Molecular insights into MYO3A kinase domain variants explain variability in both severity and progression of DFNB30 hearing impairment

References

• Abrusán, G., & Marsh, J. A. (2016). Alpha Helices are morerobust to mutations than beta strands. PLOS ComputationalBiology, 12(12), e1005242. https://doi.org/10.1371/journal.pcbi.1005242
   PubMed Web of Science ®Google Scholar
• An, B. C., Sakai, T., Komaba, S., Kishi, H., Kobayashi, S., Kim, J. Y., Ikebe, R., & Ikebe, M. (2014). Phosphorylation of the kinase domain regulates autophosphorylation of myosin IIIA and its translocation in microvilli. Biochemistry, 53(49), 7835–7845. https://doi.org/10.1021/bi501247z
   PubMed Web of Science ®Google Scholar
• Berg, J. S., Powell, B. C., & Cheney, R. E. (2001). A millennial myosin census. Molecular Biology of the Cell, 12(4), 780–794. https://doi.org/10.1091/mbc.12.4.780
   PubMed Web of Science ®Google Scholar
• Bueno, A. S., Nunes, K., Dias, A. M., Alves, L. U., Mendes, B. C., Sampaio-Silva, J., Smits, J., Yntema, H. G., Meyer, D., Lezirovitz, K., & Mingroni-Netto, R. C. (2021). Frequency and origin of the c.2090T > G p.(Leu697Trp) MYO3A variant associated with autosomal dominant hearing loss. European Journal of Human Genetics. https://doi.org/10.1038/s41431-021-00891-0
   Google Scholar
• Choi, B. Y., Park, G., Gim, J., Kim, A. R., Kim, B.-J., Kim, H.-S., Park, J. H., Park, T., Oh, S.-H., Han, K.-H., & Park, W.-Y. (2013). Diagnostic application of targeted resequencing for familial nonsyndromic hearing loss. PLoS One, 8(8), e68692. https://doi.org/10.1371/journal.pone.0068692
   PubMed Web of Science ®Google Scholar
• Craveur, P., Joseph, A. P., Esque, J., Narwani, T. J., Noël, F., Shinada, N., Goguet, M., Leonard, S., Poulain, P., Bertrand, O., Faure, G., Rebehmed, J., Ghozlane, A., Swapna, L. S., Bhaskara, R. M., Barnoud, J., Téletchéa, S., Jallu, V., Cerny, J., … de Brevern, A. G. (2015). Protein flexibility in the light of structural alphabets. Frontiers in Molecular Biosciences, 2, 20. https://doi.org/10.3389/fmolb.2015.00020
   PubMed Web of Science ®Google Scholar
• Dantas, V. G. L., Raval, M. H., Ballesteros, A., Cui, R., Gunther, L. K., Yamamoto, G. L., Alves, L. U., Bueno, A. S., Lezirovitz, K., Pirana, S., Mendes, B. C. A., Yengo, C. M., Kachar, B., & Mingroni-Netto, R. C. (2018). Characterization of a novel MYO3A missense mutation associated with a dominant form of late onset hearing loss. Scientific Reports, 8(1), 8706. https://doi.org/10.1038/s41598-018-26818-2
   PubMedGoogle Scholar
• Doll, J. (2020). A novel missense variant in MYO3A is associated with autosomal dominant high‐frequency hearing loss in a German family. Molecular Genetics & Genomic Medicine, 8(8), e1343. https://doi.org/10.1002/mgg3.1343
   PubMed Web of Science ®Google Scholar
• Dosé, A. C., & Burnside, B. (2000). Cloning and chromosomal localization of a human class III myosin. Genomics, 67(3), 333–342. https://doi.org/10.1006/geno.2000.6256
   PubMed Web of Science ®Google Scholar
• Dosé, A. C., Hillman, D. W., Wong, C., Sohlberg, L., Lin-Jones, J., & Burnside, B. (2003). Myo3A, one of two class III myosin genes expressed in vertebrate retina, is localized to the calycal processes of rod and cone photoreceptors and is expressed in the sacculus. Molecular Biology of the Cell, 14(3), 1058–1073. https://doi.org/10.1091/mbc.e02-06-0317
   PubMed Web of Science ®Google Scholar
• Gagic, Z., Ruzic, D., Djokovic, N., Djikic, T., & Nikolic, K. (2019). In silico methods for design of kinase inhibitors as anticancer drugs. Frontiers in Chemistry, 7, 873. https://doi.org/10.3389/fchem.2019.00873
   PubMed Web of Science ®Google Scholar
• Gerek, Z. N., Kumar, S., & Ozkan, S. B. (2013). Structural dynamics flexibility informs function and evolution at a proteome scale. Evolutionary Applications, 6(3), 423–433. https://doi.org/10.1111/eva.12052
   PubMed Web of Science ®Google Scholar
• Grati, M., Yan, D., Raval, M. H., Walsh, T., Ma, Q., Chakchouk, I., Kannan-Sundhari, A., Mittal, R., Masmoudi, S., Blanton, S. H., Tekin, M., King, M.-C., Yengo, C. M., & Liu, X. Z. (2016). MYO3A causes human dominant deafness and interacts with protocadherin 15-CD2 isoform. Human Mutation, 37(5), 481–487. https://doi.org/10.1002/humu.22961
   PubMed Web of Science ®Google Scholar
• Jamroz, M., Kolinski, A., & Kmiecik, S. (2014). CABS-flex predictions of protein flexibility compared with NMR ensembles. Bioinformatics (Oxford, England), 30(15), 2150–2154. https://doi.org/10.1093/bioinformatics/btu184
   PubMed Web of Science ®Google Scholar
• Jamroz, M., Orozco, M., Kolinski, A., & Kmiecik, S. (2013). Consistent view of protein fluctuations from all-atom molecular dynamics and coarse-grained dynamics with knowledge-based force-field. Journal of Chemical Theory and Computation, 9(1), 119–125. https://doi.org/10.1021/ct300854w
   PubMed Web of Science ®Google Scholar
• Kurcinski, M., Oleniecki, T., Ciemny, M. P., Kuriata, A., Kolinski, A., & Kmiecik, S. (2019). CABS-flex standalone: A simulation environment for fast modeling of protein flexibility. Bioinformatics (Oxford, England), 35(4), 694–695. https://doi.org/10.1093/bioinformatics/bty685
   PubMed Web of Science ®Google Scholar
• Kuriata, A., Gierut, A. M., Oleniecki, T., Ciemny, M. P., Kolinski, A., Kurcinski, M., & Kmiecik, S. (2018). CABS-flex 2.0: A web server for fast simulations of flexibility of protein structures. Nucleic Acids Research, 46(W1), W338–W343. https://doi.org/10.1093/nar/gky356
   PubMed Web of Science ®Google Scholar
• Lelli, A., Michel, V., Boutet de Monvel, J., Cortese, M., Bosch-Grau, M., Aghaie, A., Perfettini, I., Dupont, T., Avan, P., El-Amraoui, A., & Petit, C. (2016). Class III myosins shape the auditory hair bundles by limiting microvilli and stereocilia growth. The Journal of Cell Biology, 212(2), 231–244. https://doi.org/10.1083/jcb.201509017
   PubMed Web of Science ®Google Scholar
• Li, P., Wen, Z., Zhang, G., Zhang, A., Fu, X., & Gao, J. (2018). Knock-in mice with Myo3a Y137C mutation displayed progressive hearing loss and hair cell degeneration in the inner ear. Neural Plasticity, 2018, 4372913. https://doi.org/10.1155/2018/4372913
   PubMed Web of Science ®Google Scholar
• Likar, T., Hasanhodžić, M., Teran, N., Maver, A., Peterlin, B., & Writzl, K. (2018). Diagnostic outcomes of exome sequencing in patients with syndromic or non-syndromic hearing loss. PLoS One, 13(1), e0188578. https://doi.org/10.1371/journal.pone.0188578
   PubMed Web of Science ®Google Scholar
• Lin-Jones, J., Parker, E., Wu, M., Dosé, A., & Burnside, B. (2004). Myosin 3A transgene expression produces abnormal actin filament bundles in transgenic Xenopus laevis rod photoreceptors. Journal of Cell Science, 117(Pt 24), 5825–5834. https://doi.org/10.1242/jcs.01512
   PubMed Web of Science ®Google Scholar
• Liu, W.-H., Chang, P.-Y., Chang, S.-C., Lu, J.-J., & Wu, C.-M. (2019). Mutation screening in non-syndromic hearing loss patients with cochlear implantation by massive parallel sequencing in Taiwan. PLoS One, 14(1), e0211261. https://doi.org/10.1371/journal.pone.0211261
   PubMed Web of Science ®Google Scholar
• Miyagawa, M., Naito, T., Nishio, S., Kamatani, N., & Usami, S. (2013). Targeted exon sequencing successfully discovers rare causative genes and clarifies the molecular epidemiology of Japanese deafness patients. PLoS One, 8(8), e71381. https://doi.org/10.1371/journal.pone.0071381
   PubMed Web of Science ®Google Scholar
• Morton, C. C., & Nance, W. E. (2006). Newborn hearing screening—A silent revolution. The New England Journal of Medicine, 354(20), 2151–2164. https://doi.org/10.1056/NEJMra050700.
   PubMed Web of Science ®Google Scholar
• Mosaeilhy, A., Mohamed, M. M., Doss, G. P. C., El Abd, H. S. A., Gamal, R., Zaki, O. K., & Zayed, H. (2017). Genotype-phenotype correlation in 18 Egyptian patients with glutaric acidemia type I. Metabolic Brain Disease, 32(5), 1417–1426. https://doi.org/10.1007/s11011-017-0006-4
   PubMed Web of Science ®Google Scholar
• Neveling, K., Feenstra, I., Gilissen, C., Hoefsloot, L. H., Kamsteeg, E.-J., Mensenkamp, A. R., Rodenburg, R. J. T., Yntema, H. G., Spruijt, L., Vermeer, S., Rinne, T., van Gassen, K. L., Bodmer, D., Lugtenberg, D., de Reuver, R., Buijsman, W., Derks, R. C., Wieskamp, N., van den Heuvel, B., … Nelen, M. R. (2013). A post-hoc comparison of the utility of sanger sequencing and exome sequencing for the diagnosis of heterogeneous diseases. Human Mutation, 34(12), 1721–1726. https://doi.org/10.1002/humu.22450
   PubMed Web of Science ®Google Scholar
• Ng, K. P., Kambara, T., Matsuura, M., Burke, M., & Ikebe, M. (1996). Identification of myosin III as a protein kinase. Biochemistry, 35(29), 9392–9399. https://doi.org/10.1021/bi960181a
   PubMed Web of Science ®Google Scholar
• Oza, A. M., DiStefano, M. T., Hemphill, S. E., Cushman, B. J., Grant, A. R., Siegert, R. K., Shen, J., Chapin, A., Boczek, N. J., Schimmenti, L. A., Murry, J. B., Hasadsri, L., Nara, K., Kenna, M., Booth, K. T., Azaiez, H., Griffith, A., Avraham, K. B., Kremer, H., … Abou Tayoun, A. N., ClinGen Hearing Loss Clinical Domain Working Group (2018). Expert specification of the ACMG/AMP variant interpretation guidelines for genetic hearing loss. Human Mutation, 39(11), 1593–1613. https://doi.org/10.1002/humu.23630
   PubMed Web of Science ®Google Scholar
• Panchal, N. K., Bhale, A., Verma, V. K., & Beevi, S. S. (2020). Computational and molecular dynamics simulation approach to analyze the impactof XPD gene mutation on protein stability and function. Molecular Simulation, 46(15), 1200–1219. https://doi.org/10.1080/08927022.2020.1810852
   Web of Science ®Google Scholar
• Pollock, L. M., Chou, S.-W., & McDermott, B. M. (2016). My oh my(osin): insights into how auditory hair cells count, measure, and shape. Journal of Cell Biology, 212(2), 135–137. https://doi.org/10.1083/jcb.201512086
   PubMed Web of Science ®Google Scholar
• Qu, R., Sang, Q., Xu, Y., Feng, R., Jin, L., He, L., & Wang, L. (2016). Identification of a novel homozygous mutation in MYO3A in a Chinese family with DFNB30 non-syndromic hearing impairment. International Journal of Pediatric Otorhinolaryngology, 84, 43–47. https://doi.org/10.1016/j.ijporl.2016.02.036
   PubMed Web of Science ®Google Scholar
• Quintero, O. A., Moore, J. E., Unrath, W. C., Manor, U., Salles, F. T., Grati, M., Kachar, B., & Yengo, C. M. (2010). Intermolecular autophosphorylation regulates myosin IIIa activity and localization in parallel actin bundles. The Journal of Biological Chemistry, 285(46), 35770–35782. https://doi.org/10.1074/jbc.M110.144360
   PubMed Web of Science ®Google Scholar
• Quintero, O. A., Unrath, W. C., Stevens, S. M., Manor, U., Kachar, B., & Yengo, C. M. (2013). Myosin 3A kinase activity is regulated by phosphorylation of the kinase domain activation loop. The Journal of Biological Chemistry, 288(52), 37126–37137. https://doi.org/10.1074/jbc.M113.511014
   PubMed Web of Science ®Google Scholar
• Richards, S., Aziz, N., Bale, S., Bick, D., Das, S., Gastier-Foster, J., Grody, W. W., Hegde, M., Lyon, E., Spector, E., Voelkerding, K., & Rehm, H. L, ACMG Laboratory Quality Assurance Committee (2015). Standards and guidelines for the interpretation of sequence variants: A joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genetics in Medicine, 17(5), 405–424. https://doi.org/10.1038/gim.2015.30
   PubMed Web of Science ®Google Scholar
• Roskoski, R. (2019). Cyclin-dependent protein serine/threonine kinase inhibitors as anticancer drugs. Pharmacological Research, 139, 471–488. https://doi.org/10.1016/j.phrs.2018.11.035
   PubMed Web of Science ®Google Scholar
• Roskoski, R. (2019). Properties of FDA-approved small molecule protein kinase inhibitors. Pharmacological Research, 144, 19–50. https://doi.org/10.1016/j.phrs.2019.03.006
   PubMed Web of Science ®Google Scholar
• Roskoski, R. (2015). A historical overview of protein kinases and their targeted small molecule inhibitors. Pharmacological Research, 100, 1–23. https://doi.org/10.1016/j.phrs.2015.07.010
   PubMed Web of Science ®Google Scholar
• Schneider, M. E., Dosé, A. C., Salles, F. T., Chang, W., Erickson, F. L., Burnside, B., & Kachar, B. (2006). A new compartment at stereocilia tips defined by spatial and temporal patterns of myosin IIIa expression. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(40), 10243–10252. https://doi.org/10.1523/JNEUROSCI.2812-06.2006
   PubMed Web of Science ®Google Scholar
• Sellers, J. R. (2000). Myosins: A diverse superfamily. Biochimica et Biophysica Acta, 1496(1), 3–22. https://doi.org/10.1016/S0167-4889(00)00005-7
   PubMed Web of Science ®Google Scholar
• Shearer, A. E., & Smith, R. J. H. (2015). Massively parallel sequencing for genetic diagnosis of hearing loss: The new standard of care. Otolaryngology–Head and Neck Surgery, 153(2), 175–182. https://doi.org/10.1177/0194599815591156
   PubMed Web of Science ®Google Scholar
• Shinagawa, J. (2020). Prevalence and clinical features of hearing loss caused by EYA4 variants. Scientific Reports, 10, 3662. https://doi.org/10.1038/s41598-020-60259-0
   PubMed Web of Science ®Google Scholar
• Sommen, M., Schrauwen, I., Vandeweyer, G., Boeckx, N., Corneveaux, J. J., van den Ende, J., Boudewyns, A., De Leenheer, E., Janssens, S., Claes, K., Verstreken, M., Strenzke, N., Predöhl, F., Wuyts, W., Mortier, G., Bitner-Glindzicz, M., Moser, T., Coucke, P., Huentelman, M. J., & Van Camp, G. (2016). DNA diagnostics of hereditary hearing loss: A targeted resequencing approach combined with a mutation classification system. Human Mutation, 37(8), 812–819. https://doi.org/10.1002/humu.22999
   PubMed Web of Science ®Google Scholar
• Taylor, S. S., & Kornev, A. P. (2011). Protein kinases: Evolution of dynamic regulatory proteins. Trends in Biochemical Sciences, 36(2), 65–77. https://doi.org/10.1016/j.tibs.2010.09.006
   PubMed Web of Science ®Google Scholar
• Walsh, T., Walsh, V., Vreugde, S., Hertzano, R., Shahin, H., Haika, S., Lee, M. K., Kanaan, M., King, M.-C., & Avraham, K. B. (2002). From flies' eyes to our ears: mutations in a human class III myosin cause progressive nonsyndromic hearing loss DFNB30. Proceedings of the National Academy of Sciences of the United States of America, 99(11), 7518–7523. https://doi.org/10.1073/pnas.102091699
   PubMed Web of Science ®Google Scholar
• Walsh, V. L., Raviv, D., Dror, A. A., Shahin, H., Walsh, T., Kanaan, M. N., Avraham, K. B., & King, M.-C. (2011). A mouse model for human hearing loss DFNB30 due to loss of function of myosin IIIA. Mammalian Genome, 22(3-4), 170–177. https://doi.org/10.1007/s00335-010-9310-6
   PubMed Web of Science ®Google Scholar
• Wu, C.-C., Lin, Y.-H., Liu, T.-C., Lin, K.-N., Yang, W.-S., Hsu, C.-J., Chen, P.-L., & Wu, C.-M. (2015). Identifying children with poor cochlear implantation outcomes using massively parallel sequencing. Medicine, 94(27), e1073. https://doi.org/10.1097/MD.0000000000001073
   PubMed Web of Science ®Google Scholar
• Yang, T., Wei, X., Chai, Y., Li, L., & Wu, H. (2013). Genetic etiology study of the non-syndromic deafness in Chinese Hans by targeted next-generation sequencing. Orphanet Journal of Rare Diseases, 8, 85. https://doi.org/10.1186/1750-1172-8-85
   PubMed Web of Science ®Google Scholar
• Zaki, O. K., Krishnamoorthy, N., El Abd, H. S., Harche, S. A., Mattar, R. A., Al Disi, R. S., Nofal, M. Y., El Bekay, R., Ahmed, K. A., George Priya Doss, C., & Zayed, H. (2017). Two patients with Canavan disease and structural modeling of a novel mutation. Metabolic Brain Disease, 32(1), 171–177. https://doi.org/10.1007/s11011-016-9896-9
   PubMed Web of Science ®Google Scholar
• Zhang, M., Zhou, Q., Luo, Y., Nguyen, T., Rosenblatt, M. I., & Guaiquil, V. H. (2018). Semaphorin3A induces nerve regeneration in the adult cornea-a switch from its repulsive role in development. PLoS One, 13(1), e0191962. https://doi.org/10.1371/journal.pone.0191962
   PubMed Web of Science ®Google Scholar