Structure of Crumbs tail in complex with the PALS1 PDZ-SH3-GK tandem reveals a highly specific assembly mechanism for the apical Crumbs complex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages 17444-17449

  Li, Youjun ^a   Wei, Zhiyi ^a,b   Yan, Yan ^a   Wan, Qingwen ^c   Du, Quansheng ^c   Zhang, Mingjie ^a  

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

^b SOUTHERN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cell polarity; MAGUK; PBM; Stardust; Supramodule

Indexed keywords

GUANYLATE KINASE; PDZ PROTEIN; PROTEIN; PROTEIN CRUMBS; PROTEIN PALS1; PROTEIN SH3; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PROTEIN BINDING;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL COMMUNICATION; CELL POLARITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYST; CYTOPLASM; DISSOCIATION CONSTANT; LIGAND BINDING; MDCK CELL LINE; NONHUMAN; PDZ DOMAIN; POINT MUTATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DOG; EPITHELIUM CELL; ESCHERICHIA COLI; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SRC HOMOLOGY DOMAIN; X RAY CRYSTALLOGRAPHY;

METAZOA;

AMINO ACID SEQUENCE; ANIMALS; CELL POLARITY; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; DOGS; EPITHELIAL CELLS; ESCHERICHIA COLI; GUANYLATE KINASE; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PDZ DOMAINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SRC HOMOLOGY DOMAINS;

EID: 84916236414     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416515111     Document Type: Article

References (43)

1. Tepass U (2012) The apical polarity protein network in Drosophila epithelial cells: Regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu Rev Cell Dev Biol 28:655-685
2. Rodriguez-Boulan E, Macara IG (2014) Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 15(4):225-242
3. Martin-Belmonte F, Perez-Moreno M (2012) Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 12(1):23-38
4. Margolis B, Borg JP (2005) Apicobasal polarity complexes. J Cell Sci 118(Pt 22): 5157-5159
5. Knust E, Bossinger O (2002) Composition and formation of intercellular junctions in epithelial cells. Science 298(5600):1955-1959
6. Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747-784
7. Bulgakova NA, Knust E (2009) The Crumbs complex: From epithelial-cell polarity to retinal degeneration. J Cell Sci 122(Pt 15):2587-2596
8. Nance J, Zallen JA (2011) Elaborating polarity: PAR proteins and the cytoskeleton. Development 138(5):799-809
9. Suzuki A, Ohno S (2006) The PAR-aPKC system: Lessons in polarity. J Cell Sci 119(Pt 6): 979-987
10. Bilder D (2004) Epithelial polarity and proliferation control: Links from the Drosophila neoplastic tumor suppressors. Genes Dev 18(16):1909-1925
11. Tepass U, Theres C, Knust E (1990) crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61(5):787-799
12. Tepass U (1996) Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev Biol 177(1):217-225
13. Pocha SM, Knust E (2013) Complexities of Crumbs function and regulation in tissue morphogenesis. Curr Biol 23(7):R289-R293
14. Wodarz A, Grawe F, Knust E (1993) CRUMBS is involved in the control of apical protein targeting during Drosophila epithelial development. Mech Dev 44(2-3):175-187
15. Wodarz A, Hinz U, Engelbert M, Knust E (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82(1):67-76
16. Chen CL, et al. (2010) The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci USA 107(36):15810-15815
17. Ling C, et al. (2010) The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc Natl Acad Sci USA 107(23):10532-10537
18. Varelas X, et al. (2010) The Crumbs complex couples cell density sensing to Hippodependent control of the TGF-β-SMAD pathway. Dev Cell 19(6):831-844
19. Klebes A, Knust E (2000) A conserved motif in Crumbs is required for E-cadherin localisation and zonula adherens formation in Drosophila. Curr Biol 10(2):76-85
20. Klose S, Flores-Benitez D, Riedel F, Knust E (2013) Fosmid-based structure-function analysis reveals functionally distinct domains in the cytoplasmic domain of Drosophila Crumbs. G3 (Bethesda) 3(2):153-165
21. Sotillos S, Díaz-Meco MT, Caminero E, Moscat J, Campuzano S (2004) DaPKCdependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J Cell Biol 166(4):549-557
22. Laprise P, et al. (2006) The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell 11(3):363-374
23. Roh MH, et al. (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J Cell Biol 157(1):161-172
24. Bulgakova NA, Kempkens O, Knust E (2008) Multiple domains of Stardust differentially mediate localisation of the Crumbs-Stardust complex during photoreceptor development in Drosophila. J Cell Sci 121(Pt 12):2018-2026
25. Bachmann A, Schneider M, Theilenberg E, Grawe F, Knust E (2001) Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity. Nature 414(6864): 638-643
26. Hong Y, Stronach B, Perrimon N, Jan LY, Jan YN (2001) Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts. Nature 414(6864): 634-638
27. Stiffler MA, et al. (2007) PDZ domain binding selectivity is optimized across the mouse proteome. Science 317(5836):364-369
28. Tonikian R, et al. (2008) A specificity map for the PDZ domain family. PLoS Biol 6(9): e239
29. Ye F, Zhang M (2013) Structures and target recognition modes of PDZ domains: Recurring themes and emerging pictures. Biochem J 455(1):1-14
30. Tepass U, Knust E (1993) crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev Biol 159(1):311-326
31. Wang Q, Chen XW, Margolis B (2007) PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol Biol Cell 18(3):874-885
32. McGee AW, et al. (2001) Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol Cell 8(6):1291-1301
33. Shin H, Hsueh YP, Yang FC, Kim E, Sheng M (2000) An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J Neurosci 20(10):3580-3587
34. Pan L, Chen J, Yu J, Yu H, Zhang M (2011) The structure of the PDZ3-SH3-GuK tandem of ZO-1 protein suggests a supramodular organization of the membrane- associated guanylate kinase (MAGUK) family scaffold protein core. J Biol Chem 286(46):40069-40074
35. McGee AW, et al. (2004) Calcium channel function regulated by the SH3-GK module in beta subunits. Neuron 42(1):89-99
36. Zhu J, et al. (2011) Guanylate kinase domains of the MAGUK family scaffold proteins as specific phospho-protein-binding modules. EMBO J 30(24):4986-4997
37. Funke L, Dakoji S, Bredt DS (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu Rev Biochem 74:219-245
38. Zhang J, Lewis SM, Kuhlman B, Lee AL (2013) Supertertiary structure of the MAGUK core from PSD-95. Structure 21(3):402-413
39. McCann JJ, et al. (2012) Supertertiary structure of the synaptic MAGuK scaffold proteins is conserved. Proc Natl Acad Sci USA 109(39):15775-15780
40. Hata Y, Butz S, Südhof TC (1996) CASK: A novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16(8):2488-2494
41. Kempkens O, et al. (2006) Computer modelling in combination with in vitro studies reveals similar binding affinities of Drosophila Crumbs for the PDZ domains of Stardust and DmPar-6. Eur J Cell Biol 85(8):753-767
42. Lemmers C, et al. (2004) CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol Biol Cell 15(3):1324-1333
43. Bossuyt W, et al. (2014) An evolutionary shift in the regulation of the Hippo pathway between mice and flies. Oncogene 33(10):1218-1228.