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Abstract:

E1A is the main transforming protein in mastadenoviruses. This work uses bioinformatics to extrapolate experimental knowledge from Human adenovirus serotype 5 and 12 E1A proteins to all known serotypes. A conserved domain architecture with a high degree of intrinsic disorder acts as a scaffold for multiple linear motifs with variable occurrence mediating the interaction with over fifty host proteins. While linear motifs contribute strongly to sequence conservation within intrinsically disordered E1A regions, motif repertoires can deviate significantly from those found in prototypical serotypes. Close to one hundred predicted residue-residue contacts suggest the presence of stable structure in the CR3 domain and of specific conformational ensembles involving both short- and long-range intramolecular interactions. Our computational results suggest that E1A sequence conservation and co-evolution reflect the evolutionary pressure to maintain a mainly disordered, yet non-random conformation harboring a high number of binding motifs that mediate viral hijacking of the cell machinery. © 2018 Elsevier Inc.

Registro:

Documento: Artículo
Título:Interplay between sequence, structure and linear motifs in the adenovirus E1A hub protein
Autor:Glavina, J.; Román, E.A.; Espada, R.; de Prat-Gay, G.; Chemes, L.B.; Sánchez, I.E.
Filiación:Universidad de Buenos Aires. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN). Facultad de Ciencias Exactas y Naturales. Laboratorio de Fisiología de Proteínas, Buenos Aires, Argentina
Instituto de Química y Físico-Química Biológicas, Universidad de Buenos Aires, Junín 956, Buenos Aires, 1113AAD, Argentina
Protein Structure-Function and Engineering Laboratory, Fundación Instituto Leloir and IIBBA-CONICET, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones Biotecnológicas IIB-INTECH, Universidad Nacional de San Martín, San Martín, Buenos Aires, Argentina
Departamento de Fisiología y Biología Molecular y Celular (DFBMC), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Adenovirus; Co-evolution; E1A; Intrinsic disorder; Linear motifs; Motif repertoire; Random polymer; Sequence conservation; E1A protein; intrinsically disordered protein; E1A protein; amino acid sequence; Article; coevolution; conserved sequence; controlled study; Human adenovirus 12; Human adenovirus 5; nonhuman; priority journal; protein binding; protein conformation; protein domain; protein motif; protein protein interaction; protein structure; amino acid sequence; chemistry; genetics; human; Human adenovirus C; metabolism; protein motif; translational protein modification; Adenovirus E1A Proteins; Adenoviruses, Human; Amino Acid Motifs; Amino Acid Sequence; Humans; Protein Conformation; Protein Domains; Protein Modification, Translational
Año:2018
Volumen:525
Página de inicio:117
Página de fin:131
DOI: http://dx.doi.org/10.1016/j.virol.2018.08.012
Título revista:Virology
Título revista abreviado:Virology
ISSN:00426822
CODEN:VIRLA
CAS:Adenovirus E1A Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00426822_v525_n_p117_Glavina

Referencias:

  • Allende, J.E., Allende, C.C., Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation (1995) FASEB J., 9 (5), pp. 313-323
  • Ansieau, S., Leutz, A., The conserved Mynd domain of BS69 binds cellular and oncoviral proteins through a common PXLXP motif (2002) J. Biol. Chem., 277 (7), pp. 4906-4910
  • Ashkenazy, H., Abadi, S., Martz, E., Chay, O., Mayrose, I., Pupko, T., ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules (2016) Nucleic Acids Res, 44 (W1), pp. W344-W350
  • Avvakumov, N., Wheeler, R., D'Halluin, J.C., Mymryk, J.S., Comparative sequence analysis of the largest E1A proteins of human and simian adenoviruses (2002) J. Virol., 76 (16), pp. 7968-7975
  • Avvakumov, N., Kajon, A.E., Hoeben, R.C., Mymryk, J.S., Comprehensive sequence analysis of the E1A proteins of human and simian adenoviruses (2004) Virology, 329 (2), pp. 477-492
  • Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing (1995) J. R. Stat. Soc. Ser. B Methodol., 57 (1), pp. 289-300
  • Bondesson, M., Svensson, C., Linder, S., Akusjärvi, G., The carboxy-terminal exon of the adenovirus E1A protein is required for E4F-dependent transcription activation (1992) EMBO J., 11 (9), pp. 3347-3354
  • Borcherds, W., Becker, A., Chen, L., Chen, J., Chemes, L.B., Daughdrill, G.W., Optimal affinity enhancement by a conserved flexible linker controls p53 mimicry in MdmX (2017) Biophys. J., 112 (10), pp. 2038-2042
  • Borkosky, S.S., Camporeale, G., Chemes, L.B., Risso, M., Noval, M.G., Sánchez, I.E., Hidden structural codes in protein intrinsic disorder (2017) Biochemistry, 56 (41), pp. 5560-5569
  • Boyd, J.M., Subramanian, T., Schaeper, U., La Regina, M., Bayley, S.T., Chinnadurai, G., A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis (1993) EMBO J., 12 (2), pp. 469-478
  • Boyd, J.M., Loewenstein, P.M., Tang, Q.Q., Yu, L., Green, M., Adenovirus E1A N-terminal amino acid sequence requirements for repression of transcription in vitro and in vivo correlate with those required for E1A interference with TBP-TATA complex formation (2002) J. Virol., 76 (3), pp. 1461-1474
  • Buslje, C.M., Santos, J., Delfino, J.M., Nielsen, M., Correction for phylogeny, small number of observations and data redundancy improves the identification of coevolving amino acid pairs using mutual information (2009) Bioinformatics, 25 (9), pp. 1125-1131
  • Camporeale, G., Lorenzo, J.R., Thomas, M.G., Salvatierra, E., Borkosky, S.S., Risso, M.G., Degenerate cysteine patterns mediate two redox sensing mechanisms in the papillomavirus E7 oncoprotein (2017) Redox Biol., 11, pp. 38-50. , (October 2016)
  • Chatton, B., Bocco, J.L., Gaire, M., Hauss, C., Reimund, B., Goetz, J., Transcriptional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a (1993) Mol. Cell Biol., 13 (1), pp. 561-570
  • Chemes, L.B., Sánchez, I.E., Smal, C., de Prat-Gay, G., Targeting mechanism of the retinoblastoma tumor suppressor by a prototypical viral oncoprotein. Structural modularity, intrinsic disorder and phosphorylation of human papillomavirus E7 (2010) FEBS J., 277 (4), pp. 973-988
  • Chemes, L.B., Sánchez, I.E., de Prat-Gay, G., Kinetic recognition of the retinoblastoma tumor suppressor by a specific protein target (2011) J. Mol. Biol., 412 (2), pp. 267-284
  • Chemes, L.B., Glavina, J., Alonso, L.G., Marino-Buslje, C., de Prat-Gay, G., Sánchez, I.E., Sequence evolution of the intrinsically disordered and globular domains of a model viral oncoprotein (2012) PLoS One, 7 (10), p. e47661
  • Chemes, L.B., Glavina, J., Faivovich, J., de Prat-Gay, G., Sánchez, I.E., Evolution of linear motifs within the papillomavirus E7 oncoprotein (2012) J. Mol. Biol., 422 (3), pp. 336-346
  • Chemes, L.B., Camporeale, G., Sánchez, I.E., de Prat-Gay, G., Alonso, L.G., Cysteine-rich positions outside the structural zinc motif of human papillomavirus E7 provide conformational modulation and suggest functional redox roles (2014) Biochemistry, 53 (10), pp. 1680-1696
  • Chemes, L.B., de Prat-Gay, G., Sánchez, I.E., Convergent evolution and mimicry of protein linear motifs in host-pathogen interactions (2015) Curr. Opin. Struct. Biol., 32, pp. 91-101
  • Clementi, C., Nymeyer, H., Onuchic, J.N., Topological and energetic factors: what determines the structural details of the transition state ensemble and en-route intermediates for protein folding? An investigation for small globular proteins (2000) J. Mol. Biol., 298 (5), pp. 937-953. , (arXiv:0003460)
  • Cohen, M.J., Yousef, A.F., Massimi, P., Fonseca, G.J., Todorovic, B., Pelka, P., Dissection of the C-terminal region of E1A redefines the roles of CtBP and other cellular targets in oncogenic transformation (2013) J. Virol., 87 (18), pp. 10348-10355
  • Cohen, M.J., King, C.R., Dikeakos, J.D., Mymryk, J.S., Functional analysis of the C-terminal region of human adenovirus E1A reveals a misidentified nuclear localization signal (2014) Virology, 468–470C, pp. 238-243
  • Corbeil, H.B., Branton, P.E., Functional importance of complex formation between the retinoblastoma tumor suppressor family and adenovirus E1A proteins as determined by mutational analysis of E1A conserved region 2 (1994) J. Virol., 68 (10), pp. 6697-6709
  • Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E., WebLogo: a sequence logo generator (2004) Genome Res, 14 (6), pp. 1188-1190
  • Culp, J.S., Webster, L.C., Friedman, D.J., Smith, C.L., Huang, W.J., Wu, F.Y., The 289-amino acid E1A protein of adenovirus binds zinc in a region that is important for trans-activation (1988) Proc. Natl. Acad. Sci. USA, 85 (17), pp. 6450-6454
  • Daughdrill, G.W., Borcherds, W.M., Wu, H., Disorder predictors also predict backbone dynamics for a family of disordered proteins (2011) PLoS One, 6 (12), pp. 0-6
  • Davey, N.E., Travé, G., Gibson, T.J., How viruses hijack cell regulation (2011) Trends Biochem. Sci., 36 (3), pp. 159-169
  • Davey, N.E., Van Roey, K., Weatheritt, R.J., Toedt, G., Uyar, B., Altenberg, B., Attributes of short linear motifs (2012) Mol. Biosyst., 8 (1), pp. 268-281
  • Davison, A.J., Benko, M., Harrach, B., Genetic content and evolution of adenoviruses (2003) J. Gen. Virol., 84 (11), pp. 2895-2908
  • Dinkel, H., Van Roey, K., Michael, S., Davey, N.E., Weatheritt, R.J., Born, D., The eukaryotic linear motif resource ELM: 10 years and counting (2014) Nucleic Acids Res., 42 (Database issue), pp. D259-66
  • Doerfler, W., Böhm, P., (2004), 273, pp. 05715-1. , http://dx.doi.org/10.1007/978-3-662-05599-1, Adenoviruses: Model and Vectors in Virus-Host Interactions; of Current Topics in Microbiology and Immunology. 1 ed.; Berlin, Heidelberg: Springer Berlin Heidelberg. ISBN 978-3-642-; Dosztányi, Z., Csizmók, V., Tompa, P., Simon, I., IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content (2005) Bioinformatics, 21 (16), pp. 3433-3434
  • Dyson, H.J., Wright, P.E., Role of intrinsic protein disorder in the function and interactions of the transcriptional coactivators CREB-binding Protein (CBP) and p300 (2016) J. Biol. Chem., 291 (13), pp. 6714-6722. , (arXiv:NIHMS150003)
  • Dyson, N.J., Guida, P., McCall, C., Harlow, E., Adenovirus E1A makes two distinct contacts with the retinoblastoma protein (1992) J. Virol., 66 (7), pp. 4606-4611
  • Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res., 32 (5), pp. 1792-1797
  • Espada, R., Parra, R.G., Mora, T., Walczak, A.M., Ferreiro, D.U., Capturing coevolutionary signals inrepeat proteins (2015) BMC Bioinforma., 16 (1), p. 207. , 1407.6903, (arXiv:)
  • Ferrari, R., Pellegrini, M., Horwitz, G.A., Xie, W., Berk, A.J., Kurdistani, S.K., Epigenetic reprogramming by adenovirus e1a (2008) Science, 321 (5892), pp. 1086-1088
  • Ferreiro, D.U., Hegler, J.A., Komives, E.A., Wolynes, P.G., Localizing frustration in native proteins and protein assemblies (2007) Proc. Natl. Acad. Sci. USA, 104 (50), pp. 19819-19824
  • Ferreon, J.C., Martinez-Yamout, M.A., Dyson, H.J., Wright, P.E., Structural basis for subversion of cellular control mechanisms by the adenoviral E1A oncoprotein (2009) Proc. Natl. Acad. Sci. USA, 106 (32), pp. 13260-13265
  • Ferreon, A.C.M., Ferreon, J.C., Wright, P.E., Deniz, A.A., Modulation of allostery by protein intrinsic disorder (2013) Nature, 498 (7454), pp. 390-394
  • Geisberg, J.V., Chen, J.L., Ricciardi, R.P., Subregions of the adenovirus E1A transactivation domain target multiple components of the TFIID complex (1995) Mol. Cell. Biol., 15 (11), pp. 6283-6290
  • Good, P.I., Permutation, Parametric, and Bootstrap Tests of Hypotheses. Springer Series in Statistics (2006), 3 ed. Springer-Verlag New York (); Graham, F.L., Smiley, J., Russell, W.C., Nairn, R., Characteristics of a human cell line transformed by DNA from human adenovirus type 5 (1977) J. Gen. Virol., 36 (1), pp. 59-74
  • Haberz, P., Arai, M., Martinez-Yamout, M.A., Dyson, H.J., Wright, P.E., Mapping the interactions of adenoviral E1A proteins with the p160 nuclear receptor coactivator binding domain of CBP (2016) Protein Sci., 25 (12), pp. 2256-2267
  • Harrach, B., Benkö, M., Both, G.W., Brown, M., Davison, A.J., Echavarría, M., (2011), pp. 125-141. , http://dx.doi.org/10.1016/B978-0-12-384684-6.00009-4, In: King, A.M., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., editors. Virus Taxononmy. Ninth Report. International Committe Taxon. Viruses; chap. Family Adenoviridae; 9 ed. San Diego: Elsevier; Hateboer, G., Gennissen, A., Ramos, Y.F.M., Kerkhoven, R.M., Sonntag-Buck, V., Stunnenberg, H.G., BS69, a novel adenovirus E1A-associated protein that inhibits E1A transactivation (1995) EMBO J., 14 (13), pp. 3159-3169
  • Heck, D.V., Yee, C.L., Howley, P.M., Münger, K., Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses (1992) Proc. Natl. Acad. Sci. USA, 89 (10), pp. 4442-4446
  • Henikoff, S., Henikoff, J.G., Position-based sequence weights (1994) J. Mol. Biol., 243 (4), pp. 574-578
  • Hošek, T., Calçada, E.O., Nogueira, M.O., Salvi, M., Pagani, T.D., Felli, I.C., Structural and dynamic characterization of the molecular hub early Region 1A (E1A) from human adenovirus (2016) Chem. - A Eur. J., 22 (37), pp. 13010-13013
  • Humphrey, W., Dalke, A., Schulten, K., VMD: visual molecular dynamics (1996) J. Mol. Graph, 14 (1). , (33-8, 27-8)
  • Ikeda, M.A., Nevins, J.R., Identification of distinct roles for separate E1A domains in disruption of E2F complexes (1993) Mol. Cell. Biol., 13 (11), pp. 7029-7035
  • Isobe, T., Uchida, C., Hattori, T., Kitagawa, K., Oda, T., Kitagawa, M., Ubiquitin-dependent degradation of adenovirus E1A protein is inhibited by BS69 (2006) Biochem. Biophys. Res. Commun., 339 (1), pp. 367-374
  • Köhler, M., Görlich, D., Hartmann, E., Franke, J., Adenoviral E1A protein nuclear import is preferentially mediated by importin alpha3 (2001) Vitr. Virol., 289 (2), pp. 186-191
  • Khanal, S., Ghimire, P., Dhamoon, A., The repertoire of adenovirus in human disease: the innocuous to the deadly (2018) Biomedicines, 6 (1), p. 30
  • Kimelman, D., Miller, J.S., Porter, D., Roberts, B.E., E1a regions of the human adenoviruses and of the highly oncogenic simian adenovirus 7 are closely related (1985) J. Virol., 53 (2), pp. 399-409
  • King, C.R., Zhang, A., Tessier, T.M., Gameiro, S.F., Mymryk, J.S., Hacking the cell: network intrusion and exploitation by adenovirus E1A (2018) MBio, 9 (3), pp. 1-18
  • Larsen, P.L., Tibbetts, C., Adenovirus E1A gene autorepression: revertants of an E1A promoter mutation encode altered E1A proteins (1987) Proc. Natl. Acad. Sci. USA, 84 (December), pp. 8185-8189
  • Liu, F., Green, M.R., Promoter targeting by adenovirus E1a through interaction with different cellular DNA-binding domains (1994) Nature, 368 (6471), pp. 520-525
  • Liu, X., Marmorstein, R., Structure of the retinoblastoma protein bound to adenovirus E1A reveals the molecular basis for viral oncoprotein inactivation of a tumor suppressor (2007) Genes Dev., 21 (21), pp. 2711-2716
  • Liu, X., Clements, A., Zhao, K., Marmorstein, R., Structure of the human Papillomavirus E7 oncoprotein and its mechanism for inactivation of the retinoblastoma tumor suppressor (2006) J. Biol. Chem., 281 (1), pp. 578-586
  • Lyons, R.H., Ferguson, B.Q., Rosenberg, M., Pentapeptide nuclear localization signal in adenovirus E1a (1987) Mol. Cell. Biol., 7 (7), pp. 2451-2456
  • Madison, D.L., Yaciuk, P., Kwok, R.P.S., Lundblad, J.R., Acetylation of the adenovirus-transforming protein E1A determines nuclear localization by disrupting association with importin-alpha (2002) J. Biol. Chem., 277 (41), pp. 38755-38763
  • Martin, A.J.M., Walsh, I., Tosatto, S.C.E., MOBI: a web server to define and visualize structural mobility in NMR protein ensembles (2010) Bioinformatics, 26 (22), pp. 2916-2917
  • Mazzarelli, J.M., Mengus, G., Davidson, I., Ricciardi, R.P., The transactivation domain of adenovirus E1A interacts with the C terminus of human TAF(II)135 (1997) J. Virol., 71 (10), pp. 7978-7983
  • Meng, X., Webb, P., Yang, Y.F., Shuen, M., Yousef, A.F., Baxter, J.D., E1A and a nuclear receptor corepressor splice variant (N-CoRI) are thyroid hormone receptor coactivators that bind in the corepressor mode (2005) Proc. Natl. Acad. Sci. USA, 102 (18), pp. 6267-6272
  • Molloy, D.P., Milner, A.E., Yakub, I.K., Chinnadurai, G., Gallimore, P.H., Grand, R.J.A., Structural determinants present in the C-terminal binding protein binding site of adenovirus early Region 1A proteins (1998) J. Biol. Chem., 273 (33), pp. 20867-20876
  • Molloy, D.P., Smith, K.J., Milner, A.E., Gallimore, P.H., Grand, R.J.A., The structure of the site on adenovirus early Region 1A responsible for binding to TATA-binding protein determined by NMR spectroscopy (1999) J. Biol. Chem., 274 (6), pp. 3503-3512
  • Molloy, D.P., Barral, P.M., Bremner, K.H., Gallimore, P.H., Grand, R.J.A., Structural determinants in adenovirus 12 E1A involved in the interaction with C-terminal binding protein 1 (2000) Virology, 277 (1), pp. 156-166
  • Molloy, D.P., Mapp, K.L., Webster, R., Gallimore, P.H., Grand, R.J.A., Acetylation at a lysine residue adjacent to the CtBP binding motif within adenovirus 12 E1A causes structural disruption and limited reduction of CtBP binding (2006) Virology, 355 (2), pp. 115-126
  • Molloy, D.P., Barral, P.M., Gallimore, P.H., Grand, R.J.A., The effect of CtBP1 binding on the structure of the C-terminal region of adenovirus 12 early region 1A (2007) Virology, 363 (2), pp. 342-356
  • Morcos, F., Pagnani, A., Lunt, B., Bertolino, A., Marks, D.S., Sander, C., Direct-coupling analysis of residue coevolution captures native contacts across many protein families (2011) Proc. Natl. Acad. Sci. USA, 108 (49), pp. E1293-301
  • Ozenne, V., Bauer, F., Salmon, L., Huang, J.R., Jensen, M.R., Segard, S., Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables (2012) Bioinformatics, 28 (11), pp. 1463-1470
  • Palopoli, N., González Foutel, N.S., Gibson, T.J., Chemes, L.B., Short linear motif core and flanking regions modulate retinoblastoma protein binding affinity and specificity (2018) Protein Eng. Des. Sel., 31 (3), pp. 69-77
  • Pelka, P., Ablack, J.N.G., Fonseca, G.J., Yousef, A.F., Mymryk, J.S., Intrinsic structural disorder in adenovirus E1A: a viral molecular hub linking multiple diverse processes (2008) J. Virol., 82 (15), pp. 7252-7263
  • Perricaudet, M., Akusjärvi, G., Virtanen, A., Pettersson, U., (1979), http://dx.doi.org/10.1038/281694a0, Structure of two spliced mRNAs from the transforming region of human subgroup C adenoviruses; Phelan, C.A., Gampe, R.T., Lambert, M.H., Parks, D.J., Montana, V., Bynum, J., Structure of Rev-erb alpha bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction (2010) Nat. Struct. Mol. Biol., 17 (7), pp. 808-814
  • Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit (2013) Bioinformatics, 29 (7), pp. 845-854
  • Radko, S., Koleva, M., James, K.M.D., Jung, R., Mymryk, J.S., Pelka, P., Adenovirus E1A targets the DREF nuclear factor to regulate virus gene expression, DNA replication, and growth (2014) J. Virol., 88 (22), pp. 13469-13481
  • Radko, S., Jung, R., Olanubi, O., Pelka, P., Effects of adenovirus type 5 E1A isoforms on viral replication in arrested human cells (2015) PLoS One, 10 (10), pp. 1-18
  • Rasti, M., Grand, R.J.A., Mymryk, J.S., Gallimore, P.H., Turnell, A.S., Recruitment of CBP/p300, TATA-binding protein, and S8 to distinct regions at the N terminus of adenovirus E1A (2005) J. Virol., 79 (9), pp. 5594-5605
  • Reddy, V.S., Natchiar, S.K., Stewart, P.L., Nemerow, G.R., Crystal structure of human adenovirus at 3.5 Å resolution (2010) Science (80-), 329 (5995), pp. 1071-1075
  • Rotkiewicz, P., Skolnick, J., Fast procedure for reconstruction of full-atom protein models from reduced representations (2008) J. Comput. Chem., 29 (9), pp. 1460-1465
  • Schaeper, U., Boyd, J.M., Verma, S., Uhlmann, E., Subramanian, T., Chinnadurai, G., Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation (1995) Proc. Natl. Acad. Sci. USA, 92 (23), pp. 10467-10471
  • Schneider, T.D., Stephens, R.M., Sequence logos: a new way to display consensus sequences (1990) Nucleic Acids Res., 18 (20), pp. 6097-6100
  • Schneider, T.D., Stormo, G.D., Gold, L., Ehrenfeucht, A., Information content of binding sites on nucleotide sequences (1986) J. Mol. Biol., 188 (3), pp. 415-431
  • Shapiro, S.S., Wilk, M.B., An analysis of variance test for normality (Complete Samples) (1965) Biometrika, 52 (3), pp. 591-611
  • Singh, M., Krajewski, M., Mikolajka, A., Holak, T.A., Molecular determinants for the complex formation between the retinoblastoma protein and LXCXE sequences (2005) J. Biol. Chem., 280 (45), pp. 37868-37876
  • Sippl, M.J., Wiederstein, M., Detection of spatial correlations in protein structures and molecular complexes (2012) Structure, 20 (4), pp. 718-728
  • Strath, J., Blair, G.E., Adenovirus subversion of immune surveillance, apoptotic and growth regulatory pathways: a Model for tumorigenesis (2006) Acta Microbiol. Immunol. Hung., 53 (2), pp. 145-169
  • Subramanian, T., Kuppuswamy, M., Nasr, R.J., Chinnadurai, G., An N-terminal region of adenovirus E1a essential for cell transformation and induction of an epithelial cell growth factor (1988) Oncogene, 2 (2), pp. 105-112
  • Sułkowska, J.I., Morcos, F., Weigt, M., Hwa, T., Onuchic, J.N., Genomics-aided structure prediction (2012) Proc. Natl. Acad. Sci. USA, 109 (26), pp. 10340-10345
  • Telling, G.C., Williams, J., Constructing chimeric type 12/type 5 adenovirus E1A genes and using them to identify an oncogenic determinant of adenovirus type 12 (1994) J. Virol., 68 (2), pp. 877-887
  • Toth-Petroczy, A., Meszaros, B., Simon, I., Dunker, A.K., Uversky, V.N., Fuxreiter, M., Assessing conservation of disordered regions in proteins (2008) Open Proteom. J., 1 (1), pp. 46-53
  • Toth-Petroczy, A., Palmedo, P., Ingraham, J., Hopf, T.A., Berger, B., Sander, C., Structured states of disordered proteins from genomic sequences (2016) Cell, 167 (1), pp. 158-170. , (e12)
  • Varadi, M., Kosol, S., Lebrun, P., Valentini, E., Blackledge, M., Dunker, A.K., PE-DB: a database of structural ensembles of intrinsically disordered and of unfolded proteins (2014) Nucleic Acids Res., 42 (D1), pp. 326-335
  • Webster, L.C., Zhang, K., Chance, B., Ayene, I., Culp, J.S., Huang, W.J., Conversion of the E1A Cys4 zinc finger to a nonfunctional His2,Cys2 zinc finger by a single point mutation (1991) Proc. Natl. Acad. Sci. USA, 88 (22), pp. 9989-9993
  • Whalen, S.G., Marcellus, R.C., Barbeau, D., Branton, P.E., Importance of the Ser-132 phosphorylation site in cell transformation and apoptosis induced by the adenovirus type 5 E1A protein (1996) J. Virol., 70 (8), pp. 5373-5383
  • Whyte, P., Buchkovich, K.J., Horowitz, J.M., Friend, S.H., Raybuck, M., Weinberg, R.A., Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product (1988) Nature, 334 (6178), pp. 124-129
  • Whyte, P., Ruley, H.E., Harlow, E., Two regions of the adenovirus early region 1A proteins are required for transformation (1988) J. Virol., 62 (1), pp. 257-265
  • Williams, J., Zhang, Y., Williams, M.A., Hou, S., Kushner, D., Ricciardi, R.P., E1A-based determinants of oncogenicity in human adenovirus groups A and C (2004) Curr. Top. Microbiol Immunol., 273, pp. 245-288
  • Wright, P.E., Dyson, H.J., Intrinsically Disordered Proteins in Cellular Signaling and Regulation (2015) Nat. Rev. Mol. Cell Biol., 16 (1), pp. 18-29
  • Zhou, H.X., Quantitative account of the enhanced affinity of two linked scFvs specific for different epitopes on the same antigen (2003) J. Mol. Biol., 329 (3), pp. 1-8
  • Zhou, H.X., Polymer Models of Protein Stability, Folding, and Interactions (2004) Biochemistry, 43 (8), pp. 2141-2154

Citas:

---------- APA ----------
Glavina, J., Román, E.A., Espada, R., de Prat-Gay, G., Chemes, L.B. & Sánchez, I.E. (2018) . Interplay between sequence, structure and linear motifs in the adenovirus E1A hub protein. Virology, 525, 117-131.
http://dx.doi.org/10.1016/j.virol.2018.08.012
---------- CHICAGO ----------
Glavina, J., Román, E.A., Espada, R., de Prat-Gay, G., Chemes, L.B., Sánchez, I.E. "Interplay between sequence, structure and linear motifs in the adenovirus E1A hub protein" . Virology 525 (2018) : 117-131.
http://dx.doi.org/10.1016/j.virol.2018.08.012
---------- MLA ----------
Glavina, J., Román, E.A., Espada, R., de Prat-Gay, G., Chemes, L.B., Sánchez, I.E. "Interplay between sequence, structure and linear motifs in the adenovirus E1A hub protein" . Virology, vol. 525, 2018, pp. 117-131.
http://dx.doi.org/10.1016/j.virol.2018.08.012
---------- VANCOUVER ----------
Glavina, J., Román, E.A., Espada, R., de Prat-Gay, G., Chemes, L.B., Sánchez, I.E. Interplay between sequence, structure and linear motifs in the adenovirus E1A hub protein. Virology. 2018;525:117-131.
http://dx.doi.org/10.1016/j.virol.2018.08.012