Unphosphorylated STAT3 modulates alpha7 nicotinic receptor signaling and cytokine production in sepsis

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2580-2589

  Peña, Geber ^a   Cai, Bolin ^a   Liu, Jun ^a   Van Der Zanden, Esmerij P ^b   Deitch, Edwin A ^a   De Jonge, Wouter J ^b,c   Ulloa, Luis ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Alpha7 nicotinic receptor; Inflammation; Sepsis; STAT3; TNF

Indexed keywords

ANTIINFLAMMATORY AGENT; BUNGAROTOXIN RECEPTOR; CHRNA7 PROTEIN, MOUSE; MUTANT PROTEIN; NICOTINIC RECEPTOR; SMALL INTERFERING RNA; STAT3 PROTEIN; STATTIC; SULFOXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; MACROPHAGE; MALE; METABOLISM; MOUSE; PATHOLOGY; PHOSPHORYLATION; SECRETION (PROCESS); SEPSIS; SIGNAL TRANSDUCTION; TRANSGENE;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; CYCLIC S-OXIDES; IMMUNOMODULATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MUTANT PROTEINS; PHOSPHORYLATION; RECEPTORS, NICOTINIC; RNA, SMALL INTERFERING; SEPSIS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSGENES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77956492231     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040540     Document Type: Article

References (39)

1. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J. and Pinsky, M. R., Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 2001. 29: 1303-1310.
2. Ulloa, L., Brunner, M., Ramos, L. and Deitch, E. A., Scientific and clinical challenges in sepsis. Curr. Pharm. Des. 2009. 15: 1918-1935.
3. Tracey, K. J., Fong, Y., Hesse, D. G., Manogue, K. R., Lee, A. T., Kuo, G. C., Lowry, S. F. and Cerami, A., Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature 1987. 330: 662-664.
4. Dinarello, C. A., Therapeutic strategies to reduce IL-1 activity in treating local and systemic inflammation. Curr. Opin. Pharmacol. 2004. 4: 378-385.
5. Riedemann, N. C., Guo, R. F. and Ward, P. A., Novel strategies for the treatment of sepsis. Nat. Med. 2003. 9: 517-524.
6. Ulloa, L. and Tracey, K. J., The "cytokine profile": a code for sepsis. Trends Mol. Med. 2005. 11: 56-63.
7. Feldmann, M., Development of anti-TNF therapy for rheumatoid arthritis. Nat. Rev. Immunol. 2002. 2: 364-371.
8. Grau, G. E. and Maennel, D. N., TNF inhibition and sepsis - sounding a cautionary note. Nat. Med. 1997. 3: 1193-1195.
9. Remick, D., Manohar, P., Bolgos, G., Rodriguez, J., Moldawer, L. and Wollenberg, G., Blockade of tumor necrosis factor reduces lipopolysaccharide lethality, but not the lethality of cecal ligation and puncture. Shock 1995. 4: 89-95.
10. Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., Frazier, A. et al., HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999. 285: 248-251.
11. Mantell, L. L., Parrish, W. R. and Ulloa, L., HMGB1 as a therapeutic target for infectious and inflammatory disorders. Shock 2006. 25: 4-11.
12. Li, W., Sama, A. E. and Wang, H., Role of HMGB1 in cardiovascular diseases. Curr. Opin. Pharmacol. 2006. 6: 130-135.
13. Angus, D. C., Caring for the critically ill patient: challenges and opportunities. J. Am. Med. Assoc. 2007. 298: 456-458.
14. Wang, H., Liao, H., Ochani, M., Justiniani, M., Lin, X., Yang, L., Al-Abed, Y. et al., Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat. Med. 2004. 10: 1216-1221.
15. Ulloa, L., The vagus nerve and the nicotinic anti-inflammatory pathway. Nat. Rev. Drug Discov. 2005. 4: 673-684.
16. Wang, H., Yu, M., Ochani, M., Amella, C. A., Tanovic, M., Susarla, S., Li, J. H. et al., Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003. 421: 384-388.
17. Thomas, G. A., Rhodes, J., Mani, V., Williams, G. T., Newcombe, R. G., Russell, M. A. and Feyerabend, C., Transdermal nicotine as maintenance therapy for ulcerative colitis. N. Engl. J. Med. 1995. 332: 988-992.
18. Huston, J. M., Ochani, M., Rosas-Ballina, M., Liao, H., Ochani, K., Pavlov, V. A., Gallowitsch-Puerta, M. et al., Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med. 2006. 203: 1623-1628.
19. de Jonge, W. J., van der Zanden, E. P., The, F. O., Bijlsma, M. F., van Westerloo, D. J., Bennink, R. J., Berthoud, H. R. et al., Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2- STAT3 signaling pathway. Nat. Immunol. 2005. 6: 844-851.
20. Meydan, N., Grunberger, T., Dadi, H., Shahar, M., Arpaia, E., Lapidot, Z., Leeder, J. S. et al., Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 1996. 379: 645-648.
21. Schust, J., Sperl, B., Hollis, A., Mayer, T. U. and Berg, T., Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem. Biol. 2006. 13: 1235-1242.
22. Nakajima, K., Yamanaka, Y., Nakae, K., Kojima, H., Ichiba, M., Kiuchi, N., Kitaoka, T. et al., A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 1996. 15: 3651-3658.
23. Lotze, M. T. and Tracey, K. J., High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 2005. 5: 331-342.
24. Ulloa, L. and Messmer, D., High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev. 2006. 17: 189-201.
25. Takeda, K., Clausen, B. E., Kaisho, T., Tsujimura, T., Terada, N., Forster, I. and Akira, S., Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999. 10: 39-49.
26. Matsukawa, A., Takeda, K., Kudo, S., Maeda, T., Kagayama, M. and Akira, S., Aberrant inflammation and lethality to septic peritonitis in mice lacking STAT3 in macrophages and neutrophils. J. Immunol. 2003. 171: 6198-6205.
27. Takeda, K., Noguchi, K., Shi, W., Tanaka, T., Matsumoto, M., Yoshida, N., Kishimoto, T. and Akira, S., Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. USA 1997. 94: 3801-3804.
28. Welte, T., Zhang, S. S., Wang, T., Zhang, Z., Hesslein, D. G., Yin, Z., Kano, A. et al., STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: a critical role of STAT3 in innate immunity. Proc. Natl. Acad. Sci. USA 2003. 100: 1879-1884.
29. Lee, H., Herrmann, A., Deng, J. H., Kujawski, M., Niu, G., Li, Z., Forman, S. et al., Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell 2009. 15: 283-293.
30. Yang, J., Liao, X., Agarwal, M. K., Barnes, L., Auron, P. E. and Stark, G. R., Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev. 2007. 21: 1396-1408.
31. Yang, J. and Stark, G. R., Roles of unphosphorylated STATs in signaling. Cell Res. 2008. 18: 443-451.
32. McMurray, J. S., A new small-molecule Stat3 inhibitor. Chem. Biol. 2006. 13: 1123-1124.
33. Crandall, M., Shapiro, M. B. and West, M. A., Does splenectomy protect against immune-mediated complications in blunt trauma patients? Mol. Med. 2009. 15: 263-267.
34. Liu, H., Yao, Y. M., Yu, Y., Dong, N., Yin, H. N. and Sheng, Z. Y., Role of Janus kinase/signal transducer and activator of transcription pathway in regulation of expression and inflammation-promoting activity of high mobility group box protein 1 in rat peritoneal macrophages. Shock 2007. 27: 55-60.
35. Kim, J. H., Kim, S. J., Lee, I. S., Lee, M. S., Uematsu, S., Akira, S. and Oh, K. I., Bacterial endotoxin induces the release of high mobility group box 1 via the IFN-beta signaling pathway. J. Immunol. 2009. 182: 2458-2466.
36. Eskandari, M. K., Bolgos, G., Miller, C., Nguyen, D. T., DeForge, L. E. and Remick, D. G., Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia. J. Immunol. 1992. 148: 2724-2730.
37. Calandra, T., Echtenacher, B., Roy, D. L., Pugin, J., Metz, C. N., Hultner, L., Heumann, D. et al., Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat. Med. 2000. 6: 164-170.
38. Yan, J. J., Jung, J. S., Lee, J. E., Lee, J., Huh, S. O., Kim, H. S., Jung, K. C. et al., Therapeutic effects of lysophosphatidylcholine in experimental sepsis. Nat. Med. 2004. 10: 161-167.
39. Pena, G., Cai, B., Deitch, E. A. and Ulloa, L., JAK2 inhibition prevents innate immune responses and rescues animals from sepsis. J. Mol. Med. 2010. 88: 851-859.