ATP and UTP stimulate bone morphogenetic protein-2,-4 and -5 gene expression and mineralization by rat primary osteoblasts involving PI3K/AKT pathway

Experimental Cell Research

Volumn 319, Issue 13, 2013, Pages 2028-2036

  Ayala Peña, Victoria B ^a   Scolaro, Luis A ^b   Santillán, Graciela E ^a  

^a UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

^b Laboratorio de Virologia Ciudad Autonoma de Buenos Aires   (Argentina)

Author keywords

ATP; BMPs; Osteoblast; PI3K AKT; Purinergic receptor; UTP

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; CALCIUM; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PURINERGIC RECEPTOR; URIDINE DIPHOSPHATE; URIDINE TRIPHOSPHATE;

ANIMAL CELL; ARTICLE; BONE CELL; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL LYSATE; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84879886840     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.006     Document Type: Article

References (59)

1. Turner C.H., Pavalko F.M. Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J. Orthop. Sci. 1998, 3:346-355.
2. Duncan R.L., Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif. Tissue Int. 1995, 57:344-358.
3. Kapur S., Baylink D.J., Lau K.H. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 2003, 32:241-251.
4. Romanello M., Pani B., Bicego M., D'Andrea P. Mechanically induced ATP release from human osteoblastic cells. Biochem. Biophys. Res. Commun. 2001, 289:1275-1281.
5. Romanello M., Codognotto A., Bicego M., Pines A., Tell G., D'Andrea P. Autocrine/paracrine stimulation of purinergic receptors in osteoblasts: contribution of vesicular ATP release. Biochem. Biophys. Res. Commun. 2005, 331:1429-1438.
6. Burnstock G. Purinergic signalling-an overview. Novartis Found. Symp. 2006, 276:26-48.
7. Genetos D.C., Geist D.J., Liu D., Donahue H.J., Duncan R.L. Fluid shear-induced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J. Bone Miner. Res. 2005, 20:41-49.
8. Bowler W.B., Buckley K.A., Gartland A., Hipskind R.A., Bilbe G., Gallagher J.A. Extracellular nucleotide signaling: a mechanism for integrating local and systemic responses in the activation of bone remodeling. Bone 2001, 28:507-512.
9. Gartland A., Buckley K.A., Hipskind R.A., Bowler W.B., Gallagher J.A. P2 receptors in bone-modulation of osteoclast formation and activity via P2X7 activation. Crit. Rev. Eukaryot. Gene Expr. 2003, 13:237-242.
10. Grygorczyk R., Hanrahan J.W. CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. Am. J. Physiol. 1997, 272:C1058-C1066.
11. Lazarowski E.R., Homolya L., Boucher R.C., Harden T.K. Direct demonstration of mechanically induced release of cellular UTP and its implication for uridine nucleotide receptor activation. J. Biol. Chem. 1997, 272:24348-24354.
12. Taylor M., Tanner K.E., Freeman M.A. Finite element analysis of the implanted proximal tibia: a relationship between the initial cancellous bone stresses and implant migration. J. Biomech. 1998, 31:303-310.
13. Orriss I.R., Utting J.C., Brandao-Burch A., Colston K., Grubb B.R., Burnstock G., et al. Extracellular nucleotides block bone mineralization in vitro: evidence for dual inhibitory mechanisms involving both P2Y2 receptors and pyrophosphate. Endocrinology 2007, 148:4208-4216.
14. Ralevic V., Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 1998, 50:413-492.
15. Burnstock G. Purine and pyrimidine receptors. Cell. Mol. Life Sci. 2007, 64:1471-1483.
16. 2+ mobilization is strongly potentiated by a parathyroid hormone/cAMP-dependent protein kinase pathway independently of mitogen-activated protein kinase. J. Biol. Chem. 1999, 274:14315-14324.
17. Scodelaro Bilbao P., Boland R., Santillán G. ATP modulates transcription factors through P2Y2 and P2Y4 receptors via PKC/MAPKs and PKC/Src pathways in MCF-7 cells. Arch. Biochem. Biophys. 2010, 494:7-14.
18. Katz S., Ayala V., Santillán G., Boland R. Activation of the PI3K/Akt signaling pathway through P2Y2 receptors by extracellular ATP is involved in osteoblastic cell proliferation. Arch. Biochem. Biophys. 2011, 513:144-152.
19. Rider C.C., Mulloy B. Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem. J. 2010, 429:1-12.
20. Mukherjee A., Wilson E.M., Rotwein P. Selective signaling by Akt2 promotes bone morphogenetic protein 2-mediated osteoblast differentiation. Mol. Cell. Biol. 2010, 30:1018-1027.
21. Hogan B.L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 1996, 10:1580-1594.
22. Kishimoto Y., Lee K.H., Zon L., Hammerschmidt M., Schulte-Merker S. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 1997, 124:4457-4466.
23. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., Einhorn T., Tabin C.J., Rosen V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat. Genet. 2006, 38:1424-1429.
24. Bais M.V., Wigner N., Young M., Toholka R., Graves D.T., Morgan E.F., Gerstenfeld L.C., Einhorn T.A. BMP2 is essential for post natal osteogenesis but not for recruitment of osteogenic stem cells. Bone 2009, 45:254-266.
25. Ikegame M., Ishibashi O., Yoshizawa T., Shimomura J., Komori T., Ozawa H., Kawashima H. Tensile stress induces bone morphogenetic protein 4 in preosteoblastic and fibroblastic cells, which later differentiate into osteoblasts leading to osteogenesis in the mouse calvariae in organ culture. J. Bone Miner. Res. 2001, 16:24-32.
26. Tanno M., Furukawa K.I., Ueyama K., Harata S., Motomura S. Uniaxial cyclic stretch induces osteogenic differentiation and synthesis of bone morphogenetic proteins of spinal ligament cells derived from patients with ossification of the posterior longitudinal ligaments. Bone 2003, 33:475-484.
27. Rath B., Nam J., Knobloch T.J., Lannutti J.J., Agarwal S. Compressive forces induce osteogenic gene expression in calvarial osteoblasts. J. Biomech. 2008, 41:1095-1103.
28. Csiszar A., Lehoux S., Ungvari Z. Hemodynamic forces, vascular oxidative stress, and regulation of BMP-2/4 expression. Antioxid. Redox Signaling 2009, 11:1683-1697.
29. Tseng W., Graham L.S., Geng Y., Reddy A., Lu J., Effros R.B., Demer L., Tintut Y. PKA-induced receptor activator of NF-kappaB ligand (RANKL) expression in vascular cells mediates osteoclastogenesis but not matrix calcification. J. Biol. Chem. 2010, 285:29925-29931.
30. Wang Q., Zheng Y.P., Niu H.J. Changes in triphasic mechanical properties of proteoglycan-depleted articular cartilage extracted from osmotic swelling behavior monitored using high-frequency ultrasound. Mol. Cell. Biomech. 2010, 7:45-58.
31. 2+ ions. Br. J. Pharmacol 2003, 140:1177-1186.
32. Orriss I.R., Knight G.E., Ranasinghe S., Burnstock G., Arnett T.R. Osteoblast responses to nucleotides increase during differentiation. Bone 2006, 39:300-309.
33. Orriss I.R., Key M.L., Brandao-Burch A., Patel J.J., Burnstock G., Arnett T.R. The regulation of osteoblast function and bone mineralisation by extracellular nucleotides: the role of p2x receptors. Bone 2012, 51:389-400.
34. Panupinthu N., Rogers J.T., Zhao L., Solano-Flores L.P., Possmayer F., Sims S.M., Dixon S.J. P2X7 receptors on osteoblasts couple to production of lysophosphatidic acid: a signaling axis promoting osteogenesis. J. Cell Biol. 2008, 181:859-871.
35. Hoebertz A., Mahendran S., Burnstock G., Arnett T.R. 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. 2002, 86:413-419.
36. Zhang Y.Y., Li X., Qian S.W., Guo L., Huang H.Y., He Q., Liu Y., Ma C.G., Tang Q.Q. Down-regulation of type I Runx2 mediated by dexamethasone is required for 3T3-L1 adipogenesis. Mol. Endocrinol. 2012, 26:798-808.
37. Naito M., Omoteyama K., Mikami Y., Takahashi T., Takagi M. Inhibition of Wnt/β-catenin signaling by dexamethasone promotes adipocyte differentiation in mesenchymal progenitor cells, ROB-C26. Histochem. Cell Biol. 2012, 138:833-845.
38. O'Brien C.A., Jia D., Plotkin L.I., Bellido T., Powers C.C., Stewart S.A., Manolagas S.C., Weinstein R.S. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 2004, 145:1835-1841.
39. Quarles L.D., Yohay D.A., Lever L.W., Caton R., Wenstrup R.J. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J. Bone Miner. Res. 1992, 7:683-692.
40. Cooper L.F., Yliheikkilä P.K., Felton D.A., Whitson S.W. Spatiotemporal assessment of fetal bovine osteoblast culture differentiation indicates a role for BSP in promoting differentiation. J. Bone Miner. Res. 1998, 13:620-632.
41. Huang Z., Ren P.G., Ma T., Smith R.L., Goodman S.B. Modulating osteogenesis of mesenchymal stem cells by modifying growth factor availability. Cytokine 2010, 51:305-310.
42. Noel D., Gazit D., Bouquet C., Apparailly F., Bony C., Plence P. Short-term BMP-2 expression is sufficient for in vivo osteochondral differentiation of mesenchymal stem cells. Stem Cells 2004, 22:74-85.
43. Bandyopadhyay A., Tsuji K., Cox K., Harfe B.D., Rosen V., Tabin C.J. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet. 2006, 2:e216.
44. Ornelas I.M., Ventura A.L. Involvement of the PI3K/AKT pathway in ATP-induced proliferation of developing retinal cells in culture. Int. J. Dev. Neurosci. 2010, 28:503-511.
45. Horvath R.J., DeLeo J.A. Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J. Neurosci. 2009, 29:998-1005.
46. Jacques-Silva M.C., Rodnight R., Lenz G., Liao Z., Kong Q., Tran M., Kang Y., Gonzalez F.A., Weisman G.A., Neary J.T. P2X7 receptors stimulate AKT phosphorylation in astrocytes. Br. J. Pharmacol. 2004, 141:1106-1117.
47. Guntur A.R., Rosen C.J., Naski M.C. N-cadherin adherens junctions mediate osteogenesis through PI3K signaling. Bone 2012, 50:54-62.
48. Yang J., Zhang X., Wang W., Liu J. Insulin stimulates osteoblast proliferation and differentiation through ERK and PI3K in MG-63 cells. Cell Biochem. Funct. 2010, 28:334-341.
49. Guntur A.R., Rosen C.J. The skeleton: a multi-functional complex organ: new insights into osteoblasts and their role in bone formation: the central role of PI3Kinase. J. Endocrinol. 2011, 211:123-130.
50. Mukherjee A, Rotwein P. Selective signaling by Akt1 controls osteoblast differentiation and osteoblast-mediated osteoclast development. Mol. Cell. Biol. 2012, 32:490-500.
51. Ghosh-Choudhury N., Abboud S.L., Nishimura R., Celeste A., Mahimainathan L., Choudhury G.G. Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J. Biol. Chem. 2002, 277:33361-33368.
52. Fujita T., Azuma Y., Fukuyama R., Hattori Y., Yoshida C., Koida M., Ogita K., Komori T. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J. Cell Biol. 2004, 166:85-95.
53. Rached M.T., Kode A., Xu L., Yoshikawa Y., Paik J.H., Depinho R.A., Kousteni S. FoxO1 is a positive regulator of bone formation by favoring protein synthesis and resistance to oxidative stress in osteoblasts. Cell Metab. 2010, 11:147-160.
54. Costessi A., Pines A., D'Andrea P., Romanello M., Damante G., Cesaratto L., Quadrifoglio F., Moro L., Tell G. Extracellular nucleotides activate Runx2 in the osteoblast-like HOBIT cell line: a possible molecular link between mechanical stress and osteoblasts' response. Bone 2005, 36:418-432.
55. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
56. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771.
57. Bianco P., Fisher L.W., Young M.F., Termine J.D., Robey P.G. Expression of bone sialoprotein (BSP) in developing human tissues. Calcif. Tissue Int. 1991, 49:421-426.
58. Wade-Gueye N.M., Boudiffa M., Vanden-Bossche A., Laroche N., Aubin J.E., Vico L., Lafage-Proust M.H., Malaval L. Absence of bone sialoprotein (BSP) impairs primary bone formation and resorption: the marrow ablation model under PTH challenge. Bone 2012, 50:1064-1073.
59. Hunter G.K., Goldberg H.A. Nucleation of hydroxyapatite by bone sialoprotein. Proc. Nat. Acad. Sci. U.S.A. 1993, 90:8562-8565.