Modulowanie właściwości peptydów penetrujących do komórek

• Autorzy: Lipiński W. , Kolesińska B.

Warianty tytułu

Modulating properties of the cell penetrating peptides

• Języki publikacji: PL

Abstrakty

EN

Cell penetrating peptides (CPPs) are short peptides able to efficiently cross cellular membrane. The group includes great diversity of sequences and besides capability to enter various types of cells, their characteristic feature is lack of toxicity. CPPs can be divided according to their origin (natural and synthetic) or according to their physicochemical properties responsible for the cellpenetrating ability (cationic, amphipathic and hydrophobic). Properties of CPPs are closely related to their mechanism of internalisation. Endocytic pathway is probably the dominating mechanism for majority of CPPs, but less common energyindependent internalisation (occurring via inverted micelle, carpet-like, barrel stave pore or toroidal pore model may also play a relevant part in the uptake across membranes. CPPs have been applied in transporting various compounds. They are very effective in delivering small molecules (fluorophores, drugs, peptides), macromolecules (proteins, nucleic acids) and even nanoparticles (metal nanoparticles, liposomes). Conjunction of CPP and cargo can be achieved either covalently (peptide bond, sulphide bridge etc.) or noncovalently (electrostatic or hydrophobic interaction, hydrogen bonding). Ability to unspecific enter almost any kind of cell and tissue becomes a great problem in the case of in vivo applications. Another disadvantage of CPPs is their low plasma stability. Many strategies have been suggested to overcome these issues. Selectivity can be improved by attaching targeting ligands (e.g. short peptides, antibodies, proteins, folic acid or hyaluronic acid) or by incorporating CPPs into macromolecular drug carriers, which exploit the so called enhanced permeability and retention (EPR) effect. The most recent and most sophisticated way of improving CPPs’ stability and selectivity is the synthesis of activatable cell penetrating peptides (ACPPs). The deactivating moiety may consist of anionic sequence, polymer chain or smaller protecting groups. The deactivating parts are connected to the delivery system via linker that can be cleaved under conditions characteristic for the site of action. ACPPs may be activated by enzymes, pH and oxidative potential change, temperature or radiation. CPPs may find application in tumour therapy, diagnostics and the combination of both – theranostics. Despite many successful studies in delivering drugs and tags in vivo and in vitro, CPPs have passed only few clinical trials (some are being run currently). It is sure that this research area will develop in next years

Słowa kluczowe

PL

peptydy penetrujące do komórek; CPPs; aktywowalne peptydy; przenikanie przez błony komórkowe; cargo; transport związków chemicznych do komórek; mechanizm przenikania; diagnostyka nowotworów

EN

cell penetrating peptides; CPPs; activatable cell penetrating peptides; ACPPs; cargo; transport into the cells; mechanism of penetration

• Wydawca: Polskie Towarzystwo Chemiczne
• Czasopismo: Wiadomości Chemiczne
• Rocznik: 2017
• Tom: [Z] 71, 9-10
• Strony: 695--726
• Opis fizyczny: Bibliogr. 200 poz., rys., schem., tab.

Twórcy

autor

Lipiński W.

• Instytut Chemii Organicznej Politechniki Łódzkiej, ul. Żeromskiego 116, 90-924 Łódź

autor

Kolesińska B.

• Instytut Chemii Organicznej Politechniki Łódzkiej, ul. Żeromskiego 116, 90-924 Łódź

Bibliografia

• [1] A.D. Frankel, C.O. Pablo, Cell, 1988, 55, 1189.
• [2] M. Green, P.M. Loewenstein, Cell, 1988, 55, 1179.
• [3] A. Joliot, C. Pernelle, H. Deagostini-Bazin, A. Prochiantz, Proc. Natl Acad. Sci., 1991, 88, 1864.
• [4] D. Derossi, A.H. Joliott, G. Chassaing, A. Prochiantz, J. Biol. Chem., 1994, 269, 10444.
• [5] S. Fawell, J. Seery, Y. Daikh, C. Moore, L.L. Chen, B. Pepinsky, J. Barsoum, Proc. Natl Acad. Sci., 1994, 91, 664.
• [6] E. Vives, P. Brodin, B. Lebleu, J. Biol. Chem., 1997, 272, 16010.
• [7] D. Raucher, J. Su Ryu, Trends Mol. Med., 2015, 21, 560.
• [8] D. Zhang, J. Wang, D. Xu, J. Control. Release, 2016, 229, 130.
• [9] E. Vives, J. Control. Release, 2005, 109, 77.
• [10] D.M. Copolovici, K. Langel, E. Eriste, Ü. Langel, ACS Nano, 2014, 8, 1972.
• [11] A. Chugh, F. Eudes, J. Pept. Sci., 2008, 14, 477.
• [12] S.D. Krämer, H. Wunderli-Allenspach, Biochim. Biophys. Acta, 2003, 1609, 161.
• [13] P.O. Falnes, J. Wesche, S. Olsnes, Biochemistry, 2001, 40, 4349.
• [14] A. Elmquist, M. Lindgren, T. Bartfai, Ü. Langel, Exp. Cell Res., 2001, 269, 237.
• [15] S. Galdiero, A. Falanga, M. Vitiello, H. Browne, C. Pedone, M. Galdiero, J. Biol. Chem., 2005, 31, 28632.
• [16] F. Miletti, Drug Discov. Today, 2012, 17, 850.
• [17] P.A. Wender, D.J. Mitchell, K. Pattabiraman, E.T. Pelkey, L. Steinman, J.B. Rothbard, Proc. Natl Acad. Sci., 2000, 97, 13003.
• [18] P.M. Fischer, N.Z. Zhelev, S. Wang, J.E. Melville, R. Fĺhraeus, D.P. Lane, J. Pept. Res., 2000, 55, 163.
• [19] D.J. Mitchell, D.T. Kim, L. Steinman, C.G. Fathman, J.B. Rothbard, J. Pept. Res., 2000, 56, 318.
• [20] J.B. Rothbard, E. Kreider, C.L. VanDeusen, L. Wright, B.L. Wylie, P.A. Wender, J. Med. Chem., 2002, 45, 3612.
• [21] A. Walrant, C. Bechara, I.D. Alves, S. Sagan, Nanomedicine, 2012, 7, 133.
• [22] E. Gonçalves, E. Kitas, J. Seelig, Biochemistry, 2005, 44, 2692.
• [23] J.L. Zaro, W.-C. Shen, Biochem. Biophys. Res. Commun., 2003, 307, 241.
• [24] S. Futaki, T. Suzuki, W. Ohashi, T. Yagami, S. Tanaka, K. Ueda, Y. Sugiura, J. Biol. Chem., 2001, 276, 5836.
• [25] G. Tünnemann, G. Ter-Avetisyan, R.M. Martin, M. Stöckl, A. Herrmann, M.C. Cardoso, J. Pept. Sci., 2008, 14, 469.
• [26] S.W. Jones, R. Christison, K. Bundell, C.J. Voyce, S.M.V. Brockbank, P. Newham, M.A. Lindsay, Brit. J. Pharmacol., 2005, 145, 1093.
• [27] J. Zhou, Y. Chau, Biomater. Sci., 2016, 4, 1462.
• [28] J.S. Appelbaum, Chem. Biol., 2012, 19, 819.
• [29] A. Ziegler, J. Seelig, Biochemistry, 2007, 46, 8138.
• [30] M.C. Morris, P. Vidal, L. Chaloin, F. Heitz, G. Divita, Nucleic Acids Res., 1997, 25, 2730.
• [31] E. Gros, S. Deshayes, M.C. Morris, G. Aldrian-Herrada, J. Depollier, F. Heitz, G. Divita, Biochim. Biophys. Acta, 2006, 1758, 384.
• [32] M.C. Morris, J. Depollier, J. Mery, F. Heitz, G. Divita, Nat. Biotechnol., 2001, 19, 1173.
• [33] A. Scheller, J. Oehlke, B. Wiesner, M. Dathe, E. Krause, M. Beyermann, M. Melzig, M. Bienert, J. Pept. Sci., 1999, 5, 185.
• [34] I.D. Alves, N. Goasdoué, I. Correia, S. Aubry, C. Galanth, S. Sagan, S. Lavielle, G. Chassaing, Biochim. Biophys. Acta, 2008, 1780, 948.
• [35] E. Eiríksdóttir, K. Konate, Ü. Langel, G. Divita, S. Deshayes, Biochim. Biophys. Acta, 2010, 1798, 1119.
• [36] E. Krause, M. Beyermann, H. Fabian, M. Dathe, S. Rothemund, M. Bienert, Int. J. Pept. Protein Res., 1996, 48, 559.
• [37] J. Oehlke, E. Krause, B. Wiesner, M. Beyermann, M. Bienert, FEBS Lett., 1997, 415, 196.
• [38] H.Y. Kim, S.Y. Yum, G. Jang, D.-R. Ahn, Ahn. Sci. Rep., 2015, 5, 11719.
• [39] S. Pujals, E. Giralt, Adv. Drug Deliv. Rev., 2008, 60, 473.
• [40] K. Sadler, K.D. Eom, J.L. Yang, Y. Dimitrova, J.P. Tam, Biochemistry, 2002, 41, 14150.
• [41] D.S. Daniels, A. Schepartz, J. Am. Chem. Soc., 2007, 129, 14578.
• [42] I. Martín, M. Teixidó, E. Giralt, Chembiochem., 2011, 12, 896.
• [43] M.I. Geli, M. Torrent, D. Ludevid, Plant Cell, 1994, 6, 1911.
• [44] J.R. Marks, J. Placone, K. Hristova, W.C. Wimley, J. Am. Chem. Soc., 2011, 133, 8995.
• [45] F. Nakayama, T. Yasuda, S. Umeda, M. Asada, T. Imamura, V. Meineke, M. Akashi, J. Biol. Chem., 2011, 286, 25823.
• [46] M. Rhee, P. Davis, J. Biol. Chem., 2006, 281, 1233.
• [47] K. Montrose, Y. Yang, X. Sun, S. Wiles, G. W. Krissansen, Sci. Rep., 2013, 3, 1661.
• [48] J.D. Ochocki, U. Igbavboa, W.G. Wood, E.V. Wattenberg, M.D. Distefano, Chem. Biol. Drug Des., 2010, 76, 107.
• [49] M. Mäe, S. EL Andaloussi, P. Lundin, N. Oskolkov, H.J. Johansson, P. Guterstam, Ü. Langel, J. Control. Release, 2009, 19, 221.
• [50] S. Patel, M.R. Player, Expert. Opin. Investig. Drugs, 2008, 17, 1865.
• [51] J.R. LaRochelle, G.B. Cobb, A. Steinauer, E. Rhoades, A. Schepartz, J. Am. Chem. Soc., 2015, 137, 2536.
• [52] Q. Chu, R.E. Moellering, G.J. Hilinski, Y.-W. Kim, T.N. Grossmann, J.T.-H. Yeh, G.L. Verdine, Med. Chem. Commun., 2015, 6, 111.
• [53] S. L. Lo, S. Wang, Biomaterials, 2008, 29, 2408.
• [54] B.R. Liu, Y.W. Huang, J.G. Winiarz, H.J. Chiang, H.J. Lee, Biomaterials, 2011, 32, 3520.
• [55] J. Regberg, L. Vasconcelos, F. Madani, Ü. Langel, M. Hällbrink, Int. J. Pharm., 2016, 501, 32.
• [56] P.M. Fischer, N.Z. Zhelev, S. Wang, J.E. Melville, R. Fĺhraeus, D.P. Lane, J. Pept. Res., 2000, 55, 163.
• [57] D. Delaroche, B. Aussedat, S. Aubry, G. Chassaing, F. Burlina, G. Clodic, G. Bolbach, S. Lavielle, S. Sagan, Anal. Chem., 2007, 79, 1932.
• [58] A.N. Shirazi, N.S. El-Sayed, R.K. Tiwari, K. Tavakoli, K. Parang, Curr. Drug Deliv., 2016, 13, 409.
• [59] D. Xu, D. Dustin, L. Jiang, D.S. Samways, H. Dong, Chem. Commun., 2015, 51, 11757.
• [60] M.-L. Jobin, M. Blanchet, S. Henry, S. Chaignepain, C. Manigand, S. Castano, S. Lecomte, F. Burlina, S. Sagan, I.D. Alves, Biochim. Biophys. Acta, 2015, 1848, 593.
• [61] A.J. de Jesus, T.W. Allen, Biochim. Biophys. Acta, 2013, 1828, 864.
• [62] C. Bechara, M. Pallerla, Y. Zaltsman, F. Burlina, I.D. Alves, O. Lequin, S. Sagan, FASEB J., 2013, 27, 738.
• [63] P. Perret, M. Ahmadi, L. Riou, S. Bacot, J. Pecher, C. Poillot, A. Broisat, C. Ghezzi, M. De Waard, Int. J. Mol. Sci., 2015, 16, 27730.
• [64] D. Oupický, A.L. Parker, L.W. Seymour, J. Am. Chem. Soc., 2002, 124, 8.
• [65] J. Yoo, D.-Y. Lee, V. Gujrati, N.S. Rejinold, K.M. Lekshmi, S. Uthaman, C. Jeong, I.-K. Park, S. Jon, Y.-C. Kim, J. Control. Release, 2016, 246, 142.
• [66] K. Montrose, Y. Yang, G.W. Krissansen, Sci. Rep., 2014, 4, 4900.
• [67] J. Regberg, A. Srimanee, M. Erlandsson, R. Sillard, D.A. Dobchev, M. Karelson, Ü. Langel, Int. J. Pharm., 2014, 464, 111.
• [68] N. Oskolkov, Int. J. Pept. Res. Ther., 2011, 17, 147.
• [69] N. Purkayastha, K. Eyer, T. Robinson, P.S. Dittrich, A.K. Beck, D. Seebach, B. Kolesinska, R. Cadalbert, Chem. Biodivers., 2013, 10, 1165.
• [70] T. Kato, H. Yamashita, T. Misawa, K. Nishida, M. Kurihara, M. Tanaka, Y. Demizu, M. Oba, Bioorg. Med. Chem., 2016, 24, 2681.
• [71] M. Pooga, M. Hällbrink, M. Zorko, Ü. Langel, FASEB J., 1998, 12, 67.
• [72] J.P. Richard, K. Melikov, E. Vives, C.Ramos, B. Verbeure, M.J. Gait, L.V. Chernomordik, B. Lebleu, J. Biol. Chem., 2003, 278, 585.
• [73] S. Trabulo, A.L. Cardoso, M. Mano, M.C. Pedroso de Lima, Pharmaceuticals, 2010, 3, 961.
• [74] R.M. Steinman, I.S. Mellman, W.A. Muller, Z.A. Cohn, J. Cell Biol., 1983, 96, 1.
• [75] S.D. Conner, S.L. Schmid, Nature, 2003, 422, 37.
• [76] J.L. Zaro, W.-C. Shen, Front. Chem. Sci. Eng., 2015, 9, 407.
• [77] F. Madani, S. Lindberg, U. Langel, S. Futaki, A. Gräslund, J. Biophys., 2011, 2011, 414729.
• [78] Y. Kawaguchi, T. Takeuchi, K. Kuwata, J. Chiba, Y. Hatanaka I. Nakase, S. Futaki, Bioconjug. Chem., 2016, 27, 1119.
• [79] T. Letoha, A. Keller-Pintér, E. Kusz, C. Kolozsi, Z. Bozsó, G. Tóth, C. Vizler, Z. Oláh, L.Szilák, Biochim. Biophys. Acta, 2010, 1798, 2258.
• [80] J. Zhou, W. Liu, R.-C. Pong, G. Hao, X. Sun, J.-T. Hsieh, Amino Acids, 2012, 42, 1253.
• [81] T. Tsumuraya, M. Matsushita, PLoS One, 2014, 9, e86639.
• [82] S. Futaki, I. Nakase, A. Tadokoro, T. Takeuchi, A.T. Jones, Biochem. Soc. Trans., 2007, 35, 784
• [83] J.P. Richard, K. Melikov, H. Brooks, P. Prevot, B. Lebleu, L.V. Chernomordik, J. Biol. Chem., 2005, 280, 15300.
• [84] M. Tyagi, M. Rusnati, M. Presta, M. Giacca, J. Biol. Chem., 2001, 276, 3254.
• [85] H.L. Åmand, H.A. Rydberg, L.H. Fornander, P. Lincoln, B. Nordén, E.K. Esbjörner, Biochim. Biophys. Acta, 2012, 1818, 2669.
• [86] F. Illien, N. Rodriguez, M. Amoura, A. Joliot, M. Pallerla, S. Cribier, F. Burlina, S. Sagan, Sci. Rep., 2016, 6, 36938.
• [87] S.M. Fuchs, R.T. Raines, Biochemistry, 2004, 43, 2438.
• [88] A. Ziegler, J. Seelig, Biophys. J., 2008, 94, 2142
• [89] Y. Takechi-Haraya, R. Nadai, H. Kimura, K. Nishitsuji, K. Uchimura, K. Sakai-Kato, K. Kawakami, A. Shigenaga, T. Kawakami, A. Otaka, H. Hojo, N. Sakashita, H. Saito, Biochim. Biophys. Acta, 2016, 1858, 1339.
• [90] L.E. Prevette, N.C. Benish, A.R. Schoenecker, K.J. Braden, Biophys. Chem., 2015, 207, 40.
• [91] H.C. Christianson, M. Belting, Matrix Biol., 2014, 35, 51.
• [92] I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, S. Futaki, Biochemistry, 2007, 46, 492.
• [93] I. Mäger, E. Eiríksdóttir, K. Langel, S. El Andaloussi, Ü. Langel, Biochim. Biophys. Acta, 2010, 1798, 338.
• [94] P. Lundin, H. Johansson, P. Guterstam, T. Holm, M. Hansen, Ü. Langel, S. EL Andaloussi, Biocon-jug. Chem., 2008, 19, 2535.
• [95] K. Matsuzaki, O. Murase, N. Fujii, K. Miyajima, Biochemistry, 1996, 35, 11361.
• [96] S.J. Ludtke, K. He, W.T. Heller, T.A. Harroun, L. Yang, H.W. Huang, Biochemistry, 1996, 35, 13723.
• [97] D. Derossi, S. Calvet, A. Trembleau, A. Brunissen, G. Chassaing, A. Prochiantz, J. Biol. Chem., 1996, 271, 18188.
• [98] L. Yang, T. A. Harroun, T. M. Weiss, L. Ding, H. W. Huang, Biophys. J., 2001, 81, 1475.
• [99] G. Baumann, P. Mueller, J. Cell. Biochem., 1974, 2, 538.
• [100] Y. Pouny, D. Rapaport, A. Mor, P. Nicolas, Y. Shai, Biochemistry, 1992, 31, 12416.
• [101] J.-P. Berlose, O. Convert, D. Deross, A. Brunissen, G. Chassaing, Eur. J. Biochem., 1996, 242, 372.
• [102] E.G. Stanzl, B.M. Trantow, J.R. Vargas, P.A. Wender, Acc. Chem. Res., 2013, 46, 2944.
• [103] M. Di Pisa, G. Chassaing, J.-M. Swiecicki, Biochemistry, 2015, 54, 194.
• [104] S. Kawamoto, M.Takasu, T. Miyakawa, R. Morikawa, T. Oda, S. Futaki, H. Nagao, J. Chem. Phys., 2011, 134, 095103.
• [105] I. Nakase, M. Niwa, T. Takeuchi, K. Sonomura, N. Kawabata, Y. Koike, M. Takehashi, S. Tanaka, K. Ueda, J.C. Simpson, A.T. Jones, Y. Sugiura, S. Futaki, Mol. Ther., 2004, 10, 1011.
• [106] M. Fretz, J. Jin, R. Conibere, N.A. Penning, S. Al-Taei, G. Storm, S. Futaki, T. Takeuchi, I. Nakase, A.T. Jones, J. Control. Release, 2006, 116, 247.
• [107] M. Kosuge, T. Takeuchi, I. Nakase, A.T. Jones, S. Futaki, Bioconjug. Chem., 2008, 19, 656.
• [108] M.M. Fretz, N.A. Penning, S. Al-Taei, S. Futaki, T. Takeuchi, I. Nakase, G. Storm, A.T. Jones, Biochem. J., 2007, 403, 335.
• [109] A. Mishra, G. Hwee Lai, N.W. Schmidt, V.Z. Sun, A.R. Rodriguez, R. Tong, L. Tang, J. Cheng, T.J. Deming, D.T. Kamei, G.C.L. Wong, Proc. Natl Acad. Sci., 2011, 108, 16883.
• [110] J.M. Swiecicki, M. Di Pisa, F. Burlina, P. Lécorché, C. Mansuy, G. Chassaing, S. Lavielle, Biopolymers, 2015, 104, 533.
• [111] P. Säälik, A. Niinep, J. Pae, M. Hansen, D. Lubenets, Ü. Langel, M.Pooga, J. Control. Release, 2011, 153, 117.
• [112] D. Herce, A.E. Garcia, M.C. Cardoso, J. Am. Chem. Soc., 2014, 136, 17459.
• [113] E. Eiríksdóttir, K. Konate, Ü. Langel, G. Divita, S. Deshayes, Biochim. Biophys. Acta, 2010, 1798, 1119.
• [114] C.L. Watkins, P. Brennan, C. Fegan, K. Takayama, I. Nakase, S. Futaki, A.T. Jones, J. Control. Release, 2009, 140, 237.
• [115] J. Pae, L. Liivamägi, D. Lubenets, P. Arukuusk, Ü. Langel, M. Pooga, Biochim. Biophys. Acta, 2016, 1858, 1860.
• [116] E. Harreither, H.A Rydberg, H.L Ĺmand, V. Jadhav, L. Fliedl, C. Benda, M.A Esteban, D. Pei, N. Borth, R. Grillari-Voglauer, O. Hommerding, F. Edenhofer, B. Nordén, J. Grillari, Cell Regen., 2014, 3, 2.
• [117] A. Fittipaldi, A. Ferrari, M. Zoppé, C. Arcangeli, V. Pellegrini, F. Beltram, M. Giacca, J. Biol. Chem., 2003, 278, 34141.
• [118] C.-Y. Jiao, D. Delaroche, F. Burlina, I.D. Alves, G. Chassaing, S. Sagan, J. Biol. Chem., 2009, 284, 33957.
• [119] F. Simeoni, M.C. Morris, F. Heitz, G. Divita, Nucleic Acids Res., 2003, 31, 2717.
• [120] B.R. Liu, M.-H. Chan, H.-H. Chen, S.-Y. Lo, Y.-W. Huang, H.-J. Lee, [w:] Cell Membrane, Nova Science Publishers, Inc., 2013.
• [121] J.C. Mai, H. Shen, S.C. Watkins, T. Cheng, P.D. Robbins, J. Biol. Chem., 2002, 277, 30208.
• [122] S. Fawell, J. Seery, Y. Daikh, C. Moore, L.L. Chen, B. Pepinsky, J. Barsoum, Proc. Natl Acad. Sci., 1994, 91, 664.
• [123] S.R. Schwarze, A. Ho, A. Vocero-Akbani, S.F. Dowdy, Science, 1999, 285, 1569.
• [124] D. Sarko, B. Beijer, R.G. Boy, E.-M. Nothelfer, K. Leotta, M. Eisenhut, A. Altmann, U. Haberkorn, W. Mier, Mol. Pharmaceutics, 2010, 7, 2224.
• [125] A. Bolhassani, B. S. Jafarzade, G. Mardani, Peptides, 2017, 87, 50.
• [126] Ülo Langel, Cell-Penetrating Peptides, Humana Press Inc., 2015.
• [127] Langel, Ülo, Cell-Penetrating Peptides. Methods and Protocols, CRC Press, 2011.
• [128] K. Ezzat, E.M. Zaghloul, S.E.L. Andaloussi, T. Lehto, R. El-Sayed, T. Magdy, C.I.E. Smith, Ü. Langel, J. Control. Release, 2012, 162, 1.
• [129] S.A. Moschos, S.W. Jones, M.M. Perry, A.E. Williams, J.S. Erjefalt, J.J. Turner, P.J. Barnes, B.S. Sproat, M.J. Gait, M.A. Lindsay, Bioconjug. Chem., 2007, 18, 1450.
• [130] Z. Wang, Y. Chen, E. Liu, J. Gong, S. M. Cheol, Y. Huang, Protein Pept. Lett., 2014, 21, 1129.
• [131] N. Kamei, E.J.B. Nielsen, T. Nakakubo, Y. Aoyama, U.L. Rahbek, B.L. Pedersen, M. Takeda-Morishita, J. Pharm. Sci., 2016, 105, 747.
• [132] S.R. Schwarze, K.A. Hruska, S.F. Dowdy, Trends Cell Biol., 2000, 10, 290.
• [133] S. Liu, H. Yang, L. Wan, J. Cheng, X. Lu, Cancer Biother. Radiopharm., 2013, 28, 289.
• [134] K.J. Lim, B.H. Sung, J.R. Shin, Y.W. Lee, D.J. Kim, K.S. Yang, S.C. Kim, PLoS One, 2013, 8, e66084.
• [135] W. Wang, M. Li, Z. Zhang, C. Cui, J. Zhou, L. Yin, H. Lv, Carbohydr. Polym., 2017, 156, 97.
• [136] Y. Yamada, M. Hashida, H. Harashima, Biomaterials, 2015, 52, 189.
• [137] M.C. Shin, J. Zhang, K.A. Min, K. Lee, C. Moon, J.P. Balthasar, V.C. Yang, J. Control. Release, 2014, 194, 197.
• [138] N. Li, T. Li, C.Liu, S. Ye, J. Liang, H. Han, J. Biomed. Nanotechnol., 2016, 12, 878.
• [139] J. Chen, S. Li, Q. Shen, Eur. J. Pharm. Sci., 2012, 47, 430.
• [140] G. Sharma, A. Modgil, B. Layek, K. Arora, C. Sun, B. Law, J. Singh, J. Control. Release, 2013, 167, 1.
• [141] N. Jiménez-Mancilla, G. Ferro-Flores, C. Santos-Cuevas, B. Ocampo-García, M. Luna-Gutiérrez, E. Azorín-Vega, K. Isaac-Olivé, M. Camacho-López, E. Torres-García, J. Label Compd. Radiopharm., 2013, 56, 663.
• [142] J. Li, X. Zhang, M. Wang, X. Li, H. Mu, A. Wang, W. Liu, Y. Li, Z. Wu, K. Sun, Int. J. Pharm., 2016, 501, 112.
• [143] Y. Liu, L. Mei, Q. Yu, Q. Zhang, H. Gao, Z. Zhang, Q. He, Amino Acids, 2015, 47, 2533.
• [144] X. Xie, Y. Yang, Y, Yang, H, Zhang, Y. Li, X. Mei, Drug Deliv., 2016, 23, 2445.
• [145] W. Lin, X. Xie, J. Deng, H. Liu, Y. Chen, X. Fu, H. Liu, Y. Yang, J. Drug Target., 2016, 24, 134.
• [146] Y. Matsumura, H. Maeda, Cancer Res., 1986, 46, 6387.
• [147] H. Maeda, G.Y. Bharate, J. Daruwalla, Eur. J. Pharm. Biopharm., 2009, 71, 409.
• [148] R.A. Morshed, M.E. Muroski, Q. Dai, M.L. Wegscheid, B. Auffinger, D. Yu, Y.Han, L. Zhang, M. Wu, Y. Cheng M. S. Lesniak, Mol. Pharm., 2016, 13, 1843.
• [149] J. Zhang, M. Li. Z. Yuan, D. Wu, J. Chen, J. Feng, J. Nanopart. Res., 2016, 18, 299.
• [150] D. Yu, C. Jin, J. Leja, N. Majdalani, B. Nilsson, F. Eriksson, M. Essand, J. Virol., 2011, 85, 13114.
• [151] Y. Eto, Y. Yoshioka, R. Asavatanabodee, S. Kida, M. Maeda, Y. Mukai, H. Mizuguchi, K. Kawasaki, N. Okada, S. Nakagawa, Peptides, 2009, 30, 1548.
• [152] Y. Liu, Y. J. Kim, M. Ji, J. Fang, N. Siriwon, L.I. Zhang, P. Wang, Mol. Ther. Methods Clin. Dev., 2014, 1, 12.
• [153] D.C. Anderson, E. Nichols, R. Manger, D. Woodle, M. Barry, A.R. Fritzberg, Biochem. Biophys. Res. Commun., 1993, 194, 876.
• [154] H. He, L. Sun, J. Ye, E. Liu, S. Chen, Q. Liang, M.C. Shin, V.C. Yang, J. Control. Release, 2016, 240, 67.
• [155] S.M. van Duijnhoven, M.S. Robillard, K. Nicolay, H. Grüll, Contrast Media Mol. Imaging, 2015, 10, 59.
• [156] T. Jiang, E.S. Olson, Q.T. Nguyen, M. Roy, P.A. Jennings, R.Y. Tsien, Proc. Natl Acad. Sci., 2004, 21, 17867.
• [157] N.Q. Shi, W. Gao, B. Xiang, X.R. Qi, Int. J. Nanomedicine, 2012, 7, 1613.
• [158] C.D. Malone, E.S. Olson, R.F. Mattrey, T. Jiang, R.Y. Tsien, Q.T. Nguyen, PLoS One, 2015, 10, e0137104.
• [159] S.A. Bode, M.B. Hansen, R.A. Oerlemans, J.C. van Hest, D.W. Löwik, Bioconjug. Chem., 2015, 26, 850.
• [160] Z. Liu, M. Xiong, J. Gong, Y. Zhang, N. Bai, Y. Luo, L. Li, Y. Wei, Y. Liu, X. Tan, R. Xiang, Nat. Commun., 2014, 5, 4280.
• [161] T.J. Harris, G. von Maltzahn, M.E. Lord, J.-H. Park, A. Agrawal, D.-H. Min, M.J. Sailor, S.N. Bhatia, Small, 2008, 4, 1307.
• [162] K.-L. Veiman, K. Künnapuu, T. Lehto, K. Kiisholts, K. Pärn, Ü. Langel, K. Kurrikoff, J. Control. Release, 2015, 209, 238.
• [163] I.F. Tannock, D. Rotin, Cancer Res., 1989, 49, 4373.
• [164] X. Zhang, Y. Lin, R.J. Gillies, J. Nucl. Med., 2010, 51, 1167.
• [165] Y. Ding, D. Sun, G.L. Wang, H.G. Yang, H.F. Xu, J.H. Chen, Y. Xie, Z. Q. Wang, Int. J. Nanomedicine, 2015, 10, 6199.
• [166] H. Cheng, J.-Y. Zhu, X.-D. Xu, W.-X. Qiu, Q. Lei, K. Han, Y.-J. Cheng, X.-Z. Zhang, ACS Appl. Mater. Interfaces, 2015, 7, 16061.
• [167] D.K. Schach, W. Rock, J. Franz, M. Bonn, S.H. Parekh, T. Weidner, J. Am. Chem. Soc., 2015, 137, 12199.
• [168] J.E. Baio, D. Schach, A.V. Fuchs, L. Schmüser, N. Billecke, C. Bubeck, K. Landfester, M. Bonn, M. Bruns, C.K. Weissac, T. Weidner, Chem. Commun., 2015, 51, 273.
• [169] C. Sun, W.-C. Shen, J. Tu, J. L. Zaro, Mol. Pharm., 2014, 11, 1583.
• [170] W. Zhang, J. Song, B. Zhang, L. Liu, K. Wang, R. Wang, Bioconjug. Chem., 2011, 22, 1410.
• [171] S.H. Lee, E. Moroz, B. Castagner, J.C. Leroux, J. Am. Chem. Soc., 2014, 136, 12868.
• [172] R. Weinstain, E.N. Savariar, C.N. Felsen, R.Y. Tsien, J. Am. Chem. Soc., 2014, 136, 874.
• [173] Y. Yang, Y. Yang, X. Xie, X. Cai, H. Zhang, W. Gong, Z. Wang, X. Mei, Biomaterials, 2014, 35, 4368.
• [174] S.R. MacEwan, A. Chilkoti, Biopolymers, 2010, 94, 60.
• [175] S.M. Hearst, Q. Shao, M. Lopez, D. Raucher, P.J. Vig, J. Neurochem., 2014, 131, 101.
• [176] L.R. Walker, J.S. Ryu, E. Perkins, L.R. McNally, D. Raucher, Drug Des. Devel. Ther., 2014, 8, 1649.
• [177] S.R. MacEwan, A. Chilkoti, Nano Lett., 2014, 14, 2058.
• [178] S.-K. Wu, C.-F. Chiang, Y.-H. Hsu, T.-H. Lin, H.-C. Liou, W.-M. Fu, W.-L. Lin, Int. J. Nanomedicine, 2014, 9, 4485.
• [179] W. Lin, X. Xie, Y. Yang, X. Fu, H. Liu, Y. Yang, J. Deng, Drug Deliv., 2016, 23, 3436.
• [180] Y. Yang, X. Xie, X. Xu, X. Xia, H. Wang, L. Li, W. Dong, P. Ma, Y. Yang, Y. Liu, X. Mei, Colloids Surf. B Biointerfaces, 2016, 146, 607.
• [181] H.Li, T. Y.Tsui, W. Ma, J. Pharm. Pharmacol., 2015, 67, 1215.
• [182] Y. Yang, Y.F. Yang, X.Y. Xie, Z.Y. Wang, W. Gong, H. Zhang, Y. Li, F.L. Yu, Z.P. Li, X.G. Mei, Biomaterials, 2015, 48, 84.
• [183] Y. Yang, X. Xie, Y. Yang, Z. Li, F. Yu, W. Gong, Y. Li, H. Zhang, Z. Wang, X. Mei, Mol. Pharmaceutics, 2016, 13, 1508.
• [184] S.M. Farkhani, M. Johari-Ahar, P. Zakeri-Milani, J. Shahbazi Mojarrad, H. Valizadeh, Artif. Cells Nanomed. Biotechnol., 2016, 44, 1424.
• [185] S.Q. Wu, C.W. Chi, C.X. Yang, X.P. Yan, Anal. Chem., 2016, 88, 4114.
• [186] X. Zhao, T. Shang, X. Zhang, T. Ye, D. Wang, L. Rei, Nanoscale Res. Lett., 2016, 11, 451.
• [187] K.-H. Lin, S.-T. Hong, H.-T. Wang, Y.-L. Lo, A. M.-Y. Lin, J. C.-H. Yang, Int. J. Mol. Sci., 2016, 17, E1998.
• [188] X. Chen, M. Yuan, Q. Zhang, Y.T. Yang, H. Gao, Q. He, Curr. Pharm. Biotechnol., 2016, 17, 636.
• [189] J.W. McGowan, Q. Shao, P.J. Vig, G.L. Bidwell III, Drug Des. Devel. Ther., 2016, 10, 2803.
• [190] S. Zhu, S. Chen, Y. Gao, F. Guo, F. Li, B. Xie, J. Zhou, H. Zhong, Drug Deliv., 2016, 23, 1980.
• [191] Y. Daimon, N. Kamei, K. Kawakami, M. Takeda-Morishita, H. Izawa Y. Takechi-Haraya, H. Saito, H. Sakai, M. Abe, K. Ariga, Mol. Pharmaceutics, 2016, 13, 4034.
• [192] J.B. Rothbard, S. Garlington, Q. Lin, T. Kirschberg, E. Kreider, P.L. McGrane, P.A. Wende, P.A. Khavari, Nat. Med., 2000, 6, 1253.
• [193] M. Cohen-Avrahami, D. Libster, A. Aserin, N. Garti, J. Phys. Chem. B., 2011, 115, 10189.
• [194] M. Rizzuti, M. Nizzardo, C. Zanetta, A. Ramirez, S. Corti, Drug Discov. Today, 2015, 20, 76.
• [195] R.R. Sawant, N.R. Patel, V. . Torchilin, Eur. J. Nanomed., 2013, 5, 141.
• [196] M. D. Hill, R.H. Martin, D. Mikulis, J.H. Wong, F.L. Silver, K.G. terBrugge, G. Milot, W.M. Clark, R.L. MacDonald, M.E. Kelly, M. Boulton, I. Fleetwood, C. McDougall, T. Gunnarsson, M. Chow, C. Lum, R. Dodd, J. Poublanc, T. Krings, A.M. Demchuk, M. Goyal, R. Anderson, J. Bishop, D. Garman, M. Tymianski, Lancet Neurol., 2012, 11, 942.
• [197] M.A. Warso, J.M. Richards, D. Mehta, K. Christov, C. Schaeffer, L. Rae Bressler, T. Yamada, D. Majumdar, S.A. Kennedy, C.W. Beattie, T.K. Das Gupta, Br. J. Cancer, 2013, 108, 1061.
• [198] H. Kim, S. Moodley, M. Liu, Drug Deliv. Transl. Res., 2015, 5, 275.
• [199] R. Coriat S.J. Faivre, O. Mir, C. Dreyer, S. Ropert, M. Bouattour, R. Desjardins, F. Goldwasser, E. Raymond, Int. J. Nanomed., 2016, 11, 6207.
• [200] C. de Coupade, A. Fittipaldi, V. Chagnas, M. Michel, S. Carlier, E. Tasciotti, A. Darmon, D. Ravel, J. Kearsey, M. Giacca, F. Cailler, Biochem. J., 2005, 390, 407.

Uwagi

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2018).