The role of cell death in the pathogenesis of autoimmune disease: HMGB1 and microparticles as intercellular mediators of inflammation

Modern Rheumatology

Volumn 18, Issue 4, 2008, Pages 319-326

  Ardoin, Stacy P ^a   Pisetsky, David S ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Autoimmunity; Cell death; HMBG1; Microparticles

Indexed keywords

CELL PROTEIN; CELL SURFACE PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; MICROPARTICLE PROTEIN;

AUTOIMMUNE DISEASE; CELL DEATH; CELL NUCLEUS; DISEASE ACTIVITY; HOMEOSTASIS; HUMAN; INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; VASCULARIZATION;

APOPTOSIS; AUTOIMMUNE DISEASES; CELL-DERIVED MICROPARTICLES; HUMANS; INFLAMMATION;

EID: 49149097163     PISSN: 14397595     EISSN: 14397609     Source Type: Journal    
DOI: 10.1007/s10165-008-0054-z     Document Type: Review

References (82)

1. Muller S, Ronfani L, Bianchi ME. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med. 2004;255:332-43.
2. Wen L, Huang JK, Johnson BH, Reeck GR. A human placental cDNA clone that encodes nonhistone chromosomal protein HMG-1. Nucleic Acids Res. 1989;17:1197-214.
3. Bianchi ME, Falciola L, Ferrari S, Lilley DM. The DNA binding site of HMG1 protein is composed of two similar segments (HMG boxes), both of which have counterparts in other eukaryotic regulatory proteins. EMGO J. 1992;11:1055-63.
4. Falciola L, Spada F, Calogero S, Langst G, Voit R, Grummt I, et al. High mobility group 1 protein is not stably associated with the chromosomes of somatic cells. J Cell Biol. 1997;137:19-26.
5. Jayaraman L, Moorthy NC, Murthy KG, Manley JL, Bustin M, Prives C. High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev. 1998;12:462-72.
6. Agresti A, Lupo R, Bianchi ME, Muller S. HMGB1 interacts differently with members of the Rel family of transcription factors. Biochem Biophys Res Commun. 2003;302:421-6.
7. Boonyaratanakornkit V, Melvin V, Prendergast P, Altmann M, Ronfani R, Bianchi ME, et al. High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol Cell Biol. 1998;18:4471-87.
8. Calogero S, Grassi F, Aguzzi A, Voigtländer T, Ferrier P, Ferrari S, et al. The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat Genet. 1999;22:276-80.
9. Daston MM, Ratner N. Expression of P30, a protein with adhesive properties, in Schwann cells and neurons of the developing and regenerating peripheral nerve. J Cell Biol. 1991;112:1229-39.
10. Debryse B, Bonaldi T, Scaffidi P, Muller S, Resnati M, Sanvito F, et al. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol. 2001;152:1197-206.
11. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, et al. Blockade of RAGE-amphoterin signaling suppresses tumor growth. Nature. 2000;405:354-60.
12. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med. 2000;192:565-70.
13. Zimmermann K, Volkel D, Pable S, Lindner T, Kramberger F, Bahrami S, et al. Native versus recombinant high-mobility group B1 proteins: functional activity in vitro. Inflammation. 2004;28:221-9.
14. Wang H, Visnubhakat JM, Bloom O, Zhang M, Ombrellino M, Sama A, Tracey KJ. Proinflammatory cytokines (tumor necrosis factor and interleukin 1) stimulate release of high mobility group protein-1 by pituicytes. Surgery. 1999;126:389-92.
15. Treutiger CJ, Mullins GE, Johansson AS, Rouhiainen A, Rauvala JME, Erlandsson-Harris H, et al. High mobility group 1 B-box mediates activation of human endothelium. J Intern Med. 2003;254:375-85.
16. Mullins GE, Sunden-Cullberg J, Johansson AS, Rouhiainen A, Errlandsson-Harris H, et al. Activation of human umbilical vein endothelial cells leads to relocation and release of high-mobility group box chromosomal protein 1. Scand J Immunol. 2004;60:566-73.
17. Messmer D, Yang H, Telusma G, Knoll F, Li J, Messmer B, et al. High mobility group box protein 1: An endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol. 2004;173:307-13.
18. Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol. 2007;81:59-66.
19. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med. 2004;83:876-86.
20. Kokkola R, Andersson A, Mullins G, Ostberg T, Treutiger CJ, Arnold B et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol. 2005;61:1-9.
21. Park JS, Svetkauskaite D, He Q, Kim HY, Strassheim D, Ishizaka A et al. Involvement of toll-like receptors 2 and 4 in the cellular activation by high mobility group box 1 protein. J Biol Chem. 2004;279:7370-7.
22. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim Jy, Strassheim D, et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol. 2006;290:C917-24.
23. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 2002;10:995-1001.
24. Youn JH, Shin JS. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol. 2006;177:7889-97.
25. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418:191-5.
26. Bell CW, Jiang W, Reich CF, Pisetsky DS. The extracellular release of HMGB1 during apoptotic cell death. J Physiol Cell Physiol. 2006;291:C1318-25.
27. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285:248-51.
28. Ueno H, Matsuda T, Hashimoto S, Amaya F, Kitamura Y, Tanaka M et al. Contributions of high mobility group box protein in experimental and clinical acute lung injury, Am J Respir Crit Care Med. 2004;170:1306-10.
29. Ellerman JE, Brown CK, de Vera M, Zeh HJ, Billiar T, Rubartelli A et al. Masquerader: High mobility group box-1 and cancer. Clin Cancer Res. 2007;13:2836-48.
30. Taira T, Matsuyama W, Mitsuyama H, Kawahara KI, Higashimoto I, Maruyama I et al. Increased serum high mobility box-1 level in Churg-Strauss syndrome. Clin Exp Immunol. 2007;148:241-7.
31. Ek M, Popovic K, Harris HE, Naucler CS, Wahren-Herlenius M. Increased extracellular levels of the novel proinflammatory cytokine high mobility group box chromosomal protein 1 in minor salivary glands of patients with Sjogren's syndrome. Arthritis Rheum. 2006;54:2289-94.
32. Sobajima J, Ozaki S, Uesugi H, Osakada F, Shirakawa H, Yoshida M et al. Prevalence and characterization of perinuclear anti-neutrophil cytoplasmic antibodies (P-ANCA) directed against HMG1 and HMG2 in ulcerative colitis (UC). Clin Exp Immunol. 1998;111:402-7.
33. Kokkola R, Sundberg E, Ulfgren AK, Palmblad K, Li J, Wang H et al. High mobility group box chromosomal protein 1: A novel proinflammatory mediator in synovitis. Arthritis Rheum. 2002;46:2598-603.
34. Taniguchi N, Kawahara K, Yone K, Hashiguchi T, Yamakuchi M, Goto M et al. High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum. 2003;48:971-81.
35. Pullertis R, Jonsson IM, Verdrengh M, Bokarewa M, Andersson U, Erlandsson-Harris H et al. High mobility group box chromosomal protein 1, a DNA binding cytokine, induces arthritis. Arthritis Rheum. 2003;48:1693-700.
36. Kokkola R, Li J, Sundberg E, Aveberger AC, Palmblad K, Yang H et al. Successful treatment of collagen-induced arthritis in mice and rats by targeting extracellular high mobility group box chromosomal protein 1 activity. Arthritis Rheum. 2003;48:2052-8.
37. Goldstein RS, Bruchfeld A, Yang L, Qureshi AR, Gallowitsch-Puerta M, Patel NB et al. Cholinergic anti-inflammatory pathway activity and high mobility group box-1 (HMGB1) serum levels in patients with rheumatoid arthritis. Mol Med. 2007;13:210-5.
38. Santoro P, De Andrea M, Migliaretti G, Trapani C, Landolfo S, Gariglio M. High prevalence of autoantibodies against the nuclear high mobility group (HMG) protein SSRP1 in sera from patients with systemic lupus erythematosus, but not other rheumatic diseases. J Rheumatol. 2002;29:90-3.
39. Wittemann B, Neuer G, Michels H, Truckenbrodt H, Bautz FA. Autoantibodies to nonhistone chromosomal proteins HMG-1 and HMG-2 in sera of patients with juvenile rheumatoid arthritis. Arthritis Rheum. 1990;33:1378-83.
40. Rosenberg AM, Cordeiro DM. Relationship between sex and antibodies to high mobility group proteins 1 and 2 in juvenile idiopathic arthritis. J Rheumatol. 2000;27:2489-93.
41. Popovic K, Ek M, Espinosa A, Padyukov L, Harris HE, Warhren-Herlenius M et al. Increased expression of the novel proinflammatory cytokine high mobility group box chromosomal protein 1 in skin lesions of patients with lupus erythematosus. Arthritis Rheum. 2005;52:3639-45.
42. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol. 2007;8:487-96.
43. Desai-Mehta A, Mao C, Rajagopalan S, Robinson T, Datta SK. Structure and specificity of T cell receptors expressed by potentially pathogenic anti-DNA autoantibody-inducing T cells in human lupus. J Clin Invest. 1995;95:531-41.
44. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13:269-88.
45. Distler JHW, Pisetsky DS, Huber LC, Kalden JR, Gay S, Distler O. Microparticles as regulators of inflammation. Arthritis Rheum. 2005;52:3337-48.
46. Fritzsching B, Schwer B, Kartenbeck J, Pedal A, Horejsi V, Ott M et al. Release and intercellular transfer of CD81 via microparticles. J Immunol. 2002;169:5531-7.
47. Barry OP, Pratico D, Savani RC, FitzGerald GA. Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest. 1998;102:136-44.
48. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: A mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000;6:769-75.
49. Gilbert GE, Sims PJ, Wiedmer T, Furie B, Furie BC, Shattil SJ. Platelet-derived microparticles express high affinity receptors for factor VIII. J Biol Chem. 1991;266:17261-8.
50. Hoffman M, Monroe DM, Roberts HR. Coagulation factor IXa binding to activated platelets and platelet-derived microparticles: A flow cytometric study. Thromb Haemost. 1992;68:74-8.
51. Michelson AD, Rajasekhar D, Bednarek FJ, Barnard MR. Platelet and platelet-derived microparticle surface factor V/Va binding in whole blood: Differences between neonates and adults. Thromb Haemost. 2000;84:689-94.
52. Sims PJ, Wiedmer T, Esmon CT, Weiss JH, Shattil SJ. Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: An isolated defect in platelet procoagulant activity. J Biol Chem. 1989;264:17049-57.
53. Vallar L, Regnault V, Latger-Cannard V, Lecompte T. Beta 2-glycoprotein I binding to platelet microparticle membrane specifically reduces immunoreactivity of glycoproteins IIb/IIIa. Thromb Haemost. 2001;85:314-219.
54. Nieuwland R, Berckmans RJ, McGregor S, Boing AN, Romijn FP, Westendorp RG et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood. 2000;95:930-5.
55. Jimenez JJ, Jy W, Mauro LM, Horstman LL, Yeon S, Ahn WH. Elevated endothelial microparticles in thrombotic thrombocytopenic purpura: findings from brain and microvascular cell culture and patients with active disease. Br J Haematol. 2001;112:81-90.
56. Shet AS, Aras O, Gupta K, Hass MJ, Rausch DJ, Saba N et al. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood. 2003;102:2678-83.
57. Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation. 1997;96:3534-41.
58. Bernal-Mizrachi L, Jy W, Jimenez JJ, Pastor J, Mauro LM, Horstman LL et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J. 2003;145:962-70.
59. Chirinos JA, Heresi GA, Velasquez H, Jy W, Jimenez JJ, Ahn E et al. Elevation of endothelial microparticles, platelets, and leukocyte activation in patients with venous thromboembolism. J Am Coll Cardiol. 2005;45:1467-71.
60. Hughes M, Hayward CP, Warkentin TE, Horsewood P, Chomeyko KA, Kelton JG. Morphological analysis of microparticle generation in heparin-induced thrombocytopenia. Blood. 2000;96:188-94.
61. Simak J, Holada K, Risitano AM, Zivny JH, Young NS, Vostal JG. Elevated circulating endothelial membrane microparticles in paroxysmal nocturnal haemoglobinuria. Br J Haematol. 2004;125:804-13.
62. Brogan PA, Shan V, Brachet C, Harnden A, Mant D, Klein N et al. Endothelial and platelet microparticles in vasculitis of the young. Arthritis Rheum. 2004;50:927-36.
63. Walenga JM, Jeske WP, Messmore HL. Mechanisms of venous and arterial thrombosis in heparin-induced thrombocytopenia. J Thromb Thrombolysis. 2000;10 Suppl 1:13-20.
64. Baj-Kryworzeka M, Majka M, Pratico D, Ratajczak J, Vilaire G, Kijowski J et al. Platelet-derived microparticles stimulate proliferation, survival, adhesion and chemotaxis of hematopoietic cells. Exp Hematol. 2002;30:450-9.
65. Forlow SB, McEver RP, Nollert MU. Leukocyte-leukocyte interactions mediated by platelet microparticles under flow. Blood. 2000;95:1317-23.
66. Barry OP, Pratico D, Lawson JA, Fitzgerald GA. Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles. J Clin Invest. 1997;99:2118-27.
67. Mackenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Suprenant A. Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 2001;15:825-35.
68. Distler JH, Huber LC, Reich CF III, Gay S, Distler O, Pisetsky DS. The release of microparticles by apoptotic cells and their effects on macrophages. Apoptosis. 2005;4:731-41.
69. Martinez MC, Tesse A, Zobairi F, Andrianstsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol. 2005;288:1004-9.
70. Horstman LL, Ahn YS. Platelet microparticles: A wide-angle perspective. Crit Rev Oncol Hematol. 1999;30:111-45.
71. Piccin A, Murphy W, Smith O. Circulating microparticles: Pathophysiology and clinical implications. Blood Rev. 2007;21:157-71.
72. Butikofer P, Kuypers FA, Xu CM, Chiu DT, Lubin B. Enrichment of two glycosyl-phosphatidylinositol-anchored proteins, acetylcholinesterase and decay accelerating factor, in vesicles released from human red blood cells. Blood. 1989;74:1481-5.
73. Mallat Z, Hugel B, Ohan J, Leseche G, Freyssinet JM, Tedgui A. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: A role for apoptosis in plaque thrombogenicity. Circulation. 1999;99:348-53.
74. Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion. 2006;46:1199-209.
75. Minagar A, Jy W, Jimenez JJ, Sheremata WA, Maura LM, Mao WW et al. Elevated plasma endothelial microparticles in multiple sclerosis. Neurology. 2001;56:1319-24.
76. Knijff-Dutmer EA, Koerts J, Nieuwland R, Kalsbeek-Batenburg EM, van de Laar MA. Elevated levels of platelet microparticles are associated with disease activity in rheumatoid arthritis. Arthritis Rheum. 2002;46:1498-503.
77. Berckmans RJ, Nieuwland R, Tak PP, Boing AN, Romijn FP, Kraan MC et al. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum. 2002;46:2857-66.
78. Distler JH, Jungel A, Huber LC, Seemayer CA, Reich CF 3rd, Gay RE et al. The induction of matrix metalloproteinase and cytokine expression in synovial fibroblasts stimulated with immune cell microparticles. Proc Natl Acad Sci USA. 2005;102:2892-7.
79. Joseph JE, Harrison P, Mackie IJ, Isenberg DA, Machin SJ. Increased circulating platelet-leucocyte complexes and platelet activation in patients with antiphospholipid syndrome, systemic lupus erythematosus and rheumatoid arthritis. Br J Haematol. 2001;115:451-9.
80. Jy W, Tiede M, Bidot CG, Horstman LL, Jimenez JJ, Chirinos J, et al. Platelet activation rather than endothelial injury identifies risk of thrombosis in subjects positive for antiphospholipid antibodies. Thromb Res 2007;121(3):319-25.
81. Dignat-George F, Camoin-Jau L, Sabatier F, Arnoux D, Anfosso F, Bardin N et al. Endothelial microparticles: A potential contribution to the thrombotic complications of the antiphospholipid antibody syndrome. Thromb Haemost. 2004;91:667-73.
82. Pereira J, Alfaro G, Goycoolea M, Quiroga T, Ocqueteau M, Massardo L, et al. Circulating platelet-derived microparticles in systemic lupus erythematosus: Association with increased thrombin generation and procoagulant state. Thromb Haemost. 2006;95:94-9.