Midbody: From cellular junk to regulator of cell polarity and cell fate

Current Opinion in Cell Biology

Volumn 35, Issue , 2015, Pages 51-58

  Dionne, Lai Kuan ^a   Wang, Xiao Jing ^a   Prekeris, Rytis ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISSION ZONE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL POLARITY; CELL STRUCTURE; MIDBODY; MITOSIS; NEOPLASM; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CELL LINEAGE; GENETICS; HUMAN; MICROTUBULE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL POLARITY; HUMANS; MICROTUBULES; MITOSIS; SIGNAL TRANSDUCTION;

EID: 84938710018     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.04.010     Document Type: Review

References (61)

1. Pollard T.D. Mechanics of cytokinesis in eukaryotes. Curr Opin Cell Biol 2010, 22:50-56.
2. Fededa J.P., Gerlich D.W. Molecular control of animal cell cytokinesis. Nat Cell Biol 2012, 14:440-447.
3. Schiel J.A., Childs C., Prekeris R. Endocytic transport and cytokinesis: from regulation of the cytoskeleton to midbody inheritance. Trends Cell Biol 2013, 23:319-327.
4. Schiel J.A., et al. Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci 2011, 124(Pt 9):1411-1424.
5. Schiel J.A., et al. FIP3-endosome-dependent formation of the secondary ingression mediates ESCRT-III recruitment during cytokinesis. Nat Cell Biol 2012, 14:1068-1078.
6. Simon G.C., et al. Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J 2008, 27:1791-1803.
7. Wilson G.M., et al. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 2004, 16:849-860.
8. Elia N., et al. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A 2011, 108:4846-4851.
9. Guizetti J., et al. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 2011, 331:1616-1620.
10. Kuo T.C., et al. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat Cell Biol 2011, 13:1214-1223.
11. Pollarolo G., et al. Cytokinesis remnants define first neuronal asymmetry in vivo. Nat Neurosci 2011, 14:1525-1533.
12. Ettinger A.W., et al. Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat Commun 2011, 2:503.
13. Li D., et al. FIP5 phosphorylation during mitosis regulates apical trafficking and lumenogenesis. EMBO Rep 2014, 15:428-437.
14. Singh D., Pohl C. Coupling of rotational cortical flow, asymmetric midbody positioning, and spindle rotation mediates dorsoventral axis formation in C. elegans. Dev Cell 2014, 28:253-267.
15. Carlton J.G., Agromayor M., Martin-Serrano J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci U S A 2008, 105:10541-10546.
16. Connell J.W., et al. Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 2009, 10:42-56.
17. Skop A.R., et al. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 2004, 305:61-66.
18. Chen T.C., et al. From midbody protein-protein interaction network construction to novel regulators in cytokinesis. J Proteome Res 2009, 8:4943-4953.
19. Marzesco A.M., et al. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 2005, 118(Pt 13):2849-2858.
20. Dubreuil V., et al. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol 2007, 176:483-495.
21. Lopez-Camacho C., et al. Core binding factor beta (CBFbeta) is retained in the midbody during cytokinesis. J Cell Physiol 2014, 229:1466-1474.
22. Salzmann V., et al. Centrosome-dependent asymmetric inheritance of the midbody ring in Drosophila germline stem cell division. Mol Biol Cell 2014, 25:267-275.
23. Huang Z., et al. MiCroKiTS 4.0: a database of midbody, centrosome, kinetochore, telomere and spindle. Nucleic Acids Res 2015, 43(Database issue):D328-D334.
24. Crowell E.F., Tinevez J.Y., Echard A. A simple model for the fate of the cytokinesis midbody remnant: implications for remnant degradation by autophagy. Bioessays 2013, 35:472-481.
25. Clevers H., Loh K.M., Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 2014, 346:1248012.
26. Habib S.J., et al. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 2013, 339:1445-1448.
27. Fumoto K., et al. Wnt5a signaling controls cytokinesis by correctly positioning ESCRT-III at the midbody. J Cell Sci 2012, 125(Pt 20):4822-4832.
28. Kaplan D.D., et al. Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 2004, 279:10829-10832.
29. Gao C., et al. Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nat Cell Biol 2010, 12:781-790.
30. Andreas K., Sittinger M., Ringe J. Toward in situ tissue engineering: chemokine-guided stem cell recruitment. Trends Biotechnol 2014, 32:483-492.
31. Li M., et al. Chemokine receptor CXCR4 signaling modulates the growth factor-induced cell cycle of self-renewing and multipotent neural progenitor cells. Glia 2011, 59:108-118.
32. Muller A., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
33. Graham N.A., Graeber T.G. Complexity of metastasis-associated SDF-1 ligand signaling in breast cancer stem cells. Proc Natl Acad Sci U S A 2014, 111:7503-7504.
34. Cho H., Kehrl J.H. Localization of Gi alpha proteins in the centrosomes and at the midbody: implication for their role in cell division. J Cell Biol 2007, 178:245-255.
35. Naito Y., Okada M., Yagisawa H. Phospholipase C isoforms are localized at the cleavage furrow during cytokinesis. J Biochem 2006, 140:785-791.
36. Kasahara K., et al. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem 2007, 282:5327-5339.
37. Willard F.S., Crouch M.F. MEK, ERK, and p90RSK are present on mitotic tubulin in Swiss 3T3 cells: a role for the MAP kinase pathway in regulating mitotic exit. Cell Signal 2001, 13:653-664.
38. Balko J.M., et al. Activation of MAPK pathways due to DUSP4 loss promotes cancer stem cell-like phenotypes in basal-like breast cancer. Cancer Res 2013, 73:6346-6358.
39. Morel A.P., et al. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
40. Bernet J.D., et al. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med 2014, 20:265-271.
41. Wu C., Alman B.A. Side population cells in human cancers. Cancer Lett 2008, 268:1-9.
42. Borovski T., et al. Cancer stem cell niche: the place to be. Cancer Res 2011, 71:634-639.
43. Crowell E.F., et al. Engulfment of the midbody remnant after cytokinesis in mammalian cells. J Cell Sci 2014, 127(Pt 17):3840-3851.
44. Driessens G., et al. Defining the mode of tumour growth by clonal analysis. Nature 2012, 488:527-530.
45. Trosko J.E., et al. Ignored hallmarks of carcinogenesis: stem cells and cell-cell communication. Ann N Y Acad Sci 2004, 1028:192-201.
46. Pan H., et al. Autophagic control of cell 'stemness'. EMBO Mol Med 2013, 5:327-331.
47. Johansen T., Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7:279-296.
48. Morais-de-Sa E., Sunkel C. Adherens junctions determine the apical position of the midbody during follicular epithelial cell division. EMBO Rep 2013, 14:696-703.
49. Herszterg S., et al. Interplay between the dividing cell and its neighbors regulates adherens junction formation during cytokinesis in epithelial tissue. Dev Cell 2013, 24:256-270.
50. Morais-de-Sa E., Sunkel C.E. Connecting polarized cytokinesis to epithelial architecture. Cell Cycle 2013, 12:3583-3584.
51. Li D., Kuehn E.W., Prekeris R. Kinesin-2 mediates apical endosome transport during epithelial lumen formation. Cell Logist 2014, 4:e28928.
52. Wang T., et al. Cytokinesis defines a spatial landmark for hepatocyte polarization and apical lumen formation. J Cell Sci 2014, 127(Pt 11):2483-2492.
53. Bryant D.M., et al. A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 2010, 12:1035-1045.
54. Buckley C.E., et al. Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the zebrafish neural rod. EMBO J 2013, 32:30-44.
55. Hehnly H., et al. The centrosome regulates the Rab11-dependent recycling endosome pathway at appendages of the mother centriole. Curr Biol 2012, 22:1944-1950.
56. Westlake C.J., et al. Identification of Rab11 as a small GTPase binding protein for the Evi5 oncogene. Proc Natl Acad Sci U S A 2007, 104:1236-1241.
57. Laflamme C., et al. Evi5 promotes collective cell migration through its Rab-GAP activity. J Cell Biol 2012, 198:57-67.
58. Pohl C., Jentsch S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat Cell Biol 2009, 11:65-70.
59. Mizushima N. Autophagy: process and function. Genes Dev 2007, 21:2861-2873.
60. Abrahamsen H., Stenmark H., Platta H.W. Ubiquitination and phosphorylation of Beclin 1 and its binding partners: tuning class III phosphatidylinositol 3-kinase activity and tumor suppression. FEBS Lett 2012, 586:1584-1591.
61. Mandell M.A., et al. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev Cell 2014, 30:394-409.