The immunological mechanisms that control pneumococcal carriage

PLoS Pathogens

Volumn 13, Issue 12, 2017, Pages

  Jochems, Simon P ^a   Weiser, Jeffrey N ^b   Malley, Richard ^c   Ferreira, Daniela M ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; CASPASE RECRUITMENT DOMAIN PROTEIN 15; FRAGILE HISTIDINE TRIAD PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 17; MONOCYTE CHEMOTACTIC PROTEIN 1; OUTER SURFACE PROTEIN A; PNEUMOCOCCUS VACCINE; VACCINE;

ANTIGEN ANTIBODY REACTION; BACTERIAL CAPSULE; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; HUMAN; INFECTION CONTROL; INFECTION PREVENTION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MONOCYTE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PHARYNX DISEASE; PNEUMOCOCCAL INFECTION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; REVIEW; STREPTOCOCCUS PNEUMONIAE; TH17 CELL; HETEROZYGOTE; IMMUNOLOGY; MICROBIOLOGY; NASOPHARYNX;

CARRIER STATE; HUMANS; NASOPHARYNX; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; VACCINES, CONJUGATE;

EID: 85039920053     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006665     Document Type: Review

References (99)

1. O′Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet. 2009;374(9693):893–902. doi: 10.1016/S0140-6736(09)61204-6 19748398.
2. Welte T, Torres A, Nathwani D, Clinical and economic burden of community-acquired pneumonia among adults in Europe. Thorax. 2012;67(1):71–9. doi: 10.1136/thx.2009.129502 20729232.
3. Krone CL, van de Groep K, Trzcinski K, Sanders EA, Bogaert D, Immunosenescence and pneumococcal disease: an imbalance in host-pathogen interactions. Lancet Respir Med. 2014;2(2):141–53. doi: 10.1016/S2213-2600(13)70165-6 24503269.
4. McCullers JA, Insights into the interaction between influenza virus and pneumococcus. Clin Microbiol Rev. 2006;19(3):571–82. Epub 2006/07/19. doi: 10.1128/CMR.00058-05 16847087.
5. SanJoaquin MA, Allain TJ, Molyneux ME, Benjamin L, Everett DB, Gadabu O, et al. Surveillance Programme of IN-patients and Epidemiology (SPINE): implementation of an electronic data collection tool within a large hospital in Malawi. PLoS Med. 2013;10(3):e1001400. doi: 10.1371/journal.pmed.1001400 23554578.
6. Mortimer K, Gordon SB, Jindal SK, Accinelli RA, Balmes J, Martin WJ, 2ndHousehold air pollution is a major avoidable risk factor for cardiorespiratory disease. Chest. 2012;142(5):1308–15. doi: 10.1378/chest.12-1596 23131939.
7. Almirall J, Gonzalez CA, Balanzo X, Bolibar I, Proportion of community-acquired pneumonia cases attributable to tobacco smoking. Chest. 1999;116(2):375–9. 10453865.
8. Angoulvant F, Cohen R, Doit C, Elbez A, Werner A, Bechet S, et al. Trends in antibiotic resistance of Streptococcus pneumoniae and Haemophilus influenzae isolated from nasopharyngeal flora in children with acute otitis media in France before and after 13 valent pneumococcal conjugate vaccine introduction. BMC Infect Dis. 15:236. Epub 2015/06/22. doi: 10.1186/s12879-015-0978-9 26093673.
9. Goldblatt D, Hussain M, Andrews N, Ashton L, Virta C, Melegaro A, et al. Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study. J Infect Dis. 2005;192(3):387–93. doi: 10.1086/431524 15995951.
10. Kamng′ona AW, Hinds J, Bar-Zeev N, Gould KA, Chaguza C, Msefula C, et al. High multiple carriage and emergence of Streptococcus pneumoniae vaccine serotype variants in Malawian children. BMC Infect Dis. 2015;15:234. doi: 10.1186/s12879-015-0980-2 26088623.
11. Rodrigues F, Foster D, Nicoli E, Trotter C, Vipond B, Muir P, et al. Relationships between rhinitis symptoms, respiratory viral infections and nasopharyngeal colonization with Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus in children attending daycare. The Pediatric infectious disease journal. 2013;32(3):227–32. doi: 10.1097/INF.0b013e31827687fc 23558321.
12. Simell B, Auranen K, Kayhty H, Goldblatt D, Dagan R, O′Brien KL, The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 11(7):841–55. Epub 2012/08/24. doi: 10.1586/erv.12.53 22913260.
13. Melegaro A, Gay NJ, Medley GF, Estimating the transmission parameters of pneumococcal carriage in households. Epidemiol Infect. 2004;132(3):433–41. 15188713.
14. Wolter N, Tempia S, Cohen C, Madhi SA, Venter M, Moyes J, et al. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis. 210(10):1649–57. Epub 2014/06/08. doi: 10.1093/infdis/jiu326 24907383.
15. Albrich WC, Madhi SA, Adrian PV, van Niekerk N, Telles JN, Ebrahim N, et al. Pneumococcal colonisation density: a new marker for disease severity in HIV-infected adults with pneumonia. BMJ Open. 2014;4(8):e005953. doi: 10.1136/bmjopen-2014-005953 25113557.
16. Alpkvist H, Athlin S, Naucler P, Herrmann B, Abdeldaim G, Slotved HC, et al. Clinical and Microbiological Factors Associated with High Nasopharyngeal Pneumococcal Density in Patients with Pneumococcal Pneumonia. PLoS ONE. 2015;10(10):e0140112. doi: 10.1371/journal.pone.0140112 26466142.
17. McCullers JA, The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol. 2014;12(4):252–62. doi: 10.1038/nrmicro3231 24590244.
18. McCool TL, Cate TR, Moy G, Weiser JN, The immune response to pneumococcal proteins during experimental human carriage. J Exp Med. 2002;195(3):359–65. doi: 10.1084/jem.20011576 11828011.
19. Ferreira DM, Neill DR, Bangert M, Gritzfeld JF, Green N, Wright AK, et al. Controlled human infection and rechallenge with Streptococcus pneumoniae reveals the protective efficacy of carriage in healthy adults. Am J Respir Crit Care Med. 2013;187(8):855–64. doi: 10.1164/rccm.201212-2277OC 23370916.
20. Wright AK, Bangert M, Gritzfeld JF, Ferreira DM, Jambo KC, Wright AD, et al. Experimental human pneumococcal carriage augments IL-17A-dependent T-cell defence of the lung. PLoS Pathog. 9(3):e1003274. Epub 2013/04/05. doi: 10.1371/journal.ppat.1003274 23555269.
21. Gilks CF, Ojoo SA, Ojoo JC, Brindle RJ, Paul J, Batchelor BI, et al. Invasive pneumococcal disease in a cohort of predominantly HIV-1 infected female sex-workers in Nairobi, Kenya. Lancet. 1996;347(9003):718–23. 8602001.
22. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol. 2012;13(11):1118–28. doi: 10.1038/ni.2419 23023392.
23. Geno KA, Saad JS, Nahm MH, Discovery of novel pneumococcal serotype, 35D: a natural WciG-deficient variant of serotype 35B. J Clin Microbiol. Epub 2017/02/17. doi: 10.1128/JCM.00054-17 28202800.
24. Pollard AJ, Perrett KP, Beverley PC, Maintaining protection against invasive bacteria with protein-polysaccharide conjugate vaccines. Nat Rev Immunol. 2009;9(3):213–20. doi: 10.1038/nri2494 19214194.
25. Clutterbuck EA, Lazarus R, Yu LM, Bowman J, Bateman EA, Diggle L, et al. Pneumococcal conjugate and plain polysaccharide vaccines have divergent effects on antigen-specific B cells. J Infect Dis. 2012;205(9):1408–16. doi: 10.1093/infdis/jis212 22457293.
26. McFetridge R, Meulen AS, Folkerth SD, Hoekstra JA, Dallas M, Hoover PA, et al. Safety, tolerability, and immunogenicity of 15-valent pneumococcal conjugate vaccine in healthy adults. Vaccine. 2015;33(24):2793–9. doi: 10.1016/j.vaccine.2015.04.025 25913828.
27. Whitney CG, Farley MM, Hadler J, Harrison LH, Bennett NM, Lynfield R, et al. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med. 2003;348(18):1737–46. doi: 10.1056/NEJMoa022823 12724479.
28. Feikin DR, Kagucia EW, Loo JD, Link-Gelles R, Puhan MA, Cherian T, et al. Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites. PLoS Med. 2013;10(9):e1001517. doi: 10.1371/journal.pmed.1001517 24086113.
29. Miyaji EN, Oliveira ML, Carvalho E, Ho PL, Serotype-independent pneumococcal vaccines. Cellular and molecular life sciences: CMLS. 2013;70(18):3303–26. doi: 10.1007/s00018-012-1234-8 23269437.
30. Auranen K, Rinta-Kokko H, Goldblatt D, Nohynek H, O′Brien KL, Satzke C, et al. Colonisation endpoints in Streptococcus pneumoniae vaccine trials. Vaccine. 2013;32(1):153–8. doi: 10.1016/j.vaccine.2013.08.061 24016803.
31. Siegel SJ, Weiser JN, Mechanisms of Bacterial Colonization of the Respiratory Tract. Annu Rev Microbiol. 2015;69:425–44. doi: 10.1146/annurev-micro-091014-104209 26488280.
32. Pennington SH, Pojar S, Mitsi E, Gritzfeld JF, Nikolaou E, Solorzano C, et al. Polysaccharide-specific Memory B-cells Predict Protection Against Experimental Human Pneumococcal Carriage. Am J Respir Crit Care Med. 2016. doi: 10.1164/rccm.201512-2467OC 27403678.
33. Weinberger DM, Dagan R, Givon-Lavi N, Regev-Yochay G, Malley R, Lipsitch M, Epidemiologic evidence for serotype-specific acquired immunity to pneumococcal carriage. J Infect Dis. 2008;197(11):1511–8. doi: 10.1086/587941 18471062.
34. Magee AD, Yother J, Requirement for capsule in colonization by Streptococcus pneumoniae. Infect Immun. 2001;69(6):3755–61. doi: 10.1128/IAI.69.6.3755-3761.2001 11349040.
35. Zafar MA, Hamaguchi S, Zangari T, Cammer M, Weiser JN, Capsule Type and Amount Affect Shedding and Transmission of Streptococcus pneumoniae. mBio. 2017;8(4). doi: 10.1128/mBio.00989-17 28830943.
36. Mitsi E, Roche AM, Reine J, Zangari T, Owugha JT, Pennington SH, et al. Agglutination by anti-capsular polysaccharide antibody is associated with protection against experimental human pneumococcal carriage. Mucosal Immunol. 2016. doi: 10.1038/mi.2016.71 27579859.
37. Roche AM, Richard AL, Rahkola JT, Janoff EN, Weiser JN, Antibody blocks acquisition of bacterial colonization through agglutination. Mucosal Immunol. 2015;8(1):176–85. doi: 10.1038/mi.2014.55 24962092.
38. Romero-Steiner S, Libutti D, Pais LB, Dykes J, Anderson P, Whitin JC, et al. Standardization of an opsonophagocytic assay for the measurement of functional antibody activity against Streptococcus pneumoniae using differentiated HL-60 cells. Clin Diagn Lab Immunol. 1997;4(4):415–22. Epub 1997/07/01. 9220157.
39. Collins AM, Wright AD, Mitsi E, Gritzfeld JF, Hancock CA, Pennington SH, et al. First Human Challenge Testing of a Pneumococcal Vaccine. Double-Blind Randomized Controlled Trial. Am J Respir Crit Care Med. 2015;192(7):853–8. doi: 10.1164/rccm.201503-0542OC 26114410.
40. Gladstone RA, Jefferies JM, Tocheva AS, Beard KR, Garley D, Chong WW, et al. Five winters of pneumococcal serotype replacement in UK carriage following PCV introduction. Vaccine. 2015;33(17):2015–21. doi: 10.1016/j.vaccine.2015.03.012 25776920.
41. Devine VT, Cleary DW, Jefferies JM, Anderson R, Morris DE, Tuck AC, et al. The rise and fall of pneumococcal serotypes carried in the PCV era. Vaccine. 35(9):1293–8. Epub 2017/02/06. doi: 10.1016/j.vaccine.2017.01.035 28161425.
42. Choi EH, Zhang F, Lu YJ, Malley R, Capsular Polysaccharide (CPS) Release by Serotype 3 Pneumococcal Strains Reduces the Protective Effect of Anti-Type 3 CPS Antibodies. Clin Vaccine Immunol. 2015;23(2):162–7. doi: 10.1128/CVI.00591-15 26677201.
43. Dagan R, Juergens C, Trammel J, Patterson S, Greenberg D, Givon-Lavi N, et al. Modeling pneumococcal nasopharyngeal acquisition as a function of anticapsular serum antibody concentrations after pneumococcal conjugate vaccine administration. Vaccine. 2016;34(36):4313–20. doi: 10.1016/j.vaccine.2016.06.075 27422342.
44. Jodar L, Butler J, Carlone G, Dagan R, Goldblatt D, Kayhty H, et al. Serological criteria for evaluation and licensure of new pneumococcal conjugate vaccine formulations for use in infants. Vaccine. 2003;21(23):3265–72. 12804857.
45. World Health OWho Expert Committee on Biological Standardization. World Health Organ Tech Rep Ser. 2005;927:1–154. 16454167.
46. Millar EV, O′Brien KL, Bronsdon MA, Madore D, Hackell JG, Reid R, et al. Anticapsular serum antibody concentration and protection against pneumococcal colonization among children vaccinated with 7-valent pneumococcal conjugate vaccine. Clin Infect Dis. 2007;44(9):1173–9. doi: 10.1086/513199 17407035.
47. Ojal J, Hammitt LL, Gaitho J, Scott JAG, Goldblatt D, Pneumococcal conjugate vaccine induced IgG and nasopharyngeal carriage of pneumococci: Hyporesponsiveness and immune correlates of protection for carriage. Vaccine. 2017;35(35 Pt B):4652–7. doi: 10.1016/j.vaccine.2017.05.088 28739116.
48. Granat SM, Ollgren J, Herva E, Mia Z, Auranen K, Makela PH, Epidemiological evidence for serotype-independent acquired immunity to pneumococcal carriage. J Infect Dis. 2009;200(1):99–106. Epub 2009/05/28. doi: 10.1086/599364 19469705.
49. Hogberg L, Geli P, Ringberg H, Melander E, Lipsitch M, Ekdahl K, Age- and serogroup-related differences in observed durations of nasopharyngeal carriage of penicillin-resistant pneumococci. J Clin Microbiol. 2007;45(3):948–52. doi: 10.1128/JCM.01913-06 17202280.
50. Roca A, Bojang A, Bottomley C, Gladstone RA, Adetifa JU, Egere U, et al. Effect on nasopharyngeal pneumococcal carriage of replacing PCV7 with PCV13 in the Expanded Programme of Immunization in The Gambia. Vaccine. 2015;33(51):7144–51. doi: 10.1016/j.vaccine.2015.11.012 26592141.
51. Cobey S, Lipsitch M, Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science. 2012;335(6074):1376–80. doi: 10.1126/science.1215947 22383809.
52. Azarian T, Grant LR, Georgieva M, Hammitt LL, Reid R, Bentley SD, et al. Pneumococcal protein antigen serology varies with age and may predict antigenic profile of colonizing isolates. J Infect Dis. 2016. doi: 10.1093/infdis/jiw628
53. Prevaes SM, van Wamel WJ, de Vogel CP, Veenhoven RH, van Gils EJ, van Belkum A, et al. Nasopharyngeal colonization elicits antibody responses to staphylococcal and pneumococcal proteins that are not associated with a reduced risk of subsequent carriage. Infect Immun. 2012;80(6):2186–93. doi: 10.1128/IAI.00037-12 22451514.
54. McCool TL, Weiser JN, Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect Immun. 2004;72(10):5807–13. Epub 2004/09/24. doi: 10.1128/IAI.72.10.5807-5813.2004 15385481.
55. Odutola A, Ota MO, Antonio M, Ogundare EO, Saidu Y, Foster-Nyarko E, et al. Efficacy of a novel, protein-based pneumococcal vaccine against nasopharyngeal carriage of Streptococcus pneumoniae in infants: A phase 2, randomized, controlled, observer-blind study. Vaccine. 2017;35(19):2531–42. doi: 10.1016/j.vaccine.2017.03.071 28389097.
56. Lu YJ, Gross J, Bogaert D, Finn A, Bagrade L, Zhang Q, et al. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 2008;4(9):e1000159. doi: 10.1371/journal.ppat.1000159 18802458.
57. Zhang Z, Clarke TB, Weiser JN, Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest. 2009;119(7):1899–909. doi: 10.1172/JCI36731 19509469.
58. Lu YJ, Leite L, Goncalves VM, Dias Wde O, Liberman C, Fratelli F, et al. GMP-grade pneumococcal whole-cell vaccine injected subcutaneously protects mice from nasopharyngeal colonization and fatal aspiration-sepsis. Vaccine. 2010;28(47):7468–75. doi: 10.1016/j.vaccine.2010.09.031 20858450.
59. Vuononvirta J, Peltola V, Ilonen J, Mertsola J, He Q, The Gene Polymorphism of IL-17 G-152A is Associated with Increased Colonization of Streptococcus pneumoniae in Young Finnish Children. The Pediatric infectious disease journal. 2015;34(9):928–32. doi: 10.1097/INF.0000000000000691 26376306.
60. Zhang Q, Leong SC, McNamara PS, Mubarak A, Malley R, Finn A, Characterisation of regulatory T cells in nasal associated lymphoid tissue in children: relationships with pneumococcal colonization. PLoS Pathog. 2011;7(8):e1002175. doi: 10.1371/journal.ppat.1002175 21852948.
61. Pido-Lopez J, Kwok WW, Mitchell TJ, Heyderman RS, Williams NA, Acquisition of pneumococci specific effector and regulatory Cd4+ T cells localising within human upper respiratory-tract mucosal lymphoid tissue. PLoS Pathog. 2011;7(12):e1002396. doi: 10.1371/journal.ppat.1002396 22144893.
62. Mubarak A, Ahmed MS, Upile N, Vaughan C, Xie C, Sharma R, et al. A dynamic relationship between mucosal T helper type 17 and regulatory T-cell populations in nasopharynx evolves with age and associates with the clearance of pneumococcal carriage in humans. Clin Microbiol Infect. 2016. doi: 10.1016/j.cmi.2016.05.017 27256063.
63. Jiang XL, Zhang GL, Yang T, Yang BH, Wang LJ, Wang QH, et al. Association of Pneumococcal Carriage and Expression of Foxp3+ Regulatory T Cells and Th17 Cells in the Adenoids of Children. Respiration. 2015;90(1):25–32. doi: 10.1159/000381724 25925832.
64. Gray C, Ahmed MS, Mubarak A, Kasbekar AV, Derbyshire S, McCormick MS, et al. Activation of memory Th17 cells by domain 4 pneumolysin in human nasopharynx-associated lymphoid tissue and its association with pneumococcal carriage. Mucosal Immunol. 2014;7(3):705–17. doi: 10.1038/mi.2013.89 24220296.
65. Neill DR, Fernandes VE, Wisby L, Haynes AR, Ferreira DM, Laher A, et al. T regulatory cells control susceptibility to invasive pneumococcal pneumonia in mice. PLoS Pathog. 8(4):e1002660. Epub 2012/05/09. doi: 10.1371/journal.ppat.1002660 22563306.
66. Lundgren A, Bhuiyan TR, Novak D, Kaim J, Reske A, Lu YJ, et al. Characterization of Th17 responses to Streptococcus pneumoniae in humans: comparisons between adults and children in a developed and a developing country. Vaccine. 2012;30(26):3897–907. doi: 10.1016/j.vaccine.2012.03.082 22504663.
67. Skoberne M, Ferreira DM, Hetherington S, Fitzgerald R, Gordon SB. Pneumococcal protein vaccine GEN-004 reduces experimental human pneumococcal carriage in healthy adults. International Symposium on Pneumococci and Pneumococcal Diseases 2016. Glascow, UK2016.
68. Short KR, Reading PC, Wang N, Diavatopoulos DA, Wijburg OL, Increased nasopharyngeal bacterial titers and local inflammation facilitate transmission of Streptococcus pneumoniae. mBio. 2012;3(5). doi: 10.1128/mBio.00255-12 23015738.
69. Ronchetti R, Villa MP, Martella S, La Grutta S, Ronchetti F, Biscione GL, et al. Nasal cellularity in 183 unselected schoolchildren aged 9 to 11 years. Pediatrics. 2002;110(6):1137–42. 12456911.
70. Jochems SP, Piddock K, Rylance J, Adler H, Carniel BF, Collins A, et al. Novel Analysis of Immune Cells from Nasal Microbiopsy Demonstrates Reliable, Reproducible Data for Immune Populations, and Superior Cytokine Detection Compared to Nasal Wash. PLoS ONE. 2017;12(1):e0169805. doi: 10.1371/journal.pone.0169805 28107457.
71. Kim GL, Choi SY, Seon SH, Lee S, Park SS, Song JY, et al. Pneumococcal pep27 mutant immunization stimulates cytokine secretion and confers long-term immunity with a wide range of protection, including against non-typeable strains. Vaccine. 2016;34(51):6481–92. doi: 10.1016/j.vaccine.2016.10.071 27865564.
72. Weinberger DM, Trzcinski K, Lu YJ, Bogaert D, Brandes A, Galagan J, et al. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog. 2009;5(6):e1000476. doi: 10.1371/journal.ppat.1000476 19521509.
73. Trzcinski K, Li Y, Weinberger DM, Thompson CM, Cordy D, Bessolo A, et al. Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model. mBio. 2015;6(5):e00902–15. doi: 10.1128/mBio.00902-15 26374118.
74. van Rossum AM, Lysenko ES, Weiser JN, Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model. Infect Immun. 2005;73(11):7718–26. doi: 10.1128/IAI.73.11.7718-7726.2005 16239576.
75. Davis KM, Nakamura S, Weiser JN, Nod2 sensing of lysozyme-digested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J Clin Invest. 2011;121(9):3666–76. doi: 10.1172/JCI57761 21841315.
76. Siegel SJ, Tamashiro E, Weiser JN, Clearance of Pneumococcal Colonization in Infants Is Delayed through Altered Macrophage Trafficking. PLoS Pathog. 2015;11(6):e1005004. doi: 10.1371/journal.ppat.1005004 26107875.
77. Krone CL, Trzcinski K, Zborowski T, Sanders EA, Bogaert D, Impaired innate mucosal immunity in aged mice permits prolonged Streptococcus pneumoniae colonization. Infect Immun. 2013;81(12):4615–25. doi: 10.1128/IAI.00618-13 24082075.
78. Puchta A, Naidoo A, Verschoor CP, Loukov D, Thevaranjan N, Mandur TS, et al. TNF Drives Monocyte Dysfunction with Age and Results in Impaired Anti-pneumococcal Immunity. PLoS Pathog. 2016;12(1):e1005368. doi: 10.1371/journal.ppat.1005368 26766566.
79. Nakamura S, Davis KM, Weiser JN, Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J Clin Invest. 2011;121(9):3657–65. doi: 10.1172/JCI57762 21841308
80. Erbel C, Akhavanpoor M, Okuyucu D, Wangler S, Dietz A, Zhao L, et al. IL-17A influences essential functions of the monocyte/macrophage lineage and is involved in advanced murine and human atherosclerosis. J Immunol. 2014;193(9):4344–55. doi: 10.4049/jimmunol.1400181 25261478.
81. Gill MA, Long K, Kwon T, Muniz L, Mejias A, Connolly J, et al. Differential recruitment of dendritic cells and monocytes to respiratory mucosal sites in children with influenza virus or respiratory syncytial virus infection. J Infect Dis. 2008;198(11):1667–76. doi: 10.1086/593018 18847373.
82. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH, TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol. 2006;177(11):7980–9. 17114471.
83. Warfel JM, Zimmerman LI, Merkel TJ, Comparison of Three Whole-Cell Pertussis Vaccines in the Baboon Model of Pertussis. Clin Vaccine Immunol. 2015;23(1):47–54. doi: 10.1128/CVI.00449-15 26561389.
84. Sun K, Metzger DW, Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med. 2008;14(5):558–64. Epub 2008/04/29. doi: 10.1038/nm1765 18438414.
85. Thors V, Christensen H, Morales-Aza B, Vipond I, Muir P, Finn A, The Effects of Live Attenuated Influenza Vaccine on Nasopharyngeal Bacteria in Healthy 2 to 4 Year Olds. A Randomized Controlled Trial. Am J Respir Crit Care Med. 2016;193(12):1401–9. doi: 10.1164/rccm.201510-2000OC 26742001.
86. Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S, Wanjiru E, et al. The prevalence and risk factors for pneumococcal colonization of the nasopharynx among children in Kilifi District, Kenya. PLoS ONE. 7(2):e30787. Epub 2012/03/01. doi: 10.1371/journal.pone.0030787 22363489.
87. Glennie S, Gritzfeld JF, Pennington SH, Garner-Jones M, Coombes N, Hopkins MJ, et al. Modulation of nasopharyngeal innate defenses by viral coinfection predisposes individuals to experimental pneumococcal carriage. Mucosal Immunol. 2015. doi: 10.1038/mi.2015.35 25921341.
88. McNamee LA, Harmsen AG, Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect Immun. 2006;74(12):6707–21. doi: 10.1128/IAI.00789-06 16982840.
89. van der Sluijs KF, van Elden LJ, Nijhuis M, Schuurman R, Florquin S, Shimizu T, et al. Involvement of the platelet-activating factor receptor in host defense against Streptococcus pneumoniae during postinfluenza pneumonia. Am J Physiol Lung Cell Mol Physiol. 2006;290(1):L194–9. doi: 10.1152/ajplung.00050.2005 16100290.
90. Zhang JR, Mostov KE, Lamm ME, Nanno M, Shimida S, Ohwaki M, et al. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell. 2000;102(6):827–37. 11030626.
91. Del Donno M, Bittesnich D, Chetta A, Olivieri D, Lopez-Vidriero MT, The effect of inflammation on mucociliary clearance in asthma: an overview. Chest. 2000;118(4):1142–9. 11035690.
92. Plotkowski MC, Puchelle E, Beck G, Jacquot J, Hannoun C, Adherence of type I Streptococcus pneumoniae to tracheal epithelium of mice infected with influenza A/PR8 virus. Am Rev Respir Dis. 1986;134(5):1040–4. doi: 10.1164/arrd.1986.134.5.1040 3777666.
93. Siegel SJ, Roche AM, Weiser JN, Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe. 2014;16(1):55–67. doi: 10.1016/j.chom.2014.06.005 25011108.
94. Parker D, Martin FJ, Soong G, Harfenist BS, Aguilar JL, Ratner AJ, et al. Streptococcus pneumoniae DNA initiates type I interferon signaling in the respiratory tract. MBio. 2(3):e00016–11. Epub 2011/05/19. doi: 10.1128/mBio.00016-11 21586648.
95. Ivanov S, Paget C, Trottein F, Role of non-conventional T lymphocytes in respiratory infections: the case of the pneumococcus. PLoS Pathog. 10(10):e1004300. Epub 2014/10/10. doi: 10.1371/journal.ppat.1004300 25299581.
96. Richard AL, Siegel SJ, Erikson J, Weiser JN, TLR2 signaling decreases transmission of Streptococcus pneumoniae by limiting bacterial shedding in an infant mouse Influenza A co-infection model. PLoS Pathog. 2014;10(8):e1004339. doi: 10.1371/journal.ppat.1004339 25166617.
97. Gossec L, Coates LC, de Wit M, Kavanaugh A, Ramiro S, Mease PJ, et al. Management of psoriatic arthritis in 2016: a comparison of EULAR and GRAPPA recommendations. Nat Rev Rheumatol. 2016;12(12):743–50. doi: 10.1038/nrrheum.2016.183 27829672.
98. Li Y, Gierahn T, Thompson CM, Trzcinski K, Ford CB, Croucher N, et al. Distinct effects on diversifying selection by two mechanisms of immunity against Streptococcus pneumoniae. PLoS Pathog. 2012;8(11):e1002989. doi: 10.1371/journal.ppat.1002989 23144610.
99. Lipsitch M, Jha A, Simonsen L, Observational studies and the difficult quest for causality: lessons from vaccine effectiveness and impact studies. Int J Epidemiol. Epub 2016/07/28. doi: 10.1093/ije/dyw124 27453361.