Articles | Volume 2, issue 2
https://doi.org/10.5194/mr-2-795-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Special issue:
https://doi.org/10.5194/mr-2-795-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
09 Nov 2021
Research article |
| 09 Nov 2021
| 09 Nov 2021
Fluorine NMR study of proline-rich sequences using fluoroprolines
Davy Sinnaeve
CORRESPONDING AUTHOR
Univ. Lille, Inserm, Institut Pasteur de Lille, CHU Lille, U1167 – Risk Factors and Molecular Determinants of
Aging-Related Diseases (RID-AGE), 59000 Lille, France
CNRS, ERL9002 – Integrative Structural Biology, 59000 Lille, France
Abir Ben Bouzayene
Department of Integrative Structural Biology, IGBMC, University of Strasbourg, Inserm U1258, CNRS UMR 7104, 1 rue Laurent Fries, 67404
Illkirch, France
Emile Ottoy
Department of Organic and Macromolecular Chemistry, Ghent University,
Campus Sterre, S4, Krijgslaan 281, 9000 Ghent, Belgium
Gert-Jan Hofman
Department of Organic and Macromolecular Chemistry, Ghent University,
Campus Sterre, S4, Krijgslaan 281, 9000 Ghent, Belgium
School of Chemistry, University of Southampton, Southampton SO17 1BJ,
United Kingdom
Eva Erdmann
Department of Integrative Structural Biology, IGBMC, University of Strasbourg, Inserm U1258, CNRS UMR 7104, 1 rue Laurent Fries, 67404
Illkirch, France
Bruno Linclau
School of Chemistry, University of Southampton, Southampton SO17 1BJ,
United Kingdom
Ilya Kuprov
School of Chemistry, University of Southampton, Southampton SO17 1BJ,
United Kingdom
José C. Martins
Department of Organic and Macromolecular Chemistry, Ghent University,
Campus Sterre, S4, Krijgslaan 281, 9000 Ghent, Belgium
Vladimir Torbeev
Institut de Science et d'Ingénierie Supramoléculaires (ISIS),
International Center for Frontier Research in Chemistry (icFRC), University of Strasbourg,
CNRS UMR 7006, 67000 Strasbourg, France
Bruno Kieffer
CORRESPONDING AUTHOR
Department of Integrative Structural Biology, IGBMC, University of Strasbourg, Inserm U1258, CNRS UMR 7104, 1 rue Laurent Fries, 67404
Illkirch, France
Related subject area
Field: Liquid-state NMR | Topic: Applications – biological macromolecules
NMR side-chain assignments of the Crimean–Congo hemorrhagic fever virus glycoprotein n cytosolic domain
Facilitating the structural characterisation of non-canonical amino acids in biomolecular NMR
Site-selective generation of lanthanoid binding sites on proteins using 4-fluoro-2,6-dicyanopyridine
Imatinib disassembles the regulatory core of Abelson kinase by binding to its ATP site and not by binding to its myristoyl pocket
Localising nuclear spins by pseudocontact shifts from a single tagging site
Localising individual atoms of tryptophan side chains in the metallo-β-lactamase IMP-1 by pseudocontact shifts from paramagnetic lanthanoid tags at multiple sites
Analysis of conformational exchange processes using methyl-TROSY-based Hahn echo measurements of quadruple-quantum relaxation
Anomalous amide proton chemical shifts as signatures of hydrogen bonding to aromatic sidechains
Rapid assessment of Watson–Crick to Hoogsteen exchange in unlabeled DNA duplexes using high-power SELOPE imino 1H CEST
High-affinity tamoxifen analogues retain extensive positional disorder when bound to calmodulin
Structural polymorphism and substrate promiscuity of a ribosome-associated molecular chaperone
Small-molecule inhibitors of the PDZ domain of Dishevelled proteins interrupt Wnt signalling
Real-time nuclear magnetic resonance spectroscopy in the study of biomolecular kinetics and dynamics
The long-standing relationship between paramagnetic NMR and iron–sulfur proteins: the mitoNEET example. An old method for new stories or the other way around?
Conformational features and ionization states of Lys side chains in a protein studied using the stereo-array isotope labeling (SAIL) method
Fragile protein folds: sequence and environmental factors affecting the equilibrium of two interconverting, stably folded protein conformations
Towards resolving the complex paramagnetic nuclear magnetic resonance (NMR) spectrum of small laccase: assignments of resonances to residue-specific nuclei
Phosphoserine for the generation of lanthanide-binding sites on proteins for paramagnetic nuclear magnetic resonance spectroscopy
Louis Brigandat, Maëlys Laux, Caroline Marteau, Laura Cole, Anja Böckmann, Lauriane Lecoq, Marie-Laure Fogeron, and Morgane Callon
Magn. Reson., 5, 95–101, https://doi.org/10.5194/mr-5-95-2024, https://doi.org/10.5194/mr-5-95-2024, 2024
Short summary
Short summary
We used NMR to sequentially assign the side-chain resonances of the cytosolic domain of glycoprotein n of the Crimean–Congo hemorrhagic fever virus. The combination of cell-free protein synthesis with high-field NMR and artificial intelligence approaches facilitated a time- and effort-efficient approach. Our results will be harnessed to study the membrane-bound form of the domain and its interactions with virulence factors, which will ultimately help to understand their role in disease.
Sarah Kuschert, Martin Stroet, Yanni Ka-Yan Chin, Anne Claire Conibear, Xinying Jia, Thomas Lee, Christian Reinhard Otto Bartling, Kristian Strømgaard, Peter Güntert, Karl Johan Rosengren, Alan Edward Mark, and Mehdi Mobli
Magn. Reson., 4, 57–72, https://doi.org/10.5194/mr-4-57-2023, https://doi.org/10.5194/mr-4-57-2023, 2023
Short summary
Short summary
The 20 genetically encoded amino acids provide the basis for most proteins and peptides that make up the machinery of life. This limited repertoire is vastly expanded by the introduction of non-canonical amino acids (ncAAs). Studying the structure of protein-containing ncAAs requires new computational representations that are compatible with existing modelling software. We have developed an online tool for this to aid future structural studies of this class of complex biopolymer.
Sreelakshmi Mekkattu Tharayil, Mithun C. Mahawaththa, Akiva Feintuch, Ansis Maleckis, Sven Ullrich, Richard Morewood, Michael J. Maxwell, Thomas Huber, Christoph Nitsche, Daniella Goldfarb, and Gottfried Otting
Magn. Reson., 3, 169–182, https://doi.org/10.5194/mr-3-169-2022, https://doi.org/10.5194/mr-3-169-2022, 2022
Short summary
Short summary
Having shown that tagging a protein at a single site with different lanthanoid complexes delivers outstanding structural information at a selected site of a protein (such as active sites and ligand binding sites), we now present a simple way by which different lanthanoid complexes can be assembled on a highly solvent-exposed cysteine residue. Furthermore, the chemical assembly is selective for selenocysteine, if a selenocysteine residue can be introduced into the protein of interest.
Stephan Grzesiek, Johannes Paladini, Judith Habazettl, and Rajesh Sonti
Magn. Reson., 3, 91–99, https://doi.org/10.5194/mr-3-91-2022, https://doi.org/10.5194/mr-3-91-2022, 2022
Short summary
Short summary
We show here that binding of the anticancer drug imatinib to the ATP site of Abelson kinase and not binding to its allosteric site coincides with the opening of the kinase regulatory core at nanomolar concentrations. This has implications for the understanding of Abelson’s kinase regulation and activity during medication as well as for the design of new Abelson kinase inhibitors.
Henry W. Orton, Elwy H. Abdelkader, Lydia Topping, Stephen J. Butler, and Gottfried Otting
Magn. Reson., 3, 65–76, https://doi.org/10.5194/mr-3-65-2022, https://doi.org/10.5194/mr-3-65-2022, 2022
Short summary
Short summary
Installing a tag containing a paramagnetic metal ion on a protein can lead to large changes (pseudocontact shifts) in the resonances observed in NMR spectra. These are easily measured and contain valuable long-range structural information. The present work shows that a single tagging site furnished with different tags can be sufficient to localise atoms in proteins with high accuracy. In fact, this strategy works almost as well as the same number of tags distributed over multiple tagging sites.
Henry W. Orton, Iresha D. Herath, Ansis Maleckis, Shereen Jabar, Monika Szabo, Bim Graham, Colum Breen, Lydia Topping, Stephen J. Butler, and Gottfried Otting
Magn. Reson., 3, 1–13, https://doi.org/10.5194/mr-3-1-2022, https://doi.org/10.5194/mr-3-1-2022, 2022
Short summary
Short summary
This paper explores a method for determining the solution structure of a solvent-exposed polypeptide segment (the L3 loop), which is next to the active site of the penicillin-degrading enzyme IMP-1. Tagging three different sites on the protein with paramagnetic metal ions allowed positioning of the L3 loop with atomic resolution. It was found that the method was more robust when omitting data obtained with different metal ions if obtained with the same tag at the same tagging site.
Christopher A. Waudby and John Christodoulou
Magn. Reson., 2, 777–793, https://doi.org/10.5194/mr-2-777-2021, https://doi.org/10.5194/mr-2-777-2021, 2021
Short summary
Short summary
We describe a suite of experiments that exploit field-dependent relaxation measurements of four-spin transitions in methyl groups to characterise chemical exchange processes and which can be used as an alternative or complement to CPMG relaxation dispersion measurements. We show that these four-spin transitions benefit from the methyl TROSY effect and so provide a unique combination of slow intrinsic relaxation and high sensitivity to chemical exchange.
Kumaran Baskaran, Colin W. Wilburn, Jonathan R. Wedell, Leonardus M. I. Koharudin, Eldon L. Ulrich, Adam D. Schuyler, Hamid R. Eghbalnia, Angela M. Gronenborn, and Jeffrey C. Hoch
Magn. Reson., 2, 765–775, https://doi.org/10.5194/mr-2-765-2021, https://doi.org/10.5194/mr-2-765-2021, 2021
Short summary
Short summary
The Biological Magnetic Resonance Data Bank (BMRB) has been used to identify overall trends, for example, the relationship between chemical shift and backbone conformation. The BMRB archive has grown so that statistical outliers are sufficiently numerous to afford insights into unusual or unique structural features in proteins. We analyze amide proton chemical shift outliers to gain insights into the occurrence of hydrogen bonds between an amide NH and the p-pi cloud of aromatic sidechains.
Bei Liu, Atul Rangadurai, Honglue Shi, and Hashim M. Al-Hashimi
Magn. Reson., 2, 715–731, https://doi.org/10.5194/mr-2-715-2021, https://doi.org/10.5194/mr-2-715-2021, 2021
Short summary
Short summary
There is growing interest in mapping exchange dynamics between Watson–Crick and Hoogsteen conformations across different DNA contexts. However, current methods are ill-suited for measurements at a large scale because they require isotopically enriched samples. We report that Hoogsteen dynamics can be measured on unlabeled samples using 1H CEST experiments, which have higher throughput and lower cost relative to conventional methods and also provide new insights into Hoogsteen dynamics.
Lilia Milanesi, Clare R. Trevitt, Brian Whitehead, Andrea M. Hounslow, Salvador Tomas, Laszlo L. P. Hosszu, Christopher A. Hunter, and Jonathan P. Waltho
Magn. Reson., 2, 629–642, https://doi.org/10.5194/mr-2-629-2021, https://doi.org/10.5194/mr-2-629-2021, 2021
Short summary
Short summary
The overall aim of the study is to provide a basis from which to improve the ability of tamoxifen family drugs to reduce the activity of a secondary target protein, calmodulin, during tumour development. The main conclusion is that the binding of a tamoxifen analogue is quite unlike that of other anti-calmodulin compounds in that two drug molecules bring the two domains of calmodulin into close proximity, but they are not fixed in orientation relative to the protein.
Chih-Ting Huang, Yei-Chen Lai, Szu-Yun Chen, Meng-Ru Ho, Yun-Wei Chiang, and Shang-Te Danny Hsu
Magn. Reson., 2, 375–386, https://doi.org/10.5194/mr-2-375-2021, https://doi.org/10.5194/mr-2-375-2021, 2021
Short summary
Short summary
Trigger factor (TF) is a conserved bacterial molecular chaperone that exists in a monomer–dimer equilibrium in solution. It binds to the ribosome as a monomer to facilitate folding of nascent polypeptide chains. We showed that dimeric TF exhibits distinct domain dynamics and conformational polymorphism and that TF contains multiple substrate binding sites that are only accessible in its monomeric form. The equilibrium of TF in different oligomeric states may serve as a regulatory mechanism.
Nestor Kamdem, Yvette Roske, Dmytro Kovalskyy, Maxim O. Platonov, Oleksii Balinskyi, Annika Kreuchwig, Jörn Saupe, Liang Fang, Anne Diehl, Peter Schmieder, Gerd Krause, Jörg Rademann, Udo Heinemann, Walter Birchmeier, and Hartmut Oschkinat
Magn. Reson., 2, 355–374, https://doi.org/10.5194/mr-2-355-2021, https://doi.org/10.5194/mr-2-355-2021, 2021
Short summary
Short summary
The Wnt signalling pathway plays a major role in prevention of cancer, whereby the protein Dishevelled connects from the transmembrane receptor Frizzled to downstream effectors via its PDZ domain. Here, cycles of chemical synthesis and structural biology are applied to develop PDZ ligands that block the Frizzled–Dishevelled interaction using NMR for screening, in ligand development, and for deriving structure–activity relationships. Cellular reporter assays demonstrate their efficacy.
György Pintér, Katharina F. Hohmann, J. Tassilo Grün, Julia Wirmer-Bartoschek, Clemens Glaubitz, Boris Fürtig, and Harald Schwalbe
Magn. Reson., 2, 291–320, https://doi.org/10.5194/mr-2-291-2021, https://doi.org/10.5194/mr-2-291-2021, 2021
Short summary
Short summary
The folding, refolding and misfolding of biomacromolecules including proteins, DNA and RNA is an important area of biophysical research to understand functional and disease states of a cell. NMR spectroscopy provides detailed insight, with both high time and atomic resolution. These experiments put stringent requirements on signal-to-noise for often irreversible folding reactions. The review describes methodological approaches and highlights key applications.
Francesca Camponeschi, Angelo Gallo, Mario Piccioli, and Lucia Banci
Magn. Reson., 2, 203–221, https://doi.org/10.5194/mr-2-203-2021, https://doi.org/10.5194/mr-2-203-2021, 2021
Short summary
Short summary
The iron–sulfur cluster binding properties of human mitoNEET have been investigated by 1D and 2D 1H paramagnetic NMR spectroscopy. The NMR spectra of both oxidized and reduced mitoNEET are significantly different from those reported previously for other [Fe2S2] proteins. Our findings revealed the unique electronic properties of mitoNEET and suggests that the specific electronic structure of the cluster possibly drives the functional properties of different [Fe2S2] proteins.
Mitsuhiro Takeda, Yohei Miyanoiri, Tsutomu Terauchi, and Masatsune Kainosho
Magn. Reson., 2, 223–237, https://doi.org/10.5194/mr-2-223-2021, https://doi.org/10.5194/mr-2-223-2021, 2021
Short summary
Short summary
Although both the hydrophobic aliphatic chain and hydrophilic ζ-amino group of the lysine side chain presumably contribute to the structures and functions of proteins, the dual nature of the lysine residue has not been fully understood yet, due to the lack of appropriate methods to acquire comprehensive information on its long consecutive methylene chain at the atomic scale. We describe herein a novel strategy to address the current situation using nuclear magnetic resonance spectroscopy.
Xingjian Xu, Igor Dikiy, Matthew R. Evans, Leandro P. Marcelino, and Kevin H. Gardner
Magn. Reson., 2, 63–76, https://doi.org/10.5194/mr-2-63-2021, https://doi.org/10.5194/mr-2-63-2021, 2021
Short summary
Short summary
While most proteins adopt one conformation, several interconvert between two or more very different structures. Knowing how sequence changes and small-molecule binding can control this behavior is essential for both understanding biology and inspiring new “molecular switches” which can control cellular pathways. This work contributes by examining these topics in the ARNT protein, showing that features of both the folded and unfolded states contribute to the interconversion process.
Rubin Dasgupta, Karthick B. S. S. Gupta, Huub J. M. de Groot, and Marcellus Ubbink
Magn. Reson., 2, 15–23, https://doi.org/10.5194/mr-2-15-2021, https://doi.org/10.5194/mr-2-15-2021, 2021
Short summary
Short summary
A method is demonstrated that can help in sequence-specific NMR signal assignment to nuclear spins near a strongly paramagnetic metal in an enzyme. A combination of paramagnetically tailored NMR experiments and second-shell mutagenesis was used to attribute previously observed chemical exchange processes in the active site of laccase to specific histidine ligands. The signals of nuclei close to the metal can be used as spies to unravel the role of motions in the catalytic process.
Sreelakshmi Mekkattu Tharayil, Mithun Chamikara Mahawaththa, Choy-Theng Loh, Ibidolapo Adekoya, and Gottfried Otting
Magn. Reson., 2, 1–13, https://doi.org/10.5194/mr-2-1-2021, https://doi.org/10.5194/mr-2-1-2021, 2021
Short summary
Short summary
A new way is presented for creating lanthanide binding sites on proteins using site-specifically introduced phosphoserine residues. The paramagnetic effects of lanthanides generate long-range effects, which contain structural information and are readily measured by NMR spectroscopy. Excellent correlations between experimentally observed and back-calculated pseudocontact shifts attest to very good immobilization of the lanthanide ions relative to the proteins.
Cited articles
Ahuja, P., Cantrelle, F. X., Huvent, I., Hanoulle, X., Lopez, J., Smet, C.,
Wieruszeski, J. M., Landrieu, I., and Lippens, G.: Proline Conformation in a
Functional Tau Fragment, J. Mol. Biol., 428, 79–91, https://doi.org/10.1016/j.jmb.2015.11.023, 2016.
Aufiero, M. and Gilmour, R.: Informing Molecular Design by Stereoelectronic
Theory: The Fluorine Gauche Effect in Catalysis, Acc. Chem. Res., 51,
1701–1710, https://doi.org/10.1021/acs.accounts.8b00192, 2018.
Behrendt, R. P., White, P., and Offer, J.: Advances in Fmoc solid-phase peptide
synthesis, J. Pept. Sci., 22, 4–27, https://doi.org/10.1002/psc.2836, 2016.
Berger, A. A., Völler, J.-S., Budisa, N., and Koksch, B.: Deciphering the
Fluorine Code – The Many Hats Fluorine Wears in a Protein Environment, Acc.
Chem. Res., 50, 2093–2103, https://doi.org/10.1021/acs.accounts.7b00226, 2017.
Best, R. B., Merchant, K. A., Gopich, I. V., Schuler, B., Bax, A., and Eaton W.
A.: Effect of flexibility and cis residues in single-molecule FRET studies
of polyproline, P. Natl. Acad. Sci. USA, 104, 18964–18969, https://doi.org/10.1073/pnas.0709567104, 2007.
Boeszoermenyi, A., Chhabra, S., Dubey, A., Radeva, D. L., Burdzhiev, N. T.,
Chanev, C. D., Petrov, O. I., Gelev, V. M., Zhang, M., Anklin, C., Kovacs,
H., Wagner, G., Kuprov, I., Takeuchi, K., and Arthanari, H.: Aromatic 19F-
13C TROSY: a background-free approach to probe biomolecular structure,
function, and dynamics, Nat. Methods., 16, 333–340, https://doi.org/10.1038/s41592-019-0334-x, 2019.
Boeszoermenyi, A., Ogórek, B., Jain, A., Arthanari, H., and Wagner, G.: The
precious fluorine on the ring: fluorine NMR for biological systems, J.
Biomol. NMR., 74, 365–379, https://doi.org/10.1007/s10858-020-00331-z, 2020.
Bondi, A.: Van der waals volumes and radii, J. Phys. Chem. 68, 441–451,
https://doi.org/10.1021/j100785a001, 1964.
Borgogno, A. and Ruzza, P.: The impact of either 4-R-hydroxyproline or
4-R-fluoroproline on the conformation and SH3m-cort binding of HPK1
proline-rich peptide, Amino Acids., 44, 607–614, https://doi.org/10.1007/s00726-012-1383-y, 2013.
Chaiken, I. M., Freedman, M. H., Lyerla, J. R., and Cohen, J. S.: Preparation
and studies of 19F-labeled and enriched 13 C-labeled semisynthetic
ribonuclease-S' analogues, J. Biol. Chem., 248, 884–891, https://doi.org/10.1016/s0021-9258(19)44350-0, 1973.
Chiron, L., Coutouly, M.-A., Starck, J.-P., Rolando, C., and Delsuc, M.-A: SPIKE
a Processing Software dedicated to Fourier Spectroscopies, arXiv [preprint], arXiv:1608.06777, 2016.
Cordero, B., Gomez, V., Platero-Prats, A. E., Reves, M., Echeverrıa, J.,
Cremades, E., Barragan, F., and Alvarez, S.: Covalent radii revisited, J. Chem.
Soc. Dalt. Trans., 21, 2832–2838, https://doi.org/10.1039/b801115j, 2008.
Crowley, P. B., Kyne, C., and Monteith, W. B.: Simple and inexpensive
incorporation of 19F-Tryptophan for protein NMR spectroscopy, Chem.
Commun., 48, 10681–10683, https://doi.org/10.1039/c2cc35347d,
2012.
Dalvit, C. and Piotto, M.: 19F NMR transverse and longitudinal relaxation
filter experiments for screening: a theoretical and experimental analysis,
Magn. Reson. Chem., 55, 106–114, https://doi.org/10.1002/mrc.4500, 2017.
Debelouchina, G. T. and Muir, T. W.: A molecular engineering toolbox for the
structural biologist, Q. Rev. Biophys., 50, e7, https://doi.org/10.1017/S0033583517000051, 2017.
Deng, W., Cheeseman, J. R., and Frisch, M. J.: Calculation of nuclear spin-spin
coupling constants of molecules with first and second row atoms in study of
basis set dependence, J. Chem. Theor. Comput., 2, 1028–1037, https://doi.org/10.1021/ct600110u, 2006.
DeRider, M. L., Wilkens, S. J., Waddell, M. J., Bretscher, L. E., Weinhold,
F., Raines, R. T., and Markley, J. L.: Collagen stability: Insights from NMR
spectroscopic and hybrid density functional computational investigations of
the effect of electronegative substituents on prolyl ring conformations, J.
Am. Chem. Soc., 124, 2497–2505, https://doi.org/10.1021/ja0166904, 2002.
Dietz D., Kubyshkin V., and Budisa N.: Applying gamma-Substituted Prolines in
the Foldon Peptide: Polarity Contradicts Preorganization, Chembiochem., 16,
403–406, https://doi.org/10.1002/cbic.201402654, 2015.
Eberhardt, E. S., Panasik, N., and Raines, R. T.: Inductive effects on the
energetics of prolyl peptide bond isomerization: Implications for collagen
folding and stability, J. Am. Chem. Soc., 118, 12261–12266, https://doi.org/10.1021/ja9623119, 1996.
Edwards, L. J., Savostyanov, D. V., Welderufael, Z. T., Lee, D., and Kuprov, I.:
Quantum mechanical NMR simulation algorithm for protein-size spin systems,
J. Magn. Reson., 243, 107–113, https://doi.org/10.1016/j.jmr.2014.04.002, 2014.
Eftekharzadeh, B., Piai, A., Chiesa, G., Mungianu, D., Garcia, J.,
Pierattelli, R., Felli, I. C., and Salvatella, X.: Sequence Context Influences the
Structure and Aggregation Behavior of a PolyQ Tract, Biophys. J.,
110, 2361–2366, https://doi.org/10.1016/j.bpj.2016.04.022, 2016.
Evanics, F., Bezsonova,I., Marsh, J., Kitevski, J. L., Forman-Kay, J. D., and
Prosser, R. S.: Tryptophan Solvent Exposure in Folded and Unfolded States of
an SH3 Domain by 19F and 1H NMR, Biochemistry, 129, 1826–1835, https://doi.org/10.1021/bi061389r, 2007.
Fäcke, T. and Berger, S.: SERF, a New Method for H, H Spin-Coupling
Measurement in Organic Chemistry, J. Magn. Reson. Ser. A.,113, 114–116,
https://doi.org/10.1006/jmra.1995.1063, 1995.
Farrow, N. A., Zhang, O., Forman-Kay, J. D., and Kay, L. E.: Comparison of the
Backbone Dynamics of a Folded and an Unfolded SH3 Domain Existing in
Equilibrium in Aqueous Buffer, Biochemistry, 34, 868–878,
https://doi.org/10.1021/bi00003a021, 1995.
Ferreiro, D. U., Komives, E. A., and Wolynes, P. G.: Frustration in
biomolecules, Q. Rev. Biophys., 47, 285–363, https://doi.org/10.1017/S0033583514000092, 2014.
Gee, C. T., Arntson, K. E., Urick, A. K., Mishra, N. K., Hawk, L. M. L.,
Wisniewski, A. J., and Pomerantz, W. C. K.: Protein-observed 19F-NMR for
fragment screening, affinity quantification and druggability assessment,
Nat. Protoc., 11, 1414–1427, https://doi.org/10.1038/nprot.2016.079, 2016.
Gerig, J. and McLeod, R.: Conformations of cis- and trans-4-Fluoroproline in
Aqueous Solution, J. Am. Chem. Soc., 17, 4788–4795, https://doi.org/10.1021/ja00798a046, 1973.
Gillis, E. P., Eastman, K. J., Hill, M. D., Donnelly, D. J., and Meanwell, N.
A.: Applications of Fluorine in Medicinal Chemistry, J. Med. Chem., 58,
8315–8359, https://doi.org/10.1021/acs.jmedchem.5b00258, 2015.
Gimenez, D., Phelan, A., Murphy, C. D., and Cobb S. L.: 19F NMR as a tool
in chemical biology, J. Org. Chem., 17, 293–318, https://doi.org/10.3762/BJOC.17.28, 2021.
Goodwin, D. L. and Kuprov, I.: Auxiliary matrix formalism for interaction
representation transformations, optimal control, and spin relaxation
theories, J. Chem. Phys., 143, 084113, https://doi.org/10.1063/1.4928978, 2015.
Hofman, G. J., Ottoy, E., Light, M., Kieffer, B., Kuprov, I., Martins, J. C.,
Sinnaeve, D., Linclau, B.: Minimising conformational bias in fluoroprolines
through vicinal difluorination, Chem. Commun., 54, 5118–5121, https://doi.org/10.1039/c8cc01493k, 2018.
Hofman, G. J., Ottoy, E., Light, M. E., Kieffer, B., Martins, J. C., Kuprov,
I., Sinnaeve, D., and Linclau, B.: Synthesis and Conformational Properties of
3,4-Difluoro- l -prolines, J. Org. Chem., 84, 3100–3120, https://doi.org/10.1021/acs.joc.8b02920, 2019.
Hogben, H. J., Krzystyniak, M., Charnock, G. T. P., Hore, P. J., and Kuprov, I.:
Spinach – A software library for simulation of spin dynamics in large spin
systems, J. Magn. Reson., 208, 179–194, https://doi.org/10.1016/j.jmr.2010.11.008, 2011.
Holmgren, S. K., Taylor, K. M., Bretscher, L. E., and Raines, R. T.: Code for
Collagen's Stability Deciphered, Nature, 392, 666–667, https://doi.org/10.1038/33573, 1998.
Horng, J.-C. and Raines, R. T.: Stereoelectronic effects on polyproline
conformation, Protein Sci., 15, 74–83, https://doi.org/10.1110/ps.051779806, 2006.
Jiji, A. C., Shine, A., and Vijayan, V.: Direct Observation of
Aggregation-Induced Backbone Conformational Changes in Tau Peptides, Angew.
Chem. Int. Edit., 55, 11562–11566, https://doi.org/10.1002/anie.201606544, 2016.
Kang, Y. K.: Puckering transition of proline residue in water, J. Phys.
Chem. B., 111, 10550–10556, https://doi.org/10.1021/jp073411b,
2007.
Kieffer, B., Ben Bouzayene, A., and Sinnaeve, D.: Fluorine NMR study of proline-rich sequences using fluoroprolines, Zenodo [data set], https://doi.org/10.5281/zenodo.5548094, 2021.
Kim, T. H., Mehrabi, P., Ren, Z., Sljoka, A., Ing, C., Bezginov, A., Ye, L.,
Pomès, R., Prosser, R. S., and Pai, E. F.: The role of dimer asymmetry and
protomer dynamics in enzyme catalysis, Science, 355, 6–11, https://doi.org/10.1126/science.aag2355, 2017.
Kitevski-LeBlanc, J. L. and Prosser, R. S.: Current applications of 19F
NMR to studies of protein structure and dynamics, Prog. Nucl. Magn. Reson.
Spectrosc., 62, 1–33, https://doi.org/10.1016/j.pnmrs.2011.06.003, 2012.
Kohler, C., Recht, R., Quinternet, M., de Lamotte, F., Delsuc, M.-A., and
Kieffer, B.: Accurate Protein–Peptide Titration Experiments by Nuclear
Magnetic Resonance Using Low-Volume Samples, Methods Mol. Biol., 1286,
279–296, https://doi.org/10.1007/978-1-4939-2447-9_22, 2015.
Kovrigin, E. L.: NMR line shapes and multi-state binding equilibria, J.
Biomol. NMR., 53, 257–270, https://doi.org/10.1007/s10858-012-9636-3, 2012.
Kubyshkin, V., Davis, R., and Budisa, N.: Biochemistry of fluoroprolines: The
prospect of making fluorine a bioelement, J. Org. Chem., 17, 439–450,
https://doi.org/10.3762/BJOC.17.40, 2021.
Kuprov, I.: Diagonalization-free implementation of spin relaxation theory
for large spin systems, J. Magn. Reson., 209, 31–38, https://doi.org/10.1016/j.jmr.2010.12.004, 2011.
Kuprov, I., Wagner-Rundell, N., and Hore, P. J.: Polynomially scaling spin
dynamics simulation algorithm based on adaptive state-space restriction, J.
Magn. Reson., 189, 241–250, https://doi.org/10.1016/j.jmr.2007.09.014, 2007.
Lalevée, S., Bour, G., Quinternet, M., Samarut, E., Kessler, P.,
Vitorino, M., Bruck, N., Delsuc, M.-A., Vonesch, J.-L., Kieffer, B., and
Rochette-Egly, C.: Vinexinβ, an atypical “sensor” of retinoic acid
receptor γ signaling: union and sequestration, separation, and
phosphorylation, FASEB J., 24, 4523–4534, https://doi.org/10.1096/fj.10-160572, 2010.
Liu, J. J., Horst, R., Katritch, V., Stevens, R. C., and Wüthrich, K.:
Biased signaling pathways in β2-adrenergic receptor characterized by
19F-NMR, Science, 335, 1106–1110, https://doi.org/10.1126/science.1215802, 2012.
London, F.: Théorie quantique des courants interatomiques dans les
combinaisons aromatiques, J. Phys. Le Radium., 8, 397–409, https://doi.org/10.1051/jphysrad:01937008010039700, 1937.
London, R. E.: On the Interpretation of 13C Spin-Lattice Relaxation
Resulting from Ring Puckering in Proline, J. Am. Chem. Soc., 100,
2678–2685, https://doi.org/10.1021/ja00477a018, 1978.
Lu, M., Ishima, R., Polenova, T., and Gronenborn, A. M.: 19F NMR relaxation
studies of fluorosubstituted tryptophans, J. Biomol. NMR., 73, 401–409,
https://doi.org/10.1007/s10858-019-00268-y, 2019.
Marenich, A. V., Cramer, C. J., and Truhlar, D. G.: Universal solvation model
based on solute electron density and on a continuum model of the solvent
defined by the bulk dielectric constant and atomic surface tensions, J.
Phys. Chem. B., 113, 6378–6396, https://doi.org/10.1021/jp810292n, 2009.
Mei, H., Han, J., Klika, K. D., Izawa, K., Sato, T., Meanwell, N. A., and
Soloshonok V. A.: Applications of fluorine-containing amino acids for drug
design, Eur. J. Med. Chem., 186, 111826, https://doi.org/10.1016/j.ejmech.2019.111826, 2020.
Muttenthaler, M., King, G. F., Adams, D. J., and Alewood, P. F.: Trends in
peptide drug discovery, Nat. Rev. Drug Discov., 20, 309–325, https://doi.org/10.1038/s41573-020-00135-8, 2021.
Newberry, R. W. and Raines, R. T.: 4-Fluoroprolines: Conformational Analysis
and Effects on the Stability and Folding of Peptides and Proteins, Topics in
Heterocyclic Chemistry: Peptidomimetics I, 48, 1–11, https://doi.org/10.1007/7081_2015_196, 2016.
Odar, C., Winkler, M., and Wiltschi, B.: Fluoro amino acids: A rarity in nature,
yet a prospect for protein engineering, Biotechnol. J., 10, 427–446,
https://doi.org/10.1002/biot.201400587, 2015.
O'Hagan, D.: Understanding organofluorine chemistry. An introduction to the
C–F bond, Chem. Soc. Rev., 37, 308–319, https://doi.org/10.1039/b711844a, 2008.
O'Hagan, D.: Organofluorine chemistry: Synthesis and conformation of vicinal
fluoromethylene motifs, J. Org. Chem., 77, 3689–3699, https://doi.org/10.1021/jo300044q, 2012.
Overbeck, J. H., Kremer, W., and Sprangers, R.: A suite of 19F based
relaxation dispersion experiments to assess biomolecular motions, J. Biomol.
NMR, 74, 753–766, https://doi.org/10.1007/s10858-020-00348-4,
2020.
Panasik, N., Eberhardt, E. S., Edison, A. S., Powell, D. R., and Raines, R. T.:
Inductive effects on the structure of proline residues, Int. J. Pept.
Protein Res. 44, 262–269, https://doi.org/10.1111/j.1399-3011.1994.tb00169.x, 1994.
Pell, A. J. and Keeler, J.: Two-dimensional J-spectra with absorption-mode
lineshapes, J. Magn. Reson., 189, 293–299, https://doi.org/10.1016/j.jmr.2007.09.002, 2007.
Peterson, K. A. and Dunning, T. H.: Accurate correlation consistent basis sets
for molecular core-valence correlation effects: The second row atoms Al-Ar,
and the first row atoms B-Ne revisited, J. Chem. Phys., 117, 10548–10560,
https://doi.org/10.1063/1.1520138, 2002.
Rastinejad, F., Evilia, C., and Lu, P.: Studies of Nucleic Acids and Their
Protein Interactions by 19F NMR, Methods Enzymol., 261,
560–575, https://doi.org:10.1016/s0076-6879(95)61025-1,
1995.
Redfield, A. G.: On the Theory of Relaxation Processes, IBM J. Res. Dev., 1,
19–31, https://doi.org/10.1147/rd.11.0019, 1957.
Ruzza, P., Siligardi, G., Donella-Deana, A., Calderan, A., Hussain, R.,
Rubini, C., Cesaro, L., Osler, A., Guiotto, A., Pinna, L. A., and Borin, G.:
4-Fluoroproline derivative peptides: Effect on PPII conformation and SH3
affinity, J. Pept. Sci., 12, 462–471, https://doi.org/10.1002/psc.750, 2006.
Salwiczek, M., Nyakatura, E. K., Gerling, U. I. M., Ye, S., and Koksch, B.:
Fluorinated amino acids: Compatibility with native protein structures and
effects on protein–protein interactions, Chem. Soc. Rev., 41, 2135–2171,
https://doi.org/10.1039/c1cs15241f, 2012.
Saksela, K. and Permi, P.: SH3 domain ligand binding: What's the consensus and
where's the specificity?, FEBS Lett., 586, 2609–2614, https://doi.org/10.1016/j.febslet.2012.04.042, 2012.
Sarkar, S. K., Young, P. E., and Torchia, D. A.: Ring Dynamics of DL-Proline and
DL-Proline Hydrochloride in the Solid State: A 2H Nuclear Magnetic
Resonance Study, J. Am. Chem. Soc., 108, 6459–6464, https://doi.org/10.1021/ja00281a002, 1986.
Sharaf, N. G. and Gronenborn, A. M.: 19F-Modified Proteins and
19F-Containing Ligands as Tools in Solution NMR Studies of Protein
Interactions, Methods Enzymol., 565, 67–95, https://doi.org/10.1016/bs.mie.2015.05.014, 2015.
Sinnaeve, D.: Selective Homonuclear 2D J-Resolved Spectroscopy. eMagRes., 9,
267–282, https://doi.org/10.1002/9780470034590.emrstm1544,
2021.
Schubert, M., Labudde, D., Oschkinat, H., and Schmieder, P.: A software tool for
the prediction of Xaa-Pro peptide bond conformations in proteins based on
13C chemical shift statistics, J. Biomol. NMR., 24, 149–154, https://doi.org/10.1023/A:1020997118364, 2002.
Shoulders, M. D. and Raines, R. T.: Collagen structure and stability, Annu. Rev.
Biochem., 78, 929–958, https://doi.org/10.1146/annurev.biochem.77.032207.120833, 2009.
Stadmiller, S. S., Aguilar, J. S., Waudby, C. A., and Pielak, G. J.: Rapid
Quantification of Protein-Ligand Binding via 19F NMR Lineshape
Analysis, Biophys. J., 118, 2537–2548, https://doi.org/10.1016/j.bpj.2020.03.031, 2020.
Theillet, F.-X., Kalmar, L., Tompa, P., Han, K.-H., Selenko, P., Dunker, A.
K., Daughdrill, G. W., and Uversky, V. N.: The alphabet of intrinsic disorder,
Intrinsically Disord. Proteins., 1, e24360, https://doi.org/10.4161/idp.24360, 2013.
Thiehoff, C., Rey, Y. P., and Gilmour, R.: The Fluorine Gauche Effect: A Brief
History, Isr. J. Chem., 57, 92–100, https://doi.org/10.1002/ijch.201600038, 2017.
Torbeev, V., Ebert, M. O., Dolenc, J., and Hilvert, D.: Substitution of
proline32 by α-methylproline preorganizes β2-microglobulin
for oligomerization but not for aggregation into amyloids, J. Am. Chem.
Soc., 137, 2524–2535, https://doi.org/10.1021/ja510109p, 2015.
Torbeev, V. Y. and Hilvert, D.: Both the cis-trans equilibrium and isomerization
dynamics of a single proline amide modulate β2-microglobulin amyloid
assembly, P. Natl. Acad. Sci. USA, 110, 20051–20056, https://doi.org/10.1073/pnas.1310414110, 2013.
Urbanek, A., Popovic, M., Elena-Real, C. A., Morató, A., Estaña, A.,
Fournet, A., Allemand, F., Gil, A. M., Cativiela, C., Cortés, J.,
Jiménez, A. I., Sibille, N., and Bernadó, P.: Evidence of the Reduced
Abundance of Proline cis Conformation in Protein Poly Proline Tracts, J. Am.
Chem. Soc., 142, 7976–7986, https://doi.org/10.1021/jacs.0c02263, 2020.
Urbanek, A., Popovic, M., Morató, A., Estaña, A., Elena-Real, C. A.,
Mier, P., Fournet, A., Allemand, F., Delbecq, S., Andrade-Navarro, M. A.,
Cortés, J., Sibille, N., and Bernadó, P.: Flanking regions determine the
structure of the poly-glutamine in huntingtin through mechanisms common
among glutamine-rich human proteins, Structure, 28, 733–746, https://doi.org/10.1016/j.str.2020.04.008, 2020.
Verhoork, S. J. M., Killoran, P. M., and Coxon, C. R.: Fluorinated Prolines as
Conformational Tools and Reporters for Peptide and Protein Chemistry,
Biochemistry, 57, 6132–6143, https://doi.org/10.1021/acs.biochem.8b00787, 2018.
Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas,
M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D.: The CCPN data
model for NMR spectroscopy: Development of a software pipeline, Proteins
Struct. Funct. Genet., 59, 687–696, https://doi.org/10.1002/prot.20449, 2005.
Welte, H., Zhou, T., Mihajlenko, X., Mayans, O., and Kovermann, M.: What does
fluorine do to a protein? Thermodynamic, and highly-resolved structural
insights into fluorine-labelled variants of the cold shock protein, Sci.
Rep., 10, 1–12, https://doi.org/10.1038/s41598-020-59446-w,
2020.
Wilhelm, P., Lewandowski, B., Trapp, N., and Wennemers, H.: A crystal structure
of an oligoproline PPII-Helix, at last, J. Am. Chem. Soc., 136,
15829–15832, https://doi.org/10.1021/ja507405j, 2014.
Yoshida, A.: Studies on the mechanism of protein synthesis, Incorporation of
p-fluorophenylalanine into α-amylase of Bacillus subtilis, BBA –
Biochim. Biophys. Acta., 41, 98–103,
https://doi.org/10.1016/0006-3002(60)90373-5, 1960.
Zhang, C., Moonshi, S. S., Han, Y., Puttick, S., Peng, H., Magoling, B. J.
A., Reid, J. C., Bernardi, S., Searles, D. J., Král, P., and Whittaker, A.
K.: PFPE-Based Polymeric 19F MRI Agents: A New Class of Contrast Agents
with Outstanding Sensitivity, Macromolecules, 50, 5953–5963, https://doi.org/10.1021/acs.macromol.7b01285, 2017.
Zhao, Y. and Truhlar, D. G.: The M06 suite of density functionals for main group
thermochemistry, thermochemical kinetics, noncovalent interactions, excited
states, and transition elements: Two new functionals and systematic testing
of four M06-class functionals and 12 other functionals, Theor. Chem. Acc.,
120, 215–241, https://doi.org/10.1007/s00214-007-0310-x, 2008.
Short summary
Fluorine NMR was used to study the interaction between a proline-rich peptide and a SH3 domain using 4S- and 4R-fluorinated prolines whose potential as NMR probes has not been exploited yet. We present a comprehensive study addressing several aspects to be considered when using these residues as NMR probes, including relaxation and dynamics. We show that their conformational bias may be used to modulate the kinetics of protein binding to proline-rich motifs.
Fluorine NMR was used to study the interaction between a proline-rich peptide and a SH3 domain...
Special issue