Wild-type coxsackievirus infection dramatically alters the abundance, heterogeneity, and immunostimulatory capacity of conventional dendritic cells in vivo

Virology

Volumn 429, Issue 1, 2012, Pages 74-90

  Kemball, Christopher C ^a   Flynn, Claudia T ^a   Hosking, Martin P ^a   Botten, Jason ^b   Whitton, J Lindsay ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Coxsackievirus; Dendritic cell; Immunity; Infection; Lymphocytic choriomeningitis virus; Mouse; Spleen; T cell

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL POPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; DENDRITIC CELL; DOWN REGULATION; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SECONDARY INFECTION; SPLEEN CELL; UPREGULATION; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; COXSACKIEVIRUS INFECTIONS; DENDRITIC CELLS; ENTEROVIRUS B, HUMAN; HUMANS; MALE; MICE; MICE, INBRED C57BL;

COXSACKIEVIRUS; ENTEROVIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MURINAE;

EID: 84861198703     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.04.005     Document Type: Article

References (89)

1. + T helper cell function in vivo: differential requirement for induction of antiviral cytotoxic T-cell and antibody responses. J. Virol. 1988, 62:2102-2106.
2. Ahmed R., Salmi A., Butler L.D., Chiller J.M., Oldstone M.B.A. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice: role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 1984, 160:521-540.
3. Bautista E.M., Ferman G.S., Golde W.T. Induction of lymphopenia and inhibition of T cell function during acute infection of swine with foot and mouth disease virus (FMDV). Vet. Immunol. Immunopathol. 2003, 92:61-73.
4. + dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 2005, 175:196-200.
5. Choe S.S., Dodd D.A., Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 2005, 337:18-29.
6. Crocker S.J., Frausto R.F., Whitmire J.K., Benning N., Whitton J.L. Amelioration of coxsackievirus B3-mediated myocarditis by inhibition of tissue inhibitors of matrix metalloproteinase-1. Am. J. Pathol. 2007, 171:1762-1773.
7. Daley A.J., Isaacs D., Dwyer D.E., Gilbert G.L. A cluster of cases of neonatal coxsackievirus B meningitis and myocarditis. J. Paediatr. Child Health 1998, 34:196-198.
8. Dalod M., Hamilton T., Salomon R., Salazar-Mather T.P., Henry S.C., Hamilton J.D., Biron C.A. Dendritic cell responses to early murine cytomegalovirus infection: subset functional specialization and differential regulation by interferon alpha/beta. J. Exp. Med. 2003, 197:885-898.
9. Deitz S.B., Dodd D.A., Cooper S., Parham P., Kirkegaard K. MHC I-dependent antigen presentation is inhibited by poliovirus protein 3A. Proc. Nat. Acad. Sci. U.S.A 2000, 97:13790-13795.
10. Díaz-San Segundo F., Salguero F.J., de Avila A., de Marco M.M., Sanchez-Martin M.A., Sevilla N. Selective lymphocyte depletion during the early stage of the immune response to foot-and-mouth disease virus infection in swine. J. Virol. 2006, 80:2369-2379.
11. Dietz W.H., Peralta P.H., Johnson K.M. Ten clinical cases of human infection with venezuelan equine encephalomyelitis virus, subtype I-D. Am. J. Trop. Med. Hyg. 1979, 28:329-334.
12. Dodd D.A., Giddings T.H., Kirkegaard K. Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection. J. Virol. 2001, 75:8158-8165.
13. Dominguez P.M., Ardavin C. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 2010, 234:90-104.
14. Dudziak D., Kamphorst A.O., Heidkamp G.F., Buchholz V.R., Trumpfheller C., Yamazaki S., Cheong C., Liu K., Lee H.W., Park C.G., Steinman R.M., Nussenzweig M.C. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-111.
15. Feuer R., Mena I., Pagarigan R.R., Slifka M.K., Whitton J.L. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J. Virol. 2002, 76:4430-4440.
16. Feuer R., Pagarigan R.R., Harkins S., Liu F., Hunziker I.P., Whitton J.L. Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J. Neurosci. 2005, 25:2434-2444.
17. Geisbert T.W., Hensley L.E., Gibb T.R., Steele K.E., Jaax N.K., Jahrling P.B. Apoptosis induced in vitro and in vivo during infection by Ebola and Marburg viruses. Lab. Invest. 2000, 80:171-186.
18. Gilliet M., Cao W., Liu Y.J. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 2008, 8:594-606.
19. Grubman M.J., Moraes M.P., Diaz-San S.F., Pena L., de los S.T. Evading the host immune response: how foot-and-mouth disease virus has become an effective pathogen. FEMS Immunol. Med. Microbiol. 2008, 53:8-17.
20. +4 in the eukaryotic consensus motif. J. Virol. 2005, 79:987-996.
21. Heath W.R., Carbone F.R. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 2009, 10:1237-1244.
22. + T lymphocytes in coxsackievirus B3-induced myocarditis. J. Virol. 1995, 69:6720-6728.
23. + T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 2008, 9:155-165.
24. Huber S., Ramsingh A.I. Coxsackievirus-induced pancreatitis. Viral Immunol. 2004, 17:358-369.
25. Huhn M.H., McCartney S.A., Lind K., Svedin E., Colonna M., Flodstrom-Tullberg M. Melanoma differentiation-associated protein-5 (MDA-5) limits early viral replication but is not essential for the induction of type 1 interferons after coxsackievirus infection. Virology 2010, 401:42-48.
26. Hunziker I.P., Cornell C.T., Whitton J.L. Deletions within the 5'UTR of coxsackievirus B3: consequences for virus translation and replication. Virology 2007, 360:120-128.
27. Jakel S., Kuckelkorn U., Szalay G., Plotz M., Textoris-Taube K., Opitz E., Klingel K., Stevanovic S., Kandolf R., Kotsch K., Stangl K., Kloetzel P.M., Voigt A. Differential interferon responses enhance viral epitope generation by myocardial immunoproteasomes in murine enterovirus myocarditis. Am. J. Pathol. 2009, 175:510-518.
28. + T cells and nonspecific bone marrow-derived cells. J. Virol. 1987, 61:3930-3937.
29. Kamphuis E., Junt T., Waibler Z., Forster R., Kalinke U. Type I interferons directly regulate lymphocyte recirculation and cause transient blood lymphopenia. Blood 2006, 108:3253-3261.
30. Kastenmuller W., Gerner M.Y., Germain R.N. The in situ dynamics of dendritic cell interactions. Eur. J. Immunol. 2010, 40:2103-2106.
31. Kemball C.C., Alirezaei M., Whitton J.L. Type B coxsackieviruses and their interactions with the innate and adaptive immune systems. Future Microbiol. 2010, 5:1329-1347.
32. Kemball C.C., Fujinami R.S., Whitton J.L. Adaptive immune responses to picornaviruses. The Picornaviruses 2010, 303-319. ASM Press, Washington, D.C. E. Ehrenfeld, E. Domingo, R.P. Roos (Eds.).
33. Kemball C.C., Harkins S., Whitmire J.K., Flynn C.T., Feuer R., Whitton J.L. Coxsackievirus B3 inhibits antigen presentation in vivo, exerting a profound and selective effect on the MHC class I pathway. PLoS Pathog. 2009, 5:e1000618.
34. + T cells in lymphoid and peripheral sites of coxsackievirus B3 infection. J. Virol. 2008, 82:4331-4342.
35. Knowlton K.U., Jeon E.S., Berkley N., Wessely R., Huber S.A. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J. Virol. 1996, 70:7811-7818.
36. Kramer M., Schulte B.M., Toonen L.W., de Bruijni M.A., Galama J.M., Adema G.J., van Kuppeveld F.J. Echovirus infection causes rapid loss-of-function and cell death in human dendritic cells. Cell. Microbiol. 2007, 9:1507-1518.
37. Lee H.K., Iwasaki A. Innate control of adaptive immunity: dendritic cells and beyond. Semin. Immunol. 2007, 19:48-55.
38. Lee L.N., Burke S., Montoya M., Borrow P. Multiple mechanisms contribute to impairment of type 1 interferon production during chronic lymphocytic choriomeningitis virus infection of mice. J. Immunol. 2009, 182:7178-7189.
39. Leon B., Ardavin C. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 2008, 86:320-324.
40. Lopez-Bravo M., Ardavin C. In vivo induction of immune responses to pathogens by conventional dendritic cells. Immunity 2008, 29:343-351.
41. Luber C.A., Cox J., Lauterbach H., Fancke B., Selbach M., Tschopp J., Akira S., Wiegand M., Hochrein H., O'Keeffe M., Mann M. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 2010, 32:279-289.
42. Mena I., Fischer C., Gebhard J.R., Perry C.M., Harkins S., Whitton J.L. Coxsackievirus infection of the pancreas: evaluation of receptor expression, pathogenesis, and immunopathology. Virology 2000, 271:276-288.
43. Modlin J.F., Rotbart H.A. Group B coxsackie disease in children. Curr. Top. Microbiol. Immunol. 1997, 223:53-80.
44. Montoya M., Edwards M.J., Reid D.M., Borrow P. Rapid activation of spleen dendritic cell subsets following lymphocytic choriomeningitis virus infection of mice: analysis of the involvement of type 1 IFN. J. Immunol. 2005, 174:1851-1861.
45. Mukherjee A., Morosky S.A., Delorme-Axford E., Dybdahl-Sissoko N., Oberste M.S., Wang T., Coyne C.B. The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host Type I interferon and apoptotic signaling. PLoS Pathog. 2011, 7:e1001311.
46. Neznanov N., Kondratova A., Chumakov K.M., Angres B., Zhumabayeva B., Agol V.I., Gudkov A.V. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface. J. Virol. 2001, 75:10409-10420.
47. Nfon C.K., Toka F.N., Kenney M., Pacheco J.M., Golde W.T. Loss of plasmacytoid dendritic cell function coincides with lymphopenia and viremia during foot-and-mouth disease virus infection. Viral Immunol. 2010, 23:29-41.
48. + T cells by infected dendritic cells in vivo. Nat. Immunol. 2002, 3:265-271.
49. O'Connell J.B. The role of myocarditis in end-stage dilated cardiomyopathy. Tex. Heart Inst. J. 1987, 14:268-275.
50. O'Donnell D.R., Carrington D. Peripheral blood lymphopenia and neutrophilia in children with severe respiratory syncytial virus disease. Pediatr. Pulmonol. 2002, 34:128-130.
51. Okada H., Kobune F., Sato T.A., Kohama T., Takeuchi Y., Abe T., Takayama N., Tsuchiya T., Tashiro M. Extensive lymphopenia due to apoptosis of uninfected lymphocytes in acute measles patients. Arch. Virol. 2000, 145:905-920.
52. + T cells during reconstitution of lymphopenic environments. J. Immunol. 2003, 171:655-663.
53. Pircher H., Moskophidis D., Rohrer U., Burki K., Hengartner H., Zinkernagel R.M. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 1990, 346:629-633.
54. Probst H.C., van den B.M. Priming of CTLs by lymphocytic choriomeningitis virus depends on dendritic cells. J. Immunol. 2005, 174:3920-3924.
55. Rahnefeld A., Ebstein F., Albrecht N., Opitz E., Kuckelkorn U., Stangl K., Rehm A., Kloetzel P.M., Voigt A. Antigen-presentation capacity of dendritic cells is impaired in ongoing enterovirus myocarditis. Eur. J. Immunol. 2011.
56. Rhoades R.E., Tabor-Godwin J.M., Tsueng G., Feuer R. Enterovirus infections of the central nervous system. Virology 2011, 411:288-305.
57. Romero J.R. Pediatric group B coxsackievirus infections. Curr. Top. Microbiol. Immunol. 2008, 323:223-239.
58. Schattner A., Meshorer A., Wallach D. Involvement of interferon in virus-induced lymphopenia. Cell Immunol. 1983, 79:11-25.
59. Schulte B.M., Kramer M., Ansems M., Lanke K.H., van Doremalen N., Piganelli J.D., Bottino R., Trucco M., Galama J.M., Adema G.J., van Kuppeveld F.J. Phagocytosis of enterovirus-infected pancreatic Β-cells triggers innate immune responses in human dendritic cells. Diabetes 2010, 59:1182-1191.
60. Segura E., Villadangos J.A. Antigen presentation by dendritic cells in vivo. Curr. Opin. Immunol. 2009, 21:105-110.
61. Shen Z., Reznikoff G., Dranoff G., Rock K.L. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 1997, 158:2723-2730.
62. + dendritic cell subset. Immunol. Rev. 2010, 234:18-31.
63. + T cells during picornavirus infection. J. Virol. 2001, 75:2377-2387.
64. + T cells without selection of higher affinity TCR. Nat. Immunol. 2001, 2:711-717.
65. Sole M.J., Liu P. Viral myocarditis: a paradigm for understanding the pathogenesis and treatment of dilated cardiomyopathy. J. Am. Coll. Cardiol. 1993, 22:99A-105A.
66. Swiecki M., Colonna M. Accumulation of plasmacytoid DC: roles in disease pathogenesis and targets for immunotherapy. Eur. J. Immunol. 2010, 40:2094-2098.
67. Swiecki M., Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 2010, 234:142-162.
68. Tabor-Godwin J.M., Ruller C.M., Bagalso N., An N., Pagarigan R.R., Harkins S., Gilbert P.E., Kiosses W.B., Gude N.A., Cornell C.T., Doran K.S., Sussman M.A., Whitton J.L., Feuer R. A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J. Neurosci. 2010, 30:8676-8691.
69. Tam P.E. Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol. 2006, 19:133-146.
70. Tracy S., Chapman N.M. Group B coxsackievirus diseases. Picornaviruses: Molecular Biology 2010, 353-368. Evolution and Pathogenesis. ASM. E. Ehrenfeld, E. Domingo, R.P. Roos (Eds.).
71. van Houten N., Bouchard P.E., Moraska A., Huber S.A. Selection of an attenuated coxsackievirus B3 variant, using a monoclonal antibody reactive to myocyte antigen. J. Virol. 1991, 65:1286-1290.
72. Varela-Calvino R., Skowera A., Arif S., Peakman M. Identification of a naturally processed cytotoxic CD8 T-cell epitope of coxsackievirus B4, presented by HLA-A2.1 and located in the PEVKEK region of the P2C nonstructural protein. J. Virol. 2004, 78:13399-13408.
73. Villadangos J.A., Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 2007, 7:543-555.
74. Villadangos J.A., Young L. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 2008, 29:352-361.
75. Voigt A., Jakel S., Textoris-Taube K., Keller C., Drung I., Szalay G., Klingel K., Henklein P., Stangl K., Kloetzel P.M., Kuckelkorn U. Generation of in silico predicted coxsackievirus B3-derived MHC class I epitopes by proteasomes. Amino Acids 2010, 39:243-255.
76. Wahid R., Cannon M.J., Chow M. Dendritic cells and macrophages are productively infected by poliovirus. J. Virol. 2005, 79:401-409.
77. Wang J.P., Asher D.R., Chan M., Kurt-Jones E.A., Finberg R.W. Cutting edge: antibody-mediated TLR7-dependent recognition of viral RNA. J. Immunol. 2007, 178:3363-3367.
78. Wang J.P., Cerny A., Asher D.R., Kurt-Jones E.A., Bronson R.T., Finberg R.W. MDA5 and MAVS mediate type I IFN responses to coxsackie B virus. J. Virol. 2010, 84:254-260.
79. + T-cell epitopes shared among group B enteroviruses. J. Gen. Virol. 2008, 89:2090-2097.
80. + dendritic cells define a protective phenotype in the mouse model of coxsackievirus myocarditis. J. Virol. 2008, 82:8149-8160.
81. Weslow-Schmidt J.L., Jewell N.A., Mertz S.E., Simas J.P., Durbin J.E., Flano E. Type I interferon inhibition and dendritic cell activation during gammaherpesvirus respiratory infection. J. Virol. 2007, 81:9778-9789.
82. Wessely R., Klingel K., Knowlton K.U., Kandolf R. Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 2001, 103:756-761.
83. + T cells. J. Immunol. 2006, 176:3028-3036.
84. Whitmire J.K., Eam B., Whitton J.L. Tentative T cells: memory cells are quick to respond, but slow to divide. PLoS Pathog. 2008, 4:1-11.
85. Whitton J.L. Immunopathology during coxsackievirus infection. Springer Semin. Immunopathol. 2002, 24:201-213.
86. Wilson N.S., Behrens G.M., Lundie R.J., Smith C.M., Waithman J., Young L., Forehan S.P., Mount A., Steptoe R.J., Shortman K.D., de Koning-Ward T.F., Belz G.T., Carbone F.R., Crabb B.S., Heath W.R., Villadangos J.A. Systemic activation of dendritic cells by toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 2006, 7:165-172.
87. Young L.J., Wilson N.S., Schnorrer P., Mount A., Lundie R.J., La Gruta N.L., Crabb B.S., Belz G.T., Heath W.R., Villadangos J.A. Dendritic cell preactivation impairs MHC class II presentation of vaccines and endogenous viral antigens. Proc. Nat. Acad. Sci. U.S.A 2007, 104:17753-17758.
88. Young L.J., Wilson N.S., Schnorrer P., Proietto A., ten B.T., Matsuki Y., Mount A.M., Belz G.T., O'Keeffe M., Ohmura-Hoshino M., Ishido S., Stoorvogel W., Heath W.R., Shortman K., Villadangos J.A. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat. Immunol. 2008, 9:1244-1252.
89. Zuniga E.I., Liou L.Y., Mack L., Mendoza M., Oldstone M.B. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 2008, 4:374-386.