Pulsed Electromagnetic Fields Increased the Anti-Inflammatory Effect of A2A and A3 Adenosine Receptors in Human T/C-28a2 Chondrocytes and hFOB 1.19 Osteoblasts

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Vincenzi, Fabrizio ^a   Targa, Martina ^a   Corciulo, Carmen ^a   Gessi, Stefania ^a   Merighi, Stefania ^a   Setti, Stefania ^b   Cadossi, Ruggero ^b   Goldring, Mary B ^c   Borea, Pier Andrea ^a   Varani, Katia ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b Igea Biophysics Laboratory   (Italy)

^c HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR AGONIST; ADENOSINE A3 RECEPTOR; ADENOSINE A3 RECEPTOR AGONIST; CYCLIC AMP; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; OSTEOPROTEGERIN; PROSTAGLANDIN E2; VASCULOTROPIN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CARTILAGE CELL; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTROMAGNETIC FIELD; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; OSTEOBLAST; PROTEIN EXPRESSION; PROTEIN SECRETION; RECEPTOR UPREGULATION; RNA ANALYSIS; UPREGULATION;

ADENOSINE A2 RECEPTOR AGONISTS; ADENOSINE A3 RECEPTOR AGONISTS; CELL LINE; CELL PROLIFERATION; CHONDROCYTES; CYCLIC AMP; ELECTROMAGNETIC FIELDS; ENZYME ACTIVATION; GENE EXPRESSION; HUMANS; INFLAMMATION; NF-KAPPA B; OSTEOBLASTS; PROTEIN BINDING; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A3; RECEPTORS, PURINERGIC P1; RNA, MESSENGER;

EID: 84878622750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065561     Document Type: Article

References (60)

1. Tesch AM, MacDonald MH, Kollas-Baker C, Benton HP, (2004) Endogenously produced adenosine regulates articular cartilage matrix homeostasis: enzymatic depletion of adenosine stimulates matrix degradation. Osteoarthritis Cartilage 12: 349-359.
2. Wang J, Verdonk P, Elewaut D, Veyes EM, Verbruggen G, (2003) Homeostasis of the extracellular matrix of normal and osteoarthritic human articular cartilage chondrocytes in vitro. Osteoarthritis Cartilage 11: 801-809.
3. Fraser A, Fearon U, Billinghurst RC, Ionescu M, Reece R, et al. (2003) Turnover of type II collagen and aggrecan in cartilage matrix at the onset of inflammatory arthritis in humans: relationship to mediators of systemic and local inflammation. Arthritis Rheum 48: 3085-3095.
4. Petrov R, Melinda H, MacDonald DVM, Tech AM, Benton HP, (2005) Inhibition of adenosine kinase attenuates interleukin-1 and lipopolysaccharide indiced alterations in articular cartilage metabolism. Osteoarthritis Cartilage 13: 250-257.
5. Seeman E, (2009) Bone modeling and remodeling. Crit Rev Eukaryot Gene Expr 19: 219-233.
6. Del Fattore A, Teti A, Rucci N, (2012) Bone cells and the mechanisms of bone remodelling. Front Biosci 4: 2302-2321.
7. Confavreux C, (2011) Bone: from a reservoir of minerals to a regulator of energy metabolism. Kidney Int Supplement 121: S14-19.
8. Long F, (2011) Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 13: 27-38.
9. Rizzo A, Di Domenico M, Carratelli CR, Mazzola N, Paolillo R, (2011) Induction of proinflammatory cytokines in human osteoblastic cells by Chlamydia pneumoniae. Cytokine 56: 450-457.
10. Atkins GJ, Kostakis P, Pan B, Farrugia A, Gronthos S, et al. (2003) RANKL expression is related to the differentiation state of human osteoblasts. J Bone Miner Res 18: 1088-1098.
11. Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, et al. (2012) Bench to bedside: elucidation of the OPG-RANK-RANKL pathway and the development of denosumab. Nat Rev Drug Discov 11: 401-419.
12. Chalidis B, Sachinis N, Assiotis A, Maccauro G, (2011) Stimulation of bone formation and fracture healing with pulsed electromagnetic fields: biologic responses and clinical implications. Int J Immunopathol Pharmacol 24: 17-20.
13. De Mattei M, Caruso A, Traina GC, Pezzetti F, Baroni T, et al. (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.
14. Lin HY, Lin YJ, (2011) In vitro effects of low frequency electromagnetic fields on osteoblast proliferation and maturation in an inflammatory environment. Bioelectromagnetics 32: 552-560.
15. Sollazzo V, Palmieri A, Pezzetti F, Massari L, Carinci F, (2010) Effects of pulsed electromagnetic fields on human osteoblast like cells (MG-63): a pilot study. Clin Ortho Relat Res 468: 2260-2277.
16. De Mattei M, Pasello M, Pellati A, Stabellini G, Massari L, et al. (2003) Effects of electromagnetic fields on proteoglycan metabolism of bovine articular cartilage explants. Connect Tissue Res 44: 154-159.
17. Zorzi C, Dall'oca C, Cadossi R, Setti S, (2007) Effects of pulsed electromagnetic fields on patients' recovery after arthroscopic surgery: prospective, randomized and double-blind study. Knee Surg Sports Traumatol Arthrosc 15: 830-834.
18. Gessi S, Merighi S, Varani K, Borea PA, (2011) Adenosine receptors in health and disease. Adv Pharmacol 61: 41-75.
19. Gessi S, Merighi S, Varani K, Leung E, Mac Lennan S, et al. (2008) The A3 adenosine receptor: an enigmatic player in cell biology. Pharmacol Ther 117: 123-140.
20. Varani K, Massara A, Vincenzi F, Tosi A, Padovan M, et al. (2009) Normalization of A2A and A3 adenosine receptor up-regulation in rheumatoid arthritis patients by treatment with anti-tumor necrosis factor alpha but not methotrexate. Arthritis Rheum 60: 2880-2891.
21. Varani K, Padovan M, Vincenzi F, Targa M, Trotta F, et al. (2011) A2A and A3 adenosine receptor expression in rheumatoid arthritis: upregulation, inverse correlation with disease activity score and suppression of inflammatory cytokine and metalloproteinase release. Arthritis Res Ther 13: R197.
22. Varani K, Vincenzi F, Tosi A, Gessi S, Casetta I, et al. (2010) A2A adenosine receptor overexpression and functionality, as well as TNF-alpha levels, correlate with motor symptoms in Parkinson's disease. FASEB J 24: 587-598.
23. Varani K, Caramori G, Vincenzi F, Adcock I, Casolari P, et al. (2006) Alteration of adenosine receptors in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 173: 398-406.
24. He W, Cronstein B, (2011) The roles of adenosine and adenosine receptors in bone remodelling. Front Biosci 3: 888-895.
25. Kara FM, Doty SB, Boskey A, Goldring S, Zaidi M, et al. (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.
26. Carroll SH, Wigner NA, Kulkarni N, Johnston-Cox H, Gerstenfeld LC, et al. (2012) A2B adenosine receptor promotes mesenchymal stem cell differentiation to osteoblasts and bone formation in vivo. J Biol Chem 287: 15718-15727.
27. Takedachi M, Oohara H, Smith BJ, Iyama M, Kobashi M, et al. (2012) CD73-generated adenosine promotes osteoblast differentiation. J Cell Physiol 227: 2622-2631.
28. Varani K, Gessi S, Merighi S, Iannotta V, Cattabriga E, et al. (2002) Effect of low frequency electromagnetic fields on A2A adenosine receptors in human neutrophils. British J Pharmacol 136: 57-66.
29. Varani K, Gessi S, Merighi S, Iannotta V, Cattabriga E, et al. (2003) Alteration of A3 adenosine receptors in human neutrophils and low frequency electromagnetic fields. Biochem Pharmacol 66: 1897-1906.
30. Varani K, Vincenzi F, Targa M, Corciulo C, Fini M, et al. (2011) Effect of pulsed electromagnetic field exposure on adenosine receptors in rat brain. Bioelectromagnetics 33: 279-287.
31. Vincenzi F, Targa M, Corciulo C, Gessi S, Merighi S, et al. (2012) The anti-tumor effect of A3 adenosine receptors is potentiated by pulsed electromagnetic fields in cultured neural cancer cells. PLoS One 7: e39317.
32. Varani K, De Mattei M, Vincenzi F, Gessi S, Merighi S, et al. (2008) Characterization of adenosine receptors in bovine chondrocytes and fibroblast-like synoviocytes exposed to low frequency low energy pulsed electromagnetic fields. Osteoarthritis Cartilage 16: 292-304.
33. De Mattei M, Varani K, Masieri FF, Pellati A, Ongaro A, et al. (2009) Adenosine analogs and electromagnetic fields inhibit prostaglandin E(2) release in bovine synovial fibroblasts. Osteoarthritis Cartilage 17: 252-262.
34. Ongaro A, Varani K, Masieri F, Pellati A, Massari L, et al. (2012) Electromagnetic fields (EMFs) and adenosine receptors modulate prostaglandin E(2) and cytokine release in human osteoarthritic synovial fibroblasts. J Cell Physiol 227: 246-249.
35. Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, et al. (1994) Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. J Clin Invest 94: 2307-2316.
36. Goldring MB, (2004) Culture of immortalized chondrocytes and their use as models of chondrocyte function. Methods Mol Med 100: 37-52.
37. Claassen H, Schicht M, Brandt J, Reuse K, Schädlich R, et al. (2011) C-28/I2 and T/C-28a2 chondrocytes as well as human primary articular chondrocytes express sex hormone and insulin receptors-Useful cells in study of cartilage metabolism. Ann Anat 193: 23-9.
38. de Souza Malaspina TS, dos Santos CX, Campanelli AP, Laurindo FR, Sogayar MC, et al. (2008) Tartrate-resistant acid phosphatase activity and glutathione levels are modulated during hFOB 1.19 osteoblastic differentiation. J Mol Histol 39: 627-634.
39. Varani K, Vincenzi F, Tosi A, Targa M, Masieri FF, et al. (2010) Expression and functional role of adenosine receptors in regulating inflammatory responses in human synoviocytes. British J Pharmacol 160: 101-115.
40. Varani K, Merighi S, Gessi S, Klotz KN, Leung E, et al. (2000) [3H]-MRE 3008-F20: a novel antagonist radioligand for the pharmacological and biochemical characterization of human A3 adenosine receptors. Mol Pharmacol 57: 968-975.
41. Varani K, Gessi S, Merighi S, Vincenzi F, Cattabriga E, et al. (2005) Pharmacological characterization of novel adenosine ligands in recombinant and native human A2B receptors. Biochem Pharmacol 70: 1601-1612.
42. Varani K, Vincenzi F, Targa M, Paradiso B, Parrilli A, et al. (2013) The stimulation of A(3) adenosine receptors reduces bone-residing breast cancer in a rat preclinical model. Eur J Cancer 49: 482-491.
43. Varani K, Maniero S, Vincenzi F, Targa M, Stefanelli A, et al. (2011) A3 receptors are overexpressed in pleura from patients with mesothelioma and reduce cell growth via Akt/nuclear factor-κB pathway. Am J Respir Crit Care Med 183: 522-530.
44. Gessi S, Fogli E, Sacchetto V, Merighi S, Varani K, et al. (2010) Adenosine modulates HIF-1α, VEGF, IL-8, and foam cell formation in a human model of hypoxic foam cells. Arterioscler Thromb Vasc Biol 30: 90-97.
45. Freyria AM, Mallein-Gerin F, (2012) Chondrocytes or adult stem cells for cartilage repair: the indisputable role of growth factors. Injury 43: 259-265.
46. Dong S, Yang B, Guo H, Kang F, (2012) MicroRNAs regulate osteogenesis and chondrogenesis. Biochem Biophys Res Commun 418: 587-591.
47. Pezzetti F, De Mattei M, Caruso A, Cadossi R, Zucchini P, et al. (1999) Effects of pulsed electromagnetic fields on human chondrocytes: an in vitro study. Calcif Tissue Int 65: 396-401.
48. De Mattei M, Caruso A, Pezzetti F, Pellati A, Stabellini G, et al. (2001) Effects of pulsed electromagnetic fields on human articular chondrocyte proliferation. Connect Tissue Res 42: 269-279.
49. Tsai MT, Chang WH, Chang K, Hou RJ, Wu TW, (2007) Pulsed electromagnetic fields affect osteoblast proliferation and differentiation in bone tissue engineering. Bioelectromagnetics 28: 519-528.
50. Campo GM, Avenoso A, D'Ascola A, Scuruchi M, Prestipino V, et al. (2012) Adenosine A2A receptor activation and hyaluronan fragment inhibition reduce inflammation in mouse articular chondrocytes stimulated with interleukin-1β. FEBS J 279: 2120-2133.
51. Russell JM, Stephenson GS, Yellowley CE, Benton HP, (2007) Adenosine inhibition of lipopolysaccharide-induced interleukin-6 secretion by the osteoblastic cell line MG-63. Calcif Tissue Int 81: 316-326.
52. Fini M, Giavaresi G, Carpi A, Nicolini A, Setti S, et al. (2005) Effects of pulsed electromagnetic fields on articular hyaline cartilage: review of experimental and clinical studies. Biomed Pharmacother 59: 388-394.
53. Silva I, Branco JC, (2011) Rank/Rankl/opg: literature review. Acta Reumatol Port 36: 209-218.
54. Schwartz Z, Fisher M, Lohmann CH, Simon BJ, Boyan BD, (2009) Osteoprotegerin (OPG) production by cells in the osteoblast lineage is regulated by pulsed electromagnetic fields in cultures grown on calcium phosphate substrates. Ann Biomed Eng 37: 437-444.
55. Borsje MA, Ren Y, de Haan-Visser HW, Kuijer R, (2010) Comparison of low-intensity pulsed ultrasound and pulsed electromagnetic field treatments on OPG and RANKL expression in human osteoblast-like cells. Angle Orthod 80: 498-503.
56. Zhou J, Chen S, Guo H, Xia L, Liu H, et al. (2012) Pulsed electromagnetic field stimulates osteoprotegerin and reduces RANKL expression in ovariectomized rats. Rheumatol Int in press.
57. Xu J, Wu HF, Ang ES, Yip K, Woloszyn M, et al. (2009) NF-kappaB modulators in osteolytic bone diseases. Cytokine Growth Factor Rev 20: 7-17.
58. Novack DV, (2011) Role of NF-κB in the skeleton. Cell Res 21: 169-182.
59. Fishman P, Bar-Yehuda S, Synowitz M, Powell JD, Klotz KN, et al. (2009) Adenosine receptors and cancer. Handb Exp Pharmacol 193: 399-441.
60. Milne GR, Palmer TM, (2011) Anti-inflammatory and immunosuppressive effects of the A2A adenosine receptor. ScientificWorldJournal 11: 320-339.