Melatonin alleviates acute lung injury through inhibiting the NLRP3 inflammasome

Journal of Pineal Research

Volumn 60, Issue 4, 2016, Pages 405-414

  Zhang, Yong ^a   Li, Xiru ^b   Grailer, Jamison J ^c   Wang, Na ^a   Wang, Mingming ^a   Yao, Jianfei ^a   Zhong, Rui ^a   Gao, George F ^d   Ward, Peter A ^c   Tan, Dun Xian ^e   Li, Xiangdong ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Department of General Surgery   (China)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d INSTITUTE OF MICROBIOLOGY   (China)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

acute lung injury; histone; melatonin; NLRP inflammasome; reactive oxygen species

Indexed keywords

CRYOPYRIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MELATONIN; ANTIINFLAMMATORY AGENT; INFLAMMASOME; NLRP3 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PERITONEUM MACROPHAGE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; MACROPHAGE; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; PATHOLOGY; WESTERN BLOTTING;

ACUTE LUNG INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; INFLAMMASOMES; MACROPHAGES; MALE; MELATONIN; MICE; MICE, INBRED C57BL; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; REACTIVE OXYGEN SPECIES; X-RAY MICROTOMOGRAPHY;

EID: 84960327836     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12322     Document Type: Article

References (50)

1. Matthay MA, Ware LB, Zimmerman GA,. The acute respiratory distress syndrome. J Clin Invest 2012; 122: 2731-2740.
2. Mei SH, McCarter SD, Deng Y, et al., Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med 2007; 4: e269.
3. Standiford TJ, Ward PA,. Therapeutic targeting of acute lung injury and acute respiratory distress syndrome. Transl Res 2016; 167: 183-191.
4. Levy M, Thaiss CA, Elinav E,. Taming the inflammasome. Nat Med 2015; 21: 213-215.
5. Latz E, Xiao TS, Stutz A,. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013; 13: 397-411.
6. Lee S, Suh GY, Ryter SW, et al., Regulation and function of the nucleotide binding domain leucine-rich repeat-containing receptor, pyrin domain-containing-3 Inflammasome in lung disease. Am J Respir Cell Mol Biol 2016; 54: 151-160.
7. Miller LS, Pietras EM, Uricchio LH, et al., Inflammasome-mediated production of IL-1 beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol 2007; 179: 6933-6942.
8. Cohen TS, Prince AS,. Activation of inflammasome signaling mediates pathology of acute P. aeruginosa pneumonia. J Clin Invest 2013; 123: 1630-1637.
9. Mishra BB, Moura-Alves P, Sonawane A, et al., Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol 2010; 12: 1046-1063.
10. Allen IC, Scull MA, Moore CB, et al., The NLRP3 Inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009; 30: 556-565.
11. Dostert C, Petrilli V, van Bruggen R, et al., Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008; 320: 674-677.
12. Grailer JJ, Canning BA, Kalbitz M, et al., Critical role for the NLRP3 inflammasome during acute lung injury. J Immunol 2014; 192: 5974-5983.
13. Gasse P, Riteau N, Charron S, et al., Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am J Respir Crit Care Med 2009; 179: 903-913.
14. Jesus AA, Goldbach-Mansky R,. IL-1 blockade in autoinflammatory syndromes. Annu Rev Med 2014; 65: 223-244.
15. Baldwin AG, Brough D, Freeman S,. Inhibiting the inflammasome: a chemical perspective. J Med Chem 2015. doi: 10.1021/acs.jmedchem.5b01091.
16. Mauriz JL, Collado PS, Veneroso C, et al., A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
17. Carrillo-Vico A, Lardone PJ, Alvarez-Sanchez N, et al., Melatonin: buffering the immune system. Int J Mol Sci 2013; 14: 8638-8683.
18. Manchester LC, Coto-Montes A, Boga JA, et al., Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res 2015; 59: 403-419.
19. Xia MZ, Liang YL, Wang H, et al., Melatonin modulates TLR4-mediated inflammatory genes through MyD88- and TRIF-dependent signaling pathways in lipopolysaccharide-stimulated RAW264.7 cells. J Pineal Res 2012; 53: 325-334.
20. Deng WG, Tang ST, Tseng HP, et al., Melatonin suppresses macrophage cyclooxygenase-2 and inducible nitric oxide synthase expression by inhibiting p52 acetylation and binding. Blood 2006; 108: 518-524.
21. Ortiz F, Acuna-Castroviejo D, Doerrier C, et al., Melatonin blunts the mitochondrial/NLRP3 connection and protects against radiation-induced oral mucositis. J Pineal Res 2015; 58: 34-49.
22. Garcia JA, Volt H, Venegas C, et al., Disruption of the NF-kappaB/NLRP3 connection by melatonin requires retinoid-related orphan receptor-alpha and blocks the septic response in mice. FASEB J 2015; 29: 3863-3875.
23. Spoelstra EN, Ince C, Koeman A, et al., A novel and simple method for endotracheal intubation of mice. Lab Anim 2007; 41: 128-135.
24. Liu MH, Lin AH, Lee HF, et al., Paeonol attenuates cigarette smoke-induced lung inflammation by inhibiting ROS-sensitive inflammatory signaling. Mediators Inflamm 2014; 2014: 651890.
25. Yu W, Zheng H, Lin W, et al., Estrogen promotes Leydig cell engulfment by macrophages in male infertility. J Clin Invest 2014; 124: 2709-2721.
26. Zeng WQ, Zhang JQ, Li Y, et al., A new method to isolate and culture rat kupffer cells. PLoS ONE 2013; 8: e70832.
27. Bosmann M, Grailer JJ, Ruemmler R, et al., Extracellular histones are essential effectors of C5aR- and C5L2-mediated tissue damage and inflammation in acute lung injury. FASEB J 2013; 27: 5010-5021.
28. de Langhe E, Vande Velde G, Hostens J, et al., Quantification of lung fibrosis and emphysema in mice using automated micro-computed tomography. PLoS ONE 2012; 7: e43123.
29. Vande Velde G, Poelmans J, de Langhe E, et al., Longitudinal micro-CT provides biomarkers of lung disease and therapy in preclinical models, thereby revealing compensatory changes in lung volume. Dis Model Mech 2015. doi: 10.1242/dmm.020321.
30. Dolinay T, Kim YS, Howrylak J, et al., Inflammasome-regulated cytokines are critical mediators of acute lung injury. Am J Respir Crit Care Med 2012; 185: 1225-1234.
31. Kolb M, Margetts PJ, Anthony DC, et al., Transient expression of IL-1beta induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 2001; 107: 1529-1536.
32. Heid ME, Keyel PA, Kamga C, et al., Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol 2013; 191: 5230-5238.
33. Kasahara T, Abe K, Mekada K, et al., Genetic variation of melatonin productivity in laboratory mice under domestication. Proc Natl Acad Sci USA 2010; 107: 6412-6417.
34. Schell-Chaple HM, Puntillo KA, Matthay MA, et al., Body temperature and mortality in patients with acute respiratory distress syndrome. Am J Crit Care 2015; 24: 15-23.
35. Langheinrich AC, Leithauser B, Greschus S, et al., Acute rat lung injury: feasibility of assessment with micro-CT. Radiology 2004; 233: 165-171.
36. Cavanaugh D, Travis EL, Price RE, et al., Quantification of bleomycin-induced murine lung damage in vivo with micro-computed tomography. Acad Radiol 2006; 13: 1505-1512.
37. Martinon F, Burns K, Tschopp J,. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002; 10: 417-426.
38. Ozaki E, Campbell M, Doyle SL,. Targeting the NLRP3 inflammasome in chronic inflammatory diseases: current perspectives. J Inflamm Res 2015; 8: 15-27.
39. Ozkurede VU, Franchi L,. Immunology in clinic review series; focus on autoinflammatory diseases: role of inflammasomes in autoinflammatory syndromes. Clin Exp Immunol 2012; 167: 382-390.
40. Coll RC, Robertson AA, Chae JJ, et al., A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat Med 2015; 21: 248-255.
41. Volt H, Garcia JA, Doerrier C, et al., Same molecule but different expression: aging and sepsis trigger NLRP3 inflammasome activation, a target of melatonin. J Pineal Res 2016; 60: 193-205.
42. Aggarwal NR, King LS, D'Alessio FR,. Diverse macrophage populations mediate acute lung inflammation and resolution. Am J Physiol Lung Cell Mol Physiol 2014; 306: L709-L725.
43. Jacobs RF, Tabor DR, Burks AW, et al., Elevated interleukin-1 release by human alveolar macrophages during the adult respiratory distress syndrome. Am Rev Respir Dis 1989; 140: 1686-1692.
44. Jordan JA, Guo RF, Yun EC, et al., Role of IL-18 in acute lung inflammation. J Immunol 2001; 167: 7060-7068.
45. Kuipers MT, Aslami H, Janczy JR, et al., Ventilator-induced lung injury is mediated by the NLRP3 inflammasome. Anesthesiology 2012; 116: 1104-1115.
46. Wu J, Yan Z, Schwartz DE, et al., Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol 2013; 190: 3590-3599.
47. Mulligan MS, Ward PA,. Immune complex-induced lung and dermal vascular injury. Differing requirements for tumor necrosis factor-alpha and IL-1. J Immunol 1992; 149: 331-339.
48. Sun CK, Lee FY, Kao YH, et al., Systemic combined melatonin-mitochondria treatment improves acute respiratory distress syndrome in the rat. J Pineal Res 2015; 58: 137-150.
49. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
50. Zhang HM, Zhang Y,. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J Pineal Res 2014; 57: 131-146.