PIM-1 kinase interacts with the DNA binding domain of the vitamin D receptor: A further kinase implicated in 1,25-(OH) 2D 3 signaling

BMC Molecular Biology

Volumn 13, Issue , 2012, Pages

  Maier, Christina J ^a   Maier, Richard H ^a   Rid, Raphaela ^a   Trost, Andrea ^a   Hundsberger, Harald ^b   Eger, Andreas ^b   Hintner, Helmut ^a   Bauer, Johann W ^a   Onder, Kamil ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b IMC UNIVERSITY OF APPLIED SCIENCES KREMS   (Austria)

Author keywords

Coactivator; PIM 1 kinase; Protein protein interaction; Serine threonine kinase; Vitamin D; Vitamin D receptor

Indexed keywords

CALCITRIOL; OSTEOPONTIN; PROTEIN KINASE PIM 1; PROTEIN KINASE PIM 1 ISOFORM 2; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR; CALCITRIOL RECEPTOR; DNA; ISOPROTEIN; SMALL INTERFERING RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; HORMONE ACTION; HUMAN; HUMAN CELL; KERATINOCYTE; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; CELL LINE; CELL NUCLEUS; CHEMISTRY; DRUG ANTAGONISM; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

CALCITRIOL; CELL LINE; CELL NUCLEUS; DNA; HUMANS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-PIM-1; RECEPTORS, CALCITRIOL; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84862489015     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-13-18     Document Type: Article

References (63)

1. Carlberg C, Seuter S. The vitamin D receptor. Dermatol Clin 2007, 25:515-523. viii, 10.1016/j.det.2007.06.004, 17903610.
2. Carlberg C. Ligand-mediated conformational changes of the VDR are required for gene transactivation. J Steroid Biochem Mol Biol 2004, 89-90:227-232.
3. Privalsky ML. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol 2004, 66:315-360. 10.1146/annurev.physiol.66.032802.155556, 14977406.
4. Boyan BD, Wang L, Wong KL, Jo H, Schwartz Z. Plasma membrane requirements for 1alpha,25(OH)2D3 dependent PKC signaling in chondrocytes and osteoblasts. Steroids 2006, 71:286-290. 10.1016/j.steroids.2005.09.018, 16325216.
5. Wali RK, Baum CL, Sitrin MD, Brasitus TA. 1,25(OH)2 vitamin D3 stimulates membrane phosphoinositide turnover, activates protein kinase C, and increases cytosolic calcium in rat colonic epithelium. J Clin Invest 1990, 85:1296-1303. 10.1172/JCI114567, 296566, 2156898.
6. Losel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 2003, 4:46-56. 10.1038/nrm1009, 12511868.
7. Amson R, Sigaux F, Przedborski S, Flandrin G, Givol D, Telerman A. The human protooncogene product p33pim is expressed during fetal hematopoiesis and in diverse leukemias. Proc Natl Acad Sci U S A 1989, 86:8857-8861. 10.1073/pnas.86.22.8857, 298389, 2682662.
8. Moroy T, Grzeschiczek A, Petzold S, Hartmann KU. Expression of a Pim-1 transgene accelerates lymphoproliferation and inhibits apoptosis in lpr/lpr mice. Proc Natl Acad Sci U S A 1993, 90:10734-10738. 10.1073/pnas.90.22.10734, 47852, 7504280.
9. Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int J Biochem Cell Biol 2005, 37:726-730. 10.1016/j.biocel.2004.11.005, 15694833.
10. Shah N, Pang B, Yeoh KG, Thorn S, Chen CS, Lilly MB, Salto-Tellez M. Potential roles for the PIM1 kinase in human cancer - a molecular and therapeutic appraisal. Eur J Cancer 2008, 44:2144-2151. 10.1016/j.ejca.2008.06.044, 18715779.
11. Maier R, Brandner C, Hintner H, Bauer J, Onder K. Construction of a reading frame-independent yeast two-hybrid vector system for site-specific recombinational cloning and protein interaction screening. Biotechniques 2008, 45:235-244. 10.2144/000112897, 18778248.
12. Plevin MJ, Mills MM, Ikura M. The LxxLL motif: a multifunctional binding sequence in transcriptional regulation. Trends Biochem Sci 2005, 30:66-69. 10.1016/j.tibs.2004.12.001, 15691650.
13. Savkur RS, Burris TP. The coactivator LXXLL nuclear receptor recognition motif. J Pept Res 2004, 63:207-212. 10.1111/j.1399-3011.2004.00126.x, 15049832.
14. Barsony J, Renyi I, McKoy W. Subcellular distribution of normal and mutant vitamin D receptors in living cells. Studies with a novel fluorescent ligand. J Biol Chem 1997, 272:5774-5782. 10.1074/jbc.272.9.5774, 9038191.
15. Saris CJ, Domen J, Berns A. The pim-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG. EMBO J 1991, 10:655-664. 452698, 1825810.
16. Maita H, Harada Y, Nagakubo D, Kitaura H, Ikeda M, Tamai K, Takahashi K, Ariga H, Iguchi-Ariga SM. PAP-1, a novel target protein of phosphorylation by pim-1 kinase. Eur J Biochem 2000, 267:5168-5178. 10.1046/j.1432-1327.2000.01585.x, 10931201.
17. Wang Z, Bhattacharya N, Weaver M, Petersen K, Meyer M, Gapter L, Magnuson NS. Pim-1: a serine/threonine kinase with a role in cell survival, proliferation, differentiation and tumorigenesis. J Vet Sci 2001, 2:167-179.
18. Avila E, Diaz L, Barrera D, Halhali A, Mendez I, Gonzalez L, Zuegel U, Steinmeyer A, Larrea F. Regulation of Vitamin D hydroxylases gene expression by 1,25-dihydroxyvitamin D3 and cyclic AMP in cultured human syncytiotrophoblasts. J Steroid Biochem Mol Biol 2007, 103:90-96. 10.1016/j.jsbmb.2006.07.010, 17079137.
19. Rachez C, Gamble M, Chang CP, Atkins GB, Lazar MA, Freedman LP. The DRIP complex and SRC-1/p160 coactivators share similar nuclear receptor binding determinants but constitute functionally distinct complexes. Mol Cell Biol 2000, 20:2718-2726. 10.1128/MCB.20.8.2718-2726.2000, 85487, 10733574.
20. Feldman D, Chen T, Hirst M, Colston K, Karasek M, Cone C. Demonstration of 1,25-dihydroxyvitamin D3 receptors in human skin biopsies. J Clin Endocrinol Metab 1980, 51:1463-1465. 10.1210/jcem-51-6-1463, 6255007.
21. Milde P, Hauser U, Simon T, Mall G, Ernst V, Haussler MR, Frosch P, Rauterberg EW. Expression of 1,25-dihydroxyvitamin D3 receptors in normal and psoriatic skin. J Invest Dermatol 1991, 97:230-239. 10.1111/1523-1747.ep12480255, 1649228.
22. Selten G, Cuypers HT, Berns A. Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J 1985, 4:1793-1798. 554419, 2992942.
23. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest 2005, 115:2618-2624. 10.1172/JCI26273, 1236693, 16200194.
24. Leverson JD, Koskinen PJ, Orrico FC, Rainio EM, Jalkanen KJ, Dash AB, Eisenman RN, Ness SA. Pim-1 kinase and p100 cooperate to enhance c-Myb activity. Mol Cell 1998, 2:417-425. 10.1016/S1097-2765(00)80141-0, 9809063.
25. Mochizuki T, Kitanaka C, Noguchi K, Muramatsu T, Asai A, Kuchino Y. Physical and functional interactions between Pim-1 kinase and Cdc25A phosphatase. Implications for the Pim-1-mediated activation of the c-Myc signaling pathway. J Biol Chem 1999, 274:18659-18666. 10.1074/jbc.274.26.18659, 10373478.
26. Koike N, Maita H, Taira T, Ariga H, Iguchi-Ariga SM. Identification of heterochromatin protein 1 (HP1) as a phosphorylation target by Pim-1 kinase and the effect of phosphorylation on the transcriptional repression function of HP1(1). FEBS Lett 2000, 467:17-21. 10.1016/S0014-5793(00)01105-4, 10664448.
27. Wang Z, Bhattacharya N, Mixter PF, Wei W, Sedivy J, Magnuson NS. Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim Biophys Acta 2002, 1593:45-55. 10.1016/S0167-4889(02)00347-6, 12431783.
28. Bhattacharya N, Wang Z, Davitt C, McKenzie IF, Xing PX, Magnuson NS. Pim-1 associates with protein complexes necessary for mitosis. Chromosoma 2002, 111:80-95. 10.1007/s00412-002-0192-6, 12111331.
29. Aho TL, Sandholm J, Peltola KJ, Mankonen HP, Lilly M, Koskinen PJ. Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett 2004, 571:43-49. 10.1016/j.febslet.2004.06.050, 15280015.
30. Stewart BE, Rice RH. Differentiation-associated expression of the proto-oncogene pim-1 in cultured human keratinocytes. J Invest Dermatol 1995, 105:699-703. 10.1111/1523-1747.ep12324482, 7594647.
31. Eichmann A, Yuan L, Breant C, Alitalo K, Koskinen PJ. Developmental expression of pim kinases suggests functions also outside of the hematopoietic system. Oncogene 2000, 19:1215-1224. 10.1038/sj.onc.1203355, 10713710.
32. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000, 403:503-511. 10.1038/35000501, 10676951.
33. Cohen AM, Grinblat B, Bessler H, Kristt D, Kremer A, Schwartz A, Halperin M, Shalom S, Merkel D, Don J. Increased expression of the hPim-2 gene in human chronic lymphocytic leukemia and non-Hodgkin lymphoma. Leuk Lymphoma 2004, 45:951-955. 10.1080/10428190310001641251, 15291354.
34. Valdman A, Fang X, Pang ST, Ekman P, Egevad L. Pim-1 expression in prostatic intraepithelial neoplasia and human prostate cancer. Prostate 2004, 60:367-371. 10.1002/pros.20064, 15264249.
35. Arnold SF, Obourn JD, Yudt MR, Carter TH, Notides AC. In vivo and in vitro phosphorylation of the human estrogen receptor. J Steroid Biochem Mol Biol 1995, 52:159-171. 10.1016/0960-0760(94)00166-J, 7873451.
36. Knotts TA, Orkiszewski RS, Cook RG, Edwards DP, Weigel NL. Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J Biol Chem 2001, 276:8475-8483. 10.1074/jbc.M009805200, 11110801.
37. Rochette-Egly C, Oulad-Abdelghani M, Staub A, Pfister V, Scheuer I, Chambon P, Gaub MP. Phosphorylation of the retinoic acid receptor-alpha by protein kinase A. Mol Endocrinol 1995, 9:860-871. 10.1210/me.9.7.860, 7476969.
38. Hsieh JC, Jurutka PW, Nakajima S, Galligan MA, Haussler CA, Shimizu Y, Shimizu N, Whitfield GK, Haussler MR. Phosphorylation of the human vitamin D receptor by protein kinase C. Biochemical and functional evaluation of the serine 51 recognition site. J Biol Chem 1993, 268:15118-15126.
39. Jurutka PW, Hsieh JC, Nakajima S, Haussler CA, Whitfield GK, Haussler MR. Human vitamin D receptor phosphorylation by casein kinase II at Ser-208 potentiates transcriptional activation. Proc Natl Acad Sci U S A 1996, 93:3519-3524. 10.1073/pnas.93.8.3519, 39642, 8622969.
40. Barletta F, Freedman LP, Christakos S. Enhancement of VDR-mediated transcription by phosphorylation: correlation with increased interaction between the VDR and DRIP205, a subunit of the VDR-interacting protein coactivator complex. Mol Endocrinol 2002, 16:301-314. 10.1210/me.16.2.301, 11818502.
41. Arriagada G, Paredes R, Olate J, van Wijnen A, Lian JB, Stein GS, Stein JL, Onate S, Montecino M. Phosphorylation at serine 208 of the 1alpha,25-dihydroxy Vitamin D3 receptor modulates the interaction with transcriptional coactivators. J Steroid Biochem Mol Biol 2007, 103:425-429. 10.1016/j.jsbmb.2006.12.021, 3118558, 17368182.
42. Ellison TI, Dowd DR, MacDonald PN. Calmodulin-dependent kinase IV stimulates vitamin D receptor-mediated transcription. Mol Endocrinol 2005, 19:2309-2319. 10.1210/me.2004-0382, 15919723.
43. Gniadecki R. Stimulation versus inhibition of keratinocyte growth by 1,25-Dihydroxyvitamin D3: dependence on cell culture conditions. J Invest Dermatol 1996, 106:510-516. 10.1111/1523-1747.ep12343866, 8648185.
44. Marcinkowska E, Wiedlocha A, Radzikowski C. 1,25-Dihydroxyvitamin D3 induced activation and subsequent nuclear translocation of MAPK is upstream regulated by PKC in HL-60 cells. Biochem Biophys Res Commun 1997, 241:419-426. 10.1006/bbrc.1997.7832, 9425286.
45. Sugawara A, Yen PM, Apriletti JW, Ribeiro RC, Sacks DB, Baxter JD, Chin WW. Phosphorylation selectively increases triiodothyronine receptor homodimer binding to DNA. J Biol Chem 1994, 269:433-437.
46. Migliaccio A, Di Domenico M, Green S, de Falco A, Kajtaniak EL, Blasi F, Chambon P, Auricchio F. Phosphorylation on tyrosine of in vitro synthesized human estrogen receptor activates its hormone binding. Mol Endocrinol 1989, 3:1061-1069. 10.1210/mend-3-7-1061, 2797002.
47. van Laar JH, Berrevoets CA, Trapman J, Zegers ND, Brinkmann AO. Hormone-dependent androgen receptor phosphorylation is accompanied by receptor transformation in human lymph node carcinoma of the prostate cells. J Biol Chem 1991, 266:3734-3738.
48. Ali S, Metzger D, Bornert JM, Chambon P. Modulation of transcriptional activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region. EMBO J 1993, 12:1153-1160. 413317, 8458328.
49. Weigel NL. Steroid hormone receptors and their regulation by phosphorylation. Biochem J 1996, 319(Pt 3):657-667. 1217840, 8920964.
50. Yuan LW, Gambee JE. Phosphorylation of p300 at serine 89 by protein kinase C. J Biol Chem 2000, 275:40946-40951. 10.1074/jbc.M007832200, 11020388.
51. Rowan BG, Weigel NL, O'Malley BW. Phosphorylation of steroid receptor coactivator-1. Identification of the phosphorylation sites and phosphorylation through the mitogen-activated protein kinase pathway. J Biol Chem 2000, 275:4475-4483. 10.1074/jbc.275.6.4475, 10660621.
52. Hong SH, Privalsky ML. The SMRT corepressor is regulated by a MEK-1 kinase pathway: inhibition of corepressor function is associated with SMRT phosphorylation and nuclear export. Mol Cell Biol 2000, 20:6612-6625. 10.1128/MCB.20.17.6612-6625.2000, 86146, 10938135.
53. Zhou Y, Gross W, Hong SH, Privalsky ML. The SMRT corepressor is a target of phosphorylation by protein kinase CK2 (casein kinase II). Mol Cell Biochem 2001, 220:1-13. 10.1023/A:1011087910699, 2655343, 11451368.
54. Hermanson O, Glass CK, Rosenfeld MG. Nuclear receptor coregulators: multiple modes of modification. Trends Endocrinol Metab 2002, 13:55-60. 10.1016/S1043-2760(01)00527-6, 11854019.
55. Paredes R, Arriagada G, Cruzat F, Villagra A, Olate J, Zaidi K, van Wijnen A, Lian JB, Stein GS, Stein JL, Montecino M. Bone-specific transcription factor Runx2 interacts with the 1alpha,25-dihydroxyvitamin D3 receptor to up-regulate rat osteocalcin gene expression in osteoblastic cells. Mol Cell Biol 2004, 24:8847-8861. 10.1128/MCB.24.20.8847-8861.2004, 517904, 15456860.
56. Ward JO, McConnell MJ, Carlile GW, Pandolfi PP, Licht JD, Freedman LP. The acute promyelocytic leukemia-associated protein, promyelocytic leukemia zinc finger, regulates 1,25-dihydroxyvitamin D(3)-induced monocytic differentiation of U937 cells through a physical interaction with vitamin D(3) receptor. Blood 2001, 98:3290-3300. 10.1182/blood.V98.12.3290, 11719366.
57. Miyauchi Y, Sakaguchi N, Okada T, Makishima M, Ozono K, Michigami T. Oncogenic nucleoporin CAN/Nup214 interacts with vitamin D receptor and modulates its function. J Cell Biochem 2009, 106:1090-1101. 10.1002/jcb.22101, 19229862.
58. Lehmann B, Pietzsch J, Kampf A, Meurer M. Human keratinocyte line HaCaT metabolizes 1alpha-hydroxyvitamin D3 and vitamin D3 to 1alpha,25-dihydroxyvitamin D3 (calcitriol). J Dermatol Sci 1998, 18:118-127. 10.1016/S0923-1811(98)00033-4, 9833978.
59. Butler WT. The nature and significance of osteopontin. Connect Tissue Res 1989, 23:123-136. 10.3109/03008208909002412, 2698313.
60. Chang PL, Ridall AL, Prince CW. Calcitriol regulation of osteopontin expression in mouse epidermal cells. Endocrinology 1994, 135:863-869. 10.1210/en.135.3.863, 8070379.
61. Thompson J, Peltola KJ, Koskinen PJ, Janne OA, Palvimo JJ. Attenuation of androgen receptor-dependent transcription by the serine/threonine kinase Pim-1. Lab Invest 2003, 83:1301-1309. 10.1097/01.LAB.0000087585.03162.A3, 13679438.
62. Winn LM, Lei W, Ness SA. Pim-1 phosphorylates the DNA binding domain of c-Myb. Cell Cycle 2003, 2:258-262.
63. Iwabuchi K, Li B, Bartel P, Fields S. Use of the two-hybrid system to identify the domain of p53 involved in oligomerization. Oncogene 1993, 8:1693-1696.