Midbody Assembly and Its Regulation During Cytokinesis

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2012 Jan 27

PMID 22278743

Citations 136

Authors

Chi-Kuo Hu

Margaret Coughlin

Timothy J Mitchison

Affiliations

Soon will be listed here.

Abstract

The midbody is a transient structure that connects two daughter cells at the end of cytokinesis, with the principal function being to localize the site of abscission, which physically separates two daughter cells. Despite its importance, understanding of midbody assembly and its regulation is still limited. Here we describe how the structural composition of the midbody changes during progression throughout cytokinesis and explore the functional implications of these changes. Deriving from midzones, midbodies are organized by a set of microtubule interacting proteins that colocalize to a zone of microtubule overlap in the center. We found that these proteins split into three subgroups that relocalize to different parts of the midbody: the bulge, the dark zone, and the flanking zone. We characterized these relocalizations and defined domain requirements for three key proteins: MKLP1, KIF4, and PRC1. Two cortical proteins-anillin and RhoA-localized to presumptive abscission sites in mature midbodies, where they may regulate the endosomal sorting complex required for transport machinery. Finally, we characterized the role of Plk1, a key regulator of cytokinesis, in midbody assembly. Our findings represent the most detailed description of midbody assembly and maturation to date and may help elucidate how abscission sites are positioned and regulated.

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References

Straight A, Cheung A, Limouze J, Chen I, Westwood N, Sellers J . Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science. 2003; 299(5613):1743-7. DOI: 10.1126/science.1081412. View

Gregory S, Ebrahimi S, Milverton J, Jones W, Bejsovec A, Saint R . Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol. 2007; 18(1):25-9. DOI: 10.1016/j.cub.2007.11.050. View

Murata-Hori M, Wang Y . Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. J Cell Biol. 2002; 159(1):45-53. PMC: 2173485. DOI: 10.1083/jcb.200207014. View

Hepler P, Jackson W . Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae Baker. J Cell Biol. 1968; 38(2):437-46. PMC: 2107485. DOI: 10.1083/jcb.38.2.437. View

Boman A, Kuai J, Zhu X, Chen J, Kuriyama R, Kahn R . Arf proteins bind to mitotic kinesin-like protein 1 (MKLP1) in a GTP-dependent fashion. Cell Motil Cytoskeleton. 1999; 44(2):119-32. DOI: 10.1002/(SICI)1097-0169(199910)44:2<119::AID-CM4>3.0.CO;2-C. View

Doxsey S . Molecular links between centrosome and midbody. Mol Cell. 2005; 20(2):170-2. DOI: 10.1016/j.molcel.2005.10.010. View

Goss J, Toomre D . Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. J Cell Biol. 2008; 181(7):1047-54. PMC: 2442215. DOI: 10.1083/jcb.200712137. View

BUCK R, TISDALE J . The fine structure of the mid-body of the rat erythroblast. J Cell Biol. 1962; 13:109-15. PMC: 2106057. DOI: 10.1083/jcb.13.1.109. View

Hutterer A, Glotzer M, Mishima M . Clustering of centralspindlin is essential for its accumulation to the central spindle and the midbody. Curr Biol. 2009; 19(23):2043-9. PMC: 3349232. DOI: 10.1016/j.cub.2009.10.050. View

10.

Field C, Alberts B . Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol. 1995; 131(1):165-78. PMC: 2120607. DOI: 10.1083/jcb.131.1.165. View

11.

Yuce O, Piekny A, Glotzer M . An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol. 2005; 170(4):571-82. PMC: 2171506. DOI: 10.1083/jcb.200501097. View

12.

Pavicic-Kaltenbrunner V, Mishima M, Glotzer M . Cooperative assembly of CYK-4/MgcRacGAP and ZEN-4/MKLP1 to form the centralspindlin complex. Mol Biol Cell. 2007; 18(12):4992-5003. PMC: 2096608. DOI: 10.1091/mbc.e07-05-0468. View

13.

Piel M, Nordberg J, Euteneuer U, Bornens M . Centrosome-dependent exit of cytokinesis in animal cells. Science. 2001; 291(5508):1550-3. DOI: 10.1126/science.1057330. View

14.

Montagnac G, Echard A, Chavrier P . Endocytic traffic in animal cell cytokinesis. Curr Opin Cell Biol. 2008; 20(4):454-61. DOI: 10.1016/j.ceb.2008.03.011. View

15.

Steigemann P, Wurzenberger C, Schmitz M, Held M, Guizetti J, Maar S . Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell. 2009; 136(3):473-84. DOI: 10.1016/j.cell.2008.12.020. View

16.

Matuliene J, Kuriyama R . Role of the midbody matrix in cytokinesis: RNAi and genetic rescue analysis of the mammalian motor protein CHO1. Mol Biol Cell. 2004; 15(7):3083-94. PMC: 452566. DOI: 10.1091/mbc.e03-12-0888. View

17.

Morita E, Sandrin V, Chung H, Morham S, Gygi S, Rodesch C . Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 2007; 26(19):4215-27. PMC: 2230844. DOI: 10.1038/sj.emboj.7601850. View

18.

Straight A, Field C, Mitchison T . Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol Biol Cell. 2004; 16(1):193-201. PMC: 539163. DOI: 10.1091/mbc.e04-08-0758. View

19.

Elia N, Sougrat R, Spurlin T, Hurley J, Lippincott-Schwartz J . 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(12):4846-51. PMC: 3064317. DOI: 10.1073/pnas.1102714108. View

20.

Bastos R, Barr F . Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J Cell Biol. 2010; 191(4):751-60. PMC: 2983065. DOI: 10.1083/jcb.201008108. View