Publications

Selected Publications from the Woodside Lab

2023

“Atomistic structure of the SARS-CoV-2 pseudoknot in solution from SAXS-driven molecular dynamics” Weiwei He, Josue San Emeterio, Michael T Woodside, Serdal Kirmizialtin, Lois Pollack, Nucleic Acids Research , gkad809

“Nonlinear effects in optical trapping of titanium dioxide and diamond nanoparticles.” Anita Devi, Krishna Neupane, Haksung Jung, Keir C. Neuman, Michael T. Woodside. Biophys. J. 122:3439–3446 (2023). Link to manuscript.

“Modelling the structures of frameshift-stimulatory pseudoknots from representative bat coronaviruses.” R.V. Sekar, P.J. Oliva , M.T. Woodside, PLoS Comp. Biol. 19(5): e1011124

“Hidden depths of protein folding.” K.Neupane, M.T. Woodside, Nature Physics.

2022

“Probing the origin of prion protein misfolding via reconstruction of ancestral proteins.” L. M. Cortez , A.J. Morrison, C.R. Garen, S. Patterson, T. Uyesugi, R. Petrosyan, R. V. Sekar, M, J. Harms, M.T. Woodside, V. L. Sim, Protein Science. 31( 12):e4477

” Quantifying Oligomer Populations in Real Time during Protein Aggregation Using Single-Molecule Mass Photometry.” S. S. Paul, A. Lyons , R. Kirchner, M.T. Woodside,ACS NANO. 16 (10), 16462-16470

“Identifying Inhibitors of —1 Programmed Ribosomal Frameshifting in a Broad Spectrum of Coronaviruses.” S. Munshi, K. Neupane, S.M. Ileperuma, M.T.J. Halma, J.A. Kelly, C.F. Halpern, J.D. Dinman, S. Loerch, M.T. Woodside, Viruses. 14:177

2021

“Observing the base-by-base search for native structure along transition paths during the folding of single nucleic acid hairpins.” N.Q. Hoffer, K. Neupane, M.T. Woodside, Proc. Natl. Acad. Sci. USA.

“Single-molecule force spectroscopy of protein folding.” R. Petrosyan, A. Narayan, M.T. Woodside, J. Mol. Biol. 433.20:167207 (2021). Link to manuscript.

“Structural dynamics of the SARS-CoV-2 frameshift-stimulatory pseudoknot reveal topologically distinct conformers.” K. Neupane*, M. Zhao*, A. Lyons, S. Munshi, S.M. Ileperuma, D.B.Ritchie, N.Q. Hoffer, A. Narayan, M.T. Woodside, Nat. Commun. 12:4749 (2021). Link to manuscript.

“Mechanical strength of RNA knot in Zika virus protects against cellular defenses.” M. Zhao, M.T. Woodside. Nat. Chem. Biol. 17:975–981 (2021). Link to manuscript. Featured in an accompanying News & Views, a “Research Highlight” in Nature, “Editor’s Choice” in Science, and commentary in Sci. Transl. Med.

“Modeling the structure of the frameshift-stimulatory pseudoknot in SARS-CoV-2 reveals multiple possible conformers.” S.I. Omar, M. Zhao, R.V. Sekar,S.A. Moghadam, J.A. Tuszynksi, M.T. Woodside. PLoS Comp. Biol. 17:e1008603 (2021). Link to manuscript. 

“Unfolded and intermediate states of PrP play a key role in the mechanism of action of an anti-prion chaperone.” R. Petrosyan, S. Patra, N. Rezajooei, C.R. Garen, M.T. Woodside. Proc. Natl. Acad. Sci. USA. 118:e2010213118 (2021). Link to manuscript. 

“Internalization of α-synuclein oligomers into SH-SY5Y cells.” L.J. Shearer, N.O. Petersen, M.T. Woodside. Biophys. J. 120:877–885 (2021). Link to manuscript.

“Conformational Shannon entropy of mRNA structures measured by force spectroscopy predicts the efficiency of −1 programmed ribosomal frameshift stimulation.” M.T.J. Halma, D.B. Ritchie, M.T. Woodside. Phys. Rev. Lett. 126:038102 (2021). Link to manuscript

“Programmed −1 ribosomal frameshifting in coronaviruses: a therapeutic target.” J.A. Kelly, M.T. Woodside, J.D. Dinman. Virology. 554:75–82 (2021). Link to manuscript

2020

“Anti-frameshifting ligand active against SARS coronavirus-2 is resistant to natural mutations of the frameshift-stimulatory pseudoknot.” K. Neupane*, S. Munshi*, M. Zhao, D.B. Ritchie, S.M. Ileperuma, M.T. Woodside. J. Mol. Biol. 432:5843–5847 (2020). Link to manuscript

“Structural and functional conservation of the programmed −1 ribosomal frameshift signal of SARS coronavirus 2 (SARS-CoV-2).” J.A. Kelly, A.N. Olson, K. Neupane, S. Munshi, J. San Emeterio, L. Pollack, M.T. Woodside, J.D. Dinman. J. Biol. Chem. 295:10741–10748 (2020). Link to manuscript

2019

“Memory effects in single-molecule force spectroscopy measurements of biomolecular folding.” A.G.T. Pyo, M.T. Woodside. Phys. Chem. Chem. Phys. 21:24527–24534 (2019). Link to manuscript.

“Molecular free energy profiles from force spectroscopy experiments by inversion of observed committors.” R. Covino, M.T. Woodside, G. Hummer, A. Szabo, P. Cossio. J. Chem. Phys. 151:154115 (2019). Link to manuscript, highlighted as “Featured Article”.

“Probing the basis of α-synuclein aggregation by comparing simulations to single-molecule experiments.” C.D.M. Churchill, M.A. Healey, J. Preto, J.A. Tuszynski, M.T. Woodside. Biophys. J. 117:1125–1135 (2019). Link to manuscript.

“Probing microscopic conformational dynamics in folding reactions by measuring transition paths.” N.Q. Hoffer, M.T. Woodside. Curr. Opin. Chem. Biol. 53:68–74 (2019). Link to manuscript.

“Complex dynamics under tension in a high-efficiency frameshift stimulatory structure.” M.T.J. Halma, D.B. Ritchie, T.R. Cappellano, K. Neupane, M.T. Woodside. Proc. Natl. Acad. Sci. USA 116:19500–19505 (2019). Link to manuscript, and highlight in Commentary in PNAS.

“Characterizing the inhibition of α-synuclein oligomerisation by a pharmacological chaperone that prevents prion formation by the protein PrP.” C. Dong*, C.R. Garen*, P. Mercier, N.O. Petersen, M.T. Woodside. Prot. Sci. 28:1690–1702 (2019). Link to manuscript.

“Measuring the average shape of transition paths during the folding of a single biological molecule.” N.Q. Hoffer, K. Neupane, A.G.T. Pyo, M.T. Woodside. Proc. Natl. Acad. Sci. USA. 116:8125–8130 (2019). Link to manuscript.

“Early stages of aggregation of engineered α-synuclein monomers and oligomers in solution.” X. Li, C. Dong, M. Hoffmann, C. Garen, Leo M. Cortez, N.O Petersen, M.T. Woodside. Sci. Rep. 9:1734 (2019). Link to manuscript.

2018

“High-precision single-molecule characterization of the folding of an HIV RNA hairpin by atomic force microscopy.” R. Walder, W.J. Van Patten, D.B. Ritchie, R.K. Montange, T.W. Miller, M.T. Woodside, T.T. Perkins. Nano Lett. 18:6318–6325 (2018). Link to manuscript.

“Transition-path properties for folding reactions in the limit of small barriers.” A.G.T. Pyo, N.Q. Hoffer, K. Neupane, M.T. Woodside. J. Chem. Phys. 149:115101 (2018). Link to manuscript.

“Testing kinetic identities involving transition-path properties using single-molecule folding trajectories.” K. Neupane*, N.Q. Hoffer*, M.T. Woodside. J. Phys. Chem. B. 122:11095–11099 (2018). Link to manuscript.

“Measuring the velocity along transition paths during the folding of single biological molecules.” K. Neupane*, N.Q. Hoffer*, M.T. Woodside. Phys. Rev. Lett. 121:018102 (2018). Link to manuscript.

“Structural characteristics and membrane interactions of tandem α-synuclein oligomers.” C. Dong*, M. Hoffmann*, X. Li, M. Wang, Craig R. Garen, N.O. Petersen, M.T. Woodside. Sci. Rep. 8:6755 (2018). Link to manuscript.

“Probing position-dependent diffusion in biomolecular folding reactions using single-molecule force spectroscopy.” D.A.N. Foster, R. Petrosyan, A.G.T. Pyo, J. Lambert, A. Hoffmann, F. Wang, M.T. Woodside. Biophys. J. 114:1657–1666 (2018). Link to manuscript.

2017

“Partially native intermediates mediate misfolding of SOD1 in single-molecule folding trajectories.” S. Sen Mojumdar, Z.N. Scholl, D.R. Dee, L. Rouleau, U. Anand, C. Garen, M.T. Woodside. Nat. Commun. 8:1881 (2017). Link to manuscript. Featured in EurekAlert, MedicalXpress, Science Newsline, News Medical, 630-CHED radio.

“Conformational dynamics of the frameshift stimulatory structure in HIV-1.” D.B. Ritchie, T.R. Cappellano, C. Tittle, N. Rezajooei, L. Rouleau, W.K.A. Sikkema, M.T. Woodside. RNA 23:1376–1384 (2017). Link to manuscript.

“Direct measurement of sequence-dependent transition path times and conformational diffusion in DNA duplex formation.” K. Neupane, F. Wang, M.T. Woodside. Proc. Natl. Acad. Sci. USA 114:1329–1334 (2017). Link to manuscript.

2016

“Quantifying instrumental artifacts in folding kinetics measured by single-molecule force spectroscopy.” K. Neupane, M.T. Woodside. Biophys. J. 111:283–286 (2016). Link to manuscript.

“Pharmacological chaperone reshapes the energy landscape for folding and aggregation of the prion protein.” A.N. Gupta*, K. Neupane*, N. Rezajooei, L. Cortez, V. Sim, M.T. Woodside. Nat. Commun. 7:12058 (2016). Link to manuscript. Featured in the Edmonton Journal and Calgary Sun (June 27, 2016), Science Daily, and Phys.org.

“Comparing the energy landscapes for native folding and aggregation of PrP.” D.R. Dee, M.T. Woodside. Prion 10:207–220 (2016). Link to manuscript.

“Direct observation of transition paths during the folding of proteins and nucleic acids.” K. Neupane, D.A.N. Foster, D.R. Dee, H. Yu, F. Wang, M.T. Woodside§. Science 352:239–242 (2016). Link to manuscript and Perspective commentary, as well as link to commentary in Physics Today. Also featured in Chemical & Engineering News and Chemistry World.

“Protein folding trajectories can be described by one-dimensional diffusion over measured energy landscapes.” K. Neupane, A.P. Manuel, M.T. Woodside. Nature Physics 12:700–703 (2016). Link to manuscript.

2015

“Probing the structural dynamics of proteins and nucleic acids with optical tweezers.” D.B. Ritchie, M.T. Woodside. Curr. Opin. Struct. Biol. 34:43–51 (2015). Link to manuscript.

“Protein misfolding occurs by slow diffusion across multiple barriers in a rough energy landscape.” H. Yu*, D.R. Dee*, X. Liu, A.M. Brigley, I. Sosova, M.T. Woodside. Proc. Natl. Acad. Sci. USA 112:8308–8313 (2015). Link to manuscript.

“Reconstructing folding energy landscapes from splitting probability analysis of single-molecule trajectories.” A.P. Manuel, J. Lambert, M.T. Woodside. Proc. Natl. Acad. Sci. USA 112:7183-7188 (2015). Link to manuscript.

“Transition path probability as a test of reaction-coordinate quality reveals DNA hairpin folding is a one-dimensional diffusive process.” K. Neupane, A.P. Manuel, J. Lambert, M.T. Woodside. J. Phys. Chem. Lett., 6:1005–1010 (2015). Link to manuscript.

2014

“Reconstructing folding energy landscape profiles from non-equilibrium pulling curves with an inverse Weierstrass integral transform.” M.C. Engel, D.B. Ritchie, D.A.N. Foster, K.S.D. Beach, M.T. Woodside. Phys. Rev. Lett., 113:238104 (2014).  Link to manuscript. Featured as an “Editor’s Suggestion.”

“Determining intrachain diffusion coefficients for biopolymer dynamics from single-molecule force spectroscopy measurements.” M.T. Woodside, J. Lambert, K.S.D. Beach. Biophys J., 107:1647–1653 (2014). Link to manuscript.

“Reconstructing folding energy landscapes by single-molecule force spectroscopy.” M.T. Woodside, S.M. Block, Annu. Rev. Biophys. 43: 19-39 (2014). Link to manuscript.

“Single-molecule force spectroscopy of rapidly-fluctuating, marginally-stable structures in the intrinsically-disordered protein α-synuclein.” A. Solanki*, K. Neupane*, M.T. Woodside. Phys. Rev. Lett., 112:158103 (2014). Link to manuscript.

“Diverse metastable structures formed by small oligomers of α-synuclein probed by force spectroscopy.” K. Neupane*, A. Solanki*, I. Sosova, M. Belov, M.T. Woodside. PLoS ONE 9:e86495 (2014). Link to manuscript.

“Anti-frameshifting ligand reduces conformational plasticity of the SARS virus pseudoknot.” D.B. Ritchie, J. Soong, W.K.A. Sikkema, M.T. Woodside. J. Am. Chem. Soc., 136:2196–2199 (2014). Link to manuscript.

2013

“Single-molecule assays for investigating protein misfolding and aggregation.” A. Hoffmann, K. Neupane, M.T. Woodside. Phys. Chem. Chem. Phys. 15:7934–7948 (2013). Link to manuscript.

“Single-molecule approaches to prion protein misfolding.” H. Yu, D.R. Dee, M.T. Woodside, Prion 7:140–146 (2013). Link to manuscript.

2012

“Programmed −1 frameshifting efficiency correlates with RNA pseudoknot conformational plasticity, not resistance to mechanical unfolding.” D.B.Ritchie, D.A.N. Foster, M.T. Woodside. Proc. Natl. Acad. Sci. USA 109:16167–16172 (2012). Link to manuscript.

“Energy landscape analysis of native folding of the prion protein yields the diffusion constant, transition path time, and rates.” H. Yu*, A.N. Gupta*, X. Liu, K. Neupane, A.M. Brigley, I. Sosova, M.T. Woodside§. Proc. Natl. Acad. Sci. USA 109:14452–14457 (2012). Link to manuscript.

“Transition path times for nucleic acid folding determined from energy landscape analysis of single-molecule trajectories.” K. Neupane, D.B. Ritchie, H. Yu, D.A.N. Foster, F. Wang, M.T. Woodside. Phys. Rev. Lett. 109:068102 (2012). Links to manuscript and Viewpoint commentary in Physics.

“Phthalocyanine tetrasulfonates bind to multiple sites on natively-folded prion protein.” D. Dee*, A.N. Gupta*, M. Anikovskiy, I. Sosova, E. Grandi, L. Rivera, A.M Brigley, N.O. Petersen, M.T. Woodside. BBA Proteins & Proteomics 1824:826–832 (2012). Link to manuscript.

“Direct observation of multiple misfolding pathways in a single prion protein molecule.” H. Yu*, X. Liu*, K. Neupane, A.N. Gupta, A.M Brigley, A. Solanki, I. Sosova, M.T. Woodside. Proc. Natl. Acad. Sci. USA 109:5283–5288 (2012). Link to manuscript. Featured as an “Editor’s Choice” in Science.

2011

“Signal-pair correlation analysis of single-molecule trajectories.” A. Hoffmann, M.T. Woodside, Angewandte Chemie Intl. Ed. 50:12643–12646 (2011). Links to manuscript and Highlight commentary in ChemPhys Chem. Featured by the Editors as a “Very Important Paper” (top 5% of journal).

“Single-molecule force spectroscopy of the add adenine riboswitch relates folding to regulatory mechanism.” K. Neupane*, H. Yu*, D.A.N. Foster, F. Wang, M.T. Woodside, Nucleic Acids Res. 39:7630–7640 (2011). Link to manuscript.

“Experimental validation of free-energy-landscape reconstruction from non-equilibrium single-molecule force spectroscopy measurements.” A.N. Gupta*, A. Vincent*, K. Neupane, H. Yu, F. Wang, M.T. Woodside, Nature Physics 7:631–634 (2011). Links to manuscript and News and Views commentary.

2008 – 2010

“Folding and unfolding single RNA molecules under tension.” M.T. Woodside, C. García-García, S.M. Block, Curr. Opin. Chem. Biol. 12:640–646 (2008). Link to manuscript

“Direct observation of hierarchical folding in single riboswitch aptamers.” W.J. Greenleaf*, K.L. Frieda, D.A.N. Foster, M.T. Woodside*, S.M. Block, Science 319: 630–633 (2008). Link to manuscriptFeatured as a “Preview” in Chemistry & Biology

Postdoctoral Publications

“High-resolution, single-molecule measurements of biomolecular motion.” W.J. Greenleaf, M.T. Woodside, S.M. Block, Annu. Rev. Biophys. Biomol. Struct. 36:171–190 (2007). Link to manuscript.

“Direct measurement of the full, sequence-dependent folding landscape of a nucleic acid.” M.T. Woodside, P.C. Anthony, K. Larizadeh, W.M. Behnke-Parks, D. Herschlag, S.M. Block, Science 314:1001–1004 (2006). Link to manuscript.

“Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins.” M.T. Woodside, W.M. Behnke-Parks, K. Larizadeh, K. Travers, D. Herschlag, S.M. Block, Proc. Natl. Acad. Sci. USA 103:6190–6195 (2006). Link to manuscript. 

“Passive all-optical force clamp for high-precision laser trapping.” W.J. Greenleaf*, M.T. Woodside*, E.A. Abbondanzieri, S.M. Block§, Phys. Rev. Lett. 95:208102 (2005). Link to manuscript