Molecular mechanisms regulating immune responses in thromboangiitis obliterans: a comprehensive review

Document Type: Review Article

Authors

1 Immunology Research Group, Bu-Ali Research Institute, Mashhad University of Medical Sciences, Mashhad, Iran

2 Vascular and Endovascular Surgery Research Center, Alavi Hospital, Mashhad University of Medical Sciences, Iran

3 Neurogenic Inflammation Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

4 Department of Modern Sciences and Technologies, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

5 Immunology Research Group, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Thromboangiitis obliterans (TAO) is a thrombotic-occlusive as well as an inflammatory peripheral vascular disease with unknown etiology. Recent evidence has supported the immunopathogenesis of the disease, however, the factors contributing to the altered immune function and vascular tissue inflammation are still unclear. This review was intended to collate the more current knowledge on the regulatory molecules involved in TAO from an immunoreactive perspective. The homeostasis of the immune system as well as a variety of progenitor cell populations appear to be affected during TAO and these alterations are associated with intrinsic signaling defects that are directing to an improved understanding of the crosstalk between angiogenesis and the immune system, as well as the potential of new co-targeting strategies applying both immunotherapy and angiogenic therapy.

Keywords

Main Subjects


1. Lie JT, Mann RJ, Ludwig J. The brothers von Winiwarter, Alexander (1848-1917) and Felix (1852-1931), and thromboangiitis obliterans. Mayo Clin Proc 1979; 54:802-807.
2. Fazeli B, Modaghegh H, Ravrai H, Kazemzadeh G. Thrombophlebitis migrans as a footprint of Buerger’s disease: a prospective–descriptive study in north-east of Iran. Clin Rheumatol 2008; 27:55-57.
3. Hafezi S, Modaghegh MS. Sympathetic denervation using endovascular radiofrequency ablation in patients with thromboangiitis obliterans (Buerger’s disease). Ann Vasc Surg 2017; 45:336.
4. Modaghegh MH, Ravari H, Haghighi MZ, Rajabnejad A. Effect of folic acid therapy on homocysteine level in patients with atherosclerosis or Buerger’s disease and in healthy individuals: a clinical trial. Electron Physician 2016; 8:3138-3143.
5. Modaghegh MH, Kazemzadeh GH, Ravari H, Johari HG, Barzanuni A. Buerger’s disease in the northeast of Iran: Epidemiology and clinical features. Vascular 2015; 23:519-524.
6. Kobayashi M, Ito M, Nakagawa A, Nishikimi N, Nimura Y. Immunohistochemical analysis of arterial wall cellular infiltration in Buerger’s disease (endarteritis obliterans). J Vasc Surg 1999; 29:451-458.
7. Adar R, Papa MZ, Halpern Z, Mozes M, Shoshan S, Sofer B, et al. Cellular sensitivity to collagen in thromboangiitis obliterans. N Engl J Med 1983; 308:1113-1116.
8. Eichhorn J, Sima D, Llndschau C, Turowski A, Schmidt H, Schneider W, et al. Antiendothelial cell antibodies thromboangiitis obiiterans. Am J Med Sci 1998; 315:17-23.
9. Arslan C, Altan H, Beşirli K, Aydemir B, Kiziler AR, Denli Ş. The role of oxidative stress and antioxidant defenses in Buerger disease and atherosclerotic peripheral arterial occlusive disease. Ann Vasc Surg 2010; 24:455-460.
10. He J, Liu XY, Wang YP, Liu LB. Effects of oxidative stress on NF-κB, iNOS and NO in endothelial cells. J Fujian Med Univ 2010; 44:186-189.
11. Fazeli B, Rezaee SA. A review on thromboangiitis obliterans pathophysiology: thrombosis and angiitis, which is to blame? Vascular 2011; 19:141-153.
12. Hus I, Sokolowska B, Walter-Croneck A, Chrapko M, Nowaczynska A, Dmoszynska A. Assessment of plasma prothrombotic factors in patients with Buerger’s disease. Blood Coagul Fibrinolysis 2013; 24:133-139.
13. Csiszar A, Podlutsky A, Wolin MS, Losonczy G, Pacher P, Ungvari Z. Oxidative stress and accelerated vascular aging: implications for cigarette smoking. Front Biosci 2009; 14:3128-3144.
14. Nagata M. Inflammatory cells and oxygen radicals. Curr Drug Targets Inflamm Allergy 2005; 4:503-504.
15. Alamdari DH, Paletas K, Pegiou T, Sarigianni M, Befani C, Koliakos G. A novel assay for the evaluation of the prooxidant–antioxidant balance, before and after antioxidant vitamin administration in type II diabetes patients. Clin Biochem 2007; 40:248-254.
16. Glueck CJ, Haque M, Winarska M, Dharashivkar S, Fontaine RN, Zhu B, et al. Stromelysin-1 5A/6A and eNOS T-786C polymorphisms, MTHFR C677T and A1298C mutations, and cigarette-cannabis smoking: a pilot, hypothesis-generating study of gene-environment pathophysiological associations with Buerger’s disease. Clin Appl Thromb Hemost 2006; 12:427-439.
17. Stammler F, Diehm C, Hsu E, Stockinger K, Amendt K. [The prevalence of hyperhomocysteinemia in thromboangiitis obliterans. Does homocysteine play a role pathogenetically?]. Dtsch Med Wochenschr 1996; 121:1417-1423.
18. Akgul A, Bilgic A, Sezer S, Arat Z, Ozdemir FN, Haberal M. Low total plasma homocysteine level in relation to malnutrition, inflammation, and outcome in hemodialysis patients. J Ren Nutr 2008; 18:338-346.
19. Tyagi N, Sedoris KC, Steed M, Ovechkin AV, Moshal KS, Tyagi SC. Mechanisms of homocysteine-induced oxidative stress. Am J Physiol Heart Circ Physiol 2005; 289:H2649-H2656.
20. Barua RS, Ambrose JA, Srivastava S, DeVoe MC, Eales-Reynolds LJ. Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase. Circulation 2003; 107:2342-2347.
21. Brodmann M, Hafner F, Gary T, Seinost G, Pilger E. Impaired endothelial-dependent and endothelium-independent vasodilatation in patients with thromboangiitis obliterans. Clin Appl Thromb Hemost 2013; 19:33-36.
22. Ketha SS, Cooper LT. The role of autoimmunity in thromboangiitis obliterans (Buerger’s disease). Ann N Y Acad Sci 2013; 1285:15-25.
23. Kobayashi M, Sugimoto M, Komori K. Endarteritis obliterans in the pathogenesis of Buerger’s disease from the pathological and immunohistochemical points of view. Circ J 2014; 78:2819-2826.
24. Guo Y, Dai Y, Lai J, Fan Y. Study about correlation of anti-neutrophil cytoplasmic antibodies and anticardiolipin antibodies with thromboangiitis obliterans. Vascular 2013; 21:363-368.
25. Maslowski L, McBane R, Alexewicz P, Wysokinski WE. Antiphospholipid antibodies in thromboangiitis obliterans. Vasc Med 2002; 7:259-264.
26. Schenkein H, Berry C, Burmeister J, Brooks C, Barbour S, Best A, et al. Anti-cardiolipin antibodies in sera from patients with periodontitis. J Dent Res 2003; 82:919-922.
27. Kallenberg CG, Heeringa P, Stegeman CA. Mechanisms of disease: pathogenesis and treatment of ANCA-associated vasculitides. Nat Clin Pract Rheumatol 2006; 2:661-670.
28. Noel LH, Antineutrophil cytoplasm antibodies (ANCA): description and immunopathological role. Ann Med Interne; 2000; 151:178-183.
29. Savage CO. Pathogenesis of anti‐neutrophil cytoplasmic autoantibody (ANCA)‐associated vasculitis. Clin Exp Immunol 2011; 164:23-26.
30. Schultz DR, Diego JM, editors. Antineutrophil cytoplasmic antibodies (ANCA) and systemicvasculitis: update of assays, immunopathogenesis, controversies, and report of a novel de novo ANCA-associated vasculitis after kidney transplantation. Semin Arthritis Rheum 2000; 29:267-285.
31. Triplett DA. Antiphospholipid antibodies. Arch Pathol Lab Med 2002; 126:1424-1429.
32. Mulligan A, McAuley C. Thrombosis and psychosis--possible association with the antiphospholipid syndrome and anticardiolipin antibodies. Ir Med J 2009; 102:61.
33. Dragun D, Philippe A, Catar R, Hegner B. Autoimmune mediated G-protein receptor activation in cardiovascular and renal pathologies. Thromb Haemost 2009; 101:643-648.
34. Luft FC. Activating autoantibodies and cardiovascular disease. Physiology 2013; 28:254-261.
35. Walther T, Stepan H. Agonist autoantibodies against the angiotensin AT1 receptor in renal and hypertensive disorders. Curr Hypertens Rep 2007; 9:128-132.
36. Xia Y, Kellems RE. Receptor-activating autoantibodies and disease: preeclampsia and beyond. Expert Rev Clin Immunol 2011; 7:659-674.
37. Karczewski P, Haase H, Hempel P, Bimmler M. Agonistic antibody to the α1-adrenergic receptor mobilizes intracellular calcium and induces phosphorylation of a cardiac 15-kDa protein. Mol Cell Biochem 2010; 333:233-242.
38. Magnusson Y, Wallukat G, Waagstein F, Hjalmarson A, Hoebeke J. Autoimmunity in idiopathic dilated cardiomyopathy. Characterization of antibodies against the beta 1-adrenoceptor with positive chronotropic effect. Circulation 1994; 89:2760-2767.
39. Jahns R, Boivin V, Hein L, Triebel S, Angermann CE, Ertl G, et al. Direct evidence for a β1-adrenergic receptor–directed autoimmune attack as a cause of idiopathic dilated cardiomyopathy. J Clin Invest 2004; 113:1419-1429.
40. Wenzel K, Haase H, Wallukat G, Derer W, Bartel S, Homuth V, et al. Potential relevance of α1-adrenergic receptor autoantibodies in refractory hypertension. PloS One 2008; 3:e3742.
41. Zhou Z, Liao Y, Li L, Wei F, Wang B, Wei Y, et al. Vascular damages in rats immunized by α1-adrenoceptor peptides. Cell Mol Immunol 2008; 5:349-356.
42. Zhou Z, Liao Y-H, Wei Y, Wei F, Wang B, Li L, et al. Cardiac remodeling after long-term stimulation by antibodies against the α 1-adrenergic receptor in rats. Clin Immunol 2005; 114:164-173.
43. Klein-Weigel PF, Bimmler M, Hempel P, Schopp S, Dreusicke S, Valerius J, et al. G-protein coupled receptor auto-antibodies in thromboangiitis obliterans (Buerger’s disease) and their removal by immunoadsorption. Vasa 2014; 43:347-352.
44. Baumann G, Stangl V, Klein-Weigel P, Stangl K, Laule M, Enke-Melzer K. Successful treatment of thromboangiitis obliterans (Buerger’s disease) with immunoadsorption: results of a pilot study. Clin Res Cardiol 2011; 100:683-690.
45. Klein-Weigel P, Köning C, Härtwig A, Krüger K, Gutsche-Petrak B, Dreusicke S, et al. Immunoadsorption in thrombangiitis obliterans: a promising therapeutic option: results of a consecutive patient cohort treated in clinical routine care. Zentralbl Chir 2012; 137:460-465.
46. Chen YW, Iwai T, Umeda M, Nagasawa T, Huang Y, Takeuchi Y, et al. Elevated IgG titers to periodontal pathogens related to Buerger disease. Int J Cardiol 2007; 122:79-81.
47. Slavov E, Stanilova S, Petkov D, Dobreva Z. Cytokine production in thromboangiitis obliterans patients: new evidence for an immune-mediated inflammatory disorder. Clin Exp Rheumatol 2005; 23:219-226.
48. Czarnacki M, Zdrojowy K, Adamiec R. Review of current etiopathogenic data of Buerger disease. Pol Merkur Lekarski 2002; 13:263-265.
49. Kröger K, Kreuzfelder E, Moser C, Santosa F, Buss C, Grosse-Wilde H. Thrombangitis obliterans: subpopulationen der leukozyten und zirkulierende immunkomplexe. Vasa 2001; 30:189-194.
50. Zdrojowy K, Adamiec R, Czarnacki M. New aspects of prostaglandin E1 therapeutic influence in thrombo-angiitis obliterans. Pol Arch Med Wewn 2002; 108:1071-1077.
51. Halacheva K, Gulubova MV, Manolova I, Petkov D. Expression of ICAM-1, VCAM-1, E-selectin and TNF-α on the endothelium of femoral and iliac arteries in thromboangiitis obliterans. Acta Histochem 2002; 104:177-184.
52. Fazeli B, Rafatpanah H, Ravari H, Farid Hosseini R, Tavakol Afshari J, Valizadeh N, et al. Sera of patients with thromboangiitis obliterans activated cultured human umbilical vein endothelial cells (HUVECs) and changed their adhesive properties. Int J Rheum Dis 2014; 17:106-112.
53. Fazeli B, Rafatpanah H, Ravari H, Hosseini RF, Rezaee SR. Investigation of the expression of mediators of neovascularization from mononuclear leukocytes in thromboangiitis obliterans. Vascular 2014; 22:174-180.
54. Gulati S, Agarwal V, Sharma V, Saha K. C3 complement components & their breakdown product (C3d) in patients of thromboangiitis obliterans. Indian J Med Res 1986; 84:607-611.
55. Kim EJ, Cho BS, Lee TS, Kim SJ, Seo JW. Morphologic change of the lnternal elastic lamina in Buerger’s. J Korean Med Sci 2000; 15:44-48.
56. Lee T, Seo JW, Sumpio B, Kim S. Immunobiologic analysis of arterial tissue in Buerger’s disease. Eur J Vasc Endovasc Surg 2003; 25:451-457.
57. Buerger L. Landmark publication from the american journal of the medical sciences,’ thrombo-angiitis obliterans: a study of the vascular lesions leading to presenile spontaneous gangrene’. 1999. Am J Med Sci 2009; 337:274-284.
58. Brodmann M, Renner W, Seinost G, Pabst E. Genetic evaluation of the common variant of the endothelial nitric oxide synthase (Glu (298)-> Asp) in patients with thrombangiitis obliterans. Int Angiol 2002; 21:169-172.
59. Czarnacki M, Gacka M, Adamiec R. [A role of endothelin 1 in the pathogenesis of thromboangiitis obliterans (initital news)]. Przegl Lek 2004; 61:1346-1350.
60. Hoeft D, Kroger K, Grabbe S, Dissemond J. [Thrombangiitis obliterans: an overview]. J Dtsch Dermatol Ges 2004; 2:827-832.
61. Deng J, De S, He S, Chen B. [Correlation of expressions of ER and CD59 in Buerger disease]. Sichuan Da Xue Xue Bao Yi Xue Ban 2006; 37:427-429, 483.
62. Cui XM, Pan L, Cui L, Li Y, Zhao WG, Li ZB. Electron microscopic observation of immune complexes deposited in tunica media vasorum in patients with thromboangiitis obliterans. J Norman Bethune Univ Med Sci 2001; 27:379-381.
63. Dellalibera‐Joviliano R, Joviliano EE, Silva JSd, Evora PR. Activation of cytokines corroborate with development of inflammation and autoimmunity in thromboangiitis obliterans patients. Clin Exp Immunol 2012; 170:28-35.
64. Moussion C, Ortega N, Girard J-P. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel ‘alarmin’? PloS One 2008; 3:e3331.
65. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005; 23:479-490.
66. Chinese Clinical Trial Registry. Clinical Trial Registration NO. ChiCTR-CRC-17011428 (preliminary and unpublished data). ND.
67. Shoda T, Futamura K, Orihara K, Emi-Sugie M, Saito H, Matsumoto K, et al. Recent advances in understanding the roles of vascular endothelial cells in allergic inflammation. Allergol Int 2016; 65:21-29.
68. Azizi M, Boutouyrie P, Bura-Riviere A, Peyrard S, Laurent S, Fiessinger JN. Thromboangiitis obliterans and endothelial function. Eur J Clin Investig 2010; 40:518-526.
69. Joras M, Poredoš P, Fras Z. Endothelial dysfunction in Buerger’s disease and its relation to markers of inflammation. Eur J Clin Invest 2006; 36:376-382.
70. Makita S, Nakamura M, Murakami H, Komoda K, Kawazoe K, Hiramori K. Impaired endothelium-dependent vasorelaxation in peripheral vasculature of patients with thromboangiitis obliterans (Buerger’s disease). Circulation 1996; 94:(9 Suppl):211-215.
71. Stojkovic S, Kaun C, Basilio J, Rauscher S, Hell L, Krychtiuk KA, et al. Tissue factor is induced by interleukin-33 in human endothelial cells: a new link between coagulation and inflammation. Sci Rep 2016; 6:25171-25182.
72. Komai‐Koma M, Xu D, Li Y, McKenzie AN, McInnes IB, Liew FY. IL‐33 is a chemoattractant for human Th2 cells. Eur J Immunol 2007; 37:2779-2786.
73. Chalubinski M, Wojdan K, Luczak E, Gorzelak P, Borowiec M, Gajewski A, et al. IL-33 and IL-4 impair barrier functions of human vascular endothelium via different mechanisms. Vasc Pharmacol 2015; 73:57-63.
74. McLaren JE, Michael DR, Salter RC, Ashlin TG, Calder CJ, Miller AM, et al. IL-33 reduces macrophage foam cell formation. J Immunol 2010; 185:1222-1229.
75. Miller AM, Xu D, Asquith DL, Denby L, Li Y, Sattar N, et al. IL-33 reduces the development of atherosclerosis. J Exp Med 2008; 205:339-346.
76. Ashlin TG, Buckley ML, Salter RC, Johnson JL, Kwan AP, Ramji DP. The anti-atherogenic cytokine interleukin-33 inhibits the expression of a disintegrin and metalloproteinase with thrombospondin motifs-1,-4 and-5 in human macrophages: requirement of extracellular signal-regulated kinase, c-Jun N-terminal kinase and phosphoinositide 3-kinase signaling pathways. Int J Biochem Cell Biol 2014; 46:113-123.
77. Ali S, Huber M, Kollewe C, Bischoff SC, Falk W, Martin MU. IL-1 receptor accessory protein is essential for IL-33-induced activation of T lymphocytes and mast cells. Proc Natl Acad Sci 2007; 104:18660-18665.
78. Palmer G, Gabay C. Interleukin-33 biology with potential insights into human diseases. Nat Rev Rheumatol 2011; 7:321-329.
79. Kawai T, Akira S. TLR signaling. Cell Death Differ 2006; 13:816-825.
80. Chen Z, Nakajima T, Inoue Y, Kudo T, Jibiki M, Iwai T, et al. A single nucleotide polymorphism in the 3′-untranslated region of MyD88 gene is associated with Buerger disease but not with Takayasu arteritis in Japanese. J Hum Genet 2011; 56:545-547.
81. Pahwa R, Nallasamy P, Jialal I. Toll-like receptors 2 and 4 mediate hyperglycemia induced macrovascular aortic endothelial cell inflammation and perturbation of the endothelial glycocalyx. J Diabetes Complications 2016; 30:563-572.
82. Echavarria R, Mayaki D, Neel JC, Harel S, Sanchez V, Hussain SN. Angiopoietin-1 inhibits toll-like receptor 4 signalling in cultured endothelial cells: role of miR-146b-5p. Cardiovasc Res 2015; 106:465-477.
83. Aplin AC, Ligresti G, Fogel E, Zorzi P, Smith K, Nicosia RF. Regulation of angiogenesis, mural cell recruitment and adventitial macrophage behavior by Toll-like receptors. Angiogenesis 2014; 17:147-161.
84. Farzadnia M, Ravari H, Masoudian M, Valizadeh N, Fazeli B. Unexpected inflammation in the sympathetic ganglia in thromboangiitis obliterans. Int J Angiol 2017; 26:212-217.
85. McLachlan EM, Hu P. Inflammation in dorsal root ganglia after peripheral nerve injury: effects of the sympathetic innervation. Auton Neurosci 2014; 182:108-117.
86. Bradl M, Bauer J, Flügel A, Wekerle H, Lassmann H. Complementary contribution of CD4 and CD8 T lymphocytes to T-cell infiltration of the intact and the degenerative spinal cord. Am J Pathol 2005; 166:1441-1450.
87. Fehervari Z. Healing the CNS. Nat Immunol 2015; 16:228.
88. Yamada T, Harber P, Pettit GW, Wing DA, Oster CN. Activation of the kallikrein-kinin system in Rocky Mountain spotted fever. Ann Intern Med 1978; 88:764-768.
89. Dellalibera‐Joviliano R, Joviliano E, Évora P. Determination of kininogens levels and kallikrein/kininase II activities in patients with thromboangiitis obliterans. Scand J Immunol 2010; 72:128-133.
90. Hamza M, Wang XM, Adam A, Brahim JS, Rowan JS, Carmona GN, et al. Kinin B 1 receptors contributes to acute pain following minor surgery in humans. Mol Pain 2010; 6:12.
91. Mansueto P, Vitale G, Cascio A, Seidita A, Pepe I, Carroccio A, et al. New insight into immunity and immunopathology of Rickettsial diseases. Clin Dev Immunol 2012; 2012:967852.
92. Rathore MH. Rickettsial infection [Internet]. 2016 [cited 12 January 2018]. Available from: https://reference.medscape.com/article/968385-overview.
93. Puechal X, Fiessinger JN. Thromboangiitis obliterans or Buerger’s disease: challenges for the rheumatologist. Rheumatology 2007; 46:192-199.
94. Ashida S, Ishihara M, Ogawa H, Abiko Y. Protective effect of ticlopidine on experimentally induced peripheral arterial occlusive disease in rats. Thromb Res 1980; 18:55-67.
95. Nakata Y, Ban I, Hirai M, Shionoya S. Onset and clinicopathological course in Buerger’s disease. Angiology 1976; 27:509-517.
96. Nielubowicz J, Rosnowski A, Pruszynski B, Przetakiewicz Z, Potemkowski A. Natural history of Buerger’s disease. J Cardiovasc Surg 1980; 21:529-540.
97. Norregaard R, Kwon TH, Frokiaer J. Physiology and pathophysiology of cyclooxygenase-2 and prostaglandin E2 in the kidney. Kidney Res Clin Pract 2015; 34:194-200.
98. Ricciotti E, FitzGerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol 2011; 31:986-1000.
99. Fiessinger J, Schäfer M. Trial of iloprost versus aspirin treatment for critical limb ischaemia of thromboangiitis obliterans. Lancet 1990; 335:555-557.
100. Niźankowski R, Krolikowski W, Bielatowicz J, Szczeklik A. Prostacyclin for ischemic ulcers in peripheral arterial disease. A random assignment, placebo controlled study. Thromb Res 1985; 37:21-28.
101. Xu Y, Zhang R, Chen J, Zhang Q, Wang J, Hu J, et al. Urocortin promotes the development of vasculitis in a rat model of thromboangiitis obliterans via corticotrophin‐releasing factor type 1 receptors. Br J Pharmacol 2009; 157:1368-1379.
102. Zhang R, Xu Y, Fu H, Wang J, Jin L, Li S. Urocortin induced expression of COX‐2 and ICAM‐1 via corticotrophin‐releasing factor type 2 receptor in rat aortic endothelial cells. Br J Pharmacol 2009; 158:819-829.
103. Sahni SK, Rydkina E. Host-cell interactions with pathogenic Rickettsia species.  Future Microbiol 2009; 4:323-339.
104. Reinold H, Ahmadi S, Depner UB, Layh B, Heindl C, Hamza M, et al. Spinal inflammatory hyperalgesia is mediated by prostaglandin E receptors of the EP2 subtype. J Clin Invest 2005; 115:673-679.
105. Shireman PK. The chemokine system in arteriogenesis and hind limb ischemia. J Vasc Surg 2007; 45:A48-A56.
106. Funahashi Y, Shawber CJ, Vorontchikhina M, Sharma A, Outtz HH, Kitajewski J. Notch regulates the angiogenic response via induction of VEGFR-1. J Angiogenes Res 2010; 2:3.
107. Kimura T, Kohno H, Matsuoka Y, Murakami M, Nakatsuka R, Hase M, et al. CXCL8 enhances the angiogenic activity of umbilical cord blood‐derived outgrowth endothelial cells in vitro. Cell Biol Int 2011; 35:201-208.
108. Arenberg DA, Kunkel SL, Polverini PJ, Morris SB, Burdick MD, Glass MC, et al. Interferon-gamma-inducible protein 10 (IP-10) is an angiostatic factor that inhibits human non-small cell lung cancer (NSCLC) tumorigenesis and spontaneous metastases. J Exp Med 1996; 184:981-992.
109. Furuta S, Vadiveloo P, Romeo-Meeuw R, Morrison W, Stewart A, Mitchell G. Early inducible nitric oxide synthase 2 (NOS 2) activity enhances ischaemic skin flap survival. Angiogenesis 2004; 7:33-43.
110. Hristov M, Zernecke A, Liehn EA, Weber C. Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost 2007; 98:274-277.
111. Ringe J, Strassburg S, Neumann K, Endres M, Notter M, Burmester GR, et al. Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem 2007; 101:135-146.
112. Meyer M, Schreck R, Baeuerle PA. H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 1993; 12:2005-2015.
113. Park HS, Cho KH, Kim KL, Kim DK, Lee T. Reduced circulating endothelial progenitor cells in thromboangiitis obliterans (Buerger’s disease). Vasc Med 2013; 18:331-339.
114. Steer SA, Scarim AL, Chambers KT, Corbett JA. Interleukin-1 stimulates β-cell necrosis and release of the immunological adjuvant HMGB1. PLoS Med 2005; 3:e17.
115. Moscatelli D, Rifkin DB. Membrane and matrix localization of proteinases: a common theme in tumor cell invasion and angiogenesis. Biochim Biophys Acta 1988; 948:67-85.
116. Galis ZS, Sukhova GK, Lark MW, Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 1994; 94:2493-2503.
117. Matrisian LM. The matrix‐degrading metalloproteinases. Bioessays 1992; 14:455-463.
118. Dellalibera-Joviliano R, Jacob-Ferreira AL, Joviliano EE, Tanus-Santos JE, Évora PR. Imbalanced matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 activities in patients with thromboangiitis obliterans. Vasc Med 2012; 17:73-78.
119. Yongxin S, Wenjun D, Qiang W, Yunqing S, Liming Z, Chunsheng W. Heavy smoking before coronary surgical procedures affects the native matrix metalloproteinase-2 and matrix metalloproteinase-9 gene expression in saphenous vein conduits. Ann Thorac Surg 2013; 95:55-61.
120. De Caridi G, Bitto A, Massara M, Pallio G, Pizzino G, Serra R, et al. Increased serum HMGB-1, ICAM-1 and metalloproteinase-9 levels in Buerger’s patients. Curr Vasc Pharmacol 2016; 14:382-387.
121. Sun W, Jiao Y, Cui B, Gao X, Xia Y, Zhao Y. Immune complexes activate human endothelium involving the cell-signaling HMGB1-RAGE axis in the pathogenesis of lupus vasculitis. Lab Invest 2013; 93:626-638.
122. Bond M, Chase AJ, Baker AH, Newby AC. Inhibition of transcription factor NF-κB reduces matrix metalloproteinase-1,-3 and-9 production by vascular smooth muscle cells. Cardiovasc Res 2001; 50:556-565.
123. Hou CH, Fong YC, Tang CH. HMGB‐1 induces IL‐6 production in human synovial fibroblasts through c‐Src, Akt and NF‐κB pathways. J Cell Physiol 2011; 226:2006-2015.