Regulation of myosin activation during cell-cell contact formation by Par3-Lgl antagonism: Entosis without matrix detachment

Molecular Biology of the Cell

Volumn 23, Issue 11, 2012, Pages 2076-2091

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

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; MYOSIN; MYOSIN II; PROTEIN LETHAL GIANT LARVAE 1; PROTEIN LETHAL GIANT LARVAE 2; PROTEIN PARTITIONING DEFECTIVE 3; RHO FACTOR; UNCLASSIFIED DRUG;

ANEUPLOIDY; ANIMAL CELL; ARTICLE; BREAST EPITHELIUM; CELL CULTURE; CELL DEATH; CELL INTERACTION; CONTROLLED STUDY; ENTOSIS; HOST CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; KIDNEY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; CELL COMMUNICATION; CELL LINE; DOGS; ENDOCYTOSIS; ENTOSIS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; INTERCELLULAR JUNCTIONS; MEMBRANE PROTEINS; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; PHOSPHORYLATION; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 84861680016     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-11-0940     Document Type: Article

References (46)

1. Adams CL, Chen YT, Smith SJ, Nelson WJ (1998). Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 142, 1105-1119. (Pubitemid 28402064)
2. Atwood SX, Prehoda KE (2009). aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr Biol 19, 723-729.
3. Barros CS, Phelps CB, Brand AH (2003). Drosophila nonmuscle myosin II promotes the asymmetric segregation of cell fate determinants by cortical exclusion rather than active transport. Dev Cell 5, 829-840. (Pubitemid 37527684)
4. Betschinger J, Mechtler K, Knoblich JA (2003). The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422, 326-330. (Pubitemid 36378361)
5. Cavey M, Lecuit T (2009). Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb Perspect Biol 1, a002998.
6. Cavey M, Rauzi M, Lenne PF, Lecuit T (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453, 751-756. (Pubitemid 351793782)
7. Du Q, Macara IG (2004). Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119, 503-516. (Pubitemid 39482350)
8. 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)
9. Ehrlich JS, Hansen MD, Nelson WJ (2002). Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev Cell 3, 259-270.
10. Florey O, Krajcovic M, Sun Q, Overholtzer M (2010). Entosis. Curr Biol 20, R88-r89.
11. Green KJ, Getsios S, Troyanovsky S, Godsel LM (2010). Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol 2, a000125.
12. Hansen MD, Ehrlich JS, Nelson WJ (2002). Molecular mechanism for orienting membrane and actin dynamics to nascent cell-cell contacts in epithelial cells. J Biol Chem 277, 45371-45376. (Pubitemid 36159145)
13. Hao Y, Du Q, Chen X, 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.
14. Hurd TW, Gao L, Roh MH, Macara IG, Margolis B (2003). Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol 5, 137-142. (Pubitemid 36210848)
15. Ishiuchi T, Takeichi M (2011). Willin and Par3 cooperatively regulate epithelial apical constriction through aPKC-mediated ROCK phosphorylation. Nat Cell Biol 13, 860-866.
16. Ivanov AI, Hunt D, Utech M, Nusrat A, Parkos CA (2005). Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol Biol Cell 16, 2636-2650. (Pubitemid 40741212)
17. Ivanov AI, McCall IC, Parkos CA, Nusrat A (2004). Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell 15, 2639-2651. (Pubitemid 38691854)
18. Izumi Y, Hirose T, Tamai Y, Hirai S, Nagashima Y, Fujimoto T, Tabuse Y, Kemphues KJ, Ohno S (1998). An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol 143, 95-106. (Pubitemid 28480520)
19. Joberty G, Petersen C, Gao L, Macara IG (2000). The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2, 531-539.
20. Kishikawa M, Suzuki A, Ohno S (2008). aPKC enables development of zonula adherens by antagonizing centripetal contraction of the circumferential actomyosin cables. J Cell Sci 121, 2481-2492.
21. Kovacs EM, Goodwin M, Ali RG, Paterson AD, Yap AS (2002). Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 12, 379-382. (Pubitemid 34209284)
22. Krahn MP, Klopfenstein DR, Fischer N, Wodarz A (2010). Membrane targeting of Bazooka/PAR-3 is mediated by direct binding to phosphoinositide lipids. Curr Biol 20, 636-642.
23. Krajcovic M, et al. (2011). A non-genetic route to aneuploidy in human cancers. Nat Cell Biol 13, 324-330.
24. Krendel M, Gloushankova NA, Bonder EM, Feder HH, Vasiliev JM, Gelfand IM (1999). Myosin-dependent contractile activity of the actin cytoskeleton modulates the spatial organization of cell-cell contacts in cultured epitheliocytes. Proc Natl Acad Sci USA 96, 9666-9670. (Pubitemid 29398789)
25. Krendel MF, Bonder EM (1999). Analysis of actin filament bundle dynamics during contact formation in live epithelial cells. Cell Motil Cytoskeleton 43, 296-309. (Pubitemid 29368203)
26. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T (2000). A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2, 540-547.
27. Macara IG (2004). Parsing the polarity code. Nat Rev Mol Cell Biol 5, 220-231.
28. Martin-Belmonte F, Mostov K (2008). Regulation of cell polarity during epithelial morphogenesis. Curr Opin Cell Biol 20, 227-234.
29. Musch A, Cohen D, Yeaman C, Nelson WJ, Rodriguez-Boulan E, Brennwald PJ (2002). Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol Biol Cell 13, 158-168. (Pubitemid 34106066)
30. Nakagawa M, Fukata M, Yamaga M, Itoh N, Kaibuchi K (2001). Recruitment and activation of Rac1 by the formation of E-cadherin-mediated cell-cell adhesion sites. J Cell Sci 114, 1829-1838. (Pubitemid 32530038)
31. Overholtzer M, Brugge JS (2008). The cell biology of cell-in-cell structures. Nat Rev Mol Cell Biol 9, 796-809.
32. Overholtzer M, Mailleux AA, Mouneimne G, Normand G, Schnitt SJ, King RW, Cibas ES, Brugge JS (2007). A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 131, 966-979. (Pubitemid 350138090)
33. Plant PJ, Fawcett JP, Lin DC, Holdorf AD, Binns K, Kulkarni S, Pawson T (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat Cell Biol 5, 301-308. (Pubitemid 36432294)
34. Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, Yap AS (2005). Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 16, 4531-4542. (Pubitemid 41416439)
35. Strand D, Jakobs R, Merdes G, Neumann B, Kalmes A, Heid HW, Husmann I, Mechler BM (1994). The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J Cell Biol 127, 1361-1373.
36. Vaezi A, Bauer C, Vasioukhin V, Fuchs E (2002). Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Dev Cell 3, 367-381.
37. Vasioukhin V (2006). Lethal giant puzzle of Lgl. Dev Neurosci 28, 13-24.
38. Vasioukhin V, Bauer C, Yin M, Fuchs E (2000). Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219. (Pubitemid 30064909)
39. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009). Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10, 778-790.
40. Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-1039. (Pubitemid 44792253)
41. Yamada S, Nelson WJ (2007). Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 178, 517-527. (Pubitemid 47196158)
42. Yamanaka T, Horikoshi Y, Izumi N, Suzuki A, Mizuno K, Ohno S (2006). Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity. J Cell Sci 119, 2107-2118. (Pubitemid 43904965)
43. Yamanaka T, Horikoshi Y, Sugiyama Y, Ishiyama C, Suzuki A, Hirose T, Iwamatsu A, Shinohara A, Ohno S (2003). Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr Biol 13, 734-743. (Pubitemid 36531020)
44. Zhang H, Macara IG (2008). The PAR-6 polarity protein regulates dendritic spine morphogenesis through p190 RhoGAP and the Rho GTPase. Dev Cell 14, 216-226. (Pubitemid 351189178)
45. Zhang J, Betson M, Erasmus J, Zeikos K, Bailly M, Cramer LP, Braga VM (2005). Actin at cell-cell junctions is composed of two dynamic and functional populations. J Cell Sci 118, 5549-5562. (Pubitemid 43079295)
46. Zheng Z, Zhu H, Wan Q, Liu J, Xiao Z, Siderovski DP, Du Q (2010). LGN regulates mitotic spindle orientation during epithelial morphogenesis. J Cell Biol 189, 275-288.