Two polymorphisms facilitate differences in plasticity between two chicken major histocompatibility complex class i proteins

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Bailey, Alistair ^a,b   Van Hateren, Andy ^a,b   Elliott, Tim ^a,b   Werner, Jörn M ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TAPASIN; CARRIER PROTEIN; HLA ANTIGEN CLASS 1; BF2 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHICKEN; CONTROLLED STUDY; GENE EXPRESSION; GENE SEQUENCE; GENE STRUCTURE; GENETIC POLYMORPHISM; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PEPTIDE ANALYSIS; PHENOTYPIC PLASTICITY; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; RESIDUE ANALYSIS; SEQUENCE HOMOLOGY; ANIMAL; CHEMICAL STRUCTURE; GENETICS; IMMUNOLOGY; ALLOSTERISM; PROTEIN FUNCTION; PROTEIN POLYMORPHISM; PROTEIN TERTIARY STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CHICKENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; POLYMORPHISM, GENETIC; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION;

EID: 84897769672     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.008965     Document Type: Article

References (69)

1. Neefjes J, Jongsma ML, Paul P, Bakke O (2011) Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 11: 823-836.
2. Elliott T (1997) How does TAP associate with MHC class I molecules? Immunology Today 18: 375-379.
3. Suh WK, Mitchell EK, Yang Y, Peterson PA, Waneck GL, et al. (1996) MHC class I molecules form ternary complexes with calnexin and TAP and undergo peptide-regulated interaction with TAP via their extracellular domains. J Exp Med 184: 337-348. (Pubitemid 26324087)
4. Lewis JW, Elliott T (1998) Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr Biol 8: 717-720. (Pubitemid 28286281)
5. Cresswell P, Bangia N, Dick T, Diedrich G (1999) The nature of the MHC class I peptide loading complex. Immunol Rev 172: 21-28. (Pubitemid 30000466)
6. Ortmann B, Copeman J, Lehner PJ, Sadasivan B, Herberg JA, et al. (1997) A Critical Role for Tapasin in the Assembly and Function of Multimeric MHC Class I-TAP Complexes. Science 277: 1306-1309. (Pubitemid 27449083)
7. Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5: 103-114. (Pubitemid 26301087)
8. Williams AP, Peh CA, Purcell AW, McCluskey J, Elliott T (2002) Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16: 509-520. (Pubitemid 34442576)
9. Howarth M, Williams A, Tolstrup AB, Elliott T (2004) Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc Natl Acad Sci U S A 101: 11737-11742. (Pubitemid 39095365)
10. Androlewicz MJ, Ortmann B, van Endert PM, Spies T, Cresswell P (1994) Characteristics of peptide and major histocompatibility complex class I/beta 2-microglobulin binding to the transporters associated with antigen processing (TAP1 and TAP2). Proceedings of the National Academy of Sciences of the United States of America 91: 12716-12720.
11. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA, et al. (2004) Gene map of the extended human MHC. Nat Rev Genet 5: 889-899. (Pubitemid 39564252)
12. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, et al. (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci U S A 101: 3490-3494. (Pubitemid 38338222)
13. van Endert PM, Riganelli D, Greco G, Fleischhauer K, Sidney J, et al. (1995) The peptide-binding motif for the human transporter associated with antigen processing. J Exp Med 182: 1883-1895.
14. Boyle LH, Hermann C, Boname JM, Porter KM, Patel PA, et al. (2013) Tapasin-related protein TAPBPR is an additional component of the MHC class I presentation pathway. Proc Natl Acad Sci U S A.
15. Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, et al. (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401: 923-925.
16. Wong GK, Liu B, Wang J, Zhang Y, Yang X, et al. (2004) A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432: 717-722.
17. Kaufman J (1999) Co-evolving genes in MHC haplotypes: the "rule" for nonmammalian vertebrates? Immunogenetics 50: 228-236.
18. Shaw I, Powell TJ, Marston DA, Baker K, van Hateren A, et al. (2007) Different evolutionary histories of the two classical class I genes BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens. Journal of Immunology 178: 5744-5752. (Pubitemid 46674371)
19. Walker BA, Hunt LG, Sowa AK, Skjodt K, Gobel TW, et al. (2011) The dominantly expressed class I molecule of the chicken MHC is explained by coevolution with the polymorphic peptide transporter (TAP) genes. Proc Natl Acad Sci U S A 108: 8396-8401.
20. Wallny HJ, Avila D, Hunt LG, Powell TJ, Riegert P, et al. (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci U S A 103: 1434-1439. (Pubitemid 43191183)
21. Kaufman J, Volk H, Wallny HJ (1995) A "minimal essential Mhc" and an "unrecognized Mhc": two extremes in selection for polymorphism. Immunol Rev 143: 63-88.
22. Lewis JW, Neisig A, Neefjes J, Elliott T (1996) Point mutations in the alpha 2 domain of HLA-A2.1 define a functionally relevant interaction with TAP. Curr Biol 6: 873-883. (Pubitemid 26324631)
23. Peace-Brewer AL, Tussey LG, Matsui M, Li G, Quinn DG, et al. (1996) A point mutation in HLA-A*0201 results in failure to bind the TAP complex and to present virus-derived peptides to CTL. Immunity 4: 505-514. (Pubitemid 26354659)
24. van Hateren A, Carter R, Bailey A, Kontouli N, Williams AP, et al. (2013) A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins. J Biol Chem 288: 32797-32808.
25. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718. (Pubitemid 43076182)
26. Hess B (2009) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Abstracts of Papers of the American Chemical Society 237.
27. Pronk S, Pall S, Schulz R, Larsson P, Bjelkmar P, et al. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29: 845-854.
28. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78: 1950-1958.
29. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299. (Pubitemid 29484693)
30. Smock RG, Rivoire O, Russ WP, Swain JF, Leibler S, et al. (2010) An interdomain sector mediating allostery in Hsp70 molecular chaperones. Mol Syst Biol 6: 414.
31. Dror RO, Dirks RM, Grossman JP, Xu H, Shaw DE (2012) Biomolecular Simulation: A Computational Microscope for Molecular Biology. Annual Review of Biophysics 41: 429-452.
32. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815. (Pubitemid 24007801)
33. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2007) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci Chapter 2: Unit 2 9.
34. Koch M, Camp S, Collen T, Avila D, Salomonsen J, et al. (2007) Structures of an MHC class I molecule from B21 chickens illustrate promiscuous peptide binding. Immunity 27: 885-899. (Pubitemid 50013978)
35. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201. (Pubitemid 43205406)
36. Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) Procheck - a Program to Check the Stereochemical Quality of Protein Structures. Journal of Applied Crystallography 26: 283-291.
37. Benkert P, Biasini M, Schwede T (2011) Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27: 343-350.
38. Amadei A, Linssen AB, Berendsen HJ (1993) Essential dynamics of proteins. Proteins 17: 412-425. (Pubitemid 23358549)
39. Amadei A, Linssen AB, de Groot BL, van Aalten DM, Berendsen HJ (1996) An efficient method for sampling the essential subspace of proteins. J Biomol Struct Dyn 13: 615-625. (Pubitemid 26081108)
40. Cooper A, Dryden DT (1984) Allostery without conformational change. A plausible model. Eur Biophys J 11: 103-109.
41. Halabi N, Rivoire O, Leibler S, Ranganathan R (2009) Protein sectors: evolutionary units of three-dimensional structure. Cell 138: 774-786.
42. Reynolds KA, McLaughlin RN, Ranganathan R (2011) Hot spots for allosteric regulation on protein surfaces. Cell 147: 1564-1575.
43. McLaughlin RN Jr, Poelwijk FJ, Raman A, Gosal WS, Ranganathan R (2012) The spatial architecture of protein function and adaptation. Nature 491: 138-142.
44. Van Hateren A, James E, Bailey A, Phillips A, Dalchau N, et al. (2010) The cell biology of major histocompatibility complex class I assembly: towards a molecular understanding. Tissue Antigens 76: 259-275.
45. Simone LC, Georgesen CJ, Simone PD, Wang X, Solheim JC (2012) Productive association between MHC class I and tapasin requires the tapasin transmembrane/cytosolic region and the tapasin C-terminal Ig-like domain. Mol Immunol 49: 628-639.
46. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE (2011) How fast-folding proteins fold. Science 334: 517-520.
47. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450: 964-972.
48. de Groot BL, Hayward S, van Aalten DM, Amadei A, Berendsen HJ (1998) Domain motions in bacteriophage T4 lysozyme: a comparison between molecular dynamics and crystallographic data. Proteins 31: 116-127.
49. Elliott T, Elvin J, Cerundolo V, Allen H, Townsend A (1992) Structural requirements for the peptide-induced conformational change of free major histocompatibility complex class I heavy chains. European Journal of Immunology 22: 2085-2091.
50. Bouvier M, Wiley DC (1998) Structural characterization of a soluble and partially folded class I major histocompatibility heavy chain/beta 2m heterodimer. Nat Struct Biol 5: 377-384. (Pubitemid 28211176)
51. Springer S, Doring K, Skipper JC, Townsend AR, Cerundolo V (1998) Fast association rates suggest a conformational change in the MHC class I molecule H-2Db upon peptide binding. Biochemistry 37: 3001-3012. (Pubitemid 28145753)
52. McClendon CL, Friedland G, Mobley DL, Amirkhani H, Jacobson MP (2009) Quantifying Correlations Between Allosteric Sites in Thermodynamic Ensembles. J Chem Theory Comput 5: 2486-2502.
53. Dubay KH, Bothma JP, Geissler PL (2011) Long-range intra-protein communication can be transmitted by correlated side-chain fluctuations alone. PLoS Comput Biol 7: e1002168.
54. Bowman GR, Geissler PL (2012) Equilibrium fluctuations of a single folded protein reveal a multitude of potential cryptic allosteric sites. Proc Natl Acad Sci U S A 109: 11681-11686.
55. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of Simple Potential Functions for Simulating Liquid Water. Journal of Chemical Physics 79: 926-935.
56. Berendsen HJC, Postma JPM, Van Gunsteren WF, Hermans J (1981) Interaction models for water in relation to protein hydration; Pullman B, editor: Reidel. 331-342 p.
57. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation 4: 435-447.
58. Miyamoto S, Kollman PA (1992) Settle - an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models. Journal of Computational Chemistry 13: 952-962.
59. Nosé S (1984) A molecular dynamics method for simulations in the canonical ensemble. Molecular Physics 52: 255-268.
60. Hoover WG (1985) Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A 31: 1695-1697.
61. Parrinello M, Rahman A (1981) Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics 52: 7182-7190. (Pubitemid 12456820)
62. Nosé S, Klein ML (1983) Constant pressure molecular dynamics for molecular systems. Molecular Physics 50: 1055-1076.
63. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A Smooth Particle Mesh Ewald Method. Journal of Chemical Physics 103: 8577-8593.
64. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. Journal of Molecular Graphics 14: 33-&.
65. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF chimera - A visualization system for exploratory research and analysis. Journal of Computational Chemistry 25: 1605-1612.
66. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
67. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
68. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, et al. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: W695-699.
69. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.