Complementopathies

Blood Reviews

Volumn 31, Issue 4, 2017, Pages 213-223

  Baines, Andrea C ^a   Brodsky, Robert A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative pathway of complement; Atypical hemolytic uremic syndrome; Cold agglutinin disease; Complementopathy; HELLP syndrome; Paroxysmal nocturnal hemoglobinuria

Indexed keywords

AUTOANTIBODY; COLD AGGLUTININ; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C5A; COMPLEMENT FACTOR H; COMPLEMENT MEMBRANE ATTACK COMPLEX; DECAY ACCELERATING FACTOR; ECULIZUMAB; LECTIN; MANNOSE BINDING LECTIN; MEMBRANE COFACTOR PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; PROTEIN C; THROMBOMODULIN; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; COMPLEMENT;

ADAPTIVE IMMUNITY; BLOOD CLOTTING; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT SYSTEM; COMPLEMENTOPATHY; DNA POLYMORPHISM; DYSPNEA; ERYTHROCYTE TRANSFUSION; FATIGUE; FIBRINOLYSIS; HELLP SYNDROME; HEMATOLOGIC DISEASE; HEMOLYSIS; HEMOLYTIC UREMIC SYNDROME; HEREDITY; HUMAN; HUMORAL IMMUNITY; IMMUNOSURVEILLANCE; INFLAMMATION; INNATE IMMUNITY; OPSONIZATION; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PATTERN RECOGNITION; PLASMA EXCHANGE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RETICULOCYTE COUNT; REVIEW; THROMBOSIS; THROMBOTIC THROMBOCYTOPENIC PURPURA; ANIMAL; AUTOIMMUNE HEMOLYTIC ANEMIA; FEMALE; IMMUNOLOGY; PATHOLOGY; PREGNANCY;

ADAPTIVE IMMUNITY; ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANIMALS; ATYPICAL HEMOLYTIC UREMIC SYNDROME; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; FEMALE; HELLP SYNDROME; HEMOGLOBINURIA, PAROXYSMAL; HUMANS; IMMUNITY, INNATE; PREGNANCY;

EID: 85012876399     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2017.02.003     Document Type: Review

References (98)

1. Kaufmann, S.H., Immunology's foundation: the 100-year anniversary of the Nobel Prize to Paul Ehrlich and Elie Metchnikoff. Nat Immunol 9:7 (2008), 705–712.
2. Nesargikar, P.N., Spiller, B., Chavez, R., The complement system: history, pathways, cascade and inhibitors. Eur J Microbiol Immunol (Bp) 2:2 (2012), 103–111.
3. Merle, N.S., Church, S.E., Fremeaux-Bacchi, V., Roumenina, L.T., Complement system part I - molecular mechanisms of activation and regulation. Front Immunol, 6, 2015, 262.
4. Merle, N.S., Noe, R., Halbwachs-Mecarelli, L., Fremeaux-Bacchi, V., Roumenina, L.T., Complement system part II: role in immunity. Front Immunol, 6, 2015, 257.
5. Ricklin, D., Hajishengallis, G., Yang, K., Lambris, J.D., Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11:9 (2010), 785–797.
6. Oikonomopoulou, K., Ricklin, D., Ward, P.A., Lambris, J.D., Interactions between coagulation and complement–their role in inflammation. Semin Immunopathol 34:1 (2012), 151–165.
7. Huber-Lang, M., Sarma, J.V., Zetoune, F.S., Rittirsch, D., Neff, T.A., McGuire, S.R., et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med 12:6 (2006), 682–687.
8. Markiewski, M.M., Nilsson, B., Ekdahl, K.N., Mollnes, T.E., Lambris, J.D., Complement and coagulation: strangers or partners in crime?. Trends Immunol 28:4 (2007), 184–192.
9. Amara, U., Flierl, M.A., Rittirsch, D., Klos, A., Chen, H., Acker, B., et al. Molecular intercommunication between the complement and coagulation systems. J Immunol 185:9 (2010), 5628–5636.
10. Foley, J.H., Examining coagulation-complement crosstalk: complement activation and thrombosis. Thromb Res 141:Suppl. 2 (2016), S50–S54.
11. Lachmann, P.J., The amplification loop of the complement pathways. Adv Immunol 104 (2009), 115–149.
12. Hugli, T.E., Biochemistry and biology of anaphylatoxins. Complement 3:3 (1986), 111–127.
13. Zhou, W., The new face of anaphylatoxins in immune regulation. Immunobiol 217:2 (2012), 225–234.
14. Tegla, C.A., Cudrici, C., Patel, S., Trippe, R. 3rd, Rus, V., Niculescu, F., et al. Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res 51:1 (2011), 45–60.
15. Liszewski, M.K., Farries, T.C., Lublin, D.M., Rooney, I.A., Atkinson, J.P., Control of the complement system. Adv Immunol 61 (1996), 201–283.
16. Liszewski, M.K., Post, T.W., Atkinson, J.P., Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu Rev Immunol 9 (1991), 431–455.
17. Pangburn, M.K., Cutting edge: localization of the host recognition functions of complement factor H at the carboxyl-terminal: implications for hemolytic uremic syndrome. J Immunol 169:9 (2002), 4702–4706.
18. Nilsson, S.C., Sim, R.B., Lea, S.M., Fremeaux-Bacchi, V., Blom, A.M., Complement factor I in health and disease. Mol Immunol 48:14 (2011), 1611–1620.
19. Nilsson, S.C., Trouw, L.A., Renault, N., Miteva, M.A., Genel, F., Zelazko, M., et al. Genetic, molecular and functional analyses of complement factor I deficiency. Eur J Immunol 39:1 (2009), 310–323.
20. Degn, S.E., Hansen, A.G., Steffensen, R., Jacobsen, C., Jensenius, J.C., Thiel, S., MAp44, a human protein associated with pattern recognition molecules of the complement system and regulating the lectin pathway of complement activation. J Immunol 183:11 (2009), 7371–7378.
21. Medof, M.E., Kinoshita, T., Nussenzweig, V., Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes. J Exp Med 160 (1984), 1558–1578.
22. Rollins, S.A., Sims, P.J., The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J Immunol 144:9 (1990), 3478–3483.
23. Delvaeye, M., Conway, E.M., Coagulation and innate immune responses: can we view them separately?. Blood 114:12 (2009), 2367–2374.
24. Brodsky, R.A., Paroxysmal nocturnal hemoglobinuria. Blood 124:18 (2014), 2804–2811.
25. Schrezenmeier, H., Muus, P., Socie, G., Szer, J., Urbano-Ispizua, A., Maciejewski, J.P., et al. Baseline characteristics and disease burden in patients in the international paroxysmal nocturnal hemoglobinuria registry. Haematologica 99:5 (2014), 922–929.
26. Hill, A., Kelly, R.J., Hillmen, P., Thrombosis in paroxysmal nocturnal hemoglobinuria. Blood 121:25 (2013), 4985–4996.
27. Yamashina, M., Ueda, E., Kinoshita, T., Takami, T., Ojima, A., Ono, H., et al. Inherited comlete deficiency of 20-kilodalton homologous restriction factor (CD59) as a cause of paroxysmal nocturnal hemoglobinuria. N Engl J Med 323:17 (1990), 1184–1189.
28. Nevo, Y., Ben-Zeev, B., Tabib, A., Straussberg, R., Anikster, Y., Shorer, Z., et al. CD59 deficiency is associated with chronic hemolysis and childhood relapsing immune-mediated polyneuropathy. Blood 121:1 (2013), 129–135.
29. Schatz-Jakobsen, J.A., Zhang, Y., Johnson, K., Neill, A., Sheridan, D., Andersen, G.R., Structural basis for eculizumab-mediated inhibition of the complement terminal pathway. J Immunol 197:1 (2016), 337–344.
30. Hill, A., Hillmen, P., Richards, S.J., Elebute, D., Marsh, J.C., Chan, J., et al. Sustained response and long-term safety of eculizumab in paroxysmal nocturnal hemoglobinuria. Blood 106:7 (2005), 2559–2565.
31. Rother, R.P., Rollins, S.A., Mojcik, C.F., Brodsky, R.A., Bell, L., Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol 25:11 (2007), 1256–1264.
32. Hillmen, P., Young, N.S., Schubert, J., Brodsky, R.A., Socie, G., Muus, P., et al. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. N Engl J Med 355:12 (2006), 1233–1243.
33. Brodsky, R.A., Young, N.S., Antonioli, E., Risitano, A.M., Schrezenmeier, H., Schubert, J., et al. Multicenter phase 3 study of the complement inhibitor eculizumab for the treatment of patients with paroxysmal nocturnal hemoglobinuria. Blood 111:4 (2008), 1840–1847.
34. Hochsmann, B., Dohna-Schwake, C., Kyrieleis, H.A., Pannicke, U., Schrezenmeier, H., Targeted therapy with eculizumab for inherited CD59 deficiency. N Engl J Med 370:1 (2014), 90–92.
35. Krawitz, P.M., Hochsmann, B., Murakami, Y., Teubner, B., Kruger, U., Klopocki, E., et al. A case of paroxysmal nocturnal hemoglobinuria caused by a germline mutation and a somatic mutation in PIGT. Blood 122:7 (2013), 1312–1315.
36. Risitano, A.M., Notaro, R., Marando, L., Serio, B., Ranaldi, D., Seneca, E., et al. Complement fraction 3 binding on erythrocytes as additional mechanism of disease in paroxysmal nocturnal hemoglobinuria patients treated by eculizumab. Blood 113:17 (2009), 4094–4100.
37. Hill, A., Rother, R.P., Arnold, L., Kelly, R., Cullen, M.J., Richards, S.J., et al. Eculizumab prevents intravascular hemolysis in patients with paroxysmal nocturnal hemoglobinuria and unmasks low-level extravascular hemolysis occurring through C3 opsonization. Haematologica 95:4 (2010), 567–573.
38. DeZern, A.E., Dorr, D., Brodsky, R.A., Predictors of hemoglobin response to eculizumab therapy in paroxysmal nocturnal hemoglobinuria. Eur J Haematol 90:1 (2013), 16–24.
39. Rondelli, T., Risitano, A.M., Peffault de Latour, R., Sica, M., Peruzzi, B., Ricci, P., et al. Polymorphism of the complement receptor 1 gene correlates with hematological response to eculizumab in patients with paroxysmal nocturnal hemoglobinuria. Haematologica 99:2 (2014), 262–266.
40. Nishimura, J., Yamamoto, M., Hayashi, S., Ohyashiki, K., Ando, K., Brodsky, A.L., et al. Genetic variants in C5 and poor response to eculizumab. N Engl J Med 370:7 (2014), 632–639.
41. Brodsky, R.A., How I treat paroxysmal nocturnal hemoglobinuria. Blood 113:26 (2009), 6522–6527.
42. Hillmen, P., Muus, P., Duhrsen, U., Risitano, A.M., Schubert, J., Luzzatto, L., et al. Effect of the complement inhibitor eculizumab on thromboembolism in patients with paroxysmal nocturnal hemoglobinuria. Blood 110:12 (2007), 4123–4128.
43. Hillmen, P., Muus, P., Roth, A., Elebute, M.O., Risitano, A.M., Schrezenmeier, H., et al. Long-term safety and efficacy of sustained eculizumab treatment in patients with paroxysmal nocturnal haemoglobinuria. Br J Haematol 162:1 (2013), 62–73.
44. Nester, C.M., Barbour, T., de Cordoba, S.R., Dragon-Durey, M.A., Fremeaux-Bacchi, V., Goodship, T.H., et al. Atypical aHUS: state of the art. Mol Immunol 67:1 (2015), 31–42.
45. George, J.N., Nester, C.M., Syndromes of thrombotic microangiopathy. N Engl J Med 371:7 (2014), 654–666.
46. Noris, M., Remuzzi, G., Genetics and genetic testing in hemolytic uremic syndrome/thrombotic thrombocytopenic purpura. Semin Nephrol 30:4 (2010), 395–408.
47. Cataland, S.R., Wu, H.M., Diagnosis and management of complement mediated thrombotic microangiopathies. Blood Rev 28:2 (2014), 67–74.
48. Gavriilaki, E., Yuan, X., Ye, Z., Ambinder, A.J., Shanbhag, S.P., Streiff, M.B., et al. Modified ham test for atypical hemolytic uremic syndrome. Blood 125:23 (2015), 3637–3646.
49. Brady, T.M., Pruette, C., Loeffler, L.F., Weidemann, D., Strouse, J.J., Gavriilaki, E., et al. Typical Hus: evidence of acute phase complement activation from a daycare outbreak. J Clin Exp Nephrol, 2016, 1(2).
50. Poolpol, K., Orth-Holler, D., Speth, C., Zipfel, P.F., Skerka, C., de Cordoba, S.R., et al. Interaction of Shiga toxin 2 with complement regulators of the factor H protein family. Mol Immunol 58:1 (2014), 77–84.
51. Rodriguez de Cordoba, S., Hidalgo, M.S., Pinto, S., Tortajada, A., Genetics of atypical hemolytic uremic syndrome (aHUS). Semin Thromb Hemost 40:4 (2014), 422–430.
52. Caprioli, J., Noris, M., Brioschi, S., Pianetti, G., Castelletti, F., Bettinaglio, P., et al. Genetics of HUS: the impact of MCP, CFH, and IF mutations on clinical presentation, response to treatment, and outcome. Blood 108:4 (2006), 1267–1279.
53. Sullivan, M., Rybicki, L.A., Winter, A., Hoffmann, M.M., Reiermann, S., Linke, H., et al. Age-related penetrance of hereditary atypical hemolytic uremic syndrome. Ann Hum Genet 75:6 (2011), 639–647.
54. Sansbury, F.H., Cordell, H.J., Bingham, C., Bromilow, G., Nicholls, A., Powell, R., et al. Factors determining penetrance in familial atypical haemolytic uraemic syndrome. J Med Genet 51:11 (2014), 756–764.
55. Bresin, E., Rurali, E., Caprioli, J., Sanchez-Corral, P., Fremeaux-Bacchi, V., Rodriguez de Cordoba, S., et al. Combined complement gene mutations in atypical hemolytic uremic syndrome influence clinical phenotype. J Am Soc Nephrol 24:3 (2013), 475–486.
56. Bhattacharjee, A., Reuter, S., Trojnar, E., Kolodziejczyk, R., Seeberger, H., Hyvarinen, S., et al. The major autoantibody epitope on factor H in atypical hemolytic uremic syndrome is structurally different from its homologous site in factor H-related protein 1, supporting a novel model for induction of autoimmunity in this disease. J Biol Chem 290:15 (2015), 9500–9510.
57. Warwicker, P., Goodship, T.H., Donne, R.L., Pirson, Y., Nicholls, A., Ward, R.M., et al. Genetic studies into inherited and sporadic hemolytic uremic syndrome. Kidney Int 53:4 (1998), 836–844.
58. Hellwage, J., Jokiranta, T.S., Friese, M.A., Wolk, T.U., Kampen, E., Zipfel, P.F., et al. Complement C3b/C3d and cell surface polyanions are recognized by overlapping binding sites on the most carboxyl-terminal domain of complement factor H. J Immunol 169:12 (2002), 6935–6944.
59. Bhattacharjee, A., Lehtinen, M.J., Kajander, T., Goldman, A., Jokiranta, T.S., Both domain 19 and domain 20 of factor H are involved in binding to complement C3b and C3d. Mol Immunol 47:9 (2010), 1686–1691.
60. Clark, S.J., Ridge, L.A., Herbert, A.P., Hakobyan, S., Mulloy, B., Lennon, R., et al. Tissue-specific host recognition by complement factor H is mediated by differential activities of its glycosaminoglycan-binding regions. J Immunol 190:5 (2013), 2049–2057.
61. Blaum, B.S., Hannan, J.P., Herbert, A.P., Kavanagh, D., Uhrin, D., Stehle, T., Structural basis for sialic acid-mediated self-recognition by complement factor H. Nat Chem Biol 11:1 (2015), 77–82.
62. Diaz-Guillen, M.A., Rodriguez de Cordoba, S., Heine-Suner, D., A radiation hybrid map of complement factor H and factor H-related genes. Immunogenetics 49:6 (1999), 549–552.
63. Heinen, S., Sanchez-Corral, P., Jackson, M.S., Strain, L., Goodship, J.A., Kemp, E.J., et al. De novo gene conversion in the RCA gene cluster (1q32) causes mutations in complement factor H associated with atypical hemolytic uremic syndrome. Hum Mutat 27:3 (2006), 292–293.
64. Venables, J.P., Strain, L., Routledge, D., Bourn, D., Powell, H.M., Warwicker, P., et al. Atypical haemolytic uraemic syndrome associated with a hybrid complement gene. PLoS Med, 3(10), 2006, e431.
65. Maga, T.K., Meyer, N.C., Belsha, C., Nishimura, C.J., Zhang, Y., Smith, R.J., A novel deletion in the RCA gene cluster causes atypical hemolytic uremic syndrome. Nephrol Dial Transplant 26:2 (2011), 739–741.
66. Challis, R.C., Araujo, G.S., Wong, E.K., Anderson, H.E., Awan, A., Dorman, A.M., et al. A de novo deletion in the regulators of complement activation cluster producing a hybrid complement factor H/complement factor H-related 3 Gene in atypical hemolytic uremic syndrome. J Am Soc Nephrol 27:6 (2016), 1617–1624.
67. Fremeaux-Bacchi, V., Dragon-Durey, M.A., Blouin, J., Vigneau, C., Kuypers, D., Boudailliez, B., et al. Complement factor I: a susceptibility gene for atypical haemolytic uraemic syndrome. J Med Genet, 41(6), 2004, e84.
68. Nilsson, S.C., Kalchishkova, N., Trouw, L.A., Fremeaux-Bacchi, V., Villoutreix, B.O., Blom, A.M., Mutations in complement factor I as found in atypical hemolytic uremic syndrome lead to either altered secretion or altered function of factor I. Eur J Immunol 40:1 (2010), 172–185.
69. Bienaime, F., Dragon-Durey, M.A., Regnier, C.H., Nilsson, S.C., Kwan, W.H., Blouin, J., et al. Mutations in components of complement influence the outcome of factor I-associated atypical hemolytic uremic syndrome. Kidney Int 77:4 (2010), 339–349.
70. Alba-Dominguez, M., Lopez-Lera, A., Garrido, S., Nozal, P., Gonzalez-Granado, I., Melero, J., et al. Complement factor I deficiency: a not so rare immune defect: characterization of new mutations and the first large gene deletion. Orphanet J Rare Dis, 7, 2012, 42.
71. Gleeson, P.J., Wilson, V., Cox, T.E., Sharma, S.D., Smith-Jackson, K., Strain, L., et al. Chromosomal rearrangement - a rare cause of complement factor I associated atypical haemolytic uraemic syndrome. Immunobiol 221:10 (2016), 1124–1130.
72. Richards, A., Kemp, E.J., Liszewski, M.K., Goodship, J.A., Lampe, A.K., Decorte, R., et al. Mutations in human complement regulator, membrane cofactor protein (CD46), predispose to development of familial hemolytic uremic syndrome. Proc Natl Acad Sci U S A 100:22 (2003), 12966–12971.
73. Noris, M., Brioschi, S., Caprioli, J., Todeschini, M., Bresin, E., Porrati, F., et al. International registry of R, familial HT: familial haemolytic uraemic syndrome and an MCP mutation. Lancet 362:9395 (2003), 1542–1547.
74. Liszewski, M.K., Atkinson, J.P., Complement regulator CD46: genetic variants and disease associations. Hum Genomics, 9, 2015, 7.
75. Blom, A.M., Bergstrom, F., Edey, M., Diaz-Torres, M., Kavanagh, D., Lampe, A., et al. A novel non-synonymous polymorphism (p.Arg240His) in C4b-binding protein is associated with atypical hemolytic uremic syndrome and leads to impaired alternative pathway cofactor activity. J Immunol 180:9 (2008), 6385–6391.
76. Marinozzi, M.C., Vergoz, L., Rybkine, T., Ngo, S., Bettoni, S., Pashov, A., et al. Complement factor B mutations in atypical hemolytic uremic syndrome-disease-relevant or benign?. J Am Soc Nephrol 25:9 (2014), 2053–2065.
77. Lemaire, M., Fremeaux-Bacchi, V., Schaefer, F., Choi, M., Tang, W.H., Le Quintrec, M., et al. Recessive mutations in DGKE cause atypical hemolytic-uremic syndrome. Nat Genet 45:5 (2013), 531–536.
78. Bruneau, S., Neel, M., Roumenina, L.T., Frimat, M., Laurent, L., Fremeaux-Bacchi, V., et al. Loss of DGKepsilon induces endothelial cell activation and death independently of complement activation. Blood 125:6 (2015), 1038–1046.
79. Jozsi, M., Reuter, S., Nozal, P., Lopez-Trascasa, M., Sanchez-Corral, P., Prohaszka, Z., et al. Autoantibodies to complement components in C3 glomerulopathy and atypical hemolytic uremic syndrome. Immunol Lett 160:2 (2014), 163–171.
80. Abarrategui-Garrido, C., Martinez-Barricarte, R., Lopez-Trascasa, M., de Cordoba, S.R., Sanchez-Corral, P., Characterization of complement factor H-related (CFHR) proteins in plasma reveals novel genetic variations of CFHR1 associated with atypical hemolytic uremic syndrome. Blood 114:19 (2009), 4261–4271.
81. Jozsi, M., Strobel, S., Dahse, H.M., Liu, W.S., Hoyer, P.F., Oppermann, M., et al. Anti factor H autoantibodies block C-terminal recognition function of factor H in hemolytic uremic syndrome. Blood 110:5 (2007), 1516–1518.
82. Fremeaux-Bacchi, V., Fakhouri, F., Garnier, A., Bienaime, F., Dragon-Durey, M.A., Ngo, S., et al. Genetics and outcome of atypical hemolytic uremic syndrome: a nationwide French series comparing children and adults. Clin J Am Soc Nephrol 8:4 (2013), 554–562.
83. Legendre, C.M., Licht, C., Muus, P., Greenbaum, L.A., Babu, S., Bedrosian, C., et al. Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. N Engl J Med 368:23 (2013), 2169–2181.
84. Ardissino, G., Testa, S., Possenti, I., Tel, F., Paglialonga, F., Salardi, S., et al. Discontinuation of eculizumab maintenance treatment for atypical hemolytic uremic syndrome: a report of 10 cases. Am J Kidney Dis 64:4 (2014), 633–637.
85. Sahutoglu, T., Basturk, T., Sakaci, T., Koc, Y., Ahbap, E., Sevinc, M., et al. Can eculizumab be discontinued in aHUS?: case report and review of the literature. Medicine (Baltimore), 95(31), 2016, e4330.
86. Weinstein, L., Syndrome of hemolysis, elevated liver enzymes, and low platelet count: a severe consequence of hypertension in pregnancy. Am J Obstet Gynecol 142:2 (1982), 159–167.
87. Fang, C.J., Richards, A., Liszewski, M.K., Kavanagh, D., Atkinson, J.P., Advances in understanding of pathogenesis of aHUS and HELLP. Br J Haematol 143:3 (2008), 336–348.
88. Vaught, A.J., Gavriilaki, E., Hueppchen, N., Blakemore, K., Yuan, X., Seifert, S.M., et al. Direct evidence of complement activation in HELLP syndrome: a link to atypical hemolytic uremic syndrome. Exp Hematol 44:5 (2016), 390–398.
89. Salmon, J.E., Heuser, C., Triebwasser, M., Liszewski, M.K., Kavanagh, D., Roumenina, L., et al. Mutations in complement regulatory proteins predispose to preeclampsia: a genetic analysis of the PROMISSE cohort. PLoS Med, 8(3), 2011, e1001013.
90. Fakhouri, F., Jablonski, M., Lepercq, J., Blouin, J., Benachi, A., Hourmant, M., et al. Factor H, membrane cofactor protein, and factor I mutations in patients with hemolysis, elevated liver enzymes, and low platelet count syndrome. Blood 112:12 (2008), 4542–4545.
91. Fakhouri, F., Roumenina, L., Provot, F., Sallee, M., Caillard, S., Couzi, L., et al. Pregnancy-associated hemolytic uremic syndrome revisited in the era of complement gene mutations. J Am Soc Nephrol 21:5 (2010), 859–867.
92. Fitzpatrick, K.E., Hinshaw, K., Kurinczuk, J.J., Knight, M., Risk factors, management, and outcomes of hemolysis, elevated liver enzymes, and low platelets syndrome and elevated liver enzymes, low platelets syndrome. Obstet Gynecol 123:3 (2014), 618–627.
93. Martin, J.N. Jr., Rose, C.H., Briery, C.M., Understanding and managing HELLP syndrome: the integral role of aggressive glucocorticoids for mother and child. Am J Obstet Gynecol 195:4 (2006), 914–934.
94. Burwick, R.M., Feinberg, B.B., Eculizumab for the treatment of preeclampsia/HELLP syndrome. Placenta 34:2 (2013), 201–203.
95. Randen, U., Troen, G., Tierens, A., Steen, C., Warsame, A., Beiske, K., et al. Primary cold agglutinin-associated lymphoproliferative disease: a B-cell lymphoma of the bone marrow distinct from lymphoplasmacytic lymphoma. Haematologica 99:3 (2014), 497–504.
96. Berentsen, S., Ulvestad, E., Gjertsen, B.T., Hjorth-Hansen, H., Langholm, R., Knutsen, H., et al. Rituximab for primary chronic cold agglutinin disease: a prospective study of 37 courses of therapy in 27 patients. Blood 103:8 (2004), 2925–2928.
97. Berentsen, S., Randen, U., Vagan, A.M., Hjorth-Hansen, H., Vik, A., Dalgaard, J., et al. High response rate and durable remissions following fludarabine and rituximab combination therapy for chronic cold agglutinin disease. Blood 116:17 (2010), 3180–3184.
98. Shi, J., Rose, E.L., Singh, A., Hussain, S., Stagliano, N.E., Parry, G.C., et al. TNT003, an inhibitor of the serine protease C1s, prevents complement activation induced by cold agglutinins. Blood 123:26 (2014), 4015–4022.