Revealing the structure of stereociliary actin by x-ray nanoimaging

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12228-12237

  Piazza, Valeria ^a   Weinhausen, Britta ^a,c   Diaz, Ana ^b   Dammann, Christian ^a   Maurer, Christian ^a   Reynolds, Michael ^c   Burghammer, Manfred ^c,d   Köster, Sarah ^a,e  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^d GHENT UNIVERSITY   (Belgium)

^e Department of Molecular Neurogenetics   (Germany)

Author keywords

actin bundles; nanofocused beam; nanostructure; ptychography; stereocilia; vestibular sensory hair cells; X ray diffraction

Indexed keywords

AUDITION; DIFFRACTION PATTERNS; INTERFEROMETRY; NANOSTRUCTURES; X RAY DIFFRACTION;

ACTIN BUNDLES; NANOFOCUSED BEAM; PTYCHOGRAPHY; SENSORY HAIR CELLS; STEREOCILIA;

PROTEINS;

ACTIN;

ANIMAL; CHEMISTRY; CYTOLOGY; HAIR CELL; MOLECULAR IMAGING; MOUSE; NANOTECHNOLOGY; PROCEDURES; STEREOCILIUM; X RAY;

ACTINS; ANIMALS; HAIR CELLS, VESTIBULAR; MICE; MOLECULAR IMAGING; NANOTECHNOLOGY; STEREOCILIA; X-RAYS;

EID: 84919741368     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5041526     Document Type: Article

References (50)

1. Zhang, D.-S.; Piazza, V.; Perrin, B. J.; Rzadzinska, A. K.; Poczatek, J. C.; Wang, M.; Prosser, H. M.; Ervasti, J. M.; Corey, D. P.; Lechene, C. P. Multi-Isotope Imaging Mass Spectrometry Reveals Slow Protein Turnover in Hair-Cell Stereocilia Nature 2012, 481, 520-524
2. Chen, P. Y.; McKittrick, J.; Meyers, M. A. Biological Materials: Functional Adaptations and Bioinspired Designs Prog. Mater. Sci. 2012, 57, 1492-1704
3. Derosier, D. J.; Tilney, L. G.; Egelman, E. Actin in the Inner Ear: The Remarkable Structure of the Stereocilum Nature 1980, 287, 291-296
4. Huxley, H. E. Fifty Years of Muscle and the Sliding Filament Hypothesis Eur. J. Biochem. 2004, 271, 1403-1415
5. Huxley, H. E. X-Ray Analysis and the Problem of Muscle P. R. Soc. London B. Bio. 1953, 141, 59-62
6. Huxley, H. E.; Steward, A.; Sosa, H.; Irving, T. X-Ray Diffraction Measurements of the Extensibility of Actin and Myosin Filament in Contracting Muscle Biophys. J. 1994, 67, 2411-2421
7. Hanson, J. Evidence from Electron Microscope Studies on Actin Paracrystals concerning the Origin of the Cross-Striation in the Thin Filaments of Vertebrate Skeletal Muscle Proc. R. Soc. London B. Bio. 1973, 183, 39-58
8. Holmes, C. K.; Popp, D.; Gebhard, W.; Kabsch, W. Atomic Model of the Actin Filament Nature 1990, 347, 44-49
9. Egelman, E. H.; Orlova, A. New Insights Into Actin Filament Dynamics Curr. Opin. Struct. Biol. 1995, 5, 172-180
10. Wong, G. L. C.; Tang, J. X.; Lin, A.; Li, Y.; Janmey, P. A.; Safinya, C. R. Hierarchical Self-Assembly of F-Actin and Cationic Lipid Complexes: Stacked Three-Layer Tubule Networks Science 2000, 288, 2035-2039
11. Angelini, T. E.; Liang, H.; Wriggers, W.; Wong, G. C. L. Like-Charge Attraction Between Polyelectrolytes Induced by Counterion Charge Density Waves Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 8634-8637
12. Sanders, L. K.; Xian, W.; Guaqueta, C.; Strohman, M. J.; Vrasich, C. R.; Luitjen, E.; Wong, G. C. L. Control of Electrostatic Interactions Between F-Actin and Genetically Modified Lysozyme in Aqueous Media Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 15994-19999
13. Wong, G. C. L.; Pollack, L. Electrostatics of Strongly Charged Biological Polymers: Ion-Mediated Interactions and Self-Organization in Nucleic Acids and Proteins Annu. Rev. Phys. Chem. 2010, 61, 171-189
14. Pelletier, O.; Pokidysheva, E.; Hirst, L. S.; Bouxsein, N.; Li, Y.; Safinya, C. R. Structure of Actin Cross-Linked with α-Actinin: A Network of Bundles Phys. Rev. Lett. 2003, 91, 148102
15. Flock, A.; Bretscher, A.; Weber, K. Immunohistochemical Localization of Several Cytoskeletal Proteins in the Inner Ear Sensory and Supporting Cells Hearing Res. 1982, 7, 75-89
16. Shahin, H.; Walsh, T.; Sobe, T.; Abu Saed, J.; Rayan, A. A.; Lynch, E. D.; Lee, M. K.; Avraham, K. B.; King, M. C.; Kanaan, M. Mutations in a Novel Isoform of TRIOBP That Encodes a Filamentous-Actin Binding Protein Are Responsible for DFNB28 Recessive Nonsyndromic Hearing Loss Am. J. Hum. Genet. 2006, 78, 144-152
17. Zheng, L.; Sekerkova, G.; Vranich, K.; Tilney, L. G.; Mugnaini, E.; Bartles, J. R. The Deaf Jerker Mouse Has a Mutation in the Gene Encoding the Espin Actin-Bundling Proteins of Hair Cell Stereocilia and Lacks Espins Cell 2000, 102, 377-385
18. Lieleg, O.; Schmoller, K. M.; Purdy Drew, K. R.; Claessens, M. M. A. E.; Semmrich, C.; Zheng, L.; Bartles, J. R.; Bausch, A. R. Structural and Viscoelastic Properties of Actin Networks Formed by Espin or Pathologically Relevant Espin Mutants ChemPhysChem 2009, 10, 281-2817
19. Purdy, K. R.; Bartles, J. R.; Wong, G. C. L. Structural Polymorphism of the Actin-Espin System: A Prototypical System of Filaments and Linkers in Stereocilia Phys. Rev. Lett. 2007, 98, 058105
20. Shin, H.; Purdy Drew, K. R.; Bartles, J. R.; Wong, G. C. L.; Grason, G. M. Cooperativity and Frustration in Protein-Mediated Parallel Actin Bundles Phys. Rev. Lett. 2009, 103, 238102
21. Claessens, M. M. A. E.; Semmrich, C.; Ramos, L.; Bausch, A. R. Helical Twist Controls the Thickness of F-Actin Bundles Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 8819-8822
22. Schroer, C. G.; Kuhlmann, M.; Hunger, U. T.; Günzler, T. F.; Kurapova, O.; Feste, S.; Frehse, F.; Lengeler, B.; Drakopoulos, B.; Somogyi, A.; Simionovici, A. S.; Snigirev, A.; Snigireva, I.; Schug, C.; Schröder, W. H. Nanofocusing Parabolic Refractive X-ray Lenses Appl. Phys. Lett. 2003, 82, 1485-1487
23. Schropp, A.; Boye, P.; Feldkamp, J. M.; Hoppe, R.; Patommel, J.; Samberg, D.; Stephan, S.; Giewekemeyer, K.; Wilke, R. N.; Salditt, T.; Gulden, J.; Mancuso, A. P.; Vartanyants, I. A.; Weckert, E.; Schöder, S.; Burghammer, M.; Schroer, C. G. Hard X-Ray Nanobeam Characterization by Coherent Diffraction Microscopy Appl. Phys. Lett. 2010, 96, 091102
24. Schroer, C. G.; Kurapova, O.; Patommel, J.; Boye, P.; Feldkamp, J.; Lengeler, B.; Burghammer, M.; Riekel, C.; Vincze, L.; van der Hart, A.; Küchler, M. Hard X-Ray Nanoprobe Based on Refractive X-Ray Lenses Appl. Phys. Lett. 2005, 87, 124103
25. Sedlmair, J.; Gleber, S.-C.; Öztürk-Mert, S.; Bertilson, M.; von Hofsten, O.; Thieme, J.; Pfohl, T. Imaging of Vascular Smooth Muscle Cells with Soft X-Ray Spectromicroscopy Microsc. Microanal. 2011, 17, 991-1001
26. Weinhausen, B.; Nolting, J.-F.; Olendrowitz, C.; Langfahl-Klabes, J.; Reynolds, M.; Salditt, T.; Köster, S. X-Ray Nano-Diffraction on Cytoskeletal Networks New J. Phys. 2012, 14, 085013
27. Weinhausen, B.; Köster, S. Microfluidic Devices for X-ray Studies on Hydrated Cells Lab Chip 2012, 13, 212-215
28. Weinhausen, B.; Saldanha, O.; Wilke, R. N.; Dammann, C.; Priebe, M.; Burghammer, M.; Sprung, M.; Köster, S. Scanning X-Ray Nanodiffraction on Living Eukaryotic Cells in Microfluidic Environments Phys. Rev. Lett. 2014, 12, 088102
29. Alberts, B.; Johnson, A.; Raff, M.; Roberts, K.; Walter, P. In The Molecular Biology of the Cell; Taylor and Francis/Garland Science: New York, 2001.
30. Rusch, A.; Eatock, R. A. A Delayed Rectifier Conductance in Type I Hair Cells of the Mouse Utricle J. Neurophysiol. 1996, 76, 995-1004
31. Wilke, R. N.; Priebe, M.; Bartels, M.; Giewekemeyer, K.; Diaz, A.; Karvinen, P.; Salditt, T. Hard X-ray Imaging of Bacterial Cells: Nano-Diffraction and Ptychographic Reconstruction Opt. Express 2012, 20, 19232-19254
32. Faulkner, H. L. M.; Rodenburg, J. M. Movable Aperture Lensless Transmission Microscopy Phys. Rev. Lett. 2004, 93, 023903
33. Rodenburg, J. M.; Huerst, A. C.; Cullis, A. G.; Dobson, B. R.; Pfeiffer, F.; Bunk, O.; David, C.; Jefimovs, K.; Johnson, I. Hard-X-ray Lensless Imaging of Extended Objects Phys. Rev. Lett. 2007, 98, 034801
34. Howells, M. R.; Beetz, T.; Chapman, H. N.; Cui, C.; Holton, J. M.; Jacobsen, C. J.; Kirz, J.; Lima, E.; Marchesini, S.; Miao, H.; Sayreb, D.; Shapiroa, D. A.; Spencea, J. C. H.; Starodube, D. An Assessment of the Resolution Limitation due to Radiation-Damage in X-ray Diffraction Microscopy J. Electron Spectrosc. 2009, 170, 4-12
35. Giewekemeyer, K.; Thibault, P.; Kalbfleisch, S.; Beerlink, A.; Kewish, C. M.; Dierolf, M.; Pfeiffer, F.; Salditt, T. Quantitative Biological Imaging by Ptychographic X-Ray Diffraction Microscopy Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 529-534
36. Lima, E.; Diaz, A.; Guizar-Sicairos, M.; Gorelick, S.; Pernot, P.; Schleier, T.; Menzel, A. Cryo-Scanning X-Ray Diffraction Microscopy of Frozen-Hydrated Yeast J. Microsc. 2013, 249, 1-7
37. Hofer, D.; Ness, W.; Drenckhahn, D. Sorting of Actin Isoforms in Chicken Auditory Hair Cells J. Cell Sci. 1997, 110, 765-770
38. Furness, D. N.; Katori, Y.; Mahendrasingam, S.; Hackney, C. M. Differential Distribution of Beta- and Gamma-Actin in Guinea-Pig Cochlear Sensory and Supporting Cells Hearing Res. 2005, 207, 22-34
39. Perrin, B. J.; Sonnemann, K. J.; Ervasti, J. M. β-Actin and γ-Actin are Each Dispensable for Auditory Hair Cell Development but Required for Stereocilia Maintenance PLoS Genet. 2010, 6, 1001158
40. McGough, A.; Pope, B.; Chiu, W.; Weeds, A. Cofilin Changes the Twist of F-Actin: Implications for Actin Filament Dynamics and Cellular Function J. Cell Biol. 1997, 138, 771-781
41. Galkin, V. E.; Orlova, A.; Lukoyanova, N.; Wriggers, W.; Egelman, E. H. Actin Depolymerizing Factor Stabilizes an Existing State of F-Actin and can Change the Tilt of F-Actin Subunits J. Cell Biol. 2001, 153, 75-86
42. Liberman, M. C. Chronic Ultrastructural Changes in Acoustic Trauma: Serial-Section Reconstruction of Stereocilia and Cuticular Plates Hearing Res. 1987, 26, 65-88
43. Furness, D. N.; Mahendrasingam, S.; Ohashi, M.; Fettiplace, R.; Hackney, C. M. The Dimensions and Composition of Stereociliary Rootlets in Mammalian Cochlear Hair Cells: Comparison Between High- and Low-Frequency Cells and Evidence for a Connection to the Lateral Membrane J. Neurosci. 2008, 28, 6342-53
44. Gorelick, S.; Guzenko, V. A.; Vila-Comamala, J.; David, C. Direct e-Beam Writing of Dense and High Aspect Ratio Nanostructures in Thick Layers of PMMA for Electroplating Nanotechnology 2010, 21, 295303
45. Henrich, B.; Bergamaschi, A.; Broennimann, C.; Dinapoli, R.; Eikenberry, E. F.; Johnson, I.; Kobas, M.; Kraft, P.; Mozzanica, A.; Schmitt, B. PILATUS: A Single Photon Counting Pixel Detector for X-Ray Applications Nucl. Instrum. Meth. A 2009, 607, 247-249
46. Dierolf, M.; Thibault, P.; Menzel, A.; Kewish, C. M.; Jefimovs, K.; Schlichting, I.; von König, K.; Bunk, O.; Pfeiffer, F. Ptychographic Coherent Diffractive Imaging of Weakly Scattering Specimens New J. Phys. 2010, 12, 035017
47. Edo, T. B.; Batey, D. J.; Maiden, A. M.; Rau, C.; Wagner, U.; Pešić, Z. D.; Waigh, T. A.; Rodenburg, J. M. Sampling in X-Ray Ptychography Phys. Rev. A 2013, 87, 053850
48. Thibault, P.; Dierolf, M.; Menzel, A.; Bunk, O.; David, C.; Pfeiffer, F. High-Resolution Scanning X-ray Diffraction Microscopy Science 2008, 321, 379-382
49. Thibault, P.; Dierolf, M.; Bunk, O.; Menzel, A.; Pfeiffer, F. Probe Retrieval in Ptychographic Coherent Diffractive Imaging Ultramicroscopy 2009, 109, 338-343
50. Thibault, P.; Guizar-Sicairos, M. Maximum-Likelihood Refinement for Coherent Diffraction Imaging New J. Phys. 2012, 14, 063004