Home LiteratureArticle Details
PMID: 17369416 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Stepwise movements in vesicle transport of HER2 by motor proteins in living cells.

Biophysical journal ·Vol. 92 ·No. 11 ·2007-06-01 ·Pages 4109-20

Watanabe TM, Higuchi H

Abstract

The stepwise movements generated by myosin, dynein, and kinesin were observed in living cells in an attempt to understand the molecular mechanisms of movement within cells. First, the sequential process of the transport of vesicles, including human epidermal factor 2 receptor, after endocytosis was observed for long periods in three dimensions using quantum dots (QDs) and a three-dimensional confocal microscope. QD vesicles, after being endocytosed into the cells, moved along the membrane by transferring actin filaments and were then rapidly transported toward the nucleus along microtubules. Second, the position of vesicles was detected with a precision up to 1.9 nm and 330 micros using a new two-dimensional tracking method. The movement of the QDs transported by myosin VI lying just beneath the cell membrane consisted of 29- and 15-nm steps with a transition phase between these two steps. QD vesicles were then transported toward the nucleus or away from the nucleus toward the cell membrane with successive 8-nm steps. The stepwise movements of these motor proteins in cells were observed using new imaging methods that allowed the molecular mechanisms underlying traffic to and from the membrane to be determined.

MeSH Terms
Cell Line, Tumor Cytoplasmic Vesicles/metabolism Humans Molecular Motor Proteins/physiology Protein Transport/physiology Quantum Dots Receptor, ErbB-2/metabolism
Chemicals
Molecular Motor Proteins Receptor, ErbB-2
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Watanabe Tomonobu M
Biomedical and Engineering Research Organization, Tohoku University, Sendai, Japan.
Higuchi Hideo
References (53)
53 references, click to expand
  1. Isolation and characterization of a new human breast cancer cell line, KPL-4, expressing the Erb B family receptors and interleukin-6.
    Br J Cancer. 1999 Feb;79(5-6):707-17 PMID: 10070858
  2. A contractile activity that closes phagosomes in macrophages.
    J Cell Sci. 1999 Feb;112 ( Pt 3):307-16 PMID: 9885284
  3. Myosin-V is a processive actin-based motor.
    Nature. 1999 Aug 5;400(6744):590-3 PMID: 10448864
  4. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin.
    Mol Biol Cell. 2004 Dec;15(12):5268-82 PMID: 15385631
  5. Myosin VI: cellular functions and motor properties.
    Philos Trans R Soc Lond B Biol Sci. 2004 Dec 29;359(1452):1931-44 PMID: 15647169
  6. A flexible domain is essential for the large step size and processivity of myosin VI.
    Mol Cell. 2005 Feb 18;17(4):603-9 PMID: 15721263
  7. Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity.
    Biophys J. 2005 May;88(5):L30-2 PMID: 15764654
  8. 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
  9. Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors.
    J Cell Biol. 2005 Aug 15;170(4):619-26 PMID: 16103229
  10. Melanosomes transported by myosin-V in Xenopus melanophores perform slow 35 nm steps.
    Biophys J. 2006 Jan 1;90(1):L07-9 PMID: 16284273
  11. Observation of individual microtubule motor steps in living cells with endocytosed quantum dots.
    J Phys Chem B. 2005 Dec 29;109(51):24220-4 PMID: 16375416
  12. Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering.
    Mol Cell. 2006 Feb 3;21(3):331-6 PMID: 16455488
  13. 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
  14. Imaging and tracking of single GFP molecules in solution.
    Biophys J. 2000 Apr;78(4):2170-9 PMID: 10733995
  15. The EGF receptor: a nexus for trafficking and signaling.
    Bioessays. 2000 Aug;22(8):697-707 PMID: 10918300
  16. Myosin-V stepping kinetics: a molecular model for processivity.
    Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9482-6 PMID: 10944217
  17. Unconventional myosins: anchors in the membrane traffic relay.
    Traffic. 2000 Jan;1(1):11-8 PMID: 11208054
  18. Myosin vb is associated with plasma membrane recycling systems.
    Mol Biol Cell. 2001 Jun;12(6):1843-57 PMID: 11408590
  19. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis.
    EMBO J. 2001 Jul 16;20(14):3676-84 PMID: 11447109
  20. Biology of HER2 and its importance in breast cancer.
    Oncology. 2001;61 Suppl 2:1-13 PMID: 11694782
  21. Myosin VI is a processive motor with a large step size.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13655-9 PMID: 11707568
  22. Chemomechanical coupling of the forward and backward steps of single kinesin molecules.
    Nat Cell Biol. 2002 Oct;4(10):790-7 PMID: 12360289
  23. Immunofluorescent labeling of cancer marker Her2 and other cellular targets with semiconductor quantum dots.
    Nat Biotechnol. 2003 Jan;21(1):41-6 PMID: 12459735
  24. Cargo-binding makes a wild-type single-headed myosin-VI move processively.
    Biophys J. 2006 May 15;90(10):3643-52 PMID: 16500969
  25. Recycling endosomes.
    J Cell Sci. 2006 May 1;119(Pt 9):1679-81 PMID: 16636069
  26. Processive movement of single 22S dynein molecules occurs only at low ATP concentrations.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2533-7 PMID: 10706634
  27. The role of the ubiquitination-proteasome pathway in breast cancer: ubiquitin mediated degradation of growth factor receptors in the pathogenesis and treatment of cancer.
    Breast Cancer Res. 2003;5(1):8-15 PMID: 12559039
  28. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization.
    Science. 2003 Jun 27;300(5628):2061-5 PMID: 12791999
  29. Single- and multiple-molecule dynamics of the signaling from H-Ras to cRaf-1 visualized on the plasma membrane of living cells.
    Chemphyschem. 2003 Jul 14;4(7):748-53 PMID: 12901307
  30. Visualizing infection of individual influenza viruses.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9280-5 PMID: 12883000
  31. Alternate fast and slow stepping of a heterodimeric kinesin molecule.
    Nat Cell Biol. 2003 Dec;5(12):1079-82 PMID: 14634664
  32. Kinesin walks hand-over-hand.
    Science. 2004 Jan 30;303(5658):676-8 PMID: 14684828
  33. Quantum dot ligands provide new insights into erbB/HER receptor-mediated signal transduction.
    Nat Biotechnol. 2004 Feb;22(2):198-203 PMID: 14704683
  34. Cytoplasmic dynein functions as a gear in response to load.
    Nature. 2004 Feb 12;427(6975):649-52 PMID: 14961123
  35. Signal transduction and oncogenesis by ErbB/HER receptors.
    Int J Radiat Oncol Biol Phys. 2004 Mar 1;58(3):903-13 PMID: 14967450
  36. A monomeric myosin VI with a large working stroke.
    EMBO J. 2004 Apr 21;23(8):1729-38 PMID: 15044955
  37. Uncoated endocytic vesicles require the unconventional myosin, Myo6, for rapid transport through actin barriers.
    Mol Biol Cell. 2004 May;15(5):2253-63 PMID: 15004223
  38. Regional rheological differences in locomoting neutrophils.
    Am J Physiol Cell Physiol. 2004 Sep;287(3):C603-11 PMID: 15163623
  39. Mechanochemical coupling of two substeps in a single myosin V motor.
    Nat Struct Mol Biol. 2004 Sep;11(9):877-83 PMID: 15286720
  40. Myosin VI walks hand-over-hand along actin.
    Nat Struct Mol Biol. 2004 Sep;11(9):884-7 PMID: 15286724
  41. Tracking kinesin-driven movements with nanometre-scale precision.
    Nature. 1988 Feb 4;331(6155):450-3 PMID: 3123999
  42. Humanization of an anti-p185HER2 antibody for human cancer therapy.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4285-9 PMID: 1350088
  43. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution.
    Nature. 1995 Apr 6;374(6522):555-9 PMID: 7700383
  44. Direct observation of single kinesin molecules moving along microtubules.
    Nature. 1996 Apr 4;380(6573):451-3 PMID: 8602245
  45. Motors and membrane traffic.
    Curr Opin Cell Biol. 1997 Feb;9(1):18-28 PMID: 9013678
  46. Single molecule imaging of fluorophores and enzymatic reactions achieved by objective-type total internal reflection fluorescence microscopy.
    Biochem Biophys Res Commun. 1997 Jun 9;235(1):47-53 PMID: 9196033
  47. Movements of truncated kinesin fragments with a short or an artificial flexible neck.
    Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7275-80 PMID: 9207081
  48. Kinesin hydrolyses one ATP per 8-nm step.
    Nature. 1997 Jul 24;388(6640):386-90 PMID: 9237757
  49. The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions.
    FEBS Lett. 1997 Jun 23;410(1):83-6 PMID: 9247128
  50. Kinesin and dynein superfamily proteins and the mechanism of organelle transport.
    Science. 1998 Jan 23;279(5350):519-26 PMID: 9438838
  51. Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin.
    Cell. 1998 Jan 23;92(2):161-71 PMID: 9458041
  52. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers.
    EMBO J. 1998 Jun 15;17(12):3385-97 PMID: 9628875
  53. ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors.
    J Biol Chem. 1999 Mar 26;274(13):8865-74 PMID: 10085130
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2007-06-01
Epub
2007-00-16
Pages
4109-20
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1868978
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com