β2 glycoprotein i recognition drives Th1 inflammation in atherosclerotic plaques of patients with primary antiphospholipid syndrome

Journal of Immunology

Volumn 198, Issue 7, 2017, Pages 2640-2648

  Benagiano, Marisa ^a   Gerosa, Maria ^b   Romagnoli, Jacopo ^c   Mahler, Michael ^d   Borghi, Maria O ^b,e   Grassi, Alessia ^a   Della Bella, Chiara ^a   Emmi, Giacomo ^a   Amedei, Amedeo ^a,f   Silvestri, Elena ^a   Emmi, Lorenzo ^f   Prisco, Domenico ^a,f   Meroni, Pier Luigi ^b,e   D'Elios, Mario M ^a,f  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d INOVA DIAGNOSTICS INC   (United States)

^e Scientifico Istituto Auxologico Italiano   (Italy)

^f CAREGGI UNIVERSITY HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 GLYCOPROTEIN 1; FAS ANTIGEN; FAS LIGAND; GELATINASE B; PERFORIN; THROMBOPLASTIN;

ADULT; ANTIBODY PRODUCTION; ANTIPHOSPHOLIPID SYNDROME; ARTERY THROMBOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IN VIVO STUDY; INFLAMMATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC INFILTRATION; MALE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; T LYMPHOCYTE ACTIVATION; TH1 CELL; ATHEROSCLEROSIS; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY;

ADULT; ANTIPHOSPHOLIPID SYNDROME; ATHEROSCLEROSIS; BETA 2-GLYCOPROTEIN I; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; PLAQUE, ATHEROSCLEROTIC; TH1 CELLS;

EID: 85016258182     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600305     Document Type: Article

References (60)

1. Meroni, P. L., C. B. Chighizola, F. Rovelli, and M. Gerosa. 2014. Antiphospholipid syndrome in 2014: more clinical manifestations, novel pathogenic players and emerging biomarkers. Arthritis Res. Ther. 16: 209-225.
2. Hügli, R. W., D. Gremmelmaier, C. Jeanneret, C. Koella, A. W. Jehle, A. Tyndall, and B. C. Biedermann. 2011. Unusual vascular focal high-grade arterial stenoses in a young woman with systemic lupus erythematosus and secondary antiphospholipid syndrome. Lupus 20: 311-314.
3. Ames, P. R., A. Margarita, and J. D. Alves. 2009. Antiphospholipid antibodies and atherosclerosis: insights from systemic lupus erythematosus and primary antiphospholipid syndrome. Clin. Rev. Allergy Immunol. 37: 29-35.
4. Hollan, I., P. L. Meroni, J. M. Ahearn, J. W. Cohen Tervaert, S. Curran, C. S. Goodyear, K. A. Hestad, B. Kahaleh, M. Riggio, K. Shields, and M. C. Wasko. 2013. Cardiovascular disease in autoimmune rheumatic diseases. Autoimmun. Rev. 12: 1004-1015.
5. Ross, R. 1999. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340: 115-126.
6. Hansson, G. K., L. Jonasson, P. S. Seifert, and S. Stemme. 1989. Immune mechanisms in atherosclerosis. Arteriosclerosis 9: 567-578.
7. Benagiano, M., A. Azzurri, A. Ciervo, A. Amedei, C. Tamburini, M. Ferrari, J. L. Telford, C. T. Baldari, S. Romagnani, A. Cassone, et al. 2003. T helper type 1 lymphocytes drive inflammation in human atherosclerotic lesions. Proc. Natl. Acad. Sci. USA 100: 6658-6663.
8. Benagiano, M., F. Munari, A. Ciervo, A. Amedei, S. R. Paccani, F. Mancini, M. Ferrari, C. Della Bella, C. Ulivi, S. D'Elios, et al. 2012. Chlamydophila pneumoniae phospholipase D (CpPLD) drives Th17 inflammation in human atherosclerosis. Proc. Natl. Acad. Sci. USA 109: 1222-1227.
9. Wick, G., M. Knoflach, and Q. Xu. 2004. Autoimmune and inflammatory mechanisms in atherosclerosis. Annu. Rev. Immunol. 22: 361-403.
10. Stemme, S., B. Faber, J. Holm, O. Wiklund, J. L. Witztum, and G. K. Hansson. 1995. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 92: 3893-3897.
11. Benagiano, M., M. M. D'Elios, A. Amedei, A. Azzurri, R. van der Zee, A. Ciervo, G. Rombolà, S. Romagnani, A. Cassone, and G. Del Prete. 2005. Human 60-kDa heat shock protein is a target autoantigen of T cells derived from atherosclerotic plaques. J. Immunol. 174: 6509-6517.
12. George, J., D. Harats, B. Gilburd, A. Afek, Y. Levy, J. Schneiderman, I. Barshack, J. Kopolovic, and Y. Shoenfeld. 1999. Immunolocalization of b2-glycoprotein I (apolipoprotein H) to human atherosclerotic plaques: potential implications for lesion progression. Circulation 99: 2227-2230.
13. George, J., A. Afek, B. Gilburd, M. Blank, Y. Levy, A. Aron-Maor, H. Levkovitz, A. Shaish, I. Goldberg, J. Kopolovic, et al. 1998. Induction of early atherosclerosis in LDL-receptor-deficient mice immunized with b2-glycoprotein I. Circulation 98: 1108-1115.
14. Afek, A., J. George, Y. Shoenfeld, B. Gilburd, Y. Levy, A. Shaish, P. Keren, Z. Janackovic, I. Goldberg, J. Kopolovic, and D. Harats. 1999. Enhancement of atherosclerosis in b-2-glycoprotein I-immunized apolipoprotein E-deficient mice. Pathobiology 67: 19-25.
15. George, J., D. Harats, B. Gilburd, A. Afek, A. Shaish, J. Kopolovic, and Y. Shoenfeld. 2000. Adoptive transfer of b(2)-glycoprotein I-reactive lymphocytes enhances early atherosclerosis in LDL receptor-deficient mice. Circulation 102: 1822-1827.
16. Meroni, P. L., M. O. Borghi, E. Raschi, and F. Tedesco. 2011. Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat. Rev. Rheumatol. 7: 330-339.
17. Greco, T. P., A. M. Conti-Kelly, J. R. Anthony, T. Greco, Jr., R. Doyle, M. Boisen, K. Kojima, E. Matsuura, and J. R. Lopez. 2009. Oxidized-LDL/b2-glycoprotein I complexes are associated with disease severity and increased risk for adverse outcomes in patients with acute coronary syndromes. Am. J. Clin. Pathol. 133: 737-743.
18. Meroni, P. L., F. Peyvandi, L. Foco, L. Bernardinelli, R. Fetiveau, P. M. Mannucci, and A. Tincani. 2007. Anti-b 2 glycoprotein I antibodies and the risk of myocardial infarction in young premenopausal women. J. Thromb. Haemost. 5: 2421-2428.
19. Lim, W. 2014. Thrombotic risk in the antiphospholipid syndrome. Semin. Thromb. Hemost. 40: 741-746.
20. Steinkasserer, A., C. Estaller, E. H. Weiss, R. B. Sim, and A. J. Day. 1991. Complete nucleotide and deduced amino acid sequence of human b 2-glycoprotein I. Biochem. J. 277: 387-391.
21. Iverson, G. M., E. J. Victoria, and D. M. Marquis. 1998. Anti-b2 glycoprotein I (b2GPI) autoantibodies recognize an epitope on the first domain of b2GPI. Proc. Natl. Acad. Sci. USA 95: 15542-15546.
22. Miyakis, S., M. D. Lockshin, T. Atsumi, D. W. Branch, R. L. Brey, R. Cervera, R. H. Derksen, P. G. DE Groot, T. Koike, P. L. Meroni, et al. 2006. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J. Thromb. Haemost. 4: 295-306.
23. Chighizola, C. B., E. Raschi, A. Banzato, M. O. Borghi, V. Pengo, and P. L. Meroni. 2016. The challenges of lupus anticoagulants. Expert Rev. Hematol. 9: 389-400.
24. Pandya, J. M., A. C. Lundell, M. Hallström, K. Andersson, I. Nordström, and A. Rudin. 2016. Circulating T helper and T regulatory subsets in untreated early rheumatoid arthritis and healthy control subjects. J. Leukoc. Biol. 100: 823-833.
25. D'Elios, M. M., M. P. Bergman, A. Azzurri, A. Amedei, M. Benagiano, J. J. De Pont, F. Cianchi, C. M. Vandenbroucke-Grauls, S. Romagnani, B. J. Appelmelk, and G. Del Prete. 2001. H(+),K(+)-atpase (proton pump) is the target autoantigen of Th1-type cytotoxic T cells in autoimmune gastritis. Gastroenterology 120: 377-386.
26. Laczik, R., P. Szodoray, K. Veres, G. Lakos, S. Sipka, G. Szegedi, and P. Soltész. 2010. Oxidized LDL induces in vitro lymphocyte activation in antiphospholipid syndrome. Autoimmunity 43: 334-339.
27. Matsuura, E., L. R. Lopez, Y. Shoenfeld, and P. R. Ames. 2012. b2-glycoprotein I and oxidative inflammation in early atherogenesis: a progression from innate to adaptive immunity? Autoimmun. Rev. 12: 241-249.
28. D'Elios, M. M., R. Josien, M. Manghetti, A. Amedei, M. de Carli, M. C. Cuturi, G. Blancho, F. Buzelin, G. del Prete, and J. P. Soulillou. 1997. Predominant Th1 cell infiltration in acute rejection episodes of human kidney grafts. Kidney Int. 51: 1876-1884.
29. Maestrelli, P., G. F. Del Prete, M. De Carli, M. M. D'Elios, M. Saetta, A. Di Stefano, C. E. Mapp, S. Romagnani, and L. M. Fabbri. 1994. CD8 T-cell clones producing interleukin-5 and interferon-gamma in bronchial mucosa of patients with asthma induced by toluene diisocyanate. Scand. J. Work Environ. Health 20: 376-381.
30. de Carli, M., M. M. D'Elios, S. Mariotti, C. Marcocci, A. Pinchera, M. Ricci, S. Romagnani, and G. del Prete. 1993. Cytolytic T cells with Th1-like cytokine profile predominate in retroorbital lymphocytic infiltrates of Graves' ophthalmopathy. J. Clin. Endocrinol. Metab. 77: 1120-1124.
31. Maggi, E., M. G. Giudizi, R. Biagiotti, F. Annunziato, R. Manetti, M. P. Piccinni, P. Parronchi, S. Sampognaro, L. Giannarini, G. Zuccati, and S. Romagnani. 1994. Th2-like CD8+ T cells showing B cell helper function and reduced cytolytic activity in human immunodeficiency virus type 1 infection. J. Exp. Med. 180: 489-495.
32. Ito, H., S. Matsushita, Y. Tokano, H. Nishimura, Y. Tanaka, S. Fujisao, H. Mitsuya, H. Hashimoto, and Y. Nishimura. 2000. Analysis of T cell responses to the b 2-glycoprotein I-derived peptide library in patients with anti-b 2-glycoprotein I antibody-associated autoimmunity. Hum. Immunol. 61: 366-377.
33. Mahler, M., G. L. Norman, P. L. Meroni, and M. Khamashta. 2012. Autoantibodies to domain 1 of beta 2 glycoprotein 1: a promising candidate biomarker for risk management in antiphospholipid syndrome. Autoimmun. Rev. 12: 313-317.
34. Andreoli, L., M. Fredi, C. Nalli, S. Piantoni, R. Reggia, F. Dall'Ara, F. Franceschini, and A. Tincani. 2013. Clinical significance of IgA anticardiolipin and IgA anti-b2glycoprotein I antibodies. Curr. Rheumatol. Rep. 15: 343-351.
35. Kuwana, M. 2004. b2-glycoprotein I: antiphospholipid syndrome and T-cell reactivity. Thromb. Res. 114: 347-355.
36. Arai, T., K. Yoshida, J. Kaburaki, H. Inoko, Y. Ikeda, Y. Kawakami, and M. Kuwana. 2001. Autoreactive CD4(+) T-cell clones to b2-glycoprotein I in patients with antiphospholipid syndrome: preferential recognition of the major phospholipid-binding site. Blood 98: 1889-1896.
37. Matsuura, E., L. Shen, Y. Matsunami, N. Quan, M. Makarova, F. J. Geske, M. Boisen, S. Yasuda, K. Kobayashi, and L. R. Lopez. 2010. Pathophysiology of b2-glycoprotein I in antiphospholipid syndrome. Lupus 19: 379-384.
38. D'Elios, M. M., B. J. Appelmelk, A. Amedei, M. P. Bergman, and G. Del Prete. 2004. Gastric autoimmunity: the role of Helicobacter pylori and molecular mimicry. Trends Mol. Med. 10: 316-323.
39. Del Prete, G. F., M. De Carli, M. M. D'Elios, P. Maestrelli, M. Ricci, L. Fabbri, and S. Romagnani. 1993. Allergen exposure induces the activation of allergenspecific Th2 cells in the airway mucosa of patients with allergic respiratory disorders. Eur. J. Immunol. 23: 1445-1449.
40. D'Elios, M. M., P. Romagnani, C. Scaletti, F. Annunziato, M. Manghetti, C. Mavilia, P. Parronchi, C. Pupilli, G. Pizzolo, E. Maggi, et al. 1997. In vivo CD30 expression in human diseases with predominant activation of Th2-like T cells. J. Leukoc. Biol. 61: 539-544.
41. de Groot, P. G., and J. C. Meijers. 2011. b(2)-glycoprotein I: evolution, structure and function. J. Thromb. Haemost. 9: 1275-1284.
42. Agostinis, C., P. Durigutto, D. Sblattero, M. O. Borghi, C. Grossi, F. Guida, R. Bulla, P. Macor, F. Pregnolato, P. L. Meroni, and F. Tedesco. 2014. A noncomplement-fixing antibody to b2 glycoprotein I as a novel therapy for antiphospholipid syndrome. Blood 123: 3478-3487.
43. Amedei, A., F. Munari, C. D. Bella, E. Niccolai, M. Benagiano, L. Bencini, F. Cianchi, M. Farsi, G. Emmi, G. Zanotti, et al. 2014. Helicobacter pylori secreted peptidyl prolyl cis, trans-isomerase drives Th17 inflammation in gastric adenocarcinoma. Intern. Emerg. Med. 9: 303-309.
44. Codolo, G., A. Amedei, A. C. Steere, E. Papinutto, A. Cappon, A. Polenghi, M. Benagiano, S. R. Paccani, V. Sambri, G. Del Prete, et al. 2008. Borrelia burgdorferi NapA-driven Th17 cell inflammation in lyme arthritis. Arthritis Rheum. 58: 3609-3617.
45. D'Elios, M. M., A. Amedei, M. Manghetti, F. Costa, C. T. Baldari, A. S. Quazi, J. L. Telford, S. Romagnani, and G. Del Prete. 1999. Impaired T-cell regulation of B-cell growth in Helicobacter pylori-related gastric low-grade MALT lymphoma. Gastroenterology 117: 1105-1112.
46. Frostegard, J., A. K. Ulfgren, P. Nyberg, U. Hedin, J. Swedenborg, U. Andersson, and G. K. Hansson. 1999. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 145: 33-43.
47. Gupta, S., A. M. Pablo, Xc. Jiang, N. Wang, A. R. Tall, and C. Schindler. 1997. IFN-g potentiates atherosclerosis in ApoE knock-out mice. J. Clin. Invest. 99: 2752-2761.
48. Libby, P., and G. K. Hansson. 2015. Inflammation and immunity in diseases of the arterial tree: players and layers. Circ. Res. 116: 307-311.
49. Prat, A., K. Biernacki, B. Becher, and J. P. Antel. 2000. B7 expression and antigen presentation by human brain endothelial cells: requirement for proinflammatory cytokines. J. Neuropathol. Exp. Neurol. 59: 129-136.
50. Zadelaar, A. S., J. H. von der Thüsen, L. S. Boesten, R. C. Hoeben, M. M. Kockx, M. A. Versnel, T. J. van Berkel, L. M. Havekes, E. A. Biessen, and B. J. van Vlijmen. 2005. Increased vulnerability of pre-existing atherosclerosis in ApoE-deficient mice following adenovirus-mediated Fas ligand gene transfer. Atherosclerosis 183: 244-250.
51. Ketelhuth, D. F., and G. K. Hansson. 2016. Adaptive response of T and B cells in atherosclerosis. Circ. Res. 118: 668-678.
52. Kolodgie, F. D., J. Narula, A. P. Burke, N. Haider, A. Farb, Y. Hui-Liang, J. Smialek, and R. Virmani. 2000. Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death. Am. J. Pathol. 157: 1259-1268.
53. Geng, Y. J., L. E. Henderson, E. B. Levesque, M. Muszynski, and P. Libby. 1997. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 17: 2200-2208.
54. Boles, J., and N. Mackman. 2010. Role of tissue factor in thrombosis in antiphospholipid antibody syndrome. Lupus 19: 370-378.
55. Bäck, M., D. F. Ketelhuth, and S. Agewall. 2010. Matrix metalloproteinases in atherothrombosis. Prog. Cardiovasc. Dis. 52: 410-428.
56. Falk, E., P. K. Shah, and V. Fuster. 1995. Coronary plaque disruption. Circulation 92: 657-671.
57. Tsai, S. H., P. H. Huang, Y. J. Hsu, Y. J. Peng, C. H. Lee, J. C. Wang, J. W. Chen, and S. J. Lin. 2016. Inhibition of hypoxia inducible factor-1a attenuates abdominal aortic aneurysm progression through the down-regulation of matrix metalloproteinases. Sci. Rep. 6: 28612-28619.
58. Newby, A. C. 2016. Metalloproteinase production from macrophages - a perfect storm leading to atherosclerotic plaque rupture and myocardial infarction. Exp. Physiol. 101: 1327-1337.
59. Hansson, G. K., P. Libby, and I. Tabas. 2015. Inflammation and plaque vulnerability. J. Intern. Med. 278: 483-493.
60. Vinuesa, C. G., M. A. Linterman, D. Yu, and I. C. MacLennan. Follicular helper T cells. 2016. Annu. Rev. Immunol. 34: 335-368.