Evidence for dynein and astral microtubule-mediated cortical release and transport of Gαi/LGN/NuMA complex in mitotic cells

Molecular Biology of the Cell

Volumn 24, Issue 7, 2013, Pages 901-913

  Zheng, Zhen ^a   Wan, Qingwen ^a   Liu, Jing ^b   Zhu, Huabin ^a   Chu, Xiaogang ^a   Du, Quansheng ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DYNEIN HEAVY CHAIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MAMMALIAN HOMOLOG OF DROSOPHILA PARTNER OF INSCUTEABLE PROTEIN; NUCLEAR MITOTIC APPARATUS PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; METAPHASE; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SPINDLE POLE BODY;

ANIMALS; ANTIGENS, NUCLEAR; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; COS CELLS; CYTOPLASMIC DYNEINS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MULTIPROTEIN COMPLEXES; MUTATION; NOCODAZOLE; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PROTEIN BINDING; RNA INTERFERENCE; TUBULIN MODULATORS;

MAMMALIA;

EID: 84875442343     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-06-0458     Document Type: Article

References (80)

1. Adames NR, Cooper JA (2000). Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J Cell Biol 149, 863-874. (Pubitemid 30327238)
2. Ahringer J (2003). Control of cell polarity and mitotic spindle positioning in animal cells. Curr Opin Cell Biol 15, 73-81. (Pubitemid 36044718)
3. Ben-Yair R, Kahane N, Kalcheim C (2011). LGN-dependent orientation of cell divisions in the dermomyotome controls lineage segregation into muscle and dermis. Development 138, 4155-4166.
4. Bowman SK, Neumuller RA, Novatchkova M, Du Q, Knoblich JA (2006). The Drosophila NuMA homolog Mud regulates spindle orientation in asymmetric cell division. Dev Cell 10, 731-742. (Pubitemid 43779107)
5. Busson S, Dujardin D, Moreau A, Dompierre J, De Mey JR (1998). Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells. Curr Biol 8, 541-544. (Pubitemid 28203076)
6. Carminati JL, Stearns T (1997). Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J Cell Biol 138, 629-641. (Pubitemid 27349843)
7. Chen CA, Manning DR (2001). Regulation of G proteins by covalent modification. Oncogene 20, 1643-1652. (Pubitemid 32336853)
8. Chia W, Somers WG, Wang H (2008). Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J Cell Biol 180, 267-272. (Pubitemid 351185913)
9. Collins ES, Balchand SK, Faraci JL, Wadsworth P, Lee WL (2012). Cell cycle-regulated cortical dynein/dynactin promotes symmetric cell division by differential pole motion in anaphase. Mol Biol Cell 23, 3380-3390.
10. Colombo K, Grill SW, Kimple RJ, Willard FS, Siderovski DP, Gonczy P (2003). Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300, 1957-1961. (Pubitemid 36734605)
11. Couwenbergs C, Labbe JC, Goulding M, Marty T, Bowerman B, Gotta M (2007). Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans. J Cell Biol 179, 15-22. (Pubitemid 47606679)
12. Dujardin DL, Vallee RB (2002). Dynein at the cortex. Curr Opin Cell Biol 14, 44-49. (Pubitemid 34131655)
13. Du Q, Macara IG (2004). Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119, 503-516. (Pubitemid 39482350)
14. Du Q, Stukenberg PT, Macara IG (2001). A mammalian Partner of Inscuteable binds NuMA and regulates mitotic spindle organization. Nat Cell Biol 3, 1069-1075. (Pubitemid 33130457)
15. Du Q, Taylor L, Compton DA, Macara IG (2002). LGN blocks the ability of NuMA to bind and stabilize microtubules. A mechanism for mitotic spindle assembly regulation. Curr Biol 12, 1928-1933. (Pubitemid 35426706)
16. El-Hashash AH, Turcatel G, Al Alam D, Buckley S, Tokumitsu H, Bellusci S, Warburton D (2011). Eya1 controls cell polarity, spindle orientation, cell fate and Notch signaling in distal embryonic lung epithelium. Development 138, 1395-1407.
17. El-Hashash AH, Warburton D (2011). Cell polarity and spindle orientation in the distal epithelium of embryonic lung. Dev Dynam 240, 441-445.
18. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB, Wang Y, Vallee RB (2000). A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat Cell Biol 2, 784-791.
19. Fink J et al. (2011). External forces control mitotic spindle positioning. Nat Cell Biol 13, 771-U401.
20. Fuse N, Hisata K, Katzen AL, Matsuzaki F (2003). Heterotrimeric G proteins regulate daughter cell size asymmetry in Drosophila neuroblast divisions. Curr Biol 13, 947-954. (Pubitemid 36632144)
21. Gaetz J, Kapoor TM (2004). Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J Cell Biol 166, 465-471. (Pubitemid 39097165)
22. Gillies TE, Cabernard C (2011). Cell division orientation in animals. Curr Biol 21, R599-R609.
23. Gonczy P (2008). Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9, 355-366. (Pubitemid 351574196)
24. Gotta M, Ahringer J (2001). Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat Cell Biol 3, 297-300. (Pubitemid 32201325)
25. Gotta M, Dong Y, Peterson YK, Lanier SM, Ahringer J (2003). Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr Biol 13, 1029-1037. (Pubitemid 36726038)
26. 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. (Pubitemid 32154816)
27. Grill SW, Howard J, Schaffer E, Stelzer EH, Hyman AA (2003). The distribution of active force generators controls mitotic spindle position. Science 301, 518-521. (Pubitemid 36900309)
28. Grill SW, Hyman AA (2005). Spindle positioning by cortical pulling forces. Dev Cell 8, 461-465. (Pubitemid 40450736)
29. Hao Y, Du QS, Chen XY, Zheng Z, Balsbaugh JL, Maitra S, Shabanowitz J, Hunt DF, Macara IG (2010). Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical pins. Curr Biol 20, 1809-1818.
30. Hendricks AG, Lazarus JE, Perlson E, Gardner MK, Odde DJ, Goldman YE, Holzbaur ELF (2012). Dynein tethers and stabilizes dynamic microtubule plus ends. Curr Biol 22, 632-637.
31. Izumi Y, Ohta N, Hisata K, Raabe T, Matsuzaki F (2006). Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat Cell Biol 8, 586-593. (Pubitemid 43827351)
32. Jordan MA, Thrower D, Wilson L (1992). Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis. J Cell Sci 102, 401-416.
33. Kardon JR, Vale RD (2009). Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10, 854-865.
34. Kaushik R, Yu F, Chia W, Yang X, Bahri S (2003). Subcellular localization of LGN during mitosis: evidence for its cortical localization in mitotic cell culture systems and its requirement for normal cell cycle progression. Mol Biol Cell 14, 3144-3155. (Pubitemid 37013116)
35. Kimura K, Kimura A (2011). Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proc Natl Acad Sci USA 108, 137-142.
36. Kisselev AF, Goldberg AL (2001). Proteasome inhibitors: from research tools to drug candidates. Chem Biol 8, 739-758. (Pubitemid 32752454)
37. Kisurina-Evgenieva O, Mack G, Du Q, Macara I, Khodjakov A, Compton DA (2004). Multiple mechanisms regulate NuMA dynamics at spindle poles. J Cell Sci 117, 6391-6400. (Pubitemid 40214565)
38. Kiyomitsu T, Cheeseman IM (2012). Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol 14, 311-317.
39. Knoblich JA (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597. (Pubitemid 351253698)
40. Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F (2008). Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol 10, 93-101.
41. Kotak S, Busso C, Gonczy P (2012). Cortical dynein is critical for proper spindle positioning in human cells. J Cell Biol 199, 97-110.
42. Kunda P, Baum B (2009). The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol 19, 174-179.
43. Laan L, Pavin N, Husson J, Romet-Lemonne G, van Duijn M, Lopez MP, Vale RD, Julicher F, Reck-Peterson SL, Dogterom M (2012). Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 148, 502-514.
44. Lanier SM (2004). AGS proteins, GPR motifs and the signals processed by heterotrimeric G proteins. Biol Cell 96, 369-372. (Pubitemid 38807903)
45. Matsumura S, Hamasaki M, Yamamoto T, Ebisuya M, Sato M, Nishida E, Toyoshima F (2012). ABL1 regulates spindle orientation in adherent cells and mammalian skin. Nat Commun 3, 626.
46. Mayer TU, Kapoor TM, Haggarty SJ, King RW, Schreiber SL, Mitchison TJ (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974.
47. McCarthy EK, Goldstein B (2006). Asymmetric spindle positioning. Curr Opin Cell Biol 18, 79-85. (Pubitemid 43107612)
48. Merdes A, Ramyar K, Vechio JD, Cleveland DW (1996). A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447-458. (Pubitemid 26374319)
49. Morin X, Bellaiche Y (2011). Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev Cell 21, 102-119.
50. Morin X, Jaouen F, Durbec P (2007). Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat Neurosci 10, 1440-1448. (Pubitemid 350014675)
51. Nguyen-Ngoc T, Afshar K, Gonczy P (2007). Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat Cell Biol 9, 1294-1302. (Pubitemid 350042361)
52. Nipper RW, Siller KH, Smith NR, Doe CQ, Prehoda KE (2007). Galphai generates multiple Pins activation states to link cortical polarity and spindle orientation in Drosophila neuroblasts. Proc Natl Acad Sci USA 104, 14306-14311. (Pubitemid 350003258)
53. O'Connell CB, Wang YL (2000). Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. Mol Biol Cell 11, 1765-1774. (Pubitemid 30307911)
54. Parmentier ML, Woods D, Greig S, Phan PG, Radovic A, Bryant P, O'Kane CJ (2000). Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J Neurosci 20, RC84.
55. Pecreaux J, Roper JC, Kruse K, Julicher F, Hyman AA, Grill SW, Howard J (2006). Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr Biol 16, 2111-2122. (Pubitemid 44767627)
56. Peyre E, Jaouen F, Saadaoui M, Haren L, Merdes A, Durbec P, Morin X (2011). A lateral belt of cortical LGN and NuMA guides mitotic spindle movements and planar division in neuroepithelial cells. J Cell Biol 193, 141-154.
57. Poulson ND, Lechler T (2010). Robust control of mitotic spindle orientation in the developing epidermis. J Cell Biol 191, 915-922.
58. Sachdev P, Menon S, Kastner DB, Chuang JZ, Yeh TY, Conde C, Caceres A, Sung CH, Sakmar TP (2007). G protein beta gamma subunit interaction with the dynein light-chain component Tctex-1 regulates neurite outgrowth. EMBO J 26, 2621-2632. (Pubitemid 46884283)
59. Samora CP, Mogessie B, Conway L, Ross JL, Straube A, McAinsh AD (2011). MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat Cell Biol 13, U1040-U1059.
60. Schaefer M, Petronczki M, Dorner D, Forte M, Knoblich JA (2001). Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107, 183-194. (Pubitemid 33035945)
61. Schaefer M, Shevchenko A, Shevchenko A, Knoblich JA (2000). A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr Biol 10, 353-362. (Pubitemid 30213381)
62. Siller KH, Cabernard C, Doe CQ (2006). The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat Cell Biol 8, 594-600. (Pubitemid 43827352)
63. Siller KH, Doe CQ (2009). Spindle orientation during asymmetric cell division. Nat Cell Biol 11, 365-374.
64. Spector I, Shochet NR, Kashman Y, Groweiss A (1983). Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493-495. (Pubitemid 13189272)
65. Srinivasan DG, Fisk RM, Xu H, van den Heuvel S (2003). A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C. elegans. Genes Dev 17, 1225-1239. (Pubitemid 36583166)
66. Thery M, Racine V, Pepin A, Piel M, Chen Y, Sibarita JB, Bornens M (2005). The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7, 947-953. (Pubitemid 41486267)
67. Thyagarajan K, Afshar K, Gonczy P (2011). Polarity mediates asymmetric trafficking of the G beta heterotrimeric G-protein subunit GPB-1 in C. elegans embryos. Development 138, 2773-2782.
68. Toyoshima F, Matsumura S, Morimoto H, Mitsushima M, Nishida E (2007). PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Dev Cell 13, 796-811. (Pubitemid 350163038)
69. Toyoshima F, Nishida E (2007). Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1- and myosin X-dependent manner. EMBO J 26, 1487-1498. (Pubitemid 46480928)
70. van der Voet M, Berends CW, Perreault A, Nguyen-Ngoc T, Gonczy P, Vidal M, Boxem M, van den Heuvel S (2009). NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Galpha. Nat Cell Biol 11, 269-277.
71. Wan QW, Liu J, Zheng Z, Zhu HB, Chu XG, Dong Z, Huang S, Du QS (2012). Regulation of myosin activation during cell-cell contact formation by Par3-Lgl antagonism: entosis without matrix detachment. Mol Biol Cell 23, 2076-2091.
72. Werts AD, Roh-Johnson M, Goldstein B (2011). Dynamic localization of C. elegans TPR-GoLoco proteins mediates mitotic spindle orientation by extrinsic signaling. Development 138, 4411-4422.
73. Willard FS et al. (2008). A point mutation to Galphai selectively blocks GoLoco motif binding: direct evidence for Galpha. GoLoco complexes in mitotic spindle dynamics. J Biol Chem 283, 36698-36710.
74. Willard FS, Kimple RJ, Siderovski DP (2004). Return of the GDI: the GoLoco motif in cell division. Annu Rev Biochem 73, 925-951.
75. Williams SE, Beronja S, Pasolli HA, Fuchs E (2011). Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 470, 353-358.
76. Woodard GE, Huang NN, Cho H, Miki T, Tall GG, Kehrl JH (2010). Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol Cell Biol 30, 3519-3530.
77. Xiao ZN, Wan QW, Du QS, Zheng Z (2012). Galpha/LGN-mediated asymmetric spindle positioning does not lead to unequal cleavage of the mother cell in 3-D cultured MDCK cells. Biochem Biophys Res Commun 420, 888-894.
78. Yu F, Kuo CT, Jan YN (2006). Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51, 13-20. (Pubitemid 43963345)
79. Zheng Z, Zhu HB, Wan QW, Liu J, Xiao ZN, Siderovski DP, Du QS (2010). LGN regulates mitotic spindle orientation during epithelial morphogenesis. J Cell Biol 189, 275-288.
80. Zhu JW, Wen WY, Zheng Z, Shang Y, Wei ZY, Xiao ZN, Pan Z, Du QS, Wang WN, Zhang MJ (2011). LGN/mInsc and LGN/NuMA complex structures suggest distinct functions in asymmetric cell division for the Par3/mInsc/LGN and G alpha i/LGN/NuMA pathways. Mol Cell 43, 418-431.