PSF contacts exon 7 of SMN2 pre-mRNA to promote exon 7 inclusion

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 6, 2014, Pages 517-525

  Cho, Sunghee ^a   Moon, Heegyum ^a   Loh, Tiing Jen ^a   Oh, Hyun Kyung ^a   Williams, Darren Reese ^a   Liao, D Joshua ^b   Zhou, Jianhua ^c   Green, Michael R ^d   Zheng, Xuexiu ^a   Shen, Haihong ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b UNIVERSITY OF MINNESOTA   (United States)

^c NANTONG UNIVERSITY   (China)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Enhancer; Exon 7 splicing; PSF; RNA splicing; Spinal muscular atrophy

Indexed keywords

MESSENGER RNA PRECURSOR; SURVIVAL MOTOR NEURON PROTEIN 2;

ARTICLE; CONTROLLED STUDY; ENHANCER REGION; EXON; EXON 7; EXON SKIPPING; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; SPINAL MUSCULAR ATROPHY;

ENHANCER; EXON 7 SPLICING; PSF; RNA SPLICING; SPINAL MUSCULAR ATROPHY;

BLOTTING, WESTERN; DNA PRIMERS; EXONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUCIFERASES; NEUROBLASTOMA; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PRECURSORS; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SURVIVAL OF MOTOR NEURON 2 PROTEIN; TUMOR CELLS, CULTURED;

EID: 84900476398     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.03.003     Document Type: Article

References (51)

1. Pearn J. Incidence, prevalence, and gene frequency studies of chronic childhood spinal muscular atrophy. J. Med. Genet. 1978, 15:409-413.
2. Sugarman E.A., Nagan N., Zhu H., Akmaev V.R., Zhou Z., Rohlfs E.M., Flynn K., Hendrickson B.C., Scholl T., Sirko-Osadsa D.A., Allitto B.A. Pan-ethnic carrier screening and prenatal diagnosis for spinal muscular atrophy: clinical laboratory analysis of >72,400 specimens. Eur. J. Hum. Genet. 2012, 20:27-32.
3. T.L.Munsat, K.E.Davies, International SMA consortium meeting.(26-28 Bonn, Germany). Neuromuscul. Disord. June 1992, 2(1992):423-428.
4. MacLeod M.J., Taylor J.E., Lunt P.W., Mathew C.G., Robb S.A. Prenatal onset spinal muscular atrophy. Eur. J. Paediatr. Neurol. 1999, 3:65-72.
5. Roberts CL A.C., Mueller L., Hadler J.L. Trends in infant mortality in Connecticut, 1981-1992. J. Public Health Manag. Pract. 1997, 50-57.
6. Crawford T.O., Pardo C.A. The neurobiology of childhood spinal muscular atrophy. Neurobiol. Dis. 1996, 3:97-110.
7. Lefebvre S., Burglen L., Reboullet S., Clermont O., Burlet P., Viollet L., Benichou B., Cruaud C., Millasseau P., Zeviani M., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
8. Monani U.R., Lorson C.L., Parsons D.W., Prior T.W., Androphy E.J., Burghes A.H., McPherson J.D. A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum. Mol. Genet. 1999, 8:1177-1183.
9. Lorson C.L., Hahnen E., Androphy E.J., Wirth B. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:6307-6311.
10. DiDonato C.J., Chen X.N., Noya D., Korenberg J.R., Nadeau J.H., Simard L.R. Cloning, characterization, and copy number of the murine survival motor neuron gene: homolog of the spinal muscular atrophy-determining gene. Genome Res. 1997, 7:339-352.
11. Burnett B.G., Munoz E., Tandon A., Kwon D.Y., Sumner C.J., Fischbeck K.H. Regulation of SMN protein stability. Mol. Cell. Biol. 2009, 29:1107-1115.
12. Glinka M., Herrmann T., Funk N., Havlicek S., Rossoll W., Winkler C., Sendtner M. The heterogeneous nuclear ribonucleoprotein-R is necessary for axonal beta-actin mRNA translocation in spinal motor neurons. Hum. Mol. Genet. 2010, 19:1951-1966.
13. Fallini C., Bassell G.J., Rossoll W. Spinal muscular atrophy: the role of SMN in axonal mRNA regulation. Brain Res. 2012, 1462:81-92.
14. Zhang H., Xing L., Rossoll W., Wichterle H., Singer R.H., Bassell G.J. Multiprotein complexes of the survival of motor neuron protein SMN with Gemins traffic to neuronal processes and growth cones of motor neurons. J. Neurosci. 2006, 26:8622-8632.
15. Le T.T., Coovert D.D., Monani U.R., Morris G.E., Burghes A.H. The survival motor neuron (SMN) protein: effect of exon loss and mutation on protein localization. Neurogenetics 2000, 3:7-16.
16. Paushkin S., Gubitz A.K., Massenet S., Dreyfuss G. The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 2002, 14:305-312.
17. Meister G., Eggert C., Fischer U. SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol. 2002, 12:472-478.
18. Buhler D., Raker V., Luhrmann R., Fischer U. Essential role for the tudor domain of SMN in spliceosomal U snRNP assembly: implications for spinal muscular atrophy. Hum. Mol. Genet. 1999, 8:2351-2357.
19. Carvalho T., Almeida F., Calapez A., Lafarga M., Berciano M.T., Carmo-Fonseca M. The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body. J. Cell Biol. 1999, 147:715-728.
20. Cartegni L., Hastings M.L., Calarco J.A., de Stanchina E., Krainer A.R. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am. J. Hum. Genet. 2006, 78:63-77.
21. Zhou J., Zheng X., Shen H. Targeting RNA-splicing for SMA treatment. Mol. Cells 2012, 33:223-228.
22. Kashima T., Manley J.L. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 2003, 34:460-463.
23. Kashima T., Rao N., David C.J., Manley J.L. hnRNP A1 functions with specificity in repression of SMN2 exon 7 splicing. Hum. Mol. Genet. 2007, 16:3149-3159.
24. Cartegni L., Krainer A.R. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 2002, 30:377-384.
25. Hofmann Y., Lorson C.L., Stamm S., Androphy E.J., Wirth B. Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9618-9623.
26. Young P.J., DiDonato C.J., Hu D., Kothary R., Androphy E.J., Lorson C.L. SRp30c-dependent stimulation of survival motor neuron (SMN) exon 7 inclusion is facilitated by a direct interaction with hTra2 beta 1. Hum. Mol. Genet. 2002, 11:577-587.
27. Hofmann Y., Wirth B. hnRNP-G promotes exon 7 inclusion of survival motor neuron (SMN) via direct interaction with Htra2-beta1. Hum. Mol. Genet. 2002, 11:2037-2049.
28. Chen H.H., Chang J.G., Lu R.M., Peng T.Y., Tarn W.Y. The RNA binding protein hnRNP Q modulates the utilization of exon 7 in the survival motor neuron 2 (SMN2) gene. Mol. Cell. Biol. 2008, 28:6929-6938.
29. Miyaso H., Okumura M., Kondo S., Higashide S., Miyajima H., Imaizumi K. An intronic splicing enhancer element in survival motor neuron (SMN) pre-mRNA. J. Biol. Chem. 2003, 278:15825-15831.
30. Miyajima H., Miyaso H., Okumura M., Kurisu J., Imaizumi K. Identification of a cis-acting element for the regulation of SMN exon 7 splicing. J. Biol. Chem. 2002, 277:23271-23277.
31. Hua Y., Vickers T.A., Baker B.F., Bennett C.F., Krainer A.R. Enhancement of SMN2 exon 7 inclusion by antisense oligonucleotides targeting the exon. PLoS Biol. 2007, 5:e73.
32. Arnold W.D., Burghes A.H. Spinal muscular atrophy: development and implementation of potential treatments. Ann. Neurol. 2013, 74:348-362.
33. Cho S.I., Lee J.E., Do N.Y. Protective effect of silymarin against cisplatin-induced ototoxicity. Int. J. Pediatr. Otorhinolaryngol. 2014, 78:474-478.
34. Shen H., Kan J.L., Ghigna C., Biamonti G., Green M.R. A single polypyrimidine tract binding protein (PTB) binding site mediates splicing inhibition at mouse IgM exons M1 and M2. RNA 2004, 10:787-794.
35. Cho S.H., Kim J., Oh K.H., Hu J.K., Seo J., Oh S.S., Hur M.J., Choi Y.H., Youn S.K., Chung G.T., Choe Y.J. Outbreak of enterotoxigenic Escherichia coli O169 enteritis in schoolchildren associated with consumption of kimchi, Republic of Korea, 2012. Epidemiol. Infect. 2014, 142:616-623.
36. Prior T.W., Krainer A.R., Hua Y., Swoboda K.J., Snyder P.C., Bridgeman S.J., Burghes A.H., Kissel J.T. A positive modifier of spinal muscular atrophy in the SMN2 gene. Am. J. Hum. Genet. 2009, 85:408-413.
37. Miyamoto K., Sakurai H., Sugiura T. Proteomic identification of a PSF/p54nrb heterodimer as RNF43 oncoprotein-interacting proteins. Proteomics 2008, 8:2907-2910.
38. Ray P., Kar A., Fushimi K., Havlioglu N., Chen X., Wu J.Y. PSF suppresses tau exon 10 inclusion by interacting with a stem-loop structure downstream of exon 10. J. Mol. Neurosci. 2011, 45:453-466.
39. Buxade M., Morrice N., Krebs D.L., Proud C.G. The PSF.p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor alpha. J. Biol. Chem. 2008, 283:57-65.
40. Landeras-Bueno S., Jorba N., Perez-Cidoncha M., Ortin J. The splicing factor proline-glutamine rich (SFPQ/PSF) is involved in influenza virus transcription. PLoS Pathog. 2011, 7:e1002397.
41. Sharathchandra A., Lal R., Khan D., Das S. Annexin A2 and PSF proteins interact with p53 IRES and regulate translation of p53 mRNA. RNA Biol. 2012, 9:1429-1439.
42. Dong X., Sweet J., Challis J.R., Brown T., Lye S.J. Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol. Cell. Biol. 2007, 27:4863-4875.
43. Rosonina E., Ip J.Y., Calarco J.A., Bakowski M.A., Emili A., McCracken S., Tucker P., Ingles C.J., Blencowe B.J. Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo. Mol. Cell. Biol. 2005, 25:6734-6746.
44. Tsukahara T., Haniu H., Matsuda Y. PTB-associated splicing factor (PSF) is a PPARgamma-binding protein and growth regulator of colon cancer cells. PLoS One 2013, 8:e58749.
45. Mathur M., Samuels H.H. Role of PSF-TFE3 oncoprotein in the development of papillary renal cell carcinomas. Oncogene 2007, 26:277-283.
46. Wang G., Cui Y., Zhang G., Garen A., Song X. Regulation of proto-oncogene transcription, cell proliferation, and tumorigenesis in mice by PSF protein and a VL30 noncoding RNA. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16794-16798.
47. Cho S., Moon H., Yang X., Zhou J., Kim H.R., Shin M.G., Loh T.J., Zheng X., Shen H. Validation of trans-acting elements that promote exon 7 skipping of SMN2 in SMN2-GFP stable cell line. Biochem. Biophys. Res. Commun. 2012, 423:531-535.
48. Oh H.K., Lee E., Jang H.N., Lee J., Moon H., Sheng Z., Jun Y., Loh T.J., Cho S., Zhou J., Green M.R., Zheng X., Shen H. hnRNP A1 contacts exon 5 to promote exon 6 inclusion of apoptotic Fas gene. Apoptosis 2013, 825-835.
49. Melton A.A., Jackson J., Wang J., Lynch K.W. Combinatorial control of signal-induced exon repression by hnRNP L and PSF. Mol. Cell. Biol. 2007, 27:6972-6984.
50. Mungamuri S.K., Murk W., Grumolato L., Bernstein E., Aaronson S.A. Chromatin modifications sequentially enhance ErbB2 expression in ErbB2-positive breast cancers. Cell Rep. 2013, 5:302-313.
51. Vezain M., Saugier-Veber P., Goina E., Touraine R., Manel V., Toutain A., Fehrenbach S., Frebourg T., Pagani F., Tosi M., Martins A. A rare SMN2 variant in a previously unrecognized composite splicing regulatory element induces exon 7 inclusion and reduces the clinical severity of spinal muscular atrophy. Hum. Mutat. 2009.