Persistence of Burkholderia thailandensis E264 in lung tissue after a single binge alcohol episode
Autoři:
Victor M. Jimenez, Jr. aff001; Erik W. Settles aff001; Bart J. Currie aff003; Paul S. Keim aff001; Fernando P. Monroy aff001
Působiště autorů:
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, United States of America
aff001; Pathogen & Microbiome Institute (PMI), Northern Arizona University, Flagstaff, AZ, United States of America
aff002; Menzies School of Health Research, Charles Darwin University, Darwin, Australia
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0218147
Souhrn
Background
Binge drinking, an increasingly common form of alcohol use disorder, is associated with substantial morbidity and mortality; yet, its effects on the immune system’s ability to defend against infectious agents are poorly understood. Burkholderia pseudomallei, the causative agent of melioidosis can occur in healthy humans, yet binge alcohol intoxication is increasingly being recognized as a major risk factor. Although our previous studies demonstrated that binge alcohol exposure increased B. pseudomallei near-neighbor virulence in vivo and increased paracellular diffusion and intracellular invasion, no experimental studies have examined the extent to which bacterial and alcohol dosage play a role in disease progression. In addition, the temporal effects of a single binge alcohol dose prior to infection has not been examined in vivo.
Principal findings
In this study, we used B. thailandensis E264 a close genetic relative of B. pseudomallei, as useful BSL-2 model system. Eight-week-old female C57BL/6 mice were utilized in three distinct animal models to address the effects of 1) bacterial dosage, 2) alcohol dosage, and 3) the temporal effects, of a single binge alcohol episode. Alcohol was administered comparable to human binge drinking (≤ 4.4 g/kg) or PBS intraperitoneally before a non-lethal intranasal infection. Bacterial colonization of lung and spleen was increased in mice administered alcohol even after bacterial dose was decreased 10-fold. Lung and not spleen tissue were colonized even after alcohol dosage was decreased 20 times below the U.S legal limit. Temporally, a single binge alcohol episode affected lung bacterial colonization for more than 24 h after alcohol was no longer detected in the blood. Pulmonary and splenic cytokine expression (TNF-α, GM-CSF) remained suppressed, while IL-12/p40 increased in mice administered alcohol 6 or 24 h prior to infection. Increased lung and not intestinal bacterial invasion was observed in human and murine non-phagocytic epithelial cells exposed to 0.2% v/v alcohol in vitro.
Conclusions
Our results indicate that the effects of a single binge alcohol episode are tissue specific. A single binge alcohol intoxication event increases bacterial colonization in mouse lung tissue even after very low BACs and decreases the dose required to colonize the lungs with less virulent B. thailandensis. Additionally, the temporal effects of binge alcohol alters lung and spleen cytokine expression for at least 24 h after alcohol is detected in the blood. Delayed recovery in lung and not spleen tissue may provide a means for B. pseudomallei and near-neighbors to successfully colonize lung tissue through increased intracellular invasion of non-phagocytic cells in patients with hazardous alcohol intake.
Klíčová slova:
Cytokines – Blood – Alcohol consumption – Spleen – Mouse models – Epithelial cells – Alcohols – Burkholderia infection
Zdroje
1. Rush B. (1808). An inquiry into the effects of ardent spirits upon the human body and mind: With an account of the means of preventing, and of the remedies for curing them (4th ed.). Philadelphia: Printed for Thomas Dobson; Archibald Bartram, printer.
2. Moss M. (2005) Epidemiology of Sepsis: Race, Sex, and Chronic Alcohol Abuse. Clin Infect Dis. 41(1): S490–S497. doi: 10.1086/432003 16237652
3. Currie BJ. (2015) Melioidosis: Evolving Concepts in Epidemiology, Pathogenesis, and Treatment. Semin Respir Crit Care Med. 36: 111–125. doi: 10.1055/s-0034-1398389 25643275
4. Wiersinga WJ, Currie BJ, Peacock SJ. (2012) Melioidosis. N Engl J Med. 367: 1035–44. doi: 10.1056/NEJMra1204699 22970946
5. Glass M, Gee J, Steigerwalt A, Cavuoti D, Barton T, Hardy R, et al. (2006) Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. Journal of clinical microbiology. 44(12): 4601–4604. doi: 10.1128/JCM.01585-06 17050819
6. Currie BJ, Jacups SP, Cheng AC, Fisher DA, Anstey NM, Huffam SE, et al. (2004) Melioidosis epidemiology and risk factors from a prospective whole-population study in northern Australia. Trop Med Int Health. (11):1167–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15548312 doi: 10.1111/j.1365-3156.2004.01328.x 15548312.
7. Bhatty M, Pruett SB, Swiatlo E, Nanduri B. (2011) Alcohol abuse and Streptococcus pneumoniae infections: Consideration of virulence factors and impaired immune responses. Alcohol. Elsevier Inc. 45: 523–539. doi: 10.1016/j.alcohol.2011.02.305 21827928
8. Bermudez LE, Young LS, Martinelli J, Petrofsky M. (1993) Exposure to ethanol up-regulates the expression of Mycobacterium avium complex proteins associated with bacterial virulence. J Infect Dis. 168: 961–968. doi: 10.1093/infdis/168.4.961 8376842
9. Camarena L, Bruno V, Euskirchen G, Poggio S, Snyder M. (2010) Molecular mechanisms of ethanol-induced pathogenesis revealed by RNA-sequencing. PLoS Pathog. 6(4): e1000834. doi: 10.1371/journal.ppat.1000834 20368969
10. Gordon SB, Irving GRB, Lawson R a, Lee ME, Read RC. (2000) Intracellular Trafficking and Killing of Streptococcus pneumoniae by Human Alveolar Macrophages Are Influenced by Opsonins. Infection and Immunity 68(4): 2286–2293. doi: 10.1128/iai.68.4.2286-2293.2000 10722631
11. Jimenez V, Moreno R, Settles E, Currie BJ, Keim P, Monroy FP. (2018) A mouse model of binge alcohol consumption and Burkholderia infection. PLoS One. 13(11): 1–19. doi: 10.1371/journal.pone.0208061 30485380
12. Goral J, Karavitis J, Kovacs EJ. (2008) Exposure-dependent effects of ethanol on the innate immune system. Alcohol. 42(4): 237–247. doi: 10.1016/j.alcohol.2008.02.003 18411007
13. National Institutes of Alcohol Abuse and Alcoholism. Drinking levels defined. Available at: https://www.niaaa.nih.gov/alcohol-health/overview-alcohol-consumption/moderate-binge-drinking. Accessed February, 2019.
14. Pruett SB, Schwab C, Zheng Q, Fan R. (2004) Suppression of innate immunity by acute ethanol administration: a global perspective and a new mechanism beginning with inhibition of signaling through TLR3. J Immunol. 173: 2715–2724. doi: 10.4049/jimmunol.173.4.2715 15294990
15. Rendon JL, Janda BA, Bianco ME, Choudhry MA. (2012) Ethanol Exposure Suppresses Bone Marrow-Derived Dendritic Cell Inflammatory Responses Independent of TLR4 Expression. J Interf Cytokine Res. 32(9): 416–425. doi: 10.1089/jir.2012.0005 22812678
16. Yeligar SM, Harris FL, Hart CM, Brown LAS. (2014) Glutathione attenuates ethanol-induced alveolar macrophage oxidative stress and dysfunction by down-regulating NADPH oxidases. Am J Physiol Lung Cell Mol Physiol. 306: L429–L441. doi: 10.1152/ajplung.00159.2013 24441868
17. Yeligar SM, Chen MM, Kovacs EJ, Sisson JH, Burnham EL, Brown LA. (2016) Alcohol and lung injury and immunity. Alcohol. 55: 51–59. doi: 10.1016/j.alcohol.2016.08.005 27788778
18. Jimenez V, Moreno R, Kaufman E, Hornstra H, Settles E, Currie BJ, et al. (2017) Effects of binge alcohol exposure on Burkholderia thailandensis–alveolar macrophage interaction. Alcohol. Elsevier Ltd. 64: 55–63. doi: 10.1016/j.alcohol.2017.04.004 28965656
19. Bhatty M, Tan W, Basco M, Pruett S, Nanduri B. (2017) Binge alcohol consumption 18 h after induction of sepsis in a mouse model causes rapid overgrowth of bacteria, a cytokine storm, and decreased survival. Alcohol. 63:9–17. doi: 10.1016/j.alcohol.2016.11.007 28847384
20. Eysseric H, Gonthier B, Soubeyran A, Bessard G, Saxod R, Barret L. (1997) There is no simple method to maintain a constant ethanol concentration in long-term cell culture: Keys to a solution applied to the survey of astrocytic ethanol absorption. Alcohol. 14: 111–115. doi: 10.1016/s0741-8329(96)00112-7 9085710
21. Diercks AH, Surman SL, Navarro G, Hurwitz JL, Rosenberger CM, Dash P, et al. (2013) Characterization of innate responses to influenza virus infection in a novel lung type I epithelial cell model. J Gen Virol. 95: 350–362. doi: 10.1099/vir.0.058438-0 24243730
22. Kwapiszewska G, Herold S, von Wulffen W, Cakarova L, Seeger W, Marsh LM, et al. (2009) Surface expression of CD74 by type II alveolar epithelial cells: a potential mechanism for macrophage migration inhibitory factor-induced epithelial repair. Am J Physiol Cell Mol Physiol. 296: L442–L452. doi: 10.1152/ajplung.00525.2007 19136583
23. Nelson S, Kolls JK. (2002) Alcohol, host defense and society. Nat Rev Immunol. 2: 205–209. doi: 10.1038/nri744 11913071
24. Szabo G, Saha B. (2015) Alcohol’s Effect on Host Defense. Alcohol Res. 37 (2): 159–170. 26695755
25. D’Souza El-Guindy N, Kovacs EJ, De Witte P, Spies C, Littleton JM, De Villiers WJ et al. (2010) Laboratory models available to study alcohol-induced organ damage and immune variations; choosing the appropriate model. Alcohol Clin Exp Res. 34(9): 997–1003. doi: 10.1016/j.biotechadv.2011.08.021.Secreted
26. Morici LA, Heang J, Tate T, Didier PJ, Roy CJ. (2010) Differential susceptibility of inbred mouse strains to Burkholderia thailandensis aerosol infection. Microb Pathog. Elsevier Ltd. 48: 9–17. doi: 10.1016/j.micpath.2009.10.004 19853031
27. Passalacqua KD, Charbonneau M-E, O’Riordan MXD. (2016) Bacterial Metabolism Shapes the Host–Pathogen Interface. Virulence Mechanisms of Bacterial Pathogens, Fifth Edition. 4(3): 1–31. doi: 10.1128/microbiolspec.vmbf-0027-2015 27337445
28. Kespichayawattana W, Intachote P, Utaisincharoen P, Sirisinha S. (2004) Virulent Burkholderia pseudomallei is more efficient than avirulent Burkholderia thailandensis in invasion of and adherence to cultured human epithelial cells. Microb Pathog. 36: 287–292. doi: 10.1016/j.micpath.2004.01.001 15043863
29. Tan GYG, Liu Y, Sivalingam SP, Sim SH, Wang D, Paucod JC, et al. (2008) Burkholderia pseudomallei aerosol infection results in differential inflammatory responses in BALB/c and C57BL/6 mice. J Med Microbiol. 57: 508–515. doi: 10.1099/jmm.0.47596-0 18349373
30. Trammell R, Toth LA. (2011) Markers for Predicting Death as an Outcome for Mice Used in Infectious Disease Research. Am Assoc Lab Anim Sci. 61(6): 492–498. doi: 10.1111/j.2042-3306.1985.tb02052.x
31. Romero F, Shah D, Hoek JB, Duong M, Lang CH, Stafstrom W, et al. (2014) Chronic Alcohol Ingestion in Rats Alters Lung Metabolism, Promotes Lipid Accumulation, and Impairs Alveolar Macrophage Functions. Am J Respir Cell Mol Biol. 51(6): 840–849. doi: 10.1165/rcmb.2014-0127OC 24940828
32. George SC, Hlastala MP, Souders JE, Babb AL. (1996) Gas Exchange in the Airways. J Aerosol Med. 9(1): 25–33. doi: 10.1089/jam.1996.9.25 10172721
33. Massey VL, Beier JI, Ritzenthaler JD, Roman J, Arteel GE. (2015) Potential role of the gut/liver/lung axis in alcohol-induced tissue pathology. Biomolecules. 5: 2477–2503. doi: 10.3390/biom5042477 26437442
34. Simet S, Sisson J. Alcohol’s Effects on Lung Health and Immunity. (2015) Curr Rev. 37: 199–208.
35. Kim JS, Shukla SD. (2006) Acute in vivo effect of ethanol (binge drinking) on histone H3 modifications in rat tissues. Alcohol and Alcoholism. 41(2): 126–132. doi: 10.1093/alcalc/agh248 16314425
36. Kaphalia L, Calhoun WJ. (2013) Alcoholic lung injury: Metabolic, biochemical and immunological aspects. Toxicology Letters. 222(2): 1–21. doi: 10.1016/j.toxlet.2013.07.016 23892124
37. Kershaw CD, Guidot DM. (2008) Putting Systems Biology Approaches Into Practice Alcoholic Lung Disease: Alcoholic lung disease. Alcohol Res Health. 31(1): 66–75. 23584753
38. Barr T, Helms C, Grant K, Messaoudi I. (2016) Opposing Effects of Alcohol on the Immune System Overview of the Immune System HHS Public Access. Prog Neuropsychopharmacol Biol Psychiatry. 65: 242–251. doi: 10.1016/j.pnpbp.2015.09.001 26375241
39. Manzo-Avalos S, Saavedra-Molina A. (2010) Cellular and mitochondrial effects of alcohol consumption. International Journal of Environmental Research and Public Health. 7: 4281–4304 doi: 10.3390/ijerph7124281 21318009
40. Agarwal DP. (2001) Genetic polymorphisms of alcohol metabolizing enzymes. Pathol Biol. 49: 703–9. doi: 10.1016/s0369-8114(01)00242-5 11762132
41. Koivisto T, Salaspuro M. (1998) Acetaldehyde alters proliferation, differentiation and adhesion properties of human colon adenocarcinoma cell line Caco-2. Carcinogenesis. 19(11): 2031–2036. doi: 10.1093/carcin/19.11.2031 9855020
42. Mehta A, Guidot D. (2017) Alcohol and the lung. Alcohol Res Curr Rev. 38: 243–254.
43. Roine RP, Salmela KS, Salaspuro M. (1995) Alcohol metabolism in helicobacter pylori-infected stomach. Ann Med. 27(5): 583–588. doi: 10.3109/07853899509002473 8541036
44. Boule LA, Kovacs EJ. (2017) Alcohol, aging, and innate immunity. J Leukoc Biol. 102: 41–55. doi: 10.1189/jlb.4RU1016-450R 28522597
45. Tussey L, Felder MR. (1989) Tissue-specific genetic variation in the level of mouse alcohol dehydrogenase is controlled transcriptionally in kidney and posttranscriptionally in liver. Proc Natl Acad Sci. 86: 5903–5907. doi: 10.1073/pnas.86.15.5903 2474823
46. Joshi PC, Applewhite L, Ritzenthaler JD, Roman J, Fernandez AL, Eaton DC, et al. (2005) Chronic Ethanol Ingestion in Rats Decreases Expression and Downstream Signaling in the. 175: 6837–6845. doi: 10.4049/jimmunol.175.10.6837 16272341
47. Rowland CA, Lertmemongkolchai G, Bancroft, G. J.’Garra A, Bancroft A, Haque A, et al. (2006) Critical Role of Type 1 Cytokines in Controlling Initial Infection with Burkholderia mallei. Infect Immun. 74: 5333–5430. doi: 10.1128/IAI.02046-05 16926428
48. Bhatty M, Jan BL, Tan W, Pruett SB, Nanduri B. (2011) Role of acute ethanol exposure and TLR4 in early events of sepsis in a mouse model. Alcohol. 45: 795–803. doi: 10.1016/j.alcohol.2011.07.003 21872420
49. Sibley D, Jerrells TR. (2000) Alcohol consumption by C57BL/6 mice is associated with depletion of lymphoid cells from the gut-associated lymphoid tissues and altered resistance to oral infections with Salmonella typhimurium. J Infect Dis. 182: 482–489. doi: 10.1086/315728 10915079
50. Wuest DM, Wing AM, Lee KH. (2013) Membrane configuration optimization for a murine in vitro blood-brain barrier model. J Neurosci Methods. 212: 211–221. doi: 10.1016/j.jneumeth.2012.10.016 23131353
51. Mir H, Meena AS, Chaudhry KK, Shukla PK, Gangwar R, Manda B, et al. (2016) Occludin deficiency promotes ethanol-induced disruption of colonic epithelial junctions, gut barrier dysfunction and liver damage in mice. Biochim Biophys Acta—Gen Subj. 1860: 765–774. doi: 10.1016/j.bbagen.2015.12.013 26721332
52. Wang Y, Zhang D, Wang B, Chang B, Wang B, Tong J. (2014) Effects of alcohol on intestinal epithelial barrier permeability and expression of tight junction-associated proteins. Mol Med Rep. 9: 2352–2356. doi: 10.3892/mmr.2014.2126 24718485
53. Patel S, Behara R, Swanson GR, Forsyth CB, Voigt RM, Keshavarzian A. (2015) Alcohol and the intestine. Biomolecules. 5: 2573–2588. doi: 10.3390/biom5042573 26501334
54. Traphagen N, Tian Z, Allen-Gipson D. (2015) Chronic ethanol exposure: Pathogenesis of pulmonary disease and dysfunction. Biomolecules. 5: 2840–2853. doi: 10.3390/biom5042840 26492278
55. Osna NA, Kharbanda KK. (2016) Multi-organ alcohol-related damage: Mechanisms and treatment. Biomolecules. 6(20): 1–5. doi: 10.3390/biom6020020 27092531
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts