Paroxysmal nocturnal hemoglobinuria

Blood

Volumn 124, Issue 18, 2014, Pages 2804-2811

  Brodsky, Robert A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CD59 ANTIGEN; CYCLOPHOSPHAMIDE; DECAY ACCELERATING FACTOR; ECULIZUMAB; GLYCAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; PHOSPHATIDYLINOSITOL GLYCAN CLASS A; UNCLASSIFIED DRUG; GLYCOSYLPHOSPHATIDYLINOSITOL;

BIOSYNTHESIS; BONE MARROW DEPRESSION; BONE MARROW TRANSPLANTATION; COMPLEMENT ACTIVATION; CONGENITAL MALFORMATION; CYTOPENIA; DRUG MEGADOSE; DYSTONIA; HEMOLYSIS; HEMOLYTIC ANEMIA; HUMAN; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PROTEIN DEFICIENCY; REVIEW; SEIZURE; SOMATIC MUTATION; THROMBOSIS; GENETICS; HEMOGLOBINURIA, PAROXYSMAL; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGIC MONITORING;

BONE MARROW TRANSPLANTATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEMOGLOBINURIA, PAROXYSMAL; HUMANS; MONITORING, PHYSIOLOGIC; MUTATION;

EID: 84908565749     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-02-522128     Document Type: Review

References (87)

1. Brodsky RA. Narrative review: paroxysmal nocturnal hemoglobinuria: the physiology of complement-related hemolytic anemia. Ann Intern Med. 2008; 148(8):587-595.
2. Parker CJ. Historical aspects of paroxysmal nocturnal haemoglobinuria: 'defining the disease'. Br J Haematol. 2002; 117(1):3-22.
3. Socié G, Mary JY, de Gramont A, et al.; French Society of Haematology. Paroxysmal nocturnal haemoglobinuria: long-term follow-up and prognostic factors. Lancet. 1996; 348(9027): 573-577.
4. Nishimura J, Kanakura Y, Ware R.E., et al. Clinical course and flow cytometric analysis of paroxysmal nocturnal hemoglobinuria in the United States and Japan. Medicine (Baltimore). 2004; 83(3):193-207.
5. Strubing P. Paroxysmale haemoglobinurie. Dtsch Med Wochenschr. 1882; 8:1-16.
6. Enneking J. Eine neue form intermittierender haemoglobinurie (Haemoglobinuria paroxysmalis nocturia). Klin Wochenschr. 1928; 7:2045.
7. Ham T. Chronic hemolytic anemia with paroxysmal nocturnal hemoglobinuria. A study of the mechanism of hemolysisin relation to acid-base equilibrium. N Engl J Med. 1937; 217(23): 915-917.
8. Takeda J, Miyata T, Kawagoe K., et al. Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell. 1993; 73(4):703-711.
9. Miyata T, Takeda J, Iida Y., et al. The cloning of PIG-A, a component in the early step of GPI-anchor biosynthesis. Science. 1993; 259(5099):1318-1320.
10. Miyata T, Yamada N, Iida Y., et al. Abnormalities of PIG-A transcripts in granulocytes from patients with paroxysmal nocturnal hemoglobinuria. N Engl J Med. 1994; 330(4): 249-255.
11. Bessler M, Mason PJ, Hillmen P, et al. Paroxysmal nocturnal haemoglobinuria (PNH) is caused by somatic mutations in the PIG-A gene. EMBO J. 1994; 13(1):110-117.
12. Rother RP, Rollins SA, Mojcik C.F., Brodsky RA, Bell L. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol. 2007; 25(11):1256-1264.
13. Diep DB, Nelson KL, Raja S.M., Pleshak EN, Buckley JT. Glycosylphosphatidylinositol anchors of membrane glycoproteins are binding determinants for the channel-forming toxin aerolysin. J Biol Chem. 1998; 273(4):2355-2360.
14. Brodsky RA, Mukhina GL, Nelson K.L., Lawrence TS, Jones RJ, Buckley JT. Resistance of paroxysmal nocturnal hemoglobinuria cells to the glycosylphosphatidylinositol-binding toxin aerolysin. Blood. 1999; 93(5):1749-1756.
15. Medof ME, 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. 1984; 160(5):1558-1578.
16. Rollins SA, Sims PJ. The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J Immunol. 1990; 144(9):3478-3483.
17. Lublin DM, Atkinson JP. Decay-accelerating factor: biochemistry, molecular biology, and function. Annu Rev Immunol. 1989; 7:35-58.
18. Risitano AM, Notaro R, Marando L., et al. Complement fraction 3 binding on erythrocytes as additional mechanism of disease in paroxysmal nocturnal hemoglobinuria patients treated by eculizumab. Blood. 2009; 113(17):4094-4100.
19. Fujita M, Kinoshita T. GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim Biophys Acta. 2012; 1821(8):1050-1058.
20. Nagarajan S, Brodsky RA, Young N.S., Medof ME. Genetic defects underlying paroxysmal nocturnal hemoglobinuria that arises out of aplastic anemia. Blood. 1995; 86(12):4656-4661.
21. Bessler M, Hillmen P, Longo L., Luzzatto L, Mason PJ. Genomic organization of the X-linked gene (PIG-A) that is mutated in paroxysmal nocturnal haemoglobinuria and of a related autosomal pseudogene mapped to 12q21. Hum Mol Genet. 1994; 3(5):751-757.
22. Nafa K, Mason PJ, Hillmen P, Luzzatto L., Bessler M. Mutations in the PIG-A gene causing paroxysmal nocturnal hemoglobinuria are mainly of the frameshift type. Blood. 1995; 86(12):4650-4655.
23. Oni SB, Osunkoya BO, Luzzatto L. Paroxysmal nocturnal hemoglobinuria: evidence for monoclonal origin of abnormal red cells. Blood. 1970; 36(2):145-152.
24. Hu R, Mukhina GL, Piantadosi S, Barber J.P., Jones RJ, Brodsky RA. PIG-A mutations in normal hematopoiesis. Blood. 2005; 105(10):3848-3854.
25. Dameshek W. Riddle: what do aplastic anemia, paroxysmal nocturnal hemoglobinuria (PNH) and "hypoplastic" leukemia have in common? [Editorial] Blood. 1967; 30(2):251-254.
26. Luzzatto L, Bessler M, Rotoli B. Somatic mutations in paroxysmal nocturnal hemoglobinuria: a blessing in disguise? Cell. 1997; 88(1):1-4.
27. Young NS. The problem of clonality in aplastic anemia: Dr Dameshek's riddle, restated. Blood. 1992; 79(6):1385-1392.
28. Hanaoka N, Kawaguchi T, Horikawa K., Nagakura S, Mitsuya H, Nakakuma H. Immunoselection by natural killer cells of PIGA mutant cells missing stress-inducible ULBP. Blood. 2006; 107(3): 1184-1191.
29. Hanaoka N, Nakakuma H, Horikawa K., et al. NKG2D-mediated immunity underlying paroxysmal nocturnal haemoglobinuria and related bone marrow failure syndromes. Br J Haematol. 2009; 146(5):538-545.
30. Gargiulo L, Papaioannou M, Sica M., et al. Glycosylphosphatidylinositol-specific, CD1d-restricted T cells in paroxysmal nocturnal hemoglobinuria. Blood. 2013; 121(14):2753-2761.
31. Inoue N, Izui-Sarumaru T, Murakami Y., et al. Molecular basis of clonal expansion of hematopoiesis in 2 patients with paroxysmal nocturnal hemoglobinuria (PNH). Blood. 2006; 108(13):4232-4236.
32. Yamashina M, Ueda E, Kinoshita T., et al. Inherited complete deficiency of 20-kilodalton homologous restriction factor (CD59) as a cause of paroxysmal nocturnal hemoglobinuria. N Engl J Med. 1990; 323(17):1184-1189.
33. Nevo Y, Ben-Zeev B, Tabib A., et al. CD59 deficiency is associated with chronic hemolysis and childhood relapsing immune-mediated polyneuropathy. Blood. 2013; 121(1):129-135.
34. Krawitz PM, Höchsmann B, Murakami Y., et al. A case of paroxysmal nocturnal hemoglobinuria caused by a germline mutation and a somatic mutation in PIGT. Blood. 2013; 122(7):1312-1315.
35. Ohishi K, Inoue N, Kinoshita T. PIG-S and PIG-T, essential for GPI anchor attachment to proteins, form a complex with GAA1 and GPI8. EMBO J. 2001; 20(15):4088-4098.
36. Ohishi K, Nagamune K, Maeda Y., Kinoshita T. Two subunits of glycosylphosphatidylinositol transamidase, GPI8 and PIG-T, form a functionally important intermolecular disulfide bridge. J Biol Chem. 2003; 278(16):13959-13967.
37. Höchsmann B, Dohna-Schwake C, Kyrieleis H.A., Pannicke U., Schrezenmeier H. Targeted therapy with eculizumab for inherited CD59 deficiency. N Engl J Med. 2014; 370(1):90-92.
38. Araten DJ, Nafa K, Pakdeesuwan K., Luzzatto L. Clonal populations of hematopoietic cells with paroxysmal nocturnal hemoglobinuria genotype and phenotype are present in normal individuals. Proc Natl Acad Sci USA. 1999; 96(9):5209-5214.
39. Kaiafa G, Papadopoulos A, Ntaios G., et al. Detection of CD55- and CD59-deficient granulocytic populations in patients with myelodysplastic syndrome. Ann Hematol. 2008; 87(4):257-262.
40. Dunn DE, Tanawattanacharoen P, Boccuni P., et al. Paroxysmal nocturnal hemoglobinuria cells in patients with bone marrow failure syndromes. Ann Intern Med. 1999; 131(6):401-408.
41. Raza A, Ravandi F, Rastogi A., et al. A prospective multicenter study of paroxysmal nocturnal hemoglobinuria cells in patients with bone marrow failure. Cytometry B Clin Cytom. 2013.
42. Pu JJ, Hu R, Mukhina G.L., Carraway HE, McDevitt MA, Brodsky RA. The small population of PIG-A mutant cells in myelodysplastic syndromes do not arise from multipotent hematopoietic stem cells. Haematologica. 2012; 97(8):1225-1233.
43. Kawagoe K, Kitamura D, Okabe M., et al. Glycosylphosphatidylinositol-anchor-deficient mice: implications for clonal dominance of mutant cells in paroxysmal nocturnal hemoglobinuria. Blood. 1996; 87(9):3600-3606.
44. Rosti V, Tremml G, Soares V., Pandolfi PP, Luzzatto L, Bessler M. Murine embryonic stem cells without pig-a gene activity are competent for hematopoiesis with the PNH phenotype but not for clonal expansion. J Clin Invest. 1997; 100(5): 1028-1036.
45. Yuan X, Braunstein EM, Ye Z, et al. Generation of glycosylphosphatidylinositol anchor protein-deficient blood cells from human induced pluripotent stem cells. Stem Cells Transl Med. 2013; 2(11):819-829.
46. Johnston JJ, Gropman AL, Sapp J.C., et al. The phenotype of a germline mutation in PIGA: the gene somatically mutated in paroxysmal nocturnal hemoglobinuria. Am J Hum Genet. 2012; 90(2): 295-300.
47. van der Crabben SN, Harakalova M, Brilstra E.H., et al. Expanding the spectrum of phenotypes associated with germline PIGA mutations: a child with developmental delay, accelerated linear growth, facial dysmorphisms, elevated alkaline phosphatase, and progressive CNS abnormalities. Am J Med Genet A. 2014; 164A(1): 29-35.
48. Swoboda KJ, Margraf RL, Carey J.C., et al. A novel germline PIGA mutation in Ferro-Cerebro-Cutaneous syndrome: a neurodegenerative X-linked epileptic encephalopathy with systemic iron-overload. Am J Med Genet A. 2014; 164A(1): 17-28.
49. Belet S, Fieremans N, Yuan X., et al. Early frameshift mutation in PIGA identified in a large XLID family without neonatal lethality. Hum Mutat. 2014; 35(3):350-355.
50. Hall SE, Rosse WF. The use of monoclonal antibodies and flow cytometry in the diagnosis of paroxysmal nocturnal hemoglobinuria. Blood. 1996; 87(12):5332-5340.
51. Brodsky RA. How I treat paroxysmal nocturnal hemoglobinuria. Blood. 2009; 113(26):6522-6527.
52. Brodsky RA, Mukhina GL, Li S, et al. Improved detection and characterization of paroxysmal nocturnal hemoglobinuria using fluorescent aerolysin. Am J Clin Pathol. 2000; 114(3):459-466.
53. Borowitz MJ, Craig FE, Digiuseppe J.A., et al.; Clinical Cytometry Society. Guidelines for the diagnosis and monitoring of paroxysmal nocturnal hemoglobinuria and related disorders by flow cytometry. Cytometry B Clin Cytom. 2010; 78(4): 211-230.
54. Parker C, Omine M, Richards S., et al.; International PNH Interest Group. Diagnosis and management of paroxysmal nocturnal hemoglobinuria. Blood. 2005; 106(12):3699-3709.
55. Mukhina GL, Buckley JT, Barber J.P., Jones RJ, Brodsky RA. Multilineage glycosylphosphatidylinositol anchor-deficient haematopoiesis in untreated aplastic anaemia. Br J Haematol. 2001; 115(2):476-482.
56. Pu JJ, Mukhina G, Wang H., Savage WJ, Brodsky RA. Natural history of paroxysmal nocturnal hemoglobinuria clones in patients presenting as aplastic anemia. Eur J Haematol. 2011; 87(1): 37-45.
57. Hill A, Kelly RJ, Hillmen P. Thrombosis in paroxysmal nocturnal hemoglobinuria. Blood. 2013; 121(25):4985-4996.
58. Wiedmer T, Hall SE, Ortel T.L., Kane WH, Rosse WF, Sims PJ. Complement-induced vesiculation and exposure of membrane prothrombinase sites in platelets of paroxysmal nocturnal hemoglobinuria. Blood. 1993; 82(4):1192-1196.
59. Rother RP, Bell L, Hillmen P., Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA. 2005; 293(13):1653-1662.
60. Ritis K, Doumas M, Mastellos D., et al. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J Immunol. 2006; 177(7):4794-4802.
61. Rønne E, Pappot H., Grøndahl-Hansen J, et al. The receptor for urokinase plasminogen activator is present in plasma from healthy donors and elevated in patients with paroxysmal nocturnal haemoglobinuria. Br J Haematol. 1995; 89(3): 576-581.
62. Maroney SA, Cunningham AC, Ferrel J, et al. A GPI-anchored co-receptor for tissue factor pathway inhibitor controls its intracellular trafficking and cell surface expression. J Thromb Haemost. 2006; 4(5):1114-1124.
63. Hillmen P, Muus P, Dührsen U, et al. Effect of the complement inhibitor eculizumab on thromboembolism in patients with paroxysmal nocturnal hemoglobinuria. Blood. 2007; 110(12): 4123-4128.
64. Weitz IC, Razavi P, Rochanda L., et al. Eculizumab therapy results in rapid and sustained decreases in markers of thrombin generation and inflammation in patients with PNH independent of its effects on hemolysis and microparticle formation. Thromb Res. 2012; 130(3):361-368.
65. Moyo VM, Mukhina GL, Garrett E.S., Brodsky RA. Natural history of paroxysmal nocturnal haemoglobinuria using modern diagnostic assays. Br J Haematol. 2004; 126(1):133-138.
66. Emadi A, Brodsky RA. Successful discontinuation of anticoagulation following eculizumab administration in paroxysmal nocturnal hemoglobinuria. Am J Hematol. 2009; 84(10): 699-701.
67. Hillmen P, Elebute M, Kelly R., et al. Long-term effect of the complement inhibitor eculizumab on kidney function in patients with paroxysmal nocturnal hemoglobinuria. Am J Hematol. 2010; 85(8):553-559.
68. Hill A, Rother RP, Wang X, et al. Effect of eculizumab on haemolysis-associated nitric oxide depletion, dyspnoea, and measures of pulmonary hypertension in patients with paroxysmal nocturnal haemoglobinuria. Br J Haematol. 2010; 149(3):414-425.
69. Hill A, Sapsford RJ, Scally A, et al. Under-recognized complications in patients with paroxysmal nocturnal haemoglobinuria: raised pulmonary pressure and reduced right ventricular function. Br J Haematol. 2012; 158(3):409-414.
70. Hill A, Hillmen P, Richards S.J., et al. Sustained response and long-term safety of eculizumab in paroxysmal nocturnal hemoglobinuria. Blood. 2005; 106(7):2559-2565.
71. Hillmen P, Young NS, Schubert J, et al. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. N Engl J Med. 2006; 355(12):1233-1243.
72. Brodsky RA, Young NS, Antonioli E, et al. Multicenter phase 3 study of the complement inhibitor eculizumab for the treatment of patients with paroxysmal nocturnal hemoglobinuria. Blood. 2008; 111(4):1840-1847.
73. Hill A, Rother RP, Arnold L, et al. Eculizumab prevents intravascular hemolysis in patients with paroxysmal nocturnal hemoglobinuria and unmasks low-level extravascular hemolysis occurring through C3 opsonization. Haematologica. 2010; 95(4):567-573.
74. Hillmen P, Muus P, Röth A, et al. Long-term safety and efficacy of sustained eculizumab treatment in patients with paroxysmal nocturnal haemoglobinuria. Br J Haematol. 2013; 162(1): 62-73.
75. Kelly RJ, Hill A, Arnold L.M., et al. Long-term treatment with eculizumab in paroxysmal nocturnal hemoglobinuria: sustained efficacy and improved survival. Blood. 2011; 117(25): 6786-6792.
76. DeZern AE, Dorr D, Brodsky RA. Predictors of hemoglobin response to eculizumab therapy in paroxysmal nocturnal hemoglobinuria. Eur J Haematol. 2013; 90(1):16-24.
77. Rondelli T, Risitano AM, Peffault de Latour R, et al. Polymorphism of the complement receptor 1 gene correlates with hematological response to eculizumab in patients with paroxysmal nocturnal hemoglobinuria. Haematologica. 2014; 99(2): 262-266.
78. Nishimura J, Yamamoto M, Hayashi S., et al. Genetic variants in C5 and poor response to eculizumab. N Engl J Med. 2014; 370(7):632-639.
79. Peffault de Latour R, Schrezenmeier H, Bacigalupo A, et al. Allogeneic stem cell transplantation in paroxysmal nocturnal hemoglobinuria. Haematologica. 2012; 97(11): 1666-1673.
80. Brodsky RA. Stem cell transplantation for paroxysmal nocturnal hemoglobinuria. Haematologica. 2010; 95(6):855-856.
81. Antin JH, Ginsburg D, Smith B.R., Nathan DG, Orkin SH, Rappeport JM. Bone marrow transplantation for paroxysmal nocturnal hemoglobinuria: eradication of the PNH clone and documentation of complete lymphohematopoietic engraftment. Blood. 1985; 66(6):1247-1250.
82. Suenaga K, Kanda Y, Niiya H., et al. Successful application of nonmyeloablative transplantation for paroxysmal nocturnal hemoglobinuria. Exp Hematol. 2001; 29(5):639-642.
83. Brodsky RA, Luznik L, Bolaños-Meade J, Leffell MS, Jones RJ, Fuchs EJ. Reduced intensity HLA-haploidentical BMT with post transplantation cyclophosphamide in nonmalignant hematologic diseases. Bone Marrow Transplant. 2008; 42(8): 523-527.
84. Bolaños-Meade J., Fuchs EJ, Luznik L, et al. HLA-haploidentical bone marrow transplantation with posttransplant cyclophosphamide expands the donor pool for patients with sickle cell disease. Blood. 2012; 120(22):4285-4291.
85. Schrezenmeier H, Muus P, Socié G, et al. Baseline characteristics and disease burden in patients in the international paroxysmal nocturnal hemoglobinuria registry. Haematologica. 2014.
86. Lindorfer MA, Pawluczkowycz AW, Peek E.M., Hickman K., Taylor RP, Parker CJ. A novel approach to preventing the hemolysis of paroxysmal nocturnal hemoglobinuria: both complement-mediated cytolysis and C3 deposition are blocked by a monoclonal antibody specific for the alternative pathway of complement. Blood. 2010; 115(11): 2283-2291.
87. Risitano AM, Notaro R, Pascariello C., et al. The complement receptor 2/factor H fusion protein TT30 protects paroxysmal nocturnal hemoglobinuria erythrocytes from complement-mediated hemolysis and C3 fragment. Blood. 2012; 119(26): 6307-6316.