New insights on membrane mediated effects of 1α,25-dihydroxy vitamin D3 signaling in the musculoskeletal system

Steroids

Volumn 81, Issue , 2014, Pages 81-87

  Doroudi, Maryam ^a   Chen, Jiaxuan ^a,b   Boyan, Barbara D ^a,c   Schwartz, Zvi ^c,d  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

BMP2; CaMKII; Mineralization; Osteoblast; Pdia3

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CAVEOLIN 1; COLECALCIFEROL; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE A2; PHOSPHOLIPASE C; PROTEIN DISULFIDE ISOMERASE; CALCITRIOL RECEPTOR; DIHYDROXY-VITAMIN D3; PDIA3 PROTEIN, HUMAN; PDIA3 PROTEIN, MOUSE; VDR PROTEIN, HUMAN; VITAMIN D;

CAVEOLA; CELL MEMBRANE; MINERALIZATION; MUSCULOSKELETAL SYSTEM; MUTAGENESIS; NONHUMAN; PHENOTYPE; REVIEW; ANALOGS AND DERIVATIVES; ANIMAL; BONE MINERALIZATION; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CAVEOLAE; CAVEOLIN 1; CELL MEMBRANE; HUMANS; MICE; MUSCULOSKELETAL SYSTEM; PROTEIN DISULFIDE-ISOMERASES; RECEPTORS, CALCITRIOL; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES; VITAMIN D;

EID: 84895544922     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2013.10.019     Document Type: Review

References (81)

1. M. Garabedian, E. Pezant, L. Miravet, C. Fellot, and S. Balsan 1,25-Dihydroxycholecalciferol effect on serum phosphorus homeostasis in rats Endocrinology 98 1976 794 799
2. R. Kumar Metabolism of 1,25-dihydroxyvitamin D3 Physiol Rev 64 1984 478 504
3. 3-MARRS) and phosphate uptake in intestinal cells Proc Natl Acad Sci USA 101 2004 7392 7397
4. 3 on calcium ion fluxes in costochondral chondrocyte cultures Calcif Tissue Int 47 1990 230 236
5. A.W. Norman, W.H. Okamura, M.C. Farach-Carson, K. Allewaert, D. Branisteanu, and I. Nemere et al. Structure-function studies of 1,25-dihydroxyvitamin D3 and the vitamin D endocrine system. 1,25-Dihydroxy-pentadeuterio-previtamin D3 (as a 6-s-cis analog) stimulates nongenomic but not genomic biological responses J Biol Chem 268 1993 13811 13819
6. R. Liu, W. Li, N.J. Karin, J.J. Bergh, K. Adler-Storthz, and M.C. Farach-Carson Ribozyme ablation demonstrates that the cardiac subtype of the voltage-sensitive calcium channel is the molecular transducer of 1, 25-dihydroxyvitamin D(3)-stimulated calcium influx in osteoblastic cells J Biol Chem 275 2000 8711 8718
7. 3 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 1999 129 136
8. Z. Schwartz, H. Ehland, V.L. Sylvia, D. Larsson, R.R. Hardin, and V. Bingham et al. 1Alpha,25-dihydroxyvitamin D(3) and 24R,25-dihydroxyvitamin D(3) modulate growth plate chondrocyte physiology via protein kinase C-dependent phosphorylation of extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase Endocrinology 143 2002 2775 2786
9. 2-vitamin D3 and analogs through the ligand binding domain of the vitamin D receptor in osteoblasts and osteocytes. Mediation by Src, phosphatidylinositol 3-, and JNK kinases J Biol Chem 280 2005 14130 14137
10. 2 vitamin D3-induced anti-apoptotic PI3K/AKT signaling in osteoblasts J Bone Miner Res 23 2008 1238 1248
11. J. Chen, M. Doroudi, J. Cheung, A.L. Grozier, Z. Schwartz, and B.D. Boyan Plasma membrane Pdia3 and VDR interact to elicit rapid responses to 1alpha,25(OH)D Cell Signal 2013
12. J. Chen, R. Olivares-Navarrete, Y. Wang, T.R. Herman, B.D. Boyan, and Z. Schwartz Protein-disulfide isomerase-associated 3 (Pdia3) mediates the membrane response to 1,25-dihydroxy vitamin D3 in osteoblasts J Biol Chem 285 2010 37041 37050
13. M. Lieberherr Effects of vitamin D3 metabolites on cytosolic free calcium in confluent mouse osteoblasts J Biol Chem 262 1987 13168 13173
14. S. Morelli, A.R. de Boland, and R.L. Boland Generation of inositol phosphates, diacylglycerol and calcium fluxes in myoblasts treated with 1,25-dihydroxy vitamin D3 Biochem J 289 Pt 3 1993 675 679
15. W. Tang, V.A. Ziboh, R.R. Isseroff, and D. Martinez Novel regulatory actions of 1 alpha,25-dihydroxyvitamin D3 on the metabolism of polyphosphoinositides in murine epidermal keratinocytes J Cell Physiol 132 1987 131 136
16. 3 signaling in growth plate chondrocytes J Cell Physiol 203 2005 54 70
17. M. Doroudi, Z. Schwartz, and B.D. Boyan Phospholipase A2 activating protein is required for 1alpha,25-dihydroxyvitamin D3 dependent rapid activation of protein kinase C via Pdia3 J Steroid Biochem Mol Biol 132 2012 48 56
18. M. Doroudi, Z. Schwartz, and B.D. Boyan Phospholipase A(2) activating protein is required for 1alpha,25-dihydroxyvitamin D(3) dependent rapid activation of protein kinase C via Pdia3 J Steroid Biochem Mol Biol 132 2012 48 56
19. M.M. Muthalif, I.F. Benter, M.R. Uddin, and K.U. Malik Calcium/calmodulin-dependent protein kinase IIalpha mediates activation of mitogen-activated protein kinase and cytosolic phospholipase A2 in norepinephrine-induced arachidonic acid release in rabbit aortic smooth muscle cells J Biol Chem 271 1996 30149 30157
20. Y. Song, S. Kato, and J.C. Fleet Vitamin D receptor (VDR) knockout mice reveal VDR-independent regulation of intestinal calcium absorption and ECaC2 and calbindin D9k mRNA J Nutr 133 2003 374 380
21. 3 are retained in growth plate cartilage cells from vitamin D receptor knockout mice J Cell Biochem 90 2003 1207 1223
22. R.K. Wali, J. Kong, M.D. Sitrin, M. Bissonnette, and Y.C. Li Vitamin D receptor is not required for the rapid actions of 1,25-dihydroxyvitamin D3 to increase intracellular calcium and activate protein kinase C in mouse osteoblasts J Cell Biochem 88 2003 794 801
23. 3 J Cell Physiol 167 1996 380 393
24. S. Maeda, D.D. Dean, V.L. Sylvia, B.D. Boyan, and Z. Schwartz Metalloproteinase activity in growth plate chondrocyte cultures is regulated by 1,25-(OH)(2)D(3) and 24,25-(OH)(2)D(3) and mediated through protein kinase C Matrix Biol 20 2001 87 97
25. J.L. Costa, P.P. Eijk, M.A. van de Wiel, D. ten Berge, F. Schmitt, and C.J. Narvaez et al. Anti-proliferative action of vitamin D in MCF7 is still active after siRNA-VDR knock-down BMC Genomics 10 2009 499
26. N. Garbi, S. Tanaka, F. Momburg, and G.J. Hammerling Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57 Nat Immunol 7 2006 93 102
27. J.A. Lindquist, O.N. Jensen, M. Mann, and G.J. Hammerling ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly EMBO J 17 1998 2186 2195
28. H. Coe, J. Jung, J. Groenendyk, D. Prins, and M. Michalak ERp57 modulates STAT3 signaling from the lumen of the endoplasmic reticulum J Biol Chem 285 2010 6725 6738
29. Y. Wang, J. Chen, C.S. Lee, A. Nizkorodov, K. Riemenschneider, and D. Martin et al. Disruption of Pdia3 gene results in bone abnormality and affects 1alpha,25-dihydroxy-vitamin D3-induced rapid activation of PKC J Steroid Biochem Mol Biol 121 2010 257 260
30. I. Nemere, N. Garbi, G.J. Hammerling, and R.C. Khanal Intestinal cell calcium uptake and the targeted knockout of the 1,25D3-MARRS (membrane-associated, rapid response steroid-binding) receptor/PDIA3/Erp57 J Biol Chem 285 2010 31859 31866
31. T. Yoshizawa, Y. Handa, Y. Uematsu, S. Takeda, K. Sekine, and Y. Yoshihara et al. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning Nat Genet 16 1997 391 396
32. Y.C. Li, A.E. Pirro, M. Amling, G. Delling, R. Baron, and R. Bronson et al. 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 1997 9831 9835
33. N. Akutsu, R. Lin, Y. Bastien, A. Bestawros, D.J. Enepekides, and M.J. Black et al. Regulation of gene expression by 1alpha,25-dihydroxyvitamin D3 and its analog EB1089 under growth-inhibitory conditions in squamous carcinoma cells Mol Endocrinol 15 2001 1127 1139
34. K. Towsend, V. Trevino, F. Falciani, P.M. Stewart, M. Hewison, and M.J. Campbell Identification of VDR-responsive gene signatures in breast cancer cells Oncology 71 2006 111 123
35. Z. Schwartz, D.L. Schlader, V. Ramirez, M.B. Kennedy, and B.D. Boyan 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 1989 199 207
36. R. Gniadecki Activation of Raf-mitogen-activated protein kinase signaling pathway by 1,25-dihydroxyvitamin D3 in normal human keratinocytes J Invest Dermatol 106 1996 1212 1217
37. C. Johansen, L. Iversen, A. Ryborg, and K. Kragballe 1alpha,25- dihydroxyvitamin D3 induced differentiation of cultured human keratinocytes is accompanied by a PKC-independent regulation of AP-1 DNA binding activity J Invest Dermatol 114 2000 1174 1179
38. Z. Xiaoyu, B. Payal, O. Melissa, and L.P. Zanello 1alpha,25(OH)2-vitamin D3 membrane-initiated calcium signaling modulates exocytosis and cell survival J Steroid Biochem Mol Biol 103 2007 457 461
39. I. Nemere, and A.W. Norman The rapid, hormonally stimulated transport of calcium (transcaltachia) J Bone Miner Res 2 1987 167 169
40. 2+ influx in skeletal muscle cells. Modulation by phospholipase c, protein kinase c, and tyrosine kinases J Biol Chem 273 1998 33954 33960
41. J.M. Caffrey, and M.C. Farach-Carson Vitamin D3 metabolites modulate dihydropyridine-sensitive calcium currents in clonal rat osteosarcoma cells J Biol Chem 264 1989 20265 20274
42. L.P. Zanello, and A.W. Norman Multiple molecular mechanisms of 1 alpha,25(OH)2-vitamin D3 rapid modulation of three ion channel activities in osteoblasts Bone 33 2003 71 79
43. X. Wu, and C.T. McMurray Calmodulin kinase II attenuation of gene transcription by preventing cAMP response element-binding protein (CREB) dimerization and binding of the CREB-binding protein J Biol Chem 276 2001 1735 1741
44. L.A. Zella, M.B. Meyer, R.D. Nerenz, S.M. Lee, M.L. Martowicz, and J.W. Pike Multifunctional enhancers regulate mouse and human vitamin D receptor gene transcription Mol Endocrinol 24 2010 128 147
45. S. Jalvy, M.A. Renault, L. Lam Shang Leen, I. Belloc, A. Reynaud, and A.P. Gadeau et al. CREB mediates UTP-directed arterial smooth muscle cell migration and expression of the chemotactic protein osteopontin via its interaction with activator protein-1 sites Circ Res 100 2007 1292 1299
46. B.H. Chang, S. Mukherji, and T.R. Soderling Characterization of a calmodulin kinase II inhibitor protein in brain Proc Natl Acad Sci USA 95 1998 10890 10895
47. V.L. Sylvia, F. Del Toro, D.D. Dean, R.R. Hardin, Z. Schwartz, and B.D. Boyan Effects of 1alpha,25-(OH)(2)D(3) on rat growth zone chondrocytes are mediated via cyclooxygenase-1 and phospholipase A(2) J Cell Biochem Suppl 36 2001 32 45 [Suppl]
48. J.D. Oliver, F.J. van der Wal, N.J. Bulleid, and S. High Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins Science 275 1997 86 88
49. J.G. Elliott, J.D. Oliver, and S. High The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins J Biol Chem 272 1997 13849 13855
50. B.J. Grindel, B. Rohe, S.E. Safford, J.J. Bennett, and M.C. Farach-Carson Tumor necrosis factor-alpha treatment of HepG2 cells mobilizes a cytoplasmic pool of ERp57/1,25D-MARRS to the nucleus J Cell Biochem 112 2011 2606 2615
51. S. Coppari, F. Altieri, A. Ferraro, S. Chichiarelli, M. Eufemi, and C. Turano Nuclear localization and DNA interaction of protein disulfide isomerase ERp57 in mammalian cells J Cell Biochem 85 2002 325 333
52. G. Kozlov, P. Maattanen, J.D. Schrag, S. Pollock, M. Cygler, and B. Nagar et al. Crystal structure of the bb′ domains of the protein disulfide isomerase ERp57 Structure 14 2006 1331 1339
53. D.R. Peaper, and P. Cresswell The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading Proc Natl Acad Sci USA 105 2008 10477 10482
54. S.M. Beynon-Jones, A.N. Antoniou, and S.J. Powis Mutational analysis of the oxidoreductase ERp57 reveals the importance of the two central residues in the redox motif FEBS Lett 580 2006 1897 1902
55. N. Hirano, F. Shibasaki, R. Sakai, T. Tanaka, J. Nishida, and Y. Yazaki et al. Molecular cloning of the human glucose-regulated protein ERp57/GRP58, a thiol-dependent reductase. Identification of its secretory form and inducible expression by the oncogenic transformation Eur J Biochem 234 1995 336 342
56. E.M. Frickel, R. Riek, I. Jelesarov, A. Helenius, K. Wuthrich, and L. Ellgaard TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain Proc Natl Acad Sci USA 99 2002 1954 1959
57. Z. Schwartz, D.L. Schlader, L.D. Swain, and B.D. Boyan Direct effects of 1,25-dihydroxyvitamin D3 and 24,25-dihydroxyvitamin D3 on growth zone and resting zone chondrocyte membrane alkaline phosphatase and phospholipase-A2 specific activities Endocrinology 123 1988 2878 2884
58. F. Acconcia, P. Ascenzi, A. Bocedi, E. Spisni, V. Tomasi, and A. Trentalance et al. Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol Mol Biol Cell 16 2005 231 237
59. J. Chen, K.S. Lobachev, B.J. Grindel, M.C. Farach-Carson, S.L. Hyzy, and K.B. El-Baradie et al. Chaperone properties of pdia3 participate in rapid membrane actions of 1alpha,25-dihydroxyvitamin d3 Mol Endocrinol 27 2013 1065 1077
60. B.D. Boyan, K.L. Wong, L. Wang, H. Yao, R.E. Guldberg, and M. Drab et al. Regulation of growth plate chondrocytes by 1,25-dihydroxyvitamin D3 requires caveolae and caveolin-1 J Bone Miner Res 21 2006 1637 1647
61. M.F. Holick Resurrection of vitamin D deficiency and rickets J Clin Invest 116 2006 2062 2072
62. M.F. Holick Vitamin D deficiency N Engl J Med 357 2007 266 281
63. J.A. Huhtakangas, C.J. Olivera, J.E. Bishop, L.P. Zanello, and A.W. Norman The vitamin D receptor is present in caveolae-enriched plasma membranes and binds 1 alpha,25(OH)2-vitamin D3 in vivo and in vitro Mol Endocrinol 18 2004 2660 2671
64. M.R. Walters, D.M. Rosen, A.W. Norman, and R.A. Luben 1,25-Dihydroxyvitamin D receptors in an established bone cell line. Correlation with biochemical responses J Biol Chem 257 1982 7481 7484
65. B.D. Boyan, L.F. Bonewald, V.L. Sylvia, I. Nemere, D. Larsson, and A.W. Norman et al. Evidence for distinct membrane receptors for 1 alpha,25-(OH)(2)D(3) and 24R,25-(OH)(2)D(3) in osteoblasts Steroids 67 2002 235 246
66. M.T. Mizwicki, D. Keidel, C.M. Bula, J.E. Bishop, L.P. Zanello, and J.M. Wurtz et al. Identification of an alternative ligand-binding pocket in the nuclear vitamin D receptor and its functional importance in 1alpha,25(OH)2- vitamin D3 signaling Proc Natl Acad Sci USA 101 2004 12876 12881
67. L.P. Zanello, and A.W. Norman Rapid modulation of osteoblast ion channel responses by 1alpha,25(OH)2-vitamin D3 requires the presence of a functional vitamin D nuclear receptor Proc Natl Acad Sci USA 101 2004 1589 1594
68. D.M. Kraichely, and P.N. MacDonald Transcriptional activation through the vitamin D receptor in osteoblasts Front Biosci 3 1998 d821 d833
69. E.C. Breen, A.J. van Wijnen, J.B. Lian, G.S. Stein, and J.L. Stein 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 1994 12902 12906
70. M. Amling, M. Priemel, T. Holzmann, K. Chapin, J.M. Rueger, and R. Baron et al. 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 1999 4982 4987
71. C.S. Lee, J. Chen, Y. Wang, J.K. Williams, D.M. Ranly, and Z. Schwartz et al. 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 2011 419 427
72. J. Chen, C.S. Lee, R.M. Coleman, J.Y. Yoon, C.H. Lohmann, and J. Zustin et al. Formation of tethers linking the epiphysis and metaphysis is regulated by vitamin d receptor-mediated signaling Calcif Tissue Int 85 2009 134 145
73. T. Matsumoto, C. Igarashi, Y. Takeuchi, S. Harada, T. Kikuchi, and H. Yamato et al. Stimulation by 1,25-dihydroxyvitamin D3 of in vitro mineralization induced by osteoblast-like MC3T3-E1 cells Bone 12 1991 27 32
74. Y.D. Halvorsen, D. Franklin, A.L. Bond, D.C. Hitt, C. Auchter, and A.L. Boskey et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells Tissue Eng 7 2001 729 741
75. T. Matsumoto, Y. Kawanobe, K. Morita, and E. Ogata Effect of 1,25-dihydroxyvitamin D3 on phospholipid metabolism in a clonal osteoblast-like rat osteogenic sarcoma cell line J Biol Chem 260 1985 13704 13709
76. M. Slater, J. Patava, and R.S. Mason Role of chondroitin sulfate glycosaminoglycans in mineralizing osteoblast-like cells: effects of hormonal manipulation J Bone Miner Res 9 1994 161 169
77. M.P. Lynch, J.L. Stein, G.S. Stein, and J.B. Lian 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 1995 35 45
78. 3 down-regulates expression of Phex, a marker of the mature osteoblast Endocrinology 140 1999 1192 1199
79. L.F. Bonewald, S.E. Harris, J. Rosser, M.R. Dallas, S.L. Dallas, and N.P. Camacho et al. Von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation Calcif Tissue Int 72 2003 537 547
80. B.D. Boyan, L.F. Bonewald, E.P. Paschalis, C.H. Lohmann, J. Rosser, and D.L. Cochran et al. Osteoblast-mediated mineral deposition in culture is dependent on surface microtopography Calcif Tissue Int 71 2002 519 529
81. 3 causes a rapid increase in phosphatidylinositol-specific PLC-beta activity via phospholipase A2-dependent production of lysophospholipid Steroids 68 2003 423 437