Yin Yang 1 Intronic Binding Sequences and Splicing Elicit Intron-Mediated Enhancement of Ubiquitin C Gene Expression

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Bianchi, Marzia ^a   Crinelli, Rita ^a   Giacomini, Elisa ^a   Carloni, Elisa ^a   Radici, Lucia ^a   Magnani, Mauro ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; MESSENGER RNA; TRANSCRIPTION FACTOR YY1; UBIQUITIN C;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; ENHANCER REGION; GENE CONSTRUCT; GENE FUNCTION; GENE SILENCING; GENETIC REGULATION; HUMAN; HUMAN CELL; INTRON; MUTAGENESIS; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; RNA SPLICING;

ANALYSIS OF VARIANCE; BINDING SITES; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNOPRECIPITATION; INTRONS; LUCIFERASES; MUTAGENESIS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA SPLICING; UBIQUITIN C; YY1 TRANSCRIPTION FACTOR;

EID: 84878922026     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065932     Document Type: Article

References (61)

1. Clague MJ, Urbe S, (2010) Ubiquitin: same molecule, different degradation pathways. Cell 143: 682-685.
2. Bedford L, Lowe J, Dick LR, Mayer RJ, Brownell JE, (2011) Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Discov 10: 29-46.
3. Finley D, Bartel B, Varshavsky A, (1989) The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338: 394-401.
4. Lund PK, Moats-Staats BM, Simmons JG, Hoyt E, D'Ercole AJ, et al. (1985) Nucleotide sequence analysis of a cDNA encoding human ubiquitin reveals that ubiquitin is synthesized as a precursor. J Biol Chem 260: 7609-7613.
5. Wiborg O, Pedersen MS, Wind A, Berglund LE, Marcker KA, et al. (1985) The human ubiquitin multigene family: some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J 4: 755-759.
6. Baker RT, Board PG, (1987) The human ubiquitin gene family: structure of a gene and pseudogenes from the Ub B subfamily. Nucleic Acids Res 15: 443-463.
7. Ryu KY, Maehr R, Gilchrist CA, Long MA, Bouley DM, et al. (2007) The mouse polyubiquitin gene UbC is essential for fetal liver development, cell-cycle progression and stress tolerance. EMBO J 26: 2693-2706.
8. Schorpp M, Jager R, Schellander K, Schenkel J, Wagner EF, et al. (1996) The human ubiquitin C promoter directs high ubiquitous expression of transgenes in mice. Nucleic Acids Res 24: 1787-1788.
9. Gill DR, Smyth SE, Goddard CA, Pringle IA, Higgins CF, et al. (2001) Increased persistence of lung gene expression using plasmids containing the ubiquitin C or elongation factor 1alpha promoter. Gene Ther 8: 1539-1546.
10. Krupka N, Strappe P, Gotz J, Ittner LM, (2010) Gateway-compatible lentiviral transfer vectors for ubiquitin promoter driven expression of fluorescent fusion proteins. Plasmid 63: 155-160.
11. Samadder P, Sivamani E, Lu J, Li X, Qu R, (2008) Transcriptional and post-transcriptional enhancement of gene expression by the 5′ UTR intron of rice rubi3 gene in transgenic rice cells. Mol Genet Genomics 279: 429-439.
12. Parra G, Bradnam K, Rose AB, Korf I, (2011) Comparative and functional analysis of intron-mediated enhancement signals reveals conserved features among plants. Nucleic Acids Res 39: 5328-5337.
13. Rose AB, (2008) Intron-mediated regulation of gene expression. Curr Top Microbiol Immunol 326: 277-290.
14. Morello L, Breviario D, (2008) Plant spliceosomal introns: not only cut and paste. Curr Genomics 9: 227-238.
15. Bartlett JG, Snape JW, Harwood WA, (2009) Intron-mediated enhancement as a method for increasing transgene expression levels in barley. Plant Biotechnol J 7: 856-866.
16. Byun HM, Suh D, Jeong Y, Wee HS, Kim JM, et al. (2005) Plasmid vectors harboring cellular promoters can induce prolonged gene expression in hematopoietic and mesenchymal progenitor cells. Biochem Biophys Res Commun 332: 518-523.
17. Kimura Y, Tanaka K, (2010) Regulatory mechanisms involved in the control of ubiquitin homeostasis. J Biochem 147: 793-798.
18. Fornace AJ Jr, Alamo I Jr, Hollander MC, Lamoreaux E, (1989) Ubiquitin mRNA is a major stress-induced transcript in mammalian cells. Nucleic Acids Res 17: 1215-1230.
19. Bianchi M, Crinelli R, Giacomini E, Carloni E, Magnani M, (2009) A potent enhancer element in the 5′-UTR intron is crucial for transcriptional regulation of the human ubiquitin C gene. Gene 448: 88-101.
20. Galvagni F, Cartocci E, Oliviero S, (1998) The Dystrophin Promoter is Negatively Regulated by YY1 in Undifferentiated Muscle Cells. J Biol Chem 273: 33708-33713.
21. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
22. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
24. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
25. Towbin H, Staehelin T, Gordon J, (1992) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology 24: 145-149.
26. Crinelli R, Bianchi M, Gentilini L, Magnani M, (2002) Design and characterization of decoy oligonucleotides containing locked nucleic acids. Nucleic Acids Res 30: 2435-2443.
27. Selth LA, Close P, Svejstrup JO, (2011) Studying RNA-protein interactionsin vivo by RNA immunoprecipitation. Epigenetic Protocols (2nd Ed) Methods in Molecular Biology 791: 253-264.
28. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, et al. (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21: 2933-2942.
29. Schug J (2008) Using TESS to predict transcription factor binding sites in DNA sequence. Curr Protoc Bioinformatics Chapter 2: Unit.
30. Kim J, Kim J, (2009) YY1's longer DNA-binding motifs. Genomics 93: 152-158.
31. Yokoyama NN, Pate KT, Sprowl S, Waterman ML, (2010) A role for YY1 in repression of dominant negative LEF-1 expression in colon cancer. Nucleic Acids Res 38: 6375-6388.
32. Rylski M, Amborska R, Zybura K, Mioduszewska B, Michaluk P, et al. (2008) Yin Yang 1 is a critical repressor of matrix metalloproteinase-9 expression in brain neurons. J Biol Chem 283: 35140-35153.
33. Lalmansingh AS, Urekar CJ, Reddi PP, (2011) TDP-43 is a transcriptional repressor: the testis-specific mouse acrv1 gene is a TDP-43 target in vivo. J Biol Chem 286: 10970-10982.
34. Zaravinos A, Spandidos DA, (2010) Yin yang 1 expression in human tumors. Cell Cycle 9: 512-522.
35. Ratajewski M, Pulaski L, (2009) YY1-dependent transcriptional regulation of the human GDAP1 gene. Genomics 94: 407-413.
36. Akua T, Berezin I, Shaul O (2010) The leader intron of AtMHX can elicit, in the absence of splicing, low-level intron-mediated enhancement that depends on the internal intron sequence. BMC Plant Biol 10: 93.
37. Gazdhar A, Bilici M, Pierog J, Ayuni EL, Gugger M, et al. (2006) In vivo electroporation and ubiquitin promoter-a protocol for sustained gene expression in the lung. J Gene Med 8: 910-918.
38. Marinovic AC, Zheng B, Mitch WE, Price SR, (2002) Ubiquitin (UbC) expression in muscle cells is increased by glucocorticoids through a mechanism involving Sp1 and MEK1. J Biol Chem 277: 16673-16681.
39. Guo AM, Sun K, Su X, Wang H, Sun H (2013) YY1TargetDB: an integral information resource for Yin Yang 1 target loci. Database Article ID bat007, doi:10.1093/database/bat007.
40. Liu H, Shi Y (2005) Yin Yang I. In Zinc Finger Proteins: From Atomic Contact to Cellular Function. New york: Kluwer Academic/Plenum 182-194.
41. Gordon S, Akopyan G, Garban H, Bonavida B, (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25: 1125-1142.
42. Eliassen KA, Baldwin A, Sikorski EM, Hurt MM, (1998) Role for a YY1-Binding Element in Replication-Dependent Mouse Histone Gene Expression. Mol Cell Biol 18: 7106-7118.
43. Foti DM, Reichardt JK, (2004) YY1 binding within the human HSD3B2 gene intron 1 is required for maximal basal promoter activity: identification of YY1 as the 3_1-A factor. J Mol Endocrinol 33: 99-119.
44. Kim JD, Yu S, Choo JH, Kim J (2008) Two evolutionarily conserved sequence elements for Peg3/Usp29 Transcription. BMC Molecular Biology 9: 108.
45. Takahashi K, Nishiyama C, Nishiyama M, Okumura K, Ra C, et al. (2001) A complex composed of USF1 and USF2 activates the human FcepsilonRI alpha chain expression via a CAGCTG element in the first intron. Eur J Immunol 31: 590-599.
46. Magin TM, McEwan C, Milne M, Pow AM, Selfridge J, et al. (1992) A position- and orientation-dependent element in the first intron is required for expression of the mouse hprt gene in embryonic stem cells. Gene 122: 289-296.
47. Morello L, Giani S, Troina F, Breviario D, (2011) Testing the IMEter on rice introns and other aspects of intron-mediated enhancement of gene expression. J Exp Bot 62: 533-544.
48. Ho SH, So GM, Chow KL, (2001) Postembryonic expression of Caenorhabditis elegans mab-21 and its requirement in sensory ray differentiation. Dev Dyn 221: 422-430.
49. Hasannia S, Lotfi AS, Mahboudi F, Rezaii A, Rahbarizadeh F, et al. (2006) Elevated expression of human alpha-1 antitrypsin mediated by yeast intron in Pichia pastoris. Biotechnol Lett 28: 1545-1550.
50. Charron M, Chern JY, Wright WW, (2007) The cathepsin L first intron stimulates gene expression in rat sertoli cells. Biol Reprod 76: 813-824.
51. Rose AB, Beliakoff JA, (2000) Intron-mediated enhancement of gene expression independent of unique intron sequences and splicing. Plant Physiol 122: 535-542.
52. Nott A, Meislin SH, Moore MJ, (2003) A quantitative analysis of intron effects on mammalian gene expression. RNA 9: 607-617.
53. Culler SJ, Hoff KG, Voelker RB, Berglund JA, Smolke CD, (2010) Functional selection and systematic analysis of intronic splicing elements identify active sequence motifs and associated splicing factors. Nucleic Acids Res 38: 5152-5165.
54. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, et al. (2000) Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25: 359-371.
55. Belak ZR, Ficzycz A, Ovsenek N, (2008) Biochemical characterization of Yin Yang 1-RNA complexes. Biochem Cell Biol 86: 31-36.
56. Adams DJ, Van der WL, Mayeda A, Stamm S, Morris BJ, et al. (2001) ZNF265-a novel spliceosomal protein able to induce alternative splicing. J Cell Biol 154: 25-32.
57. Jeon Y, Lee JT, (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146: 119-133.
58. Baltz AG, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, et al. (2012) The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 46: 674-690.
59. Rose AB, Emami S, Bradnam K, Korf I, (2011) Evidence for a DNA-Based Mechanism of Intron-Mediated Enhancement. Front Plant Sci 2: 98.
60. Baum C, Schambach A, (2011) Promoter competition for gene therapy of SCID-X1. Hum Gene Ther 22: 255-256.
61. Varma NR, Janic B, Ali MM, Iskander A, Arbab AS, (2011) Lentiviral Based Gene Transduction and Promoter Studies in Human Hematopoietic Stem Cells (hHSCs). J Stem Cells Regen Med 7: 41-53.