Different promoter affinities account for specificity in MYC-dependent gene regulation

eLife

Volumn 5, Issue JULY, 2016, Pages

  Lorenzin, Francesca ^a   Benary, Uwe ^b   Baluapuri, Apoorva ^a   Walz, Susanne ^a   Jung, Lisa Anna ^a,c   von Eyss, Björn ^a,d   Kisker, Caroline ^c   Wolf, Jana ^b   Eilers, Martin ^a   Wolf, Elmar ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; DNA; PROTEIN BINDING;

APOPTOSIS; ARTICLE; BINDING AFFINITY; BIOINFORMATICS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; MATHEMATICAL MODEL; PREDICTION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIMULATION; CELL LINE; DNA SEQUENCE; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SEQUENCE ANALYSIS; THEORETICAL MODEL;

CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DNA; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MODELS, THEORETICAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MYC; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC;

EID: 84982732197     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15161     Document Type: Article

References (52)

1. Altman BJ, Hsieh AL, Sengupta A, Krishnanaiah SY, Stine ZE, Walton ZE, Gouw AM, Venkataraman A, Li B, Goraksha-Hicks P, Diskin SJ, Bellovin DI, Simon MC, Rathmell JC, Lazar MA, Maris JM, Felsher DW, Hogenesch JB, Weljie AM, Dang CV, et al. 2015. MYC disrupts the circadian clock and metabolism in cancer cells. Cell Metabolism 22: 1009-1019. doi: 10.1016/j.cmet.2015.09.003
2. Bailey TL, Machanick P. 2012. Inferring direct DNA binding from ChIP-seq. Nucleic Acids Research 40: e128. doi: 10.1093/nar/gks433
3. Ben-Shoshan SO, Simon AJ, Jacob-Hirsch J, Shaklai S, Paz-Yaacov N, Amariglio N, Rechavi G, Trakhtenbrot L. 2014. Induction of polyploidy by nuclear fusion mechanism upon decreased expression of the nuclear envelope protein LAP2b in the human osteosarcoma cell line U2OS. Molecular Cytogenetics 7: 9. doi: 10.1186/1755-8166-7-9
4. Blackwell TK, Huang J, Ma A, Kretzner L, Alt FW, Eisenman RN, Weintraub H. 1993. Binding of myc proteins to canonical and noncanonical DNA sequences. Molecular and Cellular Biology 13: 5216-5224. doi: 10.1128/MCB. 13.9.5216
5. Bouchard C, Marquardt J, Brás A, Medema RH, Eilers M. 2004. Myc-induced proliferation and transformation require Akt-mediated phosphorylation of FoxO proteins. EMBO Journal 23: 2830-2840. doi: 10.1038/sj.emboj. 7600279
6. Casey SC, Tong L, Li Y, Do R, Walz S, Fitzgerald KN, Gouw AM, Baylot V, Gütgemann I, Eilers M, Felsher DW, Li Y DR. 2016. MYC regulates the antitumor immune response through CD47 and PD-L1. Science 352: 227-231. doi: 10.1126/science.aac9935
7. Conacci-Sorrell M, McFerrin L, Eisenman RN. 2014. An overview of MYC and its interactome. Cold Spring Harbor Perspectives in Medicine 4: a014357. doi: 10.1101/cshperspect.a014357
8. Dang CV. 2012. MYC on the path to cancer. Cell 149: 22-35. doi: 10.1016/j.cell.2012.03.003
9. Eberhardy SR, Farnham PJ. 2002. Myc recruits P-TEFb to mediate the final step in the transcriptional activation of the cad promoter. Journal of Biological Chemistry 277: 40156-40162. doi: 10.1074/jbc.M207441200
10. Elkon R, Loayza-Puch F, Korkmaz G, Lopes R, van Breugel PC, Bleijerveld OB, Altelaar AF, Wolf E, Lorenzin F, Eilers M, Agami R, Puch FL. 2015. Myc coordinates transcription and translation to enhance transformation and suppress invasiveness. EMBO Reports 16: 1723-1736. doi: 10.15252/embr.201540717
11. Feng J, Liu T, Qin B, Zhang Y, Liu XS. 2012. Identifying ChIP-seq enrichment using MACS. Nature Protocols 7: 1728-1740. doi: 10.1038/nprot.2012.101
12. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, Cocito A, Amati B. 2003. Genomic targets of the human c-Myc protein. Genes & Development 17: 1115-1129. doi: 10.1101/gad.1067003
13. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ. 2005. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nature Cell Biology 7: 311-318. doi: 10.1038/ncb1224
14. Guccione E, Martinato F, Finocchiaro G, Luzi L, Tizzoni L, Dall’Olio V, Zardo G, Nervi C, Bernard L, Amati B. 2006. Myc-binding-site recognition in the human genome is determined by chromatin context. Nature Cell Biology 8: 764-770. doi: 10.1038/ncb1434
15. Guo J, Li T, Schipper J, Nilson KA, Fordjour FK, Cooper JJ, Gordân R, Price DH. 2014. Sequence specificity incompletely defines the genome-wide occupancy of Myc. Genome Biology 15: 482. doi: 10.1186/s13059-014-0482-3
16. Hateboer G, Timmers HT, Rustgi AK, Billaud M, van ‘t Veer LJ, Bernards R. 1993. TATA-binding protein and the retinoblastoma gene product bind to overlapping epitopes on c-Myc and adenovirus E1A protein. Proceedings of the National Academy of Sciences of the United States of America 90: 8489-8493. doi: 10.1073/pnas.90.18. 8489
17. Hsu TY, Simon LM, Neill NJ, Marcotte R, Sayad A, Bland CS, Echeverria GV, Sun T, Kurley SJ, Tyagi S, Karlin KL, Dominguez-Vidaña R, Hartman JD, Renwick A, Scorsone K, Bernardi RJ, Skinner SO, Jain A, Orellana M, Lagisetti C, et al. 2015. The spliceosome is a therapeutic vulnerability in MYC-driven cancer. Nature 525: 384-388. doi: 10.1038/nature14985
18. Huang da W, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37: 1-13. doi: 10.1093/nar/gkn923
19. Jaenicke LA, von Eyss B, Carstensen A, Wolf E, Xu W, Greifenberg AK, Geyer M, Eilers M, Popov N. 2016. Ubiquitin-dependent turnover of MYC antagonizes MYC/PAF1C complex accumulation to drive transcriptional elongation. Molecular Cell 61: 54-67. doi: 10.1016/j.molcel.2015.11.007
20. Janssen A, Medema RH. 2013. Genetic instability: tipping the balance. Oncogene 32: 4459-4470. doi: 10.1038/onc.2012.576
21. Ji H, Wu G, Zhan X, Nolan A, Koh C, De Marzo A, Doan HM, Fan J, Cheadle C, Fallahi M, Cleveland JL, Dang CV, Zeller KI. 2011. Cell-type independent MYC target genes reveal a primordial signature involved in biomass accumulation. PLOS One 6: e26057. doi: 10.1371/journal.pone.0026057
22. Koch B, Sanchez S, Schmidt CK, Swiersy A, Jackson SP, Schmidt OG. 2014. Confinement and deformation of single cells and their nuclei inside size-adapted microtubes. Advanced Healthcare Materials 3: 1753-1758. doi: 10.1002/adhm.201300678
23. Kress TR, Cannell IG, Brenkman AB, Samans B, Gaestel M, Roepman P, Burgering BM, Bushell M, Rosenwald A, Eilers M. 2011. The MK5/PRAK kinase and Myc form a negative feedback loop that is disrupted during colorectal tumorigenesis. Molecular Cell 41: 445-457. doi: 10.1016/j.molcel.2011.01.023
24. Kress TR, Sabò A, Amati B. 2015. MYC: connecting selective transcriptional control to global RNA production. Nature Reviews. Cancer 15: 593-607. doi: 10.1038/nrc3984
25. Lin CY, Lovén J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA. 2012. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151: 56-67. doi: 10.1016/j.cell.2012.08.026
26. Liu H, Tang X, Srivastava A, Pécot T, Daniel P, Hemmelgarn B, Reyes S, Fackler N, Bajwa A, Kladney R, Koivisto C, Chen Z, Wang Q, Huang K, Machiraju R, Sáenz-Robles MT, Cantalupo P, Pipas JM, Leone G. 2015. Redeployment of Myc and E2f1-3 drives Rb-deficient cell cycles. Nature Cell Biology 17: 1036-1048. doi: 10. 1038/ncb3210
27. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD. 1998. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94: 363-374. doi: 10.1016/S0092-8674(00)81479-8
28. Meyer N, Penn LZ. 2008. Reflecting on 25 years with MYC. Nature Reviews. Cancer 8: 976-990. doi: 10.1038/nrc2231
29. Myant K, Sansom OJ. 2011. More, more, more: downregulation of a MK5-FoxO3a-mir34b/c pathway further increases c-Myc levels in colorectal cancer. Molecular Cell 41: 369-370. doi: 10.1016/j.molcel.2011.01.028
30. Nair SK, Burley SK. 2003. X-ray structures of Myc-Max and Mad-Max recognizing DNA. Molecular bases of regulation by proto-oncogenic transcription factors. Cell 112: 193-205. doi: 10.1016/S0092-8674(02)01284-9
31. Nicol JW, Helt GA, Blanchard SG, Raja A, Loraine AE. 2009. The integrated genome browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730-2731. doi: 10.1093/bioinformatics/btp472
32. Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, Wang R, Green DR, Tessarollo L, Casellas R, Zhao K, Levens D. 2012. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151: 68-79. doi: 10.1016/j.cell.2012.08.033
33. Perna D, Fagà G, Verrecchia A, Gorski MM, Barozzi I, Narang V, Khng J, Lim KC, Sung WK, Sanges R, Stupka E, Oskarsson T, Trumpp A, Wei CL, Müller H, Amati B. 2012. Genome-wide mapping of Myc binding and gene regulation in serum-stimulated fibroblasts. Oncogene 31: 1695-1709. doi: 10.1038/onc.2011.359
34. Peukert K, Staller P, Schneider A, Carmichael G, Hänel F, Eilers M. 1997. An alternative pathway for gene regulation by Myc. EMBO Journal 16: 5672-5686. doi: 10.1093/emboj/16.18.5672
35. Quinlan AR. 2014. BEDTools: The swiss-army tool for genome feature analysis. Current Protocols in Bioinformatics 47: 1-34. doi: 10.1002/0471250953.bi1112s47
36. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141: 432-445. doi: 10.1016/j.cell.2010.03.030
37. Sabò A, Amati B. 2014. Genome recognition by MYC. Cold Spring Harbor Perspectives in Medicine 4: a014191. doi: 10.1101/cshperspect.a014191
38. Sabò A, Kress TR, Pelizzola M, de Pretis S, Gorski MM, Tesi A, Morelli MJ, Bora P, Doni M, Verrecchia A, Tonelli C, Fagà G, Bianchi V, Ronchi A, Low D, Müller H, Guccione E, Campaner S, Amati B. 2014. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 511: 488-492. doi: 10.1038/nature13537
39. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH image to imageJ: 25 years of image analysis. Nature Methods 9: 671-675. doi: 10.1038/nmeth.2089
40. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U, Hermeking H. 2011. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10: 4256-4271. doi: 10.4161/cc.10.24.18552
41. Soucek L, Whitfield JR, Sodir NM, Massó-Vallés D, Serrano E, Karnezis AN, Swigart LB, Evan GI. 2013. Inhibition of Myc family proteins eradicates KRas-driven lung cancer in mice. Genes & Development 27: 504-513. doi: 10. 1101/gad.205542.112
42. Stine ZE, Walton ZE, Altman BJ, Hsieh AL, Dang CV. 2015. MYC, metabolism, and cancer. Cancer Discovery 5: 1024-1039. doi: 10.1158/2159-8290.CD-15-0507
43. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 102: 15545-15550. doi: 10.1073/pnas.0506580102
44. Thomas LR, Wang Q, Grieb BC, Phan J, Foshage AM, Sun Q, Olejniczak ET, Clark T, Dey S, Lorey S, Alicie B, Howard GC, Cawthon B, Ess KC, Eischen CM, Zhao Z, Fesik SW, Tansey WP. 2015. Interaction with WDR5 promotes target gene recognition and tumorigenesis by MYC. Molecular Cell 58: 1-13. doi: 10.1016/j.molcel. 2015.02.028
45. van Riggelen J, Müller J, Otto T, Beuger V, Yetil A, Choi PS, Kosan C, Möröy T, Felsher DW, Eilers M. 2010. The interaction between Myc and Miz1 is required to antagonize TGFbeta-dependent autocrine signaling during lymphoma formation and maintenance. Genes & Development 24: 1281-1294. doi: 10.1101/gad.585710
46. Vo BT, Wolf E, Kawauchi D, Gebhardt A, Rehg JE, Finkelstein D, Walz S, Murphy BL, Youn YH, Han YG, Eilers M, Roussel MF. 2016. The interaction of myc with Miz1 defines medulloblastoma subgroup identity. Cancer Cell 29: 5-16. doi: 10.1016/j.ccell.2015.12.003
47. Walz S, Lorenzin F, Morton J, Wiese KE, von Eyss B, Herold S, Rycak L, Dumay-Odelot H, Karim S, Bartkuhn M, Roels F, Wüstefeld T, Fischer M, Teichmann M, Zender L, Wei CL, Sansom O, Wolf E, Eilers M. 2014. Activation and repression by oncogenic MYC shape tumour-specific gene expression profiles. Nature 511: 483-487. doi: 10.1038/nature13473
48. Wiese KE, Haikala HM, von Eyss B, Wolf E, Esnault C, Rosenwald A, Treisman R, Klefström J, Eilers M. 2015. Repression of SRF target genes is critical for Myc-dependent apoptosis of epithelial cells. EMBO Journal 34: 1554-1571. doi: 10.15252/embj.201490467
49. Wiese KE, Walz S, von Eyss B, Wolf E, Athineos D, Sansom O, Eilers M. 2013. The role of MIZ-1 in MYC-dependent tumorigenesis. Cold Spring Harbor Perspectives in Medicine 3: a014290. doi: 10.1101/cshperspect.a014290
50. Wolf E, Lin CY, Eilers M, Levens DL. 2015. Taming of the beast: shaping Myc-dependent amplification. Trends in Cell Biology 25: 241-248. doi: 10.1016/j.tcb.2014.10.006
51. Xu H, Handoko L, Wei X, Ye C, Sheng J, Wei CL, Lin F, Sung WK. 2010. A signal-noise model for significance analysis of ChIP-seq with negative control. Bioinformatics 26: 1199-1204. doi: 10.1093/bioinformatics/btq128
52. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25: 1952-1958. doi: 10.1093/bioinformatics/btp340