Variational Bayes Analysis of a Photon-based Hidden Markov Model for Single-molecule FRET Trajectories

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2012 Sep 22

PMID 22995504

Citations 22

Authors

Kenji Okamoto

Yasushi Sako

Affiliations

Soon will be listed here.

Abstract

Single-molecule fluorescence resonance energy transfer (smFRET) measurement is a powerful technique for investigating dynamics of biomolecules, for which various efforts have been made to overcome significant stochastic noise. Time stamp (TS) measurement has been employed experimentally to enrich information within the signals, while data analyses such as the hidden Markov model (HMM) have been successfully applied to recover the trajectories of molecular state transitions from time-binned photon counting signals or images. In this article, we introduce the HMM for TS-FRET signals, employing the variational Bayes (VB) inference to solve the model, and demonstrate the application of VB-HMM-TS-FRET to simulated TS-FRET data. The same analysis using VB-HMM is conducted for other models and the previously reported change point detection scheme. The performance is compared to other analysis methods or data types and we show that our VB-HMM-TS-FRET analysis can achieve the best performance and results in the highest time resolution. Finally, an smFRET experiment was conducted to observe spontaneous branch migration of Holliday-junction DNA. VB-HMM-TS-FRET was successfully applied to reconstruct the state transition trajectory with the number of states consistent with the nucleotide sequence. The results suggest that a single migration process frequently involves rearrangement of multiple basepairs.

Citing Articles

Increasing the accuracy of single-molecule data analysis using tMAVEN.

Verma A, Ray K, Bodick M, Kinz-Thompson C, Gonzalez Jr R Biophys J. 2024; 123(17):2765-2780.

PMID: 38268189 PMC: 11393709. DOI: 10.1016/j.bpj.2024.01.022.

Trends in Single-Molecule Total Internal Reflection Fluorescence Imaging and Their Biological Applications with Lab-on-a-Chip Technology.

Colson L, Kwon Y, Nam S, Bhandari A, Maya N, Lu Y Sensors (Basel). 2023; 23(18).

PMID: 37765748 PMC: 10537725. DOI: 10.3390/s23187691.

Increasing the accuracy of single-molecule data analysis using tMAVEN.

Verma A, Ray K, Bodick M, Kinz-Thompson C, Gonzalez Jr R bioRxiv. 2023; .

PMID: 37645812 PMC: 10462008. DOI: 10.1101/2023.08.15.553409.

Gold Ion Beam Milled Gold Zero-Mode Waveguides.

Messina T, Srijanto B, Collier C, Kravchenko I, Richards C Nanomaterials (Basel). 2022; 12(10).

PMID: 35630978 PMC: 9147361. DOI: 10.3390/nano12101755.

Pitching single-focus confocal data analysis one photon at a time with Bayesian nonparametrics.

Tavakoli M, Jazani S, Sgouralis I, Shafraz O, Sivasankar S, Donaphon B Phys Rev X. 2021; 10(1).

PMID: 34540355 PMC: 8445401. DOI: 10.1103/physrevx.10.011021.

References

Morimatsu M, Takagi H, Ota K, Iwamoto R, Yanagida T, Sako Y . Multiple-state reactions between the epidermal growth factor receptor and Grb2 as observed by using single-molecule analysis. Proc Natl Acad Sci U S A. 2007; 104(46):18013-8. PMC: 2084288. DOI: 10.1073/pnas.0701330104. View

Shinagawa H, Iwasaki H . Processing the holliday junction in homologous recombination. Trends Biochem Sci. 1996; 21(3):107-11. View

Antonik M, Felekyan S, Gaiduk A, Seidel C . Separating structural heterogeneities from stochastic variations in fluorescence resonance energy transfer distributions via photon distribution analysis. J Phys Chem B. 2006; 110(13):6970-8. DOI: 10.1021/jp057257+. View

Karymov M, Daniel D, Sankey O, Lyubchenko Y . Holliday junction dynamics and branch migration: single-molecule analysis. Proc Natl Acad Sci U S A. 2005; 102(23):8186-91. PMC: 1140338. DOI: 10.1073/pnas.0407210102. View

Holliday R . A mechanism for gene conversion in fungi. Genet Res. 2008; 89(5-6):285-307. DOI: 10.1017/S0016672308009476. View

Cox M, Goodman M, Kreuzer K, Sherratt D, Sandler S, Marians K . The importance of repairing stalled replication forks. Nature. 2000; 404(6773):37-41. DOI: 10.1038/35003501. View

West S . Processing of recombination intermediates by the RuvABC proteins. Annu Rev Genet. 1997; 31:213-44. DOI: 10.1146/annurev.genet.31.1.213. View

Kowalczykowski S, Dixon D, Eggleston A, Lauder S, Rehrauer W . Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 1994; 58(3):401-65. PMC: 372975. DOI: 10.1128/mr.58.3.401-465.1994. View

Chung H, Louis J, Eaton W . Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories. Proc Natl Acad Sci U S A. 2009; 106(29):11837-44. PMC: 2715475. DOI: 10.1073/pnas.0901178106. View

10.

Chung H, Gopich I, McHale K, Cellmer T, Louis J, Eaton W . Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. J Phys Chem A. 2010; 115(16):3642-56. PMC: 6407426. DOI: 10.1021/jp1009669. View

11.

Hibino K, Shibata T, Yanagida T, Sako Y . A RasGTP-induced conformational change in C-RAF is essential for accurate molecular recognition. Biophys J. 2009; 97(5):1277-87. PMC: 3325157. DOI: 10.1016/j.bpj.2009.05.048. View

12.

Campos L, Liu J, Wang X, Ramanathan R, English D, Munoz V . A photoprotection strategy for microsecond-resolution single-molecule fluorescence spectroscopy. Nat Methods. 2011; 8(2):143-6. DOI: 10.1038/nmeth.1553. View

13.

Xu C, Kim H, Hayden C, Yang H . Joint statistical analysis of multichannel time series from single quantum dot-(Cy5)n constructs. J Phys Chem B. 2007; 112(19):5917-23. DOI: 10.1021/jp075642o. View

14.

Messina T, Kim H, Giurleo J, Talaga D . Hidden Markov model analysis of multichromophore photobleaching. J Phys Chem B. 2006; 110(33):16366-76. PMC: 1995553. DOI: 10.1021/jp063367k. View

15.

Watkins L, Chang H, Yang H . Quantitative single-molecule conformational distributions: a case study with poly-(L-proline). J Phys Chem A. 2006; 110(15):5191-203. DOI: 10.1021/jp055886d. View

16.

Watkins L, Yang H . Information bounds and optimal analysis of dynamic single molecule measurements. Biophys J. 2004; 86(6):4015-29. PMC: 1304302. DOI: 10.1529/biophysj.103.037739. View

17.

Watkins L, Yang H . Detection of intensity change points in time-resolved single-molecule measurements. J Phys Chem B. 2006; 109(1):617-28. DOI: 10.1021/jp0467548. View

18.

Bronson J, Fei J, Hofman J, Gonzalez Jr R, Wiggins C . Learning rates and states from biophysical time series: a Bayesian approach to model selection and single-molecule FRET data. Biophys J. 2009; 97(12):3196-205. PMC: 2793368. DOI: 10.1016/j.bpj.2009.09.031. View

19.

Baba A, Komatsuzaki T . Construction of effective free energy landscape from single-molecule time series. Proc Natl Acad Sci U S A. 2007; 104(49):19297-302. PMC: 2148284. DOI: 10.1073/pnas.0704167104. View

20.

Karymov M, Chinnaraj M, Bogdanov A, Srinivasan A, Zheng G, Olson W . Structure, dynamics, and branch migration of a DNA Holliday junction: a single-molecule fluorescence and modeling study. Biophys J. 2008; 95(9):4372-83. PMC: 2567953. DOI: 10.1529/biophysj.108.135103. View