Mineralization of three-dimensional osteoblast cultures is enhanced by the interaction of 1α,25-dihydroxyvitamin D3 and BMP2 via two specific vitamin D receptors

Journal of Tissue Engineering and Regenerative Medicine

Volumn 10, Issue 1, 2016, Pages 40-51

  Chen, Jiaxuan ^a   Dosier, Christopher R ^b   Park, Jung Hwa ^c   De, Subhendu ^a   Guldberg, Robert E ^b   Boyan, Barbara D ^a,d   Schwartz, Zvi ^a,d  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c Georgia Institute of Technology   (United States)

^d Virginia Commonwealth University   (United States)

Author keywords

1 ,25(OH)2D3; BMP2; Mineralization; Osteoblasts; Pdia3; Polycaprolactone scaffolds; VDR

Indexed keywords

CELL CULTURE; COMPUTERIZED TOMOGRAPHY; OSTEOBLASTS; POLYCAPROLACTONE; POLYMERASE CHAIN REACTION; SCAFFOLDS (BIOLOGY); SULFUR COMPOUNDS; VITAMINS;

1Α,25(OH)2D3; 3-D CULTURES; BONE MORPHOGENETIC PROTEIN-2; MINERALISATION; OSTEOBLAST MARKERS; POLYCAPROLACTONE SCAFFOLDS; PROTEIN DISULPHIDE ISOMERASE FAMILY A MEMBER 3; PROTEIN DISULPHIDE-ISOMERASE; VITAMIN D RECEPTOR; WILD TYPES;

MINERALOGY;

BONE MORPHOGENETIC PROTEIN 2; CALCITRIOL; MESSENGER RNA; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE FAMILY A MEMBER 3; TRANSCRIPTION FACTOR DLX5; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR; ALKALINE PHOSPHATASE; CALCITRIOL RECEPTOR; DIHYDROXY-VITAMIN D3; RECOMBINANT HUMAN BONE MORPHOGENETIC PROTEIN-2; RECOMBINANT PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VITAMIN D;

ARTICLE; BONE MINERALIZATION; CELL CULTURE; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; MICRO-COMPUTED TOMOGRAPHY; OSTEOBLAST; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE TECHNIQUE; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ALKALINE PHOSPHATASE; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CALCIFICATION, PHYSIOLOGIC; CELL CULTURE TECHNIQUES; CELL LINE; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENE SILENCING; MICE; OSTEOBLASTS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CALCITRIOL; RECOMBINANT PROTEINS; RNA, MESSENGER; TISSUE SCAFFOLDS; TRANSFORMING GROWTH FACTOR BETA; VITAMIN D;

EID: 84954368927     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1770     Document Type: Article

References (54)

1. Amling M, Priemel M, Holzmann T et al. 1999; Rescue of the skeletal phenotype of vitamin D receptor-ablated mice in the setting of normal mineral ion homeostasis: formal histomorphometric and biomechanical analyses. Endocrinology 140: 4982-4987.
2. Anagnostou F, Plas C, Nefussi JR et al. 1996; Role of βGP-derived Pi in mineralization via ecto-alkaline phosphatase in cultured fetal calvaria cells. J Cell Biochem 62: 262-274.
3. Bonewald LF, Harris SE, Rosser J et al. 2003; von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif Tissue Int 72: 537-547.
4. Bonewald LF, Kester MB, Schwartz Z et al. 1992; Effects of combining transforming growth factor-β and 1, 25-dihydroxyvitamin D3 on differentiation of a human osteosarcoma (MG-63). J Biol Chem 267: 8943-8949.
5. Boyan BD, Bonewald LF, Paschalis EP et al. 2002a; Osteoblast-mediated mineral deposition in culture is dependent on surface microtopography. Calcif Tissue Int 71: 519-529.
6. Boyan BD, Bonewald LF, Sylvia VL et al. 2002b; Evidence for distinct membrane receptors for 1α, 25(OH)2D3 and 24R, 25-(OH)2D3 in osteoblasts. Steroids 67: 235-246.
7. Boyan BD, Sylvia VL, Dean DD et al. 1999; 1α, 25-(OH)2D3 modulates growth plate chondrocytes via membrane receptor-mediated protein kinase C by a mechanism that involves changes in phospholipid metabolism and the action of arachidonic acid and PGE2. Steroids 64: 129-136.
8. Boyan BD, Sylvia VL, McKinney N et al. 2003; Membrane actions of vitamin D metabolites 1α, 25(OH)2D3 and 24R, 25(OH)2D3 are retained in growth plate cartilage cells from vitamin D receptor knockout mice. J Cell Biochem 90: 1207-1223.
9. Breen EC, van Wijnen AJ, Lian JB et al. 1994; In vivo occupancy of the vitamin D responsive element in the osteocalcin gene supports vitamin D-dependent transcriptional upregulation in intact cells. Proc Natl Acad Sci USA 91: 12902-12906.
10. Chen J, Lee CS, Coleman RM et al. 2009; Formation of tethers linking the epiphysis and metaphysis is regulated by vitamin d receptor-mediated signaling. Calcif Tissue Int 85: 134-145.
11. Chen J, Olivares-Navarrete R, Wang Y et al. 2010; Protein-disulphide isomerase-associated 3 (Pdia3) mediates the membrane response to 1, 25-dihydroxyvitamin D3 in osteoblasts. J Biol Chem 285: 37041-37050.
12. Doroudi M, Schwartz Z, Boyan BD. 2012; Phospholipase A2 activating protein is required for 1α, 25-dihydroxyvitamin D3 dependent rapid activation of protein kinase C via Pdia3. J Steroid Biochem Mol Biol 132: 48-56.
13. Dosier CR, Erdman CP, Park JH et al. 2012; Resveratrol effect on osteogenic differentiation of rat and human adipose derived stem cells in a 3D culture environment. J Mech Behav Biomed Mater 11: 112-122.
14. Ecarot B, Desbarats M. 1999; 1, 25-(OH)2D3 downregulates expression of Phex, a marker of the mature osteoblast. Endocrinology 140: 1192-1199.
15. Erdman CP, Dosier CR, Olivares-Navarrete R et al. 2012; Effects of resveratrol on enrichment of adipose-derived stem cells and their differentiation to osteoblasts in two- and three-dimensional cultures. J Tissue Eng Regen Med 6(suppl 3): s34-46.
16. Halvorsen YD, Franklin D, Bond AL et al. 2001; Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7: 729-741.
17. Hassan MQ, Tare RS, Lee SH et al. 2006; BMP2 commitment to the osteogenic lineage involves activation of Runx2 by DLX3 and a homeodomain transcriptional network. J Biol Chem 281: 40515-40526.
18. Helvering LM, Sharp RL, Ou X et al. 2000; Regulation of the promoters for the human bone morphogenetic protein 2 and 4 genes. Gene 256: 123-138.
19. Hiwada K, Wachsmuth ED. 1974; Catalytic properties of alkaline phosphatase from pig kidney. Biochem J 141: 283-291.
20. Holick MF. 2006; Resurrection of vitamin D deficiency and rickets. J Clin Invest 116: 2062-2072.
21. Holick MF. 2007; Vitamin D deficiency. N Engl J Med 357: 266-281.
22. Huhtakangas JA, Olivera CJ, Bishop JE et al. 2004; The vitamin D receptor is present in caveolae-enriched plasma membranes and binds 1α, 25(OH)2-vitamin D3 in vivo and in vitro. Mol Endocrinol 18: 2660-2671.
23. Jorgensen NR, Henriksen Z, Sorensen OH et al. 2004; Dexamethasone, BMP-2, and 1, 25-dihydroxyvitamin D enhance a more differentiated osteoblast phenotype: validation of an in vitro model for human bone marrow-derived primary osteoblasts. Steroids 69: 219-226.
24. Kawasaki K, Aihara M, Honmo J et al. 1998; Effects of recombinant human bone morphogenetic protein-2 on differentiation of cells isolated from human bone, muscle, and skin. Bone 23: 223-231.
25. Kraichely DM, MacDonald PN. 1998; Transcriptional activation through the vitamin D receptor in osteoblasts. Front Biosci 3: d821-833.
26. Lee CS, Chen J, Wang Y et al. 2011; Coordinated tether formation in anatomically distinct mice growth centers is dependent on a functional vitamin D receptor and is tightly linked to three-dimensional tissue morphology. Bone 49: 419-427.
27. Lee HJ, Ji Y, Paul S et al. 2007; Activation of bone morphogenetic protein signaling by a Gemini vitamin D3 analogue is mediated by Ras/protein kinase Cα. Cancer Res 67: 11840-11847.
28. Lee HJ, Wislocki A, Goodman C et al. 2006; A novel vitamin D derivative activates bone morphogenetic protein signaling in MCF10 breast epithelial cells. Mol Pharmacol 69: 1840-1848.
29. Lee MH, Kim YJ, Kim HJ et al. 2003; BMP-2-induced Runx2 expression is mediated by Dlx5, and TGFβ1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J Biol Chem 278: 34387-34394.
30. Li YC, Pirro AE, Amling M et al. 1997; Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 94: 9831-9835.
31. Lynch MP, Stein JL, Stein GS et al. 1995; The influence of type I collagen on the development and maintenance of the osteoblast phenotype in primary and passaged rat calvarial osteoblasts: modification of expression of genes supporting cell growth, adhesion, and extracellular matrix mineralization. Exp Cell Res 216: 35-45.
32. Martin JY, Schwartz Z, Hummert TW et al. 1995; Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res 29: 389-401.
33. Matsumoto T, Igarashi C, Takeuchi Y et al. 1991; Stimulation by 1, 25-dihydroxyvitamin D3 of in vitro mineralization induced by osteoblast-like MC3T3-E1 cells. Bone 12: 27-32.
34. Matsumoto T, Kawanobe Y, Morita K et al. 1985; Effect of 1, 25-dihydroxyvitamin D3 on phospholipid metabolism in a clonal osteoblast-like rat osteogenic sarcoma cell line. J Biol Chem 260: 13704-13709.
35. Mizwicki MT, Keidel D, Bula CM et al. 2004; Identification of an alternative ligand-binding pocket in the nuclear vitamin D receptor and its functional importance in 1α, 25(OH)2-vitamin D3 signaling. Proc Natl Acad Sci USA 101: 12876-12881.
36. Nishikawa J, Matsumoto M, Sakoda K et al. 1993; Vitamin D receptor zinc finger region binds to a direct repeat as a dimer and discriminates the spacing number between each half-site. J Biol Chem 268: 19739-19743.
37. Owen TA, Bortell R, Yocum SA et al. 1990; Coordinate occupancy of AP-1 sites in the vitamin D-responsive and CCAAT box elements by Fos-Jun in the osteocalcin gene: model for phenotype suppression of transcription. Proc Natl Acad Sci USA 87: 9990-9994.
38. Peister A, Deutsch ER, Kolambkar Y et al. 2009; Amniotic fluid stem cells produce robust mineral deposits on biodegradable scaffolds. Tissue Eng Part A 15: 3129-3138.
39. Peister A, Woodruff MA, Prince JJ et al. 2011; Cell sourcing for bone tissue engineering: amniotic fluid stem cells have a delayed, robust differentiation compared to mesenchymal stem cells. Stem Cell Res 7: 17-27.
40. Romberg RW, Werness PG, Riggs BL et al. 1986; Inhibition of hydroxyapatite crystal growth by bone-specific and other calcium-binding proteins. Biochemistry 25: 1176-1180.
41. Schwartz Z, Ehland H, Sylvia VL et al. 2002; 1α, 25-dihydroxyvitamin D3 and 24R, 25-dihydroxyvitamin D3 modulate growth plate chondrocyte physiology via protein kinase C-dependent phosphorylation of extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase. Endocrinology 143: 2775-2786.
42. Schwartz Z, Gilley RM, Sylvia VL et al. 1999; Prostaglandins mediate the effects of 1, 25-(OH)2D3 and 24, 25-(OH)2D3 on growth plate chondrocytes in a metabolite-specific and cell maturation-dependent manner. Bone 24: 475-484.
43. Schwartz Z, Schlader DL, Ramirez V et al. 1989; Effects of vitamin D metabolites on collagen production and cell proliferation of growth zone and resting zone cartilage cells in vitro. J Bone Miner Res 4: 199-207.
44. Schwartz Z, Sylvia VL, Liu Y et al. 1998; Treatment of resting zone chondrocytes with bone morphogenetic protein-2 induces maturation into a phenotype characteristic of growth zone chondrocytes by downregulating responsiveness to 24, 25(OH)2D3 and upregulating responsiveness to 1, 25-(OH)2D3. Endocrine 9: 273-280.
45. Schwartz Z, Sylvia VL, Luna MH et al. 2001; The effect of 24R, 25-(OH)2D3 on protein kinase C activity in chondrocytes is mediated by phospholipase D whereas the effect of 1α, 25-(OH)(2)D(3) is mediated by phospholipase C. Steroids 66: 683-694.
46. Sequeira VB, Rybchyn MS, Tongkao-On W et al. 2012; The role of the vitamin D receptor and ERp57 in photoprotection by 1α, 25-dihydroxyvitamin D3. Mol Endocrinol 26: 574-582.
47. Slater M, Patava J, Mason RS. 1994; Role of chondroitin sulphate glycosaminoglycans in mineralizing osteoblast-like cells: effects of hormonal manipulation. J Bone Miner Res 9: 161-169.
48. Sooy K, Sabbagh Y, Demay MB. 2005; Osteoblasts lacking the vitamin D receptor display enhanced osteogenic potential in vitro. J Cell Biochem 94: 81-87.
49. Ulsamer A, Ortuno MJ, Ruiz S et al. 2008; BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 283: 3816-3826.
50. Walters MR, Rosen DM, Norman AW et al. 1982; 1, 25-Dihydroxyvitamin D receptors in an established bone cell line. Correlation with biochemical responses. J Biol Chem 257: 7481-7484.
51. Wang Y, Chen J, Lee CS et al. 2010; Disruption of Pdia3 gene results in bone abnormality and affects 1α, 25-dihydroxy-vitamin D3-induced rapid activation of PKC. J Steroid Biochem Mol Biol 121: 257-260.
52. Yoshizawa T, Handa Y, Uematsu Y et al. 1997; Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 16: 391-396.
53. Zanello LP, Norman AW. 2004; Rapid modulation of osteoblast ion channel responses by 1α, 25(OH)2-vitamin D3 requires the presence of a functional vitamin D nuclear receptor. Proc Natl Acad Sci USA 101: 1589-1594.
54. Zella LA, Meyer MB, Nerenz RD et al. 2010; Multifunctional enhancers regulate mouse and human vitamin D receptor gene transcription. Mol Endocrinol 24: 128-147.