Rat coronaviruses infect rat alveolar type I epithelial cells and induce expression of CXC chemokines

Virology

Volumn 369, Issue 2, 2007, Pages 288-298

  Miura, Tanya A ^a   Wang, Jieru ^b   Holmes, Kathryn V ^a   Mason, Robert J ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

Alveolar epithelium; Chemokine; CINC 2; CINC 3; IL 1 receptor antagonist; LIX; Neutrophil chemoattractant; Parker rat coronavirus; Sialodacryoadenitis virus

Indexed keywords

ALPHA CHEMOKINE; CHEMOATTRACTANT; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MESSENGER RNA; PROTEIN CINC 2; PROTEIN CINC 3; PROTEIN LIX; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CORONAVIRUS; GENE EXPRESSION; LUNG ALVEOLUS EPITHELIUM; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY TRACT INFLAMMATION; SIALODACRYOADENITIS VIRUS; ULTRAVIOLET IRRADIATION; VIRUS CELL INTERACTION; VIRUS STRAIN;

ANIMALS; CELLS, CULTURED; CHEMOKINES, CXC; CORONAVIRUS, RAT; EPITHELIAL CELLS; GENE EXPRESSION; INFLAMMATION MEDIATORS; PULMONARY ALVEOLI; RATS; RECEPTORS, INTERLEUKIN-1; RECEPTORS, TUMOR NECROSIS FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; VIRULENCE;

RAT CORONAVIRUS; RAT SIALODACRYOADENITIS CORONAVIRUS; RATTUS;

EID: 36048932017     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.07.030     Document Type: Article

References (80)

1. Abu-Harb M., Bell F., Finn A., Rao W.H., Nixon L., Shale D., and Everard M.L. IL-8 and neutrophil elastase levels in the respiratory tract of infants with RSV bronchiolitis. Eur. Respir. J. 14 1 (1999) 139-143
2. Auten Jr. R.L., Mason S.N., Tanaka D.T., Welty-Wolf K., and Whorton M.H. Anti-neutrophil chemokine preserves alveolar development in hyperoxia-exposed newborn rats. Am. J. Physiol.: Lung Cell. Mol. Physiol. 281 2 (2001) L336-L344
3. Bhatt P.N., and Jacoby R.O. Experimental infection of adult axenic rats with Parker's rat coronavirus. Arch. Virol. 54 4 (1977) 345-352
4. Bhatt P.N., Percy D.H., and Jonas A.M. Characterization of the virus of sialodacryoadenitis of rats: a member of the coronavirus group. J. Infect. Dis. 126 2 (1972) 123-130
5. Birch C.J., Clothier H.J., Seccull A., Tran T., Catton M.C., Lambert S.B., and Druce J.D. Human coronavirus OC43 causes influenza-like illness in residents and staff of aged-care facilities in Melbourne, Australia. Epidemiol. Infect. 133 2 (2005) 273-277
6. Borok Z., Hami A., Danto S.I., Zabski S.M., and Crandall E.D. Rat serum inhibits progression of alveolar epithelial cells toward the type I cell phenotype in vitro. Am. J. Respir. Cell Mol. Biol. 12 1 (1995) 50-55
7. Borok Z., Danto S.I., Lubman R.L., Cao Y., Williams M.C., and Crandall E.D. Modulation of t1alpha expression with alveolar epithelial cell phenotype in vitro. Am. J. Physiol. 275 1 Pt 1 (1998) L155-L164
8. Borok Z., Lubman R.L., Danto S.I., Zhang X.L., Zabski S.M., King L.S., Lee D.M., Agre P., and Crandall E.D. Keratinocyte growth factor modulates alveolar epithelial cell phenotype in vitro: expression of aquaporin 5. Am. J. Respir. Cell Mol. Biol. 18 4 (1998) 554-561
9. Chan M.C., Cheung C.Y., Chui W.H., Tsao S.W., Nicholls J.M., Chan Y.O., Chan R.W., Long H.T., Poon L.L., Guan Y., and Peiris J.S. Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir. Res. 6 (2005) 135
10. Chandrasekar B., Melby P.C., Sarau H.M., Raveendran M., Perla R.P., Marelli-Berg F.M., Dulin N.O., and Singh I.S. Chemokine-cytokine cross-talk. The ELR+ CXC chemokine LIX (CXCL5) amplifies a proinflammatory cytokine response via a phosphatidylinositol 3-kinase-NF-kappa B pathway. J. Biol. Chem. 278 7 (2003) 4675-4686
11. Chang Y.J., Liu C.Y., Chiang B.L., Chao Y.C., and Chen C.C. Induction of IL-8 release in lung cells via activator protein-1 by recombinant baculovirus displaying severe acute respiratory syndrome-coronavirus spike proteins: identification of two functional regions. J. Immunol. 173 12 (2004) 7602-7614
12. Compton S.R., Smith A.L., and Gaertner D.J. Comparison of the pathogenicity in rats of rat coronaviruses of different neutralization groups. Lab. Anim. Sci. 49 5 (1999) 514-518
13. Danto S.I., Shannon J.M., Borok Z., Zabski S.M., and Crandall E.D. Reversible transdifferentiation of alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 12 5 (1995) 497-502
14. De Albuquerque N., Baig E., Ma X., Zhang J., He W., Rowe A., Habal M., Liu M., Shalev I., Downey G.P., Gorczynski R., Butany J., Leibowitz J., Weiss S.R., McGilvray I.D., Phillips M.J., Fish E.N., and Levy G.A. Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J. Virol. 80 21 (2006) 10382-10394
15. Devalaraja R.M., Nanney L.B., Du J., Qian Q., Yu Y., Devalaraja M.N., and Richmond A. Delayed wound healing in CXCR2 knockout mice. J. Invest. Dermatol. 115 2 (2000) 234-244
16. Dinarello C.A. Biologic basis for interleukin-1 in disease. Blood 87 (1996) 2095-2147
17. Dinarello C.A. Differences between anti-tumor necrosis factor-a monoclonal antibodies and soluble TNF receptors in host defense impairment. J. Rheumatol. 32 (2005) 40-47
18. Dobbs L.G., and Mason R.J. Pulmonary alveolar type II cells isolated from rats. Release of phosphatidylcholine in response to beta-adrenergic stimulation. J. Clin. Invest. 63 3 (1979) 378-387
19. Dobbs L.G., Williams M.C., and Brandt A.E. Changes in biochemical characteristics and pattern of lectin binding of alveolar type II cells with time in culture. Biochim. Biophys. Acta 846 1 (1985) 155-166
20. Dobbs L.G., Williams M.C., and Gonzalez R. Monoclonal antibodies specific to apical surfaces of rat alveolar type I cells bind to surfaces of cultured, but not freshly isolated, type II cells. Biochim. Biophys. Acta 970 2 (1988) 146-156
21. Dunstan C.A., Salafranca M.N., Adhikari S., Xia Y., Feng L., and Harrison J.K. Identification of two rat genes orthologous to the human interleukin-8 receptors. J. Biol. Chem. 271 51 (1996) 32770-32776
22. Evans M.J., Cabral L.J., Stephens R.J., and Freeman G. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2. Exp. Mol. Pathol. 22 1 (1975) 142-150
23. Faisca P., and Desmecht D. Sendai virus, the mouse parainfluenza type 1: a longstanding pathogen that remains up-to-date. Res. Vet. Sci. 82 1 (2007) 115-125
24. Fouchier R.A., Hartwig N.G., Bestebroer T.M., Niemeyer B., de Jong J.C., Simon J.H., and Osterhaus A.D. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. U.S.A. 101 16 (2004) 6212-6216
25. Gagneten S., Scanga C.A., Dveksler G.S., Beauchemin N., Percy D., and Holmes K.V. Attachment glycoproteins and receptor specificity of rat coronaviruses. Lab. Anim. Sci. 46 2 (1996) 159-166
26. Gonzalez R., Yang Y.H., Griffin C., Allen L., Tigue Z., and Dobbs L. Freshly isolated rat alveolar type I cells, type II cells, and cultured type II cells have distinct molecular phenotypes. Am. J. Physiol.: Lung Cell. Mol. Physiol. 288 (2005) L179-L189
27. Haagmans B.L., Kuiken T., Martina B.E., Fouchier R.A., Rimmelzwaan G.F., van Amerongen G., van Riel D., de Jong T., Itamura S., Chan K.H., Tashiro M., and Osterhaus A.D. Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat. Med. 10 3 (2004) 290-293
28. Hewson C.A., Jardine A., Edwards M.R., Laza-Stanca V., and Johnston S.L. Toll-like receptor 3 is induced by and mediates antiviral activity against rhinovirus infection of human bronchial epithelial cells. J. Virol. 79 19 (2005) 12273-12279
29. Iacono K.T., Kazi L., and Weiss S.R. Both spike and background genes contribute to murine coronavirus neurovirulence. J. Virol. 80 14 (2006) 6834-6843
30. Imaizumi T., Hatakeyama M., Taima K., Ishikawa A., Yamashita K., Yoshida H., and Satoh K. Effect of double-stranded RNA on the expression of epithelial neutrophil activating peptide-78/CXCL-5 in human endothelial cells. Inflammation 28 4 (2004) 215-219
31. Jacoby R.O., Bhatt P.N., and Jonas A.M. Pathogenesis of sialodacryoadenitis in gnotobiotic rats. Vet. Pathol. 12 3 (1975) 196-209
32. Jeyaseelan S., Manzer R., Young S.K., Yamamoto M., Akira S., Mason R.J., and Worthen G.S. Induction of CXCL5 during inflammation in the rodent lung involves activation of alveolar epithelium. Am. J. Respir. Cell Mol. Biol. 32 6 (2005) 531-539
33. Kojima A., and Okaniwa A. Antigenic heterogeneity of sialodacryoadenitis virus isolates. J. Vet. Med. Sci. 53 6 (1991) 1059-1063
34. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., and Anderson L.J. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348 20 (2003) 1953-1966
35. Kuypers J., Martin E.T., Heugel J., Wright N., Morrow R., and Englund J.A. Clinical disease in children associated with newly described coronavirus subtypes. Pediatrics 119 1 (2007) e70-e76
36. Lane T.E., Asensio V.C., Yu N., Paoletti A.D., Campbell I.L., and Buchmeier M.J. Dynamic regulation of alpha- and beta-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J. Immunol. 160 2 (1998) 970-978
37. Law A.H., Lee D.C., Cheung B.K., Yim H.C., and Lau A.S. Role for nonstructural protein 1 of severe acute respiratory syndrome coronavirus in chemokine dysregulation. J. Virol. 81 1 (2007) 416-422
38. Londhe V.A., Belperio J.A., Keane M.P., Burdick M.D., Xue Y.Y., and Strieter R.M. CXCR2 is critical for dsRNA-induced lung injury: relevance to viral lung infection. J. Inflamm. (Lond.) 2 1 (2005) 4
39. Manzer R., Wang J., Nishina K., McConville G., and Mason R.J. Alveolar epithelial cells secrete chemokines in response to IL-1beta and lipopolysaccharide but not to ozone. Am. J. Respir. Cell Mol. Biol. 34 2 (2006) 158-166
40. Martin L.D., Rochelle L.G., Fischer B.M., Krunkosky T.M., and Adler K.B. Airway epithelium as an effector of inflammation: molecular regulation of secondary mediators. Eur. Respir. J. 10 9 (1997) 2139-2146
41. Mason R.J. Biology of alveolar type II cells. Respirology 11 (2006) S12-S15 (Suppl.)
42. Mason R.J., Lewis M.C., Edeen K.E., McCormick-Shannon K., Nielsen L.D., and Shannon J.M. Maintenance of surfactant protein A and D secretion by rat alveolar type II cells in vitro. Am. J. Physiol.: Lung Cell. Mol. Physiol. 282 2 (2002) L249-L258
43. McCray Jr. P.B., Pewe L., Wohlford-Lenane C., Hickey M., Manzel L., Shi L., Netland J., Jia H.P., Halabi C., Sigmund C.D., Meyerholz D.K., Kirby P., Look D.C., and Perlman S. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 81 2 (2007) 813-821
44. Melchjorsen J., Sorensen L.N., and Paludan S.R. Expression and function of chemokines during viral infections: from molecular mechanisms to in vivo function. J. Leukoc. Biol. 74 3 (2003) 331-343
45. Miller S.G., Carnell L., and Moore H.H. Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling. J. Cell Biol. 118 2 (1992) 267-283
46. Nagata N., Iwata N., Hasegawa H., Fukushi S., Yokoyama M., Harashima A., Sato Y., Saijo M., Morikawa S., and Sata T. Participation of both host and virus factors in induction of severe acute respiratory syndrome (SARS) in F344 rats infected with SARS coronavirus. J. Virol. 81 4 (2007) 1848-1857
47. Nishina K., Zhang F., Nielsen L.D., Edeen K., Wang J., and Mason R.J. Expression of CINC-2beta is related to the state of differentiation of alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 33 5 (2005) 505-512
48. Parker J.C., Cross S.S., and Rowe W.P. Rat coronavirus (RCV): a prevalent, naturally occurring pneumotropic virus of rats. Arch. Gesamte Virusforsch. 31 3 (1970) 293-302
49. Pene F., Merlat A., Vabret A., Rozenberg F., Buzyn A., Dreyfus F., Cariou A., Freymuth F., and Lebon P. Coronavirus 229E-related pneumonia in immunocompromised patients. Clin. Infect. Dis. 37 7 (2003) 929-932
50. Percy D.H., Williams K.L., and Paturzo F.X. A comparison of the sensitivity and specificity of sialodacryoadenitis virus, Parker's rat coronavirus, and mouse hepatitis virus-infected cells as a source of antigen for the detection of antibody to rat coronaviruses. Arch. Virol. 119 3-4 (1991) 175-180
51. Pyrc K., Berkhout B., and van der Hoek L. The novel human coronaviruses NL63 and HKU1. J. Virol. 81 7 (2007) 3051-3057
52. Roberts A., Paddock C., Vogel L., Butler E., Zaki S., and Subbarao K. Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J. Virol. 79 9 (2005) 5833-5838
53. Roberts A., Deming D., Paddock C.D., Cheng A., Yount B., Vogel L., Herman B.D., Sheahan T., Heise M., Genrich G.L., Zaki S.R., Baric R., and Subbarao K. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog. 3 1 (2007) e5
54. Rosenberg H.F., Bonville C.A., Easton A.J., and Domachowske J.B. The pneumonia virus of mice infection model for severe respiratory syncytial virus infection: identifying novel targets for therapeutic intervention. Pharmacol. Ther. 105 1 (2005) 1-6
55. Schmitz N., Kurrer M., Bachmann M.F., and Kopf M. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 79 10 (2005) 6641-6648
56. Schraufstatter I.U., Chung J., and Burger M. IL-8 activates endothelial cell CXCR1 and CXCR2 through Rho and Rac signaling pathways. Am. J. Physiol.: Lung Cell. Mol. Physiol. 280 6 (2001) L1094-L1103
57. Shibata F., Konishi K., Kato H., Komorita N., al-Mokdad M., Fujioka M., and Nakagawa H. Recombinant production and biological properties of rat cytokine-induced neutrophil chemoattractants, GRO/CINC-2 alpha, CINC-2 beta and CINC-3. Eur. J. Biochem. 231 2 (1995) 306-311
58. Shibata F., Konishi K., and Nakagawa H. Identification of a common receptor for three types of rat cytokine-induced neutrophil chemoattractants (CINCs). Cytokine 12 9 (2000) 1368-1373
59. Smith J.B., Wadleigh D.J., Xia Y.R., Mar R.A., Herschman H.R., and Lusis A.J. Cloning and genomic localization of the murine LPS-induced CXC chemokine (LIX) gene, Scyb5. Immunogenetics 54 8 (2002) 599-603
60. Starner T.D., Barker C.K., Jia H.P., Kang Y., and McCray Jr. P.B. CCL20 is an inducible product of human airway epithelia with innate immune properties. Am. J. Respir. Cell Mol. Biol. 29 5 (2003) 627-633
61. Stievano L., Piovan E., and Amadori A. C and CX3C chemokines: cell sources and physiopathological implications. Crit. Rev. Immunol. 24 3 (2004) 205-228
62. Sturman L.S., Holmes K.V., and Behnke J. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 33 1 (1980) 449-462
63. Tang N.L., Chan P.K., Wong C.K., To K.F., Wu A.K., Sung Y.M., Hui D.S., Sung J.J., and Lam C.W. Early enhanced expression of interferon-inducible protein-10 (CXCL-10) and other chemokines predicts adverse outcome in severe acute respiratory syndrome. Clin. Chem. 51 12 (2005) 2333-2340
64. Tirado R., Ortega A., Sarmiento R.E., and Gomez B. Interleukin-8 mRNA synthesis and protein secretion are continuously up-regulated by respiratory syncytial virus persistently infected cells. Cell. Immunol. 233 1 (2005) 61-71
65. Tseng C.T., Huang C., Newman P., Wang N., Narayanan K., Watts D.M., Makino S., Packard M.M., Zaki S.R., Chan T.S., and Peters C.J. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human Angiotensin-converting enzyme 2 virus receptor. J. Virol. 81 3 (2007) 1162-1173
66. Tsui P.T., Kwok M.L., Yuen H., and Lai S.T. Severe acute respiratory syndrome: clinical outcome and prognostic correlates. Emerg. Infect. Dis. 9 9 (2003) 1064-1069
67. Tumpey T.M., Garcia-Sastre A., Taubenberger J.K., Palese P., Swayne D.E., Pantin-Jackwood M.J., Schultz-Cherry S., Solorzano A., Van Rooijen N., Katz J.M., and Basler C.F. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J. Virol. 79 23 (2005) 14933-14944
68. Turner R.B. The role of neutrophils in the pathogenesis of rhinovirus infections. Pediatr. Infect. Dis. J. 9 11 (1990) 832-835
69. Vanderbilt J.N., Mager E.M., Allen L., Sawa T., Wiener-Kronish J., Gonzalez R., and Dobbs L.G. CXC chemokines and their receptors are expressed in type II cells and upregulated following lung injury. Am. J. Respir. Cell Mol. Biol. 29 6 (2003) 661-668
70. van der Hoek L., Pyrc K., Jebbink M.F., Vermeulen-Oost W., Berkhout R.J., Wolthers K.C., Wertheim-van Dillen P.M., Kaandorp J., Spaargaren J., and Berkhout B. Identification of a new human coronavirus. Nat. Med. 10 4 (2004) 368-373
71. Wang S.Z., Xu H., Wraith A., Bowden J.J., Alpers J.H., and Forsyth K.D. Neutrophils induce damage to respiratory epithelial cells infected with respiratory syncytial virus. Eur. Respir. J. 12 3 (1998) 612-618
72. Wang J., Wang S., Manzer R., McConville G., and Mason R.J. Ozone induces oxidative stress in rat alveolar type II and type I-like cells. Free Radical Biol. Med. 40 11 (2006) 1914-1928
73. Weiss S.R., and Navas-Martin S. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev. 69 4 (2005) 635-664
74. Williams M.C. Alveolar type I cells: molecular phenotype and development. Annu. Rev. Physiol. 65 (2003) 669-695
75. Wojcinski Z.W., and Percy D.H. Sialodacryoadenitis virus-associated lesions in the lower respiratory tract of rats. Vet. Pathol. 23 3 (1986) 278-286
76. Woo P.C., Lau S.K., Chu C.M., Chan K.H., Tsoi H.W., Huang Y., Wong B.H., Poon R.W., Cai J.J., Luk W.K., Poon L.L., Wong S.S., Guan Y., Peiris J.S., and Yuen K.Y. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79 2 (2005) 884-895
77. Yen Y.T., Liao F., Hsiao C.H., Kao C.L., Chen Y.C., and Wu-Hsieh B.A. Modeling the early events of severe acute respiratory syndrome coronavirus infection in vitro. J. Virol. 80 6 (2006) 2684-2693
78. Zhang Y., Luxon B.A., Casola A., Garofalo R.P., Jamaluddin M., and Brasier A.R. Expression of respiratory syncytial virus-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J. Virol. 75 19 (2001) 9044-9058
79. Zhou J., Stohlman S.A., Hinton D.R., and Marten N.W. Neutrophils promote mononuclear cell infiltration during viral-induced encephalitis. J. Immunol. 170 6 (2003) 3331-3336
80. Zhu Z., Tang W., Gwaltney Jr. J.M., Wu Y., and Elias J.A. Rhinovirus stimulation of interleukin-8 in vivo and in vitro: role of NF-kappaB. Am. J. Physiol. 273 4 Pt 1 (1997) L814-L824