Reovirus preferentially infects the basolateral surface and is released from the apical surface of polarized human respiratory epithelial cells

Journal of Infectious Diseases

Volumn 197, Issue 8, 2008, Pages 1189-1197

  Excoffon, Katherine J D A ^a   Guglielmi, Kristen M ^b   Wetzel, J Denise ^b   Gansemer, Nicholas D ^a   Campbell, Jacquelyn A ^b   Dermody, Terence S ^b,d   Zabner, Joseph ^a,c  

^a UNIVERSITY OF IOWA   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; JUNCTIONAL ADHESION MOLECULE A; SIALIC ACID; SIALIDASE;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL CULTURE; CELL POLARITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REOVIRUS; RESPIRATORY EPITHELIUM; VIRUS ATTACHMENT; VIRUS INFECTION; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CELL ADHESION MOLECULES; CELL POLARITY; ELECTRIC IMPEDANCE; HUMANS; IMMUNOGLOBULINS; IMMUNOHISTOCHEMISTRY; L CELLS (CELL LINE); MICE; MICROSCOPY, CONFOCAL; NEURAMINIDASE; ORTHOREOVIRUS, MAMMALIAN; REASSORTANT VIRUSES; REOVIRIDAE INFECTIONS; RESPIRATORY MUCOSA; RESPIRATORY TRACT INFECTIONS; TIGHT JUNCTIONS; VIRUS SHEDDING;

EID: 42549140281     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/529515     Document Type: Article

References (50)

1. Vogelmann R, Amieva MR, Falkow S, Nelson WJ. Breaking into the epithelial apical-junctional complex - news from pathogen hackers. Curr Opin Cell Biol 2004; 16:86-93.
2. Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 2006; 169:1901-9.
3. Neutra MR, Mantis NJ, Kraehenbuhl JP. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat Immunol 2001; 2:1004-9.
4. Bienenstock J, McDermott MR. Bronchus- and nasal-associated lymphoid tissues. Immunol Rev 2005; 206:22-31.
5. Tyler KL. Mammalian reoviruses. In: Knipe DM, Howley PM, ed. Fields virology. 4th ed. Vol 2. Philadelphia: Lippincott Williams & Wilkins, 2001:1729-45.
6. Weiner HL, Drayna D, Averill DR Jr, Fields BN. Molecular basis of reovirus virulence: role of the S1 gene. Proc Natl Acad Sci USA 1977; 74:5744-8.
7. Weiner HL, Powers ML, Fields BN. Absolute linkage of virulence and central nervous system cell tropism of reoviruses to viral hemagglutinin. J Infect Dis 1980; 141:609-16.
8. Chappell JD, Prota AE, Dermody TS, Stehle T. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J 2002; 21:1-11.
9. Chappell JD, Duong JL, Wright BW, Dermody TS. Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J Virol 2000; 74:8472-9.
10. Gentsch JR, Pacitti AF. Differential interaction of reovirus type 3 with sialylated receptor components on animal cells. Virology 1987; 161:245-8.
11. Barton ES, Connolly JL, Forrest JC, Chappell JD, Dermody TS. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 2001; 276:2200-11.
12. Barton ES, Forrest JC, Connolly JL, et al. Junction adhesion molecule is a receptor for reovirus. Cell 2001; 104:441-51.
13. Schelling P, Guglielmi KM, Kirchner E, Paetzold B, Dermody TS, Stehle T. The reovirus σ-1 aspartic acid sandwich: a trimerization motif poised for conformational change. J Biol Chem 2007; 282:11582-9.
14. Chretien I, Marcuz A, Courtet M, et al. CTX, a Xenopus thymocyte receptor, defines a molecular family conserved throughout vertebrates. Eur J Immunol 1998; 28:4094-104.
15. Stehle T, Dermody TS. Structural similarities in the cellular receptors used by adenovirus and reovirus. Viral Immunol 2004; 17:129-43.
16. Mandell KJ, McCall IC, Parkos CA. Involvement of the junctional adhesion molecule-1 (JAM1) homodimer interface in regulation of epithelial barrier function. J Biol Chem 2004; 279:16254-62.
17. Liu Y, Nusrat A, Schnell FJ, et al. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 2000; 113(Pt 13):2363-74.
18. Martin-Padura I, Lostaglio S, Schneemann M, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142:117-27.
19. Makino A, Shimojima M, Miyazawa T, Kato K, Tohya Y, Akashi H. Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J Virol 2006; 80:4482-90.
20. Wolf JL, Rubin DH, Finberg R, et al. Intestinal M cells: a pathway for entry of reovirus into the host. Science 1981; 212:471-2.
21. Wolf JL, Kauffman RS, Finberg R, Dambrauskas R, Fields BN, Trier JS. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 1983; 85:291-300.
22. Helander A, Silvey KJ, Mantis NJ, et al. The viral σ1 protein and glycoconjugates containing α2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J Virol 2003; 77:7964-77.
23. Morin MJ, Warner A, Fields BN. A pathway for entry of retroviruses into the host through M cells of the respiratory tract. J Exp Med 1994; 180:1523-7.
24. Karp PH, Moninger T, Weber SP, et al. An in vitro model of differentiated human airway epithelia: methods and evaluation of primary cultures. In: Wise C, ed. Epithelial cell culture protocols. Vol 188. Totowa, NJ: Humana Press, 2002:115-37.
25. Virgin HW, Bassel-Duby R, Fields BN, Tyler KL. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol 1988; 62:4594-604.
26. Excoffon KJ, Traver GL, Zabner J. The role of the extracellular domain in the biology of the coxsackievirus and adenovirus receptor. Am J Respir Cell Mol Biol 2005; 32:498-503.
27. Walters RW, Yi SM, Keshavjee S, et al. Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem 2001; 276:20610-6.
28. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 2001; 154:491-7.
29. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA 2001; 98:15191-6.
30. Walters R, Freimuth P, Moninger T, Ganske I, Zabner J, Welsh M. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 2002; 110:789-99.
31. Walters RW, Grunst T, Bergelson JM, Finberg RW, Welsh MJ, Zabner J. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J Biol Chem 1999; 274:10219-26.
32. Zabner J, Chillon M, Grunst T, et al. A chimeric type 2 adenovirus vector with a type 17 fiber enhances gene transfer to human airway epithelia. J Virol 1999; 73:8689-95.
33. Walters RW, Pilewski JM, Chiorini JA, Zabner J. Secreted and transmembrane mucins inhibit gene transfer with AAV4 more efficiently than AAV5. J Biol Chem 2002; 277:23709-13.
34. Connolly JL, Barton ES, Dermody TS. Reovirus binding to cell surface sialic acid potentiates virus-induced apoptosis. J Virol 2001; 75:4029-39.
35. Weiner DB, Girard K, Williams WV, McPhillips T, Rubin DH. Reovirus type 1 and type 3 differ in their binding to isolated intestinal epithelial cells. Microb Pathog 1988; 5:29-40.
36. Ambler L, Mackay M. Reovirus 1 and 3 bind and internalise at the apical surface of intestinal epithelial cells. Virology 1991; 184:162-9.
37. Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS. Structurefunction analysis of reovirus binding to junctional adhesion molecule 1: implications for the mechanism of reovirus attachment. J Biol Chem 2003; 278:48434-44.
38. Gardet A, Breton M, Trugnan G, Chwetzoff S. Role for actin in the polarized release of rotavirus. J Virol 2007; 81:4892-4.
39. Ciarlet M, Crawford SE, Estes MK. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J Virol 2001; 75:11834-50.
40. Rosenblatt J, Raff MC, Cramer LP. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 2001; 11:1847-57.
41. Connolly JL, Rodgers SE, Clarke P, et al. Reovirus-induced apoptosis requires activation of transcription factor NF-κB. J Virol 2000; 74:2981-9.
42. O'Donnell SM, Hansberger MW, Connolly JL, et al. Organ-specific roles for transcription factor NF-κB in reovirus-induced apoptosis and disease. J Clin Invest 2005; 115:2341-50.
43. Hansberger MW, Campbell JA, Danthi P, et al. IκB kinase subunits α and γ are required for activation of NF-κB and induction of apoptosis by mammalian reovirus. J Virol 2007; 81:1360-71.
44. Tesfaigzi Y. Roles of apoptosis in airway epithelia. Am J Respir Cell Mol Biol 2006; 34:537-47.
45. Baranowski E, Ruiz-Jarabo CM, Domingo E. Evolution of cell recognition by viruses. Science 2001; 292:1102-5.
46. White JM, Littman DR. Viral receptors of the immunoglobulin superfamily. Cell 1989; 56:725-8.
47. Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997; 275:1320-3.
48. Greve JM, Davis G, Meyer AM, et al. The major human rhinovirus receptor is ICAM-1. Cell 1989; 56:839-47.
49. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 1989; 56:849-53.
50. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. Entry of α herpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 1998; 280:1618-20.