Advances made toward the automation of molecular microscopy sample preparation, data collection, and image processing has shifted this method from one suited for isolated observations to a high-throughput, tightly controlled technology that is applicable to large-scale, statistically relevant biotechnology and pharmaceutical applications.  At NanoImaging Services, we are proud of a scientific team that played a pivotal role in this transformation.

Schneemann A, Sung JJ, Speir JA, Mulligan SK. 2016. Structural Characterization of Monoclonal Antibody Therapeutics by Transmission Electron Microscopy and 2D Classification Analysis. Microscopy and Microanalysis 22(S3):1082-1083.

Fox CB, Orr MT, Van Hoeven N, Parker SC, Mikasa TJ, Phan T, Beebe EA, Nana GI, Joshi SW, Tomai MA, Elvecrog J, Fouts TR, Reed SG. 2016. Adsorption of a synthetic TLR7/8 ligand to aluminum oxyhydroxide for enhanced vaccine adjuvant activity: A formulation approach. J Control Release doi:10.1016/j.jconrel.2016.11.011.

Ali SM, Sheikh S, Ahmad A, Ahmad MU, Chen P, Paithankar M, Choudhury K, Makadia RD, Kumar A, Velavan K, Satheesh CT, Singh JK, Mamillapalli G, Saptarishi D, Kale P, Patel R, Barkate HV and Ahmad I 2016. Bioequivalence Study of Pegylated Doxorubicin Hydrochloride Liposome (PEGADRIA) and DOXIL® in Ovarian Cancer Patients: Physicochemical Characterization and Pre-clinical Studies. J Nanomed Nanotechnol doi:10.4172/2157-7439.1000361.

Flynn J.A., Durr E., Swoyer R., Cejas P.J., Horton M.S., Galli J.D., Cosmi S.A., Espeseth A.S., Bett A.J., Zhang L. 2016. Stability Characterization of a Vaccine Antigen Based on the Respiratory Syncytial Virus Fusion Glycoprotein. PLoS One. doi:10.1371/journal.pone.0164789.

Sun J., Remmele R.L. Jr, Sanyal G. 2016. Analytical Characterization of an Oil-in-Water Adjuvant Emulsion. AAPS PharmSciTech. doi:10.1208/s12249-016-0626-8.

Schneider-Ohrum K., Cayatte C., Liu Y., Wang Z., Irrinki A., Cataniag F., Nguyen N., Lambert S., Liu H., Aslam S., Duke G., McCarthy M.P., McCormick L. 2016. Production of cytomegalovirus dense bodies by scalable bioprocess methods maintains immunogenicity and improves neutralizing antibody titers. J Virol. doi:10.1128/JVI.00463-16.

Kranz L.M., Diken M., Haas H., Kreiter S., Loquai C., Reuter K.C., Meng M., Fritz D., Vascotto F., Hefesha H., Grunwitz C., Vormehr M., Hüsemann Y., Selmi A., Kuhn A.N., Buck J., Derhovanessian E., Rae R., Attig S., Diekmann J., Jabulowsky R.A., Heesch S., Hassel J., Langguth P., Grabbe S., Huber C., Türeci Ö., Sahin U. 2016. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature. doi:10.1038/nature18300.

Vlasak J., Hoang V.M., Christanti S., Peluso R., Li F., Culp T.D. 2016. Use of flow cytometry for characterization of human cytomegalovirus vaccine particles. Vaccine. 34, 2321-8.

Sung J.J., Pardeshi N.N., Mulder A.M., Mulligan S.K., Quispe J., On K., Carragher B., Potter C.S., Carpenter J.F., Schneemann A. 2015. Transmission electron microscopy as an orthogonal method to characterize protein aggregates. J Pharm Sci. 104, 750-9.

Work T.M., Dagenais J., Breeden R., Schneemann A., Sung J., Hew B., Balazs G.H., Berestecky J.M. 2015. Green Turtles (Chelonia mydas) Have Novel Asymmetrical Antibodies. J Immunol. 195, 5452-60.

Krarup A., Truan D., Furmanova-Hollenstein P., Bogaert L., Bouchier P., Bisschop I.J., Widjojoatmodjo M.N., Zahn R., Schuitemaker H., McLellan J.S., Langedijk J.P. 2015. A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism. Nat Commun. 6, 8143.

Carragher B., Schneemann A., Sung J.J., Mulligan S.K., Speir J.A., On K., Potter C.S. 2015. Electron Microscopy as an Emerging Analytical Tool for Characterizing Biopharmaceuticals. Microscopy and Microanalysis 21:S3, 65-66.

Loughney J.W., Rustandi R.R., Wang D., Troutman M.C., Dick L.W. Jr, Li G., Liu Z., Li F., Freed D.C., Price C.E., Hoang V.M., Culp T.D., DePhillips P.A., Fu T.M., Ha S. 2015. Soluble Human Cytomegalovirus gH/gL/pUL128-131 Pentameric Complex, but Not gH/gL, Inhibits Viral Entry to Epithelial Cells and Presents Dominant Native Neutralizing Epitopes. J Biol Chem. 290, 15985-95.

Sitrin R.D., Zhao Q., Potter C.S., Carragher B., Washabaugh M.W. 2014. Recombinant Virus-like Particle Protein Vaccines. Vaccine Analysis: Strategies, Principles, and Control 81-112.

Dong Y., Love K.T., Dorkin J.R., Sirirungruang S., Zhang Y., Chen D., Bogorad R.L., Yin H., Chen Y., Vegas A.J., Alabi C.A., Sahay G., Olejnik K.T., Wang W., Schroeder A., Lytton-Jean A.K., Siegwart D.J., Akinc A., Barnes C., Barros S.A., Carioto M., Fitzgerald K., Hettinger J., Kumar V., Novobrantseva T.I., Qin J., Querbes W., Koteliansky V., Langer R., Anderson D.G. 2014. Lipopeptide nanoparticles for potent and selective siRNA delivery in rodents and nonhuman primates. Proc Natl Acad Sci U S A. 111, 3955-60.

Francis S.M., Taylor C.A., Tang T., Liu Z., Zheng Q., Dondero R., Thompson J.E. 2014. Lipopeptide nanoparticles for potent and selective siRNA delivery in rodents and nonhuman primates. Mol Ther. 22, 1643-1652.

Wagner J.M., Pajerowski J.D., Daniels C.L., McHugh P.M., Flynn J.A., Balliet J.W., Casimiro D.R., Subramanian S. 2014. Enhanced production of Chikungunya virus-like particles using a high-pH adapted spodoptera frugiperda insect cell line. PLoS One. 9, e94401.

Ma H., Galvin T.A., Glasner D.R., Shaheduzzaman S., Khan A.S. 2014. Identification of a novel rhabdovirus in Spodoptera frugiperda cell lines. J Virol. 88, 6576-85.

Zhao Q., Potter C.S., Carragher B., Lander G., Sworen J., Towne V., Abraham D., Duncan P., Washabaugh M.W., Sitrin R.D. 2014. Characterization of virus-like particles in GARDASIL® by cryo transmission electron microscopy. Hum Vaccin Immunother. 10, 734-9.

Fox C.B., Mulligan S.K., Sung J., Dowling Q.M., Fung H.W., Vedvick T.S., Coler R.N. 2014. Cryogenic transmission electron microscopy of recombinant tuberculosis vaccine antigen with anionic liposomes reveals formation of flattened liposomes. Int J Nanomedicine. 11, 1367-77.

Linke T., Aspelund M.T., Thompson C., Xi G., Fulton A., Wendeler M., Pabst T.M., Wang X., Wang W.K., Ram K., Hunter A.K. 2014. Development and scale-up of a commercial fed batch refolding process for an anti-CD22 two chain immunotoxin. Biotechnol Prog. 30, 1380-9.

Agadjanian, H., Chu, D., Hwang, J.Y., Wachsmann-Hogiu, S., Rentsendorj, A., Song, L., Valluripalli, V., Lubow, J., Ma, J., Sharifi, B., et al. (2012). Chemotherapy targeting by DNA capture in viral protein particles. Nanomedicine (Lond) 7, 335-352. 

Carragher, B., D. Fellmann, F. Guerra, R. Milligan, F. Mouche, J. Pulokas, J. Quispe, C. Suloway, Y. Zhu, and C.S. Potter. 2004. Rapid routine structure determination of macromolecular assemblies using electron microscopy:  current progress and remaining challenges. J. Synchrotron Rad. 11:83-85.

Carragher, B. and C.S. Potter. 2008. Advanced Transmission Electron Microscopy in Drug Development. Preclinical World. 104-107.

Carragher, B., C.S. Potter, and F.J. Sigworth. 2007. Software tools for macromolecular microscopy. J Struct Biol. 157:1-2.

Correia, I., J. Sung, R. Burton, C. G. Jakob, B. Carragher, T. Ghayur & C. Radziejewski. 2013. The structure of dual-variable-domain immunoglobulin molecules alone and bound to antigen. MAbs, 5.

Crawford R, Dogdas B, Keough E, Haas RM, Wepukhulu W, Krotzer S, Burke PA, Sepp-Lorenzino L, Bagchi A, Howell BJ. Analysis of lipid nanoparticles by Cryo-EM for characterizing siRNA delivery vehicles.

Fox, C.B. (2012). Characterization of TLR4 agonist effects on alhydrogel(R) sedimentation: A novel application of laser scattering optical profiling. Journal of Pharmaceutical Sciences.  101, 4357-4364.

Fox, C. B., V. L. Barnes, T. Evers, J. D. Chesko, T. S. Vedvick, R. N. Coler, S. G. Reed & S. L. Baldwin. 2012. Adjuvanted pandemic influenza vaccine: variation of emulsion components affects stability, antigen structure, and vaccine efficacy. Influenza Other Respi Viruses.

Hahn TJ., Courbrom D., Hamer M., Masoud M., Wong J., Taylor K., Hatch J., Sowers M., Shane E., Nathan M., Jiang H., Wei Z., Higgins J., Roh K., Burd J., Chinchilla-Olszar D., Malou-Williams M., Baskind D. P., Smith G. E. Rapid Manufacture and Release of a GMP Batch of Avian Influenza A(H7N9) Virus-Like Particle Vaccine Made Using Recombinant Baculovirus-Sf9 Insect Cell Culture Technology. BioProcess J, 2013; 12(2): 4-17.

Kale, M., Suruse, P., Singh, R., Malhotra, G., and Raut, P. (2012). Effect of Size Reduction Techniques on Doxorubicin Hydrochloride Loaded Liposomes. International Journal of Biological & Pharmaceutical Research 3, 308-316.

Lander, G.C., A. Evilevitch, M. Jeembaeva, C.S. Potter, B. Carragher, and J.E. Johnson. 2008. Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM. Structure. 16:1399-406

Lander, G.C., R. Khayat, R. Li, P.E. Prevelige, C.S. Potter, B. Carragher, and J.E. Johnson. 2009. The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure. 17:789-99.

Lander, G.C., S.M. Stagg, N.R. Voss, A. Cheng, D. Fellmann, J. Pulokas, C. Yoshioka, C. Irving, A. Mulder, P.W. Lau, D. Lyumkis, C.S. Potter, and B. Carragher. 2009. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J Struct Biol. 166:95-102.

Lander, G.C., L. Tang, S.R. Casjens, E.B. Gilcrease, P. Prevelige, A. Poliakov, C.S. Potter, B. Carragher, and J.E. Johnson. 2006. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science. 312:1791-5.

Lau, P.W., C.S. Potter, B. Carragher, and I.J. MacRae. 2009. Structure of the human Dicer-TRBP complex by electron microscopy. Structure. 17:1326-32.

Lyumkis, D., A. Moeller, A. Cheng, A. Herold, E. Hou, C. Irving, E.L. Jacovetty, P.-W. Lau, A.M. Mulder, J. Pulokas, J.D. Quispe, N.R. Voss, C.S. Potter, and B. Carragher. 2010. Automation in Single-Particle Electron Microscopy: Connecting the Pieces. Methods in Enzymology 483: 291-338. 
Mallick, S.P., B. Carragher, C.S. Potter, and D.J. Kriegman. 2005. ACE: automated CTF estimation. Ultramicroscopy. 104:8-29.

Miranda, M., Sung, J., Mulligan, S., On, K., Quispe, J. In Vitro Characterization of Liposomal Encapsulated Doxorubicin Using CryoTEM. CRS Newsletter, Volume 30, Number 3, 2013. 

Mulder, AM, Carragher B, Towne V, Meng T, Wang Y, Dieter L, Potter CS, Washabaugh MW, Sitrin RD, Zhao Q. Toolbox for Non-Intrusive Structual and Functional Analysis of Recombinant VLP Based Vaccines: A Case Study with Hepatitis B Vaccine. PLoS ONE. 2012;7(4):e33235

Mulder, A.M., A. Glavis-Bloom, C.A. Moores, M. Wagenbach, B. Carragher, L. Wordeman, and R.A. Milligan. 2009. A new model for binding of kinesin 13 to curved microtubule protofilaments. J Cell Biol. 185:51-7.

Mulder, A.M., C. Yoshioka, A. H. Beck, A.E. Bunner, R.A. Milligan, C.S. Potter, B. Carragher, and J.R. Williamson. 2010. Visualizing Ribosome Biogenesis:  Parallel Assembly Pathways for the 30S Subunit. Science. 330:673-7.
O'Keefe, M.A., J. Turner, J. Musante, C. Hetherington, A.G. Cullis, B. Carragher, R. Jenkins, J. Milgrim, R. Milligan, C.S. Potter, L. Allard, D. Blom, L. Degenhardt, and W. Sides. 2004. Laboratory design for high-performance electron microscopy. Microscopy Today:8-14

Potter, C.S., J. Pulokas, P. Smith, C. Suloway, and B. Carragher. 2004. Robotic grid loading system for a transmission electron microscope. J Struct Biol. 146:431-40..

Quispe, J., J. Damiano, S.E. Mick, D.P. Nackashi, D. Fellmann, T.G. Ajero, B. Carragher, and C.S. Potter. 2007. An improved holey carbon film for cryo-electron microscopy. Microsc Microanal. 13:365-71.

Richter A, Olbrich C, Krause M, Kissel T. Solubilization of sagopilone, a poorly water-soluble anticancer drug, using polymeric micelles for parenteral delivery.

Ripple, D.C., and Dimitrova, M.N. (2012).  Protein particles: What we know and what we do not know. Journal of Pharmaceutical Sciences 101, 3568-3579. 

Schroeder, A., Goldberg, M.S., Kastrup, C., Wang, Y., Jiang, S., Joseph, B.J., Levins, C.G., Kannan, S.T., Langer, R., and Anderson, D.G. (2012). Remotely activated protein-producing nanoparticles. Nano letters 12, 2685-2689.

Smith, R., and B. Carragher. 2008. Software tools for molecular microscopy. J Struct Biol. 163:224-8.

Stagg, S.M., C. Gurkan, D.M. Fowler, P. LaPointe, T.R. Foss, C.S. Potter, B. Carragher, and W.E. Balch. 2006. Structure of the Sec13/31 COPII coat cage. Nature. 439:234-8.

Stagg, S.M., G.C. Lander, J. Pulokas, D. Fellmann, A. Cheng, J.D. Quispe, S.P. Mallick, R.M. Avila, B. Carragher, and C.S. Potter. 2006. Automated cryoEM data acquisition and analysis of 284742 particles of GroEL. J Struct Biol. 155:470-81.

Stagg, S.M., G.C. Lander, J. Quispe, N.R. Voss, A. Cheng, H. Bradlow, S. Bradlow, B. Carragher, and C.S. Potter. 2008. A test-bed for optimizing high-resolution single particle reconstructions. J Struct Biol. 163:29-39.

Stagg, S.M., P. LaPointe, A. Razvi, C. Gurkan, C.S. Potter, B. Carragher, and W.E. Balch. 2008. Structural basis for cargo regulation of COPII coat assembly. Cell. 134:474-84.

Strable, E., D.E. Prasuhn, Jr., A.K. Udit, S. Brown, A.J. Link, J.T. Ngo, G. Lander, J. Quispe, C.S. Potter, B. Carragher, D.A. Tirrell, and M.G. Finn. 2008. Unnatural amino acid incorporation into virus-like particles. Bioconjug Chem. 19:866-75.

Suloway, C., J. Pulokas, D. Fellmann, A. Cheng, F. Guerra, J. Quispe, S. Stagg, C.S. Potter, and B. Carragher. 2005. Automated molecular microscopy: the new Leginon system. J Struct Biol. 151:41-60.

Suloway, C., J. Shi, A. Cheng, J. Pulokas, B. Carragher, C.S. Potter, S.Q. Zheng, D.A. Agard, and G.J. Jensen. 2009. Fully automated, sequential tilt-series acquisition with Leginon. J Struct Biol. 167:11-8.

Tong, J., M. M. Briggs & T. J. McIntosh. 2012. Water permeability of aquaporin-4 channel depends on bilayer composition, thickness, and elasticity. Biophys J, 103, 1899-908.

Voss, N.R., D. Lyumkis, A. Cheng, P.W. Lau, A. Mulder, G.C. Lander, E.J. Brignole, D. Fellmann, C. Irving, E.L. Jacovetty, A. Leung, J. Pulokas, J.D. Quispe, H. Winkler, C. Yoshioka, B. Carragher, and C.S. Potter. 2010. A toolbox for ab initio 3-D reconstructions in single-particle electron microscopy. J Struct Biol. 169:389-98.

Voss, N. R., C. S. Potter, R. Smith & B. Carragher. 2010. Software tools for molecular microscopy: an open-text Wikibook. Methods Enzymol, 482, 381-92.

Voss, N.R., C.K. Yoshioka, M. Radermacher, C.S. Potter, and B. Carragher. 2009. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J Struct Biol. 166:205-13.

Ward, A., S. Mulligan, B. Carragher, G. Chang, and R.A. Milligan. 2009. Nucleotide dependent packing differences in helical crystals of the ABC transporter MsbA. J Struct Biol. 165:169-75.

Yoshioka, C., B. Carragher, and C.S. Potter. 2010. Cryomesh: a new substrate for cryo-electron microscopy. Microsc Microanal. 16:43-53.

Yoshioka, C., J. Pulokas, D. Fellmann, C.S. Potter, R.A. Milligan, and B. Carragher. 2007. Automation of random conical tilt and orthogonal tilt data collection using feature-based correlation. J Struct Biol. 159:335-46.

Zhao, Q., Modis, Y., High, K., Towne, V., Meng, Y., Wang, Y., Alexandroff, J., Brown, M., Carragher, B., Potter, C.S., et al. (2012). Disassembly and reassembly of human papillomavirus virus-like particles produces more virion-like antibody reactivity. Virology journal 9, 52.

Zhu, Y., B. Carragher, R.M. Glaeser, D. Fellmann, C. Bajaj, M. Bern, F. Mouche, F. de Haas, R.J. Hall, D.J. Kriegman, S.J. Ludtke, S.P. Mallick, P.A. Penczek, A.M. Roseman, F.J. Sigworth, N. Volkmann, and C.S. Potter. 2004. Automatic particle selection: results of a comparative study. J Struct Biol. 145:3-14.

Zidovska, A., H.M. Evans, K.K. Ewert, J. Quispe, B. Carragher, C.S. Potter, and C.R. Safinya. 2009. Liquid crystalline phases of dendritic lipid-DNA self-assemblies: lamellar, hexagonal, and DNA bundles. J Phys Chem B. 113:3694-703.

Zidovska, A., K.K. Ewert, J. Quispe, B. Carragher, C.S. Potter, and C.R. Safinya. 2009. Block liposomes vesicles of charged lipids with distinctly shaped nanoscale sphere-, pear-, tube-, or rod-segments. Methods Enzymol. 465:111-28.

Zidovska, A., K.K. Ewert, J. Quispe, B. Carragher, C.S. Potter, and C.R. Safinya. 2009. The effect of salt and pH on block liposomes studied by cryogenic transmission electron microscopy. Biochim Biophys Acta. 1788:1869-76.

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