The Boulder Laboratory
For 3-D Electron Microscopy of Cells

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The Boulder Laboratory for 3D Electron Microscopy of Cells Department of MCD Biology
Campus Box 347
University of Colorado
Boulder, CO 80309


Link to A. Hoenger Publications


Briegel, A., Pilhofer, M., Gan, L., Mastronarde, D. N., McDowall, A. W., and Jensen, G. J. The challenge of determining handedness in electron tomography and the use of DNA origami gold nanoparticle helices as molecular standards. J. Struct. Biol. In Press.

Cope J, Rank KC, Gilbert SP, Rayment I, Hoenger A. (2013) Kar3Vik1 Uses a Minus-End Directed Powerstroke for Movement Along Microtubules. PLOS-one 8:e53792. PMCID: PMC3544905

Esparza JM, O'Toole E, Li L, Giddings TH Jr, Kozak B, Albee AJ, Dutcher SK. (2013) Katanin Localization Requires Triplet Microtubules in Chlamydomonas reinhardtii. PLoS One. 8:e53940. PMCID: PMC3540033

McIntosh JR, O'Toole E, Zhudenkov K, Morphew M, Schwartz C, Ataullakhanov FI, Grishchuk EL. (2013) Conserved and divergent features of kinetochores and spindle microtubule ends from five species. J Cell Biol. 200:459-74. PMCID: PMC3575531

Iconomidou VA, Leontis, A, Hoenger A, Hamodrakas SJ. (2013) Identification of a novel 'aggregation-prone' / 'amyloidogenic determinant' peptide in the sequence of the highly amyloidogenic human Calcitonin. FEBS-Letters, S0014-5793(13)00062-8. PMID: 23395606

Volkov, V.A., A.V. Zaytsev, N. Gudimchuk, P.M.Grissom, A,L. Gintsburg, F.I. Ataullakhanov, J.R. McIntosh, and E,L. Grishchuk (2013) “Long tethers provide high-force coupling of the Dam1 ring to shortening microtubules” PNAS 2013 : 1305821110v1-201305821. PMID: 23610433

Kamasaki, T., O'Toole, E., Kita, S., Osumi, M., Usukura, J., McIntosh, J.R., and G. Goshima (2013) Ultrastructural insights into intra-spindle microtubule nucleation in human somatic cells. JCB In press

2013 Submitted

Choy JS, O'Toole E, Schuster BM, Crisp MJ, Karpova TS, McNally JG, Winey M, Gardner MK, and Basrai MA. (2013) Genome-wide haploinsufficiency screen reveals a novel role for γ-TuSC in spindle organization and genome stability. Mol Biol Cell. Submitted

Gonzalez, MA, Cope, J, Rank, KC, Chen, JY, Tittmann, P, Rayment, I, Gilbert, SP, Hoenger, A. (2013) Common Mechanistic Themes for the Powerstroke of Kinesin-14 motors. J. Struct Biol. Submitted.

O'Toole E, and Dutcher SK. (2013) Site-specific basal body duplication helps establish cell geometry in Chlamydomonas. Mol. Biol Cell. Submitted.

Nazarova E, O'Toole E, Kaitna S, Francois P, Winey M and Vogel J. (2013) Distinct roles for anti-parallel microtubule pairing and overlap during early spindle assembly. Mol Biol Cell Submitted

Hepperla AJ, Willey PT, Schuster BM, Gerami-Nejad M, McClellan M, Coombes CE, Fox J, O’Toole E, Winey M, Odde DJ, and Gardner, MK. (2013) Regulation of Mitotic Spindle Architecture by Minus-end Directed Molecular Motors. Submitted


Bouchet-Marquis C, Pagratis M, Kirmse R, Hoenger A. (2012) Metallothionein as a clonable high-density marker for cryo-electron microscopy J Struct Biol. 177:119-27. PMID: 22068155

Erickson, K.D., Bouchet-Marquis, C., Heiser, K., Szomolanyi-Tsuda, E., Mishra, R., Lamothe, B., Hoenger, A., and Garcea, R.L. (2012) Nuclear Virus Factories in Polyomavirus-Infected Cells. PLOS Pathogens, (4):e1002630.

Grishchuk, E. L., J. R. McIntosh, M. Molodtsov, and F. I. Ataullakhanov (2012). Force generation by dynamic microtubule polymers. In Biophysics, vol. 7 (eds Y. E. Goldman and E. M. Ostap) Elsevier, on line publication.

Hoog JL, Bouchet-Marquis C, McIntosh JR, Hoenger A, Gull K. Cryo-electron tomography and 3-D analysis of the intact flagellum in Trypanosoma brucei. J Struct Biol. 2012 May;178(2):189-98. Epub 2012 Jan 25. PubMed PMID: 22285651; PubMed Central PMCID: PMC3355306.

Iconomidou VA, Pheida D, Hamodraka ES, Antony C, Hoenger A, Hamodrakas SJ. (2012) An amyloidogenic determinant in N-terminal pro-brain natriuretic peptide (NT-proBNP): Implications for cardiac amyloidoses. Biopolymers. Jul 25. doi: 10.1002/bip.21698.

Kirmse R, Otto H, Ludwig T. (2012) The extracellular matrix remodeled: Interdependency of matrix proteolysis, cell adhesion, and force sensing. Commun Integr Biol. 5:71-3. PMCID: PMC3291319

McIntosh JR. (2012) Motors or dynamics: what really moves chromosomes? Nat Cell Biol. 14:1234. PMID: 23196840

McIntosh JR, Molodtsov MI, Ataullakhanov FI. (2012) Biophysics of mitosis. Q Rev Biophys. 45(2):147-207. PMID: 22805482

O'Toole ET, Giddings TH Jr, Porter ME, Ostrowski LE. Computer-assisted image analysis of human cilia and Chlamydomonas flagella reveals both similarities and differences in axoneme structure. Cytoskeleton (Hoboken). 2012 Aug;69(8):577-90. doi: 10.1002/cm.21035. Epub 2012 May 22. PubMed PMID: 22573610; PubMed Central PMCID: PMC3423584.

O'Toole E, Greenan G, Lange KI, Srayko M, Müller-Reichert T. The role of γ-tubulin in centrosomal microtubule organization PLoS One. 2012;7(1):e29795. doi: 10.1371/journal.pone.0029795. Epub 2012 Jan 10. Erratum in: PLoS One. 2012;7(2). doi: 10.1371/annotation/c303c4e9-edae-4602-96b6-21c3796b89c9. PMID: 22253783

Patwardhan A, Carazo JM, Carragher B, Henderson R, Heymann JB, Hill E, Jensen GJ, Lagerstedt I, Lawson CL, Ludtke SJ, Mastronarde D, Moore WJ, Roseman A, Rosenthal P, Sorzano CO, Sanz-Garcia E, Scheres SH, Subramaniam S, Westbrook J, Winn M, Swedlow JR, Kleywegt GJ. (2012) Data management challenges in three-dimensional EM. Nat Struct Mol Biol. 19:1203-7. PMID: 23211764

Rank KC, Chen CJ, Cope J, Porche K, Hoenger A, Gilbert SP, Rayment I. (2012) Kar3Vik1, a member of the Kinesin-14 superfamily, shows a novel kinesin microtubule binding pattern. J Cell Biol. 197:957-70. PMID: 22734002

Schwartz CL, Heumann JM, Dawson SC, Hoenger A. (2012) A detailed, hierarchical study of Giardia lamblia's ventral disc reveals novel microtubule-associated protein complexes. PLoS One. 7:e43783. PMID: 22984443

Wu Y, Gu Y, Morphew MK, Yao J, Yeh FL, Dong M, Chapman ER. All three components of the neuronal SNARE complex contribute to secretory vesicle docking. J Cell Biol. 2012 Aug 6;198(3):323-30. PubMed PMID: 22869597; PubMed Central PMCID: PMC3413369.

Schwartz CL, Heumann JM, Dawson SC, Hoenger A. A Detailed, Hierarchical Study of Giardia lamblia's Ventral Disc Reveals Novel Microtubule-Associated Protein Complexes. PLoS One. 2012;7(9):e43783. Epub 2012 Sep 11. PubMed PMID: 22984443; PubMed Central PMCID: PMC3439489.


Anderson, J. R., Jones, B. W., Watt, C. B., Shaw, M. V., Yang, J.-H., DeMill, D., Lauritzen, J. S., Lin, Y., Rapp, K. D., Mastronarde, D., Koshevoy, P., Grimm, B., Tasdizen, T., Whitaker, R., and Marc, R. E.  (2011) Exploring the retinal connectome. Mol. Vis. 17:355-379.

Bouchet-Marquis C, Hoenger A. (2011) Cryo-electron tomography on vitrified sections: a critical analysis of benefits and limitations for structural cell biology. Micron. 42:152-62.

Cope BJ, Heumann J, Hoenger A. (2011) Cryo-electron tomography for structural characterization of macromolecular complexes. Curr Protoc Protein Sci. 2011 Aug;Chapter 17:Unit17.13.

Hagen KD, Hirakawa MP, House SA, Schwartz CL, Pham JK, Cipriano MJ, De La Torre MJ, Sek AC, Du G, Forsythe BM, Dawson SC. Novel structural components of the ventral disc and lateral crest in Giardia intestinalis. PLoS Negl Trop Dis. 2011 Dec;5(12):e1442. Epub 2011 Dec 20. PubMed PMID: 22206034; PubMed Central PMCID: PMC3243723.

Heumann JM, Hoenger A, Mastronarde DN. (2011) Clustering and variance maps for cryo-electron tomography using wedge-masked differences. J Struct Biol. 2011 Sep;175(3):288-99.

Hoenger A, Bouchet-Marquis C. (2011) Cellular tomography. Adv Protein Chem Struct Biol. 82:67-90.

Hoog, J.L., Bouchet-Marquis, C., McIntosh, J.R., Hoenger, A., and Gull, K. (2011). Cryo-Electron Tomography and 3-D Analysis of the Intact Flagellum in Trypanosoma brucei. J. Struct. Biol. In press.

Iconomidou VA, Cordopatis P, Hoenger A, Hamodrakas SJ. (2011) The silkmoth eggshell as a natural amyloid shield for the safe development of insect oocyte and embryo: Insights from studies of silkmoth chorion protein peptide-analogues of the B famil. Biopolymers. 96:723-33. PMID: 2252423

Kang, B.-H., Nielsen, E., Preuss, M., Mastronarde, D., Staehelin, L. A. (2011) Electron tomography of RabA4b and PI-4K-beta1 labeled trans-Golgi network compartments in Arabidopsis. Traffic 12:313-329.

Maurer SP, Bieling P, Cope J, Hoenger A, Surrey T. (2011) GTP{gamma}S microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc Natl Acad Sci U S A. 108:3988-93.

Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, Paradise S, O'Toole E, Ferguson S, Cremona O, De Camilli P. (2011) Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron. 72:587-601. PMID: 22099461

Pierson J, Vos M, McIntosh JR, Peters PJ. (2011) Perspectives on electron cryo-tomography of vitreous cryo-sections. J Electron Microsc (Tokyo). 2011;60 Suppl 1:S93-100. PMCID: PMC3156678

Raimondi A, Ferguson SM, Lou X, Armbruster M, Paradise S, Giovedi S, Messa M, Kono N, Takasaki J, Cappello V, O'Toole E, Ryan TA, De Camilli P. (2011) Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70: 1100- 14.

Schiel JA, Park K, Morphew MK, Reid E, Hoenger A, Prekeris R. (2011). Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci, 124:1411-24.

Ueda, H. Morphew, M.K., McIntosh, J.R., and Davis, M.M. (2011). CD4 T-cell synapses involve multiple distinct stages. PNAS, 108(41), 17099-17104.

West M, Zurek N, Hoenger A, Voeltz GK. (2011) A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol. 193:333-46.


Arthur CP, Dean C, Pagratis M, Chapman ER, Stowell MH. (2010) Loss of synaptotagmin IV results in a reduction in synaptic vesicles and a distortion of the Golgi structure in cultured hippocampal neurons. Neuroscience. 167(1):135-42. PMCID: PMC3102522

Briegel, A., Chen, S., Koster, A. J., Plitzko, J. M., Schwartz, C. L., and Jensen, G. J. (2010). Correlated light and electron cryo-microscopy. Methods in enzymology 481, 317-341.

Cope J, Gilbert S, Rayment I, Mastronarde D, Hoenger A. Cryo-electron tomography of microtubule-kinesin motor complexes. J Struct Biol. 2010 May;170(2):257-65. Epub 2009 Dec 16.

De Carlo S, Lin SC, Taatjes DJ, Hoenger A. (2010) Molecular basis of transcription initiation in Archaea. Transcription. 1:103-111.

Friedman, J. R., Webster, B. M., Mastronarde, D. N., Verhey, K. J., and Voeltz, G. K. (2010)  ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J. Cell Biol. 190:363-75.

Kirmse R, Bouchet-Marquis C, Page C, Hoenger A. (2010) Three-dimensional cryo-electron microscopy on intermediate filaments. Methods Cell Biol. 96:565-89.

Kirmse R, Qin Z, Weinert CM, Hoenger A, Buehler MJ, Kreplak L. (2010) Plasticity of intermediate filament subunits. PLoS One. 5:e12115.

Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, Gull K. (2010) Basal body movements orchestrate membrane organelle division and cell morphogenesis in Trypanosoma brucei. J Cell Sci. 123:2884-91.

Mathieson, E. M., Schwartz, C., and Neiman, A. M. (2010). Membrane assembly modulates the stability of the meiotic spindle-pole body. Journal of cell science 123, 2481-2490.

McDonald K, Schwarz H, Muller-Reichert T, Webb R, Buser C, Morphew M. (2010) "Tips and tricks" for high-pressure freezing of model systems. Methods Cell Biol.;96:671-93.

Muller-Reichert T, Greenan G, O'Toole E, Srayko M. The elegans of spindle assembly. Cell Mol Life Sci. 2010 Jul;67(13):2195-213. Epub 2010 Mar 26. Review.

O'Toole, ET. (2010) Chlamydomonas: Cryoprepation methods for the 3-D analysis of cellular organelles. Meth. Cell Biol. 96: 71-91.

Scassellati C, Albi E, Cmarko D, Tiberi C, Cmarkova J, Bouchet-Marquis C, Verschure PJ, Driel R, Magni MV, Fakan S. (2010) Intranuclear sphingomyelin is associated with transcriptionally active chromatin and plays a role in nuclear integrity. Biol Cell. 102:361-75.


Anderson JR, Jones BW, Yang JH, Shaw MV, Watt CB, Koshevoy P, Spaltenstein J, Jurrus E, U V K, Whitaker RT, Mastronarde D, Tasdizen T, Marc RE. A computational framework for ultrastructural mapping of neural circuitry. PLoS Biol. 2009 Mar;7(3):e1000074.

Bouchet-Marquis C, Fakan S. (2009) Cryoelectron microscopy of vitreous sections: a step further towards the native state. Methods Mol Biol. 464:425-39.

Bower, R., VanderWall, K. O'Toole, E., Fox, L., Perrone, C., Mueller, J., Wirschell, M., Kamiya, R., Goldstein, S., Sale, W.S., and Porter, M.E. (2009) IC138 defines a sub-domain at the base of the I1 dynein that regulates microtubule sliding and flagellar motility. J. Cell Biol. 20:3055-4063.

Gadelha C, Rothery S, Morphew M, McIntosh JR, Severs NJ, Gull K. Membrane domains and flagellar pocket boundaries are influenced by the cytoskeleton in African trypanosomes. Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17425-30. Epub 2009 Oct 1.

Hoenger A, McIntosh JR. Probing the macromolecular organization of cells by electron tomography. Curr Opin Cell Biol. 2009 Feb;21(1):89-96. Review.

Iribe G, Ward CW, Camelliti P, Bollensdorff C, Mason F, Burton RA, Garny A, Morphew MK, Hoenger A, Lederer WJ, Kohl P. Axial stretch of rat single ventricular cardiomyocytes causes an acute and transient increase in Ca2+ spark rate. Circ Res. 2009 Mar 27;104(6):787-95.

Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, Gull K. Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J Cell Sci. 2009 Apr 15;122(Pt 8):1081-90. Epub 2009 Mar 19.

Lu L, Ladinsky MS, Kirchhausen T. (2009) Cisternal organization of the endoplasmic reticulum during mitosis. Mol Biol Cell. 20:3471-80.

McIntosh JR, Morphew MK, Grissom PM, Gilbert SP, Hoenger A. Lattice structure of cytoplasmic microtubules in a cultured Mammalian cell. J Mol Biol. 2009 Nov 27;394(2):177-82.

O'Toole E, Muller-Reichert T. Electron tomography of microtubule end-morphologies in C. elegans embryos. Methods Mol Biol. 2009;545:135-44.

Palsdottir H, Remis JP, Schaudinn C, O'Toole E, Lux R, Shi W, McDonald KL, Costerton JW, Auer M. Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography. J Bacteriol. 2009 Apr;191(7):2077-82.

Xiong Q, Morphew MK, Schwartz CL, Hoenger AH, Mastronarde DN. CTF determination and correction for low dose tomographic tilt series. J Struct Biol. 2009 Dec;168(3):378-87. Epub 2009 Sep 2.


Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH Jr, O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI. Beta-Catenin is a Nek2 substrate involved in centrosome separation.

Blackler AR, Speers AE, Ladinsky MS, Wu CC. A shotgun proteomic method for the identification of membrane-embedded proteins and peptides.

Bouchet-Marquis C, Starkuviene V, Grabenbauer M. (2008) Golgi apparatus studied in vitreous sections. J Microsc. 230:308-16.

De Carlo S, Boisset N, Hoenger A. High-resolution single-particle 3D analysis on GroEL prepared by cryo-negative staining.

Gardner MK, Bouck DC, Paliulis LV, Meehl JB, O'Toole ET, Haase J, Soubry A, Joglekar AP, Winey M, Salmon ED, Bloom K, Odde DJ. Chromosome congression by Kinesin-5 motor-mediated disassembly of longer kinetochore microtubules.

Gardner MK, Haase J, Mythreye K, Molk JN, Anderson M, Joglekar AP, O'Toole ET, Winey M, Salmon ED, Odde DJ, Bloom K. The microtubule-based motor Kar3 and plus end-binding protein Bim1 provide structural support for the anaphase spindle.

Hayashi, M., Raimondi, A., O'Toole, E., Paradise, S., Collesi, C., Cremona, O., Ferguson, S., and De Camilli, P. (2008) Cell and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling revealed by studies of dynamin 1-null neurons. PNAS 105:2175-2180.

He W, Kivork C, Machinani S, Morphew MK, Gail AM, Tesar DB, Tiangco NE, McIntosh JR, Bjorkman PJ. (2007) A freeze substitution fixation-based gold enlarging technique for EM studies of endocytosed Nanogold-labeled molecules. J Struct Biol. 160:103-13.

He W, Ladinsky MS, Huey-Tubman KE, Jensen GJ, McIntosh JR, Björkman PJ. FcRn-mediated antibody transport across epithelial cells revealed by electron tomography.

Hoenger A, Gross H. Structural investigations into microtubule-MAP complexes.

Marx A, Muller J, Mandelkow EM, Woehlke G, Bouchet-Marquis C, Hoenger A, Mandelkow E. X-ray structure and microtubule interaction of the motor domain of Neurospora crassa NcKin3, a kinesin with unusual processivity.

Mastronarde DN. Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package.

McIntosh JR, Grishchuk EL, Morphew MK, Efremov AK, Zhudenkov K, Volkov VA, Cheeseman IM, Desai A, Mastronarde DN, Ataullakhanov FI. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion.

Morphew M, He W, Bjorkman PJ, McIntosh JR. Silver enhancement of Nanogold particles during freeze substitution for electron microscopy.

Muller-Reichert, T. Jana Mantler, Srayko, M., and O'Toole, E.T. (2008) Electron Microscopy of the early C. elegans embryo. J. Microscopy 230: 297-307.

Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, Hagiwara H, Zhang Q, Leblond G, O'Toole E, Hara C, Mizuno H, Kawano H, Fliegauf M, Yagi T, Koshida S, Miyawaki A, Zentgraf H, Seithe H, Reinhardt R, Watanabe Y, Kamiya R, Mitchell DR, Takeda H. (2008) KTu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 456: 611-616.

Reichl EM, Ren Y, Morphew MK, Delannoy M, Effler JC, Girard KD, Divi S, Iglesias PA, Kuo SC, Robinson DN. Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics.


Link to A. Hoenger 2007 Publications

Bostina, M., Bubeck, D., Schwartz, C., Nicastro, D., Filman, D. J., and Hogle, J. M. (2007). Single particle cryoelectron tomography characterization of the structure and structural variability of poliovirus-receptor-membrane complex at 30 A resolution. Journal of structural biology 160, 200-210.

Ferguson, S.M., Brasnjo, G., Hayashi, M., Wolfel, M., Collesi, C., Giovedi, S., Raimondi, S., Gong, L.W., Ariel, P., Paradise, S., O'Toole, E., Flavell, R., Cremona, O., Miesenbock, G., Ryan, T.A., and De Camilli, P. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-4.

Goldie, K.N., Wedig, T., Mitra, A., Aebi, U., Herrmann, H., and Hoenger, A. (2007) Dissecting the 3-D Structure of Vimentin Intermediate Filaments by Cryo-Electron Tomography. J. Struct. Biol. 158:378-85.

Hoog, J.L., C. Schwartz, A.T. Noon, E.T. O'Toole, D.N. Mastronarde, J.R. McIntosh and C. Antony (2007). Organization of interphase microtubules in fission yeast analyzed by electron tomography. Developmental Cell 12: 349-361.

Ladinsky, M.S. and K.E. Howell (2007). Electron tomography of immunolabeled cryosections. Methods in Cell Biology 79: 543-548.

McDonald KL, Morphew M, Verkade P, Müller-Reichert T. (2007) Recent advances in high-pressure freezing: equipment- and specimen-loading methods. Methods Mol Biol. 369:143-73.

Mogelsvang, S., M.S. Ladinsky, and K.E. Howell (2007). Fatty acid-induced lipoapoptosis, a role for Golgi sphingomyelin and glycosphingolipids. Submitted

Morphew, M.K. (2007). 3D immunolocalization with plastic sections. Methods in Cell Biology 79: 492-413.

Muller-Reichert, T., M. Srayko, A. Hyman, E.T. O'Toole and K. McDonald (2007). Correlative light and electron microscopy of early Caenorhabditis elegans embryos in mitosis. Methods in Cell Biology 79: 101-119.

O'Toole, E.T., T.H. Giddings Jr. and S.K. Dutcher (2007). Understanding microtubule organizing centers by comparing mutant and wild-type structures with electron tomography. Methods in Cell Biology 79: 125-143.

Sandberg, K. and M. Braga (2007). Segmentation of thin structures in electron micrographs using orientation fields. Journal of Structural Biology 157: 403-415.

Santarella, R., Koffa, M., Tittmann, P., Gross, H., and Hoenger, A. (2007) HURP Wraps Microtubule-Ends With an Additional Tubulin Sheet That Has a Novel Conformation of Tubulin. J. Mol. Biol.

Schwartz, C. L., Sarbash, V. I., Ataullakhanov, F. I., McIntosh, J. R., and Nicastro, D. (2007). Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. Journal of microscopy 227, 98-109.

Zheng, L., Schwartz, C., Magidson, V., Khodjakov, A., and Oliferenko, S. (2007). The spindle pole bodies facilitate nuclear envelope division during closed mitosis in fission yeast. PLoS biology 5, e170.


Link to A. Hoenger 2006 Publications

Canty, E.G., T. Starborg, Y. Lu, S.M. Humphries, D.F. Holmes, R.S. Meadows, A. Huffman, E.T. O'Toole and K.E. Kadler (2006). Actin filaments are required for fibropositor-mediated collagen fibril alignment in tendon. Journal of Biological Chemistry 15: 38592-38598.

Ladinsky, M.S., J.M. Pierson and J.R. McIntosh (2006). Vitreous cryosectioning of cells, facilitated by a micromanipulator. Journal of Microscopy 224: 129-134.

Nakanishi, H., M. Morishita, C.L. Schwartz, A. Coluccio, J. Engebrecht and A.M. Neiman (2006). Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast. Journal of Cell Science. 119: 1406-1415.

Nicastro, D., C. Schwartz, J. Pierson, R. Gaudette, M.E. Porter and J.R. McIntosh (2006). The molecular architecture of axonemes revealed by cryoelectron tomography. Science. 313: 944-948.

Pelletier, L., E.T. O'Toole, A. Schwager, A.A. Hyman and T. Müller-Reichert (2006). Centriole assembly in Caenorhabditis elegans. Nature. 444: 619-623.

Shimogawa, M.M., B. Graczyk, M.K. Gardner, S.E. Francis, E.A. White, M. Ess, J.N. Volk, C. Ruse, S. Niessen, J.R. Yates, III, E.G. Muller, K. Bloom, D.J. Odde and T.N. Davis (2006). Mps1 phosphorylation of dam1 couples kinetochores to microtubule plus ends at metaphase. Current Biology. 16: 1489-1501.

Snyder, C.M., G. Mardones, M.S. Ladinsky and K.E. Howell (2006). GMx33 associates with the trans-Golgi matrix in a dynamix manner and sorts within tubules exiting the Golgi. Molecular Biology of the Cell. 17:511-524.

Srayko, M., E.T. O'Toole, A.A. Hyman and T. Muller-Reichert (2006). Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Current Biology. 16: 1944-1949.

Storchova, Z., A. Breneman, J. Cande, J. Dunn, K. Burbank, E.T. O'Toole and D. Pellman (2006). Genome-wide genetic analysis of polyploidy in yeast. Nature. 443: 541-547.

Zheng, L., C. Schwartz, L. Wee and S. Oliferenko (2006). The fission yeast TACC-related protein, Mia1p/Alp7p, is required for formation and maintenance of persistent microtubule-organizing centers at the nuclear envelope. Molecular Biology of the Cell. 17:2212-2222.


Caldwell, J.P., D.N. Mastronarde, J.L. Woods, and W.G. Bryson (2005). The three-dimensional arrangement of intermediate filaments in Romney wool cortical cells. Journal of Structural Biology. 151:298-305.

Mastronarde, D.N. (2005). Automated electron microscope tomography using robust prediction of specimen movements. Journal of Structural Biology. 152:36-51.

McIntosh, J.R., D. Nicastro and D.N. Mastronarde (2005). New views of cells in 3D: an introduction to electron tomography. Trends in Cell Biology. 15:43-51.

Muller, E.G.D., B.E. Snydsman, I. Novik, D.W. Hailey, D.R. Gestaut, C.A. Niemann, E.T. O'Toole, T.H. Giddings, Jr., B.A. Sundin and T.N. Davis (2005). The organization of the core proteins of the yeast spindle pole body. Molecular Biology of the Cell. 16:3341-3352.

Nicastro, D., J.R. McIntosh and W. Baumeister (2005). 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proceedings of the National Academy of Sciences. 102: 15889-15894.

Ozlu, N., M. Srayko, K. Kinoshita, B. Habermann, E.T. O'Toole, T. Müller-Reichert, N. Schmalz, A. Desai and A.A. Hyman (2005). An essential function of the C. elegans ortholog of TPX2 is to localize activated aurora A kinase to mitotic spindles. Developmental Cell. 9:237-248.

Stemm-Wolf, A.J., G. Morgan, T.H. Giddings, Jr., E.A. White, R. Marchione, H.B. McDonald and M. Winey. (2005). Basil body duplication and maintenance require one member of the Tetrahymena thermophila centrin gene family. Molecular Biology of the Cell. 16:3606-3619.

Tucker, M., M. Sieber, M. Morphew and M. Han (2005). The Caenorhabditis elegans aristaless orthologue, alr-1, is required for maintaining the functional and structural integrity of the amphid sensory organs. Molecular Biology of the Cell. 16:4695-4704.

Winey, M., G.P. Morgan, P.D. Straight, T.H. Giddings, Jr. and D.N. Mastronarde (2005). Three-dimensional ultrastructure of Saccharomyces cerevisiae meiotic spindles. Molecular Biology of the Cell. 16:1178-1188.

Yoder, T.J., M.A. McElwain, S.E. Francis, J. Bagley, E.G.D. Muller, B. Pak, E.T. O'Toole, M. Winey and T.N. Davis (2005). Analysis of a spindle pole body mutant reveals a defect in biorientation and illuminates spindle forces. Molecular Biology of the Cell. 16:141-152.


Marsh, B.J., N. Volkmann, J.R. McIntosh and K.E. Howell (2004). Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proceedings of the National Academy of Sciences. 101:5565-5570.

Yokohama, R., E.T. O'Toole, S. Ghosh and D.R. Mitchell (2004). Regulation of flagellar dynein activity by a central pair kinesin. Proceedings of the National Academy of Sciences. 101:17398-17403.

Mogelsvang, S., B.J. Marsh, M.S. Ladinsky and K.E. Howell (2004). Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic. 5:338-345.

Zahn, T.R., J.R. Angleson, M.A. MacMorris, E. Domke, J.F. Hutton, C. Schwartz and J.C Hutton (2004). Dense core vesicle dynamics in Caenorhabditis elegans neurons and the role of kinesin UNC-104. Traffic. 5: 544-559.


O'Toole, E.T., K.L. McDonald, J. Mantler, J.R. McIntosh, A.A. Hyman and T. Muller-Reichert (2003). Morphologically distinct microtubule ends in the mitotic centrosome of Caenorhabditis elegans. Journal of Cell Biology. 163:451-456.

Sandberg, K., D.N. Mastronarde, and G. Beylkin (2003). A fast reconstruction algorithm for electron microscope tomography. Journal of Structural Biology. 144:61-72.

Morphew, M.K. and J.R. McIntosh (2003). The use of filter membranes for high pressure freezing of cell monolayers. Journal of Microscopy. 212:21-25.

Muller-Reichert, T., E.T. O'Toole, H. Hohenberg and K. McDonald (2003). Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure. Journal of Microscopy. 212:71-80.

Muller-Reichert, T., E. Sassoon, E.T. O'Toole, M. Romao, A.J. Ashford, A.A. Hyman and C. Antony (2003). Analysis of the distribution of the kinetochore protein Nde10p in Saccharomyces cerevisiae using 3-D modeling of mitotic spindles. Chromosoma. 111:417-428.

Nickas, M., C. Schwartz, and A. Neiman (2003). ADY4P and SPO74P are components of the meiotic spindle pole body that promote growth of the prospore membrane in yeast. Eukaryotic Cell. 2(3):431-445.

O'Toole, E.T.. T.H. Giddings, J.R. McIntosh and S.K. Dutcher (2003). Three-dimensional organization of basal bodies from wild type delta tubulin deletion strains of Chlamydomonas reinhardtii. Molecular Biology of the Cell. 14:2999-3012.

Roberts, P., S. Moshitch-Moshkovitz, E. Kvam, E.T. O'Toole, M. Winey and D.S. Goldfarb (2003). Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Molecular Biology of the Cell 14(1):129-141.

Paoletti, A., N. Bordes, R. Haddad, C. Schwartz, F. Chang and M. Bornens (2003). Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication. Molecular Biology of the Cell 14(7):2793-2808.

Stanlis, K.K.H. and J.R. McIntosh (2003). Single-strand DNA aptamers as probes for protein localization in cells. Journal of Histochemistry & Cytochemistry. 51:797-808.


Burns, C.G., R. Ohi, S. Mehta, E.T. O'Toole, M. Winey, T.A. Clark, C.W. Sugnet, M. Ares Jr. and K.L. Gould (2002). Removal of a single alpha-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae. Molecular Biology of the Cell 22(3):801-15.

Clemett, S.J., K.L. Thomas-Keprta, J. Shimmin, M. Morphew, J.R. McIntosh, D.A. Bazylinsky, J. Kirschvink, S.J. Wentworth, D.S. McKay, K. Vali, E.K. Gibson and C.S. Romanek (2002). Crystal morphology of MV-1 magnetite. American Mineralogist 87:1727-1730.

Duman, J.G., N.J. Pathak, M.S. Ladinsky, K.L. McDonald and J.G. Forte (2002). Three-dimensional reconstruction of cytoplasmic membrane networks in parietal cells. Journal of Cell Science 115(6):1251-1258.

Flory, M., M.K. Morphew, J.D. Joseph, A.R. Means, and T.N. Davis (2002). Pcp1p, a SPC110-related calmodulin target at the centrosome of the fission yeast, Schizosaccharomyces pombe. Cell Growth and Differentiation 13(2): 47-58.

Ladinsky, M.S., C.C. Wu, S. McIntosh, J.R. McIntosh and K.E. Howell (2002). Structure of the Golgi and distribution of reporter molecules at 20°C reveals the complexity of the exit compartments. Molecular Biology of the Cell 13: 2810-2825.

Marsh, B.J. and K.E. Howell (2002). The mammalian Golgi-complex debates. Nature Reviews Molecular Cell Biology 3:789-795.

McIntosh, J.R., M.S. Ladinsky, E.T. O'Toole, M.K. Morphew, J. Shimmin and D. Mastronarde (2002). Electron tomography of fast-frozen, freeze-substituted cells reveals 3-D features of membrane traffic and mitosis. ICEM 15:2003-2004.

O'Toole, E.T., M. Winey, J.R. McIntosh and D.N. Mastronarde (2002). Electron tomography of yeast cells. Methods in Enzymology. 351: 81-95.

Putkey, F.R., T. Cramer, M.K. Morphew, A.D. Silk, R.S. Johnson, J.R. McIntosh, and D.W. Cleveland (2002). Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Developmental Cell 3(3):351-365.


Giddings, T.H., E.T. O'Toole, M.K. Morphew, D.N. Mastronarde, J.R. McIntosh and M. Winey (2001). Using rapid freezing and freeze-substitution for the preparation of yeast cells for electron microscopy and three-dimensional analysis. Methods in Cell Biology 67: 27-42.

Kniola, B., E.T. O'Toole, J.R. McIntosh, B. Mellone, R. Allshire, S. Mengarelli, K. Hultenby and K. Ekwall (2001). The domain structure of centromeres is conserved from fission yeast to humans. Molecular Biology of the Cell. 12: 2767-2775.

Marsh, B.J., D.N. Mastronarde, J.R. McIntosh and K.E. Howell (2001). Structural evidence for multiple transport mechanisms through the Golgi in the pancreatic beta-cell line, HIT-T15. Biochemical Society, Membrane Group/Neuorscience Group Joint Colloquium. 461-467.

Marsh, B.J., D.N. Mastronarde, K.F. Buttle, K.E. Howell and J.R. McIntosh (2001). Organellar relationships in the Golgi region of the pancreatic beta cell, line, HIT-T15, visualized by high-resolution electron tomography. Proceedings of the National Academy of Sciences 98: 2399-2406.

Otegui, M.S., D.N. Mastronarde, B.-H. Kang, S.Y. Bednarek and L.A. Staehelin (2001). Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13: 2033-2051.

Rupp, G., E.T. O'Toole and M.E. Porter (2001). The Chlamydomonas PF6 locus encodes a large alanine/proline-rich polypeptide that is required for assembly of a central pair projection and regulates flagellar motility. Molecular Biology of the Cell 12: 739-751.

Winey, M., and E.T. O'Toole (2001). The spindle cycle in budding yeast. Nature Cell Biology 3: E23-27. abstract


Morphew, M.K., D.N. Mastronarde, E.T. O'Toole, M.S. Ladinsky, B.J. Marsh, J. Kahana and J.R. McIntosh (2000). Three dimensional immunolocalization of green fluorescent protein chimeras using rapid freezing and freeze-substitution. Microscopy and Microanalysis, 298-299.

Perrone, C.A., S.H. Myster, R. Bower, E.T. O'Toole, and M.E. Porter (2000). Insights into the structural organization of the I1 inner dynein arm from a domain analysis of the 1b dynein heavy chain. Molecular Biology of the Cell 11: 2297-2313.

Wu, C.C., R.S. Taylor, D.R. Lane, M.S. Ladinsky, J.A. Weisz and K.E. Howell (2000). GMx33: A novel family of trans-Golgi proteins identified by proteomics. Traffic 1: 963-975.


Balasundaram, D., M. Benedik, M.K. Morphew, V. Dang and H. Levine (1999). Nup124p is a nuclear pore factor of Schizosaccharomyces pombe that is important for the nuclear import and activity of the retrotransposon Tf1. Molecular Biology of the Cell 19: 5768-5784.

Hagan, I.M., A.J. Bridge, M.Morphew and R. Bartlett (1999). Cell cycle control and the mitotic spindle. British Journal of Cancer.

Ladinsky, M.S., D.N. Mastronarde, J.R. McIntosh, K.E. Howell and L.A. Staehelin (1999). Golgi structure in 3 dimensions: Functional insights from the NRK cell. Journal of Cell Biology, 144: 1135-1149.

McIntosh, J.R. and E.T. O'Toole (1999). Life cycles of yeast spindle pole bodies: getting microtubules into a closed nucleus. Biology of the Cell 91: 305-312.

Mitchell, D.R., and W.S. Sale (1999). Characterization of a Chlamydomonas insertional mutant that disrupts central pair microtubule-associated structures. Journal of Cell Biology 144: 293-304.

Morrell, J.L., M. Morphew, and K.L. Gould (1999). A Mutant of Arp2p Causes Partial Disassembly of the Arp2/3 Complex and loss of Cortical Actin Function in Fission Yeast. Molecular Biology of the Cell 10: 4201-4215.

Munoz-Centeno, M., S. McBratney, A. Monterrosa, B. Byers, C. Mann and M. Winey (1999). Saccharomyces cerevisiae MPS2 encodes a membrane protein localized at the spindle pole body and the nuclear envelope. Molecular Biology of the Cell 10: 2393-2406.

O'Toole, E.T., M. Winey and J.R. McIntosh (1999). High voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast, Saccharomyces cerevisiae. Molecular Biology of the Cell 10: 2017-2031.

Sparks, C.A., M.K. Morphew and D. McCollum (1999). Sid2p, a spindle pole body kinase that regulates the onset of cytokinesis. Journal of Cell Biology 146: 777-789.

Tirnauer, J.S., E.T. O'Toole, L. Berrueta, B.E. Bierer and D. Pellman (1999). Yeast Bim1p promotes the G1-specific dynamics of microtubules. Journal of Cell Biology 145: 993-1007.

Zeng, X., J.A. Kahana, P.A. Silver, M.K. Morphew, J.R. McIntosh, T.T. Fitch, J. Carbon and W.S. Saunders (1999). SLK19p is a centromere protein that functions to stabilize mitotic spindles. Journal of Cell Biology 26: 415-426.


Bridge, A.J., M.K. Morphew , R. Bartlett and I. Hagan (1998). The fission yeast SPB component cut12 links bipolar spindle formation to mitotic control. Genes and Development 12(7): 927-42.

Perrone, C.A., P. Yang, W.S. Sale, and M.E. Porter (1998) The Chlamydomanas IDA7 locus encodes a 140 kDa dynein intermediate chain required to assemble the I1 inner arm complex. Molecular Biology of the Cell 9: 3351-3365.

West, R.R., E.V. Vaisberg, R. Ding, P. Nurse, and J.R. McIntosh (1998). Cut11: A Gene Required for Cell Cycle-dependent Spindle Pole Body Anchoring in the Nuclear Envelope and Bipolar Spindle Formation in Schizosaccharomyces pombe. Molecular Biology of the Cell 9: 2839-2855.

Wilkinson, C.R., Wallace, M., Morphew, M., Perry, P., Allshire, R., Javerrzatm, J.P., McIntosh, J.R., and Gordon, C. (1998). Localization of the 26s proteasome during mitosis and meiosis in fission yeast. EMBO Journal 17(22): 6465-76.


Mastronarde, D.N. (1997). Dual-axis tomography: An approach with alignment methods that preserve resolution. Journal of Structural Biology 120: 343-352.

McIntosh, J.R., D.N Mastronarde, J.R. Kremer, E.T. O'Toole, M.S. Ladinsky, M.K. Morphew and K.L McDonald (1997). Three-dimensional reconstruction of cellular fine structure by electron microscopy of serial sections and serial tilts. In: Recent Advances in Microscopy of Cells, Tissues, and Organs (P.M.Motta, ed.) Antonio DelFino Editore, Rome. pp. 67-76.

Myster, S.H., J.A. Knott, E.T. O'Toole and M.E. Porter (1997). The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for the assembly of the I1 inner arm complex. Molecular Biology of the Cell 8: 607-620.

O'Toole, E.T., D.N. Mastronarde, T.H. Giddings Jr., M. Winey, D.J. Burke and J.R. McIntosh (1997). Three-dimensional analysis and ultrastructural design of mitotic spindles from the cdc20 mutant of Saccharomyces cerevisiae. Molecular Biology of the Cell 8: 1-11.

Winey, M., D. Yarar, T.H. Giddings, Jr. and D.N. Mastronarde (1997). Nuclear pore complex number and distribution throughout the Saccharomyces cerevisiae cell cycle by three-dimensional reconstruction from electron micrographs of nuclear envelopes. Molecular Biology of the Cell 8: 2119-2132.


Kremer J.R., D.N. Mastronarde and J.R. McIntosh (1996). Computer Visualization of Three-Dimensional Image Data Using IMOD. Journal of Structural Biology. 116: 71-76.

McCollum, D., A. Feoktistova, M.K. Morphew, M. Balasubramanian, and K. Gould (1996). The Schizosaccharomyces pombe actin-related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. EMBO Journal 15(23): 6438-46.

Rupp, G., E.T. O'Toole, L.C. Gardner, B.F. Mitchell and M.E. Porter (1996). The sup-pf-2 mutations of Chlamydomonas alter the activity of the outer dynein arms by modification of the gamma-dynein heavy chain. Journal of Cell Biology 135: 1853-1865.

Schlegel, A., T.H. Giddings, Jr., M.S. Ladinsky and K. Kirkegaard (1996). Cellular origin and ultrastructure of membranes induced during poliovirus infection. Journal of Virology 70:6576-6588.


Demeter, J., M. Morphew and S. Sazar (1995). A mutation in the RCC1-related protein pim1 results in nuclear envelope fragmentation in fission yeast. Proceedings of the National Academy of Sciences 92(5): 1436-1440.

O'Toole, E.T., D.N. Mastronarde, J.R. McIntosh and M.E. Porter (1995). Computer-assisted analysis of flagellar structure. In: Methods in Cell Biology, Vol. 47. Cilia and Flagella (W. Dentler and G.Witman, eds.) Academic Press, San Diego. Pp. 183-191.

Wang, J., M.S. Ladinsky and K.E. Howell (1995). Molecules and vesicle coats involved in the budding of exocytotic vesicles from the trans-Golgi network. Cold Spring Harb. Symp. Quant. Biol. 60: 139-146.

Winey, M., C.L. Mamay, E.T. O'Toole, D.N. Mastronarde, T.H. Giddings, K.L. McDonald and J.R. McIntosh (1995). Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. Journal of Cell Biology 129: 1601-1615.


King, S.J., W.B. Inwood, E.T. O'Toole, J. Power and S.K. Dutcher (1994). The bop2-1 mutation reveals radial asymmetry in the inner dynein arm region of Chlamydomonas reinhardtii. Journal of Cell Biology 126: 1255-1266.

Ladinsky, M.S., J.R. Kremer, P.S. Furcinitti, J.R. McIntosh, and K.E. Howell (1994). HVEM tomography of the trans-Golgi network: Structural insights and identification of a lace-like vesicle coat. Journal of Cell Biology 127:29-38.


Mastronarde, D.N., K.L. McDonald, R. Ding and J.R. McIntosh (1993). Interpolar spindle microtubules in PTK cells. Journal of Cell Biology 123: 1475-1489.

O'Toole, E.T., G. Wray, J.R. Kremer and J.R. McIntosh (1993). High voltage cryomicroscopy of human blood platelets. Journal of Structural Biology 110: 55-66.


McDonald, K.L., E.T. O'Toole, D.N. Mastronarde and J.R. McIntosh (1992). Kinetochore microtubules in PTK cells. Journal of Cell Biology 118: 369-383.

Mastronarde, D.N., E.T. O'Toole, K.L. McDonald, J.R. McIntosh, and M.E. Porter (1992). Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. Journal of Cell Biology 118: 1145-1162.

Wilson, C.J., D.N. Mastronarde, B. McEwen and J. Frank (1992). Measurement of neuronal surface area using high-voltage electron microscope tomography. Neuroimage 1: 11-22.


McDonald, K.L., D.N. Mastronarde, E.T. O'Toole and J.R McIntosh (1991). Computer-based tools for morphometric analysis of mitotic spindles and other microtubule systems. EMSA Bulletin 21: 1-6.


McIntosh, J.R. and K.L. McDonald (1989). The Mitotic Spindle. Scientific American 261(4): 48-56.