Non-HLA antibodies against endothelial targets bridging allo- and autoimmunity

Kidney International

Volumn 90, Issue 2, 2016, Pages 280-288

  Dragun, Duska ^a,b   Catar, Rusan ^a,b   Philippe, Aurélie ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b BERLIN INSTITUTE OF HEALTH   (Germany)

Author keywords

acute rejection; angiotensin; endothelium; renin angiotensin system; signaling

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANTIBODY; COMPLEMENT COMPONENT C4D; ENDOTHELIN A RECEPTOR; ENDOTHELIN A RECEPTOR ANTAGONIST; EVEROLIMUS; G PROTEIN COUPLED RECEPTOR; HLA ANTIBODY; HLA ANTIGEN; PERLECAN; RAPAMYCIN; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; AUTOANTIBODY; IMMUNOSUPPRESSIVE AGENT; PROTEOHEPARAN SULFATE;

ALLOIMMUNITY; ANTIBODY MEDIATED REJECTION; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; DIABETIC NEPHROPATHY; ENDOCRINE DISEASE; ENDOTHELIUM CELL; FINGER ULCER; GRAFT FAILURE; HEART DISEASE; HLA SYSTEM; HUMAN; IMMUNOADSORPTION; IMMUNOSUPPRESSIVE TREATMENT; INTRACELLULAR SIGNALING; KIDNEY DISEASE; KIDNEY TRANSPLANTATION; MACROALBUMINURIA; NONHUMAN; ORGAN TRANSPLANTATION; PLASMAPHERESIS; PREECLAMPSIA; PRIORITY JOURNAL; PROTEOMICS; PULMONARY HYPERTENSION; RENAL GRAFT DYSFUNCTION; RENAL PROTECTION; REVIEW; STEM CELL TRANSPLANTATION; ADVERSE EFFECTS; ALLOTRANSPLANTATION; GRAFT REJECTION; GRAFT SURVIVAL; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; AUTOANTIBODIES; AUTOIMMUNITY; ENDOTHELIAL CELLS; ENDOTHELIN A RECEPTOR ANTAGONISTS; GRAFT REJECTION; GRAFT SURVIVAL; HEPARAN SULFATE PROTEOGLYCANS; HLA ANTIGENS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, HUMORAL; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION; PLASMAPHERESIS; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ENDOTHELIN A; TRANSPLANTATION, HOMOLOGOUS;

EID: 84992476922     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2016.03.019     Document Type: Review

References (93)

1. 1 Halloran, P.F., Reeve, J.P., Pereira, A.B., et al. Antibody-mediated rejection, T cell-mediated rejection, and the injury-repair response: new insights from the Genome Canada studies of kidney transplant biopsies. Kidney Int 85 (2014), 258–264.
2. 2 Abrahimi, P., Liu, R., Pober, J.S., Blood vessels in allotransplantation. Am J Transplant 15 (2015), 1748–1754.
3. 3 Loupy, A., Vernerey, D., Viglietti, D., et al. Determinants and outcomes of accelerated arteriosclerosis: major impact of circulating antibodies. Circ Res 117 (2015), 470–482.
4. 4 Sis, B., Jhangri, G.S., Bunnag, S., et al. Endothelial gene expression in kidney transplants with alloantibody indicates antibody-mediated damage despite lack of C4d staining. Am J Transplant 9 (2009), 2312–2323.
5. 5 Jiang, X., Sung, Y.K., Tian, W., et al. Graft microvascular disease in solid organ transplantation. J Mol Med 92 (2014), 797–810.
6. 6 Haas, M., Sis, B., Racusen, L.C., et al. Banff 2013 meeting report: inclusion of c4d-negative antibody-mediated rejection and antibody-associated arterial lesions. Am J Transplant 14 (2014), 272–283.
7. 7 Aird, W.C., Proximate and evolutionary causation of endothelial heterogeneity. Semin Thromb Hemost 36 (2010), 276–285.
8. 8 Aird, W.C., Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 100 (2007), 174–190.
9. 9 Aird, W.C., Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 100 (2007), 158–173.
10. 10 Muczynski, K.A., Ekle, D.M., Coder, D.M., et al. Normal human kidney HLA-DR-expressing renal microvascular endothelial cells: characterization, isolation, and regulation of MHC class II expression. J Am Socf Nephrol 14 (2003), 1336–1348.
11. 11 Collins, T., Korman, A.J., Wake, C.T., et al. Immune interferon activates multiple class II major histocompatibility complex genes and the associated invariant chain gene in human endothelial cells and dermal fibroblasts. Proc Natl Acad Sci U S A 81 (1984), 4917–4921.
12. 12 Geppert, T.D., Lipsky, P.E., Antigen presentation by interferon-gamma-treated endothelial cells and fibroblasts: differential ability to function as antigen-presenting cells despite comparable Ia expression. J Immunol 135 (1985), 3750–3762.
13. 13 Cresci, B., Giannini, S., Pala, L., et al. AT1 and AT2 receptors in human glomerular endothelial cells at different passages. Microvasc Res 66 (2003), 22–29.
14. 14 Davenport, A.P., Kuc, R.E., Hoskins, S.L., et al. [125I]-PD151242: a selective ligand for endothelin ETA receptors in human kidney which localizes to renal vasculature. Br J Pharmacol 113 (1994), 1303–1310.
15. 15 Yamani, M.H., Cook, D.J., Tuzcu, E.M., et al. Systemic up-regulation of angiotensin II type 1 receptor in cardiac donors with spontaneous intracerebral hemorrhage. Am J Transplant 4 (2004), 1097–1102.
16. 16 Remuzzi, G., Perico, N., Cyclosporine-induced renal dysfunction in experimental animals and humans. Kidney Int 52:Suppl (1995), S70–S74.
17. 17 Praprotnik, S., Blank, M., Meroni, P.L., et al. Classification of anti-endothelial cell antibodies into antibodies against microvascular and macrovascular endothelial cells: the pathogenic and diagnostic implications. Arthritis Rheum 44 (2001), 1484–1494.
18. 18 Sun, Q., Cheng, Z., Cheng, D., et al. De novo development of circulating anti-endothelial cell antibodies rather than pre-existing antibodies is associated with post-transplant allograft rejection. Kidney Int 79 (2011), 655–662.
19. 19 Breimer, M.E., Rydberg, L., Jackson, A.M., et al. Multicenter evaluation of a novel endothelial cell crossmatch test in kidney transplantation. Transplantation 87 (2009), 549–556.
20. 20 Jackson, A.M., Sigdel, T.K., Delville, M., et al. Endothelial cell antibodies associated with novel targets and increased rejection. J Am Soc Nephrol 26 (2015), 1161–1171.
21. 21 Canet, E., Devalliere, J., Gerard, N., et al. Profiling posttransplant circulating antibodies in kidney transplantation using donor endothelial cells. Transplantation 93 (2012), 257–264.
22. 22 Venkatakrishnan, A.J., Deupi, X., Lebon, G., et al. Molecular signatures of G-protein-coupled receptors. Nature 494 (2013), 185–194.
23. 23 Ruster, C., Wolf, G., Angiotensin II as a morphogenic cytokine stimulating renal fibrogenesis. J Am Soc Nephrol 22 (2011), 1189–1199.
24. 24 Boesen, E.I., Endothelin receptors, renal effects and blood pressure. Curr Opin Pharmacol 21 (2015), 25–34.
25. 25 Dragun, D., Muller, D.N., Brasen, J.H., et al. Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N Engl J Med 352 (2005), 558–569.
26. 26 Zhang, H., Unal, H., Gati, C., et al. Structure of the Angiotensin receptor revealed by serial femtosecond crystallography. Cell 161 (2015), 833–844.
27. 27 Dragun, D., Catar, R., Kusch, A., et al. Non-HLA-antibodies targeting Angiotensin type 1 receptor and antibody mediated rejection. Hum Immunol 73 (2012), 1282–1286.
28. 28 Chen, D., Weber, M., McVey, J.H., et al. Complete inhibition of acute humoral rejection using regulated expression of membrane-tethered anticoagulants on xenograft endothelium. Am J Transplant 4 (2004), 1958–1963.
29. 29 Branch, D.W., Rodgers, G.M., Induction of endothelial cell tissue factor activity by sera from patients with antiphospholipid syndrome: a possible mechanism of thrombosis. Am J Obstet Gynecol 168 (1993), 206–210.
30. 30 Reinsmoen, N.L., Lai, C.H., Heidecke, H., et al. Anti-angiotensin type 1 receptor antibodies associated with antibody mediated rejection in donor HLA antibody negative patients. Transplantation 90 (2010), 1473–1477.
31. 31 Giral, M., Foucher, Y., Dufay, A., et al. Pretransplant sensitization against angiotensin II type 1 receptor is a risk factor for acute rejection and graft loss. Am J Transplant 13 (2013), 2567–2576.
32. 32 Lee, J., Huh, K.H., Park, Y., et al. The clinicopathological relevance of pretransplant anti-angiotensin II type 1 receptor antibodies in renal transplantation [e-pub ahead of print]. Nephrol Dial Transpl, 2015 accessed November 5, 2015.
33. 33 Fuss, A., Hope, C.M., Deayton, S., et al. C4d-negative antibody-mediated rejection with high anti-angiotensin II type I receptor antibodies in absence of donor-specific antibodies. Nephrology 20 (2015), 467–473.
34. 34 Taniguchi, M., Rebellato, L.M., Cai, J., et al. Higher risk of kidney graft failure in the presence of anti-angiotensin II type-1 receptor antibodies. Am J Transplant 13 (2013), 2577–2589.
35. 35 Alachkar, N., Gupta, G., Montgomery, R.A., Angiotensin antibodies and focal segmental glomerulosclerosis. N Engl J Med 368 (2013), 971–973.
36. 36 Mujtaba, M.A., Sharfuddin, A.A., Book, B.L., et al. Pre-transplant angiotensin receptor II type 1 antibodies and risk of post-transplant focal segmental glomerulosclerosis recurrence. Clin Transplant 29 (2015), 606–611.
37. 37 Reinsmoen, N.L., Lai, C.H., Mirocha, J., et al. Increased negative impact of donor HLA-specific together with non-HLA-specific antibodies on graft outcome. Transplantation 97 (2014), 595–601.
38. 38 Kelsch, R., Everding, A.S., Kuwertz-Broking, E., et al. Accelerated kidney transplant rejection and hypertensive encephalopathy in a pediatric patient associated with antibodies against angiotensin type 1 receptor and HLA class II. Transplantation 92 (2011), e57–e59.
39. 39 Banasik, M., Boratynska, M., Koscielska-Kasprzak, K., et al. The influence of non-HLA antibodies directed against angiotensin II type 1 receptor (AT1R) on early renal transplant outcomes. Transpl Int 27 (2014), 1029–1038.
40. 40 Banasik, M., Boratynska, M., Koscielska-Kasprzak, K., et al. Non-HLA antibodies: angiotensin II type 1 receptor (anti-AT1R) and endothelin-1 type A receptor (anti-ETAR) are associated with renal allograft injury and graft loss. Transplant Proc 46 (2014), 2618–2621.
41. 41 Banasik, M., Boratynska, M., Koscielska-Kasprzak, K., et al. Long-term follow-up of non-HLA and anti-HLA antibodies: incidence and importance in renal transplantation. Transplant Proc 45 (2013), 1462–1465.
42. 42 Hernández-Mendez, E.A., Arreola-Guerra, J.M., Morales-Buenrostro, L.E., et al. Pre-transplant angiotensin II type 1receptor antibodies: a risk factor for decreased kidney graft function in the early post-transplant period?. Rev Invest Clin 66 (2014), 218–224.
43. 43 In, J.W., Park, H., Rho, E.Y., et al. Anti-angiotensin type 1 receptor antibodies associated with antibody-mediated rejection in patients without preformed HLA-donor-specific antibody. Transplant Proc 46 (2014), 3371–3374.
44. 44 Jobert, A., Rao, N., Deayton, S., et al. Angiotensin II type 1 receptor antibody precipitating acute vascular rejection in kidney transplantation. Nephrology 20:Suppl 1 (2015), 10–12.
45. 45 Hiemann, N.E., Meyer, R., Wellnhofer, E., et al. Non-HLA antibodies targeting vascular receptors enhance alloimmune response and microvasculopathy after heart transplantation. Transplantation 94 (2012), 919–924.
46. 46 Kem, D.C., Li, H., Velarde-Miranda, C., et al. Autoimmune mechanisms activating the angiotensin AT1 receptor in ‘primary’ aldosteronism. J Clin Endocrinol Metab 99 (2014), 1790–1797.
47. 47 Li, H., Yu, X., Cicala, M.V., et al. Prevalence of angiotensin II type 1 receptor (AT1R)-activating autoantibodies in primary aldosteronism. J Am Soc Hypertens 9 (2015), 15–20.
48. 48 Rossitto, G., Regolisti, G., Rossi, E., et al. Elevation of angiotensin-II type-1-receptor autoantibodies titer in primary aldosteronism as a result of aldosterone-producing adenoma. Hypertension 61 (2013), 526–533.
49. 49 Riemekasten, G., Philippe, A., Nather, M., et al. Involvement of functional autoantibodies against vascular receptors in systemic sclerosis. Ann Rheum Dis 70 (2011), 530–536.
50. 50 Becker, M.O., Kill, A., Kutsche, M., et al. Vascular receptor autoantibodies in pulmonary arterial hypertension associated with systemic sclerosis. Am J Respir Crit Care Med 190 (2014), 808–817.
51. 51 Banasik, M., Boratynska, M., Koscielska-Kasprzak, K., et al. The impact of non-HLA antibodies directed against endothelin-1 type A receptors (ETAR) on early renal transplant outcomes. Transplant Immunol 30 (2014), 24–29.
52. 52 Cardinal, H., Dieude, M., Brassard, N., et al. Antiperlecan antibodies are novel accelerators of immune-mediated vascular injury. Am J Transplant 13 (2013), 861–874.
53. 53 Xia, Y., Kellems, R.E., Angiotensin receptor agonistic autoantibodies and hypertension: preeclampsia and beyond. Circ Res 113 (2013), 78–87.
54. 54 Ohe, H., Uchida, Y., Yoshizawa, A., et al. Association of anti-human leukocyte antigen and anti-angiotensin II type 1 receptor antibodies with liver allograft fibrosis after immunosuppression withdrawal. Transplantation 98 (2014), 1105–1111.
55. 55 Banasik, M., Jablecki, J., Boratynska, M., et al. Humoral immunity in hand transplantation: anti-HLA and non-HLA response. Hum Immunol 75 (2014), 859–862.
56. 56 Budding, K., van de Graaf, E.A., Hoefnagel, T., et al. Anti-ETAR and anti-AT1R autoantibodies are elevated in patients with endstage cystic fibrosis. J Cyst Fibros 14 (2015), 42–45.
57. 57 Chiron, A., Bouaziz, J.D., Carmagnat, M., et al. Anti-Angiotensin type 1 receptor antibodies in chronic graft-versus-host disease. Transplantation 98 (2014), 470–474.
58. 58 Gunther, J., Kill, A., Becker, M.O., et al. Angiotensin receptor type 1 and endothelin receptor type A on immune cells mediate migration and the expression of IL-8 and CCL18 when stimulated by autoantibodies from systemic sclerosis patients. Arthritis Res Ther, 16, 2014, R65.
59. 59 Kill, A., Tabeling, C., Undeutsch, R., et al. Autoantibodies to angiotensin and endothelin receptors in systemic sclerosis induce cellular and systemic events associated with disease pathogenesis. Arthritis Res Ther, 16, 2014, R29.
60. 60 Guo, L., Li, M., Chen, Y., et al. Anti-endothelin receptor type A autoantibodies in systemic lupus erythematosus-associated pulmonary arterial hypertension. Arthritis Rheumatol 67 (2015), 2394–2402.
61. 61 Klein-Weigel, P.F., Bimmler, M., Hempel, P., et al. G-protein coupled receptor auto-antibodies in thromboangiitis obliterans (Buerger's disease) and their removal by immunoadsorption. Vasa 43 (2014), 347–352.
62. 62 Albert, C., von Schultzendorff, M., Salaru, D., et al. In arterial occlusive disease autoantibodies against ETAR and AT(1)R correlate with each other but are not associated with classical cardiovascular risk factors. Vasa 43 (2014), 113–123.
63. 63 Lukitsch, I., Kehr, J., Chaykovska, L., et al. Renal ischemia and transplantation predispose to vascular constriction mediated by angiotensin II type 1 receptor-activating antibodies. Transplantation 94 (2012), 8–13.
64. 64 Davis, G.E., Matricryptic sites control tissue injury responses in the cardiovascular system: relationships to pattern recognition receptor regulated events. J Mol Cell Cardiol 48 (2010), 454–460.
65. 65 Soulez, M., Sirois, I., Brassard, N., et al. Epidermal growth factor and perlecan fragments produced by apoptotic endothelial cells co-ordinately activate ERK1/2-dependent antiapoptotic pathways in mesenchymal stem cells. Stem Cells 28 (2010), 810–820.
66. 66 Soulez, M., Pilon, E.A., Dieude, M., et al. The perlecan fragment LG3 is a novel regulator of obliterative remodeling associated with allograft vascular rejection. Circ Res 110 (2012), 94–104.
67. 67 Kobayashi, Y., Yamamoto, T., Chishima, F., et al. Autoantibodies isolated from patients with preeclampsia induce soluble endoglin production from trophoblast cells via interactions with angiotensin II type 1 receptor. Am J Reprod Immunol 73 (2015), 285–291.
68. 68 Venkatesha, S., Toporsian, M., Lam, C., et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12 (2006), 642–649.
69. 69 Dragun, D., Catar, R., Philippe, A., Non-HLA antibodies in solid organ transplantation: recent concepts and clinical relevance. Curr Opin Organ Transplant 18 (2013), 430–435.
70. 70 Porcheray, F., DeVito, J., Yeap, B.Y., et al. Chronic humoral rejection of human kidney allografts associates with broad autoantibody responses. Transplantation 89 (2010), 1239–1246.
71. 71 Honger, G., Cardinal, H., Dieude, M., et al. Human pregnancy and generation of anti-angiotensin receptor and anti-perlecan antibodies. Transpl Int 27 (2014), 467–474.
72. 72 Scornik, J.C., Guerra, G., Schold, J.D., et al. Value of posttransplant antibody tests in the evaluation of patients with renal graft dysfunction. Am J Transplant 7 (2007), 1808–1814.
73. 73 Stepan, H., Wallukat, G., Schultheiss, H.P., et al. Is parvovirus B19 the cause for autoimmunity against the angiotensin II type receptor?. J Reprod Immunol 73 (2007), 130–134.
74. 74 McLachlan, S.M., Nagayama, Y., Rapoport, B., Insight into Graves’ hyperthyroidism from animal models. Endocr Rev 26 (2005), 800–832.
75. 75 Zhang, X., Reed, E.F., Effect of antibodies on endothelium. Am J Transplant 9 (2009), 2459–2465.
76. 76 Zhang, X., Rozengurt, E., Reed, E.F., HLA class I molecules partner with integrin beta4 to stimulate endothelial cell proliferation and migration. Sci Signal, 3, 2010, ra85.
77. 77 Dragun, D., Philippe, A., Catar, R., et al. Autoimmune mediated G-protein receptor activation in cardiovascular and renal pathologies. Thromb Haemost 101 (2009), 643–648.
78. 78 Heyma, P., Harrison, L.C., Precipitation of the thyrotropin receptor and identification of thyroid autoantigens using Graves’ disease immunoglobulins. J Clin Invest 74 (1984), 1090–1097.
79. 79 AbdAlla, S., Lother, H., Quitterer, U., AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature 407 (2000), 94–98.
80. 80 Gregan, B., Jurgensen, J., Papsdorf, G., et al. Ligand-dependent differences in the internalization of endothelin A and endothelin B receptor heterodimers. J Biol Chem 279 (2004), 27679–27687.
81. 81 Wisler, J.W., Xiao, K., Thomsen, A.R., et al. Recent developments in biased agonism. Curr Opin Cell Biol 27 (2014), 18–24.
82. 82 Kendall, R.T., Lee, M.H., Pleasant, D.L., et al. Arrestin-dependent angiotensin AT1 receptor signaling regulates Akt and mTor-mediated protein synthesis. JBiol Chem 289 (2014), 26155–26166.
83. 83 Pilon, E.A., Dieude, M., Qi, S., et al. The perlecan fragment LG3 regulates homing of mesenchymal stem cells and neointima formation during vascular rejection. Am J Transplant 15 (2015), 1205–1218.
84. 84 Kranz, B., Kelsch, R., Kuwertz-Broking, E., et al. Acute antibody-mediated rejection in paediatric renal transplant recipients. Pediatr Nephrol 26 (2011), 1149–1156.
85. 85 Miura, S., Nakao, N., Hanzawa, H., et al. Reassessment of the unique mode of binding between angiotensin II type 1 receptor and their blockers. PloS One, 8, 2013, e79914.
86. 86 O'Callaghan, D.S., Savale, L., Yaici, A., et al. Endothelin receptor antagonists for the treatment of pulmonary arterial hypertension. Expert Opin Pharmacother 12 (2011), 1585–1596.
87. 87 Dhillon, S., Bosentan: a review of its use in the management of digital ulcers associated with systemic sclerosis. Drugs 69 (2009), 2005–2024.
88. 88 Wenzel, R.R., Littke, T., Kuranoff, S., et al. Avosentan reduces albumin excretion in diabetics with macroalbuminuria. J Am Soc Nephrol 20 (2009), 655–664.
89. 89 Chade, A.R., Tullos, N., Stewart, N.J., et al. Endothelin-a receptor antagonism after renal angioplasty enhances renal recovery in renovascular disease. J Am Soc Nephrol 26 (2015), 1071–1080.
90. 90 Wedel, J., Bruneau, S., Kochupurakkal, N., et al. Chronic allograft rejection: a fresh look. Curr Opin Organ Transplantat 20 (2015), 13–20.
91. 91 Wang, C., Yi, T., Qin, L., et al. Rapamycin-treated human endothelial cells preferentially activate allogeneic regulatory T cells. J Clin Invest 123 (2013), 1677–1693.
92. 92 Jin, Y.P., Valenzuela, N.M., Ziegler, M.E., et al. Everolimus inhibits anti-HLA I antibody-mediated endothelial cell signaling, migration and proliferation more potently than sirolimus. Am J Transplant 14 (2014), 806–819.
93. 93 Canaud, G., Bienaime, F., Tabarin, F., et al. Inhibition of the mTORC pathway in the antiphospholipid syndrome. N Engl J Med 371 (2014), 303–312.