Coinfection with Streptococcus pneumoniae modulates the B cell response to influenza virus

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 11995-12005

  Wolf, Amaya I ^a   Strauman, Maura C ^a   Mozdzanowska, Krystyna ^a   Whittle, James R R ^b   Williams, Katie L ^a   Sharpe, Arlene H ^c   Weiser, Jeffrey N ^d   Caton, Andrew J ^a   Hensley, Scott E ^a   Erikson, Jan ^a  

^a WISTAR INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FOLLICULAR HELPER CELL; GERMINAL CENTER; HELPER CELL; INFLUENZA A; LYMPHOID ORGAN; MEDIASTINUM LYMPH NODE; MIXED INFECTION; MOUSE; NONHUMAN; PNEUMOCOCCAL INFECTION; SECONDARY INFECTION; SPLEEN; VIRAL CLEARANCE; VIRUS NEUTRALIZATION; ANIMAL; BAGG ALBINO MOUSE; COMPLICATION; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; B-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; GERMINAL CENTER; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICE; MICE, INBRED BALB C; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 84907425843     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01833-14     Document Type: Article

References (71)

1. Morens DM, Taubenberger JK, Fauci AS. 2008. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198:962-970. http://dx.doi.org/10.1086/591708.
2. Mizgerd JP. 2008. Acute lower respiratory tract infection. N. Engl. J. Med. 358:716-727. http://dx.doi.org/10.1056/NEJMra074111.
3. McCullers JA. 2006. Insights into the interaction between influenza virus and pneumococcus. Clin. Microbiol. Rev. 19:571-582. http://dx.doi.org /10.1128/CMR.00058-05.
4. Obaro SK, Monteil MA, Henderson DC. 1996. The pneumococcal problem. BMJ 312:1521-1525. http://dx.doi.org/10.1136/bmj.312.7045.1521.
5. Austrian R. 1986. Some aspects of the pneumococcal carrier state. J. Antimicrob. Chemother. 18(Suppl A):35-45. http://dx.doi.org/10.1093 /jac/18.1.35.
6. McCullers JA, Rehg JE. 2002. Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J. Infect. Dis. 186:341-350. http: //dx.doi.org/10.1086/341462.
7. McCullers JA. 2014. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat. Rev. Microbiol. 12:252-262. http://dx.doi.org/10.1038/nrmicro3231.
8. Wang J, Li F, Sun R, Gao X, Wei H, Li LJ, Tian Z. 2013. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat. Comm. 4:2106. http://dx.doi.org/10.1038/ncomms3106.
9. Stelekati E, Wherry EJ. 2012. Chronic bystander infections and immunity to unrelated antigens. Cell Host Microbe 12:458-469. http://dx.doi.org/10.1016/j.chom.2012.10.001.
10. Gerhard W, Mozdzanowska K, Furchner M, Washko G, Maiese K. 1997. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol. Rev. 159:95-103. http://dx.doi.org/10.1111/j.1600-065X.1997.tb01009.x.
11. Gerhard W. 2001. The role of the antibody response in influenza virus infection. Curr. Top. Microbiol. Immunol. 260:171-190.
12. Waffarn EE, Baumgarth N. 2011. Protective B cell responses to flu-no fluke! J. Immunol. 186:3823-3829. http://dx.doi.org/10.4049/jimmunol.1002090.
13. Sealy R, Surman S, Hurwitz JL, Coleclough C. 2003. Antibody response to influenza infection of mice: different patterns for glycoprotein and nucleocapsid antigens. Immunology 108:431-439. http://dx.doi.org/10.1046/j.1365-2567.2003.01615.x.
14. Coro ES, Chang WLW, Baumgarth N. 2006. Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J. Immunol. 176:4343-4351. http://dx.doi.org/10.4049/jimmunol.176.7.4343.
15. + T cell-dependent immunoglobulin A response to influenza infection in the absence of key cognate T-B interactions. J. Exp. Med. 198:1011-1021. http://dx.doi.org/10.1084/jem.20021745.
16. Boyden AW, Legge KL, Waldschmidt TJ. 2012. Pulmonary infection with influenza A virus induces site-specific germinal center and T follicular helper cell responses. PLoS One 7:e40733. http://dx.doi.org/10.1371 /journal.pone.0040733.
17. Jones PD, Ada GL. 1987. Persistence of influenza virus-specific antibodysecreting cells and B-cell memory after primary murine influenza virus infection. Cell. Immunol. 109:53-64. http://dx.doi.org/10.1016/0008-8749(87)90291-7.
18. Hyland L, Sangster M, Sealy R, Coleclough C. 1994. Respiratory virus infection of mice provokes a permanent humoral immune response. J. Virol. 68:6083-6086.
19. Wolf AI, Mozdzanowska K, Quinn WJ, III, Metzgar M, Williams KL, Caton AJ, Meffre E, Bram RJ, Erickson LD, Allman D, Cancro MP, Erikson J. 2011. Protective antiviral antibody responses in a mouse model of influenza virus infection require TACI. J. Clin. Invest. 121:3954-3964. http://dx.doi.org/10.1172/JCI57362.
20. Joo HM, He Y, Sangster MY. 2008. Broad dispersion and lung localization of virus-specific memory B cells induced by influenza pneumonia. Proc. Natl. Acad. Sci. U. S. A. 105:3485-3490. http://dx.doi.org/10.1073 /pnas.0800003105.
21. Onodera T, Takahashi Y, Yokoi Y, Ato M, Kodama Y, Hachimura S, Kurosaki T, Kobayashi K. 2012. Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc. Natl. Acad. Sci. U. S. A. 109:2485-2490. http://dx.doi.org /10.1073/pnas.1115369109.
22. Bertram EM, Tafuri A, Shahinian A, Chan VSF, Hunziker L, Recher M, Ohashi PS, Mak TW, Watts TH. 2002. Role of ICOS versus CD28 in antiviral immunity. Eur. J. Immunol. 32:3376-3385. http://dx.doi.org/10.1002/1521-4141(200212)32:12<3376::AID-IMMU3376>3.0.CO;2-Y.
23. Lee BO, Rangel-Moreno J, Moyron-Quiroz JE, Hartson L, Makris M, Sprague F, Lund FE, Randall TD. 2005. CD4 T cell-independent antibody response promotes resolution of primary influenza infection and helps to prevent reinfection. J. Immunol. 175:5827-5838. http://dx.doi.org/10.4049/jimmunol.175.9.5827.
24. Choi Y, Baumgarth N. 2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205:3053-3064. http://dx.doi.org /10.1084/jem.20080979.
25. Crotty S. 2011. Follicular helper CD4 T cells (T FH). Annu. Rev. Immunol. 29:621-663. http://dx.doi.org/10.1146/annurev-immunol-031210-101400.
26. McHeyzer-Williams M, Okitsu S, Wang N, McHeyzer-Williams L. 2012. Molecular programming of B cell memory. Nat. Rev. Immunol. 12:24-34. http://dx.doi.org/10.1038/nri3128.
27. Shlomchik MJ, Weisel F. 2012. Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 247:52-63. http: //dx.doi.org/10.1111/j.1600-065X.2012.01124.x.
28. Vinuesa CG, Tangye SG, Moser B, Mackay CR. 2005. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 5:853-865. http://dx.doi.org/10.1038/nri1714.
29. Karnowski A, Chevrier S, Belz GT, Mount A, Emslie D, D'Costa K, Tarlinton DM, Kallies A, Corcoran LM. 2012. B and T cells collaborate in antiviral responses via IL-6, IL-21, and transcriptional activator and coactivator, Oct2 and OBF-1. J. Exp. Med. 209:2049-2064. http://dx.doi.org/10.1084/jem.20111504.
30. + T cells. J. Exp. Med. 206:69-78. http://dx.doi.org/10.1084/jem.20081571.
31. Bessa J, Kopf M, Bachmann MF. 2010. Cutting edge: IL-21 and TLR signaling regulate germinal center responses in a B cell-intrinsic manner. J. Immunol. 184:4615-4619. http://dx.doi.org/10.4049/jimmunol.0903949.
32. Sweet RA, Lee SK, Vinuesa CG. 2012. Developing connections amongst key cytokines and dysregulated germinal centers in autoimmunity. Curr. Opin. Immunol. 24:658-664. http://dx.doi.org/10.1016/j.coi.2012.10.003.
33. Harker JA, Lewis GM, Mack L, Zuniga EI. 2011. Late interleukin-6 escalates Tfollicular helper cell responses and controls a chronic viral infection. Science 334:825-829. http://dx.doi.org/10.1126/science.1208421.
34. Hunziker L, Recher M, Macpherson AJ, Ciurea A, Freigang S, Hengartner H, Zinkernagel RM. 2003. Hypergammaglobulinemia and autoantibody induction mechanisms in viral infections. Nat. Immunol. 4:343-349. http://dx.doi.org/10.1038/ni911.
35. Coutelier JP, van der Logt JT, Heessen FW, Vink A, van Snick J. 1988. Virally induced modulation of murine IgG antibody subclasses. J. Exp. Med. 168:2373-2378. http://dx.doi.org/10.1084/jem.168.6.2373.
36. Montes CL, Acosta-Rodríguez EV, Merino MC, Bermejo DA, Gruppi A. 2007. Polyclonal B cell activation in infections: infectious agents' devilry or defense mechanism of the host? J. Leukoc. Biol. 82:1027-1032. http: //dx.doi.org/10.1189/jlb.0407214.
37. Monsalvo AC, Batalle JP, Lopez MF, Krause JC, Klemenc J, Hernandez JZ, Maskin B, Bugna J, Rubinstein C, Aguilar L, Dalurzo L, Libster R, Savy V, Baumeister E, Aguilar L, Cabral G, Font J, Solari L, Weller KP, Johnson J, Echavarria M, Edwards KM, Chappell JD, Crowe JE, Williams JV, Melendi GA, Polack FP. 2011. Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes. Nat. Med. 17: 195-199. http://dx.doi.org/10.1038/nm.2262.
38. Pone EJ, Zan H, Zhang J, Al-Qahtani A, Xu Z, Casali P. 2010. Toll-like receptors and B-cell receptors synergize to induce immunoglobulin classswitch DNA recombination: relevance to microbial antibody responses. Crit. Rev. Immunol. 30:1-29. http://dx.doi.org/10.1615/CritRevImmunol.v30.i1.10.
39. + single positive cells with a class II major histocompatibility complex-restricted receptor. J. Exp. Med. 180:25-34. http://dx.doi.org/10.1084/jem.180.1.25.
40. McAdam AJ, Greenwald RJ, Levin MA, Chernova T, Malenkovich N, Ling V, Freeman GJ, Sharpe AH. 2001. ICOS is critical for CD40-mediated antibody class switching. Nature 409:102-105. http://dx.doi.org /10.1038/35051107.
41. McCool TL, Weiser JN. 2004. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect. Immun. 72:5807-5813. http://dx.doi.org/10.1128/IAI.72.10.5807-5813.2004.
42. McCool TL, Cate TR, Moy G, Weiser JN. 2002. The immune response to pneumococcal proteins during experimental human carriage. J. Exp. Med. 195:359-365. http://dx.doi.org/10.1084/jem.20011576.
43. Wolf AI, Buehler D, Hensley SE, Cavanagh LL, Wherry EJ, Kastner P, Chan S, Weninger W. 2009. Plasmacytoid dendritic cells are dispensable during primary influenza virus infection. J. Immunol. 182:871-879. http: //dx.doi.org/10.4049/jimmunol.182.2.871.
44. Whittle JR, Wheatley AK, Wu L, Lingwood D, Kanekiyo M, Ma SS, Narpala SR, Yassine HM, Frank GM, Yewdell JW, Ledgerwood JE, Wei CJ, McDermott AB, Graham BS, Koup RA, Nabel GJ. 2014. Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stemdirected antibodies from multiple Ig heavy chain lineages. J. Virol. 88: 4047-4057. http://dx.doi.org/10.1128/JVI.03422-13.
45. Mozdzanowska K, Maiese K, Gerhard W. 2000. Th cell-deficient mice control influenza virus infection more effectively than Th-and B celldeficient mice: evidence for a Th-independent contribution by B cells to virus clearance. J. Immunol. 164:2635-2643. http://dx.doi.org/10.4049 /jimmunol.164.5.2635.
46. Kavaler J, Caton AJ, Staudt LM, Gerhard W. 1991. A B cell population that dominates the primary response to influenza virus hemagglutinin does not participate in the memory response. Eur. J. Immunol. 21:2687-2695. http://dx.doi.org/10.1002/eji.1830211107.
47. Scherle PA, Palladino G, Gerhard W. 1992. Mice can recover from pulmonary influenza virus infection in the absence of class I-restricted cytotoxic T cells. J. Immunol. 148:212-217.
48. Liang S, Mozdzanowska K, Palladino G, Gerhard W. 1994. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152:1653-1661.
49. Wolf AI, Strauman MC, Mozdzanowska K, Williams KL, Osborne LC, Shen H, Liu Q, Garlick D, Artis D, Hensley SE, Caton AJ, Weiser JN, Erikson J. 2014. Pneumolysin expression by Streptococcus pneumoniae protects colonized mice from influenza virus-induced disease. Virology 462-463C:254-265. http://dx.doi.org/10.1016/j.virol.2014.06.019.
50. Marshall D, Sealy R, Sangster M, Coleclough C. 1999. TH cells primed during influenza virus infection provide help for qualitatively distinct antibody responses to subsequent immunization. J. Immunol. 163:4673-4682.
51. Rothaeusler K, Baumgarth N. 2010. B-cell fate decisions following influenza virus infection. Eur. J. Immunol. 40:366-377. http://dx.doi.org/10.1002/eji.200939798.
52. Kavaler J, Caton AJ, Staudt LM, Schwartz D, Gerhard W. 1990. A set of closely related antibodies dominates the primary antibody response to the antigenic site CB of the A/PR/8/34 influenza virus hemagglutinin. J. Immunol. 145:2312-2321.
53. Mozdzanowska K, Feng J, Eid M, Zharikova D, Gerhard W. 2006. Enhancement of neutralizing activity of influenza virus-specific antibodies by serum components. Virology 352:418-426. http://dx.doi.org/10.1016/j.virol.2006.05.008.
54. Dong C, Juedes AE, Temann UA, Shresta S, Allison JP, Ruddle NH, Flavell RA. 2001. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409:97-101. http://dx.doi.org/10.1038 /35051100.
55. Ghoneim HE, Thomas PG, McCullers JA. 2013. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J. Immunol. 191:1250-1259. http://dx.doi.org/10.4049/jimmunol.1300014.
56. Smith MW, Schmidt JE, Rehg JE, Orihuela CJ, McCullers JA. 2007. Induction of pro-and anti-inflammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp. Med. 57:82-89.
57. Kunkel EJ, Butcher EC. 2003. Plasma-cell homing. Nat. Rev. Immunol. 3:822-829. http://dx.doi.org/10.1038/nri1203.
58. Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, Lanzavecchia A, Sallusto F. 2013. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38:596-605. http://dx.doi.org/10.1016/j.immuni.2012.11.020.
59. Paus D. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203:1081-1091. http://dx.doi.org/10.1084/jem.20060087.
60. Kim TS, Hufford MM, Sun J, Fu Y-X, Braciale TJ. 2010. Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection. J. Exp. Med. 207:1161-1172. http://dx.doi.org/10.1084/jem.20092017.
61. Jelley-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, Swain SL. 2005. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J. Exp. Med. 202:697-706. http://dx.doi.org/10.1084/jem.20050227.
62. Zammit DJ, Turner DL, Klonowski KD, Lefrançois L, Cauley LS. 2006. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24:439-449. http://dx.doi.org /10.1016/j.immuni.2006.01.015.
63. Nakamura S, Davis KM, Weiser JN. 2011. Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J. Clin. Invest. 121:3657-3665. http://dx.doi.org/10.1172/JCI57762.
64. Li W, Moltedo B, Moran TM. 2012. Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gammadelta T cells. J. Virol. 86:12304-12312. http://dx.doi.org/10.1128/JVI.01269-12.
65. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Köhler G. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342. http://dx.doi.org/10.1038/368339a0.
66. Baumgarth N, Kelso A. 1996. In vivo blockade of gamma interferon affects the influenza virus-induced humoral and the local cellular immune response in lung tissue. J. Virol. 70:4411-4418.
67. Kopf M, Herren S, Wiles MV, Pepys MB, Kosco-Vilbois MH. 1998. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 188:1895-1906. http://dx.doi.org/10.1084/jem.188.10.1895.
68. Kuri T, Sorensen AS, Thomas S, Hedestam GB, Normark S, Henriques-Normark B, McInerney GM, Plant L. 2013. Influenza A virus-mediated priming enhances cytokine secretion by human dendritic cells infected with Streptococcus pneumoniae. Cell. Microbiol. 15:1385-1400. http://dx.doi.org/10.1111/cmi.12122.
69. Kim S, Caton M, Wang C, Khalil M, Zhou Z, Hardin J, Diamond B. 2008. Increased IL-12 inhibits B cells' differentiation to germinal center cells and promotes differentiation to short-lived plasmablasts. J. Exp. Med. 205:2437-2448. http://dx.doi.org/10.1084/jem.20070731.
70. García de Vinuesa C, MacLennan IC, Holman M, Klaus GG. 1999. Anti-CD40 antibody enhances responses to polysaccharide without mimicking T cell help. Eur. J. Immunol. 29:3216-3224. http://dx.doi.org/10.1002/(SICI)1521-4141(199910)29:10<3216::AID-IMMU3216>3.0.CO;2-X.
71. MacLennan ICM, Toellner K-M, Cunningham AF, Serre K, Sze DM-Y, Zúñiga E, Cook MC, Vinuesa CG. 2003. Extrafollicular antibody responses. Immunol. Rev. 194:8-18. http://dx.doi.org/10.1034/j.1600-065X.2003.00058.x.