Polarized deposition of basement membrane proteins depends on Phosphatidylinositol synthase and the levels of Phosphatidylinositol 4,5-bisphosphate

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

Volumn 111, Issue 21, 2014, Pages 7689-7694

  Devergne, Olivier ^a   Tsung, Karen ^a   Barcelo, Gail ^a   Schüpbach, Trudi ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Cell polarity; Drosophila; Oogenesis; PIK; PTEN

Indexed keywords

BASEMENT MEMBRANE PROTEIN; CALMODULIN BINDING PROTEIN; CRAG PROTEIN; CYTIDINE DIPHOSPHATE DIACYLGLYCEROL INOSITOL 3 PHOSPHATIDYLTRANSFERASE; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BIOACCUMULATION; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EPITHELIUM CELL; FEMALE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; REGULATORY MECHANISM;

CELL POLARITY; DROSOPHILA; OOGENESIS; PIK; PTEN;

ANIMALS; BASEMENT MEMBRANE; CDP-DIACYLGLYCEROL-INOSITOL 3-PHOSPHATIDYLTRANSFERASE; CELL POLARITY; CELL TRANSFORMATION, NEOPLASTIC; DROSOPHILA; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; OVARY; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE;

EID: 84901675738     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1407351111     Document Type: Article

References (40)

1. Thompson BJ (2013) Cell polarity: Models and mechanisms from yeast, worms and flies. Development 140(1):13-21.
2. Müller HA, Bossinger O (2003) Molecular networks controlling epithelial cell polarity in development. Mech Dev 120(11):1231-1256. (Pubitemid 37421160)
3. Roignot J, Peng X, Mostov K (2013) Polarity in mammalian epithelial morphogenesis. Cold Spring Harb Perspect Biol 5(2):5.
4. Ellenbroek SI, Iden S, Collard JG (2012) Cell polarity proteins and cancer. Semin Cancer Biol 22(3):208-215.
5. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2(6):442-454.
6. Rodriguez-Boulan E, Kreitzer G, Müsch A (2005) Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6(3):233-247. (Pubitemid 40314924)
7. Apodaca G, Gallo LI, Bryant DM (2012) Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol 14(12):1235-1243.
8. Leslie NR, Batty IH, Maccario H, Davidson L, Downes CP (2008) Understanding PTEN regulation: PIP2, polarity and protein stability. Oncogene 27(41):5464-5476.
9. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443(7112):651-657. (Pubitemid 44564702)
10. Martin-Belmonte F, et al. (2007) PTEN-mediated apical segregation of phosphoino-sitides controls epithelial morphogenesis through Cdc42. Cell 128(2):383-397. (Pubitemid 46123512)
11. Gassama-Diagne A, et al. (2006) Phosphatidylinositol-3, 4, 5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8(9):963-970. (Pubitemid 44314727)
12. Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422(6933):766-774. (Pubitemid 36514120)
13. Yu W, et al. (2005) Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol Biol Cell 16(2):433-445. (Pubitemid 40165545)
14. Yurchenco PD (2011) Basement membranes: Cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol 3(2):3.
15. Yurchenco PD, Amenta PS, Patton BL (2004) Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol 22(7):521-538. (Pubitemid 38283776)
16. Li S, Edgar D, Fässler R, Wadsworth W, Yurchenco PD (2003) The role of laminin in embryonic cell polarization and tissue organization. Dev Cell 4(5):613-624. (Pubitemid 36564893)
17. O'Brien LE, Zegers MM, Mostov KE (2002) Opinion: Building epithelial architecture: Insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3(7):531-537. (Pubitemid 34733434)
18. Schneider M, et al. (2006) Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development 133(19):3805-3815. (Pubitemid 44650959)
19. Denef N, Chen Y, Weeks SD, Barcelo G, Schüpbach T (2008) Crag regulates epithelial architecture and polarized deposition of basement membrane proteins in Drosophila. Dev Cell 14(3):354-364.
20. Lerner DW, et al. (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24(2):159-168.
21. Xiong B, et al. (2012) Crag is a GEF for Rab11 required for rhodopsin trafficking and maintenance of adult photoreceptor cells. PLoS Biol 10(12):e1001438.
22. Sorrosal G, Pérez L, Herranz H, Milán M (2010) Scarface, a secreted serine protease-like protein, regulates polarized localization of laminin A at the basement membrane of the Drosophila embryo. EMBO Rep 11(5):373-379.
23. Horne-Badovinac S, Bilder D (2005) Mass transit: Epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 232(3):559-574. (Pubitemid 40315279)
24. Buszczak M, et al. (2007) The carnegie protein trap library: A versatile tool for Dro-sophila developmental studies. Genetics 175(3):1505-1531. (Pubitemid 46798248)
25. Kim YJ, Guzman-Hernandez ML, Balla T (2011) A highly dynamic ER-derived phos-phatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev Cell 21(5):813-824.
26. Maffucci T (2012) An introduction to phosphoinositides. Curr Top Microbiol Immunol 362:1-42.
27. Wang T, Montell C (2006) A phosphoinositide synthase required for a sustained light response. J Neurosci 26(49):12816-12825. (Pubitemid 44904577)
28. Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci USA 98(26):15050-15055. (Pubitemid 34013967)
29. Schill NJ, Anderson RA (2009) Out, in and back again: PtdIns(4, 5)P(2) regulates cad-herin trafficking in epithelial morphogenesis. Biochem J 418(2):247-260.
30. Gervais L, Claret S, Januschke J, Roth S, Guichet A (2008) PIP5K-dependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development 135(23):3829-3838.
31. Yan Y, Denef N, Tang C, Schüpbach T (2011) Drosophila PI4KIIIalpha is required in follicle cells for oocyte polarization and Hippo signaling. Development 138(9): 1697-1703.
32. Chartier FJ, Hardy EJ, Laprise P (2011) Crumbs controls epithelial integrity by inhibiting Rac1 and PI3K. J Cell Sci 124(Pt 20):3393-3398.
33. Miner JH, Yurchenco PD (2004) Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20:255-284. (Pubitemid 39488639)
34. Rasmussen JP, Reddy SS, Priess JR (2012) Laminin is required to orient epithelial polarity in the C. elegans pharynx. Development 139(11):2050-2060.
35. O'Brien LE, et al. (2001) Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol 3(9):831-838. (Pubitemid 32842689)
36. Zuk A, Matlin KS (1996) Apical beta 1 integrin in polarized MDCK cells mediates tubulocyst formation in response to type I collagen overlay. J Cell Sci 109(Pt 7): 1875-1889. (Pubitemid 26248633)
37. Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331(6020):1071-1074.
38. Huang H, et al. (1999) PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126(23):5365-5372. (Pubitemid 30015929)
39. Zhang J, et al. (2007) Thirty-one flavors of Drosophila rab proteins. Genetics 176(2): 1307-1322. (Pubitemid 46961123)
40. Murray MA, Fessler LI, Palka J (1995) Changing distributions of extracellular matrix components during early wing morphogenesis in Drosophila. Dev Biol 168(1):150-165.