. Cell Biol. 16 (2004) 86-93
54. Walters R.W., Freimuth P., Moninger T.O., Ganske I., Zabner J., and Welsh M.J. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110 (2002) 789-799
55. Weber C., Fraemohs L., and Dejana E. The role of junctional adhesion molecules in vascular inflammation. Nat. Rev. Immunol. 7 (2007) 467-477
56. Weiner H.L., Ault K.A., and Fields B.N. Interaction of reovirus with cell surface receptors. I. Murine and human lymphocytes have a receptor for the hemagglutinin of reovirus type 3. J. Immunol. 124 (1980) 2143-2148
57. Weiner H.L., Powers M.L., and Fields B.N. Absolute linkage of virulence and central nervous system tropism of reoviruses to viral hemagglutinin. J. Infect. Dis. 141 (1980) 609-616
58. Wetzel J.D., Chappell J.D., Fogo A.B., and Dermody T.S. Efficiency of viral entry determines the capacity of murine erythroleukemia cells to support persistent infections by mammalian reoviruses. J. Virol. 71 (1997) 299-306
59. Wolf J.L., Rubin D.H., Finberg R., Kaufman R.S., Sharpe A.H., Trier J.S., and Fields B.N. Intestinal M cells: a pathway of entry of reovirus into the host. Science 212 (1981) 471-472