Oncogenic kras initiates leukemia in hematopoietic stem cells

PLoS Biology

Volumn 7, Issue 3, 2009, Pages 0537-0548

  Sabnis, Amit J ^a   Cheung, Laurene S ^a   Dail, Monique ^a   Kang, Hio Chung ^a   Santaguida, Marianne ^b   Hermiston, Michelle L ^a   Passegué, Emmanuelle ^b   Shannon, Kevin ^a   Braun, Benjamin S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE K RAS; T CELL LEUKEMIA; THYMOCYTE;

MURINAE; MUS;

EID: 65949123563     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10. 1371/journal.pbio.1000059     Document Type: Article

References (75)

1. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Dick JE (2005) Acute myeloid leukemia stem cells. Ann N Y Acad Sci 1044: 1-5.
3. Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, et al. (2006) Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442: 818-822.
4. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, et al. (2003) Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 17: 3029-3035.
5. Passegue E, Wagner EF, Weissman IL (2004) JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119: 431-443.
6. Schubbert S, Shannon K, Bollag G (2007) Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7: 295-308.
7. Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129: 865-877.
8. Downward J (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22.
9. Van Etten RA, Shannon KM (2004) Focus on myeloproliferative diseases and myelodysplastic syndromes. Cancer Cell 6: 547-552.
10. Hirsch-Ginsberg C, LeMaistre AC, Kantarjian H, Talpaz M, Cork A, et al. (1990) RAS mutations are rare events in Philadelphia chromosome- negative/bcr gene rearrangement-negative chronic myelogenous leukemia, but are prevalent in chronic myelomonocytic leukemia. Blood 76: 1214-1219.
11. Onida F, Kantarjian HM, Smith TL, Ball G, Keating MJ, et al. (2002) Prognostic factors and scoring systems in chronic myelomonocytic leukemia: a retrospective analysis of 213 patients. Blood 99: 840-849.
12. Lauchle JO, Braun BS, Loh ML, Shannon K (2006) Inherited predisposi- tions and hyperactive Ras in myeloid leukemogenesis. Pediatr Blood Cancer 46: 579-585.
13. Braun BS, Tuveson DA, Kong N, Le DT, Kogan SC, et al. (2004) Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc Natl Acad Sci U S A 101: 597-602.
14. Chan IT, Kutok JL, Williams IR, Cohen S, Kelly L, et al. (2004) Conditional expression of oncogenic K-ras from its endogenous promoter induces a myeloproliferative disease. J Clin Invest 113: 528-538.
15. Araki T, Mohi MG, Ismat FA, Bronson RT, Williams IR, et al. (2004) Mouse model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat Med 10: 849-857.
16. Le DT, Kong N, Zhu Y, Lauchle JO, Aiyigari A, et al. (2004) Somatic inactivation of Nf1 in hematopoietic cells results in a progressive myeloproliferative disorder. Blood 103: 4243-4250.
17. Tefferi A, Gilliland DG (2007) Oncogenes in myeloproliferative disorders. Cell Cycle 6: 550-566.
18. Kuhn R, Schwenk F, Aguet M, Rajewsky K (1995) Inducible gene targeting in mice. Science 269: 1427-1429.
19. Kemp R, Ireland H, Clayton E, Houghton C, Howard L, et al. (2004) Elimination of background recombination: somatic induction of Cre by combined transcriptional regulation and hormone binding affinity. Nucleic Acids Res 32: e92.
20. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
21. Christensen JL, Weissman IL (2001) Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A 98: 14541-14546.
22. Van Meter ME, Diaz-Flores E, Archard JA, Passegue E, Irish JM, et al. (2007) K-RasG12D expression induces hyperproliferation and aberrant signaling in primary hematopoietic stem/progenitor cells. Blood 109: 3945-3952.
23. Traver D, Miyamoto T, Christensen J, Iwasaki-Arai J, Akashi K, et al. (2001) Fetal liver myelopoiesis occurs through distinct, prospectively isolatable progenitor subsets. Blood 98: 627-635.
24. Akashi K, Traver D, Miyamoto T, Weissman IL (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404: 193-197.
25. Weng AP, Ferrando AA, Lee W, Morris JP 4th, Silverman LB, et al. (2004) Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
26. Lin YW, Nichols RA, Letterio JJ, Aplan PD (2006) Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107: 2540-2543.
27. O'Neil J, Calvo J, McKenna K, Krishnamoorthy V, Aster JC, et al. (2006) Activating Notch1 mutations in mouse models of T-ALL. Blood 107: 781-785.
28. Tsuji H, Ishii-Ohba H, Ukai H, Katsube T, Ogiu T (2003) Radiation-induced deletions in the 59 end region of Notch1 lead to the formation of truncated proteins and are involved in the development of mouse thymic lymphomas. Carcinogenesis 24: 1257-1268.
29. Karsunky H, Inlay M, Serwold T, Bhattacharya D, Weissman I (2008) Flk2&Thorn common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages. Blood 111: 5562-5570.
30. Huntly BJ, Shigematsu H, Deguchi K, Lee BH, Mizuno S, et al. (2004) MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 6: 587-596.
31. Land H, Parada LF, Weinberg RA (1983) Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304: 596-602.
32. Gilliland DG, Griffin JD (2002) The roles of FLT3 in hematopoiesis and leukemia. Blood 100: 1532-1542.
33. Miles DK, Freedman MH, Stephens K, Pallavicini M, Sievers E, et al. (1996) Patterns of hematopoietic lineage involvement in children with neuro- fibromatosis, type 1, and malignant myeloid disorders. Blood 88: 4314-4320.
34. Cooper LJ, Shannon KM, Loken MR, Weaver M, Stephens K, et al. (2000) Evidence that juvenile myelomonocytic leukemia can arise from a pluripotential stem cell. Blood 96: 2310-2313.
35. Matsuzaki S, Matsuda K, Miki J, Nakazawa Y, Sakashita K, et al. (2005) Development of two cytogenetically abnormal clones from multipotential hematopoietic stem cells in a patient with juvenile myelomonocytic leukemia. Leuk Res 29: 1069-1072.
36. Nakamura Y, Ito M, Yamamoto T, Yan XY, Yagasaki H, et al. (2005) Engraftment of NOD/SCID/gammac(null) mice with multilineage neoplastic cells from patients with juvenile myelomonocytic leukaemia. Br J Haematol 130: 51-57.
37. Freedman MH, Hitzler JK, Bunin N, Grunberger T, Squire J (1996) Juvenile chronic myelogenous leukemia multilineage CD34&Thorn cells: aberrant growth and differentiation properties. Stem Cells 14: 690-701.
38. Lapidot T, Grunberger T, Vormoor J, Estrov Z, Kollet O, et al. (1996) Identification of human juvenile chronic myelogenous leukemia stem cells capable of initiating the disease in primary and secondary SCID mice. Blood 88: 2655-2664.
39. Marshall C (1999) How do small GTPase signal transduction pathways regulate cell cycle entry? Curr Opin Cell Biol 11: 732-736.
40. Yu Q, Ciemerych M, Sicinski P (2005) Ras and Myc can drive oncogenic cell proliferation through individual D-cyclins. Oncogene 24: 7114-7119.
41. Kozar K, Ciemerych M, Rebel V, Shigematsu H, Zagozdzon A, et al. (2004) Mouse development and cell proliferation in the absence of D-cyclins. Cell 118: 477-491.
42. Yu Q, Geng Y, Sicinski P (2001) Specific protection against breast cancers by cyclin D1 ablation. Nature 411: 1017-1021.
43. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, et al. (2006) Pten dependence distinguishes haematopoietic stem cells from leukaemia- initiating cells. Nature 441: 475-482.
44. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, et al. (2006) PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441: 518-522.
45. MacKenzie KL, Dolnikov A, Millington M, Shounan Y, Symonds G (1999) Mutant N-ras induces myeloproliferative disorders and apoptosis in bone marrow repopulated mice. Blood 93: 2043-2056.
46. Habibian HK, Peters SO, Hsieh CC, Wuu J, Vergilis K, et al. (1998) The fluctuating phenotype of the lymphohematopoietic stem cell with cell cycle transit. J Exp Med 188: 393-398.
47. Glimm H, Oh IH, Eaves CJ (2000) Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G(2)/M transit and do not reenter G(0). Blood 96: 4185-4193.
48. Orschell-Traycoff CM, Hiatt K, Dagher RN, Rice S, Yoder MC, et al. (2000) Homing and engraftment potential of Sca-1(&Thorn)lin(-) cells fractionated on the basis of adhesion molecule expression and position in cell cycle. Blood 96: 1380-1387.
49. Fleming WH, Alpern EJ, Uchida N, Ikuta K, Spangrude GJ, et al. (1993) Functional heterogeneity is associated with the cell cycle status of murine hematopoietic stem cells. J Cell Biol 122: 897-902.
50. Passegue E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL (2005) Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med 202: 1599-1611.
51. Jude C, Climer L, Xu D, Artinger E, Fisher J, et al. (2007) Unique and independent roles for MLL in adult hematopoietic stem cells and progenitors. Cell Stem Cell 1: 324-337.
52. Hock H, Meade E, Medeiros S, Schindler J, Valk P, et al. (2004) Tel/Etv6 is an essential and selective regulator of adult hematopoietic stem cell survival. Genes Dev 18: 2336-2341.
53. Zhang Y, Taylor BR, Shannon K, Clapp DW (2001) Quantitative effects of Nf1 inactivation on in vivo hematopoiesis. J Clin Invest 108: 709-715.
54. Donovan S, See W, Bonifas J, Stokoe D, Shannon KM (2002) Hyper- activation of protein kinase B and ERK have discrete effects on survival, proliferation, and cytokine expression in Nf1-deficient myeloid cells. Cancer Cell 2: 507-514.
55. Chiang M, Xu L, Shestova O, Histen G, L'heureux S, et al. (2008) Leukemia- associated NOTCH1 alleles are weak tumor initiators but accelerate K-ras- initiated leukemia. J Clin Invest 118: 3181-3194.
56. Kindler T, Cornejo M, Scholl C, Liu J, Leeman D, et al. (2008) K-RasG12D- induced T-cell lymphoblastic lymphoma/leukemias harbor Notch1 muta- tions and are sensitive to gamma-secretase inhibitors. Blood 112: 3373-3382.
57. Dupuy AJ, Akagi K, Largaespada DA, Copeland NG, Jenkins NA (2005) Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436: 221-226.
58. Penit C, Vasseur F, Papiernik M (1988) In vivo dynamics of CD4-8- thymocytes. Proliferation, renewal and differentiation of different cell subsets studied by DNA biosynthetic labeling and surface antigen detection. Eur J Immunol 18: 1343-1350.
59. Tourigny M, Mazel S, Burtrum D, Petrie H (1997) T cell receptor (TCR)- beta gene recombination: dissociation from cell cycle regulation and developmental progression during T cell ontogeny. J Exp Med 185: 1549-1556.
60. Swat W, Shinkai Y, Cheng H, Davidson L, Alt F (1996) Activated Ras signals differentiation and expansion of CD4&Thorn8 &Thorn thymocytes. Proc Natl Acad Sci U S A 93: 4683-4687.
61. Oliveira JB, Bidere N, Niemela JE, Zheng L, Sakai K, et al. (2007) NRAS mutation causes a human autoimmune lymphoproliferative syndrome. Proc Natl Acad Sci U S A 104: 8953-8958.
62. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, et al. (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351: 657-667.
63. Mansour M, Duke V, Foroni L, Patel B, Allen C, et al. (2007) Notch-1 mutations are secondary events in some patients with T-cell acute lymphoblastic leukemia. Clin Cancer Res 13: 6964-6969.
64. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, et al. (2001) Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 15: 3243-3248.
65. Johnson L, Mercer K, Breenbaum D, Bronson R, Crowley D, et al. (2001) Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410: 1111-1116.
66. Guerra C, Mijimolle N, Dhawahir A, Dubus P, Barradas M, et al. (2003) Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context. Cancer Cell 4: 111-120.
67. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, et al. (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4: 437-450.
68. Sansom OJ, Meniel V, Wilkins JA, Cole AM, Oien KA, et al. (2006) Loss of Apc allows phenotypic manifestation of the transforming properties of an endogenous K-ras oncogene in vivo. Proc Natl Acad Sci U S A 103: 14122-14127.
69. Tuveson DA, Hingorani SR (2005) Ductal pancreatic cancer in humans and mice. Cold Spring Harb Symp Quant Biol 70: 65-72.
70. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, et al. (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532.
71. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumori- genesis. Cell 61: 759-767.
72. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, et al. (2005) Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121: 823-835.
73. Szilvassy SJ, Humphries RK, Lansdorp PM, Eaves AC, Eaves CJ (1990) Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc Natl Acad Sci U S A 87: 8736-8740.
74. Schmid I, Cole SW, Korin YD, Zack JA, Giorgi JV (2000) Detection of cell cycle subcompartments by flow cytometric estimation of DNA-RNA content in combination with dual-color immunofluorescence. Cytometry 39: 108-116.
75. Boggs DR (1984) The total marrow mass of the mouse: a simplified method of measurement. Am J Hematol 16: 277-286.