Home LiteratureArticle Details
PMID: 20886836 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Distance mapping in proteins using fluorescence spectroscopy: the tryptophan-induced quenching (TrIQ) method.

Biochemistry ·Vol. 49 ·No. 45 ·2010-11-16 ·Pages 9722-31

Mansoor SE, Dewitt MA, Farrens DL

Abstract

Studying the interplay between protein structure and function remains a daunting task. Especially lacking are methods for measuring structural changes in real time. Here we report our most recent improvements to a method that can be used to address such challenges. This method, which we now call tryptophan-induced quenching (TrIQ), provides a straightforward, sensitive, and inexpensive way to address questions of conformational dynamics and short-range protein interactions. Importantly, TrIQ only occurs over relatively short distances (∼5-15 Å), making it complementary to traditional fluorescence resonance energy transfer (FRET) methods that occur over distances too large for precise studies of protein structure. As implied in the name, TrIQ measures the efficient quenching induced in some fluorophores by tryptophan (Trp). We present here our analysis of the TrIQ effect for five different fluorophores that span a range of sizes and spectral properties. Each probe was attached to four different cysteine residues on T4 lysozyme, and the extent of TrIQ caused by a nearby Trp was measured. Our results show that, at least for smaller probes, the extent of TrIQ is distance dependent. Moreover, we also demonstrate how TrIQ data can be analyzed to determine the fraction of fluorophores involved in a static, nonfluorescent complex with Trp. Based on this analysis, our study shows that each fluorophore has a different TrIQ profile, or "sphere of quenching", which correlates with its size, rotational flexibility, and the length of attachment linker. This TrIQ-based "sphere of quenching" is unique to every Trp-probe pair and reflects the distance within which one can expect to see the TrIQ effect. Thus,TrIQ provides a straightforward, readily accessible approach for mapping distances within proteins and monitoring conformational changes using fluorescence spectroscopy.

MeSH Terms
Amino Acids/analysis Anisotropy Bacteriophage T4/enzymology,genetics Fluorescence Resonance Energy Transfer Models, Molecular Muramidase/chemistry,genetics,isolation & purification Protein Structure, Secondary Proteins/chemistry Spectrometry, Fluorescence/methods Structure-Activity Relationship Tryptophan/chemistry
Chemicals
Amino Acids Proteins Tryptophan Muramidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mansoor Steven E
Department of Biochemistry and Molecular Biology, Oregon Health and Science University, Portland, Oregon 97239-3098, United States.
Dewitt Mark A
Farrens David L
References (41)
41 references, click to expand
  1. Rhodopsin activation exposes a key hydrophobic binding site for the transducin alpha-subunit C terminus.
    J Biol Chem. 2004 Jul 9;279(28):29767-73 PMID: 15070895
  2. Determination of the distance between two spin labels attached to a macromolecule.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8239-43 PMID: 7667275
  3. Identifying transmembrane states and defining the membrane insertion boundaries of hydrophobic helices in membrane-inserted diphtheria toxin T domain.
    J Biol Chem. 1998 Sep 4;273(36):22950-6 PMID: 9722516
  4. Identification of shallow and deep membrane-penetrating forms of diphtheria toxin T domain that are regulated by protein concentration and bilayer width.
    J Biol Chem. 1997 Oct 3;272(40):25091-8 PMID: 9312118
  5. Inter- and intramolecular fluorescence quenching of organic dyes by tryptophan.
    Bioconjug Chem. 2003 Nov-Dec;14(6):1133-9 PMID: 14624626
  6. Effects of solubilization on the structure and function of the sensory rhodopsin II/transducer complex.
    J Mol Biol. 2006 Mar 10;356(5):1207-21 PMID: 16410012
  7. Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy.
    Nat Struct Biol. 1998 Jun;5(6):459-69 PMID: 9628484
  8. The magnitude of the light-induced conformational change in different rhodopsins correlates with their ability to activate G proteins.
    J Biol Chem. 2009 Jul 31;284(31):20676-83 PMID: 19497849
  9. Distance measurements by fluorescence energy homotransfer: evaluation in T4 lysozyme and correlation with dipolar coupling between spin labels.
    Biophys J. 2007 Feb 15;92(4):L27-9 PMID: 17142264
  10. Site-directed spectroscopic probes of actomyosin structural dynamics.
    Annu Rev Biophys. 2009;38:347-69 PMID: 19416073
  11. Site-directed spin-labeling study of the structure and subunit interactions along a conserved sequence in the alpha-crystallin domain of heat-shock protein 27. Evidence of a conserved subunit interface.
    Biochemistry. 1997 Dec 2;36(48):14627-34 PMID: 9398181
  12. The kamikaze approach to membrane transport.
    Nat Rev Mol Cell Biol. 2001 Aug;2(8):610-20 PMID: 11483994
  13. Rhodopsin self-associates in asolectin liposomes.
    Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3060-5 PMID: 16492772
  14. Short-range molecular rearrangements in ion channels detected by tryptophan quenching of bimane fluorescence.
    J Gen Physiol. 2006 Sep;128(3):337-46 PMID: 16940556
  15. High-throughput protein structural analysis using site-directed fluorescence labeling and the bimane derivative (2-pyridyl)dithiobimane.
    Biochemistry. 2004 Jul 27;43(29):9426-38 PMID: 15260485
  16. Monitoring the conformational changes of photoactivated rhodopsin from microseconds to seconds by transient fluorescence spectroscopy.
    Biochemistry. 2008 Nov 4;47(44):11518-27 PMID: 18847221
  17. A close look at fluorescence quenching of organic dyes by tryptophan.
    Chemphyschem. 2005 Nov 11;6(11):2277-85 PMID: 16224752
  18. Conformation of T4 lysozyme in solution. Hinge-bending motion and the substrate-induced conformational transition studied by site-directed spin labeling.
    Biochemistry. 1997 Jan 14;36(2):307-16 PMID: 9003182
  19. High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation.
    Proc Natl Acad Sci U S A. 2008 May 27;105(21):7439-44 PMID: 18490656
  20. The cytoplasmic membrane-proximal domain of the HtrII transducer interacts with the E-F loop of photoactivated Natronomonas pharaonis sensory rhodopsin II.
    J Biol Chem. 2004 Oct 8;279(41):42970-6 PMID: 15262967
  21. Principles and biophysical applications of lanthanide-based probes.
    Annu Rev Biophys Biomol Struct. 2002;31:275-302 PMID: 11988471
  22. Flavin 1, N 6 -ethenoadenine dinucleotide: dynamic and static quenching of fluorescence.
    Proc Natl Acad Sci U S A. 1973 Mar;70(3):941-3 PMID: 4515004
  23. Watching proteins move using site-directed spin labeling.
    Structure. 1996 Jul 15;4(7):779-83 PMID: 8805569
  24. Kinetics of association and dissociation of HIV-1 reverse transcriptase subunits.
    Biochemistry. 2009 Sep 29;48(38):9084-93 PMID: 19715314
  25. Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy.
    Nature. 1999 Dec 16;402(6763):809-13 PMID: 10617201
  26. Short-distance probes for protein backbone structure based on energy transfer between bimane and transition metal ions.
    Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16227-32 PMID: 19805285
  27. Fluorescence energy transfer as a spectroscopic ruler.
    Annu Rev Biochem. 1978;47:819-46 PMID: 354506
  28. Preferential substrate binding orientation by the molecular chaperone HscA.
    J Biol Chem. 2004 Jul 2;279(27):28435-42 PMID: 15100228
  29. Monitoring the interaction of a single G-protein key binding site with rhodopsin disk membranes upon light activation.
    Biochemistry. 2009 May 12;48(18):3801-3 PMID: 19301833
  30. Oligomeric state of human erythrocyte band 3 measured by fluorescence resonance energy homotransfer.
    Biophys J. 1998 Aug;75(2):1117-30 PMID: 9675213
  31. Excited-state dynamics of the fluorescent probe Lucifer Yellow in liquid solutions and in heterogeneous media.
    Photochem Photobiol Sci. 2005 Mar;4(3):260-7 PMID: 15738993
  32. Fluorescent labeling of purified beta 2 adrenergic receptor. Evidence for ligand-specific conformational changes.
    J Biol Chem. 1995 Nov 24;270(47):28268-75 PMID: 7499324
  33. Protein structure determination using long-distance constraints from double-quantum coherence ESR: study of T4 lysozyme.
    J Am Chem Soc. 2002 May 15;124(19):5304-14 PMID: 11996571
  34. Determination of protein secondary structure and solvent accessibility using site-directed fluorescence labeling. Studies of T4 lysozyme using the fluorescent probe monobromobimane.
    Biochemistry. 1999 Dec 7;38(49):16383-93 PMID: 10587464
  35. Explicit treatment of spin labels in modeling of distance constraints from dipolar EPR and DEER.
    J Am Chem Soc. 2005 Jul 6;127(26):9334-5 PMID: 15984837
  36. Mapping proximity within proteins using fluorescence spectroscopy. A study of T4 lysozyme showing that tryptophan residues quench bimane fluorescence.
    Biochemistry. 2002 Feb 26;41(8):2475-84 PMID: 11851393
  37. Intramolecular long-distance electron transfer in organic molecules.
    Science. 1988 Apr 22;240(4851):440-7 PMID: 17784065
  38. Coupling ligand structure to specific conformational switches in the beta2-adrenoceptor.
    Nat Chem Biol. 2006 Aug;2(8):417-22 PMID: 16799554
  39. Bimane fluorescence scanning suggests secondary structure near the S3-S4 linker of BK channels.
    J Biol Chem. 2009 Apr 17;284(16):10684-93 PMID: 19244238
  40. The use of site-directed fluorophore labeling and donor-donor energy migration to investigate solution structure and dynamics in proteins.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12477-81 PMID: 10535947
  41. Protein stability curves.
    Biopolymers. 1987 Nov;26(11):1859-77 PMID: 3689874
Article Info
Journal
Biochemistry
Abbr.
Biochemistry
ISSN
1520-4995
Published
2010-11-16
Epub
2010-00-26
Pages
9722-31
Language
English
Region
United States
NLM ID
0370623
PMCID
PMC3938424
Subset
IM
Grants
NIDA NIH HHS · DA018169 · United States
NIDA NIH HHS · R01 DA018169 · United States
NIDA NIH HHS · F30 DA015584 · United States
NEI NIH HHS · EY015436 · United States
NEI NIH HHS · R01 EY015436 · United States
NIDA NIH HHS · F30DA15584 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com