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Research Articles

Structure and dynamics of major histocompatibility class Ib molecule H2-M3 complexed with mitochondrial-derived peptides

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 10300-10312 | Received 25 Jan 2021, Accepted 07 Jun 2021, Published online: 28 Jun 2021

References

  • Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., & Zwart, P. H. (2010). PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica. Section D, Biological Crystallography, 66(Pt 2), 213–221. https://doi.org/10.1107/S0907444909052925
  • Adams, E. J., & Luoma, A. M. (2013). The adaptable major histocompatibility complex (MHC) fold: Structure and function of nonclassical and MHC class I-like molecules. Annual Review of Immunology, 31, 529–561. https://doi.org/10.1146/annurev-immunol-032712-095912
  • Ayres, C. M., Corcelli, S. A., & Baker, B. M. (2017). Peptide and peptide-dependent motions in MHC proteins: Immunological implications and biophysical underpinnings. Frontiers in Immunology, 8, 935. https://doi.org/10.3389/fimmu.2017.00935
  • Bayly, C. I., Cieplak, P., Cornell, W., & Kollman, P. A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. The Journal of Physical Chemistry, 97(40), 10269–10280. https://doi.org/10.1021/j100142a004
  • BioHPC. (n.d.). BioHPC Supercomputing Facility. Retrieved from https://portal.biohpc.swmed.edu
  • Bunch, T. A., Grinblat, Y., & Goldstein, L. S. B. (1988). Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res, 16(3), 1043–1061. https://doi.org/10.1093/nar/16.3.1043
  • Case, D. A., Berryman, J. T., Betz, R. M., Cerutti, D. S., Cheatham, T. E., & Darden, T. A. & (2015). AMBER 14. University of California.
  • 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
  • Dabhi, V. M., & Lindahl, K. F. (1995). MtDNA-encoded histocompatibility antigens. Methods in Enzymology, 260, 466–485. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/8592468 https://doi.org/10.1016/0076-6879(95)60159-7
  • Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010). Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography, 66(Pt 4), 486–501. https://doi.org/10.1107/S0907444910007493
  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., & Cheeseman, J. R. & (2009). Gaussian 09, Revision D.01. Gaussian, Inc.
  • Frishman, D., & Argos, P. (1995). Knowledge-based protein secondary structure assignment. Proteins, 23(4), 566–579. https://doi.org/10.1002/prot.340230412
  • Gee, M. H., Sibener, L. V., Birnbaum, M. E., Jude, K. M., Yang, X., Fernandes, R. A., Mendoza, J. L., Glassman, C. R., & Garcia, K. C. (2018). Stress-testing the relationship between T cell receptor/peptide-MHC affinity and cross-reactivity using peptide velcro. Proceedings of the National Academy of Sciences of the United States of America, 115(31), E7369–E7378. https://doi.org/10.1073/pnas.1802746115
  • Hawkins, G. D., Cramer, C. J., & Truhlar, D. G. (1996). Parametrized models of aqueous free energies of solvation based on pairwise descreening of Solute atomic charges from a dielectric medium. The Journal of Physical Chemistry, 100(51), 19824–19839. https://doi.org/10.1021/jp961710n
  • Hou, T. J., Wang, J. M., Li, Y. 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. https://doi.org/10.1021/ci100275a
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38, 27–38. https://doi.org/10.1016/0263-7855(96)00018-5
  • Jackson, M. R., Song, E. S., Yang, Y., & Peterson, P. A. (1992). Empty and peptide-containing conformers of class I major histocompatibility complex molecules expressed in Drosophila melanogaster cells. Proceedings of the National Academy of Sciences, 89(24), 12117–12121. https://doi.org/10.1073/pnas.89.24.12117
  • Jones, T. A., Zou, J.-Y., Cowan, S. W., & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallographica, A47, 110–119.
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
  • Kass, I., Buckle, A. M., & Borg, N. A. (2014). Understanding the structural dynamics of TCR-pMHC complex interactions. Trends in Immunology, 35(12), 604–612. https://doi.org/10.1016/j.it.2014.10.005
  • Klueg, K. M., Alvarado, D., Muskavitch, M. A., & Duffy, J. B. (2002). Creation of a GAL4/UAS-coupled inducible gene expression system for use in Drosophila cultured cell lines. Genesis (New York, N.Y.: 2000), 34(1-2), 119–122. https://doi.org/10.1002/gene.10148
  • Knapp, B., Demharter, S., Esmaielbeiki, R., & Deane, C. M. (2015). Current status and future challenges in T-cell receptor/peptide/MHC molecular dynamics simulations. Briefings in Bioinformatics, 16(6), 1035–1044. https://doi.org/10.1093/bib/bbv005
  • Knapp, B., Dunbar, J., & Deane, C. M. (2014). Large scale characterization of the LC13 TCR and HLA-B8 structural landscape in reaction to 172 altered peptide ligands: A molecular dynamics simulation study. PLoS Computational Biology, 10(8), e1003748 https://doi.org/10.1371/journal.pcbi.1003748
  • Knapp, B., Omasits, U., Schreiner, W., & Epstein, M. M. (2010). A comparative approach linking molecular dynamics of altered peptide ligands and MHC with in vivo immune responses. PLoS One, 5(7), e11653. https://doi.org/10.1371/journal.pone.0011653
  • Knapp, B., Ospina, L., & Deane, C. M. (2018). Avoiding false positive conclusions in molecular simulation: The importance of replicas. Journal of Chemical Theory and Computation, 14(12), 6127–6138. https://doi.org/10.1021/acs.jctc.8b00391
  • Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham, T. E. 3rd. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
  • Li, C., Li, L., Zhang, J., & Alexov, E. (2012). Highly efficient and exact method for parallelization of grid-based algorithms and its implementation in DelPhi. Journal of Computational Chemistry, 33(24), 1960–1966. https://doi.org/10.1002/jcc.23033
  • Lindahl, K. F., Hausmann, B., & Chapman, V. M. (1983). A new H-2-linked class I gene whose expression depends on a maternally inherited factor. Nature, 306(5941), 383–385. https://doi.org/10.1038/306383a0
  • Lindahl, K. F., Hausmann, B., & Guenet, J. L. (1990). Variants of Mta, the mouse maternally transmitted antigen, determined by three alleles of the extrachromosomal gene Mtf. Journal of Immunogenetics, 17(1-2), 29–41. https://doi.org/10.1111/j.1744-313x.1990.tb00857.x
  • Linehan, J. L., Harrison, O. J., Han, S.-J., Byrd, A. L., Vujkovic-Cvijin, I., Villarino, A. V., Sen, S. K., Shaik, J., Smelkinson, M., Tamoutounour, S., Collins, N., Bouladoux, N., Dzutsev, A., Rosshart, S. P., Arbuckle, J. H., Wang, C.-R., Kristie, T. M., Rehermann, B., Trinchieri, G., … Belkaid, Y. (2018). Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell, 172(4), 784–796. e718. https://doi.org/10.1016/j.cell.2017.12.033
  • Loveland, B., Wang, C. R., Yonekawa, H., Hermel, E., & Lindahl, K. F. (1990). Maternally transmitted histocompatibility antigen of mice: A hydrophobic peptide of a mitochondrially encoded protein. Cell, 60(6), 971–980. https://doi.org/10.1016/0092-8674(90)90345-F
  • MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., … Karplus, M. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. The Journal of Physical Chemistry B, 102(18), 3586–3616. https://doi.org/10.1021/jp973084f
  • MacKerell, A. D., Jr., Feig, M., & Brooks, C. L. 3rd. (2004). Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. Journal of Computational Chemistry, 25(11), 1400–1415. https://doi.org/10.1002/jcc.20065
  • Madden, D. R., Gorga, J. C., Strominger, J. L., & Wiley, D. C. (1992). The three-dimensional structure of HLA-B27 at 2.1 Å resolution suggests a general mechanism for tight peptide binding to MHC. Cell, 70(6), 1035–1048. https://doi.org/10.1016/0092-8674(92)90252-8
  • 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. https://doi.org/10.1021/acs.jctc.5b00255 PubMed PMID: 26574453; PubMed Central PMCID: PMCPMC4821407.
  • Mariuzza, R. A., Agnihotri, P., & Orban, J. (2020). The structural basis of T-cell receptor (TCR) activation: An enduring enigma. The Journal of Biological Chemistry, 295(4), 914–925. https://doi.org/10.1074/jbc.REV119.009411
  • McCammon, J. A., Gelin, B. R., & Karplus, M. (1977). Dynamics of folded proteins. Nature, 267(5612), 585–590.
  • Morse, M. C., Bleau, G., Dabhi, V. M., Hetu, F., Drobetsky, E. A., Lindahl, K. F., & Perreault, C. (1996). The COI mitochondrial gene encodes a minor histocompatibility antigen presented by H2-M3. Journal of Immunology (Baltimore, MD.: 1950), 156(9), 3301–3307. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/8617953
  • Narzi, D., Becker, C. M., Fiorillo, M. T., Uchanska-Ziegler, B., Ziegler, A., & Bockmann, R. A. (2012). Dynamical characterization of two differentially disease associated MHC class I proteins in complex with viral and self-peptides. Journal of Molecular Biology, 415(2), 429–442. https://doi.org/10.1016/j.jmb.2011.11.021
  • Natarajan, K., Jiang, J., May, N. A., Mage, M. G., Boyd, L. F., McShan, A. C., Sgourakis, N. G., Bax, A., & Margulies, D. H. (2018). The role of molecular flexibility in antigen presentation and T cell receptor-mediated signaling. Frontiers in Immunology, 9, 1657. https://doi.org/10.3389/fimmu.2018.01657
  • Navaza, J. (1994). AMoRe: An automated package for molecular replacement. Acta Crystallographica Section A Foundations of Crystallography, 50(2), 157–163. https://doi.org/10.1107/S0108767393007597
  • Otwinowski, Z., & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology, 276, 307–326.
  • Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005). Scalable molecular dynamics with NAMD. J Comput Chem, 26(16), 1781–1802. https://doi.org/10.1002/jcc.20289
  • RCoreTeam. (2016). R: A language and environment for statistical computing. Retrieved from https://www.R-project.org
  • Rognan, D., Zimmermann, N., Jung, G., & Folkers, G. (1992). Molecular dynamics study of a complex between the human histocompatibility antigen HLA-A2 and the IMP58-66 nonapeptide from influenza virus matrix protein. European Journal of Biochemistry, 208(1), 101–113. https://doi.org/10.1111/j.1432-1033.1992.tb17163.x
  • Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. C. (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
  • Shen, S.-T. (2004). Structural Studies of major histocompatibility class Ib molecule H2-M3 complexed with peptides [Ph.D. Thesis]. University of Texas Southwestern Medical Center.
  • Sibener, L. V., Fernandes, R. A., Kolawole, E. M., Carbone, C. B., Liu, F., McAffee, D., Birnbaum, M. E., Yang, X., Su, L. F., Yu, W., Dong, S., Gee, M. H., Jude, K. M., Davis, M. M., Groves, J. T., Goddard, W. A., Heath, J. R., Evavold, B. D., Vale, R. D., & Garcia, K. C. (2018). Isolation of a structural mechanism for uncoupling T cell receptor signaling from peptide-MHC binding. Cell, 174(3), 672–687.e627. https://doi.org/10.1016/j.cell.2018.06.017
  • Sitkoff, D., Sharp, K. A., & Honig, B. (1994). Accurate calculation of hydration free energies using macroscopic solvent models. The Journal of Physical Chemistry, 98(7), 1978–1988. https://doi.org/10.1021/j100058a043
  • Smith, A. R., Alonso, J. A., Ayres, C. M., Singh, N. K., Hellman, L. M., & Baker, B. M. (2021). Structurally silent peptide anchor modifications allosterically modulate T cell recognition in a receptor-dependent manner. Proceedings of the National Academy of Sciences of the United States of America, 118(4). https://doi.org/10.1073/pnas.2018125118
  • Stavrakoudis, A. (2010). Conformational flexibility in designing peptides for immunology: The molecular dynamics approach. Current Computer-Aided Drug Design, 6(3), 207–222. https://doi.org/10.2174/157340910791760073
  • TACC. (n.d.) Texas Advanced Computing Center (TACC). Retrieved from http://www.tacc.utexas/edu
  • Wang, C. R., Castano, A. R., Peterson, P. A., Slaughter, C., Lindahl, K. F., & Deisenhofer, J. (1995). Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3. Cell, 82(4), 655–664. https://doi.org/10.1016/0092-8674(95)90037-3
  • Wang, J., & Hou, T. (2012). Develop and test a solvent accessible surface area-based model in conformational entropy calculations. Journal of Chemical Information and Modeling, 52(5), 1199–1212. https://doi.org/10.1021/ci300064d
  • Wang, J. M., Hou, T. J., & Xu, X. J. (2006). Recent advances in free energy calculations with a combination of molecular mechanics and continuum models. Current Computer Aided-Drug Design, 2(3), 287–306. https://doi.org/10.2174/157340906778226454
  • Wang, C. R., Lindahl, K. F., & Deisenhofer, J. (1996). Crystal structure of the MHC class Ib molecule H2-M3. Research in Immunology, 147(5), 313–321. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/8876059 https://doi.org/10.1016/0923-2494(96)89644-1
  • Wang, C. R., Loveland, B. E., & Lindahl, K. F. (1991). H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse. Cell, 66(2), 335–345. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/1855254 https://doi.org/10.1016/0092-8674(91)90623-7
  • Wang, E., Sun, H., Wang, J., Wang, Z., Liu, H., Zhang, J. Z. H., & Hou, T. (2019). End-point binding free energy calculation with MM/PBSA and MM/GBSA: Strategies and applications in drug design. Chemical Reviews, 119(16), 9478–9508. Epub 2019/06/28. https://doi.org/10.1021/acs.chemrev.9b00055
  • Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics & Modelling, 25(2), 247–260. https://doi.org/10.1016/j.jmgm.2005.12.005
  • 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. https://doi.org/10.1002/jcc.20035
  • Wieczorek, M., Abualrous, E. T., Sticht, J., Alvaro-Benito, M., Stolzenberg, S., Noe, F., & Freund, C. (2017). Major histocompatibility complex (MHC) class I and MHC class II proteins: Conformational plasticity in antigen presentation. Frontiers in Immunology, 8, 292. https://doi.org/10.3389/fimmu.2017.00292
  • Xu, H., Chun, T., Choi, H. J., Wang, B., & Wang, C. R. (2006). Impaired response to Listeria in H2-M3-deficient mice reveals a nonredundant role of MHC class Ib-specific T cells in host defense. The Journal of Experimental Medicine, 203(2), 449–459. https://doi.org/10.1084/jem.20051866

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