Submolecular-scale imaging of α-helices and C-terminal domains of tubulins by frequency modulation atomic force microscopy in liquid

Biophysical Journal

Volumn 101, Issue 5, 2011, Pages 1270-1276

  Asakawa, Hitoshi ^a   Ikegami, Koji ^b   Setou, Mitsutoshi ^b   Watanabe, Naoki ^c   Tsukada, Masaru ^d   Fukuma, Takeshi ^a,e  

^a KANAZAWA UNIVERSITY   (Japan)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c MIZUHO INFORMATION AND RESEARCH INSTITUTE   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TUBULIN;

ANIMAL; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; METHODOLOGY; MOLECULAR IMAGING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SURFACE PROPERTY;

ANIMALS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR IMAGING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PROPERTIES; TUBULIN;

EID: 80052462220     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.07.020     Document Type: Article

References (58)

1. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the α β tubulin dimer by electron crystallography Nature 391 1998 199 203 (Pubitemid 28092482)
2. J. Löwe, and H. Li E. Nogales Refined structure of α β-tubulin at 3.5 A resolution J. Mol. Biol. 313 2001 1045 1057 (Pubitemid 33081900)
3. B. Gigant, and P.A. Curmi M. Knossow The 4 A X-ray structure of a tubulin:stathmin-like domain complex Cell 102 2000 809 816
4. H. Sosa, and D.P. Dias R.A. Milligan A model for the microtubule-Ncd motor protein complex obtained by cryo-electron microscopy and image analysis Cell 90 1997 217 224 (Pubitemid 27329707)
5. M. Kikkawa, Y. Okada, and N. Hirokawa 15 A resolution model of the monomeric kinesin motor, KIF1A Cell 100 2000 241 252 (Pubitemid 30064912)
6. H. Sui, and K.H. Downing Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography Nature 442 2006 475 478 (Pubitemid 44264799)
7. G. Binnig, C.F. Quate, and C. Gerber Atomic force microscope Phys. Rev. Lett. 56 1986 930 933
8. F.J. Giessibl Advances in atomic force microscopy Rev. Mod. Phys. 75 2003 949 983 (Pubitemid 37249573)
9. B. Drake, and C.B. Prater P.K. Hansma Imaging crystals, polymers, and processes in water with the atomic force microscope Science 243 1989 1586 1589
10. J.H. Hoh, and G.E. Sosinsky P.K. Hansma Structure of the extracellular surface of the gap junction by atomic force microscopy Biophys. J. 65 1993 149 163 (Pubitemid 23206048)
11. S. Karrasch, and M. Dolder A. Engel Covalent binding of biological samples to solid supports for scanning probe microscopy in buffer solution Biophys. J. 65 1993 2437 2446 (Pubitemid 24005975)
12. S. Karrasch, and R. Hegerl A. Engel Atomic force microscopy produces faithful high-resolution images of protein surfaces in an aqueous environment Proc. Natl. Acad. Sci. USA 91 1994 836 838 (Pubitemid 24048461)
13. J. Yang, J. Mou, and Z. Shao Molecular resolution atomic force microscopy of soluble proteins in solution Biochim. Biophys. Acta 1199 1994 105 114 (Pubitemid 24080799)
14. F.A. Schabert, C. Henn, and A. Engel Native Escherichia coli OmpF porin surfaces probed by atomic force microscopy Science 268 1995 92 94
15. D.J. Müller, and D. Fotiadis A. Engel Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope Biophys. J. 76 1999 1101 1111 (Pubitemid 29264591)
16. D.J. Müller, and F.A. Schabert A. Engel Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy Biophys. J. 68 1995 1681 1686
17. D.J. Müller, D. Fotiadis, and A. Engel Mapping flexible protein domains at subnanometer resolution with the atomic force microscope FEBS Lett. 430 1998 105 111 (Pubitemid 28307041)
18. P.L. Frederix, and T. Akiyama A. Engel Atomic force bio-analytics Curr. Opin. Chem. Biol. 7 2003 641 647 (Pubitemid 37315802)
19. P.K. Hansma, and J.P. Cleveland V. Elings Tapping mode atomic force microscopy in liquids Appl. Phys. Lett. 64 1994 1738 1740
20. M. Fritz, and M. Radmacher P.K. Hansma Imaging globular and filamentous proteins in physiological buffer solutions with tapping mode atomic force microscopy Langmuir 11 1995 3529 3535
21. S. Kasas, and N.H. Thomson P.K. Hansma Escherichia coli RNA polymerase activity observed using atomic force microscopy Biochemistry 36 1997 461 468 (Pubitemid 27056993)
22. C. Möller, and M. Allen D.J. Müller Tapping-mode atomic force microscopy produces faithful high-resolution images of protein surfaces Biophys. J. 77 1999 1150 1158 (Pubitemid 29362486)
23. D.J. Müller, and H. Janovjak K. Anderson Observing structure, function and assembly of single proteins by AFM Prog. Biophys. Mol. Biol. 79 2002 1 43 (Pubitemid 35249644)
24. G. Kada, F. Kienberger, and P. Hinterdorfer Atomic force microscopy in bionanotechnology Nano Today 3 2008 12 19 (Pubitemid 351298584)
25. D.J. Müller, and Y.F. Dufrêne Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology Nat. Nanotechnol. 3 2008 261 269 (Pubitemid 351668045)
26. N.F. Martínez, and J.R. Lozano R. Garcia Bimodal atomic force microscopy imaging of isolated antibodies in air and liquids Nanotechnology 19 2008 384011 384018
27. D. Martinez-Martin, and E.T. Herruzo R. Garcia Noninvasive protein structural flexibility mapping by bimodal dynamic force microscopy Phys. Rev. Lett. 106 2011 198101 198104
28. F. Moreno-Herrero, and J. Colchero A.M. Baró Atomic force microscopy contact, tapping, and jumping modes for imaging biological samples in liquids Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 69 2004 031915
29. T.R. Albrecht, and P. Grütter D. Ruger Frequency modulation detection using high-Q cantilevers for enhanced force microscope sensitivity J. Appl. Phys. 69 1991 668 673
30. T. Fukuma, and M. Kimura H. Yamada Development of low noise cantilever deflection sensor for multienvironment frequency-modulation atomic force microscopy Rev. Sci. Instrum. 76 2005 053704 053711
31. T. Fukuma, and K. Kobayashi H. Yamada True atomic resolution in liquid by frequency-modulation atomic force microscopy Appl. Phys. Lett. 87 2005 034101 034103
32. B.W. Hoogenboom, and H.J. Hug A. Engel Quantitative dynamic-mode scanning force microscopy in liquid Appl. Phys. Lett. 88 2006 193109 193111
33. M.J. Higgins, and M. Polcik S.P. Jarvis Structured water layers adjacent to biological membranes Biophys. J. 91 2006 2532 2542 (Pubitemid 44511708)
34. T. Fukuma, and A.S. Mostaert S.P. Jarvis Revealing molecular-level surface structure of amyloid fibrils in liquid by means of frequency modulation atomic force microscopy Nanotechnology 19 2008 384010 384015
35. H. Asakawa, and T. Fukuma The molecular-scale arrangement and mechanical strength of phospholipid/cholesterol mixed bilayers investigated by frequency modulation atomic force microscopy in liquid Nanotechnology 20 2009 264008 264014
36. H. Yamada, and K. Kobayashi K. Matsushige Molecular resolution imaging of protein molecules in liquid using frequency modulation atomic force microscopy Appl. Phys. Express 2 2009 95007 95009
37. K. Nagashima, and M. Abe Y. Mori Molecular resolution investigation of tetragonal lysozyme (110) face in liquid by frequency-modulation atomic force microscopy J. Vac. Sci. Technol. B 28 2010 C4C11-C4C14
38. B.W. Hoogenboom, and K. Suda D. Fotiadis The supramolecular assemblies of voltage-dependent anion channels in the native membrane J. Mol. Biol. 370 2007 246 255 (Pubitemid 46829218)
39. K. Ikegami, and R.L. Heier M. Setou Loss of α-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function Proc. Natl. Acad. Sci. USA 104 2007 3213 3218 (Pubitemid 46364139)
40. Y. Konishi, and M. Setou Tubulin tyrosination navigates the kinesin-1 motor domain to axons Nat. Neurosci. 12 2009 559 567
41. K. Ikegami, and M. Setou Unique post-translational modifications in specialized microtubule architecture Cell Struct. Funct. 35 2010 15 22
42. I.A.T. Schaap, and C. Carrasco C.F. Schmidt Elastic response, buckling, and instability of microtubules under radial indentation Biophys. J. 91 2006 1521 1531 (Pubitemid 44174269)
43. K.M. Munson, P.G. Mulugeta, and Z.J. Donhauser Enhanced mechanical stability of microtubules polymerized with a slowly hydrolyzable nucleotide analogue J. Phys. Chem. B 111 2007 5053 5057 (Pubitemid 46854489)
44. C. Elie-Caille, and F. Severin A.A. Hyman Straight GDP-tubulin protofilaments form in the presence of taxol Curr. Biol. 17 2007 1765 1770 (Pubitemid 47577538)
45. H.P. Miller, and L. Wilson Preparation of microtubule protein and purified tubulin from bovine brain by cycles of assembly and disassembly and phosphocellulose chromatography Methods Cell Biol. 95 2010 3 15
46. L. Hamon, and D. Panda D. Pastré Mica surface promotes the assembly of cytoskeletal proteins Langmuir 25 2009 3331 3335
47. N.H. Thomson, and S. Kasas L. Forró Large fluctuations in the disassembly rate of microtubules revealed by atomic force microscopy Ultramicroscopy 97 2003 239 247 (Pubitemid 36683298)
48. I. Arnal, and R.H. Wade How does taxol stabilize microtubules? Curr. Biol. 5 1995 900 908
49. P. Markiewicz, and M.C. Goh Atomic force microscopy probe tip visualization and improvement of images using a simple deconvolution procedure Langmuir 10 1994 5 7
50. S.G. Wolf, G. Mosser, and K.H. Downing Tubulin conformation in zinc-induced sheets and macrotubes J. Struct. Biol. 111 1993 190 199 (Pubitemid 24136646)
51. E. Nogales, and S.G. Wolf K.H. Downing Preservation of 2-D crystals of tubulin for electron crystallography J. Struct. Biol. 115 1995 199 208
52. A. Villasante, and D. Wang N.J. Cowan Six mouse α-tubulin mRNAs encode five distinct isotypes: testis-specific expression of two sister genes Mol. Cell. Biol. 6 1986 2409 2419
53. K.F. Sullivan, and D.W. Cleveland Identification of conserved isotype-defining variable region sequences for four vertebrate β tubulin polypeptide classes Proc. Natl. Acad. Sci. USA 83 1986 4327 4331 (Pubitemid 16057043)
54. T. Luchko, and J.T. Huzil J. Tuszynski Conformational analysis of the carboxy-terminal tails of human β-tubulin isotypes Biophys. J. 94 2008 1971 1982
55. D. Pal, and P. Mahapatra S. Roy Conformational properties of α-tubulin tail peptide: implications for tail-body interaction Biochemistry 40 2001 15512 15519 (Pubitemid 34015178)
56. D. Boucher, and J.C. Larcher P. Denoulet Polyglutamylation of tubulin as a progressive regulator of in vitro interactions between the microtubule-associated protein τ and tubulin Biochemistry 33 1994 12471 12477 (Pubitemid 24340453)
57. J.C. Larcher, and D. Boucher P. Denoulet Interaction of kinesin motor domains with α- and β-tubulin subunits at a τ-independent binding site. Regulation by polyglutamylation J. Biol. Chem. 271 1996 22117 22124 (Pubitemid 26303842)
58. C. Bonnet, and D. Boucher J.C. Larcher Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation J. Biol. Chem. 276 2001 12839 12848