Skip to main content
SpringerLink
Log in

Reviewing the role of P2Y receptors in specific gastrointestinal cancers

  • Review Article
  • Published:
Purinergic Signalling Aims and scope Submit manuscript

Abstract

Extracellular nucleotides are important intercellular signaling molecules that were found enriched in the tumor microenvironment. In fact, interfering with G protein-coupled P2Y receptor signaling has emerged as a promising therapeutic alternative to treat aggressive and difficult-to-manage cancers such as those affecting the gastrointestinal system. In this review, we will discuss the functions of P2Y receptors in gastrointestinal cancers with an emphasis on colorectal, hepatic, and pancreatic cancers. We will show that P2Y2 receptor up-regulation increases cancer cell proliferation, tumor growth, and metastasis in almost all studied gastrointestinal cancers. In contrast, we will present P2Y6 receptor as having opposing roles in colorectal cancer vs. gastric cancer. In colorectal cancer, the P2Y6 receptor induces carcinogenesis by inhibiting apoptosis, whereas P2Y6 suppresses gastric cancer tumor growth by reducing β-catenin transcriptional activity. The contribution of the P2Y11 receptor in the migration of liver and pancreatic cancer cells will be compared to its normal inhibitory function on this cellular process in ciliated cholangiocytes. Hence, we will demonstrate that the selective inhibition of the P2Y12 receptor activity in platelets was associated to a reduction in the risk of developing colorectal cancer and metastasis formation. We will succinctly review the role of P2Y1, P2Y4, P2Y13, and P2Y14 receptors as the knowledge for these receptors in gastrointestinal cancers is sparse. Finally, redundant ligand selectivity, nucleotide high lability, cell context, and antibody reliability will be presented as the main difficulties in defining P2Y receptor functions in gastrointestinal cancers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24:509–581

    CAS  PubMed  Google Scholar 

  2. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492

    CAS  PubMed  Google Scholar 

  3. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31–304

    CAS  PubMed  Google Scholar 

  4. Burnstock G (2013) Purinergic signalling: pathophysiology and therapeutic potential. Keio J Med 62:63–73

    CAS  PubMed  Google Scholar 

  5. Giuliani AL, Sarti AC, Di Virgilio F (2019) Extracellular nucleotides and nucleosides as signalling molecules. Immunol Lett 205:16–24

    CAS  PubMed  Google Scholar 

  6. North RA (2016) P2X receptors. Philos Trans R Soc Lond Ser B Biol Sci 371:20150427

    Google Scholar 

  7. Erb L, Weisman GA (2012) Coupling of P2Y receptors to G proteins and other signaling pathways. Wiley Interdiscip Rev Membr Transp Signal 1:789–803

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Di Virgilio F, Adinolfi E (2017) Extracellular purines, purinergic receptors and tumor growth. Oncogene 36:293–303

    PubMed  Google Scholar 

  9. Zimmermann H, Zebisch M, Strater N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8:437–502

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Lasry A, Zinger A, Ben-Neriah Y (2016) Inflammatory networks underlying colorectal cancer. Nat Immunol 17:230–240

    CAS  PubMed  Google Scholar 

  11. Parcesepe P, Giordano G, Laudanna C, Febbraro A, Pancione M (2016) Cancer-associated immune resistance and evasion of immune surveillance in colorectal Cancer. Gastroenterol Res Pract 2016:6261721

    PubMed  PubMed Central  Google Scholar 

  12. Roma-Rodrigues C, Mendes R, Baptista PV, Fernandes AR (2019) Targeting tumor microenvironment for Cancer therapy. Int J Mol Sci 20:1–31

    Google Scholar 

  13. Kenny PA, Lee GY, Bissell MJ (2007) Targeting the tumor microenvironment. Front Biosci 12:3468–3474

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ma X, Pan X, Wei Y, Tan B, Yang L, Ren H, Qian M, Du B (2016) Chemotherapy-induced uridine diphosphate release promotes breast cancer metastasis through P2Y6 activation. Oncotarget 7:29036–29050

    PubMed  PubMed Central  Google Scholar 

  15. Kuipers EJ, Grady WM, Lieberman D, Seufferlein T, Sung JJ, Boelens PG, van de Velde CJ, Watanabe T (2015) Colorectal cancer. Nat Rev Dis Primers 1:15065

    PubMed  PubMed Central  Google Scholar 

  16. Ilic M, Ilic I (2016) Epidemiology of pancreatic cancer. World J Gastroenterol 22:9694–9705

    PubMed  PubMed Central  Google Scholar 

  17. Höpfner M, Lemmer K, Jansen A, Hanski C, Riecken EO, Gavish M, Mann B, Buhr H, Glassmeier G, Scherübl H (1998) Expression of functional P2-purinergic receptors in primary cultures of human colorectal carcinoma cells. Biochem Biophys Res Commun 251:811–817

    PubMed  Google Scholar 

  18. Höpfner M, Maaser K, Barthel B, von Lampe B, Hanski C, Riecken EO, Zeitz M, Scherübl H (2001) Growth inhibition and apoptosis induced by P2Y2 receptors in human colorectal carcinoma cells: involvement of intracellular calcium and cyclic adenosine monophosphate. Int J Color Dis 16:154–166

    Google Scholar 

  19. Maaser K, Höpfner M, Kap H, Sutter AP, Barthel B, von Lampe B, Zeitz M, Scherübl H (2002) Extracellular nucleotides inhibit growth of human oesophageal cancer cells via P2Y(2)-receptors. Br J Cancer 86:636–644

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Yaguchi T, Saito M, Yasuda Y, Kanno T, Nakano T, Nishizaki T (2010) Higher concentrations of extracellular ATP suppress proliferation of Caco-2 human colonic cancer cells via an unknown receptor involving PKC inhibition. Cell Physiol Biochem 26:125–134

    CAS  PubMed  Google Scholar 

  21. Coutinho-Silva R, Stahl L, Cheung KK, de Campos NE, de Oliveira SC, Ojcius DM, Burnstock G (2005) P2X and P2Y purinergic receptors on human intestinal epithelial carcinoma cells: effects of extracellular nucleotides on apoptosis and cell proliferation. Am J Physiol Gastrointest Liver Physiol 288:G1024–G1035

    CAS  PubMed  Google Scholar 

  22. Di Virgilio F (2012) Purines, purinergic receptors, and cancer. Cancer Res 72:5441–5447

    PubMed  Google Scholar 

  23. Nylund G, Hultman L, Nordgren S, Delbro DS (2007) P2Y2- and P2Y4 purinergic receptors are over-expressed in human colon cancer. Auton Autacoid Pharmacol 27:79–84

    CAS  PubMed  Google Scholar 

  24. Künzli BM, Bernlochner MI, Rath S, Käser S, Csizmadia E, Enjyoji K, Cowan P, d’Apice A, Dwyer K, Rosenberg R, Perren A, Friess H, Maurer CA, Robson SC (2011) Impact of CD39 and purinergic signalling on the growth and metastasis of colorectal cancer. Purinergic Signal 7:231–241

    PubMed  PubMed Central  Google Scholar 

  25. Hatanaka H, Takada S, Choi YL, Fujiwara S, Soda M, Enomoto M, Kurashina K, Watanabe H, Yamashita Y, Sugano K, Mano H (2007) Transforming activity of purinergic receptor P2Y, G-protein coupled, 2 revealed by retroviral expression screening. Biochem Biophys Res Commun 356:723–726

    CAS  PubMed  Google Scholar 

  26. Li WH, Qiu Y, Zhang HQ, Liu Y, You JF, Tian XX, Fang WG (2013) P2Y2 receptor promotes cell invasion and metastasis in prostate cancer cells. Br J Cancer 109:1666–1675

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Martínez-Ramírez AS, Garay E, García-Carrancá A, Vázquez-Cuevas FG (2016) The P2RY2 receptor induces carcinoma cell migration and EMT through cross-talk with epidermal growth factor receptor. J Cell Biochem 117:1016–1026

    PubMed  Google Scholar 

  28. Qiu Y, Liu Y, Li WH, Zhang HQ, Tian XX, Fang WG (2018) P2Y2 receptor promotes the migration and invasion of breast cancer cells via EMT-related genes snail and E-cadherin. Oncol Rep 39:138–150

    CAS  PubMed  Google Scholar 

  29. Buzzi N, Bilbao PS, Boland R, de Boland AR (2009) Extracellular ATP activates MAP kinase cascades through a P2Y purinergic receptor in the human intestinal Caco-2 cell line. Biochim Biophys Acta Gen subj 1790:1651–1659

    CAS  Google Scholar 

  30. Buzzi N, Boland R, Russo de Boland A (2010) Signal transduction pathways associated with ATP-induced proliferation of colon adenocarcinoma cells. Biochim Biophys Acta 1800:946–955

    CAS  PubMed  Google Scholar 

  31. Limami Y, Pinon A, Leger DY, Pinault E, Delage C, Beneytout J-L, Simon A, Liagre B (2012) The P2Y2/Src/p38/COX-2 pathway is involved in the resistance to ursolic acid-induced apoptosis in colorectal and prostate cancer cells. Biochimie 94:1754–1763

    CAS  PubMed  Google Scholar 

  32. Vinette V, Placet M, Arguin G, Gendron FP (2015) Multidrug resistance-associated protein 2 expression is upregulated by adenosine 5′-triphosphate in colorectal Cancer cells and enhances their survival to chemotherapeutic drugs. PLoS One 10:e0136080

    PubMed  PubMed Central  Google Scholar 

  33. Choi JH, Ji YG, Lee DH (2013) Uridine triphosphate increases proliferation of human cancerous pancreatic duct epithelial cells by activating P2Y2 receptor. Pancreas 42:680–686

    CAS  PubMed  Google Scholar 

  34. Hu LP, Zhang XX, Jiang SH, Tao LY, Li Q, Zhu LL, Yang MW, Huo YM, Jiang YS, Tian GA, Cao XY, Zhang YL, Yang Q, Yang XM, Wang YH, Li J, Xiao GG, Sun YW, Zhang ZG (2019) Targeting purinergic receptor P2Y2 prevents the growth of pancreatic ductal adenocarcinoma by inhibiting Cancer cell glycolysis. Clin Cancer Res 25:1318–1330

    PubMed  Google Scholar 

  35. van Dam H, Castellazzi M (2001) Distinct roles of Jun : Fos and Jun : ATF dimers in oncogenesis. Oncogene 20:2453–2464

    PubMed  Google Scholar 

  36. Liu J, Liao Z, Camden J, Griffin KD, Garrad RC, Santiago-Pérez LI, González FA, Seye CI, Weisman GA, Erb L (2004) Src homology 3 binding sites in the P2Y2 nucleotide receptor interact with Src and regulate activities of Src, proline-rich tyrosine kinase 2, and growth factor receptors. J Biol Chem 279:8212–8218

    CAS  PubMed  Google Scholar 

  37. Kim SH, Ryu HG, Lee J, Shin J, Harikishore A, Jung HY, Kim YS, Lyu HN, Oh E, Baek NI, Choi KY, Yoon HS, Kim KT (2015) Ursolic acid exerts anti-cancer activity by suppressing vaccinia-related kinase 1-mediated damage repair in lung cancer cells. Sci Rep 5:14570

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Shanmugam MK, Dai X, Kumar AP, Tan BK, Sethi G, Bishayee A (2013) Ursolic acid in cancer prevention and treatment: molecular targets, pharmacokinetics and clinical studies. Biochem Pharmacol 85:1579–1587

    CAS  PubMed  Google Scholar 

  39. Limami Y, Pinon A, Leger DY, Mousseau Y, Cook-Moreau J, Beneytout JL, Delage C, Liagre B, Simon A (2011) HT-29 colorectal cancer cells undergoing apoptosis overexpress COX-2 to delay ursolic acid-induced cell death. Biochimie 93:749–757

    CAS  PubMed  Google Scholar 

  40. Hlavata I, Mohelnikova-Duchonova B, Vaclavikova R, Liska V, Pitule P, Novak P, Bruha J, Vycital O, Holubec L, Treska V, Vodicka P, Soucek P (2012) The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis 27:187–196

    CAS  PubMed  Google Scholar 

  41. Xie R, Xu J, Wen G, Jin H, Liu X, Yang Y, Ji B, Jiang Y, Song P, Dong H, Tuo B (2014) The P2Y2 nucleotide receptor mediates the proliferation and migration of human hepatocellular carcinoma cells induced by ATP. J Biol Chem 289:19137–19149

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Muz B, de la Puente P, Azab F, Azab AK (2015) The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckl) 3:83–92

    Google Scholar 

  43. Tak E, Jun DY, Kim SH, Park GC, Lee J, Hwang S, Song GW, Lee SG (2016) Upregulation of P2Y2 nucleotide receptor in human hepatocellular carcinoma cells. J Int Med Res 44:1234–1247

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Elsing C, Kassner A, Hubner C, Buhli H, Stremmel W (1996) Absorptive and secretory mechanisms in biliary epithelial cells. J Hepatol 24(Suppl 1):121–127

    CAS  PubMed  Google Scholar 

  45. Doctor RB, Matzakos T, McWilliams R, Johnson S, Feranchak AP, Fitz JG (2005) Purinergic regulation of cholangiocyte secretion: identification of a novel role for P2X receptors. Am J Physiol Gastrointest Liver Physiol 288:G779–G786

    CAS  PubMed  Google Scholar 

  46. Burnstock G (2014) Purinergic signalling in the gastrointestinal tract and related organs in health and disease. Purinergic Signal 10:3–50

    CAS  PubMed  Google Scholar 

  47. Elsing C, Georgiev T, Hubner CA, Boger R, Stremmel W, Schlenker T (2012) Extracellular ATP induces cytoplasmic and nuclear Ca2+ transients via P2Y2 receptor in human biliary epithelial cancer cells (Mz-Cha-1). Anticancer Res 32:3759–3767

    CAS  PubMed  Google Scholar 

  48. Rodrigues MA, Gomes DA, Leite MF, Grant W, Zhang L, Lam W, Cheng YC, Bennett AM, Nathanson MH (2007) Nucleoplasmic calcium is required for cell proliferation. J Biol Chem 282:17061–17068

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Hardingham GE, Chawla S, Johnson CM, Bading H (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260–265

    CAS  PubMed  Google Scholar 

  50. Künzli BM, Berberat PO, Giese T, Csizmadia E, Kaczmarek E, Baker C, Halaceli I, Buchler MW, Friess H, Robson SC (2007) Upregulation of CD39/NTPDases and P2 receptors in human pancreatic disease. Am J Physiol Gastrointest Liver Physiol 292:G223–G230

    PubMed  Google Scholar 

  51. Nylund G, Nordgren S, Delbro DS (2004) Expression of P2Y2 purinoceptors in MCG 101 murine sarcoma cells, and HT-29 human colon carcinoma cells. Auton Neurosci 112:69–79

    CAS  PubMed  Google Scholar 

  52. Ko T, An HJ, Ji YG, Kim OJ, Lee DH (2012) P2Y receptors regulate proliferation of human pancreatic duct epithelial cells. Pancreas 41:797–803

    CAS  PubMed  Google Scholar 

  53. Placet M, Arguin G, Molle CM, Babeu JP, Jones C, Carrier JC, Robaye B, Geha S, Boudreau F, Gendron FP (2018) The G protein-coupled P2Y(6) receptor promotes colorectal cancer tumorigenesis by inhibiting apoptosis. Biochim Biophys Acta Mol basis Dis 1864:1539–1551

    CAS  PubMed  Google Scholar 

  54. Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479–507

    CAS  PubMed  Google Scholar 

  55. Wan H, Xie R, Xu J, He J, Tang B, Liu Q, Wang S, Guo Y, Yang X, Dong TX, Carethers JM, Yang S, Dong H (2017) Anti-proliferative effects of nucleotides on gastric Cancer via a novel P2Y6/SOCE/Ca2+/beta-catenin pathway. Sci Rep 7:2459

    PubMed  PubMed Central  Google Scholar 

  56. Obexer P, Ausserlechner MJ (2014) X-linked inhibitor of apoptosis protein - a critical death resistance regulator and therapeutic target for personalized cancer therapy. Front Oncol 4:197

    PubMed  PubMed Central  Google Scholar 

  57. Kohno T, Yoshida S, Bessho M (1998) Accelerated entry into S phase associated with up-regulation of cyclin D1 as a mechanism for granulocyte colony-stimulating factor (G-CSF)-induced apoptosis of murine myeloid leukemia cells. Leuk Res 22:257–263

    CAS  PubMed  Google Scholar 

  58. Li G, Iyengar R (2002) Calpain as an effector of the Gq signaling pathway for inhibition of Wnt/beta-catenin-regulated cell proliferation. PNAS 99:13254–13259

    CAS  PubMed  Google Scholar 

  59. Shi K, Queiroz KC, Stap J, Richel DJ, Spek CA (2013) Protease-activated receptor-2 induces migration of pancreatic cancer cells in an extracellular ATP-dependent manner. J Thromb Haemost 11:1892–1902

    CAS  PubMed  Google Scholar 

  60. Ge L, Shenoy SK, Lefkowitz RJ, DeFea K (2004) Constitutive protease-activated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both beta-arrestin-1 and -2. J Biol Chem 279:55419–55424

    CAS  PubMed  Google Scholar 

  61. Morris DR, Ding Y, Ricks TK, Gullapalli A, Wolfe BL, Trejo J (2006) Protease-activated Receptor-2 is essential for factor VIIa and Xa-induced signaling, migration, and invasion of breast Cancer cells. Cancer Res 66:307–314

    CAS  PubMed  Google Scholar 

  62. Darmoul D, Gratio V, Devaud H, Laburthe M (2004) Protease-activated receptor 2 in colon cancer: trypsin-induced MAPK phosphorylation and cell proliferation are mediated by epidermal growth factor receptor transactivation. J Biol Chem 279:20927–20934

    CAS  PubMed  Google Scholar 

  63. Zhou B, Zhou H, Ling S, Guo D, Yan Y, Zhou F, Wu Y (2011) Activation of PAR2 or/and TLR4 promotes SW620 cell proliferation and migration via phosphorylation of ERK1/2. Oncol Rep 25:503–511

    CAS  PubMed  Google Scholar 

  64. Khalid M, Brisson L, Tariq M, Hao Y, Guibon R, Fromont G, Mortadza SAS, Mousawi F, Manzoor S, Roger S, Jiang LH (2017) Carcinoma-specific expression of P2Y11 receptor and its contribution in ATP-induced purinergic signalling and cell migration in human hepatocellular carcinoma cells. Oncotarget 8:37278–37290

    PubMed  PubMed Central  Google Scholar 

  65. Mansini AP, Peixoto E, Jin S, Richard S, Gradilone SA (2019) The chemosensory function of primary cilia regulates cholangiocyte migration, invasion and tumor growth. Hepatology 69:1582–1598

    CAS  PubMed  Google Scholar 

  66. Mansini AP, Peixoto E, Thelen KM, Gaspari C, Jin S, Gradilone SA (2018) The cholangiocyte primary cilium in health and disease. Biochim Biophys Acta Mol basis Dis 1864:1245–1253

    CAS  PubMed  Google Scholar 

  67. Huong PT, Nguyen LT, Nguyen XB, Lee SK, Bach DH (2019) The role of platelets in the tumor-microenvironment and the drug resistance of Cancer cells. Cancers (Basel) 11(2). https://doi.org/10.3390/cancers11020240

    CAS  PubMed Central  Google Scholar 

  68. Mitrugno A, Williams D, Kerrigan SW, Moran N (2014) A novel and essential role for FcγRIIa in cancer cell-induced platelet activation. Blood 123:249–260

    CAS  PubMed  Google Scholar 

  69. Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S (2013) Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell 24:130–137

    CAS  PubMed  Google Scholar 

  70. Patrignani P, Patrono C (2016) Aspirin and Cancer. J Am Coll Cardiol 68:967–976

    CAS  PubMed  Google Scholar 

  71. Rodriguez-Miguel A, Garcia-Rodriguez LA, Gil M, Montoya H, Rodriguez-Martin S, de Abajo FJ (2018) Clopidogrel and low-dose aspirin, alone or together, Reduce Risk of Colorectal Cancer. Clin Gastroenterol Hepatol

  72. Cea Soriano L, Soriano-Gabarro M, Garcia Rodriguez LA (2016) The protective effect of low-dose aspirin against colorectal Cancer is unlikely explained by selection Bias: results from three different study designs in clinical practice. PLoS One 11:e0159179

    PubMed  PubMed Central  Google Scholar 

  73. Guillem-Llobat P, Dovizio M, Bruno A, Ricciotti E, Cufino V, Sacco A, Grande R, Alberti S, Arena V, Cirillo M, Patrono C, FitzGerald GA, Steinhilber D, Sgambato A, Patrignani P (2016) Aspirin prevents colorectal cancer metastasis in mice by splitting the crosstalk between platelets and tumor cells. Oncotarget 7:32462–32477

    PubMed  PubMed Central  Google Scholar 

  74. Baranska J, Czajkowski R, Pomorski P (2017) P2Y1 receptors - properties and functional activities. Adv Exp Med Biol 1051:71–89

    PubMed  Google Scholar 

  75. Cortier M, Boina-Ali R, Racoeur C, Paul C, Solary E, Jeannin JF, Bettaieb A (2015) H89 enhances the sensitivity of cancer cells to glyceryl trinitrate through a purinergic receptor-dependent pathway. Oncotarget 6:6877–6886

    PubMed  PubMed Central  Google Scholar 

  76. Junankar PR, Karjalainen A, Kirk K (2002) The role of P2Y1 purinergic receptors and cytosolic Ca2+ in hypotonically activated osmolyte efflux from a rat hepatoma cell line. J Biol Chem 277:40324–40334

    CAS  PubMed  Google Scholar 

  77. Delbro DS, Nylund G, Nordgren S (2005) Demonstration of P2Y4 purinergic receptors in the HT-29 human colon cancer cell line. Auton Autacoid Pharmacol 25:163–166

    CAS  PubMed  Google Scholar 

  78. Yu W, Hill WG (2013) Lack of specificity shown by P2Y(6) receptor antibodies. Naunyn Schmiedeberg's Arch Pharmacol 386:885–891

    CAS  Google Scholar 

  79. Dreisig K, Degn M, Sund L, Hadaczek P, Samaranch L, San Sebastian W, Bankiewicz K, Rahbek Kornum B (2016) Validation of antibodies for neuroanatomical localization of the P2Y11 receptor in macaque brain. J Chem Neuroanat 78:25–33

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Mr. Louis-Thomas Gendron for his critical review of the manuscript.

Funding

This work was supported by a Canadian Institutes of Health Research operating grant [MOP-286567] and a 2019 Crohn and Colitis Canada Grants-in-Aid of Research to FPG. SDB holds an FRQ-S postdoctoral fellowship. FPG is a member of the FRQ-S-funded Centre de recherche du CHUS and the Pharmacology Institute of Sherbrooke.

Author information

Authors and Affiliations

  1. Département d’anatomie et de biologie cellulaire, Faculté de médecine et des sciences de la santé, Pavillon de recherche appliquée sur le cancer, Université de Sherbrooke, 3201 rue Jean-Mignault, Sherbrooke, Québec, J1E 4K8, Canada

    Steve Dagenais Bellefeuille, Caroline M. Molle & Fernand-Pierre Gendron

Authors
  1. Steve Dagenais Bellefeuille
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline M. Molle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernand-Pierre Gendron
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernand-Pierre Gendron.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bellefeuille, S.D., Molle, C.M. & Gendron, FP. Reviewing the role of P2Y receptors in specific gastrointestinal cancers. Purinergic Signalling 15, 451–463 (2019). https://doi.org/10.1007/s11302-019-09678-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11302-019-09678-x

Keywords

Search

Navigation