H2O2-dependent translocation of TCTP into the nucleus enables its interaction with VDR in human keratinocytes: TCTP as a further module in calcitriol signalling

Journal of Steroid Biochemistry and Molecular Biology

Volumn 118, Issue 1-2, 2010, Pages 29-40

  Rid, Raphaela ^a   Önder, Kamil ^a,b   Trost, Andrea ^b   Bauer, Johann ^b   Hintner, Helmut ^b   Ritter, Markus ^c   Jakab, Martin ^c   Costa, Ivano ^c   Reischl, Wolfgang ^d   Richter, Klaus ^a   MacDonald, Susan ^e   Jendrach, Marina ^f   Bereiter Hahn, Jürgen ^f   Breitenbach, Michael ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b Department of Dermatology   (Austria)

^c PARACELSUS MEDICAL UNIVERSITY   (Austria)

^d UNIVERSITY OF VIENNA   (Austria)

^e JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

^f GOETHE UNIVERSITY   (Germany)

Author keywords

Protein protein interaction; Skin; TCTP; VDR; Yeast two hybrid

Indexed keywords

CALCITRIOL; CALCIUM ION; COLECALCIFEROL RECEPTOR; HYDROGEN PEROXIDE; MESSENGER RNA; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; TUMOR PROTEIN; UNCLASSIFIED DRUG; CALCITRIOL RECEPTOR; DNA; RECOMBINANT PROTEIN; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN, P23; TUMOR MARKER;

APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ELECTROPHORETIC MOBILITY; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; LIGAND BINDING; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM; VITAMIN D RESPONSIVE ELEMENT; ACTIVE TRANSPORT; CELL LINE; DRUG EFFECT; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; PROTEIN BINDING;

ACTIVE TRANSPORT, CELL NUCLEUS; CALCITRIOL; CELL LINE, TRANSFORMED; CELL NUCLEUS; CYTOPLASM; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FEEDBACK, PHYSIOLOGICAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROGEN PEROXIDE; IMMUNOPRECIPITATION; KERATINOCYTES; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, CALCITRIOL; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; TWO-HYBRID SYSTEM TECHNIQUES; VITAMIN D RESPONSE ELEMENT;

EID: 72449155496     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2009.09.015     Document Type: Article

References (68)

1. Bommer U.A., and Thiele B.J. The translationally controlled tumour protein (TCTP). Int. J. Biochem. Cell Biol. 36 3 (2004) 379-385
2. Gachet Y., Tournier S., Lee M., Lazaris-Karatzas A., Poulton T., and Bommer U.A. The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J. Cell Sci. 112 Pt 8 (1999) 1257-1271
3. Yarm F.R. Plk phosphorylation regulates the microtubule-stabilizing protein TCTP. Mol. Cell. Biol. 22 17 (2002) 6209-6221
4. Bazile F., Pascal A., Arnal I., Le Clainche C., Chesnel F., and Kubiak J.Z. Complex relationship between TCTP, microtubules and actin microfilaments regulates cell shape in normal and cancer cells. Carcinogenesis 30 4 (2009) 555-565
5. Cans C., Passer B.J., Shalak V., et al. Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc. Natl. Acad. Sci. U.S.A. 100 24 (2003) 13892-13897
6. Langdon J.M., Vonakis B.M., and MacDonald S.M. Identification of the interaction between the human recombinant histamine releasing factor/translationally controlled tumor protein and elongation factor-1 delta (also known as eElongation factor-1B beta). Biochim. Biophys. Acta 1688 3 (2004) 232-236
7. Liu H., Peng H.W., Cheng Y.S., Yuan H.S., and Yang-Yen H.F. Stabilization and enhancement of the antiapoptotic activity of mcl-1 by TCTP. Mol. Cell. Biol. 25 8 (2005) 3117-3126
8. Graidist P., Phongdara A., and Fujise K. Antiapoptotic protein partners fortilin and MCL1 independently protect cells from 5-fluorouracil-induced cytotoxicity. J. Biol. Chem. 279 39 (2004) 40868-40875
9. Yang Y., Yang F., Xiong Z., et al. An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24 30 (2005) 4778-4788
10. Susini L., Besse S., Duflaut D., et al. TCTP protects from apoptotic cell death by antagonizing bax function. Cell Death Differ. 15 8 (2008) 1211-1220
11. 2+-dependent apoptosis in vivo. Biochem. J. 408 2 (2007) 181-191
12. MacDonald S.M., Rafnar T., Langdon J., and Lichtenstein L.M. Molecular identification of an IgE-dependent histamine-releasing factor. Science 269 5224 (1995) 688-690
13. Schroeder J.T., Lichtenstein L.M., and MacDonald S.M. Recombinant histamine-releasing factor enhances IgE-dependent IL-4 and IL-13 secretion by human basophils. J. Immunol. 159 1 (1997) 447-452
14. Feng Y., Liu D., Yao H., and Wang J. Solution structure and mapping of a very weak calcium-binding site of human translationally controlled tumor protein by NMR. Arch. Biochem. Biophys. 467 1 (2007) 48-57
15. Xu A., Bellamy A.R., and Taylor J.A. Expression of translationally controlled tumour protein is regulated by calcium at both the transcriptional and post-transcriptional level. Biochem. J. 342 (1999) 683-689
16. Kim M., Jung Y., Lee K., and Kim C. Identification of the calcium binding sites in translationally controlled tumor protein. Arch. Pharm. Res. 23 6 (2000) 633-636
17. Haussler M.R., Haussler C.A., Jurutka P.W., Thompson P.D., Hsieh J.C., Remus L.S., Selznick S.H., and Whitfield G.K. The vitamin D hormone and its nuclear receptor: molecular actions and disease states. J. Endocrinol. 154 (1997) S57-73
18. Shaffer P.L., and Gewirth D.T. Structural basis of VDR-DNA interactions on direct repeat response elements. Embo J. 21 9 (2002) 2242-2252
19. Jurutka P.W., Bartik L., Whitfield G.K., et al. Vitamin D receptor: key roles in bone mineral pathophysiology, molecular mechanism of action, and novel nutritional ligands. J. Bone Miner. Res. 22 (2007) V2-10
20. Ebert R., Schutze N., Adamski J., and Jakob F. Vitamin D signaling is modulated on multiple levels in health and disease. Mol. Cell. Endocrinol. 248 1-2 (2006) 149-159
21. Hawker N.P., Pennypacker S.D., Chang S.M., and Bikle D.D. Regulation of human epidermal keratinocyte differentiation by the vitamin D receptor and its coactivators DRIP205, SRC2, and SRC3. J. Invest. Dermatol. 127 4 (2007) 874-880
22. Hayes C.E., Nashold F.E., Spach K.M., and Pedersen L.B. The immunological functions of the vitamin D endocrine system. Cell Mol. Biol. (Noisy-le-grand) 49 2 (2003) 277-300
23. Reichrath J., Lehmann B., Carlberg C., Varani J., and Zouboulis C.C. Vitamins as hormones. Horm. Metab. Res. 39 2 (2007) 71-84
24. Sheffield P., Garrard S., and Derewenda Z. Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr. Purif. 15 1 (1999) 34-39
25. Oender K., Niedermayr P., Hintner H., Richter K., Koller L., Trost A., Bauer J.W., and Hundsberger H. Relative quantitation of protein-protein interaction strength within the yeast two-hybrid system via fluorescence beta-galactosidase activity detection in a high-throughput and low-cost manner. Assay Drug Dev. Technol. 4 6 (2006) 709-719
26. Rid R., Simon-Nobbe B., Langdon J., et al. Cladosporium herbarum translationally controlled tumor protein (TCTP) is an IgE-binding antigen and is associated with disease severity. Mol. Immunol. 45 2 (2008) 406-418
27. Lehmann B. HaCaT cell line as a model system for vitamin D3 metabolism in human skin. J. Invest. Dermatol. 108 1 (1997) 78-82
28. Lehmann B., Knuschke P., and Meurer M. UVB-induced conversion of 7-dehydrocholesterol to 1 alpha,25-dihydroxyvitamin D3 (calcitriol) in the human keratinocyte line HaCaT. Photochem. Photobiol. 72 6 (2000) 803-809
29. Lehmann B., Pietzsch J., Kampf A., and Meurer M. Human keratinocyte line HaCaT metabolizes 1alpha-hydroxyvitamin D3 and vitamin D3 to 1alpha,25-dihydroxyvitamin D3 (calcitriol). J. Dermatol. Sci. 18 2 (1998) 118-127
30. Ritter M., Ravasio A., Jakab M., et al. Cell swelling stimulates cytosol to membrane transposition of ICln. J. Biol. Chem. 278 50 (2003) 50163-50174
31. Cartharius K., Frech K., Grote K., et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21 13 (2005) 2933-2942
32. Bugge T.H., Pohl J., Lonnoy O., and Stunnenberg H.G. RXR alpha, a promiscuous partner of retinoic acid and thyroid hormone receptors. Embo J. 11 4 (1992) 1409-1418
33. Baxter N.J., Thaw P., Higgins L.D., Sedelnikova S.E., Bramley A.L., Price C., Waltho J.P., and Craven C.J. Backbone NMR assignment of the 19 kDa translationally controlled tumor-associated protein p23fyp from Schizosaccharomyces pombe. J. Biomol. NMR 16 1 (2000) 83-84
34. Thaw P., Baxter N.J., Hounslow A.M., Price C., Waltho J.P., and Craven C.J. Structure of TCTP reveals unexpected relationship with guanine nucleotide-free chaperones. Nat. Struct. Biol. 8 8 (2001) 701-704
35. Chung S., Kim M., Choi W., Chung J., and Lee K. Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett. 156 2 (2000) 185-190
36. Thiele H., Berger M., Skalweit A., and Thiele B.J. Expression of the gene and processed pseudogenes encoding the human and rabbit translationally controlled tumour protein (TCTP). Eur. J. Biochem. 267 17 (2000) 5473-5481
37. Baudet C., Perret E., Delpech B., Kaghad M., Brachet P., Wion D., and Caput D. Differentially expressed genes in C6.9 glioma cells during vitamin D-induced cell death program. Cell Death Differ. 5 1 (1998) 116-125
38. Carlberg C., and Seuter S. The vitamin D receptor. Dermatol. Clin. 25 4 (2007) 515-523 viii
39. Schmuth M., Watson R.E., Deplewski D., Dubrac S., Zouboulis C.C., and Griffiths C.E. Nuclear hormone receptors in human skin. Horm. Metab. Res. 39 2 (2007) 96-105
40. Feldman D., Chen T., Hirst M., Colston K., Karasek M., and Cone C. Demonstration of 1,25-dihydroxyvitamin D3 receptors in human skin biopsies. J. Clin. Endocrinol. Metab. 51 6 (1980) 1463-1465
41. Eil C., and Marx S.J. Nuclear uptake of 1,25-dihydroxy[3H]cholecalciferol in dispersed fibroblasts cultured from normal human skin. Proc. Natl. Acad. Sci. U.S.A. 78 4 (1981) 2562-2566
42. Dam T.N., Moller B., Hindkjaer J., and Kragballe K. The vitamin D3 analog calcipotriol suppresses the number and antigen-presenting function of Langerhans cells in normal human skin. J. Investig. Dermatol. Symp. Proc. 1 1 (1996) 72-77
43. Ranson M., Posen S., and Mason R.S. Human melanocytes as a target tissue for hormones: in vitro studies with 1 alpha-25, dihydroxyvitamin D3, alpha-melanocyte stimulating hormone, and beta-estradiol. J. Invest. Dermatol. 91 6 (1988) 593-598
44. Merke J., Milde P., Lewicka S., et al. Identification and regulation of 1,25-dihydroxyvitamin D3 receptor activity and biosynthesis of 1,25-dihydroxyvitamin D3 Studies in cultured bovine aortic endothelial cells and human dermal capillaries. J. Clin. Invest. 83 6 (1989) 1903-1915
45. Moras D., and Gronemeyer H. The nuclear receptor ligand-binding domain: structure and function. Curr. Opin. Cell Biol. 10 3 (1998) 384-391
46. Heery D.M., Kalkhoven E., Hoare S., and Parker M.G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387 6634 (1997) 733-736
47. Savkur R.S., and Burris T.P. The coactivator LXXLL nuclear receptor recognition motif. J. Pept. Res. 63 3 (2004) 207-212
48. Plevin M.J., Mills M.M., and Ikura M. The LxxLL motif: a multifunctional binding sequence in transcriptional regulation. Trends Biochem. Sci. 30 2 (2005) 66-69
49. Zella L.A., Chang C.Y., McDonnell D.P., and Wesley Pike J. The vitamin D receptor interacts preferentially with DRIP205-like LxxLL motifs. Arch. Biochem. Biophys. 460 2 (2007) 206-212
50. Rinnerthaler M., Jarolim S., Heeren G., et al. MMI1 (YKL056c,TMA19), the yeast orthologue of the translationally controlled tumor protein (TCTP) has apoptotic functions and interacts with both microtubules and mitochondria. Biochim. Biophys. Acta 1757 5-6 (2006) 631-638
51. Miyauchi Y., Michigami T., Sakaguchi N., Sekimoto T., Yoneda Y., Pike J.W., Yamagata M., and Ozono K. Importin 4 is responsible for ligand-independent nuclear translocation of vitamin D receptor. J. Biol. Chem. 280 49 (2005) 40901-40908
52. Prufer K., Racz A., Lin G.C., and Barsony J. Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J. Biol. Chem. 275 52 (2000) 41114-41123
53. Chen S.H., Wu P.S., Chou C.H., Yan Y.T., Liu H., Weng S.Y., and Yang-Yen H.F. A knockout mouse approach reveals that TCTP functions as an essential factor for cell proliferation and survival in a tissue- or cell type-specific manner. Mol. Biol. Cell. 18 7 (2007) 2525-2532
54. Dusso A.S., Brown A.J., and Slatopolsky E. Vitamin D. Am. J. Physiol. Renal Physiol. 289 1 (2005) F8-F28
55. Deeb K.K., Trump D.L., and Johnson C.S. Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat. Rev. Cancer 7 9 (2007) 684-700
56. Sergeev I.N. Calcium as a mediator of 1,25-dihydroxyvitamin D3-induced apoptosis. J. Steroid Biochem. Mol. Biol. 89-90 1-5 (2004) 419-425
57. Telerman A., and Amson R. The molecular programme of tumour reversion: the steps beyond malignant transformation. Nat. Rev. Cancer 9 3 (2009) 206-216
58. Li F., Zhang D., and Fujise K. Characterization of fortilin, a novel antiapoptotic protein. J. Biol. Chem. 276 50 (2001) 47542-47549
59. Tuynder M., Fiucci G., Prieur S., et al. Translationally controlled tumor protein is a target of tumor reversion. Proc. Natl. Acad. Sci. U.S.A. 101 43 (2004) 15364-15369
60. Tuynder M., Susini L., Prieur S., Besse S., Fiucci G., Amson R., and Telerman A. Biological models and genes of tumor reversion: cellular reprogramming through tpt1/TCTP and SIAH-1. Proc. Natl. Acad. Sci. U.S.A. 99 23 (2002) 14976-14981
61. Bikle D., Teichert A., Hawker N., Xie Z., and Oda Y. Sequential regulation of keratinocyte differentiation by 1,25(OH)2D3, VDR, and its coregulators. J. Steroid Biochem. Mol. Biol. 103 3-5 (2007) 396-404
62. Liu M., Lee M.H., Cohen M., Bommakanti M., and Freedman L.P. Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes Dev. 10 2 (1996) 142-153
63. Kamradt J., Rafi L., Mitschele T., Meineke V., Gartner B.C., Wolfgang T., Holick M.F., and Reichrath J. Analysis of the vitamin D system in cutaneous malignancies. Recent Results Cancer Res. 164 (2003) 259-269
64. Trump D.L., Hershberger P.A., Bernardi R.J., Ahmed S., Muindi J., Fakih M., Yu W.D., and Johnson C.S. Anti-tumor activity of calcitriol: pre-clinical and clinical studies. J. Steroid Biochem. Mol. Biol. 89-90 1-5 (2004) 519-526
65. De Haes P., Garmyn M., Carmeliet G., Degreef H., Vantieghem K., Bouillon R., and Segaert S. Molecular pathways involved in the anti-apoptotic effect of 1,25-dihydroxyvitamin D3 in primary human keratinocytes. J. Cell Biochem. 93 5 (2004) 951-967
66. Guzey M., Kitada S., and Reed J.C. Apoptosis induction by 1alpha,25-dihydroxyvitamin D3 in prostate cancer. Mol. Cancer Ther. 1 9 (2002) 667-677
67. De Haes P., Garmyn M., Degreef H., Vantieghem K., Bouillon R., and Segaert S. 1,25-Dihydroxyvitamin D3 inhibits ultraviolet B-induced apoptosis, Jun kinase activation, and interleukin-6 production in primary human keratinocytes. J. Cell Biochem. 89 4 (2003) 663-673
68. Diker-Cohen T., Koren R., Liberman U.A., and Ravid A. Vitamin D protects keratinocytes from apoptosis induced by osmotic shock, oxidative stress, and tumor necrosis factor. Ann. N.Y. Acad. Sci. 1010 (2003) 350-353