Homology modeling and molecular dynamics simulations of MUC1-9/H-2K b complex suggest novel binding interactions

Journal of Molecular Modeling

Volumn 17, Issue 7, 2011, Pages 1817-1829

  Stavrakoudis, Athanassios ^a   Tsoulos, Ioannis G ^b   Uray, Katalin ^c   Hudecz, Ferenc ^c,d   Apostolopoulos, Vasso ^e  

^a UNIVERSITY OF IOANNINA   (Greece)

^b Epirus Institute of Technology Arta   (Greece)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^e MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

Author keywords

Class I MHC; H 2Kb; Homology modeling; Molecular dynamics; MUC1; Tumor

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MUCIN 1; WATER;

ARTICLE; BINDING AFFINITY; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; BINDING SITES; H-2 ANTIGENS; HUMANS; MICE; MOLECULAR DYNAMICS SIMULATION; MUCIN-1; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION;

MURINAE;

EID: 80051792528     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-010-0884-4     Document Type: Article

References (67)

1. Agostinelli C (2009) Circular Statistics with R. URL http://cran.r- project.org/web/packages/circular/index.html
2. A Aksimentiev R Brunner J Cohen J Comer E Cruz-Chu D Hardy A Rajan A Shih G Sigalov Y Yin K Schulten 2008 Computer modeling in biotechnology: a partner in development Meth Mol Biol 474 181 234 10.1007/978-1-59745-480-3-11 1:CAS:528:DC%2BD1cXhtF2mt7vK
3. V Apostolopoulos E Lazoura 2004 Noncanonical peptides in complex with MHC class I Expert Rev Vaccin 3 151 162 10.1586/14760584.3.2.151 1:CAS:528:DC%2BD2cXislyqsrk%3D (Pubitemid 38470525)
4. V Apostolopoulos JS Haurum IF McKenzie 1997 MUC1 peptide epitopes associated with five different H-2 class I molecules Eur J Immunol 27 2579 2587 10.1002/eji.1830271017 1:CAS:528:DyaK2sXmvFanu7k%3D (Pubitemid 27453847)
5. V Apostolopoulos G Chelvanayagam PX Xing IF McKenzie 1998 Anti-MUC1 anti-bodies react directly with MUC1 peptides presented by class I H2 and HLA molecules J Immunol 161 767 775 1:CAS:528:DyaK1cXksFGkurY%3D (Pubitemid 28323540)
6. V Apostolopoulos M Yu AL Corper W Li IFC McKenzie L Teyton IA Wilson M Plebanski 2002 Crystal structure of a non-canonical high affinity peptide complexed with MHC class I: a novel use of alternative anchors J Mol Biol 318 1307 1316 10.1016/S0022-2836(02)00198-5 1:CAS:528:DC%2BD38Xkslyktro%3D (Pubitemid 34753999)
7. NA Baker D Sept S Joseph MJ Holst JA McCammon 2001 Electrostatics of nanosystems: application to microtubules and the ribosome Proc Natl Acad USA 98 10037 10041 10.1073/pnas.181342398 1:CAS:528:DC%2BD3MXmvFWisbc%3D (Pubitemid 32802969)
8. M Barinaga 1992 Getting some "backbone": how MHC binds peptides Science 257 880 881 10.1126/science.1502554 1:STN:280:DyaK38zms12qtA%3D%3D
9. HM Berman T Battistuz TN Bhat WF Bluhm PE Bourne K Burkhardt Z Feng GL Gilliland L Iype S Jain P Fagan J Marvin D Padilla V Ravichandran B Schneider N Thanki H Weissig JD Westbrook C Zardecki 2002 The Protein Data Bank Acta Crystall Sec D: Biol Crystall 58 899 907 10.1107/S0907444902003451 (Pubitemid 34653017)
10. PJ Bjorkman MA Saper B Samraoui WS Strominger DC Wiley 1987 Structure of the human class I histocombatibility antigen, HLA-A2 Nature 329 506 512 10.1038/329506a0 1:CAS:528:DyaL2sXmtlCgur0%3D (Pubitemid 17131093)
11. M Buck S Bouguet-Bonnet RW Pastor AD MacKerell Jr 2006 Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme Biophys J 90 36 38 10.1529/biophysj.105.078154
12. J Burchell J Taylor-Papadimitriou M Boshell S Gendler T Duhig 1989 A short sequence, within the amino acid tandem repeat of a cancer-associated mucin, contains immunodominant epitopes Int J Cancer 44 691 696 10.1002/ijc.2910440423 1:CAS:528:DyaK3cXps1GjsQ%3D%3D (Pubitemid 19258746)
13. G Chelvanayagam B Jakobsen X Gao S Easteal 1996 Structural comparison of major histocompatibility complex class i molecules and homology modelling of five distinct human leukocyte antigen - a alleles Protein Eng 9 1151 1164 10.1093/protein/9.12.1151 1:CAS:528:DyaK2sXot12qsQ%3D%3D
14. T Darden D York L Pedersen 1993 Particle mesh ewald: an N log(N) method for ewald sums in large systems J Chem Phys 98 10089 1092 10.1063/1.464397 1:CAS:528:DyaK3sXks1Ohsr0%3D
15. R Döker T Maurer W Kremer K Neidig HR Kalbitzer 1999 Determination of mean and standard deviation of dihedral angles Biochem Biophys Res Commun 257 348 350 10.1006/bbrc.1999.0462 (Pubitemid 29301447)
16. TJ Dolinsky JE Nielsen JA McCammon NA Baker 2004 PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucl Acids Res 32 W665 W667 10.1093/nar/gkh381 1:CAS:528:DC%2BD2cXlvFKmsbY%3D (Pubitemid 38997419)
17. SE Feller Y Zhang RW Pastor BR Brooks 1995 Constant pressure molecular dynamics simulation: the Langevin piston method J Chem Phys B 103 4613 4621 10.1063/1.470648 1:CAS:528:DyaK2MXotVentLo%3D
18. b Science 257 919 927 10.1126/science.1323877 1:CAS:528: DyaK38XlsVyqsrs%3D
19. b-ovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove Proc Natl Acad Sci USA 92 2479 2483 10.1073/pnas.92.7. 2479 1:CAS:528:DyaK2MXksl2kur4%3D
20. D Frishman P Argos 1995 Knowledge-based protein secondary structure assignment Proteins Struct Funct Genet 23 566 579 10.1002/prot.340230412 1:CAS:528:DyaK28Xht1yluw%3D%3D (Pubitemid 26009520)
21. R Galeazzi 2009 Molecular dynamics as a tool in rational drug design: current status and some major applications Curr Comput Aided Drug Des 5 225 240 10.2174/157340909789577847 1:CAS:528:DC%2BD1MXhsFWitr3I
22. S Gendler J Taylor-Papadimitriou T Duhig J Rothbard J Burchell 1988 A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats J Biol Chem 263 12820 12823 1:CAS:528:DyaL1cXls1Crt70%3D
23. NM Glykos 2006 Carma: a molecular dynamics analysis program J Comput Chem 27 1765 1768 10.1002/jcc.20482 1:CAS:528:DC%2BD28XhtVWgsLfM (Pubitemid 44476671)
24. T Hansson C Oostenbrink WF van Gunsteren 2002 Molecular dynamics simulations Curr Opin Struct Biol 12 190 196 10.1016/S0959-440X(02)00308-1 1:CAS:528:DC%2BD38XivVals7o%3D (Pubitemid 34327478)
25. HL Hoare LC Sullivan CS Clements LK Ely T Beddoe K Henderson J Lin H Reid A Brooks J Rossjohn 2008 Subtle changes in peptide conformation profoundly affect recognition of the non-classical MHC class i molecule HLA-E by the CD94-NKG2 natural killer cell receptors J Mol Biol 377 1297 1303 10.1016/j.jmb.2008.01.098 1:CAS:528:DC%2BD1cXjs1Smtr8%3D
26. R Huard R Dyall J Nikolić-Žugić 1997 The critical role of a solvent-exposed residue of an MHC class I-restricted peptide in MHC-peptide binding Int Immunol 9 1701 1707 10.1093/intimm/9.11.1701 1:CAS:528:DyaK2sXns1Kju7Y%3D (Pubitemid 27494133)
27. W Humphrey A Dalke K Schulten 1996 VMD: Visual Molecular Dynamics J Mol Graph 14 33 38 10.1016/0263-7855(96)00018-5 1:CAS:528:DyaK28Xis12nsrg%3D (Pubitemid 26152973)
28. EG Hutchinson JM Thornton 1994 A revised set of potentials for beta-turn formation in proteins Protein Sci 3 2207 22016 10.1002/pro.5560031206 1:CAS:528:DyaK2MXjslajtLc%3D
29. M Karplus 2003 Molecular dynamics of biological macromolecules: a brief history and perspective Biopolymers 68 350 358 10.1002/bip.10266 1:CAS:528:DC%2BD3sXitFylurs%3D (Pubitemid 36342871)
30. B Knapp U Omasits S Frantal W Schreiner 2009 A critical cross-validation of high throughput structural binding prediction methods for pMHC J Comp Aid Mol Des 23 301 307 10.1007/s10822-009-9259-2 1:CAS:528:DC%2BD1MXkt1yitLo%3D
31. P Kollman I Massova C Reyes B Kuhn S Huo L Chong M Lee T Lee Y Duan W Wang O Donini P Cieplak J Srinivasan DA Case TE Cheatham 2000 Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc Chem Res 33 889 897 10.1021/ar000033j 1:CAS:528:DC%2BD3cXmvFGiu7g%3D (Pubitemid 32056774)
32. AD MacKerell Jr M Feig CL Brooks 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 J Comput Chem 25 1400 1415 10.1002/jcc.20065 1:CAS:528: DC%2BD2cXlsVOgt7c%3D
33. AD MacKerell Jr M Feig CL Brooks 2004 Improved treatment of the protein backbone in empirical force fields J Am Chem Soc 126 698 699 10.1021/ja036959e 1:CAS:528:DC%2BD3sXhtVWisb7F (Pubitemid 38114337)
34. B Mallik D Morikis 2006 Applications of molecular dynamics simulations in immunology: a useful computational method in aiding vaccine design Curr Proteom 3 259 270 10.2174/157016406780655568 1:CAS:528:DC%2BD2sXmsV2isLY%3D (Pubitemid 46740373)
35. M Matsamura DH Fremont PA Peterson IA Wilson 1992 Emerging principles for the recognition of peptide antigens by MHC class I molecules Science 257 927 934 10.1126/science.1323878
36. R Meijers CC Lai Y Yang JH Liu W Zhong JH Wang EL Reinherz 2005 Crystal structures of murine MHC Class I H-2 Db and Kb molecules in complex with CTL epitopes from influenza A virus: implications for TCR repertoire selection and immunodominance J Mol Biol 345 1099 1110 10.1016/j.jmb.2004.11.023 1:CAS:528:DC%2BD2MXis1WqsA%3D%3D (Pubitemid 40092227)
37. b class I molecule devoid of the central anchor ("C") pocket J Immunol 160 2815 2823 1:CAS:528:DyaK1cXhvVWgtL4%3D (Pubitemid 28136736)
38. D Morikis JD Lambris 2004 Physical methods for structure, dynamics and binding in immunological research Trends Immunol 25 700 707 10.1016/j.it.2004. 09.009 1:CAS:528:DC%2BD2cXptl2kur8%3D (Pubitemid 39457985)
39. M Novotny M Seibert GJ Kleywegt 2007 On the precision of calculated solvent-accessible surface areas Acta Crystallogr Sec D D63 270 274 10.1107/S0907444906044118 1:CAS:528:DC%2BD2sXntl2qtA%3D%3D (Pubitemid 46197545)
40. TSG Olsson MA Williams WR Pitt JE Ladbury 2008 The thermodynamics of protein-ligand interaction and solvation: Insights for ligand design J Mol Biol 384 1002 1007 10.1016/j.jmb.2008.09.073 1:CAS:528:DC%2BD1cXhsVWls7zO
41. U Omasits B Knapp M Neumann O Steinhauser H Stockinger R Kobler W Schreiner 2008 Analysis of key parameters for molecular dynamics of pMHC molecules Mol Simul 34 781 793 10.1080/08927020802256298 1:CAS:528: DC%2BD1cXpvVKlu7Y%3D
42. PM Petrone AE Garcia 2004 MHC-peptide binding is assisted by bound water molecules J Mol Biol 338 419 435 10.1016/j.jmb.2004.02.039 1:CAS:528: DC%2BD2cXivVeltbo%3D (Pubitemid 38450741)
43. MR Price C FH O'Sullivan RW Baldwin PM Edwards SJB Tendler 1991 Immunological and structural features of the protein core of human polymorphic epithelial mucin Mol Immunol 27 795 802 10.1016/0161-5890(90)90089-I
44. M Raghavan N Del Cid SM Rizvi LR Peters 2008 MHC class I assembly: out and about Trends Immunol 29 436 443 10.1016/j.it.2008.06.004
45. MG Rudolph RL Stanfield IA Wilson 2006 How TCRs bind MHCs, peptides, and coreceptors Immunology 24 419 446 10.1146/annurev.immunol.23.021704.115658 1:CAS:528:DC%2BD28XkvFSqtLw%3D
46. SK Sadiq MD Mazzeo SJ Zasada S Manos I Stoica CV Gale SJ Watson P Kellam S Brew PV Coveney 2008 Patient-specific simulation as a basis for clinical decision-making Phil Trans R Soc A 366 3199 3219 10.1098/rsta.2008.0100
47. MA Saper PJ Bjorkman DC Wiley 1991 Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution J Mol Biol 219 277 319 10.1016/0022-2836(91)90567-P 1:CAS:528:DyaK3MXkvFSgtbw%3D
48. JA Speir J Stevens E Joly GW Butcher IA Wilson 2001 Two different, highly exposed, bulged structures for an unusually long peptide bound to rat MHC class I RT1-Aa Immunity 14 81 92 10.1016/S1074-7613(01)00091-7 1:CAS:528: DC%2BD3MXivVKntLg%3D (Pubitemid 32144689)
49. A Stavrakoudis 2008 Molecular dynamics simulations of an apoliprotein derived peptide Chem Phys Lett 461 294 299 10.1016/j.cplett.2008.07.007 1:CAS:528:DC%2BD1cXpvV2js7Y%3D
50. A Stavrakoudis 2009 A disulfide linked model of the complement protein C8γ complexed with C8α indel peptide J Mol Model 15 165 171 10.1007/s00894-008-0412-y 1:CAS:528:DC%2BD1MXntFWrsrk%3D
51. A Stavrakoudis 2010 Computational modeling and molecular dynamics simulations of a cyclic peptide mimotope of the CD52 antigen complexed with CAMPATH-1H antibody Mol Simul 36 127 137 10.1080/08927020903124593 1:CAS:528:DC%2BC3cXhvFGjtb8%3D
52. A Stavrakoudis 2010 Conformational flexibility in designing peptides for immunology: the molecular dynamics approach Curr Comput Aided Drug Des 6 207 222 10.2174/157340910791760073 1:CAS:528:DC%2BC3cXhtFSktLfI
53. C-K Tang M Katsara V Apostolopoulos 2008 Strategies used for muc1 immunotherapy: human clinical studies Expert Rev Vaccin 7 963 975 10.1586/14760584.7.7.963 1:CAS:528:DC%2BD1cXhtVOiur%2FP
54. C-K Tang M Katsara V Apostolopoulos 2008 Strategies used for muc1 immunotherapy: preclinical studies Expert Rev Vaccin 7 951 962 10.1586/14760584.7.7.951 1:CAS:528:DC%2BD1cXhtVOiur%2FJ
55. AA Tantar S Conilleau B Parent N Melab L Brillet S Roy EL Talbi D Horvath 2008 Docking and biomolecular simulations on computer grids: status and trends Curr Comput Aid Drug Des 4 235 249 10.2174/157340908785747438 1:CAS:528:DC%2BD1MXhtVKqt7Y%3D
56. VA Tatsis IG Tsoulos A Stavrakoudis 2009 Molecular dynamics simulations of the TSSPSAD peptide antigen in free and bound with CAMPATH-1H fab antibody states: the importance of the β-turn conformation Int J Pept Res Ther 15 1 9 10.1007/s10989-008-9155-y 1:CAS:528:DC%2BD1cXht1eitb%2FO
57. Tsoulos IG, Stavrakoudis A (2009) Eucb: a C++ program for molecular dynamics trajectory analysis. URL http://stavrakoudis.econ.uoi.gr/eucb
58. FE Tynan SR Burrows AM Buckle CS Clements NA Borg JJ Miles T Beddoe JC Whisstock MC Wilce SL Silins JM Burrows L Kjer-Nielsen L Kostenko AW Purcell J McCluskey J Rossjohn 2005 T cell receptor recognition of a'super-bulged'major histocompatibility complex class I-bound peptide Nat Immunol 6 1114 1122 10.1038/ni1257 1:CAS:528:DC%2BD2MXhtFamsb7E (Pubitemid 41541789)
59. WF van Gunsteren J Dolenc AE Mark 2008 Molecular simulation as an aid to experimentalists Curr Opin Struct Biol 18 149 53 10.1016/j.sbi.2007.12.007
60. S Wan PV Coveney DR Flower 2005 Peptide recognition by the T cell receptor: comparison of binding free energies from thermodynamic integration, Poisson-Boltzmann and linear interaction energy approximations Phil Trans R Soc A 363 2037 2053 10.1098/rsta.2005.1627 1:CAS:528:DC%2BD2MXhtFChtrzL (Pubitemid 41343819)
61. S Wan DR Flower PV Coveney 2008 Toward an atomistic understanding of the immune synapse: large-scale molecular dynamics simulation of a membrane-embedded TCR-pMHC-CD4 complex Mol Immunol 45 1221 1230 10.1016/j.molimm.2007.09.022 1:CAS:528:DC%2BD1cXhtF2gtg%3D%3D (Pubitemid 350299491)
62. JM Word SC Lovell JS Richardson DC Richardson 1999 Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation J Mol Biol 285 1735 1747 10.1006/jmbi.1998.2401 1:CAS:528: DyaK1MXhtV2ht7g%3D (Pubitemid 29060467)
63. P-X Xing K Reynolds GA Pietersz IFC McKenzie 1991 Effect of variaions in peptide sequence on anti-human milk fat globule membrane antibody reactions Immunology 72 304 311 1:CAS:528:DyaK3MXitVGitrk%3D
64. P-X Xing J Prenzoska IFC McKenzie 1992 Epitope mapping of anti-breast and anti-ovarian mucin monoclonal antibodies Mol Immunol 29 641 650 10.1016/0161-5890(92)90201-8 1:CAS:528:DyaK38Xkt1CnsL8%3D
65. Y Yonetani 2006 Liquid water simulation: a critical examination of cutoff length J Chem Phys 124 204501 10.1063/1.2198208 (Pubitemid 43838623)
66. Z Zavala-Ruiz I Strug BD Walker PJ Norris LJ Stern 2004 A hairpin turn in a II MHC-bound peptide orients outside the binding groove for T cell recognition Proc Nat Acad Sci USA 101 13279 13284 10.1073/pnas.0403371101 1:CAS:528:DC%2BD2cXnvFemsrY%3D (Pubitemid 39209656)
67. C Zhang A Anderson C DeLisi 1998 Structural principles that govern the peptide-binding motifs of class I MHC molecules J Mol Biol 281 929 947 10.1006/jmbi.1998.1982 1:CAS:528:DyaK1cXmtVygs7w%3D (Pubitemid 28408439)