Pseudomonas aeruginosa; Virulence Factors and Host Defense Mechanisms
Yıl 2023,
Cilt: 15 Sayı: 1, 48 - 62, 30.06.2023
Fatma Meral İnce
,
Nida Özcan
,
Nezahat Akpolat
Öz
As an opportunistic pathogen, Pseudomonas aeruginosa (P. aeruginosa) can cause both acute and chronic infections. Variable virulence components and antibiotic resistance markers in the bacterium's genome constitute the bacterium's pathogenic profile and provide the bacterium with outstanding metabolic adaptability to many conditions. The interactions of P. aeruginosa with the host are poorly understood, complicating the treatment of its infections and the development of vaccines against them. Despite decades of scientific research focusing specifically on this challenge, vaccines to prevent these dangerous infections still do not exist. The major virulence factors of P. aeruginosa and host immune responses against the bacteria are discussed in this review.
Kaynakça
- 1. Özünel L, Boyacıoğlu Zİ, Güreser AS, Taylan-Özkan A. Evaluation of antimicrobial susceptibility patterns of Pseudomonasaeruginosa and Acinetobacterbaumannii strains isolated from deep trecheal aspirate samples in Çorum Training and Research Hospital. Turk Hij Den Biyol Derg 2014; 71(2): 81-88.
- 2. Xiong J, Déraspe M, Iqbal N. Complete genome of a panresistant Pseudomonas aeruginosa strain, isolated from a patient with respiratory failure in a Canadian community hospital. Genome Announc 2017; 5: e00458-17.
- 3. Rasamiravaka T, Labtani Q, Duez P, JaziriME. T formation of biofilm, Compounds by P.aeruginosa: A review of the natural and synthetic, interfering with control mechanisms. Biomed Res Int 2015: 759348.
- 4. Davis R, Brown PD. Multiple antibiotic resistance index, fitness and virulence potential in respiratory P.aeruginosa from Jamaica. J Med Microbiol 2016; 65(4): 261-271.
- 5. Tacconelli E, Carrara E, Savoldi A. et al. Discovery, research and development of new antibiotics: The WHO priority list of antibiotic-resistant. Lancet Infect Dis 2017; 18(3): 318-327.
- 6. Botelho J, Grosso F, Peixe L. Antibiotic resistance in P.aeruginosa—Mechanisms, epidemiology and evolution. Drug Resist 2019; 44: 100640.
- 7. Sainz-Mejías M, Jurado-Martín I, McClean S. Understanding Pseudomonas aeruginosa-Host Interactions: The Ongoing Quest for an Efficacious Vaccine. Cells 2020; 9(12): 2617.
- 8. Karatuna O, Yağcı A. Virulence factors of Pseudomonas aeruginosa and quorum sensing. Türk Mikrobiyol Cem Derg 2008; 38(1): 42-51.
- 9. Alaa A. NOD-like receptor(s) and host immune responses with Pseudomonas aeruginosa infection. Inflamm Res 2018; 67: 479–493.
- 10. Skariyachan S, Sridhar VS, Packirisamy S, Kumargowda ST, Challapilli SB. Recent perspectives on the molecular basis of biofilm formation by Pseudomonas aeruginosa and approaches for treatment and biofilm dispersal. Folia Microbiol 2018; 63: 413-432.
- 11. Laverty G, Gorman S, Gilmore B. Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 2014; 3(3): 596-632.
- 12. Lambert PA. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J R SocMed 2002; 95: 22-26.
- 13. Pier GB, Ramphal R. Pseudomonas aeruginosa. In: Mandell GL, Bennett JE, Dolin, R, eds. Mandell, Douglas and Bennett’s Principles and Practice of Infectious Disease, 7th Edition, New York: Elsevier/Churchill Livingstone, 2009: 2587-2615.
- 14. Opal SM, Pop-Vicas A. Molecular Mechanisms of Antibiotic Resistance in Bacteria. In: Mandell G, Bennett J, Dolin R,eds. Mandell, Douglas and Bennett’s Principles and Practice of Infectious Disease 7th Edition, New York: Elsevier/Churchill Livingstone, 2009: 222-239.
- 15. Ulusoy S, Boşgelmez Tınaz G. Çeşitli klinik örneklerden izole edilen Pseudomonas aeruginosa suşlarında homoserin lakton üretimi ve antibiyotik duyarlılıklarının araştırılması. Cankaya Univ J Arts and Sciences 2008; 1(10): 145-151.
- 16. Harmsen M, YangL, Pamp SJ, Nielsen TT. Anupdate on P. aeruginosa biofilm formation, tolerance and dispersal. FEMS Immunol Med Microbiol 2010; 59(3): 253-68.
- 17. Roger SS, Rodney K, Barbara HI, Richard PP. The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J Immunol 2002; 169(5): 2636-2642.
- 18. Döring G, Vaccines and immunotherapy against Pseudomonas aeruginosa. Vaccine 2008; 26(8):1011-1024.
- 19. Köhler T, Curty LK, Barja F, Van Delden C, Pechere JC. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili.2000; 182(21): 5990–5996.
- 20. Barken KB, Pamp SJ, Yang L, et al. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 2008; 10(9): 2331-2343.
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- 22. Pena RT, Blasco L, Ambroa A, et al. Relationship Between Quorum Sensing and Secretion Systems. Front Microbiol 2019; 10: 1100.
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- 25. Passador L, Iglewski W. ADP-ribosylating toxins. Methods Enzymol 1994; 235: 617-31.
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- 28. Hentzer M, Teitzeli GM, Balzer GJ, Heydorn A, Molin S, Givskov M. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 2001; 183: 5395-5401.
- 29. Yang J, Toyokufu M, Sakai R, Nomur N. Influence of the alginate production on cell-to-cell communication in Pseudomonas aeruginosa PAO1. Environ Microbiol Rep 2017; 9(3): 239–249.
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- 33. Cornelis P. Putting an end to the Pseudomonas aeruginosa IQS controversy. Microbiol Open 2020; 9: e962.
- 34. Wang J, Wang C, Yu HB, et al. Bacterial quorum-sensing signal IQS induces host cell apoptosis by targeting POT1-p53 signaling pathway. Cell Microbiol 2019; 21: e13076.
- 35. Lee K, Yoon SS. Pseudomonas aeruginosa Biofilm, a Programmed Bacterial Life for Fitness. J Microbiol Biotechnol 2017; 27(6): 1053-1064.
- 36. Yan S, Wu G. Can Biofilm Be Reversed Through Quorum Sensing in Pseudomonas aeruginosa? Front Microbiol 2019; 10: 1582.
- 38. Ho BT, Dong TG, Mekalanos JJ. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 2014; 15(1): 9-21.
- 39. Miguel JC, Costa JC, Espeschit IF, Pieri FA, Benjamin LA, Moreira MAC. Increase in biofilm formation by Escherichia coli underconditions that mimic the mastitic mammary gland. Cienc Rural 2014; 44(4): 666-671.
- 40. Williamson KS, Richards LA, Perez-Osorio AC, et al. Heterogeneity in Pseudomonas aeruginosa biofilms include expression of ribosome hiber nation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 2012; 194(8): 2062-2073.
- 41. Pedrosa AP, Brandão MLL, Medeiros VM, et al. Research of virulence factors in Pseudomonas aeruginosa isolated from natural mineral waters. Rev Ambient Agua 2014; 9(2): 313-324.
- 42. Haüssler S, Becker T. The Pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLOS Pathogens 2008; 4(9): 1-8.
- 43. Gellatly SL, Hancock RE. P aeruginosa: new insights into, pathogenesis and host defenses. Pathog Dis 2013; 67: 159–173.
- 44. Oliver A, Mulet X, Causapé CL, Juan C. The increasing threat of Pseudomona saeruginosa high-risk clones. Drug Resist Updat 2015; 21(22): 41–59.
- 45. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol 2011; 35: 652–680.
- 46. McIsaac SM, Stadnyk AW, Lin TJ. Toll like receptors in the host defense against P. aeruginosa respiratory infection and cystic fibrosis. J Leukoc Biol 2012; 92: 977–985.
- 47. Lovewell RR, Patankar YR, Brent B. Mechanisms of phagocytosis and host clearance of P. aeruginosa. Am J Physiol Lung Cell Mol Physiol 2014; 306: L591–L603.
- 48. Lin CK, Barbara IK. Inflammation: A double-edgeds word in the response to Pseudomonas aeruginosa infection. J Innate Immun 2017; 9: 250–261.
- 49. Dosunmu EF, Emeh RO, Dixit S, et al. The anti-microbial peptide TP359 attenuates inflammation in human lung cells infected with Pseudomonas aeruginosa via TLR5 and MAPK pathways. PLoS ONE 2017; 12: e0176640.
- 50. Pang Z, Junkins RD, Raudonis R, et al. Regulator of calcineurin 1 differentially regulates TLR-dependent MyD88 and TRIF signaling pathways. PLoS ONE 2018; 13: e0197491.
- 51. Nakamura S, Iwanaga N, Seki M, et al. Toll-Like Receptor 4 Agonistic Antibody Promotes Host Defense against Chronic Pseudomonas aeruginosa Lung Infection in Mice. Infect Immun 2016; 84: 1986–1993.
- 52. Morris AE, Liggitt HD, Hawn TR, Shawn JS. Role of toll-like receptor 5 in the innate immune response to acute P. aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol 2009; 297: L1112–L1119.
- 53. Vijay-Kumar M, Carvalho FA, Aitken JD, Fifadara NH, Andrew TG. TLR5 or NLRC4 is necessary and sufficient for the promotion of humoral immunity by flagellin. Eur J Immunol 2010; 40: 3528–3534.
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- 55. Lee JH, Jeon J, Bai F, Jin S, Wu W, Ha UH. The Pseudomonas aeruginosa HSP70-like protein DnaK induces IL-1β expression via TLR4-dependent activation of the NF-κBand JNK signaling pathways. Comp Immunol Microbiol Infect Dis 2019; 67: 101373.
- 56. Tolle L, Yu FS, Kovach MA, et al. Standiford, T.J. Redundant and cooperative interactions between TLR5 and NLRC4 in protective lung mucosal immunity against Pseudomonas aeruginosa. J Innate Immun 2015; 7; 177–186.
- 57. Pène F, Grimaldi D, Zuber B, et al. Toll like receptor 2 deficiency increases resistance to P. aeruginosa pneumonia in the setting of sepsis-induced immune dysfunction. J Infect Dis 2012; 206: 932–942.
- 58. Benmohamed F, Medina M, Wu YZ, Maschalidi S, Jouvion G, Guillemot L. Toll-like receptor 9 deficiency protects mice against P. aeruginosa lung infection. PloS One 2014; 9: e90466.
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Yıl 2023,
Cilt: 15 Sayı: 1, 48 - 62, 30.06.2023
Fatma Meral İnce
,
Nida Özcan
,
Nezahat Akpolat
Kaynakça
- 1. Özünel L, Boyacıoğlu Zİ, Güreser AS, Taylan-Özkan A. Evaluation of antimicrobial susceptibility patterns of Pseudomonasaeruginosa and Acinetobacterbaumannii strains isolated from deep trecheal aspirate samples in Çorum Training and Research Hospital. Turk Hij Den Biyol Derg 2014; 71(2): 81-88.
- 2. Xiong J, Déraspe M, Iqbal N. Complete genome of a panresistant Pseudomonas aeruginosa strain, isolated from a patient with respiratory failure in a Canadian community hospital. Genome Announc 2017; 5: e00458-17.
- 3. Rasamiravaka T, Labtani Q, Duez P, JaziriME. T formation of biofilm, Compounds by P.aeruginosa: A review of the natural and synthetic, interfering with control mechanisms. Biomed Res Int 2015: 759348.
- 4. Davis R, Brown PD. Multiple antibiotic resistance index, fitness and virulence potential in respiratory P.aeruginosa from Jamaica. J Med Microbiol 2016; 65(4): 261-271.
- 5. Tacconelli E, Carrara E, Savoldi A. et al. Discovery, research and development of new antibiotics: The WHO priority list of antibiotic-resistant. Lancet Infect Dis 2017; 18(3): 318-327.
- 6. Botelho J, Grosso F, Peixe L. Antibiotic resistance in P.aeruginosa—Mechanisms, epidemiology and evolution. Drug Resist 2019; 44: 100640.
- 7. Sainz-Mejías M, Jurado-Martín I, McClean S. Understanding Pseudomonas aeruginosa-Host Interactions: The Ongoing Quest for an Efficacious Vaccine. Cells 2020; 9(12): 2617.
- 8. Karatuna O, Yağcı A. Virulence factors of Pseudomonas aeruginosa and quorum sensing. Türk Mikrobiyol Cem Derg 2008; 38(1): 42-51.
- 9. Alaa A. NOD-like receptor(s) and host immune responses with Pseudomonas aeruginosa infection. Inflamm Res 2018; 67: 479–493.
- 10. Skariyachan S, Sridhar VS, Packirisamy S, Kumargowda ST, Challapilli SB. Recent perspectives on the molecular basis of biofilm formation by Pseudomonas aeruginosa and approaches for treatment and biofilm dispersal. Folia Microbiol 2018; 63: 413-432.
- 11. Laverty G, Gorman S, Gilmore B. Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 2014; 3(3): 596-632.
- 12. Lambert PA. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J R SocMed 2002; 95: 22-26.
- 13. Pier GB, Ramphal R. Pseudomonas aeruginosa. In: Mandell GL, Bennett JE, Dolin, R, eds. Mandell, Douglas and Bennett’s Principles and Practice of Infectious Disease, 7th Edition, New York: Elsevier/Churchill Livingstone, 2009: 2587-2615.
- 14. Opal SM, Pop-Vicas A. Molecular Mechanisms of Antibiotic Resistance in Bacteria. In: Mandell G, Bennett J, Dolin R,eds. Mandell, Douglas and Bennett’s Principles and Practice of Infectious Disease 7th Edition, New York: Elsevier/Churchill Livingstone, 2009: 222-239.
- 15. Ulusoy S, Boşgelmez Tınaz G. Çeşitli klinik örneklerden izole edilen Pseudomonas aeruginosa suşlarında homoserin lakton üretimi ve antibiyotik duyarlılıklarının araştırılması. Cankaya Univ J Arts and Sciences 2008; 1(10): 145-151.
- 16. Harmsen M, YangL, Pamp SJ, Nielsen TT. Anupdate on P. aeruginosa biofilm formation, tolerance and dispersal. FEMS Immunol Med Microbiol 2010; 59(3): 253-68.
- 17. Roger SS, Rodney K, Barbara HI, Richard PP. The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J Immunol 2002; 169(5): 2636-2642.
- 18. Döring G, Vaccines and immunotherapy against Pseudomonas aeruginosa. Vaccine 2008; 26(8):1011-1024.
- 19. Köhler T, Curty LK, Barja F, Van Delden C, Pechere JC. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili.2000; 182(21): 5990–5996.
- 20. Barken KB, Pamp SJ, Yang L, et al. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 2008; 10(9): 2331-2343.
- 21. Bleves S, Viarre V, Salacha R, Michel GP, Filloux A, Voulhoux R. Protein secretion systems in Pseudomonas aeruginosa: A wealth of pathogenic weapons. Int J Med Microbiol 2010; 300: 534–543.
- 22. Pena RT, Blasco L, Ambroa A, et al. Relationship Between Quorum Sensing and Secretion Systems. Front Microbiol 2019; 10: 1100.
- 23. Anantharajah A, Mingeot-Leclercq MP, Van Bambeke F. Targeting the type three secretion system in Pseudomonas aeruginosa. Trends Pharmacol Sci 2016; 37: 734–749.
- 24. Sana TG, Berni B, Bleves S. The T6SSs of Pseudomonas aeruginosa strain PAO1 and their effectors: beyond bacterial-cell targeting. Front Cell Infect Microbiol 2016; 6: 61.
- 25. Passador L, Iglewski W. ADP-ribosylating toxins. Methods Enzymol 1994; 235: 617-31.
- 26. Iglewski BH, Liu PV, Kabat D. Mechanism of action of Pseudomonas aeruginosa exotoxin Aiadenosine diphosphate-ribosylation of mammalian elongation factor 2 in vitro and in vivo. Infect Immun 1977;15(1): 138-144.
- 27. Bielecki P, Glik J, Kawecki M, Vítor AP, Martins dos Santos VA. Towards understanding Pseudomonas aeruginosa burn wound infections by profiling gene expression. Biotechnol Lett 2008; 30(5): 777-790.
- 28. Hentzer M, Teitzeli GM, Balzer GJ, Heydorn A, Molin S, Givskov M. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 2001; 183: 5395-5401.
- 29. Yang J, Toyokufu M, Sakai R, Nomur N. Influence of the alginate production on cell-to-cell communication in Pseudomonas aeruginosa PAO1. Environ Microbiol Rep 2017; 9(3): 239–249.
- 30. Pearson JP, Gray KM, Passador L, et al. Structure of the autoinducer required for expression of P. aeruginosa virulence genes. Proc Natl Acad Sci U S A 1994; 91(1): 197-201.
- 31. Hirakawa H, Tomita H. Interference of bacterial cell-to-cell communication: a new concept of antimicrobial chemotherapy breaks antibiotic resistance. Front Microbiol 2013; 4: 114.
- 32. Hauser AR. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 2009 7; (9): 654-665.
- 33. Cornelis P. Putting an end to the Pseudomonas aeruginosa IQS controversy. Microbiol Open 2020; 9: e962.
- 34. Wang J, Wang C, Yu HB, et al. Bacterial quorum-sensing signal IQS induces host cell apoptosis by targeting POT1-p53 signaling pathway. Cell Microbiol 2019; 21: e13076.
- 35. Lee K, Yoon SS. Pseudomonas aeruginosa Biofilm, a Programmed Bacterial Life for Fitness. J Microbiol Biotechnol 2017; 27(6): 1053-1064.
- 36. Yan S, Wu G. Can Biofilm Be Reversed Through Quorum Sensing in Pseudomonas aeruginosa? Front Microbiol 2019; 10: 1582.
- 38. Ho BT, Dong TG, Mekalanos JJ. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 2014; 15(1): 9-21.
- 39. Miguel JC, Costa JC, Espeschit IF, Pieri FA, Benjamin LA, Moreira MAC. Increase in biofilm formation by Escherichia coli underconditions that mimic the mastitic mammary gland. Cienc Rural 2014; 44(4): 666-671.
- 40. Williamson KS, Richards LA, Perez-Osorio AC, et al. Heterogeneity in Pseudomonas aeruginosa biofilms include expression of ribosome hiber nation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 2012; 194(8): 2062-2073.
- 41. Pedrosa AP, Brandão MLL, Medeiros VM, et al. Research of virulence factors in Pseudomonas aeruginosa isolated from natural mineral waters. Rev Ambient Agua 2014; 9(2): 313-324.
- 42. Haüssler S, Becker T. The Pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLOS Pathogens 2008; 4(9): 1-8.
- 43. Gellatly SL, Hancock RE. P aeruginosa: new insights into, pathogenesis and host defenses. Pathog Dis 2013; 67: 159–173.
- 44. Oliver A, Mulet X, Causapé CL, Juan C. The increasing threat of Pseudomona saeruginosa high-risk clones. Drug Resist Updat 2015; 21(22): 41–59.
- 45. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol 2011; 35: 652–680.
- 46. McIsaac SM, Stadnyk AW, Lin TJ. Toll like receptors in the host defense against P. aeruginosa respiratory infection and cystic fibrosis. J Leukoc Biol 2012; 92: 977–985.
- 47. Lovewell RR, Patankar YR, Brent B. Mechanisms of phagocytosis and host clearance of P. aeruginosa. Am J Physiol Lung Cell Mol Physiol 2014; 306: L591–L603.
- 48. Lin CK, Barbara IK. Inflammation: A double-edgeds word in the response to Pseudomonas aeruginosa infection. J Innate Immun 2017; 9: 250–261.
- 49. Dosunmu EF, Emeh RO, Dixit S, et al. The anti-microbial peptide TP359 attenuates inflammation in human lung cells infected with Pseudomonas aeruginosa via TLR5 and MAPK pathways. PLoS ONE 2017; 12: e0176640.
- 50. Pang Z, Junkins RD, Raudonis R, et al. Regulator of calcineurin 1 differentially regulates TLR-dependent MyD88 and TRIF signaling pathways. PLoS ONE 2018; 13: e0197491.
- 51. Nakamura S, Iwanaga N, Seki M, et al. Toll-Like Receptor 4 Agonistic Antibody Promotes Host Defense against Chronic Pseudomonas aeruginosa Lung Infection in Mice. Infect Immun 2016; 84: 1986–1993.
- 52. Morris AE, Liggitt HD, Hawn TR, Shawn JS. Role of toll-like receptor 5 in the innate immune response to acute P. aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol 2009; 297: L1112–L1119.
- 53. Vijay-Kumar M, Carvalho FA, Aitken JD, Fifadara NH, Andrew TG. TLR5 or NLRC4 is necessary and sufficient for the promotion of humoral immunity by flagellin. Eur J Immunol 2010; 40: 3528–3534.
- 54. Cendra MDM, Christodoulides M, Parwez H. Signaling mediated by Toll-Like Receptor 5 sensing of Pseudomonas aeruginosa flagellin influences IL-1β and IL-18 production by primary fibroblasts derived from the human cornea. Front Cell Infect Microbiol 2017; 7: 130.
- 55. Lee JH, Jeon J, Bai F, Jin S, Wu W, Ha UH. The Pseudomonas aeruginosa HSP70-like protein DnaK induces IL-1β expression via TLR4-dependent activation of the NF-κBand JNK signaling pathways. Comp Immunol Microbiol Infect Dis 2019; 67: 101373.
- 56. Tolle L, Yu FS, Kovach MA, et al. Standiford, T.J. Redundant and cooperative interactions between TLR5 and NLRC4 in protective lung mucosal immunity against Pseudomonas aeruginosa. J Innate Immun 2015; 7; 177–186.
- 57. Pène F, Grimaldi D, Zuber B, et al. Toll like receptor 2 deficiency increases resistance to P. aeruginosa pneumonia in the setting of sepsis-induced immune dysfunction. J Infect Dis 2012; 206: 932–942.
- 58. Benmohamed F, Medina M, Wu YZ, Maschalidi S, Jouvion G, Guillemot L. Toll-like receptor 9 deficiency protects mice against P. aeruginosa lung infection. PloS One 2014; 9: e90466.
- 59. Lavoie EG, Wangdi T, Kazmierczak BI. Innate immune responses to Pseudomonas aeruginosa infection. Microbes Infect 2011; 13: 1133–1145.
- 60. Alhazmi A. NOD-like receptor(s) and host immune responses with Pseudomonas aeruginosa infection. Inflamm Res 2018; 67: 479–493.
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