Redundant mechanisms recruit actin into the contractile ring in silkworm spermatocytes

PLoS Biology

Volumn 6, Issue 9, 2008, Pages 1927-1941

  Chen, Wei ^a   Foss, Margit ^a   Tseng, Kuo Fu ^a   Zhang, Dahong ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; INSECT PROTEIN; MYOSIN; PACLITAXEL; TUBULIN MODULATOR;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CYTOKINESIS; ENZYME ACTIVITY; MICROTUBULE; NONHUMAN; PROTEIN AGGREGATION; SILKWORM; SPERMATOCYTE; ANIMAL; BOMBYX; CELL CULTURE; CELL POLARITY; CYTOLOGY; CYTOSKELETON; HUMAN; MALE; METABOLISM; PHYSIOLOGY; SPINDLE APPARATUS; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

BOMBYX MORI;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT; BOMBYX; CELL POLARITY; CELLS, CULTURED; CYTOKINESIS; CYTOSKELETON; HUMANS; INSECT PROTEINS; MALE; MICROTUBULES; MYOSINS; PACLITAXEL; RHOA GTP-BINDING PROTEIN; SPERMATOCYTES; SPINDLE APPARATUS; TUBULIN MODULATORS;

EID: 54749131947     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060209     Document Type: Article

References (68)

1. D'Avino PP, Savoian MS, Glover DM (2005) Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J Cell Sci 118: 1549-1558.
2. Burgess DR, Chang F (2005) Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol 15: 156-162.
3. Eggert US, Mitchison TJ, Field CM (2006) Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 75: 543-566.
4. Glotzer M (2004) Cleavage furrow positioning. J Cell Biol 164: 347-351.
5. Piekny A, Werner M, Glotzer M (2005) Cytokinesis: welcome to the Rho zone. Trends Cell Biol 15: 651-658.
6. Alsop GB, Zhang D (2003) Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage. J Cell Biol 162: 383-390.
7. Canman JC, Wells WA (2004) Rappaport furrows on our minds: the ASCB Cytokinesis Meeting Burlington, VT July 22-25, 2004. J Cell Biol 166: 943-948.
8. Wolpert L (1960) The mechanics and mechanism of cleavage. Int Rev Cytol 10: 163-216.
9. White JG, Borisy GG (1983) On the mechanisms of cytokinesis in animal cells. J Theor Biol 101: 289-316.
10. Yoshigaki T (1999) Simulation of density gradients of astral microtubules at cell surface in cytokinesis of sea urchin eggs. J Theor Biol 196: 211-224.
11. Hiramoto Y (1990) Mechanical properties of the cortex before and during cleavage. Ann N Y Acad Sci 582: 22-30.
12. Schroeder TE (1981) The origin of cleavage forces in dividing eggs. A mechanism in two steps. Exp Cell Res 134: 231-240.
13. 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.
14. Hird SN, White JG (1993) Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J Cell Biol 121: 1343-1355.
15. Kurz T, Pintard L, Willis JH, Hamill DR, Gonczy P, et al. (2002) Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295: 1294-1298.
16. Krendel M, Zenke FT, Bokoch GM (2002) Nucleotide exchange factor GEFH1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4: 294-301.
17. Zhou M, Wang YL (2008) Distinct pathways for the early recruitment of myosin II and actin to the cytokinetic furrow. Mol Biol Cell 19: 318-326.
18. Rappaport R (1961) Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 148: 81-89.
19. Rieder CL, Khodjakov A, Paliulis LV, Fortier TM, Cole RW, et al. (1997) Mitosis in vertebrate somatic cells with two spindles: implications for the metaphase/anaphase transition checkpoint and cleavage. Proc Natl Acad Sci U S A 94: 5107-5112.
20. Canman JC, Cameron LA, Maddox PS, Straight A, Tirnauer JS, et al. (2003) Determining the position of the cell division plane. Nature 424: 1074-1078.
21. Hu CK, Coughlin M, Field CM, Mitchison TJ (2008) Cell polarization during monopolar cytokinesis. J Cell Biol 181: 195-202.
22. Cao LG, Wang YL (1996) Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol Biol Cell 7: 225-232.
23. Bement WM, Benink HA, von Dassow G (2005) A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol 170: 91-101.
24. Saint R, Somers WG (2003) Animal cell division: a fellowship of the double ring? J Cell Sci 116: 4277-4281.
25. Bringmann H, Cowan CR, Kong J, Hyman AA (2007) LET-99, GOA-1/GPA-16, and GPR-1/2 are required for aster-positioned cytokinesis. Curr Biol 17: 185-191.
26. Bringmann H, Hyman AA (2005) A cytokinesis furrow is positioned by two consecutive signals. Nature 436: 731-734.
27. 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.
28. 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.
29. 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.
30. Bonaccorsi S, Giansanti MG, Gatti M (1998) Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J Cell Biol 142: 751-761.
31. Yamashiki N, Kawamura N (1998) Behavior of centrioles during meiosis in the male silkworm, Bombyx mori (Lepidoptera). Dev Growth Differ 40: 619-630.
32. Alsop GB, Zhang D (2004) Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J Cell Sci 117: 1591-1602.
33. Kishi K, Sasaki T, Kuroda S, Itoh T, Takai Y (1993) Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J Cell Biol 120: 1187-1195.
34. Foe VE, Field CM, Odell GM (2000) Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127: 1767-1787.
35. Cao LG, Wang YL (1990) Mechanism of the formation of contractile ring in dividing cultured animal cells. II. Cortical movement of microinjected actin filaments. J Cell Biol 111: 1905-1911.
36. DeBiasio RL, LaRocca GM, Post PL, Taylor DL (1996) Myosin II transport, organization, and phosphorylation: evidence for cortical flow/solation- contraction coupling during cytokinesis and cell locomotion. Mol Biol Cell 7: 1259-1282.
37. Yumura S (2001) Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells. J Cell Biol 154: 137-146.
38. Murthy K, Wadsworth P (2005) Myosin-II-dependent localization and dynamics of F-actin during cytokinesis. Curr Biol 15: 724-731.
39. Koppel DE, Oliver JM, Berlin RD (1982) Surface functions during mitosis. III. Quantitative analysis of ligand-receptor movement into the cleavage furrow: diffusion vs. flow. J Cell Biol 93: 950-960.
40. Ng MM, Chang F, Burgess DR (2005) Movement of membrane domains and requirement of membrane signaling molecules for cytokinesis. Dev Cell 9: 781-790.
41. Bauer T, Motosugi N, Miura K, Sabe H, Hiiragi T (2008) Dynamic rearrangement of surface proteins is essential for cytokinesis. Genesis 46: 152-162.
42. Rusan NM, Wadsworth P (2005) Centrosome fragments and microtubules are transported asymmetrically away from division plane in anaphase. J Cell Biol 168: 21-28.
43. Huisman SM, Segal M (2005) Cortical capture of microtubules and spindle polarity in budding yeast - where's the catch? J Cell Sci 118: 463-471.
44. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, et al. (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5: 599-609.
45. Janson ME, de Dood ME, Dogterom M (2003) Dynamic instability of microtubules is regulated by force. J Cell Biol 161: 1029-1034.
46. Gregory SL, Ebrahimi S, Milverton J, Jones WM, Bejsovec A, et al. (2008) Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol 18: 25-29.
47. Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12: 63-71.
48. Keating TJ, Peloquin JG, Rodionov VI, Momcilovic D, Borisy GG (1997) Microtubule release from the centrosome. Proc Natl Acad Sci U S A 94: 5078-5083.
49. Zimmerman WC, Sillibourne J, Rosa J, Doxsey SJ (2004) Mitosis-specific anchoring of gamma tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol Biol Cell 15: 3642-3657.
50. Waterman-Storer C, Duey DY, Weber KL, Keech J, Cheney RE, et al. (2000) Microtubules remodel actomyosin networks in Xenopus egg extracts via two mechanisms of F-actin transport. J Cell Biol 150: 361-376.
51. Gavin RH (1997) Microtubule-microfilament synergy in the cytoskeleton. Int Rev Cytol 173: 207-242.
52. Sider JR, Mandato CA, Weber KL, Zandy AJ, Beach D, et al. (1999) Direct observation of microtubule-f-actin interaction in cell free lysates. J Cell Sci 112: 1947-1956.
53. Shannon KB, Canman JC, Ben Moree C, Tirnauer JS, Salmon ED (2005) Taxol-stabilized microtubules can position the cytokinetic furrow in mammalian cells. Mol Biol Cell 16: 4423-4436.
54. Yonetani A, Lustig RJ, Moseley JB, Takeda T, Goode BL, et al. (2008) Regulation and targeting of the fission yeast formin cdc12p in cytokinesis. Mol Biol Cell 19: 2208-2219.
55. Vavylonis D, Wu JQ, Hao S, O'Shaughnessy B, Pollard TD (2008) Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319: 97-100.
56. Noguchi T, Mabuchi I (2001) Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. J Cell Sci 114: 401-412.
57. Feierbach B, Verde F, Chang F (2004) Regulation of a formin complex by the microtubule plus end protein tea1p. J Cell Biol 165: 697-707.
58. Nishimura Y, Yonemura S (2006) Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 119: 104-114.
59. Somers WG, Saint R (2003) A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell 4: 29-39.
60. Yuce O, Piekny A, Glotzer M (2005) An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 170: 571-582.
61. Zavortink M, Contreras N, Addy T, Bejsovec A, Saint R (2005) Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J Cell Sci 118: 5381-5392.
62. Zhao WM, Fang G (2005) MgcRacGAP controls the assembly of the contractile ring and the initiation of cytokinesis. Proc Natl Acad Sci U S A 102: 13158-13163.
63. D'Avino PP, Takeda T, Capalbo L, Zhang W, Lilley KS, et al. (2008) Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J Cell Sci 121: 1151-1158.
64. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
65. Chen Q, Lakshmikanth GS, Spudich JA, De Lozanne A (2007) The localization of inner centromeric protein (INCENP) at the cleavage furrow is dependent on Kif12 and involves interactions of the N terminus of INCENP with the actin cytoskeleton. Mol Biol Cell 18: 3366-3374.
66. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937-1940.
67. Zhang D, Nicklas RB (1999) Micromanipulation of chromosomes and spindles in insect spermatocytes. Methods Cell Biol 61: 209-218.
68. Peloquin J, Komarova Y, Borisy G (2005) Conjugation of fluorophores to tubulin. Nat Methods 2: 299-303.