376
Views
31
CrossRef citations to date
0
Altmetric
Research Articles

Measuring the structural impact of mutations on cytochrome P450 21A2, the major steroid 21-hydroxylase related to congenital adrenal hyperplasia

ORCID Icon, ORCID Icon, & ORCID Icon
Pages 1425-1434 | Received 20 Feb 2019, Accepted 09 Apr 2019, Published online: 30 Apr 2019

References

  • Anastasovska, V., Kocova, E., & Kocova, M. (2010). A p.P30L mutation at the CYP21A2 gene in Macedonian patients with nonclassical congenital adrenal hyperplasia. Balkan Journal of Medical Genetics, 13(1), 17–21. https://doi.org/10.2478/v10034-010-0014-8
  • Arnold, K., Bordoli, L., Kopp, J., & Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22(2), 195–201. doi:10.1093/bioinformatics/bti770
  • Bas, D. C., Rogers, D. M., & Jensen, J. H. (2008). Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins 73(3), 765–783. doi:10.1002/prot.22102
  • Benkert, P., Künzli, M., & Schwede, T. (2009). QMEAN server for protein model quality estimation. Nucleic Acids Research, 37(Suppl_2), W510–W514. doi:10.1093/nar/gkp322
  • Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., … Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. doi:10.1002/jcc.20290
  • Castrignanò, T., Chillemi, G., Varani, G., & Desideri, A. (2002). Molecular dynamics simulation of the RNA complex of a double-stranded RNA-binding domain reveals dynamic features of the intermolecular interface and its hydration. Biophysical Journal, 83(6), 3542–3552. doi:10.1016/S0006-3495(02)75354-X
  • Cornell, W. D., Cieplak, P., Bayly, C. I., & Kollman, P. A. (1993). Application of RESP charges to calculate conformational energies, hydrogen bond energies, and free energies of solvation. Journal of the American Chemical Society, 115(21), 9620–9631. doi:10.1021/ja00074a030
  • da Costa, C. H. S., Oliveira, A. R. S., dos Santos, A. M., da Costa, K. S., Lima, A. H. L. E., Alves, C. N., & Lameira, J. (2018). Computational study of conformational changes in human 3-hydroxy-3-methylglutaryl coenzyme reductase induced by substrate binding. Journal of Biomolecular Structure and Dynamics, 1–26. doi:10.1080/07391102.2018.1549508
  • da Costa, K. S., Galúcio, J. M. P., Leonardo, E. S., Cardoso, G., Leal, É., Conde, G., & Lameira, J. (2017). Structural and evolutionary analyses of Leishmania Alba proteins. Molecular and Biochemical Parasitology, 217, 23–31. https://doi.org/10.1016/j.molbiopara.2017.08.006
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N ⋅log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. doi:10.1063/1.464397
  • Deneux, C., Tardy, V., Dib, A., Mornet, E., Billaud, L., Charron, D., … Kuttenn, F. (2001). Phenotype-genotype correlation in 56 women with nonclassical congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Journal of Clinical Endocrinology and Metabolism, 86(1), 207–213. doi:10.1210/jcem.86.1.7131
  • Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., & Baker, N. A. (2004). PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Research, 32(Web Server), W665–W667. doi:10.1093/nar/gkh381
  • Fiser, A., & Sali, A. (2003). Modeller: generation and refinement of homology-based protein structure models. Methods in Enzymology, 374, 461–491. https://doi.org/10.1016/S0076-6879(03)74020-8
  • Fontes, N., Pereira, M., Nascimento, M., Oliveira, E., Espada, F. V., & Fonseca, M. (2012). Hiperplasia congénita da suprarrenal por deficiência de 21-hidroxilase: correlação genótipo-fenótipo. Revista Portuguesa de Endocrinologia, Diabetes e Metabolismo, 7(2), 8–12. doi:10.1016/S1646-3439(12)70003-2
  • Forest, M. G. (2004). Recent advances in the diagnosis and management of congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Human Reproduction Update, 10(6), 469–485. doi:10.1093/humupd/dmh047
  • Forouzanfar, K., Seifi, M., Hashemi-Gorji, F., Karimi, N., Estiar, M. A., Karimoei, M., … Ghergherehchi, R. (2015). Mutation analysis of the CYP21A2 gene in congenital adrenal hyperplasia. Cellular and Molecular Biology (Noisy-Le-Grand, France), 61(4), 51–55. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/26278268
  • Frezza, E., Martin, J., & Lavery, R. (2018). A molecular dynamics study of adenylyl cyclase: The impact of ATP and G-protein binding. PLoS One, 13(4), e0196207. doi:10.1371/journal.pone.0196207
  • Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. doi:10.1517/17460441.2015.1032936
  • Giammona, D. A. (1984). Examination of conformational flexibility in porphyrins and bulky-ligand binding in Myoglobin. Davis, CA: University of California. https://doi.org/10.1074/JBC.272.20.13270
  • Gonçalves, M. A., Santos, L. S., Prata, D. M., Peixoto, F. C., da Cunha, E. F. F., & Ramalho, T. C. (2017). Optimal wavelet signal compression as an efficient alternative to investigate molecular dynamics simulations: application to thermal and solvent effects of MRI probes. Theoretical Chemistry Accounts, 136(1), 15. https://doi.org/10.1007/s00214-016-2037-z
  • Haider, S., Islam, B., D'Atri, V., Sgobba, M., Poojari, C., Sun, L., … New, M. I. (2013). Structure-phenotype correlations of human CYP21A2 mutations in congenital adrenal hyperplasia. Proceedings of the National Academy of Sciences, 110(7), 2605–2610. doi:10.1073/pnas.1221133110
  • Hasemann, C. A., Kurumbail, R. G., Boddupalli, S. S., Peterson, J. A., & Deisenhofer, J. (1995). Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure (London, England: 1993), 3(1), 41–62. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7743131 doi:10.1016/S0969-2126(01)00134-4
  • Hayer-Hartl, M., Bracher, A., & Hartl, F. U. (2016). The GroEL–GroES chaperonin machine: a nano-cage for protein folding. Trends in Biochemical Sciences, 41(1), 62–76. doi:10.1016/j.tibs.2015.07.009
  • Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA Methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. doi:10.1021/ci100275a
  • Izaguirre, J. A., Catarello, D. P., Wozniak, J. M., & Skeel, R. D. (2001). Langevin stabilization of molecular dynamics. The Journal of Chemical Physics, 114(5), 2090–2098. doi:10.1063/1.1332996
  • Krieger, E., Nabuurs, S. B., & Vriend, G. (2005). Homology Modeling. Structural Bioinformatics, 857, 509–523. https://doi.org/10.1002/0471721204.ch25
  • Li, Q., Fang, Y., Li, X., Zhang, H., Liu, M., Yang, H., … Wang, Y. (2013). Mechanism of the plant cytochrome P450 for herbicide resistance: a modelling study. Journal of Enzyme Inhibition and Medicinal Chemistry, 28(6), 1182–1191. doi:10.3109/14756366.2012.719505
  • Li, W., Tang, Y., Hoshino, T., & Neya, S. (2009). Molecular modeling of human cytochrome P450 2W1 and its interactions with substrates. Journal of Molecular Graphics and Modelling, 28(2), 170–176. doi:10.1016/j.jmgm.2009.06.002
  • Ma, D., Chen, Y., Sun, Y., Yang, B., Cheng, J., Huang, M., … Xu, Z. (2014). Molecular analysis of the CYP21A2 gene in Chinese patients with steroid 21-hydroxylase deficiency. Clinical Biochemistry, 47(6), 455–463. doi:10.1016/j.clinbiochem.2014.01.019
  • Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB. Journal of Chemical Theory and Computation, 11(8), 3696–3713. doi:10.1021/acs.jctc.5b00255
  • Marino, R., Ramirez, P., Galeano, J., Perez Garrido, N., Rocco, C., Ciaccio, M., … Belgorosky, A. (2011). Steroid 21-hydroxylase gene mutational spectrum in 454 Argentinean patients: genotype-phenotype correlation in a large cohort of patients with congenital adrenal hyperplasia. Clinical Endocrinology, 75(4), 427–435. doi:10.1111/j.1365-2265.2011.04123.x
  • Mark, P., & Nilsson, L. (2001). Structure and Dynamics of the TIP3P, SPC, and SPC/E Water Models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. doi:10.1021/jp003020w
  • Melo, F., & Feytmans, E. (1998). Assessing protein structures with a non-local atomic interaction energy. Journal of Molecular Biology, 277(5), 1141–1152. doi:10.1006/jmbi.1998.1665
  • Mornet, E., & Gibrat, J. F. (2000). A 3D model of human P450c21: study of the putative effects of steroid 21-hydroxylase gene mutations. Human Genetics, 106(3), 330–339. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10798363
  • Morrison, K. L., & Weiss, G. A. (2001). Combinatorial alanine-scanning. Current Opinion in Chemical Biology, 5(3), 302–307. https://doi.org/10.1016/S1367-5931(00)00206-4 doi:10.1016/S1367-5931(00)00206-4
  • New, M. I., Abraham, M., Gonzalez, B., Dumic, M., Razzaghy-Azar, M., Chitayat, D., … Yuen, T. (2013). Genotype-phenotype correlation in 1,507 families with congenital adrenal hyperplasia owing to 21-hydroxylase deficiency. Proceedings of the National Academy of Sciences, 110(7), 2611–2616. doi:10.1073/pnas.1300057110
  • Pallan, P. S., Wang, C., Lei, L., Yoshimoto, F. K., Auchus, R. J., Waterman, M. R., … Egli, M. (2015). Human Cytochrome P450 21A2, the Major Steroid 21-Hydroxylase. Journal of Biological Chemistry, 290(21), 13128–13143. doi:10.1074/jbc.M115.646307
  • Parajes, S., Quinteiro, C., Domínguez, F., & Loidi, L. (2008). High frequency of copy number variations and sequence variants at CYP21A2 locus: implication for the genetic diagnosis of 21-hydroxylase deficiency. PLoS ONE, 3(5), e2138. doi:10.1371/journal.pone.0002138
  • Pasqualini, T., Alonso, G., Tomasini, R., Galich, A. M., Buzzalino, N., Fernandez, C., … Dain, L. (2007). Congenital adrenal hyperplasia clinical characteristics and genotype in newborn, childhood and adolescence. Medicina, 67(3), 253–261. https://doi.org/17628913
  • Robins, T., Carlsson, J., Sunnerhagen, M., Wedell, A., & Persson, B. (2006). Molecular model of human CYP21 based on mammalian CYP2C5: structural features correlate with clinical severity of mutations causing congenital adrenal hyperplasia. Molecular Endocrinology, 20(11), 2946–2964. doi:10.1210/me.2006-0172
  • Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5 doi:10.1016/0021-9991(77)90098-5
  • Sano, E., Li, W., Yuki, H., Liu, X., Furihata, T., Kobayashi, K., … Hoshino, T. (2010). Mechanism of the decrease in catalytic activity of human cytochrome P450 2C9 polymorphic variants investigated by computational analysis. Journal of Computational Chemistry, 31(15), 2746–2758. doi:10.1002/jcc.21568
  • 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. doi:10.1093/nar/gki387
  • Stikkelbroeck, N. M. M. L., Hoefsloot, L. H., De Wijs, I. J., Otten, B. J., Hermus, A. R. M. M., & Sistermans, E. A. (2003). CYP21 gene mutation analysis in 198 patients with 21-hydroxylase deficiency in the Netherlands: Six novel mutations and a specific cluster of four mutations. Journal of Clinical Endocrinology and Metabolism, 88(8), 3852–3859. doi:10.1210/jc.2002-021681
  • Tusie-Luna, M.-T., Speiser, P. W., Dumic, M., New, M. I., & White, P. C. (1991). A mutation (Pro-30 to Leu) in CYP 21 represents a potential nonclassic steroid 21-hydroxylase deficiency allele. Molecular Endocrinology, 5(5), 685–692. doi:10.1210/mend-5-5-685
  • Vrzalová, Z., Hrubá, Z., St’ahlová Hrabincová, E., Pouchlá, S., Votava, F., Kolousková, S., & Fajkusová, L. (2010). Identification of CYP21A2 mutant alleles in Czech patients with 21-hydroxylase deficiency. International Journal of Molecular Medicine, 26(4), 595–603. https://doi.org/20818501
  • Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. doi:10.1002/jcc.20035
  • White, P. C., & Speiser, P. W. (2000). Congenital adrenal hyperplasia due to 21-hydroxylase deficiency 1. Endocrine Reviews, 21(3), 245–291. doi:10.1210/edrv.21.3.0398
  • Wu, D. A., & Chung, B. C. (1991). Mutations of P450c21 (steroid 21-hydroxylase) at Cys428, Val281, and Ser268 result in complete, partial, or no loss of enzymatic activity, respectively. Journal of Clinical Investigation, 88(2), 519–523. doi:10.1172/JCI115334
  • Zhao, B., Lei, L., Kagawa, N., Sundaramoorthy, M., Banerjee, S., Nagy, L. D., … Waterman, M. R. (2012). Three-dimensional structure of steroid 21-hydroxylase (cytochrome P450 21A2) with two substrates reveals locations of disease-associated variants. Journal of Biological Chemistry, 287(13), 10613–10622. doi:10.1074/jbc.M111.323501

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.