Two wobble-splicing events affect ING4 protein subnuclear localization and degradation

Experimental Cell Research

Volumn 314, Issue 17, 2008, Pages 3130-3141

  Tsai, Kuo Wang ^a,b   Tseng, Hsiao Chun ^b,c   Lin, Wen chang ^b,d  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Degradation; GTNGT; ING4; Localization; NAGNAG; NLS; NoLS; Nucleolus; Tandem splice sites; Wobble splicing

Indexed keywords

INHIBITOR OF GROWTH 4; PROTEASOME; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; EXON; FEMALE; HALF LIFE TIME; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UBIQUITINATION;

EID: 54849361700     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.08.002     Document Type: Article

References (35)

1. He G.H., Helbing C.C., Wagner M.J., Sensen C.W., and Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol. Biol. Evol. 22 (2005) 104-116
2. Zhang X., Xu L.S., Wang Z.Q., Wang K.S., Li N., Cheng Z.H., Huang S.Z., Wei D.Z., and Han Z.G. ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett. 570 (2004) 7-12
3. Zhang X., Wang K.S., Wang Z.Q., Xu L.S., Wang Q.W., Chen F., Wei D.Z., and Han Z.G. Nuclear localization signal of ING4 plays a key role in its binding to p53. Biochem. Biophys. Res. Commun. 331 (2005) 1032-1038
4. Shiseki M., Nagashima M., Pedeux R.M., Kitahama-Shiseki M., Miura K., Okamura S., Onogi H., Higashimoto Y., Appella E., Yokota J., and Harris C.C. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res. 63 (2003) 2373-2378
5. Garkavtsev I., Kozin S.V., Chernova O., Xu L., Winkler F., Brown E., Barnett G.H., and Jain R.K. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428 (2004) 328-332
6. Kim S., Chin K., Gray J.W., and Bishop J.M. A screen for genes that suppress loss of contact inhibition: identification of ING4 as a candidate tumor suppressor gene in human cancer. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16251-16256
7. Vieyra D., Senger D.L., Toyama T., Muzik H., Brasher P.M., Johnston R.N., Riabowol K., and Forsyth P.A. Altered subcellular localization and low frequency of mutations of ING1 in human brain tumors. Clin. Cancer Res. 9 (2003) 5952-5961
8. Raho G., Miranda C., Tamborini E., Pierotti M.A., and Greco A. Detection of novel mRNA splice variants of human ING4 tumor suppressor gene. Oncogene 26 (2007) 5247-5257
9. Antoine M., Reimers K., Dickson C., and Kiefer P. Fibroblast growth factor 3, a protein with dual subcellular localization, is targeted to the nucleus and nucleolus by the concerted action of two nuclear localization signals and a nucleolar retention signal. J. Biol. Chem. 272 (1997) 29475-29481
10. Pederson T. Growth factors in the nucleolus?. J. Cell Biol. 143 (1998) 279-281
11. Zhang Y., and Xiong Y. Mutations in human ARF exon 2 disrupt its nucleolar localization and impair its ability to block nuclear export of MDM2 and p53. Mol. Cell 3 (1999) 579-591
12. Weber J.D., Taylor L.J., Roussel M.F., Sherr C.J., and Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1 (1999) 20-26
13. Unoki M., Shen J.C., Zheng Z.M., and Harris C.C. Novel splice variants of ING4 and their possible roles in the regulation of cell growth and motility. J. Biol. Chem. 281 (2006) 34677-34686
14. Tsai K.W., and Lin W.C. Quantitative analysis of wobble splicing indicates that it is not tissue specific. Genomics 88 (2006) 855-864
15. Tsai K.W., Tarn W.Y., and Lin W.C. Wobble splicing reveals the role of the branch point sequence-to-NAGNAG region in 3′ tandem splice site selection. Mol. Cell Biol. 27 (2007) 5835-5848
16. Lai C.H., Hu L.Y., and Lin W.C. Single amino-acid InDel variants generated by alternative tandem splice-donor and -acceptor selection. Biochem. Biophys. Res. Commun. 342 (2006) 197-205
17. Akerman M., and Mandel-Gutfreund Y. Alternative splicing regulation at tandem 3′ splice sites. Nucleic Acids Res. 34 (2006) 23-31
18. Hiller M., Huse K., Szafranskzi K., Rosenstiel P., Schreiber S., Backofen R., and Platzer M. Phylogenetically widespread alternative splicing at unusual GYNGYN donors. Genome Biol. 7 (2006) R65
19. Hiller M., Huse K., Szafranski K., Jahn N., Hampe J., Schreiber S., Backofen R., and Platzer M. Single-nucleotide polymorphisms in NAGNAG acceptors are highly predictive for variations of alternative splicing. Am. J. Hum. Genet. 78 (2006) 291-302
20. Chern T.M., van Nimwegen E., Kai C., Kawai J., Carninci P., Hayashizaki Y., and Zavolan M. A simple physical model predicts small exon length variations. PLoS Genet. 2 (2006) e45
21. Tadokoro K., Yamazaki-Inoue M., Tachibana M., Fujishiro M., Nagao K., Toyoda M., Ozaki M., Ono M., Miki N., Miyashita T., and Yamada M. Frequent occurrence of protein isoforms with or without a single amino acid residue by subtle alternative splicing: the case of Gln in DRPLA affects subcellular localization of the products. J. Hum. Genet. 50 (2005) 382-394
22. Hiller M., Huse K., Szafranski K., Jahn N., Hampe J., Schreiber S., Backofen R., and Platzer M. Widespread occurrence of alternative splicing at NAGNAG acceptors contributes to proteome plasticity. Nat. Genet. 36 (2004) 1255-1257
23. Kao H.W., Chen H.C., Wu C.W., and Lin W.C. Tyrosine-kinase expression profiles in human gastric cancer cell lines and their modulations with retinoic acids. Br. J. Cancer 88 (2003) 1058-1064
24. Scott M., Boisvert F.M., Vieyra D., Johnston R.N., Bazett-Jones D.P., and Riabowol K. UV induces nucleolar translocation of ING1 through two distinct nucleolar targeting sequences. Nucleic Acids Res. 29 (2001) 2052-2058
25. Brady S.N., Yu Y., Maggi Jr. L.B., and Weber J.D. ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway. Mol. Cell Biol. 24 (2004) 9327-9338
26. Itahana K., Bhat K.P., Jin A., Itahana Y., Hawke D., Kobayashi R., and Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol. Cell 12 (2003) 1151-1164
27. Rizos H., Scurr L.L., Irvine M., Alling N.J., and Kefford R.F. p14ARF regulates E2F-1 ubiquitination and degradation via a p53-dependent mechanism. Cell Cycle 6 (2007) 1741-1747
28. Zhang Z., Wang H., Li M., Rayburn E.R., Agrawal S., and Zhang R. Stabilization of E2F1 protein by MDM2 through the E2F1 ubiquitination pathway. Oncogene 24 (2005) 7238-7247
29. Wojcik C., and DeMartino G.N. Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35 (2003) 579-589
30. Shen J.C., Unoki M., Ythier D., Duperray A., Varticovski L., Kumamoto K., Pedeux R., and Harris C.C. Inhibitor of growth 4 suppresses cell spreading and cell migration by interacting with a novel binding partner, liprin alpha1. Cancer Res. 67 (2007) 2552-2558
31. Ha S., Park S., Yun C.H., and Choi Y. Characterization of nuclear localization signal in mouse ING1 homolog protein. Biochem. Biophys. Res. Commun. 293 (2002) 163-166
32. Gonzalez L., Freije J.M., Cal S., Lopez-Otin C., Serrano M., and Palmero I. A functional link between the tumour suppressors ARF and p33ING1. Oncogene 25 (2006) 5173-5179
33. Stott F.J., Bates S., James M.C., McConnell B.B., Starborg M., Brookes S., Palmero I., Ryan K., Hara E., Vousden K.H., and Peters G. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. Embo. J. 17 (1998) 5001-5014
34. den Besten W., Kuo M.L., Tago K., Williams R.T., and Sherr C.J. Ubiquitination of, and sumoylation by, the Arf tumor suppressor. Isr. Med. Assoc. J. 8 (2006) 249-251
35. Sherr C.J., Bertwistle D., W D.E.N.B., Kuo M.L., Sugimoto M., Tago K., Williams R.T., Zindy F., and Roussel M.F. p53-dependent and -independent functions of the Arf tumor suppressor. Cold Spring Harbor Symp. Quant. Biol. 70 (2005) 129-137