Oxidative stress elicits platelet/leukocyte inflammatory interactions via HMGB1: A Candidate for microvessel injury in sytemic sclerosis

Antioxidants and Redox Signaling

Volumn 20, Issue 7, 2014, Pages 1060-1074

  Maugeri, Norma ^a   Rovere Querini, Patrizia ^a,b   Baldini, Mattia ^a   Baldissera, Elena ^a   Sabbadini, Maria Grazia ^a,b   Bianchi, Marco E ^a,b   Manfredi, Angelo A ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD18; BLOOD PLATELETS; FEMALE; HMGB1 PROTEIN; HUMANS; HYPERTENSION, PULMONARY; INFLAMMATION; LEUKOCYTES; MALE; MICROVESSELS; MIDDLE AGED; NEUTROPHILS; OXIDATION-REDUCTION; OXIDATIVE STRESS; P-SELECTIN; PLATELET ACTIVATION; REACTIVE OXYGEN SPECIES; SCLERODERMA, SYSTEMIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84894067273     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5298     Document Type: Article

References (84)

1. Andersson U and Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 29: 139-162, 2011.
2. Avouac J, Borderie D, Ekindjian OG, Kahan A, and Allanore Y. High DNA oxidative damage in systemic sclerosis. J Rheumatol 37: 2540-2547, 2010.
3. Barkalow FJ, Barkalow KL, and Mayadas TN. Dimerization of P-selectin in platelets and endothelial cells. Blood 96: 3070-3077, 2000.
4. Barnes TC, Anderson ME, Edwards SW, and Moots RJ. Neutrophil-derived reactive oxygen species in SSc. Rheumatology (Oxford) 51: 1166-1169, 2012.
5. Barnes TC, Spiller DG, Anderson ME, Edwards SW, and Moots RJ. Endothelial activation and apoptosis mediated by neutrophil-dependent interleukin 6 trans-signalling: A novel target for systemic sclerosis?. Ann Rheum Dis 70: 366-372, 2011.
6. Bauer EM, Shapiro R, Zheng H, Ahmad F, Ishizawar D, Comhair SA, Erzurum SC, Billiar TR, and Bauer PM. High mobility group box-1 contributes to the pathogenesis of experimental pulmonary hypertension via activation of tolllike receptor 4. Mol Med 18: 1509-1518, 2013.
7. Beals CR, Edwards AC, Gottschalk RJ, Kuijpers TW, and Staunton DE. CD18 activation epitopes induced by leukocyte activation. J Immunol 167: 6113-6122, 2001.
8. Bhattacharyya S, Wei J, and Varga J. Understanding fibrosis in systemic sclerosis: Shifting paradigms, emerging opportunities. Nat Rev Rheumatol 8: 42-54, 2012.
9. Bianchi ME and Manfredi AA. Immunology. Dangers in and out. Science 323: 1683-1684, 2009.
10. Campana L, Bosurgi L, Bianchi ME, Manfredi AA, and Rovere-Querini P. Requirement of HMGB1 for stromal cell-derived factor-1/CXCL12-dependent migration of macrophages and dendritic cells. J Leukoc Biol 86: 609-615, 2009.
11. Castellani P, Balza E, and Rubartelli A. Inflammation, DAMPs, tumor development, and progression: A vicious circle orchestrated by redox signaling. Antioxid Redox Signal 20: 1086-1097, 2014.
12. Castiglioni A, Canti V, Rovere-Querini P, and Manfredi AA. High-mobility group box 1 (HMGB1) as a master regulator of innate immunity. Cell Tissue Res 343: 189-199, 2011.
13. Cerinic MM, Valentini G, Sorano GG, D'Angelo S, Cuomo G, Fenu L, Generini S, Cinotti S, Morfini M, Pignone A, Guiducci S, Del Rosso A, Kalfin R, Das D, and Marongiu F. Blood coagulation, fibrinolysis, and markers of endothelial dysfunction in systemic sclerosis. Semin Arthritis Rheum 32: 285-295, 2003.
14. Chan JK, Roth J, Oppenheim JJ, Tracey KJ, Vogl T, Feldmann M, Horwood N, and Nanchahal J. Alarmins: Awaiting a clinical response. J Clin Invest 122: 2711-2719, 2012.
15. Chiba S, Baghdadi M, Akiba H, Yoshiyama H, Kinoshita I, Dosaka-Akita H, Fujioka Y, Ohba Y, Gorman JV, Colgan JD, Hirashima M, Uede T, Takaoka A, Yagita H, and Jinushi M. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol 13: 832-842, 2012.
16. Dees C, Akhmetshina A, Zerr P, Reich N, Palumbo K, Horn A, Jungel A, Beyer C, Kronke G, Zwerina J, Reiter R, Alenina N, Maroteaux L, Gay S, Schett G, Distler O, and Distler JH. Platelet-derived serotonin links vascular disease and tissue fibrosis. J Exp Med 208: 961-972, 2011.
17. Distler JH, Akhmetshina A, Dees C, Jungel A, Sturzl M, Gay S, Pisetsky DS, Schett G, and Distler O. Induction of apoptosis in circulating angiogenic cells by microparticles. Arthritis Rheum 63: 2067-2077, 2011.
18. Doeuvre L, Plawinski L, Goux D, Vivien D, and Angles-Cano E. Plasmin on adherent cells: From microvesiculation to apoptosis. Biochem J 432: 365-373, 2010.
19. Dumitriu IE, Baruah P, Valentinis B, Voll RE, Herrmann M, Nawroth PP, Arnold B, Bianchi ME, Manfredi AA, and Rovere-Querini P. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 174: 7506-7515, 2005.
20. Evangelista V, Manarini S, Dell'Elba G, Martelli N, Napoleone E, Di Santo A, and Lorenzet PS. Clopidogrel inhibits platelet-leukocyte adhesion and platelet-dependent leukocyte activation. Thromb Haemost 94: 568-577, 2005.
21. Evangelista V, Pamuklar Z, Piccoli A, Manarini S, Dell'Elba G, Pecce R, Martelli N, Federico L, Rojas M, Berton G, Lowell CA, Totani L, and Smyth SS. Src family kinases mediate neutrophil adhesion to adherent platelets. Blood 109: 2461-2469, 2007.
22. Fleming JN and Schwartz SM. The pathology of scleroderma vascular disease. Rheum Dis Clin North Am 34: 41-55; vi, 2008.
23. Fumagalli L, Campa CC, Germena G, Lowell CA, Hirsch E, and Berton G. Class I phosphoinositide-3-kinases and SRC kinases play a nonredundant role in regulation of adhesion-independent and-dependent neutrophil reactive oxygen species generation. J Immunol 190: 3648-3660, 2013.
24. Gabrielli A, Avvedimento EV, and Krieg T. Scleroderma. N Engl J Med 360: 1989-2003, 2009.
25. Gabrielli A, Svegliati S, Moroncini G, Pomponio G, Santillo M, and Avvedimento EV. Oxidative stress and the pathogenesis of scleroderma: The Murrell's hypothesis revisited. Semin Immunopathol 30: 329-337, 2008.
26. Ge WS, Wu JX, Fan JG, Wang YJ, and Chen YW. Inhibition of high-mobility group box 1 expression by siRNA in rat hepatic stellate cells. World J Gastroenterol 17: 4090-4098, 2011.
27. Guiducci S, Distler JH, Jungel A, Huscher D, Huber LC, Michel BA, Gay RE, Pisetsky DS, Gay S, Matucci-Cerinic M, and Distler O. The relationship between plasmamicroparticles and disease manifestations in patients with systemic sclerosis. Arthritis Rheum 58: 2845-2853, 2008.
28. Guiducci S, Distler O, Distler JH, and Matucci-Cerinic M. Mechanisms of vascular damage in SSc-implications for vascular treatment strategies. Rheumatology (Oxford) 47(Suppl 5): V18-v20, 2008.
29. Hamada N, Maeyama T, Kawaguchi T, Yoshimi M, Fukumoto J, Yamada M, Yamada S, Kuwano K, and Nakanishi Y. The role of high mobility group box1 in pulmonary fibrosis. Am J Respir Cell Mol Biol 39: 440-447, 2008.
30. Harris HE, Andersson U, and Pisetsky DS. HMGB1: A multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol 8: 195-202, 2012.
31. Hayakawa K, Miyamoto N, Seo JH, Pham LD, Kim KW, Lo EH, and Arai K. High-mobility group box 1 from reactive astrocytes enhances the accumulation of endothelial progenitor cells in damaged white matter. J Neurochem, 2012 [Epub ahead of print]; DOI: 10.1111/jnc.12120.
32. Hayakawa K, Pham LD, Katusic ZS, Arai K, and Lo EH. Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery. Proc Natl Acad Sci USA 109: 7505-7510, 2012.
33. Herrick AL. The pathogenesis, diagnosis and treatment of Raynaud phenomenon. Nat Rev Rheumatol 8: 469-479, 2012.
34. Hoppe G, Talcott KE, Bhattacharya SK, Crabb JW, and Sears JE. Molecular basis for the redox control of nuclear transport of the structural chromatin protein Hmgb1. Exp Cell Res 312: 3526-3538, 2006.
35. Janko C, Filipovic M, Munoz LE, Schorn C, Schett G, Ivanovic-Burmazovic I, and Herrmann M. Redox modulation of HMGB1-related signaling. Antioxid Redox Signal 20: 1075-1085, 2014.
36. Kahaleh B. Vascular disease in scleroderma: Mechanisms of vascular injury. Rheum Dis Clin North Am 34: 57-71; vi, 2008.
37. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, and Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of highmobility group box-1 protein. Immunity 29: 21-32, 2008.
38. Leemans JC, Butter LM, Pulskens WP, Teske GJ, Claessen N, van Der Poll T, and Florquin S. The role of Toll-like receptor 2 in inflammation and fibrosis during progressive renal injury. PLoS One 4: E5704, 2009.
39. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr., Rowell N, and Wollheim F. Scleroderma (systemic sclerosis): Classification, subsets and pathogenesis. J Rheumatol 15: 202-205, 1988.
40. LeRoy EC and Medsger TA Jr. Criteria for the classification of early systemic sclerosis. J Rheumatol 28: 1573-1576, 2001.
41. Manetti M, Guiducci S, Romano E, Ceccarelli C, Bellando-Randone S, Conforti ML, Ibba-Manneschi L, and Matucci-Cerinic M. Overexpression of VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, leads to insufficient angiogenesis in patients with systemic sclerosis. Circ Res 109: E14-e26, 2011.
42. Mattoscio D, Evangelista V, De Cristofaro R, Recchiuti A, Pandolfi A, Di Silvestre S, Manarini S, Martelli N, Rocca B, Petrucci G, Angelini DF, Battistini L, Robuffo I, Pensabene T, Pieroni L, Furnari ML, Pardo F, Quattrucci S, Lancellotti S, Davi G, and Romano M. Cystic fibrosis transmembrane conductance regulator (CFTR) expression in human platelets: Impact on mediators and mechanisms of the inflammatory response. FASEB J 24: 3970-3980, 2010.
43. Maugeri N, Baldini M, Rovere-Querini P, Maseri A, Sabbadini MG, and Manfredi AA. Leukocyte and platelet activation in patients with giant cell arteritis and polymyalgia rheumatica: A clue to thromboembolic risks?. Autoimmunity 42: 386-388, 2009.
44. Maugeri N, Franchini S, Campana L, Baldini M, Ramirez GA, Sabbadini MG, Rovere-Querini P, and Manfredi AA. Circulating platelets as a source of the damage-Associated molecular pattern HMGB1 in patients with systemic sclerosis. Autoimmunity 45: 584-587, 2012.
45. Maugeri N, Malato S, Femia EA, Pugliano M, Campana L, Lunghi F, Rovere-Querini P, Lussana F, Podda G, Cattaneo M, Ciceri F, and Manfredi AA. Clearance of circulating activated platelets in polycythemia vera and essential thrombocythemia. Blood 118: 3359-3366, 2011.
46. Maugeri N, Rovere-Querini P, Evangelista V, Covino C, Capobianco A, Bertilaccio MT, Piccoli A, Totani L, Cianflone D, Maseri A, and Manfredi AA. Neutrophils phagocytose activated platelets in vivo: A phosphatidylserine, P-selectin, and {beta}2 integrin-dependent cell clearance program. Blood 113: 5254-5265, 2009.
47. Maugeri N, Rovere-Querini P, Evangelista V, Godino C, Demetrio M, Baldini M, Figini F, Coppi G, Slavich M, Camera M, Bartorelli A, Marenzi G, Campana L, Baldissera E, Sabbadini MG, Cianflone D, Tremoli E, D'Angelo A, Manfredi AA, and Maseri A. An intense and short-lasting burst of neutrophil activation differentiates early acute myocardial infarction from systemic inflammatory syndromes. PLoS One 7: E39484, 2012.
48. Maugeri N, Rovere-Querini P, Slavich M, Coppi G, Doni A, Bottazzi B, Garlanda C, Cianflone D, Maseri A, Mantovani A, and Manfredi AA. Early and transient release of leukocyte pentraxin 3 during acute myocardial infarction. J Immunol 187: 970-979, 2011.
49. Moore KL, Varki A, and McEver RP. GMP-140 binds to a glycoprotein receptor on human neutrophils: Evidence for a lectin-like interaction. J Cell Biol 112: 491-499, 1991.
50. Murrell DF. A radical proposal for the pathogenesis of scleroderma. J Am Acad Dermatol 28: 78-85, 1993.
51. Oyabu C, Morinobu A, Sugiyama D, Saegusa J, Tanaka S, Morinobu S, Tsuji G, Kasagi S, Kawano S, and Kumagai S. Plasma platelet-derived microparticles in patients with connective tissue diseases. J Rheumatol 38: 680-684, 2011.
52. Pauling JD, O'Donnell VB, and McHugh NJ. The contribution of platelets to the pathogenesis of Raynaud's phenomenon and systemic sclerosis. Platelets 24: 503-515, 2013.
53. Pisetsky DS. The translocation of nuclear molecules during inflammation and cell death. Antioxid Redox Signal 20: 1117-1125, 2014.
54. Pisetsky DS, Gauley J, and Ullal AJ. HMGB1 and microparticles as mediators of the immune response to cell death. Antioxid Redox Signal 15: 2209-2219, 2011.
55. Pisetsky DS, Ullal AJ, Gauley J, and Ning TC. Microparticles as mediators and biomarkers of rheumatic disease. Rheumatology (Oxford) 51: 1737-1746, 2012.
56. Postlethwaite AE and Chiang TM. Platelet contributions to the pathogenesis of systemic sclerosis. Curr Opin Rheumatol 19: 574-579, 2007.
57. Ramirez GA, Franchini S, Rovere-Querini P, Sabbadini MG, Manfredi AA, and Maugeri N. The role of platelets in the pathogenesis of systemic sclerosis. Front Immunol 3: 160, 2012.
58. Ranzato E, Patrone M, Pedrazzi M, and Burlando B. Hmgb1 promotes wound healing of 3T3 mouse fibroblasts via RAGE-dependent ERK1/2 activation. Cell Biochem Biophys 57: 9-17, 2010.
59. Rigoulet M, Yoboue ED, and Devin A. Mitochondrial ROS generation and its regulation Mechanisms involved in H2O2 signaling. Antioxid Redox Signal 14: 459-468, 2011.
60. Rosen A, Casciola-Rosen L, and Wigley F. Role of metalcatalyzed oxidation reactions in the early pathogenesis of scleroderma. Curr Opin Rheumatol 9: 538-543, 1997.
61. Rossini A, Zacheo A, Mocini D, Totta P, Facchiano A, Castoldi R, Sordini P, Pompilio G, Abeni D, Capogrossi MC, and Germani A. HMGB1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J Mol Cell Cardiol 44: 683-693, 2008.
62. Rouhiainen A, Imai S, Rauvala H, and Parkkinen J. Occurrence of amphoterin (HMG1) as an endogenous protein of human platelets that is exported to the cell surface upon platelet activation. Thromb Haemost 84: 1087-1094, 2000.
63. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, Dumitriu IE, Muller S, Iannacone M, Traversari C, Bianchi ME, and Manfredi AA. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5: 825-830, 2004.
64. Rubartelli A and Lotze MT. Inside, outside, upside down: Damage-Associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol 28: 429-436, 2007.
65. Rubartelli A and Sitia R. Stress as an intercellular signal: The emergence of stress-Associated molecular patterns (SAMP). Antioxid Redox Signal 11: 2621-2629, 2009.
66. Saketkoo LA and Distler O. Is there evidence for vasculitis in systemic sclerosis?. Curr Rheumatol Rep 14: 516-525, 2012.
67. Schiraldi M, Raucci A, Munoz LM, Livoti E, Celona B, Venereau E, Apuzzo T, De Marchis F, Pedotti M, Bachi A, Thelen M, Varani L, Mellado M, Proudfoot A, Bianchi ME, and Uguccioni M. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med 209: 551-563, 2012.
68. Servettaz A, Kavian N, Nicco C, Deveaux V, Chereau C, Wang A, Zimmer A, Lotersztajn S, Weill B, and Batteux F. Targeting the cannabinoid pathway limits the development of fibrosis and autoimmunity in a mouse model of systemic sclerosis. Am J Pathol 177: 187-196, 2009.
69. Solanilla A, Villeneuve J, Auguste P, Hugues M, Alioum A, Lepreux S, Ducroix JP, Duhaut P, Conri C, Viallard JF, Nurden AT, Constans J, and Ripoche J. The transport of high amounts of vascular endothelial growth factor by blood platelets underlines their potential contribution in systemic sclerosis angiogenesis. Rheumatology (Oxford) 48: 1036-1044, 2009.
70. Tang D, Kang R, Zeh HJ 3rd, and Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal 14: 1315-1335, 2011.
71. Totani L, Piccoli A, Manarini S, Federico L, Pecce R, Martelli N, Cerletti C, Piccardoni P, Lowell CA, Smyth SS, Berton G, and Evangelista V. Src-family kinases mediate an outside-in signal necessary for beta2 integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leucocytes tethered on E-selectin. Biochem J 396: 89-98, 2006.
72. Trojanowska M. Cellular and molecular aspects of vascular dysfunction in systemic sclerosis. Nat Rev Rheumatol 6: 453-460, 2010.
73. Ushiyama S, Laue TM, Moore KL, Erickson HP, and McEver RP. Structural and functional characterization of monomeric soluble P-selectin and comparison with membrane P-selectin. J Biol Chem 268: 15229-15237, 1993.
74. van Beijnum JR, Nowak-Sliwinska P, van Den Boezem E, Hautvast P, Buurman WA, and Griffioen AW. Tumor angiogenesis is enforced by autocrine regulation of highmobility group box 1. Oncogene 32: 363-374, 2013.
75. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, Liu J, Antonelli A, Preti A, Raeli L, Shams SS, Yang H, Varani L, Andersson U, Tracey KJ, Bachi A, Uguccioni M, and Bianchi ME. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 209: 1519-1528, 2012.
76. Venereau E, Schiraldi M, Uguccioni M, and Bianchi ME. HMGB1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol 55: 76-82, 2013.
77. Vezzoli M, Castellani P, Campana L, Corna G, Bosurgi L, Manfredi AA, Bianchi ME, Rubartelli A, and Rovere-Querini P. Redox remodeling: A candidate regulator of HMGB1 function in injured skeletal muscle. Ann N Y Acad Sci 1209: 83-90, 2010.
78. Vezzoli M, Castellani P, Corna G, Castiglioni A, Bosurgi L, Monno A, Brunelli S, Manfredi AA, Rubartelli A, and Rovere-Querini P. High-mobility group box 1 release and redox regulation accompany regeneration and remodeling of skeletal muscle. Antioxid Redox Signal 15: 2161-2174, 2011.
79. Wahamaa H, Schierbeck H, Hreggvidsdottir HS, Palmblad K, Aveberger AC, Andersson U, and Harris HE. High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts. Arthritis Res Ther 13: R136, 2011.
80. Wigley FM. Vascular disease in scleroderma. Clin Rev Allergy Immunol 36: 150-175, 2009.
81. Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, Li J, Lu B, Chavan S, Rosas-Ballina M, Al-Abed Y, Akira S, Bierhaus A, Erlandsson-Harris H, Andersson U, and Tracey KJ. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci USA 107: 11942-11947, 2010.
82. Yang H, Lundback P, Ottosson L, Erlandsson-Harris H, Venereau E, Bianchi ME, Al-Abed Y, Andersson U, Tracey KJ, and Antoine DJ. Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol Med 18: 250-259, 2012.
83. Yoshizaki A, Komura K, Iwata Y, Ogawa F, Hara T, Muroi E, Takenaka M, Shimizu K, Hasegawa M, Fujimoto M, and Sato S. Clinical significance of serum HMGB-1 and sRAGE levels in systemic sclerosis: Association with disease severity. J Clin Immunol 29: 180-189, 2009.
84. Zarbock A, Kempf T, Wollert KC, and Vestweber D. Leukocyte integrin activation and deactivation: Novel mechanisms of balancing inflammation. J Mol Med (Berl) 90: 353-359, 2012.