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Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae

DOI: 10.1371/journal.ppat.1003238

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Abstract:

Secondary bacterial infections are a leading cause of illness and death during epidemic and pandemic influenza. Experimental studies suggest a lethal synergism between influenza and certain bacteria, particularly Streptococcus pneumoniae, but the precise processes involved are unclear. To address the mechanisms and determine the influences of pathogen dose and strain on disease, we infected groups of mice with either the H1N1 subtype influenza A virus A/Puerto Rico/8/34 (PR8) or a version expressing the 1918 PB1-F2 protein (PR8-PB1-F2(1918)), followed seven days later with one of two S. pneumoniae strains, type 2 D39 or type 3 A66.1. We determined that, following bacterial infection, viral titers initially rebound and then decline slowly. Bacterial titers rapidly rise to high levels and remain elevated. We used a kinetic model to explore the coupled interactions and study the dominant controlling mechanisms. We hypothesize that viral titers rebound in the presence of bacteria due to enhanced viral release from infected cells, and that bacterial titers increase due to alveolar macrophage impairment. Dynamics are affected by initial bacterial dose but not by the expression of the influenza 1918 PB1-F2 protein. Our model provides a framework to investigate pathogen interaction during coinfections and to uncover dynamical differences based on inoculum size and strain.

References

[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. doi: 10.1086/591708
[2]  Louria DB, Blumenfeld HL, Ellis JT, Kilbourne ED, Rogers DE (1959) Studies on influenza in the pandemic of 1957–1958. II. Pulmonary complications of influenza. J Clin Investig 38: 213–265. doi: 10.1172/jci103791
[3]  Weinberger DM, Simonsen L, Jordan R, Steiner C, Miller M, et al. (2012) Impact of the 2009 influenza pandemic on pneumococcal pneumonia hospitalizations in the United States. J Infect Dis 205: 458–465. doi: 10.1093/infdis/jir749
[4]  McCullers JA, English BK (2008) Improving therapeutic strategies for secondary bacterial pneumonia following influenza. Future Microbiol 3: 397–404. doi: 10.2217/17460913.3.4.397
[5]  McCullers JA (2006) Insights into the interaction between influenza virus and pneu-mococcus. Clin Microbiol Rev 19: 571–582. doi: 10.1128/cmr.00058-05
[6]  McCullers JA, Rehg JE (2002) Lethal synergism between influenza virus and Strep-tococcus pneumoniae: Characterization of a mouse model and the role of platelet-activating factor receptor. J Infect Dis 186: 341–350. doi: 10.1086/341462
[7]  Peltola VT, Boyd KL, McAuley JL, Rehg JE, McCullers JA (2006) Bacterial sinusitis and otitis media following influenza virus infection in ferrets. Infect Immun 74: 2562–2567. doi: 10.1128/iai.74.5.2562-2567.2006
[8]  Smith AM, McCullers JA, Adler FR (2011) Mathematical model of a three-stage innate immune response to a pneumococcal lung infection. J Theor Biol 276: 106–116. doi: 10.1016/j.jtbi.2011.01.052
[9]  McAuley JL, Hornung F, Boyd KL, Smith AM, McKeon R, et al. (2007) Expres sion of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host & Microbe 2: 240–249. doi: 10.1016/j.chom.2007.09.001
[10]  McCullers JA, Bartmess KC (2003) Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J Infect Dis 187: 1000–1009. doi: 10.1086/368163
[11]  Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG (2010) influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Resp Cell Mol 42: 450–460. doi: 10.1165/rcmb.2007-0417oc
[12]  Peltola VT, Murti KG, McCullers JA (2005) influenza virus neuraminidase contributes to secondary bacterial pneumonia. J Infect Dis 192: 249–257. doi: 10.1086/430954
[13]  Navarini AA, Recher M, Lang KS, Georgiev P, Meury S, et al. (2006) Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc Natl Acad Sci USA 103: 15535–15539. doi: 10.1073/pnas.0607325103
[14]  Colamussi ML, White MR, Crouch E, Hartshorn KL (1999) influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 93: 2395–2403.
[15]  McNamee LA, Harmsen AG (2006) Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect Immun 74: 6707–6721. doi: 10.1128/iai.00789-06
[16]  Engelich G, White M, Hartshorn KL (2001) Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol 69: 50–56.
[17]  Peltola VT, McCullers JA (2004) Respiratory viruses predisposing to bacterial infections: role of neuraminidase. Pediatr Infect Dis 23: S87–S97. doi: 10.1097/01.inf.0000108197.81270.35
[18]  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. doi: 10.1172/jci57762
[19]  Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A, et al. (2009) Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 119: 1910–1920. doi: 10.1172/jci35412
[20]  Seki M, Yanagihara K, Higashiyama Y, Fukuda Y, Kaneko Y, et al. (2004) Immunokinetics in severe pneumonia due to influenza virus and bacteria coinfection in mice. Eur Respir J 24: 143–149. doi: 10.1183/09031936.04.00126103
[21]  Smith MW, Schmidt JE, Rehg JE, Orihuela CJ, McCullers JA (2007) Induction of pro- and anti-inammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp Med 57: 82–89.
[22]  van der Sluijs KF, van Elden LJR, Nijhuis M, Schuurman R, Pater JM, et al. (2004) IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J Immunol 172: 7603–7609. doi: 10.4049/jimmunol.172.12.7603
[23]  Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, et al. (2008) Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 205: 323–329. doi: 10.1084/jem.20070891
[24]  Jamieson AM, Yu S, Annicelli CH, Medzhitov R (2010) influenza virus-induced glu-cocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe 7: 103–114. doi: 10.1016/j.chom.2010.01.010
[25]  Sun K, Metzger DW (2008) Inhibition of pulmonary antibacterial defense by interferon- during recovery from influenza infection. Nat Med 14: 558–564. doi: 10.1038/nm1765
[26]  Jonsson S, Musher DM, Chapman A, Goree A, Lawrence EC (1985) Phagocytosis and killing of common bacterial pathogens of the lung by human alveolar macrophages. J Infect Dis 152: 4–13. doi: 10.1093/infdis/152.1.4
[27]  Knapp S, Leemans JC, Florquin S, Branger J, Maris NA, et al. (2003) Alveolar macrophages have a protective antiinammatory role during murine pneumococcal pneumonia. Am J Respir Crit Care Med 167: 171–179. doi: 10.1164/rccm.200207-698oc
[28]  Fillion I, Ouellet N, Simard M, Bergeron Y, Sato S, et al. (2001) Role of chemokines and formyl peptides in pneumococcal pneumonia-induced monocyte/macrophage recruitment. J Immunol 166: 7353–7361. doi: 10.4049/jimmunol.166.12.7353
[29]  Jakab GJ (1982) Immune impairment of alveolar macrophage phagocytosis during influenza virus pneumonia. Am Rev Respir Dis 126: 778–782.
[30]  Kodihalli S, Sivanandan V, Nagaraja KV, Shaw D, Halvorson DA (1994) Effect of avian influenza virus infection on the phagocytic function of systemic phagocytes and pulmonary macrophages of turkeys. Avian Dis 38: 93–102. doi: 10.2307/1591842
[31]  Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, et al. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7: 1306–1312. doi: 10.1038/nm1201-1306
[32]  Speshock JL, Doyon-Reale N, Rabah R, Neely MN, Roberts PC (2007) Filamentous influenza A virus infection predisposes mice to fatal septicemia following superin-fection with Streptococcus pneumoniae serotype 3. Infect Immun 75: 3102–3111. doi: 10.1128/iai.01943-06
[33]  Conenello GM, Tisoncik JR, Rosenzweig E, Varga ZT, Palese P, et al. (2011) A single N66S mutation in the PB1-F2 protein of influenza A virus increases virulence by inhibiting the early interferon response in vivo. J Virol 85: 652–662. doi: 10.1128/jvi.01987-10
[34]  McAuley JL, Chipuk JE, Boyd KL, Van De Velde N, Green DR, et al. (2010) PB1-F2 proteins from H5N1 and 20th century pandemic influenza viruses cause immunopathology. PLoS Pathog 6: 680–689. doi: 10.1371/journal.ppat.1001014
[35]  Le Goffc R, Bouguyon E, Chevalier C, Vidic J, Da Costa B, et al. (2010) influenza A virus protein PB1-F2 exacerbates IFN-β expression of human respiratory epithelial cells. J Immunol 185: 4812–4823. doi: 10.4049/jimmunol.0903952
[36]  Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW (2003) The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function. J Virol 77: 7214–7224. doi: 10.1128/jvi.77.13.7214-7224.2003
[37]  Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P (2005) influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1: e4. doi: 10.1371/journal.ppat.0010004
[38]  Beauchemin C, Handel A (2011) A review of mathematical models of influenza A infections within a host or cell culture: lessons learned and challenges ahead. BMC Public Health 11: S7. doi: 10.1186/1471-2458-11-s1-s7
[39]  Smith AM, Ribeiro RM (2010) Modeling the viral dynamics of influenza A virus infection. Crit Rev Immunol 30: 291–298. doi: 10.1615/critrevimmunol.v30.i3.60
[40]  Smith AM, Perelson AS (2011) influenza A virus infection kinetics: Quantitative data and models. WIREs Syst Biol Med 3: 429–445. doi: 10.1002/wsbm.129
[41]  Smith AM, Adler FR, McAuley JL, Gutenkunst RN, Ribeiro RM, et al. (2011) Effect of 1918 PB1-F2 expression on influenza A virus infection kinetics. PLoS Comput Biol 7: e1001081. doi: 10.1371/journal.pcbi.1001081
[42]  Weeks-Gorospe JN, Hurtig HR, Iverson AR, Schuneman MJ, Webby RJ, et al. (2012) Naturally occurring swine influenza A virus PB1-F2 phenotypes that contribute to superinfection with gram-positive respiratory pathogens. J Virol 86: 9035–9043. doi: 10.1128/jvi.00369-12
[43]  Brown KS, Sethna JP (2003) Statistical mechanical approaches to models with many poorly known parameters. Phys Rev E 68: 021904. doi: 10.1103/physreve.68.021904
[44]  Eslami M (1994) Theory of Sensitivity in Dynamic Systems: An Introduction. Berlin (Germany): Springer-Verlag. 600 p.
[45]  Frank PM (1978) Introduction to System Sensitivity Theory. New York (New York): Academic Press, Inc. 386 p.
[46]  Smith AM, Adler FR, Perelson AS (2010) An accurate two-phase approximate solution to an acute viral infection model. J Math Biol 60: 711–726. doi: 10.1007/s00285-009-0281-8
[47]  Berendt RF, Long GG, Walker JS (1975) influenza alone and in sequence with pneumonia due to Streptococcus pneumoniae in the squirrel monkey. J Infect Dis 132: 689–693. doi: 10.1093/infdis/132.6.689
[48]  Gerone PJ, Ward TG, Chappal WA (1957) Combined infections in mice with influenza virus and Diplococcus pneumoniae. Am J Epi 66: 331–341.
[49]  Glover RE (1941) Spread of infection from the respiratory tract of the ferret. II. Association of influenza A virus and Streptococcus type C. Brit J Exp Pathol 22: 98–107.
[50]  Jakab GJ, Warr GA, Knight ME (1979) Pulmonary and systemic defenses against challenge with Staphylococcus aureus in mice with pneumonia due to influenza A virus. J Infect Dis 140: 105–108. doi: 10.1093/infdis/140.1.105
[51]  Jones WT, Menna JH, Wennerstrom DE (1983) Lethal synergism induced in mice by influenza type A virus and type Ia group B streptococci. Infect Immun 41: 618–623.
[52]  AlonsoDeVelasco E, Verheul AF, Verhoef J, Snippe H (1995) Streptococcus pneu- moniae: virulence factors, pathogenesis, and vaccines. Microbiol Mol Biol Rev 59: 591–603.
[53]  Iverson AR, Boyd KL, McAuley JL, Plano LR, Hart ME, et al. (2011) influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 203: 880–888. doi: 10.1093/infdis/jiq113
[54]  McCullers JA, McAuley JL, Browall S, Iverson AR, Boyd KL, et al. (2010) influenza enhances susceptibility to natural acquisition of and disease due to streptococcus pneumoniae in ferrets. J Infect Dis 202: 1287–1295. doi: 10.1086/656333
[55]  Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, et al. (2012) Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37: 158–170. doi: 10.1016/j.immuni.2012.04.011
[56]  Diavatopoulos DA, Short KR, Price JT, Wilksch JJ, Brown LE, et al. (2010) influenza A virus facilitates Streptococcus pneumoniae transmission and disease. FASEB J 24: 1789–1798. doi: 10.1096/fj.09-146779
[57]  Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, et al. (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA 108: 5354–5359. doi: 10.1073/pnas.1019378108
[58]  Domínguez-Cherit G, Lapinsky SE, Macias AE, Pinto R, Espinosa-Perez L, et al. (2009) Critically ill patients with 2009 influenza A (H1N1) in Mexico. JAMA – J Am Med Assoc 302: 1880–1887. doi: 10.1001/jama.2009.1536
[59]  Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, et al. (2009) Hospi-talized patients with 2009 H1N1 influenza in the United States, April–June 2009. New Engl J Med 361: 1935–1944. doi: 10.1056/nejmoa0906695
[60]  Seo SH, Webby R, Webster RG (2004) No apoptotic deaths and different levels of inductions of inammatory cytokines in alveolar macrophages infected with influenza viruses. Virology 329: 270–279. doi: 10.1016/j.virol.2004.08.019
[61]  Didierlaurent A, Goulding J, Hussell T (2007) The impact of successive infections on the lung microenvironment. Immunol 122: 457–465. doi: 10.1111/j.1365-2567.2007.02729.x
[62]  Wu Y, Mao H, Ling MT, Chow KH, Ho PL, et al. (2011) Successive influenza virus infection and Streptococcus pneumoniae stimulation alter human dendritic cell function. BMC Infect Dis 11: 201. doi: 10.1186/1471-2334-11-201
[63]  Small CL, Shaler CR, McCormick S, Jeyanathan M, Damjanovic D, et al. (2010) influenza infection leads to increased susceptibility to subsequent bacterial super-infection by impairing NK cell responses in the lung. J Immunol 184: 2048–2056. doi: 10.4049/jimmunol.0902772
[64]  Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, et al. (2011) influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186: 1666–1674. doi: 10.4049/jimmunol.1002194
[65]  Ayala VI, Teijaro JR, Farber DL, Dorsey SG, Carbonetti NH (2011) Bordetella pertussis infection exacerbates influenza virus infection through pertussis toxin-mediated suppression of innate immunity. PLoS ONE 6: e19016. doi: 10.1371/journal.pone.0019016
[66]  Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Epidemiol 27: 493–497.
[67]  Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS (2006) Kinetics of influenza A virus infection in humans. J Virol 80: 7590–7599. doi: 10.1128/jvi.01623-05
[68]  El Ahmer OR, Raza MW, Ogilvie MM, Weir DM, Blackwell CC (1999) Binding of bacteria to HEp-2 cells infected with influenza A virus. FEMS Immunol Med Microbiol 23: 331–341. doi: 10.1111/j.1574-695x.1999.tb01255.x
[69]  Schultz-Cherry S, Hinshaw VS (1996) influenza virus neuraminidase activates latent transforming growth factor beta. J Virol 70: 8624–8629.
[70]  Tong HH, Liu X, Chen Y, James M, Demaria T (2002) Effect of neuraminidase on receptor-mediated adherence of Streptococcus pneumoniae to chinchilla tracheal epithelium. Acta Oto-Laryngologica 122: 413–419. doi: 10.1080/00016480260000111
[71]  Fischetti VA, Novick RP, Ferretti JJ (2006) Gram-positive pathogens. 2nd edition. Washington, D.C.: American Society for Microbiology Press. 849 p.
[72]  Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, et al. (2000) Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 68: 492–501. doi: 10.1128/iai.68.2.492-501.2000
[73]  Gubareva LV, Kaiser L, Hayden FG (2000) influenza virus neuraminidase in-hibitors. The Lancet 355: 827–835. doi: 10.1016/s0140-6736(99)11433-8
[74]  Myers CR, Gutenkunst RN, Sethna JP (2007) Python unleashed on systems biology. Comput Sci Eng 9: 34–37. doi: 10.1109/mcse.2007.60
[75]  Gutenkunst RN, Casey FP, Waterfall JJ, Atlas JC, Kuczenski RS, et al.. (2007) SloppyCell. Ithaca (New York): Cornell University
[76]  Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76: 297–307. doi: 10.1093/biomet/76.2.297

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