Publications

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Preprints

Cryo-electron tomography reveals the microtubule-bound form of inactive LRRK2.
S. Chen, T. Basiashvili, J. Hutchings, M. Sanz Murillo, A. Villagran Suarez, J. Alegrio Louro, A. E. Leschziner, E. Villa‡.
bioRxiv, 2024. doi: https://doi.org/10.1101/2024.06.18.599606

Asesino: a nucleus-forming phage that lacks PhuZ.
A. Prichard, A. Sy, J. Meyer, E. Villa, J. Pogliano.
bioRxiv. 2024 May 11. doi: https://doi.org/10.1101/2024.05.10.593592.

Integrative spatiotemporal map of nucleocytoplasmic transport.
B. Raveh, R. Eliasian, S. Rashkovits, D. Russel, R. Hayama, S. E. Sparks, D. Singh, R. Lim, E. Villa, M. P. Rout, D. Cowburn, A. Sali.
bioRxiv. 2024 Jan 2: 2023.2012.2031.573409. doi: 10.1101/2023.12.31.573409.

Sequential membrane- and protein-bound organelles compartmentalize genomres during phage infection.
E.G. Armbruster, J. Lee, J. Hutchings, A.R. VanderWal, E. Enustun, B.A. Adler, A. Aindow, A. Deep, Z.K. Rodriguez, C.J. Morgan, M. Ghassemian, E. Charles, B.F. Cress, D.F. Savage, J.A. Doudna, K. Pogliano, K.D. Corbett, E. Villa, J. Pogliano
bioRxiv. 2023 Sep 21:2023.09.20.558163. doi: 10.1101/2023.09.20.558163.

 

Peer-Reviewed

The Molecular Architecture of the Nuclear Basket.
D. Singh, N. Soni, J. Hutchings, I. Echeverria, F. Shaikh, M. Duquette, S. Suslov, Z. Li, T. van Eeuwen, K. Molloy, Y. Shi, J. Wang, Q. Guo, B.T. Chait, J. Fernandez-Martinez, M.P. Rout, A. Sali, E. Villa.
bioRxiv. 2024 Mar 27. doi: https://doi.org/10.1101/2024.03.27.587068.

Cell,  In press, 2024.

A mobile intron facilitates interference competition between co-infecting viruses.
E.A. Birkholz, C.J. Morgan, T.G. Laughlin, R.K. Lau, A. Prichard, S. Rangaraja, G.N. Meza, J. Lee, E.G. Armbruster, S. Suslov, K. Pogliano, J.R. Meyer, E. Villa, K.D. Corbett, J. Pogliano
bioRxiv. 2023 Sep 30:2023.09.30.560319. doi: 10.1101/2023.09.30.560319.
Science,  In press, 2024.

Cryo-Focused Ion Beam Milling of Cells.
D. Singh and E. Villa
In: F. Förster, A. Briegel (eds). Cryo-Electron Tomography: Structural Biology in situ, pp. 115-149, 2024. Springer International Publishing, Cham.

An essential and highly selective protein import pathway encoded by nucleus-forming phage.
C.J. Morgan, E. Enustun, E.G. Armbruster, E.A. Birkholz, A. Prichard, T. Forman, A. Aindow, W. Wannasrichan, S. Peters, K. Inlow, I.L. Shepherd, A. Razavilar, V. Chaikeeratisak, B.A. Adler, B.F. Cress, J.A. Doudna, K. Pogliano, E. Villa, K.D. Corbett, J. Pogliano.
PNAS, 121(19):e2321190121, 2024.

Identification of the bacteriophage nucleus protein interaction network.
E.Enustun, A. Deep, Y. Gu, K. T. Nguyen, V. Chaikeeratisak, E. Armbruster, M. Ghassemian, E. Villa, J. Pogliano‡, K. D. Corbett‡
Nature Structure & Molecular Biology,  3:1653-1662, 2023.

Bringing Structure to Cell Biology with Cryo-Electron Tomography.
L. N. Young, E. Villa‡.
Annual Reviews of Biophysics, 52:573-595, 2023.

Identifying the core genome of the nucleus-forming bacteriophage family and characterization of Erwinia phage RAY.
A. Prichard, J. Lee, T.G. Laughlin, A. Lee, K.P. Thomas, A.E. Sy, T. Spencer, A. Asavavimol, A. Cafferata, M. Cameron, N. Chiu, D. Davydov, I. Desai, G. Diaz, M. Guereca, K. Hearst, L. Huang, E. Jacobs, A. Johnson, S. Kahn, R. Koch, A. Martinez, M. Norquist, T. Pau, G. Prasad, K. Saam, M. Sandhu, A.J. Sarabia, S. Schumaker, A. Sonin, A. Uyeno, A. Zhao, K.D. Corbett, K. Pogliano, J. Meyer, J.H. Grose, E. Villa, R. Dutton, J. Pogliano‡ .
Cell Reports,  42(5):112432, 2023.

The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems.
K. Lasker‡, S. Boeynaems, V. Lam, D. Scholl, E. Stainton, A. Briner, M. Jacquemyn, D. Daelemans, A. Deniz, E. Villa, A. S. Holehouse, A. D. Gitler‡, L. Shapiro‡.
Nature Communications, 13:5643, 2022.

A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli.
E.A. Birkholz, T. G. Laughlin, S. Suslov, E. Armbruster, J. Lee, J. Wittmann, K.D. Corbett, E. Villa‡, J. Pogliano‡.
Cell Reports, 40:111179, 2022.

Architecture and self-assembly of the jumbo bacteriophage nuclear shell.
T. G. Laughlin*, A. Deep*, A. M. Prichard, C. Seitz, Y. Gu, E. Enustun, S. Suslov, K. Khanna, E. A. Birkholz, E. Armbruster, J. A. McCammon, R. E. Amaro, J. Pogliano‡, K. D. Corbett‡, E. Villa‡.
Nature, 608:429-435, 2022.

Revealing bacterial cell biology using cryo-electron tomography.
K. Khanna, E. Villa‡.
Current Opinion in Structural Biology, 75:102419, 2022.

Subcellular Organization of Viral Particles During Maturation of Nucleus-Forming Jumbo Phage.
V. Chaikeeratisak, K. Khanna, K.T. Nguyen, M.E. Egan, E. Enustun, E. Armbruster, K. Pogliano, E. Villa‡, J. Pogliano‡.
Science Advances, 8(18):eabj9670, 2022.

Comprehensive Structure and Functional Adaptations of the Yeast Nuclear Pore Complex.
C. W. Akey*‡, D. Singh*, C. Ouch*, I. Echeverria*, I. Nudelman, J. M. Varberg, Z. Yu, F. Fang, Y. Shi, J. Wang, D. Salzberg, K. Song, C. Xu, J. C. Gumbart, S. Suslov, J. Unruh, S.L. Jaspersen, B.T. Chait, A. Sali, J. Fernandez-Martinez‡, S. J. Ludtke‡, E. Villa‡, M. P. Rout‡.
Cell, 185(2):361-378. e25, 2022.
Read a Preview by Megan McCarthy and Patrick Lusk.

Entropy Regularized Deconvolution of Cellular Cryo-Transmission Electron Tomograms.
M. Croxford, M. Elbaum, M. Arigovindan, Z. Kam, D. A. Agard, E. Villa‡, J. Sedat‡.
PNAS, 118(50): e2108738118, 2021.

Selective transport of fluorescent proteins into the phage nucleus.
K.T. Nguyen, J. Sugie, K. Khanna, E.E. MacKennon, E.A. Birkholz, J. Lee, C. Beierschmitt, E. Villa, J. Pogliano‡.
PLoS ONE, 16:e0251429, 2021.

Asymmetric localization of the cell division machinery during Bacillus subtilis sporulation.
K. Khanna, J. Lopez-Garrido, J. Sugie, K. Pogliano‡, E. Villa‡.
eLife, 10:e62204, 2021.

Generating Chromosome Geometries in a Minimal Cell From Cryo-Electron Tomograms and Chromosome Conformation Capture Maps.
B.R. Gilbert, Z.R. Thornburg, V. Lam, F.M. Rashid, J.I. Glass, E. Villa, R.T. Dame, Z. Luthey-Schulten‡.
Frontiers in Molecular Biosciences, 8:644133, 2021.

The SARS-CoV-2 Nucleocapsid phosphoprotein forms mutually exclusive condensates with RNA and the membrane-associated M protein.
S. Lu*,  Q. Ye*, D. Singh, E. Villa, D.W. Cleveland‡, K. D. Corbett‡.
Nature Communications, 12:502, 2021.

Practical Approaches for Cryo-FIB Milling and Applications for Cellular Cryo-Electron Tomography.
V. Lam V., E. Villa.
In: Gonen T., Nannenga B.L. (eds) cryoEM. Methods in Molecular Biology,  vol 2215, pp 49-82, 2021. Humana, New York, NY.

HSP70 chaperones RNA-free TDP-43 into anisotropic intranuclear liquid spherical shells
H. Yu, S. Lu, K. Gasior, D. Singh, O. Tapia, S. Vazquez-Sanchez, D. Toprani, M. S. Beccari, J. R. Yates III, S. Da Cruz, J. M. Newby, M. Larfaga, A. S. Gladfelter, E. Villa, D. W. Cleveland
Science, 371(6529): eabb4309, 2021.

The in situ structure of Parkinson’s disease-linked LRRK2
R. Watanabe*,  R. Buschauer*,  J. Böhning*, M. Audagnotto, K. Lasker, T.W. Lu, D. Boassa, S. Taylor, E. Villa.
Cell, 182(6):1508-1518. e16, 2020.

Structure of LRRK2 in Parkinson’s disease and model for microtubule interaction
C. K. Deniston*, J. Salogiannis*, S. Mathea*, D. M. Snead, I. Lahiri, O. Donosa, R. Watanabe, J. Böhning, A. K Shiau, S. Knapp, E. Villa, S. L. Reck-Peterson‡, A. E. Leschziner‡
Nature,  588:344-349, 2020.

Preparing samples from whole cells using focused-ion-beam milling for cryo-electron tomography
F. R. Wagner*, R. Watanabe*, R. Schampers, D. Singh, H. Persoon, M. Schaffer,  P. Fruhstorfer, J. Plitzko, E. Villa
Nature Protocols, 15:2041-2070, 2020.

A novel vibriophage exhibits inhibitory activity against host protein synthesis machinery
K. Thammatinna, M. E. Egan, H. H. Htoo, K. Khanna, J. Sugie, J.F. Nideffer, E. Villa, A. Tassanakajon, J. Pogliano, P. Nonejuie, V. Chaikeeratisak
Scientific Reports,  10:2347, 2020.

Viral Capsid Trafficking along Treadmilling Tubulin Filaments in Bacteria
V. Chaikeeratisak, K. Khanna, K. T. Nguyen, J. Sugie, M. E. Egan, M. L. Erb, A. Vavilina, P. Nonejuie, E. Nieweglowska, K. Pogliano, D. A. Agard, E. Villa‡, J. Pogliano‡.
Cell,  177(7): 1771-1780. e12, 2019.

The molecular architecture of engulfment during Bacillus subtilis sporulation
K. Khanna, J. Lopez-Garrido, Z. Zhao, R. Watanabe, Y. Yuan, K. Pogliano‡, E. Villa‡
eLife, 8:e45257, 2019.

Chromosome Translocation Inflates Bacillus Forespores and Impacts Cellular Morphology. 
J. Lopez-Garrido, N. Ojkic, K. Khanna, F.R. Wagner, E. Villa, R.G. Endres, K. Pogliano.
Cell, 172(4):758-770. e14, 2018.

Challenges of Integrating Stochastic Dynamics and Cryo-Electron Tomograms in Whole-Cells Simulations.
T.M. Earnest, R. Watanabe, J. E. Stone, J. Mahamid, W. Baumeister, E. Villa, and Z. Luther-Schulten.
Klaus Schulten Memorial Issue, J. Phys. Chem. B., 121(15):3871–3881, 2017.

Assembly of a nucleus-like structure during viral replication in bacteria.
V. Chaikeeratisak, K. Nguyen, K. Khanna, A.F. Brilot, M.L. Erb, J.K. C. Coker,  A. Vavilina, G.L. Newton, R.Buschauer, K.Pogliano, E.Villa, D.A. Agard,  J. Pogliano.
Science, 355(6321):194-197, 2017.

Biography of Klaus Schulten.
R.E. Amaro, E. Villa, Z. Luthey-Schulten.
Journal of Physical Chemistry B, 121(15):3206, 2017.

Visualizing the molecular sociology at the HeLa cell nuclear periphery.
J. Mahamid, S. Pfeffer, M. Schaffer, E. Villa, R. Danev, L. Kuhn-Cuellar, F. Foerster, A. A. Hyman, J. M. Plitzko and W. Baumeister.
Science, 351(6276):969-972, 2016.

A photoactivable multi- inhibitor nanoliposome for tumour control and simultaneous inhibition of treatment escape pathways.
B. Q. Spring, R. B. Sears, L.Z. Zheng, Z. Mai, R. Watanabe, M. E. Sherwood, D. A. Schoenfeld, B. W. Pogue, S. P. Pereira, E. Villa, and T. Hasan.
Nature Nanotechnology11:378-387, 2016.

Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography.
B. D. Engel, M. Schaffer, L. K. Cuellar, E. Villa, J.M. Plitzko, W. Baumeister.
eLife, 4:e04889, 2015.

Architecture of the RNA polymerase II-Mediator core transcription initiation complex.
C. Plaschka, L. Lariviere, L. Wenzeck, M. Hemann, D. Tegunov, E.V. Petrotchenko, C.H. Borchers, W. Baumeister, F. Herzog, E. Villa, and P. Cramer.
Nature, 518:376-380, 2015.

Finding the right fit: chiseling structures out of cryo-electron microscopy maps.
E. Villa‡, K. Lasker‡.
Current Opinion in Structural Biology, 25:118–25, 2014.

Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography.
E. Villa, M. Schaffer, J.M. Plitzko and W. Baumeister.
Current Opinion in Structural Biology, 23(5):771–777, 2013.

Three-dimensional architecture of actin filaments in Listeria monocytogenes comet tails.
M.Jasnin, S. Asano, E. Gouin, R. Hegerl, J.M. Plitzko, E. Villa, et al.
PNAS, 110(51):20521- 20526, 2013.

Near-atomic resolution structural model of the yeast 26S proteasome.
F. Beck, P. Unverdorben, S. Bohn, A. Schweitzer , G. Pfeifer, E. Sakata, S. Nickell, J.M. Plitzko, E. Villa, W. Baumeister, F. Foerster.
PNAS 109(37):14870-14875, 2012.

Promiscuous behaviour of archaeal ribosomal proteins: Implications for eukaryotic ribosome evolution.
J.P. Armache, A.M. Anger, V. Marquez, S. Frackenberg, E. Villa, M. Thomm., R. Beckmann, D.N. Wilson.
Nucleic Acids Research, 41(2): 1284–1293, 2013.

Integrative Approaches for Cellular Cryo-electron Tomography: Correlative Imaging and Focused Ion Beam Micromachining.
A. Rigort, E. Villa, F. Baeuerlein, B.D. Engel, and J.M. Plitzko.
Methods in Cell Biology, 111:259-281, 2012.

The structure of human Tripeptidyl peptidase II as determined by a hybrid approach.
A. Schoenegge, E. Villa, F. Foerster, R. Hegerl, J. Peters, W. Baumeister, and B. Rockel.
Structure, 20(4):593-603, 2012.

Focused ion beam micromachining of eukaryotic cells for cryo-electron tomography.
A. Rigort*, F.J.B. Baeuerlein*, E. Villa, M. Eibauer, T. Laugks, W. Baumeister and J.M. Plitzko.
PNAS, 109(12):4449-4454, 2012.

Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach.
K. Lasker, F. Foerster, S. Bohn, T. Walzthoenid, E. Villa, P. Unverdorben, F. Beck, R. Aebersold, A. Sali, and W. Baumeister.
PNAS, 109(5):1380-1387, 2012.

Dynein achieves processive motion using both stochastic and coordinated stepping.
W. Qiu, N.D. Derr, B.S. Goodman, E. Villa, D. Wu, W. Shih and S.L. Reck-Peterson.
Nature Structural & Molecular Biology, 19(2):193-200, 2012.

Structure determination of macromolecular complexes by cryo-electron microscopy in vitro and in situ.
F. Foerster, E. Villa, D. Thomas, A. Korinek, and W. Baumeister.
Chapter in Comprehensive Biophysics 1, Biophysical Techniques for Structural Characterization of Macromolecules, ed. E. Egelman, and H.J. Dyson. Elsevier B. V. Academic Press, Oxford, pp. 245-276, 2012.

Structure of the no-go mRNA decay complex Dom34- Hbs1 bound to a stalled 80S ribosome.
T.Becker, J.P. Armache, A.M. Anger, E. Villa, H. Sieber, B.A. Motaal, T. Mielke, O. Berninghausen, and R. Beckmann.
Nature Structural & Molecular Biology, 18:715-20, 2011.

Applications of the molecular dynamics flexible fitting method.
L.G. Trabuco, E. Schreiner, J. Gumbart, J. Hsin, E. Villa, and K. Schulten.
Journal of Structural Biology, 173(3): 420-427, 2011.

Integration of cryo-EM with atomic and protein-protein interaction data.
F. Foerster, E. Villa.
Methods in Enzymology, 483:47-72, 2010.

Localization of eukaryote-specific ribosomal proteins in a 5.5-A cryo-EM map of the 80S eukaryotic ribosome.
 J.P. Armache*, A. Jarasch*, A.M. Anger*, E. Villa, T. Becker, S. Bhushan, F. Jossinet, M. Habeck, G. Dindar, S. Franckenberg, V. Marquez, T. Mielke, M. Thomm, O. Berninghausen, B. Beatrix, J. Soeding, E. Westhof, D.N. Wilson, and R. Beckmann.
PNAS, 107(46): 19754-19759, 2010.

Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution.
J.P. Armache*, A. Jarasch*, A.M. Anger*, E. Villa, T. Becker, S. Bhushan, F. Jossinet, M. Habeck, G. Dindar, S. Franckenberg, V. Marquez, T. Mielke, M. Thomm, O. Berninghausen, B. Beatrix, J. Soeding, E. Westhof, D.N. Wilson, and R. Beckmann.
PNAS, 107(46): 19748-19753, 2010.

Visualizing cellular processes at the molecular level by cryo-electron tomography.
K. Ben-Harush, T. Maimon, I. Patla, E. Villa, and O. Medalia.
Journal of Cell Science, 123(1):7-12, 2010.

Regulation of the protein–conducting channel by a bound ribosome.
J.Gumbart, L.G.Trabuco, E.Schreiner, E. Villa, and K. Schulten.
Structure, 17(11):1453-1464, 2009.

Structural insight into nascent polypeptide chain-mediated translational stalling.
B. Seidelt, C.A. Innis, D.N. Wilson, M. Gartmann, J.P. Armache, E. Villa, L.G. Trabuco, T. Becker, T. Mielke, K. Schulten, T.A. Steitz, and R. Beckmann.
Science, 326(5958):1412-1415, 2009.

Protein–induced membrane curvature investigated through molecular dynamics flexible fitting.
J. Hsin, J. Gumbart, L.G. Trabuco, E. Villa, P. Qian, C.N. Hunter, and K. Schulten.
Biophysical Journal, 97(1):321:329, 2009.

Molecular dynamics flexible fitting: A practical guide to combine cryo-electron microscopy and x-ray crystallography.
L.G. Trabuco*, EV*, E. Schreiner, C. B. Harrison, and K. Schulten.
Methods, 49(2):174:180, 2009.

Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis.
EV*, J. Sengupta*, L. Trabuco, J. LeBarron, W.T. Baxter, T. Shaikh, R.A. Grassucci, M. Ehrenberg, K. Schulten, and J. Frank.
PNAS, 106(4):1063:1068, 2009.

Structural model and excitonic properties of the dimeric LH1-RC-PufX complex from Rhodobacter sphaeroides.
M.K. Sener, J. Hsin, L.G. Trabuco, E. Villa, P. Qian, P.A. Bullough, C.N. Hunter, and K. Schulten.
Chemical Physics, 357(1-3):188-197, 2009.

Flexible Fitting of Atomic Structures into Electron Microscopy Maps Using Molecular Dynamics.
L. G. Trabuco*, EV*, K. Mitra, J. Frank, and K. Schulten.
Structure, 16(5):673-683, 2008.

Molecular mechanisms of cellular mechanics.
M. Gao, M. Sotomayor, E. Villa, E. Lee, and K. Schulten.
Physical Chemistry Chemical Physics,  8(32):3692-3706, 2006.

Scalable molecular dynamics with NAMD.
J. C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten.
Journal of Computational Chemistry, 26(16):1781-1802, 2005.

Structural dynamics of the Lac repressor-DNA complex revealed by a multiscale simulation.
E. Villa, A. Balaeff, and K. Schulten.
PNAS, 102(19):6783-6788, 2005.

Multi-scale method for simulating protein-DNA complexes.
E. Villa, A. Balaeff, L. Mahadevan, and K. Schulten.
Multiscale Modeling and Simulation, 2(4):527-553, 2004.

*Equal contribution; ‡Co-corresponding author