Immunophenotype characterization of hematopoietic stem cells, progenitor cells restricted to myeloid lineage and their leukemia counterparts

Neoplasma

Volumn 57, Issue 5, 2010, Pages 392-400

  Fajtova, M ^a   Babusikova, O ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

AML blast cells; CD markers; Hematopoietic stem cells; Immunophenotype; Leukemic stem cells; Lineage restricted progenitors; Multiparameter flow cytometry

Indexed keywords

CD123 ANTIGEN; CD135 ANTIGEN; CD14 ANTIGEN; CD15 ANTIGEN; CD16 ANTIGEN; CD19 ANTIGEN; CD2 ANTIGEN; CD24 ANTIGEN; CD3 ANTIGEN; CD33 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CD45 ANTIGEN; CD56 ANTIGEN; FIBRINOGEN RECEPTOR; HLA DR ANTIGEN; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; BONE MARROW CELL; CELL DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CELL RENEWAL; CELL TRANSFORMATION; CLONOGENIC ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FOLLOW UP; GRANULOCYTE PRECURSOR; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; LYMPHOID PROGENITOR CELL; MEGAKARYOCYTE ERYTHROID PROGENITOR; MYELOID PROGENITOR CELL; NEUTROPHIL; NONHUMAN; PHENOTYPE; REVIEW; STEM CELL; ANIMAL; CANCER STEM CELL; CELL LINEAGE; CYTOLOGY; IMMUNOLOGY; LEUKEMIA;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOPHENOTYPING; LEUKEMIA; MYELOID CELLS; NEOPLASTIC STEM CELLS;

EID: 79952114706     PISSN: 00282685     EISSN: None     Source Type: Journal    
DOI: 10.4149/neo_2010_05_392     Document Type: Review

References (95)

1. DOMEN J and WEISSMAN IL Self-renewal, differentiation or death: regulation and manipulation of hematopoietic stem cell fate. Molecular Medicine Today 1999; 5: 201-208. doi:10.1016/S1357-4310(99)01464-1
2. WEISSMAN IL Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000; 100: 157-68. doi:10.1016/S0092-8674(00)81692-X
3. BABUSIKOVA O, ZELEZNIKOVA T Normal maturation sequence of immunoglobulin light and heavy chains in hematogone stages 1, 2 and 3 in acute leukemia after treatment. Neoplasma 2008; 55: 501-506.
4. BABUSIKOVA O, ZELEZNIKOVA T, KIRSCHNEROVA G, KANKURI E Hematogones in acute leukemia during and after therapy. Leuk Lymphoma 2008; 49: 1935-44. doi:10.1080/ 10428190701817274
5. CIVIN CI, STRAUSS LC, BROVAL C, FACKLER MJ, SCHWARTZ JF, et al. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J. Immunol. 1984; 133: 157-165.
6. KRAUSE DS, FACLER MJ, CIVIN CI, MAY WD CD34: structure, biology and clinical utility. Blood 1996; 87: 1-13.
7. SUTHERLAND DR, KEATING A The CD34 antigen: structure, biology, and potential clinical applications. J. Hematother 1992; 1: 115-29.
8. DEAGLIO S, MEHTA K, MALAVASI F. 2001. Human CD38: a (r)evolutionary story of enzymes and receptors. Leukoc. Res. 2001; 25: 1-12. doi:10.1016/S0145-2126(00)00093-X
9. BAUM CM, WEISSMAN IL, TSUKAMOTO AS, BUCKLE AM, PEAULT B Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA. 1992; 89: 2804-2808. doi:10.1073/pnas.89.7.
10. HUANG S, TERSTAPPEN LW Lymphoid and myeloid differentiation of single human CD34+, HLA-DR+, CD38-hematopoietic stem cells. Blood 1994; 83: 1515-26.
11. HAO QL, SMOGORZEWSKA EM, BARSKY LW, CROOKS GM In vitro identification of single CD34+CD38Ǎ̌ÂÂ' cells with both lymphoid and myeloid potential. Blood 1998; 91: 4145-51.
12. MILLER JS, MCCULLAR V, PUNZEL M, LEMISCHKA IR, MOORE KA Single adult human CD34+/LinǍ̌ÂÂ'/CD38-progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells. Blood 1999; 93: 96-106.
13. KONDO M, WAGERS AJ, MANZ MG, PROHASKA SS, SCHERER DC, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annual Review of Immunology 2003; 21: 759-806.
14. HAO QL, THIEMANN FT, PETERSEN D, SMOGORZEWSKA EM, CROOKS GM Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood 1996; 88: 3306-13.
15. MILLER JS, MCCULLAR V, VERFAILLIE CM Ex vivo culture of CD34+/LinǍ̌ÂÂ'/DRǍ̌ÂÂ' cells in stroma-derived soluble factors, interleukin-3, and macrophage inflammatory protein-1ǍŽÂ± maintains not only myeloid but also lymphoid progenitors in a novel switch culture assay. Blood 1998; 91: 4516-22.
16. BABUSIKOVA O, ZELEZNIKOVA T Normal maturation sequence of immunoglobulin light and heavy chains in hematogone stages 1, 2 and 3 in acute leukemia after treatment. Neoplasma 2008; 55: 501-506.
17. BHATIA M, WANG JC, KAPP U, BONNET D, DICK JE Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci USA. 1997; 94: 5320-5325. doi:10.1073/pnas.94.10.5320
18. BHATIA M, BONNET D, MURDOCH B, GAN OI, DICK JE A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat. Med. 1998; 4:1038-45. doi:10.1038/2023
19. BONNET D, BHATIA M, WANG JCY, KAPP U, DICK JE Cytokine treatment or accessory cells are required to initiateengraftment of purified primitive human hematopoietic cells transplanted at limiting doses into NOD/SCID mice. Bone Marrow Transplantation 1999; 23: 203-9. doi:10.1038/ sj.bmt.1701564
20. GUENECHEA G, GAN OI, DORRELL C, DICK JE Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat Immunol 2001; 2: 75-82. doi:10.1038/83199
21. SROUR EF, ZANJANI ED, BRANDT JE, LEEMHUIS T, BRIDDELL RA, et al. Sustained human hematopoiesis in sheep transplanted in utero during early gestation with fractionated adult human bone marrow cells. Blood 1992; 79: 1404-12.
22. ZANJANI ED, FLAKE AW, RICE H, HEDRICK M, TAVASSOLI M. Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep. J. Clin. Invest. 1994; 93: 1051-55 doi:10.1172/ JCI117054
23. TILL JE, MCCULLOCH EA A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiation Research 1961; 14: 213-22. doi:10.2307/3570892
24. MORRISON SJ, WEISSMAN IL The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994; 1: 661-673. doi:10.1016/1074-7613(94)90037-X
25. LAROCHELLE A, VORMOOR J, HANENBERG H, WANG JCY, BHATIA M, et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 1996; 2: 1329-1337.
26. BONNET D Haematopoietic stem cells. J Pathol 2002; 197: 430-40. doi:10.1002/path.1153
27. SPERR WR, HAUSWIRTH AW, FLORIAN S, OHLER L, GEISSLER K, et al. Human leukaemic stem cells: a novel target of therapy. Eur J Clin Invest. 2004; 34: 31-40.
28. ZIEGLER BL, VALTIERI M, PORADA GA, De MARIA R, MULLER R, et al. KDR receptor: a key marker defining hematopoietic stem cells. Science 1999; 285: 1553-58
29. GUNJI Y, NAKAMURA M, OSAWA H, NAGAYOSHI K, NAKAUCHI H, et al. Human primitive hematopoietic progenitor cells are more enriched in KITlow cells than in KIThigh cells. Blood 1993; 82: 3283-9.
30. KAWASHIMA I, ZANJANI ED, ALMEIDA-PORADA G, FLAKE AW, ZENG H, et al. CD34+ human marrow cells that express low levels of Kit protein are enriched for long-term marrow-engrafting cells. Blood 1996; 87: 4136-4142.
31. HU M, KRAUSE D, GREAVES M, SHARKIS S, DEXTER M, et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 1997; 11: 774-785. doi:10.1101/gad.11.6.774
32. TAUSSIG DC, PEARCE DJ, SIMPSON C, ROHATINER AZ, LISTER TA, et al. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 2005; 106: 4086-4092.
33. ANDREWS RG, TAKAHASHI M, SEGAL GM, POWELL JS, BERNSTEIN ID, et al. The L4F3 antigen is expressed by unipotent and multipotent colony-forming cells but not by their precursors. Blood 1986; 68: 1030-1035.
34. ANDREWS RG, SINGER JW, BERNSTEIN ID Precursors of colony-forming cells in humans can be distinguished from colony-forming cells by expression of the CD33 and CD34 antigens and light scatter properties. J Exp Med 1989; 169: 1721-1731. doi:10.1084/jem.169.5.1721
35. OSAWA M, HANADA K, HAMADA H, NAKAUCHI H Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996; 273: 242-45. doi:10.1126/science.273.5272.242
36. ZANJANI ED, ALMEIDA-PORADA G, LIVINGSTON AG, FLAKE AW, OGAWA M Human bone marrowCD34-cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Exp. Hematol. 1998; 26: 353-60.
37. NAKAMURA Y, ANDO K, CHARGUI J, KAWADA H, SATO T, et al. Ex vivo generation of CD34+ cells from CD34-hematopoietic cells. Blood 1999; 94: 4053-59.
38. FUJISAKI T, BERGER MG, ROSE-JOHN S, EAVES CJ. Rapid differentiation of a rare subset of adult human Lin-CD34-CD38-cells stimulated by multiple growth factors in vitro. Blood 1999; 94: 1926-1932.
39. MORRISON SJ, WRIGHT DE, WEISSMAN IL Cyclophosphamide/ granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proceedings of the National Academy of Sciences of the USA 1997; 94: 1908-1913. doi:10.1073/pnas.94.5.1908
40. KONDO M, WEISSMAN IL, AKASHI K Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997; 91: 661-72. doi:10.1016/S0092-8674(00)80453-5
41. AKASHI K, TRAVER D, MIYAMOTO T, WEISSMAN IL A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000; 404: 193-197. doi:10.1038/ 35004599
42. TRAVER D, AKASH K, MANZ M, MERAD M, MIYAMOTO T, et al. Development of CD8ǍŽÂ±-positive dendritic cells from a common myeloid progenitor. Science 2000; 290: 2152-2154. doi:10.1126/science.290.5499.2152
43. MANZ MG, TRAVER D, MIYAMOTO T, WEISSMAN IL, AKASHI K Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 2001; 97: 3333-3341. doi:10.1182/ blood.V97.11.3333
44. GLIMM H, EISTERER W, LEE K, CASHMAN J, HOLYOAKE TL, et al. Previously undetected human haemopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice. Journal of Clinical Investigation 2001; 107: 199-206.
45. GALY A, TRAVIS M, CEN D, CHEN B Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 1995; 3: 459-73. doi:10.1016/ 1074-7613(95)90175-2
46. HAO QL, ZHU J, PRICE MA, PAYNE KJ, BARSKY LW, et al. Identification of a novel, human multilymphoid progenitor in cord blood. Blood 2001; 97: 3683-90.
47. MANZ MG, MIYAMOTO T, AKASHI K, WEISSMAN IL Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci USA 2002; 99: 11872-7. doi:10.1073/pnas.172384399
48. EDVARDSSON L, DYKES J, OLOFSSON T Isolation and characterization of human myeloid progenitor populations-TpoR as discriminator between common myeloid and megakaryocyte/erythroid progenitors. Exp Hematol. 2006; 34: 599-609. doi:10.1016/j.exphem.2006.01.017
49. MORI Y, IWASAKI H, KOHNO K, YOSHIMOTO G, KIKUSHIGE Y, et al. Identification of the human eosinophil lineage-committed progenitor: revision of phenotypic definition of the human common myeloid progenitor. The Journal of Experimental Medicine 2008; 206: 183-193. doi:10.1084/ jem.20081756
50. KATSURA Y and KAWAMOTO H Stepwise lineage restriction of progenitors in lympho-myelopoiesis. Int. Rev. Immunol. 2001; 20: 1-20
51. KAWAMOTO H, KATSURA Y A new paradigm for hematopoietic cell lineages: revision of the classical concept of the myeloid-lymphoid dichotomy. Trends Immunol 2009; 30: 193-200. doi:10.1016/j.it.2009.03.001
52. IGARASHI H, GREGORY SC, YOKOTA T, SAKAGUCHI N, KINCADE PW Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 2002; 17, 117-130. doi:10.1016/S1074-7613(02)00366-7
53. KAWAMOTO H, OHMURA K, KATSURA Y Direct evidence for the commitment of hematopoietic stem cells to T, B and myeloid lineages in murine fetal liver. Int. Immunol. 1997; 9: 1011-1019. doi:10.1093/intimm/9.7.1011
54. KAWAMOTO H, OHMURA K, FUJIMOTO S, KATSURA Y Emergence of T cell progenitors without B cell or myeloid differentiation potential at the earliest stage of hematopoiesis in the murine fetal liver. J. Immunol. 1999; 162: 2725-2731.
55. KAWAMOTO H, IKAWA T, OHMURA K, FUJIMOTO S, KATSURA Y T cell progenitors emerge earlier than B cell progenitors in the murine fetal liver. Immunity 2000; 12: 441-450. doi:10.1016/S1074-7613(00)80196-X
56. MATUTES E, MORILLA R, FARAHAT N, CARBONELL F, SWANSBURY J, et al. Definition of acute biphenotypic leukemia. Haematologica 1997; 82: 64-66.
57. CHAPIRO E, DELABESSE E, ASNAFI V, MILLIEN C, DAVI F et al. Expression of T-lineage-affiliated transcripts and TCR rearrangements in acute promyelocytic leukemia: implications for the cellular target of t(15;17). Blood 2006; 108: 3484-3493. doi:10.1182/blood-2005-09-009977
58. TERSTAPPEN LW, LOKEN MR Myeloid cell differentiation in normal bone marrow and acute myeloid leukemia assessed by multi-dimensional flow cytometry. Anal Cell Pathol 1990; 2: 229-40.
59. TERSTAPPEN LW, HOLLANDER Z, MEINERS H, LOKEN MR Quantitative comparison of myeloid antigens on five lineages of mature peripheral blood cells. J Leukoc Biol 1990; 48: 138-148.
60. VAN LOCHEM EG, VAN DER VELDEN VHJ, WIND HK, TE MARVELDE JG, WESTERDAAL NAC, et al. Immunophenotypic differentiation patterns of normal hematopoiesis in human bone marrow: Reference patterns for age-related changes and disease-induced shifts. Cytometry Part B: Clinical Cytometry Volume 60B 2004; 1: 1-13.
61. WOOD B Multicolor immunophenotyping: human immune system hematopoiesis. In: Darzynkiewicz Z, Roederer M, Tanke HJ, editors. Cytometry, 4th Edition New Developments. Elsevier Academic Press. 2004; Methods in Cell Biology 75: 559-76.
62. REYA T, MORRISON SJ, CLARKE MF, WEISSMAN IL Stem Cells, Cancer and Cancer stem cells. Nature 2001; 414: 105-111. doi:10.1038/35102167
63. LAWRENCE HJ, SAUVAGEAU G, HUMPHRIES RK, LARGMAN C. The role of HOX homeobox genes in normal and leukemic hematopoiesis. Stem Cells 1996; 14: 281-91.
64. TAIPALE J, BEACHY PA The Hedgehog and Wnt signalling pathways in cancer. Nature 2001; 411 (6835): 349-54. doi:10.1038/35077219
65. SPRADLING A, DRUMMOND-BARBOSA D, KAI T Stem cells find their niche. Nature 2001; 414 (6859): 98-104. doi:10.1038/35102160
66. COZZIO A, PASSEGUE E, AYTON PM, KARSUNKY H, CLEARY ML, et al. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17: 3029-3035.
67. SO CW, KARSUNKY H, PASSEGUE E, COZZIO A, WEISSMAN IL, et al. MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell 2003; 3: 161-171.
68. SATOH C, OGATA K Hypothesis: myeloid-restricted hematopoietic stem cells with self-renewal capacity may be the transformation site in acute myeloid leukemia. Leuk Res 2006; 30: 491-495. doi:10.1016/j.leukres.2005.08.017
69. BLAIR A, HOGGE DE, AILLES LE, LANSDORP PM, SUTHERLAND HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood 1997; 89: 3104-12.
70. BONNET D, DICK JE Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-7. doi:10.1038/ nm0797-730
71. SUTHERLAND HJ, BLAIR A, ZAPF RW Characterization of a hierarchy of human acute myeloid leukemia progenitor cells. Blood 1996; 87: 4754-61.
72. APPELBAUM FR, ROWE JM, RADICH J, DICK JE Acute myeloid leukemia. Hematology (Am Soc Hematol Educ Program) 2001; 62-86. doi:10.1182/asheducation-2001.1.62
73. RAVANDI F, ESTROV Z Eradication of leukemia stem cells as a new goal of therapy in leukemia. Clin Cancer Res 2006; 12: 340-344. doi:10.1158/1078-0432.CCR-05-1879
74. HAUSWIRTH AW, FLORIAN S, PRINTZ D, SOTLAR K, KRAUTH MT, Expression of the target receptor CD33 in CD34+/CD38-/CD123+ AML stem cells. European Journal of Clinical Investigation 2007; 37: 73-82 (10).
75. FLORIAN S, SONNECK K, HAUSWIRTH AW, KRAUTH MT, SCHERNTHANER GH, et al. Detection of molecular targets on the surface of CD34+/CD38-stem cells in various myeloid malignancies. Leukemia & Lymphoma 2006; 47: 207-222.
76. BLAIR A, HOGGE DE, SUTHERLAND HJ Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34+/CD71Ǎ̌ÂÂ'/HLAǍ̌ÂÂ'DRǍ̌ÂÂ'. Blood 1998; 92: 4325-35.
77. BLAIR A, SUTHERLAND HJ Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp Hematol 2000; 28: 660-71. doi:10.1016/S0301-472X(00)00155-7
78. VAN GOSLIGA D, SCHEPERS H, RIZO A, VAN DER KOLK D, VELLENGA E, et al. Establishing long-term cultures with self-renewing acute myeloid leukemia stem/progenitor cells. Exp Hematol 2007; 35: 1538-1549. doi:10.1016/j.exphem.2007.07.001
79. JORDAN CT, UPCHURCH D, SZILVASSY SJ, GUZMAN ML, HOWARD DS, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000; 14: 1777-1784.
80. MUÑOZ L, NOMDEDÉU JF, LÓPEZ O, CARNICER MJ, BELLIDO M, et al. Interleukin-3 receptor α chain (CD123) is widely expresssed in hematologic malignancies. Haematologica 2001; 86: 1261-1269.
81. VAN RHENEN A, MOSHAVER B, KELDER A, FELLER N, NIEUWINT AW, et al. Aberrant marker expression patterns on the CD34+CD38-stem cell compartment in acute myeloid leukemia allows to distinguish the malignant from the normal stem cell compartment both at diagnosis and in remission. Leukemia 2007; 21: 1700-1707.
82. VAN RHENEN A, FELLER N, KELDER A, WESTRA AH, ROMBOUTS E, et al. High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin Cancer Res 2005; 11: 6520-6527.
83. HOSEN N, PARK CY, TATSUMI N, OJI Y, SUGIYAMA H, et al. CD96 is a leukemic stem cell-specific marker in human acute myeloid leukemia. Proc. Nat. Acad. Sci. USA 2007; 104: 11008-11013.
84. ZELEZNIKOVA T, STEVULOVA A, KOVARIKOVA A, BABUSIKOVA O Increased myeloid precursors in regenerating bone marrow; implications for detection of minimal residual disease in acute myeloid leukemia. Neoplasma 2007; 54: 471-477.
85. OLARU D, CAMPOS L, FLANDRIN P, NADAL N, DUVAL A, et al. Multiparametric analysis of normal and postchemotherapy bone marrow: Implication for the detection of leukemia-associated immunophenotypes. Cytometry B Clin Cytom. 2008; 74: 17-24. doi:10.1002/cyto.b.20371
86. SAN MIGUEL JF, VIDRIALES MB, LOPEZ-BERGES C, DIAZ-MEDIAVILLA J, GUTIERREZ N, et al. Early immunophenotypical evaluation of minimal residual disease in acute myeloid leukemia identifies different patient risk groups and may contribute to postinduction treatment stratification. Blood 2001; 98(6): 1746-51.
87. BENNETT JM, CATOVSKY D, DANIEL MT, FLANDRIN G, GALTON DA, et al. Proposals for the classification of the acute leukaemias. French-American-British (FAB) co-operative group. Br J Haematol. 1976; 33: 451-458.
88. VARDIMAN JW, HARRIS NL, Brunning RD The World Health Organization (WHO) classification of the myeloid neoplasms. Blood 2002; 100: 2292-302. doi:10.1182/blood-2002-04-1199
89. BEHM FG, CAMPANA D. Immunophenotyping. In: Pui CH editor. Childhood leukemias. UK: Cambridge University Press; 1999; 111-44.
90. ZELEZNIKOVA T, BABUSIKOVA O The impact of cell heterogeneity and immunophenotypic changes on monitoring minimal residual disease in acute myeloid leukemia. Neoplasma 2005; 52: 517-22.
91. GHOSH S, SHINDE SC, KUMARAN GS, SAPRE RS, DHOND SR, et al. Haematologic and immunophenotypic profile of acute myeloid leukemia: An experience of Tata memorial hospital. Indian J Cancer 2003; 40: 71-76.
92. LAUNDER TM, BRAY RA, STEMPORA L, CHENGGIS ML, FARHI DC. Lymphoid-Associated antigen expression by acute myeloid leukemia. Am J Clin Pathol 1996; 106: 185-91.
93. BALL ED, DAVIS RB, GRIFFITH JD, MAYER RJ, DAVEY FR, et al. Prognostic value of lymphocyte surface markers in acute myeloid leukemia. Blood 1991; 77: 2242-50.
94. RASPADORI D, DAMIANI D, LENOCI M, RONDELLI D, TESTONI N, et al. CD56 antigenic expression in acute myeloid leukemia identifies patients with poor clinical prognosis. Leukemia 2001; 15: 1161-4. doi:10.1038/sj.leu.2402174
95. BRADSTOCK K, MATTHEWS J, BENSON E, PAGE F, BISHOP J Prognostic value of immunophenotyping in acute myeloid leukemia. Australian Leukemia study group. Blood 1994; 84: 1220-5.