Interleukin 17A promotes pneumococcal clearance by recruiting neutrophils and inducing apoptosis through a p38 mitogen-activated protein kinase-dependent mechanism in acute otitis media

Infection and Immunity

Volumn 82, Issue 6, 2014, Pages 2368-2377

  Wang, Wei ^a   Zhou, Aie ^b   Zhang, Xuemei ^a   Xiang, Yun ^a   Huang, Yifei ^a   Wang, Lei ^a   Zhang, Shuai ^a   Liu, Yusi ^a   Yin, Yibing ^a   He, Yujuan ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING TRADITIONAL CHINESE MEDICINE HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; MITOGEN ACTIVATED PROTEIN KINASE P38;

ACUTE OTITIS MEDIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; C57BL 6 MOUSE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MIDDLE EAR; MOUSE; NEUTROPHIL; NONHUMAN; OBSERVATIONAL STUDY; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STREPTOCOCCUS PNEUMONIAE; ACUTE DISEASE; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; MICROBIOLOGY; NEUTROPHIL CHEMOTAXIS; OTITIS MEDIA; PHYSIOLOGY;

ACUTE DISEASE; ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; INTERLEUKIN-17; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; OTITIS MEDIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 84900392450     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00006-14     Document Type: Article

References (42)

1. Monasta L, Ronfani L, Marchetti F, Montico M, Vecchi Brumatti L, Bavcar A, Grasso D, Barbiero C, Tamburlini G. 2012. Burden of disease caused by otitis media: systematic review and global estimates. PLoS One 7: e36226. http://dx.doi.org/10.1371/journal.pone.0036226.
2. Bakaletz LO. 2010. Immunopathogenesis of polymicrobial otitis media. J. Leukoc. Biol. 87:213-222. http://dx.doi.org/10.1189/jlb.0709518.
3. Barkai G, Leibovitz E, Givon-Lavi N, Dagan R. 2009. Potential contribution by nontypable Haemophilus influenzae in protracted and recurrent acute otitis media. Pediatr. Infect. Dis. J. 28:466-471. http://dx.doi.org/10.1097/INF.0b013e3181950c74.
4. Cua DJ, Tato M. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10:479-489. http://dx.doi.org/10.1038/nri2800.
5. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, Villanueva EC, Shah P, Kaplan MJ, Bruce AT. 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187:490-500. http://dx.doi.org/10.4049/jimmunol.1100123.
6. Xu S, Cao X. 2010. Interleukin-17 and its expanding biological functions. Cell Mol. Immunol. 7:164-174. http://dx.doi.org/10.1038/cmi.2010.21.
7. Matsuzaki G, Umemura M. 2007. Interleukin-17 as an effector molecule of innate and acquired immunity against infections. Microbiol. Immunol. 51:1139-1147. http://dx.doi.org/10.1111/j.1348-0421.2007.tb04008.x.
8. Hamada S, Umemura M, Shiono T, Tanaka K, Yahagi A, Begum MD, Oshiro K, Okamoto Y, Watanabe H, Kawakami K, Roark C, Born WK, O'Brien R, Ikuta K, Ishikawa H, Nakae S, Iwakura Y, Ohta T, Matsuzaki G. 2008. IL-17A produced by γδ T cells plays a critical role in innate immunity against listeria monocytogenes infection in the live. J. Immunol. 181:3456-3463.
9. Schulz SM, Köhler G, Holscher C, Iwakura Y, Alber G. 2008. IL-17A is produced by Th17, γδ T cells and other CD4- lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance. Int. Immunol. 20:1129-1138. http://dx.doi.org/10.1093/intimm/dxn069.
10. Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R. 2009. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31:761-771. http://dx.doi.org/10.1016/j.immuni.2009.09.016.
11. McEllistrem MC, Adams JM, Patel K, Mendelsohn AB, Kaplan SL, Bradley JS, Schutze GE, Kim KS, Mason EO, Wald ER. 2005. Acute otitis media due to penicillin-nonsusceptible Streptococcus pneumoniae before and after the introduction of the pneumococcal conjugate vaccine. Clin. Infect. Dis. 40:1738-1744. http://dx.doi.org/10.1086/429908.
12. Tong HH, Li YX, Stahl GL, Thurman JM. 2010. Enhanced susceptibility to acute pneumococcal otitis media in mice deficient in complement C1qa, factor B, and factor B/C2. Infect. Immun. 78:976-983. http://dx.doi.org/10.1128/IAI.01012-09.
13. MacArthur CJ, Hefeneider SH, Kempton JB, Parrish SK, McCoy SL, Trune DR. 2006. Evaluation of the mouse model for acute otitis media. Hear. Res. 219:12-23. http://dx.doi.org/10.1016/j.heares.2006.05.012.
14. Long JP, Tong HH, Shannon PA, DeMaria TF. 2003. Differential expression of cytokine genes and inducible nitric oxide synthase induced by opacity phenotype variants of Streptococcus pneumoniae during acute otitis media in the rat. Infect. Immun. 71:5531-5540. http://dx.doi.org/10.1128/IAI.71.10.5531-5540.2003.
15. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. 2003. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170:2106-2112.
16. Werner JL, Gessner MA, Lilly LM, Nelson MP, Metz AE, Horn D, Dunaway CW, Deshane J, Chaplin DD, Weaver CT, Brown GD, Steele C. 2011. Neutrophils produce interleukin 17A (IL-17A) in a dectin-1-and IL-23-dependent manner during invasive fungal infection. Infect. Immun. 79:3966-3977. http://dx.doi.org/10.1128/IAI.05493-11.
17. Korn T, Bettelli E, Oukka M, Kuchroo VK. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27:485-517. http://dx.doi.org/10.1146/annurev.immunol.021908.132710.
18. Nathan C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6:173-178. http://dx.doi.org/10.1038/nri1785.
19. Garvy BA, Harmsen AG. 1996. The importance of neutrophils in resistance to pneumococcal pneumonia in adult and neonatal mice. Inflammation 20:499-512. http://dx.doi.org/10.1007/BF01487042.
20. Nograles KE, Zaba LC, Guttman-Yassky E, Fuentes-Duculan J, Suárez-Fariñas M, Cardinale I, Khatcherian A, Gonzalez J, Pierson KC, White TR, Pensabene C, Coats I, Novitskaya I, Lowes MA, Krueger JG. 2008. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 159:1092-1102. http://dx.doi.org/10.1111/j.1365-2133.2008.08769.x.
21. Albanesi C, Scarponi C, Cavani A, Federici M, Nasorri F, Girolomoni G. 2000. Interleukin-17 is produced by both Th1 and Th2 lymphocytes, and modulates interferon-gamma-and interleukin-4-induced activation of human keratinocytes. J. Investig. Dermatol. 115:81-87. http://dx.doi.org/10.1046/j.1523-1747.2000.00041.x.
22. Hoeve MA, Savage ND, de Boer T, Langenberg DM, de Waal Malefyt R, Ottenhoff TH, Verreck FA. 2006. Divergent effects of IL-12 and IL-23 on the production of IL-17 by human T cells. Eur. J. Immunol. 36:661-670. http://dx.doi.org/10.1002/eji.200535239.
23. Nie H, Zheng Y, Li R, Guo TB, He D, Fang L, Liu X, Xiao L, Chen X, Wan B, Chin YE, Zhang JZ. 2013. Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis. Nat. Med. 19:322-328. http://dx.doi.org/10.1038/nm.3085.
24. Dong C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8:337-348. http://dx.doi.org/10.1038/nri2295.
25. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240. http://dx.doi.org/10.1084/jem.20041257.
26. Grommes J, Soehnlein O. 2011. Contribution of neutrophils to acute lung injury. Mol. Med. 17:293-307. http://dx.doi.org/10.2119/molmed.2010.00138.
27. Cara DC, Kaur J, Forster M, McCafferty DM, Kubes P. 2001. Role of p38 mitogen-activated protein kinase in chemokine-induced emigration and chemotaxis in vivo. J. Immunol. 167:6552-6558.
28. Yang Z, Zhang X, Darrah PA, Mosser DM. 2010. The regulation of Th1 responses by the p38 MAPK. J. Immunol. 185:6205-6213. http://dx.doi.org/10.4049/jimmunol.1000243.
29. Puddicombe SM, Davies DE. 2000. The role of MAP kinases in intracellular signal transduction in bronchial epithelium. Clin. Exp. Allergy 30:7-11. http://dx.doi.org/10.1046/j.1365-2222.2000.00709.x.
30. Chen Y, Kijlstra A, Chen Y, Yang P. 2011. IL-17A stimulates the production of inflammatory mediators via Erk1/2, p38 MAPK, PI3K/Akt, and NF-κB pathways in ARPE-19 cells. Mol. Vis. 17:3072-3077.
31. Laan M, Lötvall J, Chung KF, Lindén A. 2001. IL-17-induced cytokine release in human bronchial epithelial cells in vitro: role of mitogenactivated protein (MAP) kinases. Br. J. Pharmacol. 133:200-206. http://dx.doi.org/10.1038/sj.bjp.0704063.
32. Kawaguchi M, Kokubu F, Kuga H, Matsukura S, Hoshino H, Ieki K, Imai T, Adachi M, Huang SK. 2001. Modulation of bronchial epithelial cells by IL-17. J. Allergy Clin. Immunol. 108:804-809. http://dx.doi.org/10.1067/mai.2001.119027.
33. Mitroulis I, Kourtzelis I, Kambas K, Rafail S, Chrysanthopoulou A, Speletas M, Ritis K. 2010. Regulation of the autophagic machinery in human neutrophils. Eur. J. Immunol. 40:1461-1472. http://dx.doi.org/10.1002/eji.200940025.
34. Zychlinsky A, Sansonetti P. 1997. Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J. Clin. Invest. 100:493-495. http://dx.doi.org/10.1172/JCI119557.
35. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. 1999. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. U. S. A. 96:2396-2401. http://dx.doi.org/10.1073/pnas.96.5.2396.
36. Dockrell DH, Lee M, Lynch DH, Read RC. 2001. Immune-mediated phagocytosis and killing of Streptococcus pneumoniae are associated with direct and bystander macrophage apoptosis. J. Infect. Dis. 184:713-722. http://dx.doi.org/10.1086/323084.
37. Dockrell DH, Marriott HM, Prince LR, Ridger VC, Ince PG, Hellewell PG, Whyte MK. 2003. Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J. Immunol. 171:5380-5388.
38. Steinwede K, Henken S, Bohling J, Maus R, Ueberberg B, Brumshagen C, Brincks EL, Griffith TS, Welte T, Maus UA. 2012. TNF-related apoptosis-inducing ligand (TRAIL) exerts therapeutic efficacy for the treatment of pneumococcal pneumonia in mice. J. Exp. Med. 209:1937-1952. http://dx.doi.org/10.1084/jem.20120983.
39. Ali F, Lee ME, Iannelli F, Pozzi G, Mitchell TJ, Read RC, Dockrell DH. 2003. Streptococcus pneumoniae-associated human macrophage apoptosis after bacterial internalization via complement and Fcγ receptors correlates with intracellular bacterial load. J. Infect. Dis. 188:1119-1131. http://dx.doi.org/10.1086/378675.
40. Serhan CN, Savill J. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6:1191-1197. http://dx.doi.org/10.1038/ni1276.
41. Cai B, Chang SH, Becker EB, Bonni A, Xia Z. 2006. p38 MAP kinase mediates apoptosis through phosphorylation of BimEL at Ser-65. J. Biol. Chem. 281:25215-25222. http://dx.doi.org/10.1074/jbc.M512627200.
42. Boronkai A, Bellyei S, Szigeti A, Pozsgai E, Bognar Z, Sumegi B, Gallyas F, Jr. 2009. Potentiation of paclitaxel-induced apoptosis by galectin-13 overexpression via activation of Ask-1-p38-MAP kinase and JNK/SAPK pathways and suppression of Akt and ERK1/2 activation in U-937 human macrophage cells. Eur. J. Cell Biol. 88:753-763. http://dx.doi.org/10.1016/j.ejcb.2009.07.005.