ADAMTS13 Endopeptidase Protects against Vascular Endothelial Growth Factor InhibitorInduced Thrombotic Microangiopathy

Journal of the American Society of Nephrology

Volumn 27, Issue 1, 2016, Pages 120-131

  Erpenbeck, Luise ^a,b   Demers, Melanie ^a,b   Zsengellér, Zsuzsanna K ^b   Gallant, Maureen ^a   Cifuni, Stephen M ^a   Stillman, Isaac E ^b   Karumanchi, S Ananth ^b   Wagner, Denisa D ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULAR ENDOTHELIAL GROWTH INHIBITOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAMTS13 PROTEIN, MOUSE; METALLOPROTEINASE; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

ANEMIA; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; CONTROLLED STUDY; ELEVATED BLOOD PRESSURE; HYPERTENSION; KIDNEY FUNCTION; MICROTHROMBUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEINURIA; RETICULOCYTE; SCHISTOCYTOSIS; SYSTOLIC BLOOD PRESSURE; THROMBOCYTE COUNT; THROMBOCYTOPENIA; THROMBOTIC THROMBOCYTOPENIC PURPURA; URINALYSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; PHYSIOLOGY; THROMBOTIC MICROANGIOPATHIES;

ADAMTS13 PROTEIN; ANIMALS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; THROMBOTIC MICROANGIOPATHIES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84954422750     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014121165     Document Type: Article

References (67)

1. Besbas N, Karpman D, Landau D, Loirat C, Proesmans W, Remuzzi G, Rizzoni G, Taylor CM, Van de Kar N, Zimmerhackl LB; European Paediatric Research Group for HUS: A classification of hemolytic uremic syndrome and thrombotic thrombocytopenic purpura and related disorders. Kidney Int 70: 423-431, 2006
2. RosoveMH: Thrombotic microangiopathies. Semin Arthritis Rheum43: 797-805, 2014
3. Powe CE, Levine RJ, Karumanchi SA: Preeclampsia, a disease of the maternal endothelium: The role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 123: 2856-2869, 2011
4. Haram K, Svendsen E, Abildgaard U: The HELLP syndrome: Clinical issues andmanagement. A Review. BMCPregnancy Childbirth 9: 8, 2009
5. Bianchi V, Robles R, Alberio L, Furlan M, Lämmle B: Von Willebrand factor-cleaving protease (ADAMTS13) in thrombocytopenic disorders: A severely deficient activity is specific for thrombotic thrombocytopenic purpura. Blood 100: 710-713, 2002
6. Furlan M, Lämmle B: Aetiology and pathogenesis of thrombotic thrombocytopenic purpura and haemolytic uraemic syndrome: The role of von Willebrand factor-cleaving protease. Best Pract Res Clin Haematol 14: 437-454, 2001
7. Lämmle B, Kremer Hovinga JA, Alberio L: Thrombotic thrombocytopenic purpura. J Thromb Haemost 3: 1663-1675, 2005
8. Dong JF, Moake JL, Nolasco L, Bernardo A, Arceneaux W, Shrimpton CN, Schade AJ, McIntire LV, Fujikawa K, López JA: ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 100: 4033-4039, 2002
9. Radhi M, Carpenter SL: Thrombotic microangiopathies. ISRN Hematol 2012: 310596, 2012
10. Blake-Haskins JA, Lechleider RJ, Kreitman RJ: Thrombotic microangiopathy with targeted cancer agents. Clin Cancer Res 17: 5858-5866, 2011
11. Aref S, Goda H: Increased VWF antigen levels and decreased ADAMTS13 activity in preeclampsia. Hematology 18: 237-241, 2013
12. Veyradier A, Obert B, Haddad E, Cloarec S, Nivet H, Foulard M, Lesure F, Delattre P, Lakhdari M, Meyer D, Girma JP, Loirat C: Severe deficiency of the specific von Willebrand factor-cleaving protease (ADAMTS 13) activity in a subgroup of children with atypical hemolytic uremic syndrome. J Pediatr 142: 310-317, 2003
13. Zhu X, Wu S, Dahut WL, Parikh CR: Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: Systematic review and meta-analysis. AmJ Kidney Dis 49: 186-193, 2007
14. Feldman DR, Baum MS, Ginsberg MS, Hassoun H, Flombaum CD, Velasco S, Fischer P, Ronnen E, IshillN, Patil S, Motzer RJ: Phase I trial of bevacizumab plus escalated doses of sunitinib in patients with metastatic renal cell carcinoma. J ClinOncol 27: 1432-1439, 2009
15. Bollée G, Patey N, Cazajous G, Robert C, Goujon JM, Fakhouri F, Bruneval P, Noël LH, Knebelmann B: Thrombotic microangiopathy secondary to VEGF pathway inhibition by sunitinib. Nephrol Dial Transplant 24: 682-685, 2009
16. Jin K, Shen Y, He K, Xu Z, Li G, Teng L: Aflibercept (VEGF Trap): One more double-edged sword of anti-VEGF therapy for cancer? Clin Transl Oncol 12: 526-532, 2010
17. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M,Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE: VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 358: 1129-1136, 2008
18. Tew WP, Gordon M, Murren J, Dupont J, Pezzulli S, Aghajanian C, Sabbatini P, Mendelson D, Schwartz L, Gettinger S, Psyrri A, Cedarbaum JM, Spriggs DR: Phase 1 study of aflibercept administered subcutaneously to patients with advanced solid tumors. Clin Cancer Res 16: 358-366, 2010
19. Vigneau C, Lorcy N, Dolley-Hitze T, Jouan F, Arlot-Bonnemains Y, Laguerre B, Verhoest G, Goujon JM, Belaud-Rotureau MA, Rioux-LeclercqN: All anti-vascular endothelial growth factor drugs can induce 'pre-eclampsia-like syndrome': A RARe study. Nephrol Dial Transplant 29: 325-332, 2014
20. Patel TV, Morgan JA, Demetri GD, George S, Maki RG, Quigley M, Humphreys BD: A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J NatlCancer Inst 100: 282-284, 2008
21. Maynard SE,Min JY,Merchan J, LimKH, Li J,Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658, 2003
22. Levine RJ,Maynard SE,Qian C, LimKH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA: Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683, 2004
23. Bergmann A, Ahmad S, Cudmore M, Gruber AD, Wittschen P, Lindenmaier W, Christofori G, Gross V, Gonzalves AC, Gröne HJ, Ahmed A, Weich HA: Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mousemodel. J Cell MolMed14[6B]: 1857-1867, 2010
24. Li Z, Zhang Y, Ying Ma J, Kapoun AM, Shao Q, Kerr I, Lam A, O'Young G, Sannajust F, Stathis P, Schreiner G, Karumanchi SA, Protter AA, Pollitt NS: Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 50: 686-692, 2007
25. Kuo CJ, Farnebo F, Yu EY, Christofferson R, Swearingen RA, Carter R, von Recum HA, Yuan J, Kamihara J, Flynn E, D'Amato R, Folkman J, Mulligan RC: Comparative evaluation of the antitumor activity of antiangiogenic proteins delivered by gene transfer. Proc Natl Acad Sci U S A 98: 4605-4610, 2001
26. López JA, Chung DW: VWF self-association: More bands for the buck. Blood 116: 3693-3694, 2010
27. Motto DG, Chauhan AK, Zhu G, Homeister J, Lamb CB, Desch KC, Zhang W, Tsai HM, Wagner DD, Ginsburg D: Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J Clin Invest 115: 2752-2761, 2005
28. Schiviz A, Wuersch K, Piskernik C, Dietrich B, Hoellriegl W, Rottensteiner H, Scheiflinger F, Schwarz HP, Muchitsch EM: A new mouse model mimicking thrombotic thrombocytopenic purpura: Correction of symptoms by recombinant human ADAMTS13. Blood 119: 6128-6135, 2012
29. Li F, Hagaman JR, Kim HS, Maeda N, Jennette JC, Faber JE, Karumanchi SA, SmithiesO, TakahashiN: ENOS deficiency acts through endothelin to aggravate sFlt-1-induced pre-eclampsia-like phenotype. J Am Soc Nephrol 23: 652-660, 2012
30. Kamba T, McDonald DM: Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br J Cancer 96: 1788-1795, 2007
31. Stillman IE, Karumanchi SA: The glomerular injury of preeclampsia. J Am Soc Nephrol 18: 2281-2284, 2007
32. Savchenko AS, Borissoff JI, Martinod K, De Meyer SF, Gallant M, Erpenbeck L, Brill A, Wang Y, Wagner DD: VWF-mediated leukocyte recruitment with chromatin decondensation by PAD4 increases myocardial ischemia/reperfusion injury in mice. Blood 123: 141-148, 2014
33. Vigil-De Gracia P: Maternal deaths due to eclampsia and HELLP syndrome. Int J Gynaecol Obstet 104: 90-94, 2009
34. Hayman SR, Leung N, Grande JP, Garovic VD: VEGF inhibition, hypertension, and renal toxicity. Curr Oncol Rep 14: 285-294, 2012
35. Frangié C, Lefaucheur C, Medioni J, Jacquot C, Hill GS,NochyD: Renal thrombotic microangiopathy caused by anti-VEGF-antibody treatment for metastatic renal-cell carcinoma. Lancet Oncol 8: 177-178, 2007
36. Stokes MB, Erazo MC, D'Agati VD: Glomerular disease related to anti-VEGF therapy. Kidney Int 74: 1487-1491, 2008
37. Eremina V, Cui S,GerberH, Ferrara N, Haigh J,Nagy A, Ema M, Rossant J, Jothy S, Miner JH, Quaggin SE: Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol 17: 724-735, 2006
38. Vanhoorelbeke K, De Meyer SF: Animal models for thrombotic thrombocytopenic purpura. J Thromb Haemost 11[Suppl 1]: 2-10, 2013
39. Banno F, Kokame K, Okuda T, Honda S,Miyata S, Kato H, Tomiyama Y, Miyata T: Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura. Blood 107: 3161-3166, 2006
40. Morioka Y, Casari C, Wohner N, Cho S, Kurata S, Kitano A, Christophe OD, Lenting PJ, Li R, Denis CV, Prévost N: Expression of a structurally constrained von Willebrand factor variant triggers acute thrombotic thrombocytopenic purpura in mice. Blood 123: 3344-3353, 2014
41. Fujimura Y,Matsumoto M, Kokame K, Isonishi A, Soejima K, AkiyamaN, Tomiyama J, Natori K, Kuranishi Y, Imamura Y, Inoue N, Higasa S, Seike M, Kozuka T, Hara M,WadaH,MurataM, Ikeda Y,Miyata T,George JN: Pregnancy-induced thrombocytopenia and TTP, and the risk of fetal death, in Upshaw-Schulman syndrome: A series of 15 pregnancies in 9 genotyped patients. Br J Haematol 144: 742-754, 2009
42. Walshe TE, Dole VS, Maharaj AS, Patten IS, Wagner DD, D'Amore PA: Inhibition of VEGF or TGF-beta signaling activates endothelium and increases leukocyte rolling. Arterioscler Thromb Vasc Biol 29: 1185-1192, 2009
43. Di Marco GS, Reuter S, Hillebrand U, Amler S, König M, Larger E, Oberleithner H, Brand E, Pavenstädt H, Brand M: The soluble VEGF receptor sFlt1 contributes to endothelial dysfunction in CKD. J AmSoc Nephrol 20: 2235-2245, 2009
44. Sadler JE: Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood 112: 11-18, 2008
45. Hillgruber C, Steingräber AK, Pöppelmann B, Denis CV, Ware J, Vestweber D, Nieswandt B, Schneider SW, Goerge T: Blocking von Willebrand factor for treatment of cutaneous inflammation. J Invest Dermatol 134: 77-86, 2014
46. Chauhan AK, Kisucka J, Brill A, Walsh MT, Scheiflinger F, Wagner DD: ADAMTS13: A new link between thrombosis and inflammation. J Exp Med 205: 2065-2074, 2008
47. Zhao BQ, Chauhan AK, Canault M, Patten IS, Yang JJ, Dockal M, Scheiflinger F, Wagner DD: Von Willebrand factor-cleaving protease ADAMTS13 reduces ischemic brain injury in experimental stroke. Blood 114: 3329-3334, 2009
48. Gandhi C, Khan MM, Lentz SR, Chauhan AK: ADAMTS13 reduces vascular inflammation and the development of early atherosclerosis in mice. Blood 119: 2385-2391, 2012
49. Murrin RJ, Murray JA: Thrombotic thrombocytopenic purpura: Aetiology, pathophysiology and treatment. Blood Rev 20: 51-60, 2006
50. Grillberger R, Casina VC, Turecek PL, Zheng XL, Rottensteiner H, Scheiflinger F: Anti-ADAMTS13 IgG autoantibodies present in healthy individuals share linear epitopes with those in patients with thrombotic thrombocytopenic purpura. Haematologica 99: E58-e60, 2014
51. Rieger M, Mannucci PM, Kremer Hovinga JA, Herzog A, Gerstenbauer G, Konetschny C, Zimmermann K, Scharrer I, Peyvandi F, GalbuseraM, Remuzzi G, BöhmM, Plaimauer B, Lämmle B, Scheiflinger F: ADAMTS13 autoantibodies in patients with thrombotic microangiopathies and other immunomediated diseases. Blood 106: 1262-1267, 2005
52. Oleksowicz L, Bhagwati N, DeLeon-Fernandez M: Deficient activity of von Willebrand's factor-cleaving protease in patients with disseminated malignancies. Cancer Res 59: 2244-2250, 1999
53. Mannucci PM, Karimi M, Mosalaei A, Canciani MT, Peyvandi F: Patients with localized and disseminated tumors have reduced but measurable levels of ADAMTS-13 (von Willebrand factor cleaving protease). Haematologica 88: 454-458, 2003
54. Stepanian A, Cohen-Moatti M, Sanglier T, Legendre P, Ameziane N, Tsatsaris V, Mandelbrot L, de Prost D, Veyradier A; ECLAXIR Study Group: Von Willebrand factor and ADAMTS13: A candidate couple for preeclampsia pathophysiology. Arterioscler Thromb Vasc Biol 31: 1703-1709, 2011
55. Lechner K, Simonitsch I, Haselböck J, Jäger U, Pabinger I: Acquired immune-mediated thrombophilia in lymphoproliferative disorders. Leuk Lymphoma 52: 1836-1843, 2011
56. Yao H, Monge M, Renou M, Lecaque C, Jauréguy M, Presne C, Makdassi R, Choukroun G: Thrombotic thrombocytopenic purpura due to anti-ADAMTS13 antibodies in multiple myeloma. Clin Nephrol 81: 210-215, 2014
57. Uzan J, Carbonnel M, Piconne O, Asmar R, Ayoubi JM: Pre-eclampsia: Pathophysiology, diagnosis, and management. Vasc Health Risk Manag 7: 467-474, 2011
58. Plaimauer B, Kremer Hovinga JA, Juno C, Wolfsegger MJ, Skalicky S, SchmidtM,Grillberger L, HasslacherM, Knöbl P, Ehrlich H, Scheiflinger F: Recombinant ADAMTS13 normalizes von Willebrand factor-cleaving activity in plasma of acquired TTP patients by overriding inhibitory antibodies. J Thromb Haemost 9: 936-944, 2011
59. Piskernik C, Dietrich B, Kubik S, Ruthsatz T, Scheiflinger F, Schwarz HP, Muchitsch EM: Preclinical Safety of Baxter's Recombinant ADAMTS13 [abstract]. 54th ASH Annual Meeting and Exposition: Abstract 3381, 2012.
60. Jilma-Stohlawetz P, Gilbert JC, Gorczyca ME, Knöbl P, Jilma B: A dose ranging phase I/II trial of the von Willebrand factor inhibiting aptamer ARC1779 in patients with congenital thrombotic thrombocytopenic purpura. Thromb Haemost 106: 539-547, 2011
61. Feys HB, Roodt J, VandeputteN, Pareyn I,Mottl H, Hou S, Lamprecht S, Van Rensburg WJ, Deckmyn H, Vanhoorelbeke K: Inhibition of von Willebrand factor-platelet glycoprotein Ib interaction prevents and reverses symptoms of acute acquired thrombotic thrombocytopenic purpura in baboons. Blood 120: 3611-3614, 2012
62. Chen J, Reheman A, Gushiken FC, Nolasco L, Fu X, Moake JL, Ni H, López JA: N-acetylcysteine reduces the size and activity of von Willebrand factor in human plasma and mice. J Clin Invest 121: 593-603, 2011
63. Li GW, Rambally S, Kamboj J, Reilly S, Moake JL, Udden MM, Mims MP: Treatment of refractory thrombotic thrombocytopenic purpura with N-acetylcysteine: A case report. Transfusion 54: 1221-1224, 2014
64. Chauhan AK, Walsh MT, Zhu G, Ginsburg D, Wagner DD, Motto DG: The combined roles of ADAMTS13 and VWF in murine models of TTP, endotoxemia, and thrombosis. Blood 111: 3452-3457, 2008
65. Zini G, d'Onofrio G, Briggs C, Erber W, Jou JM, Lee SH, McFadden S, Vives-Corrons JL, Yutaka N, Lesesve JF; International Council for Standardization in Haematology (ICSH): ICSH recommendations for identification, diagnostic value, and quantitation of schistocytes. Int J Lab Hematol 34: 107-116, 2012
66. Feng M, Whitesall S, Zhang Y, Beibel M, D'Alecy L, DiPetrillo K: Validation of volume-pressure recording tail-cuff blood pressure measurements. Am J Hypertens 21: 1288-1291, 2008
67. Krege JH, Hodgin JB, Hagaman JR, Smithies O: A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 25: 1111-1115, 1995