Extracellular ATP Released by Osteoblasts Is A Key Local Inhibitor of Bone Mineralisation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Orriss, Isabel R ^a   Key, Michelle L ^a   Hajjawi, Mark O R ^a   Arnett, Timothy R ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ALKALINE PHOSPHATASE; APYRASE; BREFELDIN A; COLLAGEN; N ETHYLMALEIMIDE; NUCLEOTIDE PYROPHOSPHATASE; PHOSPHODIESTERASE; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X7 RECEPTOR;

ADIPOCYTE; ANIMAL CELL; ARTICLE; BONE MINERALIZATION; CELL COUNT; CELL PROLIFERATION; CELL STIMULATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR SPACE; HYDROLYSIS; NONHUMAN; NUCLEOTIDE TRANSPORT; OSTEOBLAST; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ADIPOCYTES; ALKALINE PHOSPHATASE; ANIMALS; APYRASE; CALCIFICATION, PHYSIOLOGIC; COLLAGEN; ENZYME ACTIVATION; EXTRACELLULAR SPACE; OSTEOBLASTS; PHOSPHORIC DIESTER HYDROLASES; PRIMARY CELL CULTURE; RATS; RECEPTORS, PURINERGIC P2X1; RECEPTORS, PURINERGIC P2X7; SIGNAL TRANSDUCTION;

EID: 84880125704     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069057     Document Type: Article

References (45)

1. Burnstock G, (1972) Purinergic nerves. Pharmacol Rev 24: 509-581. PubMed: 4404211.
2. Burnstock G, Kennedy C, (1985) Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacologist 16: 433-440.
3. Abbracchio MP, Burnstock G, (1994) Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol Ther 64: 445-475. doi:10.1016/0163-7258(94)00048-4. PubMed: 7724657.
4. Ralevic V, Burnstock G, (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492. PubMed: 9755289.
5. Burnstock G, (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64: 1471-1483 1483. doi:10.1007/s00018-007-6497-0. PubMed: 17375261.
6. Orriss IR, Burnstock G, Arnett TR, (2010) Purinergic signalling and bone remodelling. Curr Opin Pharmacol 10: 322-330. doi:10.1016/j.coph.2010.01.003. PubMed: 20189453.
7. Orriss IR, Arnett TR, (2012). p. pp. 2Y receptors in bone. WIREs Membr Transp Signal 1: 805-814.
8. Gartland A, Orriss IR, Rumney RM, Bond AP, Arnett T, et al. (2012) Purinergic signalling in osteoblasts. Front Biosci 17: 16-29. doi:10.2741/3912. PubMed: 22201729.
9. Reyes JP, Sims SM, Dixon SJ, (2011) P2 receptor expression, signaling and function in osteoclasts. Front Biosci (Schol Ed) 3: 1101-1118. PubMed: 21622259.
10. Nakamura E, Uezono Y, Narusawa K, Shibuya I, Oishi Y, et al. (2000) ATP activates DNA synthesis by acting on P2X receptors in human osteoblast-like MG-63 cells. Am J Physiol Cell Physiol 279: C510-C519. PubMed: 10913018.
11. Panupinthu N, Zhao L, Possmayer F, Ke HZ, Sims SM, et al. (2007) P2X7 nucleotide receptors mediate blebbing in osteoblasts through a pathway involving lysophosphatidic acid. J Biol Chem 282: 3403-3412. PubMed: 17135244.
12. Bowler WB, Buckley KA, Gartland A, Hipskind RA, Bilbe G, et al. (2001) Extracellular nucleotide signaling: a mechanism for integrating local and systemic responses in the activation of bone remodeling. Bone 28: 507-512. doi:10.1016/S8756-3282(01)00430-6. PubMed: 11344050.
13. Buckley KA, Wagstaff SC, McKay G, Gaw A, Hipskind RA, et al. (2001) Parathyroid hormone potentiates nucleotide-induced [Ca2+]i release in rat osteoblasts independently of Gq activation or cyclic monophosphate accumulation. A mechanism for localizing systemic responses in bone. J Biol Chem 276: 9565-9571. doi:10.1074/jbc.M005672200. PubMed: 11124938.
14. Panupinthu N, Rogers JT, Zhao L, Solano-Flores LP, Possmayer F, et al. (2008) P2X7 receptors on osteoblasts couple to production of lysophosphatidic acid: a signaling axis promoting osteogenesis. J Cell Biol 181: 859-871. doi:10.1083/jcb.200708037. PubMed: 18519738.
15. Wang N, Robaye B, Agrawal A, Skerry TM, Boeynaems JM, et al. (2012) Reduced bone turnover in mice lacking the P2Y(13) receptor of ADP. Mol Endocrinol 26: 142-152. doi:10.1210/me.2011-1083. PubMed: 22108801.
16. Zippel N, Limbach CA, Ratajski N, Urban C, Luparello C, et al. (2012) Purinergic receptors influence the differentiation of human mesenchymal stem cells. Stem Cells Dev 21: 884-900. doi:10.1089/scd.2010.0576. PubMed: 21740266.
17. Ciciarello M, Zini R, Rossi L, Salvestrini V, Ferrari D, et al. (2013) Extracellular purines promote the differentiation of human bone marrow-derived mesenchymal stem cells to the osteogenic and adipogenic Lineages. Stem Cells Dev 22: 1097-1111. PubMed: 23259837.
18. Syberg S, Brandao-Burch A, Patel JJ, Hajjawi M, Arnett TR, et al. (2012) Clopidogrel (Plavix), a P2Y12 receptor antagonist, inhibits bone cell function in vitro and decreases trabecular bone in vivo. J Bone Miner Res 27: 2373-2388. doi:10.1002/jbmr.1690. PubMed: 22714653.
19. Hoebertz A, Mahendran S, Burnstock G, Arnett TR, (2002) ATP and UTP at low concentrations strongly inhibit bone formation by osteoblasts: a novel role for the P2Y2 receptor in bone remodeling. J Cell Biochem 86: 413-419. doi:10.1002/jcb.10236. PubMed: 12210747.
20. Orriss IR, Utting JC, Brandao-Burch A, Colston K, Grubb BR, et al. (2007) Extracellular nucleotides block bone mineralization in vitro: evidence for dual inhibitory mechanisms involving both P2Y2 receptors and pyrophosphate. Endocrinology 148: 4208-4216. doi:10.1210/en.2007-0066. PubMed: 17569759.
21. Orriss IR, Key ML, Brandao-Burch A, Patel JJ, Burnstock G, et al. (2012) The regulation of osteoblast function and bone mineralisation by extracellular nucleotides: The role of P2X receptors. Bone 51: 389-400. doi:10.1016/j.bone.2012.06.013. PubMed: 22749889.
22. Romanello M, Pani B, Bicego M, D'Andrea P, (2001) Mechanically induced ATP release from human osteoblastic cells. Biochem Biophys Res Commun 289: 1275-1281. doi:10.1006/bbrc.2001.6124. PubMed: 11741333.
23. Buckley KA, Golding SL, Rice JM, Dillon JP, Gallagher JA, (2003) Release and interconversion of P2 receptor agonists by human osteoblast-like cells. FASEB J 17: 1401-1410. doi:10.1096/fj.02-0940com. PubMed: 12890693.
24. Genetos DC, Geist DJ, Liu D, Donahue HJ, Duncan RL, (2005) Fluid Shear-Induced ATP Secretion Mediates Prostaglandin Release in MC3T3-E1 Osteoblasts. J Bone Miner Res 20: 41-49. doi:10.1359/JBMR.041009. PubMed: 15619668.
25. Orriss IR, Knight GE, Utting JC, Taylor SE, Burnstock G, et al. (2009) Hypoxia stimulates vesicular ATP release from rat osteoblasts. J Cell Physiol 220: 155-162. doi:10.1002/jcp.21745. PubMed: 19259945.
26. Rumney RM, Sunters A, Reilly GC, Gartland A, (2012) Application of multiple forms of mechanical loading to human osteoblasts reveals increased ATP release in response to fluid flow in 3D cultures and differential regulation of immediate early genes. J Biomech 45: 549-554. doi:10.1016/j.jbiomech.2011.11.036. PubMed: 22176713.
27. Brandao-Burch A, Key ML, Patel JJ, Arnett TR, Orriss IR, (2012) The P2X7 receptor is an important regulator of extracellular ATP levels. Front Endocrinol (Lausanne) 3: 41. PubMed: 22654865.
28. Genetos DC, Kephart CJ, Zhang Y, Yellowley CE, Donahue HJ, (2007) Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J Cell Physiol 212: 207-214. doi:10.1002/jcp.21021. PubMed: 17301958.
29. Zimmermann H, Zebisch M, Sträter N, (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8: 437-502. doi:10.1007/s11302-012-9309-4. PubMed: 22555564.
30. Johnson KA, Hessle L, Vaingankar S, Wennberg C, Mauro S, et al. (2000) Osteoblast tissue-nonspecific alkaline phosphatase antagonizes and regulates PC-1. Am J Physiol Regul Integr Comp Physiol 279: R1365-R1377. PubMed: 11004006.
31. Hessle L, Johnson KA, Anderson HC, Narisawa S, Sali A, et al. (2002) Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci U S A 99: 9445-9449. doi:10.1073/pnas.142063399. PubMed: 12082181.
32. Orriss IR, Arnett TR, (2010) Extracellular nucleotides regulate the expression and activity of ecto-nucleotidases by osteoblasts. Bone 46S1:: S55.
33. Fleisch H, Neuman W, (1961) The role of phosphatase and polyphosphates in calcification of collagen. Helv Physiol Pharmacol Acta 19: C17-C18. PubMed: 13700175.
34. Fleisch H, Bisaz S, (1962) Mechanism of calcification: inhibitory role of pyrophosphate. Nature 195: 911. doi:10.1038/195911a0. PubMed: 13893487.
35. Orriss IR, Taylor SE, Arnett TR, (2012) Rat osteoblast cultures. Methods Mol Biol 816: 31-41. doi:10.1007/978-1-61779-415-5_3. PubMed: 22130920.
36. Brandao-Burch A, Utting JC, Orriss IR, Arnett TR, (2005) Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization. Calcif Tissue Int 77: 167-174. doi:10.1007/s00223-004-0285-8. PubMed: 16075362.
37. Razzell WE, Khorana HG, (1959) Studies on polynucleotides. III. Enzymic degradation; substrate specificity and properties of snake venom phosphodiesterase. J Biol Chem 234: 2105-2113. PubMed: 13673021.
38. Ramírez-Zacarías JL, Castro-Muñozledo F, Kuri-Harcuch W, (1992) Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 97: 493-497. doi:10.1007/BF00316069. PubMed: 1385366.
39. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
40. Burnstock G, (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87: 659-797. doi:10.1152/physrev.00043.2006. PubMed: 17429044.
41. Addison WN, Azari F, Sørensen ES, Kaartinen MT, Mckee MD, (2007) Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. J Biol Chem 282: 15872-15883. doi:10.1074/jbc.M701116200. PubMed: 17383965.
42. Bellows CG, Wang YH, Heersche JN, Aubin JE, (1994) 1,25-dihydroxyvitamin D3 stimulates adipocyte differentiation in cultures of fetal rat calvaria cells: comparison with the effects of dexamethasone. Endocrinology 134: 2221-2229. doi:10.1210/en.134.5.2221. PubMed: 8156925.
43. Ham J, Evans BA, (2012) An emerging role for adenosine and its receptors in bone homeostasis. Front Endocrinol (Lausanne) 3: 113. PubMed: 23024635.
44. Shimegi S, (1996) ATP and adenosine act as a mitogen for osteoblast-like cells (MC3T3-E1). Calcif Tissue Int 58: 109-113. doi:10.1007/BF02529732. PubMed: 8998680.
45. Evans BA, Elford C, Pexa A, Francis K, Hughes AC, et al. (2006) Human osteoblast precursors produce extracellular adenosine, which modulates their secretion of IL-6 and osteoprotegerin. J Bone Miner Res 21: 228-236. PubMed: 16418778.