DOI: 10.1083/jcb.137.1.113. Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules

Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules

10.1083/jcb.137.1.113

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Microtubules facilitate the maturation of phagosomes by favoring their interactions with endocytic compartments. Here, we show that phagosomes move within cells along tracks of several microns centrifugally and centripetally in a pH- and microtubuledependent manner. Phagosome movement was reconstituted in vitro and required energy, cytosol and membrane proteins of this organelle. The activity or presence of these phagosome proteins was regulated as the organelle matured, with “late” phagosomes moving threefold more frequently than “early” ones. The majority of moving phagosomes were minus-end directed; the remainder moved towards microtubule plus-ends and a small subset moved bi-directionally. Minus-end movement showed pharmacological characteristics expected for dyneins, was inhibited by immunodepletion of cytoplasmic dynein and could be restored by addition of cytoplasmic dynein. Plus-end movement displayed pharmacological properties of kinesin, was inhibited partially by immunodepletion of kinesin and fully by addition of an anti-kinesin IgG. Immunodepletion of dynactin, a dynein-activating complex, inhibited only minus-end directed motility. Evidence is provided for a dynactin-associated kinase required for dyneinmediated vesicle transport. Movement in both directions was inhibited by peptide fragments from kinectin (a putative kinesin membrane receptor), derived from the region to which a motility-blocking antibody binds. Polypeptide subunits from these microtubule-based motility factors were detected on phagosomes by immunoblotting or immunoelectron microscopy. This is the first study using a single in vitro system that describes the roles played by kinesin, kinectin, cytoplasmic dynein, and dynactin in the microtubule-mediated movement of a purified membrane organelle.

Bibliography

Blocker, A., Severin, F. F., Burkhardt, J. K., Bingham, J. B., Yu, H., Olivo, J.-C., Schroer, T. A., Hyman, A. A., & Griffiths, G. (1997). Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules. The Journal of Cell Biology, 137(1), 113â129.

Authors 9

Ariel Blocker (first)
Fedor F. Severin (additional)
Janis K. Burkhardt (additional)
James B. Bingham (additional)
Hanry Yu (additional)
Jean-Christophe Olivo (additional)
Trina A. Schroer (additional)
Anthony A. Hyman (additional)
Gareth Griffiths (additional)

References 107 Referenced 197

10.1083/jcb.128.5.879 / J Cell Biol / Protein phosphatase 1 regulates the cytoplasmic dynein-driven formation of endoplasmic reticulum networks in vitro by Allan (1995)
10.1006/scdb.1996.0043 / Semin Cell Biol / Role of motor proteins in organizing the endoplasmic reticulum and Golgi apparatus by Allan (1996)
10.1083/jcb.113.2.347 / J Cell Biol / Cell cycle control of microtuble-based membrane transport and tubule formation in vitro by Allan (1991)
10.1083/jcb.123.6.1373 / J Cell Biol / Cytoplasmic dynein-dependent vesicular transport from early to late endosomes by Aniento (1993)
10.1038/348346a0 / Nature (Lond) / Force generation of organelle transport measured in vivo by an infrared laser trap by Ashkin (1990)
10.1016/0092-8674(79)90057-6 / Cell / Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinctive phenotypes of differentiation by Beug (1979)
{'key': '2023072822543385400_B7'}
10.1074/jbc.271.7.3803 / J Biol Chem / MAP-dependent binding of phagosomes to microtubules by Blocker (1996)
{'key': '2023072822543385400_B9'}
10.1016/0092-8674(90)90117-W / Cell / Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells by Bomsel (1990)
10.1038/317073a0 / Nature (Lond) / A novel brain ATPase with properties expected for the fast axonal transport motor by Brady (1985)
10.1073/pnas.87.3.1061 / Proc Natl Acad Sci USA / A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm by Brady (1990)
10.1242/jcs.104.1.151 / J Cell Sci / Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro by Burkhardt (1993)
10.1083/jcb.102.6.2023 / J Cell Biol / Dynamics of microtubule depolymerization in monocytes by Cassimeris (1986)
10.1084/jem.158.2.477 / J Exp Med / Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements by D'Arcy Hart, P., M.R. Young, M.M. Jorgan, W.J. Perkins, and M.J. Geisow (1983)
10.1083/jcb.128.1.1 / J Cell Biol / A new role of motor proteins as couplers to depolymerizing microtubules by Desai (1995)
10.1083/jcb.124.5.677 / J Cell Biol / Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus by Desjardins (1994)
10.1016/S0021-9258(18)31620-X / J Biol Chem / Molecular characterization of phagosomes by Desjardins (1994)
10.1083/jcb.127.6.1671 / J Cell Biol / Differential phosphorylation in vivoof cytoplasmic dynein associated with anterogradely moving organelles by Dillman III, J.F., and K.K. Pfister (1994)
10.1083/jcb.132.4.617 / J Cell Biol / Molecular characterisation of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis by Echeverri (1996)
10.1083/jcb.127.4.1021 / J Cell Biol / Kinesin-mediated organelle translocation revealed by specific cellular manipulations by Feiguin (1994)
10.1091/mbc.6.2.161 / Mol Biol Cell / Molecular cloning and characterization of human kinectin by Fütterer (1995)
10.1038/331450a0 / Nature (Lond) / Tracking kinesin-driven movements with nanometer-scale precision by Gelles (1988)
10.1073/pnas.75.5.2220 / Proc Natl Acad Sci USA / Potent inhibition of dynein andenosintriphophatase and of the motility of cilia and sperm flagella by vanadate by Gibbons (1978)
10.1038/373671a0 / Nature (Lond) / Pathway of processive ATP hydrolysis by kinesin by Gilbert (1995)
10.1083/jcb.115.6.1639 / J Cell Biol / Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein by Gill (1991)
10.1073/pnas.70.10.2916 / Proc Natl Acad Sci USA / Mechanisms of lysosomal enzyme release from human leukocytes: microtubule assembly and membrane fusion induced by a component of complement by Goldstein (1973)
{'key': '2023072822543385400_B28'}
10.1083/jcb.108.4.1301 / J Cell Biol / Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle function in vitro by Gruenberg (1989)
10.1002/bies.950161007 / BioEssays / Regulation of organelle transport: lessons from color change in fish by Haimo (1994)
10.1242/jcs.106.3.955 / J Cell Sci / Regulation of vesicle transport in CV-1 cells and extracts by Hamm-Alvarez (1993)
10.1083/jcb.108.3.855 / J Cell Biol / Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH by Heuser (1989)
10.1016/0962-8924(96)10003-9 / Trends Cell Biol / Organelle transport along microtubules-the role of KIFs by Hirokawa (1996)
10.1016/0092-8674(89)90691-0 / Cell / Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration by Hirokawa (1989)
10.1083/jcb.114.2.295 / J Cell Biol / Kinesin associates with anterogradely transported membranous organelles in vivo by Hirokawa (1991)
10.1083/jcb.111.3.1027 / J Cell Biol / Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported organelles in vivo by Hirokawa (1990)
10.1083/jcb.108.6.2335 / J Cell Biol / The distribution, abundance and subcellular localization of kinesin by Hollenbeck (1989)
10.1111/j.1471-4159.1993.tb03513.x / J Neurochem / Phosphorylation of neuronal kinesin heavy and light chains in vivo by Hollenbeck (1993)
10.1038/346864a0 / Nature (Lond) / Radial extension of macrophage tubular lysosomes supported by kinesin by Hollenbeck (1990)
10.1146/annurev.cb.10.110194.002011 / Annu Rev Cell Biol / Dyneins: molecular structure and cellular function by Holzbaur (1994)
10.1038/351579a0 / Nature (Lond) / Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. by Holzbaur (1991)
10.1038/346335a0 / Nature (Lond) / Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum by Hopkins (1990)
{'key': '2023072822543385400_B43'}
10.1038/351206a0 / Nature (Lond) / Two different microtubule-based motor activities with opposite polarities in kinetochores by Hyman (1991)
10.1016/0076-6879(91)96041-O / Methods Enzymol / Preparation of modified tubulins by Hyman (1991)
10.1083/jcb.107.6.2657 / J Cell Biol / Inhibition of kinesin-driven motility by monoclonal antibodies to kinesin heavy chains by Ingold (1988)
10.1242/jcs.107.1.145 / J Cell Sci / Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment by Jahraus (1994)
10.1074/jbc.270.48.28806 / J Biol Chem / Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex by Karki (1995)
10.1242/jcs.95.3.433 / J Cell Sci / Plasticity of the tubular lysosomal compartment in macrophages by Knapp (1990)
10.1002/j.1460-2075.1986.tb04306.x / EMBO (Eur Mol Biol Organ) J / Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein, block its transport to the cell surface by Kreis (1986)
10.1126/science.7892610 / Science (Wash DC) / Kinectin, an essential anchor for kinesin-driven motility by Kumar (1995)
10.1002/j.1460-2075.1988.tb03269.x / EMBO (Eur Mol Biol Organ) J / Identification and characterization of p59 fyn(a src-like protein kinase) in normal and polyoma virus transformed cells by Kypta (1988)
10.1038/227680a0 / Nature (Lond) / Cleavage of structural proteins during the assembly of the heads of bacteriophage T4 by Laemmli (1970)
10.1038/316645a0 / Nature (Lond) / Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP by Lasek (1985)
10.1002/cm.970230104 / Cell Motil Cytoskeleton / Association of kinesin with characterized membrane-bound organelles by Leopold (1992)
10.1083/jcb.127.4.1009 / J Cell Biol / Cytoplasmic dynein undergoes intracellular redistribution concomitant with phosphorylation of the heavy chain in response to serum starvation and okadaic acid by Lin (1994)
10.1242/jcs.101.1.125 / J Cell Sci / Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells by Lin (1992)
10.1016/0092-8674(87)90157-7 / Cell / Identification of a microtubule-based motor in the nematode C. elegans. by Lye (1987)
10.1016/S0021-9258(17)32291-3 / J Biol Chem / Regulation of kinesin activity by phosphorylation of kinesinassociated proteins by McIlvain (1994)
10.1016/S0021-9258(18)83300-2 / J Biol Chem / Enzymes for microtubule-dependent motility by McIntosh (1989)
10.1073/pnas.91.15.7212 / Proc Natl Acad Sci USA / KAR3-encoded kinesin is a minus-enddirected motor that functions with centromere binding proteins (CBF3) on an in vitroyeast kinetochore by Middleton (1994)
10.1083/jcb.86.1.304 / J Cell Biol / The membrane proteins of the vacuolar system I. Analysis by a novel method of intralysosomal iodination by Muller (1980)
10.1083/jcb.133.3.585 / J Cell Biol / Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport by Niclas (1996)
10.1038/330181a0 / Nature (Lond) / Retrograde transport by the microtubule-associated protein MAP1C by Paschal (1987)
10.1016/S0021-9258(18)82472-3 / J Biol Chem / Characterization of a 50-kDa polypeptide in cytoplasmic dynein preparations reveals a complex with p150Gluedand a novel actin by Paschal (1993)
10.1083/jcb.113.2.261 / J Cell Biol / pH-induced microtubule-dependent redistribution of late endosomes in neuronal and epithelial cells by Parton (1991)
10.1084/jem.142.4.903 / J Exp Med / Phagolysosome formation in normal and colchicine treated macrophages by Pesanti (1975)
10.1038/345263a0 / Nature (Lond) / Cytoplasmic dynein is localized to kinetochores during mitosis by Pfarr (1990)
10.1016/0092-8674(92)90240-D / Cell / CLIP-170 links endocytic vesicles to microtubules by Pierre (1992)
10.1016/S0021-9258(18)48468-2 / J Biol Chem / Transport of phagosomal components to an endosomal compartment by Pitt (1992)
10.1172/JCI116077 / J Clin Invest / Alterations in the protein composition of maturing phagosomes by Pitt (1992)
10.1016/0962-8924(96)10017-9 / Trends Cell Biol / CLIPs for organelle-microtubule interactions by Rickard (1996)
10.1083/jcb.126.6.1455 / J Cell Biol / Microtubule dynamics in fish melanophores by Rodionov (1994)
10.1083/jcb.134.2.349 / J Cell Biol / Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesinmediated transport by Rodriguez (1996)
10.1016/0092-8674(86)90821-4 / Cell / Bidirectional pigment granule movements of melanophores are regulated by protein phosphorylation and dephosphorylation by Rozdzial (1986)
10.1016/S0021-9258(18)35926-X / J Biol Chem / The phophorylation of kinesin regulates its binding to synaptic vesicles by Sato-Yoshitake (1992)
10.1083/jcb.126.2.403 / J Cell Biol / Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin by Schafer (1994)
10.1016/S0021-9258(18)55247-9 / J Biol Chem / Motor protein-independent binding of endocytic carrier vesicles to microtubules in vitro by Scheel (1991)
10.1073/pnas.86.5.1548 / Proc Natl Acad Sci USA / Dynein is the motor for retrograde axonal transport of organelles by Schnapp (1989)
10.1016/0955-0674(94)90118-X / Curr Opin Cell Biol / Structure, function and regulation of cytoplasmic dynein by Schroer (1994)
10.1006/scdb.1996.0041 / Sem Cell Dev Biol / Structure and function of dynactin by Schroer (1996)
10.1083/jcb.115.5.1309 / J Cell Biol / Two activators of microtubule-based vesicle transport by Schroer (1991)
10.1083/jcb.107.5.1785 / J Cell Biol / The role of kinesin and other soluble factors in organelle movement along microtubules by Schroer (1988)
10.1016/0092-8674(89)90627-2 / Cell / Cytoplasmic dynein is a minus-end directed motor for membranous organelles by Schroer (1989)
10.1016/0014-5793(91)80445-9 / FEBS Lett / MAP2mediated binding of chromaffin granules to microtubules by Severin (1991)
10.1006/scdb.1996.0042 / Sem Cell Dev Biol / Regulation of kinesin and cytoplasmic dyneindriven organelle motility by Sheetz (1996)
10.1083/jcb.112.6.1189 / J Cell Biol / Nucleotide specificity of the enzymatic and motile activities of dynein, kinesin and heavy meromyosin by Shimizu (1991)
{'key': '2023072822543385400_B88'}
10.1038/345266a0 / Nature (Lond) / Localization of cytoplasmic dynein to mitotic spindles and the kinetochores by Steuer (1990)
10.1172/JCI106664 / J Clin Invest / Vesicles and properties of phagocytic vesicles from polymorphonuclear leukocytes by Stossel (1971)
10.1073/pnas.84.7.1921 / Proc Natl Acad Sci USA / Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules by Swanson (1987)
10.1242/jcs.108.5.1883 / J Cell Sci / Identification and molecular evolution of new dynein-like protein sequences in rat brain by Tanaka (1995)
10.1242/jcs.94.1.143 / J Cell Sci / Transport of phagosomes in mouse peritoneal macrophages by Toyohara (1989)
10.1083/jcb.118.5.1121 / J Cell Biol / Kinectin, a major kinesin-binding protein on the ER by Toyoshima (1992)
10.1083/jcb.133.4.831 / J Cell Biol / Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles by Vaisberg (1996)
10.1083/jcb.123.4.849 / J Cell Biol / Cytoplasmic dynein plays a role in mammalian mitotic spindle formation by Vaisberg (1993)
10.1146/annurev.cb.03.110187.002023 / Annu Rev Cell Biol / Intracellular transport using microtubule-based motors by Vale (1987)
10.1016/S0092-8674(94)90402-2 / Cell / Getting a grip on myosin by Vale (1994)
10.1083/jcb.119.6.1589 / J Cell Biol / Directional instability of microtubule transport in the presence of kinesin and dynein, two opposite polarity motor proteins by Vale (1992)
10.1016/0092-8674(85)90159-X / Cell / Organelle, bead and microtubule translocations promoted by soluble factors from the squid giant axon by Vale (1985)
10.1016/S0092-8674(85)80099-4 / Cell / Identification of a novel forcegenerating protein, kinesin, involved in microtubule-based motility by Vale (1985)
10.1016/0092-8674(89)90614-4 / Cell / One-dimensional diffusion of microtubules bound to flagellar dynein by Vale (1989)
{'key': '2023072822543385400_B103'}
10.1016/S0006-3495(95)80071-8 / Biophys J / Single cytoplasmic dynein molecules movements: characterization and comparison with kinesin by Wang (1995)
10.1074/jbc.271.2.1153 / J Biol Chem / The product of the Drosophila gene, Glued, is the functional homologue of the p150Gluedcomponent of the vertebrate dynactin complex by Waterman-Storer (1996)
10.1083/jcb.43.1.90 / J Cell Biol / Phagocytosis of latex beads by Acanthamoeba castellanii(NEFF). III Isolation of the phagocytic vesicles and their membranes by Wetzel (1969)
10.1091/mbc.6.2.171 / Mol Cell Biol / Characterization of kinectin, a kinesin-binding protein: primary sequence and N-terminal topogenic signal analysis by Yu (1995)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 6:55 p.m.)
Indexed	3 weeks ago (Aug. 7, 2025, 5:21 p.m.)
Issued	28 years, 4 months ago (April 7, 1997)
Published	28 years, 4 months ago (April 7, 1997)
Published Online	28 years, 4 months ago (April 7, 1997)
Published Print	28 years, 4 months ago (April 7, 1997)

Funders 0

None

BibTeX

@article{Blocker_1997, title={Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules}, volume={137}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.137.1.113}, DOI={10.1083/jcb.137.1.113}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Blocker, Ariel and Severin, Fedor F. and Burkhardt, Janis K. and Bingham, James B. and Yu, Hanry and Olivo, Jean-Christophe and Schroer, Trina A. and Hyman, Anthony A. and Griffiths, Gareth}, year={1997}, month=apr, pages={113–129} }

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  "abstract": "<jats:p>Microtubules facilitate the maturation of phagosomes by favoring their interactions with endocytic compartments. Here, we show that phagosomes move within cells along tracks of several microns centrifugally and centripetally in a pH- and microtubuledependent manner. Phagosome movement was reconstituted in vitro and required energy, cytosol and membrane proteins of this organelle. The activity or presence of these phagosome proteins was regulated as the organelle matured, with \u201clate\u201d phagosomes moving threefold more frequently than \u201cearly\u201d ones. The majority of moving phagosomes were minus-end directed; the remainder moved towards microtubule plus-ends and a small subset moved bi-directionally. Minus-end movement showed pharmacological characteristics expected for dyneins, was inhibited by immunodepletion of cytoplasmic dynein and could be restored by addition of cytoplasmic dynein. Plus-end movement displayed pharmacological properties of kinesin, was inhibited partially by immunodepletion of kinesin and fully by addition of an anti-kinesin IgG. Immunodepletion of dynactin, a dynein-activating complex, inhibited only minus-end directed motility. Evidence is provided for a dynactin-associated kinase required for dyneinmediated vesicle transport. Movement in both directions was inhibited by peptide fragments from kinectin (a putative kinesin membrane receptor), derived from the region to which a motility-blocking antibody binds. Polypeptide subunits from these microtubule-based motility factors were detected on phagosomes by immunoblotting or immunoelectron microscopy. This is the first study using a single in vitro system that describes the roles played by kinesin, kinectin, cytoplasmic dynein, and dynactin in the microtubule-mediated movement of a purified membrane organelle.</jats:p>",
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      "first-page": "879",
      "DOI": "10.1083/jcb.128.5.879",
      "article-title": "Protein phosphatase 1 regulates the cytoplasmic dynein-driven formation of endoplasmic reticulum networks in vitro",
      "volume": "128",
      "author": "Allan",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B2",
      "doi-asserted-by": "crossref",
      "first-page": "335",
      "DOI": "10.1006/scdb.1996.0043",
      "article-title": "Role of motor proteins in organizing the endoplasmic reticulum and Golgi apparatus",
      "volume": "7",
      "author": "Allan",
      "year": "1996",
      "journal-title": "Semin Cell Biol"
    },
    {
      "key": "2023072822543385400_B3",
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      "first-page": "347",
      "DOI": "10.1083/jcb.113.2.347",
      "article-title": "Cell cycle control of microtuble-based membrane transport and tubule formation in vitro",
      "volume": "113",
      "author": "Allan",
      "year": "1991",
      "journal-title": "J Cell Biol"
    },
    {
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      "first-page": "1373",
      "DOI": "10.1083/jcb.123.6.1373",
      "article-title": "Cytoplasmic dynein-dependent vesicular transport from early to late endosomes",
      "volume": "123",
      "author": "Aniento",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
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      "first-page": "346",
      "DOI": "10.1038/348346a0",
      "article-title": "Force generation of organelle transport measured in vivo by an infrared laser trap",
      "volume": "348",
      "author": "Ashkin",
      "year": "1990",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B6",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1016/0092-8674(79)90057-6",
      "article-title": "Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinctive phenotypes of differentiation",
      "volume": "18",
      "author": "Beug",
      "year": "1979",
      "journal-title": "Cell"
    },
    {
      "key": "2023072822543385400_B7"
    },
    {
      "key": "2023072822543385400_B8",
      "doi-asserted-by": "crossref",
      "first-page": "3803",
      "DOI": "10.1074/jbc.271.7.3803",
      "article-title": "MAP-dependent binding of phagosomes to microtubules",
      "volume": "271",
      "author": "Blocker",
      "year": "1996",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072822543385400_B9"
    },
    {
      "key": "2023072822543385400_B10",
      "doi-asserted-by": "crossref",
      "first-page": "719",
      "DOI": "10.1016/0092-8674(90)90117-W",
      "article-title": "Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells",
      "volume": "62",
      "author": "Bomsel",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072822543385400_B11",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1038/317073a0",
      "article-title": "A novel brain ATPase with properties expected for the fast axonal transport motor",
      "volume": "317",
      "author": "Brady",
      "year": "1985",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B12",
      "doi-asserted-by": "crossref",
      "first-page": "1061",
      "DOI": "10.1073/pnas.87.3.1061",
      "article-title": "A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm",
      "volume": "87",
      "author": "Brady",
      "year": "1990",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822543385400_B13",
      "doi-asserted-by": "crossref",
      "first-page": "151",
      "DOI": "10.1242/jcs.104.1.151",
      "article-title": "Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro",
      "volume": "104",
      "author": "Burkhardt",
      "year": "1993",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822543385400_B14",
      "doi-asserted-by": "crossref",
      "first-page": "2023",
      "DOI": "10.1083/jcb.102.6.2023",
      "article-title": "Dynamics of microtubule depolymerization in monocytes",
      "volume": "102",
      "author": "Cassimeris",
      "year": "1986",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B15",
      "doi-asserted-by": "crossref",
      "first-page": "477",
      "DOI": "10.1084/jem.158.2.477",
      "article-title": "Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements",
      "volume": "158",
      "author": "D'Arcy Hart, P., M.R. Young, M.M. Jorgan, W.J. Perkins, and M.J. Geisow",
      "year": "1983",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072822543385400_B16",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1083/jcb.128.1.1",
      "article-title": "A new role of motor proteins as couplers to depolymerizing microtubules",
      "volume": "128",
      "author": "Desai",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B17",
      "doi-asserted-by": "crossref",
      "first-page": "677",
      "DOI": "10.1083/jcb.124.5.677",
      "article-title": "Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus",
      "volume": "124",
      "author": "Desjardins",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B18",
      "doi-asserted-by": "crossref",
      "first-page": "32194",
      "DOI": "10.1016/S0021-9258(18)31620-X",
      "article-title": "Molecular characterization of phagosomes",
      "volume": "269",
      "author": "Desjardins",
      "year": "1994",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072822543385400_B19",
      "doi-asserted-by": "crossref",
      "first-page": "1671",
      "DOI": "10.1083/jcb.127.6.1671",
      "article-title": "Differential phosphorylation in vivoof cytoplasmic dynein associated with anterogradely moving organelles",
      "volume": "127",
      "author": "Dillman III, J.F., and K.K. Pfister",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B20",
      "doi-asserted-by": "crossref",
      "first-page": "617",
      "DOI": "10.1083/jcb.132.4.617",
      "article-title": "Molecular characterisation of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis",
      "volume": "132",
      "author": "Echeverri",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B21",
      "doi-asserted-by": "crossref",
      "first-page": "1021",
      "DOI": "10.1083/jcb.127.4.1021",
      "article-title": "Kinesin-mediated organelle translocation revealed by specific cellular manipulations",
      "volume": "127",
      "author": "Feiguin",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B22",
      "doi-asserted-by": "crossref",
      "first-page": "161",
      "DOI": "10.1091/mbc.6.2.161",
      "article-title": "Molecular cloning and characterization of human kinectin",
      "volume": "6",
      "author": "F\u00fctterer",
      "year": "1995",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072822543385400_B23",
      "doi-asserted-by": "crossref",
      "first-page": "450",
      "DOI": "10.1038/331450a0",
      "article-title": "Tracking kinesin-driven movements with nanometer-scale precision",
      "volume": "331",
      "author": "Gelles",
      "year": "1988",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B24",
      "doi-asserted-by": "crossref",
      "first-page": "2220",
      "DOI": "10.1073/pnas.75.5.2220",
      "article-title": "Potent inhibition of dynein andenosintriphophatase and of the motility of cilia and sperm flagella by vanadate",
      "volume": "79",
      "author": "Gibbons",
      "year": "1978",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822543385400_B25",
      "doi-asserted-by": "crossref",
      "first-page": "671",
      "DOI": "10.1038/373671a0",
      "article-title": "Pathway of processive ATP hydrolysis by kinesin",
      "volume": "373",
      "author": "Gilbert",
      "year": "1995",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B26",
      "doi-asserted-by": "crossref",
      "first-page": "1636",
      "DOI": "10.1083/jcb.115.6.1639",
      "article-title": "Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein",
      "volume": "115",
      "author": "Gill",
      "year": "1991",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B27",
      "doi-asserted-by": "crossref",
      "first-page": "2916",
      "DOI": "10.1073/pnas.70.10.2916",
      "article-title": "Mechanisms of lysosomal enzyme release from human leukocytes: microtubule assembly and membrane fusion induced by a component of complement",
      "volume": "70",
      "author": "Goldstein",
      "year": "1973",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822543385400_B28"
    },
    {
      "key": "2023072822543385400_B29",
      "doi-asserted-by": "crossref",
      "first-page": "1301",
      "DOI": "10.1083/jcb.108.4.1301",
      "article-title": "Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle function in vitro",
      "volume": "108",
      "author": "Gruenberg",
      "year": "1989",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B30",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1002/bies.950161007",
      "article-title": "Regulation of organelle transport: lessons from color change in fish",
      "volume": "16",
      "author": "Haimo",
      "year": "1994",
      "journal-title": "BioEssays"
    },
    {
      "key": "2023072822543385400_B31",
      "doi-asserted-by": "crossref",
      "first-page": "955",
      "DOI": "10.1242/jcs.106.3.955",
      "article-title": "Regulation of vesicle transport in CV-1 cells and extracts",
      "volume": "106",
      "author": "Hamm-Alvarez",
      "year": "1993",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822543385400_B32",
      "doi-asserted-by": "crossref",
      "first-page": "855",
      "DOI": "10.1083/jcb.108.3.855",
      "article-title": "Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH",
      "volume": "108",
      "author": "Heuser",
      "year": "1989",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B33",
      "doi-asserted-by": "crossref",
      "first-page": "135",
      "DOI": "10.1016/0962-8924(96)10003-9",
      "article-title": "Organelle transport along microtubules-the role of KIFs",
      "volume": "6",
      "author": "Hirokawa",
      "year": "1996",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2023072822543385400_B34",
      "doi-asserted-by": "crossref",
      "first-page": "867",
      "DOI": "10.1016/0092-8674(89)90691-0",
      "article-title": "Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration",
      "volume": "56",
      "author": "Hirokawa",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2023072822543385400_B35",
      "doi-asserted-by": "crossref",
      "first-page": "295",
      "DOI": "10.1083/jcb.114.2.295",
      "article-title": "Kinesin associates with anterogradely transported membranous organelles in vivo",
      "volume": "114",
      "author": "Hirokawa",
      "year": "1991",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B36",
      "doi-asserted-by": "crossref",
      "first-page": "1027",
      "DOI": "10.1083/jcb.111.3.1027",
      "article-title": "Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported organelles in vivo",
      "volume": "111",
      "author": "Hirokawa",
      "year": "1990",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B37",
      "doi-asserted-by": "crossref",
      "first-page": "2335",
      "DOI": "10.1083/jcb.108.6.2335",
      "article-title": "The distribution, abundance and subcellular localization of kinesin",
      "volume": "108",
      "author": "Hollenbeck",
      "year": "1989",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B38",
      "doi-asserted-by": "crossref",
      "first-page": "2265",
      "DOI": "10.1111/j.1471-4159.1993.tb03513.x",
      "article-title": "Phosphorylation of neuronal kinesin heavy and light chains in vivo",
      "volume": "60",
      "author": "Hollenbeck",
      "year": "1993",
      "journal-title": "J Neurochem"
    },
    {
      "key": "2023072822543385400_B39",
      "doi-asserted-by": "crossref",
      "first-page": "864",
      "DOI": "10.1038/346864a0",
      "article-title": "Radial extension of macrophage tubular lysosomes supported by kinesin",
      "volume": "346",
      "author": "Hollenbeck",
      "year": "1990",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B40",
      "doi-asserted-by": "crossref",
      "first-page": "339",
      "DOI": "10.1146/annurev.cb.10.110194.002011",
      "article-title": "Dyneins: molecular structure and cellular function",
      "volume": "10",
      "author": "Holzbaur",
      "year": "1994",
      "journal-title": "Annu Rev Cell Biol"
    },
    {
      "key": "2023072822543385400_B41",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1038/351579a0",
      "article-title": "Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued.",
      "volume": "351",
      "author": "Holzbaur",
      "year": "1991",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B42",
      "doi-asserted-by": "crossref",
      "first-page": "335",
      "DOI": "10.1038/346335a0",
      "article-title": "Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum",
      "volume": "346",
      "author": "Hopkins",
      "year": "1990",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B43"
    },
    {
      "key": "2023072822543385400_B44",
      "doi-asserted-by": "crossref",
      "first-page": "206",
      "DOI": "10.1038/351206a0",
      "article-title": "Two different microtubule-based motor activities with opposite polarities in kinetochores",
      "volume": "351",
      "author": "Hyman",
      "year": "1991",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B45",
      "doi-asserted-by": "crossref",
      "first-page": "478",
      "DOI": "10.1016/0076-6879(91)96041-O",
      "article-title": "Preparation of modified tubulins",
      "volume": "196",
      "author": "Hyman",
      "year": "1991",
      "journal-title": "Methods Enzymol"
    },
    {
      "key": "2023072822543385400_B46",
      "doi-asserted-by": "crossref",
      "first-page": "2657",
      "DOI": "10.1083/jcb.107.6.2657",
      "article-title": "Inhibition of kinesin-driven motility by monoclonal antibodies to kinesin heavy chains",
      "volume": "107",
      "author": "Ingold",
      "year": "1988",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B47",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1242/jcs.107.1.145",
      "article-title": "Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment",
      "volume": "107",
      "author": "Jahraus",
      "year": "1994",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822543385400_B48",
      "doi-asserted-by": "crossref",
      "first-page": "28806",
      "DOI": "10.1074/jbc.270.48.28806",
      "article-title": "Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex",
      "volume": "270",
      "author": "Karki",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072822543385400_B49",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1242/jcs.95.3.433",
      "article-title": "Plasticity of the tubular lysosomal compartment in macrophages",
      "volume": "95",
      "author": "Knapp",
      "year": "1990",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822543385400_B50",
      "doi-asserted-by": "crossref",
      "first-page": "931",
      "DOI": "10.1002/j.1460-2075.1986.tb04306.x",
      "article-title": "Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein, block its transport to the cell surface",
      "volume": "5",
      "author": "Kreis",
      "year": "1986",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072822543385400_B51",
      "doi-asserted-by": "crossref",
      "first-page": "1834",
      "DOI": "10.1126/science.7892610",
      "article-title": "Kinectin, an essential anchor for kinesin-driven motility",
      "volume": "267",
      "author": "Kumar",
      "year": "1995",
      "journal-title": "Science (Wash DC)"
    },
    {
      "key": "2023072822543385400_B52",
      "doi-asserted-by": "crossref",
      "first-page": "3837",
      "DOI": "10.1002/j.1460-2075.1988.tb03269.x",
      "article-title": "Identification and characterization of p59\u2009\u2009fyn(a src-like protein kinase) in normal and polyoma virus transformed cells",
      "volume": "7",
      "author": "Kypta",
      "year": "1988",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072822543385400_B53",
      "doi-asserted-by": "crossref",
      "first-page": "680",
      "DOI": "10.1038/227680a0",
      "article-title": "Cleavage of structural proteins during the assembly of the heads of bacteriophage T4",
      "volume": "227",
      "author": "Laemmli",
      "year": "1970",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B54",
      "doi-asserted-by": "crossref",
      "first-page": "645",
      "DOI": "10.1038/316645a0",
      "article-title": "Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP",
      "volume": "316",
      "author": "Lasek",
      "year": "1985",
      "journal-title": "Nature (Lond)"
    },
    {
      "key": "2023072822543385400_B55",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1002/cm.970230104",
      "article-title": "Association of kinesin with characterized membrane-bound organelles",
      "volume": "23",
      "author": "Leopold",
      "year": "1992",
      "journal-title": "Cell Motil Cytoskeleton"
    },
    {
      "key": "2023072822543385400_B56",
      "doi-asserted-by": "crossref",
      "first-page": "1009",
      "DOI": "10.1083/jcb.127.4.1009",
      "article-title": "Cytoplasmic dynein undergoes intracellular redistribution concomitant with phosphorylation of the heavy chain in response to serum starvation and okadaic acid",
      "volume": "127",
      "author": "Lin",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B57",
      "doi-asserted-by": "crossref",
      "first-page": "125",
      "DOI": "10.1242/jcs.101.1.125",
      "article-title": "Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells",
      "volume": "101",
      "author": "Lin",
      "year": "1992",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822543385400_B58",
      "doi-asserted-by": "crossref",
      "first-page": "309",
      "DOI": "10.1016/0092-8674(87)90157-7",
      "article-title": "Identification of a microtubule-based motor in the nematode C. elegans.",
      "volume": "51",
      "author": "Lye",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2023072822543385400_B59",
      "doi-asserted-by": "crossref",
      "first-page": "19176",
      "DOI": "10.1016/S0021-9258(17)32291-3",
      "article-title": "Regulation of kinesin activity by phosphorylation of kinesinassociated proteins",
      "volume": "269",
      "author": "McIlvain",
      "year": "1994",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072822543385400_B60",
      "doi-asserted-by": "crossref",
      "first-page": "6001",
      "DOI": "10.1016/S0021-9258(18)83300-2",
      "article-title": "Enzymes for microtubule-dependent motility",
      "volume": "264",
      "author": "McIntosh",
      "year": "1989",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072822543385400_B61",
      "doi-asserted-by": "crossref",
      "first-page": "7212",
      "DOI": "10.1073/pnas.91.15.7212",
      "article-title": "KAR3-encoded kinesin is a minus-enddirected motor that functions with centromere binding proteins (CBF3) on an in vitroyeast kinetochore",
      "volume": "91",
      "author": "Middleton",
      "year": "1994",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822543385400_B62",
      "doi-asserted-by": "crossref",
      "first-page": "304",
      "DOI": "10.1083/jcb.86.1.304",
      "article-title": "The membrane proteins of the vacuolar system I. Analysis by a novel method of intralysosomal iodination",
      "volume": "86",
      "author": "Muller",
      "year": "1980",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B63",
      "doi-asserted-by": "crossref",
      "first-page": "585",
      "DOI": "10.1083/jcb.133.3.585",
      "article-title": "Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport",
      "volume": "133",
      "author": "Niclas",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822543385400_B64",
      "doi-asserted-by": "crossref",
      "first-page": "181",
      "DOI": "10.1038/330181a0",
      "article-title": "Retrograde transport by the microtubule-associated protein MAP1C",
      "volume": "330",
      "author": "Paschal",
      "year": "1987",
      "journal-title": "Nature (Lond)"
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    {
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      "volume": "268",
      "author": "Paschal",
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      "author": "Pesanti",
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      "first-page": "263",
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      "author": "Pfarr",
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      "author": "Pitt",
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      "author": "Rickard",
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      "article-title": "Microtubule dynamics in fish melanophores",
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      "author": "Rodionov",
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      "volume": "134",
      "author": "Rodriguez",
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      "author": "Rozdzial",
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      "author": "Sato-Yoshitake",
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      "author": "Schafer",
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      "author": "Scheel",
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      "first-page": "1548",
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      "article-title": "Dynein is the motor for retrograde axonal transport of organelles",
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      "author": "Schnapp",
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      "author": "Schroer",
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      "DOI": "10.1006/scdb.1996.0041",
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      "author": "Schroer",
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      "author": "Severin",
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      "first-page": "329",
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      "author": "Sheetz",
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      "volume": "112",
      "author": "Shimizu",
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      "author": "Steuer",
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      "author": "Stossel",
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      "author": "Swanson",
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      "volume": "108",
      "author": "Tanaka",
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      "author": "Toyohara",
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      "author": "Toyoshima",
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      "volume": "69",
      "author": "Wang",
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