Immunomodulation with IL-4Rα antisense oligonucleotide prevents respiratory syncytial virus-mediated pulmonary disease

Journal of Immunology

Volumn 185, Issue 8, 2010, Pages 4804-4811

  Ripple, Michael J ^a   You, Dahui ^a,b   Honnegowda, Srinivasa ^a   Giaimo, Joseph D ^a   Sewell, Andrew B ^a   Becnel, David M ^a   Cormier, Stephania A ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; INTERLEUKIN 4 RECEPTOR ALPHA; ANTISENSE OLIGONUCLEOTIDE; CELL SURFACE RECEPTOR; IL4RA PROTEIN, MOUSE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CELL HYPERPLASIA; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; GOBLET CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INHIBITION KINETICS; LUNG DISEASE; LUNG FUNCTION; MOUSE; NEWBORN; NONHUMAN; PRIMARY INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; TH1 CELL; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; BLOOD; DENDRITIC CELL; DRUG ANTAGONISM; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VIROLOGY; VIRUS LOAD;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, VIRAL; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOMODULATION; LUNG DISEASES; MICE; MICE, INBRED BALB C; OLIGONUCLEOTIDES, ANTISENSE; RECEPTORS, CELL SURFACE; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; TH1 CELLS; TH2 CELLS; VIRAL LOAD;

EID: 78049517831     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000484     Document Type: Article

References (40)

1. Hall, C. B., G. A. Weinberg, M. K. Iwane, A. K. Blumkin, K. M. Edwards, M. A. Staat, P. Auinger, M. R. Griffin, K. A. Poehling, D. Erdman, et al. 2009. The burden of respiratory syncytial virus infection in young children. N. Engl. J. Med. 360:588-598.
2. Stang, P., N. Brandenburg, and B. Carter. 2001. The economic burden of respiratory syncytial virus-associated bronchiolitis hospitalizations. Arch. Pediatr. Adolesc. Med. 155:95-96.
3. Fleming, D. M., A. J. Elliot, and K. W. Cross. 2007. Morbidity profiles of patients consulting during influenza and respiratory syncytial virus active periods. Epidemiol. Infect. 135:1099-1108.
4. Wu, P., W. D. Dupont, M. R. Griffin, K. N. Carroll, E. F. Mitchel, T. Gebretsadik, and T. V. Hartert. 2008. Evidence of a causal role of winter virus infection during infancy in early childhood asthma. Am. J. Respir. Crit. Care Med. 178:1123-1129.
5. Kristjansson, S., S. P. Bjarnarson, G. Wennergren, A. H. Palsdottir, T. Arnadottir, A. Haraldsson, and I. Jonsdottir. 2005. Respiratory syncytial virus and other respiratory viruses during the first 3 months of life promote a local TH2-like response. J. Allergy Clin. Immunol. 116:805-811.
6. Sims, D. G., M. A. Downham, P. S. Gardner, J. K. Webb, and D. Weightman. 1978. Study of 8-year-old children with a history of respiratory syncytial virus bronchiolitis in infancy. BMJ 1:11-14.
7. Pullan, C. R., and E. N. Hey. 1982. Wheezing, asthma, and pulmonary dysfunction 10 years after infection with respiratory syncytial virus in infancy. Br. Med. J. (Clin. Res. Ed.) 284:1665-1669.
8. McConnochie, K. M., and K. J. Roghmann. 1984. Bronchiolitis as a possible cause of wheezing in childhood: new evidence. Pediatrics 74:1-10.
9. Mok, J. Y., and H. Simpson. 1984. Outcome for acute bronchitis, bronchiolitis, and pneumonia in infancy. Arch. Dis. Child. 59:306-309.
10. Murray, M., M. S. Webb, C. O'Callaghan, A. S. Swarbrick, and A. D. Milner. 1992. Respiratory status and allergy after bronchiolitis. Arch. Dis. Child. 67:482-487.
11. Noble, V., M. Murray, M. S. Webb, J. Alexander, A. S. Swarbrick, and A. D. Milner. 1997. Respiratory status and allergy nine to 10 years after acute bronchiolitis. Arch. Dis. Child. 76:315-319.
12. Stein, R. T., D. Sherrill, W. J. Morgan, C. J. Holberg, M. Halonen, L. M. Taussig, A. L. Wright, and F. D. Martinez. 1999. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 354:541-545.
13. Sigurs, N., P. M. Gustafsson, R. Bjarnason, F. Lundberg, S. Schmidt, F. Sigurbergsson, and B. Kjellman. 2005. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am. J. Respir. Crit. Care Med. 171:137-141.
14. Piippo-Savolainen, E., S. Remes, and M. Korppi. 2007. Does blood eosinophilia in wheezing infants predict later asthma? A prospective 18-20-year follow-up. Allergy Asthma Proc. 28:163-169.
15. Openshaw, P. J. M. 2003. RSV bronchiolitis, gammadelta T cells and asthma: are they linked? Clin. Exp. Immunol. 131:197-198.
16. Culley, F. J., J. Pollott, and P. J. Openshaw. 2002. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 196:1381-1386.
17. Dakhama, A., J. W. Park, C. Taube, A. Joetham, A. Balhorn, N. Miyahara, K. Takeda, and E. W. Gelfand. 2005. The enhancement or prevention of airway hyperresponsiveness during reinfection with respiratory syncytial virus is critically dependent on the age at first infection and IL-13 production. J. Immunol. 175:1876-1883.
18. Becnel, D., D. You, J. Erskin, D. M. Dimina, and S. A. Cormier. 2005. A role for airway remodeling during respiratory syncytial virus infection. Respir. Res. 6:122.
19. You, D., D. Becnel, K. Wang, M. Ripple, M. Daly, and S. A. Cormier. 2006. Exposure of neonates to respiratory syncytial virus is critical in determining subsequent airway response in adults. Respir. Res. 7:107.
20. Lee, H. H., C. M. Hoeman, J. C. Hardaway, F. B. Guloglu, J. S. Ellis, R. Jain, R. Divekar, D. M. Tartar, C. L. Haymaker, and H. Zaghouani. 2008. Delayed maturation of an IL-12-producing dendritic cell subset explains the early Th2 bias in neonatal immunity. J. Exp. Med. 205:2269-2280.
21. 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.
22. Webb, D. C., Y. Cai, K. I. Matthaei, and P. S. Foster. 2007. Comparative roles of IL-4, IL-13, and IL-4Ralpha in dendritic cell maturation and CD4+ Th2 cell function. J. Immunol. 178:219-227.
23. LaPorte, S. L., Z. S. Juo, J. Vaclavikova, L. A. Colf, X. Qi, N. M. Heller, A. D. Keegan, and K. C. Garcia. 2008. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132:259-272.
24. Dakhama, A., Y. M. Lee, H. Ohnishi, X. Jing, A. Balhorn, K. Takeda, and E. W. Gelfand. 2009. Virus-specific IgE enhances airway responsiveness on reinfection with respiratory syncytial virus in newborn mice. J. Allergy Clin. Immunol. 123:138-145.e5.
25. Choi, E. H., H. J. Lee, T. Yoo, and S. J. Chanock. 2002. A common haplotype of interleukin-4 gene IL4 is associated with severe respiratory syncytial virus disease in Korean children. J. Infect. Dis. 186:1207-1211.
26. Hoebee, B., E. Rietveld, L. Bont, M. Oosten, H. M. Hodemaekers, N. J. Nagelkerke, H. J. Neijens, J. L. Kimpen, and T. G. Kimman. 2003. Association of severe respiratory syncytial virus bronchiolitis with interleukin-4 and interleukin-4 receptor alpha polymorphisms. J. Infect. Dis. 187:2-11.
27. Puthothu, B., M. Krueger, J. Forster, and A. Heinzmann. 2006. Association between severe respiratory syncytial virus infection and IL13/IL4 haplotypes. J. Infect. Dis. 193:438-441.
28. Openshaw, P. J. M. 2005. Antiviral immune responses and lung inflammation after respiratory syncytial virus infection. Proc. Am. Thorac. Soc. 2:121-125.
29. Institute of Laboratory Animal Research, Commission on Life Sciences, National Research Council. 1996. Guide for the Care and Use of Laboratory Animals. National Academies Press, Washington, D. C.
30. Karras, J. G., J. R. Crosby, M. Guha, D. Tung, D. A. Miller, W. A. Gaarde, R. S. Geary, B. P. Monia, and S. A. Gregory. 2007. Anti-inflammatory activity of inhaled IL-4 receptor-alpha antisense oligonucleotide in mice. Am. J. Respir. Cell Mol. Biol. 36:276-285.
31. You, D., M. Ripple, S. Balakrishna, D. Troxclair, D. Sandquist, L. Ding, T. A. Ahlert, and S. A. Cormier. 2008. Inchoate CD8+ T cell responses in neonatal mice permit influenza-induced persistent pulmonary dysfunction. J. Immunol. 181:3486-3494.
32. Fodha, I., A. Vabret, L. Ghedira, H. Seboui, S. Chouchane, J. Dewar, N. Gueddiche, A. Trabelsi, N. Boujaafar, and F. Freymuth. 2007. Respiratory syncytial virus infections in hospitalized infants: association between viral load, virus subgroup, and disease severity. J. Med. Virol. 79:1951-1958.
33. Hussell, T., L. C. Spender, A. Georgiou, A. O'Garra, and P. J. Openshaw. 1996. Th1 and Th2 cytokine induction in pulmonary T cells during infection with respiratory syncytial virus. J. Gen. Virol. 77:2447-2455.
34. Spender, L. C., T. Hussell, and P. J. Openshaw. 1998. Abundant IFN-gamma production by local T cells in respiratory syncytial virus-induced eosinophilic lung disease. J. Gen. Virol. 79:1751-1758.
35. Sriram, U., C. Biswas, E. M. Behrens, J.-A. Dinnall, D. K. Shivers, M. Monestier, Y. Argon, and S. Gallucci. 2007. IL-4 suppresses dendritic cell response to type I interferons. J. Immunol. 179:6446-6455.
36. Kelly-Welch, A. E., M. E. F. Melo, E. Smith, A. Q. Ford, C. Haudenschild, N. Noben-Trauth, and A. D. Keegan. 2004. Complex role of the IL-4 receptor alpha in a murine model of airway inflammation: expression of the IL-4 receptor alpha on nonlymphoid cells of bone marrow origin contributes to severity of inflammation. J. Immunol. 172:4545-4555.
37. Li, L., H. H. Lee, J. J. Bell, R. K. Gregg, J. S. Ellis, A. Gessner, and H. Zaghouani. 2004. IL-4 utilizes an alternative receptor to drive apoptosis of Th1 cells and skews neonatal immunity toward Th2. Immunity 20:429-440.
38. Harker, J., A. Bukreyev, P. L. Collins, B. Wang, P. J. M. Openshaw, and J. S. Tregoning. 2007. Virally delivered cytokines alter the immune response to future lung infections. J. Virol. 81:13105-13111.
39. Harker, J. A., D. C. Lee, Y. Yamaguchi, B. Wang, A. Bukreyev, P. L. Collins, J. S. Tregoning, and P. J. Openshaw. 2010. Delivery of cytokines by recombinant virus in early life alters the immune response to adult lung infection. J. Virol. 84:5294-5302.
40. Newcomb, D. C., W. Zhou, M. L. Moore, K. Goleniewska, G. K. Hershey, J. K. Kolls, and R. S. Peebles, Jr. 2009. A functional IL-13 receptor is expressed on polarized murine CD4+ Th17 cells and IL-13 signaling attenuates Th17 cytokine production. J. Immunol. 182:5317-5321.