Experimental Hematology
Volume 37, Issue 4 , Pages 435-445.e1 , April 2009

Stem cells of GATA1-related leukemia undergo pernicious changes after 5-fluorouracil treatment

  • Kanako Abe

      Affiliations

    • Graduate School of Comprehensive Human Sciences and Center for Tsukuba Advanced Research Alliance, University of Tsukuba, Tsukuba, Japan
    • Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Japan
  • ,
  • Ritsuko Shimizu

      Affiliations

    • Graduate School of Comprehensive Human Sciences and Center for Tsukuba Advanced Research Alliance, University of Tsukuba, Tsukuba, Japan
  • ,
  • Xiaoqing Pan

      Affiliations

    • Department of Medical Biochemistry, Tohoku University Graduate School of Medicine, Sendai, Japan
  • ,
  • Hiromi Hamada

      Affiliations

    • Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Japan
  • ,
  • Hiroyuki Yoshikawa

      Affiliations

    • Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Japan
  • ,
  • Masayuki Yamamoto

      Affiliations

    • Department of Medical Biochemistry, Tohoku University Graduate School of Medicine, Sendai, Japan
    • ERATO Environmental Research Project, University of Tsukuba, Tsukuba, Japan
    • Corresponding Author InformationOffprint requests to: Masayuki Yamamoto, Ph.D., Department of Medical Biochemistry, Tohoku University Graduate School of Medicine, 2-1 Seiryo-cho, Aoba-ku, Sendai 980-8575, Japan.

Received 4 October 2008 ,Revised 25 November 2008 ,Accepted 18 December 2008.

References 

  1. Dick JE. Normal and leukemic human stem cells assayed in SCID mice. Semin Immunol. 1996;8:197–206
  2. Huntly BJ, Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer. 2005;5:311–321
  3. Wang JC, Lapidot T, Cashman JD, et al. High level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phase. Blood. 1998;91:2406–2414
  4. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–648
  5. 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
  6. Krivtsov AV, Twomey D, Feng Z, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006;442:818–822
  7. Deshpande AJ, Cusan M, Rawat VP, et al. Acute myeloid leukemia is propagated by a leukemic stem cell with lymphoid characteristics in a mouse model of CALM/AF10-positive leukemia. Cancer Cell. 2006;10:363–374
  8. Huntly BJ, Shigematsu H, Deguchi K, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6:587–596
  9. 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
  10. Crispino JD. GATA1 in normal and malignant hematopoiesis. Semin Cell Dev Biol. 2005;16:137–147
  11. Shimizu R, Engel JD, Yamamoto M. GATA1-related leukaemias. Nat Rev Cancer. 2008;8:279–287
  12. Pan X, Ohneda O, Ohneda K, et al. Graded levels of GATA-1 expression modulate survival, proliferation, and differentiation of erythroid progenitors. J Biol Chem. 2005;280:22385–22394
  13. Shimizu R, Kuroha T, Ohneda O, et al. Leukemogenesis caused by incapacitated GATA-1 function. Mol Cell Biol. 2004;24:10814–10825
  14. Takahashi S, Onodera K, Motohashi H, et al. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem. 1997;272:12611–12615
  15. Takahashi S, Komeno T, Suwabe N, et al. Role of GATA-1 in proliferation and differentiation of definitive erythroid and megakaryocytic cells in vivo. Blood. 1998;92:434–442
  16. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797–1806
  17. Hadnagy A, Gaboury L, Beaulieu R, Balicki D. SP analysis may be used to identify cancer stem cell populations. Exp Cell Res. 2006;312:3701–3710
  18. Guo Y, Lubbert M, Engelhardt M. CD34- hematopoietic stem cells: current concepts and controversies. Stem Cells. 2003;21:15–20
  19. Porter EH, Berry RJ. The efficient design of transplantable tumour assays. Br J Cancer. 1963;17:583–595
  20. Suzuki N, Ohneda O, Minegishi N, et al. Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci U S A. 2006;103:2202–2207
  21. 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
  22. Huttmann A, Liu SL, Boyd AW, Li CL. Functional heterogeneity within rhodamine123(lo) Hoechst33342(lo/sp) primitive hemopoietic stem cells revealed by pyronin Y. Exp Hematol. 2001;29:1109–1116
  23. Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149–161
  24. Gothot A, Pyatt R, McMahel J, Rice S, Srour EF. Functional heterogeneity of human CD34(+) cells isolated in subcompartments of the G0 /G1 phase of the cell cycle. Blood. 1997;90:4384–4393
  25. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242–245
  26. Huntly BJP, Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer. 2005;5:311–321
  27. 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
  28. 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
  29. Yuan Y, Zhou L, Miyamoto T, 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 U S A. 2001;98:10398–10403
  30. Miyamoto T, Nagafuji K, Akashi K, et al. Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood. 1996;87:4789–4796
  31. Ghinasi B, Sanchez M, Martelli F, et al. The hypomorphic Gata1low mutation alters the proliferation/differentiation potential of the common megakaryocytic-erythroid progenitor. Blood. 2007;109:1460–1471
  32. McDevitt MA, Shivdasani R, Fujiwara Y, Yang H, Orkin SH. A “knockdown” mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc Natl Acad Sci U S A. 1997;94:6781–6785
  33. Stachura DL, Chou ST, Weiss MJ. Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood. 2006;107:87–97
  34. Vannucchi AM, Bianchi L, Cellai C, et al. Development of myelofibrosis in mice genetically impaired for GATA-2 expression (GATA-1(low)mice). Blood. 2002;100:1123–1132
  35. Martelli F, Chinassi B, Panetta B, et al. Variegation of the phenotype induced by the Gata1low mutation in mice of different genetic back-ground. Blood. 2005;106:102–113
  36. Ito E, Kasai M, Hayashi Y, et al. Expression of erythroid-specific genes in acute megakaryoblastic leukaemia and transient myeloproliferative disorder in Down's syndrome. Br J Haematol. 1995;90:607–614
  37. Gu X, Nagano M, Kanezaki R, et al. Frequent mutations in the GATA-1 gene in the transient myeloproliferative disorder of Down syndrome. Blood. 2003;102:2960–2968
  38. Venezia TA, Merchant AA, Ramos CA, et al. Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol. 2004;2:1640–1651
  39. Doyle LA, Ross DD. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene. 2003;22:7340–7358
  40. Cheng T, Rodrigues N, Shen H, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 2000;287:1804–1808
  41. Leslie NR, Downes CP. PTEN function: how normal cells control it and tumour cells lose it. Biochem J. 2004;382:1–11
  42. Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC. PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev. 2008;22:436–448
  43. Sussman RT, Ricci MS, Hart LS, Sun SY, El-Deiry WS. Chemotherapy-resistant side-population of colon cancer cells has a higher sensitivity to TRAIL than the non-SP, a higher expression of c-Myc and TRAIL-receptor DR4. Cancer Biol Ther. 2007;6:1490–1495
  44. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol. 2006;16:253–264
  45. Wilson A, Murphy MJ, Oskarsson T, et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004;18:2747–2763
  46. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–676
  47. Wernig M, Meissner A, Cassady JP, Jaenisch R. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell. 2008;2:10–12
  48. Nakagawa M, Koyanagi M, Tanabe K, et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2008;26:101–106

PII: S0301-472X(08)00577-8

doi: 10.1016/j.exphem.2008.12.004

Experimental Hematology
Volume 37, Issue 4 , Pages 435-445.e1 , April 2009