Long astral microtubules and RACK-1 stabilize polarity domains during maintenance phase in caenorhabditis elegans embryos

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Ai, Erkang ^a,b   Poole, Daniel S ^a   Skop, Ahna R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; GREEN FLUORESCENT PROTEIN; KINESIN; KINESIN ZEN 4; PROTEIN PAR 2; PROTEIN PAR 6; RAB11 PROTEIN; RECEPTOR FOR ACTIVATED C KINASE 1; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CELL RECEPTOR; DYN 1 PROTEIN, C ELEGANS; DYN-1 PROTEIN, C ELEGANS; DYNAMIN; RACK 1 PROTEIN, C ELEGANS; RACK-1 PROTEIN, C ELEGANS;

ARTICLE; ASTRAL MICROTUBULE; CAENORHABDITIS ELEGANS; CELL POLARITY; CENTROSOME; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PROMETAPHASE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; FLUORESCENCE; METABOLISM; METAPHASE; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL POLARITY; DYNAMINS; FLUORESCENCE; METAPHASE; MICROTUBULES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA INTERFERENCE;

EID: 79955443544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019020     Document Type: Article

References (52)

1. Goldstein B, Macara IG, (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13: 609-622.
2. Boyd L, Guo S, Levitan D, Stinchcomb DT, Kemphues KJ, (1996) PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122: 3075-3084.
3. Kemphues K, (2000) PARsing embryonic polarity. Cell 101: 345-348.
4. Grill SW, Gonczy P, Stelzer EH, Hyman AA, (2001) Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409: 630-633.
5. Kimura A, Onami S, (2007) Local cortical pulling-force repression switches centrosomal centration and posterior displacement in C. elegans. J Cell Biol 179: 1347-1354.
6. Labbe JC, McCarthy EK, Goldstein B, (2004) The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J Cell Biol 167: 245-256.
7. Munro EM, (2006) PAR proteins and the cytoskeleton: a marriage of equals. Curr Opin Cell Biol 18: 86-94.
8. Severson AF, Bowerman B, (2003) Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans. J Cell Biol 161: 21-26.
9. Aceto D, Beers M, Kemphues KJ, (2006) Interaction of PAR-6 with CDC-42 is required for maintenance but not establishment of PAR asymmetry in C. elegans. Dev Biol 299: 386-397.
10. Cuenca AA, Schetter A, Aceto D, Kemphues K, Seydoux G, (2003) Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130: 1255-1265.
11. Cowan CR, Hyman AA, (2004) Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu Rev Cell Dev Biol 20: 427-453.
12. Goldstein B, Hird SN, (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122: 1467-1474.
13. O'Connell KF, Maxwell KN, White JG, (2000) The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. Dev Biol 222: 55-70.
14. Wallenfang MR, Seydoux G, (2000) Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408: 89-92.
15. Munro E, Nance J, Priess JR, (2004) Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev Cell 7: 413-424.
16. Nakayama Y, Shivas JM, Poole DS, Squirrell JM, Kulkoski JM, et al. (2009) Dynamin participates in the maintenance of anterior polarity in the Caenorhabditis elegans embryo. Dev Cell 16: 889-900.
17. Motegi F, Velarde NV, Piano F, Sugimoto A, (2006) Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev Cell 10: 509-520.
18. Velarde N, Gunsalus KC, Piano F, (2007) Diverse roles of actin in C. elegans early embryogenesis. BMC Dev Biol 7: 142.
19. Hird SN, White JG, (1993) Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J Cell Biol 121: 1343-1355.
20. Andrews R, Ahringer J, (2007) Asymmetry of early endosome distribution in C. elegans embryos. PLoS One 2: e493.
21. Siegrist SE, Doe CQ, (2007) Microtubule-induced cortical cell polarity. Genes Dev 21: 483-496.
22. Hamill DR, Severson AF, Carter JC, Bowerman B, (2002) Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains. Dev Cell 3: 673-684.
23. Sonneville R, Gonczy P, (2004) Zyg-11 and cul-2 regulate progression through meiosis II and polarity establishment in C. elegans. Development 131: 3527-3543.
24. Tsai MC, Ahringer J, (2007) Microtubules are involved in anterior-posterior axis formation in C. elegans embryos. J Cell Biol 179: 397-402.
25. Jenkins N, Saam JR, Mango SE, (2006) CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 313: 1298-1301.
26. Schonegg S, Constantinescu AT, Hoege C, Hyman AA, (2007) The Rho GTPase-activating proteins RGA-3 and RGA-4 are required to set the initial size of PAR domains in Caenorhabditis elegans one-cell embryos. Proc Natl Acad Sci U S A 104: 14976-14981.
27. Strome S, Powers J, Dunn M, Reese K, Malone CJ, et al. (2001) Spindle dynamics and the role of gamma-tubulin in early Caenorhabditis elegans embryos. Mol Biol Cell 12: 1751-1764.
28. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
29. Kamath RS, Ahringer J, (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
30. Ai E, Poole DS, Skop AR, (2009) RACK-1 directs dynactin-dependent RAB-11 endosomal recycling during mitosis in Caenorhabditis elegans. Mol Biol Cell 20: 1629-1638.
31. Shelton CA, Bowerman B, (1996) Time-dependent responses to glp-1-mediated inductions in early C. elegans embryos. Development 122: 2043-2050.
32. Abramoff MD, Magelhaes, J P, Ram, J S, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
33. Hickson GR, Matheson J, Riggs B, Maier VH, Fielding AB, et al. (2003) Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol Biol Cell 14: 2908-2920.
34. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG, (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913-924.
35. 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.
36. Bellanger JM, Gonczy P, (2003) TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr Biol 13: 1488-1498.
37. Matthews LR, Carter P, Thierry-Mieg D, Kemphues K, (1998) ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J Cell Biol 141: 1159-1168.
38. Werner M, Munro E, Glotzer M, (2007) Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr Biol 17: 1286-1297.
39. Cabernard C, Prehoda KE, Doe CQ, (2010) A spindle-independent cleavage furrow positioning pathway. Nature 467: 91-94.
40. Skop AR, White JG, (1998) The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr Biol 8: 1110-1116.
41. Mishima M, Kaitna S, Glotzer M, (2002) Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2: 41-54.
42. Portereiko MF, Saam J, Mango SE, (2004) ZEN-4/MKLP1 is required to polarize the foregut epithelium. Curr Biol 14: 932-941.
43. Nance J, (2005) PAR proteins and the establishment of cell polarity during C. elegans development. Bioessays 27: 126-135.
44. Suzuki A, Ohno S, (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119: 979-987.
45. Schenk C, Bringmann H, Hyman AA, Cowan CR, (2010) Cortical domain correction repositions the polarity boundary to match the cytokinesis furrow in C. elegans embryos. Development 137: 1743-1753.
46. Mostov K, Su T, ter Beest M, (2003) Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 5: 287-293.
47. Martin SG, McDonald WH, Yates JR 3rd, Chang F, (2005) Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev Cell 8: 479-491.
48. Wittmann T, Waterman-Storer CM, (2001) Cell motility: can Rho GTPases and microtubules point the way? J Cell Sci 114: 3795-3803.
49. Jaulin F, Xue X, Rodriguez-Boulan E, Kreitzer G, (2007) Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev Cell 13: 511-522.
50. Klopfenstein DR, Tomishige M, Stuurman N, Vale RD, (2002) Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109: 347-358.
51. Canman JC, Hoffman DB, Salmon ED, (2000) The role of pre- and post-anaphase microtubules in the cytokinesis phase of the cell cycle. Curr Biol 10: 611-614.
52. Murthy K, Wadsworth P, (2008) Dual role for microtubules in regulating cortical contractility during cytokinesis. J Cell Sci 121: 2350-2359.