The impact of arsenic trioxide and all-trans retinoic acid on p53 R273H-codon mutant glioblastoma

Tumor Biology

Volumn 35, Issue 5, 2014, Pages 4567-4580

  Karsy, Michael ^a   Albert, Ladislau ^b   Murali, Raj ^b   Jhanwar Uniyal, Meena ^b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

ATO; ATRA; CSC; GBM; MAPK

Indexed keywords

ARSENIC TRIOXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN P53; RETINOIC ACID; ANTINEOPLASTIC AGENT; MITOGEN ACTIVATED PROTEIN KINASE; ORGANOARSENIC DERIVATIVE; OXIDE;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GLIA CELL; GLIOBLASTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; BRAIN TUMOR; CODON; DRUG EFFECT; GENETICS; HUMAN; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CODON; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, P53; GLIOBLASTOMA; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASTIC STEM CELLS; OXIDES; TRETINOIN;

EID: 84902959542     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-013-1601-6     Document Type: Article

References (88)

1. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, et al. Long-term survival with glioblastoma multiforme. Brain. 2007;130:2596-606. (Pubitemid 47511715)
2. Louis DN, Ohgaki HH, Wiestler OD, Cavenee WK. WHO classification of tumours of the central nervous system. 4th ed. Albany: WHO Press; 2007.
3. Li S, Jiang T, Li G, Wang Z. Impact of p53 status to response of temozolomide in low MGMT expression glioblastomas: preliminary results. Neurol Res. 2008;30:567-70. (Pubitemid 352032552)
4. Kim EH, Yoon MJ, Kim SU, Kwon TK, Sohn S, Choi KS. Arsenic trioxide sensitizes human glioma cells, but not normal astrocytes, to TRAIL-induced apoptosis via CCAAT/enhancer-binding protein homologous protein-dependent DR5 up-regulation. Cancer Res. 2008;68:266-75. (Pubitemid 351380128)
5. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJB, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10:459-66.
6. Ohgaki H, Kleihues P. Genetic profile of astrocytic and oligodendroglial gliomas. Brain Tumor Pathol. 2011;28:177-83.
7. Wang Y, Yang J, Zheng H, Tomasek GJ, Zhang P, McKeever PE, et al. Expression of mutant p53 proteins implicates a lineage relationship between neural stemcells andmalignant astrocytic glioma in a murine model. Cancer Cell. 2009;15:514-26.
8. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen A-J, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature. 2008;455:1129-33.
9. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455:1061-8.
10. England B, Huang T, Karsy M. Current understanding of the role and targeting of tumor suppressor p53 in glioblastoma multiforme. Tumour Biol. 2013;34:2063-74.
11. Sami A, Karsy M. Targeting the PI3K/AKT/mTOR signaling pathway in glioblastoma: novel therapeutic agents and advances in understanding. Tumour Biol. 2013;34:1991-2002.
12. Okorokov AL, Orlova EV. Structural biology of the p53 tumour suppressor. Curr Opin Struct Biol. 2009;19:197-202.
13. Houillier C, Lejeune J, Benouaich-Amiel A, Laigle-Donadey F, Criniere E, Mokhtari K, et al. Prognostic impact of molecular markers in a series of 220 primary glioblastomas. Cancer. 2006;106:2218-23. (Pubitemid 43673244)
14. Felsberg J, Rapp M, Loeser S, Fimmers R, Stummer W, Goeppert M, et al. Prognostic significance of molecular markers and extent of resection in primary glioblastoma patients. Clin Cancer Res. 2009;15:6683-93.
15. Guimaraes DP, Hainaut P. TP53: a key gene in human cancer. Biochimie. 2002;84:83-93. (Pubitemid 34477096)
16. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell. 2009;137:413-31.
17. Bullock AN, Fersht AR. Rescuing the function of mutant p53. Nat Rev Cancer. 2001;1:68-76. (Pubitemid 33741882)
18. Cho Y, Gorina S, Jeffrey PD, Pavletich NP. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science. 1994;265:346-55. (Pubitemid 24259959)
19. Sanai N, Alvarez-Buylla A, Berger MS. Neural stem cells and the origin of gliomas. N Engl J Med. 2005;353:811-22.
20. Nduom EK-E, Hadjipanayis CG, VanMeir EG. Glioblastoma cancer stem-like cells: implications for pathogenesis and treatment. Cancer J. 2012;18:100-6.
21. Rich JN, Eyler CE. Cancer stem cells in brain tumor biology. Cold Spring Harb Symp Quant Biol. 2008;73:411-20.
22. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003;100:15178-83. (Pubitemid 37518036)
23. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-8. (Pubitemid 37187480)
24. Vescovi AL, Galli R, Reynolds BA. Brain tumour stemcells. Nat Rev Cancer. 2006;6:425-36.
25. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-60. (Pubitemid 44949604)
26. Karsy M, Albert L, Tobias ME, Murali R, Jhanwar-Uniyal M. All-trans retinoic acid modulates cancer stem cells of glioblastoma multiforme in an MAPK-dependent manner. Anticancer Res. 2010;30:4915-20.
27. Antman KH. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist. 2001;6 Suppl 2:1-2. (Pubitemid 32405842)
28. Dilda PJ, Hogg PJ. Arsenical-based cancer drugs. Cancer Treat Rev. 2007;33:542-64. (Pubitemid 47355338)
29. Ralph SJ. Arsenic-based antineoplastic drugs and their mechanisms of action. Met Based Drugs. 2008;2008:260146.
30. Miller WH, Schipper HM, Lee JS, Singer J, Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 2002;62:3893-903. (Pubitemid 34792653)
31. Zharova TV, Vinogradov AD. Energy-linked binding of Pi is required for continuous steady-state proton-translocating ATP hydrolysis catalyzed by F0.F1 ATP synthase. Biochemistry. 2006;45:14552-8. (Pubitemid 44865209)
32. Hong SH, Yang Z, Privalsky ML. Arsenic trioxide is a potent inhibitor of the interaction of SMRT corepressor with its transcription factor partners, including the PML-retinoic acid receptor alpha oncoprotein found in human acute promyelocytic leukemia. Mol Cell Biol. 2001;21:7172-82. (Pubitemid 32953471)
33. Eblin KE, Bowen ME, Cromey DW, Bredfeldt TG, Mash EA, Lau SS, et al. Arsenite and monomethylarsonous acid generate oxidative stress response in human bladder cell culture. Toxicol Appl Pharmacol. 2006;217:7-14. (Pubitemid 44740437)
34. Ning S, Knox SJ. Increased cure rate of glioblastoma using concurrent therapywith radiotherapy and arsenic trioxide. Int J Radiat Oncol Biol Phys. 2004;60:197-203. (Pubitemid 39165485)
35. Tomuleasa C, Soritau O, Kacso G, Fischer-Fodor E, Cocis A, Ioani H, et al. Arsenic trioxide sensitizes cancer stem cells to chemoradiotherapy. A new approach in the treatment of inoperable glioblastoma multiforme. J BUON. 2010;15:758-62.
36. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y, Kondo S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene. 2005;24:980-91. (Pubitemid 40313875)
37. Zhen Y, Zhao S, Li Q, Li Y, Kawamoto K. Arsenic trioxide-mediated Notch pathway inhibition depletes the cancer stem-like cell population in gliomas. Cancer Lett. 2010;292:64-72.
38. Ning S, Knox SJ. Optimization of combination therapy of arsenic trioxide and fractionated radiotherapy for malignant glioma. Int J Radiat Oncol Biol Phys. 2006;65:493-8.
39. Wu J, Ji Z, Liu H, Liu Y, Han D, Shi C, et al. Arsenic trioxide depletes cancer stem-like cells and inhibits repopulation of neurosphere derived from glioblastoma by downregulation of Notch pathway. Toxicol Lett. 2013;220:61-9.
40. Chiu H-W, Ho S-Y, Guo H-R, Wang Y-J. Combination treatment with arsenic trioxide and irradiation enhances autophagic effects in U118-MG cells through increased mitotic arrest and regulation of PI3K/Akt and ERK1/2 signaling pathways. Autophagy. 2009;5:472-83.
41. Dizaji MZ, Malehmir M, Ghavamzadeh A, Alimoghaddam K, Ghaffari SH. Synergistic effects of arsenic trioxide and silibinin on apoptosis and invasion in human glioblastoma U87MG cell line. Neurochem Res. 2012;37:370-80.
42. Vogelstein B, Kinzler KW. The multistep nature of cancer. Trends Genet. 1993;9:138-41. (Pubitemid 23098782)
43. Gulati N, Karsy M, Albert L, Murali R, Jhanwar-Uniyal M. Involvement of mTORC1 and mTORC2 in regulation of glioblastoma multiforme growth and motility. Int J Oncol. 2009;35:731-40.
44. Albert L, Karsy M, Murali R, Jhanwar-Uniyal M. Inhibition of mTOR activates the MAPK pathway in glioblastoma multiforme. Cancer Genomics Proteomics. 2009;6:255-61.
45. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307-10.
46. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA, Kinzler KW. Cancer genome landscapes. Science. 2013;339:1546-58.
47. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-11. (Pubitemid 33041634)
48. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G, et al. Targeting of the Bmi-1 oncogene/stem cell renewal factor by MicroRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 2008;68:9125-30.
49. Gangemi RMR, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells. 2009;27:40-8.
50. Wang J, Wang H, Li Z, Wu Q, Lathia JD, McLendon RE, et al. c-Myc is required for maintenance of glioma cancer stem cells. PLoS ONE. 2008;3:e3769.
51. Du Z, Jia D, Liu S,Wang F, Li G, Zhang Y, et al. Oct4 is expressed in human gliomas and promotes colony formation in glioma cells. Glia. 2009;57:724-33.
52. Piccirillo SGM, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444:761-5. (Pubitemid 44949605)
53. Eyler CE, Foo W-C, LaFiura KM, McLendon RE, Hjelmeland AB, Rich JN. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells. 2008;26:3027-36.
54. Kanzawa T, Kondo Y, Ito H, Kondo S, Germano I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res. 2003;63:2103-8. (Pubitemid 36538613)
55. Lin T-H, Kuo H-C, Chou F-P, Lu F-J. Berberine enhances inhibition of glioma tumor cell migration and invasiveness mediated by arsenic trioxide. BMC Cancer. 2008;8:58.
56. Grimm SA, Marymont M, Chandler JP, Muro K, Newman SB, Levy RM, et al. Phase I study of arsenic trioxide and temozolomide in combination with radiation therapy in patients with malignant gliomas. J Neurooncol. 2012;110:237-43.
57. Cohen KJ, Gibbs IC, Fisher PG, Hayashi RJ, Macy ME, Gore L. A phase I trial of arsenic trioxide chemoradiotherapy for infiltrating astrocytomas of childhood. Neuro-oncol. 2013;15:783-7.
58. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells - much more complex than expected. Mol Cancer. 2011;10:128. BioMed Central Ltd.
59. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, Jones DL, et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339-44.
60. Zhang M, Song T, Yang L, Chen R, Wu L, Yang Z, et al. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res. 2008;27:85.
61. Christensen K, Schrøder HD, Kristensen BW. CD133 identifies perivascular niches in grade II-IV astrocytomas. J Neuro-Oncol. 2008;90:157-70.
62. Strojnik T, Røsland GV, Sakariassen PO, Kavalar R, Lah T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol. 2007;68:133-43. discussion143-4.
63. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.
64. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40:499-507. (Pubitemid 351601215)
65. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008;14:123-9. (Pubitemid 351377986)
66. Beier D, Wischhusen J, Dietmaier W, Hau P, Proescholdt M, Brawanski A, et al. CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors. Brain Pathol. 2008;18:370-7. (Pubitemid 351782845)
67. Melguizo C, Prados J, González B, Ortiz R, Concha A, Alvarez PJ, et al. MGMT promoter methylation status and MGMT and CD133 immunohistochemical expression as prognostic markers in glioblastoma patients treated with temozolomide plus radiotherapy. J Transl Med. 2012;10:250.
68. Sun H, Zhang S. Arsenic trioxide regulates the apoptosis of glioma cell and glioma stem cell via down-regulation of stem cell marker Sox2. Biochem Biophys Res Commun. 2011;410:692-7.
69. Chiu H-W, Ho Y-S, Wang Y-J. Arsenic trioxide induces autophagy and apoptosis in human glioma cells in vitro and in vivo through downregulation of survivin. J Mol Med. 2011;89:927-41.
70. Song X, Chen Z, Wu C, Zhao S. Abrogating HSP response augments cell death induced by As2O3 in glioma cell lines. Can J Neurol Sci. 2010;37:504-11.
71. Zhao S, Tsuchida T, Kawakami K, Shi C, Kawamoto K. Effect of As2O3 on cell cycle progression and cyclins D1 and B1 expression in two glioblastoma cell lines differing in p53 status. Int J Oncol. 2002;21:49-55.
72. Raju GP. Arsenic: a potentially useful poison for Hedgehog-driven cancers. J Clin Invest. 2011;121:14-6.
73. Beauchamp EM, Ringer L, Bulut G, Sajwan KP, Hall MD, Lee Y-C, et al. Arsenic trioxide inhibits human cancer cell growth and tumor development in mice by blocking Hedgehog/GLI pathway. J Clin Invest. 2011;121:148-60.
74. Haga N, Fujita N, Tsuruo T. Involvement of mitochondrial aggregation in arsenic trioxide (As2O3)-induced apoptosis in human glioblastoma cells. Cancer Sci. 2005;96:825-33. (Pubitemid 43019834)
75. Liu Y, Liang Y, Zheng T, Yang G, Zhang X, Sun Z, et al. Inhibition of heme oxygenase-1 enhances anti-cancer effects of arsenic trioxide on glioma cells. J Neuro-Oncol. 2011;104:449-58.
76. Cowley S, Paterson H, Kemp P, Marshall CJ. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell. 1994;77:841-52. (Pubitemid 24187682)
77. Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, Lowe SW. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 1998;12:3008-19. (Pubitemid 28469303)
78. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 1995;80:179-85.
79. Ries S, Biederer C, Woods D, Shifman O, Shirasawa S, Sasazuki T, et al. Opposing effects of Ras on p53: transcriptional activation of mdm2 and induction of p19ARF. Cell. 2000;103:321-30.
80. Zhao S, Zhang J, Zhang X, Dong X, Sun X. Arsenic trioxide induces different gene expression profiles of genes related to growth and apoptosis in glioma cells dependent on the p53 status. Mol Biol Rep. 2008;35:421-9.
81. Yu X, Robinson JF, Gribble E, Hong SW, Sidhu JS, Faustman EM. Gene expression profiling analysis reveals arsenic-induced cell cycle arrest and apoptosis in p53-proficient and p53-deficient cells through differential gene pathways. Toxicol Appl Pharmacol. 2008;233:389-403.
82. Sathornsumetee S, Rich JN. Designer therapies for glioblastoma multiforme. Ann N YAcad Sci. 2008;1142:108-32.
83. Chen R, Nishimura MC, Bumbaca SM, Kharbanda S, Forrest WF, Kasman IM, et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell. 2010;17:362-75.
84. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res. 2005;65:6207-19. (Pubitemid 40994406)
85. Laks DR, Masterman-Smith M, Visnyei K, Angenieux B, Orozco NM, Foran I, et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells. 2009;27:980-7.
86. Lathia JD, Venere M, Rao MS, Rich JN. Seeing is believing: are cancer stem cells the Loch Nessmonster of tumor biology? Stem Cell Rev. 2011;7:227-37.
87. Jhanwar-Uniyal M, Albert L, McKenna E, Karsy M, Rajdev P, Braun A, et al. Deciphering the signaling pathways of cancer stem cells of glioblastoma multiforme: role of Akt/mTOR and MAPK pathways. Adv Enzym Regul. 2011;51:164-70.
88. Cordey M, Limacher M, Kobel S, Taylor V, Lutolf MP. Enhancing the reliability and throughput of neurosphere culture on hydrogel microwell arrays. Stem Cells. 2008;26:2586-94.