LGN regulates mitotic spindle orientation during epithelial morphogenesis

Journal of Cell Biology

Volumn 189, Issue 2, 2010, Pages 275-288

  Zheng, Zhen ^a,c   Zhu, Huabin ^a   Wan, Qingwen ^a   Liu, Jing ^a,d   Xiao, Zhuoni ^a   Siderovski, David P ^b   Du, Quansheng ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^d WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LGN PROTEIN; NUCLEAR MITOTIC APPARATUS PROTEIN; NUCLEAR PROTEIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL DIVISION; CELL POLARITY; CELL STRAIN; EPITHELIUM; MITOSIS; MITOSIS SPINDLE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION;

ANIMALS; CELL DIVISION; CELL LINE; CELL POLARITY; CELL PROLIFERATION; DOGS; EPITHELIAL CELLS; EPITHELIUM; GENE KNOCKDOWN TECHNIQUES; GENETIC VECTORS; GTP-BINDING PROTEIN ALPHA SUBUNITS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LENTIVIRUS; MEMBRANE GLYCOPROTEINS; MITOTIC SPINDLE APPARATUS; MORPHOGENESIS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PROTEIN KINASE C;

EID: 77951174042     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200910021     Document Type: Article

References (55)

1. Ahringer, J. 2003. Control of cell polarity and mitotic spindle positioning in animal cells. Curr. Opin. Cell Biol. 15:73-81. doi:10.1016/S0955-0674(02)00018-2
2. Baena-López, L.A., A. Baonza, and A. García-Bellido. 2005. The orientation of cell divisions determines the shape of Drosophila organs. Curr. Biol. 15:1640-1644. doi:10.1016/j.cub.2005.07.062
3. Bernard, M.L., Y.K. Peterson, P. Chung, J. Jourdan, and S.M. Lanier. 2001. Selective interaction of AGS3 with G-proteins and the influence of AGS3 on the activation state of G-proteins. J. Biol. Chem. 276:1585-1593. doi:10.1074/jbc.M005291200
4. Betschinger, J., and J.A. Knoblich. 2004. Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol. 14:R674-R685. doi:10.1016/j.cub.2004.08.017
5. Bowman, S.K., R.A. Neumüller, M. Novatchkova, Q. Du, and J.A. Knoblich. 2006. The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell. 10:731-742. doi:10.1016/j.devcel.2006.05. 005
6. Bryant, D.M., and K.E. Mostov. 2008. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9:887-901. doi:10.1038/nrm2523
7. Colombo, K., S.W. Grill, R.J. Kimple, F.S. Willard, D.P. Siderovski, and P. Gönczy. 2003. Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science. 300:1957-1961. doi:10.1126/science.1084146
8. Couwenbergs, C., J.C. Labbé, M. Goulding, T. Marty, B. Bowerman, and M. Gotta. 2007. Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans. J. Cell Biol. 179:15-22. doi:10.1083/jcb.200707085
9. Debnath, J., and J.S. Brugge. 2005. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer. 5:675-688. doi:10.1038/nrc1695
10. Debnath, J., S.K. Muthuswamy, and J.S. Brugge. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 30:256-268. doi:10.1016/S1046-2023(03) 00032-X
11. den Elzen, N., C.V. Buttery, M.P. Maddugoda, G. Ren, and A.S. Yap. 2009. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol. Biol. Cell. 20:3740-3750. doi:10.1091/mbc.E09-01-0023
12. Du, Q., and I.G. Macara. 2004. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell. 119:503-516. doi:10.1016/j.cell.2004.10.028
13. Du, Q., P.T. Stukenberg, and I.G. Macara. 2001. A mammalian Partner of inscuteable binds NuMA and regulates mitotic spindle organization. Nat. Cell Biol. 3:1069-1075. doi:10.1038/ncb1201-1069
14. Du, Q., L. Taylor, D.A. Compton, and I.G. Macara. 2002. LGN blocks the ability of NuMA to bind and stabilize microtubules. A mechanism for mitotic spindle assembly regulation. Curr. Biol. 12:1928-1933. doi:10.1016/S0960- 9822(02)01298-8
15. Gaglio, T., M.A. Dionne, and D.A. Compton. 1997. Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. J. Cell Biol. 138:1055-1066. doi:10.1083/jcb.138.5.1055
16. Gordon, M.B., L. Howard, and D.A. Compton. 2001. Chromosome movement in mitosis requires microtubule anchorage at spindle poles. J. Cell Biol. 152:425-434. doi:10.1083/jcb.152.3.425
17. Grill, S.W., and A.A. Hyman. 2005. Spindle positioning by cortical pulling forces. Dev. Cell. 8:461-465. doi:10.1016/j.devcel.2005.03.014
18. Grill, S.W., J. Howard, E. Schäffer, E.H. Stelzer, and A.A. Hyman. 2003. The distribution of active force generators controls mitotic spindle position. Science. 301:518-521. doi:10.1126/science.1086560
19. Horikoshi, Y., A. Suzuki, T. Yamanaka, K. Sasaki, K. Mizuno, H. Sawada, S. Yonemura, and S. Ohno. 2009. Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J. Cell Sci. 122:1595-1606. doi:10.1242/jcs.043174
20. Izumi, Y., N. Ohta, K. Hisata, T. Raabe, and F. Matsuzaki. 2006. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 8:586-593. doi:10.1038/ncb1409
21. Jaffe, A.B., N. Kaji, J. Durgan, and A. Hall. 2008. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183:625-633. doi:10.1083/jcb.200807121
22. Johnston, C.A., K. Hirono, K.E. Prehoda, and C.Q. Doe. 2009. Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell. 138:1150-1163. doi:10.1016/j.cell.2009. 07.041
23. Kaushik, R., F. Yu, W. Chia, X. Yang, and S. Bahri. 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. doi:10.1091/mbc.E03-04-0212
24. Kisurina-Evgenieva, O., G. Mack, Q. Du, I. Macara, A. Khodjakov, and D.A. Compton. 2004. Multiple mechanisms regulate NuMA dynamics at spindle poles. J. Cell Sci. 117:6391-6400. doi:10.1242/jcs.01568
25. Konno, D., G. Shioi, A. Shitamukai, A. Mori, H. Kiyonari, T. Miyata, and F. Matsuzaki. 2008. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10:93-101. doi:10.1038/ncb1673
26. Martin-Belmonte, F., A. Gassama, A. Datta, W. Yu, U. Rescher, V. Gerke, and K. Mostov. 2007. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell. 128: 383-397. doi:10.1016/j.cell.2006.11.051
27. Mayer, T.U., T.M. Kapoor, S.J. Haggarty, R.W. King, S.L. Schreiber, and T.J. Mitchison. 1999. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science. 286:971-974. doi:10.1126/science.286.5441.971
28. McCudden, C.R., F.S. Willard, R.J. Kimple, C.A. Johnston, M.D. Hains, M.B. Jones, and D.P. Siderovski. 2005. G alpha selectivity and inhibitor function of the multiple GoLoco motif protein GPSM2/LGN. Biochim. Biophys. Acta. 1745:254-264. doi:10.1016/j.bbamcr.2005.05.002
29. Merdes, A., K. Ramyar, J.D. Vechio, and D.W. Cleveland. 1996. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell. 87:447-458. doi:10.1016/S0092-8674(00)81365-3
30. Mitsushima, M., F. Toyoshima, and E. Nishida. 2009. Dual role of Cdc42 in spindle orientation control of adherent cells. Mol. Cell. Biol. 29:2816-2827. doi:10.1128/MCB.01713-08
31. Morin, X., F. Jaouen, and P. Durbec. 2007. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10:1440-1448. doi:10.1038/nn1984
32. Nipper, R.W., K.H. Siller, N.R. Smith, C.Q. Doe, and K.E. Prehoda. 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. doi:10.1073/pnas.0701812104
33. O'Brien, L.E., M.M. Zegers, and K.E. Mostov. 2002. Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3:531-537. doi:10.1038/nrm859
34. Park, D.H., and L.S. Rose. 2008. Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. Dev. Biol. 315:42-54. doi:10.1016/j.ydbio.2007.11.037
35. Rappaport, R. 1971. Cytokinesis in animal cells. Int. Rev. Cytol. 31:169-213. doi:10.1016/S0074-7696(08)60059-5
36. Roegiers, F., and Y.N. Jan. 2004. Asymmetric cell division. Curr. Opin. Cell Biol. 16:195-205. doi:10.1016/j.ceb.2004.02.010
37. Roh, M.H., O. Makarova, C.J. Liu, K. Shin, S. Lee, S. Laurinec, M. Goyal, R. Wiggins, and B. Margolis. 2002. The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157:161-172. doi:10.1083/jcb.200109010
38. Roh, M.H., S. Fan, C.J. Liu, and B. Margolis. 2003. The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J. Cell Sci. 116:2895-2906. doi:10.1242/jcs.00500
39. Saburi, S., I. Hester, E. Fischer, M. Pontoglio, V. Eremina, M. Gessler, S.E. Quaggin, R. Harrison, R. Mount, and H. McNeill. 2008. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 40:1010-1015. doi:10.1038/ng.179
40. Sanada, K., and L.H. Tsai. 2005. G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell. 122:119-131. doi:10.1016/j.cell.2005.05.009
41. Sans, N., P.Y. Wang, Q. Du, R.S. Petralia, Y.X. Wang, S. Nakka, J.B. Blumer, I.G. Macara, and R.J. Wenthold. 2005. mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell Biol. 7:1179-1190. doi:10.1038/ncb1325
42. Segalen, M., and Y. Bellaïche. 2009. Cell division orientation and planar cell polarity pathways. Semin. Cell Dev. Biol. 20:972-977. doi:10.1016/j.semcdb.2009.03.018
43. Siegrist, S.E., and C.Q. Doe. 2005. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell. 123:1323-1335. doi:10.1016/j.cell.2005.09.043
44. Siegrist, S.E., and C.Q. Doe. 2006. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development. 133:529-536. doi:10.1242/dev.02211
45. Siller, K.H., and C.Q. Doe. 2009. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11:365-374. doi:10.1038/ncb0409-365
46. Siller, K.H., C. Cabernard, and C.Q. Doe. 2006. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat. Cell Biol. 8:594-600. doi:10.1038/ncb1412
47. Tall, G.G., and A.G. Gilman. 2005. Resistance to inhibitors of cholinesterase 8A catalyzes release of Galphai-GTP and nuclear mitotic apparatus protein (NuMA) from NuMA/LGN/Galphai-GDP complexes. Proc. Natl. Acad. Sci. USA. 102:16584-16589. doi:10.1073/pnas.0508306102
48. Théry, M., and M. Bornens. 2006. Cell shape and cell division. Curr. Opin. Cell Biol. 18:648-657. doi:10.1016/j.ceb.2006.10.001
49. Théry, M., A. Jiménez-Dalmaroni, V. Racine, M. Bornens, and F. Jülicher. 2007. Experimental and theoretical study of mitotic spindle orientation. Nature. 447:493-496. doi:10.1038/nature05786
50. Toyoshima, F., and E. Nishida. 2007. Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1- and myosin X-dependent manner. EMBO J. 26:1487-1498. doi:10.1038/sj.emboj.7601599
51. Toyoshima, F., S. Matsumura, H. Morimoto, M. Mitsushima, and E. Nishida. 2007. PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Dev. Cell. 13:796-811. doi:10.1016/j.devcel.2007.10.014
52. Willard, F.S., R.J. Kimple, and D.P. Siderovski. 2004. Return of the GDI: the GoLoco motif in cell division. Annu. Rev. Biochem. 73:925-951. doi:10.1146/annurev.biochem.73.011303.073756
53. Willard, F.S., Z. Zheng, J. Guo, G.J. Digby, A.J. Kimple, J.M. Conley, C.A. Johnston, D. Bosch, M.D. Willard, V.J. Watts, 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. doi:10.1074/jbc.M804936200
54. Yasumi, M., T. Sakisaka, T. Hoshino, T. Kimura, Y. Sakamoto, T. Yamanaka, S. Ohno, and Y. Takai. 2005. Direct binding of Lgl2 to LGN during mitosis and its requirement for normal cell division. J. Biol. Chem. 280:6761-6765. doi:10.1074/jbc.C400440200
55. Yu, W., L.E. O'Brien, F. Wang, H. Bourne, K.E. Mostov, and M.M. Zegers. 2003. Hepatocyte growth factor switches orientation of polarity and mode of movement during morphogenesis of multicellular epithelial structures. Mol. Biol. Cell. 14:748-763. doi:10.1091/mbc.E02-06-0350