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Eph family receptors as therapeutic targets

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Abstract

Anti-angiogenic therapy is currently a commonly accepted and rapidly developing approach in oncology and other pathologies linked to aberrant neovascularization. Discovery and validation of additional molecular targets in angiogenesis is needed due to the limitations of the existing clinical therapeutics inhibiting activity of vascular endothelial growth factor (VEGF) and its receptors. A brief review of normal and pathological biological functions of the Eph family of receptor tyrosine kinases and their ephrin ligands is presented, and the approaches to developing therapeutics with anti- and pro-angiogenic and anti-tumor activity based on selective molecular modulation of Eph-ephrin signaling pairs are discussed. Functional roles of Eph-kinases and ephrins in such mechanisms of carcinogenesis as cell proliferation and invasion are also addressed.

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Abbreviations

EC:

vascular endothelial cells

EFN:

ephrin

EGFR:

epidermal growth factor receptor

Fc:

constant region of IgG immunoglobulins

FGF:

fibroblast growth factor

FGFR:

FGF receptor

PI3-kinase:

phosphatidylinositol-3-kinase

siRNA:

small interfering mRNA

VEGF:

vascular endothelial growth factor

VEGFR:

VEGF receptor

References

  1. Gale, N.W., Holland, S.J., Valenzuela, D.M., Flenniken, A., Pan, L., Ryan, T.E., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D.G., et al., Neuron, 1996, vol. 17, pp. 9–19.

    Article  PubMed  CAS  Google Scholar 

  2. Kullander, K. and Klein, R., Nat. Rev. Mol. Cell. Biol., 2002, vol. 3, pp. 475–486.

    Article  PubMed  CAS  Google Scholar 

  3. Pasquale, E.B., Nat. Rev. Cancer, 2010, vol. 10, pp. 165–180.

    Article  PubMed  CAS  Google Scholar 

  4. Aasheim, H.C., Patzke, S., Hjorthaug, H.S., and Finne, E.F., Biochim. Biophys. Acta, 2005, vol. 1723, pp. 1–7.

    Article  PubMed  CAS  Google Scholar 

  5. Blits-Huizinga, C.T., Nelersa, C.M., Malhotra, A., and Liebl, D.J., IUBMB Life, 2004, vol. 56, pp. 257–265.

    Article  PubMed  CAS  Google Scholar 

  6. Chrencik, J.E., Brooun, A., Kraus, M.L., Recht, M.I., Kolatkar, A.R., Han, G.W., Seifert, J.M., Widmer, H., Auer, M., and Kuhn, P., J. Biol. Chem., 2006, vol. 281, pp. 28185–28192.

    Article  PubMed  CAS  Google Scholar 

  7. Himanen, J.P., Chumley, M.J., Lackmann, M., Li, C., Barton, W.A., Jeffrey, P.D., Vearing, C., Geleick, D., Feldheim, D.A., Boyd, A.W., et al., Nat. Neurosci., 2004, vol. 7, pp. 501–509.

    Article  PubMed  CAS  Google Scholar 

  8. Alford, S.C., Bazowski, J., Lorimer, H., Elowe, S., and Howard, P.L., Exp. Cell. Res., 2007, vol. 313, pp. 4170–4179.

    Article  PubMed  CAS  Google Scholar 

  9. Egea, J. and Klein, R., Trends Cell. Biol., 2007, vol. 17, pp. 230–238.

    Article  PubMed  CAS  Google Scholar 

  10. Himanen, J.P., Yermekbayeva, L., Janes, P.W., Walker, J.R., Xu, K., Atapattu, L., Rajashankar, K.R., Mensinga, A., Lackmann, M., Nikolov, D.B., and Dhe-Paganon, S., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 10860–10865.

    Article  PubMed  CAS  Google Scholar 

  11. Seiradake, E., Harlos, K., Sutton, G., Aricescu, A.R., and Jones, E.Y., Nat. Struct. Mol. Biol., 2010, vol. 17, pp. 398–402.

    Article  PubMed  CAS  Google Scholar 

  12. Freywald, A., Sharfe, N., and Roifman, C.M., J. Biol. Chem., 2002, vol. 277, pp. 3823–3828.

    Article  PubMed  CAS  Google Scholar 

  13. Arvanitis, D. and Davy, A., Genes Dev., 2008, vol. 22, pp. 416–429.

    Article  PubMed  CAS  Google Scholar 

  14. Pasquale, E.B., Cell, 2008, vol. 133, pp. 38–52.

    Article  PubMed  CAS  Google Scholar 

  15. Miao, H. and Wang B., Int. J. Biochem. Cell. Biol., 2009, vol. 41, pp. 762–770.

    Article  PubMed  CAS  Google Scholar 

  16. Klein, R., Nat. Neurosci., 2009, vol. 12, pp. 15–20.

    Article  PubMed  CAS  Google Scholar 

  17. Himanen, J.P., Henkemeyer, M., and Nikolov, D.B., Nature, 1998, vol. 396, pp. 486–491.

    Article  PubMed  CAS  Google Scholar 

  18. Thanos, C.D., Goodwill, K.E., and Bowie, J.U., Science, 1999, vol. 283, pp. 833–836.

    Article  PubMed  CAS  Google Scholar 

  19. Stapleton, D., Balan, I., Pawson, T., and Sicheri, F., Nat. Struct. Biol., 1999, vol. 6, pp. 44–49.

    Article  PubMed  CAS  Google Scholar 

  20. Himanen, J.P., Rajashankar, K.R., Lackmann, M., Cowan, C.A., Henkemeyer, M., and Nikolov, D.B., Nature, 2001, vol. 414, pp. 933–938.

    Article  PubMed  CAS  Google Scholar 

  21. Qin, H., Shi, J., Noberini, R., Pasquale, E.B., and Song, J., J. Biol. Chem., 2008, vol. 283, pp. 29473–29484.

    Article  PubMed  CAS  Google Scholar 

  22. Qin, H., Noberini, R., Huan, X., Shi, J., Pasquale, E.B., and Song, J., J. Biol. Chem., 2010, vol. 285, pp. 644–665.

    Article  PubMed  CAS  Google Scholar 

  23. Bocharov, E.V., Mayzel, M.L., Volynsky, P.E., Mineev, K.S., Tkach, E.N., Ermolyuk, Y.S., Schulga, A.A., Efremov, R.G., and Arseniev, A.S., Biophys. J., 2010, vol. 98, pp. 881–889.

    Article  PubMed  CAS  Google Scholar 

  24. Bocharov, E.V., Mayzel, M.L., Volynsky, P.E., Goncharuk, M.V., Ermolyuk, Y.S., Schulga, A.A., Artemenko, E.O., Efremov, R.G., and Arseniev, A.S., J. Biol. Chem., 2008, vol. 283, pp. 29385–29395.

    Article  PubMed  CAS  Google Scholar 

  25. Chrencik, J.E., Brooun, A., Recht, M.I., Nicola, G., Davis, L.K., Abagyan, R., Widmer, H., Pasquale, E.B., and Kuhn, P., J. Biol. Chem., 2007, vol. 282, pp. 36505–36513.

    Article  PubMed  CAS  Google Scholar 

  26. Oganesyan, V., Damschroder, M.M., Phipps, S., Wilson, S.D., Cook, K.E., Wu, H., and Dall’Acqua, W.F., Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2010, vol. 66, pp. 730–733.

    Article  PubMed  CAS  Google Scholar 

  27. Bowden, T.A., Aricescu, A.R., Gilbert, R.J., Grimes, J.M., Jones, E.Y., and Stuart, D.I., Nat. Struct. Mol. Biol., 2008, vol. 15, pp. 567–572.

    Article  PubMed  CAS  Google Scholar 

  28. Choi, Y., Syeda, F., Walker, J.R., Finerty, P.J., Jr., Cuerrier, D., Wojciechowski, A., Liu, Q., Dhe-Paganon, S., and Gray, N.S., Bioorg. Med. Chem. Lett., 2009, vol. 19, pp. 4467–4470.

    Article  PubMed  CAS  Google Scholar 

  29. Flanagan, J.G. and Vanderhaeghen, P., Annu. Rev. Neurosci., 1998, vol. 21, pp. 309–345.

    Article  PubMed  CAS  Google Scholar 

  30. Wang, H.U., Chen, Z.F., and Anderson, D.J., Cell, 1998, vol. 93, pp. 741–753.

    Article  PubMed  CAS  Google Scholar 

  31. Gerety, S.S., Wang H.U., Chen Z.F., and Anderson D.J., Mol. Cell, 1999, vol. 4, pp. 403–414.

    Article  PubMed  CAS  Google Scholar 

  32. Kuijper, S., Turner, C.J., and Adams, R.H., Trends Cardiovasc. Med., 2007, vol. 17, pp. 145–151.

    Article  PubMed  CAS  Google Scholar 

  33. Brantley-Sieders, D.M. and Chen, J., Angiogenesis, 2004, vol. 7, pp. 17–28.

    Article  PubMed  CAS  Google Scholar 

  34. Mosch, B., Reissenweber, B., Neuber, C., and Pietzsch, J., J. Oncol., 2010, vol. 2010, p. 135285.

  35. Carmeliet, P. and Tessier-Lavigne, M., Nature, 2005, vol. 436, pp. 193–200.

    Article  PubMed  CAS  Google Scholar 

  36. Melani, M. and Weinstein, B.M., Annu. Rev. Cell. Dev. Biol., 2010, vol. 26, pp. 639–665.

    Article  PubMed  CAS  Google Scholar 

  37. Merlos-Suarez, A. and Batlle, E., Curr. Opin. Cell. Biol., 2008, vol. 20, pp. 194–200.

    Article  PubMed  CAS  Google Scholar 

  38. Matsuo, K., Adv. Exp. Med. Biol., 2010, vol. 658, pp. 95–103.

    Article  PubMed  CAS  Google Scholar 

  39. Pasquale, E.B., Nat. Rev. Mol. Cell Biol., 2005, vol. 6, pp. 462–475.

    Article  PubMed  CAS  Google Scholar 

  40. McCarron, J.K., Stringer, B.W., Day, B.W., and Boyd, A.W., Future Oncol., 2010, vol. 6, pp. 165–176.

    Article  PubMed  CAS  Google Scholar 

  41. Janes, P.W., Adikari, S., and Lackmann M., Curr. Cancer Drug Targets, 2008, vol. 8, pp. 473–479.

    Article  PubMed  CAS  Google Scholar 

  42. Campbell, T.N. and Robbins, S.M., Curr. Issues Mol. Biol., 2008, vol. 10, pp. 61–66.

    PubMed  CAS  Google Scholar 

  43. Wimmer-Kleikamp, S.H. and Lackmann, M., IUBMB Life, 2005, vol. 57, pp. 421–431.

    Article  PubMed  CAS  Google Scholar 

  44. Surawska, H., Ma, P.C., and Salgia, R., Cytokine Growth Factor Rev., 2004, vol. 15, pp. 419–433.

    Article  PubMed  CAS  Google Scholar 

  45. Foubert, P., Silvestre, J.S., Souttou, B., Barateau, V., Martin, C., Ebrahimian, T.G., Lere-Dean, C., Contreres, J.O., Sulpice, E., Levy, B.I., et al., J. Clin. Invest., 2007, vol. 117, pp. 1527–1537.

    Article  PubMed  CAS  Google Scholar 

  46. Moon, J.J., Lee, S.H., and West, J.L., Biomacromolecules, 2007, vol. 8, pp. 42–49.

    Article  PubMed  CAS  Google Scholar 

  47. Zisch, A.H., Zeisberger, S.M., Ehrbar, M., Djonov, V., Weber, C.C., Ziemiecki, A., Pasquale, E.B., and Hubbell, J.A., Biomaterials, 2004, vol. 25, pp. 3245–3257.

    Article  PubMed  CAS  Google Scholar 

  48. Negrete, O.A., Levroney, E.L., Aguilar, H.C., Bertolotti-Ciarlet, A., Nazarian, R., Tajyar, S., and Lee, B., Nature, 2005, vol. 436, pp. 401–405.

    PubMed  CAS  Google Scholar 

  49. Xu, K., Rajashankar, K.R., Chan, Y.P., Himanen, J.P., Broder, C.C., and Nikolov, D.B., Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 9953–9958.

    Article  PubMed  CAS  Google Scholar 

  50. Fabes, J., Anderson, P., Brennan, C., and Bolsover, S., Eur. J. Neurosci., 2007, vol. 26, pp. 2496–2505.

    Article  PubMed  Google Scholar 

  51. Zhao, J., Yuan, G., Cendan, C.M., Nassar, M.A., Lagerstrom, M.C., Kullander, K., Gavazzi, I., and Wood, J.N., Mol. Pain, 2010, vol. 6, p. 77.

    Article  PubMed  CAS  Google Scholar 

  52. Cercone, M.A., Schroeder, W., Schomberg, S., and Carpenter, T.C., Am. J. Physiol. Lung Cell Mol. Physiol., 2009, vol. 297, pp. L856–L863.

    Article  PubMed  CAS  Google Scholar 

  53. Edwards, C.M. and Mundy, G.R., Int. J. Med. Sci., 2008, vol. 5, pp. 263–272.

    Article  PubMed  CAS  Google Scholar 

  54. Folkman, J., N. Engl. J. Med., 1971, vol. 285, pp. 1182–1186.

    Article  PubMed  CAS  Google Scholar 

  55. Jaffe, E.A., Hum. Pathol., 1987, vol. 18, pp. 234–239.

    Article  PubMed  CAS  Google Scholar 

  56. Seaman, S., Stevens, J., Yang, M.Y., Logsdon, D., Graff-Cherry, C., and Croix, B., Cancer Cell, 2007, vol. 11, pp. 539–554.

    Article  PubMed  CAS  Google Scholar 

  57. Roesli, C. and Neri, D., J. Proteomics, 2010, vol. 73, pp. 2219–2229.

    Article  PubMed  CAS  Google Scholar 

  58. Durr, E., Yu, J., Krasinska, K.M., Carver, L.A., Yates, J.R., Testa, J.E., Oh, P., and Schnitzer, J.E., Nat. Biotechnol., 2004, vol. 22, pp. 985–992.

    Article  PubMed  CAS  Google Scholar 

  59. Oh, P., Li, Y., Yu, J., Durr, E., Krasinska, K.M., Carver, L.A., Testa, J.E., and Schnitzer, J.E., Nature, 2004, vol. 429, pp. 629–635.

    Article  PubMed  CAS  Google Scholar 

  60. Hanahan, D. and Folkman, J., Cell, 1996, vol. 86, pp. 353–364.

    Article  PubMed  CAS  Google Scholar 

  61. Ferrara, N., Hillan, K.J., Gerber, H.P., and Novotny, W., Nat. Rev. Drug. Discov., 2004, vol. 3, pp. 391–400.

    Article  PubMed  CAS  Google Scholar 

  62. Azam, F., Mehta, S., and Harris, A.L., Eur. J. Cancer, 2010, vol. 46, pp. 1323–1332.

    Article  PubMed  CAS  Google Scholar 

  63. Kessler, T., Bayer, M., Schwoppe, C., Liersch, R., Mesters, R.M., and Berdel, W.E., Recent Results Cancer Res., 2010, vol. 180, pp. 137–163.

    Article  PubMed  CAS  Google Scholar 

  64. Kumar, S.R., Singh, J., Xia, G., Krasnoperov, V., Hassanieh, L., Ley, E.J., Scehnet, J., Kumar, N.G., Hawes, D., Press, M.F., Weaver, F.A., and Gill, P.S., Am. J. Pathol., 2006, vol. 169, pp. 279–293.

    Article  PubMed  CAS  Google Scholar 

  65. Masood, R., Kumar, S.R., Sinha, U.K., Crowe, D.L., Krasnoperov, V., Reddy, R.K., Zozulya, S., Singh, J., Xia, G., Broek, D., Schonthal, A.H., and Gill, P.S., Int. J. Cancer, 2006, vol. 119, pp. 1236–1248.

    Article  PubMed  CAS  Google Scholar 

  66. Xia, G., Kumar, S.R., Stein, J.P., Singh, J., Krasnoperov, V., Zhu, S., Hassanieh, L., Smith, D.L., Buscarini, M., Broek, D., Quinn, D.A., Weaver, F.A., and Gill, P.S., Oncogene, 2006, vol. 25, pp. 769–780.

    Article  PubMed  CAS  Google Scholar 

  67. Alam, S.M., Fujimoto, J., Jahan, I., Sato, E., and Tamaya, T., Br. J. Cancer, 2008, vol. 98, pp. 845–851.

    Article  PubMed  CAS  Google Scholar 

  68. Alam, S.M., Fujimoto, J., Jahan, I., Sato, E., and Tamaya, T., Gynecol. Oncol., 2009, vol. 114, pp. 84–88.

    Article  PubMed  CAS  Google Scholar 

  69. Wykosky, J. and Debinski, W., Mol. Cancer Res., 2008, vol. 6, pp. 1795–1806.

    Article  PubMed  CAS  Google Scholar 

  70. Almog, N., Ma, L., Raychowdhury, R., Schwager, C., Erber, R., Short, S., Hlatky, L., Vajkoczy, P., Huber, P.E., Folkman, J., and Abdollahi, A., Cancer Res., 2009, vol. 69, pp. 836–844.

    Article  PubMed  CAS  Google Scholar 

  71. Pytel, D., Sliwinski, T., Poplawski, T., Ferriola, D., and Majsterek, I., Anticancer Agents Med. Chem., 2009, vol. 9, pp. 66–76.

    PubMed  CAS  Google Scholar 

  72. Hirai, H., Maru, Y., Hagiwara, K., Nishida, J., and Takaku, F., Science, 1987, vol. 238, pp. 1717–1720.

    Article  PubMed  CAS  Google Scholar 

  73. Maru, Y., Hirai, H., and Takaku, F., Oncogene, 1990, vol. 5, pp. 445–447.

    PubMed  CAS  Google Scholar 

  74. Ding, L., Getz, G., Wheeler, D.A., Mardis, E.R., McLellan, M.D., Cibulskis, K., Sougnez, C., Greulich, H., Muzny, D.M., Morgan, M.B., et al., Nature, 2008, vol. 455, pp. 1069–1075.

    Article  PubMed  CAS  Google Scholar 

  75. Lee, D.J., Schonleben, F., Banuchi, V.E., Qiu, W., Close, L.G., Assaad, A.M., and Su, G.H., Cancer. Biol. Ther., 2010, vol. 10, pp. 689–693.

    Article  PubMed  CAS  Google Scholar 

  76. Bashaw, G.J. and Klein, R., Cold Spring Harb. Perspect. Biol., 2010, vol. 2, p. a001941.

    Article  PubMed  CAS  Google Scholar 

  77. Scehnet, J.S., Ley, E.J., Krasnoperov, V., Liu, R., Manchanda, P.K., Sjoberg, E., Kostecke, A.P., Gupta, S., Kumar, S.R., and Gill, P.S., Blood, 2009, vol. 113, pp. 254–263.

    Article  PubMed  CAS  Google Scholar 

  78. Taddei, M.L., Parri, M., Angelucci, A., Onnis, B., Bianchini, F., Giannoni, E., Raugei, G., Calorini, L., Rucci, N., Teti, A., Bologna, M., and Chiarugi, P., Am. J. Pathol., 2009, vol. 174, pp. 1492–1503.

    Article  PubMed  CAS  Google Scholar 

  79. Feng, Y.X., Zhao, J.S., Li, J.J., Wang, T., Cheng, S.Q., Yuan, Y., Wang, F., Wang, X.F., and Xie, D., Hepatology, 2010, vol. 51, pp. 535–544.

    Article  PubMed  CAS  Google Scholar 

  80. Nakamoto, M. and Bergemann, A.D., Microsc. Res. Tech., 2002, vol. 59, pp. 58–67.

    Article  PubMed  CAS  Google Scholar 

  81. Castano, J., Davalos, V., Schwartz, S., Jr., and Arango, D., Histol. Histopathol., 2008, vol. 23, pp. 1011–1023.

    PubMed  CAS  Google Scholar 

  82. Vaught, D., Brantley-Sieders, D.M., and Chen, J., Breast Cancer Res., 2008, vol. 10, p. 217.

  83. Herath, N.I. and Boyd, A.W., Int. J. Cancer, 2010, vol. 126, pp. 2003–2011.

    PubMed  CAS  Google Scholar 

  84. Batlle, E., Bacani, J., Begthel, H., Jonkheer, S., Gregorieff, A., van de Born, M., Malats, N., Sancho, E., Boon, E., Pawson, T., Gallinger, S., Pals, S., and Clevers, H., Nature, 2005, vol. 435, pp. 1126–1130.

    Article  PubMed  CAS  Google Scholar 

  85. Noberini, R. and Pasquale, E.B., Cancer Cell, 2009, vol. 16, pp. 452–454.

    Article  PubMed  CAS  Google Scholar 

  86. Truitt, L., Freywald, T., DeCoteau, J., Sharfe, N., and Freywald, A., Cancer Res., 2010, vol. 70, pp. 1141–1153.

    Article  PubMed  CAS  Google Scholar 

  87. Dong, Y., Wang, J., Sheng, Z., Li, G., Ma, H., Wang, X., Zhang, R., Lu, G., Hu, Q., Sugimura, H., and Zhou, X., Mod. Pathol., 2009, vol. 22, pp. 151–160.

    Article  PubMed  CAS  Google Scholar 

  88. Tanaka, M., Kamata, R., Yanagihara, K., and Sakai, R., Cancer Sci., 2010, vol. 101, pp. 87–93.

    Article  PubMed  CAS  Google Scholar 

  89. Astin, J.W., Batson, J., Kadir, S., Charlet, J., Persad, R.A., Gillatt, D., Oxley, J.D., and Nobes, C.D., Nat. Cell. Biol., 2010, Epub 11/16/2010.

  90. Zhuang, G., Brantley-Sieders, D.M., Vaught, D., Yu, J., Xie, L., Wells, S., Jackson, D., Muraoka-Cook, R., Arteaga, C., and Chen, J., Cancer. Res., 2010, vol. 70, pp. 299–308.

    Article  PubMed  CAS  Google Scholar 

  91. Larsen, A.B., Stockhausen, M.T., and Poulsen, H.S., Cell Signal., 2010, vol. 22, pp. 636–644.

    Article  PubMed  CAS  Google Scholar 

  92. Li, J.J., Liu, D.P., Liu, G.T., and Xie, D., Oncogene, 2009, vol. 28, pp. 1759–1768.

    Article  PubMed  CAS  Google Scholar 

  93. Yokote, H., Fujita, K., Jing, X., Sawada, T., Liang, S., Yao, L., Yan, X., Zhang, Y., Schlessinger, J., and Sakaguchi, K., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 18866–18871.

    Article  PubMed  CAS  Google Scholar 

  94. Fukai, J., Yokote, H., Yamanaka, R., Arao, T., Nishio, K., and Itakura, T., Mol. Cancer. Ther., 2008, vol. 7, pp. 2768–2778.

    Article  PubMed  CAS  Google Scholar 

  95. Sawamiphak, S., Seidel, S., Essmann, C.L., Wilkinson, G.A., Pitulescu, M.E., Acker, T., and Acker-Palmer, A., Nature, 2010, vol. 465, pp. 487–491.

    Article  PubMed  CAS  Google Scholar 

  96. Wang, Y., Nakayama, M., Pitulescu, M.E., Schmidt, T.S., Bochenek, M.L., Sakakibara, A., Adams, S., Davy, A., Deutsch, U., Luthi, U., Barberis, A., Benjamin, L.E., Makinen, T., Nobes, C.D., and Adams, R.H., Nature, 2010, vol. 465, pp. 483–486.

    Article  PubMed  CAS  Google Scholar 

  97. Miao, H., Li, D.Q., Mukherjee, A., Guo, H., Petty, A., Cutter, J., Basilion, J.P., Sedor, J., Wu, J., Danielpour, D., Sloan, A.E., Cohen, M.L., and Wang, B., Cancer Cell, 2009, vol. 16, pp. 9–20.

    Article  PubMed  CAS  Google Scholar 

  98. Johnson, L.N., Q. Rev. Biophys., 2009, vol. 42, pp. 1–40.

    Article  PubMed  CAS  Google Scholar 

  99. Fabian, M.A. and Biggs, W.H., 3rd, Treiber D.K., Atteridge C.E., Azimioara M.D., Benedetti M.G., Carter, T.A., Ciceri, P., Edeen, P.T., Floyd, M., Ford, J.M., Galvin, M., Gerlach, J.L., Grotzfeld, R.M., Herrgard, S., Insko, D.E., Insko, M.A., Lai, A.G., Lelias, J.M., Mehta, S.A., Milanov, Z.V., Velasco, A.M., Wodicka, L.M., Patel, H.K., Zarrinkar, P.P., and Lockhart, D.J., Nat. Biotechnol., 2005, vol. 23, pp. 329–336.

    Article  PubMed  CAS  Google Scholar 

  100. Faivre, S., Demetri, G., Sargent, W., and Raymond, E., Nat. Rev. Drug. Discov., 2007, vol. 6, pp. 734–745.

    Article  PubMed  CAS  Google Scholar 

  101. Rix, U., Remsing Rix, L. L., Terker, A.S., Fernbach, N.V., Hantschel, O., Planyavsky, M., Breitwieser, F.P., Herrmann, H., Colinge, J., Bennett, K.L., Augustin, M., Till, J.H., Heinrich, M.C., Valent, P., and Superti-Furga, G., Leukemia, 2010, vol. 24, pp. 44–50.

    Article  PubMed  CAS  Google Scholar 

  102. Chang, Q., Jorgensen, C., Pawson, T., and Hedley, D.W., Br. J. Cancer, 2008, vol. 99, pp. 1074–1082.

    Article  PubMed  CAS  Google Scholar 

  103. Caligiuri, M., Molz, L., Liu, Q., Kaplan, F., Xu, J.P., Majeti, J.Z., Ramos-Kelsey, R., Murthi, K., Lievens, S., Tavernier, J., and Kley, N., Chem. Biol., 2006, vol. 13, pp. 711–722.

    Article  PubMed  CAS  Google Scholar 

  104. Lafleur, K., Huang, D., Zhou, T., Caflisch, A., and Nevado, C., J. Med. Chem., 2009, vol. 52, pp. 6433–6446.

    Article  PubMed  CAS  Google Scholar 

  105. Bardelle, C., Barlaam, B., Brooks, N., Coleman, T., Cross, D., Ducray, R., Green, I., Brempt, C.L., Olivier, A., and Read, J., Bioorg. Med. Chem. Lett., 2010, vol. 20, pp. 6242–6245.

    Article  PubMed  CAS  Google Scholar 

  106. Martiny-Baron, G., Holzer, P., Billy, E., Schnell, C., Brueggen, J., Ferretti, M., Schmiedeberg, N., Wood, J.M., Furet, P., and Imbach, P., Angiogenes, 2010, vol. 13, pp. 259–267.

    Article  CAS  Google Scholar 

  107. Noberini, R., Koolpe, M., Peddibhotla, S., Dahl, R., Su, Y., Cosford, N.D., Roth, G.P., and Pasquale, E.B., J. Biol. Chem., 2008, vol. 283, pp. 29461–29472.

    Article  PubMed  CAS  Google Scholar 

  108. Koolpe, M., Dail, M., and Pasquale, E.B., J. Biol. Chem., 2002, vol. 277, pp. 46974–46979.

    Article  PubMed  CAS  Google Scholar 

  109. Mitra, S., Duggineni, S., Koolpe, M., Zhu, X., Huang, Z., and Pasquale, E.B., Biochemistry, 2010, vol. 49, pp. 6687–6695.

    Article  PubMed  CAS  Google Scholar 

  110. Murai, K.K., Nguyen, L.N., Koolpe, M., McLennan, R., Krull, C.E., and Pasquale, E.B., Mol. Cell. Neurosci., 2003, vol. 24, pp. 1000–1011.

    Article  PubMed  CAS  Google Scholar 

  111. Koolpe, M., Burgess, R., Dail, M., and Pasquale, E.B., J. Biol. Chem., 2005, vol. 280, pp. 17301–17311.

    Article  PubMed  CAS  Google Scholar 

  112. Chrencik, J.E., Brooun, A., Recht, M.I., Kraus, M.L., Koolpe, M., Kolatkar, A.R., Bruce, R.H., Martiny-Baron, G., Widmer, H., Pasquale, E.B., and Kuh, P., Structure, 2006, vol. 14, pp. 321–330.

    Article  PubMed  CAS  Google Scholar 

  113. van Geer, M.A., Bakker, C.T., Koizumi, N., Mizuguchi, H., and Wesseling, J.G., Oude Elferink R.P., and Bosma P.J, World J. Gastroenterol., 2009, vol. 15, pp. 2754–2762.

    Article  PubMed  CAS  Google Scholar 

  114. Martin, T.J., Allan, E.H., Ho, P.W., Gooi, J.H., Quinn, J.M., Gillespie, M.T., Krasnoperov, V., and Sims, N.A., Adv. Exp. Med. Biol., 2010, vol. 658, pp. 51–60.

    Article  PubMed  CAS  Google Scholar 

  115. Martiny-Baron, G., Korff, T., Schaffner, F., Esser, N., Eggstein, S., Marme, D., and Augustin, H.G., Neoplasia, 2004, vol. 6, pp. 248–257.

    Article  PubMed  CAS  Google Scholar 

  116. Kertesz, N., Krasnoperov, V., Reddy, R., Leshanski, L., Kumar, S.R., Zozulya, S., and Gill, P.S., Blood, 2006, vol. 107, pp. 2330–2338.

    Article  PubMed  CAS  Google Scholar 

  117. Djokovic, D., Trindade, A., Gigante, J., Badenes, M., Silva, L., Liu, R., Li, X., Gong, M., Krasnoperov, V., Gill, P.S., and Duarte, A., BMC Cancer, 2010, vol. 10, p. 641.

    Article  PubMed  CAS  Google Scholar 

  118. Ehlken, C., Martin, G., Lange, C., Gogaki, E.G., Fiedler, U., Schaffner, F., Hansen, L.L., Augustin, H.G., and Agostini, H.T., Acta Ophthalmol., 2009. DOI: 10.1111/j.1755-3768.2009.01609.x.

  119. Maekawa, H., Oike, Y., Kanda, S., Ito, Y., Yamada, Y., Kurihara, H., Nagai, R., and Suda, T., Arterioscler. Thromb. Vasc. Biol., 2003, vol. 23, pp. 2008–2014.

    Article  PubMed  CAS  Google Scholar 

  120. Zamora, D.O., Davies, M.H., Planck, S.R., Rosenbaum, J.T., and Powers, M.R., Invest. Ophthalmol. Vis. Sci., 2005, vol. 46, pp. 2175–2182.

    Article  PubMed  Google Scholar 

  121. Davies M.H., Zamora D.O., Smith J.R., and Powers M.R., Microvasc. Res., 2009, vol. 77, pp. 382–386.

    Article  PubMed  CAS  Google Scholar 

  122. Kimura, M., Kato, Y., Sano, D., Fujita, K., Sakakibara, A., Kondo, N., Mikami, Y., and Tsukuda, M., Int. J. Oncol., 2009, vol. 34, pp. 321–327.

    PubMed  CAS  Google Scholar 

  123. Pennisi, A., Ling, W., Li, X., Khan, S., Shaughnessy, J.D., Jr., Barlogie, B., and Yaccoby, S., Blood, 2009, vol. 114, pp. 1803–1812.

    Article  PubMed  CAS  Google Scholar 

  124. Fuller, T., Korff, T., Kilian, A., Dandekar, G., and Augustin, H.G., J. Cell Sci., 2003, vol. 116, pp. 2461–2470.

    Article  PubMed  CAS  Google Scholar 

  125. Huynh-Do, U., Vindis, C., Liu, H., Cerretti, D.P., McGrew, J.T., Enriquez, M., Chen, J., and Daniel, T.O., J. Cell Sci., 2002, vol. 115, pp. 3073–3081.

    PubMed  CAS  Google Scholar 

  126. Nakada, M., Drake, K.L., Nakada, S., Niska, J.A., and Berens, M.E., Cancer Res., 2006, vol. 66, pp. 8492–8500.

    Article  PubMed  CAS  Google Scholar 

  127. Kojima, T., Chang, J.H., and Azar, D.T., Am. J. Pathol., 2007, vol. 170, pp. 764–773.

    Article  PubMed  CAS  Google Scholar 

  128. Hafner, C., Meyer, S., Langmann, T., Schmitz, G., Bataille, F., Hagen, I., Becker, B., Roesch, A., Rogler, G., Landthaler, M., and Vogt, T., World J. Gastroenterol., 2005, vol. 11, pp. 4024–4031.

    PubMed  CAS  Google Scholar 

  129. Brantley, D.M., Cheng, N., Thompson, E.J., Lin, Q., Brekken, R.A., Thorpe, P.E., Muraoka, R.S., Cerretti, D.P., Pozzi, A., Jackson, D., Lin, C., and Chen, J., Oncogene, 2002, vol. 21, pp. 7011–7026.

    Article  PubMed  CAS  Google Scholar 

  130. Dobrzanski, P., Hunter, K., Jones-Bolin, S., Chang, H., Robinson, C., Pritchard, S., Zhao, H., and Ruggeri, B., Cancer Res., 2004, vol. 64, pp. 910–919.

    Article  PubMed  CAS  Google Scholar 

  131. Chen, J., Hicks, D., Brantley-Sieders, D., Cheng, N., McCollum, G.W., Qi-Werdich, X., and Penn, J., Exp. Eye. Res., 2006, vol. 82, pp. 664–673.

    Article  PubMed  CAS  Google Scholar 

  132. Wykosky J., Gibo D.M., and Debinski W., Mol. Cancer. Ther., 2007, vol. 6, pp. 3208–3218.

    Article  PubMed  CAS  Google Scholar 

  133. Gobin, A.M., Moon, J.J., and West, J.L., Int. J. Nanomed., 2008, vol. 3, pp. 351–358.

    CAS  Google Scholar 

  134. Carles-Kinch, K., Kilpatrick, K.E., Stewart, J.C., and Kinch, M.S., Cancer Res., 2002, vol. 62, pp. 2840–2847.

    PubMed  CAS  Google Scholar 

  135. Gokmen-Polar, Y., Toroni, R.A., Hocevar, B.A., Badve, S., Zhao, Q., Shen, C., Bruckheimer, E., Kinch, M.S., and Miller, K.D., Breast Cancer Res. Treat., 2010. DOI: 10.1007/s10549-010-1004-y.

  136. Ansuini, H., Meola, A., Gunes, Z., Paradisi, V., Pezzanera, M., Acali, S., Santini, C., Luzzago, A., Mori, F., Lazzaro, D., Ciliberto, G., Nicosia, A., La Monica, N., and Vitelli, A., J. Oncol., 2009, p. 951917.

  137. Lee, J.W., Stone, R.L., Lee, S.J., Nam, E.J., Roh, J.W., Nick, A.M., Han, H.D., Shahzad, M.M., Kim, H.S., Mangala, L.S., Jennings, N.B., Mao, S., Gooya, J., Jackson, D., Coleman, R.L., and Sood, A.K., Clin. Cancer Res., 2010, vol. 16, pp. 2562–2570.

    Article  PubMed  CAS  Google Scholar 

  138. Hammond, S.A., Lutterbuese, R., Roff, S., Lutterbuese, P., Schlereth, B., Bruckheimer, E., Kinch, M.S., Coats, S., Baeuerle, P.A., Kufer, P., and Kiener, P.A., Cancer Res., 2007, vol. 67, pp. 3927–3935.

    Article  PubMed  CAS  Google Scholar 

  139. Vearing, C., Lee, F.T., Wimmer-Kleikamp, S., Spirkoska, V., To, C., Stylianou, C., Spanevello, M., Brechbiel, M., Boyd, A.W., Scott, A.M., and Lackmann, M., Cancer Res., 2005, vol. 65, pp. 6745–6754.

    Article  PubMed  CAS  Google Scholar 

  140. Nakada, M., Anderson, E.M., Demuth, T., Nakada, S., Reavie, L.B., Drake, K.L., Hoelzinger, D.B., and Berens, M.E., Int. J. Cancer, 2010, vol. 126, pp. 1155–1165.

    PubMed  CAS  Google Scholar 

  141. Mao, W., Luis, E., Ross, S., Silva, J., Tan, C., Crowley, C., Chui, C., Franz, G., Senter, P., Koeppen, H., and Polakis, P., Cancer. Res., 2004, vol. 64, pp. 781–788.

    Article  PubMed  CAS  Google Scholar 

  142. Krasnoperov, V., Kumar, S.R., Ley, E., Li, X., Scehnet, J., Liu, R., Zozulya, S., and Gill, P.S., Am. J. Pathol., 2010, vol. 176, pp. 2029–2038.

    Article  PubMed  CAS  Google Scholar 

  143. Spannuth, W.A., Mangala, L.S., Stone, R.L., Carroll, A.R., Nishimura, M., Shahzad, M.M., Lee, S.J., Moreno-Smith, M., Nick, A.M., Liu, R., Jennings, N.B., Lin, Y.G., Merritt, W.M., Coleman, R.L., Vivas-Mejia, P.E., Zhou, Y., Krasnoperov, V., Lopez-Berestein, G., Gill, P.S., and Sood, A.K., Mol. Cancer. Ther., 2010, vol. 9, pp. 2377–2388.

    Article  PubMed  CAS  Google Scholar 

  144. Bonaparte, M.I., Dimitrov, A.S., Bossart, K.N., Crameri, G., Mungall, B.A., Bishop, K.A., Choudhry, V., Dimitrov, D.S., Wang, L.F., Eaton, B.T., and Broder, C.C., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 10652–10657.

    Article  PubMed  CAS  Google Scholar 

  145. Yamaguchi, S., Tatsumi, T., Takehara, T., Sakamori, R., Uemura, A., Mizushima, T., Ohkawa, K., Storkus, W.J., and Hayashi, N., Cancer, 2007, vol. 110, pp. 1469–1477.

    Article  PubMed  CAS  Google Scholar 

  146. Yamaguchi, S., Tatsumi, T., Takehara, T., Sasakawa, A., Hikita, H., Kohga, K., Uemura, A., Sakamori, R., Ohkawa, K., and Hayashi, N., Cancer Immunol. Immunother., 2008, vol. 57, pp. 1861–1869.

    Article  PubMed  CAS  Google Scholar 

  147. Jin, M., Komohara, Y., Shichijo, S., Yamanaka, R., Nikawa, J., Itoh, K., and Yamada, A., Cancer Sci., 2008, vol. 99, pp. 1656–1662.

    Article  PubMed  CAS  Google Scholar 

  148. Yamaguchi, S., Tatsumi, T., Takehara, T., Sasakawa, A., Yamamoto, M., Kohga, K., Miyagi, T., Kanto, T., Hiramastu, N., Akagi, T., Akashi, M., and Hayashi, N., Cancer Immunol. Immunother., 2010, vol. 59, pp. 759–767.

    Article  PubMed  CAS  Google Scholar 

  149. Chen, G., Wang, Y., Zhou, M., Shi, H., Yu, Z., Zhu, Y., and Yu, F., Oncol. Rep., 2010, vol. 23, pp. 563–570.

    PubMed  CAS  Google Scholar 

  150. Nasreen, N., Mohammed, K.A., and Antony, V.B., Cancer, 2006, vol. 107, pp. 2425–2435.

    Article  PubMed  CAS  Google Scholar 

  151. Oki, M., Yamamoto, H., Taniguchi, H., Adachi, Y., Imai, K., and Shinomura, Y., World. J. Gastroenterol., 2008, vol. 14, pp. 5650–5656.

    Article  PubMed  CAS  Google Scholar 

  152. Masood, R., Xia, G., Smith, D.L., Scalia, P., Still, J.G., Tulpule, A., and Gill, P.S., Blood, 2005, vol. 105, pp. 1310–1318.

    Article  PubMed  CAS  Google Scholar 

  153. Mansson-Broberg, A., Siddiqui, A.J., Genander, M., Grinnemo, K.H., Hao, X., Andersson, A.B., Wardell, E., Sylven, C., and Corbascio, M., Biochem. Biophys. Res. Commun., 2008, vol. 373, pp. 355–359.

    Article  PubMed  CAS  Google Scholar 

  154. Garber, K., J. Natl. Cancer. Inst., 2010, vol. 102, pp. 1692–1694.

    Article  PubMed  Google Scholar 

  155. Noren, N.K. and Pasquale, E.B., Cancer Res., 2007, vol. 67, pp. 3994–3997.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. ChemDiv, Inc., 6605 Nancy Ridge Drive, San Diego, CA, 92121, USA

    S. A. Zozulya

  2. Branch of Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, prospect Nauki, 6, Pushchino, Moscow oblast, 142290, Russia

    I. P. Udovichenko

  3. Pushchino State University, prospect Nauki, 3, Pushchino, Moscow oblast, 142290, Russia

    I. P. Udovichenko

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  1. S. A. Zozulya
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Correspondence to S. A. Zozulya.

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Published in Russian in Bioorganicheskaya Khimiya, 2012, Vol. 38, No. 3, pp. 267–279.

The article was translated by the authors.

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Zozulya, S.A., Udovichenko, I.P. Eph family receptors as therapeutic targets. Russ J Bioorg Chem 38, 231–242 (2012). https://doi.org/10.1134/S106816201203017X

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