Accelerated tumor progression in mice lacking the ATP receptor P2X7

Cancer Research

Volumn 75, Issue 4, 2015, Pages 635-644

  Adinolfi, Elena ^a   Capece, Marina ^a   Franceschini, Alessia ^a   Falzoni, Simonetta ^a   Giuliani, Anna L ^a   Rotondo, Alessandra ^a,f   Sarti, Alba C ^a   Bonora, Massimo ^a   Syberg, Susanne ^b   Corigliano, Domenica ^c   Pinton, Paolo ^a   Jorgensen, Niklas R ^b   Abelli, Luigi ^a   Emionite, Laura ^d   Raffaghello, Lizzia ^e   Pistoia, Vito ^e   Di Virgilio, Francesco ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Magna Grecia University   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e G GASLINI INSTITUTE   (Italy)

^f UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; PURINERGIC P2X7 RECEPTOR; VASCULOTROPIN; ADENOSINE TRIPHOSPHATE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BONE MARROW CELL; CELL INFILTRATION; CHEMOTAXIS; COLON CARCINOMA; CONTROLLED STUDY; DENDRITIC CELL; GENE DELETION; IMMUNE RESPONSE; INFLAMMATORY CELL; LUNG METASTASIS; MELANOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; TUMOR GROWTH; TUMOR VOLUME; WILD TYPE; ANIMAL; BIOSYNTHESIS; COLON TUMOR; DEFICIENCY; EXPERIMENTAL MELANOMA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; MACROPHAGE; METABOLISM; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-1BETA; MACROPHAGES; MELANOMA, EXPERIMENTAL; MICE; RECEPTORS, PURINERGIC P2X7; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923175155     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1259     Document Type: Article

References (46)

1. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 2007;87:659-797.
2. BoursMJ, Dagnelie PC, Giuliani AL, Wesselius A,Di Virgilio F. P2 receptors and extracellular ATP: a novel homeostatic pathway in inflammation. Front Biosci 2011;3:1443-56.
3. Di Virgilio F. The P2Z purinoceptor: an intriguing role in immunity, in flammation and cell death. Immunol Today 1995;16:524-8.
4. Di Virgilio F. Purines, purinergic receptors, and cancer. Cancer Res 2012;72:5441-7.
5. Adinol fi E, Raffaghello L, Giuliani AL, Cavazzini L, Capece M, Chiozzi P, et al. Expression of the P2X7 receptor increases in vivo tumor growth. Cancer Res 2012;75:2957-2969.
6. Aymeric L, Apetoh L, Ghiringhelli F, Tesniere A, Martins I, Kroemer G, et al. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res 2010;70:855-8.
7. Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5-triphosphate and adenosine as endogenous signal molecules in immunity and infl ammation. Pharmacol Ther 2006;112:358-404.
8. Wilhelm K, Ganesan J, Muller T, Durr C, GrimmM, Beilhack A, et al. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat Med 2010;16:1434-8.
9. Vergani A, Tezza S, D'Addio F, Fotino C, Liu K, Niewczas M, et al. Long-term heart transplant survival by targeting the ionotropic purinergic receptor P2X7. Circulation 2013;127:463-75.
10. Vergani A, Fotino C, D'Addio F, Tezza S, Podetta M, Gatti F, et al. Effect of the purinergic inhibitor oxidized ATP in a model of islet allograft rejection. Diabetes 2013;62:1665-75.
11. Airoldi I, Di Carlo E, Taverniti G, D'Antuono T, Ognio E, Watanabe M, et al. Endogenous IL-12 triggers an antiangiogenic program in melanoma cells. Proc Natl Acad Sci USA 2007;104:3996-4001.
12. MichaudM,Martins I, Sukkurwala AQ, Adjemian S,Ma Y, Pellegatti P, et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011;334:1573-7.
13. Mutini C, Falzoni S, Ferrari D, Chiozzi P, Morelli A, Baricordi OR, et al. Mouse dendritic cells express the P2X7 purinergic receptor: characterization and possible participation in antigen presentation. J Immunol 1999;163:1958-65.
14. Diaz-Hernandez M, del PA, Diaz-Hernandez JI, Diez-Zaera M, Lucas JJ, Garrido JJ, et al. Inhibition of the ATP-gated P2X7 receptor promotes axonal growth and branching in cultured hippocampal neurons. J Cell Sci 2008;121:3717-28.
15. Syberg S, Petersen S, Beck Jensen JE, Gartland A, Teilmann J, Chessell I, et al. Genetic background strongly infl uences the bone phenotype of P2X7 receptor knockout mice. J Osteoporos 2012;2012: 391097.
16. Sjoo F,Hassan Z, Abedi-ValugerdiM, Griskevicius L,Nilsson C, Remberger M, et al. Myeloablative and immunosuppressive properties of treosulfan in mice. Exp Hematol 2006;34:115-21.
17. Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR, Colombo MP. Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 2003;198:1475-85.
18. InabaK, Inaba M, Romani N, AyaH,DeguchiM, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992;176:1693-702.
19. Giuliani AL, Wiener E, Lee MJ, Brown IN, Berti G, Wickramasinghe SN. Changes inmurine bone marrowmacrophages and erythroid burst-forming cells following the intravenous injection of liposome-encapsulated dichloromethylene diphosphonate (Cl2MDP). Eur J Haematol 2001;66:221-9.
20. Lemaire I, Falzoni S, Zhang B, Pellegatti P, Di Virgilio F. The P2X7 receptor and Pannexin-1 are both required for the promotion of multinucleated macrophages by the inflammatory cytokine GM-CSF. J Immunol 2011; 187:3878-87.
21. Adriouch S, Dox C, Welge V, Seman M, Koch-Nolte F, Haag F. Cutting edge: a natural P451Lmutation in the cytoplasmic domain impairs the function of the mouse P2X7 receptor. J Immunol 2002;169:4108-12.
22. Dinarello CA. A clinical perspective of IL-1beta as the gatekeeper of inflammation. Eur J Immunol 2011;41:1203-17.
23. Dunn JH, Ellis LZ, Fujita M. Inflammasomes as molecular mediators of inflammation and cancer: potential role in melanoma. Cancer Lett 2012;314:24-33.
24. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 1996;156:1531-9.
25. Labasi JM, PetrushovaN, Donovan C, McCurdy S, Lira P, Payette MM, et al. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 2002;168:6436-45.
26. Barbera-Cremades M, Baroja-Mazo A, Gomez AI, Machado F, Di Virgilio F, Pelegrin P. P2X7 receptor-stimulation causes fever via PGE2 and IL-1beta release. FASEB J 2012;26:2951-62.
27. Asgari E, Le FG, Yamamoto H, Perucha E, Sacks SS, Kohl J, et al. C3a modulates IL-1beta secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood 2013;122: 3473-81.
28. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013;19:1423-37.
29. Pellegatti P, Raffaghello L, Bianchi G, Piccardi F, Pistoia V, Di Virgilio F. Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase. PLoS ONE 2008;3:e2599.
30. Forrester T. An estimate of adenosine triphosphate release into the venous effluent from exercising human forearmmuscle. J Physiol 1972;224:611-28.
31. Falzoni S, Donvito G, Di Virgilio F. Detecting adenosine triphosphate in the pericellular space. Interface Focus 2013;3:20120101.
32. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998;50:413-92.
33. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002;82: 1013-67.
34. Gu BJ,Wiley JS. Rapid ATP-induced release ofmatrix metalloproteinase 9 is mediated by the P2X7 receptor. Blood 2006;107:4946-53.
35. Coutinho-Silva R, Correa G, Sater AA, Ojcius DM. The P2X(7) receptor and intracellular pathogens: a continuing struggle. Purinergic Signal 2009;5: 197-204.
36. Di Virgilio F. Dr. Jekyll/Mr. Hyde: the dual role of extracellular ATP. J Auton Nerv Syst 2000;81:59-63.
37. Rayah A, Kanellopoulos JM, Di Virgilio F. P2 receptors and immunity. Microbes Infect 2012;14:1254-62.
38. Adinol fi E, Callegari MG, Ferrari D, Bolognesi C, Minelli M, Wieckowski MR, et al. Basal activation of the P2X7 ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth. Mol Biol Cell 2005;16: 3260 -72.
39. Bianco F, Ceruti S, Colombo A, Fumagalli M, Ferrari D, Pizzirani C, et al. A role for P2X7 in microglial proliferation. J Neurochem 2006;99: 745-58.
40. Monif M, Reid CA, Powell KL, Smart ML, Williams DA. The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore. J Neurosci 2009;29:3781-91.
41. Burnstock G, Di Virgilio F. Purinergic signalling and cancer. Purinergic Signal 2013;9:491-540.
42. Adinolfi E, Cirillo M, Woltersdorf R, Falzoni S, Chiozzi P, Pellegatti P, et al. Trophic activity of a naturally occurring truncated isoform of the P2X7 receptor. FASEB J 2010;24:3393-404.
43. Ghalali A, Wiklund F, Zheng H, Stenius U, Hogberg J. Atorvastatin prevents ATP-driven invasiveness via P2X7 and EHBP1 signaling in PTEN-expressing prostate cancer cells. Carcinogenesis 2014;35:1547-55.
44. Ferrari D, Chiozzi P, Falzoni S, Dal Susino M, Melchiorri L, Baricordi OR, et al. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 1997;159: 1451-8.
45. Hill LM, Gavala ML, Lenertz LY, Bertics PJ. Extracellular ATP may contribute to tissue repair by rapidly stimulating purinergic receptor X7-dependent vascular endothelial growth factor release from primary human monocytes. J Immunol 2010;185:3028-34.
46. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011;11:201-12.