Neutrophil Elastase Causes Tissue Damage That Decreases Host Tolerance to Lung Infection with Species
Two distinct defense strategies can protect the host from infection:
resistance is the ability to destroy the infectious agent, and tolerance is the ability to withstand infection by minimizing the negative impact it has on the host's health without directly affecting pathogen burden. Burkholderia pseudomallei, the causative agent of melioidosis, is a Gram-negative intracellular bacteria that is categorized as a potential bioterrorism agent. Using murine models, we previously demonstrated that during B. pseudomallei infection, production of IL-1β is deleterious as it recruited excessive neutrophils to the site of infection. In the present work, we focused on the detrimental role of neutrophils during infection with B. pseudomallei and B. thailandensis. Here, we demonstrate that the excessive recruitment of neutrophils to the site of infection causes tissue damage because of release of the protease elastase. Mice lacking neutrophil elastase have increased survival even though they carry an equal amount of bacteria in their organs as compared to the wild-type C57BL/6J. Thus, neutrophil elastase is a host defense mechanism that causes tissue damage and reduces host tolerance to infection.
Vyšlo v časopise:
Neutrophil Elastase Causes Tissue Damage That Decreases Host Tolerance to Lung Infection with Species. PLoS Pathog 10(8): e32767. doi:10.1371/journal.ppat.1004327
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004327
Souhrn
Two distinct defense strategies can protect the host from infection:
resistance is the ability to destroy the infectious agent, and tolerance is the ability to withstand infection by minimizing the negative impact it has on the host's health without directly affecting pathogen burden. Burkholderia pseudomallei, the causative agent of melioidosis, is a Gram-negative intracellular bacteria that is categorized as a potential bioterrorism agent. Using murine models, we previously demonstrated that during B. pseudomallei infection, production of IL-1β is deleterious as it recruited excessive neutrophils to the site of infection. In the present work, we focused on the detrimental role of neutrophils during infection with B. pseudomallei and B. thailandensis. Here, we demonstrate that the excessive recruitment of neutrophils to the site of infection causes tissue damage because of release of the protease elastase. Mice lacking neutrophil elastase have increased survival even though they carry an equal amount of bacteria in their organs as compared to the wild-type C57BL/6J. Thus, neutrophil elastase is a host defense mechanism that causes tissue damage and reduces host tolerance to infection.
Zdroje
1. NathanC, DingA (2010) Nonresolving inflammation. Cell 140: 871–882.
2. SchneiderDS, AyresJS (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889–895.
3. MedzhitovR, SchneiderDS, SoaresMP (2012) Disease tolerance as a defense strategy. Science 335: 936–941.
4. AyresJS (2013) Inflammasome-microbiota interplay in host physiologies. Cell Host Microbe 14: 491–497.
5. WiersingaWJ, van der PollT, WhiteNJ, DayNP, PeacockSJ (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272–282.
6. Ceballos-OlveraI, SahooM, MillerMA, Del BarrioL, ReF (2011) Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1beta is deleterious. PLoS Pathog 7: e1002452.
7. KohGC, WeehuizenTA, BreitbachK, KrauseK, de JongHK, et al. (2013) Glyburide reduces bacterial dissemination in a mouse model of melioidosis. PLoS Negl Trop Dis 7: e2500.
8. KewcharoenwongC, RinchaiD, UtispanK, SuwannasaenD, BancroftGJ, et al. (2013) Glibenclamide reduces pro-inflammatory cytokine production by neutrophils of diabetes patients in response to bacterial infection. Sci Rep 3: 3363.
9. HaragaA, WestTE, BrittnacherMJ, SkerrettSJ, MillerSI (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated type III secretion system of Burkholderia pseudomallei. Infect Immun 76: 5402–5411.
10. BrettPJ, DeShazerD, WoodsDE (1998) Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48 (Pt 1) 317–320.
11. WiersingaWJ, WielandCW, van der WindtGJ, de BoerA, FlorquinS, et al. (2007) Endogenous interleukin-18 improves the early antimicrobial host response in severe melioidosis. Infect Immun 75: 3739–3746.
12. BreitbachK, WongprompitakP, SteinmetzI (2011) Distinct roles for nitric oxide in resistant C57BL/6 and susceptible BALB/c mice to control Burkholderia pseudomallei infection. BMC Immunol 12: 20.
13. BreitbachK, KlockeS, TschernigT, van RooijenN, BaumannU, et al. (2006) Role of inducible nitric oxide synthase and NADPH oxidase in early control of Burkholderia pseudomallei infection in mice. Infect Immun 74: 6300–6309.
14. MiyagiK, KawakamiK, SaitoA (1997) Role of reactive nitrogen and oxygen intermediates in gamma interferon-stimulated murine macrophage bactericidal activity against Burkholderia pseudomallei. Infect Immun 65: 4108–4113.
15. HerboldW, MausR, HahnI, DingN, SrivastavaM, et al. (2010) Importance of CXC chemokine receptor 2 in alveolar neutrophil and exudate macrophage recruitment in response to pneumococcal lung infection. Infect Immun 78: 2620–2630.
16. SpehlmannME, DannSM, HruzP, HansonE, McColeDF, et al. (2009) CXCR2-dependent mucosal neutrophil influx protects against colitis-associated diarrhea caused by an attaching/effacing lesion-forming bacterial pathogen. J Immunol 183: 3332–3343.
17. Del RioL, BennounaS, SalinasJ, DenkersEY (2001) CXCR2 deficiency confers impaired neutrophil recruitment and increased susceptibility during Toxoplasma gondii infection. J Immunol 167: 6503–6509.
18. ChanchamroenS, KewcharoenwongC, SusaengratW, AtoM, LertmemongkolchaiG (2009) Human polymorphonuclear neutrophil responses to Burkholderia pseudomallei in healthy and diabetic subjects. Infect Immun 77: 456–463.
19. EganAM, GordonDL (1996) Burkholderia pseudomallei activates complement and is ingested but not killed by polymorphonuclear leukocytes. Infect Immun 64: 4952–4959.
20. LiuPJ, ChenYS, LinHH, NiWF, HsiehTH, et al. (2013) Induction of mouse melioidosis with meningitis by CD11b+ phagocytic cells harboring intracellular B. pseudomallei as a Trojan horse. PLoS Negl Trop Dis 7: e2363.
21. EastonA, HaqueA, ChuK, LukaszewskiR, BancroftGJ (2007) A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J Infect Dis 195: 99–107.
22. CoeshottC, OhnemusC, PilyavskayaA, RossS, WieczorekM, et al. (1999) Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci U S A 96: 6261–6266.
23. GretenFR, ArkanMC, BollrathJ, HsuLC, GoodeJ, et al. (2007) NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130: 918–931.
24. GumaM, RonacherL, Liu-BryanR, TakaiS, KarinM, et al. (2009) Caspase 1-independent activation of interleukin-1beta in neutrophil-predominant inflammation. Arthritis Rheum 60: 3642–3650.
25. CrouchEC (1998) Structure, biologic properties, and expression of surfactant protein D (SP-D). Biochim Biophys Acta 1408: 278–289.
26. TaylorMD, Van DykeK, BowmanLL, MilesPR, HubbsAF, et al. (2000) A characterization of amiodarone-induced pulmonary toxicity in F344 rats and identification of surfactant protein-D as a potential biomarker for the development of the toxicity. Toxicol Appl Pharmacol 167: 182–190.
27. KunitakeR, KuwanoK, YoshidaK, MaeyamaT, KawasakiM, et al. (2001) KL-6, surfactant protein A and D in bronchoalveolar lavage fluid from patients with pulmonary sarcoidosis. Respiration 68: 488–495.
28. ChoiSM, McAleerJP, ZhengM, PociaskDA, KaplanMH, et al. (2013) Innate Stat3-mediated induction of the antimicrobial protein Reg3gamma is required for host defense against MRSA pneumonia. J Exp Med 210: 551–561.
29. RabergL, SimD, ReadAF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318: 812–814.
30. FerreiraA, MargutiI, BechmannI, JeneyV, ChoraA, et al. (2011) Sickle hemoglobin confers tolerance to Plasmodium infection. Cell 145: 398–409.
31. JamiesonAM, PasmanL, YuS, GamradtP, HomerRJ, et al. (2013) Role of tissue protection in lethal respiratory viral-bacterial coinfection. Science 340: 1230–1234.
32. Dela CruzCS, LiuW, HeCH, JacobyA, GornitzkyA, et al. (2012) Chitinase 3-like-1 promotes Streptococcus pneumoniae killing and augments host tolerance to lung antibacterial responses. Cell Host Microbe 12: 34–46.
33. BelaaouajA (2002) Neutrophil elastase-mediated killing of bacteria: lessons from targeted mutagenesis. Microbes Infect 4: 1259–1264.
34. WeinrauchY, DrujanD, ShapiroSD, WeissJ, ZychlinskyA (2002) Neutrophil elastase targets virulence factors of enterobacteria. Nature 417: 91–94.
35. KessenbrockK, DauT, JenneDE (2011) Tailor-made inflammation: how neutrophil serine proteases modulate the inflammatory response. J Mol Med (Berl) 89: 23–28.
36. PhamCT (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 6: 541–550.
37. BrinkmannV, ReichardU, GoosmannC, FaulerB, UhlemannY, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532–1535.
38. BrinkmannV, ZychlinskyA (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198: 773–783.
39. FangH, SunC, XuL, OwenRJ, AuthRD, et al. (2010) Neutrophil elastase mediates pathogenic effects of anthrax lethal toxin in the murine intestinal tract. J Immunol 185: 5463–5467.
40. VethanayagamRR, AlmyroudisNG, GrimmMJ, LewandowskiDC, PhamCT, et al. (2011) Role of NADPH oxidase versus neutrophil proteases in antimicrobial host defense. PLoS One 6: e28149.
41. AbrahamE (2003) Neutrophils and acute lung injury. Crit Care Med 31: S195–199.
42. ZemansRL, ColganSP, DowneyGP (2009) Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 40: 519–535.
43. MoraesTJ, ZurawskaJH, DowneyGP (2006) Neutrophil granule contents in the pathogenesis of lung injury. Curr Opin Hematol 13: 21–27.
44. GrommesJ, SoehnleinO (2011) Contribution of neutrophils to acute lung injury. Mol Med 17: 293–307.
45. JiangD, WenzelSE, WuQ, BowlerRP, SchnellC, et al. (2013) Human neutrophil elastase degrades SPLUNC1 and impairs airway epithelial defense against bacteria. PLoS One 8: e64689.
46. HenkeMO, JohnG, RheineckC, ChillappagariS, NaehrlichL, et al. (2011) Serine proteases degrade airway mucins in cystic fibrosis. Infect Immun 79: 3438–3444.
47. von BredowC, WiesenerA, GrieseM (2003) Proteolysis of surfactant protein D by cystic fibrosis relevant proteases. Lung 181: 79–88.
48. KozikA, MooreRB, PotempaJ, ImamuraT, Rapala-KozikM, et al. (1998) A novel mechanism for bradykinin production at inflammatory sites. Diverse effects of a mixture of neutrophil elastase and mast cell tryptase versus tissue and plasma kallikreins on native and oxidized kininogens. J Biol Chem 273: 33224–33229.
49. SakataY, AkaikeT, SugaM, IjiriS, AndoM, et al. (1996) Bradykinin generation triggered by Pseudomonas proteases facilitates invasion of the systemic circulation by Pseudomonas aeruginosa. Microbiol Immunol 40: 415–423.
50. OehmckeS, HerwaldH (2010) Contact system activation in severe infectious diseases. J Mol Med (Berl) 88: 121–126.
51. HircheTO, AtkinsonJJ, BahrS, BelaaouajA (2004) Deficiency in neutrophil elastase does not impair neutrophil recruitment to inflamed sites. Am J Respir Cell Mol Biol 30: 576–584.
52. MiaoEA, LeafIA, TreutingPM, MaoDP, DorsM, et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136–1142.
53. WangT, TownT, AlexopoulouL, AndersonJF, FikrigE, et al. (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10: 1366–1373.
54. Le GofficR, BalloyV, LagranderieM, AlexopoulouL, EscriouN, et al. (2006) Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog 2: e53.
55. HaseCC, FinkelsteinRA (1993) Bacterial extracellular zinc-containing metalloproteases. Microbiol Rev 57: 823–837.
56. ShawL, WiedowO (2011) Therapeutic potential of human elafin. Biochem Soc Trans 39: 1450–1454.
57. MottaJP, Bermudez-HumaranLG, DeraisonC, MartinL, RollandC, et al. (2012) Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Sci Transl Med 4: 158ra144.
58. CortelingR, WyssD, TrifilieffA (2002) In vivo models of lung neutrophil activation. Comparison of mice and hamsters. BMC Pharmacol 2: 1.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 8
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Disruption of Fas-Fas Ligand Signaling, Apoptosis, and Innate Immunity by Bacterial Pathogens
- Ly6C Monocyte Recruitment Is Responsible for Th2 Associated Host-Protective Macrophage Accumulation in Liver Inflammation due to Schistosomiasis
- Host Responses to Group A Streptococcus: Cell Death and Inflammation
- Pathogenicity and Epithelial Immunity