Primary infection of mice with high titer inoculum respiratory syncytial virus: Characterization and response to antiviral therapy

Canadian Journal of Physiology and Pharmacology

Volumn 83, Issue 2, 2005, Pages 198-213

  Bolger, Gordon ^a   Lapeyre, Nicole ^a   Dansereau, Nathalie ^a   Lagacé, Lisette ^a   Berry, Gerald ^b   Klosowski, Katy ^a   Mewhort, Tracy ^a   Liuzzi, Michel ^a  

^a BOEHRINGER INGELHEIM CANADA LTD   (Canada)

^b ST MARY S HOSPITAL   (Canada)

Author keywords

Antiviral therapy; Disease; Mortality; Respiratory syncytial virus

Indexed keywords

ANTIVIRUS AGENT; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PALIVIZUMAB; PROTEIN; RANTES; RIBAVIRIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY PLETHYSMOGRAPHY; CONTROLLED STUDY; DOSE RESPONSE; DRUG RESPONSE; FATALITY; FEMALE; HISTOPATHOLOGY; INFECTION PREVENTION; INFLAMMATORY DISEASE; INOCULATION; INTERSTITIAL PNEUMONIA; LUNG FUNCTION TEST; LUNG LAVAGE; MORTALITY; MOUSE; NONHUMAN; PRIMARY INFECTION; PRIORITY JOURNAL; RESPIRATORY FUNCTION DISORDER; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RNA VIRUS INFECTION; SINGLE DRUG DOSE; VASCULITIS; VIRAL BRONCHIOLITIS; VIRUS PLAQUE; VIRUS PNEUMONIA; VIRUS REPLICATION; VIRUS TITRATION; WEIGHT REDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIVIRAL AGENTS; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; LUNG; MICE; MICE, INBRED BALB C; RESPIRATORY FUNCTION TESTS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; RIBAVIRIN; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 18844365071     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/y05-007     Document Type: Article

References (74)

1. Aherne, W., Bird, T., Court, S.D.M., Gardner, P.S., and McQuillin, J. 1970. Pathological changes in virus infections of the lower respiratory tract in children. J. Clin. Pathol. 23: 7-18.
2. Becker, S., Soukup, J., and Yankaskas, J.R. 1992. Respiratory syncytial virus infection of human primary nasal and bronchial epithelial cell cultures and bronchoalveolar macrophages. Am. J. Respir. Cell Mol. Biol. 6: 369-374.
3. Biber, J.L., Jabbour, S., Parihar, R., Dierksheide, J., Hu, Y., Baumann, H. et al. 2002. Administration of two macrophage-derived interferon-gamma- inducing factors (IL-12 and IL-15) induces a lethal systemic inflammatory response in mice that is dependent on natural killer cells but does not require interferon-gamma. Cell. Immunol. 216: 31-42.
4. Blanco, J.C.G., Richardson, J.Y., Darnell, M.E.R., Rowzee, A., Pletneva, L., Porter, D.D., and Prince, G.A. 2002. Cytokine and chemokine gene expression after primary and secondary respiratory syncytial virus infection in cotton rats. J. Infect. Dis. 185: 1780-1785.
5. Boelen, A., Kwakkel, J., Barends, M., de Bond, L., Dormans, J., and Kimman, T. 2002. Effect of lack of interleukin-4, interleukin-12, interleukin-18, or the interferon-γ receptor on virus replication, cytokine response, and lung pathology during respiratory syncytial virus infection in mice. J. Med. Virol. 66: 552-560.
6. Bont, L., and Kimpen, J.L.L. 2002. Immunological mechanisms of severe respiratory syncytial virus bronchiolitis. Intensive Care Med. 28: 616-621.
7. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-253.
8. Brandenburg, A.H., Kleinjan, A, van Het Land, B., Moll, H.A., Timmerman, H.H., de Swart, R.L. et al. 2000. Type 1-like immune response is found in children with respiratory syncytial virus infection regardless of clinical severity. J. Med. Virol. 62: 267-277.
9. Bustamante-Cavillo, M.E., Velázquez, F.R., Cabrera-Munoz, L., Torres, J., Gomez-Delgado, A., Moreno, J.A.E., and Munoz-Hernandez, M. 2001. Molecular detection of respiratory syncytial virus in postmortem lung tissue samples from Mexican children deceased with pneumonia. Pediatr. Infect. Dis. J. 20: 495-501.
10. Collins, P.L., McIntosh, K., and Chanock R.M. 1996. Respiratory syncytial virus. In Fields Virology. Edited by B.N. Fields, D.M. Knipe, P.M. Howley, R.M. Chanock, J.L. Melnick, T.P. Monath, B. Roizman, and S.E. Straus. 3rd ed. Raven Publishers, Philidelphia, Pa. pp. 1313-1351.
11. Cook, P.M., Englin, R.P., and Easton, A.J. 1998. Pathogenesis of pneumovirus infections in mice: detection of pneumonia virus of mice and human respiratory syncytial virus mRNA in lungs of infected mice by in situ hybridization. J. Gen. Virol. 79: 2411-2417.
12. Crowe, J.E., Firestone, C.-Y., and Murphy, B.R. 2001. Passively acquired antibodies suppress humoral but not cell-mediated immunity in mice immunize with live attenuated respiratory syncytial virus vaccines. J. Immunol. 167: 3910-3918.
13. DeVincenzo, J.P. 2000. Therapy of respiratory syncytial virus infection. Pediatr. Infect. Dis. J. 19: 786-790.
14. Domachowske, J.B., Bonville, C.A., Gao, J.-L., Murphy, P.M., Easton, A.J., and Rosenburg, H.F. 2000. MIP-1α is produced but it does not control pulmonary inflammation in response to respiratory syncytial virus infection in mice. Cell. Immunol. 206: 1-6.
15. Downham, M.A.P.S., Gardner, P.S., McQuillan, J., and Ferris, J.A.J. 1975. Role of respiratory viruses in childhood mortality. Br. Med. J. 1: 235-239.
16. Edell, E.D., Khoshoo, V., Ross, G., and Salter, K. 2002. Early RBV treatment of bronchiolitis. Effect on long-term respiratory morbidity. Chest, 122: 935-939.
17. Englund, J.A., Pledra, P.A., Ahn, Y.-M., Gilbert, B.E., and Hiatt, P. 1994. High-dose, short duration therapy compared with standard RBV therapy in children with suspected respiratory syncytial virus infection. J. Pediatr. 425: 635-641.
18. Enhorning, G., van Schaik, S., Lundgren, C, and Vargas, I. 1998. Whole-body plethysmography, does it measure tidal volume of small animals? Can. J. Physiol. Pharmacol. 76: 945-951.
19. Fischer, J.E., Johnson, J.E., Kuli-Zade, R.K., Johnson, T.R., Aung, S., Parker, R.A., and Graham, B.S. 1997. Overexpression of interleukin-4 delays virus clearance in mice infected with respiratory syncytial virus. J. Virol. 71: 8672-8677.
20. Garofalo, R.P., Patti, J., Hintz, K.A., Hill, V., Ogra, P.L., and Welliver, R.C. 2002. Macrophage inflammatory protein-1α (not T helper type 2 cytokines) is associated with severe forms of respiratory syncytial virus bronchiolitis. J. Infec. Dis. 184: 393-399.
21. Gilbert, B.E., Wyde, P.R., Ambrose, M.W., Wilson, S.Z., and Knight, V. 1992. Further studies with short duration RBV aerosol for the treatment of influenza virus infection in mice and respiratory syncytial virus infection in cotton rats. Antivir. Res. 17: 33-42.
22. Goetsch, L., Plotnicky-Gilquin, H., Aubry, J.P, De-Lys, P., Haeuw, J.G., Bonnefoy, J.Y. et al. 2001. BBG2NA an RSV subunit vaccine candidate intramuscularly injected to human confers protection against viral challenge after nasal immunization in mice. Vaccine, 19: 4036-4042.
23. Graham, B.S., Perkins, M.D., Wright, P.F., and Karzon, D.T. 1988. Primary respiratory syncytial virus infection in mice J. Med. Virol. 26: 153-162.
24. Graham, B.S., Henderson, G.S., Tang, Y.-T., Lu, X., Neuzil, K.M., and Colley D.G. 1993. Priming immunization determines T-helper cytokine mRNA expression patterns in lungs of mice challenged with respiratory syncytial virus. J. Immunol. 151: 2032-2040.
25. Graham, B.S., Johnson, T.R., and Peebles, R.S. 2000. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology, 48: 237-247.
26. Groothuis, J.R., Woodin, K.A., Katz, R., Robertson, A.D., McBride, J.T., Hall, C.B., et al. 1990. Early RBV treatment of respiratory syncytial viral infection in high-risk children. J. Pediatr. 117: 792-798.
27. Haeberle, H.A., Kuziel, W.A., Dieterich, H.-J., Casola, A., Gatalica, Z., and Garofalo, R.P. 2001. Inducible expression of inflammatory chemokines in respiratory syncytial virus-infected mice: Role of MIP-1α in lung pathology. J. Virol. 75: 878-890.
28. Haeberle, H.A., Takizawz, R., Casola, A., Brasier, A.R., Dieterich, H.-J., van Rooijen, N. et al. 2002. Respiratory syncytial virus-induced activation of nuclear factor-κB in the lung involves alveolar macrophages and tool-like receptor 4-dependent pathways. J. Infect. Dis. 186: 1199-1206.
29. Hail, C.B. 1999. Respiratory syncytial virus: a continuing culprit and conundrum. J. Pediatr. 135: 2-7.
30. Hall, C.B., McBride, J.T., Walsh, E.E., Bell, D.M., Gala, C.L., Hildreth, S. et al. 1983. Aerosolized RBV treatment of infants with respiratory syncytial viral infection. N. Engl. J. Med. 308: 1443-1447.
31. Haraguchi, S., Day, N.K., Nelson, R.P., Emmanuel, P., Duplantier, J.E., Christodoulou, C.S., and Good, R.A. 1998. Interleukin 12 deficiency associated with recurrent infections. Proc. Natl. Acad. Sci. USA, 95: 13 125 - 13 129.
32. Harrington, R.D., Hooton, T.M., Hackman, R.C., Storch, G.A., Osborne, R., Gleaves, C.A. et al. 1992. An outbreak of respiratory syncytial virus in a bone marrow transplant center. J. Infect. Dis. 165: 987-993.
33. Harrison, A.M., Bonville, C.A., Rosenberg, H.F., and Domachowske, J.B. 1999. Respiratory syncytial virus-induced chemokine expression in the lower airways. Am. J. Respir. Crit. Care Med. 159: 1918-1924.
34. Hayes, P.J., Scott, R., and Wheeler, J. 1994. In vivo production of tumor necrosis factor-α and interleukin-6 in BALB/c mice inoculated intranasally with high a high dose of respiratory syncytial virus. J. Med. Virol. 42: 325-329.
35. Haynes, L.M., Tonkin, J., Anderson, L.J., and Tripp, R.A. 2002. Neutralizing anti-F glycoprotein and anti-substance P antibody treatment effectively reduces infection and inflammation associated with respiratory syncytial virus infection. J. Virol. 76: 6873-6881.
36. Hertz, M.I., Englund, J.A., Snover, D., Bitterman, P.B., and McGlave, P.B. 1989. Respiratory syncytial virus-induced acute lung injury in adult patients with bone marrow transplants: a clinical approach and review of the literature. Medicine (Baltim.), 68: 269-281.
37. Hornsleth, A., Loland, L., and Larsen, L.B. 2001. Cytokines and chemokines in respiratory secretion and severity of disease in infants with respiratory syncytial virus (RSV) infection. J. Clin. Virol. 21: 163-170.
38. Hultgren, C., Milich, D.R., Weiland, O., and Sallberg, M. 1998. The antiviral compound RBV modulates the T helper (Th)1/Th2 subset balance in hepatitis B and C virus-specific immune responses. J. Gen. Virol. 79: 2381-2391.
39. Hussell, T., Pennycook, A., and Openshaw, J.M. 2001. Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur. J. Immunol 31: 2566-2573.
40. Jafri, H. 2002. Role of chemokines in respiratory syncytial virus disease. Pediatr. Infect. Dis. J. 21: 454-460.
41. Johnson, S., Oliver, C., Prince, G.A., Hemming, V.G., Pfarr, D.S., Wang, S.-C. et al. 1997. Development of a humanized monoclonal antibody (MEDI-493) with a potent in vitro and in vivo activity against respiratory syncytial virus. J. Infect. Dis. 176: 1215-1224.
42. Kakuk, T.J., Soike, K., Brideau, R.J., Zaya, R.M., Cole, S.L., Zhang, J.-Y., et al. 1993. A human respiratory syncytial virus (RSV) primate model of enhanced pulmonary pathology induced with a formalin-inactivated RSV vaccine but not a recombinant FG subunit vaccine. J. Infect. Dis. 167: 553-561.
43. Kumar, M., Behera, A.K., Matuse, H., Lockey, R.F., and Mohapatra, S.S. 2000. Intranasal IFN-γ gene transfer protects BALB/c mice against respiratory syncytial virus infection. Vaccine, 18: 558-567.
44. Lindgren, C., and Grogaard, J. 1996. Reflex apnea response and inflammatory mediators in infants with respiratory tract infection. Acta Paediatr. 85: 798-803.
45. Lukacs, N.W., Tekkanat, K.K., Berlin, A., Hogaboam, C.M. Miller, A., Evanoff, H. et al. 2001. Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms. J. Immunol. 167: 1060-1065.
46. Malley, R., DeVincenzo, J., Ramilo, O., Dennehy, P.H., Meissner, H.C., Gruber, W.C. et al. 1998. Reduction of respiratory syncytial virus (RSV) in tracheal aspirates in intubated infants by use of humanized monoclonal antibody to RSV F protein. J. Infect. Dis. 178: 1555-1561.
47. Neuzil, K.M., Tang, Y.-W., and Graham, B.S. 1996. Protective role of TNF-α in respiratory syncytial virus infection in vitro and in vivo. Am. J. Med. Sci. 311: 201-204.
48. Noah, T.L., Henderson, F.W., Wortman, I.A., Devlin, R.B., Handy J., Koren, H.S., and Becker, S. 1995. Nasal cytokine production in viral acute upper respiratory infection of childhood. J. Infect. Dis. 171: 584-592.
49. Oppenshaw, P.J.M. 1995. Immunity and immunopathology to respiratory syncytial virus, the mouse model. Am. J. Respir. Crit. Care Med. 152: S59-S62.
50. Ottolini, M.G., Curtis, S.R., Mathews, A., Ottolini, S.R., and Prince, G.A. 2002. Palivizumab is highly effective in suppressing respiratory syncytial virus in an immunosuppressed animal model. Bone Marrow Transplant. 29: 117-120.
51. Peebles, R.S., Sheller, J.R., Collins, R.D., Jarzecka, A.K., Mitchell, D.B., Parker, R.A., and Graham, B. 2001. Respiratory syncytial virus infection does not increase allergen-induced type-2 cytokine production, yet increases airway hyperresponsiveness in mice. J. Med. Virol. 63: 178-188.
52. Peebles, R.S., Jr., Sheller, J.R., Collins, R.D., Jarzecka, A.K., Mithchell, D.B., Parker, R.A., and Graham, B.A. 2001. Respiratory syncytial virus infection does not increase allergen-induced type 2 cytokine production, yet increases airway hyperresponsiveness in mice. J. Med. Virol. 63: 178-188.
53. Preston, S.L., Drusano, G.L., Glue, P., Nash, J., Gupta, S.K., and McNamara, P. 1999. Pharmacokinetics and absolute bioavailability of RBV in healthy volunteers as determined by stable-isotope methodology. Antimicrob. Agents Chemother. 10: 2451-2456.
54. Prince, G.A., Jenson, A.B., Horswood, R.L., Camargo, E., and Chanook, R.M. 1978. The pathogenesis of respiratory syncytial virus infection in cotton rats. Am. J. Pathol. 93: 771-784.
55. Prince, G.A., Horswood, R.L., Berndt, J., Suffine, S.C., and Chanock, R.M. 1979. Respiratory syncytial virus infection in inbred mice. Infect. Immun. 26: 764-766.
56. Prince, G.A., Hemming, V.G., Horswood, R.L., Baron, P.A., and Chanock, R.M. 1987. Effectiveness of topically administered neutralizing antibodies in experimental immunotherapy of respiratory syncytial virus infection in cotton rats. J. Virol. 61: 1851-1854.
57. Prince, G.A., Matthews, A., Curtis, S.J., and Porter, D.D. 2000. Treatment of respiratory syncytial virus bronchiolitis and pneumonia in a cotton rat model with systemically administered monoclonal antibody (Palivizumab) and glucocorticosteroid. J. Infect. Dis. 182: 1326-1330.
58. Sarmiento, R.E., Tirado, R., and Gomez, B. 2002. Characteristics of a respiratory syncytial virus persistently infected macrophage-like culture. Virus Res. 84: 45-58.
59. Sidwell, R.W., Hurrman, J.H., Campbell, N., and Allen, L.B. 1977. Effects of RBV on viral hepatitis in laboratory animals. Ann. N.Y. Acad. Sci. 284: 239-246.
60. Schwarze, J., Cieslewicz, G., Hamelmann, E., Joetham, A., Shultz, L.D., Lamers, M.C., and Gelfand, E.W. 1999. Il-5 and eosinophils are essential for the development of airway hyperresponsiveness following acute respiratory syncytial virus infection. J. Immunol. 162: 2997-3004.
61. Stack, A.M., Mallen, R., Saladino, R.A., Montana, J.B., MacDonald, K.L., and Molrine, D.C. 2000. Primary respiratory syncytial virus infection pathology, immune response, and evaluation of vaccine challenge strains in a new mouse model. Vaccine, 18: 1412-1418.
62. Stark, J.M., McDowell, S.A., Koenigsknecht, V., Prows, D.R., Leikauf, J.E., Le Vine, A.M., and Leikauf, G.D. 2002. Genetic susceptibility to respiratory syncytial virus infection in inbred mice. J. Med. Virol. 67: 92-100.
63. Tam, R.C., Pai, B., Bard, J., Lim, C., Averett, D.R., Phan, U.T., and Milovanovic, T. 1999. Ribavirin polarizes human T cell response towards a type 1 cytokine profile. J. Hepatol. 30: 376-382.
64. Taylor, G., Stott, E.J., Hughes, M., and Collins, A.P. 1984. Respiratory syncytial virus infection in mice. Infect. Immun. 43: 649-655.
65. Tekkanat, K.K., Maassab, H., Berlin, A.A., Lincoln, P.M., Evanoff, H.L., Kaplan, M.H., and Lukacs, N.W. 2001. Role of interleukin-12 and Stat-4 in the regulation of airway inflammation and hyperreactivity in respiratory syncytial virus infection. Am. J. Pathol. 159: 631-638.
66. Thanos, D., and Maniatis, T. 1995. NF-κB: A lesson in family values. Cell, 80: 529-532.
67. Tripp, R.A., Jones, L., and Anderson, L.J. 2000a. Respiratory syncytial virus G and (or) SH glycoproteins modify CC and CXC chemokine mRNA expression in the BALB/c mouse. J. Virol. 74: 6227-6229.
68. Tripp, R.A., Moore, D., Winter, J., and Anderson, L.J. 2000b. Respiratory syncytial virus infection and G and/or SH protein expression contribute to substance P, which mediates inflammation and enhanced pulmonary disease in BALB/c mice. J. Virol. 74: 1614-1622.
69. Welliver, R.C., Garofalo, R.P., and Ogra, P.L. 2002. Beta-chemokines, but neither T helper type 1 nor T helper type 2 cytokines, correlate with severity of illness during respiratory syncitial virus infection. Pediatr. Infect. Dis. J. 21: 457-461.
70. van Schaik, S.M., Enhorning, G., Vargas, G., and Welliver, R.C. 1998. Respiratory syncytial virus affects pulmonary function in BALB/c mice. J. Infect. Dis. 177: 269-276.
71. van Schaik, S.M., Obot, S., Enhorining G., Hintz, K., Gross, K., Hancock, G.E. et al. 2000. Role of interferon gamma in the pathogenesis of primary respiratory syncytial virus infection in BALB/c mice. J. Med. Virol. 62: 257-266.
72. Vijayaraghavan, R., Schaper, M., Thompson, R., Stock, M.F., Boylstein, L.A., Juo, J.E., and Alarie, Y. 1994. Computer assisted recognition and quantitation of the effects of airborne chemicals acting at different areas of the respiratory tract in mice. Arch. Toxicol. 68: 490-499.
73. Viuff, B., Tjornoho, K., Larsen, L.E., Rontved, C.M., Uttenthal, A., Ronsholt, L., and Alexandersen, S. 2002. Replication and clearance of respiratory syncytial virus; Apoptosis is an important pathway of virus clearance after experimental infection with bovine respiratory syncytial virus. Am. J. Pathol. 161: 2195-2207.
74. Wyde, P.R., Morre-Poveda, D.K., De Clercq, E., Neyts, J., Matsuda, A., Minakawa, N. et al. 2000. Use of cotton rats to evaluate the efficacy of antivirals in treatment of measles virus infections. Antimicrob. Agents Chemother. 44: 1146-1152.