Toll-like receptor 4 limits transmission of Bordetella bronchiseptica

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Rolin, Olivier ^a   Smallridge, Will ^a   Henry, Michael ^a   Goodfield, Laura ^a   Place, David ^a   Harvill, Eric T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 4; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SHEDDING; BACTERIAL TRANSMISSION; BORDETELLA BRONCHISEPTICA; BORDETELLA BRONCHISEPTICA INFECTION; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE PREDISPOSITION; IMMUNE RESPONSE; INFECTION CONTROL; INNATE IMMUNITY; LOWER RESPIRATORY TRACT; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; WILD TYPE; ANIMAL; BORDETELLOSIS; C3H MOUSE; C57BL MOUSE; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; NOSE CAVITY; PHYSIOLOGY; RESPIRATORY TRACT INFECTION; TRANSMISSION;

ANIMALS; BACTERIAL SHEDDING; BORDETELLA BRONCHISEPTICA; BORDETELLA INFECTIONS; IMMUNITY, INNATE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; NASAL CAVITY; NEUTROPHIL INFILTRATION; RESPIRATORY TRACT INFECTIONS; TOLL-LIKE RECEPTOR 4;

EID: 84900425028     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085229     Document Type: Article

References (55)

1. Bloemendaal ALA, Vriens MR, Jansen WTM, Borel Rinkes IHM, Verhoef J, et al. (2011) Colonization and transmission of meticillin-susceptible and meticillin-resistant Staphylococcus aureus in a murine nasal colonization model. J Med Microbiol 60: 812-816. doi:10.1099/jmm.0.027532-0.
2. An CL, Gigliotti F, Harmsen AG (2003) Exposure of Immunocompetent Adult Mice to Pneumocystis carinii f. sp. muris by Cohousing: Growth of P. carinii f. sp. muris and Host Immune Response. Infection and Immunity 71: 2065-2070. doi:10.1128/IAI.71.4.2065-2070.2003. (Pubitemid 36368741)
3. Lowen AC, Mubareka S, Tumpey TM, García-Sastre A, Palese P (2006) The guinea pig as a transmission model for human influenza viruses. Proceedings of the National Academy of Sciences 103: 9988-9992. doi:10.1073/pnas.0604157103. (Pubitemid 43993610)
4. Wickham ME, Brown NF, Boyle EC, Coombes BK, Finlay BB (2007) Virulence is positively selected by transmission success between mammalian hosts. Curr Biol 17: 783-788. doi:10.1016/j.cub.2007.03.067. (Pubitemid 46635120)
5. Brockmeier SL, Lager KM (2002) Experimental airborne transmission of porcine reproductive and respiratory syndrome virus and Bordetella bronchiseptica. Vet Microbiol 89: 267-275. (Pubitemid 35284129)
6. Nicholson TL, Brockmeier SL, Loving CL, Register KB, Kehrli ME Jr, et al. (2012) Phenotypic modulation of the virulent Bvg phase is not required for pathogenesis and transmission of Bordetella bronchiseptica in swine. Infect Immun 80: 1025-1036. doi:10.1128/IAI.06016-11.
7. Hellriegel B (2001) Immunoepidemiology-bridging the gap between immunology and epidemiology. Trends Parasitol 17: 102-106.
8. Mizgerd JP, Skerrett SJ (2008) Animal models of human pneumonia. American Journal of Physiology - Lung Cellular and Molecular Physiology 294: L387-L398. doi:10.1152/ajplung.00330.2007. (Pubitemid 351468836)
9. Thakar J, Saadatpour-Moghaddam A, Harvill ET, Albert R (2009) Constraint-based network model of pathogen-immune system interactions. J R Soc Interface 6: 599-612. doi:10.1098/rsif.2008.0363.
10. Thakar J, Pilione M, Kirimanjeswara G, Harvill ET, Albert R (2007) Modeling systems-level regulation of host immune responses. PLoS Comput Biol 3: e109. doi:10.1371/journal.pcbi.0030109.
11. Mann PB, Kennett MJ, Harvill ET (2004) Toll-Like Receptor 4 Is Critical to Innate Host Defense in a Murine Model of Bordetellosis. Journal of Infectious Diseases 189: 833-836. doi:10.1086/381898. (Pubitemid 38328184)
12. Mann PB, Elder KD, Kennett MJ, Harvill ET (2004) Toll-Like Receptor 4-Dependent Early Elicited Tumor Necrosis Factor Alpha Expression Is Critical for Innate Host Defense against Bordetella bronchiseptica. Infection and Immunity 72: 6650-6658. doi:10.1128/IAI.72.11.6650-6658.2004. (Pubitemid 39425448)
13. Zhang X, Hester SE, Kennett MJ, Karanikas AT, Bendor L, et al. (2011) Interleukin-1 receptor signaling is required to overcome the effects of pertussis toxin and for efficient infection- or vaccination-induced immunity against Bordetella pertussis. Infect Immun 79: 527-541. doi:10.1128/IAI.00590- 10.
14. Kirimanjeswara GS, Mann PB, Harvill ET (2003) Role of Antibodies in Immunity to Bordetella Infections. Infection and Immunity 71: 1719-1724. doi:10.1128/IAI.71.4.1719-1724.2003. (Pubitemid 36368699)
15. Harvill ET, Cotter PA, Miller JF (1999) Pregenomic Comparative Analysis between Bordetella bronchiseptica RB50 and Bordetella pertussis Tohama I in Murine Models of Respiratory Tract Infection. Infection and Immunity 67: 6109.
16. Pilione MR, Harvill ET (2006) The Bordetella bronchiseptica Type III Secretion System Inhibits Gamma Interferon Production That Is Required for Efficient Antibody-Mediated Bacterial Clearance. Infection and Immunity 74: 1043-1049. doi:10.1128/IAI.74.2.1043-1049.2006. (Pubitemid 43185541)
17. Bemis DA, Shek WR, Clifford CB (2003) Bordetella bronchiseptica infection of rats and mice. Comp Med 53: 11-20. (Pubitemid 36323509)
18. Pathak AK, Creppage KE, Werner JR, Cattadori IM (2010) Immune regulation of a chronic bacteria infection and consequences for pathogen transmission. BMC Microbiology 10: 226. doi:10.1186/1471-2180-10-226.
19. Smirnova I, Mann N, Dols A, Derkx HH, Hibberd ML, et al. (2003) Assay of locus-specific genetic load implicates rare Toll-like receptor 4 mutations in meningococcal susceptibility. Proceedings of the National Academy of Sciences 100: 6075-6080. doi:10.1073/pnas.1031605100. (Pubitemid 36576933)
20. Rebeil R, Ernst RK, Gowen BB, Miller SI, Hinnebusch BJ (2004) Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 52: 1363-1373. doi:10.1111/j.1365-2958.2004.04059.x. (Pubitemid 38746310)
21. Miller SI, Ernst RK, Bader MW (2005) LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol 3: 36-46. doi:10.1038/nrmicro1068. (Pubitemid 40028467)
22. Mann PB, Wolfe D, Latz E, Golenbock D, Preston A, et al. (2005) Comparative Toll-Like Receptor 4-Mediated Innate Host Defense to Bordetella Infection. Infection and Immunity 73: 8144-8152. doi:10.1128/IAI.73.12.8144- 8152.2005. (Pubitemid 41740302)
23. Wolfe DN, Buboltz AM, Harvill ET (2009) Inefficient Toll-like receptor-4 stimulation enables Bordetella parapertussis to avoid host immunity. PLoS ONE 4: e4280. doi:10.1371/journal.pone.0004280.
24. Bjørnstad ON, Harvill ET (2005) Evolution and emergence of Bordetella in humans. Trends Microbiol 13: 355-359. doi:10.1016/j.tim.2005.06. 007. (Pubitemid 41073805)
25. Huang X, Du W, McClellan SA, Barrett RP, Hazlett LD (2006) TLR4 Is Required for Host Resistance in Pseudomonas aeruginosa Keratitis. Investigative Ophthalmology & Visual Science 47: 4910-4916. doi:10.1167/iovs.06-0537. (Pubitemid 46586392)
26. Packiam M, Wu H, Veit SJ, Mavrogiorgos N, Jerse AE, et al. (2012) Protective role of Toll-like receptor 4 in experimental gonococcal infection of female mice. Mucosal Immunol 5: 19-29.
27. Juneau RA, Pang B, Weimer KED, Armbruster CE, Swords WE (2011) Nontypeable Haemophilus influenzae Initiates Formation of Neutrophil Extracellular Traps. Infection and Immunity 79: 431-438. doi:10.1128/IAI.00660- 10.
28. Zola TA, Lysenko ES, Weiser JN (2008) Mucosal Clearance of Capsule-Expressing Bacteria Requires Both TLR and Nucleotide-Binding Oligomerization Domain 1 Signaling. J Immunol 181: 7909-7916.
29. Higgins SC, Lavelle EC, McCann C, Keogh B, McNeela E, et al. (2003) Toll-Like Receptor 4-Mediated Innate IL-10 Activates Antigen-Specific Regulatory T Cells and Confers Resistance to Bordetella pertussis by Inhibiting Inflammatory Pathology. The Journal of Immunology 171: 3119-3127. (Pubitemid 37093535)
30. Gopinath S, Hotson A, Johns J, Nolan G, Monack D (2013) The Systemic Immune State of Super-shedder Mice Is Characterized by a Unique Neutrophil-dependent Blunting of TH1 Responses. PLoS Pathog 9: e1003408. doi:10.1371/journal.ppat.1003408.
31. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783-801. doi:10.1016/j.cell.2006.02.015. (Pubitemid 43261452)
32. Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182. doi:10.1038/nri1785.
33. Sallusto F, Lanzavecchia A, Mackay CR (1998) Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunology Today 19: 568-574. doi:10.1016/S0167-5699(98)01346-2. (Pubitemid 28557120)
34. Khelef N, Bachelet CM, Vargaftig BB, Guiso N (1994) Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infection and Immunity 62: 2893.
35. Harvill ET, Cotter PA, Yuk MH, Miller JF (1999) Probing the Function of Bordetella bronchiseptica Adenylate Cyclase Toxin by Manipulating Host Immunity. Infection and Immunity 67: 1493.
36. Yuk MH, Harvill ET, Cotter PA, Miller JF (2000) Modulation of host immune responses, induction of apoptosis and inhibition of NF-kappaB activation by the Bordetella type III secretion system. Mol Microbiol 35: 991-1004. (Pubitemid 30137770)
37. Young HWJ, Molina JG, Dimina D, Zhong H, Jacobson M, et al. (2004) A3 Adenosine Receptor Signaling Contributes to Airway Inflammation and Mucus Production in Adenosine Deaminase-Deficient Mice. The Journal of Immunology 173: 1380-1389. (Pubitemid 38924319)
38. Gorska M (2004) Reduced airway inflammation, mucus production and airway remodeling in map kinase-activated protein kinase (MK2) knockout mice*1. Journal of Allergy and Clinical Immunology 113: S182-S183. doi:10.1016/j.jaci. 2004.01.094.
39. Antunes MB, Gudis DA, Cohen NA (2009) Epithelium, Cilia, and Mucus: Their Importance in Chronic Rhinosinusitis. Immunology and Allergy Clinics of North America 29: 631-643. doi:10.1016/j.iac.2009.07.004.
40. Harkema JR, Hotchkiss JA, Harmsen AG, Henderson RF (1988) In vivo effects of transient neutrophil influx on nasal respiratory epithelial mucosubstances. Quantitative histochemistry. The American Journal of Pathology 130: 605.
41. Harkema JR, Hotchkiss JA (1991) In vivo effects of endotoxin on nasal epithelial mucosubstances: quantitative histochemistry. Exp Lung Res 17: 743-761.
42. Wagner JG, Van Dyken SJ, Hotchkiss JA, Harkema JR (2001) Endotoxin enhancement of ozone-induced mucous cell metaplasia is neutrophil-dependent in rat nasal epithelium. Toxicol Sci 60: 338-347. (Pubitemid 32273323)
43. Strutt TM, McKinstry KK, Dibble JP, Winchell C, Kuang Y, et al. (2010) Memory CD4+ T cells induce innate responses independently of pathogen. Nature Medicine 16: 558-564. doi:10.1038/nm.2142.
44. Strutt TM, McKinstry KK, Swain SL (2011) Control of innate immunity by memory CD4 T cells. Adv Exp Med Biol 780: 57-68. doi:10.1007/978-1-4419-5632-3- 6.
45. Neutra MR, Kozlowski PA (2006) Mucosal vaccines: the promise and the challenge. Nature Reviews Immunology 6: 148-158. doi:10.1038/nri1777. (Pubitemid 43361590)
46. Jackson LA, Cherry JD, Wang S-P, Grayston JT (2000) Frequency of Serological Evidence of Bordetella Infections and Mixed Infections with other Respiratory Pathogens in University Students with Cough Illnesses. Clinical Infectious Diseases 31: 3-6. doi:10.1086/313911. (Pubitemid 32268929)
47. Mink CM, Cherry JD, Christenson P, Lewis K, Pineda E, et al. (1992) A Search for Bordetella pertussis Infection in University Students. Clinical Infectious Diseases 14: 464-471. doi:10.1093/clinids/14.2.464.
48. Andrews R, Herceg A, Roberts C (1997) Pertussis notifications in Australia, 1991 to 1997. Commun Dis Intell 21: 145-148.
49. Polyzou A, Pournaras S, Dafni U, Sofianou D, Christeli E, et al. (2004) Sero epidemiology of Bordetella pertussis immune responses in a healthy population in northern Greece. J Clin Lab Anal 18: 211-214. doi:10.1002/jcla. 20025. (Pubitemid 38585801)
50. Gzyl A, Augustynowicz E, Rabczenko D, Gniadek G, Slusarczyk J (2004) Pertussis in Poland. International Journal of Epidemiology 33: 358-365. doi:10.1093/ije/dyh012. (Pubitemid 38578836)
51. Hozbor D, Mooi F, Flores D, Weltman G, Bottero D, et al. (2009) Pertussis epidemiology in Argentina: trends over 2004-2007. J Infect 59: 225-231. doi:10.1016/j.jinf.2009.07.014.
52. Lavine JS, King AA, Bjørnstad ON (2011) Natural immune boosting in pertussis dynamics and the potential for long-term vaccine failure. Proc Natl Acad Sci USA 108: 7259-7264. doi:10.1073/pnas.1014394108.
53. Cotter PA, Miller JF (1994) BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62: 3381-3390. (Pubitemid 24232124)
54. Stainer DW, Scholte MJ (1970) A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol 63: 211-220.
55. Czuprynski CJ, Brown JF, Wagner RD, Steinberg H (1994) Administration of antigranulocyte monoclonal antibody RB6-8C5 prevents expression of acquired resistance to Listeria monocytogenes infection in previously immunized mice. Infect Immun 62: 5161-5163. (Pubitemid 24332829)