Mitosis-coupled, microtubule-dependent clustering of endosomal vesicles around centrosomes

Cell Structure and Function

Volumn 38, Issue 1, 2013, Pages 31-41

  Takatsu, Hiroyuki ^a   Katoh, Yohei ^a   Ueda, Tomoko ^a   Waguri, Satoshi ^b   Murayama, Takashi ^c   Takahashi, Senye ^a   Shin, Hye Won ^a   Nakayama, Kazuhisa ^a  

^a KYOTO UNIVERSITY   (Japan)

^b FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cytokinesis; Dynein; Recycling endosome; Spindle pole; Transferrin receptor

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; TRANSFERRIN RECEPTOR;

ANAPHASE; ARTICLE; CELL STRAIN HEK293; CELL SURFACE; CELL VACUOLE; CENTROSOME; CYTOKINESIS; ENDOSOME; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; LENTIVIRINAE; MICROTUBULE; MITOSIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMETAPHASE; PROPHASE; TELOPHASE;

ANAPHASE; CELL MEMBRANE; CENTROSOME; CYTOKINESIS; ENDOCYTOSIS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; ORGANELLES; RECEPTORS, TRANSFERRIN;

EID: 84875082698     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.12028     Document Type: Article

References (40)

1. Altan-Bonnet, N., Sougrat, R., and Lippincott-Schwartz, J. 2004. Molecular basis for Golgi maintenance and biogenesis. Curr. Opin. Cell Biol., 16: 364-372.
2. Boucrot, E. and Kirchhausen, T. 2007. Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl. Acad. Sci. USA, 104: 7939-7944.
3. Burkhardt, J.K., Echeverri, C.J., Nilsson, T., and Vallee, R.B. 1997. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol., 139: 469.
4. Colanzi, A., Suetterlin, C., and Malhotra, V. 2003. Cell-cycle-specific Golgi fragmentation: how and why? Curr. Opin. Cell Biol., 15: 462-467.
5. Dunster, K., Toh, B.H., and Sentry, J.W. 2002. Early endosomes, late endosomes, and lysosomes display distinct strategies of inheritance with similarities to Golgi-derived membranes. Eur. J. Cell Biol., 81: 117-124.
6. Echeverri, C.J., Paschal, B.M., Vaughan, K.T., and Vallee, R.B. 1996. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol., 132: 617-633.
7. Fürthauer, M. and González-Gaitán, M. 2009. Endocytosis and mitosis: a two-way relationship. Cell Cycle, 8: 3311-3318.
8. Gaietta, G.M., Giepmans, B.N.G., Deerinck, T.J., Smith, W.B., Ngan, L., Llopis, J., Adams, S.R., Tsien, R.Y., and Ellisman, M.H. 2006. Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc. Natl. Acad. Sci. USA, 103: 17777-17782.
9. Ghosh, R.N., Mallet, W.G., Soe, T.T., McGraw, T.E., and Maxfield, F.R. 1998. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol., 142: 923-936.
10. Hirose, H., Arasaki, K., Dohmae, N., Takio, K., Hatsuzawa, K., Nagahama, M., Tani, K., Yamamoto, A., Tohyama, M., and Tagaya, M. 2004. Implication of ZW10 in membrane trafficking between the endoplasmic reticulum and Golgi. EMBO J., 23: 1267-1278.
11. + channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J. Biol. Chem., 280: 13187-13194.
12. Jolly, A.L. and Gelfand, V.I. 2011. Bidirectional intracelular transport: utility and mechanism. Biochem. Soc. Trans., 39: 1126-1130.
13. Jordan, M.A., Thrower, D., and Wilson, L. 1992. Effects of vinblastin, podophyllotoxin and nocodazole on mitotic spindles: implications for the role of microtubule dynamics in mitosis. J. Cell Sci., 102: 401-416.
14. Kain, R., Angata, K., Kerjaschki, D., and Fukuda, M. 1998. Molecular cloning and expression of a novel human trans-Golgi network glycoprotein, TGN51, that contains multiple tyrosine-containing motifs. J. Biol. Chem., 273: 981-988.
15. Kawano, J., Ide, S., Oinuma, T., and Suganuma, T. 1994. A protein-specific monoclonal antibody to rat liver β1→4 galactosyltransferase and its application to immunohistochemistry. J. Histochem. Cytochem., 42: 363-369.
16. Kimoto, T., Yamada, M., Ichikawa, T., Honma, D., Cherry, R.J., Morrison, I.E.G., and Kawato, S. 2009. Digital fluorescence analysis of trafficking of single endosomes containing low-density lipoprotein in adrenocortical cells: facilitation of centripetal motion by adrenocorticotropic hormone. Mol. Cell. Endocrinol., 307: 185-195.
17. Kimura, K. and Kimura A. 2011. A novel mechanism of microtubule length-dependent force to pull centrosomes toward the cell center. BioArchitecture, 1: 74-79.
18. Kobayashi, T. and Murayama, T. 2009. Cell cycle-dependent microtubule-based dynamic transport of cytoplasmic dynein in mammalian cells. PLoS One, 4: e7827.
19. Mallard, F., Tang, B.L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B., and Johannes, L. 2002. Early/recycling ndosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol., 156: 653-664.
20. Maxfield, F.R. and McGraw, T.E. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol., 5: 121-132.
21. Montagnac, G., Echard, A., and Chavrier, P. 2008. Endocytic traffic in animal cell cytokinesis. Curr. Opin. Cell Biol., 20: 454-461.
22. Montagnac, G., Sibarita, J.-B., Loubéry, S., Daviet, L., Romao, M., Raposo, G., and Chavrier, P. 2009. ARF6 interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr. Biol., 19: 184-195.
23. Nishimoto-Morita, K., Shin, H.-W., Mitsuhashi, H., Kitamura, M., Zhang, Q., Johannes, L., and Nakayama, K. 2009. Differential effects of depletion of ARL1 and ARFRP1 on membrane trafficking between the trans-Golgi network and endosomes. J. Biol. Chem., 284: 10583-10592.
24. Sachse, M., Ramm, G., Strous, G., and Klumperman, J. 2002. Endosomes: multipurpose designs for integrating housekeeping and specialized tasks. Histochem. Cell Biol., 117: 91-104.
25. Sager, P.R., Brown, P.A., and Berlin, R.D. 1984. Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell, 39: 275-282.
26. Schweitzer, J.K., Burke, E.E., Goodson, H.V., and D'Souza-Schorey, C. 2005. Endocytosis resumes during late mitosis and is required for cytokinesis. J. Biol. Chem., 280: 41628-41635.
27. Seemann, J., Pypaert, M., Taguchi, T., Malsam, J., and Warren, G. 2002. Partitioning of the matrix fraction of the Golgi apparatus during mitosis in animal cells. Science, 295: 848-851.
28. Shin, H.-W., Kobayashi, H., Kitamura, M., Waguri, S., Suganuma, T., Uchiyama, Y., and Nakayama, K. 2005. Roles of ARFRP1 (ADP-ribosylation factor-related protein 1) in post-Golgi membrane trafficking. J. Cell Sci., 118: 4039-4048.
29. Shin, H.-W., Morinaga, N., Noda, M., and Nakayama, K. 2004. BIG2, a guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity. Mol. Biol. Cell, 15: 5283-5294.
30. Shorter, J. and Warren, G. 2002. Golgi architecture and Inheritance. Annu. Rev. Cell Dev. Biol., 18: 379-420.
31. Simon, G.C., Schonteich, E., Wu, C.C., Piekny, A., Ekiert, D., Yu, X., Gould, G.W., Glotzer, M., and Prekeris, R. 2008. Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J., 27: 1791-1803.
32. Skoufias, D.A., DeBonis, S., Saoudi, Y., Lebeau, L., Crevel, I., Cross, R., Wade, R.H., Hackney, D., and Kozielski, F. 2006. S-Trityl-L-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem., 281: 17559-17569.
33. Tabuchi, M., Tanaka, N., Nishida-Kitayama, J., Ohno, H., and Kishi, F. 2002. Alternative splicing regulates the subcellular localization of divalent metal transporter 1 isoforms. Mol. Biol. Cell, 13: 4371-4387.
34. Takahashi, S., Kubo, K., Waguri, S., Yabashi, A., Shin, H.-W., Katoh, Y., and Nakayama, K. 2012. Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J. Cell Sci., 125: 4049-4057.
35. Thomas, S., Ritter, B., Verbich, D., Sanson, C., Bourbonnière, L., McKinney, R.A., and McPherson, P.S. 2009. Intersectin regulates dendritic spine development and somatodendritic endocytosis but not synaptic vesicle recycling in hippocampal neurons J. Biol. Chem., 284: 12410-12419.
36. Uchida, Y., Hasegawa, J., Chinnapen, D., Inoue, T., Okazaki, S., Kato, R., Wakatsuki, S., Misaki, R., Koike, M., Uchiyama, Y., Iemura, S.-I., Natsume, T., Kuwahara, R., Nakagawa, T., Nishikawa, K., Mukai, K., Miyoshi, E., Taniguchi, N., Sheff, D., Lencer, W.I., Taguchi, T., and Arai, H. 2011. Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc. Natl. Acad. Sci. USA, 108: 15846-15851
37. Waguri, S., Kohmura, M., Gotow, T., Watanabe, T., Ohsawa, Y., Kominami, E., and Uchiyama, Y. 1999. The induction of autophagic vacuoles and the unique endocytic compartments, C-shaped multivesicular bodies, in GH4C1 cells after treatment with 17β-estradiol, insulin and EGF. Arch. Histol. Cytol., 62: 423-434.
38. Warren, G., Davoust, J., and Cockcroft, A. 1984. Recycling of transferrin receptors in A431 cells is inhibited during mitosis. EMBO J., 3: 2217-2225.
39. Wei, J.-H. and Seemann, J. 2009. Mitotic division of the mammalian Golgi apparatus. Sem. Cell Dev. Biol., 20: 810-816.
40. Welte, M.A. 2010. Bidirectional transport: matchmaking for motors. Curr. Biol., 20: R410-R413