Advertisement

Abl and Cell Death

  • Jean Y. J. Wang
  • Yosuke Minami
  • Jiangyu Zhu
Part of the Molecular Biology Intelligence Unit book series (MBIU)

Abstract

The Abl tyrosine kinase contains nuclear-import and -export signals and undergoes nucleo-cytoplasmic shuttling in proliferating cells. The nuclear Abl is activated by DNA damage or tumor necrosis factor to promote cell death through transcription-dependent and -independent mechanisms. The oncogenic BCR-ABL tyrosine kinase is defective in nuclear import and functions as an inhibitor of apoptosis in the cytoplasm. If allowed to function in the nucleus, BCR-ABL also induces cell death. Abl interacts with several different types of death effectors. However, the precise mechanism by which Abl tyrosine kinase regulates cell death remains to be determined.

Keywords

Ionize Radiation Nuclear Import Nuclear Export Signal Chronic Myelogenous Leukemia Cell Perillyl Alcohol 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Wang JY. Regulation of cell death by the Abl tyrosine kinase. Oncogene 2000; 19(49):5643–5650.PubMedGoogle Scholar
  2. 2.
    Zhu J, Wang JY. Death by Abl: A matter of location. Curr Top Dev Biol 2004; 59:165–192.PubMedGoogle Scholar
  3. 3.
    Woodring PJ, Hunter T, Wang JY. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J Cell Sci 2003; 116 (Pt 13):2613–2626.PubMedGoogle Scholar
  4. 4.
    Nagar B, Hantschel O, Young MA et al. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 2003; 112(6):859–871.PubMedGoogle Scholar
  5. 5.
    Wang JY. Controlling Abl: Auto-inhibition and coinhibition? Nat Cell Biol 2004; 6(1):3–7.PubMedGoogle Scholar
  6. 6.
    Hantschel O, Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 2004; 5(1):33–44.PubMedGoogle Scholar
  7. 7.
    Woodring PJ, Hunter T, Wang JY. Mitotic phosphorylation rescues Abl from F-actin-mediated inhibition. J Biol Chem 2005; 280(11):10318–10325.PubMedGoogle Scholar
  8. 8.
    Smith JM, Katz S, Mayer BJ. Activation of the Abl tyrosine kinase in vivo by Src homology 3 domains from the Src homology 2/Src homology 3 adaptor Nek. J Biol Chem 1999; 274(39):27956–27962.PubMedGoogle Scholar
  9. 9.
    Liu ZG, Baskaran R, Lea-Chou ET et al. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 1996; 384(6606):273–276.PubMedGoogle Scholar
  10. 10.
    Wang JY, Ki SW. Choosing between growth arrest and apoptosis through the retinoblastoma tumour suppressor protein, Abl and p73. Biochem Soc Trans 2001; 29 (Pt 6):666–673.PubMedGoogle Scholar
  11. 11.
    Pendergast AM. The Abl family kinases: Mechanisms of regulation and signaling. Adv Cancer Res 2002; 85:51–100.PubMedGoogle Scholar
  12. 12.
    Kharbanda S, Yuan ZM, Weichselbaum R et al. Functional role for the c-Abl protein tyrosine kinase in the cellular response to genotoxic stress. Biochim Biophys Acta 1997; 1333(2):01–7.Google Scholar
  13. 13.
    Baskaran R, Escobar SR, Wang JY. Nuclear c-Abl is a COOH-terminal repeated domain (CTD)-tyrosine (CTD)-tyrosine kinase-specific for the mammalian RNA polymerase II: Possible role in transcription elongation. Cell Growth Differ 1999; 10(6):387–396.PubMedGoogle Scholar
  14. 14.
    Baskaran R, Dahmus ME, Wang JY. Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc Natl Acad Sci USA 1993; 90(23):11167–11171.PubMedGoogle Scholar
  15. 15.
    Baskaran R, Chiang GG, Wang JY. Identification of a binding site in c-Abl tyrosine kinase for the C-terminal repeated domain of RNA polymerase II. Mol Cell Biol 1996; 16(7):3361–3369.PubMedGoogle Scholar
  16. 16.
    Feller SM, Knudsen B, Hanafusa H. c-Abl kinase regulates the protein binding activity of c-Crk. Embo J 1994; 13(10):2341–2351.PubMedGoogle Scholar
  17. 17.
    Salgia R, Uemura N, Okuda K et al. CRKL links p210BCR/ABL with paxillin in chronic myelog-enous leukemia cells. J Biol Chem 1995; 270(49):29145–29150.PubMedGoogle Scholar
  18. 18.
    Uemura N, Salgia R, Li JL et al. The BCR/ABL oncogene alters interaction of the adapter proteins CRKL and CRK with cellular proteins. Leukemia 1997; 11(3):376–385.PubMedGoogle Scholar
  19. 19.
    Woodring PJ, Litwack ED, O’Leary DD et al. Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J Cell Biol 2002; 156(5):879–892.PubMedGoogle Scholar
  20. 20.
    Kharbanda S, Ren R, Pandey P et al. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 1995; 376(6543):785–788.PubMedGoogle Scholar
  21. 21.
    Shafman T, Khanna KK, Kedar P et al. Interaction between ATM protein and c-Abl in response to DNA damage. Nature 1997; 387(6632):520–523.PubMedGoogle Scholar
  22. 22.
    Baskaran R, Wood LD, Whitaker LL et al. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 1997; 387(6632):516–519.PubMedGoogle Scholar
  23. 23.
    Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer 2003; 3(3):155–168.PubMedGoogle Scholar
  24. 24.
    Durocher D, Jackson SP. DNA-PK, ATM and ATR as sensors of DNA damage: Variations on a theme? Curr Opin Cell Biol 2001; 13(2):225–231.PubMedGoogle Scholar
  25. 25.
    Shiloh Y. ATM: Sounding the double-strand break alarm. Cold Spring Harb Symp Quant Biol 2000; 65:527–533.PubMedGoogle Scholar
  26. 26.
    Gong JG, Costanzo A, Yang HQ et al. The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature 1999; 399(6738):806–809.PubMedGoogle Scholar
  27. 27.
    Kolodner RD, Marsischky GT. Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 1999; 9(1):89–96.PubMedGoogle Scholar
  28. 28.
    Flores-Rozas H, Clark D, Kolodner RD. Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex. Nat Genet 2000; 26(3):375–378.PubMedGoogle Scholar
  29. 29.
    Drotschmann K, Hall MC, Shcherbakova PV et al. DNA binding properties of the yeast Msh2-Msh6 and Mlhl-Pmsl heterodimers. Biol Chem 2002; 383(6):969–975.PubMedGoogle Scholar
  30. 30.
    Lau PJ, Kolodner RD. Transfer of the MSH2. MSH6 complex from proliferating cell nuclear antigen to mispaired bases in DNA. J Biol Chem 2003; 278(1):14–17.PubMedGoogle Scholar
  31. 31.
    Bernstein C, Bernstein H, Payne CM et al. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: Fail-safe protection against carcinogenesis. Mutat Res 2002; 511(2):145–178.PubMedGoogle Scholar
  32. 32.
    Sampath D, Rao VA, Plunkett W. Mechanisms of apoptosis induction by nucleoside analogs. Oncogene 2003; 22(56):9063–9074.PubMedGoogle Scholar
  33. 33.
    Achanta G, Pelicano H, Feng L et al. Interaction of p53 and DNA-PK in response to nucleoside analogues: Potential role as a sensor complex for DNA damage. Cancer Res 2001; 61(24):8723–8729.PubMedGoogle Scholar
  34. 34.
    Shangary S, Brown KD, Adamson AW et al. Regulation of DNA-dependent protein kinase activity by ionizing radiation-activated abl kinase is an ATM-dependent process. J Biol Chem 2000; 275(39):30163–30168.PubMedGoogle Scholar
  35. 35.
    Yuan ZM, Shioya H, Ishiko T et al. p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature 1999; 399(6738):814–817.PubMedGoogle Scholar
  36. 36.
    Agami R, Blandino G, Oren M et al. Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature 1999; 399(6738):809–813.PubMedGoogle Scholar
  37. 37.
    White E, Prives C. DNA damage enables p73. Nature 1999; 399(6738):734–735, 737.PubMedGoogle Scholar
  38. 38.
    Huang Y, Yuan ZM, Ishiko T et al. Pro-apoptotic effect of the c-Abl tyrosine kinase in the cellular response to 1-beta-D-arabinofuranosylcytosine. Oncogene 1997; 15(16):1947–1952.PubMedGoogle Scholar
  39. 39.
    Yuan ZM, Huang Y, Ishiko T et al. Regulation of DNA damage-induced apoptosis by the c-Abl tyrosine kinase. Proc Natl Acad Sci USA 1997; 94(4):1437–1440.PubMedGoogle Scholar
  40. 40.
    Borges HL, Chao C, Xu Y et al. Radiation-induced apoptosis in developing mouse retina exhibits dose-dependent requirement for ATM phosphorylation of p53. Cell Death Differ 2004; 11(5):494–502.PubMedGoogle Scholar
  41. 41.
    Schumacher B, Hofmann K, Boulton S et al. The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr Biol 2001; 11(21):1722–1727.PubMedGoogle Scholar
  42. 42.
    Deng X, Hofmann ER, Villanueva A et al. Caenorhabditis elegans ABL-1 antagonizes p53-mediated germline apoptosis after ionizing irradiation. Nat Genet 2004; 36(8):906–912.PubMedGoogle Scholar
  43. 43.
    Yin XM. Bid, a critical mediator for apoptosis induced by the activation of Fas/TNF-Rl death receptors in hepatocytes. J Mol Med 2000; 78(4):203–211.PubMedGoogle Scholar
  44. 44.
    Yin XM. Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Res 2000; 10(3):161–167.PubMedGoogle Scholar
  45. 45.
    Chau BN, Chen TT, Wan YY et al. Tumor necrosis factor alpha-induced apoptosis requires p73 and c-ABL activation downstream of RB degradation. Mol Cell Biol 2004; 24(10):4438–4447.PubMedGoogle Scholar
  46. 46.
    Dan S, Naito M, Seimiya H et al. Activation of c-Abl tyrosine kinase requires caspase activation and is not involved in JNK/SAPK activation during apoptosis of human monocytic leukemia U937 cells. Oncogene 1999; 18(6):1277–1283.PubMedGoogle Scholar
  47. 47.
    Tan X, Wang JY. The caspase-RB connection in cell death. Trends Cell Biol 1998; 8(3):116–120.PubMedGoogle Scholar
  48. 48.
    Fattman CL, An B, Dou QP. Characterization of interior cleavage of retinoblastoma protein in apoptosis. J Cell Biochem 1997; 67(3):399–408.PubMedGoogle Scholar
  49. 49.
    Chau BN, Borges HL, Chen TT et al. Signal-dependent protection from apoptosis in mice expressing caspase-resistant Rb. Nat Cell Biol 2002; 4(10):757–765.PubMedGoogle Scholar
  50. 50.
    Welch PJ, Wang JY. A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell 1993; 75(4):779–790.PubMedGoogle Scholar
  51. 51.
    Wang JY. Nucleo-cytoplasmic communication in apoptotic response to genotoxic and inflammatory stress. Cell Res 2005; 15(1):43–48.PubMedGoogle Scholar
  52. 52.
    Barila D, Rufini A, Condo I et al. Caspase-dependent cleavage of c-Abl contributes to apoptosis. Mol Cell Biol 2003; 23(8):2790–2799.PubMedGoogle Scholar
  53. 53.
    Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114(2):181–190.PubMedGoogle Scholar
  54. 54.
    Muppidi JR, Tschopp J, Siegel RM. Life and death decisions: Secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 2004; 21(4):461–465.PubMedGoogle Scholar
  55. 55.
    Taagepera S, McDonald D, Loeb JE et al. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc Natl Acad Sci USA 1998; 95(13):7457–7462.PubMedGoogle Scholar
  56. 56.
    Vella V, Zhu J, Frasca F et al. Exclusion of c-Abl from the nucleus restrains the p73 tumor suppression function. J Biol Chem 2003; 278(27):25151–25157.PubMedGoogle Scholar
  57. 57.
    Puri PL, Bhakta K, Wood LD et al. A myogenic differentiation checkpoint activated by genotoxic stress. Nat Genet 2002; 32(4):585–593.PubMedGoogle Scholar
  58. 58.
    Vigneri P, Wang JY. Induction of apoptosis in chronic myelogenous leukemia cells through nuclear entrapment of BCR-ABL tyrosine kinase. Nat Med 2001; 7(2):228–234.PubMedGoogle Scholar
  59. 59.
    Kudo N, Matsumori N, Taoka H et al. Leptomycin B inactivates CRMl/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci USA 1999; 96(16):9112–9117.PubMedGoogle Scholar
  60. 60.
    Herzog KH, Chong MJ, Kapsetaki M et al. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 1998; 280(5366):1089–1091.PubMedGoogle Scholar
  61. 61.
    Villunger A, Michalak EM, Coultas L et al. p53-and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302(5647):1036–1038.PubMedGoogle Scholar
  62. 62.
    Pandita TK, Lieberman HB, Lim DS et al. Ionizing radiation activates the ATM kinase throughout the cell cycle. Oncogene 2000; 19(11):1386–1391.PubMedGoogle Scholar
  63. 63.
    Khanna KK, Keating KE, Kozlov S et al. ATM associates with and phosphorylates p53: Mapping the region of interaction. Nat Genet 1998; 20(4):398–400.PubMedGoogle Scholar
  64. 64.
    Khosravi R, Maya R, Gottlieb T et al. Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc Natl Acad Sci USA 1999; 96(26):14973–14977.PubMedGoogle Scholar
  65. 65.
    Goldberg Z, Vogt Sionov R, Berger M et al. Tyrosine phosphorylation of Mdm2 by c-Abl: Implications for p53 regulation. Embo J 2002; 21(14):3715–3727.PubMedGoogle Scholar
  66. 66.
    Sionov RV, Moallem E, Berger M et al. c-Abl neutralizes the inhibitory effect of Mdm2 on p53. J Biol Chem 1999; 274(13):8371–8374.PubMedGoogle Scholar
  67. 67.
    Goga A, Liu X, Hambuch TM et al. p53 dependent growth suppression by the c-Abl nuclear tyrosine kinase. Oncogene 1995; 11(4):791–799.PubMedGoogle Scholar
  68. 68.
    Sawyers CL, Mclaughlin J, Goga A et al. The nuclear tyrosine kinase c-Abl negatively regulates cell growth. Cell 1994; 77(1):121–131.PubMedGoogle Scholar
  69. 69.
    Roger R, Issaad C, Pallardy M et al. BCR-ABL does not prevent apoptotic death induced by human natural killer or lymphokine-activated killer cells. Blood 1996; 87(3):1113–1122.PubMedGoogle Scholar
  70. 70.
    Truong T, Sun G, Doorly M et al. Modulation of DNA damage-induced apoptosis by cell adhesion is independently mediated by p53 and c-Abl. Proc Nad Acad Sci USA 2003; 100(18):10281–10286.Google Scholar
  71. 71.
    Flores ER, Tsai KY, Crowley D et al. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 2002; 416(6880):560–564.PubMedGoogle Scholar
  72. 72.
    Melino G, Bernassola F, Ranalli M et al. p73 Induces apoptosis via PUMA transactivation and Bax mito-chondrial translocation. J Biol Chem 2004; 279(9):8076–8083.PubMedGoogle Scholar
  73. 73.
    Costanzo A, Merlo P, Pediconi N et al. DNA damage-dependent acetylation of p73 dictates the selective activation of apoptotic target genes. Mol Cell 2002; 9(1):175–186.PubMedGoogle Scholar
  74. 74.
    Baskaran R, Chiang GG, Mysliwiec T et al. Tyrosine phosphorylation of RNA polymerase II carboxyl-terminal domain by the Abl-related gene product. J Biol Chem 1997; 272(30):18905–18909.PubMedGoogle Scholar
  75. 75.
    Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 1996; 274(5288):782–784.PubMedGoogle Scholar
  76. 76.
    Kawai H, Nie L, Yuan ZM. Inactivation of NF-kappaB-dependent cell survival, a novel mechanism for the proapoptotic function of c-Abl. Mol Cell Biol 2002; 22(17):6079–6088.PubMedGoogle Scholar
  77. 77.
    Mihara M, Erster S, Zaika A et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11(3):577–590.PubMedGoogle Scholar
  78. 78.
    Schuler M, Maurer U, Goldstein JC et al. p53 triggers apoptosis in oncogene-expressing fibroblasts by the induction of Noxa and mitochondrial Bax translocation. Cell Death Differ 2003; 10(4):451–460.PubMedGoogle Scholar
  79. 79.
    Li H, Kolluri SK, Gu J et al. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 2000; 289(5482):1159–1164.PubMedGoogle Scholar
  80. 80.
    Jeong JH, Park JS, Moon B et al. Orphan nuclear receptor Nur77 translocates to mitochondria in the early phase of apoptosis induced by synthetic chenodeoxycholic acid derivatives in human stomach cancer cell line SNU-1. Ann NY Acad Sci 2003; 1010:171–177.PubMedGoogle Scholar
  81. 81.
    Konishi A, Shimizu S, Hirota J et al. Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 2003; 114(6):673–688.PubMedGoogle Scholar
  82. 82.
    Komatsu K, Miyashita T, Hang H et al. Human homologue of S. pombe Rad9 interacts with BCL-2/BCL-xL and promotes apoptosis. Nat Cell Biol 2000; 2(1):1–6.PubMedGoogle Scholar
  83. 83.
    Inoue T, Stuart J, Leno R et al. Nuclear import and export signals in control of the p53-related protein p73. J Biol Chem 2002; 277(17):15053–15060.PubMedGoogle Scholar
  84. 84.
    Lee MW, Hirai I, Wang HG. Caspase-3-mediated cleavage of Rad9 during apoptosis. Oncogene 2003; 22(41):6340–6346.PubMedGoogle Scholar
  85. 85.
    Yoshida K, Komatsu K, Wang HG et al. c-Abl tyrosine kinase regulates the human Rad9 checkpoint protein in response to DNA damage. Mol Cell Biol 2002; 22(10):3292–3300.PubMedGoogle Scholar
  86. 86.
    Hopkins KM, Auerbach W, Wang XY et al. Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol Cell Biol 2004; 24(16):7235–7248.PubMedGoogle Scholar
  87. 87.
    Loegering D, Arlander SJ, Hackbarth J et al. Rad9 protects cells from topoisomerase poison-induced cell death. J Biol Chem 2004; 279(18):18641–18647.PubMedGoogle Scholar
  88. 88.
    Parrilla-Castellar ER, Arlander SJ, Karnitz L. Dial 9-1-1 for DNA damage: The Rad9-Husl-Radl (9-1-1) clamp complex. DNA Repair (Amst) 2004; 3(8–9):1009–1014.PubMedGoogle Scholar
  89. 89.
    Wang JY, Cho SK. Coordination of repair, checkpoint, and cell death responses to DNA damage. Adv Protein Chem 2004; 69:101–135.PubMedGoogle Scholar
  90. 90.
    Raina D, Pandey P, Ahmad R et al. c-Abl tyrosine kinase regulates caspase-9 autocleavage in the apoptotic response to DNA damage. J Biol Chem 2005; 280(12):11147–11151.PubMedGoogle Scholar
  91. 91.
    Li B, Cong F, Tan CP et al. Aph2, a protein with a zf-DHHC motif, interacts with c-Abl and has pro-apoptotic activity. J Biol Chem 2002; 277(32):28870–28876.PubMedGoogle Scholar
  92. 92.
    Daley GQ, Baltimore D. Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein. Proc Natl Acad Sci USA 1988; 85(23):9312–9316.PubMedGoogle Scholar
  93. 93.
    Sirard C, Laneuville P, Dick JE. Expression of bcr-abl abrogates factor-dependent growth of human hematopoietic M07E cells by an autocrine mechanism. Blood 1994; 83(6):1575–1585.PubMedGoogle Scholar
  94. 94.
    Mandanas RA, Boswell HS, Lu L et al. BCR/ABL confers growth factor independence upon a murine myeloid cell line. Leukemia 1992; 6(8):796–800.PubMedGoogle Scholar
  95. 95.
    Matulonis U, Salgia R, Okuda K et al. Interleukin-3 and p210 BCR/ABL activate both unique and overlapping pathways of signal transduction in a factor-dependent myeloid cell line. Exp Hematol 1993; 21(11):1460–1466.PubMedGoogle Scholar
  96. 96.
    Mayerhofer M, Valent P, Sperr WR et al. BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor-1 alpha, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood 2002; 100(10):3767–3775.PubMedGoogle Scholar
  97. 97.
    Vejda S, Piwocka K, McKenna SL et al. Autocrine secretion of osteopontin results in degradation of I kappa B in Bcr-Abl-expressing cells. Br J Haematol 2005; 128(5):711–721.PubMedGoogle Scholar
  98. 98.
    Pierce A, Spooncer E, Wooley S et al. Bcr-Abl protein tyrosine kinase activity induces a loss of p53 protein that mediates a delay in myeloid differentiation. Oncogene 2000; 19(48):5487–5497.PubMedGoogle Scholar
  99. 99.
    Trotta R, Vignudelli T, Candini O et al. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 2003; 3(2):145–160.PubMedGoogle Scholar
  100. 100.
    Amarante-Mendes GP, Finucane DM, Martin SJ et al. Anti-apoptotic oncogenes prevent caspase-dependent and independent commitment for cell death. Cell Death Differ 1998; 5(4):298–306.PubMedGoogle Scholar
  101. 101.
    Sanchez-Garcia I, Grutz G. Tumorigenic activity of the BCR-ABL oncogenes is mediated by BCL2. Proc Natl Acad Sci USA 1995; 92(12):5287–5291.PubMedGoogle Scholar
  102. 102.
    Uckun FM, Yang Z, Sather H et al. Cellular expression of antiapoptotic BCL-2 oncoprotein in newly diagnosed childhood acute lymphoblastic leukemia: A Children’s Cancer Group Study. Blood 1997; 89(10):3769–3777.PubMedGoogle Scholar
  103. 103.
    Keeshan K, Cotter TG, McKenna SL. High Bcr-Abl expression prevents the translocation of Bax and Bad to the mitochondrion. Leukemia 2002; 16(9):1725–1734.PubMedGoogle Scholar
  104. 104.
    Deming PB, Schafer ZT, Tashker JS et al. Bcr-Abl-mediated protection from apoptosis downstream of mitochondrial cytochrome c release. Mol Cell Biol 2004; 24(23):10289–10299.PubMedGoogle Scholar
  105. 105.
    La Rosee P, Johnson K, O’Dwyer ME et al. In vitro studies of the combination of imatinib mesylate (Gleevec) and arsenic trioxide (Trisenox) in chronic myelogenous leukemia. Exp Hematol 2002; 30(7):729–737.PubMedGoogle Scholar
  106. 106.
    Nimmanapalli R, Bali P, O’Bryan E et al. Arsenic trioxide inhibits translation of mRNA of bcr-abl, resulting in attenuation of Bcr-Abl levels and apoptosis of human leukemia cells. Cancer Res 2003; 63(22):7950–7958.PubMedGoogle Scholar
  107. 107.
    Nimmanapalli R, O’Bryan E, Bhalla K. Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res 2001; 61(5):1799–1804.PubMedGoogle Scholar
  108. 108.
    Cheong JW, Chong SY, Kim JY et al. Induction of apoptosis by apicidin, a histone deacetylase inhibitor, via the activation of mitochondria-dependent caspase cascades in human Bcr-Abl-positive leukemia cells. Clin Cancer Res 2003; 9(13):5018–5027.PubMedGoogle Scholar
  109. 109.
    Nimmanapalli R, Fuino L, Bali P et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or-refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res 2003; 63(16):5126–5135.PubMedGoogle Scholar
  110. 110.
    Kim JS, Jeung HK, Cheong JW et al. Apicidin potentiates the imatinib-induced apoptosis of Bcr-Abl-positive human leukaemia cells by enhancing the activation of mitochondria-dependent caspase cascades. Br J Haematol 2004; 124(2):166–178.PubMedGoogle Scholar
  111. 111.
    Dou QP, McGuire TF, Peng Y et al. Proteasome inhibition leads to significant reduction of Bcr-Abl expression and subsequent induction of apoptosis in K562 human chronic myelogenous leukemia cells. J Pharmacol Exp Ther 1999; 289(2):781–790.PubMedGoogle Scholar
  112. 112.
    Dai Y, Rahmani M, Pei XY et al. Bortezomib and flavopiridol interact synergistically to induce apoptosis in chronic myeloid leukemia cells resistant to imatinib mesylate through both Bcr/Abl-dependent and-independent mechanisms. Blood 2004; 104(2):509–518.PubMedGoogle Scholar
  113. 113.
    Mayerhofer M, Aichberger KJ, Florian S et al. Identification of mTOR as a novel bifunctional target in chronic myeloid leukemia: Dissection of growth-inhibitory and VEGF-suppressive effects of rapamycin in leukemic cells. Faseb J 2005.Google Scholar
  114. 114.
    Mohi MG, Boulton C, Gu TL et al. Combination of rapamycin and protein tyrosine kinase (PTK) inhibitors for the treatment of leukemias caused by oncogenic PTKs. Proc Natl Acad Sci USA 2004; 101(9):3130–3135.PubMedGoogle Scholar
  115. 115.
    Tauchi T, Sumi M, Nakajima A et al. BCL-2 antisense oligonucleotide genasense is active against imatinib-resistant BCR-ABLpositive cells. Clin Cancer Res 2003; 9(11):4267–4273.PubMedGoogle Scholar
  116. 116.
    Ptasznik A, Nakata Y, Kalota A et al. Short interfering RNA (siRNA) targeting the Lyn kinase induces apoptosis in primary, and drug-resistant, BCR-ABL1(+) leukemia cells. Nat Med 2004; 10(11):1187–1189.PubMedGoogle Scholar
  117. 117.
    Planner R, Kadlec L, DeMali KA et al. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev 1999; 13(18):2400–2411.Google Scholar
  118. 118.
    Fang G, Kim CN, Perkins CL et al. CGP57148B (STI-571) induces differentiation and apoptosis and sensitizes Bcr-Abl-positive human leukemia cells to apoptosis due to antileukemic drugs. Blood 2000; 96(6):2246–2253.PubMedGoogle Scholar
  119. 119.
    Maguer-Satta V, Burl S, Liu L et al. BCR-ABL accelerates C2-ceramide-induced apoptosis. Oncogene 1998; 16(2):237–248.PubMedGoogle Scholar
  120. 120.
    Takao N, Mori R, Kato H et al. c-Abl tyrosine kinase is not essential for ataxia telangiectasia mutated functions in chromosomal maintenance. J Biol Chem 2000; 275(2):725–728.PubMedGoogle Scholar
  121. 121.
    Miller HL, Lee Y, Zhao J et al. Atm and c-Abl cooperate in the response to genotoxic stress during nervous system development. Brain Res Dev Brain Res 2003; 145(1):31–38.PubMedGoogle Scholar
  122. 122.
    Dierov J, Dierova R, Carroll M. BCR/ABL translocates to the nucleus and disrupts an ATR-dependent intra-S phase checkpoint. Cancer Cell 2004; 5(3):275–285.PubMedGoogle Scholar
  123. 123.
    Foray N, Marot D, Randrianarison V et al. Constitutive association of BRCA1 and c-Abl and its ATM-dependent disruption after irradiation. Mol Cell Biol 2002; 22(12):4020–4032.PubMedGoogle Scholar
  124. 124.
    Cong F, Tang J, Hwang BJ et al. Interaction between UV-damaged DNA binding activity proteins and the c-Abl tyrosine kinase. J Biol Chem 2002; 277(38):34870–34878.PubMedGoogle Scholar
  125. 125.
    Oelgeschlager T. Regulation of RNA polymerase II activity by CTD phosphorylation and cell cycle control. J Cell Physiol 2002; 190(2):160–169.PubMedGoogle Scholar
  126. 126.
    Kharbanda S, Pandey P, Jin S et al. Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature 1997; 386(6626):732–735.PubMedGoogle Scholar
  127. 127.
    Jin S, Kharbanda S, Mayer B et al. Binding of Ku and c-Abl at the kinase homology region of DNA-dependent protein kinase catalytic subunit. J Biol Chem 1997; 272(40):24763–24766.PubMedGoogle Scholar
  128. 128.
    Yuan SS, Chang HL, Lee EY. Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM(-/-) and c-Abl(-/-) cells. Mutat Res 2003; 525(1–2):85–92.PubMedGoogle Scholar
  129. 129.
    Yuan ZM, Huang Y, Ishiko T et al. Regulation of Rad51 function by c-Abl in response to DNA damage. J Biol Chem 1998; 273(7):3799–3802.PubMedGoogle Scholar
  130. 130.
    Chen G, Yuan SS, Liu W et al. Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J Biol Chem 1999; 274(18):12748–12752.PubMedGoogle Scholar
  131. 131.
    Kitao H, Yuan ZM. Regulation of ionizing radiation-induced Rad52 nuclear foci formation by c-Abl-mediated phosphorylation. J Biol Chem 2002; 277(50):48944–48948.PubMedGoogle Scholar
  132. 132.
    Welch PJ, Wang JY. Abrogation of retinoblastoma protein function by c-Abl through tyrosine kinase-dependent and-independent mechanisms. Mol Cell Biol 1995; 15(10):5542–5551.PubMedGoogle Scholar
  133. 133.
    Welch PJ, Wang JY. Disruption of retinoblastoma protein function by coexpression of its C pocket fragment. Genes Dev 1995; 9(1):31–46.PubMedGoogle Scholar
  134. 134.
    Wen ST, Jackson PK, Van Etten RA. The cytostatic function of c-Abl is controlled by multiple nuclear localization signals and requires the p53 and Rb tumor suppressor gene products. Embo J 1996; 15(7):1583–1595.PubMedGoogle Scholar
  135. 135.
    Cho JW, Chung J, Baek WK et al. RB-resistant Abl kinase induces delayed cell cycle progression and increases susceptibility to apoptosis upon cellular stresses through interaction with p53. Int J Oncol 2003; 22(6):1193–1199.PubMedGoogle Scholar
  136. 136.
    Yu D, Khan E, Khaleque MA et al. Phosphorylation of DNA topoisomerase 1 by the c-Abl tyrosine kinase confers camptothecin sensitivity. J Biol Chem 2004.Google Scholar
  137. 137.
    Yuan ZM, Huang Y, Fan MM et al. Genotoxic drugs induce interaction of the c-Abl tyrosine kinase and the tumor suppressor protein p53. J Biol Chem 1996; 271(43):26457–26460.PubMedGoogle Scholar
  138. 138.
    Cheng WH, von Kobbe C, Opresko PL et al. Werner syndrome protein phosphorylation by abl tyrosine kinase regulates its activity and distribution. Mol Cell Biol 2003; 23(18):6385–6395.PubMedGoogle Scholar
  139. 139.
    Wen ST, Van Etten RA. The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev 1997; 11(19):2456–2467.PubMedGoogle Scholar
  140. 140.
    Nimmanapalli R, Porosnicu M, Nguyen D et al. Cotreatment with STI-571 enhances tumor necrosis factor alpha-related apoptosis-inducing ligand (TRAIL or apo-2L)-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Clin Cancer Res 2001; 7(2):350–357.PubMedGoogle Scholar
  141. 141.
    Bedi A, Barber JP, Bedi GC et al. BCR-ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: A mechanism of resistance to multiple anticancer agents. Blood 1995; 86(3):1148–1158.PubMedGoogle Scholar
  142. 142.
    Uno K, Inukai T, Kayagaki N et al. TNF-related apoptosis-inducing ligand (TRAIL) frequently induces apoptosis in Philadelphia chromosome-positive leukemia cells. Blood 2003; 101(9):3658–3667.PubMedGoogle Scholar
  143. 143.
    McGahon AJ, Nishioka WK, Martin SJ et al. Regulation of the Fas apoptotic cell death pathway by Abl. J Biol Chem 1995; 270(38):22625–22631.PubMedGoogle Scholar
  144. 144.
    Amarante-Mendes GP, Naekyung Kim C, Liu L et al. Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome C and activation of caspase-3. Blood 1998; 91(5):1700–1705.PubMedGoogle Scholar
  145. 145.
    Amarante-Mendes GP, McGahon AJ, Nishioka WK et al. Bcl-2-independent Bcr-Abl-mediated resistance to apoptosis: Protection is correlated with up regulation of Bcl-xL. Oncogene 1998; 16(11):1383–1390.PubMedGoogle Scholar
  146. 146.
    Xenaki D, Pierce A, Underhill-Day N et al. Bcr-Abl-mediated molecular mechanism for apoptotic suppression in multipotent haemopoietic cells: A role for PKCbetall. Cell Signal 2004; 16(2):145–156.PubMedGoogle Scholar
  147. 147.
    McGahon A, Bissonnette R, Schmitt M et al. BCR-ABL maintains resistance of chronic myelog-enous leukemia cells to apoptotic cell death. Blood 1994; 83(5):1179–1187.PubMedGoogle Scholar
  148. 148.
    Slupianek A, Hoser G, Majsterek I et al. Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis. Mol Cell Biol 2002; 22(12):4189–4201.PubMedGoogle Scholar
  149. 149.
    Slupianek A, Schmutte C, Tombline G et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol Cell 2001; 8(4):795–806.PubMedGoogle Scholar
  150. 150.
    Thiesing JT, Ohno-Jones S, Kolibaba KS et al. Efficacy of STI571, an abl tyrosine kinase inhibitor, in conjunction with other antileukemic agents against bcr-abl-positive cells. Blood 2000; 96(9):3195–3199.PubMedGoogle Scholar
  151. 151.
    Mc Gee MM, Campiani G, Ramunno A et al. Pyrrolo-l,5-benzoxazepines induce apoptosis in chronic myelogenous leukemia (CML) cells by bypassing the apoptotic suppressor bcr-abl. J Pharmacol Exp Ther 2001; 296(1):31–40.Google Scholar
  152. 152.
    Nishii K, Kabarowski JH, Gibbons DL et al. ts BCR-ABL kinase activation confers increased resistance to genotoxic damage via cell cycle block. Oncogene 1996; 13(10):2225–2234.PubMedGoogle Scholar
  153. 153.
    Jamieson L, Carpenter L, Biden TJ et al. Protein kinase Ciota activity is necessary for Bcr-Abl-mediated resistance to drug-induced apoptosis. J Biol Chem 1999; 274(7):3927–3930.PubMedGoogle Scholar
  154. 154.
    Canitrot Y, Falinski R, Louat T et al. p210 BCR/ABL kinase regulates nucleotide excision repair (NER) and resistance to UV radiation. Blood 2003; 102(7):2632–2637.PubMedGoogle Scholar
  155. 155.
    Belhoussine R, Morjani H, Gillet R et al. Two distinct modes of oncoprotein expression during apoptosis resistance in vincristine and daunorubicin multidrug-resistant HL60 cells. Adv Exp Med Biol 1999; 457:365–381.PubMedGoogle Scholar
  156. 156.
    Santucci MA, Anklesaria P, Laneuville P et al. Expression of p210 bcr/abl increases hematopoietic progenitor cell radiosensitivity. Int J Radiat Oncol Biol Phys 1993; 26(5):831–836.PubMedGoogle Scholar
  157. 157.
    Abdelhaleem M. The actinomycin D-induced apoptosis in BCR-ABL-positive K562 cells is associated with cytoplasmic translocation and cleavage of RNA helicase A. Anticancer Res 2003; 23(1A):485–490.PubMedGoogle Scholar
  158. 158.
    Xu Y, Voelter-Mahlknecht S, Mahlknecht U. The histone deacetylase inhibitor suberoylanilide hydroxamic acid down-regulates expression levels of Bcr-abl, c-Myc and HDAC3 in chronic my-eloid leukemia cell lines. Int J Mol Med 2005; 15(1):169–172.PubMedGoogle Scholar
  159. 159.
    Rizzo MT, Pudlo N, Farrell L et al. Specificity of arachidonic acid-induced inhibition of growth and activation of c-jun kinases and p38 mitogen-activated protein kinase in hematopoietic cells. Prostaglandins Leukot Essent Fatty Acids 2002; 66(1):31–40.PubMedGoogle Scholar
  160. 160.
    Rizzo MT, Regazzi E, Garau D et al. Induction of apoptosis by arachidonic acid in chronic my-eloid leukemia cells. Cancer Res 1999; 59(19):5047–5053.PubMedGoogle Scholar
  161. 161.
    Urbano A, Koc Y, Foss FM. Arginine butyrate downregulates p210 bcr-abl expression and induces apoptosis in chronic myelogenous leukemia cells. Leukemia 1998; 12(6):930–936.PubMedGoogle Scholar
  162. 162.
    Puccetti E, Guller S, Orleth A et al. BCR-ABL mediates arsenic trioxide-induced apoptosis independently of its aberrant kinase activity. Cancer Res 2000; 60(13):3409–3413.PubMedGoogle Scholar
  163. 163.
    Yin T, Wu YL, Sun HP et al. Combined effects of As4S4 and imatinib on chronic myeloid leukemia cells and BCR-ABL oncoprotein. Blood 2004; 104(13):4219–4225.PubMedGoogle Scholar
  164. 164.
    Mukai M, Che XF, Furukawa T et al. Reversal of the resistance to STI571 in human chronic myelogenous leukemia K562 cells. Cancer Sci 2003; 94(6):557–563.PubMedGoogle Scholar
  165. 165.
    Hood KA, West LM, Northcote PT et al. Induction of apoptosis by the marine sponge (Mycale) metabolites, mycalamide A and pateamine. Apoptosis 2001; 6(3):207–219.PubMedGoogle Scholar
  166. 166.
    Nimmanapalli R, O’Bryan E, Huang M et al. Molecular characterization and sensitivity of STI-571 (imatinib mesylate, Gleevec)-resistant, Bcr-Abl-positive, human acute leukemia cells to SRC kinase inhibitor PD180970 and 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2002; 62(20):5761–5769.PubMedGoogle Scholar
  167. 167.
    Gorre ME, Ellwood-Yen K, Chiosis G et al. BCR-ABL point mutants isolated from patients with imatinib mesylate-resistant chronic myeloid leukemia remain sensitive to inhibitors of the BCR-ABL chaperone heat shock protein 90. Blood 2002; 100(8):3041–3044.PubMedGoogle Scholar
  168. 168.
    Maru Y, Bergmann E, Coin F et al. TFIIH functions are altered by the P210BCR-ABL oncoprotein produced on the Philadelphia chromosome. Mutat Res 2001; 483(1–2):83–88.PubMedGoogle Scholar
  169. 169.
    Jain SK, de Aos I, Inai Y et al. Inactivation of wild-type BCR/ABL tyrosine kinase in hematopoietic cells by mild hyperthermia. Leukemia 2000; 14(5):845–852.PubMedGoogle Scholar
  170. 170.
    Thijsen SF, van Oostveen JW, Schuurhuis GJ et al. Hypersensitivity of bcr-abl-positive progenitors to hyperthermia in patients with chronic myeloid leukemia. Leukemia 1997; 11(10):1762–1768.PubMedGoogle Scholar
  171. 171.
    Luchetti F, Gregorini A, Papa S et al. The K562 chronic myeloid leukemia cell line undergoes apoptosis in response to interferon-alpha. Haematologica 1998; 83(11):974–980.PubMedGoogle Scholar
  172. 172.
    Andrews IIIrd DF, Singer JW, Collins SJ. Effect of recombinant alpha-interferon on the expression of the bcr-abl fusion gene in human chronic myelogenous human leukemia cell lines. Cancer Res 1987; 47(24 Pt 1):6629–6632.PubMedGoogle Scholar
  173. 173.
    Grebenova D, Kuzelova K, Fuchs O et al. Interferon-alpha suppresses proliferation of chronic myelogenous leukemia cells K562 by extending cell cycle S-phase without inducing apoptosis. Blood Cells Mol Dis 2004; 32(1):262–269.PubMedGoogle Scholar
  174. 174.
    Feny-Dumazet H, Mamani-Matsuda M, Dupouy M et al. Nitric oxide induces the apoptosis of human BCR-ABL-positive myeloid leukemia cells: Evidence for the chelation of intracellular iron. Leukemia 2002; 16(4):708–715.Google Scholar
  175. 175.
    Baron F, Turhan AG, Giron-Michel J et al. Leukemic target susceptibility to natural killer cytotoxicity: Relationship with BCR-ABL expression. Blood 2002; 99(6):2107–2113.PubMedGoogle Scholar
  176. 176.
    Qiao N, Lam J, Reynaud D et al. The hepoxilin analog PBT-3 induces apoptosis in BCR-ABL-positive K562 leukemia cells. Anticancer Res 2003; 23(5A):3617–3622.PubMedGoogle Scholar
  177. 177.
    Chen Y, Hu D. Effects of POH in combination with STI571 on the proliferation and apoptosis of K562 cells. J Huazhong Univ Sci Technolog Med Sci 2004; 24(1):41–44.PubMedGoogle Scholar
  178. 178.
    Clark SS, Perman SM, Sahin MB et al. Antileukemia activity of perillyl alcohol (POH): Uncoupling apoptosis from G0/G1 arrest suggests that the primary effect of POH on Bcr/Abl-transformed cells is to induce growth arrest. Leukemia 2002; 16(2):213–222.PubMedGoogle Scholar
  179. 179.
    Nakajima A, Tauchi T, Sumi M et al. Efficacy of SCH66336, a farnesyl transferase inhibitor, in conjunction with imatinib against BCR-ABL-positive cells. Mol Cancer Ther 2003; 2(3):219–224.PubMedGoogle Scholar
  180. 180.
    Peters DG, Hoover RR, Gerlach MJ et al. Activity of the farnesyl protein transferase inhibitor SCH66336 against BCR/ABL-induced murine leukemia and primary cells from patients with chronic myeloid leukemia. Blood 2001; 97(5):1404–1412.PubMedGoogle Scholar
  181. 181.
    Hoover RR, Mahon FX, Melo JV et al. Overcoming STI571 resistance with the farnesyl transferase inhibitor SCH66336. Blood 2002; 100(3):1068–1071.PubMedGoogle Scholar
  182. 182.
    Tauchi T, Shin-Ya K, Sashida G et al. Activity of a novel G-quadruplex-interactive telomerase inhibitor, telomestatin (SOT-095), against human leukemia cells: Involvement of ATM-dependent DNA damage response pathways. Oncogene 2003; 22(34):5338–5347.PubMedGoogle Scholar
  183. 183.
    Tauchi T, Nakajima A, Sashida G et al. Inhibition of human telomerase enhances the effect of the tyrosine kinase inhibitor, imatinib, in BCR-ABL-positive leukemia cells. Clin Cancer Res 2002; 8(11):3341–3347.PubMedGoogle Scholar
  184. 184.
    Fujisaki T, Otsuka T, Gondo H et al. Bestatin selectively suppresses the growth of leukemic stem/progenitor cells with BCR/ABL mRNA transcript in patients with chronic myelogeneous leukemia. Int Immunopharmacol 2003; 3(6):901–907.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2006

Authors and Affiliations

  • Jean Y. J. Wang
    • 1
  • Yosuke Minami
    • 2
  • Jiangyu Zhu
    • 2
  1. 1.Division of Hematology-Oncology, Department of Medicine, Moores Cancer Center, School of MedicineUniversity of California San DiegoLa JollaUSA
  2. 2.Division of Biological SciencesUniversity of California-San DiegoLa JollaUSA

Personalised recommendations