Multiple conformations are a conserved and regulatory feature of the RB1 5' UTR

RNA

Volumn 21, Issue 7, 2015, Pages 1274-1285

  Kutchko, Katrina M ^a   Sanders, Wes ^a   Ziehr, Ben ^a,b   Phillips, Gabriela ^a   Solem, Amanda ^a   Halvorsen, Matthew ^c   Weeks, Kevin M ^d   M, Nathaniel ^e   Moorman, Nathaniel ^a,b   Laederach, Alain ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d University of North Carolina at Chapel Hill   (United States)

^e NONE

Author keywords

Covariation; Retinoblastoma; RiboSNitch; SHAPE; UTR

Indexed keywords

MESSENGER RNA; RETINOBLASTOMA PROTEIN; RETINOBLASTOMA PROTEIN 1; RNA; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION;

5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; CONTROLLED STUDY; ENTROPY; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSFECTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; NONHUMAN; PARTITION COEFFICIENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; RETINA CELL; RETINOBLASTOMA; RNA CONFORMATION; RNA STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; TAURINE CATTLE; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION; TRICHECHUS MANATUS; TRICHECHUS MANATUS LATIROSTRIS; VECTOR CONTROL; WILD TYPE; GENETICS; PHYLOGENY; PHYSIOLOGY; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

BOS TAURUS; EUKARYOTA; HOMO SAPIENS; TRICHECHUS MANATUS LATIROSTRIS;

5' UNTRANSLATED REGIONS; HUMANS; PHYLOGENY; PROTEIN CONFORMATION; RETINOBLASTOMA PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84931082831     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.049221.114     Document Type: Article

References (93)

1. Agius P, Bennett KP, Zuker M. 2010. Comparing RNA secondary structures using a relaxed base-pair score. RNA 16: 865-878.
2. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, Landthaler M, Dieterich C. 2012. doRiNA: a database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res 40: D180-D186.
3. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
4. Batey RT, Gilbert SD, Montange RK. 2004. Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432: 411-415.
5. Benjamin EJ, Dupuis J, Larson MG, Lunetta KL, Booth SL, Govindaraju DR, Kathiresan S, Keaney JF Jr, Keyes MJ, Lin JP, et al. 2007. Genome-wide association with select biomarker traits in the Framingham Heart Study. BMC Med Genet 8: S11.
6. Bernhart SH, Tafer H, Muckstein U, Flamm C, Stadler PF, Hofacker IL. 2006. Partition function and base pairing probabilities of RNA heterodimers. Algorithms Mol Biol 1: 3.
7. Bulik-Sullivan B, Selitsky S, Sethupathy P. 2013. Prioritization of genetic variants in the microRNA regulome as functional candidates in genome-wide association studies. Hum Mutat 34: 1049-1056.
8. Burckin T, Nagel R, Mandel-Gutfreund Y, Shiue L, Clark TA, Chong JL, Chang TH, Squazzo S, Hartzog G, Ares M Jr. 2005. Exploring functional relationships between components of the gene expression machinery. Nat Struct Mol Biol 12: 175-182.
9. Cancer Genome Atlas Research Network. 2012. Comprehensive genomic characterization of squamous cell lung cancers. Nature 489: 519-525.
10. Celander DW, Cech TR. 1991. Visualizing the higher order folding of a catalytic RNA molecule. Science 251: 401-407.
11. Coller J, Parker R. 2005. General translational repression by activators of mRNA decapping. Cell 122: 875-886.
12. Cowell JK, Bia B, Akoulitchev A. 1996. A novel mutation in the promoter region in a family with a mild form of retinoblastoma indicates the location of a new regulatory domain for the RB1 gene. Oncogene 12: 431-436.
13. Crick F. 1970. Central dogma of molecular biology. Nature 227: 561-563.
14. Deigan KE, Li TW, Mathews DH, Weeks KM. 2009. Accurate SHAPEdirected RNA structure determination. Proc Natl Acad Sci 106: 97-102.
15. Ding Y, Chan CY, Lawrence CE. 2004. Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Res 32: W135-W141.
16. Ding Y, Chan CY, Lawrence CE. 2005. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA 11: 1157-1166.
17. Eddy SR. 2006. Computational analysis of RNAs. Cold Spring Harb Symp Quant Biol 71: 117-128.
18. Eddy SR. 2009. A new generation of homology search tools based on probabilistic inference. Genome Inform 23: 205-211.
19. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
20. Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-37.
21. Gardner PP, Giegerich R. 2004. A comprehensive comparison of comparative RNA structure prediction approaches. BMC Bioinformatics 5: 140.
22. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, et al. 2009. Rfam: updates to the RNA families database. Nucleic Acids Res 37: D136-D140.
23. Gardner PP, Daub J, Tate J, Moore BL, Osuch IH, Griffiths-Jones S, Finn RD, Nawrocki EP, Kolbe DL, Eddy SR, et al. 2011. Rfam: Wikipedia, clans and the "decimal" release. Nucleic Acids Res 39: D141-D145.
24. George RA, Smith TD, Callaghan S, Hardman L, Pierides C, Horaitis O, Wouters MA, Cotton RG. 2008. General mutation databases: analysis and review. J Med Genet 45: 65-70.
25. Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR. 2003. Rfam: an RNA family database. Nucleic Acids Res 31: 439-441.
26. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. 2005. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33: D121-124.
27. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
28. Gutell RR, Lee JC, Cannone JJ. 2002. The accuracy of ribosomal RNA comparative structure models. Curr Opin Struct Biol 12: 301-310.
29. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, et al. 2010a. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
30. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp AC, Munschauer M, et al. 2010b. PAR-CliP - a method to identify transcriptome-wide the binding sites of RNA binding proteins. J Vis Exp: e2034.
31. Hajdin CE, Bellaousov S, Huggins W, Leonard CW, Mathews DH, Weeks KM. 2013. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc Natl Acad Sci 110: 5498-5503.
32. Halvorsen M, Martin JS, Broadaway S, Laederach A. 2010. Disease-associated mutations that alter the RNA structural ensemble. PLoS Genet 6: e1001074.
33. Huynen M, Gutell R, Konings D. 1997. Assessing the reliability of RNA folding using statistical mechanics. J Mol Biol 267: 1104-1112.
34. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. 1992. Effects of an Rb mutation in the mouse. Nature 359: 295-300.
35. Johnson LS, Eddy SR, Portugaly E. 2010. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11: 431.
36. Karabiber F, McGinnis JL, Favorov OV, Weeks KM. 2013. QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA 19: 63-73.
37. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
38. Kennedy R, Lladser ME, Yarus M, Knight R. 2008. Information, probability, and the abundance of the simplest RNA active sites. Front Biosci 13: 6060-6071.
39. Laederach A, Shcherbakova I, Jonikas MA, Altman RB, Brenowitz M. 2007. Distinct contribution of electrostatics, initial conformational ensemble, and macromolecular stability in RNA folding. Proc Natl Acad Sci 104: 7045-7050.
40. Lai D, Proctor JR, Zhu JY, Meyer IM. 2012. R-CHIE: a web server and R package for visualizing RNA secondary structures. Nucleic Acids Res 40: e95.
41. Landry JJ, Pyl PT, Rausch T, Zichner T, Tekkedil MM, Stütz AM, Jauch A, Aiyar RS, Pau G, Delhomme N, et al. 2013. The genomic and transcriptomic landscape of a HeLa cell line. G3 (Bethesda) 3: 1213-1224.
42. Lee KM, Tarn WY. 2013. Coupling pre-mRNA processing to transcription on the RNA factory assembly line. RNA Biol 10: 380-390.
43. Lee WH, Bookstein R, Hong F, Young LJ, Shew JY, Lee EY. 1987. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 235: 1394-1399.
44. Lokody I. 2014. RNA: RiboSNitches reveal heredity in RNA secondary structure. Nat Rev Genet 15: 219.
45. Macias M, Dean M, Atkinson A, Jiménez-Morales S, Garcia-Vazquez FJ, Saldaña-Alvarez Y, Ramirez-Bello J, Chávez M, Orozco L. 2008. Spectrum of RB1 gene mutations and loss of heterozygosity in Mexican patients with retinoblastoma: identification of six novel mutations. Cancer Biomark 4: 93-99.
46. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577-586.
47. Mantegna RN, Buldyrev SV, Goldberger AL, Havlin S, Peng CK, Simons M, Stanley HE. 1994. Linguistic features of noncoding DNA sequences. Phys Rev Lett 73: 3169-3172.
48. Marees T, Moll AC, Imhof SM, de Boer MR, Ringens PJ, van Leeuwen FE. 2008. Risk of second malignancies in survivors of retinoblastoma: more than 40 years of follow-up. J Natl Cancer Inst 100: 1771-1779.
49. Martin JS, Halvorsen M, Davis-Neulander L, Ritz J, Gopinath C, Beauregard A, Laederach A. 2012. Structural effects of linkage disequilibrium on the transcriptome. RNA 18: 77-87.
50. Mathews DH. 2004. Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization. RNA 10: 1178-1190.
51. McCaskill JS. 1990. The equilibrium partition function and base pair binding probabilities for RNA secondary structure. Biopolymers 29: 1105-1119.
52. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R. 2013. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41: W597-W600.
53. Mertz JA, Chadee AB, Byun H, Russell R, Dudley JP. 2009. Mapping of the functional boundaries and secondary structure of the mouse mammary tumor virus Rem-responsive element. J Biol Chem 284: 25642-25652.
54. Michel F, Westhof E. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216: 585-610.
55. Mitra S, Shcherbakova IV, Altman RB, Brenowitz M, Laederach A. 2008. High-throughput single-nucleotide structural mapping by capillary automated footprinting analysis. Nucleic Acids Res 36: e63.
56. Murray JI, Whitfield ML, Trinklein ND, Myers RM, Brown PO, Botstein D. 2004. Diverse and specific gene expression responses to stresses in cultured human cells. Mol Biol Cell 15: 2361-2374.
57. Naruse TK, Kawata H, Inoko H, Isshiki G, Yamano K, Hino M, Tatsumi N. 2002. The HLA-DOB gene displays limited polymorphism with only one amino acid substitution. Tissue Antigens 59: 512-519.
58. Nawrocki EP, Kolbe DL, Eddy SR. 2009. Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335-1337.
59. Ritz J, Martin JS, Laederach A. 2012. Evaluating our ability to predict the structural disruption of RNA by SNPs. BMC Genomics 13: S6.
60. Ritz J, Martin JS, Laederach A. 2013. Evolutionary evidence for alternative structure in RNA sequence co-variation. PLoS Comput Biol 9: e1003152.
61. Rogers E, Heitsch CE. 2014. Profiling small RNA reveals multimodal substructural signals in a Boltzmann ensemble. Nucleic Acids Res 42: e171.
62. Rogler LE, Kosmyna B, Moskowitz D, Bebawee R, Rahimzadeh J, Kutchko K, Laederach A, Notarangelo LD, Giliani S, Bouhassira E, et al. 2014. Small RNAs derived from lncRNA RNase MRP have gene-silencing activity relevant to human cartilage-hair hypoplasia. Hum Mol Genet 23: 368-382.
63. Russell R, Zhuang X, Babcock HP, Millett IS, Doniach S, Chu S, Herschlag D. 2002. Exploring the folding landscape of a structured RNA. Proc Natl Acad Sci 99: 155-160.
64. Russell R, Jarmoskaite I, Lambowitz AM. 2012. Toward a molecular understanding of RNA remodeling by DEAD-box proteins. RNA Biol 10: 44-55.
65. Sanchez M, Galy B, Dandekar T, Bengert P, Vainshtein Y, Stolte J, Muckenthaler MU, Hentze MW. 2006. Iron regulation and the cell cycle: identification of an iron-responsive element in the 3'-untranslated region of human cell division cycle 14A mRNA by a refined microarray-based screening strategy. J Biol Chem 281: 22865-22874.
66. Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, et al. 2009. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37: D5-D15.
67. Schroeder R, Barta A, Semrad K. 2004. Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 5: 908-919.
68. Siegfried NA, Busan S, Rice GM, Nelson JA, Weeks KM. 2014. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat Methods 11: 959-965.
69. Solomatin SV, Greenfeld M, Chu S, Herschlag D. 2010. Multiple native states reveal persistent ruggedness of an RNA folding landscape. Nature 463: 681-684.
70. Stenson PD, Ball EV, Mort M, Phillips AD, Shiel JA, Thomas NS, Abeysinghe S, Krawczak M, Cooper DN. 2003. Human Gene Mutation Database (HGMD): 2003 update. Hum Mutat 21: 577-581.
71. Stevens SG, Gardner PP, Brown C. 2011. Two covariance models for iron-responsive elements. RNA Biol 8: 792-801.
72. Stoddard CD, Gilbert SD, Batey RT. 2008. Ligand-dependent folding of the three-way junction in the purine riboswitch. RNA 14: 675-684.
73. Stoddard CD, Montange RK, Hennelly SP, Rambo RP, Sanbonmatsu KY, Batey RT. 2010. Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure 18: 787-797.
74. Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. 2010. Non-coding RNAs: regulators of disease. J Pathol 220: 126-139.
75. Thirumalai D, Woodson SA. 2000. Maximizing RNA folding rates: a balancing act. RNA 6: 790-794.
76. Tucker BJ, Breaker RR. 2005. Riboswitches as versatile gene control elements. Curr Opin Struct Biol 15: 342-348.
77. Ulitsky I, Bartel DP. 2013. lincRNAs: genomics, evolution, and mechanisms. Cell 154: 26-46.
78. Valverde JR, Alonso J, Palacios I, Pestana A. 2005. RB1 gene mutation up-date, a meta-analysis based on 932 reported mutations available in a searchable database. BMC Genet 6: 53.
79. Wan Y, Qu K, Zhang QC, Flynn RA, Manor O, Ouyang Z, Zhang J, Spitale RC, Snyder MP, Segal E, et al. 2014. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 505: 706-709.
80. Weinberg Z, Breaker RR. 2011. R2R - software to speed the depiction of aesthetic consensus RNA secondary structures. BMC Bioinformatics 12: 3.
81. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, et al. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35: 4809-4819.
82. Weinberg Z, Perreault J, Meyer MM, Breaker RR. 2009. Exceptional structured noncoding RNAs revealed by bacterial metagenome analysis. Nature 462: 656-659.
83. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR. 2011. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11: R31.
84. Widmann J, Stombaugh J, McDonald D, Chocholousova J, Gardner P, Iyer MK, Liu Z, Lozupone CA, Quinn J, Smit S, et al. 2012. RNASTAR: an RNA STructural Alignment Repository that provides insight into the evolution of natural and artificial RNAs. RNA 18: 1319-1327.
85. Asp transcripts. J Am Chem Soc 127: 4659-4667.
86. Wilkinson KA, Merino EJ, Weeks KM. 2006. Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc 1: 1610-1616.
87. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6: e96.
88. Wilkinson KA, Vasa SM, Deigan KE, Mortimer SA, Giddings MC, Weeks KM. 2009. Influence of nucleotide identity on ribose 2'-hydroxyl reactivity in RNA. RNA 15: 1314-1321.
89. Woodson SA. 2002. Folding mechanisms of group I ribozymes: role of stability and contact order. Biochem Soc Trans 30: 1166-1169.
90. Zarrinkar PP, Williamson JR. 1994. Kinetic intermediates in RNA folding. Science 265: 918-924.
91. Zimin AV, Delcher AL, Florea L, Kelley DR, Schatz MC, Puiu D, Hanrahan F, Pertea G, Van Tassell CP, Sonstegard TS, et al. 2009. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol 10: R42.
92. Zimin AV, Kelley DR, Roberts M, Marcais G, Salzberg SL, Yorke JA. 2012. Mis-assembled "segmental duplications" in two versions of the Bos taurus genome. PLoS One 7: e42680.
93. Zuker M, Sankoff D. 1984. RNA secondary structures and their prediction. Bull Math Bio 46: 591-621.