Genes that drive invasion and migration in Drosophila

Current Opinion in Genetics and Development

Volumn 14, Issue 1, 2004, Pages 86-91

  Starz Gaiano, Michelle ^a   Montell, Denise J ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CELL; CARCINOGENESIS; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CYTOSKELETON; DROSOPHILA; EMBRYO CELL; GENE FUNCTION; GENETIC ANALYSIS; HUMAN; METASTASIS; NONHUMAN; OVARY CELL; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REVIEW; SOMATIC CELL;

DROSOPHILA MELANOGASTER; HEXAPODA; MAMMALIA;

EID: 0842346273     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2003.12.001     Document Type: Review

References (58)

1. Ghiglione C., Devergne O., Georgenthum E., Carballes F., Medioni C., Cerezo D., Noselli S. The Drosophila cytokine receptor Domeless controls border cell migration and epithelial polarization during oogenesis. Development. 129:2002;5437-5447.
2. Silver D.L., Montell D.J. Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell. 107:2001;831-841.
3. Beccari S., Teixeira L., Rorth P. The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech Dev. 111:2002;115-123.
4. Montell D. Border-cell migration: the race is on. Nat Rev Mol Cell Biol. 4:2003;13-24.
5. Brown S., Hu N., Hombria J.C. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol. 11:2001;1700-1705.
6. Chen H., Chen X., Oh S., Marinissen M.J., Gutkind J.S., Hou S.X. mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev. 16:2002;388-398.
7. Shen Y., Devgan G., Darnell J.E. Jr., Bromberg J.F. Constitutively activated Stat3 protects fibroblasts from serum withdrawal and UV-induced apoptosis and antagonizes the proapoptotic effects of activated Stat1. Proc Natl Acad Sci USA. 98:2001;1543-1548.
8. Riddiford LM: Hormones and Drosophila development. In The Development of Drosophila Melanogaster, vol 2. Edited by Bate M, Martinez Arias A: Cold Spring Harbor, NY: Cold Spring Harbor laboratory Press; 1993:899-940.
9. Bai J., Uehara Y., Montell D.J. Regulation of invasive cell behavior by Taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell. 103:2000;1047-1058.
10. Cherbas L., Hu X., Zhimulev I., Belyaeva E., Cherbas P. EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development. 130:2003;271-284.
11. Anzick S.L., Kononen J., Walker R.L., Azorsa D.O., Tanner M.M., Guan X.Y., Sauter G., Kallioniemi O.P., Trent J.M., Meltzer P.S. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science. 277:1997;965-968.
12. Fisher B., Constantino J.P., Wickerham D.L., Redmond C.K., Kavanah M., Cronin W.M., Vogel V., Robidoux A., Dimitrov N., Atkins J.et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst. 90:1998;1371-1388.
13. Duchek P., Somogyi K., Jekely G., Beccari S., Rorth P. Guidance of cell migration by the Drosophila pdgf/vegf receptor. Cell. 107:2001;17-26.
14. Duchek P., Rorth P. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science. 291:2001;131-133.
15. McDonald J.A., Pinheiro E.M., Montell D.J. PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development. 130:2003;3469-3478 This paper directly demonstrates that PVF1 acts as an attractant by showing that ectopic expression of this molecule is sufficient to guide border cells away from their normal locations.
16. Cho N.K., Keyes L., Johnson E., Heller J., Ryner L., Karim F., Krasnow M.A. Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell. 108:2002;865-876 This work describes the hemocyte migration defects in VEGF receptor (PVR) mutant embryos, and using RNA interference, shows that blocking all three VEGF (PVR) ligands simultaneously recapitulates this phenotype. They also are able to redirect hemocytes with ectopic expression of one, but not all, of the ligands.
17. Heino T.I., Karpanen T., Wahlstrom G., Pulkkinen M., Eriksson U., Alitalo K., Roos C. The Drosophila VEGF receptor homolog is expressed in hemocytes. Mech Dev. 109:2001;69-77.
18. Affolter M., Bellusci S., Itoh N., Shilo B., Thiery J.P., Werb Z. Tube or not tube: remodeling epithelial tissues by branching morphogenesis. Dev Cell. 4:2003;11-18.
19. Lubarsky B., Krasnow M.A. Tube morphogenesis: making and shaping biological tubes. Cell. 112:2003;19-28.
20. Uv A., Cantera R., Samakovlis C. Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol. 13:2003;301-309.
21. Glazer L., Shilo B.Z. The Drosophila FGF-R homolog is expressed in the embryonic tracheal system and appears to be required for directed tracheal cell extension. Genes Dev. 5:1991;697-705.
22. Klambt C., Glazer L., Shilo B.Z. Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev. 6:1992;1668-1678.
23. Reichman-Fried M., Shilo B.Z. Breathless, a Drosophila FGF receptor homolog, is required for the onset of tracheal cell migration and tracheole formation. Mech Dev. 52:1995;265-273.
24. Sutherland D., Samakovlis C., Krasnow M.A. Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell. 87:1996;1091-1101.
25. Ribeiro C., Ebner A., Affolter M. In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev Cell. 2:2002;677-683 In this paper, GFP-tagged proteins, such as actin-GFP, are specifically expressed in the trachea, and the development of this network is observed in real time using confocal microscopy. The authors observe dynamic filopodia formation during tracheal outgrowth and demonstrate that FGF signaling is necessary and sufficient to induce these cell shape changes. Although filopodia still extend when Dpp signaling is blocked in the trachea, dorsal branches are unable to form, suggesting a distinct role for this pathway in tracheal morphogenesis.
26. Wolf C., Gerlach N., Schuh R. Drosophila tracheal system formation involves FGF-dependent cell extensions contacting bridge-cells. EMBO Rep. 3:2002;563-568.
27. Sato M., Kornberg T.B. FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev Cell. 3:2002;195-207 The authors use expression analysis and in vivo imaging to identify the precursors of the air sacs of the adult thorax, which express the FGF receptor. They go on to show that these cells extend directed filopodia towards sites of FGF expression, and fail to migrate when FGF signaling is blocked by mutations or by dominant negative proteins.
28. Bell R. What can we learn from Herceptin trials in metastatic breast cancer? Oncology. 63(Suppl):2002;39-46.
29. Ma C., Lin H., Leonard S.S., Shi X., Ye J., Luo J. Overexpression of ErbB2 enhances ethanol-stimulated intracellular signaling and invasion of human mammary epithelial and breast cancer cells in vitro. Oncogene. 22:2003;5281-5290.
30. Bange J., Prechtl D., Cheburkin Y., Specht K., Harbeck N., Schmitt M., Knyazeva T., Muller S., Gartner S., Sures I.et al. Cancer progression and tumor cell motility are associated with the FGFR4 Arg(388) allele. Cancer Res. 62:2002;840-847.
31. Starz-Gaiano M., Lehmann R. Moving towards the next generation. Mech Dev. 105:2001;5-18.
32. Kunwar PS, Starz-Gaiano M, Bainton R, Heberlein U, Lehmann R: Tre1, a G protein coupled receptor, directs transepithelial migration of Drosophila germ cells. PLoS Biol 2003, in press.
33. Molyneaux K.A., Zinszner H., Kunwar P.S., Schaible K., Stebler J., Sunshine M.J., O'Brien W., Raz E., Littman D., Wylie C.et al. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development. 130:2003;4279-4286.
34. Ara T., Nakamura Y., Egawa T., Sugiyama T., Abe K., Kishimoto T., Matsui Y., Nagasawa T. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci USA. 100:2003;5319-5323.
35. •].).
36. •].).
37. Bachelder R.E., Wendt M.A., Mercurio A.M. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res. 62:2002;7203-7206.
38. Helbig G., Christopherson K.W. II, Bhat-Nakshatri P., Kumar S., Kishimoto H., Miller K.D., Broxmeyer H.E., Nakshatri H. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem. 278:2003;21631-21638.
39. Chen Y., Stamatoyannopoulos G., Song C.Z. Down-regulation of CXCR4 by inducible small interfering RNA inhibits breast cancer cell invasion in vitro. Cancer Res. 63:2003;4801-4804.
40. Moon S.Y., Zheng Y. Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13:2003;13-22.
41. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature. 420:2002;629-635.
42. Murphy A.M., Montell D.J. Cell type-specific roles for Cdc42, Rac, and RhoL in Drosophila oogenesis. J Cell Biol. 133:1996;617-630.
43. Lee S., Kolodziej P.A. The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development. 129:2002;1509-1520.
44. Casal J., Leptin M. Identification of novel genes in Drosophila reveals the complex regulation of early gene activity in the mesoderm. Proc Natl Acad Sci USA. 93:1996;10327-10332.
45. Sasamura T., Kobayashi T., Kojima S., Qadota H., Ohya Y., Masai I., Hotta Y. Molecular cloning and characterization of Drosophila genes encoding small GTPases of the rab and rho families. Mol Gen Genet. 254:1997;486-494.
46. Schmitz A.A., Govek E.E., Bottner B., Van Aelst L. Rho GTPases: signaling, migration, and invasion. Exp Cell Res. 261:2000;1-12.
47. Fulga T.A., Rorth P. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol. 4:2002;715-719.
48. Geisbrecht E.R., Montell D.J. Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol. 4:2002;616-620.
49. Oda H., Uemura T., Takeichi M. Phenotypic analysis of null mutants for DE-cadherin and Armadillo in Drosophila ovaries reveals distinct aspects of their functions in cell adhesion and cytoskeletal organization. Genes Cells. 2:1997;29-40.
50. Niewiadomska P., Godt D., Tepass U. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J Cell Biol. 144:1999;533-547.
51. Jenkins A.B., McCaffery J.M., Van Doren M. Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis. Development. 130:2003;4417-4426 This paper describes the ensheathment of the primordial germ cells by the somatic gonadal cells in the embryos, and shows that E-cad is required in the soma for this to occur. It also shows that maternal contribution of E-cad to the germ cells is necessary for their successful migration.
52. Van Doren M., Mathews W.R., Samuels M., Moore L.A., Broihier H.T., Lehmann R. Fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development. 130:2003;2355-2364 Found in a large-scale mutagenesis screen, the fear of intimacy gene is shown to be required for the compaction of the germ cells and somatic gonadal cells into the coalesced embryonic gonad. fear of intimacy mutant embryos phenocopy E-cad mutants with respect to gonad and tracheal fusion defects.
53. Uemura T., Oda H., Kraut R., Hayashi S., Kotaoka Y., Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10:1996;659-671.
54. Wheelock M.J., Soler A.P., Knudsen K.A. Cadherin junctions in mammary tumors. J Mammary Gland Biol Neoplasia. 6:2001;275-285.
55. Guilford P. E-cadherin downregulation in cancer: fuel on the fire? Mol Med Today. 5:1999;172-177.
56. Bukholm I.K., Nesland J.M., Borresen-Dale A.L. Re-expression of E-cadherin, alpha-catenin and beta-catenin, but not of gamma-catenin, in metastatic tissue from breast cancer patients. J Pathol. 190:2000;15-19.
57. Manning D.L., Daly R.J., Lord P.G., Kelly K.F., Green C.D. Effects of oestrogen on the expression of a 4.4 kb mRNA in the ZR-75-1 human breast cancer cell line. Mol Cell Endocrinol. 59:1988;205-212.
58. Manning D.L., Robertson J.F., Ellis I.O., Elston C.W., McClelland R.A., Gee J.M., Jones R.J., Green C.D., Cannon P., Blamey R.W.et al. Oestrogen-regulated genes in breast cancer: association of pLIV1 with lymph node involvement. Eur J Cancer. 30A:1994;675-678.