Genetic and pharmacological inactivation of the purinergic P2RX7 receptor dampens inflammation but increases tumor incidence in a mouse model of colitis-associated cancer

Cancer Research

Volumn 75, Issue 5, 2015, Pages 835-845

  Hofman, Paul ^a,b,c,d   Cherfils Vicini, Julien ^a,b,d   Bazin, Marie ^a,b,d   Ilie, Marius ^a,b,c,d   Juhel, Thierry ^a,b,d   Hébuterne, Xavier ^a,b,e   Gilson, Eric ^a,b,d,e   Schmid Alliana, Annie ^b,f   Boyer, Olivier ^g,h   Adriouch, Sahil ^g,h   Vouret Craviari, Valérie ^a,b,d  

^a UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c PASTEUR HOSPITAL   (France)

^d CENTRE ANTOINE LACASSAGNE   (France)

^e CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^f INSERM   (France)

^g faculté mixte de médecine et de pharmacie de Rouen   (France)

^h UNIVERSITY OF ROUEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

P2RX7 PROTEIN, MOUSE; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X7 RECEPTOR; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; BIOSYNTHESIS; C57BL MOUSE; COLITIS; COLON TUMOR; DISEASE MODEL; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INCIDENCE; METABOLISM; MOUSE; PATHOLOGY; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; COLITIS; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INCIDENCE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PURINERGIC P2X RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2X7; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84928699565     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1778     Document Type: Article

References (49)

1. Burnstock G, Williams M. P2 purinergic receptors: modulation of cell function and therapeutic potential. J Pharmacol Exp Ther 2000;295:862-9.
2. Antonioli L, Colucci R, Pellegrini C, Giustarini G, Tuccori M, Blandizzi C, et al. The role of purinergic pathways in the pathophysiology of gut diseases: pharmacological modulation and potential therapeutic applications. Pharmacol Ther 2013;139:157-88.
3. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002;82:1013-67.
4. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2 × 7 receptor. EMBO J 2006;25:5071-82.
5. Locovei S, Scemes E, Qiu F, Spray DC, Dahl G. Pannexin1 is part of the pore forming unit of the P2X (7) receptor death complex. FEBS Lett 2007;581:483-8.
6. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, et al. The P2 × 7 receptor: a key player in IL-1 processing and release. J Immunol 2006;176:3877-83.
7. Trautmann A. Extracellular ATP in the immune system: more than just a "danger signal." Sci Signal 2009;2:pe6.
8. Cesaro A, Brest P, Hofman V, Hebuterne X, Wildman S, Ferrua B, et al. Amplification loop of the inflammatory process is induced by P2 × 7R activation in intestinal epithelial cells in response to neutrophil transepithelial migration. Am J Physiol Gastrointest Liver Physiol 2010;299:G32-42.
9. 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.
10. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, et al. Altered cytokine production in mice lacking P2X (7) receptors. J Biol Chem 2001;276:125-32.
11. Labasi JM, PetrushovaN, Donovan C, McCurdy S, Lira P, Payette MM, et al. Absence of the P2 × 7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 2002;168:6436-45.
12. Marques CC, Castelo-Branco MT, Pacheco RG, Buongusto F, do Rosario A Jr, Schanaider A, et al. Prophylactic systemic P2 × 7 receptor blockade prevents experimental colitis. Biochim Biophys Acta 2014;1842:65-78.
13. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006;6:24-37.
14. Mackenzie AB, Young MT, Adinolfi E, Surprenant A. Pseudoapoptosis induced by brief activation of ATP-gated P2 × 7 receptors. J Biol Chem 2005;280:33968-76.
15. Adinolfi E, Cirillo M, Woltersdorf R, Falzoni S, Chiozzi P, Pellegatti P, et al. Trophic activity of a naturally occurring truncated isoform of the P2 × 7 receptor. FASEB J 2010;24:3393-404.
16. Adinolfi E, Raffaghello L, Giuliani AL, Cavazzini L, Capece M, Chiozzi P, et al. Expression of P2 × 7 receptor increases in vivo tumor growth. Cancer Res 2012;72:2957-69.
17. Wiley JS, Dao-Ung LP, Gu BJ, Sluyter R, Shemon AN, Li C, et al. A loss-offunction polymorphic mutation in the cytolytic P2 × 7 receptor gene and chronic lymphocytic leukaemia: a molecular study. Lancet 2002;359:1114-9.
18. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1betadependent adaptive immunity against tumors. Nat Med 2009;15:1170-8.
19. Adinolfi E, Melchiorri L, Falzoni S, Chiozzi P, Morelli A, Tieghi A, et al. P2× 7 receptor expression in evolutive and indolent forms of chronic B lymphocytic leukemia. Blood 2002;99:706-8.
20. Greig AV, Linge C, Healy V, Lim P, Clayton E, Rustin MH, 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.
21. Slater M, Danieletto S, Gidley-Baird A, Teh LC, Barden JA. Early prostate cancer detected using expression of non-functional cytolytic P2 × 7 receptors. Histopathology 2004;44:206-15.
22. Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CH, Stanners CP, et al. Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 2009;206:2179-89.
23. Chin AC, Parkos CA. Neutrophil transepithelial migration and epithelial barrier function in IBD: potential targets for inhibiting neutrophil trafficking. Ann N Y Acad Sci 2006;1072:276-87.
24. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 2009;16:183-94.
25. Fridlender ZG, Sun J, Mishalian I, Singhal S, Cheng G, Kapoor V, et al. Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS ONE 2012;7:e31524.
26. Massague J. TGFbeta in cancer. Cell 2008;134:215-30.
27. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 2010;10:554-67.
28. Yan Z, Kim GY, Deng X, Friedman E. Transforming growth factor beta 1 induces proliferation in colon carcinoma cells by Ras-dependent, smad-independent down-regulation of p21cip1. J Biol Chem 2002;277:9870-9.
29. Filippini A, Taffs RE, Agui T, Sitkovsky MV. Ecto-ATPase activity in cytolytic T-lymphocytes. Protection from the cytolytic effects of extracellular ATP. J Biol Chem 1990;265:334-40.
30. Di Virgilio F, Bronte V, Collavo D, Zanovello P. Responses of mouse lymphocytes to extracellular adenosine 50-triphosphate (ATP). Lymphocytes with cytotoxic activity are resistant to the permeabilizing effects of ATP. J Immunol 1989;143:1955-60.
31. Baricordi OR, Ferrari D, Melchiorri L, Chiozzi P, Hanau S, Chiari E, et al. An ATP-activated channel is involved in mitogenic stimulation of human T lymphocytes. Blood 1996;87:682-90.
32. Adinolfi E, Callegari MG, Ferrari D, Bolognesi C, Minelli M, Wieckowski MR, et al. Basal activation of the P2 × 7 ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth. Mol Biol Cell 2005;16:3260-72.
33. Di Virgilio F, Ferrari D, Adinolfi E. P2X (7): a growth-promoting receptorimplications for cancer. Purinergic Signal 2009;5:251-6.
34. Neves AR, Castelo-Branco MT, Figliuolo VR, Bernardazzi C, Buongusto F, Yoshimoto A, et al. Overexpression of ATP-activated P2×7 receptors in the intestinal mucosa is implicated in the pathogenesis of Crohn's disease. Inflamm Bowel Dis 2014;20:444-57.
35. Salcedo R, Worschech A, Cardone M, Jones Y, Gyulai Z, Dai RM, et al. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J Exp Med 2010;207:1625-36.
36. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009;15:103-13.
37. Chaput N, Louafi S, Bardier A, Charlotte F, Vaillant JC, Menegaux F, et al. Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue. Gut 2009;58:520-9.
38. Hubert S, Rissiek B, Klages K, Huehn J, Sparwasser T, Haag F, et al. Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2 × 7 pathway. J Exp Med 2010;207:2561-8.
39. Adriouch S, Haag F, Boyer O, Seman M, Koch-Nolte F. Extracellular NAD (+): a danger signal hindering regulatory T cells. Microbes Infect 2012;14:1284-92.
40. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992;359:693-9.
41. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 1993;90:770-4.
42. Thomas DA, Massague J. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005;8:369-80.
43. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factorbeta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007;26:579-91.
44. Donkor MK, Sarkar A, Li MO. Tgf-beta1 produced by activated CD4 (+) T Cells Antagonizes T Cell Surveillance of Tumor Development. Oncoimmunology 2012;1:162-71.
45. Jiang LH, Baldwin JM, Roger S, Baldwin SA. Insights into the molecular mechanisms underlying mammalian P2 × 7 receptor functions and contributions in diseases, revealed by structural modeling and single nucleotide polymorphisms. Front Pharmacol 2013;4:55.
46. Miller CM, Boulter NR, Fuller SJ, Zakrzewski AM, Lees MP, Saunders BM, et al. The role of the P2X (7) receptor in infectious diseases. PLoS Pathog 2011;7:e1002212.
47. Fuller SJ, Stokes L, Skarratt KK, Gu BJ, Wiley JS. Genetics of the P2 × 7 receptor and human disease. Purinergic Signal 2009;5:257-62.
48. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012;491:119-24.
49. Solini A, Cuccato S, Ferrari D, Santini E, Gulinelli S, Callegari MG, et al. Increased P2 × 7 receptor expression and function in thyroid papillary cancer: a new potential marker of the disease? Endocrinology 2008;149:389-96.