Stem cells in paroxysmal nocturnal haemoglobinuria and aplastic anaemia: Increasing evidence for overlap of haemopoietic defect

Transfusion Medicine

Volumn 13, Issue 6, 2003, Pages 377-386

  Marsh, Judith C W ^a   Elebute, M O ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Aplastic anaemia; Bone marrow failure; Haemopoietic stem cell; Paroxysmal nocturnal haemoglobinuria

Indexed keywords

APLASTIC ANEMIA; APOPTOSIS; AUTOIMMUNITY; BLOOD CELL; BONE MARROW CULTURE; BONE MARROW SUPPRESSION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CYTOTOXICITY; DISEASE ASSOCIATION; FLOW CYTOMETRY; GENE MUTATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMOLYSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PATHOGENESIS; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE;

ADULT; ANEMIA, APLASTIC; APOPTOSIS; AUTOIMMUNE DISEASES; BONE MARROW; CHILD; CLONE CELLS; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEMATOPOIETIC STEM CELLS; HEMOGLOBINURIA, PAROXYSMAL; HUMANS; MEMBRANE PROTEINS;

EID: 0348010274     PISSN: 09587578     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3148.2003.00465.x     Document Type: Review

References (88)

1. Araten, D.J., Nafa, K., Pakdeesuwan, K. & Luzzatto, L. (1999) Clonal populations of hematopoietic cells with paroxysmal nocturnal hemoglobinuria genotype and phenotype are present in normal individuals. Proceedings of the National Academy of Sciences, 96, 5209-5214.
2. Armstrong, C., Schubert, J., Ueda, E., Knez, J.J., Gelperin, D., Hirose, S., Silber, R., Hollan, S., Schmidt, R.E. & Medof, M.E. (1992) Affected paroxysmal nocturnal hemoglobinuria T lymphocytes harbor a common defect in assembly of N-acetyl-D-glucosamine inositol phospholipid corresponding to that in class A Thy-1-murine lymphoma mutants. Journal of Biological Chemistry, 267, 25347-25351.
3. Azenishi, Y., Ueda, E., Machin, T., Nishimura, J.-I., Hirota, T., Shibano, M., Nakao, S., Kinoshita, T., Mizoguchi, H. & Kitani, T. (1999) CD59-deficient blood cells and PIG-A gene abnormalities in Japanese patients with aplastic anaemia. British Journal of Haematology, 101, 90-93.
4. Bacigalupo, A., Figari, O., Tong, J., Piaggio, G., Miceli, S., Frassoni, F., Caciagli, P., Badolati, G. & Marmont, A.M. (1992) Long-term marrow culture in patients with aplastic anemia compared with marrow transplant recipients and normal controls. Experimental Hematology, 20, 425-430.
5. Ball, S.E., Gibson, F.M., Rizzo, S., Tooze, J.A., Marsh, J.C. & Gordon-Smith, E.C. (1998) Progressive telomere shortening in aplastic anaemia. Blood, 91, 3582-3592.
6. Bessler, M., Mason, P., Hillmen, P. & Luzzatto, L. (1994) Somatic mutations and cellular selection in paroxysmal nocturnal haemoglobinuria. Lancet, 343, 951-953.
7. Brodsky, R.A., Vala, M.S., Barber, J.P., Medof, M.E. & Jones, R.J. (1997) Resistance to apoptosis caused by PIG-A gene mutations in paroxysmal nocturnal hemoglobinuria. Proceedings of the National Academy of Sciences, 94, 8756-8760.
8. Brummendorf, T.H., Maciejewski, J.P., Mak, J., Young, N.S. & Lansdorp, P.M. (2001) Telomere length in leukocyte subpopulations of patients with aplastic anaemia. Blood, 97, 895-900.
9. Chen, G., Kirby, M., Zeng, W., Young, N.S. & Maciejewski, J.P. (2002) Superior growth of glycophosphatidylinositol-anchored protein-deficient progenitor cells in vitro is due to the higher apoptotic rate of progenitors with normal phenotype in vivo. Experimental Hematology, 30, 774-782.
10. Cox, C.V., Killick, S.B., Patel, S., Elebute, M.O., Marsh, J.C., Gordon-Smith, E.C., Gibson, F.M. (2000) In vitro proliferation and differentiation of megakaryocytic progenitors in patients with aplastic anemia, paroxysmal nocturnal hemoglobinuria, and the myelodysplastic syndromes. Stem Cells, 18, 428-434.
11. Dacie, J.V., (1963) Paroxysmal nocturnal haemoglobinuria. Proceedings of the Royal Society of Medicine, 56, 587-596.
12. De Planque, M.M., Bacigalupo, A. & Wursch, A. (1989) Long term follow up of severe aplastic anaemia patients treated with antithymocyte globulin. Severe aplastic anaemia working party of the European co-operative group for bone marrow transplantation (EBMT). British Journal of Haematology, 73, 121-126.
13. Dunn, D.E., Tanawattanacharoen, P., Boccuni, P., Nagakura, S., Green, S.W., Kirby, M.R., Anil Kumar, M.S., Rosenfeld, S. & Young, N.S. (1999) Paroxysmal nocturnal haemoglobinuria cells in patients with bone marrow failure syndromes. Annals of Internal Medicine, 131, 401-408.
14. Elebute, M.O., Rizzo, S., Tooze, J.A., Marsh, J.C.W., Gordon-Smith, E.C. & Gibson, F.M. (2003) Evaluation of the haemopoietic reservoir in de-novo haemolytic paroxysmal nocturnal haemoglobinuria. British Journal of Haematology, 123, 552-560.
15. Gibson, F.M. & Gordon-Smith, E.C. (1990) Long-term culture of aplastic anaemia bone marrow. British Journal of Haematology, 75, 421-427.
16. Heeney, M.M., Ormsbee, S.M., Moody, M.A., Howard, T.A., DeCastro, C.M. & Ware, R.E. (2003) Increased expression of anti-apoptosis genes in peripheral blood cells from patients with paroxysmal nocturnal haemoglobinuria. Molecular Genetics and Metabolism, 78, 291-294.
17. Hillmen, P., Bessler, M., Mason, P.J., Watkins, W.M. & Luzzatto, L. (1993) Specific defect in N-acetylglucosamine incorporation in the biosynthesis of the glycosylphosphatidylinositol anchor in cloned cell lines from patients with paroxysmal nocturnal hemoglobinuria. Proceedings of the National Academy of Sciences, 90, 5272-5276.
18. Hillmen, P., Lewis, S.M., Bessler, M., Luzzatto, L. & Dacie, J.V. (1995) Natural history of paroxysmal nocturnal hemoglobinuria. The New England Journal of Medicine, 333, 1253-1258.
19. Horikawa, K., Nakakuma, H., Kawaguchi, T., Iwamoto, N., Nagakura, S., Kagimoto, T. & Takatsuki, K. (1997) Apoptosis resistance of blood cells from patients with paroxysmal nocturnal hemoglobinuria, aplastic anemia, and myelodysplastic syndrome. Blood, 90, 2716-2722.
20. + cells of aplastic anaemia patients. Relationship with increased apoptosis and upregulation of Fas-antigen. British Journal of Haematology, 113, 706-712.
21. Josten, K.M., Tooze, J.A., Borthwick-Clarke, C., Gordon-Smith, E.C. & Rutherford, T.R. (1991) Acquired aplastic anemia and paroxysmal nocturnal hemoglobinuria: studies on clonality. Blood, 78, 3162-3167.
22. van Kamp, H., van Imhoff, G.W., de Wolf, J.T., Smit, J.W., Halie, M.R. & Vellenga, E. (1995) The effect of cyclosporine on haematological parameters in patients with paroxysmal nocturnal haemoglobinuria. British Journal of Haematology, 89, 79-82.
23. Karadimitris, A., Li, K., Notaro, R., Araten, D.J., Nafa, K., Thertulien, R., Ladanyi, M., Stevens, A.E., Rosenfeld, S., Roberts, I.A.G. & Luzzatto, L. (2001b) Association of clonal T-cell large granular lymphocyte disease and paroxysmal nocturnal haemoglobinuria (PNH): further evidence for a pathogenetic link between T cells, aplastic anaemia and PNH. British Journal of Haematology, 115, 1010-1014.
24. Karadimitris, A. & Luzzatto, L. (2001a) The cellular pathogenesis of paroxysmal nocturnal haemoglobinuria. Leukemia, 15, 1148-1152.
25. Karadimittis, A., Manavalan, J.S., Thaler, H.T., Notaro, R., Arata, D.J., Nafa, K., Roberts, I.A.G., Weksler, M.E. & Luzzatto, L. (2000) Abnormal T-cell repertoire is associated with immune process underlying the pathogenesis of paroxysmal nocturnal haemoglobinuria. Blood, 96, 2613-2620.
26. Killick, S.B., Cox, C.V., Marsh, J.C.W., Gordon-Smith, E.C. & Gibson, F.M. (2001) Mechanisms of bone marrow progenitor cell apoptosis in aplastic anaemia and the effect of antithymocyte globulin: examination of the role of the Fas-Fas L interaction. British Journal of Haematology, 111, 1164-1169.
27. + cells in aplastic anaemia and myelodysplasia. British Journal of Haematology, 108, 582-591.
28. Killick, S.B., Mufti, G., Cavenagh, J.D., Mijovic, A., Peacock, J.L., Gordon-Smith, E.C., Bowen, D.T. & Marsh, J.C.W. (2003) A pilot study of antithymocyte globulin (ATG) in the treatment of patients with 'low risk' myelodysplasia. British Journal of Haematology, 120, 679-684.
29. Kinoshita, T. (2003) Overview of paroxysmal nocturnal haemoglobinuria: molecular genetics. In: Paroxysmal Nocturnal Haemoglobinuria and Related Disorders Molecular Aspects of Pathogenesis (eds Omine, M. & Kinoshita, T.), 3-9. Springer-Verlag, Tokyo.
30. Kinoshita, T. & Inoue, N. (2001) Relationship between aplastic anaemia and paroxysmal nocturnal haemoglobinuria. International Journal of Hematology, 75, 117-122.
31. Kook, H., Risitano, A.M., Zeng, W., Wlodarski, M., Lottemann, C., Nakamura, R., Barrett, J., Young, N.S. & Maciejewski, J.P. (2002) Changes in T-cell receptor VB repertoire in aplastic anaemia: effect of different immunosuppressive regimens. Blood, 99, 3668-3675.
32. Lewis, S.M. & Dacie, J.V. (1967) The aplastic anaemia-paroxysmal nocturnal haemoglobinuria syndrome. British Journal of Haematology, 13, 236-251.
33. Li, J.-J., Kook, H. & Chung, I.-J., (2001) Telomere length changes in patients with aplastic anaemia. British Journal of Haematology, 112, 1025-1030.
34. Luzzatto, L., Bessler, M. & Rotoli, B. (1997) Somatic mutations in paroxysmal nocturnal hemoglobinuria: a blessing in disguise? Cell, 88, 1-4.
35. Luzzatto, L., Karadimitris, A., Araten, D. & Notaro, R. (2003) The role of lymphoid cells in the pathogenesis of PNH. In: Paroxysmal Nocturnal Haemoglobinuria: Molecular Aspects of Pathogenesis (eds Omine, M. & Kinoshita, T.), 105-116. Springer-Verlag, Tokyo.
36. Maciejewski, J.P., Anderson, S., Katevas, P. & Young, N.S. (1994) Phenotypic and functional analysis of bone marrow progenitor cell compartment in bone marrow failure. British Journal of Haematology, 87, 227-234.
37. Maciejewski, J.P., Follmann, D., Nakamura, R., Saunthararajah, Y., Rivera, C.E., Simonis, T., Brown, K.E., Barrett, J.A. & Young, N.S. (2001) Increased frequency of HLA-DR2 in patients with paroxysmal nocturnal haemoglobinuria and the PNH/aplastic anaemia syndrome. Blood, 98, 3513-3519.
38. + cells of patients with aplastic anaemia. British Journal of Haematology, 91, 245-252.
39. Maciejewski, J.P., Selleri, C., Sato, T., Anderson, S., Young, N.S. (1996) A severe and consistent deficit in marrow and circulating primitive hematopoietic cells (long-term culture-initiating cells) in acquired aplastic anemia. Blood, 88, 1983-1991.
40. Maciejewski, J.P., Sloand, E.M., Sato, T., Anderson, S. & Young, N.S. (1997) Impaired hematopoiesis in paroxysmal nocturnal hemoglobinuria/aplastic anemia is not associated with a selective proliferative defect in the glycosylphosphatidylinositol-anchored protein-deficient clone. Blood, 89, 1173-1181.
41. Marsh, J.C., Chang, J., Testa, N.G., Hows, J.M. & Dexter, T.M. (1990) The hematopoietic defect in aplastic anemia assessed by long-term marrow culture. Blood, 76, 1748-1757.
42. Marsh, J.C., Chang, J., Testa, N.G., Hows, J.M. & Dexter, T.M. (1991) In vitro assessment of marrow 'stem cell' and stromal cell function in aplastic anaemia. British Journal of Haematology, 78, 258-267.
43. Melenhorst, J.J., van Krieken, J., Dreef, E., Landegent, J.E., Willemze, R. & Fibbe, W.E. (1997) T. cells selectively infiltrate bone marrow areas with residual haemopoiesis of patients with acquired aplastic anaemia. British Journal of Haematology, 99, 517-519.
44. Molldrem, J.J., Jiang, Y.Z., Stetler-Stevenson, M., Mavroudis, D., Hensel, N. & Barrett, A.J. (1998) Haematological response of patients with myelodysplastic syndrome to antithymocyte globulin is associated with a loss of lymphocyte-mediated inhibition of CFU-GM and alterations in T-cell receptor Vβ profiles. British Journal of Haematology, 102, 1314-1322.
45. Mortazavi, Y., Merk, B., McIntosh, J., Marsh, J.C.W., Schrezenmeier, H. & Rutherford, T.R. (2003) The spectrum of PIG-A gene mutations in aplastic anaemia/paroxysmal nocturnal haemoglobinuria (AA/PNH): a high incidence of multiple mutations and evidence of a mutational hot spot. Blood, 101, 2833-2841.
46. Mukhina, G.L., Buckley, J.T., Barber, J.P., Jones, R.J. & Brodsky, R.A. (2001) Multilineage glycosylphosphatidylinositol anchor-deficient haemopoiesis in untreated aplastic anaemia. British Journal of Haematology, 115, 476-482.
47. Murakami, Y., Kosaka, H., Maeda, Y., Nishimuar, J., Inoue, N., Ohishi, K., Okabe, M., Takeda, J. & Kinoshita, T. (2002) Inefficient response of T lymphocytes to glycosylphosphatidylinositol anchor-negative cells: implications for paroxysmal nocturnal haemoglobinuria. Blood, 100, 4116-4122.
48. + peripheral blood stem cells in paroxysmal nocturnal hemoglobinuria: a perspective for autologous transplantation. Leukemia, 11, 890-892.
49. Nagakura, S., Ishihara, S., Dunn, D.E., Nishimura, J., Kawaguchi, T., Horikawa, K., Hidaka, M., Kagimoto, T., Eto, N., Mitsuga, H., Kinoshita, T., Young, N.S. & Makakura, H. (2002) Decreased susceptibility of leukaemic cells with PIG-A mutation to natural killer cells in vitro. Blood, 100, 1031-1037.
50. Nagarajan, S., Brodsky, R.A., Young, N.S. & Medof, M.E. (1995) Genetic defects underlying paroxysmal nocturnal hemoglobinuria that arises out of aplastic anemia. Blood, 86, 4656-4661.
51. Najean, Y. & Haguenauer, O. (1990) Long term (5-20 years) evolution of nongrafted aplastic anaemias. The co-operative group for the study of aplastic and refractory anaemia. Blood, 76, 2222-2228.
52. Nishimura, J., Hirota, T., Kanakura, Y., Machii, T., Kagayama, T., Doi, S., Wada, H., Masaoka, T., Kanayama, Y., Fujii, H., Inoue, N., Kuwayama, M., Inoue, N., Ohishi, K. & Kinoshita, T. (2002b) Long-term support of hematopoiesis by a single stem cell clone in patients with paroxysmal nocturnal hemoglobinuria. Blood, 99, 2748-2751.
53. Nishimura, J., Ware, R.E., Burnette, A., Pendleton, A.L., Kitano, K., Hirota, T., Machii, T., Kitani, T., Smith, C.A. & Rosse, W.F. (2002a) The hematopoietic defect in PNH is not due to defective stroma but is due to defective progenitor cells. Blood Cells, Molecules & Diseases, 29, 159-167.
54. Oni, S.B., Osunkoya, B.O. & Luzzatto, L. (1970) Paroxysmal nocturnal hemoglobinuria: evidence for monoclonal origin of abnormal red cells. Blood, 36, 145-152.
55. Philpott, N.J., Scopes, J., Marsh, J.C., Gordon-Smith, E.C. & Gibson, F.M. (1995) Increased apoptosis in aplastic anemia bone marrow progenitor cells: possible pathophysiologic significance. Experimental Hematology, 23, 1642-1648.
56. Philpott, N.J., Turner, A.J., Scopes, J., Westby, M., Marsh, J.C., Gordon-Smith, E.C., Dalgleish, A.G., Gibson, F.M. (1996) The use of 7-amino actinomycin D in identifying apoptosis: simplicity of use and broad spectrum of application compared with other techniques. Blood, 87, 2244-2251.
57. Podesta, M., Piaggio, G., Frassoni, F., Pitto, A., Zikos, P., Sessarego, M., Abate, M., Teresa, V.L., Berisso, G., Bacigalupo, A. (1998) The assessment of the hematopoietic reservoir after immunosuppressive therapy or bone marrow transplantation in severe aplastic anemia. Blood, 91, 1959-1965.
58. - hematopoietic precursors in paroxysmal nocturnal hemoglobinuria. Blood, 86, 3381-3386.
59. Risitano, A.M., Kook, H., Zeng, W., Chen, G., Young, N.S. & Maciejewski, J.P. (2002) Oligoclonal and polyclonal CD4 and CD8 lymphocytes in aplastic anaemia and paroxysmal nocturnal haemoglobinuria measured by Vβ CDR3 spectratyping and flow cytometry. Blood, 100, 178-183.
60. + cells isolated from aplastic anemia patient bone marrow. Haematological Journal, 3, 230-236.
61. Rosse, W.F. (1990) Phosphatidylinositol-linked proteins and paroxysmal nocturnal hemoglobinuria. Blood, 75, 1595-1601.
62. Rosse, W.F. (1997) Paroxysmal nocturnal haemoglobinuria as a molecular disease. Medicine, 76, 63-93.
63. Rosse, W.F. & Ware, R.E. (1995) The molecular basis of paroxysmal nocturnal hemoglobinuria. Blood, 86, 3277-3286.
64. Rotoli, B. & Luzzatto, L. (1989) Paroxysmal nocturnal hemoglobinuria. Seminars in Hematology, 26, 201-207.
65. Rotoli, B., Robledo, R. & Luzzatto, L. (1982) Decreased number of circulating BFU-Es in paroxysmal nocturnal hemoglobinuria. Blood, 60, 157-159.
66. Rotoli, B., Robledo, R., Scarpato, N. & Luzzatto, L. (1984) Two populations of erythroid cell progenitors in paroxysmal nocturnal hemoglobinuria. Blood, 64, 847-851.
67. Saunthararajah, Y., Nakamura, R., Nam, J.M., Robya, J., Loberiza, F., Maciejewski, J.P., Simonis, T., Molldrem, J., Young, N.S. & Barrett, A.J. (2002) LHA DR15 (12) is overrepresented in myelodysplasic syndromes and aplastic anaemia and predicts a response to immunosuppression in myelodysplastic syndromes. Blood, 100, 1570-1574.
68. Schrezenmeier, H., Hildebrand, A., Rojewski, M., Hacker, H., Heimpel, H. & Raghavachar, A. (2000) Paroxysmal nocturnal haemoglobinuria: 'a replacement of haematopoietic tissue'. Acta Haematologica, 103, 41-48.
69. Schrezenmeier, H., Jenal, M., Herrmann, F., Heimpel, H. & Raghavachar, A. (1996) Quantitative analysis of cobblestone area-forming cells in bone marrow of patients with aplastic anemia by limiting dilution assay. Blood, 88, 4474-4480.
70. Schubert, J., Scholz, C., Geissler, R.G., Ganser, A. & Schmidt, R.E. (1997) G-CSF and cyclosporin induce an increase of normal cells in hypoplastic paroxysmal nocturnal haemoglobinuria. Annals of Hematology, 74, 225-230.
71. Scopes, J., Bagnara, M., Gordon-Smith, E.C., Ball, S.E. & Gibson, F.M. (1994) Haemopoietic progenitor cells are reduced in aplastic anaemia. British Journal of Haematology, 86, 427-430.
72. Scopes, J., Daly, S., Atkinson, R., Ball, S.E., Gordon-Smith, E.C. & Gibson, F.M. (1996) Aplastic anemia: evidence for dysfunctional bone marrow progenitor cells and the corrective effect of granulocyte colony-stimulating factor in vitro. Blood, 87, 3179-3185.
73. Sloand, E., Kim, S., Maciejewski, J.P., Tisdale, J., Follmann, D., Young, N.S. (2002) Intracellular interferon-gamma in circulating and marrow T cells detected by flow cytometry and the response to immunosuppressive therapy in patients with aplastic anaemia. Blood, 100, 1185-1191.
74. Socie, G., Mary, J.Y., de Gramont, A., Rio, B., Leporrier, M., Rose, C., Heudier, P., Rochant, H., Cahn, J.Y. & Gluckman, E. (1996) Paroxysmal nocturnal haemoglobinuria: long-term follow-up and prognostic factors. French Society of Haematology. Lancet, 348, 573-577 (see comments).
75. Socie, G., Rosenfeld, S., Frickhofen, N., Gluckman, E. & Tichelli, A. (2000) Late clonal disease of treated aplastic anaemia. Seminars in Hematology, 37, 91-101.
76. Takahashi, M., Takeda, J., Hirose, S., Hyman, R., Inoue, N., Miyata, T., Ueda, E., Kitani, T., Medof, M.E. & Kinoshita, T. (1993) Deficient biosynthesis of N-acetylglucosaminyl-phosphatidylinositol, the first intermediate of glycosyl phosphatidylinositol anchor biosynthesis, in cell lines established from patients with paroxysmal nocturnal hemoglobinuria. Journal of Experimental Medicine, 177, 517-521.
77. Takeda, J., Miyata, T., Kawagoe, K., Iida, Y., Endo, Y., Fujita, T., Takahashi, M., Kitani, T. & Kinoshita, T. (1993) Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell, 73, 703-711.
78. Terstappen, L.W., Nguyen, M., Huang, S., Lazarus, H.M. & Medof, M.E. (1993) Defective and normal haematopoietic stem cells in paroxysmal nocturnal haemoglobinuria. British Journal of Haematology, 84, 504-514.
79. Tichelli, A., Gratwohl, A., Wursch, A., Nissen, C. & Speck, B. (1988) Late haematological complications in severe aplastic anaemia. British Journal of Haematology, 69, 413-418.
80. Urabe, A. & Fujioka, S. (1982) Erythroid progenitors in paroxysmal nocturnal haemoglobinuria. British Journal of Haematology, 50, 295-298.
81. Wang, H., Chuhjo, T., Yamazaki, H. & Shiobara, S., Teramura, M., Mizoguchi, H., Nakao, S. (2001) Relative increase of granulocytes with a paroxysmal nocturnal haemoglobinuria phenotype in aplastic anaemia patients: the high prevalence at diagnosis. European Journal of Haematology, 66, 200-205.
82. Ware, R.E., Heeney, M.M., Pickens, C.V., DeCastro, C.M. & Howard, T.A. (2003) A multi-step model for the pathogenesis and evolution of PNH. In: Paroxysmal Nocturnal Haemoglobinuria and Related Disorders Molecular Aspects of Pathogenesis (eds Omine, M. & Kinoshita, T.), 41-53. Springer-Verlag, Tokyo.
83. Ware, R.E., Nishimura, J., Moody, M.A., Smith, C., Rosse, W.F. & Howard, T.A. (1998) The PIG-A mutation and absence of glycosylphosphatidylinositol-linked proteins do not confer resistance to apoptosis in paroxysmal nocturnal hemoglobinuria. Blood, 92, 2541-2550.
84. Young, N.S. (2000) Hematopoietic cell destruction by immune mechanisms in acquired aplastic anaemia. Seminars in Hematology, 37, 3-14.
85. Young, N.S. (1992) The problem of clonality in aplastic anemia: Dr Dameshek's riddle, restated. Blood, 79, 1385-1392.
86. Zeng, W., Maciejewski, J.P., Chen, G., Young, N.S. (2001) Limited heterogeneity of T cell receptor BV usage in aplastic anaemia. Journal of Clinical Investigation, 108, 765-773.
87. Zeng, W., Nakao, S., Takamatsu, H., Yachie, A., Takami, A., Kando, Y., Sugimori, A., Yamazaki, H., Miura, Y., Shiobara, S. & Matsuda, T. (1999) Characteristics of T-cell repertoire of the bone marrow in immune mediated aplastic anaemia: evidence for the involvement of antigen driven T cell response in cyclosporine dependent aplastic anaemia. Blood, 93, 3008-3016.
88. Zoumbos, N., Gascon, P., Djeu, J.Y., Young, N.S. (1985) Interferon is a mediator of haematolgocial suppression in aplastic anaemia in vitro and possibly in vivo. Proceedings of the National Academy of Sciences, 82, 188-192.