Artículo

Pelisch, F.; Gerez, J.; Druker, J.; Schor, I.E.; Muñoz, M.J.; Risso, G.; Petrillo, E.; Westman, B.J.; Lamond, A.I.; Arzt, E.; Srebrow, A. "The serine/arginine-rich protein SF2/ASF regulates protein sumoylation" (2010) Proceedings of the National Academy of Sciences of the United States of America. 107(37):16119-16124
Artículo de Acceso Abierto. Puede ser descargado en su versión final
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Protein modification by conjugation of small ubiquitin-related modifier (SUMO) is involved in diverse biological functions, such as transcription regulation, subcellular partitioning, stress response, DNA damage repair, and chromatin remodeling. Here, we show that the serine/arginine-rich protein SF2/ASF, a factor involved in splicing regulation and other RNA metabolism-related processes, is a regulator of the sumoylation pathway. The overexpression of this protein stimulates, but its knockdown inhibits SUMO conjugation. SF2/ASF interacts with Ubc9 and enhances sumoylation of specific substrates, sharing characteristics with already described SUMO E3 ligases. In addition, SF2/ASF interacts with the SUMO E3 ligase PIAS1 (protein inhibitor of activated STAT-1), regulating PIAS1-induced overall protein sumoylation. The RNA recognition motif 2 of SF2/ASF is necessary and sufficient for sumoylation enhancement. Moreover, SF2/ASF has a role in heat shock-induced sumoylation and promotes SUMO conjugation to RNA processing factors. These results add a component to the sumoylation pathway and a previously unexplored role for the multifunctional SR protein SF2/ASF.

Registro:

Documento: Artículo
Título:The serine/arginine-rich protein SF2/ASF regulates protein sumoylation
Autor:Pelisch, F.; Gerez, J.; Druker, J.; Schor, I.E.; Muñoz, M.J.; Risso, G.; Petrillo, E.; Westman, B.J.; Lamond, A.I.; Arzt, E.; Srebrow, A.
Filiación:Laboratorio de Fisiología Y Biología Molecular, Instituto de Fisiología, Biologia Molecular Y Neurociencias, Consejo Nacional de Investigaciones Cientificas Y Tecnicas, Argentina
Departamento de Fisiología, Biología Molecular Y Celular, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Pabellón II, C1428EHA Buenos Aires, Argentina
College of Life Sciences, University of Dundee, Dundee DD1 5EH, United Kingdom
Palabras clave:E3 ligase; Posttranslational modification; RNA processing; Splicing factor; protein asf; protein inhibitor of activated STAT; protein inhibitor of activated STAT1; protein sf2; protein Ubc9; regulator protein; RNA; SUMO E3 ligase; SUMO protein; ubiquitin protein ligase E3; unclassified drug; nuclear protein; protein binding; protein p53; RNA binding protein; serine-arginine-rich splicing proteins; small interfering RNA; SUMO 1 protein; ubiquitin conjugating enzyme; ubiquitin-conjugating enzyme UBC9; article; conjugation; controlled study; enzyme activity; heat shock; human; human cell; molecular recognition; priority journal; protein expression; protein function; protein processing; protein protein interaction; regulatory mechanism; RNA metabolism; RNA splicing; signal transduction; sumoylation; cell line; enzyme specificity; genetics; heat shock response; metabolism; Cell Line; Heat-Shock Response; Humans; Nuclear Proteins; Protein Binding; RNA, Small Interfering; RNA-Binding Proteins; Substrate Specificity; SUMO-1 Protein; Tumor Suppressor Protein p53; Ubiquitin-Conjugating Enzymes
Año:2010
Volumen:107
Número:37
Página de inicio:16119
Página de fin:16124
DOI: http://dx.doi.org/10.1073/pnas.1004653107
Handle:http://hdl.handle.net/20.500.12110/paper_00278424_v107_n37_p16119_Pelisch
Título revista:Proceedings of the National Academy of Sciences of the United States of America
Título revista abreviado:Proc. Natl. Acad. Sci. U. S. A.
ISSN:00278424
CODEN:PNASA
CAS:RNA, 63231-63-0; SUMO 1 protein, 182213-10-1; ubiquitin conjugating enzyme, 147154-16-3; Nuclear Proteins; RNA, Small Interfering; RNA-Binding Proteins; serine-arginine-rich splicing proteins; SUMO-1 Protein; Tumor Suppressor Protein p53; ubiquitin-conjugating enzyme UBC9; Ubiquitin-Conjugating Enzymes
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00278424_v107_n37_p16119_Pelisch.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00278424_v107_n37_p16119_Pelisch

Referencias:

  • Graveley, B.R., Sorting out the complexity of SR protein functions (2000) RNA, 6, pp. 1197-1211
  • Zhong, X.Y., Wang, P., Han, J., Rosenfeld, M.G., Fu, X.D., SR proteins in vertical integration of gene expression from transcription to RNA processing to translation (2009) Mol Cell, 35, pp. 1-10
  • Shen, H., Green, M.R., A pathway of sequential Arginine-Serine-Rich Domain-Splicing signal interactions during mammalian spliceosome assembly (2004) Molecular Cell, 16 (3), pp. 363-373. , DOI 10.1016/j.molcel.2004.10.021, PII S1097276504006379
  • Shen, H., Kan, J.L.C., Green, M.R., Arginine-Serine-Rich Domains Bound at Splicing Enhancers Contact the Branchpoint to Promote Prespliceosome Assembly (2004) Molecular Cell, 13 (3), pp. 367-376. , DOI 10.1016/S1097-2765(04)00025-5
  • Michlewski, G., Sanford, J.R., Caceres, J.F., The Splicing Factor SF2/ASF Regulates Translation Initiation by Enhancing Phosphorylation of 4E-BP1 (2008) Molecular Cell, 30 (2), pp. 179-189. , DOI 10.1016/j.molcel.2008.03.013, PII S1097276508002372
  • Long, J.C., Caceres, J.F., The SR protein family of splicing factors: Master regulators of gene expression (2009) Biochem J, 417, pp. 15-27
  • Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S., Fu, X.D., The splicing factor SC35 has an active role in transcriptional elongation (2008) Nat Struct Mol Biol, 15, pp. 819-826
  • Huang, Y., Yario, T.A., Steitz, J.A., A molecular linkbetween SR protein dephosphorylation and mRNA export (2004) Proc Natl Acad Sci USA, 101, pp. 9666-9670
  • Lemaire, R., Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: A novel function for SR proteins (2002) Genes Dev, 16, pp. 594-607
  • Zhang, Z., Krainer, A.R., Involvement of SR proteins in mRNA surveillance (2004) Mol Cell, 16, pp. 597-607
  • Sanford, J.R., Gray, N.K., Beckmann, K., Caceres, J.F., A novel role for shuttling SR proteins in mRNA translation (2004) Genes and Development, 18 (7), pp. 755-768. , DOI 10.1101/gad.286404
  • Li, X., Manley, J.L., Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability (2005) Cell, 122, pp. 365-378
  • Li, X., Wang, J., Manley, J.L., Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation (2005) Genes Dev, 19, pp. 2705-2714
  • Manley, J.L., Krainer, A.R., A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins) (2010) Genes Dev, 24, pp. 1073-1074
  • Ge, H., Manley, J.L., A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro (1990) Cell, 62 (1), pp. 25-34. , DOI 10.1016/0092-8674(90)90236-8
  • Krainer, A.R., Conway, G.C., Kozak, D., Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells (1990) Genes and Development, 4 (7), pp. 1158-1171
  • Chiodi, I., RNA recognition motif 2 directs the recruitment of SF2/ASF to nuclear stress bodies (2004) Nucleic Acids Res, 32, pp. 4127-4136
  • Metz, A., Soret, J., Vourc'h, C., Tazi, J., Jolly, C., A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules (2004) J Cell Sci, 117, pp. 4551-4558
  • Geiss-Friedlander, R., Melchior, F., Concepts in sumoylation: A decade on (2007) Nat Rev Mol Cell Biol, 8, pp. 947-956
  • Hay, R.T., SUMO: A history of modification (2005) Mol Cell, 18, pp. 1-12
  • Seeler, J.S., Dejean, A., Nuclear and unclear functions of SUMO (2003) Nat Rev Mol Cell Biol, 4, pp. 690-699
  • Melchior, F., Schergaut, M., Pichler, A., SUMO: Ligases, isopeptidases and nuclear pores (2003) Trends Biochem Sci, 28, pp. 612-618
  • Johnson, E.S., Protein modification by SUMO (2004) Annu Rev Biochem, 73, pp. 355-382
  • Desterro, J.M.P., Thomson, J., Hay, R.T., Ubch9 conjugates SUMO but not ubiquitin (1997) FEBS Letters, 417 (3), pp. 297-300. , DOI 10.1016/S0014-5793(97)01305-7, PII S0014579397013057
  • Lin, D., Identification of a substrate recognition site on Ubc9 (2002) J Biol Chem, 277, pp. 21740-21748
  • Hochstrasser, M., SP-RING for SUMO: New functions bloom for a ubiquitin-like protein (2001) Cell, 107, pp. 5-8
  • Kagey, M.H., Melhuish, T.A., Wotton, D., The polycomb protein Pc2 is a SUMO E3 (2003) Cell, 113, pp. 127-137
  • Pichler, A., Gast, A., Seeler, J.S., Dejean, A., Melchior, F., The nucleoporin RanBP2 has SUMO1 E3 ligase activity (2002) Cell, 108, pp. 109-120
  • Palvimo, J.J., PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription (2007) Biochem Soc Trans, 35, pp. 1405-1408
  • Carbia-Nagashima, A., Gerez, J., Perez-Castro, C., Paez-Pereda, M., Silberstein, S., Stalla, G.K., Holsboer, F., Arzt, E., RSUME, a Small RWD-Containing Protein, Enhances SUMO Conjugation and Stabilizes HIF-1alpha during Hypoxia (2007) Cell, 131 (2), pp. 309-323. , DOI 10.1016/j.cell.2007.07.044, PII S0092867407010240
  • Joazeiro, C.A., Weissman, A.M., RING finger proteins: Mediators of ubiquitin ligase activity (2000) Cell, 102, pp. 549-552
  • Ihara, M., Stein, P., Schultz, R.M., UBE2I (UBC9), a SUMO-conjugating enzyme, localizes to nuclear speckles and stimulates transcription in mouse oocytes (2008) Biol Reprod, 79, pp. 906-913
  • Nayler, O., Stratling, W., Bourquin, J.-P., Stagljar, I., Lindemann, L., Jasper, H., Hartmann, A.M., Stamm, S., SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements (1998) Nucleic Acids Research, 26 (15), pp. 3542-3549. , DOI 10.1093/nar/26.15.3542
  • Rappsilber, J., Ryder, U., Lamond, A.I., Mann, M., Large-scale proteomic analysis of the human spliceosome (2002) Genome Res, 12, pp. 1231-1245
  • Tan, J.A., Protein inhibitors of activated STAT resemble scaffold attachment factors and function as interacting nuclear receptor coregulators (2002) J Biol Chem, 277, pp. 16993-17001
  • Blaustein, M., Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT (2005) Nat Struct Mol Biol, 12, pp. 1037-1044
  • Blaustein, M., SF2/ASF regulates proteomic diversity by affecting the balance between translation initiation mechanisms (2009) J Cell Biochem, 107, pp. 826-833
  • Johnson, E.S., Gupta, A.A., An E3-like factor that promotes SUMO conjugation to the yeast septins (2001) Cell, 106 (6), pp. 735-744. , DOI 10.1016/S0092-8674(01)00491-3
  • Hammer, E., Heilbronn, R., Weger, S., The E3 ligase Topors induces the accumulation of polysumoylated forms of DNA topoisomerase I in vitro and in vivo (2007) FEBS Letters, 581 (28), pp. 5418-5424. , DOI 10.1016/j.febslet.2007.10.040, PII S0014579307011052
  • Rodriguez, M.S., SUMO-1 modification activates the transcriptional response of p53 (1999) EMBO J, 18, pp. 6455-6461
  • Weger, S., Hammer, E., Heilbronn, R., Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo (2005) FEBS Letters, 579 (22), pp. 5007-5012. , DOI 10.1016/j.febslet.2005.07.088, PII S0014579305009774
  • Labourier, E., Interaction between the N-terminal domain of human DNA topoisomerase I and the arginine-serine domain of its substrate determines phosphorylation of SF2/ASF splicing factor (1998) Nucleic Acids Res, 26, pp. 2955-2962
  • Kowalska-Loth, B., Girstun, A., Trzcińska, A.M., Piekiełko- Witkowska, A., Staroń, K., SF2/ASF protein binds to the cap region of human topoisomerase I through two RRM domains (2005) Biochem Biophys Res Commun, 331, pp. 398-403
  • Yunus, A.A., Lima, C.D., Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway (2006) Nat Struct Mol Biol, 13, pp. 491-499
  • Tempé, D., Piechaczyk, M., Bossis, G., SUMO under stress (2008) Biochem Soc Trans, 36, pp. 874-878
  • Golebiowski, F., System-wide changes to SUMO modifications in response to heat shock (2009) Sci Signal, 2, pp. ra24
  • Denegri, M., Chiodi, I., Corioni, M., Cobianchi, F., Riva, S., Biamonti, G., Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors (2001) Molecular Biology of the Cell, 12 (11), pp. 3502-3514
  • Biamonti, G., Nuclear stress bodies: A heterochromatin affair? (2004) Nat Rev Mol Cell Biol, 5, pp. 493-498
  • Chen, T., Boisvert, F.-M., Bazett-Jones, D.P., Richard, S., A role for the GSG domain in localizing Sam68 to novel nuclear structures in cancer cell lines (1999) Molecular Biology of the Cell, 10 (9), pp. 3015-3033
  • Poukka, H., Karvonen, U., Janne, O.A., Palvimo, J.J., Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1) (2000) Proc Natl Acad Sci USA, 97, pp. 14145-14150
  • Li, T., Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: A proteomic analysis (2004) Proc Natl Acad Sci USA, 101, pp. 8551-8556
  • Navascues, J., SUMO-1 transiently localizes to Cajal bodies in mammalian neurons (2008) J Struct Biol, 163, pp. 137-146
  • Vassileva, M.T., Matunis, M.J., SUMO modification of heterogeneous nuclear ribonucleoproteins (2004) Mol Cell Biol, 24, pp. 3623-3632
  • Vertegaal, A.C., A proteomic study of SUMO-2 target proteins (2004) J Biol Chem, 279, pp. 33791-33798
  • Blomster, H.A., Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites (2009) Mol Cell Proteomics, 8, pp. 1382-1390
  • Pungaliya, P., Kulkarni, D., Park, H.-J., Marshall, H., Zheng, H., Lackland, H., Saleem, A., Rubin, E.H., TOPORS functions as a SUMO-1 E3 ligase for chromatin-modifying proteins (2007) Journal of Proteome Research, 6 (10), pp. 3918-3923. , DOI 10.1021/pr0703674
  • Babic, I., Cherry, E., Fujita, D.J., SUMO modification of Sam68 enhances its ability to repress cyclin D1 expression and inhibits its ability to induce apoptosis (2006) Oncogene, 25, pp. 4955-4964
  • Lyman, S.K., Gerace, L., Baserga, S.J., Human Nop5/Nop58 is a component common to the box C/D small nucleolar ribonucleoproteins (1999) RNA, 5, pp. 1597-1604
  • Rajan, P., Gaughan, L., Dalgliesh, C., El-Sherif, A., Robson, C.N., Leung, H.Y., Elliott, D.J., Regulation of gene expression by the RNA-binding protein Sam68 in cancer (2008) Biochemical Society Transactions, 36 (3), pp. 505-507. , DOI 10.1042/BST0360505
  • Desterro, J.M.P., Keegan, L.P., Jaffray, E., Hay, R.T., O'Connell, M.A., Carmo-Fonseca, M., SUMO-1 modification alters ADAR1 editing activity (2005) Molecular Biology of the Cell, 16 (11), pp. 5115-5126. , DOI 10.1091/mbc.E05-06-0536
  • Vethantham, V., Rao, N., Manley, J.L., Sumoylation regulates multiple aspects of mammalian poly(A) polymerase function (2008) Genes Dev, 22, pp. 499-511
  • Vethantham, V., Rao, N., Manley, J.L., Sumoylation modulates the assembly and activity of the pre-mRNA 3′ processing complex (2007) Mol Cell Biol, 27, pp. 8848-8858
  • Mo, Y.Y., Yu, Y., Shen, Z., Beck, W.T., Nucleolar delocalization of human topoisomerase I in response to topotecan correlates with sumoylation of the protein (2002) J Biol Chem, 277, pp. 2958-2964
  • Haindl, M., Harasim, T., Eick, D., Muller, S., The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing (2008) EMBO Reports, 9 (3), pp. 273-279. , DOI 10.1038/embor.2008.3, PII EMBOR20083
  • Cazalla, D., Sanford, J.R., Cáceres, J.F., A rapid and efficient protocol to purify biologically active recombinant proteins frommammalian cells (2005) Protein Expr Purif, 42, pp. 54-58
  • Pichler, A., Knipscheer, P., Saitoh, H., Sixma, T.K., Melchior, F., The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type (2004) Nat Struct Mol Biol, 11, pp. 984-991

Citas:

---------- APA ----------
Pelisch, F., Gerez, J., Druker, J., Schor, I.E., Muñoz, M.J., Risso, G., Petrillo, E.,..., Srebrow, A. (2010) . The serine/arginine-rich protein SF2/ASF regulates protein sumoylation. Proceedings of the National Academy of Sciences of the United States of America, 107(37), 16119-16124.
http://dx.doi.org/10.1073/pnas.1004653107
---------- CHICAGO ----------
Pelisch, F., Gerez, J., Druker, J., Schor, I.E., Muñoz, M.J., Risso, G., et al. "The serine/arginine-rich protein SF2/ASF regulates protein sumoylation" . Proceedings of the National Academy of Sciences of the United States of America 107, no. 37 (2010) : 16119-16124.
http://dx.doi.org/10.1073/pnas.1004653107
---------- MLA ----------
Pelisch, F., Gerez, J., Druker, J., Schor, I.E., Muñoz, M.J., Risso, G., et al. "The serine/arginine-rich protein SF2/ASF regulates protein sumoylation" . Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 37, 2010, pp. 16119-16124.
http://dx.doi.org/10.1073/pnas.1004653107
---------- VANCOUVER ----------
Pelisch, F., Gerez, J., Druker, J., Schor, I.E., Muñoz, M.J., Risso, G., et al. The serine/arginine-rich protein SF2/ASF regulates protein sumoylation. Proc. Natl. Acad. Sci. U. S. A. 2010;107(37):16119-16124.
http://dx.doi.org/10.1073/pnas.1004653107