Skip to main content
Log in

The eye of Drosophila as a model system for studying intracellular signaling in ontogenesis and pathogenesis

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Many human diseases are caused by malfunction of basic types of cellular activity such as proliferation, differentiation, apoptosis, cell polarization, and migration. In turn, these processes are associated with different routes of intracellular signal transduction. A number of model systems have been designed to study normal and abnormal cellular and molecular processes associated with pathogenesis. The developing eye of the fruit fly Drosophila melanogaster is one of these systems. The sequential development of compound eyes of this insect makes it possible to model human neurodegenerative diseases and mechanisms of carcinogenesis. In this paper we overview the program of the eye development in Drosophila, with emphasis on intracellular signaling pathways that regulate this complex process. We discuss in detail the roles of the Notch, Hedgehog, TGFβ, Wnt, and receptor tyrosine kinase signaling pathways in Drosophila eye development and human pathology. We also briefly describe the modern methods of experimentation with this model organism to analyze the function of human pathogenic proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wolff, T., and Ready, D. F. (1993) in The Development of Drosophila melanogaster (Bate, M., and Martinez Arias, A., eds.) Cold Spring Harbor Laboratory Press, pp. 1277–1325.

  2. Kryuchkov, M., Katanaev, V. L., Enin, G. A., Sergeev, A., Timchenko, A. A., and Serdyuk, I. N. (2011) PLoS ONE, 6, e22237.

    PubMed  CAS  Google Scholar 

  3. Bernhard, C. G., Gemne, G., and Sallstrom, J. (1970) J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol., 67, 1–25.

    Google Scholar 

  4. Miller, W. H., Bernard, G. D., and Allen, J. L. (1968) Science, 162, 760–767.

    PubMed  CAS  Google Scholar 

  5. Palasantzas, G., de Hosson, J. T. M., Michielsen, K. F. L., and Stavenga, D. G. (2005) in Handbook of Nanostructured Biomaterials and Their Applications in Nanobiotechnology (Nalwa, H. S., ed.) American Scientific Publishers, pp. 273–301.

  6. Kirschfeld, K., Feiler, R., and Franceschini, N. (1978) J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol., 125, 275–284.

    CAS  Google Scholar 

  7. Salcedo, E., Huber, A., Henrich, S., Chadwell, L. V., Chou, W. H., Paulsen, R., and Britt, S. G. (1999) J. Neurosci., 19, 10716–10726.

    PubMed  CAS  Google Scholar 

  8. Papatsenko, D., Sheng, G., and Desplan, C. (1997) Development, 124, 1665–1673.

    PubMed  CAS  Google Scholar 

  9. Tomlinson, A. (2003) Dev. Cell, 5, 799–809.

    PubMed  CAS  Google Scholar 

  10. Quiring, R., Walldorf, U., Kloter, U., and Gehring, W. J. (1994) Science, 265, 785–789.

    PubMed  CAS  Google Scholar 

  11. Halder, G., Callaerts, P., and Gehring, W. J. (1995) Science, 267, 1788–1792.

    PubMed  CAS  Google Scholar 

  12. Tomlinson, A., and Struhl, G. (2001) Mol. Cell, 7, 487–495.

    PubMed  CAS  Google Scholar 

  13. Cayouette, M., and Raff, M. (2002) Nat. Neurosci., 5, 1265–1269.

    PubMed  CAS  Google Scholar 

  14. Janes, K. A., and Yaffe, M. B. (2006) Nat. Rev. Mol. Cell Biol., 7, 820–828.

    PubMed  CAS  Google Scholar 

  15. Kiel, C., Yus, E., and Serrano, L. (2010) Cell, 140, 33–47.

    PubMed  CAS  Google Scholar 

  16. Gerhart, J. (1999) Teratology, 60, 226–239.

    PubMed  CAS  Google Scholar 

  17. Levitzki, A., and Klein, S. (2010) Mol. Aspects Med., 31, 287–329.

    PubMed  CAS  Google Scholar 

  18. Artavanis-Tsakonas, S., and Muskavitch, M. A. (2010) Curr. Top. Dev. Biol., 92, 1–29.

    PubMed  CAS  Google Scholar 

  19. Ehebauer, M., Hayward, P., and Martinez-Arias, A. (2006) Sci. STKE, 2006, cm7.

    Google Scholar 

  20. Wharton, K. A., Johansen, K. M., Xu, T., and Artavanis-Tsakonas, S. (1985) Cell, 43, 567–581.

    PubMed  CAS  Google Scholar 

  21. Rebay, I., Fleming, R. J., Fehon, R. G., Cherbas, L., Cherbas, P., and Artavanis-Tsakonas, S. (1991) Cell, 67, 687–699.

    PubMed  CAS  Google Scholar 

  22. Aster, J. C., Pear, W. S., and Blacklow, S. C. (2008) Annu. Rev. Physiol., 3, 587–613.

    CAS  Google Scholar 

  23. Stanley, P., and Okajima, T. (2010) Curr. Top. Dev. Biol., 92, 131–164.

    PubMed  CAS  Google Scholar 

  24. Blaumueller, C. M., Qi, H., Zagouras, P., and Artavanis-Tsakonas, S. (1997) Cell, 90, 281–291.

    PubMed  CAS  Google Scholar 

  25. Logeat, F., Bessia, C., Brou, C., LeBail, O., Jarriault, S., Seidah, N. G., and Israel, A. (1998) Proc. Natl. Acad. Sci. USA, 95, 8108–8112.

    PubMed  CAS  Google Scholar 

  26. Zolkiewska, A. (2008) Cell. Mol. Life Sci., 65, 2056–2068.

    PubMed  CAS  Google Scholar 

  27. Jorissen, E., and de Strooper, B. (2010) Curr. Top. Dev. Biol., 92, 201–230.

    PubMed  CAS  Google Scholar 

  28. Struhl, G., and Adachi, A. (1998) Cell, 93, 649–660.

    PubMed  CAS  Google Scholar 

  29. Bray, S., and Bernard, F. (2010) Curr. Top. Dev. Biol., 92, 253–275.

    PubMed  CAS  Google Scholar 

  30. Krejci, A., Bernard, F., Housden, B. E., Collins, S., and Bray, S. J. (2009) Sci. Signal., 2, ra1.

    PubMed  Google Scholar 

  31. Heitzler, P., Bourouis, M., Ruel, L., Carteret, C., and Simpson, P. (1996) Development, 122, 161–171.

    PubMed  CAS  Google Scholar 

  32. Sprinzak, D., Lakhanpal, A., Lebon, L., Santat, L. A., Fontes, M. E., Anderson, G. A., Garcia-Ojalvo, J., and Elowitz, M. B. (2010) Nature, 465, 86–90.

    PubMed  CAS  Google Scholar 

  33. Barad, O., Rosin, D., Hornstein, E., and Barkai, N. (2010) Sci. Signal., 3, ra51.

    PubMed  Google Scholar 

  34. Bray, S. (1998) Semin. Cell Dev. Biol., 9, 591–597.

    PubMed  CAS  Google Scholar 

  35. Ellisen, L. W., Bird, J., West, D. C., Soreng, A. L., Reynolds, T. C., Smith, S. D., and Sklar, J. (1991) Cell, 66, 649–661.

    PubMed  CAS  Google Scholar 

  36. Weng, A. P., Ferrando, A. A., Lee, W., Morris, J. P. T., Silverman, L. B., Sanchez-Irizarry, C., Blacklow, S. C., Look, A. T., and Aster, J. C. (2004) Science, 306, 269–271.

    PubMed  CAS  Google Scholar 

  37. Malecki, M. J., Sanchez-Irizarry, C., Mitchell, J. L., Histen, G., Xu, M. L., Aster, J. C., and Blacklow, S. C. (2006) Mol. Cell Biol., 26, 4642–4651.

    PubMed  CAS  Google Scholar 

  38. Tang, S. C., Jeng, J. S., Lee, M. J., and Yip, P. K. (2009) Acta Neurol. Taiwan, 18, 81–90.

    PubMed  Google Scholar 

  39. Tournier-Lasserve, E., Joutel, A., Melki, J., Weissenbach, J., Lathrop, G. M., Chabriat, H., Mas, J. L., Cabanis, E. A., Baudrimont, M., Maciazek, J., et al. (1993) Nat. Genet., 3, 256–259.

    PubMed  CAS  Google Scholar 

  40. Joutel, A., Corpechot, C., Ducros, A., Vahedi, K., Chabriat, H., Mouton, P., Alamowitch, S., Domenga, V., Cecillion, M., Marechal, E., Maciazek, J., Vayssiere, C., Cruaud, C., Cabanis, E. A., Ruchoux, M. M., Weissenbach, J., Bach, J. F., Bousser, M. G., and Tournier-Lasserve, E. (1996) Nature, 383, 707–710.

    PubMed  CAS  Google Scholar 

  41. Joutel, A., Vahedi, K., Corpechot, C., Troesch, A., Chabriat, H., Vayssiere, C., Cruaud, C., Maciazek, J., Weissenbach, J., Bousser, M. G., Bach, J. F., and Tournier-Lasserve, E. (1997) Lancet, 350, 1511–1515.

    PubMed  CAS  Google Scholar 

  42. Harper, J. A., Yuan, J. S., Tan, J. B., Visan, I., and Guidos, C. J. (2003) Clin. Genet., 64, 461–472.

    PubMed  CAS  Google Scholar 

  43. Joutel, A., Andreux, F., Gaulis, S., Domenga, V., Cecillon, M., Battail, N., Piga, N., Chapon, F., Godfrain, C., and Tournier-Lasserve, E. (2000) J. Clin. Invest., 105, 597–605.

    PubMed  CAS  Google Scholar 

  44. Opherk, C., Duering, M., Peters, N., Karpinska, A., Rosner, S., Schneider, E., Bader, B., Giese, A., and Dichgans, M. (2009) Hum. Mol. Genet., 18, 2761–2767.

    PubMed  CAS  Google Scholar 

  45. Krantz, I. D., Piccoli, D. A., and Spinner, N. B. (1999) Curr. Opin. Pediatr., 11, 558–564.

    PubMed  CAS  Google Scholar 

  46. Oda, T., Elkahloun, A. G., Pike, B. L., Okajima, K., Krantz, I. D., Genin, A., Piccoli, D. A., Meltzer, P. S., Spinner, N. B., Collins, F. S., and Chandrasekharappa, S. C. (1997) Nat. Genet., 16, 235–242.

    PubMed  CAS  Google Scholar 

  47. Li, L., Krantz, I. D., Deng, Y., Genin, A., Banta, A. B., Collins, C. C., Qi, M., Trask, B. J., Kuo, W. L., Cochran, J., Costa, T., Pierpont, M. E., Rand, E. B., Piccoli, D. A., Hood, L., and Spinner, N. B. (1997) Nat. Genet., 16, 243–251.

    PubMed  CAS  Google Scholar 

  48. McDaniell, R., Warthen, D. M., Sanchez-Lara, P. A., Pai, A., Krantz, I. D., Piccoli, D. A., and Spinner, N. B. (2006) Am. J. Hum. Genet., 79, 169–173.

    PubMed  CAS  Google Scholar 

  49. Talora, C., Campese, A. F., Bellavia, D., Felli, M. P., Vacca, A., Gulino, A., and Screpanti, I. (2008) Biochim. Biophys. Acta, 1782, 489–497.

    PubMed  CAS  Google Scholar 

  50. High, F. A., and Epstein, J. A. (2008) Nat. Rev. Genet., 9, 49–61.

    PubMed  CAS  Google Scholar 

  51. Papayannopoulos, V., Tomlinson, A., Panin, V. M., Rauskolb, C., and Irvine, K. D. (1998) Science, 281, 2031–2034.

    PubMed  CAS  Google Scholar 

  52. Dominguez, M., and de Celis, J. F. (1998) Nature, 396, 276–278.

    PubMed  CAS  Google Scholar 

  53. Cho, K. O., and Choi, K. W. (1998) Nature, 396, 272–276.

    PubMed  CAS  Google Scholar 

  54. Chao, J. L., Tsai, Y. C., Chiu, S. J., and Sun, Y. H. (2004) Development, 131, 3839–3847.

    PubMed  CAS  Google Scholar 

  55. Frankfort, B. J., and Mardon, G. (2002) Development, 129, 1295–1306.

    PubMed  CAS  Google Scholar 

  56. Baonza, A., and Freeman, M. (2001) Development, 128, 3889–3898.

    PubMed  CAS  Google Scholar 

  57. Baker, N. E., and Yu, S. Y. (1997) Curr. Biol., 7, 122–132.

    PubMed  CAS  Google Scholar 

  58. Cagan, R. L., and Ready, D. F. (1989) Genes Dev., 3, 1099–1112.

    PubMed  CAS  Google Scholar 

  59. Sun, Y., Jan, L. Y., and Jan, Y. N. (1998) Development, 125, 3731–3740.

    PubMed  CAS  Google Scholar 

  60. Van Doren, M., Powell, P. A., Pasternak, D., Singson, A., and Posakony, J. W. (1992) Genes Dev., 6, 2592–2605.

    PubMed  Google Scholar 

  61. Cooper, M. T., and Bray, S. J. (2000) Curr. Biol., 10, 1507–1510.

    PubMed  CAS  Google Scholar 

  62. Miller, A. C., Lyons, E. L., and Herman, T. G. (2009) Curr. Biol., 19, 1378–1383.

    PubMed  CAS  Google Scholar 

  63. Rhyu, M. S., Jan, L. Y., and Jan, Y. N. (1994) Cell, 76, 477–491.

    PubMed  CAS  Google Scholar 

  64. Frise, E., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y., and Jan, Y. N. (1996) Proc. Natl. Acad. Sci. USA, 93, 11925–11932.

    PubMed  CAS  Google Scholar 

  65. Le Borgne, R., and Schweisguth, F. (2003) Dev. Cell, 5, 139–148.

    PubMed  Google Scholar 

  66. Fichelson, P., and Gho, M. (2003) Development, 130, 123–133.

    PubMed  CAS  Google Scholar 

  67. Nusslein-Volhard, C., and Wieschaus, E. (1980) Nature, 287, 795–801.

    PubMed  CAS  Google Scholar 

  68. Porter, J. A., Ekker, S. C., Park, W. J., von Kessler, D. P., Young, K. E., Chen, C. H., Ma, Y., Woods, A. S., Cotter, R. J., Koonin, E. V., and Beachy, P. A. (1996) Cell, 86, 21–34.

    PubMed  CAS  Google Scholar 

  69. Porter, J. A., Young, K. E., and Beachy, P. A. (1996) Science, 274, 255–259.

    PubMed  CAS  Google Scholar 

  70. Koonin, E. V. (1995) Trends Biochem. Sci., 20, 141–142.

    PubMed  CAS  Google Scholar 

  71. Chamoun, Z., Mann, R. K., Nellen, D., von Kessler, D. P., Bellotto, M., Beachy, P. A., and Basler, K. (2001) Science, 293, 2080–2084.

    PubMed  CAS  Google Scholar 

  72. Burke, R., Nellen, D., Bellotto, M., Hafen, E., Senti, K. A., Dickson, B. J., and Basler, K. (1999) Cell, 99, 803–815.

    PubMed  CAS  Google Scholar 

  73. Lee, J. J., Ekker, S. C., von Kessler, D. P., Porter, J. A., Sun, B. I., and Beachy, P. A. (1994) Science, 266, 1528–1537.

    PubMed  CAS  Google Scholar 

  74. Lawrence, P. A. (2001) Nat. Cell Biol., 3, E151–154.

    PubMed  CAS  Google Scholar 

  75. Zeng, X., Goetz, J. A., Suber, L. M., Scott, W. J., Jr., Schreiner, C. M., and Robbins, D. J. (2001) Nature, 411, 716–720.

    PubMed  CAS  Google Scholar 

  76. Panakova, D., Sprong, H., Marois, E., Thiele, C., and Eaton, S. (2005) Nature, 435, 58–65.

    PubMed  CAS  Google Scholar 

  77. Katanaev, V. L., Solis, G. P., Hausmann, G., Buestorf, S., Katanayeva, N., Schrock, Y., Stuermer, C. A., and Basler, K. (2008) EMBO J., 27, 509–521.

    PubMed  CAS  Google Scholar 

  78. Rietveld, A., Neutz, S., Simons, K., and Eaton, S. (1999) J. Biol. Chem., 274, 12049–12054.

    PubMed  CAS  Google Scholar 

  79. Ingham, P. W., Taylor, A. M., and Nakano, Y. (1991) Nature, 353, 184–187.

    PubMed  CAS  Google Scholar 

  80. Marigo, V., Davey, R. A., Zuo, Y., Cunningham, J. M., and Tabin, C. J. (1996) Nature, 384, 176–179.

    PubMed  CAS  Google Scholar 

  81. Zheng, X., Mann, R. K., Sever, N., and Beachy, P. A. (2010) Genes Dev., 24, 57–71.

    PubMed  CAS  Google Scholar 

  82. Alcedo, J., Ayzenzon, M., von Ohlen, T., Noll, M., and Hooper, J. E. (1996) Cell, 86, 221–232.

    PubMed  CAS  Google Scholar 

  83. Taipale, J., Cooper, M. K., Maiti, T., and Beachy, P. A. (2002) Nature, 418, 892–897.

    PubMed  CAS  Google Scholar 

  84. Riobo, N. A., Saucy, B., Dilizio, C., and Manning, D. R. (2006) Proc. Natl. Acad. Sci. USA, 103, 12607–12612.

    PubMed  CAS  Google Scholar 

  85. Robbins, D. J., Nybakken, K. E., Kobayashi, R., Sisson, J. C., Bishop, J. M., and Therond, P. P. (1997) Cell, 90, 225–234.

    PubMed  CAS  Google Scholar 

  86. Sisson, J. C., Ho, K. S., Suyama, K., and Scott, M. P. (1997) Cell, 90, 235–245.

    PubMed  CAS  Google Scholar 

  87. Ingham, P. W., Nakano, Y., and Seger, C. (2011) Nat. Rev. Genet., 12, 393–406.

    PubMed  CAS  Google Scholar 

  88. Jia, J., Zhang, L., Zhang, Q., Tong, C., Wang, B., Hou, F., Amanai, K., and Jiang, J. (2005) Dev. Cell, 9, 819–830.

    PubMed  CAS  Google Scholar 

  89. Mullor, J. L., Sanchez, P., and Ruiz i Altaba, A. (2002) Trends Cell Biol., 12, 562–569.

    PubMed  CAS  Google Scholar 

  90. Bale, A. E. (2002) Annu. Rev. Genom. Hum. Genet., 3, 47–65.

    CAS  Google Scholar 

  91. Belloni, E., Muenke, M., Roessler, E., Traverso, G., Siegel-Bartelt, J., Frumkin, A., Mitchell, H. F., Donis-Keller, H., Helms, C., Hing, A. V., Heng, H. H., Koop, B., Martindale, D., Rommens, J. M., Tsui, L. C., and Scherer, S. W. (1996) Nat. Genet., 14, 353–356.

    PubMed  CAS  Google Scholar 

  92. Roessler, E., Belloni, E., Gaudenz, K., Jay, P., Berta, P., Scherer, S. W., Tsui, L. C., and Muenke, M. (1996) Nat. Genet., 14, 357–360.

    PubMed  CAS  Google Scholar 

  93. Ming, J. E., Kaupas, M. E., Roessler, E., Brunner, H. G., Golabi, M., Tekin, M., Stratton, R. F., Sujansky, E., Bale, S. J., and Muenke, M. (2002) Hum. Genet., 110, 297–301.

    PubMed  CAS  Google Scholar 

  94. Binns, W., James, L. F., Shupe, J. L., and Everett, G. (1963) Am. J. Vet. Res., 24, 1164–1175.

    PubMed  CAS  Google Scholar 

  95. Keeler, R. F., and Binns, W. (1968) Teratology, 1, 5–10.

    PubMed  CAS  Google Scholar 

  96. Chen, J. K., Taipale, J., Cooper, M. K., and Beachy, P. A. (2002) Genes Dev., 16, 2743–2748.

    PubMed  CAS  Google Scholar 

  97. Epstein, E. H. (2008) Nat. Rev. Cancer, 8, 743–754.

    PubMed  CAS  Google Scholar 

  98. Xie, J. (2008) Acta Biochim. Biophys. Sin. (Shanghai), 40, 670–680.

    CAS  Google Scholar 

  99. Rubin, L. L., and de Sauvage, F. J. (2006) Nat. Rev. Drug Discov., 5, 1026–1033.

    PubMed  CAS  Google Scholar 

  100. Roignant, J. Y., and Treisman, J. E. (2009) Int. J. Dev. Biol., 53, 795–804.

    PubMed  CAS  Google Scholar 

  101. Heberlein, U., Singh, C. M., Luk, A. Y., and Donohoe, T. J. (1995) Nature, 373, 709–711.

    PubMed  CAS  Google Scholar 

  102. Heberlein, U., Wolff, T., and Rubin, G. M. (1993) Cell, 75, 913–926.

    PubMed  CAS  Google Scholar 

  103. Ma, C., Zhou, Y., Beachy, P. A., and Moses, K. (1993) Cell, 75, 927–938.

    PubMed  CAS  Google Scholar 

  104. Dominguez, M., and Hafen, E. (1997) Genes Dev., 11, 3254–3264.

    PubMed  CAS  Google Scholar 

  105. Ou, C. Y., Lin, Y. F., Chen, Y. J., and Chien, C. T. (2002) Genes Dev., 16, 2403–2414.

    PubMed  CAS  Google Scholar 

  106. Gray, A. M., and Mason, A. J. (1990) Science, 247, 1328–1330.

    PubMed  CAS  Google Scholar 

  107. Massague, J. (2000) Nat. Rev. Mol. Cell Biol., 1, 169–178.

    PubMed  CAS  Google Scholar 

  108. Raftery, L. A., and Sutherland, D. J. (1999) Dev. Biol., 210, 251–268.

    PubMed  CAS  Google Scholar 

  109. Nellen, D., Affolter, M., and Basler, K. (1994) Cell, 78, 225–237.

    PubMed  CAS  Google Scholar 

  110. Brummel, T. J., Twombly, V., Marques, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massague, J., O’Connor, M. B., and Gelbart, W. M. (1994) Cell, 78, 251–261.

    PubMed  CAS  Google Scholar 

  111. Letsou, A., Arora, K., Wrana, J. L., Simin, K., Twombly, V., Jamal, J., Staehling-Hampton, K., Hoffmann, F. M., Gelbart, W. M., Massague, J., et al. (1995) Cell, 80, 899–908.

    PubMed  CAS  Google Scholar 

  112. Ruberte, E., Marty, T., Nellen, D., Affolter, M., and Basler, K. (1995) Cell, 80, 889–897.

    PubMed  CAS  Google Scholar 

  113. Sekelsky, J. J., Newfeld, S. J., Raftery, L. A., Chartoff, E. H., and Gelbart, W. M. (1995) Genetics, 139, 1347–1358.

    PubMed  CAS  Google Scholar 

  114. Hudson, J. B., Podos, S. D., Keith, K., Simpson, S. L., and Ferguson, E. L. (1998) Development, 125, 1407–1420.

    PubMed  CAS  Google Scholar 

  115. Wisotzkey, R. G., Mehra, A., Sutherland, D. J., Dobens, L. L., Liu, X., Dohrmann, C., Attisano, L., and Raftery, L. A. (1998) Development, 125, 1433–1445.

    PubMed  CAS  Google Scholar 

  116. Das, P., Maduzia, L. L., Wang, H., Finelli, A. L., Cho, S. H., Smith, M. M., and Padgett, R. W. (1998) Development, 125, 1519–1528.

    PubMed  CAS  Google Scholar 

  117. Harradine, K. A., and Akhurst, R. J. (2006) Ann. Med., 38, 403–414.

    PubMed  CAS  Google Scholar 

  118. Lebreiro, A., Martins, E., Cruz, C., Almeida, J., Maciel, M. J., Cardoso, J. C., and Lima, C. A. (2010) Rev. Port. Cardiol., 29, 1021–1036.

    PubMed  Google Scholar 

  119. Neptune, E. R., Frischmeyer, P. A., Arking, D. E., Myers, L., Bunton, T. E., Gayraud, B., Ramirez, F., Sakai, L. Y., and Dietz, H. C. (2003) Nat. Genet., 33, 407–411.

    PubMed  CAS  Google Scholar 

  120. Meulmeester, E., and Ten Dijke, P. (2010) J. Pathol., 223, 205–218.

    PubMed  Google Scholar 

  121. Hahn, S. A., Schutte, M., Hoque, A. T., Moskaluk, C. A., da Costa, L. T., Rozenblum, E., Weinstein, C. L., Fischer, A., Yeo, C. J., Hruban, R. H., and Kern, S. E. (1996) Science, 271, 350–353.

    PubMed  CAS  Google Scholar 

  122. Sonis, S. T., van Vugt, A. G., Brien, J. P., Muska, A. D., Bruskin, A. M., Rose, A., and Haley, J. D. (1997) Oral Oncol., 33, 47–54.

    PubMed  CAS  Google Scholar 

  123. Hannon, G. J., and Beach, D. (1994) Nature, 371, 257–261.

    PubMed  CAS  Google Scholar 

  124. Datto, M. B., Li, Y., Panus, J. F., Howe, D. J., Xiong, Y., and Wang, X. F. (1995) Proc. Natl. Acad. Sci. USA, 92, 5545–5549.

    PubMed  CAS  Google Scholar 

  125. Coffey, R. J., Jr., Bascom, C. C., Sipes, N. J., Graves-Deal, R., Weissman, B. E., and Moses, H. L. (1988) Mol. Cell. Biol., 8, 3088–3093.

    PubMed  CAS  Google Scholar 

  126. Oberhammer, F. A., Pavelka, M., Sharma, S., Tiefenbacher, R., Purchio, A. F., Bursch, W., and Schulte-Hermann, R. (1992) Proc. Natl. Acad. Sci. USA, 89, 5408–5412.

    PubMed  CAS  Google Scholar 

  127. Drabsch, Y., and ten Dijke, P. (2011) J. Mammary Gland Biol. Neoplasia, 16, 97–108.

    PubMed  Google Scholar 

  128. Parvani, J. G., Taylor, M. A., and Schiemann, W. P. (2011) J. Mammary Gland Biol. Neoplasia, 16, 127–146.

    PubMed  Google Scholar 

  129. Tabata, T., and Takei, Y. (2004) Development, 131, 703–712.

    PubMed  CAS  Google Scholar 

  130. Bessa, J., Gebelein, B., Pichaud, F., Casares, F., and Mann, R. S. (2002) Genes Dev., 16, 2415–2427.

    PubMed  CAS  Google Scholar 

  131. Greenwood, S., and Struhl, G. (1999) Development, 126, 5795–5808.

    PubMed  CAS  Google Scholar 

  132. Curtiss, J., and Mlodzik, M. (2000) Development, 127, 1325–1336.

    PubMed  CAS  Google Scholar 

  133. Logan, C. Y., and Nusse, R. (2004) Annu. Rev. Cell Dev. Biol., 20, 781–810.

    PubMed  CAS  Google Scholar 

  134. Cabrera, C. V., Alonso, M. C., Johnston, P., Phillips, R. G., and Lawrence, P. A. (1987) Cell, 50, 659–663.

    PubMed  CAS  Google Scholar 

  135. Rijsewijk, F., Schuermann, M., Wagenaar, E., Parren, P., Weigel, D., and Nusse, R. (1987) Cell, 50, 649–657.

    PubMed  CAS  Google Scholar 

  136. Coudreuse, D., and Korswagen, H. C. (2007) Development, 134, 3–12.

    PubMed  CAS  Google Scholar 

  137. Port, F., and Basler, K. (2010) Traffic, 11, 1265–1271.

    PubMed  CAS  Google Scholar 

  138. Tanaka, K., Kitagawa, Y., and Kadowaki, T. (2002) J. Biol. Chem., 277, 12816–12823.

    PubMed  CAS  Google Scholar 

  139. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., 3rd, and Nusse, R. (2003) Nature, 423, 448–452.

    PubMed  CAS  Google Scholar 

  140. Kadowaki, T., Wilder, E., Klingensmith, J., Zachary, K., and Perrimon, N. (1996) Genes Dev., 10, 3116–3128.

    PubMed  CAS  Google Scholar 

  141. Van den Heuvel, M., Harryman-Samos, C., Klingensmith, J., Perrimon, N., and Nusse, R. (1993) EMBO J., 12, 5293–5302.

    PubMed  Google Scholar 

  142. Takada, R., Satomi, Y., Kurata, T., Ueno, N., Norioka, S., Kondoh, H., Takao, T., and Takada, S. (2006) Dev. Cell, 11, 791–801.

    PubMed  CAS  Google Scholar 

  143. Banziger, C., Soldini, D., Schutt, C., Zipperlen, P., Hausmann, G., and Basler, K. (2006) Cell, 125, 509–522.

    PubMed  CAS  Google Scholar 

  144. Bartscherer, K., Pelte, N., Ingelfinger, D., and Boutros, M. (2006) Cell, 125, 523–533.

    PubMed  CAS  Google Scholar 

  145. Goodman, R. M., Thombre, S., Firtina, Z., Gray, D., Betts, D., Roebuck, J., Spana, E. P., and Selva, E. M. (2006) Development, 133, 4901–4911.

    PubMed  CAS  Google Scholar 

  146. Coudreuse, D. Y., Roel, G., Betist, M. C., Destree, O., and Korswagen, H. C. (2006) Science, 312, 921–924.

    PubMed  CAS  Google Scholar 

  147. Franch-Marro, X., Wendler, F., Guidato, S., Griffith, J., Baena-Lopez, A., Itasaki, N., Maurice, M. M., and Vincent, J. P. (2008) Nat. Cell Biol., 10, 170–177.

    PubMed  CAS  Google Scholar 

  148. Port, F., Kuster, M., Herr, P., Furger, E., Banziger, C., Hausmann, G., and Basler, K. (2008) Nat. Cell Biol., 10, 178–185.

    PubMed  CAS  Google Scholar 

  149. Belenkaya, T. Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y. V., Yan, D., Selva, E. M., and Lin, X. (2008) Dev. Cell, 14, 120–131.

    PubMed  CAS  Google Scholar 

  150. Papkoff, J., and Schryver, B. (1990) Mol. Cell. Biol., 10, 2723–2730.

    PubMed  CAS  Google Scholar 

  151. Egger-Adam, D., and Katanaev, V. L. (2008) Front. Biosci., 13, 4740–4755.

    PubMed  CAS  Google Scholar 

  152. Katanaev, V. L. (2010) Biochemistry (Moscow), 75, 1428–1434.

    CAS  Google Scholar 

  153. Koval, A., Purvanov, V., Egger-Adam, D., and Katanaev, V. L. (2011) Biochem. Pharmacol., 82, 1311–1319.

    PubMed  CAS  Google Scholar 

  154. Pierce, K. L., Premont, R. T., and Lefkowitz, R. J. (2002) Nat. Rev. Mol. Cell Biol., 3, 639–650.

    PubMed  CAS  Google Scholar 

  155. Gilman, A. G. (1987) Annu. Rev. Biochem., 56, 615–649.

    PubMed  CAS  Google Scholar 

  156. Katanaev, V. L., Ponzielli, R., Semeriva, M., and Tomlinson, A. (2005) Cell, 120, 111–122.

    PubMed  CAS  Google Scholar 

  157. Koval, A., and Katanaev, V. L. (2011) Biochem. J., 433, 435–440.

    PubMed  CAS  Google Scholar 

  158. Gao, C., and Chen, Y. G. (2010) Cell. Signal., 22, 717–727.

    PubMed  CAS  Google Scholar 

  159. Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Riou, J. F., Boucaut, J. C., and Shi, D. L. (2000) EMBO J., 19, 4944–4954.

    PubMed  CAS  Google Scholar 

  160. Oldham, W. M., and Hamm, H. E. (2007) Adv. Protein Chem., 74, 67–93.

    PubMed  CAS  Google Scholar 

  161. Bikkavilli, R. K., Feigin, M. E., and Malbon, C. C. (2008) J. Cell Sci., 121, 234–245.

    PubMed  CAS  Google Scholar 

  162. Angers, S., Thorpe, C. J., Biechele, T. L., Goldenberg, S. J., Zheng, N., MacCoss, M. J., and Moon, R. T. (2006) Nat. Cell Biol., 8, 348–357.

    PubMed  CAS  Google Scholar 

  163. Egger-Adam, D., and Katanaev, V. L. (2010) Dev. Dyn., 239, 168–183.

    PubMed  CAS  Google Scholar 

  164. Jung, H., Kim, H. J., Lee, S. K., Kim, R., Kopachik, W., Han, J. K., and Jho, E. H. (2009) Exp. Mol. Med., 41, 695–706.

    PubMed  CAS  Google Scholar 

  165. Wedegaertner, P. B., Wilson, P. T., and Bourne, H. R. (1995) J. Biol. Chem., 270, 503–506.

    PubMed  CAS  Google Scholar 

  166. Kimelman, D., and Xu, W. (2006) Oncogene, 25, 7482–7491.

    PubMed  CAS  Google Scholar 

  167. Aberle, H., Bauer, A., Stappert, J., Kispert, A., and Kemler, R. (1997) EMBO J., 16, 3797–3804.

    PubMed  CAS  Google Scholar 

  168. Cortese, M. S., Uversky, V. N., and Dunker, A. K. (2008) Prog. Biophys. Mol. Biol., 98, 85–106.

    PubMed  CAS  Google Scholar 

  169. Noutsou, M., Duarte, A. M., Anvarian, Z., Didenko, T., Minde, D. P., Kuper, I., de Ridder, I., Oikonomou, C., Friedler, A., Boelens, R., Rudiger, S. G., and Maurice, M. M. (2011) J. Mol. Biol., 405, 773–786.

    PubMed  CAS  Google Scholar 

  170. Spink, K. E., Polakis, P., and Weis, W. I. (2000) EMBO J., 19, 2270–2279.

    PubMed  CAS  Google Scholar 

  171. Kishida, S., Yamamoto, H., Hino, S., Ikeda, S., Kishida, M., and Kikuchi, A. (1999) Mol. Cell. Biol., 19, 4414–4422.

    PubMed  CAS  Google Scholar 

  172. Cliffe, A., Hamada, F., and Bienz, M. (2003) Curr. Biol., 13, 960–966.

    PubMed  CAS  Google Scholar 

  173. Mao, J., Wang, J., Liu, B., Pan, W., Farr, G. H., 3rd, Flynn, C., Yuan, H., Takada, S., Kimelman, D., Li, L., and Wu, D. (2001) Mol. Cell, 7, 801–809.

    PubMed  CAS  Google Scholar 

  174. Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P., Glinka, A., and Niehrs, C. (2005) Nature, 438, 867–872.

    PubMed  CAS  Google Scholar 

  175. Zeng, X., Tamai, K., Doble, B., Li, S., Huang, H., Habas, R., Okamura, H., Woodgett, J., and He, X. (2005) Nature, 438, 873–877.

    PubMed  CAS  Google Scholar 

  176. Willert, K., and Jones, K. A. (2006) Genes Dev., 20, 1394–1404.

    PubMed  CAS  Google Scholar 

  177. Seto, E. S., and Bellen, H. J. (2006) J. Cell Biol., 173, 95–106.

    PubMed  CAS  Google Scholar 

  178. Purvanov, V., Koval, A., and Katanaev, V. L. (2010) Sci. Signal., 3, ra65.

    PubMed  Google Scholar 

  179. Moon, R. T., Kohn, A. D., de Ferrari, G. V., and Kaykas, A. (2004) Nat. Rev. Genet., 5, 691–701.

    PubMed  CAS  Google Scholar 

  180. Little, R. D., Carulli, J. P., Del Mastro, R. G., Dupuis, J., Osborne, M., Folz, C., Manning, S. P., Swain, P. M., Zhao, S. C., Eustace, B., Lappe, M. M., Spitzer, L., Zweier, S., Braunschweiger, K., Benchekroun, Y., Hu, X., Adair, R., Chee, L., FitzGerald, M. G., Tulig, C., Caruso, A., Tzellas, N., Bawa, A., Franklin, B., McGuire, S., Nogues, X., Gong, G., Allen, K. M., Anisowicz, A., Morales, A. J., Lomedico, P. T., Recker, S. M., van Eerdewegh, P., Recker, R. R., and Johnson, M. L. (2002) Am. J. Hum. Genet., 70, 11–19.

    PubMed  CAS  Google Scholar 

  181. Boyden, L. M., Mao, J., Belsky, J., Mitzner, L., Farhi, A., Mitnick, M. A., Wu, D., Insogna, K., and Lifton, R. P. (2002) N. Engl. J. Med., 346, 1513–1521.

    PubMed  CAS  Google Scholar 

  182. Gong, Y., Slee, R. B., Fukai, N., Rawadi, G., Roman-Roman, S., Reginato, A. M., Wang, H., Cundy, T., Glorieux, F. H., Lev, D., Zacharin, M., Oexle, K., Marcelino, J., Suwairi, W., Heeger, S., Sabatakos, G., Apte, S., Adkins, W. N., Allgrove, J., Arslan-Kirchner, M., Batch, J. A., Beighton, P., Black, G. C., Boles, R. G., Boon, L. M., Borrone, C., Brunner, H. G., Carle, G. F., Dallapiccola, B., de Paepe, A., Floege, B., Halfhide, M. L., Hall, B., Hennekam, R. C., Hirose, T., Jans, A., Juppner, H., Kim, C. A., Keppler-Noreuil, K., Kohlschuetter, A., LaCombe, D., Lambert, M., Lemyre, E., Letteboer, T., Peltonen, L., Ramesar, R. S., Romanengo, M., Somer, H., Steichen-Gersdorf, E., Steinmann, B., Sullivan, B., Superti-Furga, A., Swoboda, W., van den Boogaard, M. J., van Hul, W., Vikkula, M., Votruba, M., Zabel, B., Garcia, T., Baron, R., Olsen, B. R., and Warman, M. L. (2001) Cell, 107, 513–523.

    PubMed  CAS  Google Scholar 

  183. Robitaille, J., MacDonald, M. L., Kaykas, A., Sheldahl, L. C., Zeisler, J., Dube, M. P., Zhang, L. H., Singaraja, R. R., Guernsey, D. L., Zheng, B., Siebert, L. F., Hoskin-Mott, A., Trese, M. T., Pimstone, S. N., Shastry, B. S., Moon, R. T., Hayden, M. R., Goldberg, Y. P., and Samuels, M. E. (2002) Nat. Genet., 32, 326–330.

    PubMed  CAS  Google Scholar 

  184. Kaykas, A., Yang-Snyder, J., Heroux, M., Shah, K. V., Bouvier, M., and Moon, R. T. (2004) Nat. Cell Biol., 6, 52–58.

    PubMed  CAS  Google Scholar 

  185. Polakis, P. (2007) Curr. Opin. Genet. Dev., 17, 45–51.

    PubMed  CAS  Google Scholar 

  186. Turashvili, G., Bouchal, J., Burkadze, G., and Kolar, Z. (2006) Pathobiology, 73, 213–223.

    PubMed  CAS  Google Scholar 

  187. Giles, R. H., van Es, J. H., and Clevers, H. (2003) Biochim. Biophys. Acta, 1653, 1–24.

    PubMed  CAS  Google Scholar 

  188. Zhao, J., Kim, K. A., and Abo, A. (2009) Trends Biotechnol., 27, 131–136.

    PubMed  CAS  Google Scholar 

  189. Minear, S., Leucht, P., Jiang, J., Liu, B., Zeng, A., Fuerer, C., Nusse, R., and Helms, J. A. (2010) Sci. Transl. Med., 2, 29ra30.

    PubMed  Google Scholar 

  190. Van de Schans, V. A., Smits, J. F., and Blankesteijn, W. M. (2008) Eur. J. Pharmacol., 585, 338–345.

    PubMed  Google Scholar 

  191. Budnik, V., and Salinas, P. C. (2011) Curr. Opin. Neurobiol., 21, 151–159.

    PubMed  CAS  Google Scholar 

  192. De Ferrari, G. V., and Moon, R. T. (2006) Oncogene, 25, 7545–7553.

    PubMed  Google Scholar 

  193. Magdesian, M. H., Carvalho, M. M., Mendes, F. A., Saraiva, L. M., Juliano, M. A., Juliano, L., Garcia-Abreu, J., and Ferreira, S. T. (2008) J. Biol. Chem., 283, 9359–9368.

    PubMed  CAS  Google Scholar 

  194. Alvarez, A. R., Godoy, J. A., Mullendorff, K., Olivares, G. H., Bronfman, M., and Inestrosa, N. C. (2004) Exp. Cell Res., 297, 186–196.

    PubMed  CAS  Google Scholar 

  195. Cerpa, W., Toledo, E. M., Varela-Nallar, L., and Inestrosa, N. C. (2009) Drug News Perspect., 22, 579–591.

    PubMed  CAS  Google Scholar 

  196. Angers, S., and Moon, R. T. (2009) Nat. Rev. Mol. Cell Biol., 10, 468–477.

    PubMed  CAS  Google Scholar 

  197. Barker, N., and Clevers, H. (2006) Nat. Rev. Drug Discov., 5, 997–1014.

    PubMed  CAS  Google Scholar 

  198. Legent, K., and Treisman, J. E. (2008) Methods Mol. Biol., 469, 141–161.

    PubMed  CAS  Google Scholar 

  199. Cho, K. O., Chern, J., Izaddoost, S., and Choi, K. W. (2000) Cell, 103, 331–342.

    PubMed  CAS  Google Scholar 

  200. Heberlein, U., Borod, E. R., and Chanut, F. A. (1998) Development, 125, 567–577.

    PubMed  CAS  Google Scholar 

  201. Royet, J., and Finkelstein, R. (1997) Development, 124, 4793–4800.

    PubMed  CAS  Google Scholar 

  202. Baker, N. E. (1988) Development, 102, 489–497.

    PubMed  CAS  Google Scholar 

  203. Royet, J., and Finkelstein, R. (1996) Development, 122, 1849–1858.

    PubMed  CAS  Google Scholar 

  204. Baonza, A., and Freeman, M. (2002) Development, 129, 5313–5322.

    PubMed  CAS  Google Scholar 

  205. Treier, M., Bohmann, D., and Mlodzik, M. (1995) Cell, 83, 753–760.

    PubMed  CAS  Google Scholar 

  206. Treisman, J. E., and Rubin, G. M. (1995) Development, 121, 3519–3527.

    PubMed  CAS  Google Scholar 

  207. Fortini, M. E., and Rubin, G. M. (1991) Cell Tissue Res., 265, 185–191.

    PubMed  CAS  Google Scholar 

  208. Wernet, M. F., Labhart, T., Baumann, F., Mazzoni, E. O., Pichaud, F., and Desplan, C. (2003) Cell, 115, 267–279.

    PubMed  CAS  Google Scholar 

  209. Lin, H. V., Rogulja, A., and Cadigan, K. M. (2004) Development, 131, 2409–2418.

    PubMed  CAS  Google Scholar 

  210. Cordero, J., Jassim, O., Bao, S., and Cagan, R. (2004) Mech. Dev., 121, 1523–1530.

    PubMed  CAS  Google Scholar 

  211. Lim, H. Y., and Tomlinson, A. (2006) Development, 133, 3529–3537.

    PubMed  CAS  Google Scholar 

  212. Brunner, E., Brunner, D., Fu, W., Hafen, E., and Basler, K. (1999) Dev. Biol., 206, 178–188.

    PubMed  CAS  Google Scholar 

  213. Tomlinson, A., Strapps, W. R., and Heemskerk, J. (1997) Development, 124, 4515–4521.

    PubMed  CAS  Google Scholar 

  214. Wehrli, M., and Tomlinson, A. (1998) Development, 125, 1421–1432.

    PubMed  CAS  Google Scholar 

  215. Tomlinson, A., and Struhl, G. (1999) Development, 126, 5725–5738.

    PubMed  CAS  Google Scholar 

  216. Veeman, M. T., Axelrod, J. D., and Moon, R. T. (2003) Dev. Cell, 5, 367–377.

    PubMed  CAS  Google Scholar 

  217. Simons, M., and Mlodzik, M. (2008) Annu. Rev. Genet., 42, 517–540.

    PubMed  CAS  Google Scholar 

  218. Katanaev, V. L., and Tomlinson, A. (2006) Cell Cycle, 5, 2464–2472.

    PubMed  CAS  Google Scholar 

  219. Katanaev, V. L. (2001) Biochemistry (Moscow), 66, 351–368.

    CAS  Google Scholar 

  220. Vinson, C. R., Conover, S., and Adler, P. N. (1989) Nature, 338, 263–264.

    PubMed  CAS  Google Scholar 

  221. Moon, R. T., Campbell, R. M., Christian, J. L., McGrew, L. L., Shih, J., and Fraser, S. (1993) Development, 119, 97–111.

    PubMed  CAS  Google Scholar 

  222. Heisenberg, C. P., Tada, M., Rauch, G. J., Saude, L., Concha, M. L., Geisler, R., Stemple, D. L., Smith, J. C., and Wilson, S. W. (2000) Nature, 405, 76–81.

    PubMed  CAS  Google Scholar 

  223. Struhl, G., Barbash, D. A., and Lawrence, P. A. (1997) Development, 124, 2155–2165.

    PubMed  CAS  Google Scholar 

  224. Lawrence, P. A., Casal, J., and Struhl, G. (2002) Development, 129, 2749–2760.

    PubMed  CAS  Google Scholar 

  225. Yang, C. H., Axelrod, J. D., and Simon, M. A. (2002) Cell, 108, 675–688.

    PubMed  CAS  Google Scholar 

  226. Ma, D., Yang, C. H., McNeill, H., Simon, M. A., and Axelrod, J. D. (2003) Nature, 421, 543–547.

    PubMed  CAS  Google Scholar 

  227. Casal, J., Lawrence, P. A., and Struhl, G. (2006) Development, 133, 4561–4572.

    PubMed  CAS  Google Scholar 

  228. Strutt, D. I. (2001) Mol. Cell, 7, 367–375.

    PubMed  CAS  Google Scholar 

  229. Le Garrec, J. F., Lopez, P., and Kerszberg, M. (2006) Dev. Dyn., 235, 235–246.

    PubMed  Google Scholar 

  230. Krasnow, R. E., Wong, L. L., and Adler, P. N. (1995) Development, 121, 4095–4102.

    PubMed  CAS  Google Scholar 

  231. Gubb, D., and Garcia-Bellido, A. (1982) J. Embryol. Exp. Morphol., 68, 37–57.

    PubMed  CAS  Google Scholar 

  232. Wolff, T., and Rubin, G. M. (1998) Development, 125, 1149–1159.

    PubMed  CAS  Google Scholar 

  233. Taylor, J., Abramova, N., Charlton, J., and Adler, P. N. (1998) Genetics, 150, 199–210.

    PubMed  CAS  Google Scholar 

  234. Feiguin, F., Hannus, M., Mlodzik, M., and Eaton, S. (2001) Dev. Cell, 1, 93–101.

    PubMed  CAS  Google Scholar 

  235. Lu, B., Usui, T., Uemura, T., Jan, L., and Jan, Y. N. (1999) Curr. Biol., 9, 1247–1250.

    PubMed  CAS  Google Scholar 

  236. Shimada, Y., Yonemura, S., Ohkura, H., Strutt, D., and Uemura, T. (2006) Dev. Cell, 10, 209–222.

    PubMed  CAS  Google Scholar 

  237. Nielsen, E., Severin, F., Backer, J. M., Hyman, A. A., and Zerial, M. (1999) Nat. Cell Biol., 1, 376–382.

    PubMed  CAS  Google Scholar 

  238. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D., and Luo, L. (2001) Cell, 105, 81–91.

    PubMed  CAS  Google Scholar 

  239. Copp, A. J., and Greene, N. D. (2010) J. Pathol., 220, 217–230.

    PubMed  CAS  Google Scholar 

  240. Kibar, Z., Torban, E., McDearmid, J. R., Reynolds, A., Berghout, J., Mathieu, M., Kirillova, I., de Marco, P., Merello, E., Hayes, J. M., Wallingford, J. B., Drapeau, P., Capra, V., and Gros, P. (2007) N. Engl. J. Med., 356, 1432–1437.

    PubMed  CAS  Google Scholar 

  241. Wang, Y. (2009) Mol. Cancer Ther., 8, 2103–2109.

    PubMed  CAS  Google Scholar 

  242. Weeraratna, A. T., Jiang, Y., Hostetter, G., Rosenblatt, K., Duray, P., Bittner, M., and Trent, J. M. (2002) Cancer Cell, 1, 279–288.

    PubMed  CAS  Google Scholar 

  243. Kurayoshi, M., Oue, N., Yamamoto, H., Kishida, M., Inoue, A., Asahara, T., Yasui, W., and Kikuchi, A. (2006) Cancer Res., 66, 10439–10448.

    PubMed  CAS  Google Scholar 

  244. Axelrod, J. D., Matsuno, K., Artavanis-Tsakonas, S., and Perrimon, N. (1996) Science, 271, 1826–1832.

    PubMed  CAS  Google Scholar 

  245. Munoz-Descalzo, S., Sanders, P. G., Montagne, C., Johnson, R. I., Balayo, T., and Arias, A. M. (2010) Fly (Austin), 4, 182–193.

    CAS  Google Scholar 

  246. Strutt, D., Johnson, R., Cooper, K., and Bray, S. (2002) Curr. Biol., 12, 813–824.

    PubMed  CAS  Google Scholar 

  247. Das, G., Reynolds-Kenneally, J., and Mlodzik, M. (2002) Dev. Cell, 2, 655–666.

    PubMed  CAS  Google Scholar 

  248. Fanto, M., and Mlodzik, M. (1999) Nature, 397, 523–526.

    PubMed  CAS  Google Scholar 

  249. Cooper, M. T., and Bray, S. J. (1999) Nature, 397, 526–530.

    PubMed  CAS  Google Scholar 

  250. Robinson, D. R., Wu, Y. M., and Lin, S. F. (2000) Oncogene, 19, 5548–5557.

    PubMed  CAS  Google Scholar 

  251. Ullrich, A., Coussens, L., Hayflick, J. S., Dull, T. J., Gray, A., Tam, A. W., Lee, J., Yarden, Y., Libermann, T. A., Schlessinger, J., et al. (1984) Nature, 309, 418–425.

    PubMed  CAS  Google Scholar 

  252. Hafen, E., Basler, K., Edstroem, J. E., and Rubin, G. M. (1987) Science, 236, 55–63.

    PubMed  CAS  Google Scholar 

  253. Benzer, S. (1967) Proc. Natl. Acad. Sci. USA, 58, 1112–1119.

    PubMed  CAS  Google Scholar 

  254. Harris, W. A., Stark, W. S., and Walker, J. A. (1976) J. Physiol., 256, 415–439.

    PubMed  CAS  Google Scholar 

  255. Tomlinson, A., and Ready, D. F. (1986) Science, 231, 400–402.

    PubMed  CAS  Google Scholar 

  256. Reinke, R., and Zipursky, S. L. (1988) Cell, 55, 321–330.

    PubMed  CAS  Google Scholar 

  257. Basler, K., and Hafen, E. (1988) Cell, 54, 299–311.

    PubMed  CAS  Google Scholar 

  258. Simon, M. A., Bowtell, D. D., and Rubin, G. M. (1989) Proc. Natl. Acad. Sci. USA, 86, 8333–8337.

    PubMed  CAS  Google Scholar 

  259. Rogge, R. D., Karlovich, C. A., and Banerjee, U. (1991) Cell, 64, 39–48.

    PubMed  CAS  Google Scholar 

  260. Simon, M. A., Bowtell, D. D., Dodson, G. S., Laverty, T. R., and Rubin, G. M. (1991) Cell, 67, 701–716.

    PubMed  CAS  Google Scholar 

  261. Bonfini, L., Karlovich, C. A., Dasgupta, C., and Banerjee, U. (1992) Science, 255, 603–606.

    PubMed  CAS  Google Scholar 

  262. Fortini, M. E., Simon, M. A., and Rubin, G. M. (1992) Nature, 355, 559–561.

    PubMed  CAS  Google Scholar 

  263. Simon, M. A., Dodson, G. S., and Rubin, G. M. (1993) Cell, 73, 169–177.

    PubMed  CAS  Google Scholar 

  264. Olivier, J. P., Raabe, T., Henkemeyer, M., Dickson, B., Mbamalu, G., Margolis, B., Schlessinger, J., Hafen, E., and Pawson, T. (1993) Cell, 73, 179–191.

    PubMed  CAS  Google Scholar 

  265. Gaul, U., Mardon, G., and Rubin, G. M. (1992) Cell, 68, 1007–1019.

    PubMed  CAS  Google Scholar 

  266. Dickson, B., Sprenger, F., Morrison, D., and Hafen, E. (1992) Nature, 60, 600–603.

    Google Scholar 

  267. Lu, X., Melnick, M. B., Hsu, J. C., and Perrimon, N. (1994) EMBO J., 13, 2592–2599.

    PubMed  CAS  Google Scholar 

  268. Brunner, D., Oellers, N., Szabad, J., Biggs, W. H., 3rd, Zipursky, S. L., and Hafen, E. (1994) Cell, 76, 875–888.

    PubMed  CAS  Google Scholar 

  269. Bohmann, D., Ellis, M. C., Staszewski, L. M., and Mlodzik, M. (1994) Cell, 78, 973–986.

    PubMed  CAS  Google Scholar 

  270. Brunner, D., Ducker, K., Oellers, N., Hafen, E., Scholz, H., and Klambt, C. (1994) Nature, 370, 386–389.

    PubMed  CAS  Google Scholar 

  271. Kauffmann, R. C., Li, S., Gallagher, P. A., Zhang, J., and Carthew, R. W. (1996) Genes Dev., 10, 2167–2178.

    PubMed  CAS  Google Scholar 

  272. Raabe, T. (2000) Biochim. Biophys. Acta, 1496, 151–163.

    PubMed  CAS  Google Scholar 

  273. Blume-Jensen, P., and Hunter, T. (2001) Nature, 411, 355–365.

    PubMed  CAS  Google Scholar 

  274. Gschwind, A., Fischer, O. M., and Ullrich, A. (2004) Nat. Rev. Cancer, 4, 361–370.

    PubMed  CAS  Google Scholar 

  275. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A., and McGuire, W. L. (1987) Science, 235, 177–182.

    PubMed  CAS  Google Scholar 

  276. Humphrey, P. A., Wong, A. J., Vogelstein, B., Zalutsky, M. R., Fuller, G. N., Archer, G. E., Friedman, H. S., Kwatra, M. M., Bigner, S. H., and Bigner, D. D. (1990) Proc. Natl. Acad. Sci. USA, 87, 4207–4211.

    PubMed  CAS  Google Scholar 

  277. Noble, M. E., Endicott, J. A., and Johnson, L. N. (2004) Science, 303, 1800–1805.

    PubMed  CAS  Google Scholar 

  278. Capdeville, R., Buchdunger, E., Zimmermann, J., and Matter, A. (2002) Nat. Rev. Drug Discov., 1, 493–502.

    PubMed  CAS  Google Scholar 

  279. Reck, M., and Gatzemeier, U. (2005) Respir. Med., 99, 298–307.

    PubMed  Google Scholar 

  280. Bukowski, R. M., Yasothan, U., and Kirkpatrick, P. (2010) Nat. Rev. Drug Discov., 9, 17–18.

    PubMed  CAS  Google Scholar 

  281. Moy, B., Kirkpatrick, P., Kar, S., and Goss, P. (2007) Nat. Rev. Drug Discov., 6, 431–432.

    PubMed  CAS  Google Scholar 

  282. Freeman, M. (1996) Cell, 87, 651–660.

    PubMed  CAS  Google Scholar 

  283. Dominguez, M., Wasserman, J. D., and Freeman, M. (1998) Curr. Biol., 8, 1039–1048.

    PubMed  CAS  Google Scholar 

  284. Schweitzer, R., Howes, R., Smith, R., Shilo, B. Z., and Freeman, M. (1995) Nature, 376, 699–702.

    PubMed  CAS  Google Scholar 

  285. Golembo, M., Schweitzer, R., Freeman, M., and Shilo, B. Z. (1996) Development, 122, 223–230.

    PubMed  CAS  Google Scholar 

  286. Freeman, M. (1994) Mech. Dev., 48, 25–33.

    PubMed  CAS  Google Scholar 

  287. Miller, D. T., and Cagan, R. L. (1998) Development, 125, 2327–2335.

    PubMed  CAS  Google Scholar 

  288. Golic, K. G., and Lindquist, S. (1989) Cell, 59, 499–509.

    PubMed  CAS  Google Scholar 

  289. Xu, T., and Rubin, G. M. (1993) Development, 117, 1223–1237.

    PubMed  CAS  Google Scholar 

  290. Wehrli, M., Dougan, S. T., Caldwell, K., O’Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A., and DiNardo, S. (2000) Nature, 407, 527–530.

    PubMed  CAS  Google Scholar 

  291. Newsome, T. P., Asling, B., and Dickson, B. J. (2000) Development, 127, 851–860.

    PubMed  CAS  Google Scholar 

  292. Rubin, G. M., and Spradling, A. C. (1982) Science, 218, 348–353.

    PubMed  CAS  Google Scholar 

  293. Groth, A. C., Fish, M., Nusse, R., and Calos, M. P. (2004) Genetics, 166, 1775–1782.

    PubMed  CAS  Google Scholar 

  294. Bischof, J., Maeda, R. K., Hediger, M., Karch, F., and Basler, K. (2007) Proc. Natl. Acad. Sci. USA, 104, 3312–3317.

    PubMed  CAS  Google Scholar 

  295. Oberstein, A., Pare, A., Kaplan, L., and Small, S. (2005) Nat. Methods, 2, 583–585.

    PubMed  CAS  Google Scholar 

  296. Horn, C., and Handler, A. M. (2005) Proc. Natl. Acad. Sci. USA, 102, 12483–12488.

    PubMed  CAS  Google Scholar 

  297. Brand, A. H., and Perrimon, N. (1993) Development, 118, 401–415.

    PubMed  CAS  Google Scholar 

  298. Bonini, N. M., Bui, Q. T., Gray-Board, G. L., and Warrick, J. M. (1997) Development, 124, 4819–4826.

    PubMed  CAS  Google Scholar 

  299. Basler, K., Yen, D., Tomlinson, A., and Hafen, E. (1990) Genes Dev., 4, 728–739.

    PubMed  CAS  Google Scholar 

  300. Crew, J. R., Batterham, P., and Pollock, J. A. (1997) Dev. Genes Evol., 206, 481–493.

    Google Scholar 

  301. Wang, T., Jiao, Y., and Montell, C. (2007) J. Cell Biol., 177, 305–316.

    PubMed  CAS  Google Scholar 

  302. Yoshihara, Y., Mizuno, T., Nakahira, M., Kawasaki, M., Watanabe, Y., Kagamiyama, H., Jishage, K. I., Ueda, O., Suzuki, H., Tabuchi, K., Sawamoto, K., Okano, H., Noda, T., and Mori, K. (1999) Neuron, 22, 33–41.

    PubMed  CAS  Google Scholar 

  303. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007) Nature, 448, 151–156.

    PubMed  CAS  Google Scholar 

  304. Roberson, E. D., and Mucke, L. (2006) Science, 314, 781–784.

    PubMed  Google Scholar 

  305. Greeve, I., Kretzschmar, D., Tschape, J. A., Beyn, A., Brellinger, C., Schweizer, M., Nitsch, R. M., and Reifegerste, R. (2004) J. Neurosci., 24, 3899–3906.

    PubMed  CAS  Google Scholar 

  306. Finelli, A., Kelkar, A., Song, H. J., Yang, H., and Konsolaki, M. (2004) Mol. Cell. Neurosci., 26, 365–375.

    PubMed  CAS  Google Scholar 

  307. Crowther, D. C., Kinghorn, K. J., Miranda, E., Page, R., Curry, J. A., Duthie, F. A., Gubb, D. C., and Lomas, D. A. (2005) Neuroscience, 132, 123–135.

    PubMed  CAS  Google Scholar 

  308. Dawson, T. M., and Dawson, V. L. (2003) Science, 302, 819–822.

    PubMed  CAS  Google Scholar 

  309. Feany, M. B., and Bender, W. W. (2000) Nature, 404, 394–398.

    PubMed  CAS  Google Scholar 

  310. Takahashi, M., Kanuka, H., Fujiwara, H., Koyama, A., Hasegawa, M., Miura, M., and Iwatsubo, T. (2003) Neurosci. Lett., 336, 155–158.

    PubMed  CAS  Google Scholar 

  311. Chen, L., and Feany, M. B. (2005) Nat. Neurosci., 8, 657–663.

    PubMed  CAS  Google Scholar 

  312. Bates, G. P. (2005) Nat. Rev. Genet., 6, 766–773.

    PubMed  CAS  Google Scholar 

  313. Jackson, G. R., Salecker, I., Dong, X., Yao, X., Arnheim, N., Faber, P. W., MacDonald, M. E., and Zipursky, S. L. (1998) Neuron, 21, 633–642.

    PubMed  CAS  Google Scholar 

  314. Kazemi-Esfarjani, P., and Benzer, S. (2000) Science, 287, 1837–1840.

    PubMed  CAS  Google Scholar 

  315. Warrick, J. M., Chan, H. Y., Gray-Board, G. L., Chai, Y., Paulson, H. L., and Bonini, N. M. (1999) Nat. Genet., 23, 425–428.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. L. Katanaev.

Additional information

Published in Russian in Uspekhi Biologicheskoi Khimii, 2011, Vol. 51, pp. 401–458.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katanaev, V.L., Kryuchkov, M.V. The eye of Drosophila as a model system for studying intracellular signaling in ontogenesis and pathogenesis. Biochemistry Moscow 76, 1556–1581 (2011). https://doi.org/10.1134/S0006297911130116

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297911130116

Key words

Navigation