P2X7-mediated chemoprevention of epithelial cancers

Expert Opinion on Therapeutic Targets

Volumn 13, Issue 11, 2009, Pages 1313-1332

  Gorodeski, George I ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

apoptosis; cancer; chemoprevention; epithelial; P2X 7; skin

Indexed keywords

2' (3') O (4 BENZOYLBENZOYL)ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; BETA ARRESTIN 2; CASPASE 3; CASPASE 7; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2 INHIBITOR; CYTOCHROME C; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; INHIBITOR OF APOPTOSIS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BID; PROTEIN BNIP3; PROTEIN NOXA; PROTEIN P53; PURINERGIC P2X7 RECEPTOR; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; PURINERGIC P2 RECEPTOR;

3' UNTRANSLATED REGION; APOPTOSIS; APPETITE; BIOCHEMISTRY; BODY WEIGHT; CANCER CELL; CANCER RISK; CANCER SURVIVAL; CARCINOGENESIS; CELL GROWTH; CELL KILLING; CELL MEMBRANE; CELL MIGRATION; CELL PERMEABILIZATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CHANNEL GATING; CHEMOPROPHYLAXIS; CHEMOTHERAPY; CHROMATIN CONDENSATION; CHROMOSOME 12Q; CPG ISLAND; CYTOKINE PRODUCTION; CYTOPLASM; DNA DAMAGE; DNA FRAGMENTATION; DNA SYNTHESIS; DOWN REGULATION; ENDOMETRIUM; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FATIGUE; FUNCTIONAL STATUS; GENE EXPRESSION; GLYCOSYLATION; HAIR; HUMAN; HYPOXIA; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOREACTIVITY; IN VIVO STUDY; INFLAMMATION; KERATINOCYTE; LUNG NON SMALL CELL CANCER; MACROPHAGE; MENSTRUAL CYCLE; MUELLERIAN DUCT; MUSCLE STRENGTH; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; OXIDATIVE STRESS; PHAGOCYTOSIS; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMORPHISM; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TARGETING; QUALITY OF LIFE; RECEPTOR AFFINITY; REVIEW; SKIN; SKIN CANCER; SKIN PAPILLOMA; STIMULUS; THYMOCYTE; TISSUE DIFFERENTIATION; TISSUE INJURY; TRANSCRIPTION REGULATION; UPREGULATION; UTERINE CERVIX; ANIMAL; DISEASE MODEL; DRUG DELIVERY SYSTEM; DRUG EFFECT; METABOLISM; MOUSE; NEOPLASM; PATHOPHYSIOLOGY; SKIN TUMOR;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; HUMANS; MICE; NEOPLASMS, GLANDULAR AND EPITHELIAL; RECEPTORS, PURINERGIC P2; SKIN NEOPLASMS; UP-REGULATION;

EID: 73449108482     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728220903277249     Document Type: Review

References (136)

1. Croker AK, Allan AL. Cancer stem cells: implications for the progression and treatment of metastatic disease. J Cell Mol Med 2008;12:374-90 (Pubitemid 351555122)
2. Rodriguez-Nieto S, Zhivotovsky B. Role of alterations in the apoptotic machinery in sensitivity of cancer cells to treatment. Curr Pharm Des 2006;12:4411-25 (Pubitemid 44835154)
3. Wyllie AH, Kerr JFR, Currie AR. Cell death: the signifcance of apoptosis. Int Rev Cytol 1980;68:251-306
4. Ellis HM, Yuan J, Horvitz HR. Mechanisms and functions of cell death. Annul Rev Cell Biol 1991;7:663-98
5. Fawthrop DJ, Boobis AR, Davies DS. Mechanisms of cell death. Arch Toxicol 1991;65:437-44
6. Soti C, Sreedhar AS, Csermely P. Apoptosis, necrosis and cellular senescence: chaperone occupancy as a potential switch. Aging Cell 2003;2:39-45
7. Gasser S, Raulet D. The DNA damage response, immunity and cancer. Semin Cancer Biol 2006;16:344-7 (Pubitemid 44311502)
8. Kujoth GC, Leeuwenburgh C, Prolla TA. Mitochondrial DNA mutations and apoptosis in mammalian aging. Cancer Res 2006;66:7386-9 (Pubitemid 44289188)
9. Rodriguez-Nieto S, Zhivotovsky B. Role of alterations in the apoptotic machinery in sensitivity of cancer cells to treatment. Curr Pharm Des 2006;12:4411-25 (Pubitemid 44835154)
10. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70 (Pubitemid 30046295)
11. Cummings J, Ward TH, Ranson M, et al. Apoptosis pathway-targeted drugs: from the bench to the clinic. Biochim Biophys Acta 2004;1705:53-66 (Pubitemid 39610420)
12. Schmitt CA. Senescence, apoptosis and therapy: cutting the lifelines of cancer. Nat Rev Cancer 2003;3:286-95 (Pubitemid 37328864)
13. Ziegler DS, Kung AL. Therapeutic targeting of apoptosis pathways in cancer. Curr Opin Oncol 2008;20:97-103 (Pubitemid 350190988)
14. Boatright KM, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol 2003;15:725-31 (Pubitemid 37492933)
15. Klein S, McCormick F, Levitzki A. Killing time for cancer cells. Nat Rev Cancer 2005;5:573-80 (Pubitemid 40942833)
16. Lorenzo HK, Susin SA. Therapeutic potential of AIF-mediated caspase independent programmed cell death. Drug Resist Updates 2007;10:235-55
17. Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene 2003;22:8543-67 (Pubitemid 38028527)
18. Guo B, Godzik A, Reed JC. Bcl-G, a novel pro-apoptotic member of the Bcl-2 family. J Biol Chem 2001;276:2780-5
19. Antonsson B, Martinou JC. The Bcl-2 protein family. Exp Cell Res 2000;256:50-7 (Pubitemid 30211166)
20. Green DR. Apoptotic pathways: ten minutes to dead. Cell 2005;121:671-4 (Pubitemid 40797590)
21. Oliver L, Vallette FM. The role of caspases in cell death and differentiation. Drug Resist Updates 2005;8:163-70 (Pubitemid 41267066)
22. Iannolo G, Conticello C, Memeo L, De Maria R. Apoptosis in normal and cancer stem cells. Crit Rev Oncol Hematol 2008;66:42-51 (Pubitemid 351330196)
23. Nachmias B, Ashhab Y, Ben-Yehuda D. The inhibitor of apoptosis protein family (IAPs): an emerging therapeutic target in cancer. Semin Cancer Biol 2004;14:231-43 (Pubitemid 38824584)
24. Reed JC. Drug Insight: cancer therapy strategies based on restoration of endogenous cell death mechanisms. Nat Clin Pract Oncol 2006;3:388-98 (Pubitemid 44027293)
25. Qiao L, Wong BCY. Targeting apoptosis as an approach for gastrointestinal cancer therapy. Drug Resist Updates 2009;12:55-64
26. Thorburn A, Behbakht K, Ford H. TRAIL receptor-targeted therapeutics: resistance mechanisms and strategies to avoid them. Drug Resist Updates 2008;11:17-24
27. Kucharczak J, Simmons MJ, Fan Y, Gelinas C. To be, or not to be: NF-κB is the answer-role of Rel/NF-κB in the regulation of apoptosis. Oncogene 2003;22:8961-82 (Pubitemid 38121698)
28. Ghobrial IM, Witzig TE, Adjei AA. Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin 2005;55:178-94 (Pubitemid 40826487)
29. Li QX, Yu DH, Liu G, et al. Selective anticancer strategies via intervention of the death pathways relevant to cell transformation. Cell Death Differ 2008;15:1197-210 (Pubitemid 351984750)
30. Gore SD, Jones C, Kirkpatrick P. Decitabine. Nat Rev Drug Discov 2006;5:891-2 (Pubitemid 44660602)
31. Reu FJ, Bae SI, Cherkassky L, et al. Overcoming resistance to interferon-induced apoptosis of renal carcinoma and melanoma cells by DNA demethylation. J Clin Oncol 2006;24:3771-9 (Pubitemid 46622316)
32. Gartel AL. Transcriptional inhibitors, p53 and apoptosis. Biochim Biophys Acta 2008;1786:83-6
33. Cornett WR, McCall LM, Petersen R P, et al. Randomized multicenter trial of hyperthermic isolated limb perfusion with melphalan alone compared with melphalan plus tumor necrosis factor: American College of Surgeons Oncology Group Trial Z0020. J Clin Oncol 2006;24:4196-201 (Pubitemid 46622299)
34. Jo M, Kim TH, Seol DW, et al. Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat Med 2000;6:564-7 (Pubitemid 30305907)
35. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003;22:8628-33 (Pubitemid 38019198)
36. Rigaud S, Fondaneche MC, Lambert N, et al. XIAP defciency in humans causes an X-linked lymphoproliferative syndrome. Nature 2006;444:110-4 (Pubitemid 44684766)
37. Renvoize C, Biola A, Pallardy M, Breard J. Apoptosis: identifcation of dying cells. Cell Biol Toxicol 1998;14:111-20
38. Wang Q, Wang L, Feng YH, et al. P2X7-receptor mediated apoptosis of human cervical epithelial cells. Am J Physiol 2004;287:C1349-58 (Pubitemid 39382894)
39. Li X, Zhou L, Feng YH, et al. The P2X7 receptor: A novel biomarker of uterine epithelial cancers. Cancer Epidemiol Biomarkers Prev 2006;15:1-8
40. Wang Q, Li X, Wang L, et al. Anti-apoptotic effects of estrogen in normal and in cancer human cervical epithelial cells. Endocrinology 2004;145:5568-79 (Pubitemid 39564597)
41. Wang L, Feng YH, Gorodeski GI. Epidermal growth factor facilitates epinephrine inhibition of P2X7-receptor mediated pore formation and apoptosis: a novel signaling network. Endocrinology 2005;146:164-74 (Pubitemid 40051736)
42. Feng YH, Wang L, Wang Q, et al. ATP stimulates GRK-3-phosphorylation and beta-arrestin-2-dependent internalization of P2X7-receptor. Am J Physiol 2005;288:C1342-56 (Pubitemid 40991071)
43. Buell GN, Talabot F, Gos A, et al. Gene structure and chromosomal localization of the human P2X7 receptor. Receptors Channels 1998;5:347-54 (Pubitemid 28499715)
44. Zhou L, Luo L, Qi X, et al. Regulation of P2X7 gene transcription. Purinergic Signal 2009;5:409-26
45. Kim M, Jiang LH, Wilson HL, et al. Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J 2001;20:6347-58 (Pubitemid 33078708)
46. Dubyak GR, el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 1993;265:C577-606
47. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998;50:413-92 (Pubitemid 28477681)
48. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002;82:1013-67
49. Surprenant A, North RA. Signaling at purinergic P2X receptors. Annu Rev Physiol 2009;71:333-59
50. Feng YH, Li X, Wang L, et al. A truncated P2X7 receptor variant (P2X7-j) endogenously expressed in cervical cancer cells antagonizes the full-length P2X7 receptor through hetero-oligomerization. J Biol Chem 2006;281:17228-37
51. Boldt W, Klapperstuck M, Buttner C, et al. Glu496Ala polymorphism of human P2X7 receptor does not affect its electrophysiological phenotype. Am J Physiol 2003;284:C749-56 (Pubitemid 36237527)
52. Surprenant A, Rassendren F, Kawashima E, et al. The cytolytic P2Z receptor for extracellular ATP identifed as a P2X receptor (P2X7). Science 1996;272:735-8
53. Denlinger LC, Sommer JA, Parker K, et al. Mutation of a dibasic amino acid motif within the C-terminus of the P2X7 nucleotide receptor results in traffcking defects and impaired function. J Immunol 2003;171:1304-11 (Pubitemid 36900061)
54. Cheewatrakoolpong B, Gilchrest H, Anthes JC, Greenfeder S. Identifcation and characterization of splice variants of the human P2X7 ATP channel. Biochem Biophys Res Commun 2005;332:17-27 (Pubitemid 40719451)
55. Fu W, McCormick T, Qi X, et al. Activation of P2X7-mediated apoptosis Inhibits DMBA/TPA-induced formation of skin papillomas and cancer in mice. BMC Cancer 2009;9:114. Published online 20 April 2009 doi:10.1186/1471-2407-9-114
56. Sperlágh B, Haskó G, Németh Z, Vizi ES. ATP released by LPS increases nitric oxide production in raw 264.7 macrophage cell line via P2Z/P2X7 receptors. Neurochem Int 1998;33:209-15 (Pubitemid 28418291)
57. Grahames CBA, Michel AD, Chessell I P, Humphrey DPA. Pharmacological characterization of ATP-and LPS-induced IL-1b release in human monocytes. Br J Pharmacol 1999;127:1915-21 (Pubitemid 29392888)
58. Henriksen KL, Novak I. Effect of ATP on intracellular pH in pancreatic ducts involves P2X7 receptors. Cell Physiol Biochem 2003;13:93-102 (Pubitemid 36359438)
59. Loomis WH, Namiki S, Ostrom RS, et al. Hypertonic stress increases T-cell interleukin-2 expression through a mechanism that involves ATP release, P2 receptor, and p38 MAPK activation. J Biol Chem 2003;278:4590-6 (Pubitemid 36800956)
60. Mitchell CH, Lu W, Hu H, et al. The P2X7 receptor in retinal ganglion cells: a neuronal model of pressure-induced damage and protection by a shifting purinergic balance. Purinergic Signal 2009;5:241-9
61. Yegutkin GG. Nucleotide-and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 2008;1783:673-94
62. Hübschmann MV, Skladchikova G. The role of ATP in the regulation of NCAM function. Neurochem Res 2008. DOI 10.1007/s11064-008-9769-7
63. Ferrari D, Chiozzi P, Falzoni S, et al. Extracellular ATP triggers IL-1beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 1997;159:1451-8 (Pubitemid 127484125)
64. Aggarwal BB, Rath PC. TNF-induced signaling in apoptosis. J Clin Immunol 1999;19:350-64 (Pubitemid 30039103)
65. Humphreys BJ, Rice J, Kertesy SB, Dubyak GR. Stress-activated protein kinase/JNK activation and apoptotic induction by the macrophage P2X7 nucleotide receptor. J Biol Chem 2000;275:26792-8
66. Ferrari D, Wesselborg S, Bauer MK, Schulze-Osthoff K. Extracellular ATP activates transcription factor NF-κB through the P2Z purinoreceptor by selectively targeting NF-κB p65. J Cell Biol 1997;139:1635-43 (Pubitemid 28079229)
67. Petrou S, Ugur M, Drummond RM, et al. P2X7 purinoceptor expression in Xenopus oocytes is not suffcient to produce a pore-forming P2Z-like receptor. FEBS Lett 1997;411:339-45 (Pubitemid 27301481)
68. Schilling W P, Wasylyna T, Dubyak GR, et al. Maitotoxin and P2Z/P2X7 purinergic receptors stimulation activate a common cytolytic pore. Am J Physiol 1999;277:C766-76 (Pubitemid 29525916)
69. Klapperstuck M, Buttner C, Bohm T, et al. Characteristics of P2X7 receptors from human B lymphocytes expressed in Xenopus oocytes. Biochim Biophys Acta 2000;1467:444-56 (Pubitemid 30665596)
70. Locovei S, Scemes E, Qiu F, et al. Pannexin1 is part of the pore forming unit of the P2X7R death complex. FEBS Lett 2007;581:483-8 (Pubitemid 46149626)
71. Iglesias R, Locovei S, Roque A, et al. P2X7 receptor-Pannexin1 complex: Pharmacology and signaling. Am J Physiol 2008;295:C752-60
72. Pelegrin P, Surprenant A. The P2X7 receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal 2009;5:129-37
73. Ma W, Korngreen A, Weil S, et al. Pore properties and pharmacological features of the P2X receptor channel in airway ciliated cells. J Physiol 2006;571:503-17 (Pubitemid 43329544)
74. Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol Pharmacol 2007;72:1447-56 (Pubitemid 350146082)
75. Boumechache M, Masin M, Edwardson JM, et al. Analysis of assembly and traffcking of native P2X4 and P2X7 receptor complexes in rodent immune cells. J Biol Chem 2009;284:13446-54
76. Greig AV, Linge C, Healy V, et al. Expression of purinergic receptors in non-melanoma skin cancers and their functional roles in A431 cells. J Invest Dermatol 2003;121:315-27 (Pubitemid 36969906)
77. Lee HY, Bardini M, Burnstock G. Distribution of P2X receptors in the urinary bladder and the ureter of the rat. J Urol 2000;163:2002-7 (Pubitemid 30366802)
78. Menzies J, Paul A, Kennedy C. P2X7 subunit-like immunoreactivity in the nucleus of visceral smooth muscle cells of the guinea pig. Auton Neurosci 2003;106:103-9 (Pubitemid 36870913)
79. Franke H, Gunther A, Grosche J, et al. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 2004;636:86-99
80. Jiang LH, Kim M, Spelta V, et al. Subunit arrangement in P2X receptors. J Neurosci 2003;23:8903-10 (Pubitemid 37210903)
81. Li X, Gorodeski GI. Apically sorted P2X7 receptors mediate purinergic-induced pore formation preferentially in apical domains of the plasma membrane. Nucleosides Nucleotides Nucleic Acids 2006;25:1045-9 (Pubitemid 44651845)
82. Li X, Qi X, Zhou L, et al. P2X7 receptor expression is decreased in epithelial cancer cells of ectodermal, uro-genital sinus, and distal paramesonephric-duct origin. Purinergic Signal 2009;5:351-68
83. Li M, Luo J, Brooks CL, Gu W. Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 2002;277:50607-11 (Pubitemid 36042220)
84. Yang SH, Sharrocks AD. Convergence of the SUMO and MAPK pathways on the ETS-domain transcription factor Elk-1. Biochem Soc Symp 2006;73:121-9 (Pubitemid 44884519)
85. Yang Q, Kardava L, St Leger A, et al. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J Immunol 2008;181:5885-94
86. Mathis DJ, Elkaim R, Kédinger C, et al. Specifc in vitro initiation of transcription on the adenovirus type 2 early and late EII transcription units. Proc Natl Acad Sci USA 1981;78:7383-7 (Pubitemid 12186145)
87. Hamel PA, Gill RM, Phillips RA, Gallie BL. Transcriptional repression of the E2-containing promoters EIIaE, c-myc, and RB1 by the product of the RB1 gene. Mol Cell Biol 1992;12:3431-8
88. Zheng N, Fraenkel E, Pabo CO, Pavletich N P. Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP. Genes Dev 1999;13:666-74 (Pubitemid 29155973)
89. Pardee AB, Li CJ, Reddy G P. Regulation in S phase by E2F. Cell Cycle 2004;3:1091-4 (Pubitemid 40268618)
90. Laptenko O, Prives C. Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 2006;13:951-61
91. Turner CM, Tam FWK, Lai PC, et al. Increased expression of the pro-apoptotic ATP-sensitive P2X7 receptor in experimental and human glomerulonephritis. Nephrol Dial Transplant 2007;22:386-95 (Pubitemid 46189881)
92. Schulze-Lohoff E, Hugo C, Rost S, et al. Extracellular ATP causes apoptosis and necrosis of cultured mesangial cells via P2Z/P2X7 receptors. Am J Physiol 1998;275:F962-71
93. Zhou L, Qi X, Luo L, et al. Poly(ADP-ribose) polymerase (PARP) decreases apoptosis and stimulates growth of HeLa cells by decreasing stability of P2X7 mRNA. The 99th AACR Annual Meeting, Apr 12-16, 2008; San Diego, CA (Experimental Therapy 2: Abstract #2692). Available from: http://www.aacrmeetingabstracts. org/cgi/content/meeting-abstract/2008/1-Annual-Meeting/2692?maxtoshow=&HITS= 10&h its=10&RESULTFORMAT=&author1=go rodeski&andorexactfulltext= and&searchid=1&FIRSTINDEX=0&sortspec=r elevance&resourcetype= HWCIT [Last accessed 28 August 2009]
94. Zhou L, Qi X, Potashkin JA, et al. Micro-RNAs miR-186 and miR-150 downregulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3′-untranslated region of the gene that decrease steady-state levels of the transcript. J Biol Chem 2008;283:28274-86
95. Lu J, Getz G, Miska EA, et al. MicroRNA expression profles classify human cancers. Nature 2005;435:834-8 (Pubitemid 40839735)
96. Cheng AM, Byrom MW, Shelton J, Ford L P. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005;33:1290-7 (Pubitemid 41439922)
97. Georgiou JG, Skarratt KK, Fuller SJ, et al. Human epidermal and monocyte-derived Langerhans cells express functional P2X7 receptors. J Invest Dermatol 2005;125:482-90
98. Chen L, Brosnan CF. Regulation of immune response by P2X7 receptor. Crit Rev Immunol 2006;26:499-513
99. Lenertz LY, Gavala ML, Hill LM, Bertics PJ. Cell signaling via the P2X7 nucleotide receptor: linkage to ROS production, gene transcription, and receptor traffcking. Purinergic Signal 2009;5:175-87
100. Sperlágh B, Vizi ES, Wirkner K, Illes P. P2X7 receptors in the nervous system. Prog Neurobiol 2006;78:327-46
101. Li J, Meyer R, Duncan RL, Turner CH. P2X7 nucleotide receptor plays an important role in callus remodeling during fracture repair. Calcif Tissue Int 2009;84:405-12
102. Nakamoto T, Brown DA, Catalán MA, et al. Purinergic P2X7 receptors mediate ATP-induced saliva secretion by the mouse submandibular gland. J Biol Chem 2009;284:4815-22
103. Qu Y, Dubyak GR. P2X7 receptors regulate multiple types of membrane traffcking responses and non-classical secretion pathways. Purinergic Signal 2009;5:163-7
104. Li X, Qi X, Zhou L, et al. Decreased expression of P2X7 in endometrial epithelial pre-cancerous and cancer cells. Gynecol Oncol 2007;106:233-43 (Pubitemid 46898600)
105. Eckert RL, Crish J F, Robinson NA. The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation. Physiol Rev 1997;77:397-424 (Pubitemid 27184344)
106. Solini A, Cuccato S, Ferrari D, et al. Increased P2X7 receptor expression and function in thyroid papillary cancer: A new potential marker of the disease? Endocrinology 2008;149:389-96
107. Tryndyak V, Kovalchuk O, Pogribny I P. Identifcation of differentially methylated sites within unmethylated DNA domains in normal and cancer cells. Anal Biochem 2006;356:202-7 (Pubitemid 44291651)
108. Sibilia M, Kroismayr R, Lichtenberger BM, et al. The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 2007;75:770-87 (Pubitemid 350086174)
109. Song SH, Lee JK, Oh MJ, et al. Risk factors for the progression or persistence of untreated mild dysplasia of the uterine cervix. Int J Gynecol Cancer 2006;16:1608-13
110. Romagnoli R, Baraldi PG, Cruz-Lopez O, et al. The P2X7 receptor as a therapeutic target. Expert Opin Ther Targets 2008;12:647-61
111. Rapaport E. Treatment of human tumor cells with ADP or ATP yields arrest of growth in the S phase of the cell cycle. J Cell Physiol 1983;114:279-83 (Pubitemid 13161547)
112. Agteresch HJ, Dagnelie PC, van der Gaast A, et al. Randomized clinical trial of adenosine 5′-triphosphate in patients with advanced non-small-cell lung cancer. J Natl Cancer Inst 2000;92:321-8 (Pubitemid 30117735)
113. Agteresch HJ, Burgers SA, van der Gaast A, et al. Randomized clinical trial of adenosine 5′-triphosphate on tumor growth and survival in advanced lung cancer patients. Anticancer Drugs 2003;14:639-44 (Pubitemid 37297264)
114. Agteresch HJ, Rietveld T, Kerkhofs LG, et al. Benefcial effects of adenosine triphosphate on nutritional status in advanced lung cancer patients: a randomized clinical trial. J Clin Oncol 2002;20:371-8 (Pubitemid 34072518)
115. Leij-Halfwerk S, Agteresch HJ, Sijens PE, Dagnelie PC. Adenosine triphosphate infusion increases liver energy status in advanced lung cancer patients: an in vivo 31P magnetic resonance spectroscopy. Hepatology 2002;35:421-4 (Pubitemid 34106384)
116. White N, Burnstock G. P2 receptors and cancer. Trends Pharmacol Sci 2006;27:211-7
117. Di Virgilio F, Ferrari D, Adinolf E. P2X7: a growth-promoting receptor-implications for cancer. Purinergic Signal 2009;5:251-6
118. Matsuoka I, Ohkubo S. ATP-and adenosine-mediated signaling in the central nervous system: adenosine receptor activation by ATP through rapid and localized generation of adenosine by ecto-nucleotidases. J Pharmacol Sci 2004;94:95-9 (Pubitemid 38405119)
119. Shabbir M, Burnstock G. Purinergic receptor-mediated effects of adenosine 5′-triphosphate in urological malignant diseases. Int J Urol 2009;16:143-50
120. Shabbir M, Thompson C, Jarmulowiczc M, et al. Effect of extracellular ATP on the growth of hormone-refractory prostate cancer in vivo. BJU Int 2008;102:108-12 (Pubitemid 351799448)
121. Shabbir M, Ryten M, Thompson C, et al. Purinergic receptor-mediated effects of ATP in high-grade bladder cancer. BJU Int 2008;101:106-12 (Pubitemid 350233572)
122. Williams N, Coleman PS. Exploring the adenine nucleotide binding sites on mitochondrial F1-ATPase with a new photoaffnity probe, 3′-O-(4-benzoyl) benzoyl adenosine 5′-triphosphate. J Biol Chem 1982;257:2834-41
123. Michel AD, Xing M, Humphrey PPA. Serum constituents can affect 2′-& 3′-O-(4-benzoylbenzoyl)-ATP potency at P2X7 receptors. Br J Pharmacol 2001;132:1501-8 (Pubitemid 32281039)
124. Armstrong JN, Brust TB, Lewis RG, MacVicar BA. Activation of presynaptic P2X7-like receptors depresses mossy fber CA3 synaptic transmission through p38 mitogen-activated protein kinase. J Neuroscience 2002;22:5938-45 (Pubitemid 35387638)
125. Boyer JL, Romero-Avila T, Schachter JB, Harden TK. Identifcation of competitive antagonists of the P2Y1 receptor. Mol Pharmacol 1996;50:1323-9 (Pubitemid 26384871)
126. Boyer JL, Harden TK. Irreversible activation of phospholipase C-coupled P2Y-purinergic receptors by 3′-O-(4-benzoyl)benzoyl adenosine 5′-triphosphate. Mol Pharmacol 1989;39:831-5 (Pubitemid 20019553)
127. Vigne P, Hechler B, Gachet C, et al. Benzoyl ATP is an antagonist of rat and human P2Y1 receptors and of platelet aggregation. Biochem Biophys Res Commun 1999;256:94-7 (Pubitemid 29298923)
128. Blanchard DK, Hoffmann SL, Djeu JY. Inhibition of extracellular ATP-mediated lysis of human macrophages by calmodulin antagonists. J Cell Biochem 1995;57:452-64
129. Bianchi BR, Lynch KJ, Touma E, et al. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 1999;376:127-38 (Pubitemid 29320178)
130. Kukley M, Stausberg P, Adelmann G, et al. Ecto-nucleotidases and nucleoside transporters mediate activation of adenosine receptors on hippocampal mossy fbers by P2X7 receptor agonist 2′-3′-O-(4-benzoylbenzoyl)- ATP. J Neuroscience 2004;24:7128-39 (Pubitemid 39096378)
131. Baraldi PG, Di Virgilio F, Romagnoli R. Agonists and antagonists acting at P2X7 receptor. Curr Top Med Chem 2004;4:1707-17 (Pubitemid 39654456)
132. Glick A, Ryscavage A, Perez-Lorenzo R, et al. The high-risk benign tumor: evidence from the two-stage skin cancer model and relevance for human cancer. Mol Carcinogenesis 2007;46:605-10 (Pubitemid 47255175)
133. Woodworth CD, Michael E, Smith L, et al. Strain-dependent differences in malignant conversion of mouse skin tumors is an inherent property of the epidermal keratinocyte. Carcinogenesis 2004;25:1771-8 (Pubitemid 39214320)
134. Reibel J. Prognosis of oral pre-malignant lesions: Signifcance of clinical, histopathological, and molecular biological characteristics. Crit Rev Oral Biol Med 2003;14:47-62
135. Fu W, Cockerell CJ. The actinic (solar) keratosis: a 21st century perspective. Arch Dermatol 2003;139:66-70
136. Lindeque BG. Management of cervical premalignant lesions. Best Pract Res Clin Obstet Gynaecol 2005;19:545-61 (Pubitemid 41263805)