TLR4-mediated induction of TLR2 signaling is critical in the pathogenesis and resolution of otitis media

Innate Immunity

Volumn 15, Issue 4, 2009, Pages 205-215

  Leichtle, Anke ^a,b   Hernandez, Michelle ^c   Pak, Kwang ^a   Yamasaki, Kenshi ^a   Cheng Chun Fang, C F ^a   Webster, Nicholas J ^d   Ryan, Allen F ^a   Wasserman, Stephen I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Haemophilus influenzae; Innate immunity; Otitis media; TLR; TNF

Indexed keywords

INTERLEUKIN 10; MESSENGER RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CELL INFILTRATION; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE INDUCTION; HAEMOPHILUS INFLUENZAE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OTITIS MEDIA; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CHILD; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OTITIS MEDIA; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MUS;

EID: 67949104967     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425909103170     Document Type: Article

References (56)

1. Infante-Rivard C., Fernandez A. Otitis media in children: Frequency, risk factors, and research avenues. Epidemiol Rev 1993; 15: 444-465.
2. Klein JO The burden of otitis media. Vaccine 2000; 1: S2-S8.
3. Seibert JW, Danner CJ Eustachian tube function and the middle ear. Otolaryngol Clin North Am 2006; 39: 1221-1235.
4. Luong A., Roland PS The link between allergic rhinitis and chronic otitis media with effusion in atopic patients. Otolaryngol Clin North Am 2008; 41: 311-323.
5. Mandel EM, Doyle WJ, Winther B., Alper CM The incidence, prevalence and burden of otitis media in unselected children aged 1-8 years followed by weekly otoscopy through the 'common cold' season. Int J Pediatr Otorhinolaryngol 2008; 72: 491-499.
6. Leibovitz E. Acute otitis media in children aged less than 2 years: Drug treatment issues. Paediatr Drugs 2006; 8: 337-346.
7. Leibovitz E. The challenge of recalcitrant acute otitis media: pathogens, resistance, and treatment strategy. Pediatr Infect Dis J 2007; 26: S8-S11.
8. Leibovitz E., Jacobs MR, Dagan R. Haemophilus influenzae: A significant pathogen in acute otitis media. Pediatr Infect Dis J 2004; 23: 1142-1152.
9. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu Rev Immunol 2003; 21: 335-376.
10. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001; 1: 135-145.
11. Krishnan J., Selvarajoo K., Tsuchiya M., Lee G., Choi S. Toll-like receptor signal transduction. Exp Mol Med 2007; 39: 421-438.
12. Shuto T., Xu H., Wang B. et al. Activation of NF-kappa B by nontypeable Hemophilus influenzae is mediated by Toll-like receptor 2-TAK1-dependent NIK-IKK alpha/beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA 2001; 98: 8774-8779.
13. Trinchieri G., Sher A. Cooperation of Toll-like receptor signals in innate immune defense. Nat Rev Immunol 2007; 7: 179-190.
14. Leake ER, Holmes K., Lim DJ, DeMaria TF Peptidoglycan isolated from nontypeable Haemophilus influenzae induces experimental otitis media in the chinchilla. J Infect Dis 1994; 170: 1532-1538.
15. DeMaria TF, Apicella MA, Nichols WA, Leake ER Evaluation of the virulence of nontypeable Haemophilus influenzae lipooligosaccharide htrB and rfaD mutants in the Chinchilla model of otitis media. Infect Immun 1997; 65: 4431-4435.
16. Shuto T., Imasato A., Jono H. et al. Glucocorticoids synergistically enhance nontypeable Haemophilus influenzae-induced Toll-like receptor 2 expression via a negative cross-talk with p38 MAP kinase. J Biol Chem 2002; 277: 17263-17270.
17. Watanabe T., Jono H., Han J., Lim DJ, Li JD Synergistic activation of NF-kappaB by nontypeable Haemophilus influenzae and tumor necrosis factor alpha. Proc Natl Acad Sci USA 2004; 101: 3563-3568.
18. Chen R., Lim JH, Jono H. et al. Nontypeable Haemophilus influenzae lipoprotein P6 induces MUC5AC mucin transcription via TLR2-TAK1-dependent p38 MAPK-AP1 and IKKbetaIkappaBalpha-NF-kappaB signaling pathways. Biochem Biophys Res Commun 2004; 324: 1087-1094.
19. Emonts M., Veenhoven RH, Wiertsema SP et al. Genetic polymorphisms in immunoresponse genes TNFA, IL6, IL10, and TLR4 are associated with recurrent acute otitis media. Pediatrics 2007; 120: 814-823.
20. Patel JA, Nair S., Revai K. et al. Association of proinflammatory cytokine gene polymorphisms with susceptibility to otitis media. Pediatrics 2006; 118: 2273-2279.
21. Hirano T., Kodama S., Fujita K., Maeda K., Suzuki M. Role of Toll-like receptor 4 in innate immune responses in a mouse model of acute otitis media. FEMS Immunol Med Microbiol 2007; 49: 75-83.
22. Wieland CW, Florquin S., Maris NA et al. The MyD88-dependent, but not the MyD88-independent, pathway of TLR4 signalling is important in clearing nontypeable Haemophilus influenzae from the mouse lung. J Immunol 2005; 175: 6042-6049.
23. Leendertse M., Willems RJ, Giebelen IA et al. TLR2-dependent MyD88 signalling contributes to early host defense in murine Enterococcus faecium peritonitis. J Immunol 2008; 180: 4865-4874.
24. Ebmeyer J., Furukawa M., Pak K. et al. Role of mast cells in otitis media. J Allergy Clin Immunol 2005; 116: 1129-1135.
25. Hoshino K., Takeuchi O., Kawai T. et al. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J Immunol 1999; 162: 3749-3752.
26. Takeuchi O., Hoshino K., Kawai T. et al. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 1999; 11: 443-451.
27. Melhus A., Ryan AF A mouse model for acute otitis media. Apmis 2003; 111: 989-994.
28. Hsiao A., Ideker T., Olefsky JM, Subramaniam S. VAMPIRE microarray suite: A web-based platform for the interpretation of gene expression data. Nucleic Acids Res 2005; 33: W627-W632.
29. Hernandez M., Leichtle A., Pak K. et al. Myeloid differentiation primary response gene 88 is required for the resolution of otitis media. J Infect Dis 2008; 198: 1862-1869.
30. Schauber J., Dorschner RA, Coda AB et al. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007; 117: 803-811.
31. Melhus A., Ryan AF Expression of cytokine genes during pneumococcal and nontypeable Haemophilus influenzae acute otitis media in the rat. Infect Immun 2000; 68: 4024-4031.
32. Furukawa M., Ebmeyer J., Pak K. et al. Jun N-terminal protein kinase enhances middle ear mucosal proliferation during bacterial otitis media. Infect Immun 2007; 75: 2562-2571.
33. Mollen KP, Anand RJ, Tsung A., Prince JM, Levy RM, Billiar TR Emerging paradigm: Toll-like receptor 4-sentinel for the detection of tissue damage. Shock 2006; 26: 430-437.
34. Hellstrom S., Laurent C., Yoon YJ Distribution of hyaluronan in the middle and inner ear. A light microscopical study in the rat using a hyaluronan-binding protein as a specific probe. ORL J Otorhinolaryngol Relat Spec 1994; 56: 253-256.
35. Stenfors LE Non-specific and specific immunity to bacterial invasion of the middle ear cavity. Int J Pediatr Otorhinolaryngol 1999; 49(Suppl 1): S223-S226.
36. Harada T., Juhn SK, Kim Y., Sakakura Y. Immunohistochemical distribution of extracellular matrix components and keratin in experimentally induced otitis media. Ann Otol Rhinol Laryngol 1999; 108: 769-776.
37. McGuire JF Surfactant in the middle ear and Eustachian tube: A review. Int J Pediatr Otorhinolaryngol 2002; 66: 1-15.
38. Tonnaer EL, Hafmans TG, Van Kuppevelt TH, Sanders EA, Verweij PE, Curfs JH Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect 2006; 8: 316-322.
39. Lee HY, Andalibi A., Webster P. et al. Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect Dis 2004; 4: 12.
40. MacArthur CJ, Hefeneider SH, Kempton JB, Trune DR C3H/HeJ mouse model for spontaneous chronic otitis media. Laryngoscope 2006; 116: 1071-1079.
41. Weiss DS, Raupach B., Takeda K., Akira S., Zychlinsky A. Toll-like receptors are temporally involved in host defense. J Immunol 2004; 172: 4463-4469.
42. Lorenz E., Chemotti DC, Jiang AL, McDougal LD Differential involvement of Toll-like receptors 2 and 4 in the host response to acute respiratory infections with wild-type and mutant Haemophilus influenzae strains. Infect Immun 2005; 73: 2075-2082.
43. Hoebe K., Du X., Georgel P. et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003; 424: 743-748.
44. Lemaitre B., Nicolas E., Michaut L., Reichhart JM, Hoffmann JA The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996; 86: 973-983.
45. Fritz JH, Girardin SE How Toll-like receptors and Nod-like receptors contribute to innate immunity in mammals. J Endotoxin Res 2005; 11: 390-394.
46. Fan J., Frey RS, Malik AB TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J Clin Invest 2003; 112: 1234-1243.
47. O'Grady NP, Preas HL, Pugin J. et al. Local inflammatory responses following bronchial endotoxin instillation in humans. Am J Respir Crit Care Med 2001; 163: 1591-1598.
48. Manderscheid PA, Bodkin RP, Davidson BA, Jensen E., Russo TA, Knight PR Bacterial clearance and cytokine profiles in a murine model of postsurgical nosocomial pneumonia. Clin Diagn Lab Immunol 2004; 11: 742-751.
49. Fujita M., Ikegame S., Harada E. et al. TNF receptor 1 and 2 contribute in different ways to resistance to Legionella pneumophila-induced mortality in mice. Cytokine 2008; 44: 298-303.
50. Couper KN, Blount DG, Riley EM IL-10: The master regulator of immunity to infection. J Immunol 2008; 180: 5771-5777.
51. Sun L., Guo RF, Newstead MW, Standiford TJ, Macariola DR, Shanley TP Effect of IL-10 on neutrophil recruitment and survival after Pseudomonas aeruginosa challenge. Am J Respir Cell Mol Biol 2008. doi:10.1165/ rcmb.2008-0202OC [Epub ahead of print].
52. Ogawa Y., Duru EA, Ameredes BT Role of IL-10 in the resolution of airway inflammation. Curr Mol Med 2008; 8: 437-445.
53. Obonyo M., Sabet M., Cole SP et al. Deficiencies of myeloid differentiation factor 88, Toll-like receptor 2 (TLR2), or TLR4 produce specific defects in macrophage cytokine secretion induced by Helicobacter pylori. Infect Immun 2007; 75: 2408-2414.
54. Goodwin JH, Post JC The genetics of otitis media. Curr Allergy Asthma Rep 2002; 2: 304-308.
55. Casselbrant ML, Mandel EM Genetic susceptibility to otitis media. Curr Opin Allergy Clin Immunol 2005; 5: 1-4.
56. Wiertsema SP, Khoo SK, Baynam G. et al. Association of CD14 promoter polymorphism with otitis media and pneumococcal vaccine responses. Clin Vaccine Immunol 2006; 13: 892-897.