Modulation of A1 and A2B adenosine receptor activity: A new strategy to sensitise glioblastoma stem cells to chemotherapy

Cell Death and Disease

Volumn 5, Issue 11, 2014, Pages

  Daniele, S ^a   Zappelli, E ^a   Natali, L ^a   Martini, C ^a   Trincavelli, M L ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR AGONIST; ADENOSINE A2 RECEPTOR AGONIST; ADENOSINE A2B RECEPTOR; ANTINEOPLASTIC AGENT; BAY 606583; CYCLOHEXYLADENOSINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; TEMOZOLOMIDE; UNCLASSIFIED DRUG; DACARBAZINE; LIGAND;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; GLIA; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANALOGS AND DERIVATIVES; BRAIN NEOPLASMS; CELL SEPARATION; CELL SHAPE; DRUG EFFECTS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ADENOSINE A1 RECEPTOR AGONISTS; ADENOSINE A2 RECEPTOR AGONISTS; APOPTOSIS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SEPARATION; CELL SHAPE; CELL SURVIVAL; DACARBAZINE; GLIOBLASTOMA; HUMANS; LIGANDS; NEOPLASTIC STEM CELLS; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2B;

EID: 84927918136     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.487     Document Type: Article

References (64)

1. Dolecek TA, Propp JM, Stroup NE, Kruchko C. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2004-2008. Neuro-Oncology 2012; 14: 1-49.
2. Legler JM, Ries LA, Smith MA, Warren JL, Heineman EF, Kaplan R et al. Cancer surveillance series (corrected): brain and other central nervous system cancers: recent trends in incidence and mortality. J Natl Cancer Inst 1999; 91: 1382-1390.
3. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359: 492-507.
4. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006; 13: 1238-1241.
5. Smalley M, Piggott L, Clarkson R. Breast cancer stem cells: obstacles to therapy. Cancer Lett 2013; 338: 57-62.
6. Van Rhenen A, Feller N, Kelder A, Westra AH, Rombouts E, Zweegman S et al. High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin Cancer Res 2005; 11: 6520-6527.
7. Aguado T, Carracedo A, Julien B, Velasco G, Milman G, Mechoulam R et al. Cannabinoids induce glioma stem-like cell differentiation and inhibit gliomagenesis. J Biol Chem 2007; 282: 6854-6862.
8. Ahmed N, Salsman VS, Kew Y, Shaffer D, Powell S, Zhang YJ et al. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res 2010; 16: 474-485.
9. Aloy MT, Hadchity E, Bionda C, Diaz-Latoud C, Claude L, Rousson R et al. Protective role of Hsp27 protein against gamma radiation-induced apoptosis and radiosensitization effects of Hsp27 gene silencing in different human tumor cells. Int J Radiat Oncol Biol Phys 2008; 70: 543-553.
10. Altaner C. Glioblastoma and stem cells. Neoplasma 2008; 55: 369-374.
11. Balyasnikova IV, Franco-Gou R, Mathis JM, Lesniak MS. Genetic modification of mesenchymal stem cells to express a single-chain antibody against EGFRvIII on the cell surface. J Tissue Eng Regen Med 2010; 4: 247-258.
12. Bar EE, Chaudhry A, Lin A, Fan X, Schreck K, Matsui W et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007; 25: 2524-2533.
13. Chalmers AJ. Radioresistant glioma stem cells-therapeutic obstacle or promising target? DNA Repair 2007; 6: 1391-1394.
14. Cho DY, Lin SZ, Yang WK, Hsu DM, Lin HL, Lee HC et al. The role of cancer stem cells (CD133(+)) in malignant gliomas. Cell Transplant 2011; 20: 121-125.
15. Fan X, Salford LG, Widegren B. Glioma stem cell: evidence and limitation. Semin Cancer Biol 2007; 17: 214-218.
16. Gadji M, Crous AM, Fortin D, Krcek J, Torchia M, Mai S et al. EGF receptor inhibitors in the treatment of glioblastoma multiform: old clinical allies and newly emerging therapeutic concepts. Eur J Pharmacol 2009; 625: 23-30.
17. Hughes SA, Achanta P, Ho AL, Duenas VJ, Quiñones-Hinojosa A. Biological horizons for targeting brain malignancy. Adv Exp Med Biol 2010; 671: 93-104.
18. Rappa G, Mercapide J, Anzanello F, Prasmickaite L, Xi Y, Ju J et al. Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets. Exp Cell Res 2008; 314: 2110-2122.
19. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458: 780-783.
20. 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: 756-760.
21. Yu SC, Ping YF, Yi L, Zhou ZH, Chen JH, Yao XH et al. Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer Lett 2008; 265: 124-134.
22. Qiang L, Yang Y, Ma YJ, Chen FH, Zhang LB, Liu W et al. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett 2009; 279: 13-21.
23. Beier D, Röhrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 2008; 68: 5706-5715.
24. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol Cancer 2011; 10: 128-138.
25. Happold C, Roth P, Wick W, Schmidt N, Florea AM, Silginer M et al. Distinct molecular mechanisms of acquired resistance to temozolomide in glioblastoma cells. J Neurochem 2012; 122: 444-455.
26. Morrone FB, Jacques-Silva MC, Horn AP, Bernardi A, Schwartsmann G, Rodnight R et al. Extracellular nucleotides and nucleosides induce proliferation and increase nucleoside transport in human glioma cell lines. J Neurooncol 2003; 64: 211-218.
27. Wei W, Ryu JK, Choi HB, McLarnon JG. Expression and function of the p2x(7) receptor in rat c6 glioma cells. Cancer Lett 2008; 260: 79-87.
28. Gessi S, Sacchetto V, Fogli E, Merighi S, Varani K, Baraldi PG et al. Modulation of metalloproteinase-9 in U87MG glioblastoma cells by A3 adenosine receptors. Biochem Pharmacol 2010; 79: 1483-1495.
29. Morrone FB, Horn AP, Stella J, Spiller F, Sarkis JJ, Salbego CG et al. Increased resistance of glioma cell lines to extracellular ATP cytotoxicity. J Neurooncol 2005; 71: 135-140.
30. Fredholm BB, Ijzerman AP, Jacobson KA, Linden J, Müller CE. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol Rev 2011; 63: 1-34.
31. Merighi S, Mirandola P, Varani K, Gessi S, Leung E, Baraldi PG et al. A glance at adenosine receptors: novel target for antitumor therapy. Pharmacol Ther 2003; 100: 31-48.
32. Gessi S, Merighi S, Varani K, Leung E, Mac Lennan S, Borea PA. The A3 adenosine receptor: an enigmatic player in cell biology. Pharmacol Ther 2008; 117: 123-140.
33. Ledur PF, Villodre ES, Paulus R, Cruz LA, Flores DG, Lenz G. Extracellular ATP reduces tumor sphere growth and cancer stem cell population in glioblastoma cells. Purinergic Signal 2012; 8: 39-48.
34. Gessi S, Merighi S, Sacchetto V, Simioni C, Borea PA. Adenosine receptors and cancer. Biochim Biophys Acta 2011; 1: 1400-1412.
35. Piccirillo SG, 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: 761-765.
36. Castillo CA, León D, Ruiz MA, Albasanz JL, Martín M. Modulation of adenosine A1 and A2A receptors in C6 glioma cells during hypoxia: involvement of endogenous adenosine. J Neurochem 2008; 105: 2315-2329.
37. Castillo CA, Albasanz JL, Fernández M, Martín M. Endogenous expression of adenosine A1, A2 and A3 receptors in rat C6 glioma cells. Neurochem Res 2007; 32: 1056-1070.
38. Marteau F, Le Poul E, Communi D, Communi D, Labouret C, Savi P et al. Pharmacological characterization of the human P2Y13 receptor. Mol Pharmacol 2003; 64: 104-112.
39. Dhalla AK, Shryock JC, Shreeniwas R, Belardinelli L. Pharmacology and therapeutic applications of A1 adenosine receptor ligands. Curr Top Med Chem 2003; 3: 369-385.
40. 2B receptor ligands: past, present and future trends. Curr Top Med Chem 2010; 10: 923-940.
41. Luthin DR, Olsson RA, Thompson RD, Sawmiller DR, Linden J. Characterization of two affinity states of adenosine A2a receptors with a new radioligand, 2-[2-(4-amino-3-[125I] iodophenyl) ethylamino]adenosine. Mol Pharmacol 1995; 47: 307-313.
42. Lim MH, Kim HO, Moon HR, Lee SJ, Chun MW, Gao ZG et al. Design, synthesis and binding affinity of 3'-fluoro analogues of Cl-IB-MECA as adenosine A3 receptor ligands. Bioorg Med Chem Lett 2003; 13: 817-820.
43. Cho DY, Lin SZ, Yang WK, Lee HC, Hsu DM, Lin HL et al. Targeting cancer stem cells for treatment of glioblastoma multiforme. Cell Transplant 2013; 22: 731-739.
44. Sunayama J, Matsuda K, Sato A, Tachibana K, Suzuki K, Narita Y et al. Crosstalk between the PI3K/mTOR and MEK/ERK pathways involved in the maintenance of self-renewal and tumorigenicity of glioblastoma stem-like cells. Stem Cells 2010; 28: 1930-1939.
45. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15: 501-513.
46. Platet N, Liu SY, Atifi ME, Oliver L, Vallette FM, Berger F et al. Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 2007; 258: 286-290.
47. Gilbertson RJ, Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007; 7: 733-736.
48. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K, Tofilon PJ. Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol Cancer Res 2009; 7: 489-497.
49. Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD et al. Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009; 28: 3949-3959.
50. Bar EE, Lin A, Mahairaki V, Matsui W, Eberhart CG. Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 2010; 177: 1491-1502.
51. Méndez O, Zavadil J, Esencay M, Lukyanov Y, Santovasi D, Wang SC et al. Knock down of HIF-1alpha in glioma cells reduces migration in vitro and invasion in vivo and impairs their ability to form tumor spheres. Mol Cancer 2010; 9: 133.
52. Blum R, Jacob-Hirsch J, Amariglio N, Rechavi G, Kloog Y. Ras inhibition in glioblastoma down-regulates hypoxia-inducible factor-1alpha, causing glycolysis shutdown and cell death. Cancer Res 2005; 65: 999-1006.
53. Tait SW, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11: 621-632.
54. Timmer JC, Salvesen GS. Caspase substrates. Cell Death Differ 2007; 14: 66-72.
55. Johannessen TC, Prestegarden L, Grudic A, Hegi ME, Tysnes BB, Bjerkvig R. The DNA repair protein ALKBH2 mediates temozolomide resistance in human glioblastoma cells. Neuro-Oncology 2013; 15: 269-278.
56. Zhuang W, Long L, Zheng B, Ji W, Yang N, Zhang Q et al. Curcumin promotes differentiation of glioma-initiating cells by inducing autophagy. Cancer Sci 2012; 103: 684-690.
57. Zhuang W, Li B, Long L, Chen L, Huang Q, Liang Z. Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity. Int J Cancer 2011; 129: 2720-2731.
58. Diamandis P, Wildenhain J, Clarke ID, Sacher AG, Graham J, Bellows DS et al. Chemical genetics reveals a complex functional ground state of neural stem cells. Nat Chem Biol 2007; 3: 268-273.
59. Sunayama J, Sato A, Matsuda K, Tachibana K, Suzuki K, Narita Y et al. Dual blocking of mTor and PI3K elicits a prodifferentiation effect on glioblastoma stem-like cells. Neuro Oncol 2010; 12: 1205-1219.
60. Pietras A, Hansford LM, Johnsson AS, Bridges E, Sjölund J, Gisselsson D et al. HIF-2alpha maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells. Proc Natl Acad Sci USA 2009; 106: 16805-16810.
61. Hu YY, Fu LA, Li SZ, Chen Y, Li JC, Han J et al. Hif-1α and Hif-2α differentially regulate Notch signaling through competitive interaction with the intracellular domain of Notch receptors in glioma stem cells. Cancer Lett 2014; 349: 67-76.
62. Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002; 25: 471-490.
63. Gao ZG, Ye K, Göblyös A, Ijzerman AP, Jacobson KA. Flexible modulation of agonist efficacy at the human A3 adenosine receptor by the imidazoquinoline allosteric enhancer LUF6000. BMC Pharmacol 2008; 8: 20-30.
64. Fernando P, Brunette S, Megeney LA. Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. FASEB J 2005; 19: 671-673.