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“Smart” liposomal nanocontainers in biology and medicine

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Abstract

The perspectives of using liposomes for delivery of drugs to desired parts of the human body have been intensively investigated for more than 30 years. During this time many inventions have been suggested and different kinds of liposomal devices developed, and a number of them have reached the stages of preclinical or clinical trials. The latest techniques can be used to develop biocompatible nano-sized liposomal containers having some abilities of artificial intellect, such as the presence of sensory and responsive units. However, only a few have been clinically approved. Further improvements in this area depend on our knowledge of the interactions of drugs with the lipid bilayer of liposomes. Further studies on liposomal transport through the human body, their targeting of cells requiring therapeutic treatment, and finally, the development of techniques for controlled drug delivery to desired acceptors on cell surfaces or in cytoplasm are still required.

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Abbreviations

CHEMS:

cholesteryl hemisuccinate

DOPE:

dioleoyl phosphatidylethanolamine

DPPC:

dipalmitoyl phosphatidylcholine

DSPC:

distearoyl phosphatidylcholine

EPR:

enhanced permeability and retention

FR:

folate receptor

HePC:

hexadecyl phosphocholine

IR:

infrared light

OA:

oleic acid

PA:

phosphatidic acid

PC:

phosphatidylcholine

PE:

phosphatidylethanolamine

PEG:

polyethyleneglycol

PS:

phosphatidylserine

RES:

reticuloendothelial system

RFC:

reduced folate carrier

UV:

ultraviolet light

References

  1. Dass, C. R. (2008) Meth. Mol. Biol., 437, 177–182.

    Article  CAS  Google Scholar 

  2. Huwyler, J., Drewe, J., and Krahenbuhl, S. (2008) Int. J. Nanomed., 3, 21–29.

    Article  CAS  Google Scholar 

  3. Schiffelers, R. M., and Storm, G. (2008) Int. J. Pharm., 364, 258–264.

    Article  CAS  PubMed  Google Scholar 

  4. Torchilin, V. P. (2006) Annu. Rev. Biomed. Eng., 8, 343–375.

    Article  CAS  PubMed  Google Scholar 

  5. Hermida, R. C., Fernandez, J. R., Ayala, D. E., Mojon, A., Alonso, I., and Smolensky, M. (2001) Chronobiol. Int., 18, 475–489.

    Article  CAS  PubMed  Google Scholar 

  6. Gref, R., Minamitake, Y., Peracchia, M. T., Trubetskoy, V., Torchilin, V., and Langer, R. (1994) Science, 263, 1600–1603.

    Article  CAS  PubMed  Google Scholar 

  7. Frank, M. M., and Fries, L. F. (1991) Immunol. Today, 12, 322–326.

    Article  CAS  PubMed  Google Scholar 

  8. Kaul, G., and Amiji, M. (2002) Pharm. Res., 19, 1061–1067.

    Article  CAS  PubMed  Google Scholar 

  9. Dumortier, G., Grossiord, J. L., Agnely, F., and Chaumeil, J. C. (2006) Pharm. Res., 23, 2709–2728.

    Article  CAS  PubMed  Google Scholar 

  10. Gabizon, A., Shmeeda, H., Horowitz, A. T., and Zalipsky, S. (2004) Adv. Drug Deliv. Rev., 56, 1177–1192.

    Article  CAS  PubMed  Google Scholar 

  11. Illum, L., Davis, S. S., Muller, R. H., Mak, E., and West, P. (1987) Life Sci., 40, 367–374.

    Article  CAS  PubMed  Google Scholar 

  12. Nishiyama, N., and Kataoka, K. (2003) Adv. Exp. Med. Biol., 519, 155–177.

    Article  CAS  PubMed  Google Scholar 

  13. Parveen, S., and Sahoo, S. K. (2006) Clin. Pharmacokinet., 45, 965–988.

    Article  CAS  PubMed  Google Scholar 

  14. Redhead, H. M., Davis, S. S., and Illum, L. (2001) J. Control Release, 70, 353–363.

    Article  CAS  PubMed  Google Scholar 

  15. Sharpe, M., Easthope, S. E., Keating, G. M., and Lamb, H. M. (2002) Drugs, 62, 2089–2126.

    Article  CAS  PubMed  Google Scholar 

  16. Torchilin, V. P. (2002) Adv. Drug Deliv. Rev., 54, 235–252.

    Article  CAS  PubMed  Google Scholar 

  17. Zhang, W., Liu, J., Li, S., Chen, M., and Liu, H. (2008) J. Microencapsul., 25, 203–209.

    Article  CAS  PubMed  Google Scholar 

  18. Owens, D. E., III, and Peppas, N. A. (2006) Int. J. Pharm., 307, 93–102.

    Article  CAS  PubMed  Google Scholar 

  19. Awasthi, V. D., Garcia, D., Goins, B. A., and Phillips, W. T. (2003) Int. J. Pharm., 253, 121–132.

    Article  CAS  PubMed  Google Scholar 

  20. Prencipe, G., Tabakman, S. M., Welsher, K., Liu, Z., Goodwin, A. P., Zhang, L., Henry, J., and Dai, H. (2009) J. Am. Chem. Soc., 131, 4783–4787.

    Article  CAS  PubMed  Google Scholar 

  21. Shi, B., Fang, C., and Pei, Y. (2006) J. Pharm. Sci., 95, 1873–1887.

    Article  CAS  PubMed  Google Scholar 

  22. Allen, T. M., Mumbengegwi, D. R., and Charrois, G. J. (2005) Clin. Cancer Res., 11, 3567–3573.

    Article  CAS  PubMed  Google Scholar 

  23. Allen, T. M. (1994) Trends Pharmacol. Sci., 15, 215–220.

    Article  CAS  PubMed  Google Scholar 

  24. Lasic, D. D. (1996) Nature, 380, 561–562.

    Article  CAS  PubMed  Google Scholar 

  25. Gill, P. S., Espina, B. M., Muggia, F., Cabriales, S., Tulpule, A., Esplin, J. A., Liebman, H. A., Forssen, E., Ross, M. E., and Levine, A. M. (1995) J. Clin. Oncol., 13, 996–1003.

    CAS  PubMed  Google Scholar 

  26. Charrois, G. J., and Allen, T. M. (2003) Biochim. Biophys. Acta, 1609, 102–108.

    Article  CAS  PubMed  Google Scholar 

  27. Nagayasu, A., Uchiyama, K., and Kiwada, H. (1999) Adv. Drug Deliv. Rev., 40, 75–87.

    Article  CAS  PubMed  Google Scholar 

  28. Ishida, O., Maruyama, K., Sasaki, K., and Iwatsuru, M. (1999) Int. J. Pharm., 190, 49–56.

    Article  CAS  PubMed  Google Scholar 

  29. Lukyanov, A. N., Hartner, W. C., and Torchilin, V. P. (2004) J. Control Release, 94, 187–193.

    Article  CAS  PubMed  Google Scholar 

  30. Li, S. D., and Huang, L. (2008) Mol. Pharm., 5, 496–504.

    Article  CAS  PubMed  Google Scholar 

  31. Brannon-Peppas, L., and Blanchette, J. O. (2004) Adv. Drug Deliv. Rev., 56, 1649–1659.

    Article  CAS  PubMed  Google Scholar 

  32. Mayer, L. D., Nayar, R., Thies, R. L., Boman, N. L., Cullis, P. R., and Bally, M. B. (1993) Cancer Chemother. Pharmacol., 33, 17–24.

    Article  CAS  PubMed  Google Scholar 

  33. Zou, Y., Ling, Y. H., Reddy, S., Priebe, W., and Perez-Soler, R. (1995) Int. J. Cancer, 61, 666–671.

    Article  CAS  PubMed  Google Scholar 

  34. Allen, T. M., Hansen, C., Martin, F., Redemann, C., and Yau-Young, A. (1991) Biochim. Biophys. Acta, 1066, 29–36.

    Article  CAS  PubMed  Google Scholar 

  35. Klibanov, A. L., Maruyama, K., Beckerleg, A. M., Torchilin, V. P., and Huang, L. (1991) Biochim. Biophys. Acta, 1062, 142–148.

    Article  CAS  PubMed  Google Scholar 

  36. Litzinger, D. C., and Huang, L. (1992) Biochim. Biophys. Acta, 1113, 201–227.

    CAS  PubMed  Google Scholar 

  37. Litzinger, D. C., Buiting, A. M., van Rooijen, N., and Huang, L. (1994) Biochim. Biophys. Acta, 1190, 99–107.

    Article  CAS  PubMed  Google Scholar 

  38. Maruyama, K., Yuda, T., Okamoto, A., Kojima, S., Suginaka, A., and Iwatsuru, M. (1992) Biochim. Biophys. Acta, 1128, 44–49.

    CAS  PubMed  Google Scholar 

  39. Allen, T. M., Cheng, W. W., Hare, J. I., and Laginha, K. M. (2006) Anticancer Agents Med. Chem., 6, 513–523.

    Article  CAS  PubMed  Google Scholar 

  40. Ojugo, A. S., McSheehy, P. M., McIntyre, D. J., McCoy, C., Stubbs, M., Leach, M. O., Judson, I. R., and Griffiths, J. R. (1999) NMR Biomed., 12, 495–504.

    Article  CAS  PubMed  Google Scholar 

  41. Stubbs, M., McSheehy, P. M., Griffiths, J. R., and Bashford, C. L. (2000) Mol. Med. Today, 6, 15–19.

    Article  CAS  PubMed  Google Scholar 

  42. Bergstrand, N., Arfvidsson, M. C., Kim, J. M., Thompson, D. H., and Edwards, K. (2003) Biophys. Chem., 104, 361–379.

    Article  CAS  PubMed  Google Scholar 

  43. Connor, J., and Huang, L. (1986) Cancer Res., 46, 3431–3435.

    CAS  PubMed  Google Scholar 

  44. Duzgunes, N., Straubinger, R. M., Baldwin, P. A., Friend, D. S., and Papahadjopoulos, D. (1985) Biochemistry, 24, 3091–3098.

    Article  CAS  PubMed  Google Scholar 

  45. Straubinger, R. M., Duzgunes, N., and Papahadjopoulos, D. (1985) FEBS Lett., 179, 148–154.

    Article  CAS  PubMed  Google Scholar 

  46. Collins, D., Litzinger, D. C., and Huang, L. (1990) Biochim. Biophys. Acta, 1025, 234–242.

    Article  CAS  PubMed  Google Scholar 

  47. De Oliveira, M. C., Rosilio, V., Lesieur, P., Bourgaux, C., Couvreur, P., Ollivon, M., and Dubernet, C. (2000) Biophys. Chem., 87, 127–137.

    Article  PubMed  Google Scholar 

  48. Drummond, D. C., and Daleke, D. L. (1995) Chem. Phys. Lipids, 75, 27–41.

    Article  CAS  PubMed  Google Scholar 

  49. Hong, M. S., Lim, S. J., Oh, Y. K., and Kim, C. K. (2002) J. Pharm. Pharmacol., 54, 51–58.

    Article  CAS  PubMed  Google Scholar 

  50. Kim, M. J., Lee, H. J., Lee, I. A., Kim, I. Y., Lim, S. K., Cho, H. A., and Kim, J. S. (2008) Arch. Pharm. Res., 31, 539–546.

    Article  CAS  PubMed  Google Scholar 

  51. Liu, D., and Huang, L. (1990) Biochim. Biophys. Acta, 1022, 348–354.

    Article  CAS  PubMed  Google Scholar 

  52. Mignet, N., Richard, C., Seguin, J., Largeau, C., Bessodes, M., and Scherman, D. (2008) Int. J. Pharm., 361, 194–201.

    Article  CAS  PubMed  Google Scholar 

  53. Reddy, J. A., and Low, P. S. (2000) J. Control Release, 64, 27–37.

    Article  CAS  PubMed  Google Scholar 

  54. Tari, A. M., Fuller, N., Boni, L. T., Collins, D., Rand, P., and Huang, L. (1994) Biochim. Biophys. Acta, 1192, 253–262.

    Article  CAS  PubMed  Google Scholar 

  55. Drummond, D. C., Zignani, M., and Leroux, J. (2000) Prog. Lipid Res., 39, 409–460.

    Article  CAS  PubMed  Google Scholar 

  56. Turk, M. J., Reddy, J. A., Chmielewski, J. A., and Low, P. S. (2002) Biochim. Biophys. Acta, 1559, 56–68.

    Article  CAS  PubMed  Google Scholar 

  57. Leroux, J., Roux, E., Le Garrec, D., Hong, K., and Drummond, D. C. (2001) J. Control Release, 72, 71–84.

    Article  CAS  PubMed  Google Scholar 

  58. Mizoue, T., Horibe, T., Maruyama, K., Takizawa, T., Iwatsuru, M., Kono, K., Yanagie, H., and Moriyasu, F. (2002) Int. J. Pharm., 237, 129–137.

    Article  CAS  PubMed  Google Scholar 

  59. Roux, E., Francis, M., Winnik, F. M., and Leroux, J. C. (2002) Int. J. Pharm., 242, 25–36.

    Article  CAS  PubMed  Google Scholar 

  60. Yatvin, M. B., Weinstein, J. N., Dennis, W. H., and Blumenthal, R. (1978) Science, 202, 1290–1293.

    Article  CAS  PubMed  Google Scholar 

  61. Mabrey, S., and Sturtevant, J. M. (1976) Proc. Natl. Acad. Sci. USA, 73, 3862–3866.

    Article  CAS  PubMed  Google Scholar 

  62. Mills, J. K., and Needham, D. (2005) Biochim. Biophys. Acta, 1716, 77–96.

    Article  CAS  PubMed  Google Scholar 

  63. Lindner, L. H., Eichhorn, M. E., Eibl, H., Teichert, N., Schmitt-Sody, M., Issels, R. D., and Dellian, M. (2004) Clin. Cancer Res., 10, 2168–2178.

    Article  CAS  PubMed  Google Scholar 

  64. Lindner, L. H., Hossann, M., Vogeser, M., Teichert, N., Wachholz, K., Eibl, H., Hiddemann, W., and Issels, R. D. (2008) J. Control Release, 125, 112–120.

    Article  CAS  PubMed  Google Scholar 

  65. Sundar, S., Jha, T. K., Thakur, C. P., Engel, J., Sindermann, H., Fischer, C., Junge, K., Bryceson, A., and Berman, J. (2002) N. Engl. J. Med., 347, 1739–1746.

    Article  CAS  PubMed  Google Scholar 

  66. Leonard, R., Hardy, J., van Tienhoven, G., Houston, S., Simmonds, P., David, M., and Mansi, J. (2001) J. Clin. Oncol., 19, 4150–4159.

    CAS  PubMed  Google Scholar 

  67. Collini, P., Premchand, N., Lockwood, D., and Greig, J. (2009) Ann. Trop. Med. Parasitol., 103, 455–459.

    Article  CAS  PubMed  Google Scholar 

  68. Papagiannaros, A., Hatziantoniou, S., Lelong-Rebel, I. H., Papaioannou, G. T., Dimas, K., and Demetzos, C. (2006) In vivo, 20, 129–135.

    CAS  PubMed  Google Scholar 

  69. Papagiannaros, A., Hatziantoniou, S., Dimas, K., Papaioannou, G. T., and Demetzos, C. (2006) Biomed. Pharmacother., 60, 36–42.

    Article  CAS  PubMed  Google Scholar 

  70. Lohmann, D., and Petrak, K. (1989) Crit Rev. Ther. Drug Carrier Syst., 5, 263–320.

    CAS  PubMed  Google Scholar 

  71. Alvarez-Lorenzo, C., and Concheiro, A. (2008) Mini. Rev. Med. Chem., 8, 1065–1074.

    Article  CAS  PubMed  Google Scholar 

  72. Alvarez-Lorenzo, C., Bromberg, L., and Concheiro, A. (2009) Photochem. Photobiol., 85, 848–860.

    Article  CAS  PubMed  Google Scholar 

  73. Mochizuki-Oda, N., Kataoka, Y., Cui, Y., Yamada, H., Heya, M., and Awazu, K. (2002) Neurosci. Lett., 323, 207–210.

    Article  CAS  PubMed  Google Scholar 

  74. Li, Z., Zhang, M., Zhang, X., Dai, S., Yu, X., and Wang, Y. (2009) Eur. J. Appl. Physiol., 107, 281–287.

    Article  CAS  PubMed  Google Scholar 

  75. Hogset, A., Prasmickaite, L., Selbo, P. K., Hellum, M., Engesaeter, B. O., Bonsted, A., and Berg, K. (2004) Adv. Drug Deliv. Rev., 56, 95–115.

    Article  CAS  PubMed  Google Scholar 

  76. Prasmickaite, L., Hogset, A., Engesaeter, B. B., Bonsted, A., and Berg, K. (2004) Expert. Opin. Biol. Ther., 4, 1403–1412.

    Article  CAS  PubMed  Google Scholar 

  77. Shieh, M. J., Peng, C. L., Lou, P. J., Chiu, C. H., Tsai, T. Y., Hsu, C. Y., Yeh, C. Y., and Lai, P. S. (2008) J. Control Release, 129, 200–206.

    Article  CAS  PubMed  Google Scholar 

  78. Mojzisova, H., Bonneau, S., Maillard, P., Berg, K., and Brault, D. (2009) Photochem. Photobiol. Sci., 8, 778–787.

    Article  CAS  PubMed  Google Scholar 

  79. Thompson, D. H., Gerasimov, O. V., Wheeler, J. J., Rui, Y., and Anderson, V. C. (1996) Biochim. Biophys. Acta, 1279, 25–34.

    Article  PubMed  Google Scholar 

  80. Nishiyama, N., Arnida, Jang, W. D., Date, K., Miyata, K., and Kataoka, K. (2006) J. Drug Target, 14, 413–424.

    Article  CAS  PubMed  Google Scholar 

  81. Nishiyama, N., Morimoto, Y., Jang, W. D., and Kataoka, K. (2009) Adv. Drug Deliv. Rev., 61, 327–338.

    Article  CAS  PubMed  Google Scholar 

  82. Henderson, B. W., and Dougherty, T. J. (1992) Photochem. Photobiol., 55, 145–157.

    Article  CAS  PubMed  Google Scholar 

  83. Moan, J., and Juzenas, P. (2006) J. Environ. Pathol. Toxicol. Oncol., 25, 29–50.

    PubMed  Google Scholar 

  84. Tarr, M., and Valenzeno, D. P. (2003) Photochem. Photobiol. Sci., 2, 355–361.

    Article  CAS  PubMed  Google Scholar 

  85. Moan, J., and Berg, K. (1991) Photochem. Photobiol., 53, 549–553.

    Article  CAS  PubMed  Google Scholar 

  86. Bondurant, B., Mueller, A., and O’Brien, D. F. (2001) Biochim. Biophys. Acta, 1511, 113–122.

    Article  CAS  PubMed  Google Scholar 

  87. Spratt, T., Bondurant, B., and O’Brien, D. F. (2003) Biochim. Biophys. Acta, 1611, 35–43.

    Article  CAS  PubMed  Google Scholar 

  88. Zhao, Y. (2007) Chem. Rec., 7, 286–294.

    Article  CAS  PubMed  Google Scholar 

  89. Zhao, Y. (2009) J. Mater. Chem., 19, 4887–4895.

    Article  CAS  Google Scholar 

  90. Bisby, R. H., Mead, C., and Morgan, C. G. (2000) Biochem. Biophys. Res. Commun., 276, 169–173.

    Article  CAS  PubMed  Google Scholar 

  91. Yagai, S., Karatsu, T., and Kitamura, A. (2005) Chemistry, 11, 4054–4063.

    Article  CAS  PubMed  Google Scholar 

  92. Bisby, R. H., Mead, C., and Morgan, C. G. (2000) Photochem. Photobiol., 72, 57–61.

    Article  CAS  PubMed  Google Scholar 

  93. Bisby, R. H., Mead, C., Mitchell, A. C., and Morgan, C. G. (1999) Biochem. Biophys. Res. Commun., 262, 406–410.

    Article  CAS  PubMed  Google Scholar 

  94. Liu, X. M., Yang, B., Wang, Y. L., and Wang, J. Y. (2005) Biochim. Biophys. Acta, 1720, 28–34.

    Article  CAS  PubMed  Google Scholar 

  95. Ishii, K., Hamada, T., Hatakeyama, M., Sugimoto, R., Nagasaki, T., and Takagi, M. (2009) Chembiochem., 10, 251–256.

    Article  CAS  PubMed  Google Scholar 

  96. Hamada, T., Sato, Y. T., Yoshikawa, K., and Nagasaki, T. (2005) Langmuir, 21, 7626–7628.

    Article  CAS  PubMed  Google Scholar 

  97. Huang, S. L. (2008) Adv. Drug Deliv. Rev., 60, 1167–1176.

    Article  CAS  PubMed  Google Scholar 

  98. O’Brien, W. D., Jr. (2007) Prog. Biophys. Mol. Biol., 93, 212–255.

    Article  PubMed  Google Scholar 

  99. Unger, E. C., Zutshi, R., Matsunaga, T. O., and Ramaswami, R. (2006) in Nanoparticulates as Drug Carriers (Torchilin, V., ed.) Imperial College Press, London, pp. 225–254.

    Chapter  Google Scholar 

  100. Church, C. C. (2002) Ultrasound Med. Biol., 28, 1349–1364.

    Article  PubMed  Google Scholar 

  101. Yang, X., and Church, C. C. (2005) J. Acoust. Soc. Am., 118, 3595–3606.

    Article  PubMed  Google Scholar 

  102. Miller, A. P., and Nanda, N. C. (2004) Ultrasound Med. Biol., 30, 425–434.

    Article  PubMed  Google Scholar 

  103. Dijkmans, P. A., Juffermans, L. J., Musters, R. J., van Wamel, A., ten Cate, F. J., van Gilst, W., Visser, C. A., de Jong, N., and Kamp, O. (2004) Eur. J. Echocardiogr., 5, 245–256.

    Article  CAS  PubMed  Google Scholar 

  104. Unger, E. C., Porter, T., Culp, W., Labell, R., Matsunaga, T., and Zutshi, R. (2004) Adv. Drug Deliv. Rev., 56, 1291–1314.

    Article  CAS  PubMed  Google Scholar 

  105. Lindner, J. R., Song, J., Xu, F., Klibanov, A. L., Singbartl, K., Ley, K., and Kaul, S. (2000) Circulation, 102, 2745–2750.

    CAS  PubMed  Google Scholar 

  106. Lindner, J. R., Dayton, P. A., Coggins, M. P., Ley, K., Song, J., Ferrara, K., and Kaul, S. (2000) Circulation, 102, 531–538.

    CAS  PubMed  Google Scholar 

  107. Lindner, J. R., Song, J., Christiansen, J., Klibanov, A. L., Xu, F., and Ley, K. (2001) Circulation, 104, 2107–2112.

    Article  CAS  PubMed  Google Scholar 

  108. Naito, Y., Ito, M., Watanabe, T., and Suzuki, H. (2005) Digestion, 72, 164–180.

    Article  PubMed  Google Scholar 

  109. Willmann, J. K., Cheng, Z., Davis, C., Lutz, A. M., Schipper, M. L., Nielsen, C. H., and Gambhir, S. S. (2008) Radiology, 249, 212–219.

    Article  PubMed  Google Scholar 

  110. Willmann, J. K., Paulmurugan, R., Chen, K., Gheysens, O., Rodriguez-Porcel, M., Lutz, A. M., Chen, I. Y., Chen, X., and Gambhir, S. S. (2008) Radiology, 246, 508–518.

    Article  PubMed  Google Scholar 

  111. Korpanty, G., Chen, S., Shohet, R. V., Ding, J., Yang, B., Frenkel, P. A., and Grayburn, P. A. (2005) Gene Ther., 12, 1305–1312.

    Article  CAS  PubMed  Google Scholar 

  112. Weller, G. E., Wong, M. K., Modzelewski, R. A., Lu, E., Klibanov, A. L., Wagner, W. R., and Villanueva, F. S. (2005) Cancer Res., 65, 533–539.

    CAS  PubMed  Google Scholar 

  113. Andonian, S., Coulthard, T., Smith, A. D., Singhal, P. S., and Lee, B. R. (2009) J. Endourol., 23, 373–378.

    Article  PubMed  Google Scholar 

  114. Fatar, M., Stroick, M., Griebe, M., Alonso, A., Kreisel, S., Kern, R., Hennerici, M., and Meairs, S. (2008) Ultrasound Med. Biol., 34, 1414–1420.

    Article  CAS  PubMed  Google Scholar 

  115. Jing, X. X., Wang, Z. G., Ran, H. T., Li, L., Wu, X., Li, X. D., Peng, X. Q., Yang, C. J., Li, X. S., and Zhang, Q. X. (2008) Clin. Imaging, 32, 178–182.

    Article  PubMed  Google Scholar 

  116. Title, L. M., Iles, S. E., Gardner, M. J., Penney, C. J., Clements, J. C., and Horacek, B. M. (2003) J. Electrocardiol., 36, 17–26.

    Article  PubMed  Google Scholar 

  117. Kee, P. H., Abruzzo, T. A., Smith, D. A., Kopechek, J. A., Wang, B., Huang, S. L., MacDonald, R. C., Holland, C. K., and McPherson, D. D. (2008) J. Liposome Res., 18, 263–277.

    Article  CAS  PubMed  Google Scholar 

  118. Hernot, S., and Klibanov, A. L. (2008) Adv. Drug Deliv. Rev., 60, 1153–1166.

    Article  CAS  PubMed  Google Scholar 

  119. Bull, J. L. (2007) Expert. Opin. Drug Deliv., 4, 475–493.

    Article  CAS  PubMed  Google Scholar 

  120. Kheirolomoom, A., Dayton, P. A., Lum, A. F., Little, E., Paoli, E. E., Zheng, H., and Ferrara, K. W. (2007) J. Control Release, 118, 275–284.

    Article  CAS  PubMed  Google Scholar 

  121. Liu, Y., Miyoshi, H., and Nakamura, M. (2006) J. Control Release, 114, 89–99.

    Article  CAS  PubMed  Google Scholar 

  122. Korpanty, G., Carbon, J. G., Grayburn, P. A., Fleming, J. B., and Brekken, R. A. (2007) Clin. Cancer Res., 13, 323–330.

    Article  CAS  PubMed  Google Scholar 

  123. Imada, T., Tatsumi, T., Mori, Y., Nishiue, T., Yoshida, M., Masaki, H., Okigaki, M., Kojima, H., Nozawa, Y., Nishiwaki, Y., Nitta, N., Iwasaka, T., and Matsubara, H. (2005) Arterioscler. Thromb. Vasc. Biol., 25, 2128–2134.

    Article  CAS  PubMed  Google Scholar 

  124. Meijering, B. D., Henning, R. H., van Gilst, W. H., Gavrilovic, I., van Wamel, A., and Deelman, L. E. (2007) J. Drug Target, 15, 664–671.

    Article  CAS  PubMed  Google Scholar 

  125. Shen, Z. P., Brayman, A. A., Chen, L., and Miao, C. H. (2008) Gene Ther., 15, 1147–1155.

    Article  CAS  PubMed  Google Scholar 

  126. Hynynen, K., McDannold, N., Vykhodtseva, N., and Jolesz, F. A. (2003) Acta Neurochir. Suppl., 86, 555–558.

    CAS  PubMed  Google Scholar 

  127. Meairs, S., and Alonso, A. (2007) Prog. Biophys. Mol. Biol., 93, 354–362.

    Article  PubMed  Google Scholar 

  128. Hynynen, K., McDannold, N., Vykhodtseva, N., and Jolesz, F. A. (2001) Radiology, 220, 640–646.

    Article  CAS  PubMed  Google Scholar 

  129. Tachibana, K., and Tachibana, S. (1995) Circulation, 92, 1148–1150.

    CAS  PubMed  Google Scholar 

  130. Shaw, G. J., Meunier, J. M., Huang, S. L., Lindsell, C. J., McPherson, D. D., and Holland, C. K. (2009) Thromb. Res., 124, 306–310.

    Article  CAS  PubMed  Google Scholar 

  131. Polyak, B., and Friedman, G. (2009) Expert. Opin. Drug Deliv., 6, 53–70.

    Article  CAS  PubMed  Google Scholar 

  132. Arruebo, M., Fernandez-Pacheco, R., Ibarra, M. R., and Santamaria, J. (2007) Nanotoday, 2, 22–32.

    Google Scholar 

  133. Schenck, J. F. (2005) Prog. Biophys. Mol. Biol., 87, 185–204.

    Article  PubMed  Google Scholar 

  134. Haik, Y., Pai, V., and Chen, C. J. (2001) J. Magn. Magn. Mater., 225, 180–186.

    Article  CAS  Google Scholar 

  135. Chakeres, D. W., and de Vocht, F. (2005) Prog. Biophys. Mol. Biol., 87, 255–265.

    Article  PubMed  Google Scholar 

  136. Seiyama, A., Seki, J., Iwamoto, M., and Yanagida, T. (2005) Dyn. Med., 4, 5.

    Article  PubMed  Google Scholar 

  137. Chan, P., Eng, L. F., Lee, Y. L., and Lin, V. W. (1999) J. Neurosci. Res., 55, 238–244.

    Article  CAS  PubMed  Google Scholar 

  138. Dobson, J. (2009) Drug. Dev. Res., 67, 55–60.

    Article  CAS  Google Scholar 

  139. Iacob, G., Rotariu, O., Strachan, N. J., and Hafeli, U. O. (2004) Biorheology, 41, 599–612.

    CAS  PubMed  Google Scholar 

  140. Olsvik, O., Popovic, T., Skjerve, E., Cudjoe, K. S., Hornes, E., Ugelstad, J., and Uhlen, M. (1994) Clin. Microbiol. Rev., 7, 43–54.

    CAS  PubMed  Google Scholar 

  141. Pankhurst, Q. A., Connolly, J., Jones, S. K., and Dobson, J. (2003) J. Phys. D.: Appl. Phys., 36, R167–R181.

    Article  CAS  Google Scholar 

  142. Lubbe, A. S., Alexiou, C., and Bergemann, C. (2001) J. Surg. Res., 95, 200–206.

    Article  CAS  PubMed  Google Scholar 

  143. Kaminski, M. D., and Rosengart, A. J. (2005) J. Magn. Magn. Mater., 293, 389–403.

    Article  CAS  Google Scholar 

  144. Margolis, L. B., Namiot, V. A., and Kljukin, L. M. (1983) Biochim. Biophys. Acta, 735, 193–195.

    Article  CAS  PubMed  Google Scholar 

  145. De Cuyper, M., and Joniau, M. (1988) Eur. Biophys. J., 15, 311–319.

    Article  PubMed  Google Scholar 

  146. Soenen, S. J., Baert, J., and de Cuyper, M. (2007) Chembiochem., 8, 2067–2077.

    Article  CAS  PubMed  Google Scholar 

  147. Martina, M. S., Fortin, J. P., Menager, C., Clement, O., Barratt, G., Grabielle-Madelmont, C., Gazeau, F., Cabuil, V., and Lesieur, S. (2005) J. Am. Chem. Soc., 127, 10676–10685.

    Article  CAS  PubMed  Google Scholar 

  148. Viroonchatapan, E., Ueno, M., Sato, H., Adachi, I., Nagae, H., Tazawa, K., and Horikoshi, I. (1995) Pharm. Res., 12, 1176–1183.

    Article  CAS  PubMed  Google Scholar 

  149. Viroonchatapan, E., Sato, H., Ueno, M., Adachi, I., Murata, J., Saiki, I., Tazawa, K., and Horikoshi, I. (1998) J. Drug Target, 5, 379–390.

    Article  CAS  PubMed  Google Scholar 

  150. Viroonchatapan, E., Sato, H., Ueno, M., Adachi, I., Tazawa, K., and Horikoshi, I. (1996) Life Sci., 58, 2251–2261.

    Article  CAS  PubMed  Google Scholar 

  151. Chiu, G. N., Abraham, S. A., Ickenstein, L. M., Ng, R., Karlsson, G., Edwards, K., Wasan, E. K., and Bally, M. B. (2005) J. Control Release, 104, 271–288.

    CAS  PubMed  Google Scholar 

  152. Laurent, S., Forge, D., Port, M., Roch, A., Robic, C., Vander, E. L., and Muller, R. N. (2008) Chem. Rev., 108, 2064–2110.

    Article  CAS  PubMed  Google Scholar 

  153. Fortin, J. P., Wilhelm, C., Servais, J., Menager, C., Bacri, J. C., and Gazeau, F. (2007) J. Am. Chem. Soc., 129, 2628–2635.

    Article  CAS  PubMed  Google Scholar 

  154. Ito, A., Shinkai, M., Honda, H., and Kobayashi, T. (2005) J. Biosci. Bioeng., 100, 1–11.

    Article  CAS  PubMed  Google Scholar 

  155. Kawai, N., Ito, A., Nakahara, Y., Futakuchi, M., Shirai, T., Honda, H., Kobayashi, T., and Kohri, K. (2005) Prostate, 64, 373–381.

    Article  CAS  PubMed  Google Scholar 

  156. Gupta, A. K., and Gupta, M. (2005) Biomaterials, 26, 3995–4021.

    Article  CAS  PubMed  Google Scholar 

  157. Shinkai, M., Le, B., Honda, H., Yoshikawa, K., Shimizu, K., Saga, S., Wakabayashi, T., Yoshida, J., and Kobayashi, T. (2001) Jpn. J. Cancer Res., 92, 1138–1145.

    CAS  PubMed  Google Scholar 

  158. Zhao, X., Li, H., and Lee, R. J. (2008) Expert. Opin. Drug Deliv., 5, 309–319.

    Article  CAS  PubMed  Google Scholar 

  159. Elnakat, H., and Ratnam, M. (2004) Adv. Drug Deliv. Rev., 56, 1067–1084.

    Article  CAS  PubMed  Google Scholar 

  160. Campbell, I. G., Jones, T. A., Foulkes, W. D., and Trowsdale, J. (1991) Cancer Res., 51, 5329–5338.

    CAS  PubMed  Google Scholar 

  161. Coney, L. R., Tomassetti, A., Carayannopoulos, L., Frasca, V., Kamen, B. A., Colnaghi, M. I., and Zurawski, V. R., Jr. (1991) Cancer Res., 51, 6125–6132.

    CAS  PubMed  Google Scholar 

  162. Weitman, S. D., Lark, R. H., Coney, L. R., Fort, D. W., Frasca, V., Zurawski, V. R., Jr., and Kamen, B. A. (1992) Cancer Res., 52, 3396–3401.

    CAS  PubMed  Google Scholar 

  163. Low, P. S., Henne, W. A., and Doorneweerd, D. D. (2008) Acc. Chem. Res., 41, 120–129.

    Article  CAS  PubMed  Google Scholar 

  164. Gibbs, D. D., Theti, D. S., Wood, N., Green, M., Raynaud, F., Valenti, M., Forster, M. D., Mitchell, F., Bavetsias, V., Henderson, E., and Jackman, A. L. (2005) Cancer Res., 65, 11721–11728.

    Article  CAS  PubMed  Google Scholar 

  165. Lu, Y., and Low, P. S. (2002) Adv. Drug Deliv. Rev., 54, 675–693.

    Article  CAS  PubMed  Google Scholar 

  166. Salazar, M. D., and Ratnam, M. (2007) Cancer Metastasis Rev., 26, 141–152.

    Article  CAS  PubMed  Google Scholar 

  167. Jackman, A. L., Theti, D. S., and Gibbs, D. D. (2004) Adv. Drug Deliv. Rev., 56, 1111–1125.

    Article  CAS  PubMed  Google Scholar 

  168. Nagayoshi, R., Nakamura, M., Ijiri, K., Yoshida, H., Komiya, S., and Matsuyama, T. (2003) Clin. Exp. Rheumatol., 21, 719–725.

    CAS  PubMed  Google Scholar 

  169. Theti, D. S., Bavetsias, V., Skelton, L. A., Titley, J., Gibbs, D., Jansen, G., and Jackman, A. L. (2003) Cancer Res., 63, 3612–3618.

    CAS  PubMed  Google Scholar 

  170. Low, P. S., and Antony, A. C. (2004) Adv. Drug Deliv. Rev., 56, 1055–1058.

    Article  CAS  PubMed  Google Scholar 

  171. Kamen, B. A., and Caston, J. D. (1986) Biochem. Pharmacol., 35, 2323–2329.

    Article  CAS  PubMed  Google Scholar 

  172. Da Costa, M., and Rothenberg, S. P. (1996) Biochim. Biophys. Acta, 1292, 23–30.

    PubMed  Google Scholar 

  173. Leamon, C. P., and Low, P. S. (1993) Biochem. J., 291(Pt. 3), 855–860.

    CAS  PubMed  Google Scholar 

  174. Leamon, C. P., and Low, P. S. (1992) J. Biol. Chem., 267, 24966–24971.

    CAS  PubMed  Google Scholar 

  175. Leamon, C. P., Pastan, I., and Low, P. S. (1993) J. Biol. Chem., 268, 24847–24854.

    CAS  PubMed  Google Scholar 

  176. Turek, J. J., Leamon, C. P., and Low, P. S. (1993) J. Cell Sci., 106(Pt. 1), 423–430.

    CAS  PubMed  Google Scholar 

  177. Lee, R. J., and Low, P. S. (1994) J. Biol. Chem., 269, 3198–3204.

    CAS  PubMed  Google Scholar 

  178. Lee, R. J., and Low, P. S. (1995) Biochim. Biophys. Acta, 1233, 134–144.

    Article  PubMed  Google Scholar 

  179. Zhao, X. B., Muthusamy, N., Byrd, J. C., and Lee, R. J. (2007) J. Pharm. Sci., 96, 2424–2435.

    Article  CAS  PubMed  Google Scholar 

  180. Pan, X. Q., Wang, H., and Lee, R. J. (2003) Pharm. Res., 20, 417–422.

    Article  CAS  PubMed  Google Scholar 

  181. Lu, Y., Wu, J., Wu, J., Gonit, M., Yang, X., Lee, A., Xiang, G., Li, H., Liu, S., Marcucci, G., Ratnam, M., and Lee, R. J. (2007) Mol. Pharm., 4, 707–712.

    Article  CAS  PubMed  Google Scholar 

  182. Ni, S., Stephenson, S. M., and Lee, R. J. (2002) Anticancer Res., 22, 2131–2135.

    CAS  PubMed  Google Scholar 

  183. Pan, X. Q., and Lee, R. J. (2005) Anticancer Res., 25, 343–346.

    CAS  PubMed  Google Scholar 

  184. Sudimack, J. J., Guo, W., Tjarks, W., and Lee, R. J. (2002) Biochim. Biophys. Acta, 1564, 31–37.

    Article  CAS  PubMed  Google Scholar 

  185. Wu, J., Liu, Q., and Lee, R. J. (2006) Int. J. Pharm., 316, 148–153.

    Article  CAS  PubMed  Google Scholar 

  186. Stephenson, S. M., Yang, W., Stevens, P. J., Tjarks, W., Barth, R. F., and Lee, R. J. (2003) Anticancer Res., 23, 3341–3345.

    CAS  PubMed  Google Scholar 

  187. Sudimack, J. J., Adams, D., Rotaru, J., Shukla, S., Yan, J., Sekido, M., Barth, R. F., Tjarks, W., and Lee, R. J. (2002) Pharm. Res., 19, 1502–1508.

    Article  CAS  PubMed  Google Scholar 

  188. Stevens, P. J., Sekido, M., and Lee, R. J. (2004) Anticancer Res., 24, 161–165.

    CAS  PubMed  Google Scholar 

  189. Chiu, S. J., Marcucci, G., and Lee, R. J. (2006) Anticancer Res., 26, 1049–1056.

    CAS  PubMed  Google Scholar 

  190. Goren, D., Horowitz, A. T., Tzemach, D., Tarshish, M., Zalipsky, S., and Gabizon, A. (2000) Clin. Cancer Res., 6, 1949–1957.

    CAS  PubMed  Google Scholar 

  191. Gabizon, A., Horowitz, A. T., Goren, D., Tzemach, D., Shmeeda, H., and Zalipsky, S. (2003) Clin. Cancer Res., 9, 6551–6559.

    CAS  PubMed  Google Scholar 

  192. Sofou, S., and Sgouros, G. (2008) Expert. Opin. Drug Deliv., 5, 189–204.

    Article  CAS  PubMed  Google Scholar 

  193. Torchilin, V. (2008) Expert. Opin. Drug Deliv., 5, 1003–1025.

    Article  CAS  PubMed  Google Scholar 

  194. Gregoriadis, G., and Neerunjun, E. D. (1975) Biochem. Biophys. Res. Commun., 65, 537–544.

    Article  CAS  PubMed  Google Scholar 

  195. Leserman, L. D., Weinstein, J. N., Blumenthal, R., Sharrow, S. O., and Terry, W. D. (1979) J. Immunol., 122, 585–591.

    CAS  PubMed  Google Scholar 

  196. Hansen, C. B., Kao, G. Y., Moase, E. H., Zalipsky, S., and Allen, T. M. (1995) Biochim. Biophys. Acta, 1239, 133–144.

    Article  PubMed  Google Scholar 

  197. Allen, T. M., Brandeis, E., Hansen, C. B., Kao, G. Y., and Zalipsky, S. (1995) Biochim. Biophys. Acta, 1237, 99–108.

    Article  PubMed  Google Scholar 

  198. Sapra, P., Tyagi, P., and Allen, T. M. (2005) Curr. Drug Deliv., 2, 369–381.

    Article  CAS  PubMed  Google Scholar 

  199. Sofou, S., Kappel, B. J., Jaggi, J. S., McDevitt, M. R., Scheinberg, D. A., and Sgouros, G. (2007) Bioconj. Chem., 18, 2061–2067.

    Article  CAS  Google Scholar 

  200. Klibanov, A. L., Muzykantov, V. R., Ivanov, N. N., and Torchilin, V. P. (1985) Anal. Biochem., 150, 251–257.

    Article  CAS  PubMed  Google Scholar 

  201. Kirpotin, D. B., Drummond, D. C., Shao, Y., Shalaby, M. R., Hong, K., Nielsen, U. B., Marks, J. D., Benz, C. C., and Park, J. W. (2006) Cancer Res., 66, 6732–6740.

    Article  CAS  PubMed  Google Scholar 

  202. Mamot, C., Drummond, D. C., Noble, C. O., Kallab, V., Guo, Z., Hong, K., Kirpotin, D. B., and Park, J. W. (2005) Cancer Res., 65, 11631–11638.

    Article  CAS  PubMed  Google Scholar 

  203. Elbayoumi, T. A., and Torchilin, V. P. (2006) Pharm. Eng., 26, 96–104.

    Google Scholar 

  204. Elbayoumi, T. A., Pabba, S., Roby, A., and Torchilin, V. P. (2007) J. Liposome Res., 17, 1–14.

    Article  CAS  PubMed  Google Scholar 

  205. Elbayoumi, T. A., and Torchilin, V. P. (2009) Mol. Pharm., 6, 246–254.

    Article  CAS  PubMed  Google Scholar 

  206. Emfietzoglou, D., Kostarelos, K., Papakostas, A., Yang, W. H., Ballangrud, A., Song, H., and Sgouros, G. (2005) J. Nucl. Med., 46, 89–97.

    CAS  PubMed  Google Scholar 

  207. Erdogan, S., Roby, A., and Torchilin, V. P. (2006) Mol. Pharm., 3, 525–530.

    Article  CAS  PubMed  Google Scholar 

  208. Erdogan, S., Roby, A., Sawant, R., Hurley, J., and Torchilin, V. P. (2006) J. Liposome Res., 16, 45–55.

    Article  CAS  PubMed  Google Scholar 

  209. Kabalka, G. W., Davis, M. A., Moss, T. H., Buonocore, E., Hubner, K., Holmberg, E., Maruyama, K., and Huang, L. (1991) Magn Reson. Med., 19, 406–415.

    Article  CAS  PubMed  Google Scholar 

  210. Torchilin, V. P. (2000) Curr. Pharm. Biotechnol., 1, 183–215.

    Article  CAS  PubMed  Google Scholar 

  211. Elbayoumi, T. A., and Torchilin, V. P. (2009) Clin. Cancer Res., 15, 1973–1980.

    Article  CAS  PubMed  Google Scholar 

  212. Jonasdottir, T. J., Fisher, D. R., Borrebaek, J., Bruland, O. S., and Larsen, R. H. (2006) Anticancer Res., 26, 2841–2848.

    CAS  PubMed  Google Scholar 

  213. Sofou, S., Thomas, J. L., Lin, H. Y., McDevitt, M. R., Scheinberg, D. A., and Sgouros, G. (2004) J. Nucl. Med., 45, 253–260.

    CAS  PubMed  Google Scholar 

  214. Matsumura, Y., Gotoh, M., Muro, K., Yamada, Y., Shirao, K., Shimada, Y., Okuwa, M., Matsumoto, S., Miyata, Y., Ohkura, H., Chin, K., Baba, S., Yamao, T., Kannami, A., Takamatsu, Y., Ito, K., and Takahashi, K. (2004) Ann. Oncol., 15, 517–525.

    Article  CAS  PubMed  Google Scholar 

  215. Matsumura, Y. (2003) Adv. Exp. Med. Biol., 519, 179–193.

    CAS  PubMed  Google Scholar 

  216. Barrajon-Catalan, E., Menendez-Gutierrez, M. P., Falco, A., Carrato, A., Saceda, M., and Micol, V. (2009) Cancer Lett., 290, 192–203.

    Article  PubMed  CAS  Google Scholar 

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Published in Russian in Biokhimiya, 2010, Vol. 75, No. 7, pp. 920–935.

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Tarahovsky, Y.S. “Smart” liposomal nanocontainers in biology and medicine. Biochemistry Moscow 75, 811–824 (2010). https://doi.org/10.1134/S0006297910070023

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