Direct evidence of imino acid-aromatic interactions in native collagen protein by DNP-enhanced solid-state NMR spectroscopy

Journal of Physical Chemistry Letters

Volumn 5, Issue 22, 2014, Pages 4044-4048

  Singh, Chandan ^a,c   Rai, Ratan Kumar ^a   Aussenac, Fabien ^b   Sinha, Neeraj ^a  

^a SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

^b Bruker Corporation   (United States)

^c BANARAS HINDU UNIVERSITY   (India)

Author keywords

1H 13C heteronuclear correlation; CH interaction; Cross peak; Polyadenosine diphosphate ribose (PAR); Sensitivity enhancement; Sugar

Indexed keywords

AMINO ACIDS; AROMATIC COMPOUNDS; CARBOXYLIC ACIDS; LIGHT POLARIZATION; MUSCULOSKELETAL SYSTEM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SUGARS;

AROMATIC AMINO ACID; AROMATIC INTERACTIONS; CROSS PEAKS; DIPHOSPHATES; DYNAMIC NUCLEAR POLARIZATION; HETERONUCLEAR CORRELATION; SENSITIVITY ENHANCEMENTS; SOLID-STATE NMR SPECTROSCOPY;

COLLAGEN;

EID: 84912572978     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz502081j     Document Type: Article

References (29)

1. Shoulders, M. D.; Raines, R. T. Collagen Structure and Stability. Annu. Rev. Biochem. 2009, 78, 929-958.
2. Gelse, K.; Pöschl, E.; Aigner, T. Collagens - Structure, Function, and Biosynthesis. Adv. Drug Delivery Rev. 2003, 55, 1531-1546.
3. Bella, J.; Eaton, M.; Brodsky, B.; Berman, H. M. Crystal and Molecular Structure of a Collagen-Like Peptide at 1.9 A˚ Resolution. Science 1994, 266, 75-81.
4. Rai, R. K.; Sinha, N. Dehydration-Induced Structural Changes in the Collagen-Hydroxyapatite Interface in Bone by High-Resolution Solid-State NMR Spectroscopy. J. Phys. Chem. C 2011, 115, 14219-14227.
5. Zhu, P.; Xu, J.; Sahar, N.; Morris, M. D.; Kohn, D. H.; Ramamoorthy, A. Time-Resolved Dehydration-Induced Structural Changes in an Intact Bovine Cortical Bone Revealed by Solid-State NMR Spectroscopy. J. Am. Chem. Soc. 2009, 131, 17064-17065.
6. Wang, Y.; Azaïs, T.; Robin, M.; Vallée, A.; Catania, C.; Legriel, P.; Pehau-Arnaudet, G.; Babonneau, F.; Giraud-Guille, M.-M.; Nassif, N. The Predominant Role of Collagen in the Nucleation, Growth, Structure and Orientation of Bone Apatite. Nat. Mater. 2012, 11, 724-733.
7. Viguet-Carrin, S.; Garnero, P.; Delmas, P. The Role of Collagen in Bone Strength. Osteoporosis Int. 2006, 17, 319-336.
8. Hu, Y.-Y.; Rawal, A.; Schmidt-Rohr, K. Strongly Bound Citrate Stabilizes the Apatite Nanocrystals in Bone. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 22425-22429.
9. Szpak, P. Fish Bone Chemistry and Ultrastructure: Implications for Taphonomy and Stable Isotope Analysis. J. Archaeol. Sci. 2011, 38, 3358-3372.
10. Plevin, M. J.; Bryce, D. L.; Boisbouvier, J. Direct Detection of CH/π Interactions in Proteins. Nat. Chem. 2010, 2, 466-471.
11. Kar, K.; Ibrar, S.; Nanda, V.; Getz, T. M.; Kunapuli, S. P.; Brodsky, B. Aromatic Interactions Promote Self-Association of Collagen Triple-Helical Peptides to Higher-Order Structures. Biochemistry 2009, 48, 7959-7968.
12. Luo, W.; Hong, M. Conformational Changes of an Ion Channel Detected through Water-Protein Interactions Using Solid-State NMR Spectroscopy. J. Am. Chem. Soc. 2010, 132, 2378-2384.
13. Tycko, R. Solid-State NMR Studies of Amyloid Fibril Structure. Annu. Rev. Phys. Chem. 2011, 62, 279-299.
14. Cross, T. A.; Sharma, M.; Yi, M.; Zhou, H.-X. Influence of Solubilizing Environments on Membrane Protein Structures. Trends Biochem. Sci. 2014, 36, 117-125.
15. Mroue, K. H.; MacKinnon, N.; Xu, J.; Zhu, P.; McNerny, E.; Kohn, D. H.; Morris, M. D.; Ramamoorthy, A. High-Resolution Structural Insights into Bone: A Solid-State NMR Relaxation Study Utilizing Paramagnetic Doping. J. Phys. Chem. B 2012, 116, 11656-11661.
16. Mroue, K. H.; Zhang, R.; Zhu, P.; McNerny, E.; Kohn, D. H.; Morris, M. D.; Ramamoorthy, A. Acceleration of Natural-Abundance Solid-State MAS NMR Measurements on Bone by Paramagnetic Relaxation from Gadolinium-DTPA. J. Magn. Reson. 2014, 244, 90-97.
17. Chow, W. Y.; Rajan, R.; Muller, K. H.; Reid, D. G.; Skepper, J. N.; Wong, W. C.; Brooks, R. A.; Green, M.; Bihan, D.; Farndale, R. W.; et al. NMR Spectroscopy of Native and in Vitro Tissues Implicates PolyADP Ribose in Biomineralization. Science 2014, 344, 742-746.
18. Griffin, R. G.; Prisner, T. F. High Field Dynamic Nuclear Polarization - The Renaissance. Phys. Chem. Chem. Phys. 2010, 12, 5737-5740.
19. Overhauser, A. W. Polarization of Nuclei in Metals. Phys. Rev. 1953, 92, 411-415.
20. Carver, T. R.; Slichter, C. P. Polarization of Nuclear Spins in Metals. Phys. Rev. 1953, 92, 212-213.
21. Rossini, A. J.; Widdifield, C. M.; Zagdoun, A.; Lelli, M.; Schwarzwälder, M.; Copéret, C.; Lesage, A.; Emsley, L. Dynamic Nuclear Polarization Enhanced NMR Spectroscopy for Pharmaceutical Formulations. J. Am. Chem. Soc. 2014, 136, 2324-2334.
22. Rossini, A. J.; Zagdoun, A.; Hegner, F.; Schwarzwälder, M.; Gajan, D.; Copéret, C.; Lesage, A.; Emsley, L. Dynamic Nuclear Polarization NMR Spectroscopy of Microcrystalline Solids. J. Am. Chem. Soc. 2012, 134, 16899-16908.
23. Cheng, C.-Y.; Han, S. Dynamic Nuclear Polarization Methods in Solids and Solutions to Explore Membrane Proteins and Membrane Systems. Annu. Rev. Phys. Chem. 2013, 64, 507-532.
24. Kobayashi, T.; Lafon, O.; Lilly Thankamony, A. S.; Slowing, I. I.; Kandel, K.; Carnevale, D.; Vitzthum, V.; Vezin, H.; Amoureux, J.-P.; Bodenhausen, G.; et al. Analysis of Sensitivity Enhancement by Dynamic Nuclear Polarization in Solid-State NMR: A Case Study of Functionalized Mesoporous Materials. Phys. Chem. Chem. Phys. 2013, 15, 5553-5562.
25. Singh, C.; Rai, R. K.; Sinha, N. Experimental Aspect of Solid-State Nuclear Magnetic Resonance Studies of Biomaterials such as Bones. Solid State Nucl. Mag 2013, 54, 18-25.
26. Ladizhansky, V.; Vega, S. Polarization Transfer Dynamics in Lee-Goldburg Cross Polarization Nuclear Magnetic Resonance Experiments on Rotating Solids. J. Chem. Phys. 2000, 112, 7158-7168.
27. Biological Magnetic Resonance Data Bank. http://www.bmrb.wisc.edu (2014).
28. Takahashi, H.; Lee, D.; Dubois, L.; Bardet, M.; Hediger, S.; De Paëpe, G. Rapid Natural-Abundance 2D 13 C-13C Correlation Spectroscopy Using Dynamic Nuclear Polarization Enhanced Solid-State NMR and Matrix-Free Sample Preparation. Angew. Chem., Int. Ed. 2012, 51, 11766-11769.
29. Rosay, M.; Weis, V.; Kreischer, K. E.; Temkin, R. J.; Griffin, R. G. Two-Dimensional 13 C-13 C Correlation Spectroscopy with Magic Angle Spinning and Dynamic Nuclear Polarization. J. Am. Chem. Soc. 2002, 124, 3214-3215.