Genes that drive invasion and migration in Drosophila.

Successful cell migration depends on the careful regulation of the timing of movement, the guidance of motile cells, and cytoskeletal and adhesive changes within the cells. This review focuses on genes that act cell-autonomously to promote these aspects of cell migration in Drosophila. We discuss recent advances in understanding the migration of the ovarian border cells, embryonic blood cells, primordial germ cells, somatic gonadal precursors, and tracheal cells. Comparison of genes that regulate these processes to those that promote tumorigenesis and metastasis in mammals demonstrates that studies in fruit flies are uncovering new genes highly relevant to cancer biology.

[1]  Eric Johnson,et al.  Developmental Control of Blood Cell Migration by the Drosophila VEGF Pathway , 2002, Cell.

[2]  P. Rørth,et al.  Guidance of Cell Migration by the Drosophila PDGF/VEGF Receptor , 2001, Cell.

[3]  U. Tepass,et al.  DE-Cadherin Is Required for Intercellular Motility during Drosophila Oogenesis , 1999, The Journal of cell biology.

[4]  Xianglin Shi,et al.  Overexpression of ErbB2 enhances ethanol-stimulated intracellular signaling and invasion of human mammary epithelial and breast cancer cells in vitro , 2003, Oncogene.

[5]  D. Montell,et al.  Cell type-specific roles for Cdc42, Rac, and RhoL in Drosophila oogenesis , 1996, The Journal of cell biology.

[6]  Y. Matsui,et al.  Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1) , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Gutkind,et al.  mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. , 2002, Genes & development.

[8]  P. Meltzer,et al.  AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. , 1997, Science.

[9]  R. Lehmann,et al.  fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila , 2003, Development.

[10]  Nobuyuki Itoh,et al.  Tube or not tube: remodeling epithelial tissues by branching morphogenesis. , 2003, Developmental cell.

[11]  P. Rørth,et al.  Invasive cell migration is initiated by guided growth of long cellular extensions , 2002, Nature Cell Biology.

[12]  H. Nakshatri,et al.  NF-κ B Promotes Breast Cancer Cell Migration and Metastasis by Inducing the Expression of the Chemokine Receptor CXCR4* , 2003, Journal of Biological Chemistry.

[13]  G. Stamatoyannopoulos,et al.  Down-regulation of CXCR4 by inducible small interfering RNA inhibits breast cancer cell invasion in vitro. , 2003, Cancer research.

[14]  M. Van Doren,et al.  Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis , 2003, Development.

[15]  M. Krasnow,et al.  branchless Encodes a Drosophila FGF Homolog That Controls Tracheal Cell Migration and the Pattern of Branching , 1996, Cell.

[16]  D. Montell,et al.  Myosin VI is required for E-cadherin-mediated border cell migration , 2002, Nature Cell Biology.

[17]  A. P. Soler,et al.  Cadherin Junctions in Mammary Tumors , 2001, Journal of Mammary Gland Biology and Neoplasia.

[18]  Stephen Brown,et al.  Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless , 2001, Current Biology.

[19]  D. Meyer,et al.  Guidance of Primordial Germ Cell Migration by the Chemokine SDF-1 , 2002, Cell.

[20]  B. Shilo,et al.  breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. , 1992, Genes & development.

[21]  J. Darnell,et al.  Constitutively activated Stat3 protects fibroblasts from serum withdrawal and UV-induced apoptosis and antagonizes the proapoptotic effects of activated Stat1. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Affolter,et al.  In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. , 2002, Developmental cell.

[23]  R. Bell.  What Can We Learn from Herceptin® Trials in Metastatic Breast Cancer? , 2002, Oncology.

[24]  C. Nüsslein-Volhard,et al.  A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor , 2003, Nature.

[25]  D. Montell,et al.  Regulation of Invasive Cell Behavior by Taiman, a Drosophila Protein Related to AIB1, a Steroid Receptor Coactivator Amplified in Breast Cancer , 2000, Cell.

[26]  D. Montell,et al.  PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman , 2003, Development.

[27]  I. Ellis,et al.  Oestrogen-regulated genes in breast cancer: association of pLIV1 with lymph node involvement. , 1994, European journal of cancer.

[28]  Seungbok Lee,et al.  The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. , 2002, Development.

[29]  B. Shilo,et al.  Breathless, a Drosophila FGF receptor homolog, is required for the onset of tracheal cell migration and tracheole formation , 1995, Mechanisms of Development.

[30]  D. Montell,et al.  Border-cell migration: the race is on , 2003, Nature Reviews Molecular Cell Biology.

[31]  T. Uemura,et al.  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 , 1997, Genes to cells : devoted to molecular & cellular mechanisms.

[32]  R. Bachelder,et al.  Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. , 2002, Cancer research.

[33]  B. Shilo,et al.  The Drosophila FGF-R homolog is expressed in the embryonic tracheal system and appears to be required for directed tracheal cell extension. , 1991, Genes & development.

[34]  A. Hall,et al.  Rho GTPases in cell biology , 2002, Nature.

[35]  R. Lehmann,et al.  The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival , 2003, Development.

[36]  M. Krasnow,et al.  Tube Morphogenesis Making and Shaping Biological Tubes , 2003, Cell.

[37]  R. Lehmann,et al.  Tre1, a G Protein-Coupled Receptor, Directs Transepithelial Migration of Drosophila Germ Cells , 2003, PLoS biology.

[38]  M. Leptin,et al.  Identification of novel genes in Drosophila reveals the complex regulation of early gene activity in the mesoderm. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[39]  R. Schuh,et al.  Drosophila tracheal system formation involves FGF‐dependent cell extensions contacting bridge‐cells , 2002, EMBO reports.

[40]  C K Redmond,et al.  Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. , 1999, Journal of the National Cancer Institute.

[41]  C. Samakovlis,et al.  Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. , 2003, Trends in cell biology.

[42]  Fabrice Carballès,et al.  The Drosophila cytokine receptor Domeless controls border cell migration and epithelial polarization during oogenesis , 2002, Development.

[43]  A. Børresen-Dale,et al.  Re‐expression of E‐cadherin, α‐catenin and β‐catenin, but not of γ‐catenin, in metastatic tissue from breast cancer patients , 2000 .

[44]  Makoto Sato,et al.  FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. , 2002, Developmental cell.

[45]  H. Höfler,et al.  Cancer progression and tumor cell motility are associated with the FGFR4 Arg(388) allele. , 2002, Cancer research.

[46]  I. Zhimulev,et al.  EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue , 2003, Development.

[47]  P. Guilford.  E-cadherin downregulation in cancer: fuel on the fire? , 1999, Molecular medicine today.

[48]  T. Uemura,et al.  Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. , 1996, Genes & development.

[49]  P. Lord,et al.  Effects of oestrogen on the expression of a 4.4 kb mRNA in the ZR-75-1 human breast cancer cell line , 1988, Molecular and Cellular Endocrinology.

[50]  Yi Zheng,et al.  Rho GTPase-activating proteins in cell regulation. , 2003, Trends in cell biology.

[51]  P. Rørth,et al.  Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. , 2001, Science.

[52]  D. Montell,et al.  Paracrine Signaling through the JAK/STAT Pathway Activates Invasive Behavior of Ovarian Epithelial Cells in Drosophila , 2001, Cell.

[53]  L. Van Aelst,et al.  Rho GTPases: signaling, migration, and invasion. , 2000, Experimental cell research.

[54]  Y. Ohya,et al.  Molecular cloning and characterization of Drosophila genes encoding small GTPases of the rab and rho families , 1997, Molecular and General Genetics MGG.

[55]  R. Lehmann,et al.  Moving towards the next generation , 2001, Mechanisms of Development.