Vitamin D and alternative splicing of RNA

Journal of Steroid Biochemistry and Molecular Biology

Volumn 148, Issue , 2015, Pages 310-317

  Zhou, Rui ^a,b   Chun, Rene F ^a   Lisse, Thomas S ^c   Garcia, Alejandro J ^a   Xu, Jianzhong ^b   Adams, John S ^a   Hewison, Martin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

Author keywords

Heterogenous nuclear ribonucleoprotein C; RNA; Splicing; Transcription; Vitamin D

Indexed keywords

1,25 DIHYDROXYERGOCALCIFEROL; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; MESSENGER RNA PRECURSOR; MICRORNA; STEROID HORMONE; VITAMIN D; VITAMIN D RECEPTOR; CALCITRIOL RECEPTOR; RNA; VITAMIN;

ALTERNATIVE RNA SPLICING; BIOLOGICAL FUNCTIONS; DNA METHYLATION; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOMICS; HISTONE ACETYLATION; HUMAN; RECEPTOR BINDING; REVIEW; RNA PROCESSING; RNA SPLICING; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS;

ALTERNATIVE SPLICING; GENE EXPRESSION REGULATION; HUMANS; RECEPTORS, CALCITRIOL; RNA; VITAMIN D; VITAMINS;

EID: 84925542975     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.09.025     Document Type: Article

References (87)

1. M.R. Haussler, G.K. Whitfield, I. Kaneko, C.A. Haussler, D. Hsieh, J.C. Hsieh, and P.W. Jurutka Molecular mechanisms of vitamin D action Calcif. Tissue Int. 92 2013 77 98
2. M.R. Haussler, C.A. Haussler, G.K. Whitfield, J.C. Hsieh, P.D. Thompson, T.K. Barthel, L. Bartik, J.B. Egan, Y. Wu, J.L. Kubicek, C.L. Lowmiller, E.W. Moffet, R.E. Forster, and P.W. Jurutka The nuclear vitamin D receptor controls the expression of genes encoding factors which feed the fountain of youth to mediate healthful aging J Steroid Biochem. Mol. Biol. 121 2010 88 97
3. D.J. Mangelsdorf, and R.M. Evans The RXR heterodimers and orphan receptors Cell 83 1995 841 850
4. P.W. Jurutka, L. Bartik, G.K. Whitfield, D.R. Mathern, T.K. Barthel, M. Gurevich, J.C. Hsieh, M. Kaczmarska, C.A. Haussler, and M.R. Haussler Vitamin D receptor: key roles in bone mineral pathophysiology, molecular mechanism of action, and novel nutritional ligands J. Bone Miner. Res. 22 Suppl. 2 2007 V2 10
5. J.W. Pike, M.B. Meyer, and K.A. Bishop Regulation of target gene expression by the vitamin D receptor - an update on mechanisms Rev. Endocr. Metab. Disord. 13 2012 45 55
6. C. Carlberg, and M.J. Campbell Vitamin D receptor signaling mechanisms: integrated actions of a well-defined transcription factor Steroids 78 2013 127 136
7. M.B. Meyer, and J.W. Pike Corepressors (NCoR and SMRT) as well as coactivators are recruited to positively regulated 1alpha Pike, 25-dihydroxyvitamin D3-responsive genes J. Steroid Biochem. Mol. Biol. 136 2013 120 124
8. M.L. Martowicz, M.B. Meyer, and J.W. Pike The mouse RANKL gene locus is defined by a broad pattern of histone H4 acetylation and regulated through distinct distal enhancers J. Cell. Biochem. 112 2011 2030 2045
9. K. Skorija, M. Cox, J.M. Sisk, D.R. Dowd, P.N. MacDonald, C.C. Thompson, and M.B. Demay Ligand-independent actions of the vitamin D receptor maintain hair follicle homeostasis Mol. Endocrinol. 19 2005 855 862
10. A.S. Dusso, A.J. Brown, and E. Slatopolsky Vitamin D Am. J. Physiol. Renal. Physiol. 289 2005 F8 28
11. C. Carlberg Genome-wide (over) view on the actions of vitamin D Front. Physiol. 5 2014 167
12. M.B. Meyer, P.D. Goetsch, and J.W. Pike Genome-wide analysis of the VDR/RXR cistrome in osteoblast cells provides new mechanistic insight into the actions of the vitamin D hormone J. Steroid Biochem. Mol. Biol. 121 2010 136 141
13. M.B. Meyer, P.D. Goetsch, and J.W. Pike A downstream intergenic cluster of regulatory enhancers contributes to the induction of CYP24A1 expression by 1α, 25-dihydroxyvitamin D3 J. Biol. Chem. 285 2010 15599 15610
14. S. Kim, M. Yamazaki, L.A. Zella, N.K. Shevde, and J.W. Pike Activation of receptor activator of NF-κB ligand gene expression by 1,25-dihydroxyvitamin D3 is mediated through multiple long-range enhancers Mol. Cell. Biol. 26 2006 6469 6486
15. R.D. Nerenz, M.L. Martowicz, and J.W. Pike An enhancer 20 kilobases upstream of the human receptor activator of nuclear factor-kappaB ligand gene mediates dominant activation by 1,25-dihydroxyvitamin D3 Mol. Endocrinol. 22 2008 1044 1056
16. P. Tuoresmaki, S. Vaisanen, A. Neme, S. Heikkinen, and C. Carlberg Patterns of genome-wide VDR locations Carlberg PLoS One 9 2014 e96105
17. P.K. Singh, C.L. Doig, V.K. Dhiman, B.M. Turner, D.J. Smiraglia, and M.J. Campbell Epigenetic distortion to VDR transcriptional regulation in prostate cancer cells J. Steroid Biochem. Mol. Biol. 2012
18. C.M. Banwell, D.P. MacCartney, M. Guy, A.E. Miles, M.R. Uskokovic, J. Mansi, P.M. Stewart, L.P. O'Neill, B.M. Turner, K.W. Colston, and M.J. Campbell Altered nuclear receptor corepressor expression attenuates vitamin D receptor signaling in breast cancer cells Clin. Cancer Res. 12 2006 2004 2013
19. J.W. Pike, and M.B. Meyer Fundamentals of vitamin D hormone-regulated gene expression J. steroid Biochem. Mol. Biol. 2013
20. F. Pereira, A. Barbachano, P.K. Singh, M.J. Campbell, A. Munoz, and M.J. Larriba Vitamin D has wide regulatory effects on histone demethylase genes Cell Cycle 11 2012 1081 1089
21. P.T. Liu, M. Wheelwright, R. Teles, E. Komisopoulou, K. Edfeldt, B. Ferguson, M.D. Mehta, A. Vazirnia, T.H. Rea, E.N. Sarno, T.G. Graeber, and R.L. Modlin MicroRNA-21 targets the vitamin D-dependent antimicrobial pathway in leprosy Nat. Med. 18 2012 267 273
22. W.L. Wang, N. Chatterjee, S.V. Chittur, J. Welsh, and M.P. Tenniswood Effects of 1α,25 dihydroxyvitamin D3 and testosterone on miRNA and mRNA expression in LNCaP cells Mol. Cancer 10 2011 58
23. T.S. Lisse, R.F. Chun, S. Rieger, J.S. Adams, and M. Hewison Vitamin D activation of functionally distinct regulatory miRNAs in primary human osteoblasts J. Bone Miner. Res. 28 2013 1478 1488
24. T.S. Lisse, J.S. Adams, and M. Hewison Vitamin D and MicroRNAs in Bone Crit. Rev. Eukaryot Gene Expr. 23 2013 195 214
25. Cooper, L. Wan, and G. Dreyfuss RNA and disease Cell 136 2009 777 793
26. C.L. Will, and R. Luhrmann Spliceosome structure and function Cold Spring Harb. Perspect. Biol. 3 2011
27. M.C. Wahl, C.L. Will, and R. Luhrmann The spliceosome: design principles of a dynamic RNP machine Cell 136 2009 701 718
28. Z.X. Lu, P. Jiang, and Y. Xing Genetic variation of pre-mRNA alternative splicing in human populations Wiley Interdiscip. Rev. RNA 3 2012 581 592
29. B. Diesel, U. Fischer, and E. Meese Gene amplification and splice variants of 25-hydroxyvitamin D3 1 Meese, alpha-hydroxylase (CYP27B1) in glioblastoma multiforme - a possible role in tumor progression? Recent Results Cancer Res. 164 2003 151 155
30. B. Diesel, J. Radermacher, M. Bureik, R. Bernhardt, M. Seifert, J. Reichrath, U. Fischer, and E. Meese Vitamin D(3) metabolism in human glioblastoma multiforme: functionality of CYP27B1 splice variants, metabolism of calcidiol, and effect of calcitriol Clin. Cancer Res. 11 2005 5370 5380
31. J.N. Flanagan, L. Wang, V. Tangpricha, J. Reichrath, T.C. Chen, and M.F. Holick Regulation of the 25-hydroxyvitamin D-1α-hydroxylase gene and its splice variant Recent Results Cancer Res. 164 2003 157 167
32. S. Wu, S. Ren, L. Nguyen, J.S. Adams, and M. Hewison Splice variants of the CYP27b1 gene and the regulation of 1 Hewison, 25-dihydroxyvitamin D3 production Endocrinology 148 2007 3410 3418
33. T. Mitschele, B. Diesel, M. Friedrich, V. Meineke, R.M. Maas, B.C. Gartner, J. Kamradt, E. Meese, W. Tilgen, and J. Reichrath Analysis of the vitamin D system in basal cell carcinomas (BCCs) Lab. Invest. J. Techn. Method Pathol. 84 2004 693 702
34. D. Fischer, M. Thome, S. Becker, T. Cordes, K. Diedrich, M. Friedrich, and M. Thill Expression of 25-hydroxyvitamin D3-24-hydroxylase in benign and malignant ovarian cell lines and tissue Anticancer Res. 29 2009 3635 3639
35. T. Cordes, D. Diesing, S. Becker, D. Fischer, K. Diedrich, and M. Friedrich Expression of splice variants of 1alpha-hydroxylase in mcf-7 breast cancer cells J. Steroid Biochem. Mol. Biol. 103 2007 326 329
36. J. Radermacher, B. Diesel, M. Seifert, W. Tilgen, J. Reichrath, U. Fischer, and E. Meese Expression analysis of CYP27B1 in tumor biopsies and cell cultures Anticancer Res. 26 2006 2683 2686
37. M.B. Omdahl The 25-Hydroxyvitamin D-24-Hydroxylase 2005 Elsevier New York
38. G. Jones, D.E. Prosser, and M. Kaufmann Cytochrome P450-mediated metabolism of vitamin D J. Lipid Res. 55 2014 13 31
39. S. Ren, L. Nguyen, S. Wu, C. Encinas, J.S. Adams, and M. Hewison Alternative splicing of vitamin D-24-hydroxylase: a novel mechanism for the regulation of extrarenal 1,25-dihydroxyvitamin D synthesis J. Biol. Chem. 280 2005 20604 20611
40. J.R. Muindi, A. Nganga, K.L. Engler, L.J. Coignet, C.S. Johnson, and D.L. Trump CYP24 splicing variants are associated with different patterns of constitutive and calcitriol-inducible CYP24 activity in human prostate cancer cell lines J. Steroid. Biochem. Mol. Biol. 103 2007 334 337
41. H.C. Horvath, Z. Khabir, T. Nittke, S. Gruber, G. Speer, T. Manhardt, E. Bonner, and E. Kallay CYP24A1 splice variants - implications for the antitumorigenic actions of 1,25-(OH) 2D3 in colorectal cancer J. Steroid Biochem. Mol. Biol. 121 2010 76 79
42. X. Peng, N. Tiwari, S. Roy, L. Yuan, G. Murillo, R.R. Mehta, R.V. Benya, and R.G. Mehta Regulation of CYP24 splicing by 1,25-dihydroxyvitamin D(3) in human colon cancer cells J. Endocrinol. 212 2012 207 215
43. N.J. Proudfoot, A. Furger, and M.J. Dye Integrating mRNA processing with transcription Cell 108 2002 501 512
44. D.L. Bentley Coupling mRNA processing with transcription in time and space Nat. Rev. Genet. 15 2014 163 175
45. P. Cramer, C.G. Pesce, F.E. Baralle, and A.R. Kornblihtt Functional association between promoter structure and transcript alternative splicing Proc. Natl. Acad. Sci. U. S. A. 94 1997 11456 11460
46. E.C. Merkhofer, P. Hu, and T.L. Johnson Introduction to cotranscriptional RNA splicing Method Mol. Biol. 1126 2014 83 96
47. D. Auboeuf, A. Honig, S.M. Berget, and B.W. O'Malley Coordinate regulation of transcription and splicing by steroid receptor coregulators Science 298 2002 416 419
48. D. Auboeuf, D.H. Dowhan, X. Li, K. Larkin, L. Ko, S.M. Berget, and B.W. O'Malley CoAA a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing Mol. Cell. Biol. 24 2004 442 453
49. D.H. Dowhan, E.P. Hong, D. Auboeuf, A.P. Dennis, M.M. Wilson, S.M. Berget, and B.W. O'Malley Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta Mol. Cell. 17 2005 429 439
50. C. Zhang, D.R. Dowd, A. Staal, C. Gu, J.B. Lian, A.J. van Wijnen, G.S. Stein, and P.N. MacDonald Nuclear coactivator-62 kDa/Ski-interacting protein is a nuclear matrix-associated coactivator that may couple vitamin D receptor-mediated transcription and RNA splicing J. Biol. Chem. 278 2003 35325 35336
51. J. Sun, A.L. Blair, S.E. Aiyar, and R. Li Cofactor of BRCA1 modulates androgen-dependent transcription and alternative splicing J. Steroid Biochem. Mol. Biol. 107 2007 131 139
52. D. Auboeuf, D.H. Dowhan, M. Dutertre, N. Martin, S.M. Berget, and B.W. O'Malley A subset of nuclear receptor coregulators act as coupling proteins during synthesis and maturation of RNA transcripts Mol. Cell. Biol. 25 2005 5307 5316
53. G.M. Leong, N. Subramaniam, L.L. Issa, J.B. Barry, T. Kino, P.H. Driggers, M.J. Hayman, J.A. Eisman, and E.M. Gardiner Ski-interacting protein, a bifunctional nuclear receptor coregulator that interacts with N-CoR/SMRT and p300 Biochem. Biophys. Res. Commun. 315 2004 1070 1076
54. E.M. Makarov, O.V. Makarova, H. Urlaub, M. Gentzel, C.L. Will, M. Wilm, and R. Luhrmann Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome Science 298 2002 2205 2208
55. M. Ambrozkova, F. Puta, I. Fukova, M. Skruzny, J. Brabek, and P. Folk The fission yeast ortholog of the coregulator SKIP interacts with the small subunit of U2AF Biochem. Biophys. Res. Commun. 284 2001 1148 1154
56. I. Cristobo, M.J. Larriba, V. de los Rios, F. Garcia, A. Munoz, and J.I. Casal Proteomic analysis of 1α, 25-dihydroxyvitamin D3 action on human colon cancer cells reveals a link to splicing regulation J. Proteomics 75 2011 384 397
57. M.J. Campbell Vitamin D and the RNA transcriptome: more than mRNA regulation Front. Physiol. 5 2014 181
58. Lisse, M. Hewison, and J.S. Adams Hormone response element binding proteins: novel regulators of vitamin D and estrogen signaling Steroids 76 2011 331 339
59. B.M. Merrill, S.F. Barnett, W.M. LeStourgeon, and K.R. Williams Primary structure differences between proteins C1 and C2 of HeLa 40S nuclear ribonucleoprotein particles Nucleic Acids Res. 17 1989 8441 8449
60. T.S. Lisse, K. Vadivel, S.P. Bajaj, R. Zhou, R.F. Chun, M. Hewison, and J.S. Adams The heterodimeric structure of heterogeneous nuclear ribonucleoprotein C1/C2 dictates 1,25-dihydroxyvitamin D-directed transcriptional events in osteoblasts Bone Res. 2 2014
61. A.L. Beyer, M.E. Christensen, B.W. Walker, and W.M. LeStourgeon Identification and characterization of the packaging proteins of core 40S hnRNP particles Cell 11 1977 127 138
62. M. Huang, J.E. Rech, S.J. Northington, P.F. Flicker, A. Mayeda, A.R. Krainer, and W.M. LeStourgeon The C-protein tetramer binds 230-240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles Mol. Cell. Biol. 14 1994 518 533
63. J.G. McAfee, S.R. Soltaninassab, M.E. Lindsay, and W.M. LeStourgeon Proteins C1 and C2 of heterogeneous nuclear ribonucleoprotein complexes bind RNA in a highly cooperative fashion: support for their contiguous deposition on pre-mRNA during transcription Biochemistry 35 1996 1212 1222
64. M. Gorlach, M. Wittekind, R.A. Beckman, L. Mueller, and G. Dreyfuss Interaction of the RNA-binding domain of the hnRNP C proteins with RNA EMBO J. 11 1992 3289 3295
65. L. Wan, J.K. Kim, V.W. Pollard, and G. Dreyfuss Mutational definition of RNA-binding and protein-protein interaction domains of heterogeneous nuclear RNP C1 J. Biol. Chem. 276 2001 7681 7688
66. J. Konig, K. Zarnack, G. Rot, T. Curk, M. Kayikci, B. Zupan, D.J. Turner, N.M. Luscombe, and J. Ule iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution Nat. Struct. Mol. Biol. 17 2010 909 915
67. F. Weighardt, G. Biamonti, and S. Riva The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism Bioessays 18 1996 747 756
68. M. Muller-McNicoll, and K.M. Neugebauer How cells get the message: dynamic assembly and function of mRNA-protein complexes Nat. Rev. Genet. 14 2013 275 287
69. Y.D. Choi, P.J. Grabowski, P.A. Sharp, and G. Dreyfuss Heterogeneous nuclear ribonucleoproteins: role in RNA splicing Science 231 1986 1534 1539
70. H. Sierakowska, W. Szer, P.J. Furdon, and R. Kole Antibodies to hnRNP core proteins inhibit in vitro splicing of human beta-globin pre-mRNA Nucleic Acids Res. 14 1986 5241 5254
71. J.P. Venables, C.S. Koh, U. Froehlich, E. Lapointe, S. Couture, L. Inkel, A. Bramard, E.R. Paquet, V. Watier, M. Durand, J.F. Lucier, J. Gervais-Bird, K. Tremblay, P. Prinos, R. Klinck, S.A. Elela, and B. Chabot Multiple and specific mRNA processing targets for the major human hnRNP proteins Mol. Cell. Biol. 28 2008 6033 6043
72. J.M. Izquierdo Heterogeneous ribonucleoprotein C displays a repressor activity mediated by T-cell intracellular antigen-1-related/like protein to modulate Fas exon 6 splicing through a mechanism involving Hu antigen R Nucleic Acids Res. 38 2010 8001 8014
73. A. McCloskey, I. Taniguchi, K. Shinmyozu, and M. Ohno hnRNP C tetramer measures RNA length to classify RNA polymerase II transcripts for export Science 335 2012 1643 1646
74. J.M. Izquierdo Hu antigen R (HuR) functions as an alternative pre-mRNA splicing regulator of Fas apoptosis-promoting receptor on exon definition J. Biol. Chem. 283 2008 19077 19084
75. J. Konig, K. Zarnack, G. Rot, T. Curk, M. Kayikci, B. Zupan, D.J. Turner, N.M. Luscombe, and J. Ule iCLIP - transcriptome-wide mapping of protein-RNA interactions with individual nucleotide resolution J. Vis. Exp. 2011
76. K. Zarnack, J. Konig, M. Tajnik, I. Martincorena, S. Eustermann, I. Stevant, A. Reyes, S. Anders, N.M. Luscombe, and J. Ule Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements Cell 152 2013 453 466
77. I. Vorechovsky Transposable elements in disease-associated cryptic exons Hum. Genet. 127 2010 135 154
78. R.W. Anantha, A.L. Alcivar, J. Ma, H. Cai, S. Simhadri, J. Ule, J. Konig, and B. Xia Requirement of heterogeneous nuclear ribonucleoprotein C for BRCA gene expression and homologous recombination PLoS One 8 2013 e61368
79. H. Chen, M. Hewison, and J.S. Adams Functional characterization of heterogeneous nuclear ribonuclear protein C1/C2 in vitamin D resistance: a novel response element-binding protein J. Biol. Chem. 281 2006 39114 39120
80. T.S. Lisse, T. Liu, M. Irmler, J. Beckers, H. Chen, J.S. Adams, and M. Hewison Gene targeting by the vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling FASEB J. 25 2011 937 947
81. H. Chen, B. Hu, E.A. Allegretto, and J.S. Adams The vitamin D response element-binding protein. A novel dominant-negative regulator of vitamin D-directed transactivation J. Biol. Chem. 275 2000 35557 35564
82. H. Chen, M. Hewison, B. Hu, and J.S. Adams Heterogeneous nuclear ribonucleoprotein (hnRNP) binding to hormone response elements: a cause of vitamin D resistance Proc. Natl. Acad. Sci. U. S. A. 100 2003 6109 6114
83. J.S. Adams, and M.A. Gacad Phenotypic diversity of the cellular 1,25-dihydroxyvitamin D3-receptor interaction among different genera of New World primates J. Clin. Endocrinol. Metab. 66 1988 224 229
84. J.S. Adams, H. Chen, R.F. Chun, L. Nguyen, S. Wu, S.Y. Ren, J. Barsony, and M.A. Gacad Novel regulators of vitamin D action and metabolism: lessons learned at the Los Angeles zoo J. Cell. Biochem. 88 2003 308 314
85. M. Hewison, A.R. Rut, K. Kristjansson, R.E. Walker, M.J. Dillon, M.R. Hughes, and J.L. O'Riordan Tissue resistance to 1,25-dihydroxyvitamin D without a mutation of the vitamin D receptor gene Clin. Endocrinol. (Oxf) 39 1993 663 670
86. X. Ji, and X.D. Fu The mediator couples transcription and splicing Mol. Cell. 45 2012 433 434
87. Y. Huang, W. Li, X. Yao, Q.J. Lin, J.W. Yin, Y. Liang, M. Heiner, B. Tian, J. Hui, and G. Wang Mediator complex regulates alternative mRNA processing via the MED23 subunit Mol. Cell. 45 2012 459 469