A postmitotic function and distinct localization mechanism for centralspindlin at a stable intercellular bridge

Developmental Biology

Volumn 376, Issue 1, 2013, Pages 13-22

  Zhou, Kang ^a   Rolls, Melissa M ^a   Hanna Rose, Wendy ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

C. elegans; CYK 4; Intercellular bridge; Microtubules; ZEN 4

Indexed keywords

CELL CYCLE PROTEIN; CENTRALSPINDLIN; CYK 4 PROTEIN; F ACTIN; REGULATOR PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ZEN 4 PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE PROGRESSION; CELL JUNCTION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINESIS; GERM LINE; GONAD; HERMAPHRODITIC SPECIES; MICROTUBULE; MITOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN TARGETING; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

EID: 84875388642     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.01.020     Document Type: Article

References (45)

1. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
2. Canman J.C., Lewellyn L., Laband K., Smerdon S.J., Desai A., Bowerman B., Oegema K. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 2008, 322:1543-1546.
3. Cuenca A.A., Schetter A., Aceto D., Kemphues K., Seydoux G. Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 2003, 130:1255-1265.
4. D'Avino P.P. How to scaffold the contractile ring for a safe cytokinesis-lessons from Anillin-related proteins. J. Cell Sci. 2009, 122:1071-1079.
5. D'Avino P.P., Takeda T., Capalbo L., Zhang W., Lilley K.S., Laue E.D., Glover D.M. Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J. Cell Sci. 2008, 121:1151-1158.
6. Frenette P., Haines E., Loloyan M., Kinal M., Pakarian P., Piekny A. An Anillin-Ect2 complex stabilizes central spindle microtubules at the cortex during cytokinesis. PLoS One 2012, 7:e34888.
7. Greenbaum M.P., Ma L., Matzuk M.M. Conversion of midbodies into germ cell intercellular bridges. Dev. Biol. 2007, 305:389-396.
8. Gregory S.L., Ebrahimi S., Milverton J., Jones W.M., Bejsovec A., Saint R. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr. Biol. 2008, 18:25-29.
9. Gumienny T.L., Lambie E., Hartwieg E., Horvitz H.R., Hengartner M.O. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999, 126:1011-1022.
10. Haglund K., Nezis I.P., Stenmark H. Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development. Commun. Integr. Biol 2011, 4:1-9.
11. Hall D.H., Winfrey V.P., Blaeuer G., Hoffman L.H., Furuta T., Rose K.L., Hobert O., Greenstein D. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 1999, 212:101-123.
12. Hime G.R., Brill J.A., Fuller M.T. Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci. 1996, 109(12):2779-2788.
13. Hirsh D., Oppenheim D., Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 1976, 49:200-219.
14. Hutterer A., Glotzer M., Mishima M. Clustering of centralspindlin is essential for its accumulation to the central spindle and the midbody. Curr. Biol 2009, 19:2043-2049.
15. Jantsch-Plunger V., Gonczy P., Romano A., Schnabel H., Hamill D., Schnabel R., Hyman A.A., Glotzer M. CYK-4: a Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 2000, 149:1391-1404.
16. Jaramillo-Lambert A., Ellefson M., Villeneuve A.M., Engebrecht J. Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 2007, 308:206-221.
17. Kamath R.S., Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30:313-321.
18. Liu J., Maduzia L.L., Shirayama M., Mello C.C. NMY-2 maintains cellular asymmetry and cell boundaries, and promotes a SRC-dependent asymmetric cell division. Dev. Biol. 2010, 339:366-373.
19. Loria A., Longhini K.M., Glotzer M. The RhoGAP Domain of CYK-4 has an essential role in RhoA activation. Curr. Biol 2012.
20. Maddox A.S., Habermann B., Desai A., Oegema K. Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 2005, 132:2837-2848.
21. Matuliene J., Kuriyama R. Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol. Biol Cell 2002, 13:1832-1845.
22. McCarter J., Bartlett B., Dang T., Schedl T. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 1999, 205:111-128.
23. Miller A.L., Bement W.M. Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 2009, 11:71-77.
24. Motegi F., Velarde N.V., Piano F., Sugimoto A. Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev. Cell. 2006, 10:509-520.
25. Ong S., Foote C., Tan C. Mutations of DMYPT cause over constriction of contractile rings and ring canals during Drosophila germline cyst formation. Dev. Biol 2010, 346:161-169.
26. Ong S., Tan C. Germline cyst formation and incomplete cytokinesis during Drosophila melanogaster oogenesis. Dev. Biol 2010, 337:84-98.
27. 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, 18:4992-5003.
28. Piekny A.J., Glotzer M. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 2008, 18:30-36.
29. Piekny A.J., Maddox A.S. The myriad roles of Anillin during cytokinesis. Semin Cell Dev. Biol. 2010, 21:881-891.
30. Piekny A.J., Mains P.E. Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J. Cell Sci 2002, 115:2271-2282.
31. Portereiko M.F., Saam J., Mango S.E. ZEN-4/MKLP1 is required to polarize the foregut epithelium. Curr. Biol. 2004, 14:932-941.
32. Raich W.B., Moran A.N., Rothman J.H., Hardin J. Cytokinesis and midzone microtubule organization in Caenorhabditis elegans require the kinesin-like protein ZEN-4. Mol. Biol Cell. 1998, 9:2037-2049.
33. Ratheesh A., Gomez G.A., Priya R., Verma S., Kovacs E.M., Jiang K., Brown N.H., Akhmanova A., Stehbens S.J., Yap A.S. Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol. 2012, 14(8):818-828.
34. Robinson D.N., Cant K., Cooley L. Morphogenesis of Drosophila ovarian ring canals. Development 1994, 120:2015-2025.
35. Severson A.F., Hamill D.R., Carter J.C., Schumacher J., Bowerman B. The aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis. Curr. Biol. 2000, 10:1162-1171.
36. Sonnichsen, B., L.B. Koski, A. Walsh, P. Marschall, B. Neumann, M. Brehm, A.M. Alleaume, J. Artelt, P. Bettencourt, E. Cassin, M. Hewitson, C. Holz, M. Khan, S. Lazik, C. Martin, B. Nitzsche, M. Ruer, J. Stamford, M. Winzi, R. Heinkel, M. Roder, J. Finell, H. Hantsch, S.J. Jones, M. Jones, F. Piano, K.C. Gunsalus, K. Oegema, P. Gonczy, A. Coulson, A.A. Hyman, and C.J. Echeverri, Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature, 2005. 434(7032): p. 462-9.
37. Stiernagle T. Maintenance of C. elegans. WormBook 2006, 1-11.
38. Su K.C., Takaki T., Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell 2011, 21:1104-1115.
39. Weber J.E., Russell L.D. A study of intercellular bridges during spermatogenesis in the rat. Am. J. Anat. 1987, 180:1-24.
40. Wolke U., Jezuit E.A., Priess J.R. Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 2007, 134:2227-2236.
41. Xu X., Vogel B.E. A secreted protein promotes cleavage furrow maturation during cytokinesis. Curr. Biol. 2011, 21:114-119.
42. Yuce O., Piekny A., Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 2005, 170:571-582.
43. Zhang L., Maddox A.S. Anillin. Curr. Biol. 2010, 20:R135-R136.
44. Zhou K., Rolls M.M., Hall D.H., Malone C.J., Hanna-Rose W. A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J. Cell Biol. 2009, 186:229-241.
45. Zonies S., Motegi F., Hao Y., Seydoux G. Symmetry breaking and polarization of the C. elegans zygote by the polarity protein PAR-2. Development 2010, 137:1669-1677.