α7 nicotinic acetylcholine receptor signaling inhibits inflammasome activation by preventing mitochondrial DNA release

Molecular Medicine

Volumn 20, Issue 1, 2014, Pages 350-358

  Lu, Ben ^a,b   Kwan, Kevin ^b   Levine, Yaakov A ^b,c   Olofsson, Peder S ^b   Yang, Huan ^b   Li, Jianhua ^b   Joshi, Sonia ^b   Wang, Haichao ^d   Andersson, Ulf ^e   Chavan, Sangeeta S ^b   Tracey, Kevin J ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c Setpoint Medical ^*  (United States)

^d NORTH SHORE UNIVERSITY HOSPITAL   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

3 (2,4 DIMETHOXYBENZYLIDENE)ANABASEINE; ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; BUNGAROTOXIN RECEPTOR; CALCIUM; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INFLAMMASOME; MITOCHONDRIAL DNA; WATER; CRYOPYRIN; CARRIER PROTEIN; CHOLINERGIC RECEPTOR STIMULATING AGENT; CHRNA7 PROTEIN, HUMAN; CHRNA7 PROTEIN, MOUSE; CIAS1 PROTEIN, MOUSE; CYTOKINE; LIPOPOLYSACCHARIDE; NLRP3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; CYTOPLASM; DENDRITIC CELL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG EFFECT; EMBRYO; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VAGUS NERVE STIMULATION; CELL DAMAGE; IMMUNOCOMPETENT CELL; INTRACELLULAR SIGNALING; MITOCHONDRIAL DNA RELEASE; NERVE STIMULATION; PROTEIN FUNCTION; SECRETION (PROCESS); TRANSPORT KINETICS; VAGUS NERVE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; GENETICS; HEK293 CELL LINE; KNOCKOUT MOUSE; METABOLISM;

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; CHOLINERGIC AGONISTS; CYTOKINES; DENDRITIC CELLS; DNA, MITOCHONDRIAL; HEK293 CELLS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84921913008     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2013.00117     Document Type: Article

References (31)

1. Okin D, Medzhitov R. (2012) Evolution of inflammatory diseases. Curr. Biol. 22:R733-40.
2. Andersson U, Tracey KJ. (2012) Reflex principles of immunological homeostasis. Annu. Rev. Immunol. 30:313-35.
3. Olofsson PS, Rosas-Ballina M, Levine YA, Tracey KJ. (2012) Rethinking inflammation: neural circuits in the regulation of immunity. Immunol. Rev. 248:188-204.
4. Rosas-Ballina M, et al. (2011) Acetylcholinesynthesizing T cells relay neural signals in a vagus nerve circuit. Science. 334:98-101.
5. Koopman FA, et al. (2012) Pilot study of stimulation of the cholinergic anti-inflammatory pathway with an implantable vagus nerve stimulation device in patients with rheumatoid arthritis. Arthritis Rheum. 64(10 Suppl):S195. Abstract No. 451.
6. Andersson U, Tracey KJ (2011) HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 29:139-62.
7. Patel VS, et al. (2013) High mobility group box-1 mediates hyperoxia-induced impairment of Pseudomonas aeruginosa clearance and inflammatory lung injury in mice. Am. J. Respir. Cell. Mol. Biol. 48:280-7.
8. Wang H, et al. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science. 285:248-51.
9. Chavan SS, et al. (2012) HMGB1 mediates cognitive impairment in sepsis survivors. Mol. Med. 18:930-7.
10. Willingham SB, et al. (2009) NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome- dependent and -independent pathways. J. Immunol. 183:2008-15.
11. Lu B, Wang H, Andersson U, Tracey KJ. (2013) Regulation of HMGB1 release by inflammasomes. Protein Cell. 4:163-7.
12. Lamkanfi M, et al. (2010) Inflammasomedependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 185:4385-92.
13. Kayagaki N, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature. 479:117-21.
14. Qin S, et al. (2006) Role of HMGB1 in apoptosis mediated sepsis lethality. J. Exp. Med. 203:1637-42.
15. Lu B, et al. (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature. 488:670-4.
16. Hett EC, et al. (2013) Chemical genetics reveals a kinase-independent role for protein kinase R in pyroptosis. Nat. Chem. Biol. 9:398-405.
17. Wang H, et al. (2004) Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat. Med. 10:1216-21.
18. Huston JM, et al. (2007) Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit. Care. Med. 35:2762-8.
19. Shimada K, et al. (2012) Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 36:401-14.
20. Nakahira K, et al. (2011) Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12:222-30.
21. Rosas-Ballina M, et al. (2009) The selective alpha7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE. Mol. Med. 15:195-202.
22. Wang H, et al. (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 421:384-8.
23. Zhou R, Yazdi AS, Menu P, Tschopp J. (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature. 469:221-5.
24. Murakami T, et al. (2012) Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 109:11282-7.
25. Gergalova G, et al. (2012) Mitochondria express α7 nicotinic acetylcholine receptors to regulate Ca2+ accumulation and cytochrome c release: study on isolated mitochondria. PLoS One. 7:e31361.
26. Kalashnyk OM, Gergalova GL, Komisarenko SV, Skok MV. (2012) Intracellular localization of nicotinic acetylcholine receptors in human cell lines. Life Sci. 91:1033-7.
27. Gulbransen BD, et al. (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 18:600-4.
28. Rathinam VA, Vanaja SK, Fitzgerald KA. (2012) Regulation of inflammasome signaling. Nat. Immunol. 13:333-2.
29. Muñoz-Planillo R, et al. (2013) K(+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity. 38:1142-53.
30. Strowig T, Henao-Mejia J, Elinav E, Flavell R. (2012) Inflammasomes in health and disease. Nature. 481:278-86.
31. Borovikova LV, et al. (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 405:458-62.