Border-cell migration: the race is on

Denise J. Montell

doi:10.1038/nrm1006

journal article Jan 01, 2003

Border-cell migration: the race is on

Denise J. Montell

Nature Reviews Molecular Cell Biology Vol. 4 No. 1 pp. 13-24 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/nrm1006

Topics

No keywords indexed for this article. Browse by subject →

References

59

[1]

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, 1047–1058 (2000). This paper reports the surprising finding that Ecdysone, signalling through the Ecdysone receptor and its coactivator Taiman, regulates border-cell migration. 10.1016/s0092-8674(00)00208-7

[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, 831–841 (2001). This paper reports the identification of the signal and signalling pathway that distinguishes the cells that acquire the ability to migrate from those that cannot. 10.1016/s0092-8674(01)00607-9

[3]

Duchek, P., Somogyi, K., Jekely, G., Beccari, S. & Rørth, P. Guidance of cell migration by the Drosophila pdgf/vegf receptor. Cell 107, 17–26 (2001). This paper reports the identification of a growth factor expressed in the germline, which acts through a receptor tyrosine kinase expressed by all of the follicle cells and which is involved in guiding the border cells to the oocyte. 10.1016/s0092-8674(01)00502-5

[4]

King, R. C. Ovarian Development in Drosophila melanogaster (Academic, New York, 1970).

[5]

Spradling, A. C. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez-Arias, A.) 1–70 (Cold Spring Harbor Laboratory Press, New York, 1993).

[6]

Margolis, J. & Spradling, A. C. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807 (1995). 10.1242/dev.121.11.3797

[7]

Montell, D. J., Rørth, P. & Spradling, A. C. slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71, 51–62 (1992). This paper reports the identification of the first mutation showing border-cell migration defects and the cloning of the corresponding gene. 10.1016/0092-8674(92)90265-e

[8]

Savant-Bhonsale, S. & Montell, D. J. torso-like encodes the localized determinant of Drosophila terminal pattern formation. Genes Dev. 7, 2548–2555 (1993). 10.1101/gad.7.12b.2548

[9]

Rørth, P. & Montell, D. J. Drosophila C/EBP: a tissue-specific DNA-binding protein required for embryonic development. Genes Dev. 6, 2299–2311 (1992). 10.1101/gad.6.12a.2299

[10]

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, 29–40 (1997). 10.1046/j.1365-2443.1997.d01-284.x

[11]

Niewiadomska, P., Godt, D. & Tepass, U. DE-cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144, 533–547 (1999). This work reports the finding that DE-cadherin is required both in border cells and in nurse cells for border-cell migration to occur. 10.1083/jcb.144.3.533

[12]

Takeichi, M. Cadherins in cancer: implications for invasion and metastasis. Curr. Opin. Cell Biol. 5, 806–811 (1993). 10.1016/0955-0674(93)90029-p

[13]

Fujita, Y. et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nature Cell Biol. 4, 222–231 (2002). 10.1038/ncb758

[14]

Sundfeldt, K. et al. E-cadherin expression in human epithelial ovarian cancer and normal ovary. Int. J. Cancer 74, 275–280 (1997). 10.1002/(sici)1097-0215(19970620)74:3<275::aid-ijc7>3.0.co;2-w

[15]

Kim, J. B. et al. N-Cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J. Cell Biol. 151, 1193–1206 (2000). 10.1083/jcb.151.6.1193

[16]

Lilien, J., Balsamo, J., Arregui, C. & Xu, G. Turn-off, drop-out: functional state switching of cadherins. Dev. Dyn. 224, 18–29 (2002). 10.1002/dvdy.10087

[17]

Liu, Y. & Montell, D. J. jing: a downstream target of slbo required for developmental control of border cell migration. Development 128, 321–330 (2001). 10.1242/dev.128.3.321

[18]

Geisbrecht, E. R. & Montell, D. J. Myosin VI is required for E-cadherin-mediated border cell migration. Nature Cell Biol. 4, 616–620 (2002). 10.1038/ncb830

[19]

Liu, Y. & Montell, D. J. Identification of mutations that cause cell migration defects in mosaic clones. Development 126, 1869–1878 (1999). 10.1242/dev.126.9.1869

[20]

Rørth, P. et al. Systematic gain-of-function genetics in Drosophila. Development 125, 1049–1057 (1998). 10.1242/dev.125.6.1049

[21]

Han, D. D., Stein, D. & Stevens, L. M. Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. Development 127, 573–583 (2000). 10.1242/dev.127.3.573

[22]

Aaronson, D. S. & Horvath, C. M. A road map for those who don't know JAK–STAT. Science 296, 1653–1655 (2002). 10.1126/science.1071545

[23]

Harrison, D. A., McCoon, P. E., Binari, R., Gilman, M. & Perrimon, N. Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 12, 3252–3263 (1998). 10.1101/gad.12.20.3252

[24]

Beccari, S., Teixeira, L. & Rørth, P. The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech. Dev. 111, 115–123 (2002). 10.1016/s0925-4773(01)00615-3

[25]

LaBonne, C. & Bronner-Fraser, M. Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. Dev. Biol. 221, 195–205 (2000). 10.1006/dbio.2000.9609

[26]

Yamashita, S. et al. Stat3 controls cell movements during zebrafish gastrulation. Dev. Cell 2, 363–375 (2002). 10.1016/s1534-5807(02)00126-0

[27]

Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis

S. Sano

The EMBO Journal 1999 10.1093/emboj/18.17.4657

[28]

The role of STATs in transcriptional control and their impact on cellular function

Jacqueline Bromberg, James E Darnell

Oncogene 2000 10.1038/sj.onc.1203476

[29]

Buettner, R., Mora, L. B. & Jove, R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 8, 945–954 (2002).

[30]

Anzick, S. L. et al. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277, 965–968 (1997). 10.1126/science.277.5328.965

[31]

Chen, J. D. Steroid/nuclear receptor coactivators. Vitam. Horm. 58, 391–448 (2000). 10.1016/s0083-6729(00)58032-7

[32]

Fisher, B. 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, 1371–1388 (1998). 10.1093/jnci/90.18.1371

[33]

Riddiford, L. M. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez Arias, A.) 899–940 (Cold Spring Harbor Laboratory Press, New York, 1993).

[34]

Su, M. et al. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585–594 (2000). 10.1242/dev.127.3.585

[35]

Yu, T. W. & Bargmann, C. I. Dynamic regulation of axon guidance. Nature Neurosci. 4, 1169–1176 (2001). 10.1038/nn748

[36]

Hedgecock, E. M., Culotti, J. G. & Hall, D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61–85 (1990). 10.1016/0896-6273(90)90444-k

[37]

DeVore, D. L., Horvitz, H. R. & Stern, M. J. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83, 611–620 (1995). 10.1016/0092-8674(95)90101-9

[38]

Simpson, J. H., Bland, K. S., Fetter, R. D. & Goodman, C. S. Short-range and long-range guidance by Slit and its Robo receptors: a combinatorial code of Robo receptors controls lateral position. Cell 103, 1019–1032 (2000). 10.1016/s0092-8674(00)00206-3

[39]

Heino, T. I. et al. The Drosophila VEGF receptor homolog is expressed in hemocytes. Mech. Dev. 109, 69–77 (2001). 10.1016/s0925-4773(01)00510-x

[40]

Cho, N. K. et al. Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108, 865–876 (2002). 10.1016/s0092-8674(02)00676-1

[41]

Duchek, P. & Rørth, P. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291, 131–133 (2001). This paper shows that signalling through the Egf receptor controls the late, dorsalward migration of the border cells. 10.1126/science.291.5501.131

[42]

Wasserman, J. D. & Freeman, M. An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355–364 (1998). 10.1016/s0092-8674(00)81767-5

[43]

Carl, T. F., Dufton, C., Hanken, J. & Klymkowsky, M. W. Inhibition of neural crest migration in Xenopus using antisense slug RNA. Dev. Biol. 213, 101–115 (1999). 10.1006/dbio.1999.9320

[44]

O'Rourke, M. P. & Tam, P. P. Twist functions in mouse development. Int. J. Dev. Biol. 46, 401–413 (2002).

[45]

Gomperts, M., Garcia-Castro, M., Wylie, C. & Heasman, J. Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120, 135–141 (1994). 10.1242/dev.120.1.135

[46]

Kulesa, P. M. & Fraser, S. E. In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. Development 127, 1161–1172 (2000). 10.1242/dev.127.6.1161

[47]

Alexandre, D. & Ghysen, A. Somatotopy of the lateral line projection in larval zebrafish. Proc. Natl Acad. Sci. USA 96, 7558–7562 (1999). 10.1073/pnas.96.13.7558

[48]

Nabeshima, K., Inoue, T., Shimao, Y., Kataoka, H. & Koono, M. Cohort migration of carcinoma cells: differentiated colorectal carcinoma cells move as coherent cell clusters or sheets. Histol. Histopathol. 14, 1183–1197 (1999).

[49]

Liu, H., Chen, B., Zardi, L. & Ramos, D. M. Soluble fibronectin promotes migration of oral squamous-cell carcinoma cells. Int. J. Cancer 78, 261–267 (1998). 10.1002/(sici)1097-0215(19981005)78:2<261::aid-ijc22>3.0.co;2-c

[50]

Xie, T. & Spradling, A. C. A niche maintaining germ line stem cells in the Drosophila ovary. Science 290, 328–330 (2000). 10.1126/science.290.5490.328

Showing 50 of 59 references

Cited By

297

Cellular memory in eukaryotic chemotaxis depends on the background chemoattractant concentration

Richa Karmakar, Man-Ho Tang · 2021

Physical Review E

Non-apoptotic function of Drosophila caspase activation in epithelial thorax closure and wound healing

Yuya Fujisawa, Hina Kosakamoto · 2019

Development

JNK Signaling Controls Border Cell Cluster Integrity and Collective Cell Migration

Flora Llense, Enrique Martin-Blanco · 2008

Current Biology