245
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Structural systems biology approach delineate the functional implications of SNPs in exon junction complex interaction network

ORCID Icon, ORCID Icon &
Pages 11969-11986 | Received 03 Feb 2022, Accepted 26 Dec 2022, Published online: 08 Jan 2023

References

  • Agache, I., Miller, R., Gern, J. E., Hellings, P. W., Jutel, M., Muraro, A., Phipatanakul, W., Quirce, S., & Peden, D. (2019). Emerging concepts and challenges in implementing the exposome paradigm in allergic diseases and asthma: a Practall document. Allergy, 74(3), 449–463. https://doi.org/10.1111/all.13690
  • Ballut, L., Marchadier, B., Baguet, A., Tomasetto, C., Séraphin, B., & Le Hir, H. (2005). The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nature Structural & Molecular Biology, 12(10), 861–869. https://doi.org/10.1038/nsmb990
  • Banerjee, A., & Mitra, P. (2020). Estimating the effect of single-point mutations on protein thermodynamic stability and analyzing the mutation landscape of the p53 protein. Journal of Chemical Information and Modeling, 60(6), 3315–3323. https://doi.org/10.1021/acs.jcim.0c00256
  • Barbosa, I., Haque, N., Fiorini, F., Barrandon, C., Tomasetto, C., Blanchette, M., & Le Hir, H. (2012). Human CWC22 escorts the helicase eIF4AIII to spliceosomes and promotes exon junction complex assembly. Nature Structural & Molecular Biology, 19(10), 983–990. https://doi.org/10.1038/nsmb.2380
  • Bendl, J., Stourac, J., Salanda, O., Pavelka, A., Wieben, E. D., Zendulka, J., Brezovsky, J., & Damborsky, J. (2014). PredictSNP: Robust and accurate consensus classifier for prediction of disease-related mutations. PLoS Computational Biology, 10(1), e1003440. https://doi.org/10.1371/journal.pcbi.1003440
  • Bhagavatham, S. K. S., Pulukool, S. K., Pradhan, S. S., Saiswaroop, R., Naik, A. A., Datta Darshan, V. M., Sivaramakrishnan, V. (2022). Systems biology approach delineates critical Pathways Associated with Disease Progression in Rheumatoid Arthritis. Journal of Biomolecular Structure and Dynamics, 40, 1–22.
  • Bhuvanagiri, M., Schlitter, A. M., Hentze, M. W., & Kulozik, A. E. (2010). NMD: RNA biology meets human genetic medicine. The Biochemical Journal, 430(3), 365–377. https://doi.org/10.1042/BJ20100699
  • Bono, F., Cook, A. G., Grünwald, M., Ebert, J., & Conti, E. (2010). Nuclear import mechanism of the EJC component Mago-Y14 revealed by structural studies of importin 13. Molecular Cell, 37(2), 211–222. https://doi.org/10.1016/j.molcel.2010.01.007
  • Bono, F., Ebert, J., Unterholzner, L., Güttler, T., Izaurralde, E., & Conti, E. (2004). Molecular insights into the interaction of PYM with the Mago–Y14 core of the exon junction complex. EMBO Reports, 5(3), 304–310. https://doi.org/10.1038/sj.embor.7400091
  • Bono, F., & Gehring, N. H. (2011). Assembly, disassembly and recycling: The dynamics of exon junction complexes. RNA Biology, 8(1), 24–29. https://doi.org/10.4161/rna.8.1.13618
  • Bordeira-Carriço, R., Pêgo, A. P., Santos, M., & Oliveira, C. (2012). Cancer syndromes and therapy by stop-codon readthrough. Trends in Molecular Medicine, 18(11), 667–678. https://doi.org/10.1016/j.molmed.2012.09.004
  • Buchwald, G., Ebert, J., Basquin, C., Sauliere, J., Jayachandran, U., Bono, F., Le Hir, H., & Conti, E. (2010). Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proceedings of the National Academy of Sciences of the United States of America, 107(22), 10050–10055. https://doi.org/10.1073/pnas.1000993107
  • Buß, O., Rudat, J., & Ochsenreither, K. (2018). FoldX as protein engineering tool: Better than random based approaches? Computational and Structural Biotechnology Journal, 16, 25–33. https://doi.org/10.1016/j.csbj.2018.01.002
  • Capriotti, E., Fariselli, P., & Casadio, R. (2005). I-Mutant2. 0: Predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Research, 33(Web Server issue), W306–W310. https://doi.org/10.1093/nar/gki375
  • Christensen, N. J., & Kepp, K. P. (2012). Accurate stabilities of laccase mutants predicted with a modified FoldX protocol. Journal of Chemical Information and Modeling, 52(11), 3028–3042. https://doi.org/10.1021/ci300398z
  • Cui, Y., Hagan, K. W., Zhang, S., & Peltz, S. W. (1995). Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes & Development, 9(4), 423–436. https://doi.org/10.1101/gad.9.4.423
  • De Baets, G., Van Durme, J., Reumers, J., Maurer-Stroh, S., Vanhee, P., Dopazo, J., Schymkowitz, J., & Rousseau, F. (2012). SNPeffect 4.0: On-line prediction of molecular and structural effects of protein-coding variants. Nucleic Acids Research, 40(Database issue), D935–D939. https://doi.org/10.1093/nar/gkr996
  • De Oliveira, C. C. S., Pereira, G. R. C., De Alcantara, J. Y. S., Antunes, D., Caffarena, E. R., & De Mesquita, J. F. (2019). In silico analysis of the V66M variant of human BDNF in psychiatric disorders: An approach to precision medicine. PloS One, 14(4), e0215508. https://doi.org/10.1371/journal.pone.0215508
  • De Souza, C., Madden, J., Koestler, D. C., Minn, D., Montoya, D. J., Minn, K., Raetz, A. G., Zhu, Z., Xiao, W.-W., Tahmassebi, N., Reddy, H., Nelson, N., Karnezis, A. N., & Chien, J. (2021). Effect of the p53 P72R polymorphism on mutant TP53 allele selection in human cancer. Journal of the National Cancer Institute, 113(9), 1246–1257. https://doi.org/10.1093/jnci/djab019
  • Dehouck, Y., Kwasigroch, J. M., Gilis, D., & Rooman, M. (2011). PoPMuSiC 2.1: A web server for the estimation of protein stability changes upon mutation and sequence optimality. BMC Bioinformatics, 12, 151–112. https://doi.org/10.1186/1471-2105-12-151
  • Gatfield, D., Unterholzner, L., Ciccarelli, F. D., Bork, P., & Izaurralde, E. (2003). Nonsense-mediated mRNA decay in Drosophila: At the intersection of the yeast and mammalian pathways. The EMBO Journal, 22(15), 3960–3970. https://doi.org/10.1093/emboj/cdg371
  • Gehring, N. H., Kunz, J. B., Neu-Yilik, G., Breit, S., Viegas, M. H., Hentze, M. W., & Kulozik, A. E. (2005). Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Molecular Cell, 20(1), 65–75. https://doi.org/10.1016/j.molcel.2005.08.012
  • Gehring, N. H., Lamprinaki, S., Hentze, M. W., & Kulozik, A. E. (2009). The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biology, 7(5), e1000120. https://doi.org/10.1371/journal.pbio.1000120
  • Gehring, N. H., Lamprinaki, S., Kulozik, A. E., & Hentze, M. W. (2009). Disassembly of exon junction complexes by PYM. Cell, 137(3), 536–548. https://doi.org/10.1016/j.cell.2009.02.042
  • Genomes Project Consortium. (2012). An integrated map of genetic variation from 1,092 human genomes. Nature, 491, 56–65.
  • Gerasimavicius, L., Liu, X., & Marsh, J. A. (2020). Identification of pathogenic missense mutations using protein stability predictors. Scientific Reports, 10(1), 1–10. https://doi.org/10.1038/s41598-020-72404-w
  • Gromiha, M. M. (2007). Prediction of protein stability upon point mutations. Biochemical Society Transactions, 35(Pt 6), 1569–1573. https://doi.org/10.1042/BST0351569
  • Han, S., Yang, B.-Z., Kranzler, H. R., Liu, X., Zhao, H., Farrer, L. A., Boerwinkle, E., Potash, J. B., & Gelernter, J. (2013). Integrating GWASs and human protein interaction networks identifies a gene subnetwork underlying alcohol dependence. American Journal of Human Genetics, 93(6), 1027–1034. https://doi.org/10.1016/j.ajhg.2013.10.021
  • He, F., Brown, A. H., & Jacobson, A. (1997). Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Molecular and Cellular Biology, 17(3), 1580–1594. https://doi.org/10.1128/MCB.17.3.1580
  • Hegele, A., Kamburov, A., Grossmann, A., Sourlis, C., Wowro, S., Weimann, M., Will, C. L., Pena, V., Lührmann, R., & Stelzl, U. (2012). Dynamic protein-protein interaction wiring of the human spliceosome. Molecular Cell, 45(4), 567–580. https://doi.org/10.1016/j.molcel.2011.12.034
  • Hir, H., Le, Saulière, J., & Wang, Z. (2016). The exon junction complex as a node of post-transcriptional networks. Nature Reviews. Molecular Cell Biology, 17(1), 41–54. https://doi.org/10.1038/nrm.2015.7
  • Isken, O., & Maquat, L. E. (2008). The multiple lives of NMD factors: Balancing roles in gene and genome regulation. Nature Reviews. Genetics, 9(9), 699–712. https://doi.org/10.1038/nrg2402
  • Jensen, M. K., Pers, T. H., Dworzynski, P., Girman, C. J., Brunak, S., & Rimm, E. B. (2011). Protein interaction-based genome-wide analysis of incident coronary heart disease. Circulation. Cardiovascular Genetics, 4(5), 549–556. https://doi.org/10.1161/CIRCGENETICS.111.960393
  • Kadlec, J., Izaurralde, E., & Cusack, S. (2004). The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nature Structural & Molecular Biology, 11(4), 330–337. https://doi.org/10.1038/nsmb741
  • Karchin, R. (2009). Next generation tools for the annotation of human SNPs. Briefings in Bioinformatics, 10(1), 35–52. https://doi.org/10.1093/bib/bbn047
  • Keeling, K. M., & Bedwell, D. M. (2011). Suppression of nonsense mutations as a therapeutic approach to treat genetic diseases. Wiley Interdisciplinary Reviews. RNA, 2(6), 837–852. https://doi.org/10.1002/wrna.95
  • Kerr, T. P., Sewry, C. A., Robb, S. A., & Roberts, R. G. (2001). Long mutant dystrophins and variable phenotypes: Evasion of nonsense-mediated decay? Human Genetics, 109(4), 402–407. https://doi.org/10.1007/s004390100598
  • Kiel, C., & Serrano, L. (2014). Structure‐energy‐based predictions and network modelling of RAS opathy and cancer missense mutations. Molecular Systems Biology, 10(5), 727. https://doi.org/10.1002/msb.20145092
  • Kunz, J. B., Neu-Yilik, G., Hentze, M. W., Kulozik, A. E., & Gehring, N. H. (2006). Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA (New York, N.Y.), 12(6), 1015–1022. https://doi.org/10.1261/rna.12506
  • Kwasigroch, J. M., Gilis, D., Dehouck, Y., & Rooman, M. (2002). PoPMuSiC, rationally designing point mutations in protein structures. Bioinformatics (Oxford, England), 18(12), 1701–1702. https://doi.org/10.1093/bioinformatics/18.12.1701
  • Linde, L., & Kerem, B. (2008). Introducing sense into nonsense in treatments of human genetic diseases. Trends in Genetics : TIG, 24(11), 552–563. https://doi.org/10.1016/j.tig.2008.08.010
  • Liu, Q., Xun, G., & Feng, Y. (2019). The state-of-the-art strategies of protein engineering for enzyme stabilization. Biotechnology Advances, 37(4), 530–537. https://doi.org/10.1016/j.biotechadv.2018.10.011
  • Mendell, J. T., Sharifi, N. A., Meyers, J. L., Martinez-Murillo, F., & Dietz, H. C. (2004). Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nature Genetics, 36(10), 1073–1078. https://doi.org/10.1038/ng1429
  • Mingot, J.-M., Kostka, S., Kraft, R., Hartmann, E., & Görlich, D. (2001). Importin 13: A novel mediator of nuclear import and export. The EMBO Journal, 20(14), 3685–3694. https://doi.org/10.1093/emboj/20.14.3685
  • Moldovean, S. N., & Chiş, V. (2020). Molecular dynamics simulations applied to structural and dynamical transitions of the Huntingtin protein: A review. ACS Chemical Neuroscience, 11(2), 105–120. https://doi.org/10.1021/acschemneuro.9b00561
  • Montojo, J., Zuberi, K., Rodriguez, H., Kazi, F., Wright, G., Donaldson, S. L., Morris, Q., & Bader, G. D. (2010). GeneMANIA Cytoscape plugin: Fast gene function predictions on the desktop. Bioinformatics (Oxford, England), 26(22), 2927–2928. https://doi.org/10.1093/bioinformatics/btq562
  • Naik, A. A., Narayanan, A., Khanchandani, P., Sridharan, D., Sukumar, P., Srimadh Bhagavatam, S. K., Seshagiri, P. B., & Sivaramakrishnan, V. (2020). Systems analysis of avascular necrosis of femoral head using integrative data analysis and literature mining delineates pathways associated with disease. Scientific Reports, 10(1), 1–20. https://doi.org/10.1038/s41598-020-75197-0
  • Naik, A. A., & Sivaramakrishnan, V. (2021). Systems analysis of steroid induced osteonecrosis shows role for heme and vitamin D in pathogenesis. Gene Reports, 25, 101383. https://doi.org/10.1016/j.genrep.2021.101383
  • Neu-Yilik, G., Amthor, B., Gehring, N. H., Bahri, S., Paidassi, H., Hentze, M. W., & Kulozik, A. E. (2011). Mechanism of escape from nonsense-mediated mRNA decay of human β-globin transcripts with nonsense mutations in the first exon. RNA (New York, N.Y.), 17(5), 843–854. https://doi.org/10.1261/rna.2401811
  • Ng, P. C., & Henikoff, S. (2001). Predicting deleterious amino acid substitutions. Genome Research, 11(5), 863–874. https://doi.org/10.1101/gr.176601
  • Pejaver, V., Urresti, J., Lugo-Martinez, J., Pagel, K. A., Lin, G. N., Nam, H.-J., Mort, M., Cooper, D. N., Sebat, J., Iakoucheva, L. M., Mooney, S. D., & Radivojac, P. (2020). Inferring the molecular and phenotypic impact of amino acid variants with MutPred2. Nature Communications, 11(1), 1–13. https://doi.org/10.1038/s41467-020-19669-x
  • Perrin-Vidoz, L., Sinilnikova, O. M., Stoppa-Lyonnet, D., Lenoir, G. M., & Mazoyer, S. (2002). The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Human Molecular Genetics, 11(23), 2805–2814. https://doi.org/10.1093/hmg/11.23.2805
  • Pradhan, S. S. (2022). Integrated multi-omic analysis of Huntington disease and yeast model delineates pathways modulating protein aggregation. Disease Models & Mechanisms, 15(10), 1–20.
  • Prokunina, L., & Alarcón-Riquelme, M. E. (2004). Regulatory SNPs in complex diseases: Their identification and functional validation. Expert Reviews in Molecular Medicine, 6(10), 1–15. https://doi.org/10.1017/S1462399404007690
  • Pulukool, S. K., Bhagavatham, S. K. S., Kannan, V., Sukumar, P., Dandamudi, R. B., Ghaisas, S., Kunchala, H., Saieesh, D., Naik, A. A., Pargaonkar, A., Sharma, A., & Sivaramakrishnan, V. (2021). Elevated dimethylarginine, ATP, cytokines, metabolic remodeling involving tryptophan metabolism and potential microglial inflammation characterize primary open angle glaucoma. Scientific Reports, 11(1), 1–19. https://doi.org/10.1038/s41598-021-89137-z
  • Rakoczy, E. P., Kiel, C., McKeone, R., Stricher, F., & Serrano, L. (2011). Analysis of disease-linked rhodopsin mutations based on structure, function, and protein stability calculations. Journal of Molecular Biology, 405(2), 584–606. https://doi.org/10.1016/j.jmb.2010.11.003
  • Ramensky, V., Bork, P., & Sunyaev, S. (2002). Human non‐synonymous SNPs: Server and survey. Nucleic Acids Research, 30(17), 3894–3900. https://doi.org/10.1093/nar/gkf493
  • Sai Swaroop, R., Akhil, P. S., Sai Sanwid, P., Bandana, P., Raksha, R. K., Meghana, M., Bibha, C., & Sivaramakrishnan, V. (2022). Integrated multi-omic data analysis and validation with yeast model show oxidative phosphorylation modulates protein aggregation in amyotrophic lateral sclerosis. Journal of Biomolecular Structure and Dynamics, 1(20), 1–20. https://doi.org/10.1080/07391102.2022.2090441
  • Saltzman, A. L., Kim, Y. K., Pan, Q., Fagnani, M. M., Maquat, L. E., & Blencowe, B. J. (2008). Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Molecular and Cellular Biology, 28(13), 4320–4330. https://doi.org/10.1128/MCB.00361-08
  • Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F., & Serrano, L. (2005). The FoldX web server: An online force field. Nucleic Acids Research, 33(Web Server), W382–W388. https://doi.org/10.1093/nar/gki387
  • Scott, M. A., Woolums, A. R., Swiderski, C. E., Perkins, A. D., Nanduri, B., Smith, D. R., Karisch, B. B., Epperson, W. B., & Blanton, J. R. (2020). Whole blood transcriptomic analysis of beef cattle at arrival identifies potential predictive molecules and mechanisms that indicate animals that naturally resist bovine respiratory disease. PloS One, 15(1), e0227507. https://doi.org/10.1371/journal.pone.0227507
  • Shibuya, T., Tange, T. Ø., Sonenberg, N., & Moore, M. J. (2004). eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nature Structural & Molecular Biology, 11(4), 346–351. https://doi.org/10.1038/nsmb750
  • Shibuya, T., Tange, T. Ø., Stroupe, M. E., & Moore, M. J. (2006). Mutational analysis of human eIF4AIII identifies regions necessary for exon junction complex formation and nonsense-mediated mRNA decay. RNA (New York, N.Y.), 12(3), 360–374. https://doi.org/10.1261/rna.2190706
  • Sim, N.-L., Kumar, P., Hu, J., Henikoff, S., Schneider, G., & Ng, P. C. (2012). SIFT web server: Predicting effects of amino acid substitutions on proteins. Nucleic Acids Research, 40(Web Server Issue), W452–W457. https://doi.org/10.1093/nar/gks539
  • Singh, G., Kucukural, A., Cenik, C., Leszyk, J. D., Shaffer, S. A., Weng, Z., & Moore, M. J. (2012). The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell, 151(4), 750–764. https://doi.org/10.1016/j.cell.2012.10.007
  • Slayton, R. L., Deschenes, S. P., & Willing, M. C. (2000). Nonsense mutations in the COL1A1 gene preferentially reduce nuclear levels of mRNA but not hnRNA in osteogenesis imperfecta type I cell strains. Matrix Biology : Journal of the International Society for Matrix Biology, 19(1), 1–9. https://doi.org/10.1016/s0945-053x(99)00056-6
  • Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P.-L., & Ideker, T. (2011). Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics (Oxford, England), 27(3), 431–432. https://doi.org/10.1093/bioinformatics/btq675
  • Soremekun, O. S., & Soliman, M. E. S. (2019). From genomic variation to protein aberration: Mutational analysis of single nucleotide polymorphism present in ULBP6 gene and implication in immune response. Computers in Biology and Medicine, 111, 103354. https://doi.org/10.1016/j.compbiomed.2019.103354
  • Steckelberg, A.-L., Boehm, V., Gromadzka, A. M., & Gehring, N. H. (2012). CWC22 connects pre-mRNA splicing and exon junction complex assembly. Cell Reports, 2(3), 454–461. https://doi.org/10.1016/j.celrep.2012.08.017
  • Stransky, N., Egloff, A. M., Tward, A. D., Kostic, A. D., Cibulskis, K., Sivachenko, A., Kryukov, G. V., Lawrence, M. S., Sougnez, C., McKenna, A., Shefler, E., Ramos, A. H., Stojanov, P., Carter, S. L., Voet, D., Cortés, M. L., Auclair, D., Berger, M. F., Saksena, G., … Grandis, J. R. (2011). The mutational landscape of head and neck squamous cell carcinoma. Science (80-), 333(6046), 1157–1160. https://doi.org/10.1126/science.1208130
  • Tarpey, P. S., Raymond, F. L., Nguyen, L. S., Rodriguez, J., Hackett, A., Vandeleur, L., Smith, R., Shoubridge, C., Edkins, S., Stevens, C., O'Meara, S., Tofts, C., Barthorpe, S., Buck, G., Cole, J., Halliday, K., Hills, K., Jones, D., Mironenko, T., … Gécz, J. (2007). Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nature Genetics, 39(9), 1127–1133.
  • Tate, J. G., Bamford, S., Jubb, H. C., Sondka, Z., Beare, D. M., Bindal, N., Boutselakis, H., Cole, C. G., Creatore, C., Dawson, E., Fish, P., Harsha, B., Hathaway, C., Jupe, S. C., Kok, C. Y., Noble, K., Ponting, L., Ramshaw, C. C., Rye, C. E., … Forbes, S. A. (2019). COSMIC: The catalogue of somatic mutations in cancer. Nucleic Acids Research, 47(D1), D941–D947. https://doi.org/10.1093/nar/gky1015
  • Van Durme, J., Delgado, J., Stricher, F., Serrano, L., Schymkowitz, J., & Rousseau, F. (2011). A graphical interface for the FoldX forcefield. Bioinformatics (Oxford, England), 27(12), 1711–1712. https://doi.org/10.1093/bioinformatics/btr254
  • Vogelsang, M., & Komel, R. (2011). Non-truncating hMLH1 variants identified in Slovenian gastric cancer patients are not associated with Lynch Syndrome: A functional analysis report. Familial Cancer, 10(2), 255–263. https://doi.org/10.1007/s10689-010-9409-7
  • Wang, W., Czaplinski, K., Rao, Y., & Peltz, S. W. (2001). The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. The EMBO Journal, 20(4), 880–890. https://doi.org/10.1093/emboj/20.4.880
  • Weng, Y., Czaplinski, K., & Peltz, S. W. (1996). Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Molecular and Cellular Biology, 16(10), 5477–5490. https://doi.org/10.1128/MCB.16.10.5477

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.