Fine refinement of solid-state molecular structures of Leu- and met-enkephalins by NMR crystallography

Journal of Physical Chemistry B

Volumn 118, Issue 12, 2014, Pages 3298-3309

  Pawlak, Tomasz ^a   Potrzebowski, Marek J ^a  

^a CENTRE OF MOLECULAR AND MACROMOLECULAR STUDIES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR STRUCTURE; X RAY CRYSTALLOGRAPHY;

CAMBRIDGE CRYSTALLOGRAPHIC DATA CENTERS; CRYSTAL AND MOLECULAR STRUCTURE; MAGNETICALLY ACTIVES; MOLECULAR DISORDERS; NMR CRYSTALLOGRAPHY; PROJECTOR AUGMENTED WAVES; SOLID-STATE MOLECULAR STRUCTURE; STRUCTURE REFINEMENTS;

POLYPEPTIDES;

LEUCINE ENKEPHALIN; METENKEPHALIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLOGRAPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CRYSTALLOGRAPHY; ENKEPHALIN, LEUCINE; ENKEPHALIN, METHIONINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR STRUCTURE;

EID: 84897141733     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp500379e     Document Type: Article

References (71)

1. Waseda, Y.; Matsubara, E.; Shinoda, K. X-Ray Diffraction Crystallography; Springer: Heidelberg, Germany, 2011.
2. Harris, R. K.; Wasylishen, R. E.; Duer, M. J. NMR Crystallography in Encyclopedia of Magnetic Resonance; John Wiley & Sons Ltd.: New York, 2009.
3. 13C Solid-State MAS NMR Spectroscopy and GIPAW Chemical-Shift Calculations J. Phys. Chem. A 2010, 114, 10435-10442
4. Webber, A. L.; Elena, B.; Griffin, J. M.; Yates, J. R.; Pham, T. N.; Mauri, F.; Pickard, C. J.; Gil, A. M.; Stein, R.; Lesage Complete (1)H Resonance Assignment of Beta-Maltose from (1)H-(1)H DQ-DQ CRAMPS and (1)H (DQ-DUMBO)-(13)C SQ Refocused INEPT 2D Solid-State NMR Spectra and First Principles GIPAW Calculations Phys. Chem. Chem. Phys. 2010, 12, 6970-6983
5. Harris, R. K.; Cadars, S.; Emsley, L.; Yates, J. R.; Pickard, C. J.; Jetti, R. K.; Griesser, U. NMR Crystallography of Oxybuprocaine Hydrochloride, Modification II°Phys. Chem. Chem. Phys. 2007, 9, 360-368
6. Salager, E.; Stein, R. S.; Pickard, C. J.; Elena, B.; Emsley, L. Powder NMR Crystallography of Thymol Phys. Chem. Chem. Phys. 2009, 11, 2610-2621
7. 1H Solid-State NMR Spectroscopy J. Am. Chem. Soc. 2010, 132, 2564-2566
8. Harris, R. K.; Hodgkinson, P.; Zorin, V.; Dumez, J.-N.; Elena-Herrmann, B.; Emsley, L.; Salager, E.; Stein, R. S. Computation and NMR Crystallography of Terbutaline Sulfate Magn. Reson. Chem. 2010, 48, S103-S112
9. Yates, J. R.; Dobbins, S. E.; Pickard, C. J.; Mauri, F.; Ghi, P. Y.; Harris, R. K. A Combined First Principles Computational and Solid-State NMR Study of a Molecular Crystal: Flurbiprofen Phys. Chem. Chem. Phys. 2005, 7, 1402-1407
10. Yates, J. R.; Pham, T. N.; Pickard, C. J.; Mauri, F.; Amado, A. M.; Gil, A. M.; Brown, S. P. Probing Intermolecular Crystal Packing in "-Indomethacin by High-Resolution (1)H Solid-State NMR Spectroscopy J. Am. Chem. Soc. 2005, 127, 10216-10220
11. Ośmiałowski, B.; Kolehmainen, E.; Ikonen, S.; Ahonen, K.; Lofman, M. NMR Crystallography of 2-Acylamino-6-[1 H ]-Pyridones: Solid-State NMR, GIPAW Computational, and Single Crystal X-Ray Diffraction Studies J. Mol. Struct. 2011, 106, 678-683
12. Drašković, B. M.; Bogdanović, G. A.; Neelakantan, M. A.; Chamayou, A.-C.; Thalamuthu, S.; Avadhut, Y. S.; Schmedt Auf Der Günne, J.; Banerjee, S.; Janiak, C. N-O -Vanillylidene- l -Histidine: Experimental Charge Density Analysis of a Double Zwitterionic Amino Acid Schiff-Base Compound Cryst. Growth Des. 2010, 10, 1665-1676
13. 13C NMR Chemical Shifts Assignment for Cholesterol Crystals by Combined CP-MAS Spectral Editing and ab Initio GIPAW Calculations with Dispersion Forces J. Phys. Chem. A 2012, 116, 3765-3769
14. Hušák, M.; Kratochvíl, B.; Jegorov, A.; Brus, J.; Maixner, J.; Rohlíček, J. Simvastatin: Structure Solution of Two New Low-Temperature Phases from Synchrotron Powder Diffraction and SS-NMR Struct. Chem. 2010, 21, 511-518
15. Santos, S. M.; Rocha, J.; Mafra, L. NMR Crystallography: Toward Chemical Shift-Driven Crystal Structure Determination of the β-Lactam Antibiotic Amoxicillin Trihydrate Cryst. Growth Des. 2013, 13, 2390-2395
16. Pawlak, T.; Paluch, P.; Trzeciak-Karlikowska, K.; Jeziorna, A.; Potrzebowski, M. J. Study of the Thermal Processes in Molecular Crystals of Peptides by Means of NMR Crystallography CrystEngComm 2013, 15, 8680-8692
17. Hughes, J.; Smith, T. W.; Kosterlitz, H. W.; Fothergill, L. A.; Morgan, B. A.; Morris, H. R. Identification of Two Related Pentapeptides from the Brain with Potent Opiate Agonist Activity Nature 1975, 258, 577-580
18. Simantov, R.; Snyder, S. H. Morphine-like Peptides in Mammalian Brain: Isolation, Structure Elucidation, and Interactions with the Opiate Receptor Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 2515-2519
19. Lee, H.-K.; Smith, M. D; Smith, B. J.; Grussendorf, J.; Xu, L.; Gillies, R. J.; White, H. S.; Bulaj, G. Anticonvulsant Met-Enkephalin Analogues Containing Backbone Spacers Reveal Alternative Non-Opioid Signaling in the Brain ACS Chem. Biol. 2009, 4, 659-671
20. Griffin, J. F.; Langs, D. A.; Smith, G. D.; Blundell, T. L.; Tickle, I. J.; Bedarkar, S. The Crystal Structures of [Met5]Enkephalin and a Third Form of [Leu5]Enkephalin: Observations of a Novel Pleated Beta-Sheet Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 3272-3276
21. Karle, I. L.; Karle, J.; Mastropaolo, D.; Camerman, A.; Camerman, N. [Leu5]Enkephalin: Four Cocrystallizing Conformers with Extended Backbones That Form an Antiparallel [Beta]-Sheet Acta Crystallogr. 1983, B39, 625-637
22. Smith, G. D.; Griffin, J. F. Conformation of [Leu5]Enkephalin from X-ray Diffraction: Features Important for Recognition at Opiate Receptor Science 1978, 199, 1214-1216
23. Blundell, T. L.; Hearn, L.; Tickle, I. J.; Palmer, R. A.; Morgan, B. A.; Smith, G. D.; Griffin, J. F. Crystal Structure of [Leu5]Enkephalin Science 1979, 205, 220
24. Camerman, A.; Mastropaolo, D.; Karle, I. L.; Karle, J.; Camerman, N. Crystal Structure of Leucine-Enkephalin Nature 1983, 306, 447-450
25. Mastropaolo, D.; Camerman, A.; Camerman, N. Crystal Structure of Methionine-Enkephalin Biochem. Biophys. Res. Commun. 1986, 134, 698-703
26. Clark, S. J.; Segall, M. D.; Pickard, C. J.; Hasnip, P. J.; Probert, M. J.; Refson, K.; Payne, M. C. First Principles Methods Using CASTEP Z. Kristallogr. 2005, 220, 567-570
27. Segall, M. D.; Lindan, P. J. D.; Probert, M. J.; Pickard, C. J.; Hasnip, P. J.; Clark, S. J.; Payne, M. C. First-Principles Simulation: Ideas, Illustrations and the CASTEP Code J. Phys.: Condens. Matter 2002, 14, 2717-2744
28. Pickard, C. J.; Mauri, F. All-Electron Magnetic Response with Pseudopotentials: NMR Chemical Shifts Phys. Rev. B 2001, 63, 245101
29. Yates, J. R.; Pickard, C. J.; Mauri, F. Calculation of NMR Chemical Shifts for Extended Systems Using Ultrasoft Pseudopotentials Phys. Rev. B 2007, 76, 024401
30. Fung, B. M.; Khitrin, A. K.; Ermolaev, K. An Improved Broadband Decoupling Sequence for Liquid Crystals and Solids J. Magn. Reson. 2000, 142, 97-101
31. Antzutkin, O. N.; Shekar, S. C.; Levitt, M. H. Two-Dimensional Sideband Separation in Magic-Angle-Spinning NMR J. Magn. Reson., Ser. A 1995, 115, 7-19
32. Topspin, version 3.0; Bruker Biospin Gmbh, Karlsruhe, Germany.
33. Dvinskikh, S. V.; Sandstrom, D. Frequency Offset Refocused PISEMA-Type Sequences J. Magn. Reson. 2005, 175, 163-169
34. Mao, K.; Wiench, J. W.; Lin, V. S.-Y.; Pruski, M. Indirectly Detected Through-Bond Chemical Shift Correlation NMR Spectroscopy in Solids Under Fast MAS: Studies of Organic-Inorganic Hybrid Materials J. Magn. Reson. 2009, 196, 92-95
35. 15N NMR by Indirect Detection with High-Speed Magic Angle Spinning J. Magn. Reson. 2000, 142, 199-204
36. Morcombe, C. R.; Zilm, K. W. Chemical Shift Referencing in MAS Solid State NMR J. Magn. Reson. 2003, 162, 479-486
37. Perdew, J. P.; Burke, K.; Ernzerhof, K. M. Generalized Gradient Approximation Made Simple Phys. Rev. Lett. 1996, 77, 3865
38. Vanderbilt, D. Soft Self-Consistent Pseudopotentials in a Generalized Eigenvalue Formalism Phys. Rev. B 1990, 41, 7892
39. Monkhorst, H. J.; Pack, J. D. On Special Points for Brillouin Zone Integrations Phys. Rev. B 1976, 13, 5188
40. Nocedal, J.; Wright, S. J. Numerical Optimization, 2 nd ed.; Springer-Verlag: Berlin, NY, 2006.
41. Trzeciak-Karlikowska, K.; Bujacz, A.; Jeziorna, A.; Ciesielski, W.; Bujacz, G. D.; Gajda, J.; Pentak, D.; Potrzebowski, M. J. Solid-State NMR and X-ray Diffraction Study of Structure and Dynamics of Dihydrate and Anhydrous Form of Tyr-Ala-Phe Cryst. Growth Des. 2009, 9, 4051-4059
42. 15N NMR Study on Crystalline Leu- and Met-Enkephalins: Distinction of Polymorphs, Backbone Dynamics, and Local Conformational Rearrangements Induced by Dehydration or Freezing of Motions of Bound Solvent Molecules J. Phys. Chem. B 1998, 102, 2826-2834
43. 2H NMR Spectroscopy J. Phys. Chem. A 1999, 103, 3356-3363
44. Brown, P. B. Probing Proton-Proton Proximities in the Solid State Prog. Nucl. Magn. Res. 2007, 50, 199-251
45. 1H Solid-State NMR Solid State Nucl. Magn. Reson. 2012, 41, 1-27
46. Chu, P.-J.; Potrzebowski, M. J.; Scott, A. I.; Gao, Y. Conformational Studies of N -Benzoyl- l -Phenylalanine by Combined Rotation and Multiple-Pulse Spectroscopy Proton Nuclear Magnetic Resonance J. Am. Chem. Soc. 1990, 112, 881-883
47. Lange, A.; Scholz, I.; Manolikas, T.; Ernst, M.; Meier, B. H. Low-Power Cross Polarization in Fast Magic-Angle Spinning NMR Experiments Chem. Phys. Lett. 2009, 468, 100-105
48. Ernst, M.; Samoson, A.; Meier, B. H. Low-Power Decoupling in Fast Magic-Angle Spinning NMR Chem. Phys. Lett. 2001, 348, 293-302
49. Hediger, S.; Meier, B. H.; Ernst, R. R. Rotor-Synchronized Amplitude-Modulated Nuclear Magnetic Resonance Spin-Lock Sequences for Improved Cross Polarization under Fast Magic Angle Sample Spinning J. Chem. Phys. 1995, 102, 4000-4011
50. Caravatti, P.; Bodenhausen, G.; Ernst, R. R. Heteronuclear Solid-State Correlation Spectroscopy Chem. Phys. Lett. 1982, 89, 363-367
51. Caravatti, P.; Braunschweiler, L.; Ernst, R. R. Heteronuclear Correlation Spectroscopy in Rotating Solids Chem. Phys. Lett. 1983, 100, 305-310
52. 13C NMR Heteronuclear Dipolar-Correlation Spectroscopy of Solids with Frequency-Switched Lee-Goldburg Homonuclear Decoupling J. Magn. Reson. 1997, 124, 516-519
53. Zhou, D. H.; Rienstra, C. E. Rapid Analysis of Organic Compounds by Proton-Detected Heteronuclear Correlation NMR Spectroscopy with 40 kHz Magic-Angle Spinning Angew. Chem., Int. Ed. 2008, 47, 7328-7331
54. Mao, K. M.; Pruski, M. Directly and Indirectly Detected Through-Bond Heteronuclear Correlation Solid-State NMR Spectroscopy under Fast MAS J. Magn. Reson. 2009, 201, 165-174
55. Dixon, W. T. Spinning-Sideband-Free and Spinning-Sideband-Only NMR Spectra in Spinning Samples J. Chem. Phys. 1982, 77, 1800-1809
56. Pawlak, T.; Trzeciak-Karlikowska, K.; Czernek, J.; Ciesielski, W.; Potrzebowski, M. J. Computed and Experimental Chemical Shift Parameters for Rigid and Flexible YAF Peptides in the Solid State J. Phys. Chem. B 2012, 116, 1974-1983
57. Robinson, M.; Haynes, P. D. Dynamical Effects in ab Initio NMR Calculations: Classical Force Fields Fitted to Quantum Forces J. Chem. Phys. 2010, 133, 084109
58. Cadars, S.; Lesage, A.; Pickard, C. J.; Sautet, P.; Emsley, L. Characterizing Slight Structural Disorder in Solids by Combined Solid-State NMR and First Principles Calculations J. Phys. Chem. A 2009, 113, 902-911
59. Schanda, P.; Meier, B. H.; Ernst, M. Accurate Measurement of One-Bond H-X Heteronuclear Dipolar Couplings in MAS Solid-State NMR J. Magn. Reson. 2011, 210, 246-259
60. Burum, D. P.; Ernst, R. R. Net Polarization Transfer via a J-Ordered State for Signal J. Magn. Reson. 1980, 39, 163-168
61. Morris, G. A.; Freeman, R. Enhancement of Nuclear Magnetic Resonance Signals by Polarization Transfer J. Am. Chem. Soc. 1979, 101, 760-762
62. Ramamoorthy, A.; Wei, Y.; Lee, D. K. PISEMA Solid-State NMR Spectroscopy Annu. Rep. NMR Spectrosc. 2004, 52, 1-52
63. Ramamoorthy, A.; Opella, S. J. Two-Dimensional Chemical Shift/Heteronuclear Dipolar Coupling Spectra Obtained with Polarization Inversion Spin Exchange at the Magic Angle and Magic-Angle Sample Spinning (PISEMAMAS) Solid State Nucl. Magn. Reson. 1995, 4, 387-392
64. Yamamoto, K.; Ermakov, V. L.; Lee, D. K.; Ramamoorthy, A. PITANSEMA-MAS, a Solid-State NMR Method To Measure Heteronuclear Dipolar Couplings under MAS Chem. Phys. Lett. 2005, 408, 118-122
65. Wu, C. H.; Ramamoorthy, A.; Opella, S. J. High-Resolution Heteronuclear Dipolar Solid-State NMR Spectroscopy J. Magn. Reson., Ser. A 1994, 109, 270-272
66. Fu, R.; Tian, C.; Kim, H.; Smith, S. A.; Cross, T. A. The Effect of Hartmann-Hahn Mismatching on Polarization Inversion Spin Exchange at the Magic Angle J. Magn. Reson. 2002, 159, 167-174
67. Hong, M.; Yao, X.; Jakes, K.; Huster, D. Investigation of Molecular Motions by Lee-Goldburg Cross-Polarization NMR Spectroscopy J. Phys. Chem. B 2002, 106, 7355-7364
68. Dudenko, D. V.; Yates, J. R.; Harris, K. D.M.; Brown, S. P. An NMR Crystallography DFT-D Approach To Analyse the Role of Intermolecular Hydrogen Bonding and π-π Interactions in Driving Cocrystallisation of Indomethacin and Nicotinamide CrystEngComm 2013, 15, 8797-8807
69. Dracinsky, M.; Bour, P. Vibrational Averaging of the Chemical Shift in Crystalline Alpha-Glycine J. Comput. Chem. 2012, 33, 1080-1089
70. Dracinsky, M.; Hodgkinson, P. A Molecular Dynamics Study of the Effects of Fast Molecular Motions on Solid-State NMR Parameters CrystEngComm 2013, 15, 8705-8712
71. 13C NMR Shift Tensors and Lattice-Including Electronic Structure Methods CrystEngComm 2013, 15, 8693-8704