Direct or indirect stimulation of adenosine A2Areceptors enhances bone regeneration as well as bone morphogenetic protein-2

FASEB Journal

Volumn 29, Issue 4, 2015, Pages 1577-1590

  Mediero, Aránzazu ^a   Wilder, Tuere ^a   Perez Aso, Miguel ^a   Cronstein, Bruce N ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bone formation; CGS21680; Dipyridamole; Osteoblast; Osteoclast

Indexed keywords

2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); ADENOSINE; ADENOSINE A2A RECEPTOR; BONE MORPHOGENETIC PROTEIN 2; DIPYRIDAMOLE; 2-(4-(2-CARBOXYETHYL)PHENETHYLAMINO)-5'-N-ETHYLCARBOXAMIDOADENOSINE; ADENOSINE A2 RECEPTOR AGONIST; BMP2 PROTEIN, MOUSE; PHENETHYLAMINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEFECT; BONE REGENERATION; CONTROLLED STUDY; EC50; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WILD TYPE; WOUND HEALING; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL COUNT; CYTOLOGY; DRUG EFFECTS; FEMALE; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALIA;

ADENOSINE; ADENOSINE A2 RECEPTOR AGONISTS; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL COUNT; DIPYRIDAMOLE; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOCLASTS; PHENETHYLAMINES; RECEPTOR, ADENOSINE A2A;

EID: 84926654729     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-265066     Document Type: Article

References (54)

1. Schindeler, A., McDonald, M. M., Bokko, P., and Little, D. G. (2008) Bone remodeling during fracture repair: The cellular picture. Semin. Cell Dev. Biol. 19, 459-466
2. Tsiridis, E., Upadhyay, N., and Giannoudis, P. (2007) Molecular aspects of fracture healing: which are the important molecules? Injury 38(Suppl 1), S11-S25
3. Pape, H. C., Marcucio, R., Humphrey, C., Colnot, C., Knobe, M., and Harvey, E. J. (2010) Trauma-induced inflammation and fracture healing. J. Orthop. Trauma 24, 522-525
4. Riley, E. H., Lane, J. M., Urist, M. R., Lyons, K. M., and Lieberman, J. R. (1996) Bone morphogenetic protein-2: biology and applications. Clin. Orthop. Relat. Res. (324):39-46
5. Boden, S. D., Kang, J., Sandhu, H., and Heller, J. G. (2002) Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies. Spine 27, 2662-2673
6. Onishi, T., Ishidou, Y., Nagamine, T., Yone, K., Imamura, T., Kato, M., Sampath, T. K., ten Dijke, P., and Sakou, T. (1998) Distinct and overlapping patterns of localization of bone morphogenetic protein (BMP) family members and a BMP type II receptor during fracture healing in rats. Bone 22, 605-612
7. den Boer, F. C., Wippermann, B. W., Blokhuis, T. J., Patka, P., Bakker, F. C., and Haarman, H. J. (2003) Healing of segmental bone defects with granular porous hydroxyapatite augmented with recombinant human osteogenic protein-1 or autologous bone marrow. J. Orthopaedic Res. 21, 521-528
8. Cook, S. D., Salkeld, S. L., Patron, L. P., Sargent, M. C., and Rueger, D. C. (2002) Healing course of primate ulna segmental defects treated with osteogenic protein-1. J. Invest. Surg. 5, 69-79
9. White, A. P., Vaccaro, A. R., Hall, J. A., Whang, P. G., Friel, B. C., and McKee, M. D. (2007) Clinical applications of BMP-7/OP-1 in fractures, nonunions and spinal fusion. Int. Orthop. 31, 735-741
10. Glassman, S. D., Howard, J., Dimar, J., Sweet, A., Wilson, G., and Carreon, L. (2011) Complications with recombinant human bone morphogenic protein-2 in posterolateral spine fusion: a consecutive series of 1037 cases. Spine 36, 1849-1854
11. Carragee, E. J., Hurwitz, E. L., and Weiner, B. K. (2011) A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned. Spine J. 11, 471-491
12. Spiro, A. S., Beil, F. T., Baranowsky, A., Barvencik, F., Schilling, A. F., Nguyen, K., Khadem, S., Seitz, S., Rueger, J. M., Schinke, T., and Amling, M. (2010) BMP-7-induced ectopic bone formation and fracture healing is impaired by systemic NSAID application in C57BL/6-mice. J. Orthopaedic Res. 28, 785-791
13. Fredholm, B. B., IJzerman, A. P., Jacobson, K. A., Linden, J., and Müller, C. E. (2011) International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors - an update. Pharmacol. Rev. 63, 1-34
14. He, W., and Cronstein, B. N. (2012) Adenosine A1 receptor regulates osteoclast formation by altering TRAF6/TAK1 signaling. Purinergic Signal. 8, 327-337
15. Kara, F. M., Chitu, V., Sloane, J., Axelrod, M., Fredholm, B. B., Stanley, E. R., and Cronstein, B. N. (2010) Adenosine A1 receptors (A1Rs) play a critical role in osteoclast formation and function. FASEB J. 24, 2325-2333
16. Kara, F. M., Doty, S. B., Boskey, A., Goldring, S., Zaidi, M., Fredholm, B. B., and Cronstein, B. N. (2010) 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
17. Mediero, A., Kara, F. M., Wilder, T., and Cronstein, B. N. (2012) Adenosine A(2A) receptor ligation inhibits osteoclast formation. Am J Pathol. 180, 775-786
18. Mediero, A., Frenkel, S. R., Wilder, T., He, W., Mazumder, A., and Cronstein, B. N. (2012) Adenosine A2A receptor activation prevents wear particle-induced osteolysis. Sci. Transl. Med. 4, 135ra165.
19. Mediero, A., and Cronstein, B. N. (2013) Adenosine and bone metabolism. Trends Endocrinol. Metab. 24, 290-300
20. 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 stromal cells. J. Cell. Physiol. 226, 1353-1366
21. He, W., Mazumder, A., Wilder, T., and Cronstein, B. N. (2013) Adenosine regulates bone metabolism via A1, A2A, and A2B receptors in bone marrow cells from normal humans and patients with multiple myeloma. FASEB J. 27, 3446-3454
22. Gharibi, B., Abraham, A. A., Ham, J., and Evans, B. A. (2011) Adenosine receptor subtype expression and activation influence the differentiation of mesenchymal stem cells to osteoblasts and adipocytes. J. Bone Mineral Res. 26, 2112-2124
23. Mediero, A., Perez-Aso, M., Wilder, T., and Cronstein, B. N. (2014) Methotrexate prevents wear particle-induced inflammatory osteolysis via activation of the adenosine A2A receptor [Epub ahead of print]. Arthritis Rheumatol. 10.1002/art.38971
24. Cooper, G. M., Mooney, M. P., Gosain, A. K., Campbell, P. G., Losee, J. E., and Huard, J. (2010) Testing the critical size in calvarial bone defects: revisiting the concept of a critical-size defect. Plast. Reconstr. Surg. 125, 1685-1692
25. Montesinos, M. C., Desai, A., and Cronstein, B. N. (2006) Suppression of inflammation by low-dose methotrexate is mediated by adenosine A2A receptor but not A3 receptor activation in thioglycollate-induced peritonitis. Arthritis Res. Ther. 8, R53
26. Lassailly, F., Griessinger, E., and Bonnet, D. (2010) "Microenvironmental contaminations" induced by fluorescent lipophilic dyes used for noninvasive in vitro and in vivo cell tracking. Blood 115, 5347-5354
27. Van Gaalen, S. M., Kruyt, M. C., Geuze, R. E., de Bruijn, J. D., Alblas, J., and Dhert, W. J. (2010) Use of fluorochrome labels in in vivo bone tissue engineering research. Tissue Eng. Part B Rev. 16, 209-217
28. Harmatys, K. M., Cole, E. L., and Smith, B. D. (2013) In vivo imaging of bone using a deep-red fluorescent molecular probe bearing multiple iminodiacetate groups. Mol. Pharm. 10, 4263-4271
29. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
30. Mediero, A., Kara, F. M., Wilder, T., and Cronstein, B. N. (2012) Adenosine A(2A) receptor ligation inhibits osteoclast formation. Am. J. Pathol. 180, 775-786
31. Schmitz, J. P., and Hollinger, J. O. (1986) The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin. Orthop. Relat. Res. (205):299-308
32. Carroll, S. H., Wigner, N. A., Kulkarni, N., Johnston-Cox, H., Gerstenfeld, L. C., and Ravid, K. (2012) A2B adenosine receptor promotes mesenchymal stem cell differentiation to osteoblasts and bone formation in vivo. J. Biol. Chem. 287, 15718-15727
33. Evans, B. A., 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 osteoprotegerin. J. Bone Mineral Res. 21, 228-236
34. 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
35. Gharibi, B., Abraham, A. A., Ham, J., and Evans, B. A. (2012) Contrasting effects of A1 and A2b adenosine receptors on adipogenesis. Int J Obes (Lond) 36, 397-406
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
37. De Mattei, M., Caruso, A., Traina, G. C., Pezzetti, F., Baroni, T., and Sollazzo, V. (1999) Correlation between pulsed electromagnetic fields exposure time and cell proliferation increase in human osteosarcoma cell lines and human normal osteoblast cells in vitro. Bioelectromagnetics 20, 177-182
38. Mediero, A., Perez-Aso, M., and Cronstein, B. N. (2013) Activation of adenosine A(2A) receptor reduces osteoclast formation via PKA- and ERK1/2-mediated suppression of NFκB nuclear translocation. Br. J. Pharmacol. 169, 1372-1388
39. Chan, E. S., and Cronstein, B. N. (2010) Methotrexate - how does it really work? Nat Rev Rheumatol 6, 175-178
40. Chaudary, N., Naydenova, Z., Shuralyova, I., and Coe, I. R. (2004) Hypoxia regulates the adenosine transporter, mENT1, in the murine cardiomyocyte cell line, HL-1. Cardiovasc. Res. 61, 780-788
41. Eltzschig, H. K., Abdulla, P., Hoffman, E., Hamilton, K. E., Daniels, D., Schönfeld, C., Löffler, M., Reyes, G., Duszenko, M., Karhausen, J., Robinson, A., Westerman, K. A., Coe, I. R., and Colgan, S. P. (2005) HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J. Exp. Med. 202, 1493-1505
42. Morote-Garcia, J. C., Rosenberger, P., Nivillac, N. M., Coe, I. R., and Eltzschig, H. K. (2009) Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136, 607-618
43. Pennycooke, M., Chaudary, N., Shuralyova, I., Zhang, Y., and Coe, I. R. (2001) Differential expression of human nucleoside transporters in normal and tumor tissue. Biochem. Biophys. Res. Commun. 280, 951-959
44. Li, H., Smolen, G. A., Beers, L. F., Xia, L., Gerald, W., Wang, J., Haber, D. A., and Lee, S. B. (2008) Adenosine transporter ENT4 is a direct target of EWS/WT1 translocation product and is highly expressed in desmoplastic small round cell tumor. PLoS ONE 3, e2353
45. Utting, J. C., Robins, S. P., Brandao-Burch, A., Orriss, I. R., Behar, J., and Arnett, T. R. (2006) Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp. Cell Res. 312, 1693-1702
46. Knowles, H. J., Cleton-Jansen, A. M., Korsching, E., and Athanasou, N. A. (2010) Hypoxia-inducible factor regulates osteoclast-mediated bone resorption: role of angiopoietin-like 4. FASEB J. 24, 4648-4659
47. Frey, J. L., Stonko, D. P., Faugere, M.-C., and Riddle, R. C. (2014) Hypoxia-inducible factor-1a restricts the anabolic actions of parathyroid hormone. Bone Res. 2, 14005
48. Khoa, N. D., Postow, M., Danielsson, J., and Cronstein, B. N. (2006) Tumor necrosis factor-alpha prevents desensitization of Galphas-coupled receptors by regulating GRK2 association with the plasma membrane. Mol. Pharmacol. 69, 1311-1319
49. Khoa, N. D., Montesinos, M. C., Reiss, A. B., Delano, D., Awadallah, N., and Cronstein, B. N. (2001) Inflammatory cytokines regulate function and expression of adenosine A(2A) receptors in human monocytic THP-1 cells. J. Immunol. 167, 4026-4032
50. Yang, Z., Day, Y. J., Toufektsian, M. C., Ramos, S. I., Marshall, M., Wang, X. Q., French, B. A., and Linden, J. (2005) Infarct-sparing effect of A2A-adenosine receptor activation is due primarily to its action on lymphocytes. Circulation 111, 2190-2197
51. Yang, Z., Day, Y. J., Toufektsian, M. C., Xu, Y., Ramos, S. I., Marshall, M. A., French, B. A., and Linden, J. (2006) Myocardial infarct-sparing effect of adenosine A2A receptor activation is due to its action on CD4+ T lymphocytes. Circulation 114, 2056-2064
52. Cerqueira, M. D. (2004) The future of pharmacologic stress: selective A2A adenosine receptor agonists. Am. J. Cardiol. 94, 33D-40D
53. Lam, J. Y., Chaitman, B. R., Glaenzer, M., Byers, S., Fite, J., Shah, Y., Goodgold, H., and Samuels, L. (1988) Safety and diagnostic accuracy of dipyridamole-thallium imaging in the elderly. J. Am. Coll. Cardiol. 11, 585-589
54. Lette, J., Tatum, J. L., Fraser, S., Miller, D. D., Waters, D. D., Heller, G., Stanton, E. B., Bom, H. S., Leppo, J., and Nattel, S. (1995) Safety of dipyridamole testing in 73,806 patients: the Multicenter Dipyridamole Safety Study. J. Nuclear Cardiol. 2, 3-17