Versatile Vibrational Energy Sensors for Proteins

Overview

Journal Angew Chem Int Ed Engl

Specialty Chemistry

Date 2022 Feb 28

PMID 35226765

Authors

Jan G Loffler

Erhan Deniz

Carolin Feid

Valentin G Franz

Jens Bredenbeck

Affiliations

Soon will be listed here.

Abstract

Vibrational energy transfer (VET) is emerging as key mechanism for protein functions, possibly playing an important role for energy dissipation, allosteric regulation, and enzyme catalysis. A deep understanding of VET is required to elucidate its role in such processes. Ultrafast VIS-pump/IR-probe spectroscopy can detect pathways of VET in proteins. However, the requirement of having a VET donor and a VET sensor installed simultaneously limits the possible target proteins and sites; to increase their number we compare six IR labels regarding their utility as VET sensors. We compare these labels in terms of their FTIR, and VET signature in VET donor-sensor dipeptides in different solvents. Furthermore, we incorporated four of these labels in PDZ3 to assess their capabilities in more complex systems. Our results show that different IR labels can be used interchangeably, allowing for free choice of the right label depending on the system under investigation and the methods available.

Citing Articles

Biomolecular dynamics in the 21st century.

Brooks 3rd C, MacKerell Jr A, Post C, Nilsson L Biochim Biophys Acta Gen Subj. 2023; 1868(2):130534.

PMID: 38065235 PMC: 10842176. DOI: 10.1016/j.bbagen.2023.130534.

Genetically encoded non-canonical amino acids reveal asynchronous dark reversion of chromophore, backbone, and side-chains in EL222.

Chaudhari A, Chatterjee A, Domingos C, Andrikopoulos P, Liu Y, Andersson I Protein Sci. 2023; 32(4):e4590.

PMID: 36764820 PMC: 10019195. DOI: 10.1002/pro.4590.

A Triplet Label Extends Two-Dimensional Infrared Spectroscopy from Pico- to Microseconds.

Brunst H, Masood H, Thun A, Kondratiev A, Wille G, van Wilderen L Angew Chem Int Ed Engl. 2022; 61(49):e202211490.

PMID: 36128955 PMC: 10098663. DOI: 10.1002/anie.202211490.

Versatile Vibrational Energy Sensors for Proteins.

Loffler J, Deniz E, Feid C, Franz V, Bredenbeck J Angew Chem Int Ed Engl. 2022; 61(21):e202200648.

PMID: 35226765 PMC: 9401566. DOI: 10.1002/anie.202200648.

References

Wolfshorndl M, Baskin R, Dhawan I, Londergan C . Covalently bound azido groups are very specific water sensors, even in hydrogen-bonding environments. J Phys Chem B. 2011; 116(3):1172-9. DOI: 10.1021/jp209899m. View

Bloem E, Koziol K, Waldauer S, Buchli B, Walser R, Samatanga B . Ligand binding studied by 2D IR spectroscopy using the azidohomoalanine label. J Phys Chem B. 2012; 116(46):13705-12. DOI: 10.1021/jp3095209. View

Maj M, Ahn C, Blasiak B, Kwak K, Han H, Cho M . Isonitrile as an Ultrasensitive Infrared Reporter of Hydrogen-Bonding Structure and Dynamics. J Phys Chem B. 2016; 120(39):10167-10180. DOI: 10.1021/acs.jpcb.6b04319. View

Doyle D, Lee A, Lewis J, Kim E, Sheng M, Mackinnon R . Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell. 1996; 85(7):1067-76. DOI: 10.1016/s0092-8674(00)81307-0. View

Gai X, Coutifaris B, Brewer S, Fenlon E . A direct comparison of azide and nitrile vibrational probes. Phys Chem Chem Phys. 2011; 13(13):5926-30. PMC: 3101501. DOI: 10.1039/c0cp02774j. View

Kobayashi T, Nureki O, Ishitani R, Yaremchuk A, Tukalo M, Cusack S . Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion. Nat Struct Biol. 2003; 10(6):425-32. DOI: 10.1038/nsb934. View

Pagano P, Guo Q, Ranasinghe C, Schroeder E, Robben K, Hase F . Oscillatory Active-site Motions Correlate with Kinetic Isotope Effects in Formate Dehydrogenase. ACS Catal. 2021; 9(12):11199-11206. PMC: 8118594. DOI: 10.1021/acscatal.9b03345. View

Agarwal P, Geist A, Gorin A . Protein dynamics and enzymatic catalysis: investigating the peptidyl-prolyl cis-trans isomerization activity of cyclophilin A. Biochemistry. 2004; 43(33):10605-18. DOI: 10.1021/bi0495228. View

Levin D, Schmitz A, Hines S, Hines K, Tucker M, Brewer S . Synthesis and Evaluation of the Sensitivity and Vibrational Lifetimes of Thiocyanate and Selenocyanate Infrared Reporters. RSC Adv. 2016; 43(6):36231-36237. PMC: 4841628. DOI: 10.1039/C5RA27363C. View

10.

Thielges M . Transparent window 2D IR spectroscopy of proteins. J Chem Phys. 2021; 155(4):040903. PMC: 8302233. DOI: 10.1063/5.0052628. View

11.

Chalyavi F, Schmitz A, Fetto N, Tucker M, Brewer S, Fenlon E . Extending the vibrational lifetime of azides with heavy atoms. Phys Chem Chem Phys. 2020; 22(32):18007-18013. PMC: 8276756. DOI: 10.1039/d0cp02814b. View

12.

Davarifar A, Antoniou D, Schwartz S . The promoting vibration in human heart lactate dehydrogenase is a preferred vibrational channel. J Phys Chem B. 2011; 115(51):15439-44. PMC: 3245336. DOI: 10.1021/jp210347h. View

13.

Park J, Kwon H, Mondal S, Han H, Kwak K, Cho M . Two-dimensional IR spectroscopy reveals a hidden Fermi resonance band in the azido stretch spectrum of β-azidoalanine. Phys Chem Chem Phys. 2020; 22(34):19223-19229. DOI: 10.1039/d0cp02693j. View

14.

Park J, Mondal S, Kwon H, Sahu P, Han H, Kwak K . Effect of isotope substitution on the Fermi resonance and vibrational lifetime of unnatural amino acids modified with IR probe: A 2D-IR and pump-probe study of 4-azido-L-phenyl alanine. J Chem Phys. 2020; 153(16):164309. DOI: 10.1063/5.0025289. View

15.

Fafarman A, Webb L, Chuang J, Boxer S . Site-specific conversion of cysteine thiols into thiocyanate creates an IR probe for electric fields in proteins. J Am Chem Soc. 2006; 128(41):13356-7. PMC: 2516909. DOI: 10.1021/ja0650403. View

16.

Schultz K, Supekova L, Ryu Y, Xie J, Perera R, Schultz P . A genetically encoded infrared probe. J Am Chem Soc. 2006; 128(43):13984-5. DOI: 10.1021/ja0636690. View

17.

Rodgers J, Zhang W, Bazewicz C, Chen J, Brewer S, Gai F . Kinetic Isotope Effect Provides Insight into the Vibrational Relaxation Mechanism of Aromatic Molecules: Application to Cyano-phenylalanine. J Phys Chem Lett. 2016; 7(7):1281-7. PMC: 4824650. DOI: 10.1021/acs.jpclett.6b00325. View

18.

Neumann-Staubitz P, Neumann H . The use of unnatural amino acids to study and engineer protein function. Curr Opin Struct Biol. 2016; 38:119-28. DOI: 10.1016/j.sbi.2016.06.006. View

19.

Kimmerlin T, Seebach D . '100 years of peptide synthesis': ligation methods for peptide and protein synthesis with applications to beta-peptide assemblies. J Pept Res. 2005; 65(2):229-60. DOI: 10.1111/j.1399-3011.2005.00214.x. View

20.

Ota N, Agard D . Intramolecular signaling pathways revealed by modeling anisotropic thermal diffusion. J Mol Biol. 2005; 351(2):345-54. DOI: 10.1016/j.jmb.2005.05.043. View