Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-11T01:31:46.581Z Has data issue: false hasContentIssue false
  • English
  • Français

Understanding nano-bio interactions to improve nanocarriers for drug delivery

Published online by Cambridge University Press:  13 March 2014

Ryan M. Pearson ,
Hao-jui Hsu ,
Jason Bugno  and
Seungpyo Hong
Ryan M. Pearson
Affiliation:
University of Illinois at Chicago; rpears2@uic.edu
Hao-jui Hsu
Affiliation:
University of Illinois at Chicago; hhsu24@uic.edu
Jason Bugno
Affiliation:
University of Illinois at Chicago; jbugno2@uic.edu
Seungpyo Hong
Affiliation:
University of Illinois at Chicago; sphong@uic.edu
Get access

Abstract

The ability of cancer-targeted nanoparticles (NPs) to reach their site of action and evoke a desired biological response after intravenous injection is critical to achieve clinically significant in vivo efficacy. Throughout their journey in the body, NPs must successfully traverse biological environments such as blood circulation and tumor microenvironments. The interactions that occur at the interface between NPs and biological components are complex, requiring a thorough understanding of the “nano-bio” interactions to design NPs with maximal therapeutic indices. In this article, we review the challenges presented by the multiscale, important biocompartments that NPs face, describe the crucial nano-bio interactions present at each stage, and discuss potential strategies to overcome those challenges. This review suggests design considerations for NPs to optimally modulate their physicochemical properties to achieve desired biological responses, which are expected to aid chemists, engineers, and clinical scientists to design and develop highly effective delivery platforms for cancer therapy.

Keywords

Nanoscalebiomaterialpolymerbiomedical
Type
Research Article
Information
MRS Bulletin , Volume 39 , Issue 3: Organic Nanoparticles for Drug Delivery and Imaging , March 2014 , pp. 227 - 237
Copyright
Copyright © Materials Research Society 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Peer, D., Karp, J.M., Hong, S., Farokhzad, O.C., Margalit, R., Langer, R., Nat. Nanotechnol. 2, 751 (2007).Google Scholar
Mura, S., Couvreur, P., Adv. Drug Deliv. Rev. 64, 1394 (2012).Google Scholar
Zamboni, W.C., Torchilin, V., Patri, A.K., Hrkach, J., Stern, S., Lee, R., Nel, A., Panaro, N.J., Grodzinski, P., Clin. Cancer Res. 18, 3229 (2012).Google Scholar
Chauhan, V.P., Jain, R.K., Nat. Mater. 12, 958 (2013).Google Scholar
van der Meel, R., Vehmeijer, L.J.C., Kok, R.J., Storm, G., van Gaal, E.V.B., Adv. Drug Deliv. Rev. 65, 1284 (2013).Google Scholar
Sengupta, S., Kulkarni, A., ACS Nano 7, 2878 (2013).Google Scholar
Davis, M.E., Mol. Pharm. 6, 659 (2009).Google Scholar
Hubbell, J.A., Langer, R., Nat. Mater. 12, 963 (2013).Google Scholar
Kim, S., Shi, Y., Kim, J.Y., Park, K., Cheng, J.X., Expert Opin. Drug Deliv. 7, 49 (2010).Google Scholar
Chrastina, A., Massey, K.A., Schnitzer, J.E., Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3, 421 (2011).Google Scholar
Nel, A.E., Mädler, L., Velegol, D., Xia, T., Hoek, E.M.V., Somasundaran, P., Klaessig, F., Castranova, V., Thompson, M., Nat. Mater. 8, 543 (2009).Google Scholar
Nichols, J.W., Bae, Y.H., Nano Today 7, 606 (2012).Google Scholar
Doane, T., Burda, C., Adv. Drug Deliv. Rev. 65, 607 (2013).CrossRefGoogle Scholar
Jain, R.K., Cancer Metast. Rev. 9, 253 (1990).Google Scholar
Kamoun, W.S., Chae, S.S., Lacorre, D.A., Tyrrell, J.A., Mitre, M., Gillissen, M.A., Fukumura, D., Jain, R.K., Munn, L.L., Nat. Methods 7, 655 (2010).Google Scholar
Padera, T.P., Stoll, B.R., Tooredman, J.B., Capen, D., Tomaso, E. di, Jain, R.K., Nature 427, 695 (2004).Google Scholar
Kerbel, R.S., Carcinogenesis 21, 505 (2000).CrossRefGoogle Scholar
Torchilin, V., Adv. Drug Deliv. Rev. 63, 131 (2011).CrossRefGoogle Scholar
Hobbs, S.K., Monsky, W.L., Yuan, F., Roberts, W.G., Griffith, L., Torchilin, V.P., Jain, R.K., Proc. Natl. Acad. Sci. U.S.A. 95, 4607 (1998).CrossRefGoogle Scholar
Hashizume, H., Baluk, P., Morikawa, S., McLean, J.W., Thurston, G., Roberge, S., Jain, R.K., McDonald, D.M., Am. J. Pathol. 156, 1363 (2000).Google Scholar
Tannock, I.F., Rotin, D., Cancer Res. 49, 4373 (1989).Google Scholar
Cardone, R.A., Casavola, V., Reshkin, S.J., Nat. Rev. Cancer 5, 786 (2005).CrossRefGoogle Scholar
Swietach, P., Vaughan-Jones, R., Harris, A., Cancer Metast. Rev. 26, 299 (2007).CrossRefGoogle Scholar
Švastová, E., Hulíková, A., Rafajová, M., Zat’ovičová, M., Gibadulinová, A., Casini, A., Cecchi, A., Scozzafava, A., Supuran, C.T., Pastorek, J.R., Pastoreková, S., FEBS Lett. 577, 439 (2004).Google Scholar
Cook, J.A., Gius, D., Wink, D.A., Krishna, M.C., Russo, A., Mitchell, J.B., Semin. Radiat. Oncol. 14, 259 (2004).Google Scholar
Acharya, A., Das, I., Chandhok, D., Saha, T., Oxid. Med. Cell. Longev. 3, 23 (2010).Google Scholar
Lu, P., Weaver, V.M., Werb, Z., J. Cell. Biol. 196, 395 (2012).Google Scholar
Ramanujan, S., Pluen, A., McKee, T.D., Brown, E.B., Boucher, Y., Jain, R.K., Biophys. J. 83, 1650 (2002).Google Scholar
Jain, R.K., Stylianopoulos, T., Nat. Rev. Clin. Oncol. 7, 653 (2010).Google Scholar
Jain, R.K., Cancer Res. 48, 2641 (1988).Google Scholar
Jain, R.K., Sci. Am. 271, 58 (1994).Google Scholar
Raemdonck, K., Braeckmans, K., Demeester, J., De Smedt, S.C., Chem. Soc. Rev. 43, 444 (2014).Google Scholar
Policastro, L.L., Ibañez, I.L., Notcovich, C., Duran, H.A., Podhajcer, O.L., Antioxid. Redox. Sign. 19, 854 (2013).CrossRefGoogle Scholar
Sun, H., Meng, F., Cheng, R., Deng, C., Zhong, Z., Expert Opin. Drug Deliv. 10, 1109 (2013).Google Scholar
Ganta, S., Devalapally, H., Shahiwala, A., Amiji, M., J. Control. Release 126, 187 (2008).CrossRefGoogle Scholar
Azagarsamy, M.A., Yesilyurt, V., Thayumanavan, S., J. Am. Chem. Soc. 132, 4550 (2010).Google Scholar
Danhier, F., Feron, O., Préat, V., J. Control. Release 148, 135 (2010).Google Scholar
Maeda, H., Sawa, T., Konno, T., J. Control. Release 74, 47 (2001).CrossRefGoogle Scholar
Cho, K., Wang, X., Nie, S., Chen, Z.G., Shin, D.M., Clin. Cancer Res. 14, 1310 (2008).CrossRefGoogle Scholar
Kratz, F., Warnecke, A., J. Control. Release 164, 221 (2012).CrossRefGoogle Scholar
Simonsen, T.G., Gaustad, J.V., Leinaas, M.N., Rofstad, E.K., PloS one 7 , (2012).Google Scholar
Prabhakar, U., Maeda, H., Jain, R.K., Sevick-Muraca, E.M., Zamboni, W., Farokhzad, O. C., Barry, S.T., Gabizon, A., Grodzinski, P., Blakey, D.C., Cancer Res. 73, 2412 (2013).Google Scholar
Heldin, C.H., Rubin, K., Pietras, K., Ostman, A., Nat. Rev. Cancer 4, 806 (2004).Google Scholar
Yu, M., Tannock, I.F., Cancer Cell 21, 327 (2012).Google Scholar
Lee, S.-M., Nguyen, S.T., Macromolecules 46 (23), 9169 (2013).Google Scholar
Stuart, M.A., Huck, W.T., Genzer, J., Muller, M., Ober, C., Stamm, M., Sukhorukov, G.B., Szleifer, I., Tsukruk, V.V., Urban, M., Winnik, F., Zauscher, S., Luzinov, I., Minko, S., Nat. Mater. 9, 101 (2010).Google Scholar
Cabane, E., Zhang, X., Langowska, K., Palivan, C., Meier, W., Biointerphases 7, 1 (2012).Google Scholar
Patil, R., Portilla-Arias, J., Ding, H., Konda, B., Rekechenetskiy, A., Inoue, S., Black, K.L., Holler, E., Ljubimova, J.Y., Int. J. Mol. Sci. 13, 11681 (2012).CrossRefGoogle Scholar
Frantz, C., Stewart, K.M., Weaver, V.M., J. Cell Sci. 123, 4195 (2010).Google Scholar
Netti, P.A., Berk, D.A., Swartz, M.A., Grodzinsky, A.J., Jain, R.K., Cancer Res. 60, 2497 (2000).Google Scholar
Anna, A.B., Gary, L.B., Stella, P.P., Yeudall, W.A., Biomed. Mater. 8 (2013).Google Scholar
Popovic, Z., Liu, W., Chauhan, V.P., Lee, J., Wong, C., Greytak, A.B., Insin, N., Nocera, D.G., Fukumura, D., Jain, R.K., Bawendi, M.G., Angew. Chem. Int. Edit. 49, 8649 (2010).Google Scholar
Chauhan, V.P., Popovic, Z., Chen, O., Cui, J., Fukumura, D., Bawendi, M.G., Jain, R.K., Angew. Chem. Int. Edit. Engl. 50, 11417 (2011).Google Scholar
Kim, B., Han, G., Toley, B.J., Kim, C.K., Rotello, V.M., Forbes, N.S., Nat. Nanotechnol. 5, 465 (2010).CrossRefGoogle Scholar
De Jong, W.H., Borm, P.J., Int. J. Nanomed. 3, 133 (2008).Google Scholar
Huang, K., Ma, H., Liu, J., Huo, S., Kumar, A., Wei, T., Zhang, X., Jin, S., Gan, Y., Wang, P.C., He, S., Zhang, X., Liang, X.-J., ACS Nano 6, 4483 (2012).Google Scholar
Cabral, H., Matsumoto, Y., Mizuno, K., Chen, Q., Murakami, M., Kimura, M., Terada, Y., Kano, M.R., Miyazono, K., Uesaka, M., Nishiyama, N., Kataoka, K., Nat. Nanotechnol. 6, 815 (2011).Google Scholar
Sunoqrot, S., Liu, Y., Kim, D.-H., Hong, S., Mol. Pharm. 10, 2157 (2012).Google Scholar
Pluen, A., Netti, P.A., Jain, R.K., Berk, D.A., Biophys. J. 77, 542 (1999).Google Scholar
Waite, C.L., Roth, C.M., Crit. Rev. Biomed. Eng. 40, 21 (2012).Google Scholar
Stylianopoulos, T., Poh, M.-Z., Insin, N., Bawendi, M.G., Fukumura, D., Munn, L., Jain, R.K., Biophys. J. 99, 1342 (2010).CrossRefGoogle Scholar
Goodman, T.T., Olive, P.L., Pun, S.H., Int. J. Nanomed. 2, 265 (2007).Google Scholar
Goodman, T.T., Chen, J., Matveev, K., Pun, S.H., Biotechnol. Bioeng. 101, 388 (2008).CrossRefGoogle Scholar
Jain, R.K., Science 307, 58 (2005).Google Scholar
Fukumura, D., Jain, R.K., Microvasc. Res. 74, 72 (2007).Google Scholar
Spector, A.A., Yorek, M.A., J. Lipid. Res. 26, 1015 (1985).Google Scholar
Verma, A., Stellacci, F., Small 6, 12 (2010).Google Scholar
Albelda, S.M., Buck, C.A., FASEB J. 4, 2868 (1990).Google Scholar
Dale, T.C., Biochem. J. 329 (Pt 2), 209 (1998).Google Scholar
Slamon, D.J., Godolphin, W., Jones, L.A., Holt, J.A., Wong, S.G., Keith, D.E., Levin, W.J., Stuart, S.G., Udove, J., Ullrich, A., Science 244, 707 (1989).CrossRefGoogle Scholar
Ruoslahti, E., Annu. Rev. Cell Dev. Biol. 12, 697 (1996).Google Scholar
Bostwick, D.G., Pacelli, A., Blute, M., Roche, P., Murphy, G.P., Cancer 82, 2256 (1998).Google Scholar
Al-Hajj, M., Wicha, M.S., Benito-Hernandez, A., Morrison, S.J., Clarke, M.F., Proc. Natl. Acad. Sci. U.S.A. 100, 3983 (2003).Google Scholar
Li, S., Huang, S., Peng, S.B., Int. J. Oncol. 27, 1329 (2005).Google Scholar
Hanahan, D., Weinberg, R.A., Cell 100, 57 (2000).Google Scholar
Hynes, N. E., Lane, H.A., Nat. Rev. Cancer 5, 341 (2005).Google Scholar
Simnick, A.J., Valencia, C.A., Liu, R., Chilkoti, A., ACS Nano 4, 2217 (2010).Google Scholar
Koivunen, E., Gay, D.A., Ruoslahti, E., J. Biol. Chem. 268, 20205 (1993).Google Scholar
Mirshafiee, V., Mahmoudi, M., Lou, K., Cheng, J., Kraft, M.L., Chem. Commun. 49, 2557 (2013).Google Scholar
Salvati, A., Pitek, A.S., Monopoli, M.P., Prapainop, K., Bombelli, F.B., Hristov, D.R., Kelly, P.M., Aberg, C., Mahon, E., Dawson, K.A., Nat. Nanotechnol. 8, 137 (2013).Google Scholar
Valencia, P.M., Hanewich-Hollatz, M.H., Gao, W., Karim, F., Langer, R., Karnik, R., Farokhzad, O.C., Biomaterials 32, 6226 (2011).Google Scholar
Monopoli, M.P., Aberg, C., Salvati, A., Dawson, K.A., Nat. Nanotechnol. 7, 779 (2012).Google Scholar
Hermanson, G.T., Bioconjugate Techniques (Elsevier, NY, 2008).Google Scholar
Verma, A., Stellacci, F., Small 6, 12 (2010).Google Scholar
Leroueil, P.R., Hong, S., Mecke, A., Baker, J.R. Jr., Orr, B.G., Holl, M.M., Acc. Chem. Res. 40, 335 (2007).Google Scholar
Miller, C.R., Bondurant, B., McLean, S.D., McGovern, K.A., O′Brien, D.F., Biochemistry 37, 12875 (1998).Google Scholar
Hong, S., Rattan, R., Majoros, I.J., Mullen, D.G., Peters, J.L., Shi, X., Bielinska, A.U., Blanco, L., Orr, B.G., Baker, J.R. Jr., Holl, M.M., Bioconjug. Chem. 20, 1503 (2009).Google Scholar
Hong, S.P., Bielinska, A.U., Mecke, A., Keszler, B., Beals, J.L., Shi, X.Y., Balogh, L., Orr, B.G., Baker, J.R., Holl, M.M.B., Bioconjug. Chem. 15, 774 (2004).Google Scholar
Pearson, R.M., Patra, N., Hsu, H.-J., Uddin, S., Kral, P., Hong, S., ACS Macro Lett. 2, 77 (2013).Google Scholar
Lammers, T., Hennink, W.E., Storm, G., Brit. J. Cancer 99, 392 (2008).Google Scholar
Byrne, J.D., Betancourt, T., Brannon-Peppas, L., Adv. Drug Deliv. Rev. 60, 1615 (2008).Google Scholar
Kiziltepe, T., Ashley, J.D., Stefanick, J.F., Qi, Y.M., Alves, N.J., Handlogten, M.W., Suckow, M.A., Navari, R.M., Bilgicer, B., Blood Cancer J. 2, e64 (2012).Google Scholar
Acharya, S., Dilnawaz, F., Sahoo, S.K., Biomaterials 30, 5737 (2009).Google Scholar
Mammen, M., Choi, S.-K., Whitesides, G.M., Angew. Chem. Int. Edit. Engl. 37, 2754 (1998).Google Scholar
Davis, M.E., Chen, Z.G., Shin, D.M., Nat. Rev. Drug Discov. 7, 771 (2008).Google Scholar
Lee, C.C., MacKay, J.A., Frechet, J.M., Szoka, F.C., Nat. Biotechnol. 23, 1517 (2005).Google Scholar
Pearson, R.M., Bae, J.W., Hong, S., Nanoparticulate Drug Delivery Systems: Strategies, Technologies, and Applications (Wiley, NY, 2013).Google Scholar
Hong, S., Leroueil, P.R., Majoros, I.N.J., Orr, B.G., Baker, J.R., Banaszak Holl, M.M., Chem. Biol. 14, 107 (2007).Google Scholar
Myung, J.H., Gajjar, K.A., Saric, J., Eddington, D.T., Hong, S., Angew. Chem. Int. Edit. Engl. 50, 11769 (2011).Google Scholar
Poon, Z., Chen, S., Engler, A.C., Lee, H.I., Atas, E., von Maltzahn, G., Bhatia, S.N., Hammond, P.T., Angew. Chem. Int. Edit. Engl. 49, 7266 (2010).Google Scholar
Bae, Y., Jang, W.D., Nishiyama, N., Fukushima, S., Kataoka, K., Mol. Biosyst. 1, 242 (2005).Google Scholar
Tenzer, S., Docter, D., Kuharev, J., Musyanovych, A., Fetz, V., Hecht, R., Schlenk, F., Fischer, D., Kiouptsi, K., Reinhardt, C., Landfester, K., Schild, H., Maskos, M., Knauer, S.K., Stauber, R.H., Nat. Nanotechnol. 8, 772 (2013).Google Scholar
Stefanick, J.F., Ashley, J.D., Kiziltepe, T., Bilgicer, B., ACS Nano 7, 2935 (2013).Google Scholar
Petros, R.A., DeSimone, J.M., Nat. Rev. Drug Discov. 9, 615 (2010).Google Scholar
Khalil, I.A., Kogure, K., Akita, H., Harashima, H., Pharmacol. Rev. 58, 32 (2006).Google Scholar
Hong, S., Leroueil, P.R., Janus, E.K., Peters, J.L., Kober, M.M., Islam, M.T., Orr, B.G., Baker, J.R. Jr., Banaszak Holl, M.M., Bioconjug. Chem. 17, 728 (2006).Google Scholar
Hillaireau, H., Couvreur, P., Cell. Mol. Life Sci. 66, 2873 (2009).Google Scholar
Aderem, A., Underhill, D.M., Annu. Rev. Immunol. 17, 593 (1999).Google Scholar
Champion, J.A., Walker, A., Mitragotri, S., Pharm. Res. 25, 1815 (2008).Google Scholar
Galli, S.J., Maurer, M., Lantz, C.S., Curr. Opin. Immunol. 11, 53 (1999).Google Scholar
Savina, A., Amigorena, S., Immunol. Rev. 219, 143 (2007).Google Scholar
Conner, S.D., Schmid, S.L., Nature 422, 37 (2003).Google Scholar
Hayer, A., Stoeber, M., Ritz, D., Engel, S., Meyer, H.H., Helenius, A., J. Cell. Biol. 191, 615 (2010).Google Scholar
Pelkmans, L., Helenius, A., Traffic 3, 311 (2002).Google Scholar
Parton, R.G., Simons, K., Nat. Rev. Mol. Cell Bio. 8, 185 (2007).Google Scholar
Sigismund, S., Argenzio, E., Tosoni, D., Cavallaro, E., Polo, S., Di Fiore, P.P., Dev. Cell 15, 209 (2008).Google Scholar
Goldstein, J.L., Brown, M.S., Anderson, R.G.W., Russell, D.W., Schneider, W.J., Annu. Rev. Cell Biol. 1, 1 (1985).CrossRefGoogle Scholar
Mayor, S., Pagano, R.E., Nat. Rev. Mol. Cell Bio. 8, 603 (2007).CrossRefGoogle Scholar
Mann, A., Thakur, G., Shukla, V., Ganguli, M., Drug Discov. Today 13, 152 (2008).Google Scholar
Duvshani-Eshet, M., Keren, H., Oz, S., Radzishevsky, I.S., Mor, A., Machluf, M., J. Gene Med. 10, 1150 (2008).CrossRefGoogle Scholar
Lange, A., Mills, R.E., Lange, C.J., Stewart, M., Devine, S.E., Corbett, A.H., J. Biol. Chem. 282, 5101 (2007).Google Scholar
Suomalainen, A., Semin. Fetal Neonat. Med. 16, 236 (2011).Google Scholar
Midoux, P., Mendes, C., Legrand, A., Raimond, J., Mayer, R., Monsigny, M., Roche, A.C., Nucleic Acids Res. 21, 871 (1993).Google Scholar
Chan, C.-L., Majzoub, R.N., Shirazi, R.S., Ewert, K.K., Chen, Y.-J., Liang, K.S., Safinya, C.R., Biomaterials 33, 4928 (2012).Google Scholar
Dominska, M., Dykxhoorn, D.M., J. Cell Sci. 123, 1183 (2010).Google Scholar
Varkouhi, A.K., Scholte, M., Storm, G., Haisma, H.J., J. Control. Release 151, 220 (2011).Google Scholar
Behr, J.P., Bioconjug. Chem. 5, 382 (1994).Google Scholar
Horth, M., Lambrecht, B., Khim, M.C., Bex, F., Thiriart, C., Ruysschaert, J.M., Burny, A., Brasseur, R., EMBO J. 10, 2747 (1991).Google Scholar
Marsh, M., Helenius, A., Adv. Virus. Res. 36, 107 (1989).Google Scholar
Carver, L.A., Schnitzer, J.E., Nat. Rev. Cancer 3, 571 (2003).Google Scholar
Rejman, J., Conese, M., Hoekstra, D., J. Liposome Res. 16, 237 (2006).Google Scholar
Sahay, G., Kim, J.O., Kabanov, A.V., Bronich, T.K., Biomaterials 31, 923 (2010).Google Scholar
Branden, L.J., Mohamed, A.J., Smith, C.I., Nat. Biotechnol. 17, 784 (1999).Google Scholar
Rajendran, L., Knolker, H.J., Simons, K., Nat. Rev. Drug Discov. 9, 29 (2010).Google Scholar
Fernandez, C.A., Baumhover, N.J., Anderson, K., Rice, K.G., Bioconjug. Chem. 21, 723 (2010).Google Scholar
Zhang, H., Mitin, A., Vinogradov, S.V., Bioconjug. Chem. 20, 120 (2009).Google Scholar
Gupta, B., Levchenko, T.S., Torchilin, V.P., Adv. Drug Deliv. Rev. 57, 637 (2005).Google Scholar
Min, S.-H., Kim, D.M., Kim, M.N., Ge, J., Lee, D.C., Park, I.Y., Park, K.C., Hwang, J.-S., Cho, C.-W., Yeom, Y.I., Biomaterials 31, 1858 (2010).CrossRefGoogle Scholar
Zhu, J., Qiu, Z., Wiese, C., Ishii, Y., Friedrichsen, J., Rajashekara, G., Splitter, G.A., J. Biol. Chem. 280, 16038 (2005).Google Scholar
Ziegler, A., Seelig, J., Biochemistry 46, 8138 (2007).Google Scholar
Callahan, J., Kopecek, J., Biomacromolecules 7, 2347 (2006).Google Scholar
D′Souza, G.G.M., Rammohan, R., Cheng, S.-M., Torchilin, V.P., Weissig, V., J. Control. Release 92, 189 (2003).Google Scholar
Weissig, V., Lasch, J., Erdos, G., Meyer, H.W., Rowe, T.C., Hughes, J., Pharm. Res. 15, 334 (1998).Google Scholar
Chen, L.B., Annu. Rev. Cell Biol. 4, 155 (1988).Google Scholar
Wallace, D C., Gene 354, 169 (2005).Google Scholar
Hoshino, A., Fujioka, K., Oku, T., Nakamura, S., Suga, M., Yamaguchi, Y., Suzuki, K., Yasuhara, M., Yamamoto, K., Microbiol. Immunol. 48, 985 (2004).Google Scholar
Lee, M., Choi, J.S., Choi, M.J., Pak, Y.K., Rhee, B.D., Ko, K.S., J. Drug Target. 15, 115 (2007).Google Scholar
Rozenzhak, S.M., Kadakia, M.P., Caserta, T.M., Westbrook, T.R., Stone, M.O., Naik, R.R., Chem. Commun. 17, 2217 (2005).Google Scholar
Vakoc, B.J., Lanning, R.M., Tyrrell, J.A., Padera, T.P., Bartlett, L.A., Stylianopoulos, T., Munn, L.L., Tearney, G.J., Fukumura, D., Jain, R.K., Bouma, B.E., Nat. Med. 15, 1219 (2009).Google Scholar
Harris, J.M., Martin, N., Modi, M., Clin. Pharmacokinet. 40, 539 (2001).Google Scholar
Harris, J.M., Chess, R.B., Nat. Rev. Drug Discov. 2, 214 (2003).Google Scholar
Owens Iii, D.E., Peppas, N.A., Int. J. Pharm. 307, 93 (2006).Google Scholar
Lee, E.S., Gao, Z., Bae, Y.H., J. Control. Release 132, 164 (2008).CrossRefGoogle Scholar
Pearson, R.M., Sunoqrot, S., Hsu, H.-J., Bae, J.W., Hong, S., Ther. Deliv. 3, 941 (2012).Google Scholar