The quadruplex r(CGG)n destabilizing cationic porphyrin TMPyP4 cooperates with hnRNPs to increase the translation efficiency of fragile X premutation mRNA

Nucleic Acids Research

Volumn 37, Issue 8, 2009, Pages 2712-2722

  Ofer, Noa ^a   Weisman Shomer, Pnina ^a   Shklover, Jeny ^a   Fry, Michael ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

5,10,15,20 TETRA(N METHYL 4 PYRIDYL)PORPHYRIN; FRAGILE X MENTAL RETARDATION PROTEIN; GUANINE QUADRUPLEX; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; LUCIFERIN; MESSENGER RNA; PORPHYRIN DERIVATIVE; TRANSCRIPTION FACTOR RUNX; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; FRAGILE X SYNDROME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REPORTER GENE; RNA STABILITY; RNA TRANSCRIPTION; RNA TRANSLATION; TRINUCLEOTIDE REPEAT;

5' UNTRANSLATED REGIONS; CCAAT-BINDING FACTOR; CELL LINE; FRAGILE X MENTAL RETARDATION PROTEIN; G-QUADRUPLEXES; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; PORPHYRINS; PROTEIN BIOSYNTHESIS; TRINUCLEOTIDE REPEAT EXPANSION;

ORYCTOLAGUS CUNICULUS;

EID: 65849117023     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp130     Document Type: Article

References (35)

1. Penagarikano,O., Mulle,J.G. and Warren,S.T. (2007) The pathophysiology of fragile X syndrome. Annu. Rev. Genomics Hum. Genet., 8, 109-129.
2. Garber,K.B., Visootsak,J. and Warren,S.T. (2008) Fragile X syndrome. Eur. J. Hum. Genet., 16, 666-672.
3. Pieretti,M., Zhang,F.P., Fu,Y.H., Warren,S.T., Oostra,B.A., Caskey,C.T. and Nelson,D.L. (1991) Absence of expression of the FMR-1 gene in fragile X syndrome. Cell, 66, 817-822.
4. Coffey,S.M., Cook,K., Tartaglia,N., Tassone,F., Nguyen,D.V., Pan,R., Bronsky,H.E., Yuhas,J., Borodyanskaya,M., Grigsby,J. et al. (2008) Expanded clinical phenotype of women with the FMR1 premutation. Am. J. Med. Genet. A, 146A, 1009-1016.
5. Hagerman,P.J. and Hagerman,R.J. (2004) The fragile-X premutation: A maturing perspective. Am. J. Hum. Genet., 74, 805-816.
6. Allingham-Hawkins,D.J., Babul-Hirji,R., Chitayat,D., Holden,J.J., Yang,K.T., Lee,C., Hudson,R., Gorwill,H., Nolin,S.L., Glicksman,A. et al. (1999) Fragile X premutation is a significant risk factor for premature ovarian failure: The International Collaborative POF in Fragile X study-preliminary data. Am. J. Med. Genet., 83, 322-325.
7. Hagerman,R.J., Leehey,M., Heinrichs,W., Tassone,F., Wilson,R., Hills,J., Grigsby,J., Gage,B. and Hagerman,P.J. (2001) Intention tremor, parkinsonism, and generalized brain atrophy in male carriers of fragile X. Neurology, 57, 127-130.
8. Berry-Kravis,E., Lewin,F., Wuu,J., Leehey,M., Hagerman,R., Hagerman,P. and Goetz,C.G. (2003) Tremor and ataxia in fragile X premutation carriers: Blinded videotape study. Ann. Neurol., 53, 616-623.
9. 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. Tassone,F., Hagerman,R.J., Taylor,A.K., Gane,L.W., Godfrey,T.E. and Hagerman,P.J. (2000) Elevated levels of FMR1 mRNA in carrier males: A new mechanism of involvement in the fragile-X syndrome. Am. J. Hum. Genet., 66, 6-15.
11. Kenneson,A., Zhang,F., Hagedorn,C.H. and Warren,S.T. (2001) Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers. Hum. Mol. Genet., 10, 1449-1454.
12. Tassone,F., Beilina,A., Carosi,C., Albertosi,S., Bagni,C., Li,L., Glover,K., Bentley,D. and Hagerman,P.J. (2007) Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA, 13 555-562.
13. Brouwer,J.R., Mientjes,E.J., Bakker,C.E., Nieuwenhuizen,I.M., Severijnen,L.A., Van der Linde,H.C., Nelson,D.L., Oostra,B.A. and Willemsen,R. (2007) Elevated Fmr1 mRNA levels and reduced protein expression in a mouse model with an unmethylated Fragile X full mutation. Exp. Cell Res., 313, 244-253.
14. Primerano,B., Tassone,F., Hagerman,R.J., Hagerman,P., Amaldi,F. and Bagni,C. (2002) Reduced FMR1 mRNA translation efficiency in fragile X patients with premutations. RNA, 8, 1482-1488.
15. Feng,Y., Zhang,F., Lokey,L.K., Chastain,J.L., Lakkis,L., Eberhart,D. and Warren,S.T. (1995) Translational suppression by trinucleotide repeat expansion at FMR1. Science, 268, 731-734.
16. Handa,V., Saha,T. and Usdin,K. (2003) The fragile X syndrome repeats form RNA hairpins that do not activate the interferon-inducible protein kinase, PKR, but are cut by Dicer. Nucleic Acids Res., 31, 6243-6248.
17. Zumwalt,M., Ludwig,A., Hagerman,P.J. and Dieckmann,T. (2007) Secondary structure and dynamics of the r(CGG) repeat in the mRNA of the fragile X mental retardation 1 (FMR1) gene. RNA Biol., 4, 93-100.
18. Khateb,S., Weisman-Shomer,P., Hershco,I., Loeb,L.A. and Fry,M. (2004) Destabilization of tetraplex structures of the fragile X repeat sequence (CGG)n is mediated by homolog-conserved domains in three members of the hnRNP family. Nucleic Acids Res., 32, 4145-4154.
19. Khateb,S., Weisman-Shomer,P., Hershco-Shani,I., Ludwig,A.L. and Fry,M. (2007) The tetraplex (CGG)n destabilizing proteins hnRNP A2 and CBF-A enhance the in vivo translation of fragile X premutation mRNA. Nucleic Acids Res., 35, 5775-5788.
20. Kumari,S., Bugaut,A., Huppert,J.L. and Balasubramanian,S. (2007) An RNA G-quadruplex in the 50 UTR of the NRAS protooncogene modulates translation. Nat. Chem. Biol., 3, 218-221.
21. Arora,A., Dutkiewicz,M., Scaria,V., Hariharan,M., Maiti,S. and Kurreck,J. (2008) Inhibition of translation in living eukaryotic cells by an RNA G-quadruplex motif. RNA, 14, 1290-1296.
22. Wieland,M. and Hartig,J.S. (2007) RNA quadruplex-based modulation of gene expression. Chem. Biol., 14, 757-763.
23. Han,H., Langley,D.R., Rangan,A. and Hurley,L.H. (2001) Selective interactions of cationic porphyrins with G-quadruplex structures. J. Am. Chem. Soc., 123, 8902-8913.
24. Grand,C.L., Han,H., Munoz,R.M., Weitman,S., Von Hoff,D.D., Hurley,L.H. and Bearss,D.J. (2002) The cationic porphyrin TMPyP4 down-regulates c-MYC and human telomerase reverse transcriptase expression and inhibits tumor growth in vivo. Mol. Cancer Ther., 1, 565-573.
25. n. Nucleic Acids Res., 31, 3963-3970.
26. Keniry,M.A. (2000) Quadruplex structures in nucleic acids. Biopolymers, 56, 123-146.
27. Bardin,C. and Leroy,J.L. (2008) The formation pathway of tetramolecular G-quadruplexes. Nucleic Acids Res., 36, 477-488.
28. n are destabilized by two heterogeneous nuclear ribonucleoprotein-related telomeric DNA-binding proteins. J. Biol. Chem., 275, 2231-2238.
29. n. Nucleic Acids Res., 30, 3672-3681.
30. Han,F.X., Wheelhouse,T.T. and Hurley,L.H. (1999) Interaction of TMPyP4 and TMPyP2 with quadruplex DNA. Structural basis for the differential effects on telomerase inhibition. J. Am. Chem. Soc., 121, 3561-3570.
31. Brown,W.T., Houck,G.E. Jr., Jeziorowska,A., Levinson,F.N., Ding,X., Dobkin,C., Zhong,N., Henderson,J., Brooks,S.S. and Jenkins,E.C. (1993) Rapid fragile X carrier screening and prenatal diagnosis using a nonradioactive PCR test. J. Am. Med. Assoc., 270, 1569-1575.
32. Hagerman,R.J. and Hagerman,P.J. (2002) The fragile X premutation: Into the phenotypic fold. Curr. Opin. Genet. Dev., 12, 278-283.
33. 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.
34. Jin,P., Duan,R., Qurashi,A., Qin,Y., Tian,D., Rosser,T.C., Liu,H., Feng,Y. and Warren,S.T. (2007) Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome. Neuron, 55, 556-564.
35. Sofola,O.A., Jin,P., Qin,Y., Duan,R., Liu,H., de Haro,M., Nelson,D.L. and Botas,J. (2007) RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron, 55, 565-571.