Specific activation of A3, A2a and A1 adenosine receptors in CD73-knockout mice affects B16F10 melanoma growth, neovascularization, angiogenesis and macrophage infiltration

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Koszałka, Patrycja ^a   Gołuńska, Monika ^a   Urban, Aleksandra ^a   Stasiłojć, Grzegorz ^a   Stanisławowski, Marcin ^a   Majewski, Marceli ^a   Składanowski, Andrzej C ^a   Bigda, Jacek ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A3 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; VASCULOTROPIN RECEPTOR 2; ADENOSINE; ADENOSINE RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL INFILTRATION; CONTROLLED STUDY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; MACROPHAGE INFILTRATION; MALE; MELANOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR AFFINITY; TUMOR VASCULARIZATION; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DEFICIENCY; EXPERIMENTAL MELANOMA; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; IMMUNOLOGY; MACROPHAGE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SIGNAL TRANSDUCTION; UPREGULATION; VASCULARIZATION;

5'-NUCLEOTIDASE; ADENOSINE; ANIMALS; CELL PROLIFERATION; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKOUT TECHNIQUES; MACROPHAGES; MALE; MELANOMA, EXPERIMENTAL; MICE; NEOVASCULARIZATION, PATHOLOGIC; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A3; RECEPTORS, PURINERGIC P1; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84962487133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151420     Document Type: Article

References (52)

1. Allard B, Turcotte M, Spring K, Pommey S, Royal I, Stagg J. Anti-CD73 therapy impairs tumor angiogenesis. Int J Cancer. 2014;134:1466-1473. doi: 10.1002/ijc.28456 PMID: 23982901
2. Zimmermann H, Zebisch M, Sträter N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 2012;8:437-502. doi: 10.1007/s11302-012-9309-4 PMID: 22555564
3. Stagg J, Divisekera U, Duret H, Sparwasser T, Teng MW, Darcy PK, Smyth MJ. CD73-deficient mice have increased antitumor immunity and are resistant to experimental metastasis. Cancer Res. 2011;71:2892-2900. doi: 10.1158/0008-5472. CAN-10-4246 PMID: 21292811
4. Koszałka P, Gołuńska M, Stanisławowski M, Urban A, Stasiłojć G, Majewski M, et al. CD73 on B16F10 melanoma cells in CD73-deficient mice promotes tumor growth, angiogenesis, neovascularization, macrophage infiltration and metastasis. Int J Biochem Cell Biol. 2015;69:1-10. doi: 10.1016/j.biocel. 2015.10.003 PMID: 26545615
5. Yegutkin GG, Marttila-Ichihara F, Karikoski M, Niemelä J, Laurila JP, Elima K, Jalkanen S, Salmi M. Altered purinergic signaling in CD73-deficient mice inhibits tumor progression. Eur J Immunol. 2011;41:1231-1241. doi: 10.1002/eji.201041292 PMID: 21469131
6. Wang L, Tang S, Wang Y, Xu S, Yu J, Zhi X, et al. Ecto-5'-nucleotidase (CD73) promotes tumor angiogenesis. Clin Exp Metastasis. 2013;30:671-680. doi: 10.1007/s10585-013-9571-z PMID: 23508889
7. Auchampach JA. Adenosine receptors and angiogenesis. Circ Res. 2007;101:1075-1077. PMID: 18040023
8. Gacche RN, Meshram RJ. Targeting tumor micro-environment for design and development of novel anti-angiogenic agents arresting tumor growth. Prog Biophys Mol Biol. 2013;113:333-354. doi: 10. 1016/j.pbiomolbio.2013.10.001 PMID: 24139944
9. Fredholm BB, Irenius E, Kull B, Schulte G. Comparison of the potency of adenosine as an agonist at human adenosine receptors expressed in Chinese hamster ovary cells. Biochem Pharmacol. 2001;61:443-448. PMID: 11226378
10. Schulte G, Fredholm BB. Signalling from adenosine receptors to mitogen-activated protein kinases. Cell Signal. 2003;15:813-827. PMID: 12834807
11. Adair TH. Growth regulation of the vascular system: an emerging role for adenosine. Am J Physiol. 2005;289:R283-296.
12. Headrick JP, Ashton KJ, Rose'Meyer RB, Peart JN. Cardiovascular adenosine receptors: Expression, actions and interactions. Pharmacol Ther. 2013;140:92-111. doi: 10.1016/j.pharmthera.2013.06.002 PMID: 23764371
13. Ryzhov S, Novitskiy SV, Zaynagetdinov R, Goldstein AE, Carbone DP, Biaggioni I, et al. Host A (2B) adenosine receptors promote carcinoma growth. Neoplasia. 2008;10:987-995. PMID: 18714400
14. 3 adenosine receptors. Circ Res. 2003;92:485-492. PMID: 12600879
15. Clark AN, Youkey R, Liu X, Jia L, Blatt R, Day YJ, et al. A1 adenosine receptor activation promotes angiogenesis and release of VEGF from monocytes. Circ Res. 2007;101:1130-1138. PMID: 17901362
16. Koszalka P, Özüyaman B, Huo Y, Zernecke A, Flögel U, Braun N, et al. Targeted disruption of cd73/ecto-5'-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ Res. 2004;95:814-821. PMID: 15358667
17. Koszałka P, Pryszlak A, Gołuńska M, Kolasa J, Stasiłojć G, Składanowski AC, Bigda JJ. Inhibition of CD73 stimulates the migration and invasion of B16F10 melanoma cells in vitro, but results in impaired angiogenesis and reduced melanoma growth in vivo. Oncol Rep. 2014;31:819-827. doi: 10.3892/or. 2013.2883 PMID: 24297662
18. Kelava T, Avar I, Čulo F. Biological actions of drug solvents. Period Biol. 2011;113:311-320.
19. Shibuya M. Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases. J Biochem. 2013;153:13-19. doi: 10.1093/jb/mvs136 PMID: 23172303
20. Barr MP, Bouchier-Hayes DJ, Harmey JJ. Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia. Int J Oncol. 2008;32:41-48. PMID: 18097541
21. Chen B, Longtine MS, Sadovsky Y, Nelson DM. Hypoxia downregulates p53 but induces apoptosis and enhances expression of BAD in cultures of human syncytiotrophoblasts. Am J Physiol Cell Physiol. 2010;299:C968-C976. doi: 10.1152/ajpcell.00154.2010 PMID: 20810912
22. Koizumi K, Tsutsumi Y, Yoshioka Y, Watanabe M, Okamoto T, Mukai Y, et al. Anti-angiogenic Effects of Dimethyl Sulfoxide on Endothelial Cells. Biol Pharm Bull. 2003;26:1295-1298. PMID: 12951474
23. Voronov E, Carmi Y, Apte RN. The role IL-1 in tumor-mediated angiogenesis. Front Physiol. 2014;5:114. doi: 10.3389/fphys.2014.00114 PMID: 24734023
24. Lázár-Molnár E, Hegyesi H, Tóth S, Falus A. Autocrine and paracrine regulation by cytokines and growth factors in melanoma. Cytokine. 2000;12:547-554. PMID: 10843728
25. Eljaszewicz A, Wiese M, Helmin-Basa A, Jankowski M, Gackowska L, Kubiszewska I, et al. Collaborating with the enemy: function of macrophages in the development of neoplastic disease. Mediators Inflamm. 2013;2013:1-11.
26. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13. doi: 10.12703/P6-13 PMID: 24669294
27. Gessi S, Merighi S, Sacchetto V, Simioni C, Borea PA. Adenosine receptors and cancer. Biochim Biophys Acta. 2011;1808:1400-1412. doi: 10.1016/j.bbamem.2010.09.020 PMID: 20888788
28. Fishman P, Bar-Yehuda S, Synowitz M, Powell JD, Klotz KN, Gessi S, Borea PA. Adenosine receptors and cancer. Handb Exp Pharmacol. 2009;193:399-341. doi: 10.1007/978-3-540-89615-9-14 PMID: 19639290
29. Merighi S, Mirandola P, Milani D, Varani K, Gessi S, Klotz KN, et al. Adenosine receptors as mediators of both cell proliferation and cell death of cultured human melanoma cells. J Invest Dermatol. 2002;119:923-933. PMID: 12406340
30. Lyons J, Bastian BC, McCormick F. MC1R and cAMP signaling inhibit cdc25B activity and delay cell cycle progression in melanoma cells. Proc Natl Acad Sci U S A. 2013;110:13845-13850. doi: 10. 1073/pnas.1201917110 PMID: 23908401
31. Nardin C, Fitzpatrick L, Zippin JH. Diverse effects of cAMP signaling in melanoma support the role of distinct cAMP microdomains in melanomagenesis, metastasis, and resistance to therapy. OA Dermatology. 2014;2:5.
32. Klinger M, Freissmuth M, Nanoff C. Adenosine receptors: G protein-mediated signalling and the role of accessory proteins. Cell Signal. 2002;14:99-108. PMID: 11781133
33. Koo N, Kim KM. Distinct effects on M2-type pyruvate kinase are involved in the dimethylsulfoxideinduced modulation of cellular proliferation and degranulation of mast cells. Arch Pharm Res. 2009;32:1637-1642. doi: 10.1007/s12272-009-2118-9 PMID: 20091279
34. Yu HN, Lee YR, Noh EM, Lee KS, Song EK, Han MK, et al. Tumor necrosis factor-alpha enhances DMSO-induced differentiation of HL-60 cells through the activation of ERK/MAPK pathway. Int J Hematol. 2008;87:189-194. doi: 10.1007/s12185-008-0037-z PMID: 18256785
35. Dewhirst MW, Richardson R, Cardenas-Navia I, Cao Y. The relationship between the tumor physiologic microenvironment and angiogenesis. Hematol Oncol Clin N Am. 2004;18:973-990.
36. Burghoff S, Gong X, Viethen C, Jacoby C, Flögel U, Bongardt S, et al. Growth and metastasis of B16-F10 melanoma cells is not critically dependent on host CD73 expression in mice. BMC Cancer. 2014;14:898. doi: 10.1186/1471-2407-14-898 PMID: 25465225
37. Eter N, Spitznas M. DMSO mimics inhibitory effect of thalidomide on choriocapillary endothelial cell proliferation in culture. Br J Ophthalmol. 2002;86:1303-1305. PMID: 12386094
38. Martin MJ, Hayward R, Viros A, Marais R. Metformin accelerates the growth of BRAF V600E-driven melanoma by upregulating VEGF-A. Cancer Discov. 2012;2:344-355. doi: 10.1158/2159-8290. CD-11-0280 PMID: 22576211
39. Choi SB, Park JB, Song TJ, Choi SY. Molecular mechanism of HIF-1-independent VEGF expression in a hepatocellular carcinoma cell line. Int J Mol Med. 2011;28:449-454. doi: 10.3892/ijmm.2011.719 PMID: 21667015
40. 2 receptors in retinal capillary endothelial cells. Invest Ophthalmol Vis Sci. 1996;37:1311-1321. PMID: 8641834
41. Rumjahn SM, Yokdang N, Baldwin KA, Thai J, Buxton IL. Purinergic regulation of vascular endothelial growth factor signaling in angiogenesis. Br J Cancer. 2009;100:1465-1470. doi: 10.1038/sj.bjc. 6604998 PMID: 19367276
42. 2A receptor stimulation increases angiogenesis by down-regulating production of the antiangiogenic matrix protein thrombospondin 1. Mol Pharmacol. 2005;67:1406-1413. PMID: 15673602
43. Leek RD, Landers RJ, Harris AL, Lewis CE. Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br J Cancer. 1999;79:991-995. PMID: 10070902
44. Lewis JS, Landers RJ, Underwood JC, Harris AL, Lewis CE. Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol. 2000;192:150-158. PMID: 11004690
45. Brennan JK, Lee KS, Frazel MA, Keng PC, Young DA. Interactions of dimethyl sulfoxide and granulocytemacrophage colony-stimulating factor on the cell cycle kinetics and phosphoproteins of G1-enriched HL-60 cells: evidence of early effects on lamin B phosphorylation. J Cell Physiol. 1991;146:425-434. PMID: 2022696
46. Deng R, Wang SM, Yin T, Ye TH, Shen GB, Li L, et al. Dimethyl Sulfoxide Suppresses Mouse 4T1 Breast Cancer Growth by Modulating Tumor-Associated Macrophage Differentiation. J Breast Cancer. 2014;17:25-32. doi: 10.4048/jbc.2014.17.1.25 PMID: 24744794
47. 2 a receptor stimulation prevents proteinuria in diabetic rats by promoting an anti-inflammatory phenotype without affecting oxidative stress. Acta Physiol (Oxf). 2015;214:311-318.
48. 3 receptor agonist, N6-(3-iodobenzyl)-adenosine-5'-N-methyluronamide, is protective in two murine models of colitis. Eur J Pharmacol. 2003;466:323-329. PMID: 12694816
49. Cassetta L, Cassol E, Poli G. Macrophage polarization in health and disease. ScientificWorldJournal. 2011;11:2391-2402. doi: 10.1100/2011/213962 PMID: 22194670
50. 2B receptors. FASEB J. 2012;26:376-386. doi: 10.1096/fj. 11-190934 PMID: 21926236
51. Haskó G, Pacher P. Regulation of Macrophage Function by Adenosine. Arterioscler Thromb Vasc Biol. 2012;32:865-869. doi: 10.1161/ATVBAHA.111.226852 PMID: 22423038
52. Stagg J. The double-edge sword effect of anti-CD73 cancer therapy. Oncoimmunology. 2012;1:217-218. PMID: 22720247