Leukemia Research
Volume 33, Issue 12 , Pages 1650-1657 , December 2009

Growth inhibition of AML cells with specific chromosome abnormalities by monoclonal antibodies to receptors for vascular endothelial growth factor

  • Norikazu Imai

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Hiroshi Miwa

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 561 62 3311x3540; fax: +81 561 63 3401.
    • ,
  • Masato Shikami

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Kazuto Suganuma

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Mayuko Gotoh

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Akihito Hiramatsu

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Motohiro Wakabayashi

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Masaya Watarai

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Ichiro Hanamura

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Akira Imamura

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Hidetsugu Mihara

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan
    • ,
  • Kenya Shitara

      Affiliations

    • Antibody Business Office, Pharmaceuticals Business Unit, Kyowa Hakko Kogyo Co, Ltd., Tokyo, Japan
    • ,
  • Masabumi Shibuya

      Affiliations

    • Department of Molecular Oncology, Tokyo Medical and Dental University, Tokyo, Japan
    • ,
  • Masakazu Nitta

      Affiliations

    • Department of Internal Medicine, Division of Hematology, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan

Received 14 January 2009 ,Revised 26 February 2009 ,Accepted 7 March 2009.

References 

  1. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836–841
  2. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841–846
  3. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002;109:625–637
  4. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med. 2004;10:64–71
  5. Suda T, Arai F, Hirao A. Hematopoietic stem cells and their niche. Trends Immunol. 2005;26:426–433
  6. Jin L, Hope KJ, Zhai Q, Smadja-Joffe , Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med. 2006;12:1167–1174
  7. Krause DS, Lazarides K, von Andrian UH, Van Etten RA. Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat Med. 2006;12:1175–1180
  8. Ninomiya M, Abe A, Katsumi A, Xu J, Ito M, Arai F, et al. Homing, proliferation and survival sites of human leukemia cells in vivo in immunodeficient mice. Leukemia. 2007;21:136–142
  9. Dias S, Hattori K, Heissig B, Zhu Z, Wu Y, Witte L, et al. Inhibition of both paracrine and autocrine VEGF/VEGFR-2 signaling pathways is essential to induce long-term remission of xenotransplanted human leukemias. Proc Natl Acad Sci USA. 2001;98:10857–10862
  10. Santos SC, Dias S. Internal and external autocrine VEGF/KDR loops regulate survival of subsets of acute leukemia through distinct signaling pathways. Blood. 2004;103:3883–3889
  11. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669–676
  12. List AF, Glinsmann-Gibson B, Stadheim C, Meuillet EJ, Bellamy W, Powis G. Vascular endothelial growth factor receptor-1 and receptor-2 initiate a phosphatidylinositide 3-kinase-dependent clonogenic response in acute myeloid leukemia cells. Exp Hematol. 2004;32:526–535
  13. Giles FJ, Stopeck AT, Silverman LR, Lancet JE, Cooper MA, Hannah AL, et al. SU5416, a small molecule tyrosine kinase receptor inhibitor, has biologic activity in patients with refractory acute myeloid leukemia or myelodysplastic syndromes. Blood. 2003;102:795–801
  14. Fiedler W, Mesters R, Tinnefeld H, Loges S, Staib P, Duhrsen U, et al. A phase 2 clinical study of SU5416 in patients with refractory acute myeloid leukemia. Blood. 2003;102:2763–2767
  15. Fiedler W, Serve H, Döhner H, Schwittay M, Ottmann OG, O’Farrell AM, et al. A phase 1 study of SU11248 in the treatment of patients with refractory or resistant acute myeloid leukemia (AML) or not amenable to conventional therapy for the disease. Blood. 2005;105:986–993
  16. Giles FJ, Bellamy WT, Estrov Z, O’Brien SM, Verstovsek S, Ravandi F, et al. The anti-angiogenesis agent, AG-013736, has minimal activity in elderly patients with poor prognosis acute myeloid leukemia (AML) or myelodysplastic syndrome (MDS). Leuk Res. 2006;30:801–811
  17. Roboz GJ, Giles FJ, List AF, Cortes JE, Carlin R, Kowalski M, et al. Phase 1 study of PTK787/ZK 222584, a small molecule tyrosine kinase receptor inhibitor, for the treatment of acute myeloid leukemia and myelodysplastic syndrome. Leukemia. 2006;20:952–957
  18. Karp JE, Gojo I, Pili R, Gocke CD, Greer J, Guo C, et al. Targeting vascular endothelial growth factor for relapsed and refractory adult acute myelogenous leukemias: therapy with sequential 1-beta-D-arabinofuranosylcytosine, mitoxantrone, and bevacizumab. Clin Cancer Res. 2004;10:3577–3585
  19. Hiramatsu A, Miwa H, Shikami M, Ikai T, Tajima E, Yamamoto H, et al. Disease-specific expression of VEGF and its receptors in AML cells: possible autocrine pathway of VEGF/type1 receptor of VEGF in t(15;17) AML and VEGF/type2 receptor of VEGF in t(8;21) AML. Leuk Lymphoma. 2006;47:89–95
  20. Imai N, Shikami M, Miwa H, Suganuma K, Hiramatsu A, Watarai M, et al. t(8;21) acute myeloid leukaemia cells are dependent on vascular endothelial growth factor (VEGF)/VEGF receptor type2 pathway and phosphorylation of Akt. Br J Haematol. 2006;135:673–682
  21. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol. 2006;3:24–40
  22. Sawano A, Iwai S, Sakurai Y, Ito M, Shitara K, Nakahata T, et al. Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood. 2001;97:785–791
  23. Saito M, Hamasaki M, Shibuya M. Induction of tube formation by angiopoietin-1 in endothelial cell/fibroblast co-culture is dependent on endogenous VEGF. Cancer Sci. 2003;94:782–790
  24. Willmore E, de Caux S, Sunter NJ, Tilby MJ, Jackson GH, Austin CA, et al. A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood. 2004;103:4659–4665
  25. Grimwade D, Walker H, Oliver F, Wheatley K, Harrison C, Harrison G, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood. 1998;92:2322–2333
  26. Grimwade D, Walker H, Harrison G, Oliver F, Chatters S, Harrison CJ, et al. The predictive value of hierarchical cytogenetic classification in older adults with acute myeloid leukemia (AML): analysis of 1065 patients entered into the United Kingdom Medical Research Council AML11 trial. Blood. 2001;98:1312–1320
  27. Slovak ML, Kopecky KJ, Cassileth PA, Harrington DH, Theil KS, Mohamed A, et al. Karyotypic analysis predicts outcome of preremission and postremission therapy in adult acute myeloid leukemia: a Southwest Oncology Group/Eastern Cooperative Oncology Group Study. Blood. 2000;96:4075–4083
  28. Byrd JC, Mrózek K, Dodge RK, Carroll AJ, Edwards CG, Arthur DC, et al. Pretreatment cytogenetic abnormalities are predictive of induction success, cumulative incidence of relapse, and overall survival in adult patients with de novo acute myeloid leukemia: results from Cancer and Leukemia Group B (CALGB 8461). Blood. 2002;100:4325–4336
  29. Schoch C, Schnittger S, Klause M, Kern W, Hiddemann W, Haferlach T. AML with 11q23/MLL abnormalities as defined by the WHO classification: incidence, partner chromosomes, FAB subtype, age distribution, and prognostic impact in an unselected series of 1897 cytogenetically analyzed AML cases. Blood. 2003;102:2395–2402
  30. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269:26988–26995
  31. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA. 1998;95:9349–9354
  32. Pillozzi S, Brizzi MF, Bernabei PA, Bartolozzi B, Caporale R, Basile V, et al. VEGFR-1 (FLT-1), beta1 integrin, and hERG K+ channel for a macromolecular signaling complex in acute myeloid leukemia: role in cell migration and clinical outcome. Blood. 2007;110:1238–1250
  33. Ikai T, Miwa H, Shikami M, Hiramatsu A, Tajima E, Yamamoto H, et al. Placenta growth factor stimulates the growth of Philadelphia chromosome positive acute lymphoblastic leukemia cells by both autocrine and paracrine pathways. Eur J Haematol. 2005;75:273–279
  34. Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer. 2003;3:89–101
  35. Reilly JT. Class III receptor tyrosine kinases: role in leukaemogenesis. Br J Haematol. 2002;116:744–757
  36. 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
  37. Wang YY, Zhou GB, Yin T, Chen B, Shi JY, Liang WX, et al. AML1-ETO and C-KIT mutation/overexpression in t(8;21) leukemia: implication in stepwise leukemogenesis and response to Gleevec. Proc Natl Acad Sci USA. 2005;102:1104–1109
  38. Nanri T, Matsuno N, Kawakita T, Suzushima H, Kawano F, Mitsuya H, et al. Mutations in the receptor tyrosine kinase pathway are associated with clinical outcome in patients with acute myeloblastic leukemia harboring t(8;21)(q22;q22). Leukemia. 2005;19:1361–1366
  39. Zheng R, Levis M, Piloto O, Brown P, Baldwin BR, Gorin NC, et al. FLT3 ligand causes autocrine signaling in acute myeloid leukemia cells. Blood. 2004;103:267–274

PII: S0145-2126(09)00114-3

doi: 10.1016/j.leukres.2009.03.006

Leukemia Research
Volume 33, Issue 12 , Pages 1650-1657 , December 2009

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