Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
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 155:733–752
Aguet F et al (2016) Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy. Mol Biol Cell 27:3418–3435. https://doi.org/10.1091/mbc.E16-03-0164
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. https://doi.org/10.1083/jcb.200803096
Albertson R, Riggs B, Sullivan W (2005) Membrane traffic: a driving force in cytokinesis. Trends Cell Biol 15:92–101. https://doi.org/10.1016/j.tcb.2004.12.008
Arias CI, Siri SO, Conde C (2015) Involvement of SARA in axon and dendrite growth. PLoS ONE 10:e0138792. https://doi.org/10.1371/journal.pone.0138792
Aster JC, Pear WS, Blacklow SC (2008) Notch signaling in leukemia. Annu Rev Pathol 3:587–613. https://doi.org/10.1146/annurev.pathmechdis.3.121806.154300
Barbieri E, Di Fiore PP, Sigismund S (2016) Endocytic control of signaling at the plasma membrane. Curr Opin Cell Biol 39:21–27. https://doi.org/10.1016/j.ceb.2016.01.012
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. https://doi.org/10.1111/boc.201400083
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. https://doi.org/10.1091/mbc.E09-11-0926
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 271:12111–12116
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 131:1831–1838
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. https://doi.org/10.1016/s1534-5807(02)00215-0
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
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
Berndt N et al (2017) Ubiquitylation-independent activation of Notch signalling by delta. Elife 6:e27346. https://doi.org/10.7554/eLife.27346
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. https://doi.org/10.1016/j.ydbio.2010.12.008
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 59:89–108
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. https://doi.org/10.1126/science.1132524
Boucrot E (2008) What does the plasma membrane do during mitosis? Med Sci (Paris) 24:34–36. https://doi.org/10.1051/medsci/200824134
Boucrot E, Howes MT, Kirchhausen T, Parton RG (2011) Redistribution of caveolae during mitosis. J Cell Sci 124:1965–1972. https://doi.org/10.1242/jcs.076570
Boucrot E, Kirchhausen T (2007) Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci U S A 104:7939–7944. https://doi.org/10.1073/pnas.0702511104
Boucrot E, Kirchhausen T (2008) Mammalian cells change volume during mitosis. PLoS ONE 3:e1477. https://doi.org/10.1371/journal.pone.0001477
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. https://doi.org/10.1038/ncb2307
Bray D, White JG (1988) Cortical flow in animal cells. Science 239:883–888
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 139:469–484
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. https://doi.org/10.1073/pnas.1103720108
Cayrol C, Cougoule C, Wright M (2002) The beta2-adaptin clathrin adaptor interacts with the mitotic checkpoint kinase BubR1. Biochem Biophys Res Commun 298:720–730
Champion L, Linder MI, Kutay U (2017) Cellular reorganization during mitotic entry. Trends cell biol 27:26–41. https://doi.org/10.1016/j.tcb.2016.07.004
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. https://doi.org/10.1242/jcs.03023
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. https://doi.org/10.1016/j.bbamcr.2015.10.021
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. https://doi.org/10.1523/JNEUROSCI.6170-09.2010
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. https://doi.org/10.1073/pnas.0907008106
Chen J, Zhang M (2013) The Par3/Par6/aPKC complex and epithelial cell polarity. Exp Cell Res 319:1357–1364. https://doi.org/10.1016/j.yexcr.2013.03.021
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. https://doi.org/10.1016/j.cub.2011.11.058
Chitnis A (2006) Why is delta endocytosis required for effective activation of Notch? Dev Dyn 235:886–894. https://doi.org/10.1002/dvdy.20683
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. https://doi.org/10.1016/j.cell.2012.05.047
Conner SD, Wessel GM (1999) Syntaxin is required for cell division. Mol Biol Cell 10:2735–2743
Cotton M, Benhra N, Le Borgne R (2013) Numb inhibits the recycling of Sanpodo in Drosophila sensory organ precursor. Curr Biol 23:581–587. https://doi.org/10.1016/j.cub.2013.02.020
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. https://doi.org/10.1038/nature07854
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. https://doi.org/10.1016/j.cub.2013.03.002
Couturier L, Vodovar N, Schweisguth F (2012) Endocytosis by numb breaks Notch symmetry at cytokinesis. Nat Cell Biol 14:131–139. https://doi.org/10.1038/ncb2419
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 125:767–775
Dambournet D et al (2011) Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13:981–988. https://doi.org/10.1038/ncb2279
Danilchik MV, Bedrick SD, Brown EE, Ray K (2003) Furrow microtubules and localized exocytosis in cleaving Xenopus laevis embryos. J Cell Sci 116:273–283
de-la-Concha A, Dietrich U, Weigel D, Campos-Ortega JA (1988) Functional interactions of neurogenic genes of Drosophila melanogaster Genetics 118:499–508
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. https://doi.org/10.1002/cm.970090105
de Celis JF, Bray SJ (2000) The abruptex domain of Notch regulates negative interactions between Notch, its ligands and fringe. Development 127:1291–1302
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. https://doi.org/10.1016/S1534-5807(01)00091-0
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. https://doi.org/10.1038/nature16443
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. https://doi.org/10.1038/ncb2284
Dexter JS (1914) The analysis of a case of continuous variation in drosophila by a study of its linkage relations. Am Nat 48:712–758
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. https://doi.org/10.1038/nrm3244
Durrbach A, Louvard D, Coudrier E (1996) Actin filaments facilitate two steps of endocytosis. J Cell Sci 109(Pt 2):457–465
Dyer N et al (2007) Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134:4437–4447. https://doi.org/10.1242/dev.010983
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 https://doi.org/10.1016/j.cell.2005.08.017
Eskelinen EL et al (2002) Inhibition of autophagy in mitotic animal cells. Traffic 3:878–893
F. PD (1939) Effects of Notch deficiencies. Drosoph Inf Serv 12
Feng B, Schwarz H, Jesuthasan S (2002) Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. Exp Cell Res 279:14–20
Fenner F (1999) The birth of the cell. Immunol Cell Biol 77:468
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)
Fielding AB, Royle SJ (2013) Mitotic inhibition of clathrin-mediated endocytosis. Cell Mol Life Sci 70:3423–3433. https://doi.org/10.1007/s00018-012-1250-8
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. https://doi.org/10.1038/sj.emboj.7600803
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. https://doi.org/10.1073/pnas.1117401109
Finger FP, White JG (2002) Fusion and fission: membrane trafficking in animal cytokinesis. Cell 108:727–730
Firestone AJ et al (2012) Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature 484:125–129. https://doi.org/10.1038/nature10936
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. https://doi.org/10.1038/srep06213
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. https://doi.org/10.1371/journal.pone.0024479
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. https://doi.org/10.1002/1097-0169(200103)48:3<213::AID-CM1010>3.0.CO;2-V
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. https://doi.org/10.1083/jcb.201411001
Gonzalez-Gaitan M, Jackle H (1997) Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88:767–776
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. https://doi.org/10.1038/nsmb1227
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. https://doi.org/10.1083/jcb.200712137
Gray GE et al (1999) Human ligands of the Notch receptor. Am J Pathol 154:785–794. https://doi.org/10.1016/S0002-9440(10)65325-4
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. https://doi.org/10.1016/j.cell.2005.07.027
Gudejko HF, Alford LM, Burgess DR (2012) Polar expansion during cytokinesis. Cytoskeleton (Hoboken) 69:1000–1009. https://doi.org/10.1002/cm.21078
Guerrini A (1995) A history of the life sciences. Lois N. Magner Isis 86:89. https://doi.org/10.1086/357086
Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of numb and Notch. Neuron 17:27–41
Hartenstein V, Posakony JW (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev Biol 142:13–30
Hehnly H, Doxsey S (2014) Rab11 endosomes contribute to mitotic spindle organization and orientation. Dev Cell 28:497–507. https://doi.org/10.1016/j.devcel.2014.01.014
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 7:661–670
Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389–400
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. https://doi.org/10.1073/pnas.0800695105
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. https://doi.org/10.1002/jnr.10263
Hill E, Clarke M, Barr FA (2000) The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis. EMBO J 19:5711–5719. https://doi.org/10.1093/emboj/19.21.5711
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. https://doi.org/10.1038/onc.2011.527
Hori K (2004) Drosophila deltex mediates suppressor of hairless-independent and late-endosomal activation of Notch signaling. Development 131:5527–5537. https://doi.org/10.1242/dev.01448
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. https://doi.org/10.1007/978-1-4614-0899-4_14
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
Iannolo G et al (1997) Mapping of the molecular determinants involved in the interaction between eps15 and AP-2. Cancer Res 57:240–245
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. https://doi.org/10.1038/sj.onc.1203295
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. https://doi.org/10.1046/j.1365-2443.2002.00519.x
Itoh M et al (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by delta. Dev Cell 4:67–82
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. https://doi.org/10.1016/j.devcel.2005.06.010
Jafar-Nejad H, Norga K, Bellen H (2002) Numb: “adapting” Notch for endocytosis. Dev Cell 3:155–156
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 9:738–745
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. https://doi.org/10.1091/mbc.E15-11-0751
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. https://doi.org/10.1242/jcs.085407
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. https://doi.org/10.7554/eLife.00829
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. https://doi.org/10.1006/bbrc.1999.2058
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. https://doi.org/10.1016/j.cub.2006.07.020
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. https://doi.org/10.1038/ncb3119
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. https://doi.org/10.1016/j.cub.2011.12.016
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. https://doi.org/10.1016/S1534-5807(01)00092-2
Langridge PD, Struhl G (2017) Epsin-dependent ligand endocytosis activates Notch by force. Cell 171:1383–1396. e1312. https://doi.org/10.1016/j.cell.2017.10.048
Lanzetti L (2012) A novel function of Rab5 in mitosis. Small GTPases 3:168–172. https://doi.org/10.4161/sgtp.19987
Le Borgne R, Schweisguth F (2003) Unequal segregation of neuralized biases Notch activation during asymmetric cell division. Dev Cell 5:139–148
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. https://doi.org/10.1007/Bf00848482
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. https://doi.org/10.1242/jcs.130344
Lewis J (1998) Notch signalling and the control of cell fate choices in vertebrates. Semin Cell Dev Biol 9:583–589. https://doi.org/10.1006/scdb.1998.0266
Loubery S et al (2017) Sara phosphorylation state controls the dispatch of endosomes from the central spindle during asymmetric division. Nat Commun 8:15285. https://doi.org/10.1038/ncomms15285
Loubery S, Gonzalez-Gaitan M (2014) Monitoring Notch/delta endosomal trafficking and signaling in Drosophila. Methods Enzymol 534:301–321. https://doi.org/10.1016/B978-0-12-397926-1.00017-2
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. https://doi.org/10.1016/j.cub.2014.07.054
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. https://doi.org/10.1016/j.cub.2015.02.053
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. https://doi.org/10.1111/j.1600-0854.2008.00704.x
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 4:753–759
Maddox AS, Burridge K (2003) RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 160:255–265. https://doi.org/10.1083/jcb.200207130
Matteoni R, Kreis TE (1987) Translocation and clustering of endosomes and lysosomes depends on microtubules. J Cell Biol 105:1253–1265
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. https://doi.org/10.1242/dev.128876
McGill MA, Dho SE, Weinmaster G, McGlade CJ (2009) Numb regulates post-endocytic trafficking and degradation of Notch1. J Biol Chem 284:26427–26438. https://doi.org/10.1074/jbc.M109.014845
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. https://doi.org/10.1016/j.devcel.2012.04.005
Metchnikoff E (1883) Untersuchungen über die mesodermalen Phagocyten einiger. Wirbeltiere Biol Zentralbl 3:560–565
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. https://doi.org/10.1111/tra.12057
Ming Guo LYJ, Yuh Nung Jan (1996) Control of daughter cell fates during asymmetric division: interaction of numb and Notch. Neuron
Miserey-Lenkei S, Colombo MI (2016) Small RAB GTPases regulate multiple steps of mitosis. Front Cell Dev Biol 4:2. https://doi.org/10.3389/fcell.2016.00002
Montagnac G, Chavrier P (2008) Endosome positioning during cytokinesis. Biochem Soc Trans 36:442–443. https://doi.org/10.1042/BST0360442
Montagne C, Gonzalez-Gaitan M (2014) Sara endosomes and the asymmetric division of intestinal stem cells. Development 141:2014–2023. https://doi.org/10.1242/dev.104240
Mosesson Y, Mills GB, Yarden Y (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8:835–850. http://www.nature.com/nrc/journal/v8/n11/suppinfo/nrc2521_S1.html
Motley A, Bright NA, Seaman MN, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162:909–918. https://doi.org/10.1083/jcb.200305145
Murphy C et al (1996) Endosome dynamics regulated by a Rho protein. Nature 384:427–432. https://doi.org/10.1038/384427a0
Murray JW, Yin D, Wolkoff AW (2017) Reduction of organelle motility by removal of potassium and other solutes. PLOS ONE 12:e0184898. https://doi.org/10.1371/journal.pone.0184898
Muskavitch MA (1994) Delta-Notch signaling and Drosophila cell fate choice. Dev Biol 166:415–430. https://doi.org/10.1006/dbio.1994.1326
Neto H, Collins LL, Gould GW (2011) Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 437:13–24. https://doi.org/10.1042/BJ20110153
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. https://doi.org/10.1083/jcb.200609014
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. https://doi.org/10.1016/j.bbalip.2005.02.007
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 5:231–243
Oliver JM, Seagrave JC (1987) The blocked pinocytic activity of mitotic cells is restored in mitotic-interphase hybrids. Exp Cell Res 171:475–482
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. https://doi.org/10.1242/dev.01434
Özlü N et al (2015) Quantitative comparison of a human cancer cell surface proteome between interphase and mitosis. EMBO J 34:251–265. https://doi.org/10.15252/embj.201385162
Parks AL, Klueg KM, Stout JR, Muskavitch MA (2000) Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127:1373–1385
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 1:807–816
Pelissier A, Chauvin J-P, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13:1848–1857. https://doi.org/10.1016/j.cub.2003.10.023
Pellinen T et al (2008) Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev Cell 15:371–385. https://doi.org/10.1016/j.devcel.2008.08.001
Poodry CA (1990) Shibire, a neurogenic mutant of Drosophila. Dev Biol 138:464–472
Prekeris R (2011) Actin regulation during abscission: unexpected roles of Rab35 and endocytic transport. Cell Res 21:1283–1285. https://doi.org/10.1038/cr.2011.131
Pypaert M, Lucocq JM, Warren G (1987) Coated pits in interphase and mitotic A431 cells. Eur J Cell Biol 45:23–29
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 114:1159–1166
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. https://doi.org/10.1038/ncb1888
Ramaswami M, Rao S, van der Bliek A, Kelly RB, Krishnan KS (1993) Genetic studies on dynamin function in Drosophila. J Neurogenet 9:73–87
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 123:337–348
Randazzo PA (2003) RhoD, Src, and hDia2C in endosome motility. Dev Cell 4:287–288
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):837–849
Raucher D, Sheetz MP (1999a) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506
Raucher D, Sheetz MP (1999b) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506. https://doi.org/10.1083/jcb.144.3.497
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 76:477–491
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. https://doi.org/10.1083/jcb.200305115
Robertson AS, Smythe E, Ayscough KR (2009) Functions of actin in endocytosis. Cell Mol Life Sci 66:2049–2065. https://doi.org/10.1007/s00018-009-0001-y
Salbreux G, Charras G, Paluch E (2012) Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol 22:536–545. https://doi.org/10.1016/j.tcb.2012.07.001
Salcini AE et al (1997) Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev 11:2239–2249
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. https://doi.org/10.1038/ncomms7249
Santolini E, Puri C, Salcini AE, Gagliani MC, Pelicci PG, Tacchetti C, Di Fiore PP (2000) Numb is an endocytic protein. J Cell Biol 151:1345–1352
Schiel JA, Prekeris R (2010) Making the final cut—mechanisms mediating the abscission step of cytokinesis. Sci World J 10:1424–1434. https://doi.org/10.1100/tsw.2010.129
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. https://doi.org/10.1074/jbc.M504497200
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. https://doi.org/10.1074/jbc.M201569200
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. https://doi.org/10.1074/jbc.M201569200
Schweitzer JK, D’Souza-Schorey C (2005) A requirement for ARF6 during the completion of cytokinesis. Exp Cell Res 311:74–83. https://doi.org/10.1016/j.yexcr.2005.07.033
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. https://doi.org/10.1016/j.semcdb.2010.09.002
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. https://doi.org/10.1073/pnas.1103516108
Seugnet L, Simpson P, Haenlin M (1997) Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev Biol 192:585–598. https://doi.org/10.1006/dbio.1997.8723
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. https://doi.org/10.1038/cr.2016.34
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. https://doi.org/10.1073/pnas.052342699
Sirotkin V (2011) Cell biology: actin keeps endocytosis on a short leash. Curr Biol 21:R552–R554. https://doi.org/10.1016/j.cub.2011.06.029
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 11:735–746
Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119:4589–4598. https://doi.org/10.1242/jcs.03247
Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622. https://doi.org/10.1038/nrm2748
Spana EP, Doe CQ (1996) Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21–26
Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525. https://doi.org/10.1038/nrm2728
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. https://doi.org/10.1038/nature09642
Swanson JA, Locke A, Ansel P, Hollenbeck PJ (1992) Radial movement of lysosomes along microtubules in permeabilized macrophages. J Cell Sci 103(Pt 1):201–209
Tacheva-Grigorova SK, Santos AJ, Boucrot E, Kirchhausen T (2013) Clathrin-mediated endocytosis persists during unperturbed mitosis. Cell Rep 4:659–668. https://doi.org/10.1016/j.celrep.2013.07.017
Takatsu H et al (2013) Mitosis-coupled, microtubule-dependent clustering of endosomal vesicles around centrosomes. Cell Struct Func 38:31–41. https://doi.org/10.1247/csf.12028
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 12:2111–2117
Tian X, Hansen D, Schedl T, Skeath JB (2004) Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 131:5807–5815. https://doi.org/10.1242/dev.01459
Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL (1998) SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95:779–791
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. https://doi.org/10.1038/342942a0
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 58:349–360
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. https://doi.org/10.1038/ncomms2624
Wang W, Struhl G (2004) Drosophila epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131:5367–5380. https://doi.org/10.1242/dev.01413
Warren G, Davoust J, Cockcroft A (1984) Recycling of transferrin receptors in A431 cells is inhibited during mitosis. EMBO J 3:2217–2225
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 97:1623–1628
Wilkin MB, Baron M (2005) Endocytic regulation of Notch activation and down-regulation (review). Mol Membr Biol 22:279–289. https://doi.org/10.1080/09687860500129778
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. https://doi.org/10.1091/mbc.E04-10-0927
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. https://doi.org/10.1371/journal.pone.0036362
Xu KMN, Egan SE (2010) Notch signaling in lung development and disease. In: Curie Madame (ed) Bioscience. Landes Bioscience, Database Austin (TX)
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. https://doi.org/10.1091/mbc.E04-09-0774
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. https://doi.org/10.1242/jcs.114934
Yu X, Prekeris R, Gould GW (2007) Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 86:25–35. https://doi.org/10.1016/j.ejcb.2006.10.002
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 92:6414–6418
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. https://doi.org/10.1016/j.cub.2013.05.015
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. https://doi.org/10.1091/mbc.E07-09-0862
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Daeden, A., Gonzalez-Gaitan, M. (2018). Endosomal Trafficking During Mitosis and Notch-Dependent Asymmetric Division. In: Lamaze, C., Prior, I. (eds) Endocytosis and Signaling. Progress in Molecular and Subcellular Biology, vol 57. Springer, Cham. https://doi.org/10.1007/978-3-319-96704-2_11
Download citation
DOI: https://doi.org/10.1007/978-3-319-96704-2_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-96703-5
Online ISBN: 978-3-319-96704-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)