Hoenger Lab
University of Colorado at Boulder
Department of Molecular, Cellular and Developmental Biology

Structural and Functional Investigations
into Cytoskeletal Assemblies by
Cryo Electron Microscopy
and 3D Image Analysis


Selected Recent Publications:

Goulbourne CN, Gin P, Tatar A, Nobumori C, Hoenger A, Jiang H, Grovenor CR, Adeyo O, Esko JD, Goldberg IJ, Reue K, Tontonoz P, Bensadoun A, Beigneux AP, Young SG, Fong LG. (2014) The GPIHBP1-LPL Complex Is Responsible for the Margination of Triglyceride-Rich Lipoproteins in Capillaries. Cell Metab. 2014 Apr 8. pii: S1550-4131

Maurer SP, Fourniol FJ, Hoenger A, Surrey T. (2014) Seeded microtubule growth for cryoelectron microscopy of end-binding proteins. Methods Mol Biol. 1136:247-60.

Hoog JL, Lacomble S, O'Toole ET, Hoenger A, McIntosh JR, Gull K. (2014) Modes of flagellar assembly in Chlamydomonas reinhardtii and Trypanosoma brucei. Elife. 2014;3:e01479.

Hoenger, A. (2014) High-resolution cryo-electron microscopy on macromolecular complexes and cell organelles. Protoplasma, 251:417-427.

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. 184:335-344.

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

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.

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.

Rank KC, Chen CJ, Cope J, Porche K, Hoenger A, Gilbert SP, Rayment I. Kar3Vik1, a member of the kinesin-14 superfamily, shows a novel kinesin microtubule binding pattern. J Cell Biol. 2012 Jun 25;197(7):957-70. PubMed PMID: 22734002.

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.

Bouchet-Marquis C, Pagratis M, Kirmse R, Hoenger A. Metallothionein as a clonable high-density marker for cryo-electron microscopy. J Struct Biol. 2012 Jan;177(1):119-27. Epub 2011 Oct 31. PubMed PMID: 22068155; PubMed Central PMCID:PMC3261350.

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 (9):e43783. Epub 2012 Sep 11. PubMed PMID: 22984443; PubMed Central PMCID: PMC3439489.

Erickson KD, Bouchet-Marquis C, Heiser K, Szomolanyi-Tsuda E, Mishra R, Lamothe B, Hoenger A, Garcea RL. Virion assembly factories in the nucleus of polyomavirus-infected cells. PLoS Pathog. 2012;8(4):e1002630. Epub 2012 Apr 5. PubMed PMID: 22496654; PubMed Central PMCID: PMC3320610.

Heumann JM, Hoenger A, Mastronarde DN. Clustering and variance maps for cryo-electron tomography using wedge-masked differences. J Struct Biol. 2011 Sep;175(3):288-99. Epub 2011 May 17. PubMed PMID: 21616153; PubMed Central PMCID: PMC3150390.

Cope J, Heumann J, Hoenger A. Cryo-electron tomography for structural characterization of macromolecular complexes. Curr Protoc Protein Sci. 2011 Aug;Chapter 17:Unit17.13. PubMed PMID: 21842467; PubMed Central PMCID: PMC3254243.

Iconomidou VA, Pheida D, Hamodraka ES, Antony C, Hoenger A, Hamodrakas SJ. An amyloidogenic determinant in N-terminal pro-brain natriuretic peptide (NT-proBNP): Implications for cardiac amyloidoses. Biopolymers. 2011 Jul 25. doi: 10.1002/bip.21698. [Epub ahead of print] PubMed PMID: 21792845.

Daikeler T, Tzankov A, Hoenger G, Gasser O, Tyndall A, Gratwohl A, Hess C. Minimal T-cell requirements for triggering haemophagocytosis associated with Epstein-Barr virus-driven B-cell proliferation: a clinical case study. Ann Rheum Dis. 2011 Jul;70(7):1338-9. Epub 2011 Jan 7. PubMed PMID: 21216813.

Schiel JA, Park K, Morphew MK, Reid E, Hoenger A, Prekeris R. Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci. 2011 May 1;124(Pt 9) 1411-24. Epub 2011 Apr 12. PubMed PMID: 21486954; PubMed Central PMCID: PMC3078810.

West M, Zurek N, Hoenger A, Voeltz GK. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol. 2011 Apr 18;193(2):333-46. PubMed PMID: 21502358; PubMed Central PMCID: PMC3080256.

Maurer SP, Bieling P, Cope J, Hoenger A, Surrey T. GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):3988-93. Epub 2011 Feb 22. PubMed PMID: 21368119; PubMed Central PMCID: PMC3053978.

Daikeler T, Hoenger G, Oehri I, Tyndall A, Gratwohl A, Brander C, Klimkait T, Gasser O, Hess C. Dominant Epstein-Barr virus-specific T-cell responses are maintained during moderate and intense immunosuppressive treatment. Ann Rheum Dis. 2011 Feb;70(2):395-6. Epub 2010 Jul 19. PubMed PMID: 20643766.

Bouchet-Marquis C, Hoenger A. Cryo-electron tomography on vitrified sections: a critical analysis of benefits and limitations for structural cell biology. Micron. 2011 Feb;42(2):152-62. Epub 2010 Jul 13. Review. PubMed PMID: 20675145.

Durovic B, Zenhaeusern G, Hoenger G, Gasser O, Schaub S, Hess C. Allo-induced acute-phase response; IL-6 identifies a subset of individuals at risk for graft injury. Scand J Immunol. 2011 Feb 73(2):156-8. doi: 10.1111/j.1365-3083.2010.02489.x. PubMed PMID: 21198758.

Hoenger A, Bouchet-Marquis C. Cellular tomography. Adv Protein Chem Struct Biol. 2011;82:67-90. Review. PubMed PMID: 21501819.

Iconomidou VA, Cordopatis P, Hoenger A, Hamodrakas SJ. 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 family. Biopolymers. 2011;96(6):723-33. doi: 10.1002/bip.21606. Epub 2011 Feb 18. PubMed PMID: 22252423.

De Carlo S, Lin SC, Taatjes DJ, Hoenger A. Molecular basis of transcription initiation in Archaea. Transcription. 2010 Sep-Oct;1(2):103-11. PubMed PMID: 21326901; PubMed Central PMCID: PMC3023638.

Kirmse R, Qin Z, Weinert CM, Hoenger A, Buehler MJ, Kreplak L. Plasticity of intermediate filament subunits. PLoS One. 2010 Aug 12;5(8):e12115. Erratum in: PLoS One. 2010;5(9) doi:10.1371 annotation/8f182672-e11e-48d5-8a74-c401b8bd5ecc. Hoenger, Andrea [corrected to Hoenger, Andreas]. PubMed PMID: 20814582; PubMed Central PMCID: PMC2930322.

Kirmse R, Bouchet-Marquis C, Page C, Hoenger A. Three-dimensional cryo-electron microscopy on intermediate filaments. Methods Cell Biol. 2010;96:565-89. PubMed PMID: 20869538.

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.

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. Epub 2009 Sep 19.

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.

Marx A, Hoenger A, Mandelkow E. Structures of kinesin motor proteins. Cell Motil Cytoskeleton. 2009 Nov;66(11):958-66. 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. Epub 2009 Feb 5.

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

Marx A, Hoenger A, Mandelkow E. Structures of kinesin motor proteins. Cell Motil Cytoskeleton. 2009 Nov;66(11):958-66.

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

Small JV, Auinger S, Nemethova M, Koestler S, Goldie KN, Hoenger A, Resch GP. Unravelling the structure of the lamellipodium. J Microsc. 2008 Sep;231(3):479-85.

Bouchet-Marquis C, Starkuviene V, Grabenbauer M. Golgi apparatus studied in vitreous sections. J Microsc. 2008 May;230(Pt 2):308-16.

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. Biochemistry. 2008 Feb 19;47(7):1848-61. Epub 2008 Jan 19.

De Carlo S, Boisset N, Hoenger A. High-resolution single-particle 3D analysis on GroEL prepared by cryo-negative staining. Micron. 2008 Oct;39(7):934-43. Epub 2007 Nov 17.

Woodward JD, Weber BW, Scheffer MP, Benedik MJ, Hoenger A, Sewell BT. Helical structure of unidirectionally shadowed metal replicas of cyanide hydratase from Gloeocercospora sorghi.

Hoenger A, Gross H. Structural investigations into microtubule-MAP complexes. Methods Cell Biol. 2008;84:425-44.

Hoenger A, Nicastro D. Electron microscopy of microtubule-based cytoskeletal machinery. Methods Cell Biol. 2007;79:437-62. Review.

Norlen L, Masich S, Goldie KN, Hoenger A. Structural analysis of vimentin and keratin intermediate filaments by cryo-electron tomography. Exp Cell Res. 2007 Jun 10;313(10):2217-27.

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. J Struct Biol. 2007 Jun;158(3):378-85.

Sandblad, L., Busch, E.K., Tittmann, P., Gross, H., Brunner, D., and Hoenger, A. (2006) The Schizosaccharomyces pombe EB1 Homolog Mal3p Binds and Stabilizes the Microtubule Lattice Seam. Cell, 127:1-10.

Santarella, R., Koffa, M., Tittmann, P., Gross, H., and Hoenger, A. (2006) HURP Wraps Microtubule-Ends With an Additional Tubulin Sheet That Has a Novel Conformation of Tubulin. J. Mol. Biol. Volume 365, Issue 5,2 February 2007, Pages 1587-1595

Iconomidou VA, Chryssikos GD, Gionis V, Galanis AS, Cordopatis P, Hoenger A, Hamodrakas SJ. (2006) Amyloid fibril formation propensity is inherent into the hexapeptide tandemly repeating sequence of the central domain of silkmoth chorion proteins of the A-family. 156:480-8.

Krzysiak, T.C., Wendt, T., Sproul, L.R., Gross, H., Gilbert, S.P. and Hoenger, A. (2006) A Structural Model for Monastrol Inhibition of Dimeric Kinesin Eg5. EMBO J. 2006 May 17; 25(10): 2263 2273.

Ribbeck K, Groen AC, Santarella R, Bohnsack MT, Raemaekers T, Kocher T, Gentzel M, Gorlich D, Wilm M, Carmeliet G, Mitchison TJ, Ellenberg J, Hoenger, A, Mattaj IW. NuSAP, a Mitotic RanGTP Target That Stabilizes and Cross-links Microtubules. Mol Biol Cell. 2006 Jun;17(6):2646-60

Hizlan D, Mishima M, Tittmann P, Gross H, Glotzer M, Hoenger A. (2006) Structural analysis of the ZEN-4/CeMKLP1 motor domain and its interaction with microtubules. J Struct Biol. 153:73-84.

Marx A, Muller J, Mandelkow EM, Hoenger A, Mandelkow E. (2005) Interaction of kinesin motors, microtubules, and MAPs. J Muscle Res Cell Motil. 17:1-13.

Grabenbauer M, Geerts WJ, Fernadez-Rodriguez J, Hoenger A, Koster AJ, Nilsson T. (2005) Correlative microscopy and electron tomography of GFP through photooxidation. Nat Methods. 11:857-62.

Krebs, A., Goldie, K.N., and Hoenger, A. (2005) Structural rearrangements in alpha- and beta-tubulin upon microtubule formation. EMBO Reports, 6:227-32.

Santarella, R.A., Skiniotis, G., Goldie, K.N., Mandelkow, E-M., Gross, H., Mandelkow, E., and Hoenger, A. (2004) Microtubule Surface-Decoration Properties of Human TAU-40. J. Mol. Biol. 339: 539-553.

Schoehn, G., Mavrakis, M., Albertini, A., Wade, R., Hoenger, A., and Ruigrok, R.W.H. (2004) 12 Structure of Trypsin Treated Measles Virus N-RNA. J. Mol. Biol. 339: 301-312.

Klumpp, L.M., Hoenger, A., and Gilbert, S. (2004). Kinesin s second step. Proc. Natl. Acad. Sci. 101: 3444-3449.

Klumpp, L.M., Brendza, K.M., Gatial, J.E., Hoenger, A., Saxton, W., and Gilbert, S. (2004) Microtubule-Kinesin Interface reveal a Site Critical for Communication. Biochemistry 43: 2792-2803.

Skiniotis, G., Cochran, J. Gilbert, S.P., and Hoenger, A. (2004) The C-terminus of Tubulin Modulates Nucleotide-Dependent Kinesin Binding. EMBO J. 23: 989-999.

Hamodrakas, SJ., Hoenger, A., and Iconomidou, V.A. (2004) Amyloid fibrillogenesis of silkmoth chorion proteine peptide-analogues via a lipid-crystalline intermediate phase. J. Struct. Biol. 145:226-235.

Krebs, A., Goldie, K. N., and Hoenger, A. (2004) Complex Formation with Kinesin Motor Domains Affects the Structure of Microtubules. J. Mol. Biol. 335: 139-153.

Wendt, T., Karabay, A. Walker, R.A., Gross, H., and Hoenger, A. (2003) A Structural Analysis of the Interaction between Ncd Tail and Tubulin Protofilaments. J. Mol. Biol, 333: 541-552.

De Marco, V., Goldie, K.N., de Marco, A., Correia, J., and Hoenger, A. (2003) Dimerization Properties of a Xenopus Laevis Kinesin-II C-terminal Stalk Fragment. EMBO Reports, 4: 717-722.

Iconomidou, V.A., Chryssikos, G.D., Gionis, V., Hoenger, A., and Hamodrakas, S.J. (2003) FT-Raman spectroscopy as diagnostic tool of Congo red binding to amyloids. Biopolymers, 72: 185-92.

Schatz, C.A., Santarella, R., Hoenger, A., Karsenti, E., Mattaj, I.W., Gruss, O.J. and Carazo-Salas, R. E. (2003) Importin a-Regulated Nucleation of Microtubules by TPX2. EMBO J. 22: 2060-70.

Skiniotis, Y., Surrey, T., Altmann, S., Gross, H., Song Y.H., Mandelkow, E., and Hoenger, A. (2003) An SH3 Domain engineered between the Kinesin Linker and Neck allows a detailed Localization of the Neck-Linker Region by Cryo-Electron Microscopy. EMBO J. 22: 1518-28.

Raae, A.J., Banuelos, S., Yianne, J., Torbjorn, O., Goldie, K.N., Wendt, T., Hoenger, A., and Saraste, M. (2003) Actin binding of Minispectrin. BBA  Proteins and Proteomics, Vol. 1646: 67-76.

Klumpp, L.M., Brendza, K.M., Rosenberg, J.M., Hoenger, A., Gilbert, S.P. (2003) Motor domain Mutation traps Kinesin as a Microtubule-rigor Complex. Biochemistry, 42: 2595-2606.

Wendt, T.G., Volkmann, N., Goldie, K.N., Muller, J., Mandelkow, E., and Hoenger, A. (2002) Microtubule Binding Patterns of the Reverse Kinesin Motor Ncd reveal a Minus-End Directed Power Stroke. EMBO J. 21: 5969-5978.

Lopez de la Paz, M., Goldie, K., Zurdo, J., Lacroix, E., Dobson, C.M., Hoenger, A., and Serrano, L. (2002) De novo designed peptide-based amyloid fibrils. Proc. Natl. Acad. Sci. 99: 16052-16057.

Resch, G. P., Goldie, K. N., Hoenger, A. and Small, J. V. (2002) Pure F-Actin Networks are Distorted and Branched by Steps in the Critical Point Drying Technique. J. Struct. Biol., 137, 305-312.

Resch, G. P., Goldie, K. N., Krebs, A., Hoenger, A. and Small, J. V. (2002) Visualisation of the Actin Cytoskeleton by Cryo-Electron Microscopy. J. Cell. Sci., 115, 1877-82.

Song, Y.H. Marx, A., Mueller, J., Woehlke, G., Schliwa, M., Krebs, A., Hoenger, A., and Mandelkow, E. (2001) Structure of a fast kinesin: implications for ATPase mechanism and interactions with microtubules. EMBO J. 20: 6213-25.

De Marco, V., Burkhard, P., Le Bot, N., Vernos, I., and Hoenger, A. (2001) Analysis of heterodimer formation by Xklp3A/B, a newly cloned kinesin-II from Xenopus laevis. EMBO J. 20: 3370-9.

Iconomidou, V.A., Chryssikos, G.D., Gionis, V., Vriend, G., Hoenger, A., and Hamodrakas, S.J. (2001) Amyloid-like fibrils from an 18-residue peptide analogue of a part of the central domain of the B-family of silkmoth chorion proteins. FEBS Lett. 499: 268-73.

Beuron, F., and Hoenger, A. (2001) Structural analysis of the microtubule-kinesin complex by cryo-electron microscopy. Methods Mol. Biol. 164: 235-54.

Hoenger, A., Doerhoefer, M., Woehlke, G., Tittmann, P., Gross, H., Song, Y.-H., and Mandelkow, E. (2000) Surface Topography of Microtubule Walls Decorated with Monomeric and Dimeric Kinesin Constructs. Biol. Chem. 381: 1001-11.

Steinmetz, M.O., Hoenger, A., Stoffler, D., Noegel, A.A., Aebi, U., Schoenenberger, C.A. (2000) Polymerization, three-dimensional structure and mechanical properties of Dictyostelium versus rabbit muscle actin filaments. J. Mol. Biol. 303: 171-84.

Hoenger, A., Thormaehlen, M., Diaz-Avalos, R., Doerhoefer, M., Goldie, K., Mueller, J., and Mandelkow, E. (2000) A new Look at the Microtubule Binding Patterns of Dimeric Kinesins. J. Mol. Biol. 297, 1087-1103.

Mandelkow, E. and Hoenger, A. (1999) Structures of Kinesin and Kinesin-Microtubule Interactions. Curr. Opin. Cell. Biol. 11, 34-44.

Steinmetz, M. O., Hoenger, A., Tittmann, P., Fuchs, K., Gross, H., and Aebi, U. (1998) An Atomic Model of Actin Tubes: Combining Electron Microscopy and X-ray Crystallography. (1998) J. Mol. Biol. 278: 703-11.

Hoenger, A., Sack, S., Thormaehlen, M., Marx, A., Mueller, J., Gross, H., and Mandelkow, E. (1998) Image Reconstructions of Microtubules Decorated with Monomeric and Dimeric Kinesins: Comparison with X-ray Structure and Implications for Motility. J. Cell Biol. 141, 419-430.

Steinmetz, M. O., Stoffler, D., Hoenger, A., Bremer, A., and Aebi, U. Actin: from Cell Biology to Atomic Detail. (1997) J. Struct. Biol. 119, 295-320.

Sosa, H., Dias, P. D., Hoenger, A., Whittaker, M., Wilson-Kubalek., E., Sablin, E., Fletterick, R., Vale, R. D., and Milligan, R. A. A Model for the Microtubule-Ncd Motor Protein Complex obtained by Cryo-Electron Microscopy and Image Analysis. (1997) Cell, 90, 217-224.

Sosa, H., Hoenger, A., and Milligan, R. A. (1997) Three Different Approaches to Motor decorated Microtubule 3-D structure. J. Struct. Biol. 118, 149-158.

Hoenger, A., and Milligan, R. A. (1997) Motor Domains of Ncd and Kinesin interact with Microtubule Protofilaments with the same Binding Geometry. J. Mol. Biol. J. Mol. Biol. 265, 553-564.

Hoenger, A., and Milligan, R. A. (1996) Polarity of 2-D and 3-D maps of Tubulin sheets and motor-decorated Tubulin Sheets. J. Mol. Biol. 263, 114-119.

Hoenger, A. and Aebi, U. (1996) 3-D Reconstruction from Ice-embedded and Negatively stained Biomacromolecular Assemblies: A Critical Comparison. J. Struct. Biol. 117, 99-116

Hoenger, A., Sablin, E. P., Vale R. D., Fletterick, R. J., and Milligan, R. A. (1995) Three dimensional Structure of a Tubulin-Motor Protein Complex. Nature 376, 271-274.

El Kouhen, R., Hoenger, A., Engel, A., and Pages, J. M. (1994) In Vitro Approaches to Investigation of the early Steps of Colicin-OmpF Interaction. Eur. J. Biochem. 224, 723-728.


University of Colorado, MCDB, 347 UCB, Boulder, CO 80309-0347