Guiding nanomaterials to tumors for breast cancer precision medicine: from tumor-targeting small-molecule discovery to targeted nanodrug delivery

Abeylath, S. C., Ganta, S., Iyer, A. K. & Amiji, M. Combinatorial-designed multifunctional polymeric nanosystems for tumor-targeted therapeutic delivery. Acc. Chem. Res. 44, 1009–1017 (2011).

Caldorera-Moore, M. E., Liechty, W. B. & Peppas, N. A. Responsive theranostic systems: integration of diagnostic imaging agents and responsive controlled release drug delivery carriers. Acc. Chem. Res. 44, 1061–1070 (2011).

Shi, J. J., Xiao, Z. Y., Kamaly, N. & Farokhzad, O. C. Self-assembled targeted nanoparticles: evolution of technologies and bench to bedside translation. Acc. Chem. Res. 44, 1123–1134 (2011).

Koo, H., Huh, M. S., Sun, I. C., Yuk, S. H., Choi, K., Kim, K. & Kwon, I. C. In vivo targeted delivery of nanoparticles for theranosis. Acc. Chem. Res. 44, 1018–1028 (2011).

Scott, A. M., Wolchok, J. D. & Old, L. J. Antibody therapy of cancer. Nat. Rev. Cancer 12, 278–287 (2012).

Loo, D. T. & Mather, J. P. Antibody-based identification of cell surface antigens: targets for cancer therapy. Curr. Opin. Pharmacol. 8, 627–631 (2008).

Trikha, M., Corringham, R., Klein, B. & Rossi, J. F. Targeted anti-interleukin-6 monoclonal antibody therapy for cancer: a review of the rationale and clinical evidence. Clin. Cancer Res. 9, 4653–4665 (2003).

Schrama, D., Reisfeld, R. A. & Becker, J. C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov. 5, 147–159 (2006).

Milenic, D. E., Brady, E. D. & Brechbiel, M. W. Antibody-targeted radiation cancer therapy. Nat. Rev. Drug Discov. 3, 488–498 (2004).

Srinivasarao, M., Galliford, C. V. & Low, P. S. Principles in the design of ligand-targeted cancer therapeutics and imaging agents. Nat. Rev. Drug Discov. 14, 203–219 (2015).

Hilgenbrink, A. R. & Low, P. S. Folate receptor-mediated drug targeting: from therapeutics to diagnostics. J. Pharm. Sci. 94, 2135–2146 (2005).

Paulos, C. M., Turk, M. J., Breur, G. J. & Low, P. S. Folate receptor-mediated targeting of therapeutic and imaging agents to activated macrophages in rheumatoid arthritis. Adv. Drug Delivery Rev. 56, 1205–1217 (2004).

Landmark, K. J., DiMaggio, S., Ward, J., Kelly, C. V., Vogt, S., Hong, S., Kotlyar, A., Myc, A., Thomas, T. P., Penner-Hahn, J. E., Baker, J. R., Holl, M. M.B. & Orr, B. G. Synthesis, characterization, and in vitro testing of superparamagnetic iron oxide nanoparticles targeted using folic acid-conjugated dendrimers. ACS Nano 2, 773–783 (2008).

Fan, N. C., Cheng, F. Y., Ho, J. A.A. & Yeh, C. S. Photocontrolled targeted drug delivery: photocaged biologically active folic acid as a light-responsive tumor-targeting molecule. Angew. Chem. Int. Ed. 51, 8806–8810 (2012).

Zuber, G., Zammut-Italiano, L., Dauty, E. & Behr, J. P. Targeted gene delivery to cancer cells: directed assembly of nanometric DNA particles coated with folic acid. Angew. Chem. Int. Ed. 42, 2666–2669 (2003).

Lee, Y. H., Lee, H., Kim, Y. B., Kim, J. Y., Hyeon, T., Park, H., Messersmith, P. B. & Park, T. G. Bioinspired surface immobilization of hyaluronic acid on monodisperse magnetite nanocrystals for targeted cancer imaging. Adv. Mater. 20, 4154–4157 (2008).

Cho, H. J., Yoon, H. Y., Koo, H., Ko, S. H., Shim, J. S., Lee, J. H., Kim, K., Kwon, I. C. & Kim, D. D. Self-assembled nanoparticles based on hyaluronic acid-ceramide (HA-CE) and Pluronic (R) for tumor-targeted delivery of docetaxel. Biomaterials 32, 7181–7190 (2011).

Jiang, T. Y., Zhang, Z. H., Zhang, Y. L., Lv, H. X., Zhou, J. P., Li, C. C., Hou, L. L. & Zhang, Q. Dual-functional liposomes based on pH-responsive cell-penetrating peptide and hyaluronic acid for tumor-targeted anticancer drug delivery. Biomaterials 33, 9246–9258 (2012).

Li, J. C., He, Y., Sun, W. J., Luo, Y., Cai, H. D., Pan, Y. Q., Shen, M. W., Xia, J. D. & Shi, X. Y. Hyaluronic acid-modified hydrothermally synthesized iron oxide nanoparticles for targeted tumor MR imaging. Biomaterials 35, 3666–3677 (2014).

Chen, C., Ke, J. Y., Zhou, X. E., Yi, W., Brunzelle, J. S., Li, J., Yong, E. L., Xu, H. E. & Melcher, K. Structural basis for molecular recognition of folic acid by folate receptors. Nature 500, 486–489 (2013).

Mankoff, D. A., Link, J. M., Linden, H. M., Sundararajan, L. & Krohn, K. A. Tumor receptor imaging. J. Nucl. Med. 49, 149s–163s (2008).

Zhao, X. B., Li, H. & Lee, R. J. Targeted drug delivery via folate receptors. Expert Opin. Drug Deliv. 5, 309–319 (2008).

Ahrens, T., Assmann, V., Fieber, C., Termeer, C. C., Herrlich, P., Hofmann, M. & Simon, J. C. CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation. J. Invest. Dermatol. 116, 93–101 (2001).

Collins, F. S. & Varmus, H. A new initiative on precision medicine. N. Engl. J. Med. 372, 793–795 (2015).

Schork, N. J. Time for one-person trials. Nature 520, 609–611 (2015).

Huang, X. H., El-Sayed, I. H., Qian, W. & El-Sayed, M. A. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Chem. Soc. 128, 2115–2120 (2006).

Cho, S. K., Emoto, K., Su, L. J., Yang, X., Flaig, T. W. & Park, W. Functionalized gold nanorods for thermal ablation treatment of bladder cancer. J. Biomed. Nanotechnol. 10, 1267–1276 (2014).

Cheng, Y., Meyers, J. D., Agnes, R. S., Doane, T. L., Kenney, M. E., Broome, A. M., Burda, C. & Basilion, J. P. Addressing brain tumors with targeted gold nanoparticles: a new gold standard for hydrophobic drug delivery? Small 7, 2301–2306 (2011).

von Maltzahn, G., Park, J. H., Agrawal, A., Bandaru, N. K., Das, S. K., Sailor, M. J. & Bhatia, S. N. Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Res. 69, 3892–3900 (2009).

Arap, W., Pasqualini, R. & Ruoslahti, E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279, 377–380 (1998).

Matsuo, A. L., Juliano, M. A., Figueiredo, C. R., Batista, W. L., Tanaka, A. S. & Travassos, L. R. A new phage-display tumor-homing peptide fused to antiangiogenic peptide generates a novel bioactive molecule with antimelanoma activity. Mol. Cancer Res. 9, 1471–1478 (2011).

Du, B., Han, H. H., Wang, Z. Q., Kuang, L. S., Wang, L., Yu, L. P., Wu, M. A., Zhou, Z. L. & Qian, M. Targeted drug delivery to hepatocarcinoma in vivo by phage-displayed specific binding peptide. Mol. Cancer Res. 8, 135–144 (2010).

Newton, J. R., Kelly, K. A., Mahmood, U., Weissleder, R. & Deutscher, S. L. In vivo selection of phage for the optical Imaging of PC-3 human prostate carcinoma in mice. Neoplasia 8, 772–780 (2006).

Wang, T., Hartner, W. C., Gillespie, J. W., Praveen, K. P., Yang, S. H., Mei, L. A., Petrenko, V. A. & Torchilin, V. P. Enhanced tumor delivery and antitumor activity in vivo of liposomal doxorubicin modified with MCF-7-specific phage fusion protein. Nanomedicine 10, 421–430 (2014).

Wang, T., D'Souza, G. G. M., Bedi, D., Fagbohun, O. A., Potturi, L. P., Papahadjopoulos-Sternberg, B., Petrenko, V. A. & Torchilin, V. P. Enhanced binding and killing of target tumor cells by drug-loaded liposomes modified with tumor-specific phage fusion coat protein. Nanomed 5, 563–574 (2010).

Wang, T., Petrenko, V. A. & Torchilin, V. P. Paclitaxel-loaded polymeric micelles modified with MCF-7 cell-specific phage protein: enhanced binding to target cancer cells and increased cytotoxicity. Mol. Pharm. 7, 1007–1014 (2010).

Wang, T., Yang, S. H., Petrenko, V. A. & Torchilin, V. P. Cytoplasmic delivery of liposomes into MCF-7 breast cancer cells mediated by cell-specific phage fusion coat protein. Mol. Pharm. 7, 1149–1158 (2010).