Dimerization of FIR upon FUSE DNA binding suggests a mechanism of c-myc inhibition

EMBO Journal

Volumn 27, Issue 1, 2008, Pages 277-289

  Crichlow, Gregg V ^a   Zhou, Hongwen ^a   Hsiao, Hsin Hao ^a   Frederick, Kendra B ^b   Debrosse, Maxime ^a   Yang, Yuande ^a   Folta Stogniew, Ewa J ^a   Chung, Hye Jung ^c   Fan, Chengpeng ^a   De La Cruz, Enrique M ^b   Levens, David ^c   Lolis, Elias ^a   Braddock, Demetrios ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

c myc; FBP interacting repressor; Gene transcription; RRM domain; X ray crystallography

Indexed keywords

BINDING PROTEIN; DIMER; FUSE BINDING PROTEIN; FUSE BINDING PROTEIN INTERACTING REPRESSOR PROTEIN; NUCLEIC ACID; REPRESSOR PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL GROWTH; CRYSTAL STRUCTURE; DIMERIZATION; DNA BINDING; GEL PERMEATION CHROMATOGRAPHY; GENETIC TRANSCRIPTION; HOMEOSTASIS; LIGHT SCATTERING; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA; DNA HELICASES; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; TRANSCRIPTION FACTOR TFIIH;

EID: 38049008000     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601936     Document Type: Article

References (60)

1. Allain FH, Gilbert DE, Bouvet P, Feigon J (2000) Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target. J Mol Biol 303: 227-241
2. Amrute SB, Abdul-Manan Z, Pandey V, Williams KR, Modak MJ (1994) Purification and nucleic acid binding properties of a fragment of type C1/C2 heterogeneous nuclear ribonucleoprotein from thymic nuclear extracts. Biochemistry 33: 8282-8291
3. Auweter SD, Oberstrass FC, Allain FH (2006) Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res 34: 4943-4959
4. Bae E, Reiter NJ, Bingman CA, Kwan SS, Lee D, Phillips Jr GN, Butcher SE, Brow DA (2007) Structure and interactions of the first three RNA recognition motifs of splicing factor prp24. J Mol Biol 367: 1447-1458
5. Braddock DT, Baber JL, Levens D, Clore GM (2002a) Molecular basis of sequence-specific single-stranded DNA recognition by KH domains: solution structure of a complex between hnRNP KKH3 and single-stranded DNA. EMBO J 21: 3476-3485
6. Braddock DT, Cai ML, Baber JL, Huang Y, Clore GM (2001) Rapid identification of medium- to large-scale interdomain motion in modular proteins using dipolar couplings. J Am Chem Soc 123: 8634-8635
7. Braddock DT, Louis JM, Baber JL, Levens D, Clore GM (2002b) Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature 415: 1051-1056
8. Chung HJ, Liu J, Dundr M, Nie Z, Sanford S, Levens D (2006) FBPs are calibrated molecular tools to adjust gene expression. Mol Cell Biol 26: 6584-6597
9. Conte MR, Grune T, Ghuman J, Kelly G, Ladas A, Matthews S, Curry S (2000) Structure of tandem RNA recognition motifs from polypyrimidine tract binding protein reveals novel features of the RRM fold. EMBO J 19: 3132-3141
10. Dang CV, Resar LMS, Emison E, Kim S, Li Q, Prescott JE, Wonsey D, Zeller K (1999) Function of the c-Myc oncogenic transcription factor. Exp Cell Res 253: 63-77
11. Davis AC, Wims M, Spotts GD, Hann SR, Bradley A (1993) A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev 7: 671-682
12. DeLano WL (2002) The PyMOL Molecular Graphics System. Palo Alto, CA: DeLano Scientific, http://www.pymol.org
13. Deo RC, Bonanno JB, Sonenberg N, Burley SK (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98: 835-845
14. Ding J, Hayashi MK, Zhang Y, Manche L, Krainer AR, Xu RM (1999) Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev 13: 1102-1115
15. Duncan R, Bazar L, Michelotti G, Tomonaga T, Krutzsch H, Avigan M, Levens D (1994) Sequence-specific, single-strand binding-protein activates the far upstream element of c-Myc and defines a new DNA-binding motif. Genes Dev 8: 465-480
16. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132
17. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Hancock DC (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128
18. Fernandez EJ, Wilken J, Thompson DA, Peiper SC, Lolis E (2000) Comparison of the structure of vMIP-II with eotaxin-1, RANTES, and MCP-3 suggests a unique mechanism for CCR3 activation. Biochemistry 39: 12837-12844
19. Folta-Stogniew E, Williams KR (1999) Determination of molecular masses of proteins in solution: implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory. J Biomol Tech 10: 51-63
20. Handa N, Nureki O, Kurimoto K, Kim I, Sakamoto H, Shimura Y, Muto Y, Yokoyama S (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398: 579-585
21. He L, Bradrick TD, Karpova TS, Wu X, Fox MH, Fischer R, McNally JG, Knutson JR, Grammer AC, Lipsky PE (2003) Flow cytometric measurement of fluorescence (Forster) resonance energy transfer from cyan fluorescent protein to yellow fluorescent protein using single-laser excitation at 458 nm. Cytometry A 53: 39-54
22. He LS, Liu JH, Collins I, Sanford S, O'Connell B, Benham CJ, Levens D (2000) Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J 19: 1034-1044
23. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47 (Part 2): 110-119
24. Kabsch W (1976) A solution for the best rotation to relate two sets of vectors. Acta Crystallogr A 32: 922-923
25. Kantardjieff KA, Rupp B (2003) Matthews coefficient probabilities: improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals. Protein Sci 12: 1865-1871
26. Kraulis PJ (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950
27. Law MJ, Rice AJ, Lin P, Laird-Offringa IA (2006) The role of RNA structure in the interaction of U1A protein with U1 hairpin II RNA. RNA 12: 1168-1178
28. Liu J, Kouzine F, Nie Z, Chung HJ, Elisha-Feil Z, Weber A, Zhao K, Levens D (2006) The FUSE/FBP/FIR/TFIIH system is a molecular machine programming a pulse of c-myc expression. EMBO J 25: 2119-2130
29. Liu JH, Akoulitchev S, Weber A, Ge H, Chuikov S, Libutti D, Wang XW, Conaway JW, Harris CC, Conaway RC, Reinberg D, Levens D (2001) Defective interplay of activators and repressors with TFIIH in xeroderma pigmentosum. Cell 104: 353-363
30. Liu JH, He LS, Collins I, Ge H, Libutti D, Li JF, Egly JM, Levens D (2000) The FBP interacting repressor targets TFIIH to inhibit activated transcription. Mol Cell 5: 331-341
31. Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131
32. Mateyak MK, Obaya AJ, Adachi S, Sedivy JM (1997) Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ 8: 1039-1048
33. Matsushita K, Tomonaga T, Shimada H, Shioya A, Higashi M, Matsubara H, Harigaya K, Nomura F, Libutti D, Levens D, Ochiai T (2006) An essential role of alternative splicing of c-myc suppressor FUSE-binding protein-interacting repressor in carcinogenesis. Cancer Res 66: 1409-1417
34. Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497
35. Menssen A, Hermeking H (2002) Characterization of the c-MYC-regulated transcriptome by SAGE: identification and analysis of c-MYC target genes. Proc Natl Acad Sci USA 99: 6274-6279
36. Merritt EA, Bacon DJ (1997) Raster3D photorealistic molecular graphics. Methods Enzymol 277: 505-524
37. Michelotti GA, Michelotti EF, Pullner A, Duncan RC, Eick D, Levens D (1996) Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo. Mol Cell Biol 16: 2656-2669
38. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255
39. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wenter P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, Allain FH (2005) Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 309: 2054-2057
40. Orian A, van Steensel B, Delrow J, Bussemaker HJ, Li L, Sawado T, Williams E, Loo LW, Cowley SM, Yost C, Pierce S, Edgar BA, Parkhurst SM, Eisenman RN (2003) Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev 17: 1101-1114
41. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
42. Page-McCaw PS, Amonlirdviman K, Sharp PA (1999) PUF60: a novel U2AF65-related splicing activity. RNA 5: 1548-1560
43. Perrakis A, Sixma TK, Wilson KS, Lamzin VS (1997) wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallogr D 53: 448-455
44. Poleev A, Hartmann A, Stamm S (2000) A trans-acting factor, isolated by the three-hybrid system, that influences alternative splicing of the amyloid precursor protein minigene. Eur J Biochem 267: 4002-4010
45. Quinn LM, Dickins RA, Coombe M, Hime GR, Bowtell DD, Richardson H (2004) Drosophila Hfp negatively regulates dmyc and stg to inhibit cell proliferation. Development 131: 1411-1423
46. Rimmele ME, Belasco JG (1998) Target discrimination by RNA-binding proteins: role of the ancillary protein U2′ and a critical leucine residue in differentiating the RNA-binding specificity of spliceosomal proteins U1A and U2B″. RNA 4: 1386-1396
47. Shamoo Y, Abdul-Manan N, Patten AM, Crawford JK, Pellegrini MC, Williams KR (1994) Both RNA-binding domains in heterogenous nuclear ribonucleoprotein A1 contribute toward single-stranded-RNA binding. Biochemistry 33: 8272-8281
48. Shamoo Y, Abdul-Manan N, Williams KR (1995) Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res 23: 725-728
49. Sickmier EA, Frato KE, Shen H, Paranawithana SR, Green MR, Kielkopf CL (2006) Structural basis of polypyrimidine tract recognition by the essential pre-mRNA splicing factor, U2AF65. Mol Cell 23: 49-59
50. Skrisovska L, Bourgeois CF, Stefl R, Grellscheid SN, Kister L, Wenter P, Elliott DJ, Stevenin J, Allain FH (2007) The testis-specific human protein RBMY recognizes RNA through a novel mode of interaction. EMBO Rep 8: 372-379
51. Terwilliger TC (1999) Reciprocal-space solvent flattening. Acta Crystallogr D 55: 1863-1871
52. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55 (Part 4): 849-861
53. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680
54. Trumpp A, Refaeli Y, Oskarsson T, Gasser S, Murphy M, Martin GR, Bishop JM (2001) c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 414: 768-773
55. Van Buskirk C, Schupbach T (2002) Half pint regulates alternative splice site selection in Drosophila. Dev Cell 2: 343-353
56. Vitali F, Henning A, Oberstrass FC, Hargous Y, Auweter SD, Erat M, Allain FH (2006) Structure of the two most C-terminal RNA recognition motifs of PTB using segmental isotope labeling. EMBO J 25: 150-162
57. Wang XM, Tanaka Hall TM (2001) Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat Struct Biol 8: 141-145
58. Wen J, Arakawa T, Talvenheimo J, Welcher AA, Horan T, Kita Y, Tseng J, Nicolson M, Philo JS (1996) Techniques in Protein Chemistry. San Diego: Academic
59. Zamore PD, Patton JG, Green MR (1992) Cloning and domain structure of the mammalian splicing factor U2AF. Nature 355: 609-614
60. Zhou Z, Licklider LJ, Gygi SP, Reed R (2002) Comprehensive proteomic analysis of the human spliceosome. Nature 419: 182-185