Fast Magic-Angle Spinning 19F NMR Spectroscopy of HIV-1 Capsid Protein Assemblies
Mingzhang Wang
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
These authors contributed equally.
Search for more papers by this authorManman Lu
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
These authors contributed equally.
Search for more papers by this authorMatthew P. Fritz
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorCaitlin M. Quinn
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Search for more papers by this authorIn-Ja L. Byeon
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorChang-Hyeock Byeon
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorJochem Struppe
Bruker Biospin Corporation, 15 Fortune Drive, Billerica, MA, USA
Search for more papers by this authorWerner Maas
Bruker Biospin Corporation, 15 Fortune Drive, Billerica, MA, USA
Search for more papers by this authorCorresponding Author
Angela M. Gronenborn
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorCorresponding Author
Tatyana Polenova
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorMingzhang Wang
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
These authors contributed equally.
Search for more papers by this authorManman Lu
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
These authors contributed equally.
Search for more papers by this authorMatthew P. Fritz
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorCaitlin M. Quinn
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Search for more papers by this authorIn-Ja L. Byeon
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorChang-Hyeock Byeon
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorJochem Struppe
Bruker Biospin Corporation, 15 Fortune Drive, Billerica, MA, USA
Search for more papers by this authorWerner Maas
Bruker Biospin Corporation, 15 Fortune Drive, Billerica, MA, USA
Search for more papers by this authorCorresponding Author
Angela M. Gronenborn
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Department of Structural Biology, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorCorresponding Author
Tatyana Polenova
Department of Chemistry and Biochemistry, University of Delaware, Brown Laboratories, Newark, DE, 19716 USA
Pittsburgh Center for HIV Protein Interactions, University of Pittsburgh School of Medicine, 1051 Biomedical Science Tower 3, 3501 Fifth Avenue, Pittsburgh, PA, 15261 USA
Search for more papers by this authorGraphical Abstract
Think big: The structural characterization of large biological systems is a challenge by conventional techniques. Fast MAS 19F NMR spectroscopy was found to be an attractive means for investigating protein assemblies (see picture). In the investigation of HIV-1 capsid protein assemblies, high spectral resolution was attained in 19F–19F correlation spectra, permitting the detection of nanometer distances of the order of 20 Å.
Abstract
19F NMR spectroscopy is an attractive and growing area of research with broad applications in biochemistry, chemical biology, medicinal chemistry, and materials science. We have explored fast magic angle spinning (MAS) 19F solid-state NMR spectroscopy in assemblies of HIV-1 capsid protein. Tryptophan residues with fluorine substitution at the 5-position of the indole ring were used as the reporters. The 19F chemical shifts for the five tryptophan residues are distinct, reflecting differences in their local environment. Spin-diffusion and radio-frequency-driven-recoupling experiments were performed at MAS frequencies of 35 kHz and 40–60 kHz, respectively. Fast MAS frequencies of 40–60 kHz are essential for consistently establishing 19F–19F correlations, yielding interatomic distances of the order of 20 Å. Our results demonstrate the potential of fast MAS 19F NMR spectroscopy for structural analysis in large biological assemblies.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
| Filename | Description |
|---|---|
| anie201809060-sup-0001-misc_information.pdf1.1 MB | Supplementary |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1C. M. Quinn, T. Polenova, Q. Rev. Biophys. 2017, 50, e 1.
- 2A. Loquet, N. El Mammeri, J. Stanek, M. Berbon, B. Bardiaux, G. Pintacuda, B. Habenstein, Methods 2018, 138–139, 26–38.
- 3D. Aucoin, D. Camenares, X. Zhao, J. Jung, T. Sato, S. O. Smith, J. Magn. Reson. 2009, 197, 77–86.
- 4R. Linser, B. Bardiaux, V. Higman, U. Fink, B. Reif, J. Am. Chem. Soc. 2011, 133, 5905–5912.
- 5J. S. Retel, A. J. Nieuwkoop, M. Hiller, V. A. Higman, E. Barbet-Massin, J. Stanek, L. B. Andreas, W. T. Franks, B. J. van Rossum, K. R. Vinothkumar, L. Handel, G. G. de Palma, B. Bardiaux, G. Pintacuda, L. Emsley, W. Kuhlbrandt, H. Oschkinat, Nat. Commun. 2017, 8, 2073.
- 6M. T. Colvin, R. Silvers, Q. Z. Ni, T. V. Can, I. Sergeyev, M. Rosay, K. J. Donovan, B. Michael, J. Wall, S. Linse, R. G. Griffin, J. Am. Chem. Soc. 2016, 138, 9663–9674.
- 7M. D. Tuttle, G. Comellas, A. J. Nieuwkoop, D. J. Covell, D. A. Berthold, K. D. Kloepper, J. M. Courtney, J. K. Kim, A. M. Barclay, A. Kendall, W. Wan, G. Stubbs, C. D. Schwieters, V. M. Lee, J. M. George, C. M. Rienstra, Nat. Struct. Mol. Biol. 2016, 23, 409–415.
- 8C. Shi, P. Fricke, L. Lin, V. Chevelkov, M. Wegstroth, K. Giller, S. Becker, M. Thanbichler, A. Lange, Sci. Adv. 2015, 1, e 1501087.
- 9S. Yan, C. Guo, G. Hou, H. Zhang, X. Lu, J. C. Williams, T. Polenova, Proc. Natl. Acad. Sci. USA 2015, 112, 14611–14616.
- 10L. He, B. Bardiaux, M. Ahmed, J. Spehr, R. Konig, H. Lunsdorf, U. Rand, T. Luhrs, C. Ritter, Proc. Natl. Acad. Sci. USA 2016, 113, E 272–281.
- 11S. Wang, R. A. Munro, L. Shi, I. Kawamura, T. Okitsu, A. Wada, S. Y. Kim, K. H. Jung, L. S. Brown, V. Ladizhansky, Nat. Methods 2013, 10, 1007–1012.
- 12S. G. Zech, A. J. Wand, A. E. McDermott, J. Am. Chem. Soc. 2005, 127, 8618–8626.
- 13M. L. Gilchrist, K. Monde, Y. Tomita, T. Iwashita, K. Nakanishi, A. E. McDermott, J. Magn. Reson. 2001, 152, 1–6.
- 14M. Roos, T. Wang, A. A. Shcherbakov, M. Hong, J. Phys. Chem. B 2018, 122, 2900–2911.
- 15Y. G. Gakh, A. A. Gakh, A. M. Gronenborn, Magn. Reson. Chem. 2000, 38, 551–558.
- 16N. G. Sharaf, A. M. Gronenborn in Isotope Labeling of Biomolecules—Labeling Methods, Vol. 565 (Ed.: ), Elsevier Academic Press, San Diego, 2015, pp. 67–95.
- 17P. B. Crowley, C. Kyne, W. B. Monteith, Chem. Commun. 2012, 48, 10681–10683.
- 18R. Campos-Olivas, R. Aziz, G. L. Helms, J. N. S. Evans, A. M. Gronenborn, FEBS Lett. 2002, 517, 55–60.
- 19M. N. Asada, T. Nemoto, H. Mimura, J. Pharm. Sci. 2016, 105, 1233–1238.
- 20F. Zhang, Q. Zhou, G. Yang, L. An, F. Li, J. Wang, Chem. Commun. 2018, 54, 3879–3882.
- 21J. L. Kitevski-LeBlanc, R. S. Prosser, Prog. Nucl. Magn. Reson. Spectrosc. 2012, 62, 1–33.
- 22K. Koch, S. Afonin, M. Ieronimo, M. Berditsch, A. S. Ulrich in Solid State NMR, Vol. 306 (Ed.: ), Springer, Heidelberg, 2012, pp. 89–118.
- 23J. K. Williams, D. Tietze, M. Lee, J. Wang, M. Hong, J. Am. Chem. Soc. 2016, 138, 8143–8155.
- 24U. A. Hellmich, N. Pfleger, C. Glaubitz, Photochem. Photobiol. 2009, 85, 535–539.
- 25K. P. Nartowski, D. Malhotra, L. E. Hawarden, J. Sibik, D. Iuga, J. A. Zeitler, L. Fábián, Y. Z. Khimyak, Angew. Chem. 2016, 128, 9050–9054.
10.1002/ange.201602936 Google Scholar
- 26A. A. Shcherbakov, M. Hong, J. Biomol. NMR 2018, 71, 31–43.
- 27M. Lu, S. Sarkar, M. Wang, J. Kraus, M. Fritz, C. M. Quinn, S. Bai, S. T. Holmes, C. Dybowski, G. P. A. Yap, J. Struppe, I. V. Sergeyev, W. Maas, A. M. Gronenborn, T. Polenova, J. Phys. Chem. B 2018, 122, 6148–6155.
- 28M. Wang, C. M. Quinn, J. R. Perilla, H. Zhang, R. Shirra, Jr., G. Hou, I. J. Byeon, C. L. Suiter, S. Ablan, E. Urano, T. J. Nitz, C. Aiken, E. O. Freed, P. Zhang, K. Schulten, A. M. Gronenborn, T. Polenova, Nat. Commun. 2017, 8, 1779.
- 29P. Zhang, X. Meng, G. Zhao, Methods Mol. Biol. 2013, 955, 381–399.
- 30C. M. Quinn, M. Lu, C. L. Suiter, G. Hou, H. Zhang, T. Polenova, Prog. Nucl. Magn. Reson. Spectrosc. 2015, 86–87, 21–40.
- 31M. J. Bayro, B. Chen, W. M. Yau, R. Tycko, J. Mol. Biol. 2014, 426, 1109–1127.
- 32N. Bloembergen, Physica 1949, 15, 386–426.
- 33A. E. Bennett, C. M. Rienstra, J. M. Griffiths, W. Zhen, P. T. J. Lansbury, R. G. Griffin, J. Chem. Phys. 1998, 108, 9463–9479.
- 34I. J. L. Byeon, G. J. Hou, Y. Han, C. L. Suiter, J. Ahn, J. Jung, C. H. Byeon, A. M. Gronenborn, T. Polenova, J. Am. Chem. Soc. 2012, 134, 6455–6466.
- 35S. Du, L. Betts, R. Yang, H. Shi, J. Concel, J. Ahn, C. Aiken, P. Zhang, J. I. Yeh, J. Mol. Biol. 2011, 406, 371–386.
- 36A. T. Gres, K. A. Kirby, V. N. KewalRamani, J. J. Tanner, O. Pornillos, S. G. Sarafianos, Science 2015, 349, 99–103.
- 37S. Tang, T. Murakami, B. E. Agresta, S. Campbell, E. O. Freed, J. G. Levin, J. Virol. 2001, 75, 9357–9366.
- 38C. T. Lemke, S. Titolo, U. von Schwedler, N. Goudreau, J. F. Mercier, E. Wardrop, A. M. Faucher, R. Coulombe, S. S. Banik, L. Fader, A. Gagnon, S. H. Kawai, J. Rancourt, M. Tremblay, C. Yoakim, B. Simoneau, J. Archambault, W. I. Sundquist, S. W. Mason, J. Virol. 2012, 86, 6643–6655.
- 39O. Pornillos, B. K. Ganser-Pornillos, S. Banumathi, Y. Hua, M. Yeager, J. Mol. Biol. 2010, 401, 985–995.
- 40E. R. deAzevedo, W. G. Hu, T. J. Bonagamba, K. Schmidt-Rohr, J. Am. Chem. Soc. 1999, 121, 8411–8412.
- 41G. Hou, S. Yan, J. Trebosc, J. P. Amoureux, T. Polenova, J. Magn. Reson. 2013, 232, 18–30.
- 42K.-Y. Huang, A. B. Siemer, A. E. McDermott, J. Magn. Reson. 2011, 208, 122–127.
