Clathrin-mediated endocytosis is inhibited during mitosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 17, 2012, Pages 6572-6577

  Fielding, Andrew B ^a   Willox, Anna K ^a   Okeke, Emmanuel ^a   Royle, Stephen J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cell division; Endosomal recycling; Moonlighting; Prometaphase; Receptor trafficking

Indexed keywords

CD8 ANTIGEN; CLATHRIN; SOMATOMEDIN B RECEPTOR; TRANSFERRIN RECEPTOR;

ARTICLE; CELL ASSAY; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; FEMALE; FLOW CYTOMETRY; HELA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; INTERPHASE; MITOSIS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN LOCALIZATION; PROTEIN MOTIF;

CLATHRIN; ENDOCYTOSIS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MITOSIS; RECEPTORS, TRANSFERRIN;

EID: 84860136231     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1117401109     Document Type: Article

References (45)

1. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE (2001) Biological basket weaving: Formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 17:517-568. (Pubitemid 33096185)
2. Traub LM (2009) Tickets to ride: Selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583-596.
3. Fawcett DW (1965) Surface specializations of absorbing cells. J Histochem Cytochem 13:75-91.
4. Berlin RD, Oliver JM, Walter RJ (1978) Surface functions during Mitosis I: Phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell 15:327-341. (Pubitemid 9052402)
5. Marsh M, Helenius A (1980) Adsorptive endocytosis of Semliki Forest virus. J Mol Biol 142:439-454. (Pubitemid 11165623)
6. Berlin RD, Oliver JM (1980) Surface functions during mitosis. II. Quantitation of pinocytosis and kinetic characterization of the mitotic cycle with a new fluorescence technique. J Cell Biol 85:660-671. (Pubitemid 10007435)
7. Warren G, Davoust J, Cockcroft A (1984) Recycling of transferrin receptors in A431 cells is inhibited during mitosis. EMBO J 3:2217-2225.
8. Pypaert M, Lucocq JM, Warren G (1987) Coated pits in interphase and mitotic A431 cells. Eur J Cell Biol 45:23-29.
9. Pypaert M, Mundy D, Souter E, Labbé JC, Warren G (1991) Mitotic cytosol inhibits invagination of coated pits in broken mitotic cells. J Cell Biol 114:1159-1166. (Pubitemid 21909876)
10. Oliver JM, Seagrave JC, Pfeiffer JR, Feibig ML, Deanin GG (1985) Surface functions during mitosis in rat basophilic leukemia cells. J Cell Biol 101:2156-2166. (Pubitemid 16169945)
11. Sager PR, Brown PA, Berlin RD (1984) Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell 39:275-282. (Pubitemid 15191210)
12. Quintart J, Leroy-Houyet MA, Trouet A, Baudhuin P (1979) Endocytosis and chloroquine accumulation during the cell cycle of hepatoma cells in culture. J Cell Biol 82:644-653. (Pubitemid 10222835)
13. Illinger D, Italiano L, Beck JP, Waltzinger C, Kuhry JG (1993) Comparative evolution of endocytosis levels and of the cell surface area during the L929 cell cycle: A fluorescence study with TMA-DPH. Biol Cell 79:265-268. (Pubitemid 24110563)
14. Woodman PG, Adamczewski JP, Hunt T, Warren G (1993) In vitro fusion of endocytic vesicles is inhibited by cyclin A-cdc2 kinase. Mol Biol Cell 4:541-553. (Pubitemid 23150918)
15. Schweitzer JK, Burke EE, Goodson HV, D'Souza-Schorey C (2005) Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem 280:41628-41635. (Pubitemid 41832225)
16. Raucher D, Sheetz MP (1999) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497-506. (Pubitemid 29234529)
17. Chen H, Slepnev VI, Di Fiore PP, De Camilli P (1999) The interaction of epsin and Eps15 with the clathrin adaptor AP-2 is inhibited by mitotic phosphorylation and enhanced by stimulation-dependent dephosphorylation in nerve terminals. J Biol Chem 274: 3257-3260. (Pubitemid 29077157)
18. Warren G (1993) Membrane partitioning during cell division. Annu Rev Biochem 62: 323-348.
19. Warren G (1985) Membrane traffic and organelle division. Trends Biochem Sci 10: 439-443.
20. Royle SJ (2011) Mitotic moonlighting functions for membrane trafficking proteins. Traffic 12:791-798.
21. Scita G, Di Fiore PP (2010) The endocytic matrix. Nature 463:464-473.
22. Boucrot E, Kirchhausen T (2007) Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci USA 104:7939-7944. (Pubitemid 47185855)
23. Boucrot E, Kirchhausen T (2008) Mammalian cells change volume during mitosis. PLoS ONE 3:e1477.
24. Chetrit D, et al. (2011) Negative regulation of the endocytic adaptor disabled-2 (Dab2) in mitosis. J Biol Chem 286:5392-5403.
25. Fürthauer M, González-Gaitán M (2009) Endocytosis and mitosis: A two-way relationship. Cell Cycle 8:3311-3318.
26. Neto H, Collins LL, Gould GW (2011) Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 437:13-24.
27. Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597-608.
28. Kozik P, Francis RW, Seaman MN, Robinson MS (2010) A screen for endocytic motifs. Traffic 11:843-855.
29. Nilsson T, Jackson M, Peterson PA (1989) Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58: 707-718. (Pubitemid 19210964)
30. Seaman MN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165:111-122.
31. Seaman MN (2007) Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci 120:2378-2389.
32. Lobel P, Fujimoto K, Ye RD, Griffiths G, Kornfeld S (1989) Mutations in the cytoplasmic domain of the 275 kd mannose 6-phosphate receptor differentially alter lysosomal enzyme sorting and endocytosis. Cell 57:787-796. (Pubitemid 19149818)
33. Lin SX, Mallet WG, Huang AY, Maxfield FR (2004) Endocytosed cation-independent mannose 6-phosphate receptor traffics via the endocytic recycling compartment en route to the trans-Golgi network and a subpopulation of late endosomes. Mol Biol Cell 15:721-733. (Pubitemid 38146488)
34. Vassilev LT, et al. (2006) Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 103:10660-10665. (Pubitemid 44078033)
35. Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389-400. (Pubitemid 19065841)
36. Royle SJ, Bright NA, Lagnado L (2005) Clathrin is required for the function of the mitotic spindle. Nature 434:1152-1157. (Pubitemid 40663496)
37. Liu L, Shi H, Chen X, Wang Z (2011) Regulation of EGF-stimulated EGF receptor endocytosis during M phase. Traffic 12:201-217.
38. Mills IG (2007) The interplay between clathrin-coated vesicles and cell signalling. Semin Cell Dev Biol 18:459-470.
39. Habela CW, Sontheimer H (2007) Cytoplasmic volume condensation is an integral part of mitosis. Cell Cycle 6:1613-1620. (Pubitemid 47327948)
40. Stewart MP, et al. (2011) Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469:226-230.
41. Coupin GT, Muller CD, Rémy-Kristensen A, Kuhry JG (1999) Cell surface membrane homeostasis and intracellular membrane traffic balance in mouse L929 cells. J Cell Sci 112:2431-2440. (Pubitemid 29381033)
42. Erickson CA, Trinkaus JP (1976) Microvilli and blebs as sources of reserve surface membrane during cell spreading. Exp Cell Res 99:375-384.
43. Follett EA, Goldman RD (1970) The occurrence of microvilli during spreading and growth of BHK21-C13 fibroblasts. Exp Cell Res 59:124-136.
44. Kunda P, Baum B (2009) The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol 19:174-179.
45. Devenport D, Oristian D, Heller E, Fuchs E (2011) Mitotic internalization of planar cell polarity proteins preserves tissue polarity. Nat Cell Biol 13:893-902.