Respiratory Syncytial Virus (RSV) infection in elderly mice results in altered antiviral gene expression and enhanced pathology

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Wong, Terianne M ^a,b   Boyapalle, Sandhya ^a,b   Sampayo, Viviana ^b   Nguyen, Huy D ^b   Bedi, Raminder ^b   Kamath, Siddharth G ^b   Moore, Martin L ^c,d   Mohapatra, Subhra ^a,b   Mohapatra, Shyam S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; OSTEOPONTIN; CYTOKINE;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC ANALYSIS; HISTOPATHOLOGY; IN VIVO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LUNG ALVEOLUS MACROPHAGE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PNEUMONIA; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS STRAIN; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DISEASE MODEL; GENETICS; HUMAN; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; KINETICS; LEUKOCYTE; LUNG ALVEOLUS; MACROPHAGE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

AGING; ANIMALS; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; KINETICS; LEUKOCYTES; MACROPHAGES; MICE; MICE, INBRED BALB C; PNEUMONIA; PULMONARY ALVEOLI; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; SIGNAL TRANSDUCTION;

EID: 84895859623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088764     Document Type: Article

References (66)

1. Cherukuri A, Patton K, Gasser RA Jr, Zuo F, Woo J, et al. (2013) Adults 65 years old and older have reduced numbers of functional memory T cells to respiratory syncytial virus fusion protein. Clin Vaccine Immunol 20: 239-247.
2. Johnstone J, Majumdar SR, Fox JD, Marrie TJ (2008) Viral infection in adults hospitalized with community-acquired pneumonia: prevalence, pathogens, and presentation. Chest 134: 1141-1148.
3. Schlender J, Bossert B, Buchholz U, Conzelmann KK (2000) Bovine respiratory syncytial virus nonstructural proteins NS1 and NS2 cooperatively antagonize alpha/beta interferon-induced antiviral response. J Virol 74: 8234-8242. (Pubitemid 30666671)
4. Tran KC, Collins PL, Teng MN (2004) Effects of altering the transcription termination signals of respiratory syncytial virus on viral gene expression and growth in vitro and in vivo. J Virol 78: 692-699. (Pubitemid 38067590)
5. Gonzalez PA, Prado CE, Leiva ED, Carreno LJ, Bueno SM, et al. (2008) Respiratory syncytial virus impairs T cell activation by preventing synapse assembly with dendritic cells. Proc Natl Acad Sci U S A 105: 14999-15004.
6. Mohapatra SS, Boyapalle S (2008) Epidemiologic, experimental, and clinical links between respiratory syncytial virus infection and asthma. Clin Microbiol Rev 21: 495-504.
7. Cabalka AK (2004) Physiologic risk factors for respiratory viral infections and immunoprophylaxis for respiratory syncytial virus in young children with congenital heart disease. Pediatr Infect Dis J 23: S41-45.
8. Gern JE (2009) Rhinovirus and the initiation of asthma. Curr Opin Allergy Clin Immunol 9: 73-78.
9. Eisenhut M (2006) Extrapulmonary manifestations of severe respiratory syncytial virus infection - a systematic review. Crit Care 10: R107.
10. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289: 179-186. (Pubitemid 36068705)
11. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE (2005) Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352: 1749-1759. (Pubitemid 40570923)
12. Busse PJ, Mathur SK (2010) Age-related changes in immune function: effect on airway inflammation. J Allergy Clin Immunol 126: 690-699; quiz 700-691.
13. Fulton RB, Varga SM (2009) Effects of aging on the adaptive immune response to respiratory virus infections. Aging health 5: 775.
14. Bruunsgaard H, Pedersen M, Pedersen BK (2001) Aging and proinflammatory cytokines. Curr Opin Hematol 8: 131-136. (Pubitemid 32324632)
15. Qian F, Wang X, Zhang L, Lin A, Zhao H, et al. (2011) Impaired interferon signaling in dendritic cells from older donors infected in vitro with West Nile virus. J Infect Dis 203: 1415-1424.
16. Lukacs NW, Smit JJ, Mukherjee S, Morris SB, Nunez G, et al. (2010) Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation. J Immunol 185: 2231-2239.
17. van der Windt GJ, Hoogerwerf JJ, de Vos AF, Florquin S, van der Poll T (2010) Osteopontin promotes host defense during Klebsiella pneumoniae-induced pneumonia. Eur Respir J 36: 1337-1345.
18. Abel B, Freigang S, Bachmann MF, Boschert U, Kopf M (2005) Osteopontin is not required for the development of th1 responses and viral immunity. The Journal of Immunology 175: 6006-6013. (Pubitemid 41508086)
19. Xanthou G, Alissafi T, Semitekolou M, Simoes DCM, Economidou E, et al. (2007) Osteopontin has a crucial role in allergic airway disease through regulation of dendritic cell subsets. Nat Med 13: 570-578. (Pubitemid 46828486)
20. Ashkar S, Weber GF, Panoutsakopoulou V, Sanchirico ME, Jansson M, et al. (2000) Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287: 860-864. (Pubitemid 30084330)
21. Panda A, Qian F, Mohanty S, van Duin D, Newman FK, et al. (2010) Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol 184: 2518-2527.
22. Zhang Y, Wang Y, Gilmore X, Xu K, Wyde PR, et al. (2002) An aged mouse model for RSV infection and diminished CD8(+) CTL responses. Exp Biol Med (Maywood) 227: 133-140.
23. Curtis SJ, Ottolini MG, Porter DD, Prince GA (2002) Age-dependent replication of respiratory syncytial virus in the cotton rat. Exp Biol Med (Maywood) 227: 799-802.
24. Cherukuri A, Stokes KL, Patton K, Kuo H, Sakamoto K, et al. (2012) An adjuvanted respiratory syncytial virus fusion protein induces protection in aged BALB/c mice. Immun Ageing 9: 21.
25. Boukhvalova MS, Yim KC, Kuhn KH, Hemming JP, Prince GA, et al. (2007) Age-related differences in pulmonary cytokine response to respiratory syncytial virus infection: modulation by anti-inflammatory and antiviral treatment. J Infect Dis 195: 511-518. (Pubitemid 46214393)
26. Stokes KL, Chi MH, Sakamoto K, Newcomb DC, Currier MG, et al. (2011) Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice. J Virol 85: 5782-5793.
27. Giles BM, Ross TM (2011) A computationally optimized broadly reactive antigen (COBRA) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets. Vaccine 29: 3043-3054.
28. Mukherjee S, Lindell DM, Berlin AA, Morris SB, Shanley TP, et al. (2011) IL-17-induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease. Am J Pathol 179: 248-258.
29. Moore ML, Chi MH, Luongo C, Lukacs NW, Polosukhin VV, et al. (2009) A chimeric A2 strain of respiratory syncytial virus (RSV) with the fusion protein of RSV strain line 19 exhibits enhanced viral load, mucus, and airway dysfunction. J Virol 83: 4185-4194.
30. Cyr SL, Jones T, Stoica-Popescu I, Burt D, Ward BJ (2007) C57Bl/6 mice are protected from respiratory syncytial virus (RSV) challenge and IL-5 associated pulmonary eosinophilic infiltrates following intranasal immunization with Protollin-eRSV vaccine. Vaccine 25: 3228-3232. (Pubitemid 46505048)
31. Boyapalle S, Wong T, Garay J, Teng M, San Juan-Vergara H, et al. (2012) Respiratory syncytial virus NS1 protein colocalizes with mitochondrial antiviral signaling protein MAVS following infection. PLoS One 7: e29386.
32. Lindell DM, Morris SB, White MP, Kallal LE, Lundy PK, et al. (2011) A novel inactivated intranasal respiratory syncytial virus vaccine promotes viral clearance without Th2 associated vaccine-enhanced disease. PLoS One 6: e21823.
33. Aeffner F, Davis IC (2012) Respiratory syncytial virus reverses airway hyperresponsiveness to methacholine in ovalbumin-sensitized mice. PLoS One 7: e46660.
34. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, et al. (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res 38: W214-220.
35. Eigenbrod T, Franchi L, Munoz-Planillo R, Kirschning CJ, Freudenberg MA, et al. (2012) Bacterial RNA mediates activation of caspase-1 and IL-1beta release independently of TLRs 3, 7, 9 and TRIF but is dependent on UNC93B. J Immunol 189: 328-336.
36. Boehmer ED, Meehan MJ, Cutro BT, Kovacs EJ (2005) Aging negatively skews macrophage tlr2- and tlr4-mediated pro-inflammatory responses without affecting the il-2-stimulated pathway. Mechanisms of Ageing and Development 126: 1305-1313. (Pubitemid 41572248)
37. Kovacs EJ, Palmer JL, Fortin CF, Fulop T Jr, Goldstein DR, et al. (2009) Aging and innate immunity in the mouse: impact of intrinsic and extrinsic factors. Trends Immunol 30: 319-324.
38. Liang S, Domon H, Hosur KB, Wang M, Hajishengallis G (2009) Age-related alterations in innate immune receptor expression and ability of macrophages to respond to pathogen challenge in vitro. Mech Ageing Dev 130: 538-546.
39. Renshaw M, Rockwell J, Engleman C, Gewirtz A, Katz J, et al. (2002) Cutting edge: impaired Toll-like receptor expression and function in aging. J Immunol 169: 4697-4701. (Pubitemid 35217128)
40. Solana R, Pawelec G, Tarazona R (2006) Aging and innate immunity. Immunity 24: 491-494. (Pubitemid 43728154)
41. Bendelja K, Vojvoda V, Aberle N, Cepin-Bogovic J, Gagro A, et al. (2010) Decreased Toll-like receptor 8 expression and lower TNF-alpha synthesis in infants with acute RSV infection. Respir Res 11: 143.
42. Poeck H, Bscheider M, Gross O, Finger K, Roth S, et al. (2010) Recognition of RNA virus by RIG-i results in activation of card9 and inflammasome signaling for interleukin 1b production. Nat Immunol 11: 63-69.
43. Bartlett DB, Firth CM, Phillips AC, Moss P, Baylis D, et al. (2012) The age-related increase in low-grade systemic inflammation (Inflammaging) is not driven by cytomegalovirus infection. Aging Cell 11: 912-915.
44. Schmitz N, Kurrer M, Bachmann MF, Kopf M (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 79: 6441-6448. (Pubitemid 40617247)
45. Ramirez A, Rathinam V, Fitzgerald K, Golenbock D, Mathew A (2012) Defective pro-IL-1beta responses in macrophages from aged mice. Immunity & Ageing 9: 27.
46. Zhao W, Wang L, Zhang L, Yuan C, Kuo PC, et al. (2010) Differential expression of intracellular and secreted osteopontin isoforms by murine macrophages in response to toll-like receptor agonists. J Biol Chem 285: 20452-20461.
47. Zhou W, Hashimoto K, Moore ML, Elias JA, Zhu Z, et al. (2006) IL-13 is associated with reduced illness and replication in primary respiratory syncytial virus infection in the mouse. Microbes Infect 8: 2880-2889. (Pubitemid 44920303)
48. Ehre C, Worthington EN, Liesman RM, Grubb BR, Barbier D, et al. (2012) Overexpressing mouse model demonstrates the protective role of Muc5ac in the lungs. Proc Natl Acad Sci U S A 109: 16528-16533.
49. Schlafer S, Meyer RL, Sutherland DS, Stadler B (2012) Effect of osteopontin on the initial adhesion of dental bacteria. J Nat Prod 75: 2108-2112.
50. Matsui Y, Iwasaki N, Kon S, Takahashi D, Morimoto J, et al. (2009) Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum 60: 2362-2371.
51. Inoue M, Williams KL, Gunn MD, Shinohara ML (2012) NLRP3 inflammasome induces chemotactic immune cell migration to the CNS in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 109: 10480-10485.
52. Stout-Delgado HW, Vaughan SE, Shirali AC, Jaramillo RJ, Harrod KS (2012) Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin. J Immunol 188: 2815-2824.
53. Paliwal P, Pishesha N, Wijaya D, Conboy IM (2012) Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration. Aging (Albany NY) 4: 553-566.
54. Prasse A, Stahl M, Schulz G, Kayser G, Wang L, et al. (2009) Essential role of osteopontin in smoking-related interstitial lung diseases. Am J Pathol 174: 1683-1691.
55. Konno S, Kurokawa M, Uede T, Nishimura M, Huang SK (2011) Role of osteopontin, a multifunctional protein, in allergy and asthma. Clin Exp Allergy 41: 1360-1366.
56. Chiba S, Rashid MM, Okamoto H, Shiraiwa H, Kon S, et al. (2000) The role of osteopontin in the development of granulomatous lesions in lung. Microbiol Immunol 44: 319-332. (Pubitemid 30241792)
57. O'Regan A (2003) The role of osteopontin in lung disease. Cytokine Growth Factor Rev 14: 479-488.
58. Xuan JW, Hota C, Shigeyama Y, D'Errico JA, Somerman MJ, et al. (1995) Site-directed mutagenesis of the arginine-glycine-aspartic acid sequence in osteopontin destroys cell adhesion and migration functions. J Cell Biochem 57: 680-690.
59. Morimoto J, Sato K, Nakayama Y, Kimura C, Kajino K, et al. (2011) Osteopontin modulates the generation of memory CD8+ T cells during influenza virus infection. J Immunol 187: 5671-5683.
60. Sato K, Iwai A, Nakayama Y, Morimoto J, Takada A, et al. (2012) Osteopontin is critical to determine symptom severity of influenza through the regulation of NK cell population. Biochem Biophys Res Commun 417: 274-279.
61. Takahashi F, Takahashi K, Okazaki T, Maeda K, Ienaga H, et al. (2001) Role of osteopontin in the pathogenesis of bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 24: 264-271. (Pubitemid 32228374)
62. Kohan M, Breuer R, Berkman N (2009) Osteopontin Induces Airway Remodeling and Lung Fibroblast Activation in a Murine Model of Asthma. American Journal of Respiratory Cell and Molecular Biology 41: 290-296.
63. Alvarez-Rodriguez L, Lopez-Hoyos M, Munoz-Cacho P, Martinez-Taboada VM (2012) Aging is associated with circulating cytokine dysregulation. Cell Immunol 273: 124-132.
64. Lowery EM, Brubaker AL, Kuhlmann E, Kovacs EJ (2013) The aging lung. Clin Interv Aging 8: 1489-1496.
65. Camous X, Pera A, Solana R, Larbi A (2012) NK Cells in Healthy Aging and Age-Associated Diseases. Journal of Biomedicine and Biotechnology 2012: 8.
66. Harker JA, Godlee A, Wahlsten JL, Lee DC, Thorne LG, et al. (2010) Interleukin 18 coexpression during respiratory syncytial virus infection results in enhanced disease mediated by natural killer cells. J Virol 84: 4073-4082.