Extracellular adenosine sensing-a metabolic cell death priming mechanism downstream of p53

Molecular Cell

Volumn 50, Issue 3, 2013, Pages 394-406

  Long, Jaclyn S ^a   Crighton, Diane ^a   O'Prey, James ^a   MacKay, Gillian ^a   Zheng, Liang ^a   Palmer, Timothy M ^b   Gottlieb, Eyal ^a   Ryan, Kevin M ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CASPASE 3; CASPASE 7; CASPASE 9; LIGAND; PROTEIN BCL 2; PROTEIN P53; PUMA PROTEIN; RECEPTOR PROTEIN; ADENOSINE A2B RECEPTOR; APOPTOSIS REGULATORY PROTEIN; CASPASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER THERAPY; CELL DEATH; CELL VIABILITY; CELLS; CHEMOTHERAPY; CONTROLLED STUDY; DRUG EXPOSURE; HYPOXIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SOLID TUMOR; STIMULATION; ANIMAL; ANOXIA; C57BL MOUSE; CELL STRAIN HCT116; CELL SURVIVAL; DOWN REGULATION; GENETICS; HUMAN; METABOLISM; TUMOR CELL LINE; UPREGULATION;

ADENOSINE; ANIMALS; ANOXIA; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASES; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DOWN-REGULATION; HCT116 CELLS; HUMANS; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, ADENOSINE A2B; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84887193301     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.03.016     Document Type: Article

References (50)

1. Aghaei M., Karami-Tehrani F., Panjehpour M., Salami S., Fallahian F. Adenosine induces cell-cycle arrest and apoptosis in androgen-dependent and -independent prostate cancer cell lines, LNcap-FGC-10, DU-145, and PC3. Prostate 2012, 72:361-375.
2. Bensaad K., Tsuruta A., Selak M.A., Vidal M.N., Nakano K., Bartrons R., Gottlieb E., Vousden K.H. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006, 126:107-120.
3. Béroud C., Soussi T. The UMD-p53 database: new mutations and analysis tools. Hum. Mutat. 2003, 21:176-181.
4. Blay J., White T.D., Hoskin D.W. The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res. 1997, 57:2602-2605.
5. Borrmann T., Hinz S., Bertarelli D.C., Li W., Florin N.C., Scheiff A.B., Müller C.E. 1-alkyl-8-(piperazine-1-sulfonyl)phenylxanthines: development and characterization of adenosine A2B receptor antagonists and a new radioligand with subnanomolar affinity and subtype specificity. J. Med. Chem. 2009, 52:3994-4006.
6. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J. Cell Sci. 2009, 122:437-441.
7. Crighton D., Ryan K.M. Splicing DNA-damage responses to tumour cell death. Biochim. Biophys. Acta 2004, 1705:3-15.
8. Crighton D., Wilkinson S., O'Prey J., Syed N., Smith P., Harrison P.R., Gasco M., Garrone O., Crook T., Ryan K.M. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006, 126:121-134.
9. Dawicki D.D., Chatterjee D., Wyche J., Rounds S. Extracellular ATP and adenosine cause apoptosis of pulmonary artery endothelial cells. Am. J. Physiol. 1997, 273:L485-L494.
10. Decking U.K., Schlieper G., Kroll K., Schrader J. Hypoxia-induced inhibition of adenosine kinase potentiates cardiac adenosine release. Circ. Res. 1997, 81:154-164.
11. Donehower L.A., Harvey M., Slagle B.L., McArthur M.J., Montgomery C.A., Butel J.S., Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356:215-221.
12. Doolette D.J. Mechanism of adenosine accumulation in the hippocampal slice during energy deprivation. Neurochem. Int. 1997, 30:211-223.
13. Dubey R.K., Gillespie D.G., Mi Z., Jackson E.K. Adenosine inhibits growth of human aortic smooth muscle cells via A2B receptors. Hypertension 1998, 31:516-521.
14. el-Deiry W.S., Kern S.E., Pietenpol J.A., Kinzler K.W., Vogelstein B. Definition of a consensus binding site for p53. Nat. Genet. 1992, 1:45-49.
15. Feoktistov I., Goldstein A., Sheller J.R., Schwartz L.B., Biaggioni I. Immunological characterization of A(2B) adenosine receptors in human mast cells. Drug Dev. Res. 2003, 58:461-471.
16. Fishman P., Bar-Yehuda S., Vagman L. Adenosine and other low molecular weight factors released by muscle cells inhibit tumor cell growth. Cancer Res. 1998, 58:3181-3187.
17. Fredholm B.B., IJzerman A.P., Jacobson K.A., Klotz K.N., Linden J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 2001, 53:527-552.
18. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
19. Headrick J.P., Willis R.J. 5'-Nucleotidase activity and adenosine formation in stimulated, hypoxic and underperfused rat heart. Biochem. J. 1989, 261:541-550.
20. Helgason G.V., O'Prey J., Ryan K.M. Oncogene-induced sensitization to chemotherapy-induced death requires induction as well as deregulation of E2F1. Cancer Res. 2010, 70:4074-4080.
21. Hermeking H., Eick D. Mediation of c-Myc-induced apoptosis by p53. Science 1994, 265:2091-2093.
22. Hoh J., Jin S., Parrado T., Edington J., Levine A.J., Ott J. The p53MH algorithm and its application in detecting p53-responsive genes. Proc. Natl. Acad. Sci. USA 2002, 99:8467-8472.
23. Ide T., Brown-Endres L., Chu K., Ongusaha P.P., Ohtsuka T., El-Deiry W.S., Aaronson S.A., Lee S.W. GAMT, a p53-inducible modulator of apoptosis, is critical for the adaptive response to nutrient stress. Mol. Cell 2009, 36:379-392.
24. Kitakaze M., Hori M., Takashima S., Sato H., Inoue M., Kamada T. Ischemic preconditioning increases adenosine release and 5'-nucleotidase activity during myocardial ischemia and reperfusion in dogs. Implications for myocardial salvage. Circulation 1993, 87:208-215.
25. Latini S., Bordoni F., Pedata F., Corradetti R. Extracellular adenosine concentrations during in vitro ischaemia in rat hippocampal slices. Br. J. Pharmacol. 1999, 127:729-739.
26. Lelièvre V., Muller J.M., Falcòn J. Adenosine modulates cell proliferation in human colonic carcinoma. II. Differential behavior of HT29, DLD-1, Caco-2 and SW403 cell lines. Eur. J. Pharmacol. 1998, 341:299-308.
27. Lowe S.W., Ruley H.E., Jacks T., Housman D.E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993, 74:957-967.
28. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., Hurley P.J., Bunz F., Hwang P.M. p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653.
29. McCurrach M.E., Connor T.M., Knudson C.M., Korsmeyer S.J., Lowe S.W. bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc. Natl. Acad. Sci. USA 1997, 94:2345-2349.
30. Muzio M., Salvesen G.S., Dixit V.M. FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem. 1997, 272:2952-2956.
31. Nishiyama A., Kimura S., He H., Miura K., Rahman M., Fujisawa Y., Fukui T., Abe Y. Renal interstitial adenosine metabolism during ischemia in dogs. Am. J. Physiol. Renal Physiol. 2001, 280:F231-F238.
32. Ohta A., Gorelik E., Prasad S.J., Ronchese F., Lukashev D., Wong M.K., Huang X., Caldwell S., Liu K., Smith P., et al. A2A adenosine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. USA 2006, 103:13132-13137.
33. Okumura K., Huang S., Sinicrope F.A. Induction of Noxa sensitizes human colorectal cancer cells expressing Mcl-1 to the small-molecule Bcl-2/Bcl-xL inhibitor, ABT-737. Clin. Cancer Res. 2008, 14:8132-8142.
34. Oltersdorf T., Elmore S.W., Shoemaker A.R., Armstrong R.C., Augeri D.J., Belli B.A., Bruncko M., Deckwerth T.L., Dinges J., Hajduk P.J., et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435:677-681.
35. Pellicciari C., Manfredi A.A., Bottone M.G., Schaack V., Barni S. A single-step staining procedure for the detection and sorting of unfixed apoptotic thymocytes. Eur. J. Histochem. 1993, 37:381-390.
36. Raskovalova T., Huang X., Sitkovsky M., Zacharia L.C., Jackson E.K., Gorelik E. Gs protein-coupled adenosine receptor signaling and lytic function of activated NK cells. J. Immunol. 2005, 175:4383-4391.
37. Rathbone M.P., Middlemiss P.J., Kim J.K., Gysbers J.W., DeForge S.P., Smith R.W., Hughes D.W. Adenosine and its nucleotides stimulate proliferation of chick astrocytes and human astrocytoma cells. Neurosci. Res. 1992, 13:1-17.
38. Rounds S., Yee W.L., Dawicki D.D., Harrington E., Parks N., Cutaia M.V. Mechanism of extracellular ATP- and adenosine-induced apoptosis of cultured pulmonary artery endothelial cells. Am. J. Physiol. 1998, 275:L379-L388.
39. Ryan K.M., Ernst M.K., Rice N.R., Vousden K.H. Role of NF-kappaB in p53-mediated programmed cell death. Nature 2000, 404:892-897.
40. Van Belle H., Goossens F., Wynants J. Formation and release of purine catabolites during hypoperfusion, anoxia, and ischemia. Am. J. Physiol. 1987, 252:H886-H893.
41. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., Kong N., Kammlott U., Lukacs C., Klein C., et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004, 303:844-848.
42. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
43. Vousden K.H., Prives C. Blinded by the Light: The Growing Complexity of p53. Cell 2009, 137:413-431.
44. Vousden K.H., Ryan K.M. p53 and metabolism. Nat. Rev. Cancer 2009, 9:691-700.
45. Wang L., Du F., Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008, 133:693-703.
46. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
47. Wilkinson S., O'Prey J., Fricker M., Ryan K.M. Hypoxia-selective macroautophagy and cell survival signaled by autocrine PDGFR activity. Genes Dev. 2009, 23:1283-1288.
48. Yu J., Wang Z., Kinzler K.W., Vogelstein B., Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:1931-1936.
49. Zhao Z., Kapoian T., Shepard M., Lianos E.A. Adenosine-induced apoptosis in glomerular mesangial cells. Kidney Int. 2002, 61:1276-1285.
50. Zhou Q., Snipas S., Orth K., Muzio M., Dixit V.M., Salvesen G.S. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 1997, 272:7797-7800.