The Par3/Par6/aPKC complex and epithelial cell polarity

Experimental Cell Research

Volumn 319, Issue 10, 2013, Pages 1357-1364

  Chen, Jia ^a,b   Zhang, Mingjie ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adhesion forces; Apical; Basolateral; Cell polarity; Epithelia; Par complex

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); APICAL PROTEIN KINASE C; GLYCOGEN SYNTHASE KINASE 3BETA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HAMMERHEAD RIBOZYME; MYOSIN II; PAR3 PROTEIN; PAR6 PROTEIN; PDZ PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE C; RHO KINASE; SCAFFOLD PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

APICAL MEMBRANE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL POLARITY; CELL STRUCTURE; CELL SURFACE; COMPLEX FORMATION; DROSOPHILA; EPITHELIUM CELL; EXTRACELLULAR MATRIX; NONHUMAN; OLIGOMERIZATION; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ZEBRA FISH;

EID: 84877927201     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.03.021     Document Type: Review

References (69)

1. Tepass U., Hartenstein V. The development of cellular junctions in the Drosophila embryo. Dev. Biol. 1994, 161:563-596.
2. Johnston D., Ahringer J. Cell polarity in eggs and epithelia: parallels and diversity. Cell 2010, 141:757-774.
3. Tepass U. Epithelial differentiation in Drosophila. BioEssays 1997, 19:673-682.
4. Tepass U., Hartenstein V. Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 1994, 120:579-590.
5. Yarnitzky T., Volk T. Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev. Biol. 1995, 169:609-618.
6. Klein G., Langegger M., Timpl R., Ekblom P. Role of laminin A chain in the development of epithelial cell polarity. Cell 1988, 55:331-341.
7. Urbano J.M., Torgler C.N., Molnar C., Tepass U., Lopez-Varea A., Brown N.H., de Celis J.F., Martin-Bermudo M.D. Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 2009, 136:4165-4176.
8. Collins J.E., Fleming T.P. Epithelial differentiation in the mouse preimplantation embryo: making adhesive cell contacts for the first time. Trends Biochem. Sci. 1995, 20:307-312.
9. Kemphues K.J., Priess J.R., Morton D.G., Cheng N.S. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 1988, 52:311-320.
10. Tabuse Y., Izumi Y., Piano F., Kemphues K.J., Miwa J., Ohno S. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 1998, 125:3607-3614.
11. Wodarz A., Ramrath A., Kuchinke U., Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 1999, 402:544-547.
12. Plant P.J., Fawcett J.P., Lin D.C., Holdorf A.D., Binns K., Kulkarni S., Pawson T. A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 2003, 5:301-308.
13. Hurd T.W., Gao L., Roh M.H., Macara I.G., Margolis B. Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol. 2003, 5:137-142.
14. Lin D., Edwards A.S., Fawcett J.P., Mbamalu G., Scott J.D., Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2000, 2:540-547.
15. Shi S.H., Jan L.Y., Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 2003, 112:63-75.
16. Macara I.G. Par proteins: partners in polarization. Curr. Biol. 2004, 14:R160-162.
17. U. Tepass, The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival, Annu. Rev. Cell Dev. Biol. (2012).
18. Sato T., Fujita N., Yamada A., Ooshio T., Okamoto R., Irie K., Takai Y. Regulation of the assembly and adhesion activity of E-cadherin by nectin and afadin for the formation of adherens junctions in Madin-Darby canine kidney cells. J. Biol. Chem. 2006, 281:5288-5299.
19. Suzuki A., Yamanaka T., Hirose T., Manabe N., Mizuno K., Shimizu M., Akimoto K., Izumi Y., Ohnishi T., Ohno S. Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J. Cell. Biol. 2001, 152:1183-1196.
20. Joberty G., Petersen C., Gao L., Macara I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2000, 2:531-539.
21. Horikoshi Y., Suzuki A., Yamanaka T., Sasaki K., Mizuno K., Sawada H., Yonemura S., Ohno S. Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J. Cell Sci. 2009, 122:1595-1606.
22. Doerflinger H., Vogt N., Torres I.L., Mirouse V., Koch I., Nüsslein-Volhard C., Johnston D. Bazooka is required for polarisation of the Drosophila anterior-posterior axis. Development 2010, 137:1765-1773.
23. Morais-de-Sá E., Mirouse V., Johnston D. aPKC phosphorylation of Bazooka defines the apical/lateral border in Drosophila epithelial cells. Cell 2010, 141:509-523.
24. Bryant D.M., Mostov K.E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 2008, 9:887-901.
25. Yamanaka T., Horikoshi Y., Suzuki A., Sugiyama Y., Kitamura K., Maniwa R., Nagai Y., Yamashita A., Hirose T., Ishikawa H., Ohno S. PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 2001, 6:721-731.
26. Benton R., Johnston D. A conserved oligomerization domain in drosophila Bazooka/PAR-3 is important for apical localization and epithelial polarity. Curr. Biol. 2003, 13:1330-1334.
27. Mizuno K., Suzuki A., Hirose T., Kitamura K., Kutsuzawa K., Futaki M., Amano Y., Ohno S. Self-association of PAR-3-mediated by the conserved N-terminal domain contributes to the development of epithelial tight junctions. J. Biol. Chem. 2003, 278:31240-31250.
28. Feng W., Wu H., Chan L.-N., Zhang M. The Par-3 NTD adopts a PB1-like structure required for Par-3 oligomerization and membrane localization. EMBO J. 2007, 26:2786-2796.
29. Chan J.R., Jolicoeur C., Yamauchi J., Elliott J., Fawcett J.P., Ng B.K., Cayouette M. The polarity protein Par-3 directly interacts with p75NTR to regulate myelination. Science 2006, 314:832-836.
30. Ebnet K., Aurrand-Lions M., Kuhn A., Kiefer F., Butz S., Zander K., Meyer zu Brickwedde M.K., Suzuki A., Imhof B.A., Vestweber D. The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity. J. Cell Sci. 2003, 116:3879-3891.
31. Itoh M., Sasaki H., Furuse M., Ozaki H., Kita T., Tsukita S. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J. Cell Biol. 2001, 154:491-497.
32. Takekuni K., Ikeda W., Fujito T., Morimoto K., Takeuchi M., Monden M., Takai Y. Direct binding of cell polarity protein PAR-3 to cell-cell adhesion molecule nectin at neuroepithelial cells of developing mouse. J. Biol. Chem. 2003, 278:5497-5500.
33. C.G. Yu, T.J. Harris, Interactions between the PDZ domains of Bazooka (Par-3) and phosphatidic acid: in vitro characterization and role in epithelial development, Mol. Biol. Cell (2012).
34. Wu H., Feng W., Chen J., Chan L.N., Huang S., Zhang M. PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol. Cell 2007, 28:886-898.
35. Feng W., Wu H., Chan L.N., Zhang M. Par-3-mediated junctional localization of the lipid phosphatase PTEN is required for cell polarity establishment. J. Biol. Chem. 2008, 283:23440-23449.
36. Chen S., Chen J., Shi H., Wei M., Castaneda-Castellanos D.R., Bultje R.S., Pei X., Kriegstein A.R., Zhang M., Shi S.H. Regulation of microtubule stability and organization by Mammalian par3 in specifying neuronal polarity. Dev. Cell 2013, 24:26-40.
37. Wang C., Shang Y., Yu J., Zhang M. Substrate recognition mechanism of atypical protein kinase Cs revealed by the structure of PKCiota in complex with a substrate peptide from Par-3. Structure 2012, 20:791-801.
38. Nishimura T., Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 2007, 13:15-28.
39. Krahn M.P., Klopfenstein D.R., Fischer N., Wodarz A. Membrane targeting of Bazooka/PAR-3 is mediated by direct binding to phosphoinositide lipids. Curr. Biol. 2010, 20:636-642.
40. Zhang H., Macara I.G. The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis. Nat. Cell Biol. 2006, 8:227-237.
41. Nishimura T., Yamaguchi T., Kato K., Yoshizawa M., Nabeshima Y., Ohno S., Hoshino M., Kaibuchi K. PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat. Cell Biol. 2005, 7:270-277.
42. Chen X., Macara I.G. Par-3 controls tight junction assembly through the Rac exchange factor Tiam1. Nat. Cell Biol. 2005, 7:262-269.
43. Nishimura T., Kato K., Yamaguchi T., Fukata Y., Ohno S., Kaibuchi K. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat. Cell Biol. 2004, 6:328-334.
44. Sonawane M., Martin-Maischein H., Schwarz H., Nusslein-Volhard C. Lgl2 and E-cadherin act antagonistically to regulate hemidesmosome formation during epidermal development in zebrafish. Development 2009, 136:1231-1240.
45. Zovein A.C., Luque A., Turlo K.A., Hofmann J.J., Yee K.M., Becker M.S., Fassler R., Mellman I., Lane T.F., Iruela-Arispe M.L. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev. Cell 2010, 18:39-51.
46. Benton R., Johnston D. Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 2003, 115:691-704.
47. Betschinger J., Mechtler K., Knoblich J.A. The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 2003, 422:326-330.
48. Yamanaka T., Horikoshi Y., Sugiyama Y., Ishiyama C., Suzuki A., Hirose T., Iwamatsu A., Shinohara A., Ohno S. Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr. Biol 2003, 13:734-743.
49. Yamanaka T., Horikoshi Y., Izumi N., Suzuki A., Mizuno K., Ohno S. Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity. J. Cell Sci. 2006, 119:2107-2118.
50. Hutterer A., Betschinger J., Petronczki M., Knoblich J.A. Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 2004, 6:845-854.
51. Müsch A., Cohen D., Yeaman C., Nelson W.J., Rodriguez-Boulan E., Brennwald P.J. Mammalian homolog of Drosophila Tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol. Biol. Cell 2002, 13:158-168.
52. Bilder D., Schober M., Perrimon N. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 2002, 5:53-58.
53. Tanentzapf G., Tepass U. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 2002, 5:46-52.
54. +-ATPase form a novel group of epithelial polarity proteins. Nature 2009, 459:1141-1145.
55. Genova J.L., Fehon R.G. Neuroglian, gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J. Cell Biol. 2003, 161:979-989.
56. M. Burute, M. Thery, Spatial segregation between cell-cell and cell-matrix adhesions, Curr Opin Cell Biol (2012).
57. Nelson W.J. Epithelial cell polarity from the outside looking in. News Physiolo. Sci. 2003, 18:143-146.
58. Tseng Q., Duchemin-Pelletier E., Deshiere A., Balland M., Guillou H., Filhol O., Thery M. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc Natl Acad Sci USA 2012, 109:1506-1511.
59. 2 may provide a structural basis for the polymerization of claudins. J. Biol. Chem. 2007, 282:35988-35999.
60. Huo L., Wen W., Wang R., Kam C., Xia J., Feng W., Zhang M. Cdc42-dependent formation of the ZO-1/MRCKbeta complex at the leading edge controls cell migration. EMBO J. 2011, 30:665-678.
61. Schluter M.A., Margolis B. Apicobasal polarity in the kidney. Exp. Cell Res. 2012, 318:1033-1039.
62. Datta A., Bryant D.M., Mostov K.E. Molecular regulation of lumen morphogenesis. Curr. Biol. 2011, 21:R126-136.
63. Wang A.Z., OJAKIAN G.K., NELSON W.J. Steps in the morphogenesis of a polarized epithelium I. Uncoupling the roles of cell-cell and cell-substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci. 1990, 95:137-151.
64. Yu W., Datta A., Leroy P., O'Brien L.E., Mak G., Jou T.S., Matlin K.S., Mostov K.E., Zegers M.M. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell 2005, 16:433-445.
65. Chartier F.J., Hardy E.J., Laprise P. Crumbs controls epithelial integrity by inhibiting Rac1 and PI3K. J. Cell Sci. 2011, 124:3393-3398.
66. A.E. Rodriguez-Fraticelli, M. Auzan, M.A. Alonso, M. Bornens, F. Martin-Belmonte, Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis, J. Cell Biol. (2012).
67. Martin-Belmonte F., Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat. Rev. Cancer 2012, 12:23-38.
68. Knoblich J.A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 2010, 11:849-860.
69. Bryant D.M., Datta A., Rodriguez-Fraticelli A.E., Peranen J., Martin-Belmonte F., Mostov K.E. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 2010, 12:1035-1045.