Abstract
Nonviral vectors such as complexes of plasmid DNA with cationic lipids known as lipoplexes are considered as an attractive alternative to virus-based delivery systems. Unlike viruses, lipoplexes do not suffer from immunological and mutational hazards, though the efficiency of lipoplexes is often not sufficient for therapeutic purposes and require higher level of transfection than achieved until now. A number of critical steps responsible for transfection efficiency are discussed here. They include processes of lipoplexes formation, interaction with cell surface, their internalization into cell, and DNA release and delivery into the nucleus. All these processes should be thoroughly studied to be able to enhance the transfection efficacy.
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Friedmann, T., and Roblin, R. (1972) Science, 175, 949–955.
Peng, Z., Yu, Q., and Bao, L. (2008) IDrugs, 11, 346–350.
Guan, Y. S., Liu, Y., Zhou, X. P., Li, X., He, Q., and Sun, L. (2006) Gut, 55, 1684.
Peng, Z. (2005) Hum. Gene Ther., 16, 1016–1027.
Wilson, J. M. (2005) Hum. Gene Ther., 16, 1014–1015.
Chada, S., Menander, K. B., Bocangel, D., Roth, J. A., and Ramesh, R. (2008) Front. Biosci., 13, 1959–1967.
Krimsky, S. (2005) Genewatch., 18, 10–13.
Nemunaitis, J. M., and Nemunaitis, J. (2008) Future Oncol., 4, 759–768.
Kaiser, J. (2007) Science, 317, 580.
Check, E. (2005) Nature, 433, 561.
Li, Z., Dullmann, J., Schiedlmeier, B., Schmidt, M., von Kalle, C., Meyer, J., Forster, M., Stocking, C., Wahlers, A., Frank, O., Ostertag, W., Kuhlcke, K., Eckert, H. G., Fehse, B., and Baum, C. (2002) Science, 296, 497.
Marshall, E. (2002) Science, 298, 34–35.
Schroder, A. R., Shinn, P., Chen, H., Berry, C., Ecker, J. R., and Bushman, F. (2002) Cell, 110, 521–529.
Woods, N. B., Muessig, A., Schmidt, M., Flygare, J., Olsson, K., Salmon, P., Trono, D., von Kalle, C., and Karlsson, S. (2003) Blood, 101, 1284–1289.
Ferber, D. (2001) Science, 294, 1638–1642.
Karmali, P. P., and Chaudhuri, A. (2007) Med. Res. Rev., 27, 696–722.
Nguyen, L. T., Atobe, K., Barichello, J. M., Ishida, T., and Kiwada, H. (2007) Biol. Pharm. Bull., 30, 751–757.
Felgner, P. L., Gadek, T. R., Holm, M., Roman, R., Chan, H. W., Wenz, M., Northrop, J. P., Ringold, G. M., and Danielsen, M. (1987) Proc. Natl. Acad. Sci. USA, 84, 7413–7417.
Felgner, P. L., and Ringold, G. M. (1989) Nature, 337, 387–388.
Edelstein, M. L., Abedi, M. R., and Wixon, J. (2007) J. Gene Med., 9, 833–842.
Alexander, B. L., Ali, R. R., Alton, E. W., Bainbridge, J. W., Braun, S., Cheng, S. H., Flotte, T. R., Gaspar, H. B., Grez, M., Griesenbach, U., Kaplitt, M. G., Ott, M. G., Seger, R., Simons, M., Thrasher, A. J., Thrasher, A. Z., and Yla-Herttuala, S. (2007) Gene Ther., 14, 1439–1447.
Aiuti, A., Bachoud-Levi, A. C., Blesch, A., Brenner, M. K., Cattaneo, F., Chiocca, E. A., Gao, G., High, K. A., Leen, A. M., Lemoine, N. R., McNeish, I. A., Meneguzzi, G., Peschanski, M., Roncarolo, M. G., Strayer, D. S., Tuszynski, M. H., Waxman, D. J., and Wilson, J. M. (2007) Gene Ther., 14, 1555–1563.
Willard, H. F. (2000) Science, 290, 1308–1309.
Blow, N. (2007) Nature, 450, 1117–1120.
Szoka, F. (2008) Science, 319, 578–579.
Urnov, F. D., Miller, J. C., Lee, Y. L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D., and Holmes, M. C. (2005) Nature, 435, 646–651.
Kaiser, J. (2005) Science, 310, 1894–1896.
Torchilin, V. P. (2005) Nat. Rev. Drug Discov., 4, 145–160.
Zuhorn, I. S., Engberts, J. B., and Hoekstra, D. (2007) Eur. Biophys. J., 36, 349–362.
Moghimi, S. M., Hunter, A. C., and Murray, J. C. (2005) FASEB J., 19, 311–330.
Curiel, D. T., Agarwal, S., Wagner, E., and Cotten, M. (1991) Proc. Natl. Acad. Sci. USA, 88, 8850–8854.
Graham, F. L., and van der Eb, A. J. (1973) Virology, 52, 456–467.
Bally, M. B., Harvie, P., Wong, F. M., Kong, S., Wasan, E. K., and Reimer, D. L. (1999) Adv. Drug Deliv. Rev., 38, 291–315.
De Smedt, S. C., Remaut, K., Lucas, B., Braeckmans, K., Sanders, N. N., and Demeester, J. (2005) Adv. Drug Deliv. Rev., 57, 191–210.
Roth, C. M. (2005) Biophys. J., 89, 2286–2295.
Ruponen, M., Honkakoski, P., Ronkko, S., Pelkonen, J., Tammi, M., and Urtti, A. (2003) J. Control Release, 93, 213–217.
Suh, J., Dawson, M., and Hanes, J. (2005) Adv. Drug Deliv. Rev., 57, 63–78.
Wiethoff, C. M., Gill, M. L., Koe, G. S., Koe, J. G., and Middaugh, C. R. (2002) J. Biol. Chem., 277, 44980–44987.
Zabner, J., Fasbender, A. J., Moninger, T., Poellinger, K. A., and Welsh, M. J. (1995) J. Biol. Chem., 270, 18997–19007.
Katsel, P. L., O’Connell, B., Mizuno, T. M., Mobbs, C. V., and Greenstein, R. J. (2000) Int. J. Surg. Invest., 1, 415–429.
Montana, G., Bondi, M. L., Carrotta, R., Picone, P., Craparo, E. F., San Biagio, P. L., Giammona, G., and di Carlo, M. (2007) Bioconj. Chem., 18, 302–308.
Pan, X., Guan, J., Yoo, J. W., Epstein, A. J., Lee, L. J., and Lee, R. J. (2008) Int. J. Pharm., 358, 263–270.
Asasutjarit, R., Lorenzen, S. I., Sirivichayakul, S., Ruxrungtham, K., Ruktanonchai, U., and Ritthidej, G. C. (2007) Pharm. Res., 24, 1098–1107.
Takashima, Y., Saito, R., Nakajima, A., Oda, M., Kimura, A., Kanazawa, T., and Okada, H. (2007) Int. J. Pharm., 343, 262–269.
Basarkar, A., Devineni, D., Palaniappan, R., and Singh, J. (2007) Int. J. Pharm., 343, 247–254.
Zhang, Y., Zhang, Y., Chen, J., Zhang, B., Pan, Y., Ren, L., Zhao, J., Luo, Y., Zhai, D., Wang, S., and Wang, J. (2007) Nanomedicine, 3, 144–153.
MacDonald, R. C., Rakhmanova, V. A., Choi, K. L., Rosenzweig, H. S., and Lahiri, M. K. (1999) J. Pharm. Sci., 88, 896–904.
MacDonald, R. C., Ashley, G. W., Shida, M. M., Rakhmanova, V. A., Tarahovsky, Y. S., Pantazatos, D. P., Kennedy, M. T., Pozharski, E. V., Baker, K. A., Jones, R. D., Rosenzweig, H. S., Choi, K. L., Qiu, R., and McIntosh, T. J. (1999) Biophys. J., 77, 2612–2629.
Gao, X., and Huang, L. (1991) Biochem. Biophys. Res. Commun., 179, 280–285.
Farhood, H., Bottega, R., Epand, R. M., and Huang, L. (1992) Biochim. Biophys. Acta, 1111, 239–246.
Nakanishi, M. (2003) Curr. Med. Chem., 10, 1289–1296.
Ewert, K. K., Evans, H. M., Zidovska, A., Bouxsein, N. F., Ahmad, A., and Safinya, C. R. (2006) J. Am. Chem. Soc., 128, 3998–4006.
Audouy, S., and Hoekstra, D. (2001) Mol. Membr. Biol., 18, 129–143.
Chesnoy, S., and Huang, L. (2000) Annu. Rev. Biophys. Biomol. Struct., 29, 27–47.
Katsel, P. L., and Greenstein, R. J. (2000) Biotechnol. Annu. Rev., 5, 197–220.
Maslov, M. A., Syicheva, E. V., Morozova, N. G., and Serebrennikova, G. A. (2000) Russ. Chem. Bull., 49, 385–401.
Niculescu-Duvaz, D., Heyes, J., and Springer, C. J. (2003) Curr. Med. Chem., 10, 1233–1261.
Cherstvy, A. G. (2007) J. Phys. Chem. B, 111, 7914–7927.
Pantazatos, S. P., and MacDonald, R. C. (2003) J. Membr. Biol., 191, 99–112.
Kennedy, M. T., Pozharski, E. V., Rakhmanova, V. A., and MacDonald, R. C. (2000) Biophys. J., 78, 1620–1633.
Rakhmanova, V. A., Pozharski, E. V., and MacDonald, R. C. (2004) J. Membr. Biol., 200, 35–45.
Wasan, E. K., Harvie, P., Edwards, K., Karlsson, G., and Bally, M. B. (1999) Biochim. Biophys. Acta, 1461, 27–46.
Clausen-Schaumann, H., and Gaub, H. E. (1999) Langmuir, 15, 8246–8251.
Huebner, S., Battersby, B. J., Grimm, R., and Cevc, G. (1999) Biophys. J., 76, 3158–3166.
Fang, Y., and Yang, J. (1997) J. Phys. Chem. B, 101, 441–449.
Radler, J. O., Koltover, I., Salditt, T., and Safinya, C. R. (1997) Science, 275, 810–814.
Ewert, K., Slack, N. L., Ahmad, A., Evans, H. M., Lin, A. J., Samuel, C. E., and Safinya, C. R. (2004) Curr. Med. Chem., 11, 133–149.
Lin, A. J., Slack, N. L., Ahmad, A., Koltover, I., George, C. X., Samuel, C. E., and Safinya, C. R. (2000) J. Drug Target, 8, 13–27.
Safinya, C. R. (2001) Curr. Opin. Struct. Biol., 11, 440–448.
Koltover, I., Salditt, T., Radler, J. O., and Safinya, C. R. (1998) Science, 281, 78–81.
Schmutz, M., Durand, D., Debin, A., Palvadeau, Y., Etienne, A., and Thierry, A. R. (1999) Proc. Natl. Acad. Sci. USA, 96, 12293–12298.
Safinya, C. R., Ewert, K., Ahmad, A., Evans, H. M., Raviv, U., Needleman, D. J., Lin, A. J., Slack, N. L., George, C., and Samuel, C. E. (2006) Philos. Transact. A Math. Phys. Eng. Sci., 364, 2573–2596.
Battersby, B. J., Grimm, R., Huebner, S., and Cevc, G. (1998) Biochim. Biophys. Acta, 1372, 379–383.
Gustafsson, J., Arvidson, G., Karlsson, G., and Almgren, M. (1995) Biochim. Biophys. Acta, 1235, 305–312.
Barreleiro, P. C., May, R. P., and Lindman, B. (2002) Faraday Discuss., 122, 191–201.
Oberle, V., Bakowsky, U., Zuhorn, I. S., and Hoekstra, D. (2000) Biophys. J., 79, 1447–1454.
Pozharski, E. V., and MacDonald, R. C. (2007) Mol. Pharm., 4, 962–974.
Tarahovsky, Y. S., Khusainova, R. S., Gorelov, A. V., Nicolaeva, T. I., Deev, A. A., Dawson, A. K., and Ivanitsky, G. R. (1996) FEBS Lett., 390, 133–136.
Sternberg, B., Sorgi, F. L., and Huang, L. (1994) FEBS Lett., 356, 361–366.
Sternberg, B., Hong, K., Zheng, W., and Papahadjopoulos, D. (1998) Biochim. Biophys. Acta, 1375, 23–35.
Ewert, K., Evans, H. M., Ahmad, A., Slack, N. L., Lin, A. J., Martin-Herranz, A., and Safinya, C. R. (2005) Adv. Genet., 53, 119–155.
Feitosa, E., Barreleiro, P. C., and Olofsson, G. (2000) Chem. Phys. Lipids, 105, 201–213.
Barreleiro, P. C., Olofsson, G., and Alexandridis, P. (2000) J. Phys. Chem. B, 104, 7795–7802.
Zantl, R., Baicu, L., Artzner, F., Sprenger, I., Rapp, G., and Radler, J. O. (1999) J. Phys. Chem. B, 103, 10300–10310.
Lobo, B. A., Rogers, S. A., Choosakoonkriang, S., Smith, J. G., Koe, G., and Middaugh, C. R. (2002) J. Pharm. Sci., 91, 454–466.
Tarahovsky, Y. S., Rakhmanova, V. A., Epand, R. M., and MacDonald, R. C. (2002) Biophys. J., 82, 264–273.
Simberg, D., Danino, D., Talmon, Y., Minsky, A., Ferrari, M. E., Wheeler, C. J., and Barenholz, Y. (2001) J. Biol. Chem., 276, 47453–47459.
Zuhorn, I. S., Oberle, V., Visser, W. H., Engberts, J. B., Bakowsky, U., Polushkin, E., and Hoekstra, D. (2002) Biophys. J., 83, 2096–2108.
Hafez, I. M., Maurer, N., and Cullis, P. R. (2001) Gene Ther., 8, 1188–1196.
Hafez, I. M., and Cullis, P. R. (2001) Adv. Drug Deliv. Rev., 47, 139–148.
Lin, A. J., Slack, N. L., Ahmad, A., George, C. X., Samuel, C. E., and Safinya, C. R. (2003) Biophys. J., 84, 3307–3316.
Congiu, A., Pozzi, D., Esposito, C., Castellano, C., and Mossa, G. (2004) Colloids Surf. B. Biointerfaces, 36, 43–48.
Rakhmanova, V. A., McIntosh, T. J., and MacDonald, R. C. (2000) Cell. Mol. Biol. Lett., 5, 51–65.
Koynova, R., and MacDonald, R. C. (2003) Biophys. J., 85, 2449–2465.
Wang, L., and MacDonald, R. C. (2004) Gene Ther., 11, 1358–1362.
Wang, L., and MacDonald, R. C. (2007) Mol. Pharm., 4, 615–623.
Koynova, R., Wang, L., and MacDonald, R. C. (2007) J. Phys. Chem. B, 111, 7786–7795.
Koynova, R., Wang, L., and MacDonald, R. C. (2006) Proc. Natl. Acad. Sci. USA, 103, 14373–14378.
Koynova, R., Tarahovsky, Y. S., Wang, L., and MacDonald, R. C. (2007) Biochim. Biophys. Acta, 1768, 375–386.
Tenchov, B. G., Wang, L., Koynova, R., and MacDonald, R. C. (2008) Biochim. Biophys. Acta, 1778, 2405–2412.
Koynova, R., Wang, L., and MacDonald, R. C. (2008) Mol. Pharm., 5, 739–744.
Tarahovsky, Y. S., Koynova, R., and MacDonald, R. C. (2004) Biophys. J., 87, 1054–1064.
Mislick, K. A., and Baldeschwieler, J. D. (1996) Proc. Natl. Acad. Sci. USA, 93, 12349–12354.
Arnberg, N., Kidd, A. H., Edlund, K., Nilsson, J., Pring-Akerblom, P., and Wadell, G. (2002) Virology, 302, 33–43.
Pankov, R., Markovska, T., Antonov, P., Ivanova, L., and Momchilova, A. (2006) Chem. Biol. Interact., 164, 167–173.
Pires, P., Simoes, S., Nir, S., Gaspar, R., Duzgunes, N., and Pedroso de Lima, M. C. (1999) Biochim. Biophys. Acta, 1418, 71–84.
Saito, Y., Kawakami, S., Yabe, Y., Yamashita, F., and Hashida, M. (2006) Biol. Pharm. Bull., 29, 1986–1990.
Pelisek, J., Gaedtke, L., DeRouchey, J., Walker, G. F., Nikol, S., and Wagner, E. (2006) J. Gene Med., 8, 186–197.
Ross, P. C., and Hui, S. W. (1999) Gene Ther., 6, 651–659.
Rejman, J., Oberle, V., Zuhorn, I. S., and Hoekstra, D. (2004) Biochem. J., 377, 159–169.
Kawaura, C., Noguchi, A., Furuno, T., and Nakanishi, M. (1998) FEBS Lett., 421, 69–72.
Nakanishi, M., and Noguchi, A. (2001) Adv. Drug Deliv. Rev., 52, 197–207.
Trubetskoy, V. S., Wong, S. C., Subbotin, V., Budker, V. G., Loomis, A., Hagstrom, J. E., and Wolff, J. A. (2003) Gene Ther., 10, 261–271.
Simberg, D., Weisman, S., Talmon, Y., and Barenholz, Y. (2004) Crit. Rev. Ther. Drug Carrier Syst., 21, 257–317.
Wrobel, I., and Collins, D. (1995) Biochim. Biophys. Acta, 1235, 296–304.
Friend, D. S., Papahadjopoulos, D., and Debs, R. J. (1996) Biochim. Biophys. Acta, 1278, 41–50.
Briane, D., Lesage, D., Cao, A., Coudert, R., Lievre, N., Salzmann, J. L., and Taillandier, E. (2002) J. Histochem. Cytochem., 50, 983–991.
Cao, A., Briane, D., Coudert, R., Vassy, J., Lievre, N., Olsman, E., Tamboise, E., Salzmann, J. L., Rigaut, J. P., and Taillandier, E. (2000) Antisense Nucleic Acid Drug Dev., 10, 369–380.
Tamaddon, A. M., Shirazi, F. H., and Moghimi, H. R. (2007) Int. J. Pharm., 336, 174–182.
Thurston, G., McLean, J. W., Rizen, M., Baluk, P., Haskell, A., Murphy, T. J., Hanahan, D., and McDonald, D. M. (1998) J. Clin. Invest., 101, 1401–1413.
Holmen, S. L., Vanbrocklin, M. W., Eversole, R. R., Stapleton, S. R., and Ginsberg, L. C. (1995) In vitro Cell Dev. Biol. Anim., 31, 347–351.
Colin, M., Maurice, M., Trugnan, G., Kornprobst, M., Harbottle, R. P., Knight, A., Cooper, R. G., Miller, A. D., Capeau, J., Coutelle, C., and Brahimi-Horn, M. C. (2000) Gene Ther., 7, 139–152.
El Ouahabi, A., Thiry, M., Schiffmann, S., Fuks, R., Nguyen-Tran, H., Ruysschaert, J. M., and Vandenbranden, M. (1999) J. Histochem. Cytochem., 47, 1159–1166.
Hasegawa, S., Hirashima, N., and Nakanishi, M. (2001) Gene Ther., 8, 1669–1673.
Ondrej, V., Lukasova, E., Falk, M., and Kozubek, S. (2007) Acta Biochim. Pol., 54, 657–663.
Rejman, J., Bragonzi, A., and Conese, M. (2005) Mol. Ther., 12, 468–474.
Rejman, J., Conese, M., and Hoekstra, D. (2006) J. Liposome Res., 16, 237–247.
Colin, M., Maurice, M., Trugnan, G., Kornprobst, M., Harbottle, R. P., Knight, A., Cooper, R. G., Miller, A. D., Capeau, J., Coutelle, C., and Brahimi-Horn, M. C. (2000) Gene Ther., 7, 139–152.
Huth, U., Wieschollek, A., Garini, Y., Schubert, R., and Peschka-Suss, R. (2004) Cytometry A, 57, 10–21.
Sakurai, F., Inoue, R., Nishino, Y., Okuda, A., Matsumoto, O., Taga, T., Yamashita, F., Takakura, Y., and Hashida, M. (2000) J. Control Release, 66, 255–269.
Zuhorn, I. S., Kalicharan, R., and Hoekstra, D. (2002) J. Biol. Chem., 277, 18021–18028.
Tate, M. W., Eikenberry, E. F., Turner, D. C., Shyamsunder, E., and Gruner, S. M. (1991) Chem. Phys. Lipids, 57, 147–164.
Watson, P., Jones, A. T., and Stephens, D. J. (2005) Adv. Drug Deliv. Rev., 57, 43–61.
Wang, L., and MacDonald, R. C. (2004) Mol. Ther., 9, 729–737.
Chebotareva, N. A. (2007) Biochemistry (Moscow), 72, 1478–1490.
Ellis, R. J. (2007) Adv. Exp. Med. Biol., 594, 1–13.
Lukacs, G. L., Haggie, P., Seksek, O., Lechardeur, D., Freedman, N., and Verkman, A. S. (2000) J. Biol. Chem., 275, 1625–1629.
Hirashima, N., Minatani, K., Hattori, Y., Ohwada, T., and Nakanishi, M. (2007) Biol. Pharm. Bull., 30, 1117–1122.
Zhou, X., and Huang, L. (1994) Biochim. Biophys. Acta, 1189, 195–203.
Cheng, J., Zeidan, R., Mishra, S., Liu, A., Pun, S. H., Kulkarni, R. P., Jensen, G. S., Bellocq, N. C., and Davis, M. E. (2006) J. Med. Chem., 49, 6522–6531.
Ciftci, K., and Levy, R. J. (2001) Int. J. Pharm., 218, 81–92.
Legendre, J. Y., and Szoka, F. C., Jr. (1992) Pharm. Res., 9, 1235–1242.
Akinc, A., Thomas, M., Klibanov, A. M., and Langer, R. (2005) J. Gene Med., 7, 657–663.
Pan, H., Zheng, Q., Guo, X., Liu, Y., Li, C., and Song, Y. (2006) J. Huazhong. Univ. Sci. Technol. Med. Sci., 26, 513–516.
Hafez, I. M., Ansell, S., and Cullis, P. R. (2000) Biophys. J., 79, 1438–1446.
Hafez, I. M., and Cullis, P. R. (2004) Meth. Enzymol., 387, 113–134.
Bhattacharya, S., and Mandal, S. S. (1998) Biochemistry, 37, 7764–7777.
Xu, Y., and Szoka, F. C., Jr. (1996) Biochemistry, 35, 5616–5623.
Kinnunen, P. K., Rytomaa, M., Koiv, A., Lehtonen, J., Mustonen, P., and Aro, A. (1993) Chem. Phys. Lipids, 66, 75–85.
Israelachvili, J. N., Marcelja, S., and Horn, R. G. (1980) Q. Rev. Biophys., 13, 121–200.
Israelachvili, J. N., Mitchell, D. J., and Ninham, B. W. (1977) Biochim. Biophys. Acta, 470, 185–201.
Israelachvili, J. N., and Mitchell, D. J. (1975) Biochim. Biophys. Acta, 389, 13–19.
Tate, M. W., Eikenberry, E. F., Turner, D. C., Shyamsunder, E., and Gruner, S. M. (1991) Chem. Phys. Lipids, 57, 147–164.
Gruner, S. M. (1985) Proc. Natl. Acad. Sci. USA, 82, 3665–3669.
Epand, R. M. (2007) Meth. Mol. Biol., 400, 15–26.
De Kruijff, B. (1997) Curr. Opin. Chem. Biol., 1, 564–569.
Cooke, I. R., and Deserno, M. (2006) Biophys. J., 91, 487–495.
Tarahovsky, Y. S., Arsenault, A. L., MacDonald, R. C., McIntosh, T. J., and Epand, R. M. (2000) Biophys. J., 79, 3193–3200.
Lewis, R. N., and McElhaney, R. N. (2000) Biophys. J., 79, 1455–1464.
Cevc, G., and Richardsen, H. (1999) Adv. Drug Deliv. Rev., 38, 207–232.
Marrink, S. J., and Tieleman, D. P. (2002) Biophys. J., 83, 2386–2392.
Marrink, S. J., and Mark, A. E. (2004) Biophys. J., 87, 3894–3900.
Siegel, D. P. (1999) Biophys. J., 76, 291–313.
Yang, L., Ding, L., and Huang, H. W. (2003) Biochemistry, 42, 6631–6635.
Stegmann, T., and Legendre, J. Y. (1997) Biochim. Biophys. Acta, 1325, 71–79.
Harvie, P., Wong, F. M., and Bally, M. B. (1998) Biophys. J., 75, 1040–1051.
Scherman, D., Bessodes, M., Cameron, B., Herscovici, J., Hofland, H., Pitard, B., Soubrier, F., Wils, P., and Crouzet, J. (1998) Curr. Opin. Biotechnol., 9, 480–485.
Inoh, Y., Kitamoto, D., Hirashima, N., and Nakanishi, M. (2004) J. Control Release, 94, 423–431.
Almofti, M. R., Harashima, H., Shinohara, Y., Almofti, A., Baba, Y., and Kiwada, H. (2003) Arch. Biochem. Biophys., 410, 246–253.
Stebelska, K., Wyrozumska, P., Gubernator, J., and Sikorski, A. F. (2007) Cell Mol. Biol. Lett., 12, 39–50.
Colin, M., Maurice, M., Trugnan, G., Kornprobst, M., Harbottle, R. P., Knight, A., Cooper, R. G., Miller, A. D., Capeau, J., Coutelle, C., and Brahimi-Horn, M. C. (2000) Gene Ther., 7, 139–152.
Farago, O., Ewert, K., Ahmad, A., Evans, H. M., Gronbech-Jensen, N., and Safinya, C. R. (2008) Biophys. J., 95, 836–846.
Ahmad, A., Evans, H. M., Ewert, K., George, C. X., Samuel, C. E., and Safinya, C. R. (2005) J. Gene Med., 7, 739–748.
Noguchi, A., Furuno, T., Kawaura, C., and Nakanishi, M. (1998) FEBS Lett., 433, 169–173.
Altman, P. L., and Katz, D. D. (1976) in Cell Biology, Federal American Society for Experimental Biologists, Bethesda, Maryland.
Lesage, D., Cao, A., Briane, D., Lievre, N., Coudert, R., Raphael, M., Salzmann, J., and Taillandier, E. (2002) Biochim. Biophys. Acta, 1564, 393–402.
Brunner, S., Furtbauer, E., Sauer, T., Kursa, M., and Wagner, E. (2002) Mol. Ther., 5, 80–86.
Brunner, S., Sauer, T., Carotta, S., Cotten, M., Saltik, M., and Wagner, E. (2000) Gene Ther., 7, 401–407.
Tseng, W. C., Haselton, F. R., and Giorgio, T. D. (1999) Biochim. Biophys. Acta, 1445, 53–64.
Mortimer, I., Tam, P., MacLachlan, I., Graham, R. W., Saravolac, E. G., and Joshi, P. B. (1999) Gene Ther., 6, 403–411.
Kamiya, H., Fujimura, Y., Matsuoka, I., and Harashima, H. (2002) Biochem. Biophys. Res. Commun., 298, 591–597.
Bergen, J. M., and Pun, S. H. (2008) J. Gene Med., 10, 187–197.
Dowty, M. E., Williams, P., Zhang, G., Hagstrom, J. E., and Wolff, J. A. (1995) Proc. Natl. Acad. Sci. USA, 92, 4572–4576.
Pollard, H., Remy, J. S., Loussouarn, G., Demolombe, S., Behr, J. P., and Escande, D. (1998) J. Biol. Chem., 273, 7507–7511.
Escriou, V., Carriere, M., Bussone, F., Wils, P., and Scherman, D. (2001) J. Gene Med., 3, 179–187.
Lechardeur, D., Sohn, K. J., Haardt, M., Joshi, P. B., Monck, M., Graham, R. W., Beatty, B., Squire, J., O’Brodovich, H., and Lukacs, G. L. (1999) Gene Ther., 6, 482–497.
Rolland, A. (2006) Expert. Opin. Drug Deliv., 3, 1–10.
Doye, V., and Hurt, E. (1997) Curr. Opin. Cell Biol., 9, 401–411.
Wente, S. R. (2000) Science, 288, 1374–1377.
Stoffler, D., Feja, B., Fahrenkrog, B., Walz, J., Typke, D., and Aebi, U. (2003) J. Mol. Biol., 328, 119–130.
Pante, N., and Kann, M. (2002) Mol. Biol. Cell, 13, 425–434.
Ludtke, J. J., Zhang, G., Sebestyen, M. G., and Wolff, J. A. (1999) J. Cell Sci., 112, 2033–2041.
Hartmann, L., Hafele, S., Peschka-Suss, R., Antonietti, M., and Borner, H. G. (2008) Chemistry, 14, 2025–2033.
Lambert, O., Letellier, L., Gelbart, W. M., and Rigaud, J. L. (2000) Proc. Natl. Acad. Sci. USA, 97, 7248–7253.
Zuber, G., Zammut-Italiano, L., Dauty, E., and Behr, J. P. (2003) Angew. Chem. Int. Ed. Engl., 42, 2666–2669.
Chauhan, A., Tikoo, A., Kapur, A. K., and Singh, M. (2007) J. Control Release, 117, 148–162.
Kim, K., Han, J. S., Kim, H. A., and Lee, M. (2008) Biotechnol. Lett., 30, 1331–1337.
Torchilin, V. P. (2008) Adv. Drug Deliv. Rev., 60, 548–558.
Chan, C. K., and Jans, D. A. (2002) Immunol. Cell Biol., 80, 119–130.
Hebert, E. (2003) Biol. Cell, 95, 59–68.
Liu, G., Li, D., Pasumarthy, M. K., Kowalczyk, T. H., Gedeon, C. R., Hyatt, S. L., Payne, J. M., Miller, T. J., Brunovskis, P., Fink, T. L., Muhammad, O., Moen, R. C., Hanson, R. W., and Cooper, M. J. (2003) J. Biol. Chem., 278, 32578–32586.
Belting, M., Sandgren, S., and Wittrup, A. (2005) Adv. Drug Deliv. Rev., 57, 505–527.
Salman, H., Abu-Arish, A., Oliel, S., Loyter, A., Klafter, J., Granek, R., and Elbaum, M. (2005) Biophys. J., 89, 2134–2145.
Gump, J. M., and Dowdy, S. F. (2007) Trends Mol. Med., 13, 443–448.
Lo, S. L., and Wang, S. (2008) Biomaterials, 29, 2408–2414.
Meyer, M., Zintchenko, A., Ogris, M., and Wagner, E. (2007) J. Gene Med., 9, 797–805.
Boeckle, S., Wagner, E., and Ogris, M. (2005) J. Gene Med., 7, 1335–1347.
Prongidi-Fix, L., Sugawara, M., Bertani, P., Raya, J., Leborgne, C., Kichler, A., and Bechinger, B. (2007) Biochemistry, 46, 11253–11262.
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Published in Russian in Biokhimiya, 2009, Vol. 74, No. 12, pp. 1589–1602.
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Tarahovsky, Y.S. Cell transfection by DNA-lipid complexes — Lipoplexes. Biochemistry Moscow 74, 1293–1304 (2009). https://doi.org/10.1134/S0006297909120013
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DOI: https://doi.org/10.1134/S0006297909120013