Thrombotic microangiopathies: Towards a pathophysiology-based classification

Cardiovascular and Hematological Disorders - Drug Targets

Volumn 9, Issue 1, 2009, Pages 36-50

  Coppo, Paul ^a   Veyradier, Agnès ^b  

^a HÔPITAL SAINT ANTOINE   (France)

^b HÔPITAL ANTOINE BÉCLÈRE   (France)

Author keywords

ADAMTS13; Autoimmune disease; Complement; Hemolytic uremic syndrome; Thrombocytopenia; Thrombotic microangiopathies; Thrombotic thrombocytopenic purpura

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; ANTINEOPLASTIC AGENT; AZATHIOPRINE; CHEMOKINE; CLOPIDOGREL; COMPLEMENT FACTOR H; CYANOCOBALAMIN; CYCLOSPORIN A; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; IMMUNOMODULATING AGENT; INTERLEUKIN 1; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MEMBRANE COFACTOR PROTEIN; MITOMYCIN C; PROSTAGLANDIN; SHIGA TOXIN; TICLOPIDINE; TUMOR NECROSIS FACTOR ALPHA; VINCRISTINE; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN; AUTOANTIBODY;

ARTICLE; BREAST CANCER; CELL ACTIVATION; CLINICAL FEATURE; CYANOCOBALAMIN DEFICIENCY; DISEASE SEVERITY; ENDOTHELIUM LESION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMODIALYSIS; HEMOLYTIC UREMIC SYNDROME; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERTENSION; IMMUNOMODULATION; PATHOPHYSIOLOGY; PLASMAPHERESIS; PREGNANCY COMPLICATION; PROSTATE CANCER; REHYDRATION; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; STOMACH CANCER; STREPTOCOCCUS PNEUMONIA; THROMBOCYTE ADHESIVENESS; THROMBOGENESIS; THROMBOTIC THROMBOCYTOPENIC PURPURA; ANIMAL; AUTOIMMUNITY; CLASSIFICATION; DRUG DELIVERY SYSTEM; GENETICS; HOSPITALIZATION; METABOLISM; MICROCIRCULATION; REVIEW; THROMBOCYTE AGGREGATION;

ADAM PROTEINS; ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; DRUG DELIVERY SYSTEMS; HEMOLYTIC-UREMIC SYNDROME; HUMANS; MICROCIRCULATION; PLATELET AGGREGATION; PURPURA, THROMBOTIC THROMBOCYTOPENIC; SEVERITY OF ILLNESS INDEX; VON WILLEBRAND FACTOR;

EID: 65549151257     PISSN: 1871529X     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152909787581318     Document Type: Article

References (90)

1. Moschcowitz E. Hyaline thrombosis of the terminal arterioles and capillaries: a hitherto undercribed disease. Proc. N. Y. Pathol. Soc., 1924, 24, 21-24.
2. Gasser, C.; Gautier, E.; Steck, A.; Siebenmann, R.E.; Oechslin, R. Hämolytish-uramische syndrome: bilaterale Nierenrindennekrosen bei akuten erworsenen hämolytischen Anämien. Schweiz Med. Wochenschr., 1955, 85, 905-909.
3. Wada, H.; Kaneko, T.; Ohiwa, M.; Tanigawa, M.; Hayashi, T.; Tamaki, S.N.; Minami, K.; Deguchi, K.; Suzuki, T.; Nakano. Increased levels of vascular endothelial cell markers in thrombotic thrombocytopenic purpura. Am. J. Hematol., 1993, 44(2), 101-105.
4. Gerritsen, M.E.; Bloor, C.M. Endothelial cell gene expression in response to injury. FASEB J., 1993, 7(6), 523-532.
5. Ridolfi, R.L.; Bell, W.R. Thrombotic thrombocytopenic purpura. Report of 25 cases and review of the literature. Medicine (Baltimore), 1981, 60(6), 413-428.
6. Mitra, D.; Jaffe, E.A.; Weksler, B.; Hajjar, K.A.; Soderland, C.; Laurence, J. Thrombotic thrombocytopenic purpura and sporadic hemolytic-uremic syndrome plasmas induce apoptosis in restricted lineages of human microvascular endothelial cells. Blood, 1997, 89(4), 1224-1234.
7. Dang, C.T.; Magid, M.S.; Weksler, B.; Chadburn, A.; Laurence, J. Enhanced endothelial cell apoptosis in splenic tissues of patients with thrombotic thrombocytopenic purpura. Blood, 1999, 93(4), 1264-1270.
8. Moake, J.L.; Turner, N.A.; Stathopoulos, N.A.; Nolasco, L.H.; Hellums, J.D. Involvement of large plasma von Willebrand factor (vWF) multimers and unusually large vWF forms derived from endothelial cells in shear stress-induced platelet aggregation. J. Clin. Invest., 1986, 78(6), 1456-1461.
9. Moake, J.L.; Rudy, C.K.; Troll, J.H.; Weinstein, M.J.; Colannino, N.M.; Azocar, J.; Seder, R.H.; Hong, S.L.; Deykin, D. Unusually large plasma factor VIII: von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura. N. Engl. J. Med., 1982, 307(23), 1432-1435.
10. Tsai, H.M. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood, 1996, 87(10), 4235-4244.
11. Furlan, M.; Robles, R.; Lamie, B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood, 1996, 87(10), 4223-4234.
12. Levy, G.G.; Nichols, W.C.; Lian, E.C.; Foroud, T.; McClintick, J.J.; McGee, B.M.; Yang, A.Y.; Siemieniak, D.R.; Stark, K.R.; Gruppo, R.; Sarode, R.; Shurin, S.B.; Chandrasekaran, V.; Stabler, S.P.; Sabio, H.; Bouhassira, E.E.; Upshaw, J.D., Jr.; Ginsburg, D.; Tsai, H.M. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature, 2001, 413(6855), 488-494.
13. Sadler, J.E. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood, 2008, 112(1), 11-18.
14. Xie, L.; Chesterman, C.N.; Hogg, P.J. Control of von Willebrand factor multimer size by thrombospondin-1. J. Exp. Med., 2001, 193 (12), 1341-1349.
15. Chauhan, A.K.; Kisucka, J.; Brill, A.; Walsh, M.T.; Scheiflinger, F.; Wagner, D.D. ADAMTS13, a new link between thrombosis and inflammation. J. Exp. Med., 2008, 205(9), 2065-2074.
16. Chauhan, A.K.; Motto, D.G.; Lamb, C.B.; Bergmeier, W.; Dockal, M.; Plaimauer, B.; Scheiflinger, F.; Ginsburg, D.; Wagner, D.D. Systemic antithrombotic effects of ADAMTS13. J. Exp. Med., 2006, 203(3), 767-776.
17. Moore, J.C.; Hayward, C.P.; Warkentin, T.E.; Kelton, J.G. Decreased von Willebrand factor protease activity associated with thrombocytopenic disorders. Blood, 2001, 98(6), 1842-1846.
18. Mannucci, P.M.; Vanoli, M.; Forza, I.; Canciani, M.T.; Scorza, R. Von Willebrand factor cleaving protease (ADAMTS-13) in 123 patients with connective tissue diseases (systemic lupus erythematosus and systemic sclerosis). Haematologica, 2003, 88(8), 914-918.
19. Mannucci, P.M.; Canciani, M.T.; Forza, I.; Lussana, F.; Lattuada, A.; Rossi, E. Changes in health and disease of the metalloprotease that cleaves von Willebrand factor. Blood, 2001, 98(9), 2730-2735.
20. Furlan, M.; Robles, R.; Galbusera, M.; Remuzzi, G.; Kyrle, P.A.; Brenner, B.; Krause, M.; Scharrer, I.; Aumann, V.; Mittler, U.; Solenthaler, M.; Lämmle, B. Von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura and the hemolytic-uremic syndrome. N. Engl. J. Med., 1998, 339(22), 1578-1584.
21. Tsai, H.M.; Lian, E.C. Antibodies to von Willebrand factorcleaving protease in acute thrombotic thrombocytopenic purpura. N. Engl. J. Med., 1998, 339(22), 1585-1594.
22. Bianchi, V.; Robles, R.; Alberio, L.; Furlan, M.; Lammle, B. Von Willebrand factor-cleaving protease (ADAMTS13) in thrombocytopenic disorders: a severely deficient activity is specific for thrombotic thrombocytopenic purpura. Blood, 2002, 100(2), 710-713.
23. Veyradier, A.; Obert, B.; Houllier, A.; Meyer, D.; Girma, J.P. Specific von Willebrand factor-cleaving protease in thrombotic microangiopathies: a study of 111 cases. Blood, 2001, 98(6), 1765-1772.
24. Veyradier, A.; Lavergne, J.M.; Ribba, A.S.; Obert, B.; Loirat, C.; Meyer, D.; Girma, J.P. Ten candidate ADAMTS13 mutations in six French families with congenital thrombotic thrombocytopenic purpura (Upshaw-Schulman syndrome). J. Thromb. Haemost., 2004, 2(3), 424-429.
25. Motto, D.G.; Chauhan, A.K.; Zhu, G.; Homeister, J.; Lamb, C.B.; Desch, K.C.; Zhang, W.; Tsai, H.M.; Wagner, D.D.; Ginsburg, D. Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J. Clin. Invest., 2005, 115(10), 2752-2761.
26. Chauhan, A.K.; Walsh, M.T.; Zhu, G.; Ginsburg, D.; Wagner, D.D.; Motto, D.G. The combined roles of ADAMTS13 and VWF in murine models of TTP, endotoxemia, and thrombosis. Blood, 2008, 111(7), 3452-3457.
27. Vesely, S.K.; George, J.N.; Lammle, B.; Studt, J.D.; Alberio, L.; El-Harake, M.A.; Raskob, G.E. ADAMTS13 activity in thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: relation to presenting features and clinical outcomes in a prospective cohort of 142 patients. Blood, 2003, 102(1), 60-68.
28. Scheiflinger, F.; Knobl, P.; Trattner, B.; Plaimauer, B.; Mohr, G.; Dockal, M.; Dorner, F.; Rieger, M. Nonneutralizing IgM and IgG antibodies to von Willebrand factor-cleaving protease (ADAMTS-13) in a patient with thrombotic thrombocytopenic purpura. Blood, 2003, 102(9), 3241-3243.
29. Ferrari, S.; Scheiflinger, F.; Rieger, M.; Mudde, G.; Wolf, M.; Coppo, P.; Girma3, J-P.; Azoulay, E.; Brun-Buisson, C.; Fakhouri, F.; Mira, J-P.; Oksenhendler, E.; Poullin, P.; Rondeau, E.; Schleinitz, N.; Schlemmer, B.; Teboul, J-L.; Vanhille, P.; Vernant, J-P.; Meyer, D.; Veyradier, A. Prognostic value of anti-ADAMTS13 antibodies features (Ig isotype, titer and inhibitory effect) in a cohort of 35 adult French patients undergoing a first episode of thrombotic microangiopathy with an undetectable ADAMTS13 activity. Blood, 2007, 109(7), 2815-2822.
30. Klaus, C.; Plaimauer, B.; Studt, J.D.; Dorner, F.; Lammle, B.; Mannucci, P.M.; Scheiflinger, F. Epitope mapping of ADAMTS13 autoantibodies in acquired thrombotic thrombocytopenic purpura. Blood, 2004, 103(12), 4514-4519.
31. Rieger, M.; Mannucci, P.M.; Kremer Hovinga, J.A.; Herzog, A.; Gerstenbauer, G.; Konetschny, C.; Zimmermann, K.; Scharrer, I.; Peyvandi, F.; Galbusera, M.; Remuzzi, G.; Böhm, M.; Plaimauer, B.; Lämmle, B.; Scheiflinger, F. ADAMTS13 autoantibodies in patients with thrombotic microangiopathies and other immunomediated diseases. Blood, 2005, 106(4), 1262-1267.
32. Schneppenheim, R.; Budde, U.; Oyen, F.; Angerhaus, D.; Aumann, V.; Drewke, E.; Hassenpflug, W.; Häberle, J.; Kentouche, Kohne, E.; Kurnik, K.; Mueller-Wiefel, D.; Obser, T.; Santer, R.; Sykora, K.W. Von Willebrand factor cleaving protease and ADAMTS13 mutations in childhood TTP. Blood, 2003, 101(5), 1845-1850.
33. Pene, F.; Vigneau, C.; Auburtin, M.; Moreau, D.; Zahar, J.R.; Coste, J.; Heshmati, F.; Mira, J.P. Outcome of severe adult thrombotic microangiopathies in the intensive care unit. Intensive Care Med., 2005, 31(1), 71-78.
34. Patschan, D.; Witzke, O.; Duhrsen, U.; Erbel, R.; Philipp, T.; Herget-Rosenthal, S. Acute myocardial infarction in thrombotic microangiopathies--clinical characteristics, risk factors and outcome. Nephrol. Dial. Transplant., 2006, 21(6),1549-1554.
35. Hosler, G.A.; Cusumano, A.M.; Hutchins, G.M. Thrombotic thrombocytopenic purpura and hemolytic uremic syndrome are distinct pathologic entities. A review of 56 autopsy cases. Arch. Pathol. Lab. Med., 2003, 127(7), 834-839.
36. Musio, F.; Bohen, E.M.; Yuan, C.M.; Welch, P.G. Review of thrombotic thrombocytopenic purpura in the setting of systemic lupus erythematosus. Semin. Arthritis Rheum., 1998, 28(1), 1-19.
37. Tandon, N.N.; Rock, G.; Jamieson, G.A. Anti-CD36 antibodies in thrombotic thrombocytopenic purpura. Br. J. Haematol., 1994, 88(4), 816-825.
38. Coppo, P.; Bengoufa, D.; Veyradier, A.; Wolf, M.; Bussel, A.; Millot, G.A.; Malot, S.; Heshmati, F.; Mira, J.P.; Boulanger, E.; Galicier, L.; Durey-Dragon, M.A.; Frémeaux-Bacchi, V.; Ramakers, M.; Pruna, A.; Bordessoule, D.; Gouilleux, V.; Scrobohaci, M.L.; Vernant, J.P.; Moreau, D.; Azoulay, E.; Schlemmer, B.; Guillevin, L.; Lassoued, K. Severe ADAMTS13 deficiency in adult idiopathic thrombotic microangiopathies defines a subset of patients characterized by various autoimmune manifestations, lower platelet count, and mild renal involvement. Medicine (Baltimore), 2004, 83(4), 233-234.
39. Brunner, H.I.; Freedman, M.; Silverman, E.D. Close relationship between systemic lupus erythematosus and thrombotic thrombocytopenic purpura in childhood. Arthritis. Rheum., 1999, 42(11), 2346-2355.
40. Scully, M.; Yarranton, H.; Liesner, R.; Cavenagh, J.; Hunt, B.; Benjamin, S.; Bevan, D.; Mackie, I.; Machin, S. Regional UK TTP Registry: correlation with laboratory ADAMTS 13 analysis and clinical features. Br. J. Haematol., 2008, 142(5), 819-826.
41. Studt, J.D.; Hovinga, J.A.; Radonic, R.; Gasparovic, V.; Ivanovic, D.; Merkler, M.; Wirthmueller, U.; Dahinden, C.; Furlan, M.; Lämmle, B. Familial acquired thrombotic thrombocytopenic purpura: ADAMTS13 inhibitory autoantibodies in identical twins. Blood, 2004, 103(11), 4195-4197.
42. Tsai, H.M. High titers of inhibitors of von Willebrand factorcleaving metalloproteinase in a fatal case of acute thrombotic thrombocytopenic purpura. Am. J. Hematol., 2000, 65(3), 251-255.
43. Zheng, X.L.; Kaufman, R.M.; Goodnough, L.T.; Sadler, J.E. Effect of plasma exchange on plasma ADAMTS13 metalloprotease activity, inhibitor level, and clinical outcome in patients with idiopathic and nonidiopathic thrombotic thrombocytopenic purpura. Blood, 2004, 103(11), 4043-4049.
44. Coppo, P.; Wolf, M.; Veyradier, A.; Bussel, A.; Malot, S.; Millot, G.A.; Daubin, C.; Bordessoule, D.; Pène, F.; Mira, J.P.; Heshmati, F.; Maury, E.; Guidet, B.; Boulanger, E.; Galicier, L.; Parquet, N.; Vernant, J.P.; Rondeau, E.; Azoulay, E.; Schlemmer, B. Prognostic value of inhibitory anti-ADAMTS13 antibodies in adult-acquired thrombotic thrombocytopenic purpura. Br. J. Haematol., 2006, 132(1), 66-74.
45. Peyvandi, F.; Lavoretano, S.; Palla, R.; Feys, H.B.; Vanhoorelbeke, K.; Battaglioli, T.; Valsecchi, C.; Canciani, M.T.; Fabris, F.; Zver, S.; Réti, M.; Mikovic, D.; Karimi, M.; Giuffrida, G.; Laurenti, L.; Mannucci, P.M. ADAMTS13 and anti-ADAMTS13 antibodies as markers for recurrence of acquired thrombotic thrombocytopenic purpura during remission. Haematologica, 2008, 93(2), 232-239.
46. Mannucci, P.M.; Peyvandi, F. TTP and ADAMTS13, When is testing appropriate? Hematol. Am. Soc. Hematol. Educ. Program, 2007, 2007, 121-126.
47. Uchida, T.; Wada, H.; Mizutani, M.; Iwashita, M.; Ishihara, H.; Shibano, T.; Suzuki, M.; Matsubara, Y.; Soejima, K.; Matsumoto, M.; Fujimura, Y.; Ikeda, Y.; Murata, M.; Research Project on Genetics of Thrombosis. Identification of novel mutations in ADAMTS13 in an adult patient with congenital thrombotic thrombocytopenic purpura. Blood, 2004, 104(7), 2081-2083.
48. Rock, G.A.; Shumak, K.H.; Buskard, N.A.; Blanchette, V.S.; Kelton, J.G.; Nair, R.C.; Spasoff, R.A. Comparison of plasma exchange with plasma infusion in the treatment of thrombotic thrombocytopenic purpura. Canadian Apheresis Study Group. N. Engl. J. Med., 1991, 325(6), 393-397.
49. Bell, W.R.; Braine, H.G.; Ness, P.M.; Kickler, T.S. Improved survival in thrombotic thrombocytopenic purpura-hemolytic uremic syndrome. Clinical experience in 108 patients. N. Engl. J. Med., 1991, 325(6), 398-403.
50. Coppo, P.; Bussel, A.; Charrier, S.; Adrie, C.; Galicier, L.; Boulanger, E.; Veyradier, A.; Leblanc, T.; Alberti, C.; Azoulay, E.; Le Gall, J.R.; Schlemmer, B. High-dose plasma infusion versus plasma exchange as early treatment of thrombotic thrombocytopenic purpura/hemolytic-uremic syndrome. Medicine (Baltimore), 2003, 82(1), 27-38.
51. Bird, J.M.; Cummins, D.; Machin, S.J. Cyclophosphamide for chronic relapsing thrombotic thrombocytopenic purpura. Lancet, 1990, 336(8714), 565-566.
52. Fakhouri, F.; Vernant, J.P.; Veyradier, A.; Wolf, M.; Kaplanski, G.; Binaut, R.; Rieger, M.; Scheiflinger, F.; Poullin, P.; Deroure, B.; Delarue, R.; Lesavre, P.; Vanhille, P.; Hermine, O.; Remuzzi, G.; Grünfeld, J.P. Efficiency of curative and prophylactic treatment with rituximab in ADAMTS13-deficient thrombotic thrombocytopenic purpura: a study of 11 cases. Blood, 2005, 106(6), 1932-1937.
53. Scully, M.; Cohen, H.; Cavenagh, J.; Benjamin, S.; Starke, R.; Killick, S.; Mackie, I.; Machin, S.J. Remission in acute refractory and relapsing thrombotic thrombocytopenic purpura following rituximab is associated with a reduction in IgG antibodies to ADAMTS-13. Br. J. Haematol., 2007, 136(3), 451-461.
54. Tarr, P.I.; Gordon, C.A.; Chandler, W.L. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet, 2005, 365(9464), 1073-1086.
55. Zipfel, P.F.; Heinen, S.; Jozsi, M.; Skerka, C. Complement and diseases: defective alternative pathway control results in kidney and eye diseases. Mol. Immunol., 2006, 43(1-2), 97-106.
56. Siegler, R.L.; Pysher, T.J.; Lou, R.; Tesh, V.L.; Taylor, F.B., Jr. Response to Shiga toxin-1, with and without lipopolysaccharide, in a primate model of hemolytic uremic syndrome. Am. J. Nephrol., 2001, 21(5), 420-425.
57. Warwicker, P.; Goodship, T.H.; Donne, R.L.; Pirson, Y.; Nicholls, A.; Ward, R.M.; Turnpenny, P.; Goodship, J.A. Genetic studies into inherited and sporadic hemolytic uremic syndrome. Kidney Int., 1998, 53(4), 836-844.
58. Atkinson, J.P.; Goodship, T.H. Complement factor H and the hemolytic uremic syndrome. J. Exp. Med., 2007, 204(6), 1245-1248.
59. Caprioli, J.; Noris, M.; Brioschi, S.; Pianetti, G.; Castelletti, F.; Bettinaglio, P.; Mele, C.; Bresin, E.; Cassis, L.; Gamba, S.; Porrati, F.; Bucchioni, S.; Monteferrante, G.; Fang, C.J.; Liszewski, M.K.; Kavanagh, D.; Atkinson, J.P.; Remuzzi, G.; International Registry of Recurrent and Familial HUS/TTP. Genetics of HUS: the impact of MCP, CFH, and IF mutations on clinical presentation, response to treatment, and outcome. Blood, 2006, 108(4), 1267-1279.
60. Pickering, M.C.; de Jorge, E.G.; Martinez-Barricarte, R.; Recalde, S.; Garcia-Layana, A.; Rose, K.L.; Moss, J.; Walport, M.J.; Cook, H.T.; de Córdoba, S.R.; Botto, M. Spontaneous hemolytic uremic syndrome triggered by complement factor H lacking surface recognition domains. J. Exp. Med., 2007, 204(6), 1249-1256.
61. Dragon-Durey, M.A.; Frémeaux-Bacchi, V.; Loirat, C.; Blouin, J.; Niaudet, P.; Deschenes, G.; Coppo, P.; Herman Fridman, W.; Weiss, L. Heterozygous and homozygous factor h deficiencies associated with hemolytic uremic syndrome or membranoproliferative glomerulonephritis: report and genetic analysis of 16 cases. J. Am. Soc. Nephrol., 2004,15(3), 787-795.
62. Noris, M.; Brioschi, S.; Caprioli, J.; Todeschini, M.; Bresin, E.; Porrati, F.; Gamba, S.; Remuzzi, G.; International Registry of Recurrent and Familial HUS/TTP. Familial haemolytic uraemic syndrome and an MCP mutation. Lancet, 2003, 362(9395), 1542-1547.
63. Fremeaux-Bacchi, V.; Dragon-Durey, M.A.; Blouin, J.; Vigneau, C.; Kuypers, D.; Boudailliez, B.; Loirat, C.; Rondeau, E.; Fridman, W.H. Complement factor I: a susceptibility gene for atypical haemolytic uraemic syndrome. J. Med. Genet., 2004, 41(6), e84.
64. Goodship, T.H.; Liszewski, M.K.; Kemp, E.J.; Richards, A.; Atkinson, J.P. Mutations in CD46, a complement regulatory protein, predispose to atypical HUS. Trends Mol. Med., 2004, 10(5), 226-231.
65. Kavanagh, D.; Kemp, E.J.; Mayland, E.; Winney, R.J.; Duffield, J.S.; Warwick, G.; Richard, A.; Ward, R.; Goodship, J.A.; Goodship, T.H. Mutations in complement factor I predispose to development of atypical hemolytic uremic syndrome. J. Am. Soc. Nephrol., 2005, 16(7), 2150-215.
66. Goicoechea de Jorge, E.; Harris, C.L.; Esparza-Gordillo, J.; Carreras, L.; Arranz, E.A.; Garrido, C.A.; López-Trascasa, M.; Sánchez-Corral, P.; Morgan, B.P.; Rodríguez de Córdoba S. Gainof-function mutations in complement factor B are associated with atypical hemolytic uremic syndrome. Proc. Natl. Acad. Sci. USA, 2007, 104(1), 240-245.
67. Fremeaux-Bacchi, V.; Miller, E.C.; Liszewski, M.K.; Strain, L.; Blouin, J.; Brown, A.L.; Moghal, N.; Kaplan, B.S.; Weiss, R.A.; Lhotta, K.; Kapcer, G.; Mattoo, T.; Nivet, H.; Wong, W.; Gie, S.; de Ligny, B.H.; Fischbach, M.; Gupta, R.; Hauhart, R.; Meunier, V.; Loriat, C.; Dragon-Durey, M.A.; Fridman, W.H.; Janssen, B.J.; Goodship, T.H.; Atkinson, J.P. Mutations in complement C3 predispose to development of atypical hemolytic uremic syndrome. Blood, 2008, 112(13), 4948-4952.
68. Hageman, G.S.; Anderson, D.H.; Johnson, L.V.; Hancox, L.S.; Taiber, A.J.; Hardisty, L.I.; Hageman, J.L.; Stockman, H.A.; Borchardt, J.D.; Gehrs, K.M.; Smith, R.J.; Silvestri, G.; Russell, S.R.; Klaver, C.C.; Barbazetto, I.; Chang, S.; Yannuzzi, L.A.; Barile, G.R.; Merriam, J.C.; Smith, R.T.; Olsh, A.K.; Bergeron, J.; Zernant J.; Merriam, J.E.; Gold, B.; Dean, M.; Allikmets, R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc. Natl. Acad. Sci. USA, 2005, 102(20), 7227-7232.
69. Fakhouri, F.; Jablonski, M.; Lepercq, J.; Blouin, J.; Benachi, A.; Hourmant, M.; Pirson, Y.; Durrbach, A.; Grunfeld, J.P.; Knebelmann, B.; Fremeaux-Bacchi, V. Factor H, membrane cofactor protein and Factor I mutations in patients with HELLP syndrome. Blood, 2008, 112(12), 4542-4545.
70. Sharma, A.P.; Greenberg, C.R.; Prasad, A.N.; Prasad, C. Hemolytic uremic syndrome (HUS) secondary to cobalamin C (cblC) disorder. Pediatr. Nephrol., 2007, 22, 2097-2103.
71. Bale, J.F., Jr.; Brasher, C.; Siegler, R.L. CNS manifestations of the hemolytic-uremic syndrome. Relationship to metabolic alterations and prognosis. Am. J. Dis. Child, 1980,134(9), 869-872.
72. Theobald, I.; Kuwertz-Broking, E.; Schiborr, M.; Heindel, W. Central nervous system involvement in hemolytic uremic syndrome (HUS) - a retrospective analysis of cerebral CT and MRI studies. Clin. Nephrol., 2001, 56(6), S3-8.
73. Garg, A.X.; Suri, R.S.; Barrowman, N.; Rehman, F.; Matsell, D.; Rosas-Arellano, M.P.; Salvadori, M.; Haynes, R.B.; Clark, W.F. Long-term renal prognosis of diarrhea-associated hemolytic uremic syndrome: a systematic review, meta-analysis, and meta-regression. JAMA, 2003, 290(10), 1360-1370.
74. Sellier-Leclerc, A.L.; Fremeaux-Bacchi, V.; Dragon-Durey, M.A.; Macher, M.A.; Niaudet, P.; Guest, G.; Boudailliez, B.; Bouissou, F.; Deschenes, G.; Gie, S.; Tsimaratos, M.; Fischbach, M.; Morin, D.; Nivet, H.; Alberti, C.; Loirat, C.; French Society of Pediatric Nephrology. Differential impact of complement mutations on clinical characteristics in atypical hemolytic uremic syndrome. J. Am. Soc. Nephrol., 2007, 18(8), 2392-2400.
75. Loirat, C.; Fremeaux-Bacchi, V. Hemolytic uremic syndrome recurrence after renal transplantation. Pediatr. Transplant, 2008, 126), 619-629.
76. Roy, V.; Rizvi, M.A.; Vesely, S.K.; George, J.N. Thrombotic thrombocytopenic purpura-like syndromes following bone marrow transplantation: an analysis of associated conditions and clinical outcomes. Bone Marrow Transplant, 2001, 27(6), 641-646.
77. Francis, K.K.; Kalyanam, N.; Terrell, D.R.; Vesely, S.K.; George, J.N. Disseminated malignancy misdiagnosed as thrombotic thrombocytopenic purpura: A report of 10 patients and a systematic review of published cases. Oncologist, 2007, 12(1), 11-19.
78. Bennett, C.L.; Weinberg, P.D.; Rozenberg-Ben-Dror, K.; Yarnold, P.R.; Kwaan, H.C.; Green, D. Thrombotic thrombocytopenic purpura associated with ticlopidine. A review of 60 cases. Ann. Intern. Med., 1998, 128(7), 541-544.
79. Bennett, C.L.; Connors, J.M.; Carwile, J.M.; Moake, J.L.; Bell, W.R.; Tarantolo, S.R.; McCarthy, L.J.; Sarode, R.; Hatfield, A.J.; Feldman, M.D.; Davidson, C.J.; Tsai, H.M. Thrombotic thrombocytopenic purpura associated with clopidogrel. N. Engl. J. Med., 2000, 342(24), 1773-1777.
80. Bennett, C.L.; Kim, B.; Zakarija, A.; Bandarenko, N.; Pandey, D.K.; Buffie, C.G.; McKoy, J.M.; Tevar, A.D.; Cursio, J.F.; Yarnold, P.R.; Kwaan, H.C.; De Masi, D.; Sarode, R.; Raife, T.J.; Kiss, J.E.; Raisch, D.W.; Davidson, C.; Sadler, J.E.; Ortel, T.L.; Zheng, X.L.; Kato, S.; Matsumoto, M.; Uemura, M.; Fujimura, Y.; SERF-TTP Research Group. Two mechanistic pathways for thienopyridine-associated thrombotic thrombocytopenic purpura: a report from the SERF-TTP Research Group and the RADAR Project. J. Am. Coll. Cardiol., 2007, 50(12), 1138-1143.
81. Mauro, M.; Zlatopolskiy, A.; Raife, T.J.; Laurence, J. Thienopyridine-linked thrombotic microangiopathy: association with endothelial cell apoptosis and activation of MAP kinase signalling cascades. Br. J. Haematol., 2004, 124(2), 200-210.
82. Eremina, V.; Jefferson, J.A.; Kowalewska, J.; Hochster, H.; Haas, M.; Weisstuch, J.; Richardson, C.; Kopp, J.B.; Kabir, M.G.; Backx, P.H.; Gerber, H.P.; Ferrara, N.; Barisoni, L.; Alpers, C.E.; Quaggin, S.E. VEGF inhibition and renal thrombotic microangiopathy. N. Engl. J. Med., 2008, 358(11), 1129-1136.
83. Bell, W.R.; Chulay, J.D.; Feinberg, J.E. Manifestations resembling thrombotic microangiopathy in patients with advanced human immunodeficiency virus (HIV) disease in a cytomegalovirus prophylaxis trial (ACTG 204). Medicine (Baltimore), 1997, 76(5), 369-380.
84. Gervasoni, C.; Ridolfo, A.L.; Vaccarezza, M.; Parravicini, C.; Vago, L.; Adorni, F.; Cappelletti, A.; d'Arminio Monforte, A.; Galli, M. Thrombotic microangiopathy in patients with acquired immunodeficiency syndrome before and during the era of introduction of highly active antiretroviral therapy. Clin. Infect. Dis., 2002, 35(12), 1534-1540.
85. Becker, S.; Fusco, G.; Fusco, J.; Balu, R.; Gangjee, S.; Brennan, C.; Feinberg, J. HIV-associated thrombotic microangiopathy in the era of highly active antiretroviral therapy: an observational study. Clin. Infect. Dis., 2004, 39(Suppl 5), S267-275.
86. Gadallah, M.F.; el-Shahawy, M.A.; Campese, V.M.; Todd, J.R.; King, J.W. Disparate prognosis of thrombotic microangiopathy in HIV-infected patients with and without AIDS. Am. J. Nephrol., 1996, 16(5), 446-450.
87. Ahmed, S.; Siddiqui, R.K.; Siddiqui, A.K.; Zaidi, S.A.; Cervia, J. HIV associated thrombotic microangiopathy. Postgrad. Med. J., 2002, 78(923), 520-525.
88. Novitzky, N.; Thomson, J.; Abrahams, L.; du Toit, C.; McDonald, A. Thrombotic thrombocytopenic purpura in patients with retroviral infection is highly responsive to plasma infusion therapy. Br. J. Haematol., 2005, 128(3), 373-379.
89. Malak, S.; Wolf, M.; Millot, G.A.; Mariotte, E.; Veyradier, A.; Meynard, J.L.; Korach, J.M.; Malot, S.; Bussel, A.; Azoulay, E.; Boulanger, E.; Galicier, L.; Devaux, E.; Eschwege, V.; Gallien, S.; Adrie, C.; Schlemmer, B; Rondeau, E.; Coppo, P. Human immunodeficiency virus-associated thrombotic microangiopathies: clinical characteristics and outcome according to ADAMTS13 activity. Scand. J. Immunol., 2008, 68(3), 337-344.
90. Hillmen, P.; Young, N.S.; Schubert, J.; Brodsky, R.A.; Socié, G.; Muus, P.; Röth, A.; Szer, J.; Elebute, M.O.; Nakamura, R.; Browne, P.; Risitano, A.M.; Hill, A.; Schrezenmeier, H.; Fu, C.L.; Maciejewski, J.; Rollins, S.A.; Mojcik, C.F.; Rother, R.P.; Luzzatto, L. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria.N. Engl. J. Med., 2006, 355(12), 1233-1243.