A role for immune complexes in enhanced respiratory syncytial virus disease

Journal of Experimental Medicine

Volumn 196, Issue 6, 2002, Pages 859-865

  Polack, Fernando P ^a,b   Teng, Michael N ^d   Collins, Peter L ^d   Prince, Gregory A ^e   Exner, Marcus ^f   Regele, Heinz ^g   Lirman, Dario D ^a,b   Rabold, Richard ^c   Hoffman, Scott J ^a,b   Karp, Christopher L ⁱ   Kleeberger, Steven R ^h   Wills Karp, Marsha ⁱ   Karron, Ruth A ^a,b  

^a SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e Virion Systems Inc   (United States)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

^g UNIVERSITY OF VIENNA   (Austria)

^h NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

ⁱ CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

Author keywords

Airway hyperresponsiveness; Compliment; Enhanced disease; Immune complexes; Respiratory syncytial virus

Indexed keywords

COMPLEMENT COMPONENT C3; IMMUNOGLOBULIN G; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOPSY; B LYMPHOCYTE; BRONCHIOLITIS; BRONCHOSPASM; COMPLEMENT ACTIVATION; CONTROLLED STUDY; FEMALE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VIRUS INFECTION; VIRUS PNEUMONIA; VIRUS TITRATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIGEN-ANTIBODY COMPLEX; BRONCHIAL HYPERREACTIVITY; COMPLEMENT ACTIVATION; COMPLEMENT C3; FEMALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; VACCINES, INACTIVATED; VIRAL PROTEINS;

EID: 0037120001     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20020781     Document Type: Article

References (30)

1. Collins, P.L., R.M. Chanock, and B.R. Murphy. 2001. Fields Virology. D.M. Knipe and P.M. Howley, editors. Lippincott Williams and Wilkins, Philadelphia, PA. 1443-1486.
2. Kim, H.W., J.G. Canchola, C.D. Brandt, G. Pyles, R.M. Chanock, K. Jensen, and R.H. Parrott. 1969. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am. J. Epidemiol. 89:422-434.
3. Graham, B.S. 1995. Pathogenesis of respiratory syncytial virus vaccine-augmented pathology. Am. J. Respir. Crit. Care Med. 152:S63-S66.
4. Connors, M., N.A. Giese, A.B. Kulkarni, C.Y. Firestone, H.C. Morse III, and B.R. Murphy. 1994. Enhanced pulmonary histopathology induced by respiratory syncytial virus (RSV) challenge of FI RSV-immunized BALB/c mice is abrogated by depletion of interleukin-4 (IL-4) and IL-10. J. Virol. 68:5321-5325.
5. Graham, B.S., G.S. Henderson, Y.W. Tang, X. Lu, K.M. Neuzil, and D.G. Colley. 1993. Priming immunization determines T helper cytokine mRNA expression patterns in lungs of mice challenged with respiratory syncytial virus. J. Immunol. 151:2032-2040.
6. Hancock, G.E., D.J. Speelman, K. Heers, E. Bortell, J. Smith, and C. Cosco. 1996. Generation of atypical pulmonary inflammatory responses in BALB/c mice after immunization with the native attachment (G) glycoprotein of respiratory syncytial virus. J. Virol. 70:7783-7791.
7. Openshaw, P.J., S.L. Clarke, and F.M. Record. 1992. Pulmonary eosinophilic response to respiratory syncytial virus infection in mice sensitized to the major surface glycoprotein G. Int. Immunol. 4: 493-498
8. Hussell, T., A. Georgiou, T.E. Sparer, S. Matthews, P. Pala, P.J. Openshaw. 1998. Host genetic determinants of vaccine-induced eosinophilia during respiratory syncytial virus infection. J. Immunol. 161:6215-6222.
9. Prince, G.A., A.B. Jenson, V.G. Hemming, B.R. Murphy, E.E. Walsh, R.L. Horswood, and R.M. Chanock. 1986. Enhancement of respiratory syncytial virus pulmonary pathology in cotton rats by prior intramuscular inoculation of FI virus. J. Virol. 57:721-728.
10. Gershwin, L.J., E.S. Schelegle, R.A. Gunther, M.L. Anderson, A.R. Woolums, D.R. Larochelle, G.A. Boyle, K.E. Friebertshauser, and R.S. Singer. 1998. A bovine model of vaccine enhanced respiratory syncytial virus pathophysiology. Vaccine. 16:1225-1236.
11. Prince, G.A., S.J. Curtis, K.C. Yim, and D.D. Porter. 2001. Vaccine-enhanced respiratory syncytial virus disease in cotton rats following immunization with Lot 100 or a newly prepared reference vaccine. J. Gen. Virol. 82:2881-2888.
12. Murphy, B.R., A. Sotnikov, P.R. Paradiso, S.W. Hildreth, A.B. Jenson, R.B. Baggs, L. Lawrence, J.J. Zubak, R.M. Chanock, J.A. Beeler, et al. 1989. Immunization of cotton rats with the fusion (F) and large (G) glycoproteins of respiratory syncytial virus (RSV) protects against RSV challenge without potentiating RSV disease. Vaccine. 7:533-540.
13. Connors, M., P.L. Collins, C.Y. Firestone, A.V. Sotnikov, A. Waitze, A.R. Davis, P.P. Hung, R.M. Chanock, and B.R. Murphy. 1992. Cotton rats previously immunized with a chimeric RSV FG glycoprotein develop enhanced pulmonary pathology when infected with RSV, a phenomenon not encountered following immunization with vaccinia-RSV recombinants or RSV. Vaccine. 10:475-484.
14. Polack, F.P., P.G. Auwaerter, S.H. Lee, H.C. Nousari, A. Valsamakis, K.M. Leiferman, A. Diwan, R.J. Adams, and D.E. Griffin. 1999. Production of atypical measles in rhesus macaques: evidence for disease mediated by IC formation and eosinophils in the presence of fusion-inhibiting antibodies. Nat. Med. 5:629-634.
15. Anderson, C.F., and D.M. Mosser. 2002. Cutting edge: biasing immune responses by directing antigen to macrophage fc-gamma receptors. J. Immunol. 168:3697-3701.
16. Teng, M.N., S.S. Whitehead, and P.L. Collins. 2001. Contribution of the respiratory syncytial virus G glycoprotein and its secreted and membrane-bound forms to virus replication in vitro and in vivo. Virology. 289:283-296.
17. Peebles, R.S., Jr., J.R. Sheller, R.D. Collins, K. Jarzecka, D.B. Mitchell, and B.S. Graham. 2000. Respiratory syncytial virus (RSV)-induced AHR in allergically sensitized mice is inhibited by live RSV and exacerbated by FI RSV. J. Infect. Dis. 182:671-677.
18. Regele, H., M. Exner, B. Watschinger, C. Wenter, M. Wahrmann, C. Osterreicher, M.D. Saemann, N. Mersich, W.H. Horl, G.J. Zlabinger, G.A. Bohmig. 2001. Endothelial C4d deposition is associated with inferior kidney allograft outcome independently of cellular rejection. Nephrol. Dial. Transplant. 16:2058-2066.
19. Groothuis, J.R., E.A. Simoes, M.J. Levin, C.B. Hall, C.E. Long, W.J. Rodriguez, J. Arrobio, H.C. Meissner, D.R. Fulton, R.C. Welliver, et al. 1993. Prophylactic administration of respiratory syncytial virus immune globulin to high-risk infants and young children. The Respiratory Syncytial Virus Immune Globulin Study Group. N. Engl. J. Med. 329:1524-1530.
20. Devey, M.E., and M.W. Steward. 1980. The induction of chronic antigen-antibody complex disease in selectively bred mice producing either high or low affinity antibody to protein antigens. Immunology. 41:303-311.
21. + T lymphocytes downregulate T helper cell type 2 cytokine secretion and pulmonary eosinophilia during experimental murine respiratory syncytial virus infection. J. Exp. Med. 186: 421-432.
22. + T cells control Th2-driven pathology during pulmonary respiratory syncytial virus infection. Eur. J. Immunol. 27:3341-3349.
23. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T.Y. Neben, C.L. Karp, and D.D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science. 282:2258-2261.
24. + T cells. J. Virol. 66:7444-7451.
25. Kim, H.W., S.L. Leikin, J. Arrobio, C.D. Brandt, R.M. Chanock, and R.H. Parrott. 1976. Cell-mediated immunity to respiratory syncytial virus induced by inactivated vaccine or by infection. Pediatr. Res. 10:75-78.
26. Kraus, P.J., J.D. Cherry, J.M. Carney, M.J. Naiditch, and K. O'Connor. 1980. Measles-specific lymphocyte reactivity and serum antibody in subjects with different measles histories. Am. J. Dis. Child. 134:567-571.
27. Humbles, A.A., B. Lu, C.A. Nilsson, C. Lilly, E. Israel, Y. Fujiwara, N.P. Gerard, and C. Gerard. 2000. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature. 406:998-1001.
28. Karp, C.L., A. Grupe, E. Schadt, S.L. Ewart, M. Keane- Moore, P.J. Cuomo, J. Kohl, L. Wahl, D. Kuperman, S. Germer, et al. 2000. Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nat. Immunol. 1:221-226.
29. Hopken, U.E., B. Lu, N.P. Gerard, and C. Gerard. 1997. Impaired inflammatory responses in the reverse arthus reaction through genetic deletion of the C5a receptor. J. Exp. Med. 186:749-756.
30. Zhang, Y., B.F. Ramos, and B.A. Jakschik. 1992. Neutrophil recruitment by tumor necrosis factor from mast cells in IC peritonitis. Science. 258:1957-1959.