Lysozyme M deficiency leads to an increased susceptibility to Streptococcus pneumoniae-induced otitis media

BMC Infectious Diseases

Volumn 8, Issue , 2008, Pages

  Shimada, Jun ^a,b   Moon, Sung K ^a   Lee, Haa Yung ^a   Takeshita, Tamotsu ^c   Pan, Huiqi ^a   Woo, Jeong Im ^a   Gellibolian, Robert ^a   Yamanaka, Noboru ^b   Lim, David J ^a,d  

^a HOUSE EAR INSTITUTE   (United States)

^b WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^c HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOZYME; LYSOZYME M; UNCLASSIFIED DRUG; LYSOZYME M, MOUSE; LYSOZYME P, MOUSE; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; AUDITORY TUBE; BACTERIAL COUNT; BACTERICIDAL ACTIVITY; CELL TYPE; CONTROLLED STUDY; DIFFUSION; DISEASE PREDISPOSITION; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME LOCALIZATION; ENZYME METABOLISM; ENZYME SPECIFICITY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OTITIS MEDIA; PROTEIN DEPLETION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; C57BL MOUSE; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY;

ANIMALS; DISEASE SUSCEPTIBILITY; EUSTACHIAN TUBE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MURAMIDASE; OTITIS MEDIA; PNEUMOCOCCAL INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; STREPTOCOCCUS PNEUMONIAE;

EID: 55349096465     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-8-134     Document Type: Article

References (45)

1. Bluestone CD Studies in otitis media: Children's Hospital of Pittsburgh-University of Pittsburgh progress report-2004 The Laryngoscope 2004, 114(11 Pt 3 Suppl 105):1-26. 10.1097/ 01.mlg.0000148223.45374.ec 15514559
2. Stool SE Field MJ The impact of otitis media The Pediatric infectious disease journal 1989, 8(1 Suppl):S11-14. 2494641
3. Gates GA Cost-effectiveness considerations in otitis media treatment Otolaryngol Head Neck Surg 1996, 114(4):525-530. 10.1016/ S0194-5998(96)70243-7 8643261
4. Dagan R Treatment of acute otitis media - challenges in the era of antibiotic resistance Vaccine 2000, 19(Suppl 1):S9-S16. 10.1016/ S0264-410X(00)00272-3 11163457
5. Bluestone CD Current concepts in eustachian tube function as related to otitis media Auris, nasus, larynx 1985, 12(Suppl 1):S1-4. 3915201
6. Seibert JW Danner CJ Eustachian tube function and the middle ear Otolaryngologic clinics of North America 2006, 39(6):1221-1235. 10.1016/ j.otc.2006.08.011 17097443
7. Tonnaer EL Rijkers GT Meis JF Klaassen CH Bogaert D Hermans PW Curfs JH Genetic relatedness between pneumococcal populations originating from the nasopharynx, adenoid, and tympanic cavity of children with otitis media J Clin Microbiol 2005, 43(7):3140-3144. 1169158 16000426 10.1128/ JCM.43.7.3140-3144.2005
8. Tonnaer EL Sanders EA Curfs JH Bacterial otitis media: A new non-invasive rat model Vaccine 2003, 21(31):4539-4544. 10.1016/ S0264-410X(03)00501-2 14575765
9. Lim DJ Chun YM Lee HY Moon SK Chang KH Li JD Andalibi A Cell biology of tubotympanum in relation to pathogenesis of otitis media - a review Vaccine 2000, 19(Suppl 1):S17-25. 10.1016/S0264-410X(00)00273-5 11163458
10. Ganz T Antimicrobial polypeptides Journal of leukocyte biology 2004, 75(1):34-38. 10.1189/jlb.0403150 12960278
11. Konstan MW Cheng PW Boat TF A comparative study of lysozyme and its secretion by tracheal epithelium Experimental lung research 1982, 3(2):175-181. 10.3109/01902148209063291 7106064
12. Prager EM Jolles P Animal lysozymes c and g: An overview Exs 1996, 75:9-31. 8765292
13. Hanamure Y Lim DJ Normal distribution of lysozyme- and lactoferrin-secreting cells in the chinchilla tubotympanum Am J Otolaryngol 1986, 7(6):410-425. 10.1016/S0196-0709(86)80017-5 3541659
14. Hammer MF Schilling JW Prager EM Wilson AC Recruitment of lysozyme as a major enzyme in the mouse gut: Duplication, divergence, and regulatory evolution J Mol Evol 1987, 24(3):272-279. 10.1007/BF02111240 3106642
15. Cross M Mangelsdorf I Wedel A Renkawitz R Mouse lysozyme M gene: isolation, characterization, and expression studies Proc Natl Acad Sci USA 1988, 85(17):6232-6236. 281943 3413093 10.1073/pnas.85.17.6232
16. Ganz T Gabayan V Liao HI Liu L Oren A Graf T Cole AM Increased inflammation in lysozyme M-deficient mice in response to Micrococcus luteus and its peptidoglycan Blood 2003, 101(6):2388-2392. 10.1182/ blood-2002-07-2319 12411294
17. Cole AM Thapa DR Gabayan V Liao HI Liu L Ganz T Decreased clearance of Pseudomonas aeruginosa from airways of mice deficient in lysozyme M Journal of leukocyte biology 2005, 78(5):1081-1085. 10.1189/jlb.0205073 16204648
18. Faust N Varas F Kelly LM Heck S Graf T Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages Blood 2000, 96(2):719-726. 10887140
19. Melhus A Ryan AF A mouse model for acute otitis media Apmis 2003, 111(10):989-994. 10.1034/j.1600-0463.2003.1111012.x 14616553
20. Brooks-Walter A Briles DE Hollingshead SK The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein, PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia Infect Immun 1999, 67(12):6533-6542. 97064 10569772
21. Moon SK Lee HY Pan H Takeshita T Park R Cha K Andalibi A Lim DJ Synergistic effect of interleukin 1 alpha on nontypeable Haemophilus influenzae-induced up-regulation of human beta-defensin 2 in middle ear epithelial cells BMC infectious diseases 2006, 6:12. 1368979 16433908 10.1186/1471-2334-6-12
22. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods (San Diego, Calif) 2001, 25(4):402-408. 11846609
23. Osserman EF Lawlor DP Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia J Exp Med 1966, 124(5):921-952. 2138258 5224561 10.1084/jem.124.5.921
24. Lehrer RI Rosenman M Harwig SS Jackson R Eisenhauer P Ultrasensitive assays for endogenous antimicrobial polypeptides J Immunol Methods 1991, 137(2):167-173. 10.1016/0022-1759(91)90021-7 1901580
25. Smith JJ Travis SM Greenberg EP Welsh MJ Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid Cell 1996, 85(2):229-236. 10.1016/S0092-8674(00)81099-5 8612275
26. Agrawal S Husein M MacRae D Complications of otitis media: An evolving state The Journal of otolaryngology 2005, 34(Suppl 1):S33-39. 16089238
27. Block SL Harrison CJ Hedrick JA Tyler RD Smith RA Keegan E Chartrand SA Penicillin-resistant Streptococcus pneumoniae in acute otitis media: risk factors, susceptibility patterns and antimicrobial management The Pediatric infectious disease journal 1995, 14(9):751-759. 10.1097/ 00006454-199509000-00005 8559623
28. Ganz T Defensins: Antimicrobial peptides of innate immunity Nature reviews 2003, 3(9):710-720. 10.1038/nri1180 12949495
29. Guina T Yi EC Wang H Hackett M Miller SI A PhoP-regulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides Journal of bacteriology 2000, 182(14):4077-4086. 94595 10869088 10.1128/JB.182.14.4077-4086.2000
30. Guo L Lim KB Poduje CM Daniel M Gunn JS Hackett M Miller SI Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides Cell 1998, 95(2):189-198. 10.1016/S0092-8674(00)81750-X 9790526
31. Peschel A Otto M Jack RW Kalbacher H Jung G Gotz F Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides The Journal of biological chemistry 1999, 274(13):8405-8410. 10.1074/jbc.274.13.8405 10085071
32. Liu YS Lim DJ Lang RW Birck HG Chronic middle ear effusions. Immunochemical and bacteriological investigations Arch Otolaryngol 1975, 101(5):278-286. 805583
33. Park K Lim DJ Development of secretory elements in murine tubotympanum: lysozyme and lactoferrin immunohistochemistry The Annals of otology, rhinology, and laryngology 1993, 102(5):385-395. 8489170
34. Lim DJ Liu YS Birck H Secretory lysozyme of the human middle ear mucosa: immunocytochemical localization The Annals of otology, rhinology, and laryngology 1976, 85(1 Pt 1):50-60. 944008
35. Chung MH Choi JY Lee WS Kim HN Yoon JH Compositional difference in middle ear effusion: Mucous versus serous The Laryngoscope 2002, 112(1):152-155. 10.1097/00005537-200201000-00027 11802055
36. Ibrahim HR Aoki T Pellegrini A Strategies for new antimicrobial proteins and peptides: Lysozyme and aprotinin as model molecules Current pharmaceutical design 2002, 8(9):671-693. 10.2174/1381612023395349 11945164
37. Masschalck B van Houdt R van Haver EG Michiels CW Inactivation of gram-negative bacteria by lysozyme, denatured lysozyme, and lysozyme-derived peptides under high hydrostatic pressure Applied and environmental microbiology 2001, 67(1):339-344. 10.1128/ AEM.67.1.339-344.2001
38. Nash JA Ballard TN Weaver TE Akinbi HT The peptidoglycan-degrading property of lysozyme is not required for bactericidal activity in vivo J Immunol 2006, 177(1):519-526. 16785549
39. Majcherczyk PA Langen H Heumann D Fountoulakis M Glauser MP Moreillon P Digestion of Streptococcus pneumoniae cell walls with its major peptidoglycan hydrolase releases branched stem peptides carrying proinflammatory activity The Journal of biological chemistry 1999, 274(18):12537-12543. 10.1074/jbc.274.18.12537 10212231
40. Ibrahim HR Thomas U Pellegrini A A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action The Journal of biological chemistry 2001, 276(47):43767-43774. 10.1074/jbc.M106317200 11560930
41. Akinbi HT Epaud R Bhatt H Weaver TE Bacterial killing is enhanced by expression of lysozyme in the lungs of transgenic mice J Immunol 2000, 165(10):5760-5766. 11067934
42. Markart P Faust N Graf T Na CL Weaver TE Akinbi HT Comparison of the microbicidal and muramidase activities of mouse lysozyme M and P Biochem J 2004, 380(Pt 2):385-392. 1224176 14977423 10.1042/BJ20031810
43. Lee HY Andalibi A Webster P Moon SK Teufert K Kang SH Li JD Nagura M Ganz T Lim DJ Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae BMC infectious diseases 2004, 4:12. 428576 15125783 10.1186/1471-2334-4-12
44. Ellison RT 3rd Giehl TJ Killing of gram-negative bacteria by lactoferrin and lysozyme J Clin Invest 1991, 88(4):1080-1091. 295557 1918365 10.1172/ JCI115407
45. Short ML Nickel J Schmitz A Renkawitz R Lysozyme gene expression and regulation Exs 1996, 75:243-257. 8765303