Basolateral junctions are sufficient to suppress epithelial invasion during Drosophila oogenesis

Developmental Dynamics

Volumn 236, Issue 2, 2007, Pages 364-373

  Szafranski, Przemyslaw ^a   Goode, Scott ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Basolateral junction; Cell migration; Dlg; Drosophila; Fas2; Tumor invasion

Indexed keywords

CELL PROTEIN; DISC LARGE PROTEIN; FASCICLIN II; LETHAL GIANT LARVAE PROTEIN; NEUROGLIAN; UNCLASSIFIED DRUG;

ARTICLE; BASOLATERAL MEMBRANE; CANCER INVASION; CELL DIFFERENTIATION; CELL MIGRATION; DROSOPHILA; EPITHELIUM CELL; HISTOCHEMISTRY; NONHUMAN; OOCYTE DEVELOPMENT; OVARY; PRIORITY JOURNAL; TUMOR CELL;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL LINE, TUMOR; CELL MOVEMENT; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIAL CELLS; HISTOCYTOCHEMISTRY; INTERCELLULAR JUNCTIONS; NEOPLASM INVASIVENESS; OOGENESIS; TUMOR SUPPRESSOR PROTEINS;

METAZOA;

EID: 33846910851     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21020     Document Type: Article

References (53)

1. Abdelilah-Seyfried S, Cox DN, Jan YN. 2003. Bazooka is a permissive factor for the invasive behavior of discs large tumor cells in Drosophila ovarian follicular epithelia. Development 130:1927-1935.
2. Arlt MJ, Novak-Hofer I, Gast D, Gschwend V, Moldenhauer G, Grunberg J, Honer M, Schubiger PA, Altevogt P, Kruger A. 2006. Efficient inhibition of intra-peritoneal tumor growth and dissemination of human ovarian carcinoma cells in nude mice by anti-L1-cell adhesion molecule monoclonal antibody treatment. Cancer Res 66:936-943.
3. Bateman J, Reddy RS, Saito H, Van Vactor D. 2001. The receptor tyrosine phosphatase Dlar and integrins organize actin filaments in the Drosophila follicular epithelium. Curr Biol 11:1317-1327.
4. Bazzoni G. 2003. The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 15:525-530.
5. Bennett V, Baines AJ. 2001. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81:1353-1392.
6. Bilder D. 2004. Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev 18:1909-1925.
7. Bilder D, Perrimon N. 2000. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676-680.
8. Bilder D, Li M, Perrimon N. 2000. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289:113-116.
9. Bunch TA, Salatino R, Engelsgjerd MC, Mukai L, West RF, Brower DL. 1992. Characterization of mutant alleles of myospheroid, the gene encoding the beta subunit of the Drosophila PS integrins. Genetics 132:519-528.
10. Cheng Y, Endo K, Wu K, Rodan AR, Heberlein U, Davis RL. 2001. Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105:757-768.
11. Deng WM, Ruohola-Baker H. 2000. Laminin A is required for follicle cell-oocyte signaling that leads to establishment of the anterior-posterior axis in Drosophila. Curr Biol 10:683-686.
12. Dubreuil RR, MacVicar G, Dissanayake S, Liu C, Homer D, Hortsch M. 1996. Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J Cell Biol 133:647-655.
13. Firestein BL, Rongo C. 2001. DLG-1 is a MAGUK similar to SAP97 and is required for adherens junction formation. Mol Biol Cell 12:3465-3475.
14. Fogar P, Basso D, Pasquali C, De Paoli M, Sperti C, Roveroni G, Pedrazzoli S, Plebani M. 1997. Neural cell adhesion molecule (N-CAM) in gastrointestinal neoplasias. Anticancer Res 17:1227-1230.
15. Geisbrecht ER, Montell DJ. 2004. A role for Drosophila IAP1-mediated caspase inhibition in Rac-dependent cell migration. Cell 118:111-125.
16. Goode S, Perrimon N. 1997. Inhibition of patterned cell shape change and cell invasion by Discs large during Drosophila oogenesis. Genes Dev 11:2532-2544.
17. Goode S, Melnick M, Chou TB, Perrimon N. 1996. The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis. Development 122:3863-3879.
18. Goode S, Wei J, Kishore S. 2005. Novel spatiotemporal patterns of epithelial tumor invasion in Drosophila discs large egg chambers. Dev Dyn 232:855-864.
19. Goodman CS, Davis GW, Zito K. 1997. The many faces of fasciclin II: Genetic analysis reveals multiple roles for a cell adhesion molecule during the generation of neuronal specificity. Cold Spring Harb Symp Quant Biol 62:479-491.
20. Grunert S, Jechlinger M, Beug H. 2003. Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol 4:657-665.
21. Gutzeit HO, Eberhardt W, Gratwohl E. 1991. Laminin and basement membrane-associated microfilaments in wild-type and mutant Drosophila ovarian follicles. J Cell Sci 100:781-788.
22. Hortsch M, Homer D, Malhotra JD, Chang S, Frankel J, Jefford G, Dubreuil RR. 1998. Structural requirements for outside-in and inside-out signaling by Drosophila neuroglian, a member of the L1 family of cell adhesion molecules. J Cell Biol 142:251-261.
23. Huang JH, Rajkovic A, Szafranski P, Ochsner S, Richards J, Goode S. 2003. Expression of Drosophila neoplastic tumor suppressor genes discslarge, scribble, and lethal giant larvae in the mammalian ovary. Gene Expr Patterns 3:3-11.
24. Hynes RO. 2003. Metastatic potential: generic predisposition of the primary tumor or rare, metastatic variants-or both? Cell 113:821-823.
25. Knust E. 2002. Regulation of epithelial cell shape and polarity by cell-cell adhesion (review). Mol Membr Biol 19:113-120.
26. Knust E, Bossinger O. 2002. Composition and formation of intercellular junctions in epithelial cells. Science 298:1955-1959.
27. Larue L, Bellacosa A. 2005. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways. Oncogene 24:7443-7454.
28. Lee JK, Brandin E, Branton D, Goldstein LS. 1997. alpha-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster. Development 124:353-362.
29. Lue RA, Brandin E, Chan EP, Branton D. 1996. Two independent domains of hDlg are sufficient for subcellular targeting: the PDZ1-2 conformational unit and an alternatively spliced domain. J Cell Biol 135:1125-1137.
30. Luo L, Liao YJ, Jan LY, Jan YN. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8:1787-1802.
31. Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, Phan H, Philp AV, Yang M, Glover D, Kaiser K, Palter K, Selleck S. 1997. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209:310-322.
32. Marmorstein AD, Gan YC, Bonilha VL, Finnemann SC, Csaky KG, Rodriguez-Boulan E. 1998. Apical polarity of N-CAM and EMMPRIN in retinal pigment epithelium resulting from suppression of basolateral signal recognition. J Cell Biol 142:697-710.
33. Mellman I. 2000. Quo vadis: polarized membrane recycling in motility and phagocytosis. J Cell Biol 149:529-530.
34. Montell DJ. 2003. Border-cell migration: the race is on. Nat Rev Mol Cell Biol 4:13-24.
35. Nelson WJ. 2003. Adaptation of core mechanisms to generate cell polarity. Nature 422:766-774.
36. Niewiadomska P, Godt D, Tepass U. 1999. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J Cell Biol 144:533-547.
37. Pagliarini RA, Xu T. 2003. A genetic screen in Drosophila for metastatic behavior. Science 302:1227-1231.
38. Peifer M, Orsulic S, Sweeton D, Wieschaus E. 1993. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118:1191-1207.
39. Perl AK, Dahl U, Wilgenbus P, Cremer H, Semb H, Christofori G. 1999. Reduced expression of neural cell adhesion molecule induces metastatic dissemination of pancreatic beta tumor cells. Nat Med 5:286-291.
40. Perrimon N, Mahowald AP. 1987. Multiple functions of segment polarity genes in Drosophila. Dev Biol 119:587-600.
41. Pinheiro EM, Montell DJ. 2004. Requirement for Par-6 and Bazooka in Drosophila border cell migration. Development 131:5243-5251.
42. Roesler J, Srivatsan E, Moatamed F, Peters J, Livingston EH. 1997. Tumor suppressor activity of neural cell adhesion molecule in colon carcinoma. Am J Surg 174:251-257.
43. Sanson B, White P, Vincent JP. 1996. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383:627-630.
44. Schimanski CC, Schmitz G, Kashyap A, Bosserhoff AK, Bataille F, Schafer SC, Lehr HA, Berger MR, Galle PR, Strand S, Strand D. 2005. Reduced expression of Hugl-1, the human homologue of Drosophila tumour suppressor gene lgl, contributes to progression of colorectal cancer. Oncogene 24:3100-3109.
45. Shook D, Keller R. 2003. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev 120:1351-1383.
46. Szafranski P, Goode S. 2004. A Fasciclin 2 morphogenetic switch organizes epithelial cell cluster polarity and motility. Development 131:2023-2036.
47. Tanentzapf G, Smith C, McGlade J, Tepass U. 2000. Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J Cell Biol 151:891-904.
48. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142.
49. Thomas GH, Zarnescu DC, Juedes AE, Bales MA, Londergan A, Korte CC, Kiehart DP. 1998. Drosophila betaHeavy-spectrin is essential for development and contributes to specific cell fates in the eye. Development 125:2125-2134.
50. 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.
51. Wei J, Hortsch M, Goode S. 2004. Neuroglian stabilizes epithelial structure during Drosophila oogenesis. Dev Dyn 230:800-808.
52. Wodarz A, Ramrath A, Grimm A, Knust E. 2000. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol 150:1361-1374.
53. Zarnescu DC, Thomas GH. 1999. Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila. J Cell Biol 146:1075-1086.