Ethanol impairs mucosal immunity against Streptococcus pneumoniae infection by disrupting interleukin 17 gene expression

Infection and Immunity

Volumn 83, Issue 5, 2015, Pages 2082-2088

  Trevejo Nunez, Giraldina ^a   Chen, Kong ^a   Dufour, Jason P ^b   Bagby, Gregory J ^c   Horne, William T ^a   Nelson, Steve ^c   Kolls, Jay K ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CARBON TETRACHLORIDE; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TRANSCRIPTOME;

ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL IMMUNITY; BACTERIAL LOAD; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; GENE EXPRESSION; GENETIC ANALYSIS; HOST RESISTANCE; IMMUNE RESPONSE; LUNG ALVEOLUS EPITHELIUM; LUNG BURDEN; MALE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIMATE MODEL; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RHESUS MONKEY; SIGNAL TRANSDUCTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; STREPTOCOCCUS PNEUMONIAE; ANIMAL; BIOSYNTHESIS; BRONCHUS; COHORT ANALYSIS; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; IMMUNOLOGY; MUCOSA;

ANIMALS; BRONCHI; COHORT STUDIES; DISEASE MODELS, ANIMAL; ETHANOL; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNITY, MUCOSAL; INTERLEUKIN-17; MACACA MULATTA; MALE; MICE; MUCOUS MEMBRANE; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 84928189176     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02869-14     Document Type: Article

References (29)

1. Abbott AC. 1896. The influence of acute alcoholism on the normal vital resistance of rabbits to infection. J Exp Med 1:447-481.
2. Rubin G. 1904. The influence of alcohol, ether, and chloroform on natural immunity in its relation to leucocytosis and phagocytosis. J Infect Dis 1:425-444. http://dx.doi.org/10.1093/infdis/1.3.425.
3. Bouchery EE, Harwood HJ, Sacks JJ, Simon CJ, Brewer RD. 2011. Economic costs of excessive alcohol consumption in the U.S., 2006. Am J Prev Med 41:516-524. http://dx.doi.org/10.1016/j.amepre.2011.06.045.
4. Picard C, Puel A, Bonnet M, Ku CL, Bustamante J, Yang K, Soudais C, Dupuis S, Feinberg J, Fieschi C, Elbim C, Hitchcock R, Lammas D, Davies G, Al-Ghonaium A, Al-Rayes H, Al-Jumaah S, Al-Hajjar S, Al-Mohsen IZ, Frayha HH, Rucker R, Hawn TR, Aderem A, Tufenkeji H, Haraguchi S, Day NK, Good RA, Gougerot-Pocidalo MA, Ozinsky A, Casanova JL. 2003. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299:2076-2079. http://dx.doi.org/10.1126/science.1081902.
5. von Bernuth H, Picard C, Jin Z, Pankla R, Xiao H, Ku CL, Chrabieh M, Mustapha IB, Ghandil P, Camcioglu Y, Vasconcelos J, Sirvent N, Guedes M, Vitor AB, Herrero-Mata MJ, Arostegui JI, Rodrigo C, Alsina L, Ruiz-Ortiz E, Juan M, Fortuny C, Yague J, Anton J, Pascal M, Chang HH, Janniere L, Rose Y, Garty BZ, Chapel H, Issekutz A, Marodi L, Rodriguez-Gallego C, Banchereau J, Abel L, Li X, Chaussabel D, Puel A, Casanova JL. 2008. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321:691-696. http://dx.doi.org/10.1126/science.1158298.
6. Zhang Z, Clarke TB, Weiser JN. 2009. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119:1899-1909. http://dx.doi.org/10.1172/JCI36731.
7. Lu YJ, Gross J, Bogaert D, Finn A, Bagrade L, Zhang Q, Kolls JK, Srivastava A, Lundgren A, Forte S, Thompson CM, Harney KF, Anderson PW, Lipsitch M, Malley R. 2008. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog 4:e1000159. http://dx.doi.org/10.1371/journal.ppat.1000159.
8. Gu C, Wu L, Li X. 2013. IL-17 family: cytokines, receptors and signaling. Cytokine 64:477-485. http://dx.doi.org/10.1016/j.cyto.2013.07.022.
9. Laan M, Cui ZH, Hoshino H, Lotvall J, Sjostrand M, Gruenert DC, Skoogh BE, Linden A. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 162:2347-2352.
10. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194:519-527. http://dx.doi.org/10.1084/jem.194.4.519.
11. McAllister F, Henry A, Kreindler JL, Dubin PJ, Ulrich L, Steele C, Finder JD, Pilewski JM, Carreno BM, Goldman SJ, Pirhonen J, Kolls JK. 2005. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growthrelated oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J Immunol 175:404-412. http://dx.doi.org/10.4049/jimmunol.175.1.404.
12. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, Pociask DA, Reinhart TA, McAllister F, Edeal J, Gaus K, Husain S, Kreindler JL, Dubin PJ, Pilewski JM, Myerburg MM, Mason CA, Iwakura Y, Kolls JK. 2008. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14:275-281. http://dx.doi.org/10.1038/nm1710.
13. Molina PE, Amedee AM, Veazey R, Dufour J, Volaufova J, Bagby GJ, Nelson S. 2014. Chronic binge alcohol consumption does not diminish effectiveness of continuous antiretroviral suppression of viral load in SIV-infected macaques. Alcohol Clin Exp Res 9:2335-2344. http://dx.doi.org/10.1111/acer.12507.
14. Nelson S, Happel KI, Zhang P, Myers L, Dufour JP, Bagby GJ. 2013. Effect of bacterial pneumonia on lung simian immunodeficiency virus (SIV) replication in alcohol consuming SIV-infected rhesus macaques. Alcohol Clin Exp Res 37:969-977. http://dx.doi.org/10.1111/acer.12070.
15. Dubin PJ, Martz A, Eisenstatt JR, Fox MD, Logar A, Kolls JK. 2012. Interleukin-23-mediated inflammation in Pseudomonas aeruginosa pulmonary infection. Infect Immun 80:398-409. http://dx.doi.org/10.1128/IAI.05821-11.
16. Finsterbusch M, Voisin MB, Beyrau M, Williams TJ, Nourshargh S. 2014. Neutrophils recruited by chemoattractants in vivo induce microvascular plasma protein leakage through secretion of TNF. J Exp Med 211:1307-1314. http://dx.doi.org/10.1084/jem.20132413.
17. Yao L, Yago T, Shao B, Liu Z, Silasi-Mansat R, Setiadi H, Lupu F, McEver RP. 2013. Elevated CXCL1 expression in gp130-deficient endothelial cells impairs neutrophil migration in mice. Blood 122:3832-3842. http://dx.doi.org/10.1182/blood-2012-12-473835.
18. Boespflug ND, Kumar S, McAlees JW, Phelan JD, Grimes HL, Hoebe K, Hai T, Filippi MD, Karp CL. 2014. ATF3 is a novel regulator of mouse neutrophil migration. Blood 123:2084-2093. http://dx.doi.org/10.1182/blood-2013-06-510909.
19. Boe DM, Nelson S, Zhang P, Bagby GJ. 2001. Acute ethanol intoxication suppresses lung chemokine production following infection with Streptococcus pneumoniae. J Infect Dis 184:1134-1142. http://dx.doi.org/10.1086/323661.
20. Boe DM, Nelson S, Zhang P, Quinton L, Bagby GJ. 2003. Alcoholinduced suppression of lung chemokine production and the host defense response to Streptococcus pneumoniae. Alcohol Clin Exp Res 27:1838-1845. http://dx.doi.org/10.1097/01.ALC.0000095634.82310.53.
21. Quinton LJ, Nelson S, Zhang P, Happel KI, Gamble L, Bagby GJ. 2005. Effects of systemic and local CXC chemokine administration on the ethanolinduced suppression of pulmonary neutrophil recruitment. Alcohol Clin Exp Res 29:1198-1205. http://dx.doi.org/10.1097/01.ALC.0000171927.66130.AA.
22. Siggins RW, Melvan JN, Welsh DA, Bagby GJ, Nelson S, Zhang P. 2011. Alcohol suppresses the granulopoietic response to pulmonary Streptococcus pneumoniae infection with enhancement of STAT3 signaling. J Immunol 186:4306-4313. http://dx.doi.org/10.4049/jimmunol.1002885.
23. Smith RJ, Sam LM, Leach KL, Justen JM. 1992. Postreceptor events associated with human neutrophil activation by interleukin-8. J Leukoc Biol 52:17-26.
24. Barlic J, Andrews JD, Kelvin AA, Bosinger SE, DeVries ME, Xu L, Dobransky T, Feldman RD, Ferguson SS, Kelvin DJ. 2000. Regulation of tyrosine kinase activation and granule release through beta-arrestin by CXCRI. Nat Immunol 1:227-233. http://dx.doi.org/10.1038/79767.
25. Zhang P, Nelson S, Holmes MC, Summer WR, Bagby GJ. 2002. Compartmentalization of macrophage inflammatory protein-2, but not cytokine-induced neutrophil chemoattractant, in rats challenged with intratracheal endotoxin. Shock 17:104-108. http://dx.doi.org/10.1097/00024382-200202000-00004.
26. Quinton LJ, Nelson S, Zhang P, Boe DM, Happel KI, Pan W, Bagby GJ. 2004. Selective transport of cytokine-induced neutrophil chemoattractant from the lung to the blood facilitates pulmonary neutrophil recruitment. Am J Physiol Lung Cell Mol Physiol 286:L465-L472. http://dx.doi.org/10.1152/ajplung.00153.2003.
27. Cook RT. 1998. Alcohol abuse, alcoholism, and damage to the immune system-a review. Alcohol Clin Exp Res 22:1927-1942. http://dx.doi.org/10.1111/j.1530-0277.1998.tb05900.x.
28. Bertola A, Mathews S, Ki SH, Wang H, Gao B. 2013. Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat Protoc 8:627-637. http://dx.doi.org/10.1038/nprot.2013.032.
29. Mathews S, Xu M, Wang H, Bertola A, Gao B. 2014. Animals models of gastrointestinal and liver diseases. Animal models of alcohol-induced liver disease: pathophysiology, translational relevance, and challenges. Am J Physiol Gastrointest Liver Physiol 306:G819-G823. http://dx.doi.org/10.1152/ajpgi.00041.2014.