Live Imaging of Influenza Infection of the Trachea Reveals Dynamic Regulation of CD8+ T Cell Motility by Antigen

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Lambert Emo, Kris ^a   Hyun, Young Min ^a,b   Reilly, Emma ^a   Barilla, Christopher ^a   Gerber, Scott ^a   Fowell, Deborah ^a   Kim, Minsoo ^a   Topham, David J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BROMETHOL; PANCURONIUM BROMIDE; PENTOBARBITAL; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD OXYGEN TENSION; CD8+ T LYMPHOCYTE; CELL MOTILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; IMAGING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOLOGY; INFLUENZA; INFLUENZA A (H3N2); LUNG LAVAGE; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; PULSE OXIMETRY; SPLEEN CELL; STAINING; TRACHEA; TRANSGENIC MOUSE; VIRAL CLEARANCE; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; EPITHELIUM CELL; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; PATHOLOGY; TRACHEITIS; VIROLOGY;

ANIMALS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTES, CYTOTOXIC; TRACHEA; TRACHEITIS;

EID: 84989952346     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005881     Document Type: Article

References (52)

1. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD, Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101(13):4620–4. doi: 10.1073/pnas.030800110115070767; PubMed Central PMCID: PMC384796.
2. Matrosovich M, Zhou N, Kawaoka Y, Webster R, The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol. 1999;73(2):1146–55. 9882316; PubMed Central PMCID: PMCPMC103935.
3. Heider A, Mochalova L, Harder T, Tuzikov A, Bovin N, Wolff T, et al. Alterations in hemagglutinin receptor-binding specificity accompany the emergence of highly pathogenic avian influenza viruses. J Virol. 2015;89(10):5395–405. doi: 10.1128/JVI.03304-1425741006; PubMed Central PMCID: PMCPMC4442535.
4. Hers JF, Disturbances of the ciliated epithelium due to influenza virus. The American review of respiratory disease. 1966;93(Suppl 3):162–77. 5333643.
5. Hers JF, Mulder J, Rapid tentative post-mortem diagnosis of influenza with the aid of cytological smears of the tracheal epithelium. J Pathol Bacteriol. 1951;63(2):329–32. 14851173.
6. Hers JF, Mulder J, Rapid post-mortem diagnosis of influenza by cytologic examination of smears from the tracheal epithelium]. Ned Tijdschr Geneeskd. 1950;94(28):1997–2002. 15439413.
7. Kilbourne ED, Kilbourne ED, Influenza. New York: Plenum Medical Book Company; 1987. 359 p.
8. Tumpey TM, Maines TR, Van Hoeven N, Glaser L, Solorzano A, Pappas C, et al. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science. 2007;315(5812):655–9. Epub 2007/02/03. doi: 10.1126/science.113621217272724.
9. Brankston G, Gitterman L, Hirji Z, Lemieux C, Gardam M, Transmission of influenza A in human beings. Lancet Infect Dis. 2007;7(4):257–65. doi: 10.1016/S1473-3099(07)70029-417376383.
10. Bridges CB, Kuehnert MJ, Hall CB, Transmission of influenza: implications for control in health care settings. Clin Infect Dis. 2003;37(8):1094–101. doi: 10.1086/37829214523774.
11. Hers JF, Mulder J, Broad aspects of the pathology and pathogenesis of human influenza. The American review of respiratory disease. 1961;83(Pt 2):84–97. 13713780.
12. Topham DJ, Tripp RA, Doherty PC, CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J Immunol. 1997;159(11):5197–200. Epub 1998/04/21. 9548456.
13. Hou S, Doherty PC, Clearance of Sendai virus by CD8+ T cells requires direct targeting to virus-infected epithelium. Eur J Immunol. 1995;25(1):111–6. 7843219
14. Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG, Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev. 1997;159:105–17. Epub 1998/01/07. 9416506.
15. Hou S, Doherty PC, Zijlstra M, Jaenisch R, Katz JM, Delayed clearance of Sendai virus in mice lacking class I MHC- restricted CD8+ T cells. J Immunol. 1992;149(4):1319–25. 1354233
16. Eichelberger M, Allan W, Zijlstra M, Jaenisch R, Doherty PC, Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J Exp Med. 1991;174(4):875–80. 1919440
17. Lim K, Hyun YM, Lambert-Emo K, Capece T, Bae S, Miller R, et al. Neutrophil trails guide influenza-specific CD8(+) T cells in the airways. Science. 2015;349(6252):aaa4352. doi: 10.1126/science.aaa435226339033.
18. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol. 2007;171(4):1215–23. 17717141.
19. Lambert-Emo K, Hyun YM, Overstreet MG, Kim M, Fowell DJ, Topham DJ, Influenza Tracheitis: A model system for live imaging of lymphocytes responding to infection of the mucosal epithelium. Manuscript in preparation. 2012.
20. Hers JF, Mudler J, Masurel N, vd KL, Tyrrell DA, Studies on the pathogenesis of influenza virus pneumonia in mice. J Pathol Bacteriol. 1962;83:207–17. 13906877.
21. Westerberg SC, Smith CB, Wiley BB, Jensen CG, Pathogenesis of influenza virus infection in mouse tracheal organ cultures. Proc Soc Exp Biol Med. 1972;140(3):846–51. Epub 1972/07/01. 5039382.
22. Doherty PC, Hamilton-Easton AM, Topham DJ, Riberdy J, Brooks JW, Cardin RD, Consequences of viral infections for lymphocyte compartmentalization and homeostasis. Semin Immunol. 1997;9(6):365–73. Epub 1998/02/07. doi: 10.1006/smim.1997.00949405265.
23. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR, T cell receptor antagonist peptides induce positive selection. Cell. 1994;76(1):17–27. 8287475.
24. Thomas PG, Brown SA, Yue W, So J, Webby RJ, Doherty PC, An unexpected antibody response to an engineered influenza virus modifies CD8+ T cell responses. Proc Natl Acad Sci U S A. 2006. 16473934.
25. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN, Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity. 1997;6(6):715–26. 9208844.
26. Lee HY, Topham DJ, Park SY, Hollenbaugh J, Treanor J, Mosmann TR, et al. Simulation and prediction of the adaptive immune response to influenza A virus infection. J Virol. 2009;83(14):7151–65. Epub 2009/05/15. doi: 10.1128/JVI.00098-0919439465; PubMed Central PMCID: PMC2704765.
27. Topham DJ, Castrucci MR, Wingo FS, Belz GT, Doherty PC, The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J Immunol. 2001;167(12):6983–90. Epub 2001/12/12. 11739518.
28. Polakos NK, Klein I, Richter MV, Zaiss DM, Giannandrea M, Crispe IN, et al. Early intrahepatic accumulation of CD8+ T cells provides a source of effectors for nonhepatic immune responses. J Immunol. 2007;179(1):201–10. Epub 2007/06/21. 17579039.
29. Allan W, Tabi Z, Cleary A, Doherty PC, Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J Immunol. 1990;144(10):3980–6. 1692070
30. Richter M, Ray SJ, Chapman TJ, Austin SJ, Rebhahn J, Mosmann TR, et al. Collagen distribution and expression of collagen-binding alpha1beta1 (VLA-1) and alpha2beta1 (VLA-2) integrins on CD4 and CD8 T cells during influenza infection. J Immunol. 2007;178(7):4506–16. Epub 2007/03/21. 17372009.
31. Looney MR, Thornton EE, Sen D, Lamm WJ, Glenny RW, Krummel MF, Stabilized imaging of immune surveillance in the mouse lung. Nature methods. 2011;8(1):91–6. Epub 2010/12/15. doi: 10.1038/nmeth.154321151136; PubMed Central PMCID: PMC3076005.
32. Verhoeven D, Teijaro JR, Farber DL, Pulse-oximetry accurately predicts lung pathology and the immune response during influenza infection. Virology. 2009;390(2):151–6. Epub 2009/06/06. doi: 10.1016/j.virol.2009.05.00419493556; PubMed Central PMCID: PMC2776688.
33. Lessin AW, Parkes MW, The relation between sedation and body temperature in the mouse. Br J Pharmacol Chemother. 1957;12(2):245–50. 13446381; PubMed Central PMCID: PMCPMC1509669.
34. Gargiulo S, Greco A, Gramanzini M, Esposito S, Affuso A, Brunetti A, et al. Mice anesthesia, analgesia, and care, Part II: anesthetic considerations in preclinical imaging studies. ILAR J. 2012;53(1):E70–81. doi: 10.1093/ilar.53.1.7023382272.
35. Nitsch R, Pohl EE, Smorodchenko A, Infante-Duarte C, Aktas O, Zipp F, Direct impact of T cells on neurons revealed by two-photon microscopy in living brain tissue. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2004;24(10):2458–64. doi: 10.1523/JNEUROSCI.4703-03.200415014121.
36. Matheu MP, Teijaro JR, Walsh KB, Greenberg ML, Marsolais D, Parker I, et al. Three phases of CD8 T cell response in the lung following H1N1 influenza infection and sphingosine 1 phosphate agonist therapy. PLoS One. 2013;8(3):e58033. Epub 2013/03/28. doi: 10.1371/journal.pone.005803323533579; PubMed Central PMCID: PMC3606384.
37. Tripp RA, Hou S, McMickle A, Houston J, Doherty PC, Recruitment and proliferation of CD8+ T cells in respiratory virus infections. J Immunol. 1995;154(11):6013–21. 7751644
38. Wu H, Kumar A, Miao H, Holden-Wiltse J, Mosmann TR, Livingstone AM, et al. Modeling of influenza-specific CD8+ T cells during the primary response indicates that the spleen is a major source of effectors. J Immunol. 2011;187(9):4474–82. Epub 2011/09/29. doi: 10.4049/jimmunol.110144321948988; PubMed Central PMCID: PMC3197949.
39. Beltman JB, Maree AF, de Boer RJ, Analysing immune cell migration. Nat Rev Immunol. 2009;9(11):789–98. doi: 10.1038/nri263819834485.
40. Mrass P, Kinjyo I, Ng LG, Reiner SL, Pure E, Weninger W, CD44 mediates successful interstitial navigation by killer T cells and enables efficient antitumor immunity. Immunity. 2008;29(6):971–85. doi: 10.1016/j.immuni.2008.10.01519100702; PubMed Central PMCID: PMCPMC2757129.
41. Waffarn EE, Baumgarth N, Protective B cell responses to flu—no fluke! J Immunol. 2011;186(7):3823–9. doi: 10.4049/jimmunol.100209021422252; PubMed Central PMCID: PMCPMC3154207.
42. Masopust D, Schenkel JM, The integration of T cell migration, differentiation and function. Nat Rev Immunol. 2013;13(5):309–20. Epub 2013/04/20. doi: 10.1038/nri344223598650.
43. Ariotti S, Beltman JB, Chodaczek G, Hoekstra ME, van Beek AE, Gomez-Eerland R, et al. Tissue-resident memory CD8+ T cells continuously patrol skin epithelia to quickly recognize local antigen. Proc Natl Acad Sci U S A. 2012;109(48):19739–44. doi: 10.1073/pnas.120892710923150545; PubMed Central PMCID: PMCPMC3511734.
44. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN, Localization, quantitation, and in situ detection of specific peptide- MHC class I complexes using a monoclonal antibody. Immunity. 1997;6(6):715–26. 9208844
45. Taubenberger JK, Morens DM, The pathology of influenza virus infections. Annu Rev Pathol. 2008;3:499–522. doi: 10.1146/annurev.pathmechdis.3.121806.15431618039138; PubMed Central PMCID: PMCPMC2504709.
46. Doherty PC, Blanden RV, Zinkernagel RM, Specificity of virus-immune effector T cells for H-2K or H-2D compatible interactions: implications for H-antigen diversity. Transplant Rev. 1976;29:89–124. 58463.
47. Miller MJ, Wei SH, Parker I, Cahalan MD, Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science. 2002;296(5574):1869–73. doi: 10.1126/science.107005112016203.
48. Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, Locksley R, et al. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J Exp Med. 2012;209(6):1183–99. doi: 10.1084/jem.2011266722585735; PubMed Central PMCID: PMCPMC3371730.
49. Richter MV, Topham DJ, The alpha1beta1 integrin and TNF receptor II protect airway CD8+ effector T cells from apoptosis during influenza infection. J Immunol. 2007;179(8):5054–63. Epub 2007/10/04. 17911590.
50. Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, et al. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity. 2004;20(2):167–79. Epub 2004/02/21. 14975239.
51. Yang J, Huck SP, McHugh RS, Hermans IF, Ronchese F, Perforin-dependent elimination of dendritic cells regulates the expansion of antigen-specific CD8+ T cells in vivo. Proc Natl Acad Sci U S A. 2006;103(1):147–52. doi: 10.1073/pnas.050905410316373503; PubMed Central PMCID: PMCPMC1324995.
52. Overstreet MG, Gaylo A, Angermann BR, Hughson A, Hyun YM, Lambert K, et al. Inflammation-induced interstitial migration of effector CD4(+) T cells is dependent on integrin alphaV. Nat Immunol. 2013;14(9):949–58. Epub 2013/08/13. doi: 10.1038/ni.268223933892.