Moderate alcohol induces stress proteins HSF1 and hsp70 and inhibits proinflammatory cytokines resulting in endotoxin tolerance

Journal of Immunology

Volumn 193, Issue 4, 2014, Pages 1975-1987

  Muralidharan, Sujatha ^a   Ambade, Aditya ^a   Fulham, Melissa A ^a   Deshpande, Janhavee ^a   Catalano, Donna ^a   Mandrekar, Pranoti ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ALCOHOL CONSUMPTION; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTOXIN TOLERANCE; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HSF1 GENE; HSP70 GENE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; INTRACELLULAR SIGNALING; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MIDDLE AGED; MONOCYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; TRANSCRIPTION INITIATION;

ADOLESCENT; ADULT; ALCOHOL DRINKING; ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENDOTOXINS; ETHANOL; FEMALE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MACROPHAGES; MALE; MICE; MIDDLE AGED; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B P50 SUBUNIT; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, MESSENGER; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84905985745     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303468     Document Type: Article

References (66)

1. Kumar, H. , T. Kawai, and S. Akira. 2011. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30: 16-34.
2. Kawai, T. , and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
3. Nelson, S. , and J. K. Kolls. 2002. Alcohol, host defence and society. Nat. Rev. Immunol. 2: 205-209.
4. Szabo, G. 1998. Monocytes, alcohol use, and altered immunity. Alcohol. Clin. Exp. Res. 22(5 Suppl)216S-219S.
5. D'Souza, A. J. , S. D. Desai, X. L. Rudner, M. N. Kelly, S. Ruan, and J. E. Shellito. 2013. Suppression of the macrophage proteasome by ethanol impairs MHC class I antigen processing and presentation. PLoS ONE 8: e56890.
6. Mandrekar, P. , V. Jeliazkova, D. Catalano, and G. Szabo. 2007. Acute alcohol exposure exerts anti-inflammatory effects by inhibiting IkappaB kinase activity and p65 phosphorylation in human monocytes. J. Immunol. 178: 7686-7693.
7. Pruett, S. B. , and R. Fan. 2009. Ethanol inhibits LPS-induced signaling and modulates cytokine production in peritoneal macrophages in vivo in a model for binge drinking. BMC Immunol. 10: 49.
8. Szabo, G. , S. Chavan, P. Mandrekar, and D. Catalano. 1999. Acute alcohol consumption attenuates interleukin-8 (IL-8) and monocyte chemoattractant peptide-1 (MCP-1) induction in response to ex vivo stimulation. J. Clin. Immunol. 19: 67-76.
9. Verma, B. K. , M. Fogarasi, and G. Szabo. 1993. Down-regulation of tumor necrosis factor alpha activity by acute ethanol treatment in human peripheral blood monocytes. J. Clin. Immunol. 13: 8-22.
10. Mandrekar, P. , S. Bala, D. Catalano, K. Kodys, and G. Szabo. 2009. The opposite effects of acute and chronic alcohol on lipopolysaccharide-induced inflammation are linked to IRAK-M in human monocytes. J. Immunol. 183: 1320-1327.
11. Bala, S. , A. Tang, D. Catalano, J. Petrasek, O. Taha, K. Kodys, and G. Szabo. 2012. Induction of Bcl-3 by acute binge alcohol results in toll-like receptor 4/LPS tolerance. J. Leukoc. Biol. 92: 611-620.
12. Xiong, Y. , and A. E. Medvedev. 2011. Induction of endotoxin tolerance in vivo inhibits activation of IRAK4 and increases negative regulators IRAK-M, SHIP-1, and A20. J. Leukoc. Biol. 90: 1141-1148.
13. Carmody, R. J. , Q. Ruan, S. Palmer, B. Hilliard, and Y. H. Chen. 2007. Negative regulation of toll-like receptor signaling by NF-kappaB p50 ubiquitination blockade. Science 317: 675-678.
14. Hoek, J. B. , and J. G. Pastorino. 2002. Ethanol, oxidative stress, and cytokineinduced liver cell injury. Alcohol 27: 63-68.
15. Kannan, M. , L. Wang, and Y. J. Kang. 2004. Myocardial oxidative stress and toxicity induced by acute ethanol exposure in mice. Exp. Biol. Med. (Maywood) 229: 553-559.
16. Yeligar, S. M. , F. L. Harris, C. M. Hart, and L. A. Brown. 2012. Ethanol induces oxidative stress in alveolar macrophages via upregulation of NADPH oxidases. J. Immunol. 188: 3648-3657.
17. Muralidharan, S. , and P. Mandrekar. 2013. Cellular stress response and innate immune signaling: integrating pathways in host defense and inflammation. J. Leukoc. Biol. 94: 1167-1184.
18. Ding, X. Z. , C. M. Fernandez-Prada, A. K. Bhattacharjee, and D. L. Hoover. 2001. Over-expression of hsp-70 inhibits bacterial lipopolysaccharide- induced production of cytokines in human monocyte-derived macrophages. Cytokine 16: 210-219.
19. Snyder, Y. M. , L. Guthrie, G. F. Evans, and S. H. Zuckerman. 1992. Transcriptional inhibition of endotoxin-induced monokine synthesis following heat shock in murine peritoneal macrophages. J. Leukoc. Biol. 51: 181-187.
20. Pirkkala, L. , P. Nykanen, and L. Sistonen. 2001. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15: 1118-1131.
21. Singh, I. S. , J. R. He, L. Hester, M. J. Fenton, and J. D. Hasday. 2004. Bacterial endotoxin modifies heat shock factor-1 activity in RAW 264. 7 cells: implications for TNF-alpha regulation during exposure to febrile range temperatures. J. Endotoxin Res. 10: 175-184.
22. Xie, Y. , C. Chen, M. A. Stevenson, P. E. Auron, and S. K. Calderwood. 2002. Heat shock factor 1 represses transcription of the IL-1beta gene through physical interaction with the nuclear factor of interleukin 6. J. Biol. Chem. 277: 11802-11810.
23. Song, M. , M. R. Pinsky, and J. A. Kellum. 2008. Heat shock factor 1 inhibits nuclear factor-kappaB nuclear binding activity during endotoxin tolerance and heat shock. J. Crit. Care 23: 406-415.
24. Mandrekar, P. , D. Catalano, V. Jeliazkova, and K. Kodys. 2008. Alcohol exposure regulates heat shock transcription factor binding and heat shock proteins 70 and 90 in monocytes and macrophages: implication for TNF-alpha regulation. J. Leukoc. Biol. 84: 1335-1345.
25. Szabo, G. , P. Mandrekar, L. Girouard, and D. Catalano. 1996. Regulation of human monocyte functions by acute ethanol treatment: decreased tumor necrosis factor-alpha, interleukin-1 beta and elevated interleukin-10, and transforming growth factor-beta production. Alcohol. Clin. Exp. Res. 20: 900-907.
26. Griffin, R. , A. M. Poe, J. M. Cross, L. W. Rue, III, and G. McGwin, Jr. 2009. The association between blood alcohol level and infectious complications among burn patients. J. Burn Care Res. 30: 395-399.
27. Mandrekar, P. , D. Catalano, and G. Szabo. 1999. Inhibition of lipopolysaccharide-mediated NFkappaB activation by ethanol in human monocytes. Int. Immunol. 11: 1781-1790.
28. Michels, A. A. , B. Kanon, A. W. Konings, K. Ohtsuka, O. Bensaude, and H. H. Kampinga. 1997. Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J. Biol. Chem. 272: 33283-33289.
29. Guha, M. , M. A. O'Connell, R. Pawlinski, A. Hollis, P. McGovern, S. F. Yan, D. Stern, and N. Mackman. 2001. Lipopolysaccharide activation of the MEKERK1/2 pathway in human monocytic cells mediates tissue factor and tumor necrosis factor alpha expression by inducing Elk-1 phosphorylation and Egr-1 expression. Blood 98: 1429-1439.
30. Jacobs, A. T. , and L. J. Marnett. 2009. HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. J. Biol. Chem. 284: 9176-9183.
31. Ambade, A. , D. Catalano, A. Lim, and P. Mandrekar. 2012. Inhibition of heat shock protein (molecular weight 90 kDa) attenuates proinflammatory cytokines and prevents lipopolysaccharide-induced liver injury in mice. Hepatology 55: 1585-1595.
32. Medvedev, A. E. , I. Sabroe, J. D. Hasday, and S. N. Vogel. 2006. Tolerance to microbial TLR ligands: molecular mechanisms and relevance to disease. J. Endotoxin Res. 12: 133-150.
33. Zou, J. , Y. Guo, T. Guettouche, D. F. Smith, and R. Voellmy. 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94: 471-480.
34. Chou, S. D. , T. Prince, J. Gong, and S. K. Calderwood. 2012. mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS ONE 7: e39679.
35. Guzhova, I. V. , Z. A. Darieva, A. R. Melo, and B. A. Margulis. 1997. Major stress protein Hsp70 interacts with NF-kB regulatory complex in human T-lymphoma cells. Cell Stress Chaperones 2: 132-139.
36. Singh, I. S. , J. R. He, S. Calderwood, and J. D. Hasday. 2002. A high affinity HSF-1 binding site in the 59-untranslated region of the murine tumor necrosis factor-alpha gene is a transcriptional repressor. J. Biol. Chem. 277: 4981-4988.
37. Szabo, G. 1999. Consequences of alcohol consumption on host defence. Alcohol Alcohol. 34: 830-841.
38. Drechsler, Y. , A. Dolganiuc, O. Norkina, L. Romics, W. Li, K. Kodys, F. H. Bach, P. Mandrekar, and G. Szabo. 2006. Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J. Immunol. 177: 2592-2600.
39. Greenberg, S. S. , O. Jie, X. Zhao, and J. F. Wang. 1998. Role of PKC and tyrosine kinase in ethanol-mediated inhibition of LPS-inducible nitric oxide synthase. Alcohol 16: 167-175.
40. Norkina, O. , A. Dolganiuc, D. Catalano, K. Kodys, P. Mandrekar, A. Syed, M. Efros, and G. Szabo. 2008. Acute alcohol intake induces SOCS1 and SOCS3 and inhibits cytokine-induced STAT1 and STAT3 signaling in human monocytes. Alcohol. Clin. Exp. Res. 32: 1565-1573.
41. Dai, Q. , and S. B. Pruett. 2006. Ethanol suppresses LPS-induced Toll-like receptor 4 clustering, reorganization of the actin cytoskeleton, and associated TNF-alpha production. Alcohol. Clin. Exp. Res. 30: 1436-1444.
42. Cláudio, N. , A. Dalet, E. Gatti, and P. Pierre. 2013. Mapping the crossroads of immune activation and cellular stress response pathways. EMBO J. 32: 1214-1224.
43. Zhang, Z. , G. J. Bagby, D. Stoltz, P. Oliver, P. O. Schwarzenberger, and J. K. Kolls. 2001. Prolonged ethanol treatment enhances lipopolysaccharide/ phorbol myristate acetate-induced tumor necrosis factor-alpha production in human monocytic cells. Alcohol. Clin. Exp. Res. 25: 444-449.
44. Nagy, L. E. 2003. Recent insights into the role of the innate immune system in the development of alcoholic liver disease. Exp. Biol. Med. (Maywood) 228: 882-890.
45. Xue, H. , D. Slavov, and P. E. Wischmeyer. 2012. Glutamine-mediated dual regulation of heat shock transcription factor-1 activation and expression. J. Biol. Chem. 287: 40400-40413.
46. Chen, Y. H. , C. M. Yang, S. P. Chang, and M. L. Hu. 2009. C/EBP beta and C/EBP delta expression is elevated in the early phase of ethanol-induced hepatosteatosis in mice. Acta Pharmacol. Sin. 30: 1138-1143.
47. He, L. , M. J. Ronis, and T. M. Badger. 2002. Ethanol induction of class I alcohol dehydrogenase expression in the rat occurs through alterations in CCAAT/enhancer binding proteins beta and gamma. J. Biol. Chem. 277: 43572-43577.
48. Norkina, O. , A. Dolganiuc, T. Shapiro, K. Kodys, P. Mandrekar, and G. Szabo. 2007. Acute alcohol activates STAT3, AP-1, and Sp-1 transcription factors via the family of Src kinases to promote IL-10 production in human monocytes. J. Leukoc. Biol. 82: 752-762.
49. Shi, L. , R. Kishore, M. R. McMullen, and L. E. Nagy. 2002. Chronic ethanol increases lipopolysaccharide-stimulated Egr-1 expression in RAW 264. 7 macrophages: contribution to enhanced tumor necrosis factor alpha production. J. Biol. Chem. 277: 14777-14785.
50. Akagi, R. , M. Ohno, K. Matsubara, M. Fujimoto, A. Nakai, and S. Inouye. 2013. Glutamine protects intestinal barrier function of colon epithelial cells from ethanol by modulating Hsp70 expression. Pharmacology 91: 104-111.
51. Pignataro, L. , F. P. Varodayan, L. E. Tannenholz, P. Protiva, and N. L. Harrison. 2013. Brief alcohol exposure alters transcription in astrocytes via the heat shock pathway. Brain Behav. 3: 114-133.
52. Islam, A. , P. Abraham, C. D. Hapner, P. A. Deuster, and Y. Chen. 2013. Tissuespecific upregulation of HSP72 in mice following short-term administration of alcohol. Cell Stress Chaperones 18: 215-222.
53. Li, Q. , and J. Ren. 2007. Chronic alcohol consumption alters mammalian target of rapamycin (mTOR), reduces ribosomal p70s6 kinase and p4E-BP1 levels in mouse cerebral cortex. Exp. Neurol. 204: 840-844.
54. Hong-Brown, L. Q. , C. R. Brown, A. A. Kazi, D. S. Huber, A. M. Pruznak, and C. H. Lang. 2010. Alcohol and PRAS40 knockdown decrease mTOR activity and protein synthesis via AMPK signaling and changes in mTORC1 interaction. J. Cell. Biochem. 109: 1172-1184.
55. Murshid, A. , S. D. Chou, T. Prince, Y. Zhang, A. Bharti, and S. K. Calderwood. 2010. Protein kinase A binds and activates heat shock factor 1. PLoS ONE 5: e13830.
56. Holmberg, C. I. , V. Hietakangas, A. Mikhailov, J. O. Rantanen, M. Kallio, A. Meinander, J. Hellman, N. Morrice, C. MacKintosh, R. I. Morimoto, et al. 2001. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20: 3800-3810.
57. Dohrman, D. P. , I. Diamond, and A. S. Gordon. 1996. Ethanol causes translocation of cAMP-dependent protein kinase catalytic subunit to the nucleus. Proc. Natl. Acad. Sci. USA 93: 10217-10221.
58. Mosser, D. D. , N. G. Theodorakis, and R. I. Morimoto. 1988. Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol. Cell. Biol. 8: 4736-4744.
59. Shi, Y. , Z. Tu, D. Tang, H. Zhang, M. Liu, K. Wang, S. K. Calderwood, and X. Xiao. 2006. The inhibition of LPS-induced production of inflammatory cytokines by HSP70 involves inactivation of the NF-kappaB pathway but not the MAPK pathways. Shock 26: 277-284.
60. Percival, S. S. , and C. A. Sims. 2000. Wine modifies the effects of alcohol on immune cells of mice. J. Nutr. 130: 1091-1094.
61. Watzl, B. , A. Bub, K. Briviba, and G. Rechkemmer. 2002. Acute intake of moderate amounts of red wine or alcohol has no effect on the immune system of healthy men. Eur. J. Nutr. 41: 264-270.
62. Xu, J. M. , and G. P. Shi. 2012. Emerging role of mast cells and macrophages in cardiovascular and metabolic diseases. Endocr. Rev. 33: 71-108.
63. Frantz, S. , and M. Nahrendorf. 2014. Cardiac macrophages and their role in ischaemic heart disease. Cardiovasc. Res. 102: 240-248.
64. Maier, R. V. 2001. Ethanol abuse and the trauma patient. Surg. Infect. (Larchmt). 2: 133-141; discussion 141-134.
65. Xia, Y. , Y. Liu, P. Rocchi, M. Wang, Y. Fan, F. Qu, J. L. Iovanna, and L. Peng. 2012. Targeting heat shock factor 1 with a triazole nucleoside analog to elicit potent anticancer activity on drug-resistant pancreatic cancer. Cancer Lett. 318: 145-153.
66. Goloudina, A. R. , O. N. Demidov, and C. Garrido. 2012. Inhibition of HSP70: a challenging anti-cancer strategy. Cancer Lett. 325: 117-124