Regulation of polymeric immunoglobulin receptor expression by reovirus

Journal of General Virology

Volumn 86, Issue 8, 2005, Pages 2347-2357

  Pal, Kasturi ^a   Kaetzel, Charlotte S ^b   Brundage, Kathleen ^a   Cunningham, Cynthia A ^a   Cuff, Christopher F ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; ANTISERUM; BAFILOMYCIN A1; CALPASTATIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN RECEPTOR; VIRUS ANTIBODY;

ACIDIFICATION; ANALYSIS OF VARIANCE; ARTICLE; CELL STRAIN HT29; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INCUBATION TIME; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RECEPTOR UPREGULATION; REOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; TRANSCYTOSIS; VIRUS INACTIVATION; VIRUS INFECTION; VIRUS REPLICATION;

CALPAIN; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; INTESTINAL MUCOSA; LEUPEPTINS; MAMMALIAN ORTHOREOVIRUS 3; RECEPTORS, POLYMERIC IMMUNOGLOBULIN; ULTRAVIOLET RAYS; UP-REGULATION;

REOVIRUS SP.;

EID: 21244458166     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80690-0     Document Type: Article

References (93)

1. Ackermann, L. W. & Denning, G. M. (2004). Nuclear factor-κB contributes to interleukin-4- and interferon-dependent polymeric immunoglobulin receptor expression in human intestinal epithelial cells. Immunology 111, 75-85.
2. Ackermann, L. W., Wollenweber, L. A. & Denning, G. M. (1999). IL-4 and IFN-γ increase steady state levels of polymeric Ig receptor mRNA in human airway and intestinal epithelial cells. J Immunol 162, 5112-5118.
3. Andrejeva, J., Childs, K. S., Young, D. F., Carlos, T. S., Stock, N., Goodbourn, S. & Randall, R. E. (2004). The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc Natl Acad Sci U S A 101, 17264-17269.
4. Barton, E. S., Connolly, J. L., Forrest, J. C., Chappell, J. D. & Dermody, T. S. (2001a). Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 276, 2200-2211.
5. Barton, E. S., Forrest, J. C., Connolly, J. L., Chappell, J. D., Liu, Y., Schnell, F. J., Nusrat, A., Parkos, C. A. & Dermody, T. S. (2001b). Junction adhesion molecule is a receptor for reovirus. Cell 104, 441-451.
6. Blanch, V. J., Piskurich, J. F. & Kaetzel, C. S. (1999). Cutting edge: coordinate regulation of IFN regulatory factor-1 and the polymeric Ig receptor by proinflammatory cytokines. J Immunol 162, 1232-1235.
7. Borsa, J., Morash, B. D., Sargent, M. D., Copps, T. P., Lievaart, P. A. & Szekely, J. G. (1979). Two modes of entry of reovirus particles into L cells. J Gen Virol 45, 161-170.
8. Borsa, J., Sargent, M. D., Lievaart, P. A. & Copps, T. P. (1981). Reovirus: evidence for a second step in the intracellular uncoating and transcriptase activation process. Virology 111, 191-200.
9. Bowman, E. J., Siebers, A. & Altendorf, K. (1988). Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85, 7972-7976.
10. Brandtzaeg, P. (1978). Polymeric IgA is complexed with secretory component (SC) on the surface of human intestinal epithelial cells. Scand J Immunol 8, 39-52.
11. Brandtzaeg, P. (1985). Role of J chain and secretory component in receptor-mediated glandular and hepatic transport of immunoglobulins in man. Scand J Immunol 22, 111-146.
12. Brandtzaeg, P., Berstad, A. E., Farstad, I. N. & 7 other authors (1997). Mucosal immunity - a major adaptive defence mechanism. Behring Inst Mitt 98, 1-23.
13. Branski, D., Lebenthal, E., Faden, H., Hatch, T. F. & Krasner, J. (1980). Small intestinal epithelial brush border enzymatic changes in suckling mice infected with reovirus type 3. Pediatr Res 14, 803-805.
14. Canning, W. M. & Fields, B. N. (1983). Ammonium chloride prevents lytic growth of reovirus and helps to establish persistent infection in mouse L cells. Science 219, 987-988.
15. Cario, E. & Podolsky, D. K. (2000). Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68, 7010-7017.
16. Chappell, J. D., Gunn, V. L., Wetzel, J. D., Baer, G. S. & Dermody, T. S. (1997). Mutations in type 3 reovirus that determine binding to sialic acid are contained in the fibrous tail domain of viral attachment protein σ1. J Virol 71, 1834-1841.
17. Chappell, J. D., Duong, J. L., Wright, B. W. & Dermody, T. S. (2000). Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J Virol 74, 8472-8479.
18. Chen, F., Lu, Y., Kuhn, D. C., Maki, M., Shi, X., Sun, S. C. & Demers, L. M. (1997). Calpain contributes to silica-induced IκB-α degradation and nuclear factor-κB activation. Arch Biochem Biophys 342, 383-388.
19. Chintalacharuvu, K. R., Piskurich, J. F., Lamm, M. E. & Kaetzel, C. S. (1991). Cell polarity regulates the release of secretory component, the epithelial receptor for polymeric immunoglobulins, from the surface of HT-29 colon carcinoma cells. J Cell Physiol 148, 35-47.
20. Clarke, P., Meintzer, S. M., Widmann, C., Johnson, G. L. & Tyler, K. L. (2001). Reovirus infection activates JNK and the JNK-dependent transcription factor c-Jun. J Virol 75, 11275-11283.
21. Coffey, M. C., Strong, J. E., Forsyth, P. A. & Lee, P. W. (1998). Reovirus therapy of tumors with activated Ras pathway. Science 282, 1332-1334.
22. Connolly, J. L. & Dermody, T. S. (2002). Virion disassembly is required for apoptosis induced by reovirus. J Virol 76, 1632-1641.
23. Connolly, J. L., Rodgers, S. E., Clarke, P., Ballard, D. W., Kerr, L. D., Tyler, K. L. & Dermody, T. S. (2000). Reovirus-induced apoptosis requires activation of transcription factor NF-κB. J Virol 74, 2981-2989.
24. Connolly, J. L., Barton, E. S. & Dermody, T. S. (2001). Reovirus binding to cell surface sialic acid potentiates virus-induced apoptosis. J Virol 75, 4029-4039.
25. Croall, D. E. & DeMartino, G. N. (1991). Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol Rev 71, 813-847.
26. Cuff, C. F., Lavi, E., Cebra, C. K., Cebra, J. J. & Rubin, D. H. (1990). Passive immunity to fatal reovirus serotype 3-induced meningoencephalitis mediated by both secretory and transplacental factors in neonatal mice. J Virol 64, 1256-1263.
27. Cuff, C. F., Cebra, C. K., Rubin, D. H. & Cebra, J. J. (1993). Developmental relationship between cytotoxic alpha/beta T cell receptor-positive intraepithelial lymphocytes and Peyer's patch lymphocytes. Eur J Immunol 23, 1333-1339.
28. DeBiasi, R. L., Squier, M. K. T., Pike, B., Wynes, M., Dermody, T. S., Cohen, J. J. & Tyler, K. L. (1999). Reovirus-induced apoptosis is preceded by increased cellular calpain activity and is blocked by calpain inhibitors. J Virol 73, 695-701.
29. DeBiasi, R. L., Edelstein, C. L., Sherry, B. & Tyler, K. L. (2001). Calpain inhibition protects against virus-induced apoptotic myocardial injury. J Virol 75, 351-361.
30. Denning, G. M. (1996). IL-4 and IFN-γ synergistically increase total polymeric IgA receptor levels in human intestinal epithelial cells. Role of protein tyrosine kinases. J Immunol 156, 4807-4814.
31. Diebold, S. S., Kaisho, T., Hemmi, H., Akira, S. & Reis e Sousa, C. (2004). Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531.
32. Elewaut, D., DiDonato, J. A., Kim, J. M., Truong, F., Eckmann, L. & Kagnoff, M. F. (1999). NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol 163, 1457-1466.
33. Ensminger, W. D. & Tamm, I. (1969). Cellular DNA and protein synthesis in reovirus-infected L cells. Virology 39, 357-360.
34. Fan, J.-Y., Boyce, C. S. & Cuff, C. F. (1998). T-helper 1 and T-helper 2 cytokine responses in gut-associated lymphoid tissue following enteric reovirus infection. Cell Immunol 188, 55-63.
35. Farone, A. L., O'Brien, P. C. & Cox, D. C. (1993). Tumor necrosis factor-α induction by reovirus serotype 3. J Leukoc Biol 53, 133-137.
36. Forrest, J. C., Campbell, J. A., Schelling, P., Stehle, T. & Dermody, T. S. (2003). Structure-function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J Biol Chem 278, 48434-48444.
37. Fulton, J. R., Smith, J., Cunningham, C. & Cuff, C. F. (2004). Influence of the route of infection on development of T-cell receptor β-chain repertoires of reovirus-specific cytotoxic T lymphocytes. J Virol 78, 1582-1590.
38. Funami, K., Matsumoto, M., Oshiumi, H., Akazawa, T., Yamamoto, A. & Seya, T. (2004). The cytoplasmic 'linker region' in toll-like receptor 3 controls receptor localization and signaling. Int Immunol 16, 1143-1154.
39. Hacker, H., Mischak, H., Miethke, T., Liptay, S., Schmid, R., Sparwasser, T., Heeg, K., Lipford, G. B. & Wagner, H. (1998). CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J 17, 6230-6240.
40. Hamamdzic, D., Phillips-Dorsett, T., Altman-Hamamdzic, S., London, S. D. & London, L. (2001). Reovirus triggers cell type-specific proinflammatory responses dependent on the autocrine action of IFN-β. Am J Physiol Lung Cell Mol Physiol 280, L18-L29.
41. Hell, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H. & Bauer, S. (2004). Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526-1529.
42. Helander, A., Silvey, K. J., Mantis, N. J., Hutchings, A. B., Chandran, K., Lucas, W. T., Nibert, M. L. & Neutra, M. R. (2003). 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 77, 7964-7977.
43. Hooper, L. V., Wong, M. H., Thelin, A., Hansson, L., Falk, P. G. & Gordon, J. I. (2001). Molecular analysis of commensal host-microbial relationships in the intestine. Science 291, 881-884.
44. Kamal, A., Ying, Y. & Anderson, R. G. (1998). Annexin VI-mediated loss of spectrin during coated pit budding is coupled to delivery of LDL to lysosomes. J Cell Biol 142, 937-947.
45. Kang, D. C., Gopalkrishnan, R. V., Wu, O., Jankowsky, E., Pyle, A. M. & Fisher, P. B. (2002). mda-5: an interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci U S A 99, 637-642.
46. Kato, H., Kato, R., Fujihashi, K. & McGhee, J. R. (2001). Role of mucosal antibodies in viral infections. Curr Top Microbiol Immunol 260, 201-228.
47. Kauffman, R. S., Wolf, J. L., Finberg, R., Trier, J. S. & Fields, B. N. (1983). The σ1 protein determines the extent of spread of reovirus from the gastrointestinal tract of mice. Virology 124, 403-410.
48. Kobayashi, K. (1971). Studies on human secretory IgA: comparative studies of the IgA-bound secretory piece and the free secretory piece protein. Immunochemistry 8, 785-800.
49. Kudo, H. & Graham, A. F. (1966). Selective inhibition of reovirus induced RNA in L cells. Biochem Biophys Res Commun 24, 150-155.
50. Labrada, L., Bodelon, G., Vinuela, J. & Benavente, J. (2002). Avian reoviruses cause apoptosis in cultured cells: viral uncoating, but not viral gene expression, is required for apoptosis induction. J Virol 76, 7932-7941.
51. Lamm, M. E. (1997). Interaction of antigens and antibodies at mucosal surfaces. Annu Rev Microbiol 51, 311-340.
52. Li, K., Chen, Z., Kato, N., Gale, M., Jr & Lemon, S. M. (2005). Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-β production in hepatocytes. J Biol Chem 280, 16739-16747.
53. Liu, Z.-Q., Kunimatsu, M., Yang, J.-P., Ozaki, Y., Sasaki, M. & Okamoto, T. (1996). Proteolytic processing of nuclear factor κB by calpain in vitro. FEBS Lett 385, 109-113.
54. London, S. D., Rubin, D. H. & Cebra, J. J. (1987). Gut mucosal immunization with reovirus serotype 1/L stimulates virus-specific cytotoxic T cell precursors as well as IgA memory cells in Peyer's patches. J Exp Med 165, 830-847.
55. London, S. D., Cebra, J. J. & Rubin, D. H. (1989). The reovirus-specific cytotoxic T cell response is not restricted to serotypically unique epitopes associated with the virus hemagglutinin. Microb Pathog 6, 43-50.
56. London, S. D., Cebra-Thomas, J. A., Rubin, D. H. & Cebra, J. J. (1990). CD8 lymphocyte subpopulations in Peyer's patches induced by reovirus serotype 1 infection. J Immunol 144, 3187-3194.
57. Major, A. S., Rubin, D. H. & Cuff, C. F. (1998). Mucosal immunity to reovirus infection. Curr Top Microbiol Immunol 233, 163-177.
58. Martínez, C. G., Guinea, R., Benavente, J. & Carrasco, L. (1996). The entry of reovirus into L cells is dependent on vacuolar proton-ATPase activity. J Virol 70, 576-579.
59. Mathers, A. R. & Cuff, C. F. (2004). Role of interleukin-4 (IL-4) and IL-10 in serum immunoglobulin G antibody responses following mucosal or systemic reovirus infection. J Virol 78, 3352-3360.
60. Matsumoto, M., Funami, K., Tanabe, M., Oshiumi, H., Shingai, M., Seto, Y., Yamamoto, A. & Seya, T. (2003). Subcellular localization of Toll-like receptor 3 in human dendritic cells. J Immunol 171, 3154-3162.
61. Morin, M. J., Warner, A. & Fields, B. N. (1994). A pathway for entry of retroviruses into the host through M cells of the respiratory tract. J Exp Med 180, 1523-1527.
62. Morin, M. J., Warner, A. & Fields, B. N. (1996). Reovirus infection in rat lungs as a model to study the pathogenesis of viral pneumonia. J Virol 70, 541-548.
63. Mostov, K. E. & Deitcher, D. L. (1986). Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell 46, 613-621.
64. Murachi, T. (1989). Intracellular regulatory system involving calpain and calpastatin. Biochem Int 18, 263-294.
65. Musil, L. S. & Baenziger, J. U. (1987). Cleavage of membrane secretory component to soluble secretory component occurs on the cell surface of rat hepatocyte monolayers. J Cell Biol 104, 1725-1733.
66. Norderhaug, I. N., Johansen, F. E., Schjerven, H. & Brandtzaeg, P. (1999). Regulation of the formation and external transport of secretory immunoglobulins. Crit Rev Immunol 19, 481-508.
67. Organ, E. L. & Rubin, D. H. (1998). Pathogenesis of reovirus gastrointestinal and hepatobiliary disease. Curr Top Microbiol Immunol 233, 67-83.
68. Prota, A. E., Campbell, J. A., Schelling, P. & 7 other authors (2003). Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc Natl Acad Sci U S A 100, 5366-5371.
69. Rincheval-Arnold, A., Belair, L., Cencic, A. & Djiane, J. (2002a). Up-regulation of polymeric immunoglobulin receptor mRNA in mammary epithelial cells by IFN-γ. Mol Cell Endocrinol 194, 95-105.
70. Rincheval-Arnold, A., Belair, L. & Djiane, J. (2002b). Developmental expression of pIgR gene in sheep mammary gland and hormonal regulation. J Dairy Res 69, 13-26.
71. Rubin, D., Weiner, H. L., Fields, B. N. & Greene, M. I. (1981). Immunologic tolerance after oral administration of reovirus: requirement for two viral gene products for tolerance induction. J Immunol 127, 1697-1701.
72. Rubin, D. H., Kornstein, M. J. & Anderson, A. O. (1985). Reovirus serotype 1 intestinal infection: a novel replicative cycle with ileal disease. J Virol 53, 391-398.
73. Rubin, D. H., Weiner, D. B., Dworkin, C., Greene, M. I., Maul, G. G. & Williams, W. V. (1992). Receptor utilization by reovirus type 3: distinct binding sites on thymoma and fibroblast cell lines result in differential compartmentalization of virions. Microb Pathog 12, 351-365.
74. Schjerven, H., Brandtzaeg, P. & Johansen, F. E. (2000). Mechanism of IL-4-mediated up-regulation of the polymeric Ig receptor: role of STAT6 in cell type-specific delayed transcriptional response. J Immunol 165, 3898-3906.
75. Schjerven, H., Brandtzaeg, P. & Johansen, F. E. (2001). A novel NF-κB/Rel site in intron 1 cooperates with proximal promoter elements to mediate TNF-α-induced transcription of the human polymeric Ig receptor. J Immunol 167, 6412-6420.
76. Sharpe, A. H. & Fields, B. N. (1981). Reovirus inhibition of cellular DNA synthesis: role of the S1 gene. J Virol 38, 389-392.
77. Sharpe, A. H. & Fields, B. N. (1982). Reovirus inhibition of cellular RNA and protein synthesis: role of the S4 gene. Virology 122, 381-391.
78. Smith, R. E., Zweerink, H. J. & Joklik, W. K. (1969). Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39, 791-810.
79. Song, W., Vaerman, J. P. & Mostov, K. E. (1995). Dimeric and tetrameric IgA are transcytosed equally by the polymeric Ig receptor. J Immunol 155, 715-721.
80. Strong, J. E., Coffey, M. C., Tang, D., Sabinin, P. & Lee, P. W. (1998). The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 17, 3351-3362.
81. Sturzenbecker, L. J., Nibert, M., Furlong, D. & Fields, B. N. (1987). Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J Virol 61, 2351-2361.
82. Sumpter, R., Jr, Loo, Y. M., Foy, E., Li, K., Yoneyama, M., Fujita, T., Lemon, S. M. & Gale, M., Jr (2005). Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79, 2689-2699.
83. Tamer, C. M., Lamm, M. E., Robinson, J. K., Piskurich, J. F. & Kaetzel, C. S. (1995). Comparative studies of transcytosis and assembly of secretory IgA in Madin-Darby canine kidney cells expressing human polymeric Ig receptor. J Immunol 155, 707-714.
84. Tyler, K. L., Squier, M. K. T., Rodgers, S. E., Schneider, B. E., Oberhaus, S. M., Grdina, T. A., Cohen, J. J. & Dermody, T. S. (1995). Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein σ1. J Virol 69, 6972-6979.
85. Wang, K. K. & Yuen, P. W. (1994). Calpain inhibition: an overview of its therapeutic potential. Trends Pharmacol Sci 15, 412-419.
86. Weiner, H. L. & Fields, B. N. (1977). Neutralization of reovirus: the gene responsible for the neutralization antigen. J Exp Med 146, 1305-1310.
87. Weltzin, R., Lucia-Jandris, P., Michetti, P., Fields, B. N., Kraehenbuhl, J. P. & Neutra, M. R. (1989). Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J Cell Biol 108, 1673-1685.
88. Wolf, J. L., Rubin, D. H., Finberg, R., Kauffman, R. S., Sharpe, A. H., Trier, J. S. & Fields, B. N. (1981). Intestinal M cells: a pathway for entry of reovirus into the host. Science 212, 471-472.
89. Wolf, J. L., Kauffman, R. S., Finberg, R., Dambrauskas, R., Fields, B. N. & Trier, J. S. (1983). Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 85, 291-300.
90. Wolf, J. L., Dambrauskas, R., Sharpe, A. H. & Trier, J. S. (1987). Adherence to and penetration of the intestinal epithelium by reovirus type 1 in neonatal mice. Gastroenterology 92, 82-91.
91. +-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 266, 17707-17712.
92. Youngman, K. R., Fiocchi, C. & Kaetzel, C. S. (1994). Inhibition of IFN-γ activity in supernatants from stimulated human intestinal mononuclear cells prevents up-regulation of the polymeric Ig receptor in an intestinal epithelial cell line. J Immunol 153, 675-681.
93. Zweerink, H. J. & Joklik, W. K. (1970). Studies on the intracellular synthesis of reovirus-specified proteins. Virology 41, 501-518.