Endosomal Trafficking During Mitosis and Notch-Dependent Asymmetric Division

  • Alicia Daeden
  • Marcos Gonzalez-GaitanEmail author
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 57)


Endocytosis is key in a number of cell events. In particular, its role during cell division has been a challenging question: while early studies examined whether endocytosis occurs during cell division, recent works show that, during division, cells do perform endocytosis actively. More importantly, during asymmetric cell division, endocytic pathways also control Notch signaling: endocytic vesicles regulate the presence, at the plasma membrane, of receptors and ligands at different levels between the two-daughter cells. Both early and late endocytic compartments have been shown to exert key regulatory controls by up-regulating or down-regulating Notch signaling in those cells. This biased Notch signaling enable finally cell fate assignation and specification which play a central role in development and physiology. In this chapter, we cover a number of significant works on endosomal trafficking evincing the importance of endocytosis in Notch-mediated cell fate specification during development.


  1. Abdelilah-Seyfried S et al (2000) A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 155:733–752PubMedPubMedCentralGoogle Scholar
  2. Aguet F et al (2016) Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy. Mol Biol Cell 27:3418–3435. Scholar
  3. Albertson R, Cao J, Hsieh TS, Sullivan W (2008) Vesicles and actin are targeted to the cleavage furrow via furrow microtubules and the central spindle. J Cell Biol 181:777–790. Scholar
  4. Albertson R, Riggs B, Sullivan W (2005) Membrane traffic: a driving force in cytokinesis. Trends Cell Biol 15:92–101. Scholar
  5. Arias CI, Siri SO, Conde C (2015) Involvement of SARA in axon and dendrite growth. PLoS ONE 10:e0138792. Scholar
  6. Aster JC, Pear WS, Blacklow SC (2008) Notch signaling in leukemia. Annu Rev Pathol 3:587–613. Scholar
  7. Barbieri E, Di Fiore PP, Sigismund S (2016) Endocytic control of signaling at the plasma membrane. Curr Opin Cell Biol 39:21–27. Scholar
  8. Bardin S, Miserey-Lenkei S, Hurbain I, Garcia-Castillo D, Raposo G, Goud B (2015) Phenotypic characterization of RAB6A knockout mouse embryonic fibroblasts vol 107.
  9. Benhra N, Vignaux F, Dussert A, Schweisguth F, Le Borgne R (2010) Neuralized promotes basal to apical transcytosis of delta in epithelial cells. Mol Biol Cell 21:2078–2086. Scholar
  10. Benmerah A, Begue B, Dautry-Varsat A, Cerf-Bensussan N (1996) The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J Biol Chem 271:12111–12116CrossRefPubMedGoogle Scholar
  11. Benmerah A, Gagnon J, Begue B, Megarbane B, Dautry-Varsat A, Cerf-Bensussan N (1995) The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J Cell Biol 131:1831–1838CrossRefPubMedGoogle Scholar
  12. Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA (2002) The endocytic protein alpha-adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev Cell 3:221–231. CrossRefPubMedGoogle Scholar
  13. 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 85:660–671CrossRefPubMedGoogle Scholar
  14. Berlin RD, Oliver JM, Walter RJ (1978) Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell 15:327–341CrossRefPubMedGoogle Scholar
  15. Berndt N et al (2017) Ubiquitylation-independent activation of Notch signalling by delta. Elife 6:e27346. Scholar
  16. Bhat KM, Gaziova I, Katipalla S (2011) Neuralized mediates asymmetric division of neural precursors by two distinct and sequential events: promoting asymmetric localization of numb and enhancing activation of Notch-signaling. Dev Biol 351:186–198. Scholar
  17. Bluemink JG, de Laat SW (1973) New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs of Xenopus laevis. I. Electron microscope observations. J Cell Biol 59:89–108CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bokel C, Schwabedissen A, Entchev E, Renaud O, Gonzalez-Gaitan M (2006) Sara endosomes and the maintenance of Dpp signaling levels across mitosis. Science 314:1135–1139. Scholar
  19. Boucrot E (2008) What does the plasma membrane do during mitosis? Med Sci (Paris) 24:34–36. Scholar
  20. Boucrot E, Howes MT, Kirchhausen T, Parton RG (2011) Redistribution of caveolae during mitosis. J Cell Sci 124:1965–1972. Scholar
  21. Boucrot E, Kirchhausen T (2007) Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci U S A 104:7939–7944. Scholar
  22. Boucrot E, Kirchhausen T (2008) Mammalian cells change volume during mitosis. PLoS ONE 3:e1477. Scholar
  23. Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13:1124–1131. Scholar
  24. Bray D, White JG (1988) Cortical flow in animal cells. Science 239:883–888CrossRefPubMedGoogle Scholar
  25. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139:469–484CrossRefPubMedPubMedCentralGoogle Scholar
  26. Capalbo L, D’Avino PP, Archambault V, Glover DM (2011) Rab5 GTPase controls chromosome alignment through Lamin disassembly and relocation of the NuMA-like protein Mud to the poles during mitosis. Proc Natl Acad Sci U S A 108:17343–17348. Scholar
  27. Cayrol C, Cougoule C, Wright M (2002) The beta2-adaptin clathrin adaptor interacts with the mitotic checkpoint kinase BubR1. Biochem Biophys Res Commun 298:720–730CrossRefPubMedGoogle Scholar
  28. Champion L, Linder MI, Kutay U (2017) Cellular reorganization during mitotic entry. Trends cell biol 27:26–41. Scholar
  29. Chanez AL, Hehl AB, Engstler M, Schneider A (2006) Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J Cell Sci 119:2968–2974. Scholar
  30. Chapman G, Major JA, Iyer K, James AC, Pursglove SE, Moreau JL, Dunwoodie SL (2016) Notch1 endocytosis is induced by ligand and is required for signal transduction. Biochim Biophys Acta 1863:166–177. Scholar
  31. Chapouton P et al (2010) Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells. J Neurosci 30:7961–7974. Scholar
  32. Chen H et al (2009) Embryonic arrest at midgestation and disruption of Notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proc Natl Acad Sci U S A 106:13838–13843. Scholar
  33. Chen J, Zhang M (2013) The Par3/Par6/aPKC complex and epithelial cell polarity. Exp Cell Res 319:1357–1364. Scholar
  34. Chesneau L, Dambournet D, Machicoane M, Kouranti I, Fukuda M, Goud B, Echard A (2012) An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol 22:147–153. Scholar
  35. Chitnis A (2006) Why is delta endocytosis required for effective activation of Notch? Dev Dyn 235:886–894. Scholar
  36. Cocucci E, Aguet F, Boulant S, Kirchhausen T (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150:495–507. Scholar
  37. Conner SD, Wessel GM (1999) Syntaxin is required for cell division. Mol Biol Cell 10:2735–2743CrossRefPubMedPubMedCentralGoogle Scholar
  38. Cotton M, Benhra N, Le Borgne R (2013) Numb inhibits the recycling of Sanpodo in Drosophila sensory organ precursor. Curr Biol 23:581–587. Scholar
  39. Coumailleau F, Furthauer M, Knoblich JA, Gonzalez-Gaitan M (2009) Directional delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458:1051–1055. Scholar
  40. Couturier L, Mazouni K, Schweisguth F (2013) Numb localizes at endosomes and controls the endosomal sorting of Notch after asymmetric division in Drosophila. Curr Biol 23:588–593. Scholar
  41. Couturier L, Vodovar N, Schweisguth F (2012) Endocytosis by numb breaks Notch symmetry at cytokinesis. Nat Cell Biol 14:131–139. Scholar
  42. Crowe R, Henrique D, Ish-Horowicz D, Niswander L (1998) A new role for Notch and delta in cell fate decisions: patterning the feather array. Development 125:767–775PubMedGoogle Scholar
  43. Dambournet D et al (2011) Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13:981–988. Scholar
  44. Danilchik MV, Bedrick SD, Brown EE, Ray K (2003) Furrow microtubules and localized exocytosis in cleaving Xenopus laevis embryos. J Cell Sci 116:273–283CrossRefPubMedGoogle Scholar
  45. de-la-Concha A, Dietrich U, Weigel D, Campos-Ortega JA (1988) Functional interactions of neurogenic genes of Drosophila melanogaster Genetics 118:499–508Google Scholar
  46. De Brabander M, Nuydens R, Geerts H, Hopkins CR (1988) Dynamic behavior of the transferrin receptor followed in living epidermoid carcinoma (A431) cells with nanovid microscopy. Cell Motil Cytoskeleton 9:30–47. Scholar
  47. de Celis JF, Bray SJ (2000) The abruptex domain of Notch regulates negative interactions between Notch, its ligands and fringe. Development 127:1291–1302Google Scholar
  48. Deblandre GA, Lai EC, Kintner C (2001) Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev Cell 1:795–806. Scholar
  49. Derivery E, Seum C, Daeden A, Loubery S, Holtzer L, Julicher F, Gonzalez-Gaitan M (2015) Polarized endosome dynamics by spindle asymmetry during asymmetric cell division. Nature 528:280–285. Scholar
  50. 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. Scholar
  51. Dexter JS (1914) The analysis of a case of continuous variation in drosophila by a study of its linkage relations. Am Nat 48:712–758CrossRefGoogle Scholar
  52. Dobrowolski R, De Robertis EM (2011) Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles. Nat Rev Mol Cell Biol 13:53–60. Scholar
  53. Durrbach A, Louvard D, Coudrier E (1996) Actin filaments facilitate two steps of endocytosis. J Cell Sci 109(Pt 2):457–465PubMedGoogle Scholar
  54. Dyer N et al (2007) Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134:4437–4447.
  55. Emery G, Hutterer A, Berdnik D, Mayer B, Wirtz-Peitz F, Gaitan MG, Knoblich JA (2005) Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122:763–773
  56. Eskelinen EL et al (2002) Inhibition of autophagy in mitotic animal cells. Traffic 3:878–893CrossRefPubMedGoogle Scholar
  57. F. PD (1939) Effects of Notch deficiencies. Drosoph Inf Serv 12Google Scholar
  58. Feng B, Schwarz H, Jesuthasan S (2002) Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. Exp Cell Res 279:14–20CrossRefPubMedGoogle Scholar
  59. Fenner F (1999) The birth of the cell. Immunol Cell Biol 77:468CrossRefGoogle Scholar
  60. Fernando Aniento NE, Grittiths G, Gruenberg J (1993) Cytoplasmic dynein-dependent vesicular trans port from early to late endosomes. J Cell Biol 123(6):1373–1387. (Part 1)Google Scholar
  61. Fielding AB, Royle SJ (2013) Mitotic inhibition of clathrin-mediated endocytosis. Cell Mol Life Sci 70:3423–3433. Scholar
  62. Fielding AB et al (2005) Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 24:3389–3399. Scholar
  63. Fielding AB, Willox AK, Okeke E, Royle SJ (2012) Clathrin-mediated endocytosis is inhibited during mitosis. Proc Natl Acad Sci U S A 109:6572–6577. Scholar
  64. Finger FP, White JG (2002) Fusion and fission: membrane trafficking in animal cytokinesis. Cell 108:727–730CrossRefPubMedGoogle Scholar
  65. Firestone AJ et al (2012) Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature 484:125–129.
  66. Fischer-Friedrich E, Hyman AA, Julicher F, Muller DJ, Helenius J (2014) Quantification of surface tension and internal pressure generated by single mitotic cells. Sci Rep 4:6213. Scholar
  67. Flores-Rodriguez N, Rogers SS, Kenwright DA, Waigh TA, Woodman PG, Allan VJ (2011) Roles of dynein and dynactin in early endosome dynamics revealed using automated tracking and global analysis. PLoS ONE 6:e24479. Scholar
  68. Gerald NJ, Damer CK, O’Halloran TJ, De Lozanne A (2001) Cytokinesis failure in clathrin-minus cells is caused by cleavage furrow instability. Cell Motil Cytoskeleton 48:213–223.<213::AID-CM1010>3.0.CO;2-VCrossRefPubMedGoogle Scholar
  69. Gomez-Lamarca MJ, Snowdon LA, Seib E, Klein T, Bray SJ (2015) Rme-8 depletion perturbs Notch recycling and predisposes to pathogenic signaling. J Cell Biol 210:303–318. Scholar
  70. Gonzalez-Gaitan M, Jackle H (1997) Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88:767–776CrossRefPubMedGoogle Scholar
  71. Gordon WR, Vardar-Ulu D, Histen G, Sanchez-Irizarry C, Aster JC, Blacklow SC (2007) Structural basis for autoinhibition of Notch. Nat Struct Mol Biol 14:295. CrossRefPubMedGoogle Scholar
  72. Goss JW, Toomre DK (2008) Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. J Cell Biol 181:1047–1054. Scholar
  73. Gray GE et al (1999) Human ligands of the Notch receptor. Am J Pathol 154:785–794. Scholar
  74. Gromley A et al (2005) Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123:75–87. Scholar
  75. Gudejko HF, Alford LM, Burgess DR (2012) Polar expansion during cytokinesis. Cytoskeleton (Hoboken) 69:1000–1009. Scholar
  76. Guerrini A (1995) A history of the life sciences. Lois N. Magner Isis 86:89. Scholar
  77. Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of numb and Notch. Neuron 17:27–41CrossRefPubMedGoogle Scholar
  78. Hartenstein V, Posakony JW (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev Biol 142:13–30CrossRefPubMedGoogle Scholar
  79. Hehnly H, Doxsey S (2014) Rab11 endosomes contribute to mitotic spindle organization and orientation. Dev Cell 28:497–507. Scholar
  80. Henrique D, Hirsinger E, Adam J, Le Roux I, Pourquie O, Ish-Horowicz D, Lewis J (1997) Maintenance of neuroepithelial progenitor cells by delta-Notch signalling in the embryonic chick retina. Curr Biol 7:661–670CrossRefPubMedGoogle Scholar
  81. Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389–400CrossRefPubMedGoogle Scholar
  82. Heuss SF, Ndiaye-Lobry D, Six EM, Israel A, Logeat F (2008) The intracellular region of Notch ligands Dll1 and Dll3 regulates their trafficking and signaling activity. Proc Natl Acad Sci U S A 105:11212–11217. Scholar
  83. Hicks C, Ladi E, Lindsell C, Hsieh JJ, Hayward SD, Collazo A, Weinmaster G (2002) A secreted Delta1-Fc fusion protein functions both as an activator and inhibitor of Notch1 signaling. J Neurosci Res 68:655–667. Scholar
  84. Hill E, Clarke M, Barr FA (2000) The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis. EMBO J 19:5711–5719. Scholar
  85. Högnäs G et al (2011) Cytokinesis failure due to derailed integrin traffic induces aneuploidy and oncogenic transformation in vitro and in vivo. Oncogene 31:3597. Scholar
  86. Hori K (2004) Drosophila deltex mediates suppressor of hairless-independent and late-endosomal activation of Notch signaling. Development 131:5527–5537. Scholar
  87. Hu Y-Y, Zheng M-h, Zhang R, Liang Y-M, Han H (2012) Notch signaling pathway and cancer metastasis. In: Reichrath J, Reichrath S (eds) Notch Signaling in embryology and cancer. Springer US, New York, NY, pp 186–198.
  88. Hu Y, Chuang J-Z, Xu K, McGraw TG, Sung C-H (2002) SARA, a FYVE domain protein, affects Rab5-mediated endocytosis. J Cell Sci 115:4755–4763 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Iannolo G et al (1997) Mapping of the molecular determinants involved in the interaction between eps15 and AP-2. Cancer Res 57:240–245PubMedGoogle Scholar
  90. Imatani A, Callahan R (2000) Identification of a novel NOTCH-4/INT-3 RNA species encoding an activated gene product in certain human tumor cell lines. Oncogene 19:223–231. Scholar
  91. Itoh F et al (2002) The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-β/Smad signalling. Genes Cells 7:321–331. CrossRefPubMedGoogle Scholar
  92. Itoh M et al (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by delta. Dev Cell 4:67–82CrossRefPubMedGoogle Scholar
  93. Jafar-Nejad H et al (2005) Sec15, a component of the exocyst, promotes Notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev Cell 9:351–363. Scholar
  94. Jafar-Nejad H, Norga K, Bellen H (2002) Numb: “adapting” Notch for endocytosis. Dev Cell 3:155–156CrossRefPubMedGoogle Scholar
  95. Jantsch-Plunger V, Glotzer M (1999) Depletion of syntaxins in the early Caenorhabditis elegans embryo reveals a role for membrane fusion events in cytokinesis. Curr Biol 9:738–745CrossRefPubMedGoogle Scholar
  96. Johnson SA, Zitserman D, Roegiers F (2016) Numb regulates the balance between Notch recycling and late-endosome targeting in Drosophila neural progenitor cells. Mol Biol Cell 27:2857–2866. Scholar
  97. Kaplan A, Reiner O (2011) Linking cytoplasmic dynein and transport of Rab8 vesicles to the midbody during cytokinesis by the doublecortin domain-containing 5 protein. J Cell Sci 124:3989–4000. Scholar
  98. Kaur S, Fielding AB, Gassner G, Carter NJ, Royle SJ (2014) An unmet actin requirement explains the mitotic inhibition of clathrin-mediated endocytosis. Elife 3:e00829. Scholar
  99. Kogo H, Fujimoto T (2000) Concentration of caveolin-1 in the cleavage furrow as revealed by time-lapse analysis. Biochem Biophys Res Commun 268:82–87. Scholar
  100. Kouranti I, Sachse M, Arouche N, Goud B, Echard A (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16:1719–1725. CrossRefPubMedGoogle Scholar
  101. Kressmann S, Campos C, Castanon I, Furthauer M, Gonzalez-Gaitan M (2015) Directional Notch trafficking in sara endosomes during asymmetric cell division in the spinal cord. Nat Cell Biol 17:333–339. Scholar
  102. Kunda P, Rodrigues NT, Moeendarbary E, Liu T, Ivetic A, Charras G, Baum B (2012) PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Curr Biol 22:231–236. Scholar
  103. Lai EC, Deblandre GA, Kintner C, Rubin GM (2001) Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of Delta. Dev Cell 1:783–794. Scholar
  104. Langridge PD, Struhl G (2017) Epsin-dependent ligand endocytosis activates Notch by force. Cell 171:1383–1396. e1312.
  105. Lanzetti L (2012) A novel function of Rab5 in mitosis. Small GTPases 3:168–172.
  106. Le Borgne R, Schweisguth F (2003) Unequal segregation of neuralized biases Notch activation during asymmetric cell division. Dev Cell 5:139–148CrossRefPubMedGoogle Scholar
  107. Lehmann R, Jimenez F, Dietrich U, Camposortega JA (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila-Melanogaster. Wilhelm Rouxs Arch Dev Biol 192:62–74. Scholar
  108. Leitch CC, Lodh S, Prieto-Echague V, Badano JL, Zaghloul NA (2014) Basal body proteins regulate Notch signaling through endosomal trafficking. J Cell Sci 127:2407–2419. Scholar
  109. Lewis J (1998) Notch signalling and the control of cell fate choices in vertebrates. Semin Cell Dev Biol 9:583–589. Scholar
  110. Loubery S et al (2017) Sara phosphorylation state controls the dispatch of endosomes from the central spindle during asymmetric division. Nat Commun 8:15285. Scholar
  111. Loubery S, Gonzalez-Gaitan M (2014) Monitoring Notch/delta endosomal trafficking and signaling in Drosophila. Methods Enzymol 534:301–321. Scholar
  112. Loubery S, Seum C, Moraleda A, Daeden A, Furthauer M, Gonzalez-Gaitan M (2014) Uninflatable and Notch control the targeting of Sara endosomes during asymmetric division. Curr Biol 24:2142–2148. Scholar
  113. Loubéry S, Seum C, Moraleda A, Daeden A, Fürthauer M, Gonzalez-Gaitan M (2015) Uninflatable and Notch control the targeting of Sara Endosomes during asymmetric division. Curr Biol 25:817–818. Scholar
  114. Loubery S, Wilhelm C, Hurbain I, Neveu S, Louvard D, Coudrier E (2008) Different microtubule motors move early and late endocytic compartments. Traffic 9:492–509. Scholar
  115. Low SH, Li X, Miura M, Kudo N, Quinones B, Weimbs T (2003) Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev Cell 4:753–759CrossRefPubMedGoogle Scholar
  116. Maddox AS, Burridge K (2003) RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 160:255–265. Scholar
  117. Matteoni R, Kreis TE (1987) Translocation and clustering of endosomes and lysosomes depends on microtubules. J Cell Biol 105:1253–1265CrossRefPubMedGoogle Scholar
  118. Mavor LM, Miao H, Zuo Z, Holly RM, Xie Y, Loerke D, Blankenship JT (2016) Rab8 directs furrow ingression and membrane addition during epithelial formation in Drosophila melanogaster. Development 143:892–903.
  119. McGill MA, Dho SE, Weinmaster G, McGlade CJ (2009) Numb regulates post-endocytic trafficking and degradation of Notch1. J Biol Chem 284:26427–26438. Scholar
  120. Meloty-Kapella L, Shergill B, Kuon J, Botvinick E, Weinmaster G (2012) Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Dev Cell 22:1299–1312. Scholar
  121. Metchnikoff E (1883) Untersuchungen über die mesodermalen Phagocyten einiger. Wirbeltiere Biol Zentralbl 3:560–565Google Scholar
  122. Militello RD, Munafo DB, Beron W, Lopez LA, Monier S, Goud B, Colombo MI (2013) Rab24 is required for normal cell division. Traffic 14:502–518. Scholar
  123. Ming Guo LYJ, Yuh Nung Jan (1996) Control of daughter cell fates during asymmetric division: interaction of numb and Notch. NeuronGoogle Scholar
  124. Miserey-Lenkei S, Colombo MI (2016) Small RAB GTPases regulate multiple steps of mitosis. Front Cell Dev Biol 4:2. Scholar
  125. Montagnac G, Chavrier P (2008) Endosome positioning during cytokinesis. Biochem Soc Trans 36:442–443. Scholar
  126. Montagne C, Gonzalez-Gaitan M (2014) Sara endosomes and the asymmetric division of intestinal stem cells. Development 141:2014–2023. Scholar
  127. Mosesson Y, Mills GB, Yarden Y (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8:835–850.
  128. Motley A, Bright NA, Seaman MN, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162:909–918. Scholar
  129. Murphy C et al (1996) Endosome dynamics regulated by a Rho protein. Nature 384:427–432. Scholar
  130. Murray JW, Yin D, Wolkoff AW (2017) Reduction of organelle motility by removal of potassium and other solutes. PLOS ONE 12:e0184898. Scholar
  131. Muskavitch MA (1994) Delta-Notch signaling and Drosophila cell fate choice. Dev Biol 166:415–430. Scholar
  132. Neto H, Collins LL, Gould GW (2011) Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 437:13–24. Scholar
  133. Nichols JT, Miyamoto A, Olsen SL, D’Souza B, Yao C, Weinmaster G (2007) DSL ligand endocytosis physically dissociates Notch1 heterodimers before activating proteolysis can occur. J Cell Biol 176:445–458. Scholar
  134. Nieland TJ, Ehrlich M, Krieger M, Kirchhausen T (2005) Endocytosis is not required for the selective lipid uptake mediated by murine SR-BI. Biochim Biophys Acta 1734:44–51. Scholar
  135. O’Connor-Giles KM, Skeath JB (2003) Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev Cell 5:231–243CrossRefPubMedGoogle Scholar
  136. Oliver JM, Seagrave JC (1987) The blocked pinocytic activity of mitotic cells is restored in mitotic-interphase hybrids. Exp Cell Res 171:475–482CrossRefPubMedGoogle Scholar
  137. Overstreet E, Fitch E, Fischer JA (2004) Fat facets and liquid facets promote delta endocytosis and delta signaling in the signaling cells. Development 131:5355–5366. Scholar
  138. Özlü N et al (2015) Quantitative comparison of a human cancer cell surface proteome between interphase and mitosis. EMBO J 34:251–265. Scholar
  139. Parks AL, Klueg KM, Stout JR, Muskavitch MA (2000) Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127:1373–1385PubMedPubMedCentralGoogle Scholar
  140. Pavlopoulos E, Pitsouli C, Klueg KM, Muskavitch MA, Moschonas NK, Delidakis C (2001) Neuralized encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev Cell 1:807–816CrossRefPubMedGoogle Scholar
  141. Pelissier A, Chauvin J-P, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13:1848–1857. Scholar
  142. Pellinen T et al (2008) Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev Cell 15:371–385. Scholar
  143. Poodry CA (1990) Shibire, a neurogenic mutant of Drosophila. Dev Biol 138:464–472CrossRefPubMedGoogle Scholar
  144. Prekeris R (2011) Actin regulation during abscission: unexpected roles of Rab35 and endocytic transport. Cell Res 21:1283–1285. Scholar
  145. Pypaert M, Lucocq JM, Warren G (1987) Coated pits in interphase and mitotic A431 cells. Eur J Cell Biol 45:23–29PubMedGoogle Scholar
  146. Pypaert M, Mundy D, Souter E, Labbe JC, Warren G (1991) Mitotic cytosol inhibits invagination of coated pits in broken mitotic cells. J Cell Biol 114:1159–1166CrossRefPubMedGoogle Scholar
  147. Rajan A, Tien AC, Haueter CM, Schulze KL, Bellen HJ (2009) The Arp2/3 complex and WASp are required for apical trafficking of delta into microvilli during cell fate specification of sensory organ precursors. Nat Cell Biol 11:815–824. Scholar
  148. Ramaswami M, Rao S, van der Bliek A, Kelly RB, Krishnan KS (1993) Genetic studies on dynamin function in Drosophila. J Neurogenet 9:73–87CrossRefPubMedGoogle Scholar
  149. Ramos RG, Grimwade BG, Wharton KA, Scottgale TN, Artavanis-Tsakonas S (1989) Physical and functional definition of the Drosophila Notch locus by P element transformation Genetics 123:337–348Google Scholar
  150. Randazzo PA (2003) RhoD, Src, and hDia2C in endosome motility. Dev Cell 4:287–288CrossRefPubMedGoogle Scholar
  151. Rapp S, Saffrich R, Anton M, Jakle U, Ansorge W, Gorgas K, Just WW (1996) Microtubule-based peroxisome movement. J Cell Sci 109(Pt 4):837–849PubMedGoogle Scholar
  152. Raucher D, Sheetz MP (1999a) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506CrossRefPubMedPubMedCentralGoogle Scholar
  153. Raucher D, Sheetz MP (1999b) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506. Scholar
  154. Rhyu MS, Jan LY, Jan YN (1994) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76:477–491CrossRefPubMedGoogle Scholar
  155. Riggs B et al (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol 163:143–154. Scholar
  156. Robertson AS, Smythe E, Ayscough KR (2009) Functions of actin in endocytosis. Cell Mol Life Sci 66:2049–2065. Scholar
  157. Salbreux G, Charras G, Paluch E (2012) Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol 22:536–545. Scholar
  158. Salcini AE et al (1997) Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev 11:2239–2249CrossRefPubMedPubMedCentralGoogle Scholar
  159. Saleem M, Morlot S, Hohendahl A, Manzi J, Lenz M, Roux A (2015) A balance between membrane elasticity and polymerization energy sets the shape of spherical clathrin coats. Nat Commun 6:6249. Scholar
  160. Santolini E, Puri C, Salcini AE, Gagliani MC, Pelicci PG, Tacchetti C, Di Fiore PP (2000) Numb is an endocytic protein. J Cell Biol 151:1345–1352CrossRefPubMedPubMedCentralGoogle Scholar
  161. Schiel JA, Prekeris R (2010) Making the final cut—mechanisms mediating the abscission step of cytokinesis. Sci World J 10:1424–1434. Scholar
  162. 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. Scholar
  163. Schweitzer JK, D’Souza-Schorey C (2002a) Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis. J Biol Chem 277:27210–27216. Scholar
  164. Schweitzer JK, D’Souza-Schorey C (2002b) Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis. J Biol Chem 277:27210–27216. Scholar
  165. Schweitzer JK, D’Souza-Schorey C (2005) A requirement for ARF6 during the completion of cytokinesis. Exp Cell Res 311:74–83. Scholar
  166. Schweitzer JK, Sedgwick AE, D’Souza-Schorey C (2011) ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin Cell Dev Biol 22:39–47. Scholar
  167. Serio G, Margaria V, Jensen S, Oldani A, Bartek J, Bussolino F, Lanzetti L (2011) Small GTPase Rab5 participates in chromosome congression and regulates localization of the centromere-associated protein CENP-F to kinetochores. Proc Natl Acad Sci U S A 108:17337–17342. Scholar
  168. Seugnet L, Simpson P, Haenlin M (1997) Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev Biol 192:585–598. Scholar
  169. Shao X et al (2016) Numb regulates vesicular docking for homotypic fusion of early endosomes via membrane recruitment of Mon1b. Cell Res 26:593–612. Scholar
  170. Shuster CB, Burgess DR (2002) Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis. Proc Natl Acad Sci U S A 99:3633–3638. Scholar
  171. Sirotkin V (2011) Cell biology: actin keeps endocytosis on a short leash. Curr Biol 21:R552–R554. Scholar
  172. Skop AR, Bergmann D, Mohler WA, White JG (2001) Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex. Curr Biol CB 11:735–746CrossRefPubMedGoogle Scholar
  173. Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119:4589–4598. Scholar
  174. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622. Scholar
  175. Spana EP, Doe CQ (1996) Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21–26CrossRefPubMedGoogle Scholar
  176. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525. Scholar
  177. Stewart MP, Helenius J, Toyoda Y, Ramanathan SP, Muller DJ, Hyman AA (2011) Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469:226–230. Scholar
  178. Swanson JA, Locke A, Ansel P, Hollenbeck PJ (1992) Radial movement of lysosomes along microtubules in permeabilized macrophages. J Cell Sci 103(Pt 1):201–209PubMedGoogle Scholar
  179. Tacheva-Grigorova SK, Santos AJ, Boucrot E, Kirchhausen T (2013) Clathrin-mediated endocytosis persists during unperturbed mitosis. Cell Rep 4:659–668. Scholar
  180. Takatsu H et al (2013) Mitosis-coupled, microtubule-dependent clustering of endosomal vesicles around centrosomes. Cell Struct Func 38:31–41. Scholar
  181. Thompson HM, Skop AR, Euteneuer U, Meyer BJ, McNiven MA (2002) The large GTPase dynamin associates with the spindle midzone and is required for cytokinesis. Curr Biol 12:2111–2117CrossRefPubMedPubMedCentralGoogle Scholar
  182. Tian X, Hansen D, Schedl T, Skeath JB (2004) Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 131:5807–5815.
  183. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL (1998) SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95:779–791CrossRefPubMedGoogle Scholar
  184. Tuomikoski T, Felix MA, Doree M, Gruenberg J (1989) Inhibition of endocytic vesicle fusion in vitro by the cell-cycle control protein kinase cdc2. Nature 342:942–945. Scholar
  185. Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN (1989) Numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58:349–360CrossRefPubMedGoogle Scholar
  186. Valapala M, Hose S, Gongora C, Dong L, Wawrousek EF, Samuel Zigler J, Sinha D (2013) Impaired endolysosomal function disrupts Notch signalling in optic nerve astrocytes. Nat Commun 4:1629. Scholar
  187. Wang W, Struhl G (2004) Drosophila epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131:5367–5380. Scholar
  188. Warren G, Davoust J, Cockcroft A (1984) Recycling of transferrin receptors in A431 cells is inhibited during mitosis. EMBO J 3:2217–2225PubMedPubMedCentralCrossRefGoogle Scholar
  189. Warren G, Featherstone C, Griffiths G, Burke B (1983) Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J Cell Biol 97:1623–1628CrossRefPubMedGoogle Scholar
  190. Wilkin MB, Baron M (2005) Endocytic regulation of Notch activation and down-regulation (review). Mol Membr Biol 22:279–289. Scholar
  191. Wilson GM et al (2005) The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 16:849–860. Scholar
  192. Xie G, Zhang H, Du G, Huang Q, Liang X, Ma J, Jiao R (2012) Uif, a large transmembrane protein with EGF-like repeats, can antagonize Notch signaling in Drosophila. PLoS ONE 7:e36362. Scholar
  193. Xu KMN, Egan SE (2010) Notch signaling in lung development and disease. In: Curie Madame (ed) Bioscience. Landes Bioscience, Database Austin (TX)Google Scholar
  194. Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16:964–975. Scholar
  195. Yousefian J, Troost T, Grawe F, Sasamura T, Fortini M, Klein T (2013) Dmon1 controls recruitment of Rab7 to maturing endosomes in Drosophila. J Cell Sci 126:1583–1594. Scholar
  196. Yu X, Prekeris R, Gould GW (2007) Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 86:25–35. Scholar
  197. Zagouras P, Stifani S, Blaumueller CM, Carcangiu ML, Artavanis-Tsakonas S (1995) Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc Natl Acad Sci U S A 92:6414–6418CrossRefPubMedPubMedCentralGoogle Scholar
  198. Zajac AL, Goldman YE, Holzbaur EL, Ostap EM (2013) Local cytoskeletal and organelle interactions impact molecular-motor- driven early endosomal trafficking. Curr Biol 23:1173–1180. Scholar
  199. Zhang H, Squirrell JM, White JG (2008) RAB-11 permissively regulates spindle alignment by modulating metaphase microtubule dynamics in Caenorhabditis elegans early embryos. Mol Biol Cell 19:2553–2565. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biochemistry DepartmentUniversity of GenevaGenevaSwitzerland

Personalised recommendations