Structural and functional insights into a novel homozygous missense pathogenic variant in CUL7 identified in consanguineous Pakistani family

References

• Adzhubei, I. A., Schmidt, S., Peshkin, L., Ramensky, V. E., Gerasimova, A., Bork, P., Kondrashov, A. S., & Sunyaev, S. R. (2010). A method and server for predicting damaging missense mutations. Nature Methods, 7(4), 248–249. https://doi.org/10.1038/nmeth0410-248
   PubMed Web of Science ®Google Scholar
• Akalın, A., Şimşek‐Kiper, P. Ö., Taşkıran, E. Z., Karaosmanoğlu, B., Utine, G. E., & Boduroğlu, K. (2023). A novel biallelic CRIPT variant in a patient with short stature, microcephaly, and distinctive facial features. American Journal of Medical Genetics Part A, 191(4), 1119–1127. https://doi.org/10.1002/ajmg.a.63120
   PubMed Web of Science ®Google Scholar
• Barker, K. (1998). Phenol-chloroform isoamyl alcohol (PCI) DNA extraction. At the Bench.
   Google Scholar
• Cai, W., Nunziata, S., Rascoe, J., & Stulberg, M. J. (2019). SureSelect targeted enrichment, a new cost effective method for the whole genome sequencing of Candidatus Liberibacter asiaticus. Scientific Reports, 9(1), 18962. https://doi.org/10.1038/s41598-019-55144-4
   PubMedGoogle Scholar
• Capriotti, E., & Fariselli, P. (2017). PhD-SNPg: A webserver and lightweight tool for scoring single nucleotide variants. Nucleic Acids Research, 45(W1), W247–W252. https://doi.org/10.1093/nar/gkx369
   PubMed Web of Science ®Google Scholar
• Capriotti, E., Altman, R. B., & Bromberg, Y. (2013). Collective judgment predicts disease-associated single nucleotide variants. BMC Genomics. 14(Suppl 3), S2. https://doi.org/10.1186/1471-2164-14-S3-S2
   PubMedGoogle Scholar
• Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., & Richardson, D. C. (2010). MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallographica. Section D, Biological Crystallography, 66(Pt 1), 12–21. https://doi.org/10.1107/S0907444909042073
   PubMed Web of Science ®Google Scholar
• Clayton, P. E., Hanson, D., Magee, L., Murray, P. G., Saunders, E., Abu‐Amero, S. N., Moore, G. E., & Black, G. C. (2012). Exploring the spectrum of 3‐M syndrome, a primordial short stature disorder of disrupted ubiquitination. Clinical Endocrinology, 77(3), 335–342. https://doi.org/10.1111/j.1365-2265.2012.04428.x
   PubMed Web of Science ®Google Scholar
• Deeb, A., Afandi, O., Attia, S., & El Fatih, A. (2015). 3-M syndrome: A novel CUL7 mutation associated with respiratory distress and a good response to GH therapy. Endocrinology, Diabetes & Metabolism Case Reports, 2015. https://doi.org/10.1530/EDM-15-0012
   Google Scholar
• DeLano, W. L. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter on Protein Crystallography, 40(1), 82–92.
   Google Scholar
• Dias, D. C., Dolios, G., Wang, R., & Pan, Z.-Q. (2002). CUL7: A DOC domain-containing cullin selectively binds Skp1⋅ Fbx29 to form an SCF-like complex. Proceedings of the National Academy of Sciences of the United States of America, 99(26), 16601–16606. https://doi.org/10.1073/pnas.252646399
   PubMed Web of Science ®Google Scholar
• Fairley, S., Lowy-Gallego, E., Perry, E., & Flicek, P. (2020). The International Genome Sample Resource (IGSR) collection of open human genomic variation resources. Nucleic Acids Research, 48(D1), D941–D947. https://doi.org/10.1093/nar/gkz836
   PubMed Web of Science ®Google Scholar
• Güven, A., & Cebeci, A. N. (2011). 3M syndrome: A report of four cases in two families. Journal of Clinical Research in Pediatric Endocrinology, 3(3), 154–159. https://doi.org/10.4274/jcrpe.v3i3.30
   PubMed Web of Science ®Google Scholar
• Hanson, D., Murray, P. G., O'Sullivan, J., Urquhart, J., Daly, S., Bhaskar, S. S., Biesecker, L. G., Skae, M., Smith, C., Cole, T., Kirk, J., Chandler, K., Kingston, H., Donnai, D., Clayton, P. E., & Black, G. C. M. (2011). Exome sequencing identifies CCDC8 mutations in 3-M syndrome, suggesting that CCDC8 contributes in a pathway with CUL7 and OBSL1 to control human growth. American Journal of Human Genetics, 89(1), 148–153. https://doi.org/10.1016/j.ajhg.2011.05.028
   PubMed Web of Science ®Google Scholar
• Hanson, D., Murray, P. G., Sud, A., Temtamy, S. A., Aglan, M., Superti-Furga, A., Holder, S. E., Urquhart, J., Hilton, E., Manson, F. D. C., Scambler, P., Black, G. C. M., & Clayton, P. E. (2009). The primordial growth disorder 3-M syndrome connects ubiquitination to the cytoskeletal adaptor OBSL1. American Journal of Human Genetics, 84(6), 801–806. https://doi.org/10.1016/j.ajhg.2009.04.021
   PubMed Web of Science ®Google Scholar
• Huber, C., Delezoide, A.-L., Guimiot, F., Baumann, C., Malan, V., Le Merrer, M., Da Silva, D. B., Bonneau, D., Chatelain, P., Chu, C., Clark, R., Cox, H., Edery, P., Edouard, T., Fano, V., Gibson, K., Gillessen-Kaesbach, G., Giovannucci-Uzielli, M.-L., Graul-Neumann, L. M., … Cormier-Daire, V. (2009). A large-scale mutation search reveals genetic heterogeneity in 3M syndrome. European Journal of Human Genetics : EJHG, 17(3), 395–400. https://doi.org/10.1038/ejhg.2008.200
   PubMed Web of Science ®Google Scholar
• Huber, C., Dias-Santagata, D., Glaser, A., O'Sullivan, J., Brauner, R., Wu, K., Xu, X., Pearce, K., Wang, R., Uzielli, M. L. G., Dagoneau, N., Chemaitilly, W., Superti-Furga, A., Dos Santos, H., Mégarbané, A., Morin, G., Gillessen-Kaesbach, G., Hennekam, R., Van der Burgt, I., … Cormier-Daire, V. (2005). Identification of mutations in CUL7 in 3-M syndrome. Nature Genetics, 37(10), 1119–1124. https://doi.org/10.1038/ng1628
   PubMed Web of Science ®Google Scholar
• Human Genome Reference Consortium. (n.d). The Human Feb. 2009 Assembly (GRCh37/hg19). http://www.ncbi.nlm.nih.gov/projects/genome/assembly/grc/index.shtml
   Google Scholar
• Isik, E., Arican, D., Atik, T., Ooi, J. E., Darcan, S., Ozen, S., Simsek Kiper, P. O., Utine, E., Cogulu, O., & Ozkinay, F. (2021). A rare cause of syndromic short stature: 3M syndrome in three families. American Journal of Medical Genetics. Part A, 185(2), 461–468. https://doi.org/10.1002/ajmg.a.61989
   PubMed Web of Science ®Google Scholar
• Johnson, A. D., Handsaker, R. E., Pulit, S. L., Nizzari, M. M., O'Donnell, C. J., & de Bakker, P. I. W. (2008). SNAO: A web based tool for identification and annotation of proxy SNPs using hapMap. Bioinformatics (Oxford, England), 24(24), 2938–2939. https://doi.org/10.1093/bioinformatics/btn564
   PubMed Web of Science ®Google Scholar
• Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583–589. https://doi.org/10.1038/s41586-021-03819-2
   PubMed Web of Science ®Google Scholar
• Karczewski, K. J., Francioli, L. C., Tiao, G., Cummings, B. B., Alföldi, J., Wang, Q., Collins, R. L., Laricchia, K. M., Ganna, A., Birnbaum, D. P., Gauthier, L. D., Brand, H., Solomonson, M., Watts, N. A., Rhodes, D., Singer-Berk, M., England, E. M., Seaby, E. G., Kosmicki, J. A., … MacArthur, D. G, (2020). The mutational constraint spectrum quantified from variation in 141,456 humans. Nature, 581(7809), 434–443. https://doi.org/10.1038/s41586-020-2308-7
   PubMed Web of Science ®Google Scholar
• Karczewski, K. J., Weisburd, B., Thomas, B., Solomonson, M., Ruderfer, D. M., Kavanagh, D., Hamamsy, T., Lek, M., Samocha, K. E., Cummings, B. B., Birnbaum, D., Daly, M. J., & MacArthur, D. G. (2017). The ExAC browser: Displaying reference data information from over 60 000 exomes. Nucleic Acids Research, 45(D1), D840–D845. https://doi.org/10.1093/nar/gkw971
   PubMed Web of Science ®Google Scholar
• Khachnaoui-Zaafrane, K., Ouertani, I., Zanati, A., Kandara, H., Maazoul, F., & Mrad, R. (2022). 3M syndrome: A Tunisian seven-cases series. European Journal of Medical Genetics, 65(3), 104448. https://doi.org/10.1016/j.ejmg.2022.104448
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A. (2001). PDBsum: Summaries and analyses of PDB structures. Nucleic Acids Research, 29(1), 221–222. https://doi.org/10.1093/nar/29.1.221
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics (Oxford, England), 25(14), 1754–1760. https://doi.org/10.1093/bioinformatics/btp324
   PubMed Web of Science ®Google Scholar
• López-Blanco, J. R., Aliaga, J. I., Quintana-Ortí, E. S., & Chacón, P. (2014). IMODS: Internal coordinates normal mode analysis server. Nucleic Acids Research, 42(Web Server issue), W271–W276. https://doi.org/10.1093/nar/gku339
   PubMed Web of Science ®Google Scholar
• Lopéz-Blanco, J. R., Garzón, J. I., & Chacón, P. (2011). iMod: Multipurpose normal mode analysis in internal coordinates. Bioinformatics (Oxford, England), 27(20), 2843–2850. https://doi.org/10.1093/bioinformatics/btr497
   PubMed Web of Science ®Google Scholar
• Mahmood, K., Jung, C., Philip, G., Georgeson, P., Chung, J., Pope, B. J., & Park, D. J. (2017). Variant effect prediction tools assessed using independent, functional assay-based datasets: Implications for discovery and diagnostics. Human Genomics, 11(1), 1–8. https://doi.org/10.1186/s40246-017-0104-8
   PubMedGoogle Scholar
• Maksimova, N., Hara, K., Miyashia, A., Nikolaeva, I., Shiga, A., Nogovicina, A., Sukhomyasova, A., Argunov, V., Shvedova, A., Ikeuchi, T., Nishizawa, M., Kuwano, R., & Onodera, O. (2007). Clinical, molecular and histopathological features of short stature syndrome with novel CUL7 mutation in Yakuts: New population isolate in Asia. Journal of Medical Genetics, 44(12), 772–778. https://doi.org/10.1136/jmg.2007.051979
   PubMed Web of Science ®Google Scholar
• Meazza, C., Lausch, E., Pagani, S., Bozzola, E., Calcaterra, V., Superti-Furga, A., Silengo, M., & Bozzola, M. (2013). 3-M syndrome associated with growth hormone deficiency: 18 year follow-up of a patient. Italian Journal of Pediatrics, 39(1), 1–6. https://doi.org/10.1186/1824-7288-39-21
   PubMedGoogle Scholar
• Mehmood, A., Kaushik, A. C., Wang, Q., Li, C.-D., & Wei, D.-Q. (2021). Bringing structural implications and deep learning-based drug identification for KRAS mutants. Journal of Chemical Information and Modeling, 61(2), 571–586. https://doi.org/10.1021/acs.jcim.0c00488
   PubMed Web of Science ®Google Scholar
• Mehmood, A., Nawab, S., Jin, Y., Kaushik, A. C., & Wei, D.-Q. (2023). Mutational impacts on the N and C terminal domains of the MUC5B protein: A transcriptomics and structural biology study. ACS Omega. 8(4), 3726–3735. https://doi.org/10.1021/acsomega.2c04871
   PubMedGoogle Scholar
• Mi, H., Muruganujan, A., Huang, X., Ebert, D., Mills, C., Guo, X., & Thomas, P. D. (2019). Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v. 14.0). Nature Protocols, 14(3), 703–721. https://doi.org/10.1038/s41596-019-0128-8
   PubMed Web of Science ®Google Scholar
• Miller, J. D., McKusick, V. A., Malvaux, P., Temtamy, S., & Salinas, C. (1975). The 3-M syndrome: A heritable low birthweight dwarfism. Birth Defects Original Article Series, 11(5), 39–47.
   PubMedGoogle Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera—A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Sambrook, J., Fritsch, E., & Maniatis, T. (1989). Molecular cloning: A laboratory manual. Cold Spring Harbor, Cold Spring Harbor Laboratory Press.
   Google Scholar
• Sarikas, A., Xu, X., Field, L. J., & Pan, Z.-Q. (2008). The cullin7 E3 ubiquitin ligase: A novel player in growth control. Cell Cycle (Georgetown, Tex.), 7(20), 3154–3161. https://doi.org/10.4161/cc.7.20.6922
   PubMed Web of Science ®Google Scholar
• Schrödinger, LLC. (2019). 1: Desmond Molecular Dynamics System, DE Shaw Research, New York, NY, 2019. Maestro-Desmond Interoperability Tools, Schrödinger.
   Google Scholar
• Schwarz, J. M., Rödelsperger, C., Schuelke, M., & Seelow, D. (2010). MutationTaster evaluates disease-causing potential of sequence alterations. Nature Methods, 7(8), 575–576. https://doi.org/10.1038/nmeth0810-575
   PubMed Web of Science ®Google Scholar
• Shapiro, L., Chatterjee, S., Ramadan, D. G., Davies, K. M., Savage, M. O., Metherell, L. A., & Storr, H. L. (2017). Whole-exome sequencing gives additional benefits compared to candidate gene sequencing in the molecular diagnosis of children with growth hormone or IGF-1 insensitivity. European Journal of Endocrinology, 177(6), 485–501. https://doi.org/10.1530/EJE-17-0453
   PubMed Web of Science ®Google Scholar
• Shaw, D. E., Dror, R. O., Salmon, J. K., Grossman, J., Mackenzie, K. M., Bank, J. A., Young, C., Deneroff, M. M., Batson, B., & Bowers, K. J. (2009). Millisecond-scale molecular dynamics simulations on Anton. (pp. 1–11) [Paper presentation]. https://doi.org/10.1145/1654059.1654126
   Google Scholar
• Sherry, S. T., Ward, M., & Sirotkin, K. (1999). DbSNP—database for single nucleotide polymorphisms and other classes of minor genetic variation. Genome Research, 9(8), 677–679. https://doi.org/10.1101/gr.9.8.677
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Stenson, P. D., Ball, E. V., Mort, M., Phillips, A. D., Shiel, J. A., Thomas, N. S., Abeysinghe, S., Krawczak, M., & Cooper, D. N. (2003). Human gene mutation database (HGMD®): 2003 update. Human Mutation, 21(6), 577–581. https://doi.org/10.1002/humu.10212
   PubMed Web of Science ®Google Scholar
• Szklarczyk, D., Kirsch, R., Koutrouli, M., Nastou, K., Mehryary, F., Hachilif, R., Gable, A. L., Fang, T., Doncheva, N. T., Pyysalo, S., Bork, P., Jensen, L. J., & von Mering, C. (2023). The STRING database in 2023: Protein–protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Research, 51(D1), D638–D646. https://doi.org/10.1093/nar/gkac1000
   PubMed Web of Science ®Google Scholar
• Temtamy, S. A., Aglan, M. S., Ashour, A. M., Ramzy, M. I., Hosny, L. A., & Mostafa, M. I. (2006). 3-M syndrome: A report of three Egyptian cases with review of the literature. Clinical Dysmorphology, 15(2), 55–64. https://doi.org/10.1097/01.mcd.0000198926.01706.33
   PubMed Web of Science ®Google Scholar
• The UniProt Consortium. (2023). UniProt: The Universal Protein knowledgebase in 2023. Nucleic Acids Research, 51(D1), D523–D531.
   PubMed Web of Science ®Google Scholar
• Tong, S.-Y., Fan, K., Zhou, Z.-W., Liu, L.-Y., Zhang, S.-Q., Fu, Y., Wang, G.-Z., Zhu, Y., & Yu, Y.-C. (2022). MvPPT: A highly efficient and sensitive pathogenicity prediction tool for missense variants. Genomics, Proteomics & Bioinformatics. Epub ahead of print. https://doi.org/10.1016/j.gpb.2022.07.005
   Web of Science ®Google Scholar
• Tsutsumi, T., Kuwabara, H., Arai, T., Xiao, Y., & DeCaprio, J. A. (2008). Disruption of the Fbxw8 gene results in pre-and postnatal growth retardation in mice. Molecular and Cellular Biology, 28(2), 743–751. https://doi.org/10.1128/MCB.01665-07
   PubMed Web of Science ®Google Scholar
• Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., & Rozen, S. G. (2012). Primer3—New capabilities and interfaces. Nucleic Acids Research, 40(15), e115. https://doi.org/10.1093/nar/gks596
   PubMed Web of Science ®Google Scholar
• Van Aalten, D. M., De Groot, B. L., Findlay, J. B., Berendsen, H. J., & Amadei, A. (1997). A comparison of techniques for calculating protein essential dynamics. Journal of Computational Chemistry, 18(2), 169–181. https://doi.org/10.1002/(SICI)1096-987X(19970130)18:2<169::AID-JCC3>3.0.CO;2-T
   Web of Science ®Google Scholar
• Van der Auwera, G. A., & O’Connor, B. D. (2020). Genomics in the cloud: Using Docker, GATK, and WDL in Terra. O’Reilly Media.
   Google Scholar
• Van der Wal, G., Otten, B., Brunner, H., & Van der Burgt, I. (2001). 3-M syndrome: Description of six new patients with review of the literature. Clinical Dysmorphology, 10(4), 241–252. https://doi.org/10.1097/00019605-200110000-00002
   PubMed Web of Science ®Google Scholar
• Van Zundert, G., Rodrigues, J., Trellet, M., Schmitz, C., Kastritis, P., Karaca, E., Melquiond, A., van Dijk, M., De Vries, S., & Bonvin, A. (2016). The HADDOCK2. 2 web server: User-friendly integrative modeling of biomolecular complexes. Journal of Molecular Biology, 428(4), 720–725. https://doi.org/10.1016/j.jmb.2015.09.014
   PubMed Web of Science ®Google Scholar
• Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., Žídek, A., Green, T., Tunyasuvunakool, K., Petersen, S., Jumper, J., Clancy, E., Green, R., Vora, A., Lutfi, M., … Velankar, S. (2022). AlphaFold Protein Structure Database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Research, 50(D1), D439–D444. https://doi.org/10.1093/nar/gkab1061
   PubMed Web of Science ®Google Scholar
• Venselaar, H., Te Beek, T. A. H., Kuipers, R. K. P., Hekkelman, M. L., & Vriend, G. (2010). Protein structure analysis of mutations causing inheritable diseases. An e-Science approach with life scientist friendly interfaces. BMC Bioinformatics, 11, 548. https://doi.org/10.1186/1471-2105-11-548
   PubMed Web of Science ®Google Scholar
• Wang, Q., Mehmood, A., Wang, H., Xu, Q., Xiong, Y., & Wei, D.-Q. (2019). Computational screening and analysis of lung cancer related non-synonymous single nucleotide polymorphisms on the human kirsten rat sarcoma gene. Molecules, 24(10), 1951. https://doi.org/10.3390/molecules24101951
   PubMed Web of Science ®Google Scholar
• Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427
   PubMed Web of Science ®Google Scholar
• Wüthrich, K., Wagner, G., Richarz, R., & Braun, W. (1980). Correlations between internal mobility and stability of globular proteins. Biophysical Journal, 32(1), 549–560. https://doi.org/10.1016/S0006-3495(80)84989-7
   PubMed Web of Science ®Google Scholar
• Yu, B., & Zhang, C. (2011). In silico PCR analysis. Methods in Molecular Biology, 760, 91–107.
   PubMedGoogle Scholar