Translocation of Endogenous Danger Signal HMGB1 From Nucleus to Membrane Microvesicles in Macrophages

Journal of Cellular Physiology

Volumn 231, Issue 11, 2016, Pages 2319-2326

  Chen, Yan ^a,b   Li, Guangping ^b   Liu, Yanxia ^c   Werth, Victoria P ^d,e   Williams, Kevin Jon ^a,f   Liu, Ming Lin ^a,d,e  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SECOND HOSPITAL OF TIANJIN MEDICAL UNIVERSITY   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN;

ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CONDITIONED MEDIUM; CYTOPLASM; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; MACROPHAGE; MEMBRANE MICROPARTICLE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TOBACCO; ULTRACENTRIFUGATION;

EID: 84978429956     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25352     Document Type: Article

References (58)

1. Andersson U, Tracey KJ. 2011. HMGB1 is a therapeutic target for sterile inflammation and infection. Ann Rev Immunol 29:139–162.
2. Arnson Y, Shoenfeld Y, Amital H. 2010. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34:J258–J265.
3. Bezerra FS, Valenca SS, Pires KM, Lanzetti M, Pimenta WA, Schmidt AC, Porto LC, Zin WA. 2011. Long-term exposure to cigarette smoke impairs lung function and increases HMGB-1 expression in mice. Respir Physiol Neurobiol 177:120–126.
4. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME. 2003. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22:5551–5560.
5. Bulanova E, Budagyan V, Orinska Z, Klinger M, Bulfone-Paus S. 2009. Mast cells secrete IL-15 by microvesicles shedding upon P2 × 7 receptor stimulation. Cell Commun Signal 7:A70.
6. Buzas EI, Gyorgy B, Nagy G, Falus A, Gay S. 2014. Emerging role of extracellular vesicles in inflammatory diseases. Nat Rev Rheumatol 10:356–364.
7. Caldwell RB, Lattemann CT. 2004. Simple and reliable method to precipitate proteins from bacterial culture supernatant. Appl Environ Microbiol 70:610–612.
8. Chen GY, Nunez G. 2010. Sterile inflammation: Sensing and reacting to damage. Nat Rev Immunol 10:826–837.
9. Chen Y, Li G, Liu Y, Williams KJ, Liu ML. 2013. Exposure of human macrophages to tobacco smoke induces Hmgb1 release on microvesicles that cause monocyte recruitment and impairment of insulin signaling in adipocytes. Arterioscler Thromb Vasc Biol 33:A162.
10. Chen Y, Li G, Liu Y, Williams KJ, Wu XD, Liu ML. 2012. Hmgb1 on microvesicles mediates macrophage adipocyte crosstalk and impairs insulin signaling in adipocytes. Circulation 126:A16541.
11. Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey RA, Earp HS, Matsushima G, Reap EA. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 196:135–140.
12. Degryse B, Bonaldi T, Scaffidi P, Muller S, Resnati M, Sanvito F, Arrigoni G, Bianchi ME. 2001. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J cell Biol 152:1197–1206.
13. Deng L, Wang Y, Peng Y, Wu Y, Ding Y, Jiang Y, Shen Z, Fu Q. 2015. Osteoblast-derived microvesicles: A novel mechanism for communication between osteoblasts and osteoclasts. Bone 79:37–42.
14. Domagala-Kulawik J. 2008. Effects of cigarette smoke on the lung and systemic immunity. J Physiol Pharmacol 59:19–34.
15. Ferhani N, Letuve S, Kozhich A, Thibaudeau O, Grandsaigne M, Maret M, Dombret MC, Sims GP, Kolbeck R, Coyle AJ, Aubier M, Pretolani M. 2010. Expression of high-mobility group box 1 and of receptor for advanced glycation end products in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 181:917–927.
16. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF. 2003. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 101:2652–2660.
17. Folkesson M, Li C, Frebelius S, Swedenborg J, Wagsater D, Williams KJ, Eriksson P, Roy J, Liu ML. 2015. Proteolytically active ADAM10 and ADAM17 carried on membrane Microvesicles in human abdominal aortic aneurysms. Thromb Haemost 114:1165–1174.
18. Gallo RL, Bernard JJ. 2014. Innate immune sensors stimulate inflammatory and immunosuppressive responses to UVB radiation. J Invest Dermatol 134:1508–1511.
19. Giron-Michel J, Giuliani M, Fogli M, Brouty-Boye D, Ferrini S, Baychelier F, Eid P, Lebousse-Kerdiles C, Durali D, Biassoni R, Charpentier B, Vasquez A, Chouaib S, Caignard A, Moretta L, Azzarone B. 2005. Membrane-bound and soluble IL-15/IL-15Ralpha complexes display differential signaling and functions on human hematopoietic progenitors. Blood 106:2302–2310.
20. Gougeon ML, Melki MT, Saidi H. 2012. HMGB1, an alarmin promoting HIV dissemination and latency in dendritic cells. Cell Death Differ 19:96–106.
21. Heijink IH, Pouwels SD, Leijendekker C, de Bruin HG, Zijlstra GJ, van der Vaart H, Ten Hacken NH, van Oosterhout AJ, Nawijn MC, van der Toorn M. 2015. Cigarette smoke-induced damage-associated molecular pattern release from necrotic neutrophils triggers proinflammatory mediator release. Am J Respir Cell Mol Biol 52:554–562.
22. Johannsen A, Susin C, Gustafsson A. 2014. Smoking and inflammation: Evidence for a synergistic role in chronic disease. Periodontol 2000 64:111–126.
23. Kim DK, Lee J, Kim SR, Choi DS, Yoon YJ, Kim JH, Go G, Nhung D, Hong K, Jang SC, Kim SH, Park KS, Kim OY, Park HT, Seo JH, Aikawa E, Baj-Krzyworzeka M, van Balkom BW, Belting M, Blanc L, Bond V, Bongiovanni A, Borras FE, Buee L, Buzas EI, Cheng L, Clayton A, Cocucci E, Dela Cruz CS, Desiderio DM, Di Vizio D, Ekstrom K, Falcon-Perez JM, Gardiner C, Giebel B, Greening DW, Gross JC, Gupta D, Hendrix A, Hill AF, Hill MM, Nolte-'t Hoen E, Hwang DW, Inal J, Jagannadham MV, Jayachandran M, Jee YK, Jorgensen M, Kim KP, Kim YK, Kislinger T, Lasser C, Lee DS, Lee H, van Leeuwen J, Lener T, Liu ML, Lotvall J, Marcilla A, Mathivanan S, Moller A, Morhayim J, Mullier F, Nazarenko I, Nieuwland R, Nunes DN, Pang K, Park J, Patel T, Pocsfalvi G, Del Portillo H, Putz U, Ramirez MI, Rodrigues ML, Roh TY, Royo F, Sahoo S, Schiffelers R, Sharma S, Siljander P, Simpson RJ, Soekmadji C, Stahl P, Stensballe A, Stepien E, Tahara H, Trummer A, Valadi H, Vella LJ, Wai SN, Witwer K, Yanez-Mo M, Youn H, Zeidler R, Gho YS. 2015. EVpedia: A community web portal for extracellular vesicles research. Bioinformatics 31:933–939.
24. Krakowiak A, Sliwkiewicz K, Nowakowska-Swirta E, Winnicka R, Politanski P. 2015. High-mobility group box 1 protein levels in serum of subjects after exposure to fire smoke—Short communication. Pneumonol Alergol Pol 83:203–207.
25. Lecube A, Pachon G, Petriz J, Hernandez C, Simo R. 2011. Phagocytic activity is impaired in type 2 diabetes mellitus and increases after metabolic improvement. PLoS ONE 6:e23366.
26. Li C, Liu Y, Chen Y, Yu D, Williams KJ, Liu ML. 2013. Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke. Am J Pathol 182:1552–1562.
27. Li M, Li C, Liu Y, Chen Y, Wu X, Yu D, Werth VP, Williams KJ, Liu ML. 2015. Decreased secretion of adiponectin through its intracellular accumulation in adipose tissue during tobacco smoke exposure. Nutr Metab 12:15.
28. Li M, Yu D, Williams KJ, Liu ML. 2010. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol 30:1818–1824.
29. Li S, Sun Y, Liang CP, Thorp EB, Han S, Jehle AW, Saraswathi V, Pridgen B, Kanter JE, Li R, Welch CL, Hasty AH, Bornfeldt KE, Breslow JL, Tabas I, Tall AR. 2009. Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet. Circ Res 105:1072–1082.
30. Liu G, Wang J, Park YJ, Tsuruta Y, Lorne EF, Zhao X, Abraham E. 2008. High mobility group protein-1 inhibits phagocytosis of apoptotic neutrophils through binding to phosphatidylserine. J Immunol 181:4240–4246.
31. Liu M, Xu H, Bashir M, Sharma M, Williams K, Anyanwu C, Okawa J, Werth VP. 2014. Proinflammatory microvesicles in patients with cutaneous lupus erythematosus. J Invest Dermatol 134:S13.
32. Liu ML, Reilly MP, Casasanto P, McKenzie SE, Williams KJ. 2007. Cholesterol enrichment of human monocyte/macrophages induces surface exposure of phosphatidylserine and the release of biologically-active tissue factor-positive microvesicles. Arterioscler Thromb Vasc Biol 27:430–435.
33. Liu ML, Scalia R, Mehta JL, Williams KJ. 2012. Cholesterol-induced membrane microvesicles as novel carriers of damage-associated molecular patterns: Mechanisms of formation, action, and detoxification. Arterioscler Thromb Vasc Biol 32:2113–2121.
34. Liu ML, Williams KJ. 2012. Microvesicles: Potential markers and mediators of endothelial dysfunction. Curr Opin Endocrinol Diabetes Obes 19:121–127.
35. Morel O, Toti F, Hugel B, Freyssinet JM. 2004. Cellular microparticles: A disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol 11:156–164.
36. Nakashima T, Kobayashi Y, Yamasaki S, Kawakami A, Eguchi K, Sasaki H, Sakai H. 2000. Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand: Modulation of the expression by osteotropic factors and cytokines. Biochem Biophys Res Commun 275:768–775.
37. Nativel B, Marimoutou M, Thon-Hon VG, Gunasekaran MK, Andries J, Stanislas G, Planesse C, Da Silva CR, Cesari M, Iwema T, Gasque P, Viranaicken W. 2013. Soluble HMGB1 is a novel adipokine stimulating IL-6 secretion through RAGE receptor in SW872 preadipocyte cell line: Contribution to chronic inflammation in fat tissue. PLoS ONE 8:e76039.
38. Perricone C, Versini M, Ben-Ami D, Gertel S, Watad A, Segel MJ, Ceccarelli F, Conti F, Cantarini L, Bogdanos DP, Antonelli A, Amital H, Valesini G, Shoenfeld Y. 2016. Smoke and autoimmunity: The fire behind the disease. Autoimmun Rev 15:354–374.
39. Pisetsky DS. 2014. The expression of HMGB1 on microparticles released during cell activation and cell death in vitro and in vivo. Mol Med (Cambridge, Mass) 20:158–163.
40. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. 2006. Membrane-derived microvesicles: Important and underappreciated mediators of cell-to-cell communication. Leukemia 20:1487–1495.
41. Richens TR, Linderman DJ, Horstmann SA, Lambert C, Xiao YQ, Keith RL, Boe DM, Morimoto K, Bowler RP, Day BJ, Janssen WJ, Henson PM, Vandivier RW. 2009. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am J Respir Crit Care Med 179:1011–1021.
42. Rouhiainen A, Kuja-Panula J, Wilkman E, Pakkanen J, Stenfors J, Tuominen RK, Lepantalo M, Carpen O, Parkkinen J, Rauvala H. 2004. Regulation of monocyte migration by amphoterin (HMGB1). Blood 104:1174–1182.
43. Saiwichai T, Sangalangkarn V, Kawahara K, Oyama Y, Chaichalotornkul S, Narkpinit S, Harnyuttanakorn P, Singhasivanon P, Maruyama I, Tancharoen S. 2010. Green tea extract supplement inhibition of HMGB1 release in rats exposed to cigarette smoke. Southeast Asian J Trop Med Public Health 41:250–258.
44. Schiller M, Heyder P, Ziegler S, Niessen A, Classen L, Lauffer A, Lorenz HM. 2012. During apoptosis HMGB1 is translocated into apoptotic cell-derived membraneous vesicles. Autoimmunity 46:342–346.
45. Seong SY, Matzinger P. 2004. Hydrophobicity: An ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4:469–478.
46. Shen H, Kreisel D, Goldstein DR. 2013. Processes of sterile inflammation. J Immunol 191:2857–2863.
47. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. 2010. HMGB1 and RAGE in inflammation and cancer. Ann Rev Immunol 28:367–388.
48. Tang D, Kang R, Xiao W, Wang H, Calderwood SK, Xiao X. 2007. The anti-inflammatory effects of heat shock protein 72 involve inhibition of high-mobility-group box 1 release and proinflammatory function in macrophages. J Immunol 179:1236–1244.
49. Tsuchiya K, Hara H, Kawamura I, Nomura T, Yamamoto T, Daim S, Dewamitta SR, Shen Y, Fang R, Mitsuyama M. 2010. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J Immunol 185:1186–1195.
50. Tsung A, Tohme S, Billiar TR. 2014. High-mobility group box-1 in sterile inflammation. J Intern Med 276:425–443.
51. Tsung A, Zheng N, Jeyabalan G, Izuishi K, Klune JR, Geller DA, Lotze MT, Lu L, Billiar TR. 2007. Increasing numbers of hepatic dendritic cells promote HMGB1-mediated ischemia-reperfusion injury. J Leukocyte Biol 81:119–128.
52. Turner JG, Dawson J, Sullivan DM. 2012. Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol 83:1021–1032.
53. Wang Y, Chen L, Liu ML. 2014. Microvesicles and diabetic complications—Novel mediators, potential biomarkers and therapeutic targets. Acta Pharmacol Sin 35:433–443.
54. Yanai H, Taniguchi T. 2014. Nucleic acid sensing and beyond: Virtues and vices of high-mobility group box 1. J Intern Med 276:444–453.
55. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S. 2008. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210–213.
56. You R, Lu W, Shan M, Berlin JM, Samuel EL, Marcano DC, Sun Z, Sikkema WK, Yuan X, Song L, Hendrix AY, Tour JM, Corry DB, Kheradmand F. 2015. Nanoparticulate carbon black in cigarette smoke induces DNA cleavage and Th17-mediated emphysema. Elife 4:e09623.
57. Youn JH, Shin JS. 2006. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol 177:7889–7897.
58. Yuan X, Shan M, You R, Frazier MV, Hong MJ, Wetsel RA, Drouin S, Seryshev A, Song LZ, Cornwell L, Rossen RD, Corry DB, Kheradmand F. 2015. Activation of C3a receptor is required in cigarette smoke-mediated emphysema. Mucosal Immunol 8:874–885.