Acute clearance of human metapneumovirus occurs independently of natural killer cells

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10963-10969

  Wen, Sherry C ^a   Tollefson, Sharon J ^a   Johnson, Monika ^a   Gilchuk, Pavlo ^a   Boyd, Kelli L ^a   Shepherd, Bryan ^a   Joyce, Sebastian ^a   Williams, John V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; PROGRAMMED DEATH 1 RECEPTOR; CYTOKINE;

ADAPTIVE IMMUNITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HISTOPATHOLOGY; HUMAN; HUMAN METAPNEUMOVIRUS; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG ALVEOLUS CELL; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL DEPLETION; VIRAL CLEARANCE; VIRUS LOAD; VIRUS TITRATION; ANIMAL; C57BL MOUSE; IMMUNOLOGY; LUNG; METAPNEUMOVIRUS; PARAMYXOVIRUS INFECTION; PHYSIOLOGY; T LYMPHOCYTE; VIROLOGY;

ANIMALS; CYTOKINES; HUMANS; KILLER CELLS, NATURAL; LUNG; METAPNEUMOVIRUS; MICE; MICE, INBRED C57BL; PARAMYXOVIRIDAE INFECTIONS; T-LYMPHOCYTES;

EID: 84906342669     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01558-14     Document Type: Article

References (51)

1. van den Hoogen BG, de Jong JC, Groen J, Kuiken T, de Groot R, Fouchier RA, Osterhaus AD. 2001. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat. Med. 7:719-724. http://dx.doi.org/10.1038/89098.
2. Williams JV. 2005. Human metapneumovirus: an important cause of respiratory disease in children and adults. Curr. Infect. Dis. Rep. 7:204-210. http://dx.doi.org/10.1007/s11908-005-0036-7.
3. Bukowski JF, Woda BA, Welsh RM. 1984. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52:119-128.
4. Lanier LL. 2008. Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 8:259-268. http://dx.doi.org/10.1038/nri2276.
5. Rager-Zisman B, Quan PC, Rosner M, Moller JR, Bloom BR. 1987. Role of NK cells in protection of mice against herpes simplex virus-1 infection. J. Immunol. 138:884-888.
6. Pak-Wittel MA, Yang L, Sojka DK, Rivenbark JG, Yokoyama WM. 2013. Interferon-γ mediates chemokine-dependent recruitment of natural killer cells during viral infection. Proc. Natl. Acad. Sci. U. S. A. 110: E50-E59. http://dx.doi.org/10.1073/pnas.1220456110.
7. Orange JS. 2013. Natural killer cell deficiency. J. Allergy Clin. Immunol. 132:515-525. http://dx.doi.org/10.1016/j.jaci.2013.07.020.
8. Stein-Streilein J, Guffee J, Fan W. 1988. Locally and systemically derived natural killer cells participate in defense against intranasally inoculated influenza virus. Reg. Immunol. 1:100-105.
9. Harker JA, Godlee A, Wahlsten JL, Lee DC, Thorne LG, Sawant D, Tregoning JS, Caspi RR, Bukreyev A, Collins PL, Openshaw PJ. 2010. Interleukin 18 coexpression during respiratory syncytial virus infection results in enhanced disease mediated by natural killer cells. J. Virol. 84: 4073-4082. http://dx.doi.org/10.1128/JVI.02014-09.
10. Zhou G, Juang SW, Kane KP. 2013. NK cells exacerbate the pathology of influenza virus infection in mice. Eur. J. Immunol. 43:929-938. http://dx .doi.org/10.1002/eji.201242620.
11. Williams JV, Tollefson SJ, Johnson JE, Crowe JE, Jr. 2005. The cotton rat (Sigmodon hispidus) is a permissive small animal model of human metapneumovirus infection, pathogenesis, and protective immunity. J. Virol. 79:10944-10951. http://dx.doi.org/10.1128/JVI.79.17.10944-10951.2005.
12. Alter G, Malenfant JM, Altfeld M. 2004. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294:15-22. http://dx.doi.org/10.1016/j.jim.2004.08.008.
13. Erickson JJ, Gilchuk P, Hastings AK, Tollefson SJ, Johnson M, Downing MB, Boyd KL, Johnson JE, Kim AS, Joyce S, Williams JV. 2012. Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J. Clin. Invest. 122:2967-2982. http://dx.doi.org/10.1172/JCI62860.
14. Werfel T, Boeker M, Kapp A. 1997. Rapid expression of the CD69 antigen on T cells and natural killer cells upon antigenic stimulation of peripheral blood mononuclear cell suspensions. Allergy 52:465-469. http: //dx.doi.org/10.1111/j.1398-9995.1997.tb01031.x.
15. Biacchesi S, Pham QN, Skiadopoulos MH, Murphy BR, Collins PL, Buchholz UJ. 2005. Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J. Virol. 79:12608-12613. http://dx.doi.org/10.1128/JVI.79.19.12608 -12613.2005.
16. Abdul-Careem MF, Mian MF, Yue G, Gillgrass A, Chenoweth MJ, Barra NG, Chew MV, Chan T, Al-Garawi AA, Jordana M, Ashkar AA. 2012. Critical role of natural killer cells in lung immunopathology during influenza infection in mice. J. Infect. Dis. 206:167-177. http://dx.doi.org/10 .1093/infdis/jis340.
17. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, Angelosanto JM, Laidlaw BJ, Yang CY, Sathaliyawala T, Kubota M, Turner D, Diamond JM, Goldrath AW, Farber DL, Collman RG, Wherry EJ, Artis D. 2011. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12:1045- 1054. http://dx.doi.org/10.1038/ni.2131.
18. Alvarez R, Harrod KS, Shieh WJ, Zaki S, Tripp RA. 2004. Human metapneumovirus persists in BALB/c mice despite the presence of neutralizing antibodies. J. Virol. 78:14003-14011. http://dx.doi.org/10.1128 /JVI.78.24.14003-14011.2004.
19. Liu P, Shu Z, Qin X, Dou Y, Zhao Y, Zhao X. 2013. A live attenuated human metapneumovirus vaccine strain provides complete protection against homologous viral infection and cross-protection against heterologous viral infection in BALB/c mice. Clin. Vaccine Immunol. 20:1246- 1254. http://dx.doi.org/10.1128/CVI.00145-13.
20. Kolli D, Bataki EL, Spetch L, Guerrero-Plata A, Jewell AM, Piedra PA, Milligan GN, Garofalo RP, Casola A. 2008. T lymphocytes contribute to antiviral immunity and pathogenesis in experimental human metapneumovirus infection. J. Virol. 82:8560-8569. http://dx.doi.org/10.1128/JVI .00699-08.
21. Huck B, Neumann-Haefelin D, Schmitt-Graeff A, Weckmann M, Mattes J, Ehl S, Falcone V. 2007. Human metapneumovirus induces more severe disease and stronger innate immune response in BALB/c mice as compared with respiratory syncytial virus. Respir. Res. 8:6. http://dx.doi .org/10.1186/1465-9921-8-6.
22. Hamelin ME, Yim K, Kuhn KH, Cragin RP, Boukhvalova M, Blanco JC, Prince GA, Boivin G. 2005. Pathogenesis of human metapneumovirus lung infection in BALB/c mice and cotton rats. J. Virol. 79:8894-8903. http://dx.doi.org/10.1128/JVI.79.14.8894-8903.2005.
23. Hamelin ME, Prince GA, Gomez AM, Kinkead R, Boivin G. 2006. Human metapneumovirus infection induces long-term pulmonary inflammation associated with airway obstruction and hyperresponsiveness in mice. J. Infect. Dis. 193:1634-1642. http://dx.doi.org/10.1086/504262.
24. Darniot M, Pitoiset C, Petrella T, Aho S, Pothier P, Manoha C. 2009. Age-associated aggravation of clinical disease after primary metapneumovirus infection of BALB/c mice. J. Virol. 83:3323-3332. http://dx.doi.org /10.1128/JVI.02198-08.
25. Darniot M, Petrella T, Aho S, Pothier P, Manoha C. 2005. Immune response and alteration of pulmonary function after primary human metapneumovirus (hMPV) infection of BALB/c mice. Vaccine 23:4473- 4480. http://dx.doi.org/10.1016/j.vaccine.2005.04.027.
26. Chakraborty K, Zhou Z, Wakamatsu N, Guerrero-Plata A. 2012. Interleukin- 12p40 modulates human metapneumovirus-induced pulmonary disease in an acute mouse model of infection. PLoS One 7:e37173. http: //dx.doi.org/10.1371/journal.pone.0037173.
27. Smyth MJ, Crowe NY, Godfrey DI. 2001. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int. Immunol. 13:459-463. http://dx.doi.org/10.1093/intimm/13.4.459.
28. Shi FD, Wang HB, Li H, Hong S, Taniguchi M, Link H, Van Kaer L, Ljunggren HG. 2000. Natural killer cells determine the outcome of B cell-mediated autoimmunity. Nat. Immunol. 1:245-251. http://dx.doi .org/10.1038/79792.
29. Ashkar AA, Rosenthal KL. 2003. Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J. Virol. 77:10168-10171. http://dx.doi.org /10.1128/JVI.77.18.10168-10171.2003.
30. Laffont S, Seillet C, Ortaldo J, Coudert JD, Guery JC. 2008. Natural killer cells recruited into lymph nodes inhibit alloreactive T-cell activation through perforin-mediated killing of donor allogeneic dendritic cells. Blood 112:661-671. http://dx.doi.org/10.1182/blood-2007-10-120089.
31. Cleaver JO, You D, Michaud DR, Pruneda FA, Juarez MM, Zhang J, Weill PM, Adachi R, Gong L, Moghaddam SJ, Poynter ME, Tuvim MJ, Evans SE. 2014. Lung epithelial cells are essential effectors of inducible resistance to pneumonia. Mucosal Immunol. 7:78-88. http://dx.doi.org /10.1038/mi.2013.26.
32. Nishikado H, Mukai K, Kawano Y, Minegishi Y, Karasuyama H. 2011. NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo. J. Immunol. 186:5766-5771. http://dx.doi.org /10.4049/jimmunol.1100370.
33. Suzuki K, Nakazato H, Matsui H, Hasumi M, Shibata Y, Ito K, Fukabori Y, Kurokawa K, Yamanaka H. 2001. NK cell-mediated anti-tumor immune response to human prostate cancer cell, PC-3: immunogene therapy using a highly secretable form of interleukin-15 gene transfer. J. Leukoc. Biol. 69:531-537.
34. Van Kaer L. 2004. Regulation of immune responses by CD1d-restricted natural killer T cells. Immunol. Res. 30:139-153. http://dx.doi.org/10 .1385/IR:30:2:139.
35. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. 2008. Functions of natural killer cells. Nat. Immunol. 9:503-510. http://dx.doi.org/10.1038 /ni1582.
36. - NKT cell population. Proc. Natl. Acad. Sci. U. S. A. 105:11287-11292. http://dx.doi.org/10.1073/pnas.0801631105.
37. Alymova IV, Portner A, Takimoto T, Boyd KL, Babu YS, McCullers JA. 2005. The novel parainfluenza virus hemagglutinin-neuraminidase inhibitor BCX 2798 prevents lethal synergism between a paramyxovirus and Streptococcus pneumoniae. Antimicrob. Agents Chemother. 49:398-405. http://dx.doi.org/10.1128/AAC.49.1.398-405.2005.
38. Tregoning JS, Yamaguchi Y, Harker J, Wang B, Openshaw PJ. 2008. The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J. Virol. 82:4115-4124. http://dx.doi.org/10.1128/JVI.02313-07.
39. Nedvetzki S, Sowinski S, Eagle RA, Harris J, Vely F, Pende D, Trowsdale J, Vivier E, Gordon S, Davis DM. 2007. Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses. Blood 109:3776-3785. http://dx.doi.org/10.1182/blood -2006-10-052977.
40. Herd KA, Mahalingam S, Mackay IM, Nissen M, Sloots TP, Tindle RW. 2006. Cytotoxic T-lymphocyte epitope vaccination protects against human metapneumovirus infection and disease in mice. J. Virol. 80:2034-2044. http://dx.doi.org/10.1128/JVI.80.4.2034-2044.2006.
41. Cook KD, Whitmire JK. 2013. The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J. Immunol. 190:641-649. http://dx.doi.org/10.4049/jimmunol.1202448.
42. Lang PA, Lang KS, Xu HC, Grusdat M, Parish IA, Recher M, Elford AR, Dhanji S, Shaabani N, Tran CW, Dissanayake D, Rahbar R, Ghazarian M, Brustle A, Fine J, Chen P, Weaver CT, Klose C, Diefenbach A, Haussinger D, Carlyle JR, Kaech SM, Mak TW, Ohashi PS. 2012. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl. Acad. Sci. U. S. A. 109:1210-1215. http://dx.doi.org/10.1073/pnas.1118834109.
43. Lünemann A, Lünemann JD, Munz C. 2009. Regulatory NK-cell functions in inflammation and autoimmunity. Mol. Med. 15:352-358. http: //dx.doi.org/10.2119/molmed.2009.00035.
44. Waggoner SN, Cornberg M, Selin LK, Welsh RM. 2012. Natural killer cells act as rheostats modulating antiviral T cells. Nature 481:394-398. http://dx.doi.org/10.1038/nature10624.
45. Noone CM, Paget E, Lewis EA, Loetscher MR, Newman RW, Johnson PA. 2008. Natural killer cells regulate T-cell proliferation during human parainfluenza virus type 3 infection. J. Virol. 82:9299-9302. http://dx.doi .org/10.1128/JVI.00717-08.
46. Hussell T, Openshaw PJ. 1998. Intracellular IFN-γ expression in natural killer cells precedes lung CD8+ T cell recruitment during respiratory syncytial virus infection. J. Gen. Virol. 79:2593-2601.
47. *0702 transgenic, H-2KbDb doubleknockout mice: phenotypical and functional characterization in response to influenza virus. Int. Immunol. 15:765-772. http://dx.doi.org/10.1093 /intimm/dxg073.
48. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77: 4911-4927. http://dx.doi.org/10.1128/JVI.77.8.4911-4927.2003.
49. Flemming A. 2012. Cancer: PD1 makes waves in anticancer immunotherapy. Nat. Rev. Drug Discov. 11:601. http://dx.doi.org/10.1038/nrd3806.
50. Jeisy-Scott V, Kim JH, Davis WG, Cao W, Katz JM, Sambhara S. 2012. TLR7 recognition is dispensable for influenza virus A infection but important for the induction of hemagglutinin-specific antibodies in response to the 2009 pandemic split vaccine in mice. J. Virol. 86:10988-10998. http: //dx.doi.org/10.1128/JVI.01064-12.
51. Laham FR, Israele V, Casellas JM, Garcia AM, Lac Prugent CM, Hoffman SJ, Hauer D, Thumar B, Name MI, Pascual A, Taratutto N, Ishida MT, Balduzzi M, Maccarone M, Jackli S, Passarino R, Gaivironsky RA, Karron RA, Polack NR, Polack FP. 2004. Differential production of inflammatory cytokines in primary infection with human metapneumovirus and with other common respiratory viruses of infancy. J. Infect. Dis. 189:2047-2056. http://dx.doi.org/10.1086/383350.