The role of extracellular histone in organ injury

Cell Death and Disease

Volumn 8, Issue 5, 2017, Pages

  Silk, Eleanor ^a   Zhao, Hailin ^a   Weng, Hao ^b   Ma, Daqing ^a  

^a CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^b SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE;

ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; EXTRACELLULAR SPACE; HUMAN; INFLAMMATION; METABOLISM; PATHOLOGY;

ANIMALS; EXTRACELLULAR SPACE; HISTONES; HUMANS; INFLAMMATION; MODELS, BIOLOGICAL; ORGAN SPECIFICITY;

EID: 85028636130     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2017.52     Document Type: Review

References (106)

1. Eltzschig HK, Eckle T. Ischemia and reperfusion–from mechanism to translation. Nat Med 2011; 17: 1391–1401.
2. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187: 2626–2631.
3. Rock KL, Latz E, Ontiveros F, Kono H. The sterile inflammatory response. Annu Rev Immunol 2010; 28: 321–342.
4. Zhao H, Jaffer T, Eguchi S, Wang Z, Linkermann A, Ma D. Role of necroptosis in the pathogenesis of solid organ injury 2015; 6: 1–10.
5. Lenz A, Franklin GA, Cheadle WG. Systemic inflammation after trauma. Injury 2007; 38: 1336–1345.
6. Doenecke D, Karlson P, Kossel A, Miescher F, Schulze E, Steiger E et al. Albrecht Kossel and the discovery of histones. Trends Biochem Sci 1984; 9: 404–405.
7. Campos EI, Reinberg D. Histones: annotating chromatin. Annu Rev Genet 2009; 43: 559–599.
8. Zentner GE, Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 2013; 20: 259–266.
9. Bhaumik SR, Smith E, Shilatifard A. Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 2007; 14: 1008–1016.
10. Bird A. Perceptions of epigenetics. Nature 2007; 447: 396–398.
11. Felsenfeld G, Groudine M. Controlling the double helix. Nature 2003; 421: 448–453.
12. Venkatesh S, Workman JL. Histone exchange, chromatin structure and the regulation of transcription. Nat Rev Mol Cell Biol 2015; 16: 178–189.
13. Chen R, Kang R, Fan X-G, Tang D. Release and activity of histone in diseases. Cell Death Dis 2014; 5: e1370.
14. Andrews AJ, Luger K. Nucleosome structure(s) and stability: variations on a theme. Annu Rev Biophys 2011; 40: 99–117.
15. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403: 41–45.
16. Allam R, Scherbaum CR, Darisipudi MN, Mulay SR, Hägele H, Lichtnekert J et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 2012; 23: 1375–1388.
17. Huang H, Chen H-W, Evankovich J, Yan W, Rosborough BR, Nace GW et al. Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J Immunol 2013; 191: 2665–2679.
18. Allam R, Kumar SVR, Darisipudi MN, Anders H-J. Extracellular histones in tissue injury and inflammation. J Mol Med (Berl) 2014; 92: 465–472.
19. Abrams ST, Zhang N, Manson J, Liu T, Dart C, Baluwa F et al. Circulating histones are mediators of trauma-associated lung injury. Am J Respir Crit Care Med 2013; 187: 160–169.
20. Marsman G, Zeerleder S, Luken BM. Extracellular histones, cell-free DNA, or nucleosomes: differences in immunostimulation. Cell Death Dis 2016; 7: e2518.
21. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318–1321.
22. Gauthier VJ, Tyler LN, Mannik M. Blood clearance kinetics and liver uptake of mononucleosomes in mice. J Immunol 1996; 156: 1151–1156.
23. Holdenrieder S, Stieber P, Bodenmüller H, Busch M, Von Pawel J, Schalhorn A et al. Circulating nucleosomes in serum. Ann N Y Acad Sci 2001; 945: 93–102.
24. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE. Cell death. N Engl J Med 2009; 361: 1570–1583.
25. Klein B, Lütz-Meindl U, Kerschbaum HH. From the nucleus to the plasma membrane: translocation of the nuclear proteins histone H3 and lamin B1 in apoptotic microglia. Apoptosis 2014; 19: 759–775.
26. Wu D, Ingram A, Lahti JH, Mazza B, Grenet J, Kapoor A et al. Apoptotic release of histones from nucleosomes. J Biol Chem 2002; 277: 12001–12008.
27. Wickman GR, Julian L, Mardilovich K, Schumacher S, Munro J, Rath N et al. Blebs produced by actin-myosin contraction during apoptosis release damage-associated molecular pattern proteins before secondary necrosis occurs. Cell Death Differ 2013; 20: 1293–1305.
28. Remijsen Q, Vanden Berghe T, Wirawan E, Asselbergh B, Parthoens E, De Rycke R et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21: 290–304.
29. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009; 184: 205–213.
30. Papayannopoulos V, Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol 2009; 30: 513–521.
31. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532–1535.
32. von Köckritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M et al. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 2008; 111: 3070–3080.
33. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880–15885.
34. Kessenbrock K, Krumbholz M, Schönermarck U, Back W, Gross WL, Werb Z et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15: 623–625.
35. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012; 7: e32366.
36. Bosmann M, Grailer JJ, Ruemmler R, Russkamp NF, Zetoune FS, Sarma JV 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.
37. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012; 18: 1386–1393.
38. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463–469.
39. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008; 8: 279–289.
40. Ekaney ML, Otto GP, Sossdorf M, Sponholz C, Boehringer M, Loesche W et al. Impact of plasma histones in human sepsis and their contribution to cellular injury and inflammation. Crit Care 2014; 18: 543.
41. Johansson PI, Windeløv NA, Rasmussen LS, Sørensen AM, Ostrowski SR. Blood levels of histone-complexed DNA fragments are associated with coagulopathy, inflammation and endothelial damage early after trauma. J Emerg Trauma Shock 2013; 6: 171–175.
42. Kawai C, Kotani H, Miyao M, Ishida T, Jemail L, Abiru H et al. Circulating extracellular histones are clinically relevant mediators of multiple organ injury. Am J Pathol 2016; 186: 829–843.
43. Holdenrieder S, Nagel D, Schalhorn A, Heinemann V, Wilkowski R, von Pawel J et al. Clinical relevance of circulating nucleosomes in cancer. Ann N Y Acad Sci 2008; 1137: 180–189.
44. Hou W, Zhang Q, Yan Z, Chen R, Zeh Iii HJ, Kang R et al. Strange attractors: DAMPs and autophagy link tumor cell death and immunity. Cell Death Dis 2013; 4: e966.
45. Dwivedi N, Radic M. Citrullination of autoantigens implicates NETosis in the induction of autoimmunity. Ann Rheum Dis 2014; 73: 483–491.
46. Monach PA, Hueber W, Kessler B, Tomooka BH, BenBarak M, Simmons BP et al. A broad screen for targets of immune complexes decorating arthritic joints highlights deposition of nucleosomes in rheumatoid arthritis. Proc Natl Acad Sci USA 2009; 106: 15867–15872.
47. Pratesi F, Dioni I, Tommasi C, Alcaro MC, Paolini I, Barbetti F et al. Antibodies from patients with rheumatoid arthritis target citrullinated histone 4 contained in neutrophils extracellular traps. Ann Rheum Dis 2014; 73: 1414–1422.
48. Bosch X. Systemic lupus erythematosus and the neutrophil. N Engl J Med 2011; 365: 758–760.
49. Leffler J, Martin M, Gullstrand B, Tydén H, Lood C, Truedsson L et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 2012; 188: 3522–3531.
50. Migliorini A, Anders H-J. A novel pathogenetic concept-antiviral immunity in lupus nephritis. Nat Rev Nephrol 2012; 8: 183–189.
51. Duce JA, Smith DP, Blake RE, Crouch PJ, Li Q-X, Masters CL et al. Linker histone H1 binds to disease associated amyloid-like fibrils. J Mol Biol 2006; 361: 493–505.
52. Chaput C, Zychlinsky A. Sepsis: the dark side of histones. Nat Med 2009; 15: 1245–1246.
53. De Meyer SF, Suidan GL, Fuchs TA, Monestier M, Wagner DD. Extracellular chromatin is an important mediator of ischemic stroke in mice. Arterioscler Thromb Vasc Biol 2012; 32: 1884–1891.
54. Gilthorpe JD, Oozeer F, Nash J, Calvo M, Bennett DL, Lumsden A et al. Extracellular histone H1 is neurotoxic and drives a pro-inflammatory response in microglia. F1000Res 2013; 2: 148.
55. Vogel B, Shinagawa H, Hofmann U, Ertl G, Frantz S. Acute DNase1 treatment improves left ventricular remodeling after myocardial infarction by disruption of free chromatin. Basic Res Cardiol 2015; 110: 15.
56. Savchenko AS, Borissoff JI, Martinod K, De Meyer SF, Gallant M, Erpenbeck L et al. VWF-mediated leukocyte recruitment with chromatin decondensation by PAD4 increases myocardial ischemia/reperfusion injury in mice. Blood 2014; 123: 141–148.
57. Caudrillier A, Kessenbrock K, Gilliss BM, Nguyen JX, Marques MB, Monestier M et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122: 2661–2671.
58. Wen Z, Liu Y, Li F, Ren F, Chen D, Li X et al. Circulating histones exacerbate inflammation in mice with acute liver failure. J Cell Biochem 2013; 114: 2384–2391.
59. Huang H, Evankovich J, Yan W, Nace G, Zhang L, Ross M et al. Endogenous histones function as alarmins in sterile inflammatory liver injury through Toll-like receptor 9 in mice. Hepatology 2011; 54: 999–1008.
60. Huang H, Tohme S, Al-Khafaji AB, Tai S, Loughran P, Chen L et al. Damage-associated molecular pattern-activated neutrophil extracellular trap exacerbates sterile inflammatory liver injury. Hepatology 2015; 62: 600–614.
61. Ou X, Cheng Z, Liu T, Tang Z, Huang W, Szatmary P et al. Circulating histone levels reflect disease severity in animal models of acute pancreatitis. Pancreas 2015; 44: 1089–1095.
62. O’Neill LAJ, Golenbock D, Bowie AG. The history of Toll-like receptors-redefining innate immunity. Nat Rev Immunol 2013; 13: 453–460.
63. Tang D, Kang R, Coyne CB, Zeh HJ, Lotze MT. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 2012; 249: 158–175.
64. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4: 499–511.
65. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 2011; 118: 1952–1961.
66. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocyto-penia in mice. Blood 2011; 118: 3708–3714.
67. Yang X, Li L, Liu J, Lv B, Chen F. Extracellular histones induce tissue factor expression in vascular endothelial cells via TLR and activation of NF-κB and AP-1. Thromb Res 2016; 137: 211–218.
68. Leemans JC, Stokman G, Claessen N, Rouschop KM, Teske GJD, Kirschning CJ et al. Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest 2005; 115: 2894–2903.
69. Bamboat ZM, Balachandran VP, Ocuin LM, Obaid H, Plitas G, DeMatteo RP. Toll-like receptor 9 inhibition confers protection from liver ischemia-reperfusion injury. Hepatology 2010; 51: 621–632.
70. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature 2012; 481: 278–286.
71. Schroder K, Tschopp J. The inflammasomes. Cell 2010; 140: 821–832.
72. Pereira LF, Marco FM, Boimorto R, Caturla A, Bustos A, De la Concha EG et al. Histones interact with anionic phospholipids with high avidity; its relevance for the binding of histone-antihistone immune complexes. Clin Exp Immunol 1994; 97: 175–180.
73. Abrams ST, Zhang N, Dart C, Wang SS, Thachil J, Guan Y et al. Human CRP defends against the toxicity of circulating histones. J Immunol 2013; 191: 2495–2502.
74. Deb P, Sharma S, Hassan KM, Bakhai A, Heuschmann PU, Berger K et al. Pathophysiologic mechanisms of acute ischemic stroke: an overview with emphasis on therapeutic significance beyond thrombolysis. Pathophysiology 2010; 17: 197–218.
75. Geiger S, Holdenrieder S, Stieber P, Hamann GF, Bruening R, Ma J et al. Nucleosomes in serum of patients with early cerebral stroke. Cerebrovasc Dis 2006; 21: 32–37.
76. Geiger S, Holdenrieder S, Stieber P, Hamann GF, Bruening R, Ma J et al. Nucleosomes as a new prognostic marker in early cerebral stroke. J Neurol 2007; 254: 617–623.
77. Jickling GC, Liu D, Ander BP, Stamova B, Zhan X, Sharp FR. Targeting neutrophils in ischemic stroke: translational insights from experimental studies. J Cereb Blood Flow Metab 2015; 35: 888–901.
78. Bolton SJ, Russelakis-Carneiro M, Betmouni S, Perry VH. Non-nuclear histone H1 is upregulated in neurones and astrocytes in prion and Alzheimer’s diseases but not in acute neurodegeneration. Neuropathol Appl Neurobiol 1999; 25: 425–432.
79. Burke AP, Virmani R. Pathophysiology of acute myocardial infarction. Med Clin North Am 2007; 91: 553–572 ix.
80. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005; 353: 1685–1693.
81. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 2012; 122: 2731–2740.
82. Martin TR, Matute-Bello G. Experimental models and emerging hypotheses for acute lung injury. Crit Care Clin 2011; 27: 735–752.
83. Mishra B, von der Ohe M, Schulze C, Bian S, Makhina T, Loers G et al. Functional role of the interaction between polysialic acid and extracellular histone H1. J Neurosci 2010; 30: 12400–12413.
84. Ciesla DJ, Moore EE, Johnson JL, Burch JM, Cothren CC, Sauaia A. The role of the lung in postinjury multiple organ failure. Surgery 2005; 138: 749–57–8.
85. Martin AM, Soloway HB, Simmons RL. Pathologic anatomy of the lungs following shock and trauma. J Trauma 1968; 8: 687–699.
86. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389: 251–260.
87. Abakushin DN, Zamulaeva IA, Poverenny AM. Histones evoke thymocyte death in vitro; histone-binding immunoglobulins decrease their cytotoxicity. Biochemistry (Mosc) 1999; 64: 693–698.
88. Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost 2011; 9: 1795–1803.
89. Ganapathy V, Shyamala Devi CS. Effect of histone H1 on the cytosolic calcium levels in human breast cancer MCF 7 cells. Life Sci 2005; 76: 2631–2641.
90. Kleine TJ, Lewis PN, Lewis SA. Histone-induced damage of a mammalian epithelium: the role of protein and membrane structure. Am J Physiol Cell Physiol 1997; 273: C1925–C1936.
91. Akamatsu N, Sugawara Y, Kokudo N. Acute liver failure and liver transplantation. Intractable Rare Dis Res 2013; 2: 77–87.
92. Sharfuddin AA, Molitoris BA. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol 2011; 7: 189–200.
93. Kanagasundaram NS. Pathophysiology of ischaemic acute kidney injury. Ann Clin Biochem An Int J Biochem Lab Med 2015; 52: 193–205.
94. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011; 121: 4210–4221.
95. Rosin DL, Okusa MD. Dying cells and extracellular histones in AKI: beyond a NET effect? J Am Soc Nephrol 2012; 23: 1275–1277.
96. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM et al. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 2007; 117: 2847–2859.
97. Fernández-del Castillo C, Harringer W, Warshaw AL, Vlahakes GJ, Koski G, Zaslavsky AM et al. Risk factors for pancreatic cellular injury after cardiopulmonary bypass. N Engl J Med 1991; 325: 382–387.
98. Gullo L, Cavicchi L, Tomassetti P, Spagnolo C, Freyrie A, D’Addato M. Effects of ischemia on the human pancreas. Gastroenterology 1996; 111: 1033–1038.
99. Kang R, Zhang Q, Hou W, Yan Z, Chen R, Bonaroti J et al. Intracellular Hmgb1 inhibits inflammatory nucleosome release and limits acute pancreatitis in mice. Gastroenterology 2014; 146: 1097–1107.
100. Kang R, Lotze MT, Zeh HJ, Billiar TR, Tang D. Cell death and DAMPs in acute pancreatitis. Mol Med 2014; 20: 466–477.
101. Li Y, Liu Z, Liu B, Zhao T, Chong W, Wang Y et al. Citrullinated histone H3: a novel target for the treatment of sepsis. Surgery 2014; 156: 229–234.
102. Lewis HD, Liddle J, Coote JE, Atkinson SJ, Barker MD, Bax BD et al. Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation. Nat Chem Biol 2015; 11: 189–191.
103. Kolaczkowska E, Jenne CN, Surewaard BGJ, Thanabalasuriar A, Lee W-Y, Sanz M-J et al. Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat Commun 2015; 6: 6673.
104. Kutcher ME, Xu J, Vilardi RF, Ho C, Esmon CT, Cohen MJ. Extracellular histone release in response to traumatic injury: implications for a compensatory role of activated protein C. J Trauma Acute Care Surg 2012; 73: 1389–1394.
105. Martí-Carvajal AJ, Solà I, Lathyris D, Cardona AF. Human recombinant activated protein C for severe sepsis. Cochrane Database Syst Rev 2012; (3): CD004388.
106. Fernández JA, Xu X, Liu D, Zlokovic BV, Griffin JH. Recombinant murine-activated protein C is neuroprotective in a murine ischemic stroke model. Blood Cells Mol Dis 2003; 30: 271–276.