Eosinophils promote antiviral immunity in mice infected with influenza A virus

Journal of Immunology

Volumn 198, Issue 8, 2017, Pages 3214-3226

  Samarasinghe, Amali E ^a,b   Melo, Rossana C N ^c   Duan, Susu ^b   Le Messurier, Kim S ^a   Liedmann, Swantje ^b   Surman, Sherri L ^b   Lee, James J ^d   Hurwitz, Julia L ^b   Thomas, Paul G ^b   McCullers, Jonathan A ^a,b  

^a LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^d MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL FUNCTION; CELL TRANSPORT; CONTROLLED STUDY; DEGRANULATION; DISEASE ACTIVITY; EOSINOPHIL; FEMALE; IMMUNE RESPONSE; IN VITRO STUDY; INFLUENZA A; INFLUENZA A VIRUS; INNATE IMMUNITY; LOEFFLER PNEUMONIA; LUNG COMPLIANCE; LYMPHOCYTE COUNT; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; UPREGULATION; VIRUS IDENTIFICATION; VIRUS STRAIN; ANIMAL; ASTHMA; CD8+ T LYMPHOCYTE; COMPLICATION; CONFOCAL MICROSCOPY; DISEASE MODEL; FLOW CYTOMETRY; HYPERSENSITIVITY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; ORTHOMYXOVIRUS INFECTION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ASTHMA; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; EOSINOPHILS; FLOW CYTOMETRY; HYPERSENSITIVITY; INFLUENZA A VIRUS; LYMPHOCYTE ACTIVATION; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; ORTHOMYXOVIRIDAE INFECTIONS; PULMONARY EOSINOPHILIA;

EID: 85017399812     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600787     Document Type: Article

References (66)

1. Allard, R., P. Leclerc, C. Tremblay, and T. N. Tannenbaum. 2010. Diabetes and the severity of pandemic influenza A (H1N1) infection. Diabetes Care 33: 1491-1493.
2. Jain, S., L. Kamimoto, A. M. Bramley, A. M. Schmitz, S. R. Benoit, J. Louie, D. E. Sugerman, J. K. Druckenmiller, K. A. Ritger, R. Chugh, et al. 2009. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N. Engl. J. Med. 361: 1935-1944.
3. Nguyen-Van-Tam, J. S., P. J. M. Openshaw, A. Hashim, E. M. Gadd, W. S. Lim, M. G. Semple, R. C. Read, B. L. Taylor, S. J. Brett, J. McMenamin, et al. 2010. Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May-6666September 2009). Thorax 65: 645-651.
4. Dawood, F. S., L. Kamimoto, T. A. D'Mello, A. Reingold, K. Gershman, J. Meek, K. E. Arnold, M. Farley, P. Ryan, R. Lynfield, et al. 2011. Children with asthma hospitalized with seasonal or pandemic influenza, 2003-2009. Pediatrics 128: e27-e32.
5. Van Kerkhove, M. D., K. A. Vandemaele, V. Shinde, G. Jaramillo-Gutierrez, A. Koukounari, C. A. Donnelly, L. O. Carlino, R. Owen, B. Paterson, L. Pelletier, et al. 2011. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: A global pooled analysis. PLoS Med. 8: e1001053.
6. Gilca, R., G. De Serres, N. Boulianne, N. Ouhoummane, J. Papenburg, M. Douville-Fradet, É . Fortin, M. Dionne, G. Boivin, and D. M. Skowronski. 2011. Risk factors for hospitalization and severe outcomes of 2009 pandemic H1N1 influenza in Quebec, Canada. Influenza Other Respi. Viruses 5: 247-255.
7. Louie, J. K., M. Acosta, K. Winter, C. Jean, S. Gavali, R. Schechter, D. Vugia, K. Harriman, B. Matyas, C. A. Glaser, et al. 2009. Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA 302: 1896-1902.
8. Vaillant, L., G. La Ruche, A. Tarantola, and P. Barboza, Epidemic Intelligence Team at InVS. 2009. Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009. Euro Surveill. 14: pii=19309.
9. Bramley, A. M., S. Dasgupta, J. Skarbinski, L. Kamimoto, A. M. Fry, L. Finelli, and S. Jain, 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team. 2012. Intensive care unit patients with 2009 pandemic influenza A (H1N1pdm09) virus infection-United States, 2009. Influenza Other Respi. Viruses 6: e134-e142.
10. Myles, P., J. S. Nguyen-Van-Tam, M. G. Semple, S. J. Brett, B. Bannister, R. C. Read, B. L. Taylor, J. McMenamin, J. E. Enstone, K. G. Nicholson, et al. 2013. Differences between asthmatics and nonasthmatics hospitalised with influenza A infection. Eur. Respir. J. 41: 824-831.
11. Yang, J. W., L. C. Fan, X. Y. Miao, B. Mao, M. H. Li, H. W. Lu, S. Liang, and J. F. Xu. 2015. Corticosteroids for the treatment of human infection with influenza virus: A systematic review and meta-analysis. Clin. Microbiol. Infect. 21: 956-963.
12. Nedel, W. L., D. G. Nora, J. I. Salluh, T. Lisboa, and P. Póvoa. 2016. Corticosteroids for severe influenza pneumonia: A critical appraisal. World J. Crit. Care Med. 5: 89-95.
13. Samarasinghe, A. E., S. N. Woolard, K. L. Boyd, S. A. Hoselton, J. M. Schuh, and J. A. McCullers. 2014. The immune profile associated with acute allergic asthma accelerates clearance of influenza virus. Immunol. Cell Biol. 92: 449-459.
14. Fraenkel, D. J., P. G. Bardin, G. Sanderson, F. Lampe, S. L. Johnston, and S. T. Holgate. 1995. Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects. Am. J. Respir. Crit. Care Med. 151: 879-886.
15. Kimpen, J. L., R. Garofalo, R. C. Welliver, and P. L. Ogra. 1992. Activation of human eosinophils in vitro by respiratory syncytial virus. Pediatr. Res. 32: 160-164.
16. Domachowske, J. B., C. A. Bonville, K. D. Dyer, and H. F. Rosenberg. 1998. Evolution of antiviral activity in the ribonuclease A gene superfamily: evidence for a specific interaction between eosinophil-derived neurotoxin (EDN/RNase 2) and respiratory syncytial virus. Nucleic Acids Res. 26: 5327-5332.
17. Domachowske, J. B., K. D. Dyer, A. G. Adams, T. L. Leto, and H. F. Rosenberg. 1998. Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res. 26: 3358-3363.
18. Phipps, S., C. E. Lam, S. Mahalingam, M. Newhouse, R. Ramirez, H. F. Rosenberg, P. S. Foster, and K. I. Matthaei. 2007. Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood 110: 1578-1586.
19. Adamko, D. J., B. L. Yost, G. J. Gleich, A. D. Fryer, and D. B. Jacoby. 1999. Ovalbumin sensitization changes the inflammatory response to subsequent parainfluenza infection. Eosinophils mediate airway hyperresponsiveness, m(2) muscarinic receptor dysfunction, and antiviral effects. J. Exp. Med. 190: 1465-1478.
20. Percopo, C. M., K. D. Dyer, S. I. Ochkur, J. L. Luo, E. R. Fischer, J. J. Lee, N. A. Lee, J. B. Domachowske, and H. F. Rosenberg. 2014. Activated mouse eosinophils protect against lethal respiratory virus infection. Blood 123: 743-752.
21. Dyer, K. D., J. M. Moser, M. Czapiga, S. J. Siegel, C. M. Percopo, and H. F. Rosenberg. 2008. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J. Immunol. 181: 4004-4009.
22. La Gruta, N. L., W. T. Rothwell, T. Cukalac, N. G. Swan, S. A. Valkenburg, K. Kedzierska, P. G. Thomas, P. C. Doherty, and S. J. Turner. 2010. Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120: 1885-1894.
23. Crowe, S. R., S. J. Turner, S. C. Miller, A. D. Roberts, R. A. Rappolo, P. C. Doherty, K. H. Ely, and D. L. Woodland. 2003. Differential antigen presentation regulates the changing patterns of CD8+ T cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 198: 399-410.
24. Karttunen, J., and N. Shastri. 1991. Measurement of ligand-induced activation in single viable T cells using the lacZ reporter gene. Proc. Natl. Acad. Sci. USA 88: 3972-3976.
25. Sanderson, S., and N. Shastri. 1994. LacZ inducible, antigen/MHC-specific T cell hybrids. Int. Immunol. 6: 369-376.
26. Melo, R. C. N., and P. F. Weller. 2010. Piecemeal degranulation in human eosinophils: A distinct secretion mechanism underlying inflammatory responses. Histol. Histopathol. 25: 1341-1354.
27. Yewdell, J. W., E. Frank, and W. Gerhard. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. J. Immunol. 126: 1814-1819.
28. Ghosh, S., A. E. Samarasinghe, S. A. Hoselton, G. P. Dorsam, and J. M. Schuh. 2014. Hyaluronan deposition and co-localization with inflammatory cells and collagen in a murine model of fungal allergic asthma. Inflamm. Res. 63: 475-484.
29. Hoselton, S. A., A. E. Samarasinghe, J. M. Seydel, and J. M. Schuh. 2010. An inhalation model of airway allergic response to inhalation of environmental Aspergillus fumigatus conidia in sensitized BALB/c mice. Med. Mycol. 48: 1056-1065.
30. Samarasinghe, A. E., S. A. Hoselton, and J. M. Schuh. 2011. A comparison between intratracheal and inhalation delivery of Aspergillus fumigatus conidia in the development of fungal allergic asthma in C57BL/6 mice. Fungal Biol. 115: 21-29.
31. Shi, H. Z., A. Humbles, C. Gerard, Z. Jin, and P. F. Weller. 2000. Lymph node trafficking and antigen presentation by endobronchial eosinophils. J. Clin. Invest. 105: 945-953.
32. Carretero, R., I. M. Sektioglu, N. Garbi, O. C. Salgado, P. Beckhove, and G. J. Hämmerling. 2015. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat. Immunol. 16: 609-617.
33. Ogbogu, P. U., D. R. Rosing, and M. K. Horne, III. 2007. Cardiovascular manifestations of hypereosinophilic syndromes. Immunol. Allergy Clin. North Am. 27: 457-475.
34. Neuwirth, A., J. Dobes, J. Oujezdská, O. Ballek, M. Benesová, Z. Sumník, J. Vceláková, S. Kolousková, B. Obermannová, M. Kolár, et al. 2012. Eosinophils from patients with type 1 diabetes mellitus express high level of myeloid alpha-defensins and myeloperoxidase. Cell. Immunol. 273: 158-163.
35. McKenna, J. J., A. M. Bramley, J. Skarbinski, A. M. Fry, L. Finelli, and S. Jain, 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team. 2013. Asthma in patients hospitalized with pandemic influenza A(H1N1)pdm09 virus infection-United States, 2009. BMC Infect. Dis. 13: 57.
36. Dyer, K. D., C. M. Percopo, E. R. Fischer, S. J. Gabryszewski, and H. F. Rosenberg. 2009. Pneumoviruses infect eosinophils and elicit MyD88-dependent release of chemoattractant cytokines and interleukin-6. Blood 114: 2649-2656.
37. Drake, M. G., E. R. Bivins-Smith, B. J. Proskocil, Z. Nie, G. D. Scott, J. J. Lee, N. A. Lee, A. D. Fryer, and D. B. Jacoby. 2016. Human and mouse eosinophils have antiviral activity against parainfluenza virus. Am. J. Respir. Cell Mol. Biol. 55: 387-394.
38. Yang, D., Q. Chen, H. F. Rosenberg, S. M. Rybak, D. L. Newton, Z. Y. Wang, Q. Fu, V. T. Tchernev, M. Wang, B. Schweitzer, et al. 2004. Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. J. Immunol. 173: 6134-6142.
39. Lotfi, R., and M. T. Lotze. 2008. Eosinophils induce DC maturation, regulating immunity. J. Leukoc. Biol. 83: 456-460.
40. Bender, B. S., T. Croghan, L. Zhang, and P. A. Small, Jr. 1992. Transgenic mice lacking class I major histocompatibility complex-restricted T cells have delayed viral clearance and increased mortality after influenza virus challenge. J. Exp. Med. 175: 1143-1145.
41. Topham, D. J., R. A. Tripp, and P. C. Doherty. 1997. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159: 5197-5200.
42. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
43. Hamilton-Easton, A., and M. Eichelberger. 1995. Virus-specific antigen presentation by different subsets of cells from lung and mediastinal lymph node tissues of influenza virus-infected mice. J. Virol. 69: 6359-6366.
44. Miller, M. A., A. P. Ganesan, N. Luckashenak, M. Mendonca, and L. C. Eisenlohr. 2015. Endogenous antigen processing drives the primary CD4+ T cell response to influenza. Nat. Med. 21: 1216-1222.
45. Lucey, D. R., A. Nicholson-Weller, and P. F. Weller. 1989. Mature human eosinophils have the capacity to express HLA-DR. Proc. Natl. Acad. Sci. USA 86: 1348-1351.
46. Del Pozo, V., B. De Andrés, E. Martín, B. Cárdaba, J. C. Fernández, S. Gallardo, P. Tramón, F. Leyva-Cobian, P. Palomino, and C. Lahoz. 1992. Eosinophil as antigen-presenting cell: activation of T cell clones and T cell hybridoma by eosinophils after antigen processing. Eur. J. Immunol. 22: 1919-1925.
47. Sedgwick, J. B., W. J. Calhoun, R. F. Vrtis, M. E. Bates, P. K. McAllister, and W. W. Busse. 1992. Comparison of airway and blood eosinophil function after in vivo antigen challenge. J. Immunol. 149: 3710-3718.
48. Weller, P. F., T. H. Rand, T. Barrett, A. Elovic, D. T. Wong, and R. W. Finberg. 1993. Accessory cell function of human eosinophils. HLA-DR-dependent, MHC-restricted antigen-presentation and IL-1 alpha expression. J. Immunol. 150: 2554-2562.
49. Ohkawara, Y., K. G. Lim, Z. Xing, M. Glibetic, K. Nakano, J. Dolovich, K. Croitoru, P. F. Weller, and M. Jordana. 1996. CD40 expression by human peripheral blood eosinophils. J. Clin. Invest. 97: 1761-1766.
50. Woerly, G., N. Roger, S. Loiseau, D. Dombrowicz, A. Capron, and M. Capron. 1999. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon gamma): inhibition by immunoglobulin a complexes. J. Exp. Med. 190: 487-495.
51. Spencer, L. A., C. T. Szela, S. A. Perez, C. L. Kirchhoffer, J. S. Neves, A. L. Radke, and P. F. Weller. 2009. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J. Leukoc. Biol. 85: 117-123.
52. van Rijt, L. S., N. Vos, D. Hijdra, V. C. de Vries, H. C. Hoogsteden, and B. N. Lambrecht. 2003. Airway eosinophils accumulate in the mediastinal lymph nodes but lack antigen-presenting potential for naive T cells. J. Immunol. 171: 3372-3378.
53. MacKenzie, J. R., J. Mattes, L. A. Dent, and P. S. Foster. 2001. Eosinophils promote allergic disease of the lung by regulating CD4(+) Th2 lymphocyte function. J. Immunol. 167: 3146-3155.
54. Wang, H. B., I. Ghiran, K. Matthaei, and P. F. Weller. 2007. Airway eosinophils: allergic inflammation recruited professional antigen-presenting cells. J. Immunol. 179: 7585-7592.
55. Jacobsen, E. A., A. D. Doyle, D. C. Colbert, K. R. Zellner, C. A. Protheroe, W. E. LeSuer, N. A. Lee, and J. J. Lee. 2015. Differential activation of airway eosinophils induces IL-13-mediated allergic Th2 pulmonary responses in mice. Allergy 70: 1148-1159.
56. Throsby, M., A. Herbelin, J. M. Pléau, and M. Dardenne. 2000. CD11c+ eosinophils in the murine thymus: developmental regulation and recruitment upon MHC class I-restricted thymocyte deletion. J. Immunol. 165: 1965-1975.
57. Shi, H. Z., C. Q. Xiao, C. Q. Li, X. Y. Mo, Q. L. Yang, J. Leng, and Y. Q. Chen. 2004. Endobronchial eosinophils preferentially stimulate T helper cell type 2 responses. Allergy 59: 428-435.
58. Duez, C., A. Dakhama, A. Tomkinson, P. Marquillies, A. Balhorn, A. B. Tonnel, D. L. Bratton, and E. W. Gelfand. 2004. Migration and accumulation of eosinophils toward regional lymph nodes after airway allergen challenge. J. Allergy Clin. Immunol. 114: 820-825.
59. Lim, K., Y. M. Hyun, K. Lambert-Emo, T. Capece, S. Bae, R. Miller, D. J. Topham, and M. Kim. 2015. Neutrophil trails guide influenza-specific CD8+ T cells in the airways. Science 349: aaa4352.
60. Tate, M. D., Y. M. Deng, J. E. Jones, G. P. Anderson, A. G. Brooks, and P. C. Reading. 2009. Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J. Immunol. 183: 7441-7450.
61. Tate, M. D., L. J. Ioannidis, B. Croker, L. E. Brown, A. G. Brooks, and P. C. Reading. 2011. The role of neutrophils during mild and severe influenza virus infections of mice. PLoS One 6: e17618.
62. Tate, M. D., A. G. Brooks, P. C. Reading, and J. D. Mintern. 2012. Neutrophils sustain effective CD8(+) T-cell responses in the respiratory tract following influenza infection. Immunol. Cell Biol. 90: 197-205.
63. Fernandez-Sesma, A., S. Marukian, B. J. Ebersole, D. Kaminski, M. S. Park, T. Yuen, S. C. Sealfon, A. García-Sastre, and T. M. Moran. 2006. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 80: 6295-6304.
64. Oh, S., J. M. McCaffery, and M. C. Eichelberger. 2000. Dose-dependent changes in influenza virus-infected dendritic cells result in increased allogeneic T-cell proliferation at low, but not high, doses of virus. J. Virol. 74: 5460-5469.
65. Jacobsen, E. A., K. R. Zellner, D. Colbert, N. A. Lee, and J. J. Lee. 2011. Eosinophils regulate dendritic cells and Th2 pulmonary immune responses following allergen provocation. J. Immunol. 187: 6059-6068.
66. Lee, J. J., E. A. Jacobsen, M. P. McGarry, R. P. Schleimer, and N. A. Lee. 2010. Eosinophils in health and disease: The LIAR hypothesis. Clin. Exp. Allergy 40: 563-575.