A Double-Armed, Hydrophilic Transition Metal Complex As a Paramagnetic NMR Probe

Overview

Journal Angew Chem Int Ed Engl

Specialty Chemistry

Date 2019 Jul 18

PMID 31314159

Citations 9

Authors

Qing Miao

Wei-Min Liu

Thomas Kock

Anneloes Blok

Monika Timmer

Mark Overhand

Marcellus Ubbink

Affiliations

Soon will be listed here.

Abstract

Synthetic metal complexes can be used as paramagnetic probes for the study of proteins and protein complexes. Herein, two transition metal NMR probes (TraNPs) are reported. TraNPs are attached through two arms to a protein to generate a pseudocontact shift (PCS) using cobalt(II), or paramagnetic relaxation enhancement (PRE) with manganese(II). The PCS analysis of TraNPs attached to three different proteins shows that the size of the anisotropic component of the magnetic susceptibility depends on the probe surroundings at the surface of the protein, contrary to what is observed for lanthanoid-based probes. The observed PCS are relatively small, making cobalt-based probes suitable for localized studies, such as of an active site. The obtained PREs are stronger than those obtained with nitroxide spin labels and the possibility to generate both PCS and PRE offers advantages. The properties of TraNPs in comparison with other cobalt-based probes are discussed.

Citing Articles

Metalation of a Hierarchical Self-Assembly Consisting of -Stacked Cubes through Single-Crystal-to-Single-Crystal Transformation.

Wang B, Nan Z, Liu J, Lu Z, Wang W, Zhuo Z Molecules. 2023; 28(13).

PMID: 37446584 PMC: 10343287. DOI: 10.3390/molecules28134923.

Rigidified and Hydrophilic DOTA-like Lanthanoid Ligands: Design, Synthesis, and Dynamic Properties.

Miao Q, Dekkers R, Gupta K, Overhand M, Dasgupta R, Ubbink M Inorg Chem. 2023; 62(9):3776-3787.

PMID: 36802549 PMC: 9996828. DOI: 10.1021/acs.inorgchem.2c03768.

Host Spin-Crossover Thermodynamics Indicate Guest Fit.

Zheng J, von Krbek L, Ronson T, Nitschke J Angew Chem Int Ed Engl. 2022; 61(50):e202212634.

PMID: 36264645 PMC: 10098494. DOI: 10.1002/anie.202212634.

Paramagnetic Chemical Probes for Studying Biological Macromolecules.

Miao Q, Nitsche C, Orton H, Overhand M, Otting G, Ubbink M Chem Rev. 2022; 122(10):9571-9642.

PMID: 35084831 PMC: 9136935. DOI: 10.1021/acs.chemrev.1c00708.

Measuring transverse relaxation in highly paramagnetic systems.

Invernici M, Trindade I, Cantini F, Louro R, Piccioli M J Biomol NMR. 2020; 74(8-9):431-442.

PMID: 32710399 PMC: 7508935. DOI: 10.1007/s10858-020-00334-w.

References

Vranken W, Boucher W, Stevens T, Fogh R, Pajon A, Llinas M . The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins. 2005; 59(4):687-96. DOI: 10.1002/prot.20449. View

Banci L, Bertini I, Eltis L, Felli I, Kastrau D, Luchinat C . The three-dimensional structure in solution of the paramagnetic high-potential iron-sulfur protein I from Ectothiorhodospira halophila through nuclear magnetic resonance. Eur J Biochem. 1994; 225(2):715-25. DOI: 10.1111/j.1432-1033.1994.00715.x. View

Nitsche C, Otting G . Pseudocontact shifts in biomolecular NMR using paramagnetic metal tags. Prog Nucl Magn Reson Spectrosc. 2017; 98-99:20-49. DOI: 10.1016/j.pnmrs.2016.11.001. View

Barthelmes K, Reynolds A, Peisach E, Jonker H, DeNunzio N, Allen K . Engineering encodable lanthanide-binding tags into loop regions of proteins. J Am Chem Soc. 2010; 133(4):808-19. PMC: 3043167. DOI: 10.1021/ja104983t. View

Otting G . Protein NMR using paramagnetic ions. Annu Rev Biophys. 2010; 39:387-405. DOI: 10.1146/annurev.biophys.093008.131321. View

Garcia de la Torre J, Huertas M, Carrasco B . HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J Magn Reson. 2000; 147(1):138-46. DOI: 10.1006/jmre.2000.2170. View

Yang F, Wang X, Pan B, Su X . Single-armed phenylsulfonated pyridine derivative of DOTA is rigid and stable paramagnetic tag in protein analysis. Chem Commun (Camb). 2016; 52(77):11535-8. DOI: 10.1039/c6cc06114a. View

Swarbrick J, Ung P, Dennis M, Lee M, Chhabra S, Graham B . Installation of a Rigid EDTA-Like Motif into a Protein α-Helix for Paramagnetic NMR Spectroscopy with Cobalt(II) Ions. Chemistry. 2015; 22(4):1228-32. DOI: 10.1002/chem.201503139. View

Gochin M . A high-resolution structure of a DNA-chromomycin-Co(II) complex determined from pseudocontact shifts in nuclear magnetic resonance. Structure. 2000; 8(4):441-52. DOI: 10.1016/s0969-2126(00)00124-6. View

10.

Nguyen T, Ozawa K, Stanton-Cook M, Barrow R, Huber T, Otting G . Generation of pseudocontact shifts in protein NMR spectra with a genetically encoded cobalt(II)-binding amino acid. Angew Chem Int Ed Engl. 2011; 50(3):692-4. DOI: 10.1002/anie.201005672. View

11.

Park S, Wang V, Radoicic J, De Angelis A, Berkamp S, Opella S . Paramagnetic relaxation enhancement of membrane proteins by incorporation of the metal-chelating unnatural amino acid 2-amino-3-(8-hydroxyquinolin-3-yl)propanoic acid (HQA). J Biomol NMR. 2014; 61(3-4):185-96. PMC: 4398598. DOI: 10.1007/s10858-014-9884-5. View

12.

Liu W, Keizers P, Hass M, Blok A, Timmer M, Sarris A . A pH-sensitive, colorful, lanthanide-chelating paramagnetic NMR probe. J Am Chem Soc. 2012; 134(41):17306-13. DOI: 10.1021/ja307824e. View

13.

Bertini I, Luchinat C, Parigi G, Pierattelli R . NMR spectroscopy of paramagnetic metalloproteins. Chembiochem. 2005; 6(9):1536-49. DOI: 10.1002/cbic.200500124. View

14.

Kooshapur H, Schwieters C, Tjandra N . Conformational Ensemble of Disordered Proteins Probed by Solvent Paramagnetic Relaxation Enhancement (sPRE). Angew Chem Int Ed Engl. 2018; 57(41):13519-13522. PMC: 6396310. DOI: 10.1002/anie.201807365. View

15.

Lescanne M, Skinner S, Blok A, Timmer M, Cerofolini L, Fragai M . Methyl group assignment using pseudocontact shifts with PARAssign. J Biomol NMR. 2017; 69(4):183-195. PMC: 5736784. DOI: 10.1007/s10858-017-0136-3. View

16.

Wahsner J, Gale E, Rodriguez-Rodriguez A, Caravan P . Chemistry of MRI Contrast Agents: Current Challenges and New Frontiers. Chem Rev. 2018; 119(2):957-1057. PMC: 6516866. DOI: 10.1021/acs.chemrev.8b00363. View

17.

Loh C, Graham B, Abdelkader E, Tuck K, Otting G . Generation of pseudocontact shifts in proteins with lanthanides using small "clickable" nitrilotriacetic acid and iminodiacetic acid tags. Chemistry. 2015; 21(13):5084-92. DOI: 10.1002/chem.201406274. View

18.

Ebright Y, Chen Y, Pendergrast P, Ebright R . Incorporation of an EDTA-metal complex at a rationally selected site within a protein: application to EDTA-iron DNA affinity cleaving with catabolite gene activator protein (CAP) and Cro. Biochemistry. 1992; 31(44):10664-70. DOI: 10.1021/bi00159a004. View

19.

Canales A, Mallagaray A, Perez-Castells J, Boos I, Unverzagt C, Andre S . Breaking pseudo-symmetry in multiantennary complex N-glycans using lanthanide-binding tags and NMR pseudo-contact shifts. Angew Chem Int Ed Engl. 2013; 52(51):13789-93. DOI: 10.1002/anie.201307845. View

20.

Maltsev A, Grishaev A, Roche J, Zasloff M, Bax A . Improved cross validation of a static ubiquitin structure derived from high precision residual dipolar couplings measured in a drug-based liquid crystalline phase. J Am Chem Soc. 2014; 136(10):3752-5. PMC: 3954408. DOI: 10.1021/ja4132642. View