MicroRNA-155 is required for clearance of Streptococcus pneumoniae from the nasopharynx

Infection and Immunity

Volumn 82, Issue 11, 2014, Pages 4824-4833

  Verschoor, Chris P ^a   Dorrington, Michael G ^a   Novakowski, Kyle E ^a   Kaiser, Julie ^a   Radford, Katherine ^b   Nair, Parameswaran ^b   Anipindi, Varun ^a   Kaushic, Charu ^a   Surette, Michael G ^a   Bowdish, Dawn M E ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MICRORNA 155; SMALL UNTRANSLATED RNA; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; MICRORNA; MIRN155 MICRORNA, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL LOAD; BACTERICIDAL ACTIVITY; CD4+ T LYMPHOCYTE; CELL STRUCTURE; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; KNOCKOUT MOUSE; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE RECEPTOR WITH COLLAGENOUS STRUCTURE; MOUSE; NASOPHARYNX; NONHUMAN; PNEUMOCOCCAL INFECTION; POLARIZATION; REGULATORY MECHANISM; STREPTOCOCCUS PNEUMONIAE; TH1 CELL; TH17 CELL; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; PHAGOCYTOSIS; PHYSIOLOGY;

ANIMALS; CARRIER STATE; GENE EXPRESSION REGULATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MICRORNAS; NASOPHARYNX; PHAGOCYTOSIS; STREPTOCOCCUS PNEUMONIAE;

EID: 84907961899     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02251-14     Document Type: Article

References (42)

1. Isaacman DJ, McIntosh ED, Reinert RR. 2010. Burden of invasive pneumococcal disease and serotype distribution among Streptococcus pneumoniae isolates in young children in Europe: impact of the 7-valent pneumococcal conjugate vaccine and considerations for future conjugate vaccines. Int. J. Infect. Dis. 14:e197-e209. http://dx.doi.org/10.1016/j.ijid.2009.05.010.
2. Melzer M, Welch C. 2013. 30-day mortality in UK patients with bacteraemic community-acquired pneumonia. Infection 41:1005-1011. http://dx.doi.org/10.1007/s15010-013-0462-7.
3. Cohen JM, Khandavilli S, Camberlein E, Hyams C, Baxendale HE, Brown JS. 2011. Protective contributions against invasive Streptococcus pneumoniae pneumonia of antibody and Th17-cell responses to nasopharyngeal colonisation. PLoS One 6(10):e25558. http://dx.doi.org/10.1371/journal.pone.0025558.
4. Huang SS, Platt R, Rifas-Shiman SL, Pelton SI, Goldmann D, Finkelstein JA. 2005. Post-PCV7 changes in colonizing pneumococcal serotypes in 16 Massachusetts communities, 2001 and 2004. Pediatrics 116:e408-e413. http://dx.doi.org/10.1542/peds.2004-2338.
5. Hammitt LL, Bruden DL, Butler JC, Baggett HC, Hurlburt DA, Reasonover A, Hennessy TW. 2006. Indirect effect of conjugate vaccine on adult carriage of Streptococcus pneumoniae: an explanation of trends in invasive pneumococcal disease. J. Infect. Dis. 193:1487-1494. http://dx.doi.org/10.1086/503805.
6. Moffitt KL, Gierahn TM, Lu Y, Gouveia P, Alderson M, Flechtner JB, Higgins DE, Malley R. 2011. T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe 9:158-165. http://dx.doi.org/10.1016/j.chom.2011.01.007.
7. Marqués JM, Rial A, Muñoz N, Pellay F-X, Van Maele L, Léger H, Camou T, Sirard J-C, Benecke A, Chabalgoity JA. 2012. Protection against Streptococcus pneumoniae serotype 1 acute infection shows a signature of Th17- and IFN-γ-mediated immunity. Immunobiology 217:420-429. http://dx.doi.org/10.1016/j.imbio.2011.10.012.
8. Lu Y-J, Gross J, Bogaert D, Finn A, Bagrade L, Zhang Q, Kolls JK, Srivastava A, Lundgren A, Forte S, Thompson CM, Harney KF, Anderson PW, Lipsitch M, Malley R. 2008. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 4(9): e1000159. http://dx.doi.org/10.1371/journal.ppat.1000159.
9. Zhang Z, Clarke TB, Weiser JN. 2009. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J. Clin. Invest. 119:1899-1909. http://dx.doi.org/10.1172/JCI36731.
10. 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.
11. Dorrington MG, Roche AM, Chauvin SE, Tu Z, Mossman KL, Weiser JN, Bowdish DME. 2013. MARCO is required for TLR2- and Nod2-mediated responses to Streptococcus pneumoniae and clearance of pneumococcal colonization in the murine nasopharynx. J. Immunol. 190:250-258. http://dx.doi.org/10.4049/jimmunol.1202113.
12. Faraoni I, Antonetti FR, Cardone J, Bonmassar E. 2009. miR-155 gene: a typical multifunctional microRNA. Biochim. Biophys. Acta 1792:497-505. http://dx.doi.org/10.1016/j.bbadis.2009.02.013.
13. Tam W, Ben-Yehuda D, Hayward WS. 1997. bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Mol. Cell. Biol. 17:1490-1502.
14. Metzler M, Wilda M, Busch K, Viehmann S, Borkhardt A. 2004. High expression of precursor microRNA-155/BICRNAin children with Burkitt lymphoma. Genes Chromosomes Cancer 39:167-169. http://dx.doi.org/10.1002/gcc.10316.
15. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, Lund E, Dahlberg JE. 2005. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. U. S. A. 102:3627-3632. http://dx.doi.org/10.1073/pnas.0500613102.
16. O'Connell RM, Kahn D, Gibson WSJ, Round JL, Scholz RL, Chaudhuri AA, Kahn ME, Rao DS, Baltimore D. 2010. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33:607-619. http://dx.doi.org/10.1016/j.immuni.2010.09.009.
17. Koch M, Mollenkopf H-J, Klemm U, Meyer TF. 2012. Induction of microRNA-155 is TLR- and type IV secretion system-dependent in macrophages and inhibits DNA-damage induced apoptosis. Proc. Natl. Acad. Sci. U. S. A. 109:E1153-1162. http://dx.doi.org/10.1073/pnas.1116125109.
18. Wang P, Hou J, Lin L, Wang C, Liu X, Li D, Ma F, Wang Z, Cao X. 2010. Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J. Immunol. 185:6226-6233. http://dx.doi.org/10.4049/jimmunol.1000491.
19. Xu F, Kang Y, Zhang H, Piao Z, Yin H, Diao R, Xia J, Shi L. 2013. Akt1-mediated regulation of macrophage polarization in a murine model of Staphylococcus aureus pulmonary infection. J. Infect. Dis. 208:528-538. http://dx.doi.org/10.1093/infdis/jit177.
20. Cremer TJ, Ravneberg DH, Clay CD, Piper-Hunter MG, Marsh CB, Elton TS, Gunn JS, Amer A, Kanneganti T-D, Schlesinger LS, Butchar JP, Tridandapani S. 2009. MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced proinflammatory cytokine response. PLoS One 4(12):e8508. http://dx.doi.org/10.1371/journal.pone.0008508.
21. Kumar R, Halder P, Sahu SK, Kumar M, Kumari M, Jana K, Ghosh Z, Sharma P, Kundu M, Basu J. 2012. Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell. Microbiol. 14:1620-1631. http://dx.doi.org/10.1111/j.1462-5822.2012.01827.x.
22. Yao R, Ma Y-L, Liang W, Li H-H, Ma Z-J, Yu X, Liao Y-H. 2012. MicroRNA-155 modulates Treg and Th17 cells differentiation and Th17 cell function by targeting SOCS1. PLoS One 7(10):e46082. http://dx.doi.org/10.1371/journal.pone.0046082.
23. Murugaiyan G, Beynon V, Mittal A, Joller N, Weiner HL. 2011. Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 187:2213-2221. http://dx.doi.org/10.4049/jimmunol.1003952.
24. Oertli M, Engler DB, Kohler E, Koch M, Meyer TF, Müller A. 2011. MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic gastritis and colitis. J. Immunol. 187:3578-3586. http://dx.doi.org/10.4049/jimmunol.1101772.
25. 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.
26. Kafka D, Ling E, Feldman G, Benharroch D, Voronov E, Givon-Lavi N, Iwakura Y, Dagan R, Apte RN, Mizrachi-Nebenzahl Y. 2008. Contribution of IL-1 to resistance to Streptococcus pneumoniae infection. Int. Immunol. 20:1139-1146. http://dx.doi.org/10.1093/intimm/dxn071.
27. Ferreira DM, Oliveira MLS, Moreno AT, Ho PL, Briles DE, Miyaji EN. 2010. Protection against nasal colonization with Streptococcus pneumoniae by parenteral immunization with a DNA vaccine encoding PspA (pneumococcal surface protein A). Microb. Pathog. 48:205-213. http://dx.doi.org/10.1016/j.micpath.2010.02.009.
28. Zhang Q, Bagrade L, Bernatoniene J, Clarke E, Paton JC, Mitchell TJ, Nunez DA, Finn A. 2007. Low CD4 T cell immunity to pneumolysin is associated with nasopharyngeal carriage of pneumococci in children. J. Infect. Dis. 195:1194-1202. http://dx.doi.org/10.1086/512617.
29. Dinarello CA. 2009. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27:519-550. http://dx.doi.org/10.1146/annurev.immunol.021908.132612.
30. Fang R, Tsuchiya K, Kawamura I, Shen Y, Hara H, Sakai S, Yamamoto T, Fernandes-Alnemri T, Yang R, Hernandez-Cuellar E, Dewamitta SR, Xu Y, Qu H, Alnemri ES, Mitsuyama M. 2011. Critical roles of ASC inflammasomes in caspase-1 activation and host innate resistance to Streptococcus pneumoniae infection. J. Immunol. 187:4890-4899. http://dx.doi.org/10.4049/jimmunol.1100381.
31. van Rossum AM, Lysenko ES, Weiser JN. 2005. Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model. Infect. Immun. 73:7718-7726. http://dx.doi.org/10.1128/IAI.73.11.7718-7726.2005.
32. Domingo-Gonzalez R, Katz S, Serezani CH, Moore TA, Levine AM, Moore BB. 2013. Prostaglandin E2-induced changes in alveolar macrophage scavenger receptor profiles differentially alter phagocytosis of Pseudomonas aeruginosa and Staphylococcus aureus post-bone marrow transplant. J. Immunol. 190:5809-5817. http://dx.doi.org/10.4049/jimmunol.1203274.
33. Ghorpade DS, Leyland R, Kurowska-Stolarska M, Patil SA, Balaji KN. 2012. MicroRNA-155 is required for Mycobacterium bovis BCG-mediated apoptosis of macrophages. Mol. Cell. Biol. 32:2239-2253. http://dx.doi.org/10.1128/MCB.06597-11.
34. Shahrara S, Pickens SR, Mandelin AM 2nd, Karpus WJ, Huang Q, Kolls JK, Pope RM. 2010. IL-17-mediated monocyte migration occurs partially through CC chemokine ligand 2/monocyte chemoattractant protein-1 induction. J. Immunol. 184:4479-4487. http://dx.doi.org/10.4049/jimmunol.0901942.
35. Barin JG, Baldeviano GC, Talor MV, Wu L, Ong S, Quader F, Chen P, Zheng D, Caturegli P, Rose NR, Ciháková D. 2012. Macrophages participate in IL-17-mediated inflammation. Eur. J. Immunol. 42:726-736. http://dx.doi.org/10.1002/eji.201141737.
36. Smith E, Prasad K-MR, Butcher M, Dobrian A, Kolls JK, Ley K, Galkina E. 2010. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 121:1746-1755. http://dx.doi.org/10.1161/CIRCULATIONAHA.109.924886.
37. Hu R, Huffaker TB, Kagele DA, Runtsch MC, Bake E, Chaudhuri AA, Round JL, O'Connell RM. 2013. MicroRNA-155 confers encephalogenic potential to Th17 cells by promoting effector gene expression. J. Immunol. 190:5972-5980. http://dx.doi.org/10.4049/jimmunol.1300351.
38. Verschoor ML, Wilson LA, Singh G. 2010. Mechanisms associated with mitochondrial-generated reactive oxygen species in cancer. Can. J. Physiol. Pharmacol. 88:204-219. http://dx.doi.org/10.1139/Y09-135.
39. Zhang J, Cheng Y, Cui W, Li M, Li B, Guo L. 2014. MicroRNA-155 modulates Th1 and Th17 cell differentiation and is associated with multiple sclerosis and experimental autoimmune encephalomyelitis. J. Neuroimmunol. 266:56-63. http://dx.doi.org/10.1016/j.jneuroim.2013.09.019.
40. Santosuosso M, Divangahi M, Zganiacz A, Xing Z. 2002. Reduced tissue macrophage population in the lung by anticancer agent cyclophosphamide: restoration by local granulocyte macrophage-colony-stimulating factor gene transfer. Blood 99:1246-1252. http://dx.doi.org/10.1182/blood.V99.4.1246.
41. Davis KM, Nakamura S, Weiser JN. 2011. Nod2 sensing of lysozymedigested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J. Clin. Invest. 121:3666-3676. http://dx.doi.org/10.1172/JCI57761.
42. Ghaffar F, Friedland IR, McCracken, GH, Jr. 1999. Dynamics of nasopharyngeal colonization by Streptococcus pneumoniae. Pediatr. Infect. Dis. J. 18:638-646. http://dx.doi.org/10.1097/00006454-199907000-00016.