3D Electron Microscopy Of Molecular Assemblies
Zhang Lab University of Pittsburgh School of Medicine Department of Structural Biology
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Wang M., Quinn C.M., Perilla J.R., Zhang H., Shirra Jr. R., Hou G., Byeon I.J., Suiter C.L., Ablan S., Urano E., Nitz T.J., Aiken C., Freed E.O., Zhang P., Schulten K., Gronenborn A.M., Polenova T. (2017) Modulation of protein dynamics during HIV capsid maturation. Nat Commun, in press.
Alvarez F.J.D., He S., Perilla J.R., Jang S., Schulten K., Engelman A.N., Scheres S.H.W. and Zhang P.* (2017) CryoEM structure of MxB reveals a novel oligomerization interface critical for HIV restriction. Sci. Adv. 3(9):e1701264.
Cassidy C.K., Himes B.A., Luthey-Schulten Z. and Zhang P.*(2017) CryoEM-based Hybrid Modeling Approaches for Structure Determination. Curr. Opin. Micro. Biol. 43:14-23.
Perilla J.R., Zhao G., Lu M., Ning J., Hou G., Byeon I.L, Gronenborn A.M., Polenova T. and Zhang P.* (2017) CryoEM Structure Refinement by Integrating NMR Chemical Shifts with Molecular Dynamics Simulations. J Phys. Chem. B, 121(15):3853-3863.
Yang M., Chan H., Zhao G., Bahng J.H., Zhang P.*, Petr Kršąl P. and Kotov N.A. (2017) Self-assembly of Nanoparticles into Biomimetic Capsid-like Nanoshells. Nat. Chem. 9(3):287-294.

Clare D.K., Siebert C.A., Hecksel C., Hagen C., Mordhorst V., Grange M., Ashton A.W., Walsh M.A., Grščnewald K., Saibil H.R., Stuart D.I., Zhang P.* (2017) Electron Bio-Imaging Centre (eBIC): the UK national research facility for biological electron microscopy. Acta Crystallogr D Struct Biol 73, 488-495.

Ning J., Erdemci-Tandogan G., Yufenyuy E.L., Wagner J., Himes B.A., Zhao G., Aiken C., Zandi R. and Zhang P.* (2016) In vitro Protease Cleavage and Computer Simulations Reveal the HIV-1 Capsid Maturation Pathway. Nat Commun. 7, 13689.
Merg A.D., Boatz J.C., Mandal A., Zhao G., Mokashi-Punekar S., Liu C., Wang X., Zhang P., van der Wel P.C.A. and Rosi N.L. (2016) Peptide-Directed Assembly of Single-Helical Gold Nanoparticle Superstructures Exhibiting Intense Chiroptical Activity. J. Am. Chem. Soc. 138 (41), 13655-13663.
Tillman TS, Alvarez FJ, Reinert NJ, Liu C, Wang D, Xu Y, Xiao K, Zhang P. and Tang P. (2016) Functional Human α7 Nicotinic Acetylcholine Receptor (nAChR) Generated from Escherichia coli. J Biol Chem. 291(35):18276-82
Sun J., Chen Y., Li K., Huang Y., Fu X., Zhang X., Zhao W., Wei Y., Xu L., Zhang P., Venkataramanan R. and Li S. (2016) A Prodrug Micellar Carrier Assembled from Polymers with Pendant Farnesyl Thiosalicylic Acid Moieties for Improved Delivery of Paclitaxel. Acta Biomater. 43:282-91.
Liu C., Perilla J. R., Ning J., Lu M., Hou G., Ramalho R., Bedwell G., Byeon I., Ahn J., Gronenborn A. M., Prevelige P., Rousso I., Aiken, C., Polenova T., Schulten K. and Zhang P.* (2016) Cyclophilin A Stabilizes the HIV-1 Capsid through a Novel Non-canonical Binding Site. Nat Commun. 7, 10714.

Cassidy C. K, Himes B. A., Alvarez F. J., Ma J., Zhao G., Perilla J. R., Schulten K. and Zhang P.* (2015) CryoEM and Computer Simulations Reveal a Novel Kinase Conformational Switch in Bacterial Chemotaxis Signaling. Elife. 2015 Nov 19;4. pii: e08419. doi: 10.7554/eLife.08419.
Lu M., Hou G., Zhang H., Suiter C.L., Ahn J., Byeon I.L., Perilla J.R., Langmead C., Hung I., Gorkov P.L., Gan Z., Brey W., Aiken C., Zhang P., Schulten K., Gronenborn A.M. and Polenova T. (2015) Dynamic Allostery Governs Cyclophylin A - HIV Capsid Interplay. Proc Natl Acad Sci USA 112(47):14617-22.
Lu J., Liu C., Wang P., Ghazwani M., Xu J., Huang Y., Ma X., Zhang P., Li S. (2015) The Self-assembling Camptothecin-tocopherol Prodrug: An Effective Approach for Formulating Camptothecin. Biomaterials 62:176-87.
Yeom J., Yeom B., Chan H., Smith K.W., Dominguez-Medina S., Bahng J.H., Zhao G., Chang W., Chang S.J., Chuvilin A., Melnikau D., Rogach A.L., Zhang P., Link S., Král P. and Kotov N.A. (2015) Chiral Templating of Self-Assembling Nanostructures by Circularly Polarized Light. Nat Mater 14(1):66-72.

Fu X., Himes B., Ke D., Rice W. J., Ning J. and Zhang P.* (2014) Controlled Bacterial Lysis for Electron Tomography of Native Cell Membranes. Structure 22(12):1875-82.
Fribourgh J. L., Nguyen H. C., Matreyek K. A., Alvarez  F. J. D., Summers B. J., Dewdney T. G., Aiken C., Zhang P., Engelman A. and Xiong Y. (2014) Structural Insight into HIV-1 Restriction by Myxovirus Resistance Protein 2 (MxB). Cell Host & Microbe 16(5):627-38.
Saini S. G., Liu C., Zhang P. and Lee T. H. (2014). Membrane Tethering by the Atlastin GTPase Depends on GTP Hydrolysis But Not on Forming the Crossover Configuration. Mol Biol Cell 25(24):3942-53.
Park J., Nguyen T. D., Silveira G. Q., Bahng J. H., Srivastava S., Zhao G., Sun K., Zhang P., Sharon C. Glotzer S. C. and Kotov N. A. (2014). Terminal Supraparticle Assemblies from Similarly Charged Protein Molecules and Nanoparticles. Nat Commun. 20(5):3593.
Schirra R. T. Jr and Zhang P.* (2014) Correlative Fluorescence and Electron Microscopy. Curr Protoc Cytom. 70:12.36.1–12.36.10.
Zhao G. and Zhang P.* (2014) CryoEM Analysis of Capsid Assembly and Structural Changes upon Interactions with a Host Restriction Factor, TRIM5α. Human Retroviruses: Methods in Molecular Biology 1087, 13-28.
Hickey R. J., Koski J., Meng X., Riggleman R. A., Zhang P., Park S. J. (2014) Size-controlled Self-assembly of Superparamagnetic Polymersomes. ACS Nano 8(1),495-502.

Zhao G., Perilla J.R., Yufenyuy E.L., Meng X., Chen B., Ning J., Ahn J.,Gronenborn A.M., Schulten K., Aiken C. and Zhang P.* (2013) Structure of the Mature HIV-1 Capsid by Cryo-EM and All-Atom Molecular Dynamics Simulation. Nature 497, 643-646. Featured on Nature Cover.
Zhang P.* (2013) Correlative Cryo-electron Tomography and Optical Microscopy of Cells. Curr Opin Struct Biol. 23(5):763-70.
Zhang P., Huang Y., Makhov A.M., Gao X., Zhang P. and Li S. (2013) Characterization of Spherulites as a Lipidic Carrier for Low and High Molecular Weight Agents. Pharm Res. 30(6):1525-35.
Mowrey D., Cui T., Jia Y., Ma D., Makhov A.M.,Zhang P., Tang P. and Xu Y. (2013) Open-Channel Structures of the Human Glycine Receptor α1 Full-Length Transmembrane Domain.Structure 21(10):1897-904.
Song C., Blaber M.G., Zhao G., Zhang P., Fry H.C., Schatz G.C. and Rosi N.L. (2013) Tailorable Plasmonic Circular Dichroism Properties of Helical Nanoparticle Superstructures. Nano Letter 13(7):3256-61.
Hickey R. J., Meng X., Zhang P. and Park S. (2013) Low-dimensional Nanoparticle Clustering in Polymer Micelles and Their Transverse Relaxivity Rates. ACS Nano 7(7):5824-5833.
Aiken C. and Zhang P.(2013) HIV-1 Maturation. Springer Book on Advances in HIV-1 Assembly and Release 153-166.
Jun S., Zhao G., Ning J., Gibson G., Watkins S. and Zhang P.* (2013) Correlative Microscopy for 3D Structural Analysis of Dynamic Interactions. J Vis Exp. 76: e50386, doi:10.3791/50386. 
Gao X., Huang Y., Makhov A., Epperly M, Lu J., Grab S., Zhang P., Rohan L., Xie X., Wipf P., Greenberger J. and Li S. (2013) Nano-assembly of Surfactants with Interfacial Drug-Interactive Motifs as Tailor-Designed Drug Carriers. Mol. Pharmaceut.10(1):187-198.
Yang Y., Bhatti A., Ke D., Gonzalez-Juarrero M., Lenaerts A., Kremer L., Guerardel Y., Zhang P. and Ojhaa A. K.(2013) Exposure to a cutinase-like serine esterase triggers rapid lysis of multiple mycobacterial species. J. Biol. Chem. 288(1):382-392.
Zhang P.*, Meng X. and Zhao G. (2013) Tubular Crystals and Helical Arrays: Structural Determination of HIV-1 Capsid Assemblies Using Iterative Helical Real-Space Reconstruction. Methods Mol Biol 955: 381-399.

Yang H., Ji X., Zhao G., Ning J., Zhao Q., Aiken C., Gronenborn A. M., Zhang P. and Xiong Y. (2012) Structural Insight into HIV-1 Capsid Recognition by Rhesus TRIM5α. Proc Natl Acad Sci  USA 109(45): 18372-18377.
Wang K., Strunk K., Zhao G., Gray J. L. and Zhang P.* (2012) 3D structure determination of native mammalian cells using cryo-FIB and cryo-electron tomography. J Struct Biol 180(2): 318-326.
Meng X., Zhao G., Yufenyuy E., Ke D., Ning J., DeLucia M., Ahn J., Gronenborn A.M., Aiken C.* and Zhang P.* (2012) Protease Cleavage Leads to Formation of Mature Trimer Interface in HIV-1 Capsid. PLoS Pathog 8(8): e1002886.
Strunk K., Wang K., Ke D., Gray J. L. and Zhang P.* (2012) Thinning of large mammalian cells for cryo-TEM characterization by cryo-FIB milling. J. Microscopy 247(3):220-227.

Jun S., Ke D., Debiec K., Zhao G., Meng X., Ambrose Z., Gibson G. A., Watkins S. C. and Zhang P.* (2011) Direct Visualization of HIV-1 with Correlative Live-Cell Microscopy and Cryo-Electron Tomography. Structure 19(11):1573-1581.
Zhao G., Ke D., Vu T., Ahn J., Shah V. B., Yang R., Aiken C., Charlton L. M., Gronenborn A. M. and Zhang P.* (2011) Rhesus TRIM5α Disrupts the HIV-1 Capsid at the InterHexamer Interfaces.  PLoS Pathog 7(3):e1002009.
Meng X., Zhao G. and Zhang P.* (2011) Structure of HIV-1 Capsid Assemblies by Cryo-electron Microscopy and Iterative Helical Real-space Reconstruction. J Vis Exp (54), e3041, DOI: 10.3791/3041
Ahn J., Novince Z., Concel J., Byeon C., Makhov A. M., Byeon I. L., Zhang P. and Gronenborn A. M. (2011) The Cullin-RING E3 ubiquitin ligase CRL4-DCAF1 complex dimerizes via a short helical region in DCAF1. Biochemistry 50(8): 1359-1367.
Morin-Leisk J., Saini S.G., Makhov A., Meng X., Zhang P. and Lee T. H. (2011) An intra-molecular salt bridge drives the soluble domain of GTP-bound atlastin into the 'post-fusion' conformation. J. Cell Biol. 195(4):605-615
Du S., Betts L., Yang R., Shi H., Concel J., Ahn J., Aiken C., Zhang P., Yeh J. I. (2011) Structure of the HIV-1 Full-Length Capsid in a Conformationally-Trapped Unassembled State Induced by Small-Molecule Binding. J. Mol. Biol. 406(3):371-386.
Hwang L., Zhao G., Zhang P. and Rosi, N.L. (2011) Size-controlled Peptide-directed synthesis of hollow spherical gold nanoparticle superstructures. Small 7(14):1939-1942.

Song C., Zhao G., Zhang P. and Rosi N.L. (2010) Expeditious Synthesis and Assembly of Spherical Gold Nanoparticle Superstructures. J. Am. Chem. Soc. 132(40):14033-14035.
Byeon In-ja L., Meng X, Jung J., G. Zhao, Yang R., Shi J., Ahn J., Concel J., Aiken C., Zhang P.* and Gronenborn A. M.* (2009) Structural Convergence between CryoEM and NMR Reveals Novel Intersubunit Interactions Critical for HIV-1 Capsid Assembly and Function. Cell 139: 780-790.
Zhang P.* (2009) Electron Tomography.  McGraw-Hill Encyclopedia of Science and Technology, 11th edition.
Chen C., Zhang P., & Rosi N.L. (2008) A New Peptide-Based Method for the Design and Synthesis of Nanoparticle Superstructures:  Construction of Highly-Ordered Gold Nanoparticle Double-Helices. J. Am. Chem. Soc. 130(41):13555-13557.
Khursigara C.M., Wu X., Zhang P.*, Lefman J. and Subramaniam S. (2008) Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors. Proc Natl Acad Sci USA 105(43):16555-16560.
Zhang P.*, Khursigara C.M., Hartnell L.M., Subramaniam S. (2007) Direct visualization of E.coli chemotaxis receptor arrays using cryo-electron microscopy. Proc Natl Acad Sci USA 104(10):3777-3781
Zhang P.*, Weis R. M., Peters P. J., Subramaniam S. (2007) Electron tomography of bacterial chemotaxis receptor assemblie. Methods Cell Biol. 79:373-384.

Prior to 2006
Zhang P.*, Juliani J., Lefman J., Land W., Smith S., Lee S., Leapman R., Kessel M., Rouault T., Subramaniam S. (2005) Electron tomography of degenerating neurons in mice with abnormal regulation of iron metabolism.  J. Struct. Biol.  150(2):144-153
Lefman J, Zhang P.*, Hirai T., Weis R. M., Juliani J., Bliss D., Kessel M., Bos E., Peters P. J., Subramaniam S. (2004) Three-Dimensional Electron Microscopic Imaging of Membrane Invaginations in Escherichia coli Overproducing the Chemotaxis Receptor Tsr. J. Bacteriol.  186(15):5052-5061. 
Zhang P.*, Bos E., Heymann J., Helmut Peters P., Kessel M., Subramaniam S. (2004) Direct visualization of receptor arrays in frozen-hydrated cells and sections from bacteria overproducing the chemotaxis receptor Tsr.  J. Microscopy  216(1):76-83.
Chen Y., Zhang P., Egelman E. H., Hinshaw J. (2004) The stalk region of dynamin drives the constriction of dynamin tubes.  Nature Struct. Mol. Biol. 11(6):574-575
Borgnia M. J., Shi D., Zhang P., Subramaniam S., Milne J. L. S. (2004) Visualization of &alpha-helical features in a density map constructed using 9 molecular images of the 1.8 MDa icosahedral core of pyruvate dehydrogenase. J. Struct. Biol. 147(2):136-145.
Shen W., Zhang P., German D., Rouault T., Subramaniam S. (2004) A template-propagation method for segmentation of filamentous structures in electron tomograms. IEEE Int. Symp. Biomed. Imaging 1:1-4.
Subramaniam, S., Zhang, P., Lefman, J., Juliani, J., Kessel, M. (2003) Electron tomography: A powerful tool for three-dimensional cellular microscopy. ASM News 60:240-245.
Zhang P.*, Borgnia M. J., Mooney P., Shi D., Pan M., O'Herron P., Mao A., Brogan D., L. S. Milne J. L. S., Subramaniam S. (2003) Automated image acquisition and processing using a new generation of 4K x 4K CCD cameras for cryo electron microscopic studies of macromolecular assemblies. J. Struct. Biol. 143(2):135-144.
Zhang P.* and Hinshaw J. E. (2001) Three-dimensional reconstruction of dynamin in the constricted state. Nat Cell Biol. 3:922-926.
Zhang P.*, Beatty A., Milne J. L. S., Subramaniam S. (2001). Automated data collection with a Tecnai 12 electron microscope: applications for molecular imaging by cryo-microscopy. J. Struct. Biol. 135:251-261.
Young H. S., Xu C., Zhang P., Stokes D. L. (2001) Locating the thapsigargin binding site on Ca(2+)-ATPase by cryoelectron microscopy. J. Mol. Biol. 308(2): 231-240.
Stokes D. L., Auer M., Zhang P., Kuhlbrandt W. (1999) Comparison of H+-ATPase and Ca2+-ATPase suggests that a large conformational change initiates P-type ion pump reaction cycles. Curr. Biol. 9(13):672-679.
Zhang P.*, Toyoshima C., Yonekura K., Green M. N., Stokes D. L. (1998) Structure of the calcium pump from sarcoplasmic reticulum at 8Å resolution. Nature 392:835-839.
Stokes D. L., Zhang P., Toyoshima C., Yonekura K., Ogawa H., Lewis M. R., Shi D. (1998) Cryoelectron microscopy of the calcium pump from sarcoplasmic reticulum: two crystal forms reveal two different conformations. Acta Physiol Scand Suppl 643:35-43.
Luthin D. R., Lee K. S., Okonkwo D., Zhang P., and Linden J. (1995) Photoaffinity labeling with 2-[2-(4-azido-3-[125I]-iodophenyl) ethylamino]adenosine and autoradiography with 2-[2-(4-amino-3-[125I] iodophenyl) ethylamino] adenosine of A2a adenosine receptors in rat brain. J. Neurochemistry 65:2072-2079.
Zheng J. G., Li Q., Zhang P., Feng D. (1992) A TEM study of one-dimensional incommensurate modulation on (001) plane of single crystal Bi2Sr2CaCu2Oy. Supercon. Sci. Technol. 5:472-475.
Zheng J. G., Li Q., Zhang P., Wang L., Wei M., Feng D. (1991) HREM studies on stacking faults in YBa2Cu3O7-y. Progress in Natural Science 1(4):323-327.