Long-range transcriptional regulation by the p110 CUX1 homeodomain protein on the ENCODE array

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Vadnais, Charles ^a,b   Awan, Arif A ^a   Harada, Ryoko ^a   Clermont, Pier Luc ^b   Leduy, Lam ^a   Bérubé, Ginette ^a   Nepveu, Alain ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

ChAP chip; Chromatin immunoprecipitation; Cut homeobox 1 (CUX1); ENCODE and promoter microarrays; Expression profiling; Lentivirus overexpression; Regulation at a distance; shRNA; Transcriptional activation and repression

Indexed keywords

ALANINE; ARGININE; CYSTEINE; DNA; PROTEIN CUX1; PROTEIN P110; THYMINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; DNA HYBRIDIZATION; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE LOCATION; GENE LOCUS; GENE MAPPING; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENETIC DISTANCE; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; FEMALE; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; REPRESSOR PROTEINS; TISSUE ARRAY ANALYSIS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTIONAL ACTIVATION;

LENTIVIRUS;

EID: 84876075513     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-258     Document Type: Article

References (75)

1. Jenuwein T, Allis CD. Translating the histone code. Science 2001, 293(5532):1074-1080. 10.1126/science.1063127, 11498575.
2. Turner BM. Cellular memory and the histone code. Cell 2002, 111(3):285-291. 10.1016/S0092-8674(02)01080-2, 12419240.
3. MacQuarrie KL, Fong AP, Morse RH, Tapscott SJ. Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet 2011, 27(4):141-148. 10.1016/j.tig.2011.01.001, 3068217, 21295369.
4. Mantripragada KK, Buckley PG, Diaz de Stahl T, Dumanski JP. Genomic microarrays in the spotlight. Trends Genet 2004, 20(2):87-94. 10.1016/j.tig.2003.12.008, 14746990.
5. Bosher JM, Labouesse M. RNA interference: genetic wand and genetic watchdog. Nat Cell Biol 2000, 2(2):E31-E36. 10.1038/35000102, 10655601.
6. Hofmann A, Nolan GP, Blau HM. Rapid retroviral delivery of tetracycline-inducible genes in a single autoregulatory cassette [see comments]. Proc Natl Acad Sci U S A 1996, 93(11):5185-5190. 10.1073/pnas.93.11.5185, 39219, 8643550.
7. Paulus W, Baur I, Boyce FM, Breakefield XO, Reeves SA. Self-contained, tetracycline-regulated retroviral vector system for gene delivery to mammalian cells. J Virol 1996, 70(1):62-67. 189788, 8523582.
8. Meyerson M, Gabriel S, Getz G. Advances in understanding cancer genomes through second-generation sequencing. Nat Rev Genet 2010, 11(10):685-696. 10.1038/nrg2841, 20847746.
9. Gilmour DS, Lis JT. In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol Cell Biol 1985, 5(8):2009-2018. 366919, 3018544.
10. Marzio G, Tyagi M, Gutierrez MI, Giacca M. HIV-1 tat transactivator recruits p300 and CREB-binding protein histone acetyltransferases to the viral promoter. Proc Natl Acad Sci U S A 1998, 95(23):13519-13524. 10.1073/pnas.95.23.13519, 24851, 9811832.
11. Consortium EP. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 2004, 306(5696):636-640.
12. Farnham PJ. Insights from genomic profiling of transcription factors. Nat Rev Genet 2009, 10(9):605-616. 10.1038/nrg2636, 2846386, 19668247.
13. Amati B, Land H. Myc-Max-Mad: a transcription factor network controlling cell cycle progression, differentiation and death. Curr Op Genet Dev 1994, 4(1):102-108. 10.1016/0959-437X(94)90098-1, 8193530.
14. Bieda M, Xu X, Singer MA, Green R, Farnham PJ. Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006, 16(5):595-605. 10.1101/gr.4887606, 1457046, 16606705.
15. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, Piccolboni A, Sementchenko V, Cheng J, Williams AJ. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004, 116(4):499-509. 10.1016/S0092-8674(04)00127-8, 14980218.
16. Lin CY, Loven J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA. Transcriptional Amplification in Tumor Cells with Elevated c-Myc. Cell 2012, 151(1):56-67. 10.1016/j.cell.2012.08.026, 23021215.
17. Sansregret L, Nepveu A. The multiple roles of CUX1: Insights from mouse models and cell-based assays. Gene 2008, 412(1-2):84-94.
18. Moon NS, Berube G, Nepveu A. CCAAT displacement activity involves Cut repeats 1 and 2, not the Cut homeodomain. J Biol Chem 2000, 275(40):31325-31334.
19. Moon NS, Premdas P, Truscott M, Leduy L, Berube G, Nepveu A. S Phase-Specific Proteolytic Cleavage Is Required to Activate Stable DNA Binding by the CDP/Cut Homeodomain Protein. Mol Cell Biol 2001, 21:6332-6345. 10.1128/MCB.21.18.6332-6345.2001, 87367, 11509674.
20. Goulet B, Baruch A, Moon NS, Poirier M, Sansregret LL, Erickson A, Bogyo M, Nepveu A. A Cathepsin L Isoform that Is Devoid of a Signal Peptide Localizes to the Nucleus in S Phase and Processes the CDP/Cux Transcription Factor. Mol Cell 2004, 14(2):207-219. 10.1016/S1097-2765(04)00209-6, 15099520.
21. Harada R, Vadnais C, Sansregret L, Leduy L, Berube G, Robert F, Nepveu A. Genome-wide location analysis and expression studies reveal a role for p110 CUX1 in the activation of DNA replication genes. Nucleic Acids Res 2008, 36(1):189-202. 2248751, 18003658.
22. Kedinger V, Sansregret L, Harada R, Vadnais C, Cadieux C, Fathers K, Park M, Nepveu A. p110 CUX1 homeodomain protein stimulates cell migration and invasion in part through a regulatory cascade culminating in the repression of E-cadherin and occludin. J Biol Chem 2009, 284(40):27701-27711. 10.1074/jbc.M109.031849, 2785698, 19635798.
23. Coqueret O, Berube G, Nepveu A. The mammalian Cut homeodomain protein functions as a cell-cycle-dependent transcriptional repressor which downmodulates p21WAF1/CIP1/SDI1 in S phase. EMBO J 1998, 17(16):4680-4694. 10.1093/emboj/17.16.4680, 1170797, 9707427.
24. Santaguida M, Ding Q, Berube G, Truscott M, Whyte P, Nepveu A. Phosphorylation of the CCAAT displacement protein (CDP)/Cux transcription factor by cyclin A-Cdk1 modulates its DNA binding activity in G(2). J Biol Chem 2001, 276(49):45780-45790. 10.1074/jbc.M107978200, 11584018.
25. Santaguida M, Nepveu A. Differential regulation of CDP/Cux p110 by cyclin A/Cdk2 and cyclin A/Cdk1. J Biol Chem 2005, 280(38):32712-32721. 10.1074/jbc.M505417200, 16081423.
26. Sansregret L, Gallo D, Santaguida M, Leduy L, Harada R, Nepveu A. Hyperphosphorylation by cyclin B/CDK1 in mitosis resets CUX1 DNA binding clock at each cell cycle. J Biol Chem 2010, 285(43):32834-32843. 10.1074/jbc.M110.156406, 2963374, 20729212.
27. Truscott M, Denault JB, Goulet B, Leduy L, Salvesen GS, Nepveu A. Carboxyl-terminal proteolytic processing of CUX1 by a caspase enables transcriptional activation in proliferating cells. J Biol Chem 2007, 282(41):30216-30226. 10.1074/jbc.M702328200, 17681953.
28. Ellis T, Gambardella L, Horcher M, Tschanz S, Capol J, Bertram P, Jochum W, Barrandon Y, Busslinger M. The transcriptional repressor CDP (Cutl1) is essential for epithelial cell differentiation of the lung and the hair follicle. Genes Dev 2001, 15(17):2307-2319. 10.1101/gad.200101, 312776, 11544187.
29. Sinclair AM, Lee JA, Goldstein A, Xing D, Liu S, Ju R, Tucker PW, Neufeld EJ, Scheuermann RH. Lymphoid apoptosis and myeloid hyperplasia in CCAAT displacement protein mutant mice. Blood 2001, 98(13):3658-3667. 10.1182/blood.V98.13.3658, 11739170.
30. Luong MX, van der Meijden CM, Xing D, Hesselton R, Monuki ES, Jones SN, Lian JB, Stein JL, Stein GS, Neufeld EJ. Genetic ablation of the CDP/Cux protein C terminus results in hair cycle defects and reduced male fertility. Mol Cell Biol 2002, 22(5):1424-1437. 10.1128/MCB.22.5.1424-1437.2002, 134686, 11839809.
31. Ledford AW, Brantley JG, Kemeny G, Foreman TL, Quaggin SE, Igarashi P, Oberhaus SM, Rodova M, Calvet JP, Vanden Heuvel GB. Deregulated Expression of the Homeobox Gene Cux-1 in Transgenic Mice Results in Downregulation of p27(kip1) Expression during Nephrogenesis, Glomerular Abnormalities, and Multiorgan Hyperplasia. Dev Biol 2002, 245(1):157-171. 10.1006/dbio.2002.0636, 11969263.
32. Brantley JG, Sharma M, Alcalay NI, Heuvel GBV. Cux-1 transgenic mice develop glomerulosclerosis and interstitial fibrosis. Kidney Int 2003, 63(4):1240-1248. 10.1046/j.1523-1755.2003.00889.x, 12631340.
33. Cadieux C, Kedinger V, Yao L, Vadnais C, Drossos M, Paquet M, Nepveu A. Mouse mammary tumor virus p75 and p110 CUX1 transgenic mice develop mammary tumors of various histologic types. Cancer Res 2009, 69(18):7188-7197. 10.1158/0008-5472.CAN-08-4899, 19738070.
34. Cadieux C, Harada R, Paquet M, Cote O, Trudel M, Nepveu A, Bouchard M. Polycystic kidneys caused by sustained expression of Cux1 isoform p75. J Biol Chem 2008, 283(20):13817-13824. 10.1074/jbc.M709332200, 18356167.
35. Cadieux C, Fournier S, Peterson AC, Bedard C, Bedell BJ, Nepveu A. Transgenic mice expressing the p75 CCAAT-displacement protein/Cut homeobox isoform develop a myeloproliferative disease-like myeloid leukemia. Cancer Res 2006, 66(19):9492-9501. 10.1158/0008-5472.CAN-05-4230, 17018605.
36. Heuvel GBV, Bodmer R, McConnell KR, Nagami GT, Igarashi P. Expression Of a Cut-Related Homeobox Gene In Developing and Polycystic Mouse Kidney. Kidney Int 1996, 50(2):453-461. 10.1038/ki.1996.336, 8840273.
37. Sansregret L, Goulet B, Harada R, Wilson B, Leduy L, Bertoglio J, Nepveu A. The p110 isoform of the CDP/Cux transcription factor accelerates entry into S phase. Mol Cell Biol 2006, 26(6):2441-2455. 10.1128/MCB.26.6.2441-2455.2006, 1430290, 16508018.
38. Sansregret L, Vadnais C, Livingstone J, Kwiatkowski N, Awan A, Cadieux C, Leduy L, Hallett MT, Nepveu A. Cut homeobox 1 causes chromosomal instability by promoting bipolar division after cytokinesis failure. Proc Natl Acad Sci U S A 2011, 108(5):1949-1954. 10.1073/pnas.1008403108, 3033318, 21245318.
39. Michl P, Ramjaun AR, Pardo OE, Warne PH, Wagner M, Poulsom R, D'Arrigo C, Ryder K, Menke A, Gress T. CUTL1 is a target of TGF(beta) signaling that enhances cancer cell motility and invasiveness. Cancer Cell 2005, 7(6):521-532. 10.1016/j.ccr.2005.05.018, 15950902.
40. Michl P, Downward J. CUTL1: a key mediator of TGFbeta-induced tumor invasion. Cell Cycle 2006, 5(2):132-134. 10.4161/cc.5.2.2311, 16357536.
41. Aleksic T, Bechtel M, Krndija D, von Wichert G, Knobel B, Giehl K, Gress TM, Michl P. CUTL1 promotes tumor cell migration by decreasing proteasome-mediated Src degradation. Oncogene 2007, 26(40):5939-5949. 10.1038/sj.onc.1210398, 17369846.
42. Ripka S, Neesse A, Riedel J, Bug E, Aigner A, Poulsom R, Fulda S, Neoptolemos J, Greenhalf W, Barth P. CUX1: target of Akt signalling and mediator of resistance to apoptosis in pancreatic cancer. Gut 2010, 59(8):1101-1110. 10.1136/gut.2009.189720, 20442202.
43. Cubelos B, Sebastian-Serrano A, Beccari L, Calcagnotto ME, Cisneros E, Kim S, Dopazo A, Alvarez-Dolado M, Redondo JM, Bovolenta P. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 2010, 66(4):523-535. 10.1016/j.neuron.2010.04.038, 2894581, 20510857.
44. Scacheri PC, Davis S, Odom DT, Crawford GE, Perkins S, Halawi MJ, Agarwal SK, Marx SJ, Spiegel AM, Meltzer PS. Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet 2006, 2(4):e51. 10.1371/journal.pgen.0020051, 1428788, 16604156.
45. Yang A, Zhu Z, Kapranov P, McKeon F, Church GM, Gingeras TR, Struhl K. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006, 24(4):593-602. 10.1016/j.molcel.2006.10.018, 17188034.
46. Krig SR, Jin VX, Bieda MC, O'Geen H, Yaswen P, Green R, Farnham PJ. Identification of genes directly regulated by the oncogene ZNF217 using chromatin immunoprecipitation (ChIP)-chip assays. J Biol Chem 2007, 282(13):9703-9712. 10.1074/jbc.M611752200, 2269729, 17259635.
47. Harada R, Berube G, Tamplin OJ, Denis-Larose C, Nepveu A. DNA-binding specificity of the cut repeats from the human cut-like protein. Mol Cell Biol 1995, 15(1):129-140. 231920, 7799919.
48. Harada R, Nepveu A. Chromatin affinity purification. Meth Mol Biol (Clifton, NJ) 2012, 809(22113280):237-253.
49. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B. A high-resolution map of active promoters in the human genome. Nature 2005, 436(7052):876-880. 10.1038/nature03877, 1895599, 15988478.
50. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122(1):33-43. 10.1016/j.cell.2005.05.008, 16009131.
51. Ruiz-Llorente S, de Pau EC, Sastre-Perona A, Montero-Conde C, Gomez-Lopez G, Fagin JA, Valencia A, Pisano DG, Santisteban P. Genome-wide analysis of Pax8 binding provides new insights into thyroid functions. BMC Genomics 2012, 13:147. 10.1186/1471-2164-13-147, 3403905, 22531031.
52. Li Q, Harju S, Peterson KR. Locus control regions: coming of age at a decade plus. Trends Genet 1999, 15(10):403-408. 10.1016/S0168-9525(99)01780-1, 10498936.
53. Gaszner M, Felsenfeld G. Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 2006, 7(9):703-713. 10.1038/nrg1925, 16909129.
54. Gross DS, Garrard WT. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 1988, 57:159-197. 10.1146/annurev.bi.57.070188.001111, 3052270.
55. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B. The accessible chromatin landscape of the human genome. Nature 2012, 489(7414):75-82. 10.1038/nature11232, 22955617.
56. Ernst J, Kellis M. ChromHMM: automating chromatin-state discovery and characterization. Nat Methods 2012, 9(3):215-216. 10.1038/nmeth.1906, 3577932, 22373907.
57. Vadnais C, Davoudi S, Afshin M, Harada R, Dudley R, Clermont PL, Drobetsky E, Nepveu A. CUX1 transcription factor is required for optimal ATM/ATR-mediated responses to DNA damage. Nucleic Acids Res 2012, 40(10):4483-4495. 10.1093/nar/gks041, 3378881, 22319212.
58. Seguin L, Liot C, Mzali R, Harada R, Siret A, Nepveu A, Bertoglio J. CUX1 and E2F1 regulate coordinated expression of the mitotic complex genes Ect2, MgcRacGAP, and MKLP1 in S phase. Mol Cell Biol 2009, 29(2):570-581. 10.1128/MCB.01275-08, 2612504, 19015243.
59. Truscott M, Harada R, Vadnais C, Robert F, Nepveu A. p110 CUX1 cooperates with E2F transcription factors in the transcriptional activation of cell cycle-regulated genes. Mol Cell Biol 2008, 28(10):3127-3138. 10.1128/MCB.02089-07, 2423173, 18347061.
60. Kraus MH, Yuasa Y, Aaronson SA. A position 12-activated H-ras oncogene in all HS578T mammary carcinosarcoma cells but not normal mammary cells of the same patient. Proc Natl Acad Sci U S A 1984, 81(17):5384-5388. 10.1073/pnas.81.17.5384, 391708, 6089200.
61. Geck P, Maffini MV, Szelei J, Sonnenschein C, Soto AM. Androgen-induced proliferative quiescence in prostate cancer cells: the role of AS3 as its mediator. Proc Natl Acad Sci U S A 2000, 97(18):10185-10190. 10.1073/pnas.97.18.10185, 27796, 10963680.
62. Saqr HE, Omran O, Dasgupta S, Yu RK, Oblinger JL, Yates AJ. Endogenous GD3 ganglioside induces apoptosis in U-1242 MG glioma cells. J Neurochem 2006, 96(5):1301-1314. 10.1111/j.1471-4159.2005.03640.x, 16441517.
63. Sipione S, Rigamonti D, Valenza M, Zuccato C, Conti L, Pritchard J, Kooperberg C, Olson JM, Cattaneo E. Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses. Hum Mol Genet 2002, 11(17):1953-1965. 10.1093/hmg/11.17.1953, 12165557.
64. Weinmann AS, Farnham PJ. Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods 2002, 26(1):37-47. 10.1016/S1046-2023(02)00006-3, 12054903.
65. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Seraphin B. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 2001, 24(3):218-229. 10.1006/meth.2001.1183, 11403571.
66. Ren B, Cam H, Takahashi Y, Volkert T, Terragni J, Young RA, Dynlacht BD. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev 2002, 16(2):245-256. 10.1101/gad.949802, 155321, 11799067.
67. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 2010, Chapter 19:Unit 19 10 11-21.
68. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15(10):1451-1455. 10.1101/gr.4086505, 1240089, 16169926.
69. Goecks J, Nekrutenko A, Taylor J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11(8):R86. 10.1186/gb-2010-11-8-r86, 2945788, 20738864.
70. Bailey TL. DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 2011, 27(12):1653-1659. 10.1093/bioinformatics/btr261, 3106199, 21543442.
71. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37(Web Server issue):W202-W208. 2703892, 19458158.
72. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. Quantifying similarity between motifs. Genome Biol 2007, 8(2):R24. 10.1186/gb-2007-8-2-r24, 1852410, 17324271.
73. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
74. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37(1):1-13. 10.1093/nar/gkn923, 2615629, 19033363.
75. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.