Gatekeeper pathways and cellular background in the pathogenesis and therapy of AML

Leukemia

Volumn 19, Issue 10, 2005, Pages 1719-1728

  Cammenga, Jorg ^a,b  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b LUND UNIVERSITY   (Sweden)

Author keywords

AML; Gatekeepers; Hematopoietic stem progenitor cells; Therapy; Transcription factors

Indexed keywords

ANTINEOPLASTIC AGENT; CCAAT ENHANCER BINDING PROTEIN ALPHA; ETHYLNITROSOUREA; HOX PROTEIN; ONCOPROTEIN; RETINOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX1; TUMOR SUPPRESSOR PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; CANCER MODEL; CANCER THERAPY; CELL PROLIFERATION; CELL RENEWAL; CLINICAL STUDY; DATA ANALYSIS; GENETIC DISORDER; HEMATOPOIESIS; HUMAN; LEUKEMIA CELL; LEUKEMOGENESIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTO ONCOGENE; REVIEW; SAMPLING; STEM CELL; TARGET CELL; THEORY; TREATMENT PLANNING; TUMOR SUPPRESSOR GENE;

EID: 27144523745     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/sj.leu.2403894     Document Type: Review

References (97)

1. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-767.
2. Kinzler KW, Vogelstein B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 1997; 386: 761-763.
3. McCormack E, Bruserud O, Gjertsen BT. Animal models of acute myelogenous leukaemia - development, application and future perspectives. Leukemia 2005; 19: 687-706.
4. Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer 2003; 3: 89-101.
5. Zhang P, Iwasaki-Arai J, Iwasaki H, Fenyus ML, Dayaram T, Owens BM et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity 2004; 21: 853-863.
6. Ichikawa M, Asai T, Saito T, Yamamoto G, Seo S, Yamazaki I et al. AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med 2004; 10: 299-304.
7. Smith ML, Cavenagh JD, Lister TA, Fitzgibbon J. Mutation of CEBPA in familial acute myeloid leukemia. N Engl J Med 2004; 351: 2403-2407.
8. Song WJ, Sullivan MG, Legare RD, Hutchings S, Tan X, Kufrin D et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia [see comments]. Nat Genet 1999; 23: 166-175.
9. Daser A, Rabbitts TH. Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev 2004; 18: 965-974.
10. Owens BM, Hawley RG. HOX and non-Hox homeobox genes in leukemic hematopoiesis. Stem Cells 2002; 20: 364-379.
11. Buonamici S, Chakraborty S, Senyuk V, Nucifora G. The role of EVI1 in normal and leukemic cells. Blood Cells Mol Dis 2003; 31: 206-212.
12. Cuenco GM, Ren R. Both AML1 and EVI1 oncogenic components are required for the cooperation of AML1/MDS1/EVI1 with BCR/ABL in the induction of acute myelogenous leukemia in mice. Oncogene 2004; 23: 569-579.
13. Buonamici S, Li D, Chi Y, Zhao R, Wang X, Brace L et al. EVI1 induces myelodysplastic syndrome in mice. J Clin Invest 2004; 114: 713-719.
14. Cuenco GM, Nucifora G, Ren R. Human AML1/MDS1/EVI1 fusion protein induces an acute myelogenous leukemia (AML) in mice: A model for human AML. Proc Natl Acad Sci USA 2000; 97: 1760-1765.
15. Mueller BU, Pabst T, Osato M, Asou N, Johansen LM, Minden MD et al. Heterozygous PU.1 mutations are associated with acute myeloid leukemia. Blood 2002; 100: 998-1007.
16. Dohner K, Tobis K, Bischof T, Hein S, Schlenk RF, Frohling S et al. Mutation analysis of the transcription factor PU.1 in younger adults (16 to 60 years) with acute myeloid leukemia: A study of the AML Study Group Ulm (AMLSG ULM). Blood 2003; 102: 3850 author reply 3850-1.
17. Vegesna V, Takeuchi S, Hofmann WK, Ikezoe T, Tavor S, Krug U et al. C/EBP-beta, C/EBP-delta, PU.1, AML1 genes: Mutational analysis in 381 samples of hematopoietic and solid malignancies. Leuk Res 2002; 26: 451-457.
18. Lamandin C, Sagot C, Roumier C, Lepelley P, De Botton S, Cosson A et al. Are PU.1 mutations frequent genetic events in acute myeloid leukemia (AML)? Blood 2002; 100: 4680-4681.
19. Rosenbauer F, Wagner K, Zhang P, Knobeloch KP, Iwama A, Tenen DG. pDP4, a novel glycoprotein secreted by mature granulocytes, is regulated by transcription factor PU.1. Blood 2004; 103: 4294-4301.
20. He LZ, Bhaumik M, Tribioli C, Rego EM, Ivins S, Zelent A et al. Two critical hits for promyelocytic leukemia. Mol Cell 2000; 6 1131-1141.
21. Speck NA, Gilliland DG. Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer 2002; 2: 502-513.
22. Okuda T, Cai Z, Yang S, Lenny N, Lyu CJ, van Deursen JM et al. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood 1998; 91: 3134-3143.
23. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 1996; 84 321-330.
24. Yergeau DA, Hetherington CJ, Wang Q, Zhang P, Sharpe AH, Binder M et al. Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat Genet 1997; 15 303-306.
25. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci USA 1996; 93: 3444-3449.
26. Osato M. Point mutations in the RUNX1/AML1 gene: Another actor in RUNX leukemia. Oncogene 2004; 23: 4284-4296.
27. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, Wilde MD et al. Impaired energy homeostasis in C/EBP alpha knockout mice. Science 1995; 269: 1108-1112.
28. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha- deficient mice. Proc Natl Acad Sci USA 1997; 94: 569-574.
29. Pabst T, Mueller BU, Zhang P, Radomska HS, Narravula S, Schnittger S et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat Genet 2001; 27: 263-270.
30. Schwieger M, Lohler J, Fischer M, Herwig U, Tenen DG, Stocking C. A dominant-negative mutant of C/EBPalpha, associated with acute myeloid leukemias, inhibits differentiation of myeloid and erythroid progenitors of man but not mouse. Blood 2004; 103: 2744-2752.
31. Porse BT, Pedersen TA, Xu X, Lindberg B, Wewer UM, Friis-Hansen L et al. E2F repression by C/EBPalpha is required for adipogenesis and granulopoiesis in vivo. Cell 2001; 107: 247-258.
32. McKnight SL. McBindall - a better name for CCAAT/enhancer binding proteins? Cell 2001; 107: 259-261.
33. Nerlov C. C/EBPalpha mutations in acute myeloid leukaemias. Nat Rev Cancer 2004; 4: 394-400.
34. Barjesteh van Waalwijk van Doorn-Khosrovani S, Erpelinck C, Meijer J, van Oosterhoud S, van Putten WL, Valk PJ et al. Biallelic mutations in the CEBPA gene and low CEBPA expression levels as prognostic markers in intermediate-risk AML. Hematol J 2003; 4 31-40.
35. Gombart AF, Hofmann WK, Kawano S, Takeuchi S, Krug U, Kwok SH et al. Mutations in the gene encoding the transcription factor CCAAT/ enhancer binding protein [alpha] in myelodysplastic syndromes and acute myeloid leukemias. Blood 2002; 99: 1332-1340.
36. Preudhomme C, Sagot C, Boissel N, Cayuela JM, Tigaud I, de Botton S et al. Favorable prognostic significance of CEBPA mutations in patients with de novo acute myeloid leukemia: A study from the Acute Leukemia French Association (ALFA). Blood 2002; 100: 2717-2723.
37. Wechsler J, Greene M, McDevitt MA, Anastasi J, Karp JE, Le Beau MM et al. Acquired mutations in GATA1 in the megakaryoblastic leukemia of Down syndrome. Nat Genet 2002; 32: 148-152.
38. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004; 10: 789-799.
39. Pedersen-Bjergaard J, Andersen MK, Christiansen DH, Nerlov C. Genetic pathways in therapy-related myelodysplasia and acute myeloid leukemia. Blood 2002; 99: 1909-1912.
40. Greaves MF, Wiemels J. Origins of chromosome translocations in childhood leukaemia. Nat Rev Cancer 2003; 3: 639-649.
41. de Guzman CG, Warren AJ, Zhang Z, Gartland L, Erickson P, Drabkin H et al. Hematopoietic stem cell expansion and distinct myeloid developmental abnormalities in a murine model of the AML1-ETO translocation. Mol Cell Biol 2002; 22: 5506-5517.
42. Schwieger M, Lohler J, Friel J, Scheller M, Horak I, Stocking C. AML1-ETO inhibits maturation of multiple lymphohematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency. J Exp Med 2002; 196: 1227-1240.
43. Higuchi M, O'Brien D, Kumaravelu P, Lenny N, Yeoh EJ, Downing JR. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 2002; 1: 63-74.
44. Mulloy JC, Cammenga J, Berguido FJ, Wu K, Zhou P, Comenzo RL et al. Maintaining the self-renewal and differentiation potential of human CD34+ hematopoietic cells using a single genetic element. Blood 2003; 102: 4369-4376.
45. Mulloy JC, Cammenga J, MacKenzie KL, Berguido FJ, Moore MA, Nimer SD. The AML1-ETO fusion protein promotes the expansion of human hematopoietic stem cells. Blood 2002; 99: 15-23.
46. Heath V, Suh HC, Holman M, Renn K, Gooya JM, Parkin S et al. C/ EBP\{alpha\} deficiency results in hyperproliferation of hematopoietic progenitor cells and disrupts macrophage development in vitro and in vivo. Blood 2004; 104: 1639-1647.
47. Kim HG, De Guzman CG, Swindle CS, Cotta CV, Gartland L, Scott EW et al. The ETS-family transcription factor, PU.1, is necessary for the maintenance of fetal liver hematopoietic stem cells. Blood 2004; 104: 3894-3900.
48. Kelly LM, Liu Q, Kutok JL, Williams IR, Boulton CL, Gilliland DG. FLT3 internal tandem duplication mutations associated with human acute myeloid leukemias induce myeloproliferative disease in a murine bone marrow transplant model. Blood 2002; 99: 310-318.
49. Grisolano JL, O'Neal J, Cain J, Tomasson MH. An activated receptor tyrosine kinase, TEL/PDGFbetaR, cooperates with AML1/ETO to induce acute myeloid leukemia in mice. Proc Natl Acad Sci USA 2003; 100: 9506-9511.
50. Pretlow TP. Aberrant crypt foci and K-ras mutations: Earliest recognized players or innocent bystanders in colon carcinogenesis? Gastroenterology 1995; 108: 600-603.
51. Jen J, Powell SM, Papadopoulos N, Smith KJ, Hamilton SR, Vogelstein B et al. Molecular determinants of dysplasia in colorectal lesions. Cancer Res 1994; 54: 5523-5526.
52. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003; 423: 409-414.
53. Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004; 303: 1483-1487.
54. Jurlander J, Caligiuri MA, Ruutu T, Baer MR, Strout MP, Oberkircher AR et al. Persistence of the AML1/ETO fusion transcript in patients treated with allogeneic bone marrow transplantation for t(8;21) leukemia [see comments]. Blood 1996; 88: 2183-2191.
55. Kwong YL, Wong KF, Chan V, Chan CH. Persistence of AML1 rearrangement in peripheral blood cells in t(8;21). Cancer Genet Cytogenet 1996; 88: 151-154.
56. Neubauer A, Dodge RK, George SL, Davey FR, Silver RT, Schiffer CA et al. Prognostic importance of mutations in the ras proto-oncogenes in de novo acute myeloid leukemia. Blood 1994; 83: 1603-1611.
57. Nakao M, Yokota S, Iwai T, Kaneko H, Horiike S, Kashima K et al. Internal tandem duplication of the flt3 gene found in acute myeloid leukemia. Leukemia 1996; 10: 1911-1918.
58. Schnittger S, Schoch C, Dugas M, Kern W, Staib P, Wuchter C et al. Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: Correlation to cytogenetics, FAB subtype, and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood 2002; 100: 59-66.
59. Thiede C, Steudel C, Mohr B, Schaich M, Schakel U, Platzbecker U et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: Association with FAB subtypes and identification of subgroups with poor prognosis. Blood 2002; 99: 4326-4335.
60. Care RS, Valk PJ, Goodeve AC, Abu-Duhier FM, Geertsma-Kleinekoort WM, Wilson GA et al. Incidence and prognosis of c-KIT and FLT3 mutations in core binding factor (CBF) acute myeloid leukaemias. Br J Haematol 2003; 121: 775-777.
61. Gari M, Goodeve A, Wilson G, Winship P, Langabeer S, Linch D et al. c-kit proto-oncogene exon 8 in-frame deletion plus insertion mutations in acute myeloid leukaemia. Br J Haematol 1999; 105 894-900.
62. Gilliland DG, Tallman MS. Focus on acute leukemias. Cancer Cell 2002; 1: 417-420.
63. Yuan Y, Zhou L, Miyamoto T, Iwasaki H, Harakawa N, Hetherington CJ et al. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc Natl Acad Sci USA 2001; 98: 10398-10403.
64. Castilla LH, Garrett L, Adya N, Orlic D, Dutra A, Anderson S et al. The fusion gene Cbfb-MYH11 blocks myeloid differentiation and predisposes mice to acute myelomonocytic leukaemia [letter]. Nat Genet 1999; 23: 144-146.
65. Castilla LH, Perrat P, Martinez NJ, Landrette SF, Keys R, Oikemus S et al. Identification of genes that synergize with Cbfb-MYH11 in the pathogenesis of acute myeloid leukemia. Proc Natl Acad Sci USA 2004; 101: 4924-4929.
66. Kelly LM, Kutok JL, Williams IR, Boulton CL, Amaral SM, Curley DP et al. PML/RARalpha and FLT3-ITD induce an APL-like disease in a mouse model. Proc Natl Acad Sci USA 2002; 99: 8283-8288.
67. Kogan SC, Brown DE, Shultz DB, Truong BT, Lallemand-Breitenbach V, Guillemin MC et al. BCL-2 cooperates with promyelocytic leukemia retinoic acid receptor alpha chimeric protein (PMLRARalpha) to block neutrophil differentiation and initiate acute leukemia. J Exp Med 2001; 193: 531-543.
68. Blackburn AC, Brown JS, Naber SP, Otis CN, Wood JT, Jerry DJ. BALB/c alleles for Prkdc and Cdkn2a interact to modify tumor susceptibility in Trp53+/- mice. Cancer Res 2003; 63: 2364-2368.
69. Randle DH, Zindy F, Sherr CJ, Roussel MF. Differential effects of p19Arf and p16Ink4a loss on senescence of murine bone marrow-derived preB cells and macrophages. Proc Natl Acad Sci USA 2001; 98: 9654-9659.
70. Lewis JL, Chinswangwatanakul W, Zheng B, Marley SB, Nguyen DX, Cross NCP et al. The influence of INK4 proteins on growth and self-renewal kinetics of hematopoietic progenitor cells. Blood 2001; 97: 2604-2610.
71. Linggi B, Muller-Tidow C, van de Locht L, Hu M, Nip J, Serve H et al. The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia. Nat Med 2002; 8: 743-750.
72. 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.
73. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997; 91: 661-672.
74. Passegue E, Jamieson CH, Ailles LE, Weissman IL. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc Natl Acad Sci USA 2003; 100 (Suppl 1): 11842-11849.
75. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
76. Grimwade D, Enver T. Acute promyelocytic leukemia: Where does it stem from? Leukemia 2004; 18: 375-384.
77. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
78. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003; 423: 255-260.
79. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003; 423: 302-305.
80. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci USA 2000; 97: 7521-7526.
81. So CW, Karsunky H, Passegue E, Cozzio A, Weissman IL, Cleary ML. MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell 2003; 3: 161-171.
82. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17: 3029-3035.
83. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003; 17: 2298-2307.
84. So CW, Karsunky H, Wong P, Weissman IL, Cleary ML. Leukemic transformation of hematopoietic progenitors by MLL-GAS7 in the absence of Hoxa7 or Hoxa9. Blood 2004; 103: 3192-3199.
85. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004; 351: 657-667.
86. Buske C, Feuring-Buske M, Abramovich C, Spiekermann K, Eaves CJ, Coulombel L et al. Deregulated expression of HOXB4 enhances the primitive growth activity of human hematopoietic cells. Blood 2002; 100: 862-868.
87. Schiedlmeier B, Klump H, Will E, Arman-Kalcek G, Li Z, Wang Z et al. High-level ectopic HOXB4 expression confers a profound in vivo competitive growth advantage on human cord blood CD34+ cells, but impairs lymphomyeloid differentiation. Blood 2003; 101: 1759-1768.
88. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003; 423: 448-452.
89. Muller-Tidow C, Steffen B, Cauvet T, Tickenbrock L, Ji P, Diederichs S et al. Translocation products in acute myeloid leukemia activate the Wnt signaling pathway in hematopoietic cells. Mol Cell Biol 2004; 24: 2890-2904.
90. Zheng X, Beissert T, Kukoc-Zivojnov N, Puccetti E, Altschmied J, Strolz C et al. Gamma-catenin contributes to leukemogenesis induced by AML-associated translocation products by increasing the self-renewal of very primitive progenitor cells. Blood 2004; 103: 3535-3543.
91. de The H, Lavau C, Marchio A, Chomienne C, Degos L, Dejean A. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991; 66: 675-684.
92. Lin RJ, Nagy L, Inoue S, Shao W, Miller Jr WH, Evans RM. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature 1998; 391: 811-814.
93. Brown D, Kogan S, Lagasse E, Weissman I, Alcalay M, Pelicci PG et al. A PMLRARalpha transgene initiates murine acute promyelocytic leukemia. Proc Natl Acad Sci USA 1997; 94: 2551-2556.
94. Grisolano JL, Wesselschmidt RL, Pelicci PG, Ley TJ. Altered myeloid development and acute leukemia in transgenic mice expressing PML-RAR alpha under control of cathepsin G regulatory sequences. Blood 1997; 89: 376-387.
95. He LZ, Tribioli C, Rivi R, Peruzzi D, Pelicci PG, Soares V et al. Acute leukemia with promyelocytic features in PML/RARalpha transgenic mice. Proc Natl Acad Sci USA 1997; 94: 5302-5307.
96. Ley TJ, Minx PJ, Walter MJ, Ries RE, Sun H, McLellan M et al. A pilot study of high-throughput, sequence-based mutational profiling of primary human acute myeloid leukemia cell genomes. Proc Natl Acad Sci USA 2003; 100: 14275-14280.
97. Cammenga J, Mulloy JC, Berguido FJ, MacGrogan D, Viale A, Nimer SD. Induction of C/EBPalpha activity alters gene expression and differentiation of human CD34+ cells. Blood 2003; 101: 2206-2214.