Skip to main content
SpringerLink
Log in

Terahertz optical measurements of correlated motions with possible allosteric function

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

Abstract

A suggested mechanism for allosteric response is the distortion of the energy landscape with agonist binding changing the protein structure’s access to functional configurations. Intramolecular vibrations are indicative of the energy landscape and may have trajectories that enable functional conformational change. Here, we discuss the development of an optical method to measure the intramolecular vibrations in proteins, namely, crystal anisotropy terahertz microscopy, and the various approaches which can be used to identify the spectral data with specific structural motions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Acbas G, Niessen KA, Snell EH, Markelz AG (2014) Optical measurements of long-range protein vibrations. Nat Commun 5:3076. doi:10.1038/ncomms4076

    Article  PubMed  Google Scholar 

  • Achterhold K, Keppler C, Ostermann A, Bürck U, Sturhahn W, Alp EE, Parak FG (2002) Vibrational dynamics of myoglobin determined by the phonon-assisted Mössbauer effect. Phys Rev E 65:051916. doi:10.1103/PhysRevE.65.051916

    Article  CAS  Google Scholar 

  • Bahar I, Rader AJ (2005) Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 15:586–592

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Balog E, Becker T, Oettl M, Lechner R, Daniel R, Finney J, Smith JC (2004) Direct determination of vibrational density of states change on ligand binding to a protein. Phys Rev Lett 93:28103

    Article  Google Scholar 

  • Balog E, Perahia D, Smith JC, Merzel F (2011) Vibrational softening of a protein on ligand binding. J Phys Chem B 115:6811–6817

    Article  CAS  PubMed  Google Scholar 

  • Bhabha G, Ekiert DC, Jennewein M, Zmasek CM, Tuttle LM, Kroon G, Dyson HJ, Godzik, Wilson IA, Wright PE (2013) Divergent evolution of protein conformational dynamics in dihydrofolate reductase. Nat Struct Mol Biol 20:1243–1262. doi:10.1038/nsmb.2676

  • Biehl R, Hoffmann B, Monkenbusch M, Falus P, Préost S, Merkel R, Richter D (2008) Direct observation of correlated interdomain motion in alcohol dehydrogenase. Phys Rev Lett 101:138102

    Article  PubMed  Google Scholar 

  • oehr DD, Schnell JR, McElheny D, Bae S-H, Duggan BM, Benkovic SJ, Dyson HJ, Wright PE (2013) A distal mutation perturbs dynamic amino acid networks in dihydrofolate reductase. Biochemistry 52:4605–4619. doi:10.1021/bi400563c

  • Brooks CL, Karplus M, Pettitt BM (1988) Proteins: a theoretical perspective of dynamics, structure, and thermodynamics. John Wiley & Sons, New York

    Google Scholar 

  • Bruccoleri RE, Karplus M, McCammon JA (1986) The hinge-bending mode of a lysozyme inhibitor complex. Biopolymers 25:1767–1802. doi:10.1002/bip.360250916

    Article  CAS  PubMed  Google Scholar 

  • Chakkittakandy R, Corver JAWM, Planken PCM (2008) Quasi-near field terahertz generation and detection. Opt Express 16:12794–12805

    Article  CAS  PubMed  Google Scholar 

  • Changeux JP, Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308:1424–1428. doi:10.1126/science.1108595

    Article  CAS  PubMed  Google Scholar 

  • Chung EW, Nettleton EJ, Morgan CJ, Gross M, Miranker A, Radford SE, Dobson CM, Robinson CV (1997) Hydrogen exchange properties of proteins in native and denatured states monitored by mass spectrometry and NMR. Protein Sci 6:1316–1324. doi:10.1002/pro.5560060620

  • Crowe TW, Globus T, Woolard DL, Hesler JL (2004) Terahertz sources and detectors and their application to biological sensing. Philos Trans R Soc Lond Ser A Math Phys Eng Sci 362:365–374

    Article  CAS  Google Scholar 

  • Edwards GS, Davis CC, Saffer JD, Swicord ML (1984) Resonant microwave absorption of selected DNA molecules. Phys Rev Lett 53:1284–1287

    Article  CAS  Google Scholar 

  • Falconer RJ, Markelz AG (2012) Terahertz spectroscopic analysis of peptides and proteins. J Infrared Millim THz Waves 33:973–988

    Article  CAS  Google Scholar 

  • Globus TR, Woolard DL, Samuels AC, Gelmont BL, Hesler J, Crowe TW, Bykhovskaia M (2002) Submillimeter-wave Fourier transform spectroscopy of biological macromolecules. J Appl Phys 91:6105–6113

    Article  CAS  Google Scholar 

  • Globus T, Woolard D, Crowe TW, Khromova T, Gelmont B, Hesler J (2006) Terahertz Fourier transform characterization of biological materials in a liquid phase. J Phys D Appl Phys 39:3405–3413

    Article  CAS  Google Scholar 

  • Grossman M, Born B, Heyden M, Tworowski D, Fields GB, Sagi I, Havenith M (2011) Correlated structural kinetics and retarded solvent dynamics at the metalloprotease active site. Nat Struct Mol Biol 18:1102–1113. doi:10.1038/nsmb.2120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gunasekaran K, Ma BY, Nussinov R (2004) Is allostery an intrinsic property of all dynamic proteins? Proteins Struct Funct Bioinf 57:433–443. doi:10.1002/prot.20232

    Article  CAS  Google Scholar 

  • He YF, Chen JY, Knab JR, Zheng WJ, Markelz AG (2011) Evidence of protein collective motions on the picosecond timescale. Biophys J 100:1058–1065. doi:10.1016/j.bpj.2010.12.3731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hilser VJ, Whitten ST (2014) Using the COREX/BEST server to model the native-state ensemble. Protein Dyn Methods Protoc 1084:255–269. doi:10.1007/978-1-62703-658-0_14

    CAS  Google Scholar 

  • Hilser VJ, Wrabl JO, Motlagh HN (2012) Structural and energetic basis of allostery. Annu Rev Biophys 41(41):585–609. doi:10.1146/annurev-biophys-050511-102319

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karplus M, Kuriyan J (2005) Molecular dynamics and protein function. Proc Natl Acad Sci USA 102:6679–6685

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knab JR, Adam AJL, Chakkittakandy R, Planken PCM (2010) Terahertz near-field microspectroscopy. Appl Phys Lett 97 doi:10.1063/1.3467192

  • Korter TM, Balu R, Campbell MB, Beard MC, Gregurick SK, Heilweil EJ (2006) Terahertz spectroscopy of solid serine and cysteine. Chem Phys Lett 418:65–70

    Article  CAS  Google Scholar 

  • Koshland DE, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365–385. doi:10.1021/bi00865a047

    Article  CAS  PubMed  Google Scholar 

  • Kröll J, Darmo J, Unterrainer K (2007) Terahertz optical activity of sucrose single-crystals. Vib Spectrosc 43:324–329

    Article  Google Scholar 

  • Levy RM, Rojas OL, Friesner RA (1984) Quasi-harmonic method for calculating vibrational spectra from classical simulations on multidimensional anharmonic potential surfaces. J Phys Chem 88:4233–4238

    Article  CAS  Google Scholar 

  • Lindsay SM, Lee SA, Powell JW, Weidlich T, DeMarco C, Lewen GD, Tao NJ, Rupprecht A (1988) The origin of the A to B transition in DNA fibers and films. Biopolymers 27:1015–1043

  • Lisy V, Miskovsky P, Brutovsky B, Chinsky L (1997) Internal DNA modes below 25 cm-1: a resonance Raman spectroscopy observation. J Biomol Struct Dyn 14:517–523

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Chu XQ, Lagi M, Zhang Y, Fratini E, Baglioni P, Alatas A, Said A, Alp E, Chen SH (2008) Studies of Phononlike low-energy excitations of protein molecules by inelastic X-ray scattering. Phys Rev Lett 101:135501. doi:10.1103/PhysRevLett.101.135501

  • Luong TQ, Verma PK, Mitra RK, Havenith M (2011) Do hydration dynamics follow the structural perturbation during thermal denaturation of a protein: a terahertz absorption study. Biophys J 101:925–933

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Markelz AG (2008) Terahertz dielectric sensitivity to biomolecular structure and function. IEEE J Sel Top Quantum Electron 14:180–190

    Article  CAS  Google Scholar 

  • McLeish TCB, Rodgers TL, Wilson MR (2013) Allostery without conformation change: modelling protein dynamics at multiple scales. Phys Biol 10:056004. doi:10.1088/1478-3975/10/5/056004

    Article  CAS  PubMed  Google Scholar 

  • Mittleman D (2003) Sensing with terahertz radiation. Springer, Berlin Heidelberg New York

  • Monod J, Wyman J, Changeux JP (1965) On nature of allosteric transitions—a plausible model. J Mol Biol 12:88–118

    Article  CAS  PubMed  Google Scholar 

  • Motlagh HN, Hilser VJ (2012) Agonism/antagonism switching in allosteric ensembles. Proc Natl Acad Sci USA 109:4134–4139. doi:10.1073/pnas.1120519109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nussinov R, Tsai CJ (2013) Allostery in disease and in drug discovery. Cell 153:293–305. doi:10.1016/j.cell.2013.03.034

    Article  CAS  PubMed  Google Scholar 

  • Parak FG (2003) Physical aspects of protein dynamics. Rep Prog Phys 66:103–129

    Article  CAS  Google Scholar 

  • Parthasarathy R, Globus T, Khromova T, Swami N, Woolard D (2005) Dielectric properties of biological molecules in the Terahertz gap. Appl Phys Lett 87:113901

    Article  Google Scholar 

  • Petrone P, Pande VS (2006) Can conformational change be described by only a few normal modes? Biophys J 90:1583–1593

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Powell JW, Edwards GS, Genzel L, Kremer F, Wittlin A, Kubasek W, Peticolas W (1987) Investigation of far-infrared vibrational modes in polynucleotides. Phys Rev A 35:3929–3939

    Article  CAS  PubMed  Google Scholar 

  • Powell JW, Peticolas WL, Genzel L (1991) Observation of the far-infrared spectrum of five oligonucleotides. J Mol Struct 247:107–118

    Article  CAS  Google Scholar 

  • Rheinstadter MC, Schmalzl K, Wood K, Strauch D (2009) Protein-protein interaction in purple membrane. Phys Rev Lett 103:128104. doi:10.1103/PhysRevLett.103.128104

    Article  PubMed  Google Scholar 

  • Rodgers TL, Townsend PD, Burnell D et al (2013) Modulation of global low-frequency motions underlies allosteric regulation: demonstration in CRP/FNR family transcription factors. PLoS Biol 11(9):e1001651. doi:10.1371/journal.pbio.1001651

  • Sakai K (2005) Terahertz optoelectronics. Springer, Berlin Heidelberg New York

  • Singh R, George DK, Benedict JB, Korter TM, Markelz AG (2012) Improved mode assignment for molecular crystals through anisotropic terahertz spectroscopy. J Phys Chem C 116:10359–10364

    Article  CAS  Google Scholar 

  • Tan ML, Bizzarri AR, Xiao Y, Cannistraro S, Ichiye T, Manzoni C, Cerullo G, Adams MW, Jenney FE Jr, Cramer SP (2007) Observation of terahertz vibrations in Pyrococcus furiosus rubredoxin via impulsive coherent vibrational spectroscopy and nuclear resonance vibrational spectroscopy—interpretation by molecular mechanics. J Inorg Biochem 101:375–384. doi:10.1016/j.jinorgbio.2006.09.031

  • Teeter MM, Case DA (1990) Harmonic and quasiharmonic descriptions of crambin. J Phys Chem 94:8091–8097

    Article  CAS  Google Scholar 

  • Toncrova H, McLeish TCB (2010) Substrate-modulated thermal fluctuations affect long-range allosteric signaling in protein homodimers: exemplified in CAP. Biophys J 98:2317–2326. doi:10.1016/j.bpj.2010.01.039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tsai CJ, Del Sol A, Nussinov R (2009) Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms. Mol Biosyst 5:207–216. doi:10.1039/b819720b

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Turton DA, Senn HM, Harwood T, Lapthorn AJ, Ellis EM, Wynne K (2014) Terahertz underdamped vibrational motion governs protein-ligand binding in solution. Nat Commun 5:3999. doi:10.1038/ncomms4999

  • Tych KM, Burnett AD, Wood CD, Cunningham JE, Pearson AR, Davies AG, Linfield EH (2011) Applying broadband terahertz time-domain spectroscopy to the analysis of crystalline proteins: a dehydration study. J Appl Crystallogr 44:129–133. doi:10.1107/s0021889810043372

    Article  CAS  Google Scholar 

  • Walther M, Fischer BM, Jepsen PU (2003) Noncovalent intermolecular forces in polycrystalline and amorphous saccharides in the far infrared. Chem Phys Lett 288:261–268

    CAS  Google Scholar 

  • Weidlich T, Lindsay SM, Rui Q, Rupprecht A, Peticolas WL, Thomas GA (1990) A raman-study of low-frequency intrahelical modes in A-Dna, B- Dna, and C-Dna. J Biomol Struct Dyn 8:139–171

    Article  CAS  PubMed  Google Scholar 

  • Woolard DL et al (2002) Submillimeter-wave phonon modes in DNA macromolecules. Phys Rev E 65:051903. doi:10.1103/PhysRevE.65.051903

  • Xiao YM et al (2005) Normal mode analysis of Pyrococcus furiosus rubredoxin via nuclear resonance vibrational spectroscopy (NRVS) and resonance Raman spectroscopy. J Am Chem Soc 127:14596–14606. doi:10.1021/ja042960h

    Article  CAS  PubMed  Google Scholar 

  • Zhu LY, Zhong G, Unno M, Sligar SG, Champion PM (1996) Femtosecond coherence spectroscopy of heme proteins. Biospectroscopy 2:301–309

    Article  CAS  Google Scholar 

Download references

Compliance with Ethical Standards

ᅟ

Funding

All calculations were performed using facilities provided by The Center for Computational Research, SUNY, Buffalo. We thank the National Science Foundation MRI^2 grant DBI2959989 for support.

Conflict of interest

Andrea G. Markelz, Katherine A. Niessen, and Mengyang Xu declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Authors and Affiliations

  1. Department of Physics, University at Buffalo (SUNY), Buffalo, NY, 14260, USA

    Katherine A. Niessen, Mengyang Xu & A. G. Markelz

Authors
  1. Katherine A. Niessen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mengyang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. Markelz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Markelz.

Additional information

This article is part of a Special Issue on 'The Role of Protein Dynamics in Allosteric Effects' edited by Gordon Roberts

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niessen, K.A., Xu, M. & Markelz, A.G. Terahertz optical measurements of correlated motions with possible allosteric function. Biophys Rev 7, 201–216 (2015). https://doi.org/10.1007/s12551-015-0168-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-015-0168-4

Keywords

Search

Navigation