Polarizable atomic multipole X-ray refinement: application to peptide crystals.
Recent advances in computational chemistry have produced force fields based on a polarizable atomic multipole description of biomolecular electrostatics. In this work, the Atomic Multipole Optimized Energetics for Biomolecular Applications (AMOEBA) force field is applied to restrained refinement of molecular models against X-ray diffraction data from peptide crystals. A new formalism is also developed to compute anisotropic and aspherical structure factors using fast Fourier transformation (FFT) of Cartesian Gaussian multipoles. Relative to direct summation, the FFT approach can give a speedup of more than an order of magnitude for aspherical refinement of ultrahigh-resolution data sets. Use of a sublattice formalism makes the method highly parallelizable. Application of the Cartesian Gaussian multipole scattering model to a series of four peptide crystals using multipole coefficients from the AMOEBA force field demonstrates that AMOEBA systematically underestimates electron density at bond centers. For the trigonal and tetrahedral bonding geometries common in organic chemistry, an atomic multipole expansion through hexadecapole order is required to explain bond electron density. Alternatively, the addition of interatomic scattering (IAS) sites to the AMOEBA-based density captured bonding effects with fewer parameters. For a series of four peptide crystals, the AMOEBA-IAS model lowered R(free) by 20-40% relative to the original spherically symmetric scattering model.
Schnieders
Michael J
MJ
Department of Chemistry, Stanford University, Stanford, CA 94305, USA.
Fenn
Timothy D
TD
Pande
Vijay S
VS
Brunger
Axel T
AT
D002625:Chemistry, Organic; D019295:Computational Biology; D005583:Fourier Analysis; D008962:Models, Theoretical; D010446:Peptide Fragments / Q000737:chemistry* / Q000378:metabolism; D011487:Protein Conformation; D012984:Software; D013223:Statistics as Topic; D014961:X-Ray Diffraction
D010446:Peptide Fragments
Nat Protoc. 2007;2(11):2728-33
18007608
Curr Pharm Des. 2006;12(17):2121-58
16796560
Nature. 2002 Nov 7;420(6911):102-6
12422224
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3171-6
10737790
Adv Protein Chem. 2003;66:27-85
14631816
Acta Crystallogr B. 2002 Aug;58(Pt 4):721-7
12149563
J Chem Phys. 2006 Mar 14;124(10):104101
16542062
Acta Crystallogr C. 2006 Aug;62(Pt 8):o454-7
16891717
J Chem Phys. 2007 Mar 28;126(12):124114
17411115
Adv Protein Chem. 2005;72:79-104
16581373
Proteins. 2004 Jun 1;55(4):792-804
15146478
Structure. 1997 Mar 15;5(3):325-36
9083112
Biopolymers. 2003 Jan;68(1):91-109
12579582
J Mol Biol. 1988 Oct 5;203(3):803-16
3062181
J Phys Chem A. 2007 Aug 23;111(33):8170-6
17665882
Methods Enzymol. 1997;277:243-69
18488313
Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21
9757107
Acta Crystallogr B. 2000 Aug;56(Pt 4):728-37
10944266
J Chem Theory Comput. 2018 Oct 9;14(10):5273-5289
30176213
J Comput Chem. 2002 Dec;23(16):1497-506
12395419
Science. 1987 Jan 23;235(4787):458-60
17810339
J Comput Chem. 2005 May;26(7):682-90
15754305
Angew Chem Int Ed Engl. 2005 Oct 28;44(42):6810-1
16187393
Nucleic Acids Res. 2000 Jan 1;28(1):235-42
10592235
Acta Crystallogr D Biol Crystallogr. 2007 Nov;63(Pt 11):1194-7
18007035
Biochemistry. 1998 Sep 29;37(39):13446-52
9753430
Acta Crystallogr A. 2007 Mar;63(Pt 2):108-25
17301471
Acta Crystallogr A. 2004 Jan;60(Pt 1):19-32
14691324
J Chem Theory Comput. 2007 Nov;3(6):2083-97
26636202
Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948-54
12393927
Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13665-70
11707581
Proc Natl Acad Sci U S A. 1997 May 13;94(10):5018-23
9144182
J Chem Theory Comput. 2005 Jul;1(4):694-715
26641692
J Mol Biol. 2000 Feb 25;296(3):787-801
10677281
J Chem Phys. 2005 Apr 1;122(13):134508
15847482
Org Biomol Chem. 2006 Sep 7;4(17):3242-51
17036112
Annu Rev Biophys Biomol Struct. 2005;34:43-69
15869383
Acta Crystallogr D Biol Crystallogr. 2007 Dec;63(Pt 12):1254-68
18084073
J Chem Theory Comput. 2007 Nov;3(6):1960-1986
18978934
J Chem Theory Comput. 2005 Nov;1(6):1128-32
26631656
Acta Crystallogr A. 2004 Sep;60(Pt 5):357-64
15477672
Nucleic Acids Res. 2001 Mar 1;29(5):1208-15
11222771
Acta Crystallogr A. 1989 Jun 1;45 ( Pt 6):396-409
2619971
Acta Crystallogr A. 1990 Jul 1;46 ( Pt 7):585-93
2206482
Acta Crystallogr D Biol Crystallogr. 2007 Feb;63(Pt 2):160-70
17242509
Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8742-7
12855766
J Chem Phys. 2004 Jan 1;120(1):73-87
15267263