Localization of the T-cell response to RSV infection is altered in infant mice

Pediatric Pulmonology

Volumn 53, Issue 2, 2018, Pages 145-153

  Eichinger, Katherine M ^a   Kosanovich, Jessica L ^a   Empey, Kerry M ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

airway; IFN ; infant mice; RSV; T cell response

Indexed keywords

F PROTEIN; RECOMBINANT GAMMA INTERFERON; UNCLASSIFIED DRUG; VIRAL PROTEIN; ANTIVIRUS AGENT; CD44 PROTEIN, MOUSE; GAMMA INTERFERON; HYALURONIC ACID BINDING PROTEIN; T BOX TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD4+ TBET+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CD8+ TBET+ T LYMPHOCYTE; CELL ISOLATION; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG MECHANISM; INFANT; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL VIRUS INFECTION; T LYMPHOCYTE SUBPOPULATION; TISSUE DISTRIBUTION; ANIMAL; BAGG ALBINO MOUSE; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODEL; DRUG EFFECT; IMMUNOLOGY; LUNG; METABOLISM;

ANIMALS; ANTIVIRAL AGENTS; BRONCHOALVEOLAR LAVAGE FLUID; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; HYALURONAN RECEPTORS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; LUNG; MICE; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; T-BOX DOMAIN PROTEINS;

EID: 85033235271     PISSN: 87556863     EISSN: 10990496     Source Type: Journal    
DOI: 10.1002/ppul.23911     Document Type: Article

References (40)

1. Mizgerd JP. Lung infection–a public health priority. PLoS Med. 2006; 3:e76.
2. Global Health Estimates 2015: Deaths by Cause, Age, Sex, by Country and by Region, 2000–2015. Geneva: World Health Organization; 2016.
3. Nair H, Nokes DJ, Gessner BD, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet. 2010; 375:1545–1555.
4. Branche AR, Falsey AR. Respiratory syncytial virus infection in older adults: an under-recognized problem. Drugs Aging. 2015; 32:261–269.
5. Wegzyn C, Toh LK, Notario G, et al. Safety and effectiveness of palivizumab in children at high risk of serious disease due to respiratory syncytial virus infection: a systematic review. Infect Dis Ther. 2014; 3:133–158.
6. Hall CB, Weinberg GA, Blumkin AK, et al. Respiratory syncytial virus-associated hospitalizations among children less than 24 months of age. Pediatrics. 2013; 132:e341–e348.
7. Hall CB, Weinberg GA, Iwane MK, et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009; 360:588–598.
8. Cannon MJ, Openshaw PJ, Askonas BA. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J Exp Med. 1988; 168:1163–1168.
9. Graham BS, Bunton L, Wright PF, Karzon DT. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J Clin Invest. 1991; 88:1026–1033.
10. Lee S, Stokes KL, Currier MG, Sakamoto K, Lukacs NW, Celis E, Moore ML. Vaccine-Elicited CD8(+) T cells protect against respiratory syncytial virus strain A2-Line19F-Induced pathogenesis in BALB/c mice. J Virol. 2012; 86:13016–13024.
11. Ostler T, Ehl S. Pulmonary T cells induced by respiratory syncytial virus are functional and can make an important contribution to long-lived protective immunity. Eur J Immunol. 2002; 32:2562–2569.
12. Hall CB, Powell KR, MacDonald NE, Gala CL, Menegus ME, Suffin SC, Cohen HJ. Respiratory syncytial viral infection in children with compromised immune function. N Engl J Med. 1986; 315:77–81.
13. Johnson JE, Gonzales RA, Olson SJ, Wright PF, Graham BS. The histopathology of fatal untreated human respiratory syncytial virus infection. Mod Pathol. 2006; 20:108–119.
14. Welliver TP, Garofalo RP, Hosakote Y, et al. Severe human lower respiratory tract illness caused by respiratory syncytial virus and influenza virus is characterized by the absence of pulmonary cytotoxic lymphocyte responses. J Infect Dis. 2007; 195:1126–1136.
15. Everard ML, Swarbrick A, Wrightham M, et al. Analysis of cells obtained by bronchial lavage of infants with respiratory syncytial virus infection. Arch Dis Child. 1994; 71:428–432.
16. Heidema J, Lukens MV, van Maren WW, et al. CD8+ T cell responses in bronchoalveolar lavage fluid and peripheral blood mononuclear cells of infants with severe primary respiratory syncytial virus infections. J Immunol. 2007; 179:8410–8417.
17. Lines JL, Hoskins S, Hollifield M, Cauley LS, Garvy BA. The migration of T cells in response to influenza virus is altered in neonatal mice. J Immunol. (Baltimore, Md: 1950) 2010; 185:2980–2988.
18. Kristjansson S, Bjarnarson SP, Wennergren G, Palsdottir AH, Arnadottir T, Haraldsson A, Jonsdottir I. Respiratory syncytial virus and other respiratory viruses during the first 3 months of life promote a local TH2-like response. J Allergy Clin Immunol. 2005; 116:805–811.
19. Lee FE, Walsh EE, Falsey AR, et al. Human infant respiratory syncytial virus (RSV)-specific type 1 and 2 cytokine responses ex vivo during primary RSV infection. J Infect Dis. 2007; 195:1779–1788.
20. Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med. 2003; 168:633–639.
21. Hussell T, Baldwin CJ, O'Garra A, Openshaw PJ. CD8+ T cells control Th2-driven pathology during pulmonary respiratory syncytial virus infection. Eur J Immunol. 1997; 27:3341–3349.
22. Arulanandam BP, Mittler JN, Lee WT, O'Toole M, Metzger DW. Neonatal administration of IL-12 enhances the protective efficacy of antiviral vaccines. J Immunol. 2000; 164:3698–3704.
23. Pertmer TM, Oran AE, Madorin CA, Robinson HL. Th1 genetic adjuvants modulate immune responses in neonates. Vaccine. 2001; 19:1764–1771.
24. Empey KM, Orend JG, Peebles RS, Egana L, Norris KA, Oury TD, Kolls JK. Stimulation of immature lung macrophages with intranasal interferon gamma in a novel neonatal mouse model of respiratory syncytial virus infection. PLoS ONE. 2012; 7.
25. Graham BS, Perkins MD, Wright PF, Karzon DT. Primary respiratory syncytial virus infection in mice. J Med Virol. 1988; 26:153–162.
26. Qureshi MH, Garvy BA. Neonatal T cells in an adult lung environment are competent to resolve Pneumocystis carinii pneumonia. J Immunol. 2001; 166:5704–5711.
27. Fitzpatrick EA, You D, Shrestha B, et al. A neonatal murine model of MRSA pneumonia. PLoS ONE. 2017; 12:e0169273.
28. Tregoning JS, Yamaguchi Y, Harker J, Wang B, Openshaw PJ. The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J Virol. 2008; 82:4115–4124.
29. Liesman RM, Buchholz UJ, Luongo CL, et al. RSV-encoded NS2 promotes epithelial cell shedding and distal airway obstruction. J Clin Invest. 2014; 124:2219–2233.
30. Villenave R, Thavagnanam S, Sarlang S, et al. In vitro modeling of respiratory syncytial virus infection of pediatric bronchial epithelium, the primary target of infection in vivo. Proc Natl Acad Sci USA. 2012; 109:5040–5045.
31. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol. 2002; 76:5654–5666.
32. Lukens MV, Claassen EA, de Graaff PM, et al. Characterization of the CD8+ T cell responses directed against respiratory syncytial virus during primary and secondary infection in C57BL/6 mice. Virology. 2006; 352:157–168.
33. Chang J, Braciale TJ. Respiratory syncytial virus infection suppresses lung CD8+ T-cell effector activity and peripheral CD8+ T-cell memory in the respiratory tract. Nat Med. 2002; 8:54–60.
34. Ostler T, Davidson W, Ehl S. Virus clearance and immunopathology by CD8+ T cells during infection with respiratory syncytial virus are mediated by IFN-γ. Eur J Immunol. 2002; 32:2117–2123.
35. Kumar M, Behera AK, Matsuse H, Lockey RF, Mohapatra SS. Intranasal IFN-γ gene transfer protects BALB/c mice against respiratory syncytial virus infection. Vaccine. 1999; 18:558–567.
36. Eichinger KM, Egana L, Orend JG, Resetar E, Anderson KB, Patel R, Empey KM. Alveolar macrophages support interferon gamma-mediated viral clearance in RSV-infected neonatal mice. Respir Res. 2015; 16:122.
37. Lee YM, Miyahara N, Takeda K, et al. IFN-gamma production during initial infection determines the outcome of reinfection with respiratory syncytial virus. Am J Respir Crit Care Med. 2008; 177:208–218.
38. Ö Sercan, Hämmerling GJ, Arnold B, Schüler T. Cutting edge: innate immune cells contribute to the IFN-γ-Dependent regulation of antigen-Specific CD8+ T cell homeostasis. J Immunol. 2006; 176:735–739.
39. Sercan Ö, Stoycheva D, Hämmerling GJ, Arnold B, Schüler T. IFN-γ receptor signaling regulates memory CD8+ T cell differentiation. J Immunol. 2010; 184:2855–2862.
40. Stoycheva D, Deiser K, Stärck L, Nishanth G, Schlüter D, Uckert W, Schüler T. IFN-γ regulates CD8+ memory T cell differentiation and survival in response to weak, but not strong, TCR signals. J Immunol. 2015; 194:553–559.