Genetic variations regulate alternative splicing in the 5' untranslated regions of the mouse glioma-associated oncogene 1, Gli1

BMC Molecular Biology

Volumn 11, Issue , 2010, Pages

  Palaniswamy, Ramesh ^a   Teglund, Stephan ^a   Lauth, Matthias ^a   Zaphiropoulos, Peter G ^a   Shimokawa, Takashi ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; MESSENGER RNA; TRANSCRIPTION FACTOR GLI1; GLI PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; SONIC HEDGEHOG PROTEIN;

5' UNTRANSLATED REGION; ALLELE; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXON; EXON SKIPPING; GENE EXPRESSION PROFILING; GENETIC REGULATION; GENETIC VARIABILITY; GENOTYPE; GLIOMA; INTRON; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; TRANSCRIPTION INITIATION SITE; ANIMAL; C57BL MOUSE; CEREBELLUM; CEREBELLUM TUMOR; CYTOLOGY; GENETIC POLYMORPHISM; GENETICS; MEDULLOBLASTOMA; METABOLISM; MOLECULAR GENETICS; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; UPREGULATION;

ERINACEIDAE;

5' UNTRANSLATED REGIONS; ALLELES; ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CEREBELLAR NEOPLASMS; CEREBELLUM; EMBRYONIC DEVELOPMENT; EXONS; GENOTYPE; HEDGEHOG PROTEINS; INTRONS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MEDULLOBLASTOMA; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; UP-REGULATION;

EID: 77951578530     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-11-32     Document Type: Article

References (42)

1. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40(12):1413-1415. 10.1038/ng.259, 18978789.
2. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456(7221):470-476. 10.1038/nature07509, 2593745, 18978772.
3. Davuluri RV, Suzuki Y, Sugano S, Plass C, Huang TH. The functional consequences of alternative promoter use in mammalian genomes. Trends Genet 2008, 24(4):167-177. 10.1016/j.tig.2008.01.008, 18329129.
4. Nagasaki H, Arita M, Nishizawa T, Suwa M, Gotoh O. Species-specific variation of alternative splicing and transcriptional initiation in six eukaryotes. Gene 2005, 364:53-62. 10.1016/j.gene.2005.07.027, 16219431.
5. Kwan T, Benovoy D, Dias C, Gurd S, Provencher C, Beaulieu P, Hudson TJ, Sladek R, Majewski J. Genome-wide analysis of transcript isoform variation in humans. Nat Genet 2008, 40(2):225-231. 10.1038/ng.2007.57, 18193047.
6. Hughes TA. Regulation of gene expression by alternative untranslated regions. Trends Genet 2006, 22(3):119-122. 10.1016/j.tig.2006.01.001, 16430990.
7. Pickering BM, Willis AE. The implications of structured 5' untranslated regions on translation and disease. Semin Cell Dev Biol 2005, 16(1):39-47. 10.1016/j.semcdb.2004.11.006, 15659338.
8. Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev Cell 2008, 15(6):801-812. 10.1016/j.devcel.2008.11.010, 19081070.
9. Hahn H, Wicking C, Zaphiropoulos PG, Gailani MR, Shanley S, Chidambaram A, Vorechovsky I, Holmberg E, Unden AB, Gillies S, et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996, 85(6):841-851. 10.1016/S0092-8674(00)81268-4, 8681379.
10. Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003, 425(6960):846-851. 10.1038/nature01972, 14520411.
11. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruiz i Altaba A. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci USA 2004, 101(34):12561-12566. 10.1073/pnas.0404956101, 514658, 15314219.
12. Yuan Z, Goetz JA, Singh S, Ogden SK, Petty WJ, Black CC, Memoli VA, Dmitrovsky E, Robbins DJ. Frequent requirement of hedgehog signaling in non-small cell lung carcinoma. Oncogene 2007, 26(7):1046-1055. 10.1038/sj.onc.1209860, 16909105.
13. Zaphiropoulos PG, Shimokawa T. Splicing variations in components of Patched/Hedgehog signaling. Trends Cell Mol Biol 2008, 3:31-35.
14. Nybakken K, Vokes SA, Lin TY, McMahon AP, Perrimon N. A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nat Genet 2005, 37(12):1323-1332. 10.1038/ng1682, 16311596.
15. Kinzler KW, Ruppert JM, Bigner SH, Vogelstein B. The GLI gene is a member of the Kruppel family of zinc finger proteins. Nature 1988, 332(6162):371-374. 10.1038/332371a0, 2832761.
16. Ruiz i Altaba A. The works of GLI and the power of hedgehog. Nat Cell Biol 1999, 1(6):E147-148. 10.1038/14099, 10559974.
17. Nilsson M, Unden AB, Krause D, Malmqwist U, Raza K, Zaphiropoulos PG, Toftgård R. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc Natl Acad Sci USA 2000, 97(7):3438-3443. 10.1073/pnas.050467397, 16258, 10725363.
18. Wang XQ, Rothnagel JA. Post-transcriptional regulation of the gli1 oncogene by the expression of alternative 5' untranslated regions. J Biol Chem 2001, 276(2):1311-1316. 10.1074/jbc.M005191200, 11032829.
19. Shimokawa T, Tostar U, Lauth M, Palaniswamy R, Kasper M, Toftgård R, Zaphiropoulos PG. Novel human glioma-associated oncogene 1 (GLI1) splice variants reveal distinct mechanisms in the terminal transduction of the hedgehog signal. J Biol Chem 2008, 283(21):14345-14354. 10.1074/jbc.M800299200, 2386930, 18378682.
20. Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F. A Novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res 2009, 69(17):6790-6798. 10.1158/0008-5472.CAN-09-0886, 19706761.
21. Chen JK, Taipale J, Young KE, Maiti T, Beachy PA. Small molecule modulation of Smoothened activity. Proc Natl Acad Sci USA 2002, 99(22):14071-14076. 10.1073/pnas.182542899, 137838, 12391318.
22. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997, 277(5329):1109-1113. 10.1126/science.277.5329.1109, 9262482.
23. Kimura H, Stephen D, Joyner A, Curran T. Gli1 is important for medulloblastoma formation in Ptc1+/- mice. Oncogene 2005, 24(25):4026-4036.
24. Sterner DA, Carlo T, Berget SM. Architectural limits on split genes. Proc Natl Acad Sci USA 1996, 93(26):15081-15085. 10.1073/pnas.93.26.15081, 26359, 8986767.
25. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 2009, 37(9):e67. 10.1093/nar/gkp215, 2685110, 19339519.
26. Reese MG, Eeckman FH, Kulp D, Haussler D. Improved splice site detection in Genie. J Comput Biol 1997, 4(3):311-323. 10.1089/cmb.1997.4.311, 9278062.
27. Nakamura T, Aikawa T, Iwamoto-Enomoto M, Iwamoto M, Higuchi Y, Pacifici M, Kinto N, Yamaguchi A, Noji S, Kurisu K, et al. Induction of osteogenic differentiation by hedgehog proteins. Biochem Biophys Res Commun 1997, 237(2):465-469. 10.1006/bbrc.1997.7156, 9268735.
28. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009, 136(4):777-793. 10.1016/j.cell.2009.02.011, 19239895, 2866189.
29. Hull J, Campino S, Rowlands K, Chan MS, Copley RR, Taylor MS, Rockett K, Elvidge G, Keating B, Knight J, et al. Identification of common genetic variation that modulates alternative splicing. PLoS Genet 2007, 3(6):e99. 10.1371/journal.pgen.0030099, 1904363,1904363, 17571926.
30. Lindström E, Shimokawa T, Toftgård R, Zaphiropoulos PG. PTCH mutations: distribution and analyses. Hum Mutat 2006, 27(3):215-219. 10.1002/humu.20296, 16419085.
31. Resch AM, Ogurtsov AY, Rogozin IB, Shabalina SA, Koonin EV. Evolution of alternative and constitutive regions of mammalian 5'UTRs. BMC Genomics 2009, 10:162. 10.1186/1471-2164-10-162, 2674463, 19371439.
32. Svärd J, Rozell B, Toftgård R, Teglund S. Tumor suppressor gene cooperativity in compound Patched1 and suppressor of fused heterozygous mutant mice. Mol Carcinog 2009, 48(5):408-419. 10.1002/mc.20479, 2674531, 18781608.
33. Yadav VK, Abraham JK, Mani P, Kulshrestha R, Chowdhury S. QuadBase: genome-wide database of G4 DNA--occurrence and conservation in human, chimpanzee, mouse and rat promoters and 146 microbes. Nucleic Acids Res 2008, (36 Database):D381-385. 2238983, 17962308.
34. Patel DJ, Phan AT, Kuryavyi V. Human telomere, oncogenic promoter and 5'-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res 2007, 35(22):7429-7455. 10.1093/nar/gkm711, 2190718, 17913750.
35. Kumari S, Bugaut A, Huppert JL, Balasubramanian S. An RNA G-quadruplex in the 5' UTR of the NRAS proto-oncogene modulates translation. Nat Chem Biol 2007, 3(4):218-221. 10.1038/nchembio864, 2206252, 17322877.
36. Calvo SE, Pagliarini DJ, Mootha VK. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci USA 2009, 106(18):7507-7512. 10.1073/pnas.0810916106, 2669787, 19372376.
37. Shimokawa T, Rahnama F, Zaphiropoulos PG. A novel first exon of the Patched1 gene is upregulated by Hedgehog signaling resulting in a protein with pathway inhibitory functions. FEBS Lett 2004, 578(1-2):157-162. 10.1016/j.febslet.2004.11.006, 15581634.
38. Shimokawa T, Svärd J, Heby-Henricson K, Teglund S, Toftgård R, Zaphiropoulos PG. Distinct roles of first exon variants of the tumor-suppressor Patched1 in Hedgehog signaling. Oncogene 2007, 26(34):4889-4896. 10.1038/sj.onc.1210301, 17310997.
39. Taipale J, Chen JK, Cooper MK, Wang B, Mann RK, Milenkovic L, Scott MP, Beachy PA. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 2000, 406(6799):1005-1009. 10.1038/35023008, 10984056.
40. Rahnama F, Shimokawa T, Lauth M, Finta C, Kogerman P, Teglund S, Toftgård R, Zaphiropoulos PG. Inhibition of GLI1 gene activation by Patched1. Biochem J 2006, 394(Pt 1):19-26. 1385998, 16229683.
41. Svärd J, Heby-Henricson K, Persson-Lek M, Rozell B, Lauth M, Bergström A, Ericson J, Toftgård R, Teglund S. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev Cell 2006, 10(2):187-197. 10.1016/j.devcel.2005.12.013, 16459298.
42. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356(6366):215-221. 10.1038/356215a0, 1552940.