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PMID: 17085593 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Two modes of microtubule sliding driven by cytoplasmic dynein.

Shima T, Kon T, Imamula K, Ohkura R, Sutoh K

Abstract

Dynein is a huge multisubunit microtubule (MT)-based motor, whose motor domain resides in the heavy chain. The heavy chain comprises a ring of six AAA (ATPases associated with diverse cellular activities) modules with two slender protruding domains, the tail and stalk. It has been proposed that during the ATP hydrolysis cycle, this tail domain swings against the AAA ring as a lever arm to generate the power stroke. However, there is currently no direct evidence to support the model that the tail swing is tightly linked to dynein motility. To address the question of whether the power stroke of the tail drives MT sliding, we devised an in vitro motility assay using genetically biotinylated cytoplasmic dyneins anchored on a glass surface in the desired orientation with a biotin-streptavidin linkage. Assays on the dyneins with the site-directed biotin tag at eight different locations provided evidence that robust MT sliding is driven by the power stroke of the tail. Furthermore, the assays revealed slow MT sliding independent of dynein orientation on the glass surface, which is mechanically distinct from the sliding driven by the power stroke of the tail.

MeSH Terms
Animals Biological Assay/instrumentation,methods Biotin/metabolism Cytoplasm/metabolism Dictyostelium/chemistry Dyneins/chemistry,genetics,metabolism Microtubules/chemistry,genetics,metabolism,ultrastructure Models, Molecular Protein Structure, Tertiary Recombinant Fusion Proteins/genetics,metabolism Streptavidin/metabolism
Chemicals
Recombinant Fusion Proteins Biotin Streptavidin Dyneins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Shima Tomohiro
Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan.
Kon Takahide
Imamula Kenji
Ohkura Reiko
Sutoh Kazuo
References (52)
52 references, click to expand
  1. Structural comparison of purified dynein proteins with in situ dynein arms.
    J Mol Biol. 1984 Dec 25;180(4):1083-118 PMID: 6241263
  2. Four ATP-binding sites in the midregion of the beta heavy chain of dynein.
    Nature. 1991 Aug 15;352(6336):643-5 PMID: 1830928
  3. Rotation and translocation of microtubules in vitro induced by dyneins from Tetrahymena cilia.
    Cell. 1988 Feb 12;52(3):459-69 PMID: 2964278
  4. AAA domains and organization of the dynein motor unit.
    J Cell Sci. 2000 Jul;113 ( Pt 14):2521-6 PMID: 10862709
  5. Efficient control of gene expression by a tetracycline-dependent transactivator in single Dictyostelium discoideum cells.
    Gene. 2000 Jul 11;252(1-2):71-82 PMID: 10903439
  6. Distinct but overlapping sites within the cytoplasmic dynein heavy chain for dimerization and for intermediate chain and light intermediate chain binding.
    J Biol Chem. 2000 Oct 20;275(42):32769-74 PMID: 10893223
  7. The light chain binding domain of expressed smooth muscle heavy meromyosin acts as a mechanical lever.
    J Biol Chem. 2000 Nov 24;275(47):37167-72 PMID: 10945998
  8. Single-molecule tracking of myosins with genetically engineered amplifier domains.
    Nat Struct Biol. 2001 Mar;8(3):226-9 PMID: 11224566
  9. The motor domain determines the large step of myosin-V.
    Nature. 2002 Jan 10;415(6868):192-5 PMID: 11805840
  10. Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein.
    J Cell Biol. 1992 Dec;119(6):1597-604 PMID: 1469051
  11. Direction of microtubule movement is an intrinsic property of the motor domains of kinesin heavy chain and Drosophila ncd protein.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5209-13 PMID: 8506368
  12. DYNEINS: molecular structure and cellular function.
    Annu Rev Cell Biol. 1994;10:339-72 PMID: 7888180
  13. Rigor and relaxed outer dynein arms in replicas of cryofixed motile flagella.
    J Mol Biol. 1995 Jun 30;250(1):52-63 PMID: 7602596
  14. Targeting of motor proteins.
    Science. 1996 Mar 15;271(5255):1539-44 PMID: 8599110
  15. The neck region of the myosin motor domain acts as a lever arm to generate movement.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4459-64 PMID: 8633089
  16. Phase partition analysis of nucleotide binding to axonemal dynein.
    Biochemistry. 1996 Jul 16;35(28):9204-11 PMID: 8703926
  17. Overexpression of cytoplasmic dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium.
    Mol Biol Cell. 1996 Jun;7(6):935-48 PMID: 8816999
  18. Identification of a microtubule-binding domain in a cytoplasmic dynein heavy chain.
    J Biol Chem. 1997 Aug 8;272(32):19714-8 PMID: 9242627
  19. An extended microtubule-binding structure within the dynein motor domain.
    Nature. 1997 Dec 11;390(6660):636-9 PMID: 9403697
  20. Kinesin and dynein superfamily proteins and the mechanism of organelle transport.
    Science. 1998 Jan 23;279(5350):519-26 PMID: 9438838
  21. Structural characterization of a dynein motor domain.
    J Mol Biol. 1998 Mar 13;276(5):927-37 PMID: 9566197
  22. A single myosin head moves along an actin filament with regular steps of 5.3 nanometres.
    Nature. 1999 Jan 14;397(6715):129-34 PMID: 9923673
  23. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes.
    Genome Res. 1999 Jan;9(1):27-43 PMID: 9927482
  24. Cytoplasmic dynein and dynactin in cell division and intracellular transport.
    Curr Opin Cell Biol. 1999 Feb;11(1):45-53 PMID: 10047518
  25. Interaction mapping of a dynein heavy chain. Identification of dimerization and intermediate-chain binding domains.
    J Biol Chem. 1999 May 28;274(22):15447-53 PMID: 10336435
  26. Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor.
    Nature. 1999 Aug 5;400(6744):586-90 PMID: 10448863
  27. ATP hydrolysis cycle-dependent tail motions in cytoplasmic dynein.
    Nat Struct Mol Biol. 2005 Jun;12(6):513-9 PMID: 15880123
  28. Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement?
    Science. 2005 Jun 3;308(5727):1469-72 PMID: 15817813
  29. A lever-arm rotation drives motility of the minus-end-directed kinesin Ncd.
    Nature. 2006 Feb 16;439(7078):875-8 PMID: 16382238
  30. A flexible linkage between the dynein motor and its cargo.
    J Mol Biol. 2006 Mar 31;357(3):701-6 PMID: 16466743
  31. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5741-5 PMID: 16585530
  32. Myosin-V is a mechanical ratchet.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8680-5 PMID: 16731631
  33. Single-molecule analysis of dynein processivity and stepping behavior.
    Cell. 2006 Jul 28;126(2):335-48 PMID: 16873064
  34. Head-head coordination is required for the processive motion of cytoplasmic dynein, an AAA+ molecular motor.
    J Struct Biol. 2006 Oct;156(1):182-9 PMID: 16677823
  35. The dynein microtubule motor.
    Biochim Biophys Acta. 2000 Mar 17;1496(1):60-75 PMID: 10722877
  36. Retrograde transport by the microtubule-associated protein MAP 1C.
    Nature. 1987 Nov 12-18;330(6144):181-3 PMID: 3670402
  37. Cytoplasmic dynein-associated structures move bidirectionally in vivo.
    J Cell Sci. 2002 Apr 1;115(Pt 7):1453-60 PMID: 11896193
  38. Subunit organization in cytoplasmic dynein subcomplexes.
    Protein Sci. 2002 May;11(5):1239-50 PMID: 11967380
  39. The molecular motor toolbox for intracellular transport.
    Cell. 2003 Feb 21;112(4):467-80 PMID: 12600311
  40. Dynein structure and power stroke.
    Nature. 2003 Feb 13;421(6924):715-8 PMID: 12610617
  41. The third P-loop domain in cytoplasmic dynein heavy chain is essential for dynein motor function and ATP-sensitive microtubule binding.
    Mol Biol Cell. 2003 Apr;14(4):1355-65 PMID: 12686593
  42. Neck length and processivity of myosin V.
    J Biol Chem. 2003 Aug 1;278(31):29201-7 PMID: 12740393
  43. Processivity of the single-headed kinesin KIF1A through biased binding to tubulin.
    Nature. 2003 Jul 31;424(6948):574-7 PMID: 12891363
  44. Rotation of the stalk/neck and one head in a new crystal structure of the kinesin motor protein, Ncd.
    EMBO J. 2003 Oct 15;22(20):5382-9 PMID: 14532111
  45. The structure of dynein-c by negative stain electron microscopy.
    J Struct Biol. 2004 Apr-May;146(1-2):205-16 PMID: 15037251
  46. A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive the robust sliding of microtubules.
    J Biol Chem. 2004 May 28;279(22):22799-802 PMID: 15051717
  47. Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein.
    Biochemistry. 2004 Sep 7;43(35):11266-74 PMID: 15366936
  48. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  49. Purification and assay of microtubule-associated proteins (MAPs).
    Methods Enzymol. 1982;85 Pt B:409-16 PMID: 7121279
  50. Substructure of the outer dynein arm.
    J Cell Biol. 1982 Dec;95(3):798-815 PMID: 6218174
  51. The sodium ion translocating oxalacetate decarboxylase of Klebsiella pneumoniae. Sequence of the biotin-containing alpha-subunit and relationship to other biotin-containing enzymes.
    J Biol Chem. 1988 Jul 15;263(20):9640-5 PMID: 2454915
  52. Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain.
    Nature. 1991 Aug 15;352(6336):640-3 PMID: 1830927
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-11-21
Epub
2006-00-03
Pages
17736-40
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1634414
Subset
IM
Corrections
CommentIn
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