A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells

Biomaterials

Volumn 33, Issue 11, 2012, Pages 3205-3215

  Barradas, Ana M C ^a   Fernandes, Hugo A M ^a   Groen, Nathalie ^a   Chai, Yoke Chin ^b   Schrooten, Jan ^b   Van de Peppel, Jeroen ^c   Van Leeuwen, Johannes P T M ^c   Van Blitterswijk, Clemens A ^a   De Boer, Jan ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Bone morphogenetic protein; Calcium phosphate; Osteogenesis; Stem cell

Indexed keywords

BONE DEFECT; BONE HOMEOSTASIS; BONE MORPHOGENETIC PROTEINS; BONE REGENERATION; BONE TISSUE ENGINEERING; CALCIUM CHANNELS; CALCIUM SENSING RECEPTORS; EXTRACELLULAR; HUMAN BONES; IN-SITU; IN-VITRO; MESENCHYMAL STROMAL CELLS; MICROARRAY ANALYSIS; MORPHOLOGICAL CHANGES; OSTEOGENESIS; OSTEOGENIC; OSTEOGENIC DIFFERENTIATION; OSTEOPROGENITORS; SIGNALING CASCADES; SIGNALING PATHWAYS; UP-REGULATION;

BONE; CALCIUM PHOSPHATE; CYTOLOGY; GENE EXPRESSION; PROTEINS; STEM CELLS; TISSUE ENGINEERING;

CALCIUM;

BONE MORPHOGENETIC PROTEIN 2; CALCIUM; CALCIUM CHANNEL L TYPE; INTRACELLULAR CALCIUM SENSING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PROTEIN C FOS;

ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE MARROW DERIVED MESENCHYMAL STROMAL CELL; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STROMA CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

CALCIUM; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OSTEOGENESIS; TISSUE ENGINEERING;

EID: 84856576550     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.01.020     Document Type: Article

References (62)

1. Barradas A.M.C., Yuan H., van Blitterswijk C.A., Habibovic P. Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 2011, 21:407-429.
2. Siddappa R., Martens A., Doorn J., Leusink A., Olivo C., Licht R., et al. cAMP/PKA pathway activation in human mesenchymal stem cells invitro results in robust bone formation invivo. Proc Natl Acad Sci U S A 2008, 105(20):7281-7286.
3. Quarto R., Mastrogiacomo M., Cancedda R., Kutepov S.M., Mukhachev V., Lavroukov A., et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. NEngl J Med 2001, 344(5):385-386.
4. Gan Y., Dai K., Zhang P., Tang T., Zhu Z., Lu J. The clinical use of enriched bone marrow stem cells combined with porous beta-tricalcium phosphate in posterior spinal fusion. Biomaterials 2008, 29(29):3973-3982.
5. Yamasaki T., Yasunaga Y., Ishikawa M., Hamaki T., Ochi M. Bone-marrow-derived mononuclear cells with a porous hydroxyapatite scaffold for the treatment of osteonecrosis of the femoral head: a preliminary study. JBone Joint Surg Br 2010, 92-B(3):337-341.
6. Okamoto M., Dohi Y., Ohgushi H., Shimaoka H., Ikeuchi M., Matsushima A., et al. Influence of the porosity of hydroxyapatite ceramics on invitro and invivo bone formation by cultured rat bone marrow stromal cells. JMater Sci Mater Med 2006, 17(4):327-336.
7. Rouahi M., Gallet O., Champion E., Dentzer J., Hardouin P., Anselme K. Influence of hydroxyapatite microstructure on human bone cell response. JBiomed Mater Res A 2006, 78A(2):222-235.
8. Fellah B.H., Delorme B., Sohier J., Magne D., Hardouin P., Layrolle P. Macrophage and osteoblast responses to biphasic calcium phosphate microparticles. JBiomed Mater Res A 2010, 93A(4):1588-1595.
9. dos Santos EA, Farina M., Soares G.A., Anselme K. Chemical and topographical influence of hydroxyapatite and beta-tricalcium phosphate surfaces on human osteoblastic cell behavior. JBiomed Mater Res A 2009, 89A(2):510-520.
10. Yuan H., Fernandes H., Habibovic P., de Boer J., Barradas A.M., de Ruiter A., et al. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci U S A 2010, 107(31):13614-13619.
11. Khoshniat S., Bourgine A., Julien M., Petit M., Pilet P., Rouillon T., et al. Phosphate-dependent stimulation of MGP and OPN expression in osteoblasts via the ERK1/2 pathway is modulated by calcium. Bone 2011, 48(4):894-902.
12. Nakamura S., Matsumoto T., Sasaki J.-I., Egusa H., Lee K.Y., Nakano T., et al. Effect of calcium ion concentrations on osteogenic differentiation and hematopoietic stem cell niche-related protein expression in osteoblasts. Tissue Eng A 2010, 16(8):2467-2473.
13. Dvorak M.M., Siddiqua A., Ward D.T., Carter D.H., Dallas S.L., Nemeth E.F., et al. Physiological changes in extracellular calcium concentration directly control osteoblast function in the absence of calciotropic hormones. Proc Natl Acad Sci U S A 2004, 101(14):5140-5145.
14. Kanaya S., Nemoto E., Ebe Y., Somerman M.J., Shimauchi H. Elevated extracellular calcium increases fibroblast growth factor-2 gene and protein expression levels via a cAMP/PKA dependent pathway in cementoblasts. Bone 2010, 47(3):564-572.
15. Honda Y., Anada T., Kamakura S., Nakamura M., Sugawara S., Suzuki O. Elevated extracellular calcium stimulates secretion of bone morphogenetic protein 2 by a macrophage cell line. Biochem Biophys Res Commun 2006, 345(3):1155-1160.
16. Chai Y.C., Roberts S.J., Schrooten J., Luyten F.P. Probing the osteoinductive effect of calcium phosphate by using an invitro biomimetic model. Tissue Eng Part A 2010, 17(7-8):1083-1097.
17. Rosen V. BMP2 signaling in bone development and repair. Cytokine Growth Factor Rev 2009, 20(5-6):475-480.
18. Lee K.S., Kim H.J., Li Q.L., Chi X.Z., Ueta C., Komori T., et al. Runx2 is a common target of transforming growth factor beta 1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 2000, 20(23):8783-8792.
19. Matsubara T., Kida K., Yamaguchi A., Hata K., Ichida F., Meguro H., et al. BMP2 regulates osterix through Msx2 and Runx2 during osteoblast differentiation. JBiol Chem 2008, 283(43):29119-29125.
20. Thimm J., Mechler A., Lin H., Rhee S., Lal R. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. JBiol Chem 2005, 280(11):10646-10654.
21. Raya A., Kawakami Y., Rodriguez-Esteban C., Ibanes M., Rasskin-Gutman D., Rodriguez-Leon J., et al. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 2004, 427(6970):121-128.
22. Hofer A.M., Lefkimmiatis K. Extracellular calcium and cAMP: second messengers as "third messengers. Physiology 2007, 22(5):320-327.
23. Brown E.M., Gamba G., Riccardi D., Lombardi M., Butters R., Kifor O., et al. Clonning and characterization of an extracellular ca2+ sensing receptor from bovine parathyroid. Nature 1993, 366(6455):575-580.
24. Chang W., Tu C., Chen T.-H., Komuves L., Oda Y., Pratt S.A., et al. Expression and signal transduction of calcium-sensing receptors in cartilage and bone. Endocrinology 1999, 140(12):5883-5893.
25. House M.G., Kohlmeier L., Chattopadhyay N., Kifor O., Yamaguchi T., Leboff M.S., et al. Expression of an extracellular calcium-sensing receptor in human and mouse bone marrow cells. JBone Miner Res 1997, 12(12):1959-1970.
26. Skerry T.M. Identification of novel signaling pathways during functional adaptation of the skeleton to mechanical loading: the role of glutamate as a paracrine signaling agent in the skeleton. JBone Miner Metab 1999, 17(1):66-70.
27. Pi M., Faber P., Ekema G., Jackson P.D., Ting A., Wang N., et al. Identification of a novel extracellular cation-sensing G-protein-coupled receptor. JBiol Chem 2005, 280(48):40201-40209.
28. Pi M., Zhang L., Lei S.-F., Huang M.-Z., Zhu W., Zhang J., et al. Impaired osteoblast function in GPRC6A null mice. JBone Miner Res 2010, 25(5):1092-1102.
29. Major M.L., Cheung H.S., Misra R.P. Basic calcium phosphate crystals activate c-fos expression through a Ras/ERK dependent signaling mechanism. Biochem Biophys Res Commun 2007, 355(3):654-660.
30. Ma S., Yang Y., Carnes D.L., Kim K., Park S., Oh S.H., et al. Effects of dissolved calcium and phosphorous on osteoblast responses. JOral Implantol 2005, 31(2):61-67.
31. Alves H., Munoz-Najar U., De Wit J., Renard A.J.S., Hoeijmakers J.H.J., Sedivy J.M., et al. Alink between the accumulation of DNA damage and loss of multi-potency of human mesenchymal stromal cells. JCell Mol Med 2010, 14(12):2729-2738.
32. Du P., Kibbe W.A., Lin S.M. lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008, 24(13):1547-1548.
33. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol February 2004, Available from URL:. http://www.ncbi.nlm.nih.gov/pubmed/16646809.
34. Carpenter A., Jones T., Lamprecht M., Clarke C., Kang I., Friman O., et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006, 7(10):R100.
35. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004, 6(4):483-495.
36. Dalby M.J., Gadegaard N., Tare R., Andar A., Riehle M.O., Herzyk P., et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 2007, 6(12):997-1003.
37. Unadkat H.V., Hulsman M., Cornelissen K., Papenburg B.J., Truckenmueller R.K., Post G.F., et al. An algorithm-based topographical biomaterials library to instruct cell fate. Proc Natl Acad Sci U S A 2011, 108(40):16565-16570.
38. Wang Y.-K., Yu X., Cohen D.M., Wozniak M.A., Yang M.T., Gao L., et al. Bone Morphogenetic Protein-2-induced signaling and osteogenesis is regulated by cell shape, RhoA/ROCK, and cytoskeletal tension. Stem Cells Dev Ocotber 2011, Available from URL:. http://dx.doi.org/10.1089/scd.2011.0293, 10.1089/scd.2011.0293.
39. Siddappa R., Licht R., van Blitterswijk C., de Boer J. Donor variation and loss of multipotency during invitro expansion of human mesenchymal stem cells for bone tissue engineering. JOrthop Res 2007, 25(8):1029-1041.
40. Brown E.M., Lian J.B. New insights in bone biology: unmasking skeletal effects of the extracellular calcium-sensing receptor. Sci Signal 2008, 1(35):pe40.
41. Aguirre A., González A., Planell J.A., Engel E. Extracellular calcium modulates invitro bone marrow-derived Flk-1+ CD34+ progenitor cell chemotaxis and differentiation through a calcium-sensing receptor. Biochem Biophys Res Commun 2010, 393(1):156-161.
42. He Y., Zhang H., Teng J., Huang L., Li Y., Sun C. Involvement of calcium-sensing receptor in inhibition of lipolysis through intracellular cAMP and calcium pathways in human adipocytes. Biochem Biophys Res Commun 2011, 404(1):393-399.
43. Saidak Z., Brazier M., Kamel S., MentaverriAgonists R., Allosteric Modulators of the Calcium-Sensing Receptor and Their Therapeutic Applications. Mol Pharmacol 2009, 76(6):1131-1144.
44. Ara T., Hattori T., Fujinami Y. Pharmacological evidences for the stimulation of calcium-sensing receptors by nifedipine in gingival fibroblasts. JPharmacol 2011, 2(1):30-35.
45. Tada H., Nemoto E., Kanaya S., Hamaji N., Sato H., Shimauchi H. Elevated extracellular calcium increases expression of bone morphogenetic protein-2 gene via a calcium channel and ERK pathway in human dental pulp cells. Biochem Biophys Res Commun 2010, 394(4):1093-1097.
46. Piek E., Sleumer L.S., van Someren E.P., Heuver L., de Haan J.R., de Grijs I., et al. Osteo-transcriptomics of human mesenchymal stem cells: Accelerated gene expression and osteoblast differentiation induced by vitamin D reveals c-MYC as an enhancer of BMP2-induced osteogenesis. Bone 2010, 46(3):613-627.
47. Zhu L.-L., Zaidi S., Peng Y., Zhou H., Moonga B.S., Blesius A., et al. Induction of a program gene expression during osteoblast differentiation with strontium ranelate. Biochem Biophys Res Commun 2007, 355(2):307-311.
48. Verberckmoes S.C., De Broe M.E., D'Haese P.C. Dose-dependent effects of strontium on osteoblast function and mineralization. Kidney Int 2003, 64(2):534-543.
49. Takaoka S., Yamaguchi T., Yano S., Yamauchi M., Sugimoto T. The calcium-sensing receptor (CaR) is involved in strontium ranelate-induced osteoblast differentiation and mineralization. Horm Metab Res 2010, 42(09):627-631.
50. Hofer A.M., Brown E.M. Extracellular calcium sensing and signalling. Nat Rev Mol Cell Biol 2003, 4(7):530-538.
51. He Y.-H., He Y., Liao X.-L., Niu Y.-C., Wang G., Zhao C., et al. The calcium-sensing receptor promotes adipocyte differentiation and adipogenesis through PPAR-gamma pathway. Mol Cell Biochem 2012, 361(1):321-328.
52. Broadhead G.K., Mun H.C., Avlani V.A., Jourdon O., Church W.B., Christopoulos A., et al. Allosteric modulation of the calcium-sensing receptor by gamma-glutamyl peptides inhibition of PTH secretion, supression of intracellular cAMP levels, and a common mechanism of action with L-amino acids. JBiol Chem 2011, 286(11):8786-8797.
53. Zuccotti A., Clementi S., Reinbothe T., Torrente A., Vandael D.H., Pirone A. Structural and functional differences between L-type calcium channels: crucial issues for future selective targeting. Trends Pharmacol Sci 2011, 32(6):366-375.
54. Lacampagne A., Gannier Fo, Argibay J., Garnier D., Le Guennec J.-Y. The stretch-activated ion channel blocker gadolinium also blocks L-type calcium channels in isolated ventricular myocytes of the guinea-pig. Biochim Biophys Acta 1994, 1191(1):205-208.
55. Salzer U., Hinterdorfer P., Hunger U., Borken C., Prohaska R. Ca++-dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood 2002, 99(7):2569-2577.
56. Fu M., Zhang J., Lin Y., Zhu X., Zhao L., Ahmad M., et al. Early stimulation and late inhibition of peroxisome proliferator-activated receptor gamma (PPAR gamma) gene expression by transforming growth factor beta in human aortic smooth muscle cells: role of early growth-response factor-1 (Egr-1), activator protein 1 (AP1) and Smads. Biochem J 2003, 370(3):1019-1025.
57. Mayer S.I., Muller I., Mannebach S., Endo T., Thiel G. Signal transduction of pregnenolone sulfate in insulinoma cells. JBiol Chem 2011, 286(12):10084-10096.
58. Helvering L.M., Sharp R.L., Ou X., Geiser A.G. Regulation of the promoters for the human bone morphogenetic protein 2 and 4 genes. Gene 2000, 256(1-2):123-138.
59. Kim R.H., Shapiro H.S., Li J.J., Wrana J.L., Sodek J. Characterization of the human bone sialoprotein (BSP) gene and its promoter sequence. Matrix Biol 1994, 14(1):31-40.
60. Lammi J., Huppunen J., Aarnisalo P. Regulation of the osteopontin gene by the orphan nuclear receptor NURR1 in osteoblasts. Mol Endocrinol 2004, 18(6):1546-1557.
61. Pirih F.Q., Tang A., Ozkurt I.C., Nervina J.M., Tetradis S. Nuclear orphan receptor Nurr1 directly transactivates the osteocalcin gene in osteoblasts. JBiol Chem 2004, 279(51):53167-53174.
62. Kovalovsky Dn, Refojo Dn, Liberman A.C., Hochbaum D., Pereda M.P., Coso O.A., et al. Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: involvement of calcium, protein kinase A, and MAPK pathways. Mol Endocrinol 2002, 16(7):1638-1651.