Chaperone properties of Pdia3 participate in rapid membrane actions of 1α,25-dihydroxyvitamin D3

Molecular Endocrinology

Volumn 27, Issue 7, 2013, Pages 1065-1077

  Chen, Jiaxuan ^a   Lobachev, Kirill S ^a   Grindel, Brian J ^b   Farach Carson, Mary C ^b   Hyzy, Sharon L ^a,c   El Baradie, Khairat B ^a   Olivares Navarrete, Rene ^a,c   Doroudi, Maryam ^a   Boyan, Barbara D ^a,c   Schwartz, Zvi ^a,c  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b RICE UNIVERSITY   (United States)

^c Virginia Commonwealth University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CALCITRIOL; CALRETICULIN; CAVEOLIN 1; CHAPERONE; ISOMERASE; MEMBRANE RECEPTOR; MUTANT PROTEIN; PHOSPHOLIPASE A2; PROSTAGLANDIN E2; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE FAMILY A MEMBER 3; PROTEIN KINASE C; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CATALYSIS; CELL CULTURE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE CONSTRUCT; GENE OVEREXPRESSION; MOUSE; MYRISTYLATION; NONHUMAN; ONCOGENE SRC; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; LIPOYLATION; MICE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; MYRISTIC ACIDS; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TUNICAMYCIN; VITAMIN D;

EID: 84879477869     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1277     Document Type: Article

References (72)

1. Chen J, Olivares-Navarrete R, Wang Y, Herman TR, Boyan BD, Schwartz Z. Protein-disulfide isomerase-associated 3 (Pdia3) mediates the membrane response to 1,25-dihydroxyvitamin D3 in osteoblasts. J Biol Chem. 2010;285:37041-37050.
2. Schwartz Z, Schlader DL, Ramirez V, Kennedy MB, Boyan BD. 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. 1989;4:199-207.
3. Tishkoff DX, Nibbelink KA, Holmberg KH, Dandu L, Simpson RU. Functional vitamin D receptor (VDR) in the t-tubules of cardiac myocytes: VDR knockout cardiomyocyte contractility. Endocrinology. 2008;149:558-564.
4. Becklund BR, Hansen DW Jr, Deluca HF. Enhancement of 1,25-dihydroxyvitamin D3-mediated suppression of experimental autoimmune encephalomyelitis by calcitonin. Proc Natl Acad Sci U S A. 2009;106:5276-5281.
5. Mathieu C, Waer M, Casteels K, Laureys J, Bouillon R. Prevention of type I diabetes inNODmice by nonhypercalcemic doses of a new structural analog of 1,25-dihydroxyvitamin D3, KH1060. Endocrinology. 1995;136:866-872.
6. Yudoh K, Matsuno H, Kimura T. 1α,25-Dihydroxyvitamin D3 inhibits in vitro invasiveness through the extracellular matrix and in vivo pulmonary metastasis of B16 mouse melanoma. J Lab Clin Med. 1999;133:120-128.
7. Lee HJ, Paul S, Atalla N, et al. Gemini vitamin D analogues inhibit estrogen receptor-positive and estrogen receptor-negative mammary tumorigenesis without hypercalcemic toxicity. Cancer Prev Res (Phila). 2008;1:476-484.
8. Wali RK, Bissonnette M, Khare S, Hart J, Sitrin MD, Brasitus TA. 1α,25-Dihydroxy-16-ene-23-yne-26,27-hexafluorocholecalciferol, a noncalcemic analogue of 1α,25-dihydroxyvitamin D3, inhibits azoxymethane-induced colonic tumorigenesis. Cancer Res. 1995; 55:3050-3054.
9. Boyan BD, Sylvia VL, Dean DD, et al. 1,25-(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. 1999;64:129-136.
10. Schwartz Z, Gilley RM, Sylvia VL, Dean DD, Boyan BD. 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. 1999;24:475-484.
11. Schwartz Z, Graham EJ, Wang L, et al. Phospholipase A2 activating protein (PLAA) is required for 1α,25(OH)2D3 signaling in growth plate chondrocytes. J Cell Physiol. 2005;203:54-70.
12. Doroudi M, Schwartz Z, Boyan BD. Phospholipase A2 activating protein is required for 1α,25-dihydroxyvitaminD3 dependent rapid activation of protein kinase C via Pdia3. J Steroid Biochem Mol Biol. 2012;132:48-56.
13. Boyan BD, Wang L, Wong KL, Jo H, Schwartz Z. Plasma membrane requirements for 1α,25(OH)2D3 dependent PKC signaling in chondrocytes and osteoblasts. Steroids. 2006;71:286-290.
14. Schwartz Z, Sylvia VL, Luna MH, et al. 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)2D3 is mediated by phospholipase C. Steroids. 2001;66:683-694.
15. Schwartz Z, Ehland H, Sylvia VL, Let al. 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. 2002;143:2775-2786.
16. Buitrago C, Vazquez G, De Boland AR, Boland RL. Activation of Src kinase in skeletal muscle cells by 1,25-(OH2)-vitamin D3 correlates with tyrosine phosphorylation of the vitamin D receptor (VDR) and VDR-Src interaction. J Cell Biochem. 2000;79:274-281.
17. Boland R, De Boland AR, Buitrago C, et al. Non-genomic stimulation of tyrosine phosphorylation cascades by 1,25(OH)2D3 by VDR-dependent and-independent mechanisms in muscle cells. Steroids. 2002;67:477-482.
18. Buitrago C, Vazquez G, De Boland AR, Boland R. The vitamin D receptor mediates rapid changes in muscle protein tyrosine phosphorylation induced by 1,25(OH)2D3. Biochem Biophys Res Commun. 2001;289:1150-1156.
19. Nemere I, Garbi N, Hämmerling GJ, Khanal RC. 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. 2010;285:31859-31866.
20. Van Cromphaut SJ, Dewerchin M, Hoenderop JG, et al. Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects. Proc Natl Acad Sci U S A. 2001;98: 13324-13329.
21. Nemere I, Dormanen MC, Hammond MW, Okamura WH, Norman AW. Identification of a specific binding protein for 1α,25-dihydroxyvitamin D3 in basal-lateral membranes of chick intestinal epithelium and relationship to transcaltachia. J Biol Chem. 1994; 269:23750-23756.
22. Nemere I, Farach-Carson MC, Rohe B, et al. Ribozyme knockdown functionally links a 1,25(OH)2D3 membrane binding protein (1,25D3-MARRS) and phosphate uptake in intestinal cells. Proc Natl Acad Sci U S A. 2004;101:7392-7397.
23. Nemere I, Schwartz Z, Pedrozo H, Sylvia VL, Dean DD, Boyan BD. Identification of a membrane receptor for 1,25-dihydroxyvitamin D3 which mediates rapid activation of protein kinase C. J Bone Miner Res. 1998;13:1353-1359.
24. Boyan BD, Bonewald LF, Sylvia VL, et al. Evidence for distinct membrane receptors for 1α,25-(OH)2D3 and 24R,25-(OH)2D3 in osteoblasts. Steroids. 2002;67:235-246.
25. Pedrozo HA, Schwartz Z, Rimes S, et al. Physiological importance of the 1,25(OH)2D3 membrane receptor and evidence for a membrane receptor specific for 24,25(OH)2D3. J Bone Miner Res. 1999; 14:856-867.
26. Schwartz Z, Shaked D, Hardin RR, et al. 1α,25(OH)2D3 causes a rapid increase in phosphatidylinositol-specific PLC-β activity via phospholipase A2-dependent production of lysophospholipid. Steroids. 2003;68:423-437.
27. Boyan BD, Sylvia VL, McKinney N, Schwartz Z. 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. 2003;90:1207-1223.
28. Olivares-Navarrete R, Sutha K, Hyzy SL, et al. Osteogenic differentiation of stem cells alters vitamin D receptor expression. Stem Cells Dev. 2012;21:1726-1735.
29. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307:1625-1630.
30. Boyan BD, Wong KL, Wang L, et al. Regulation of growth plate chondrocytes by 1,25-dihydroxyvitamin D3 requires caveolae and caveolin-1. J Bone Miner Res. 2006;21:1637-1647.
31. Garbi N, Tanaka S, Momburg F, Hämmerling GJ. Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat Immunol. 2006;7:93-102.
32. Costa JL, Eijk PP, van de Wiel MA, et al. Anti-proliferative action of vitaminDin MCF7 is still active after siRNA-VDR knock-down. BMC Genomics. 2009;10:499.
33. Sylvia VL, Schwartz Z, Ellis EB, et al. Nongenomic regulation of protein kinase C isoforms by the vitamin D metabolites 1α,25-(OH)2D3 and 24R,25-(OH)2D3. J Cell Physiol. 1996;167:380-393.
34. Lindquist JA, Jensen ON, Mann M, Hämmerling GJ. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J. 1998;17:2186-2195.
35. Peaper DR, Wearsch PA, Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 2005;24:3613-3623.
36. Peaper DR, Cresswell P. The redox activity of ERp57 is not essential for its functions inMHCclass I peptide loading. Proc Natl Acad Sci U S A. 2008;105:10477-10482.
37. Kim YS, MacDonald PN, Dedhar S, Hruska KA. Association of 1α,25-dihydroxyvitaminD3-occupied vitaminDreceptors with cellular membrane acceptance sites. Endocrinology. 1996;137:3649-3658.
38. Kozlov G, Maattanen P, Schrag JD, et al. Crystal structure of the bb domains of the protein disulfide isomerase ERp57. Structure. 2006;14:1331-1339.
39. Beynon-Jones SM, Antoniou AN, Powis SJ. Mutational analysis of the oxidoreductase ERp57 reveals the importance of the two central residues in the redox motif. FEBS Lett. 2006;580:1897-1902.
40. Hirano N, Shibasaki F, Sakai R, 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. 1995;234: 336-342.
41. Frickel EM, Riek R, Jelesarov I, Helenius A, Wuthrich K, Ellgaard L. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc Natl Acad Sci U S A. 2002;99: 1954-1959.
42. Leach MR, Cohen-Doyle MF, Thomas DY, Williams DB. Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J Biol Chem. 2002;277:29686-29697.
43. Wu W, Beilhartz G, Roy Y, et al. Nuclear translocation of the 1,25D3-MARRS (membrane associated rapid response to steroids) receptor protein and NFκB in differentiating NB4 leukemia cells. Exp Cell Res. 2010;316:1101-1108.
44. Grindel BJ, Rohe B, Safford SE, Bennett JJ, Farach-Carson MC. Tumor necrosis factor-α treatment of HepG2 cells mobilizes a cytoplasmic pool of ERp57/1,25D3-MARRS to the nucleus. J Cell Biochem. 2011;112:2606-2615.
45. Schwartz Z, Schlader DL, Swain LD, Boyan BD. 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. 1988;123:2878-2884.
46. Acconcia F, Ascenzi P, Bocedi A, et al. Palmitoylation-dependent estrogen receptor α membrane localization: regulation by 17β-estradiol. Mol Biol Cell. 2005;16:231-237.
47. Marino M, Ascenzi P. Steroid hormone rapid signaling: the pivotal role of S-palmitoylation. IUBMB Life. 2006;58:716-719.
48. Li L, Haynes MP, Bender JR. Plasma membrane localization and function of the estrogen receptor α variant (ER46) in human endothelial cells. Proc Natl Acad Sci U S A. 2003;100:4807-4812.
49. Franceschi RT, Iyer BS, Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res. 1994;9:843-854.
50. Huhtakangas JA, Olivera CJ, Bishop JE, Zanello LP, Norman AW. 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. 2004;18:2660-2671.
51. Perret B, Chap HJ, Douste-Blazy L. Asymmetric distribution of arachidonic acid in the plasma membrane of human platelets. A determination using purified phospholipases and a rapid method for membrane isolation. Biochim Biophys Acta. 1979;556:434-446.
52. 2+ receptor is essential for its expression at the cell surface. Endocrinology. 1997;138:1916-1922.
53. Vaandrager AB, Ehlert EM, Jarchau T, Lohmann SM, de Jonge HR. N-terminal myristoylation is required for membrane localization of cGMP-dependent protein kinase type II. J Biol Chem. 1996; 271:7025-7029.
54. Obeid M. ERP57 membrane translocation dictates the immunogenicity of tumor cell death by controlling the membrane translocation of calreticulin. J Immunol. 2008;181:2533-2543.
55. Coppolino MG, Woodside MJ, Demaurex N, Grinstein S, St-Arnaud R, Dedhar S. Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature. 1997;386:843-847.
56. Rendon-Huerta E, Mendoza-Hernandez G, Robles-Flores M. Characterization of calreticulin as a protein interacting with protein kinase C. Biochem J. 1999;344(Pt 2):469-475.
57. Liu R, Li W, Karin NJ, Bergh JJ, Adler-Storthz K, Farach-Carson MC. Ribozyme ablation demonstrates that the cardiac subtype of the voltage-sensitive calcium channel is the molecular transducer of 1, 25-dihydroxyvitamin D3-stimulated calcium influx in osteoblastic cells. J Biol Chem. 2000;275:8711-8718.
58. Buitrago C, Boland R. Caveolae and caveolin-1 are implicated in 1α,25(OH)2-vitamin D3-dependent modulation of Src, MAPK cascades and VDR localization in skeletal muscle cells. J Steroid Biochem Mol Biol. 2010;121:169-175.
59. Eufemi M, Coppari S, Altieri F, Grillo C, Ferraro A, Turano C. ERp57 is present in STAT3-DNA complexes. Biochem Biophys Res Commun. 2004;323:1306-1312.
60. Elliott JG, Oliver JD, High S. The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins. J Biol Chem. 1997;272:13849-13855.
61. Clive DR, Greene JJ. Cooperation of protein disulfide isomerase and redox environment in the regulation of NF-κB and AP1 binding to DNA. Cell Biochem Funct. 1996;14:49-55.
62. Grillo C, D'Ambrosio C, Scaloni A, et al. Cooperative activity of Ref-1/APE and ERp57 in reductive activation of transcription factors. Free Rad Biol Med. 2006;41:1113-1123.
63. Langer MD, Guo H, Shashikanth N, Pierce JM, Leckband DE. N-glycosylation alters cadherin-mediated intercellular binding kinetics. J Cell Sci. 2012;125(Pt 10):2478-2485.
64. Uittenbogaard A, Smart EJ. Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae [retracted in: J Biol Chem. 2013;288:6585]. J Biol Chem. 2000;275:25595-25599.
65. Khanal RC, Nemere I. The ERp57/GRp58/1,25D3-MARRS receptor: multiple functional roles in diverse cell systems. Curr Med Chem. 2007;14:1087-1093.
66. Schwartz Z, Sylvia VL, Larsson D, et al. 1α,25(OH)2D3 regulates chondrocyte matrix vesicle protein kinase C (PKC) directly via Gprotein-dependent mechanisms and indirectly via incorporation of PKC during matrix vesicle biogenesis. J Biol Chem. 2002;277: 11828-11837.
67. Mumby SM, Heukeroth RO, Gordon JI, Gilman AG. G-protein α-subunit expression, myristoylation, and membrane association in COS cells. Proc Natl Acad Sci U S A. 1990;87:728-732.
68. David-Pfeuty T, Bagrodia S, Shalloway D. Differential localization patterns of myristoylated and nonmyristoylated c-Src proteins in interphase and mitotic c-Src overexpresser cells. J Cell Sci. 1993; 105(Pt 3):613-628.
69. Rollins TE, Smith WL. Subcellular localization of prostaglandinforming cyclooxygenase in Swiss mouse 3T3 fibroblasts by electron microscopic immunocytochemistry. J Biol Chem. 1980;255:4872-4875.
70. Muthalif MM, Benter IF, Uddin MR, Malik KU. Calcium/calmodulin-dependent protein kinase IIα mediates activation of mitogenactivated protein kinase and cytosolic phospholipase A2 in norepinephrine-induced arachidonic acid release in rabbit aortic smooth muscle cells. J Biol Chem. 1996;271:30149-30157.
71. Sylvia VL, Schwartz Z, Schuman L, et al. Maturation-dependent regulation of protein kinase C activity by vitamin D3 metabolites in chondrocyte cultures. J Cell Physiol. 1993;157:271-278.
72. Swain LD, Schwartz Z, Boyan BD. 1,25-(OH)2D3 and 24,25-(OH)2D3 regulation of arachidonic acid turnover in chondrocyte cultures is cell maturation-specific and may involve direct effects on phospholipase A2. Biochim Biophys Acta. 1992;1136:45-51.