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Biochemistry (Moscow)

, Volume 78, Issue 11, pp 1228–1237 | Cite as

Malignant melanoma and melanocortin 1 receptor

  • A. A. Rosenkranz
  • T. A. Slastnikova
  • M. O. Durymanov
  • A. S. Sobolev
Review

Abstract

The conventional chemotherapeutic treatment of malignant melanoma still remains poorly efficient in most cases. Thus the use of specific features of these tumors for development of new therapeutic modalities is highly needed. Melanocortin 1 receptor (MC1R) overexpression on the cell surface of the vast majority of human melanomas, making MC1R a valuable marker of these tumors, is one of these features. Naturally, MC1R plays a key role in skin protection against damaging ultraviolet radiation by regulating eumelanin production. MC1R activation is involved in regulation of melanocyte cell division. This article reviews the peculiarities of regulation and expression of MC1R, melanocytes, and melanoma cells, along with the possible connection of MC1R with signaling pathways regulating proliferation of tumor cells. MC1R is a cell surface endocytic receptor, thus considered perspective for diagnostics and targeted drug delivery. A number of new therapeutic approaches that utilize MC1R, including endoradiotherapy with Auger electron and α- and β-particle emitters, photodynamic therapy, and gene therapy are now being developed.

Key words

melanoma melanocortin 1 receptor α-melanocyte-stimulating hormone receptor endocytosis cancer therapy diagnostics 

Abbreviations

ACTH

adrenocorticotropin

AGRP

agouti-related protein

α-MSH

α-melanocyte-stimulating hormone

ARRB1

arrestin-beta-1

ARRB2

arrestin-beta-2

ASIP

agouti signal protein

Bcl-2

apoptosis regulator from B-cell lymphoma 2

BD3

β-defensin 3

BRAF

v-Raf murine sarcoma viral oncogene homolog B1

CDKN2A

cyclin-dependent kinase inhibitor 2A

CRE

cAMP-responsive element

CREB

cAMP-responsive element-binding protein

ERK

extracellular signal-regulated kinases

GPCR

G-protein coupled receptors

GRK

GPCR kinase

I-κB

nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor

LET

linear energy transfer

MAPK

mitogen-activated protein kinases

MC1R

melanocortin 1 receptor

MGRN1

mahogunin RING finger-1 (ubiquitin E3 ligase with RING-domain)

MITF

microphthalmia transcription factor

MRAP

melanocortin-2-receptor accessory protein

mTor

mammalian target of rapamycin

NEDD9

neural precursor cell expressed, developmentally down-regulated 9

NF-κB

nuclear factor kappa-light-chain-enhancer of activated B cells

NIS

Na-I symporter

PKA

protein kinase A

RING

real interesting new gene

Sdc2

syndecane-2

TUBB3

β-III-tubulin

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Supplementary material

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References

  1. 1.
    Chissov, V. I., Starinsky, V. V., and Petrova, G. V. (eds.) Malignant Neoplasms in Russia in 2011 (Morbidity and Mortality), PA Herzen MNIOI Company, Ministry of Health of Russian Federation, Moscow.Google Scholar
  2. 2.
    Siegel, R., Ward, E., Brawley, O., and Jemal, A. (2011) CA Cancer J. Clin., 61, 212–236.PubMedGoogle Scholar
  3. 3.
    Al-Hilli, Z., Evoy, D., Geraghty, J. G., McDermott, E. W., and Prichard, R. S. (2013) in Melanoma — From Early Detection to Treatment (Duc, T. H., ed.) InTech, Rijeka, pp. 411–437.Google Scholar
  4. 4.
    Lee, B., Mukhi, N., and Liu, D. (2012) J. Hematol. Oncol., 5, 1–7.Google Scholar
  5. 5.
    Balch, C. M., Gershenwald, J. E., Soong, S. J., Thompson, J. F., Atkins, M. B., Byrd, D. R., Buzaid, A. C., Cochran, A. J., Coit, D. G., Ding, S., Eggermont, A. M., Flaherty, K. T., Gimotty, P. A., Kirkwood, J. M., McMasters, K. M., Mihm, M. C., Jr., Morton, D. L., Ross, M. I., Sober, A. J., and Sondak, V. K. (2009) J. Clin. Oncol., 27, 6199–6206.PubMedGoogle Scholar
  6. 6.
    Pleshkan, V. V., Zinov’eva, M. V., and Sverdlov, E. D. (2011) Mol. Biol. (Moscow), 45, 416–433.Google Scholar
  7. 7.
    Eggermont, A. M. (2010) Ann. Oncol., 21, vii339–vii344.PubMedGoogle Scholar
  8. 8.
    Slominski, A. T., Zmijewski, M. A., Skobowiat, C., Zbytek, B., Slominski, R. M., and Steketee, J. D. (2012) Adv. Anat. Embryol. Cell Biol., 212, v–115.PubMedGoogle Scholar
  9. 9.
    Abdel-Malek, Z. A., Knittel, J., Kadekaro, A. L., Swope, V. B., and Starner, R. (2008) Photochem. Photobiol., 84, 501–508.PubMedGoogle Scholar
  10. 10.
    Anisimov, V. V., and Vagner, R. I. (1995) Skin Melanoma. Part 1. Epidemiology, Etiology, Pathogenesis, Prevention [in Russian], Nauka, St. Petersburg.Google Scholar
  11. 11.
    Slominski, A., Wortsman, J., Carlson, A. J., Matsuoka, L. Y., Balch, C. M., and Mihm, M. C. (2001) Arch. Pathol. Lab Med., 125, 1295–1306.PubMedGoogle Scholar
  12. 12.
    Wikberg, J. E., Muceniece, R., Mandrika, I., Prusis, P., Lindblom, J., Post, C., and Skottner, A. (2000) Pharmacol. Res., 42, 393–420.PubMedGoogle Scholar
  13. 13.
    Ibrahim, N., and Haluska, F. G. (2009) Annu. Rev. Pathol., 4, 551–579.PubMedGoogle Scholar
  14. 14.
    Kim, M., Gans, J. D., Nogueira, C., Wang, A., Paik, J. H., Feng, B., Brennan, C., Hahn, W. C., Cordon-Cardo, C., Wagner, S. N., Flotte, T. J., Duncan, L. M., Granter, S. R., and Chin, L. (2006) Cell, 125, 1269–1281.PubMedGoogle Scholar
  15. 15.
    Moore, S. R., Persons, D. L., Sosman, J. A., Bobadilla, D., Bedell, V., Smith, D. D., Wolman, S. R., Tuthill, R. J., Moon, J., Sondak, V. K., and Slovak, M. L. (2008) Clin. Cancer Res., 14, 2927–2935.PubMedGoogle Scholar
  16. 16.
    Tsao, H., Chin, L., Garraway, L. A., and Fisher, D. E. (2012) Genes Dev., 26, 1131–1155.PubMedGoogle Scholar
  17. 17.
    Jang, S., and Atkins, M. B. (2013) Lancet Oncol., 14, e60–e69.PubMedGoogle Scholar
  18. 18.
    Eberle, A. N. (1981) Biochem. Soc. Trans., 9, 37–39.PubMedGoogle Scholar
  19. 19.
    Tatro, J. B., Atkins, M., Mier, J. W., Hardarson, S., Wolfe, H., Smith, T., Entwistle, M. L., and Reichlin, S. (1990) J. Clin. Invest., 85, 1825–1832.PubMedGoogle Scholar
  20. 20.
    Tatro, J. B., Wen, Z., Entwistle, M. L., Atkins, M. B., Smith, T. J., Reichlin, S., and Murphy, J. R. (1992) Cancer Res., 52, 2545–2548.PubMedGoogle Scholar
  21. 21.
    Funasaka, Y., Sato, H., Chakraborty, A. K., Ohashi, A., Chrousos, G. P., and Ichihashi, M. (1999) J. Investig. Dermatol. Symp. Proc., 4, 105–109.PubMedGoogle Scholar
  22. 22.
    Loir, B., Perez, S. C., Ghanem, G., Lozano, J. A., Garcia-Borron, J. C., and Jimenez-Cervantes, C. (1999) Cell Mol. Biol. (Noisy-le-Grand), 45, 1083–1092.Google Scholar
  23. 23.
    Salazar-Onfray, F., Lopez, M., Lundqvist, A., Aguirre, A., Escobar, A., Serrano, A., Korenblit, C., Petersson, M., Chhajlani, V., Larsson, O., and Kiessling, R. (2002) Br. J. Cancer, 87, 414–422.PubMedGoogle Scholar
  24. 24.
    Lopez, M. N., Pereda, C., Ramirez, M., Mendoza-Naranjo, A., Serrano, A., Ferreira, A., Poblete, R., Kalergis, A. M., Kiessling, R., and Salazar-Onfray, F. (2007) Invest. Ophthalmol. Vis. Sci., 48, 1219–1227.PubMedGoogle Scholar
  25. 25.
    Ogbah, Z., Puig-Butille, J. A., Simonetta, F., Badenas, C., Cervera, R., Mila, J., Benitez, D., Malvehy, J., Vilella, R., and Puig, S. (2012) Anticancer Res., 32, 1245–1251.PubMedGoogle Scholar
  26. 26.
    Halaban, R. (2000) Pigment Cell Res., 13, 4–14.PubMedGoogle Scholar
  27. 27.
    Muffley, L. A., Zhu, K. Q., Engrav, L. H., Gibran, N. S., and Hocking, A. M. (2011) J. Histochem. Cytochem., 59, 278–288.PubMedGoogle Scholar
  28. 28.
    Eves, P. C., and Haycock, J. W. (2010) Adv. Exp. Med. Biol., 681, 19–28.PubMedGoogle Scholar
  29. 29.
    Scherer, D., and Kumar, R. (2010) Mutat. Res., 705, 141–153.PubMedGoogle Scholar
  30. 30.
    Li, G., and Herlyn, M. (2000) Mol. Med. Today, 6, 163–169.PubMedGoogle Scholar
  31. 31.
    Chakraborty, A. K., Funasaka, Y., Slominski, A., Ermak, G., Hwang, J., Pawelek, J. M., and Ichihashi, M. (1996) Biochim. Biophys. Acta, 1313, 130–138.PubMedGoogle Scholar
  32. 32.
    Chakraborty, A. K., Funasaka, Y., Pawelek, J. M., Nagahama, M., Ito, A., and Ichihashi, M. (1999) J. Invest. Dermatol., 112, 853–860.PubMedGoogle Scholar
  33. 33.
    D’Orazio, J. A., Nobuhisa, T., Cui, R., Arya, M., Spry, M., Wakamatsu, K., Igras, V., Kunisada, T., Granter, S. R., Nishimura, E. K., Ito, S., and Fisher, D. E. (2006) Nature, 443, 340–344.PubMedGoogle Scholar
  34. 34.
    Tada, A., Suzuki, I., Im, S., Davis, M. B., Cornelius, J., Babcock, G., Nordlund, J. J., and Abdel-Malek, Z. A. (1998) Cell Growth Differ., 9, 575–584.PubMedGoogle Scholar
  35. 35.
    Scott, M. C., Suzuki, I., and Abdel-Malek, Z. A. (2002) Pigment Cell Res., 15, 433–439.PubMedGoogle Scholar
  36. 36.
    Suzuki, I., Cone, R. D., Im, S., Nordlund, J., and Abdel-Malek, Z. A. (1996) Endocrinology, 137, 1627–1633.PubMedGoogle Scholar
  37. 37.
    Rouzaud, F., Annereau, J. P., Valencia, J. C., Costin, G. E., and Hearing, V. J. (2003) FASEB J., 17, 2154–2156.PubMedGoogle Scholar
  38. 38.
    Rouzaud, F., Kadekaro, A. L., Abdel-Malek, Z. A., and Hearing, V. J. (2005) Mutat. Res., 571, 133–152.PubMedGoogle Scholar
  39. 39.
    Siegrist, W., Stutz, S., and Eberle, A. N. (1994) Cancer Res., 54, 2604–2610.PubMedGoogle Scholar
  40. 40.
    Xia, Y., Skoog, V., Muceniece, R., Chhajlani, V., and Wikberg, J. E. (1995) Eur. J. Pharmacol., 288, 277–283.PubMedGoogle Scholar
  41. 41.
    Mandrika, I., Petrovska, R., and Wikberg, J. (2005) Biochem. Biophys. Res. Commun., 326, 349–354.PubMedGoogle Scholar
  42. 42.
    Zanna, P. T., Sanchez-Laorden, B. L., Perez-Oliva, A. B., Turpin, M. C., Herraiz, C., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2008) Biochem. Biophys. Res. Commun., 368, 211–216.PubMedGoogle Scholar
  43. 43.
    Beaumont, K. A., Liu, Y. Y., and Sturm, R. A. (2009) Prog. Mol. Biol. Transl. Sci., 88, 85–153.PubMedGoogle Scholar
  44. 44.
    Wong, W., and Minchin, R. F. (1996) Int. J. Biochem. Cell Biol., 28, 1223–1232.PubMedGoogle Scholar
  45. 45.
    Sanchez-Mas, J., Guillo, L. A., Zanna, P., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2005) Mol. Endocrinol., 19, 1035–1048.PubMedGoogle Scholar
  46. 46.
    Sanchez-Laorden, B. L., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2007) J. Biol. Chem., 282, 3241–3251.PubMedGoogle Scholar
  47. 47.
    Abrisqueta, M., Herraiz, C., Perez Oliva, A. B., Sanchez-Laorden, B. L., Olivares, C., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2013) J. Cell Sci., jcs.128322; Advance Online Article June 7, 2013.Google Scholar
  48. 48.
    Xia, Y., Muceniece, R., and Wikberg, J. E. (1996) Cancer Lett., 98, 157–162.PubMedGoogle Scholar
  49. 49.
    Thornwall, M., Dimitriou, A., Xu, X., Larsson, E., and Chhajlani, V. (1997) Horm. Res., 48, 215–218.PubMedGoogle Scholar
  50. 50.
    Chan, L. F., Webb, T. R., Chung, T. T., Meimaridou, E., Cooray, S. N., Guasti, L., Chapple, J. P., Egertova, M., Elphick, M. R., Cheetham, M. E., Metherell, L. A., and Clark, A. J. (2009) Proc. Natl. Acad. Sci. USA, 106, 6146–6151.PubMedGoogle Scholar
  51. 51.
    He, L., Gunn, T. M., Bouley, D. M., Lu, X. Y., Watson, S. J., Schlossman, S. F., Duke-Cohan, J. S., and Barsh, G. S. (2001) Nat. Genet., 27, 40–47.PubMedGoogle Scholar
  52. 52.
    Perez-Oliva, A. B., Olivares, C., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2009) J. Biol. Chem., 284, 31714–31725.PubMedGoogle Scholar
  53. 53.
    Eberle, A. N., Siegrist, W., Bagutti, C., Chluba-De Tapia, J., Solca, F., Wikberg, J. E., and Chhajlani, V. (1993) Ann. N. Y. Acad. Sci., 680, 320–341.PubMedGoogle Scholar
  54. 54.
    Garcia-Borron, J. C., Sanchez-Laorden, B. L., and Jimenez-Cervantes, C. (2005) Pigment Cell Res., 18, 393–410.PubMedGoogle Scholar
  55. 55.
    Peters, E. M., Tobin, D. J., Seidah, N. G., and Schallreuter, K. U. (2000) J. Invest. Dermatol., 114, 430–437.PubMedGoogle Scholar
  56. 56.
    Dalziel, M., Kolesnichenko, M., das Neves, R. P., Iborra, F., Goding, C., and Furger, A. (2011) Nucleic Acids Res., 39, 2378–2392.PubMedGoogle Scholar
  57. 57.
    Ramachandrappa, S., Gorrigan, R. J., Clark, A. J., and Chan, L. F. (2013) Front. Endocrinol. (Lausanne), 4, 9.Google Scholar
  58. 58.
    Bohm, M., Metze, D., Schulte, U., Becher, E., Luger, T. A., and Brzoska, T. (1999) Exp. Dermatol., 8, 453–461.PubMedGoogle Scholar
  59. 59.
    Wikberg, J. E. (1999) Eur. J. Pharmacol., 375, 295–310.PubMedGoogle Scholar
  60. 60.
    Hartmeyer, M., Scholzen, T., Becher, E., Bhardwaj, R. S., Schwarz, T., and Luger, T. A. (1997) J. Immunol., 159, 1930–1937.PubMedGoogle Scholar
  61. 61.
    Luger, T. A., Scholzen, T. E., Brzoska, T., and Bohm, M. (2003) Ann. N. Y. Acad. Sci., 994, 133–140.PubMedGoogle Scholar
  62. 62.
    Roberts, D. W., Newton, R. A., Beaumont, K. A., Helen, L. J., and Sturm, R. A. (2006) Pigment Cell Res., 19, 76–89.PubMedGoogle Scholar
  63. 63.
    Sturm, R. A. (2009) Hum. Mol. Genet., 18, R9–17.Google Scholar
  64. 64.
    Ibrahim, N., and Haluska, F. G. (2009) Annu. Rev. Pathol., 4, 551–579.PubMedGoogle Scholar
  65. 65.
    Demenais, F., Mohamdi, H., Chaudru, V., Goldstein, A. M., Newton Bishop, J. A., Bishop, D. T., Kanetsky, P. A., Hayward, N. K., Gillanders, E., Elder, D. E., Avril, M. F., Azizi, E., van Belle, P., Bergman, W., Bianchi-Scarra, G., Bressac-de Paillerets, B., Calista, D., Carrera, C., Hansson, J., Harland, M., Hogg, D., Hoiom, V., Holland, E. A., Ingvar, C., Landi, M. T., Lang, J. M., Mackie, R. M., Mann, G. J., Ming, M. E., Njauw, C. J., Olsson, H., Palmer, J., Pastorino, L., Puig, S., Randerson-Moor, J., Stark, M., Tsao, H., Tucker, M. A., van der Velden, P., Yang, X. R., and Gruis, N. (2010) J. Natl. Cancer Inst., 102, 1568–1583.PubMedGoogle Scholar
  66. 66.
    Beaumont, K. A., Wong, S. S., Ainger, S. A., Liu, Y. Y., Patel, M. P., Millhauser, G. L., Smith, J. J., Alewood, P. F., Leonard, J. H., and Sturm, R. A. (2011) Eur. J. Pharmacol., 660, 103–110.PubMedGoogle Scholar
  67. 67.
    Chung, H., Lee, J. H., Jeong, D., Han, I. O., and Oh, E. S. (2012) J. Biol. Chem., 287, 19326–19335.PubMedGoogle Scholar
  68. 68.
    Flaherty, K. T., Hodi, F. S., and Fisher, D. E. (2012) Nat. Rev. Cancer, 12, 349–361.PubMedGoogle Scholar
  69. 69.
    Herraiz, C., Journe, F., Abdel-Malek, Z., Ghanem, G., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2011) Mol. Endocrinol., 25, 138–156.PubMedGoogle Scholar
  70. 70.
    Herraiz, C., Jimenez-Cervantes, C., Zanna, P., and Garcia-Borron, J. C. (2009) FEBS Lett., 583, 3269–3274.PubMedGoogle Scholar
  71. 71.
    Herraiz, C., Journe, F., Ghanem, G., Jimenez-Cervantes, C., and Garcia-Borron, J. C. (2012) Int. J. Biochem. Cell Biol., 44, 2244–2252.PubMedGoogle Scholar
  72. 72.
    Abdel-Malek, Z. A. (2001) Cell Mol. Life Sci., 58, 434–441.PubMedGoogle Scholar
  73. 73.
    Wikberg, J. E., Muceniece, R., Mandrika, I., Prusis, P., Lindblom, J., Post, C., and Skottner, A. (2000) Pharmacol. Res., 42, 393–420.PubMedGoogle Scholar
  74. 74.
    Bousquet, C., and Melmed, S. (1999) J. Biol. Chem., 274, 10723–10730.PubMedGoogle Scholar
  75. 75.
    Voisey, J., and Van Daal, A. (2002) Pigment Cell Res., 15, 10–18.PubMedGoogle Scholar
  76. 76.
    Swope, V. B., Jameson, J. A., McFarland, K. L., Supp, D. M., Miller, W. E., McGraw, D. W., Patel, M. A., Nix, M. A., Millhauser, G. L., Babcock, G. F., and Abdel-Malek, Z. A. (2012) J. Invest. Dermatol., 132, 2255–2262.PubMedGoogle Scholar
  77. 77.
    Murphy, J. R., Bishai, W., Borowski, M., Miyanohara, A., Boyd, J., and Nagle, S. (1986) Proc. Natl. Acad. Sci. USA, 83, 8258–8262.PubMedGoogle Scholar
  78. 78.
    Wen, Z. L., Tao, X., Lakkis, F., Kiyokawa, T., and Murphy, J. R. (1991) J. Biol. Chem., 266, 12289–12293.PubMedGoogle Scholar
  79. 79.
    Ghanem, G. E., Libert, A., Arnould, R., Vercammen, A., and Lejeune, F. (1991) Melanoma Res., 1, 105–114.PubMedGoogle Scholar
  80. 80.
    Lejeune, F. J., and Ghanem, G. E. (1993) Ann. N. Y. Acad. Sci., 680, 391–400.PubMedGoogle Scholar
  81. 81.
    O’Hare, K. B., Duncan, R., Strohalm, J., Ulbrich, K., and Kopeckova, P. (1993) J. Drug Target, 1, 217–229.PubMedGoogle Scholar
  82. 82.
    Ogawa, Y., Kawahara, H., Yagi, N., Kodaka, M., Tomohiro, T., Okada, T., Konakahara, T., and Okuno, H. (1999) Lipids, 34, 387–394.PubMedGoogle Scholar
  83. 83.
    Chan, C. K., and Jans, D. A. (2001) Gene Ther., 8, 166–171.PubMedGoogle Scholar
  84. 84.
    Rosenkranz, A. A., Lunin, V. G., Gulak, P. V., Sergienko, O. V., Shumiantseva, M. A., Voronina, O. L., Gilyazova, D. G., John, A. P., Kofner, A. A., Mironov, A. F., Jans, D. A., and Sobolev, A. S. (2003) FASEB J., 17, 1121–1123.PubMedGoogle Scholar
  85. 85.
    Rosenkranz, A. A., Lunin, V. G., Sergienko, O. V., Giliazova, D. G., Voronina, O. L., Ians, D. E., Kofner, A. A., Shumiantseva, M. A., Mironov, A. F., and Sobolev, A. S. (2003) Genetika, 39, 259–268.Google Scholar
  86. 86.
    Slastnikova, T. A., Rosenkranz, A. A., Gulak, P. V., Schiffelers, R. M., Lupanova, T. N., Khramtsov, Y. V., Zalutsky, M. R., and Sobolev, A. S. (2012) Int. J. Nanomed., 7, 467–482.Google Scholar
  87. 87.
    Slastnikova, T. A., Rosenkranz, A. A., Lupanova, T. N., Gulak, P. V., Gnuchev, N. V., and Sobolev, A. S. (2012) Dokl. Biochem. Biophys., 446, 235–237.PubMedGoogle Scholar
  88. 88.
    Zhang, X., Oulad-Abdelghani, M., Zelkin, A. N., Wang, Y., Haikel, Y., Mainard, D., Voegel, J. C., Caruso, F., and Benkirane-Jessel, N. (2010) Biomaterials, 31, 1699–1706.PubMedGoogle Scholar
  89. 89.
    Vannucci, L., Falvo, E., Fornara, M., Di Micco, P., Benada, O., Krizan, J., Svoboda, J., Hulikova-Capkova, K., Morea, V., Boffi, A., and Ceci, P. (2012) Int. J. Nanomed., 7, 1489–1509.Google Scholar
  90. 90.
    Kameyama, K., Montague, P. M., and Hearing, V. J. (1988) J. Cell Physiol., 137, 35–44.PubMedGoogle Scholar
  91. 91.
    Siegrist, W., Solca, F., Stutz, S., Giuffre, L., Carrel, S., Girard, J., and Eberle, A. N. (1989) Cancer Res., 49, 6352–6358.PubMedGoogle Scholar
  92. 92.
    Miao, Y., Whitener, D., Feng, W., Owen, N. K., Chen, J., and Quinn, T. P. (2003) Bioconj. Chem., 14, 1177–1184.Google Scholar
  93. 93.
    Sobolev, A. S. (2009) Biochemistry (Moscow), 74, 1567–1574.Google Scholar
  94. 94.
    Sobolev, A. S. (2008) Bioessays, 30, 278–287.PubMedGoogle Scholar
  95. 95.
    Lu, W., Xiong, C., Zhang, R., Shi, L., Huang, M., Zhang, G., Song, S., Huang, Q., Liu, G. Y., and Li, C. (2012) J. Control Release, 161, 959–966.PubMedGoogle Scholar
  96. 96.
    Abdel-Malek, Z. A. (2010) Adv. Exp. Med. Biol., 681, 126–132.PubMedGoogle Scholar
  97. 97.
    Eberle, A. N., Bapst, J. P., Calame, M., Tanner, H., and Froidevaux, S. (2010) Adv. Exp. Med. Biol., 681, 133–142.PubMedGoogle Scholar
  98. 98.
    Graham, M. M., and Menda, Y. (2011) J. Nucl. Med., 52, 56S–63S.PubMedGoogle Scholar
  99. 99.
    Quinn, T., Zhang, X., and Miao, Y. (2010) G. Ital. Dermatol. Venereol., 145, 245–258.PubMedGoogle Scholar
  100. 100.
    Haskell-Luevano, C., Nikiforovich, G., Sharma, S. D., Yang, Y. K., Dickinson, C., Hruby, V. J., and Gantz, I. (1997) J. Med. Chem., 40, 1738–1748.PubMedGoogle Scholar
  101. 101.
    Chen, J., Cheng, Z., Miao, Y., Jurisson, S. S., and Quinn, T. P. (2002) Cancer, 94, 1196–1201.PubMedGoogle Scholar
  102. 102.
    Chen, J., Cheng, Z., Owen, N. K., Hoffman, T. J., Miao, Y., Jurisson, S. S., and Quinn, T. P. (2001) J. Nucl. Med., 42, 1847–1855.PubMedGoogle Scholar
  103. 103.
    Cheng, Z., Chen, J., Miao, Y., Owen, N. K., Quinn, T. P., and Jurisson, S. S. (2002) J. Med. Chem., 45, 3048–3056.PubMedGoogle Scholar
  104. 104.
    Guo, H., Yang, J., Gallazzi, F., Prossnitz, E. R., Sklar, L. A., and Miao, Y. (2009) Bioconj. Chem., 20, 2162–2168.Google Scholar
  105. 105.
    Guo, H., Yang, J., Gallazzi, F., and Miao, Y. (2011) J. Nucl. Med., 52, 608–616.PubMedGoogle Scholar
  106. 106.
    Guo, H., Shenoy, N., Gershman, B. M., Yang, J., Sklar, L. A., and Miao, Y. (2009) Nucl. Med. Biol., 36, 267–276.PubMedGoogle Scholar
  107. 107.
    Guo, H., Yang, J., Gallazzi, F., and Miao, Y. (2010) J. Nucl. Med., 51, 418–426.PubMedGoogle Scholar
  108. 108.
    Miao, Y., Gallazzi, F., Guo, H., and Quinn, T. P. (2008) Bioconj. Chem., 19, 539–547.Google Scholar
  109. 109.
    Miao, Y., Benwell, K., and Quinn, T. P. (2007) J. Nucl. Med., 48, 73–80.PubMedGoogle Scholar
  110. 110.
    Wei, L., Zhang, X., Gallazzi, F., Miao, Y., Jin, X., Brechbiel, M. W., Xu, H., Clifford, T., Welch, M. J., Lewis, J. S., and Quinn, T. P. (2009) Nucl. Med. Biol., 36, 345–354.PubMedGoogle Scholar
  111. 111.
    Yang, J., Guo, H., Gallazzi, F., Berwick, M., Padilla, R. S., and Miao, Y. (2009) Bioconj. Chem., 20, 1634–1642.Google Scholar
  112. 112.
    Yang, J., Guo, H., Padilla, R. S., Berwick, M., and Miao, Y. (2010) Bioorg. Med. Chem., 18, 6695–6700.PubMedGoogle Scholar
  113. 113.
    Yang, J., and Miao, Y. (2012) Bioorg. Med. Chem. Lett., 22, 1541–1545.PubMedGoogle Scholar
  114. 114.
    Raposinho, P. D., Correia, J. D., Alves, S., Botelho, M. F., Santos, A. C., and Santos, I. (2008) Nucl. Med. Biol., 35, 91–99.PubMedGoogle Scholar
  115. 115.
    Morais, M., Oliveira, B. L., Correia, J. D., Oliveira, M. C., Jimenez, M. A., Santos, I., and Raposinho, P. D. (2013) J. Med. Chem., 56, 1961–1973.PubMedGoogle Scholar
  116. 116.
    Guo, H., Yang, J., Shenoy, N., and Miao, Y. (2009) Bioconj. Chem., 20, 2356–2363.Google Scholar
  117. 117.
    Vaidyanathan, G., and Zalutsky, M. R. (1997) Nucl. Med. Biol., 24, 171–178.PubMedGoogle Scholar
  118. 118.
    Cheng, Z., Zhang, L., Graves, E., Xiong, Z., Dandekar, M., Chen, X., and Gambhir, S. S. (2007) J. Nucl. Med., 48, 987–994.PubMedGoogle Scholar
  119. 119.
    Ren, G., Liu, Z., Miao, Z., Liu, H., Subbarayan, M., Chin, F. T., Zhang, L., Gambhir, S. S., and Cheng, Z. (2009) J. Nucl. Med., 50, 1865–1872.PubMedGoogle Scholar
  120. 120.
    Cantorias, M. V., Figueroa, S. D., Quinn, T. P., Lever, J. R., Hoffman, T. J., Watkinson, L. D., Carmack, T. L., and Cutler, C. S. (2009) Nucl. Med. Biol., 36, 505–513.PubMedGoogle Scholar
  121. 121.
    Martin, M. E., Sue, O. M., Leverich, W. M., Kloepping, K. C., Walsh, S. A., and Schultz, M. K. (2013) Recent Results Cancer Res., 194, 149–175.PubMedGoogle Scholar
  122. 122.
    McQuade, P., Miao, Y., Yoo, J., Quinn, T. P., Welch, M. J., and Lewis, J. S. (2005) J. Med. Chem., 48, 2985–2992.PubMedGoogle Scholar
  123. 123.
    Wei, L., Butcher, C., Miao, Y., Gallazzi, F., Quinn, T. P., Welch, M. J., and Lewis, J. S. (2007) J. Nucl. Med., 48, 64–72.PubMedGoogle Scholar
  124. 124.
    Durymanov, M. O., Slastnikova, T. A., Kuzmich, A. I., Kramtsov, Yu. V., Ulasov, A. V., Rosenkranz, A. A., Egorov, S. V., Sverdlov, E. D., and Sobolev, A. S. (2013) Biomaterials; DOI: 10.1016/j.biomaterials.2013.08.076.Google Scholar
  125. 125.
    Miao, Y., Owen, N. K., Fisher, D. R., Hoffman, T. J., and Quinn, T. P. (2005) J. Nucl. Med., 46, 121–129.PubMedGoogle Scholar
  126. 126.
    Miao, Y., Hylarides, M., Fisher, D. R., Shelton, T., Moore, H., Wester, D. W., Fritzberg, A. R., Winkelmann, C. T., Hoffman, T., and Quinn, T. P. (2005) Clin. Cancer Res., 11, 5616–5621.PubMedGoogle Scholar
  127. 127.
    Miao, Y., Shelton, T., and Quinn, T. P. (2007) Cancer Biother. Radiopharm., 22, 333–341.PubMedGoogle Scholar
  128. 128.
    Durymanov, M. O., Beletkaia, E. A., Ulasov, A. V., Khramtsov, Y. V., Trusov, G. A., Rodichenko, N. S., Slastnikova, T. A., Vinogradova, T. V., Uspenskaya, N. Y., Kopantsev, E. P., Rosenkranz, A. A., Sverdlov, E. D., and Sobolev, A. S. (2012) J. Control Release, 163, 211–219.PubMedGoogle Scholar
  129. 129.
    Szardenings, M., Muceniece, R., Mutule, I., Mutulis, F., and Wikberg, J. E. (2000) Peptides, 21, 239–243.PubMedGoogle Scholar
  130. 130.
    Slastnikova, T. A., Koumarianou, E., Rosenkranz, A. A., Vaidyanathan, G., Lupanova, T. N., Sobolev, A. S., and Zalutsky, M. R. (2012) EJNMMI Res., 2, 59.PubMedGoogle Scholar
  131. 131.
    Szardenings, M., Tornroth, S., Mutulis, F., Muceniece, R., Keinanen, K., Kuusinen, A., and Wikberg, J. E. (1997) J. Biol. Chem., 272, 27943–27948.PubMedGoogle Scholar
  132. 132.
    Haskell-Luevano, C., Hendrata, S., North, C., Sawyer, T. K., Hadley, M. E., Hruby, V. J., Dickinson, C., and Gantz, I. (1997) J. Med. Chem., 40, 2133–2139.PubMedGoogle Scholar
  133. 133.
    Weeden, T., Stefano, J., Duan, S., Edling, A., Hou, L., Chuang, W. L., Perricone, M. A., Pan, C., and Dzuris, J. L. (2011) J. Pept. Sci., 17, 47–55.PubMedGoogle Scholar
  134. 134.
    Barkey, N. M., Tafreshi, N. K., Josan, J. S., De Silva, C. R., Sill, K. N., Hruby, V. J., Gillies, R. J., Morse, D. L., and Vagner, J. (2011) J. Med. Chem., 54, 8078–8084.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  • A. A. Rosenkranz
    • 1
    • 2
    • 3
  • T. A. Slastnikova
    • 1
  • M. O. Durymanov
    • 1
    • 2
  • A. S. Sobolev
    • 1
    • 2
    • 3
  1. 1.Institute of Gene BiologyRussian Academy of SciencesMoscowRussia
  2. 2.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia
  3. 3.Targeted Delivery of Pharmaceuticals “Translek” LLCMoscowRussia

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