Tumor invasion and metastasis in Drosophila: A bold past, a bright future

Rhoda K.A. Stefanatos; Marcos Vidal

doi:10.1016/j.jgg.2011.09.004

Volume 38 Issue 10

Oct. 2011

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Tumor invasion and metastasis in Drosophila: A bold past, a bright future

doi: 10.1016/j.jgg.2011.09.004

Beatson Institute for Cancer Research, Garscube Estate, Switchback Rd, Bearsden, Glasgow G61 1BD, UK

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Corresponding author: E-mail address: m.vidal@beatson.gla.ac.uk (Marcos Vidal)
Received Date: 2011-07-25
Accepted Date: 2011-09-06
Rev Recd Date: 2011-09-05

Available Online: 2011-09-17

Publish Date: 2011-10-20

Abstract

Abstract

Invasion and metastasis are the most deadly hallmarks of cancer. Once a cancer has acquired the ability to colonize new sites in the body it becomes dramatically more difficult to treat. This has made it a focus of much of cancer research. The humble fruit fly, Drosophila melanogaster, has despite its relative simplicity, made significant contributions to the understanding of tumor progression. In this review we outline and highlight those with an emphasis on modeling the genetic and epigenetic changes required for invasion and metastasis. We will revisit the early years of cancer modeling in Drosophila where the first parallels were drawn between Drosophila and vertebrate neoplasms and highlight recent advances using genetic screens and interactions with the epithelial microenvironment and innate immune system. We focus on the power and limitations of current fly models of metastasis.
- Cancer,
- Metastasis

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References(63)

References

[1]	Adams, M.D., Celniker, S.E., Holt, R.A. et al. Science, 287 (2000),pp. 2185-2195
[2]	Albini, A., Sporn, M.B. The tumour microenvironment as a target for chemoprevention Nat. Rev. Cancer, 7 (2007),pp. 139-147
[3]	Beaucher, M., Hersperger, E., Page-McCaw, A. et al. Dev. Biol., 303 (2007),pp. 625-634
[4]	Beaucher, M., Goodliffe, J., Hersperger, E. et al. Dev. Biol., 301 (2007),pp. 287-297
[5]	Bernards, R., Weinberg, R. Metastasis genes: a progression puzzle Nature, 418 (2002),p. 823
[6]	Bilder, D., Li, M., Perrimon, N. Science, 289 (2000),pp. 113-116
[7]	Bridges, C.B., Brehme, K.S.
[8]	Brumby, A.M., Richardson, H.E. EMBO J., 22 (2003),pp. 5769-5779
[9]	Brumby, A.M., Goulding, K.R., Schlosser, T. et al. Genetics, 188 (2011),pp. 105-125
[10]	Chan, H.Y., Bonini, N.M. Cell Death Differ., 7 (2000),pp. 1075-1080
[11]	Charroux, B., Royet, J. Fly, 4 (2010),pp. 40-47
[12]	Cordero, J., Vidal, M., Sansom, O. APC as a master regulator of intestinal homeostasis and transformation: from flies to vertebrates Cell Cycle, 8 (2009),pp. 2926-2931
[13]	Cordero, J.B., Sansom, O.J. Wnt signalling and its role in stem cell-driven intestinal regeneration and hyperplasia Acta Physiol (2011)
[14]	Cordero, J.B., Macagno, J.P., Stefanatos, R.K. et al. Oncogenic Ras diverts a host TNF tumor suppressor activity into tumor promoter Dev. Cell, 18 (2010),pp. 999-1011
[15]	Dang, D.T., Perrimon, N. Dev. Genet., 13 (1992),pp. 367-375
[16]	Edwards, A., Gladstone, M., Yoon, P. et al. Dis. Model Mech., 4 (2011),pp. 496-503
[17]	Ferres-Marco, D., Gutierrez-Garcia, I., Vallejo, D.M. et al. Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing Nature, 439 (2006),pp. 430-436
[18]	Gateff, E. Science, 200 (1978),pp. 1448-1459
[19]	Hanahan, D., Weinberg, R.A. Hallmarks of cancer: the next generation Cell, 144 (2011),pp. 646-674
[20]	Hogan, C., Dupré-Crochet, S., Norman, M. et al. Characterization of the interface between normal and transformed epithelial cells Nat. Cell Biol., 11 (2009),pp. 460-467
[21]	Huang, J., Wu, S., Barrera, J. et al. Cell, 122 (2005),pp. 421-434
[22]	Huang, S., Houghton, P.J. Targeting mTOR signaling for cancer therapy Curr. Opin. Pharmacol., 3 (2003),pp. 371-377
[23]	Humbert, P.O., Grzeschik, N.A., Brumby, A.M. et al. Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module Oncogene, 27 (2008),pp. 6888-6907
[24]	Igaki, T., Pastor-Pareja, J.C., Aonuma, H. et al. Dev. Cell, 16 (2009),pp. 458-465
[25]	Jiang, H., Patel, P.H., Kohlmaier, A. et al. Cell, 137 (2009),pp. 1343-1355
[26]	Kajita, M., Hogan, C., Harris, A.R. et al. Interaction with surrounding normal epithelial cells influences signalling pathways and behaviour of Src-transformed cells J. Cell Sci., 123 (2010),pp. 171-180
[27]	Lee, T., Luo, L. Trends Neurosci., 24 (2001),pp. 251-254
[28]	Lee, W.C., Beebe, K., Sudmeier, L. et al. Development, 136 (2009),pp. 2255-2264
[29]	McCarthy, N. Cancer genetics: networking on the fly Nat. Rev. Genet., 10 (2009),p. 150
[30]	McClure, K.D., Sustar, A., Schubiger, G. Dev. Biol., 319 (2008),pp. 68-77
[31]	Mechler, B.M., McGinnis, W., Gehring, W.J. EMBO J., 4 (1985),pp. 1551-1557
[32]	Micchelli, C.A., Perrimon, N. Nature, 439 (2006),pp. 475-479
[33]	Montell, D.J. Border-cell migration: the race is on Nat. Rev. Mol. Cell Biol., 4 (2003),pp. 13-24
[34]	Moreno, E., Basler, K., Morata, G. Nature, 416 (2002),pp. 755-759
[35]	Nguyen, D.X., Massagué, J. Genetic determinants of cancer metastasis Nat. Rev. Genet., 8 (2007),pp. 341-352
[36]	Ohlstein, B., Spradling, A. Nature, 439 (2006),pp. 470-474
[37]	Ohsawa, S., Sugimura, K., Takino, K. et al. Dev. Cell, 20 (2011),pp. 315-328
[38]	Pagliarini, R.A., Xu, T. Science, 302 (2003),pp. 1227-1231
[39]	Parisi, F., Vidal, M. Cell Adh. Migr., 5 (2011),pp. 366-372
[40]	Podsypanina, K., Du, Y.-C.N., Jechlinger, M. et al. Seeding and propagation of untransformed mouse mammary cells in the lung Science, 321 (2008),pp. 1841-1844
[41]	Raftery, L.A., Sutherland, D.J. Dev. Biol., 210 (1999),pp. 251-268
[42]	Harshbarger, J.C., Taylor, R.L. Neoplasms of insects Annu. Rev. Entomol., 13 (1968),pp. 159-190
[43]	Ryoo, H.D., Gorenc, T., Steller, H. Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways Dev. Cell, 7 (2004),pp. 491-501
[44]	Schafer, M., Werner, S. Cancer as an overhealing wound: an old hypothesis revisited Nat. Rev. Mol. Cell Biol., 9 (2008),pp. 628-638
[45]	Schneider, D. Nat. Rev. Genet., 1 (2000),pp. 218-226
[46]	St John, M.A., Xu, T. Understanding human cancer in a fly? Am. J. Hum. Genet., 61 (1997),pp. 1006-1010
[47]	Stark, M. J. Cancer Res., 3 (1918),pp. 279-299
[48]	Stefanatos, R., Sanz, A. Mitochondrial complex I: a central regulator of the aging process Cell Cycle, 10 (2011),pp. 1528-1532
[49]	Stern, C.
[50]	Theodosiou, N.A., Xu, T. Methods, 14 (1998),pp. 355-365
[51]	Toba, G., Ohsako, T., Miyata, N. et al. Genetics, 151 (1999),pp. 725-737
[52]	Valanne, S., Wang, J.-H., Rämet, M. J. Immunol., 186 (2011),pp. 649-656
[53]	Vallejo, D.M., Caparros, E., Dominguez, M. Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells EMBO J., 30 (2011),pp. 756-769
[54]	Vidal, M., Cagan, R.L. Curr. Opin. Genet. Dev., 16 (2006),pp. 10-16
[55]	Vidal, M., Larson, D.E., Cagan, R.L. Dev. Cell, 10 (2006),pp. 33-44
[56]	Vidal, M., Wells, S., Ryan, A. et al. Cancer Res., 65 (2005),pp. 3538-3541
[57]	Vidal, M., Warner, S., Read, R. et al. Cancer Res., 67 (2007),pp. 10278-10285
[58]	Willecke, M., Toggweiler, J., Basler, K. Oncogene (2011)
[59]	Woodhouse, E., Hersperger, E., Shearn, A. Dev. Genes Evol., 207 (1998),pp. 542-550
[60]	Woodhouse, E., Hersperger, E., Stetler-Stevenson, W.G. et al. Cell Growth Differ., 5 (1994),pp. 151-159
[61]	Woodhouse, E.C., Fisher, A., Bandle, R.W. et al. Proc. Natl. Acad. Sci. USA, 100 (2003),pp. 11463-11468
[62]	Wu, M., Pastor-Pareja, J.C., Xu, T. Interaction between RasV12 and scribbled clones induces tumour growth and invasion Nature, 463 (2010),pp. 545-548
[63]	Yoshida, H., Cheng, W., Hung, J. et al. Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 8144-8149