An emerging role for adenosine and its receptors in bone homeostasis

Frontiers in Endocrinology

Volumn 3, Issue SEP, 2012, Pages

  Ham, Jack ^a   Evans, Bronwen A J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Adenosine; Adenosine receptors; Bone; Mesenchymal stem cells; Osteoblasts; Osteoclasts

Indexed keywords

EID: 84874374156     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2012.00113     Document Type: Review

References (82)

1. Bar-Yehuda, S., Rath-Wolfson, L., Del Valle, L., Ochaion, A., Cohen, S., Patoka, R., Zozulya, G., Barer, F., Atar, E., Pina-Oviedo, S., Perez-Liz, G., Castel, D., and Fishman, P. (2009). Induction of an anti-inflammatory effect and prevention of cartilage damage in rat knee osteoarthritis by CF101 treatment. Arthritis Rheum. 60,3061-3071.
2. Bianchi, V., and Spychala, J. (2003). Mammalian 5'-nucleotidases. J. Biol. Chem. 278,46195-46198.
3. Blackburn, M. R. (2003). Too much of a good thing: adenosine overload in adenosine-deaminase-deficientmice. Trends Pharmacol. Sci. 24, 66-70.
4. Boison, D. (2011). Modulators of nucleoside metabolism in the therapy of brain diseases. Curr. Top. Med. Chem. 11, 1068-1086.
5. Boyle, D. L., Kowaluk, E. A., Jarvis, M. F., Lee, C. H., Bhagwat, S. S., Williams, M., and Firestein, G. S. (2001). Anti-inflammatory effects of ABT-702, a novel non-nucleoside adenosine kinase inhibitor, in rat adjuvant arthritis. J. Pharmacol Exp. Ther. 296, 495-500.
6. Burnstock, G. (2011). Introductory overview to purinergic signalling. Front. Biosci. 3, 896-900.
7. Carroll, S. H., Wigner, N. A., Kulkarni, N., Johnston-Cox, H., Gerstenfeld, L. C., and Ravid, K. (2012). A2B adenosine receptor promotes mes-enchymal stem cell differentiation to osteoblasts and bone formation in vivo. J. Biol. Chem. 287, 15718-15727.
8. Chan, E. S., and Cronstein, B. N. (2010). Methotrexate - how does it really work? Nat. Rev. Rheumatol. 6, 175-178.
9. Chieng, B., and Bekkers, J. M. (2001). Inhibition of calcium channels by opioid- and adenosine-receptor agonists in neurons of the nucleus accumbens. Br. J. Pharmacol. 133, 337-344.
10. Collis, M. G., and Hourani, S. M. (1993). Adenosine receptor subtypes. Trends Pharmacol. Sci. 14, 360-366.
11. Costa, M. A., Barbosa, A., Neto, E., Sá-e-Sousa, A., Freitas, R., Neves, J. M., Magalhães-Cardoso, T., Ferreirinha, F., and Correia-de-Sá, P. (2011). On the role of subtype selective adenosine receptor agonists during proliferation and osteogenic differentiation of human primary bone marrow stro-mal cells. J. Cell. Physiol. 226, 1353-1366.
12. Di Lorio, P., Battaglia, G., Ciccarelli, R., Ballerini, P., Giuliani, P., Poli, A., Nicoletti, F., and Caciagli, E (1996). Interaction between A1 adenosine and class II metabotropic gluta-mate receptors in the regulation of purine and glutamate release from rat hippocampal slices. J. Neurochem. 67, 302-309.
13. Eltzschig, H. K., Ibla, J. C., Furuta, G. T., Leonard, M. O., Jacobson, K. A., Enjyoji, K., Robson, S. C., and Colgan, S. P. (2003). Coordinated adenine nucleotide phospho-hydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2b receptors. J. Exp. Med. 198, 783-796.
14. Evans, B. A. J., Elford, C., Pexa, A., Francis, K., Hughes, A. C., Deussen, A., and Ham, J. (2006). Human osteoblast precursors produce extracellular adenosine, which modulates their secretion of IL-6 and osteo-protegerin. J. Bone Miner. Res. 21, 228-236.
15. Fatokun, A. A., Stone, T. W., and Smith, R. A. (2006). Hydrogen peroxide-induced oxidative stress in MC3T3-E1 cells: the effects of glutamate and protection by purines. Bone 39, 542-551.
16. Ferre, S., Popoli, P., Rimondini, R., Reggio, R., Kehr, J., and Fuxe, K. (1999). Adenosine A2A and group I metabotropic glutamate receptors synergistically modulate the binding characteristics of dopamine D2 receptors in the rat striatum. Neu-ropharmacology 38, 129-140.
17. Fredholm, B. B. (2003). Adenosine receptors as targets for drug development. Drug News Perspect. 16, 283-289.
18. Fredholm, B. B. (2010). Adenosine receptors as drug targets. Exp. Cell Res. 316, 1284-1288.
19. Fredholm, B. B., Ijzerman, A. P., Jacob-son, K. A., Klotz, K.-N., and Linden, J. (2001). International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53, 527-552.
20. Fredholm, B. B., Ijzerman, A. P., Jacob-son, K. A., Klotz, K.-N., and Linden, J. (2011). International Union of Pharmacology. LXXX1. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 63, 1-34.
21. Fuxe, K., Ferre, S., Genedani, S., Franco, R., and Agnati, L. F. (2007). Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function. Physiol. Behav. 92, 210-217.
22. Gartland, A., Orriss, I. R., Rumney, R. M., Bond, A. P., Arnett, T., and Gallagher, J. A. (2012). Purinergic signalling in osteoblasts. Front. Biosci. 17,16-29.
23. Gharibi, B., Abraham, A. A., Ham, J., and Evans, B. A. J. (2011a). Adenosine receptor subtype expression and activation influence the differentiation of mesenchymal stem cells to osteoblasts and adipocytes. J. Bone Miner. Res. 26,2112-2124.
24. Gharibi, B., Abraham, A. A., Ham, J., and Evans, B. A. J. (2011b). Contrasting effects of A1 and A2b adenosine receptors on adipogenesis. Int. J. Obes. 36, 397-406.
25. Hasko, G., Pacher, P., Vizi, E. S., and Illes, P. (2005). Adenosine receptor signaling in the brain immune system. Trends Pharmacol. Sci. 26, 511-516.
26. He, W., and Cronstein, B. N. (2012). Adenosine A(1) receptor regulates osteoclast formation by altering TRAF6/TAK1 signaling. Purinergic Signal. 8, 327-337.
27. Hoebertz, A., Arnett, T. R., and Burn-stock, G. (2003). Regulation of bone resorption and formation by purines and pyrimidines. Trends Pharmacol. Sci. 24,290-297.
28. Hong, R. (1989). Associations of the skeletal and immune systems. Am. J. Med. Genet. 34, 55-59.
29. Huang, L.-F., Guo, F.-Q., Liang, Y.-Z., Li, B.-Y., and Cheng, B.-M. (2004). Simple and rapid determination of adenosine in human syn-ovial fluid with high performance liquid chromatography-mass spec-trometry. J. Pharm. Biomed. 36, 877-882.
30. Hunsucker, S. A., Mitchell, B. S., and Spychala, J. (2005). The 5;-nucleotidases as regulators of nucleotide and drug metabolism. Pharmacol. Ther. 107, 1-30.
31. Jacobson, K. A., and Gao, Z. G. (2006). Adenosine receptors as therapeutic targets. Nat. Rev. Drug Discov. 5, 247-264.
32. Jeyabalan, J., Shah, M., Viollet, B., and Chenu, C. (2012). AMP-activated protein kinase pathway and bone metabolism. J. Endocrinol. 212, 277-290.
33. Kanazawa, I., Yamaguchi, T., Yano, S., Yamauchi, M., and Sugimoto, T. (2008). Metformin enhances MC3T3-E1 cells via AMP kinase as well as eNOS and BMP-2 expression. Biochem. Biophys. Res. Commun. 375, 414-419.
34. Kara, F. M., Chitu, V., Sloane, J., Axel-rod, M., Fredholm, B. B., Stanley, E. R., and Cronstein, B. N. (2010a). Adenosine A1 receptors (A1Rs) play a critical role in osteoclast formation and function. FASEB J. 24, 2325-2333.
35. Kara, F. M., Doty, S. B., Boskey, A., Goldring, S., Zaidi, M., Fredholm, B. B., and Cronstein, B. N. (2010b). Adenosine A(1) receptors regulate bone resorption in mice: adenosine A(1) receptor blockade or deletion increases bone density and prevents ovariectomy-induced bone loss in adenosine A(1) receptor-knockout mice. Arthritis Rheum. 62, 534-541.
36. Katebi, M., Soleimani, M., and Cronstein, B. N. (2009). Adenosine A2A receptors play an active role in mouse bone marrow-derived mesenchymal stem cell development. J. Leukoc. Biol. 85, 438-444. Erratum in: J. Leukoc. Biol. 2011; 89, 1009.
37. Kim, D. S., and Palmiter, R. D. (2008). Interaction of dopamine and adenosine receptor function in behavior: studies with dopamine-deficient mice. Front. Biosci. 13, 2311-2318.
38. Kudlacek, O., Just, H., Korkhov, V M., Vartian, N., Klinger, M., Pankevych, H., Yang, Q., Nanoff, C., Freissmuth, M., and Boehm, S. (2003). The human D2 dopamine receptor synergizes with the A2A adenosine receptor to stimulate adenylyl cyclase in PC 12 cells. Neuropsychopharmacology 28, 1317-1327.
39. Latini, S., Bordini, F., Pedata, F., and Corradetti, R. (1999). Extracellular adenosine concentrations during in vitro ischemia in rat hippocampal slices. Br. J. Pharmacol. 126, 729-739.
40. Lee, J. E., Cornell, K. A., Riscoe, M. K., and Howell, P. L. (2001). Structure of E. coli 5;-methylthioadenosine/ S-adenosylhomocysteine nucleosi-dase reveals similarity to the purine nucleoside phosphorylases. Structure 9,941-953.
41. Lee, Y. S., Kim, Y. S., Lee, S. Y., Kim, G. H., Kim, B. J., Lee, S. H., Lee, K. U., Kim, G. S., Kim, S. W., and Koh, J. M. (2010). AMP kinase acts as a negative regulator of RANKL in the differentiation of osteoclasts. Bone 47, 926-937.
42. Lewis, B. M., Pexa, A., Francis, K., Verma, V., McNicol, A. M., Scan-lon, M., Deussen, A., Evans, W. H., Rees, D. A., and Ham, J. (2006). Adenosine stimulates con-nexin 43 expression and gap junc-tional communication in pituitary folliculostellate cells. FASEB J. 20, 2585-2587.
43. Lloyd, H. G., and Fredholm, B. B. (1995). Involvement of adenosine deaminase and adenosine kinase in regulating extracellular adenosine concentration in rat hippocampal slices. Neurochem. Int. 26, 387-395.
44. Mackenzie, N. C., Zhu, D., Milne, E. M., van't Hof, R., Martin, A., Quarles, D. L., Millán, J. L., Far-quharson, C., and MacRae, V E. (2012). Altered bone development and an increase in FGF-23 expression in Enppl~/~ mice. PLoS ONE 7, e32177. doi: 10.1371/journal.pone. 0032177
45. Mazzon, E., Esposito, E., Impel-lizzeri, D., Di Paola, R., Melani, A., Bramanti, P., Pedata, F., and Cuzzocrea, S. (2011). CGS 21680, an agonist of the adenosine (A2a) receptor, reduces progression of murine type II collagen-induced arthritis. J. Rheumatol. 38, 2119-2129.
46. McCool, B. A., and Farroni, J. S. (2001). A1 adenosine receptors inhibit multiple voltage-gated Ca2+ channel subtypes in acutely isolated rat basolateral amygdala neurons. Br. J. Pharmacol. 132, 879-888.
47. Mediero, A., Kara, F. M., Wilder, T., and Cronstein, B. N. (2012a). Adenosine A(2A) receptor ligation inhibits osteoclast formation. Am. J. Pathol. 180,775-786.
48. Mediero, A., Frenkel, S. R., Wilder, T., He, W., Mazumder, A., and Cronstein, B. N. (2012b). Adenosine A2A receptor activation prevents wear particle-induced osteolysis. Sci. Transl. Med. 4, 135-165.
49. Mei, Y. A., Le Foll, F., Vaudry, H., and Cazin, L. (1996). Adenosine inhibits L- and N-type calcium channels in pituitary melanotrophs. Evidence for the involvement of a G protein in calcium channel gating. J. Neuroen-docrinol. 8, 85-91.
50. Merrill, J. T., Shen, C., Schreib-man, D., Coffey, D., Zakharenko, O., Fisher, R., Lahita, R. G., Salmon, J., and Cronstein, B. N. (1997). Adenosine A1 receptor promotion of multinucleated giant cell formation by human mono-cytes: amechanism for methotrexate-induced nodulosis in rheumatoid arthritis. Arthritis Rheum. 40, 1308-1315.
51. Montesinos, M. C., Yap, Y. S., Desai, A., Posadas, I., McCrary, C. T., and Cronstein, B. N. (2000). Reversal of the anti-inflammatory effects of methotrexate by the non-selective adenosine receptor antagonists and caffeine: evidence that the anti-inflammatory effects of methotrexate are mediated via multiple adenosine receptors in rat adjuvant arthritis. Arthritis Rheum. 43, 656-663.
52. Muller, C. E., and Jacobson, K. A. (2011). Recent developments in adenosine receptor ligands and their potential as novel drugs. Biochim. Biophys. Acta 1808, 1290-1308.
53. Ochaion, A., Bar-Yehuda, S., Cohen, S., Del Valle, L., Perez-Liz, G., Madi, L., Barer, F., Farbstein, M., Fishman-Furman, S., Reitblat, T., Amital, H., Levi, Y., Molad, Y., Mader, R., Tish-ler, M., Langevitz, P., Zabutti, A., and Fishman, P. (2006). Methotrex-ate enhances the anti-inflammatory effect of CF101 via up-regulation of the A3 adenosine receptor expression. Arthritis Res. Ther. 8,R169.
54. Olah, M. E., and Stiles, G. L. (1995). Adenosine receptor subtypes: characterization and therapeutic regulation. Annu. Rev. Pharmacol. 35, 581-606.
55. Olah, M. E., and Stiles, G. L. (2000). The role of receptor structure in determining adenosine receptor activity. Pharmacol. Ther. 85, 55-75.
56. Paisansathan, C., Xu, H., Vetri, E, Hernandez, M., and Pelli-grino, D. A. (2010). Interactions between adenosine and K+ channel-related pathways in the coupling of somatosensory activation and pial arteriolar dilation. Am. J. Physiol. Heart Circ. Physiol. 299, H2009-H2017.
57. Pak, M. A., Haas, H. L., Decking, U. K., and Schrader, J. (1994). Inhibition of adenosine kinase increases endogenous adenosine and depresses neuronal activity in hippocam-pal slices. Neuropharmacology 33, 1049-1053.
58. Pedata, F., Pugliese, A. M., Coppi, E., Popoli, P., Morelli, M., Schwarzschild, M. A., and Melani, A. (2007). Adenosine in the central nervous system: effects on neurotransmis-sion and neuroprotection. Immunol. Endocr. Metab. Agents Med. Chem. 7, 304-321.
59. Pellegatti, P., Falzoni, S., Donvito, G., Lemaire, I., and Di Virgilio, E (2011). P2X7 receptor drives osteoclast fusion by increasing the extracellular adenosine concentration. FASEBJ. 25, 1264-1274.
60. Picher, M., Burch, L. H., Hirsh, A. J., Spychala, J., and Boucher, R. C. (2003). Ecto 5'-nucleotidase and nonspecific alkaline phosphatase two AMP-hydrolyzing ectoenzymes with distinct roles in human airways. J. Biol. Chem. 278, 13468-13479.
61. Quinn, J. M., Tam, S., Sims, N. A., Saleh, H., McGregor, N. E., Poulton, I. J., Scott, J. W., Gillespie, M. T., Kemp, B. E., and van Denderen, B. J. (2010). Germline deletion of AMP-activated protein kinase beta subunits reduces bone mass without altering osteoclast differentiation or function. FASEB. J. 24, 275-285.
62. Ralph, J. A., McEvoy, A. N., Kane, D., Bresnihan, B., FitzGerald, O., and Murphy, E. P. (2005). Modulation of orphan nuclear receptor NURR1 expression by methotrexate in human inflammatoryjoint disease involves adenosine A2a receptor-mediated responses. J. Immunol. 175, 555-565.
63. Rath-Wolfson, L., Bar-Yehuda, S., Madi, L., Ochaion, A., Cohen, S., Zabutti, A., and Fishman, P. (2006). IB-MECA, an A3 adenosine receptor agonist prevents bone resorp-tion in rats with adjuvant induced arthritis. Clin. Exp. Rheumatol. 24, 400-406.
64. Reyes, J. P., Sims, S. M., and Dixon, S. J. (2011). P2 receptor expression, signaling and function in osteoclasts. Front. Biosci. (Schol. Ed.) 3, 1101-1118.
65. Robson, S. C. (2011). Role of CD73 and extracellular adenosine in disease: presented by Maria P. Abbrac-chio. Purinergic Signal. 7, 367-372.
66. Sala-Newby, G. B., Skladanowski, A. C., and Newby, A. C. (1999). The mechanism of adenosine formation in cells cloning of cytosolic 5'-nucleotidase-1. J. Biol. Chem. 274, 17789-17793.
67. Sauer, A. V., Mrak, E., Hernandez, R. J., Zacchi, E., Cavani, E, Casiraghi, M., Grunebaum, E., Roifman, C. M., Cervi, M. C., Ambrosi, A., Carlucci, F., Roncar-olo, M. G., Villa, A., Rubinacci, A., and Aiuti, A. (2009). ADA-deficient SCID is associated with specific microenvironment and bone pheno-type characterized by RANKL/OPG imbalance and osteoblast insufficiency. Blood 114, 3216-3226.
68. Shah, M., Kola, B., Bataveljic, A., Arnett, T. R., Viollet, B., Saxon, L., Korbonits, M., and Chenu, C. (2010). AMP-activated protein kinase (AMPK) activation regulates in vitro bone formation and bone mass. Bone 47, 309-319.
69. Shimegi, S. (1996). ATP and adenosine act as a mitogen for osteoblast-like cells (MC3T3-E1). Calcif. Tissue Int. 58,109-113.
70. Shimegi, S. (1998). Mitogenic action of adenosine on osteoblast-like cells, MC3T3-E1. Calcif. Tissue Int. 62, 418-425.
71. Sottofattori, E., Anzaldi, M., and Ottonello, L. (2001). HPLC determination of adenosine in human syn-ovial fluid. J. Pharm. Biomed. Anal. 24,1143-1146.
72. Spychala, J. (2000). Tumor promoting functions of adenosine. Pharmacol. Ther. 87, 161-173.
73. Spychala, J., Datta, N. S., Takabayashi, K., Datta, M., Fox, I. H., Gribbin, T., and Mitchell, B. S. (1996). Cloning of human adenosine kinase cDNA: sequence similarity to micro-bial ribokinases and fructokinases. Proc. Natl. Acad. Sci. U.S.A. 93, 1232-1237.
74. St. Hilaire, C., Ziegler, S. G., Markello, T. C., Brusco, A., Groden, C., Gill, E, Carlson-Donohoe, H., Leder-man, R. J., Chen, M. Y., Yang, D., Siegenthaler, M. P., Arduino, C., Mancini, C., Freudenthal, B., Stanescu, H. C., Zdebik, A. A., Cha-ganti, R. K., Nussbaum, R. L., Kleta, R., Gahl, W. A., and Boehm, M. (2011). NT5E mutations and arterial calcification. N. Engl. J. Med. 364, 432-442.
75. Synder, E E, and Lukey, T. (1982). Kinetic considerations for the regulation of adenosine and deoxyadeno-sine metabolism in mouse and human tissues based on a thymocyte model. Biochim. Biophys. Acta 696, 299-307.
76. Takedachi, M., Oohara, H., Smith, B. J., Iyama, M., Kobashi, M., Maeda, K., Long, C. L., Humphrey, M. B., Stoecker, B. J., Toyosawa, S., Thompson, L. F., and Murakami, S. (2012). CD73-generated adenosine promotes osteoblast differentiation. J. Cell. Physiol. 227, 2622-2631.
77. Teramachi, J., Kukita, A., Li, Y J., Ushijima, Y., Ohkuma, H., Wada, N., Watanabe, T., Nakamura, S., and Kukita, T. (2011). Adenosine abolishes MTX-induced suppression of osteoclastogenesis and inflammatory bone destruction in adjuvant-induced arthritis. Lab. Invest. 91, 719-731.
78. Uehara, R., Suzuki, Y., and Ichikawa, Y. (2001). Methotrexate (MTX) inhibits osteoblastic differentiation in vitro: possible mechanism of MTX osteopathy. J. Rheumatol. 28, 251-256.
79. Van Belle, H., Goosens, F., andWynants, J. (1987). Formation and release of purine catabolites during hypoper-fusion, anoxia and ischemia. Am. J. Physiol. 252, H886-H893.
80. Wolos, J. A., Frondorf, K. A., and Esser, R. E. (1993). Immunosuppres-sion mediated by the inhibitor of S-adenosyl-L-homocysteine hydro-lase. Prevention and treatment of collagen-induced arthritis. J. Immunol. 151,526-534.
81. Yaar, R., Jones, M. R., Chen, J. F., and Ravid, K. (2005). Animal models for the study of adenosine receptor function. J. Cell. Physiol. 202, 9-20.
82. Yang, D., Zhang, Y., Nguyen, H. G., Koupenova, M., Chauhan, A. K., Makitalo, M., Jones, M. R., St. Hilaire, C., Seldin, D. C., Toselli, P., Lam-perti, E., Schreiber, B. M., Gavras, H., Wagner, D. D., and Ravid, K. (2006). The A2B adenosine receptor protects against inflammation and excessive vascular adhesion.J. Clin. Invest. 116, 1913-1923.