Border-cell migration: the race is on

The conversion of stationary epithelial cells into migratory, invasive cells is important for normal embryonic development and tumour metastasis. Border-cell migration in the ovary of Drosophila melanogaster has emerged as a simple, genetically tractable model for studying this process. Three distinct signals, which are also upregulated in cancer, control border-cell migration, so identifying further genes that are involved in border-cell migration could provide new insights into tumour invasion.

[1]  N. Perrimon,et al.  Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. , 1998, Genes & development.

[2]  P. Rørth,et al.  Drosophila C/EBP: a tissue-specific DNA-binding protein required for embryonic development. , 1992, Genes & development.

[3]  J. Chen,et al.  Steroid/nuclear receptor coactivators. , 2000, Vitamins and hormones.

[4]  J. C. Li,et al.  Development in DROSOPHILA MELANOGASTER. , 1927, Genetics.

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

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

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

[8]  R. L. Tucker,et al.  The ecdysoneless (ecd1ts) mutation disrupts ecdysteroid synthesis autonomously in the ring gland of Drosophila melanogaster. , 1987, Developmental biology.

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

[10]  A. Spradling,et al.  Identification and behavior of epithelial stem cells in the Drosophila ovary. , 1995, Development.

[11]  D. Montell,et al.  Jing: a downstream target of slbo required for developmental control of border cell migration. , 2001, Development.

[12]  M. García-Castro,et al.  Interactions between primordial germ cells play a role in their migration in mouse embryos. , 1994, Development.

[13]  K. Edwards,et al.  Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. , 1996, Development.

[14]  U. Tepass,et al.  Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis , 2000, The Journal of cell biology.

[15]  W. Birchmeier,et al.  Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex , 2002, Nature Cell Biology.

[16]  D. Montell,et al.  Identification of mutations that cause cell migration defects in mosaic clones. , 1999, Development.

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

[18]  A. Ghysen,et al.  Somatotopy of the lateral line projection in larval zebrafish. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  K. Sass,et al.  N-Cadherin Extracellular Repeat 4 Mediates Epithelial to Mesenchymal Transition and Increased Motility , 2000, The Journal of cell biology.

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

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

[22]  D. Hall,et al.  The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans , 1990, Neuron.

[23]  M. Takeichi.  Cadherins in cancer: implications for invasion and metastasis. , 1993, Current opinion in cell biology.

[24]  J. Hanken,et al.  Inhibition of neural crest migration in Xenopus using antisense slug RNA. , 1999, Developmental biology.

[25]  A. Spradling,et al.  slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C EBP , 1992, Cell.

[26]  L. Stevens,et al.  Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. , 2000, Development.

[27]  J. Lilien,et al.  Turn‐off, drop‐out: Functional state switching of cadherins , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[28]  S. Fraser,et al.  In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. , 2000, Development.

[29]  L. Zardi,et al.  Soluble fibronectin promotes migration of oral squamous‐cell carcinoma cells , 1998, International journal of cancer.

[30]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[31]  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.

[32]  A. Schier,et al.  Stat3 Controls Cell Movements during Zebrafish Gastrulation. , 2002, Developmental cell.

[33]  M. Freeman,et al.  An Autoregulatory Cascade of EGF Receptor Signaling Patterns the Drosophila Egg , 1998, Cell.

[34]  T. Xu,et al.  Mosaic analysis using FLP recombinase. , 1994, Methods in cell biology.

[35]  D. Montell,et al.  torso-like encodes the localized determinant of Drosophila terminal pattern formation. , 1993, Genes & development.

[36]  Cori Bargmann,et al.  Dynamic regulation of axon guidance , 2001, Nature Neuroscience.

[37]  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.

[38]  J. Darnell,et al.  The role of STATs in transcriptional control and their impact on cellular function , 2000, Oncogene.

[39]  S. Enerbäck,et al.  E‐cadherin expression in human epithelial ovarian cancer and normal ovary , 1997, International journal of cancer.

[40]  P. Rørth,et al.  The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. , 2000, Molecular cell.

[41]  M. Bronner‐Fraser,et al.  Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. , 2000, Developmental biology.

[42]  S. Akira,et al.  Keratinocyte‐specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis , 1999, The EMBO journal.

[43]  Julie H. Simpson,et al.  Short-Range and Long-Range Guidance by Slit and Its Robo Receptors A Combinatorial Code of Robo Receptors Controls Lateral Position , 2000, Cell.

[44]  R. King.  Ovarian Development in Drosophila Melanogaster , 1970 .

[45]  K. Nabeshima,et al.  Cohort migration of carcinoma cells: differentiated colorectal carcinoma cells move as coherent cell clusters or sheets. , 1999, Histology and histopathology.

[46]  D. Aaronson,et al.  A Road Map for Those Who Don't Know JAK-STAT , 2002, Science.

[47]  J. Culotti,et al.  Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. , 2000, Development.

[48]  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.

[49]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[50]  G. Rubin,et al.  Systematic gain-of-function genetics in Drosophila. , 1998, Development.

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

[52]  R. Jove,et al.  Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. , 2002, Clinical cancer research : an official journal of the American Association for Cancer Research.

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

[54]  A. Spradling,et al.  A niche maintaining germ line stem cells in the Drosophila ovary. , 2000, Science.

[55]  H. Horvitz,et al.  An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites , 1995, Cell.

[56]  M. Mckeown,et al.  The Drosophila retinoid X receptor homolog ultraspiracle functions in both female reproduction and eye morphogenesis. , 1992, Development.

[57]  P. Tam,et al.  Twist functions in mouse development. , 2002, The International journal of developmental biology.