SUMO Modification of the RNA-Binding Protein La Regulates Cell Proliferation and STAT3 Protein Stability

REFERENCES

• Gaidamakov S, Maximova OA, Chon H, Blewett NH, Wang H, Crawford AK, Day A, Tulchin N, Crouch RJ, Morse HC, III, Blitzer RD, Maraia RJ. 2014. Targeted deletion of the gene encoding the La autoantigen (Sjogren's syndrome antigen B) in B cells or the frontal brain causes extensive tissue loss. Mol Cell Biol 34:123–131. https://doi.org/10.1128/MCB.01010-13.
   PubMed Web of Science ®Google Scholar
• Park JM, Kohn MJ, Bruinsma MW, Vech C, Intine RV, Fuhrmann S, Grinberg A, Mukherjee I, Love PE, Ko MS, DePamphilis ML, Maraia RJ. 2006. The multifunctional RNA-binding protein La is required for mouse development and for the establishment of embryonic stem cells. Mol Cell Biol 26:1445–1451. https://doi.org/10.1128/MCB.26.4.1445-1451.2006.
   PubMed Web of Science ®Google Scholar
• Bayfield MA, Maraia RJ. 2009. Precursor-product discrimination by La protein during tRNA metabolism. Nat Struct Mol Biol 16:430–437. https://doi.org/10.1038/nsmb.1573.
   PubMed Web of Science ®Google Scholar
• Fan H, Goodier JL, Chamberlain JR, Engelke DR, Maraia RJ. 1998. 5′ processing of tRNA precursors can be modulated by the human La antigen phosphoprotein. Mol Cell Biol 18:3201–3211. https://doi.org/10.1128/MCB.18.6.3201.
   PubMed Web of Science ®Google Scholar
• Wolin SL, Cedervall T. 2002. The La protein. Annu Rev Biochem 71:375–403. https://doi.org/10.1146/annurev.biochem.71.090501.150003.
   PubMed Web of Science ®Google Scholar
• Yoo CJ, Wolin SL. 1997. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell 89:393–402. https://doi.org/10.1016/S0092-8674(00)80220-2.
   PubMed Web of Science ®Google Scholar
• Liu Y, Tan H, Tian H, Liang C, Chen S, Liu Q. 2011. Autoantigen La promotes efficient RNAi, antiviral response, and transposon silencing by facilitating multiple-turnover RISC catalysis. Mol Cell 44:502–508. https://doi.org/10.1016/j.molcel.2011.09.011.
   PubMed Web of Science ®Google Scholar
• Liang C, Xiong K, Szulwach KE, Zhang Y, Wang Z, Peng J, Fu M, Jin P, Suzuki HI, Liu Q. 2013. Sjogren syndrome antigen B (SSB)/La promotes global microRNA expression by binding microRNA precursors through stem-loop recognition. J Biol Chem 288:723–736. https://doi.org/10.1074/jbc.M112.401323.
   PubMed Web of Science ®Google Scholar
• Hasler D, Lehmann G, Murakawa Y, Klironomos F, Jakob L, Grasser FA, Rajewsky N, Landthaler M, Meister G. 2016. The lupus autoantigen La prevents mis-channeling of tRNA fragments into the human microRNA pathway. Mol Cell 63:110–124. https://doi.org/10.1016/j.molcel.2016.05.026.
   PubMed Web of Science ®Google Scholar
• Ali N, Siddiqui A. 1997. The La antigen binds 5′ noncoding region of the hepatitis C virus RNA in the context of the initiator AUG codon and stimulates internal ribosome entry site-mediated translation. Proc Natl Acad Sci U S A 94:2249–2254. https://doi.org/10.1073/pnas.94.6.2249.
   PubMed Web of Science ®Google Scholar
• Belsham GJ, Sonenberg N, Svitkin YV. 1995. The role of the La autoantigen in internal initiation. Curr Top Microbiol Immunol 203:85–98.
   PubMed Web of Science ®Google Scholar
• Costa-Mattioli M, Svitkin Y, Sonenberg N. 2004. La autoantigen is necessary for optimal function of the poliovirus and hepatitis C virus internal ribosome entry site in vivo and in vitro. Mol Cell Biol 24:6861–6870. https://doi.org/10.1128/MCB.24.15.6861-6870.2004.
   PubMed Web of Science ®Google Scholar
• Petz M, Them N, Huber H, Beug H, Mikulits W. 2012. La enhances IRES-mediated translation of laminin B1 during malignant epithelial to mesenchymal transition. Nucleic Acids Res 40:290–302. https://doi.org/10.1093/nar/gkr717.
   PubMed Web of Science ®Google Scholar
• Petz M, Them NC, Huber H, Mikulits W. 2012. PDGF enhances IRES-mediated translation of laminin B1 by cytoplasmic accumulation of La during epithelial to mesenchymal transition. Nucleic Acids Res 40:9738–9749. https://doi.org/10.1093/nar/gks760.
   PubMed Web of Science ®Google Scholar
• Trotta R, Vignudelli T, Candini O, Intine RV, Pecorari L, Guerzoni C, Santilli G, Byrom MW, Goldoni S, Ford LP, Caligiuri MA, Maraia RJ, Perrotti D, Calabretta B. 2003. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 3:145–160. https://doi.org/10.1016/S1535-6108(03)00020-5.
   PubMed Web of Science ®Google Scholar
• Holcik M, Korneluk RG. 2000. Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: role of La autoantigen in XIAP translation. Mol Cell Biol 20:4648–4657. https://doi.org/10.1128/MCB.20.13.4648-4657.2000.
   PubMed Web of Science ®Google Scholar
• Heise T, Kota V, Brock A, Morris AB, Rodriguez RM, Zierk AW, Howe PH, Sommer G. 2016. The La protein counteracts cisplatin-induced cell death by stimulating protein synthesis of anti-apoptotic factor Bcl2. Oncotarget 7:29664–29676. https://doi.org/10.18632/oncotarget.8819.
   PubMedGoogle Scholar
• Sommer G, Dittmann J, Kuehnert J, Reumann K, Schwartz PE, Will H, Coulter BL, Smith MT, Heise T. 2011. The RNA-binding protein La contributes to cell proliferation and CCND1 expression. Oncogene 30:434–444. https://doi.org/10.1038/onc.2010.425.
   PubMed Web of Science ®Google Scholar
• Spangberg K, Wiklund L, Schwartz S. 2001. Binding of the La autoantigen to the hepatitis C virus 3′ untranslated region protects the RNA from rapid degradation in vitro. J Gen Virol 82:113–120. https://doi.org/10.1099/0022-1317-82-1-113.
   PubMed Web of Science ®Google Scholar
• Brenet F, Dussault N, Borch J, Ferracci G, Delfino C, Roepstorff P, Miquelis R, Ouafik L. 2005. Mammalian peptidylglycine alpha-amidating monooxygenase mRNA expression can be modulated by the La autoantigen. Mol Cell Biol 25:7505–7521. https://doi.org/10.1128/MCB.25.17.7505-7521.2005.
   PubMed Web of Science ®Google Scholar
• Heise T, Guidotti LG, Cavanaugh VJ, Chisari FV. 1999. Hepatitis B virus RNA-binding proteins associated with cytokine-induced clearance of viral RNA from the liver of transgenic mice. J Virol 73:474–481.
   PubMed Web of Science ®Google Scholar
• Heise T, Guidotti LG, Chisari FV. 1999. La autoantigen specifically recognizes a predicted stem-loop in hepatitis B virus RNA. J Virol 73:5767–5776.
   PubMed Web of Science ®Google Scholar
• McLaren R, Caruccio N, Ross J. 1997. Human La protein: a stabilizer of histone mRNA. Mol Cell Biol 17:3028–3036. https://doi.org/10.1128/MCB.17.6.3028.
   PubMed Web of Science ®Google Scholar
• Al-Ejeh F, Darby JM, Brown MP. 2007. The La autoantigen is a malignancy-associated cell death target that is induced by DNA-damaging drugs. Clin Cancer Res 13:5509s–5518s. https://doi.org/10.1158/1078-0432.CCR-07-0922.
   PubMed Web of Science ®Google Scholar
• Sommer G, Rossa C, Chi AC, Neville BW, Heise T. 2011. Implication of RNA-binding protein La in proliferation, migration and invasion of lymph node-metastasized hypopharyngeal SCC cells. PLoS One 6:e25402. https://doi.org/10.1371/journal.pone.0025402.
   PubMed Web of Science ®Google Scholar
• Simons FH, Broers FJ, Van Venrooij WJ, Pruijn GJ. 1996. Characterization of cis-acting signals for nuclear import and retention of the La (SS-B) autoantigen. Exp Cell Res 224:224–236. https://doi.org/10.1006/excr.1996.0132.
   PubMed Web of Science ®Google Scholar
• Horke S, Reumann K, Schweizer M, Will H, Heise T. 2004. Nuclear trafficking of La protein depends on a newly identified nucleolar localization signal and the ability to bind RNA. J Biol Chem 279:26563–26570. https://doi.org/10.1074/jbc.M401017200.
   PubMed Web of Science ®Google Scholar
• Intine RV, Dundr M, Vassilev A, Schwartz E, Zhao Y, Zhao Y, Depamphilis ML, Maraia RJ. 2004. Nonphosphorylated human La antigen interacts with nucleolin at nucleolar sites involved in rRNA biogenesis. Mol Cell Biol 24:10894–10904. https://doi.org/10.1128/MCB.24.24.10894-10904.2004.
   PubMed Web of Science ®Google Scholar
• Hussain RH, Zawawi M, Bayfield MA. 2013. Conservation of RNA chaperone activity of the human La-related proteins 4, 6 and 7. Nucleic Acids Res 41:8715–8725. https://doi.org/10.1093/nar/gkt649.
   PubMed Web of Science ®Google Scholar
• Kuehnert J, Sommer G, Zierk AW, Fedarovich A, Brock A, Fedarovich D, Heise T. 2015. Novel RNA chaperone domain of RNA-binding protein La is regulated by AKT phosphorylation. Nucleic Acids Res 43:581–594. https://doi.org/10.1093/nar/gku1309.
   PubMed Web of Science ®Google Scholar
• Bachmann M, Chang S, Slor H, Kukulies J, Muller WE. 1990. Shuttling of the autoantigen La between nucleus and cell surface after UV irradiation of human keratinocytes. Exp Cell Res 191:171–180. https://doi.org/10.1016/0014-4827(90)90002-R.
   PubMed Web of Science ®Google Scholar
• Brenet F, Socci ND, Sonenberg N, Holland EC. 2009. Akt phosphorylation of La regulates specific mRNA translation in glial progenitors. Oncogene 28:128–139. https://doi.org/10.1038/onc.2008.376.
   PubMed Web of Science ®Google Scholar
• Fok V, Friend K, Steitz JA. 2006. Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J Cell Biol 173:319–325. https://doi.org/10.1083/jcb.200601026.
   PubMed Web of Science ®Google Scholar
• Fan H, Sakulich AL, Goodier JL, Zhang X, Qin J, Maraia RJ. 1997. Phosphorylation of the human La antigen on serine 366 can regulate recycling of RNA polymerase III transcription complexes. Cell 88:707–715. https://doi.org/10.1016/S0092-8674(00)81913-3.
   PubMed Web of Science ®Google Scholar
• Intine RV, Sakulich AL, Koduru SB, Huang Y, Pierstorff E, Goodier JL, Phan L, Maraia RJ. 2000. Control of transfer RNA maturation by phosphorylation of the human La antigen on serine 366. Mol Cell 6:339–348. https://doi.org/10.1016/S1097-2765(00)00034-4.
   PubMed Web of Science ®Google Scholar
• Schwartz EI, Intine RV, Maraia RJ. 2004. CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate rpL37 5′-terminal oligopyrimidine mRNA metabolism. Mol Cell Biol 24:9580–9591. https://doi.org/10.1128/MCB.24.21.9580-9591.2004.
   PubMed Web of Science ®Google Scholar
• Intine RV, Tenenbaum SA, Sakulich AL, Keene JD, Maraia RJ. 2003. Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs. Mol Cell 12:1301–1307. https://doi.org/10.1016/S1097-2765(03)00429-5.
   PubMed Web of Science ®Google Scholar
• Girdwood DW, Tatham MH, Hay RT. 2004. SUMO and transcriptional regulation. Semin Cell Dev Biol 15:201–210. https://doi.org/10.1016/j.semcdb.2003.12.001.
   PubMed Web of Science ®Google Scholar
• Johnson ES. 2004. Protein modification by SUMO. Annu Rev Biochem 73:355–382. https://doi.org/10.1146/annurev.biochem.73.011303.074118.
   PubMed Web of Science ®Google Scholar
• Hay RT. 2005. SUMO: a history of modification. Mol Cell 18:1–12. https://doi.org/10.1016/j.molcel.2005.03.012.
   PubMed Web of Science ®Google Scholar
• van Niekerk EA, Willis DE, Chang JH, Reumann K, Heise T, Twiss JL. 2007. Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc Natl Acad Sci U S A 104:12913–12918. https://doi.org/10.1073/pnas.0611562104.
   PubMed Web of Science ®Google Scholar
• Kota V, Sommer G, Durette C, Thibault P, van Niekerk EA, Twiss JL, Heise T. 2016. SUMO-modification of the La protein facilitates binding to mRNA in vitro and in cells. PLoS One 11:e0156365. https://doi.org/10.1371/journal.pone.0156365.
   PubMedGoogle Scholar
• Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, Cox J, Barton GJ, Mann M, Hay RT. 2009. System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2:ra24. https://doi.org/10.1126/scisignal.2000282.
   PubMed Web of Science ®Google Scholar
• Hendriks IA, D'Souza RC, Yang B, Verlaan-de Vries M, Mann M, Vertegaal AC. 2014. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21:927–936. https://doi.org/10.1038/nsmb.2890.
   PubMed Web of Science ®Google Scholar
• Hendriks IA, D'Souza RC, Chang JG, Mann M, Vertegaal AC. 2015. System-wide identification of wild-type SUMO-2 conjugation sites. Nat Commun 6:7289. https://doi.org/10.1038/ncomms8289.
   PubMed Web of Science ®Google Scholar
• Tammsalu T, Matic I, Jaffray EG, Ibrahim AF, Tatham MH, Hay RT. 2014. Proteome-wide identification of SUMO2 modification sites. Sci Signal 7:rs2. https://doi.org/10.1126/scisignal.2005146.
   PubMed Web of Science ®Google Scholar
• Geiger JL, Grandis JR, Bauman JE. 2016. The STAT3 pathway as a therapeutic target in head and neck cancer: barriers and innovations. Oral Oncol 56:84–92. https://doi.org/10.1016/j.oraloncology.2015.11.022.
   PubMed Web of Science ®Google Scholar
• Banerjee K, Resat H. 2016. Constitutive activation of STAT3 in breast cancer cells: a review. Int J Cancer 138:2570–2578. https://doi.org/10.1002/ijc.29923.
   PubMed Web of Science ®Google Scholar
• Peek R, Pruijn GJ, Van Venrooij WJ. 1996. Interaction of the La (SS-B) autoantigen with small ribosomal subunits. Eur J Biochem 236:649–655. https://doi.org/10.1111/j.1432-1033.1996.0649d.x.
   PubMedGoogle Scholar
• Pudi R, Srinivasan P, Das S. 2004. La protein binding at the GCAC site near the initiator AUG facilitates the ribosomal assembly on the hepatitis C virus RNA to influence internal ribosome entry site-mediated translation. J Biol Chem 279:29879–29888. https://doi.org/10.1074/jbc.M403417200.
   PubMed Web of Science ®Google Scholar
• McBratney S, Sarnow P. 1996. Evidence for involvement of trans-acting factors in selection of the AUG start codon during eukaryotic translational initiation. Mol Cell Biol 16:3523–3534. https://doi.org/10.1128/MCB.16.7.3523.
   PubMed Web of Science ®Google Scholar
• Wei J, Yuan Y, Jin C, Chen H, Leng L, He F, Wang J. 2012. The ubiquitin ligase TRAF6 negatively regulates the JAK-STAT signaling pathway by binding to STAT3 and mediating its ubiquitination. PLoS One 7:e49567. https://doi.org/10.1371/journal.pone.0049567.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Yamamoto Y, Muromoto R, Ikeda O, Sekine Y, Grusby MJ, Kaisho T, Matsuda T. 2011. PDLIM2 inhibits T helper 17 cell development and granulomatous inflammation through degradation of STAT3. Sci Signal 4:ra85. https://doi.org/10.1126/scisignal.2001637.
   PubMed Web of Science ®Google Scholar
• Chen J, Bardes EE, Aronow BJ, Jegga AG. 2009. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 37:W305–W311. https://doi.org/10.1093/nar/gkp427.
   PubMed Web of Science ®Google Scholar
• Kamitani T, Kito K, Nguyen HP, Yeh ET. 1997. Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J Biol Chem 272:28557–28562. https://doi.org/10.1074/jbc.272.45.28557.
   PubMed Web of Science ®Google Scholar