Small Molecule Recognition and Tools to Study Modulation of r(CGG)exp in Fragile X-Associated Tremor Ataxia Syndrome

ACS Chemical Biology

Volumn 11, Issue 9, 2016, Pages 2456-2465

  Yang, Wang Yong ^a   He, Fang ^b,d   Strack, Rita L ^c   Oh, Seok Yoon ^b   Frazer, Michelle ^b   Jaffrey, Samie R ^c   Todd, Peter K ^b   Disney, Matthew D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d TEXAS A AND M UNIVERSITY KINGSVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSFER RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; ATAXIA; BINDING AFFINITY; CAG REPEAT; DISEASE ASSOCIATION; FEMALE; FRAGILE X SYNDROME; GAIN OF FUNCTION MUTATION; HUMAN; HUMAN CELL; NEUROMODULATION; OPEN READING FRAME; PRIORITY JOURNAL; RIBOSOME; RNA BINDING; RNA METABOLISM; RNA SPLICING; RNA TRANSCRIPTION; RNA TRANSLATION; THERMODYNAMICS; THERMOSTABILITY; TREMOR ATAXIA SYNDROME; ANIMAL; GENETICS; HELA CELL LINE; TREMOR; TRINUCLEOTIDE REPEAT;

ANIMALS; ATAXIA; FRAGILE X SYNDROME; HELA CELLS; HUMANS; RNA SPLICING; RNA, MESSENGER; TREMOR; TRINUCLEOTIDE REPEATS;

EID: 84987896886     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00147     Document Type: Article

References (31)

1. Atkins, J. F., Gesteland, R. F., and Cech, T. R. (2011) RNA Worlds: From Life's Orignis to Diversity in Gene Regulation, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
2. Cooper, T. A., Wan, L., and Dreyfuss, G. (2009) RNA and disease Cell 136, 777-793 10.1016/j.cell.2009.02.011
3. Orr, H. T. and Zoghbi, H. Y. (2007) Trinucleotide repeat disorders Annu. Rev. Neurosci. 30, 575-621 10.1146/annurev.neuro.29.051605.113042
4. Pushechnikov, A., Lee, M. M., Childs-Disney, J. L., Sobczak, K., French, J. M., Thornton, C. A., and Disney, M. D. (2009) Rational design of ligands targeting triplet repeating transcripts that cause RNA dominant disease: application to myotonic muscular dystrophy type 1 and spinocerebellar ataxia type 3 J. Am. Chem. Soc. 131, 9767-9779 10.1021/ja9020149
5. Coffey, S. M., Cook, K., Tartaglia, N., Tassone, F., Nguyen, D. V., Pan, R., Bronsky, H. E., Yuhas, J., Borodyanskaya, M., Grigsby, J., Doerflinger, M., Hagerman, P. J., and Hagerman, R. J. (2008) Expanded clinical phenotype of women with the FMR1 premutation Am. J. Med. Genet., Part A 146A, 1009-1016 10.1002/ajmg.a.32060
6. Rodriguez-Revenga, L., Madrigal, I., Pagonabarraga, J., Xuncla, M., Badenas, C., Kulisevsky, J., Gomez, B., and Mila, M. (2009) Penetrance of FMR1 premutation associated pathologies in fragile X syndrome families. Eur Eur. J. Hum. Genet. 17, 1359-1362 10.1038/ejhg.2009.51
7. Amiri, K., Hagerman, R. J., and Hagerman, P. J. (2008) Fragile X associated tremor/ataxia syndrome: an aging face of the fragile X gene Arch. Neurol. 65, 19-25 10.1001/archneurol.2007.30
8. Berry-Kravis, E., Abrams, L., Coffey, S. M., Hall, D. A., Greco, C., Gane, L. W., Grigsby, J., Bourgeois, J. A., Finucane, B., Jacquemont, S., Brunberg, J. A., Zhang, L., Lin, J., Tassone, F., Hagerman, P. J., Hagerman, R. J., and Leehey, M. A. (2007) Fragile X-associated tremor/ataxia syndrome: Clinical features, genetics, and testing guidelines Mov. Disord. 22, 2018-2030 10.1002/mds.21493
9. Jacquemont, S., Hagerman, R. J., Hagerman, P. J., and Leehey, M. A. (2007) Fragile-X syndrome and fragile X-associated tremor/ataxia syndrome: two faces of FMR1 Lancet Neurol. 6, 45-55 10.1016/S1474-4422(06)70676-7
10. Sellier, C., Rau, F., Liu, Y., Tassone, F., Hukema, R. K., Gattoni, R., Schneider, A., Richard, S., Willemsen, R., Elliott, D. J., Hagerman, P. J., and Charlet-Berguerand, N. (2010) Sam68 sequestration and partial loss of function are associated with splicing alterations in FXTAS patients EMBO J. 29, 1248-1261 10.1038/emboj.2010.21
11. Willemsen, R., Hoogeveen-Westerveld, M., Reis, S., Holstege, J., Severijnen, L. A., Nieuwenhuizen, I. M., Schrier, M., van Unen, L., Tassone, F., Hoogeveen, A. T., Hagerman, P. J., Mientjes, E. J., and Oostra, B. A. (2003) The FMR1 CGG repeat mouse displays ubiquitin-positive intranuclear neuronal inclusions; implications for the cerebellar tremor/ataxia syndrome Hum. Mol. Genet. 12, 949-959 10.1093/hmg/ddg114
12. Jin, P., Zarnescu, D. C., Zhang, F., Pearson, C. E., Lucchesi, J. C., Moses, K., and Warren, S. T. (2003) RNA-mediated neurodegeneration caused by the fragile X premutation rCGG repeats in Drosophila Neuron 39, 739-747 10.1016/S0896-6273(03)00533-6
13. Tassone, F., Hagerman, R. J., Garcia-Arocena, D., Khandjian, E. W., Greco, C. M., and Hagerman, P. J. (2004) Intranuclear inclusions in neural cells with premutation alleles in fragile X associated tremor/ataxia syndrome J. Med. Genet. 41, e43 10.1136/jmg.2003.012518
14. Greco, C. M., Berman, R. F., Martin, R. M., Tassone, F., Schwartz, P. H., Chang, A., Trapp, B. D., Iwahashi, C., Brunberg, J., Grigsby, J., Hessl, D., Becker, E. J., Papazian, J., Leehey, M. A., Hagerman, R. J., and Hagerman, P. J. (2006) Neuropathology of fragile X-associated tremor/ataxia syndrome (FXTAS) Brain 129, 243-255
15. Sellier, C., Freyermuth, F., Tabet, R., Tran, T., He, F., Ruffenach, F., Alunni, V., Moine, H., Thibault, C., Page, A., Tassone, F., Willemsen, R., Disney, M. D., Hagerman, P. J., Todd, P. K., and Charlet-Berguerand, N. (2013) Sequestration of DROSHA and DGCR8 by expanded CGG RNA repeats alters microRNA processing in fragile X-associated tremor/ataxia syndrome Cell Rep. 3, 869-880 10.1016/j.celrep.2013.02.004
16. Chawla, G., Lin, C. H., Han, A., Shiue, L., Ares, M., Jr., and Black, D. L. (2009) Sam68 regulates a set of alternatively spliced exons during neurogenesis Mol. Cell. Biol. 29, 201-213 10.1128/MCB.01349-08
17. Todd, P. K., Oh, S. Y., Krans, A., He, F., Sellier, C., Frazer, M., Renoux, A. J., Chen, K. C., Scaglione, K. M., Basrur, V., Elenitoba-Johnson, K., Vonsattel, J. P., Louis, E. D., Sutton, M. A., Taylor, J. P., Mills, R. E., Charlet-Berguerand, N., and Paulson, H. L. (2013) CGG repeat-associated translation mediates neurodegeneration in fragile X tremor ataxia syndrome Neuron 78, 440-455 10.1016/j.neuron.2013.03.026
18. Zu, T., Gibbens, B., Doty, N. S., Gomes-Pereira, M., Huguet, A., Stone, M. D., Margolis, J., Peterson, M., Markowski, T. W., Ingram, M. A. C., Nan, Z., Forster, C., Low, W. C., Schoser, B., Somia, N. V., Clark, H. B., Schmechel, S., Bitterman, P. B., Gourdon, G., Swanson, M. S., Moseley, M., and Ranum, L. P. W. (2011) Non-ATG-initiated translation directed by microsatellite expansions Proc. Natl. Acad. Sci. U. S. A. 108, 260-265 10.1073/pnas.1013343108
19. Pearson, C. E. (2011) Repeat associated non-ATG translation initiation: one DNA, two transcripts, seven reading frames, potentially nine toxic entities! PLoS Genet. 7, e1002018 10.1371/journal.pgen.1002018
20. exp and improves defects in fragile X-associated tremor ataxia syndrome ACS Chem. Biol. 7, 1711-1718 10.1021/cb300135h
21. Yang, W.-Y., Wilson, H. D., Velagapudi, S. P., and Disney, M. D. (2015) Inhibition of non-ATG translational events in cells via covalent small molecules targeting RNA J. Am. Chem. Soc. 137, 5336-5345 10.1021/ja507448y
22. Chaires, J. B., Ragazzon, P. A., and Garbett, N. C. (2003) A competition dialysis assay for the study of structure-selective ligand binding to nucleic acids. Curr. Protoc. Nucleic Acid Chem, Chapter 8, Unit 8 3, John Wiley & Sons, Inc., Hoboken, NJ.
23. 2 by two-dimensional NMR and simulated annealing Biochemistry 35, 14077-14089 10.1021/bi9615710
24. Nagaraj, N., Wisniewski, J. R., Geiger, T., Cox, J., Kircher, M., Kelso, J., Pääbo, S., and Mann, M. (2011) Deep proteome and transcriptome mapping of a human cancer cell line Mol. Syst. Biol. 7, 548 10.1038/msb.2011.81
25. Lefever, S., Vandesompele, J., Speleman, F., and Pattyn, F. (2009) RTPrimerDB: the portal for real-time PCR primers and probes Nucleic Acids Res. 37, D942-D945 10.1093/nar/gkn777
26. Strack, R. L., Disney, M. D., and Jaffrey, S. R. (2013) A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA Nat. Methods 10, 1219-1224 10.1038/nmeth.2701
27. Lee, M. M., Childs-Disney, J. L., Pushechnikov, A., French, J. M., Sobczak, K., Thornton, C. A., and Disney, M. D. (2009) Controlling the specificity of modularly assembled small molecules for RNA via ligand module spacing: targeting the RNAs that cause myotonic muscular dystrophy J. Am. Chem. Soc. 131, 17464-17472 10.1021/ja906877y
28. Rzuczek, S. G., Gao, Y., Tang, Z.-Z., Thornton, C. A., Kodadek, T., and Disney, M. D. (2013) Features of modularly assembled compounds that impart bioactivity against an RNA target ACS Chem. Biol. 8, 2312-2321 10.1021/cb400265y
29. Tran, T., Childs-Disney, J. L., Liu, B., Guan, L., Rzuczek, S., and Disney, M. D. (2014) Targeting the r(CGG) repeats that cause FXTAS with modularly assembled small molecules and oligonucleotides ACS Chem. Biol. 9, 904-912 10.1021/cb400875u
30. Guan, L. and Disney, M. D. (2013) Covalent small molecule-RNA complex formation enables cellular profiling of small molecule-RNA interactions Angew. Chem., Int. Ed. 52, 10010-10013 10.1002/anie.201301639
31. Chen, L.-S., Tassone, F., Sahota, P., and Hagerman, P. J. (2003) The (CGG)n repeat element within the 5′ untranslated region of the FMR1 message provides both positive and negative cis effects on in vivo translation of a downstream reporter Hum. Mol. Genet. 12, 3067-3074 10.1093/hmg/ddg331