Interactions of Renal-Clearable Gold Nanoparticles with Tumor Microenvironments: Vasculature and Acidity Effects
Prof. Dr. Mengxiao Yu
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorDr. Chen Zhou
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorProf. Dr. Li Liu
Department of Radiology, The University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390 USA
Search for more papers by this authorDr. Shanrong Zhang
Advanced Imaging Research Center, The University of Texas Southwestern Medical Center, Dallas, TX, USA
Search for more papers by this authorDr. Shasha Sun
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorJulia D. Hankins
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorCorresponding Author
Prof. Dr. Xiankai Sun
Department of Radiology, The University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390 USA
Search for more papers by this authorCorresponding Author
Prof. Dr. Jie Zheng
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorProf. Dr. Mengxiao Yu
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorDr. Chen Zhou
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorProf. Dr. Li Liu
Department of Radiology, The University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390 USA
Search for more papers by this authorDr. Shanrong Zhang
Advanced Imaging Research Center, The University of Texas Southwestern Medical Center, Dallas, TX, USA
Search for more papers by this authorDr. Shasha Sun
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorJulia D. Hankins
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorCorresponding Author
Prof. Dr. Xiankai Sun
Department of Radiology, The University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390 USA
Search for more papers by this authorCorresponding Author
Prof. Dr. Jie Zheng
Department of Chemistry and Biochemistry, The University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX, 75080 USA
Search for more papers by this authorAbstract
The success of nanomedicines in the clinic depends on our comprehensive understanding of nano–bio interactions in tumor microenvironments, which are characterized by dense leaky microvasculature and acidic extracellular pH (pHe) values. Herein, we investigated the accumulation of ultrasmall renal-clearable gold NPs (AuNPs) with and without acidity targeting in xenograft mouse models of two prostate cancer types, PC-3 and LNCaP, with distinct microenvironments. Our results show that both sets of AuNPs could easily penetrate into the tumors but their uptake and retention were mainly dictated by the tumor microvasculature and the enhanced permeability and retention effect over the entire targeting process. On the other hand, increased tumor acidity indeed enhanced the uptake of AuNPs with acidity targeting, but only for a limited period of time. By making use of simple surface chemistry, these two effects can be synchronized in time for high tumor targeting, opening new possibilities to further improve the targeting efficiencies of nanomedicines.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
ange201612647-sup-0001-misc_information.pdf4.7 MB | Supplementary |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1S. Wilhelm, A. J. Tavares, Q. Dai, S. Ohta, J. Audet, H. F. Dvorak, W. C. W. Chan, Nat. Rev. Mater. 2016, 1, 16014.
- 2
- 2aY. Kato, S. Ozawa, C. Miyamoto, Y. Maehata, A. Suzuki, T. Maeda, Y. Baba, Cancer Cell Int. 2013, 13, 89;
- 2bF. Danhier, O. Feron, V. Preat, J. Controlled Release 2010, 148, 135–146;
- 2cD. Fukumura, R. K. Jain, Microvasc. Res. 2007, 74, 72–84;
- 2dJ. M. Brown, A. J. Giaccia, Cancer Res. 1998, 58, 1408–1416.
- 3
- 3aM. X. Yu, J. Zheng, ACS Nano 2015, 9, 6655–6674;
- 3bA. Albanese, P. S. Tang, W. C. W. Chan, Annu. Rev. Biomed. Eng. 2012, 14, 1–16.
- 4
- 4aL. Yao, J. Daniels, A. Moshnikova, S. Kuznetsov, A. Ahmed, D. M. Engelman, Y. K. Reshetnyak, O. A. Andreev, Proc. Natl. Acad. Sci. USA 2013, 110, 465–470;
- 4bJ. Z. Du, T. M. Sun, W. J. Song, J. Wu, J. Wang, Angew. Chem. Int. Ed. 2010, 49, 3621–3626; Angew. Chem. 2010, 122, 3703–3708;
- 4cK. J. Zhou, Y. G. Wang, X. N. Huang, K. Luby-Phelps, B. D. Sumer, J. M. Gao, Angew. Chem. Int. Ed. 2011, 50, 6109–6114; Angew. Chem. 2011, 123, 6233–6238;
- 4dS. H. Crayton, A. Tsourkas, ACS Nano 2011, 5, 9592–9601.
- 5
- 5aX. Guo, L. Huang, Acc. Chem. Res. 2012, 45, 971–979;
- 5bM. Wang, M. Thanou, Pharmacol. Res. 2010, 62, 90–99.
- 6
- 6aH. S. Choi, W. H. Liu, F. B. Liu, K. Nasr, P. Misra, M. G. Bawendi, J. V. Frangioni, Nat. Nanotechnol. 2010, 5, 42–47;
- 6bH. S. Choi, W. Liu, P. Misra, E. Tanaka, J. P. Zimmer, B. I. Ipe, M. G. Bawendi, J. V. Frangioni, Nat. Biotechnol. 2007, 25, 1165–1170.
- 7
- 7aE. Phillips, O. Penate-Medina, P. B. Zanzonico, R. D. Carvajal, P. Mohan, Y. P. Ye, J. Humm, M. Gonen, H. Kalaigian, H. Schoder, H. W. Strauss, S. M. Larson, U. Wiesner, M. S. Bradbury, Sci. Transl. Med. 2014, 6, 260ra149;
- 7bA. A. Burns, J. Vider, H. Ow, E. Herz, O. Penate-Medina, M. Baumgart, S. M. Larson, U. Wiesner, M. Bradbury, Nano Lett. 2009, 9, 442–448.
- 8
- 8aC. Zhou, M. Long, Y. Qin, X. Sun, J. Zheng, Angew. Chem. Int. Ed. 2011, 50, 3168–3172; Angew. Chem. 2011, 123, 3226–3230;
- 8bC. Zhou, G. Y. Hao, P. Thomas, J. B. Liu, M. X. Yu, S. S. Sun, O. K. Oz, X. K. Sun, J. Zheng, Angew. Chem. Int. Ed. 2012, 51, 10118–10122; Angew. Chem. 2012, 124, 10265–10269;
- 8cJ. Xu, C. Peng, M. Yu, J. Zheng, WIREs Nanomed. Nanobiotechnol. 2017, e1453 DOI: 10.1002/wnan.1453.
- 9
- 9aM. Yu, J. Liu, X. Ning, J. Zheng, Angew. Chem. Int. Ed. 2015, 54, 15434–15438; Angew. Chem. 2015, 127, 15654–15658;
- 9bM. Yu, J. Zhou, B. Du, X. Ning, C. Authement, L. Gandee, P. Kapur, J.-T. Hsieh, J. Zheng, Angew. Chem. Int. Ed. 2016, 55, 2787–2791; Angew. Chem. 2016, 128, 2837–2841.
- 10
- 10aJ. Liu, M. Yu, C. Zhou, S. Yang, X. Ning, J. Zheng, J. Am. Chem. Soc. 2013, 135, 4978–4981;
- 10bJ. Liu, M. Yu, X. Ning, C. Zhou, S. Yang, J. Zheng, Angew. Chem. Int. Ed. 2013, 52, 12572–12576; Angew. Chem. 2013, 125, 12804–12808;
- 10cS. Tang, C. Peng, J. Xu, B. Du, Q. Wang, R. D. Vinluan, M. Yu, M. J. Kim, J. Zheng, Angew. Chem. Int. Ed. 2016, 55, 16039–16043; Angew. Chem. 2016, 128, 16273–16277;
- 10dC. Peng, X. Gao, J. Xu, B. Du, X. Ning, S. Tang, R. M. Bachoo, M. Yu, W.-P. Ge, J. Zheng, Nano Res. 2017, DOI: 10.1007/s12274-017-1472-z.
- 11
- 11aH. M. Chen, G. D. Wang, X. L. Sun, T. Todd, F. Zhang, J. Xie, B. Z. Shen, Adv. Funct. Mater. 2016, 26, 3973–3982;
- 11bH. M. Kang, J. Gravier, K. Bao, H. Wada, J. H. Lee, Y. Baek, G. El Fakhri, S. Gioux, B. P. Rubin, J. L. Coll, H. S. Choi, Adv. Mater. 2016, 28, 8162–8168;
- 11cX. L. Huang, F. Zhang, L. Zhu, K. Y. Choi, N. Guo, J. X. Guo, K. Tackett, P. Anilkumar, G. Liu, Q. M. Quan, H. S. Choi, G. Niu, Y. P. Sun, S. Lee, X. Y. Chen, ACS Nano 2013, 7, 5684–5693.
- 12K. C. Mei, J. Bai, S. Lorrio, J. T. W. Wang, K. T. Al-Jamal, Biomaterials 2016, 106, 276–285.
- 13
- 13aJ. A. Foekens, H. A. Peters, N. Grebenchtchikov, M. P. Look, M. E. Meijer-van Gelder, A. Geurts-Moespot, T. H. van der Kwast, C. G. J. Sweep, J. G. M. Klijn, Cancer Res. 2001, 61, 5407–5414;
- 13bA. Eberhard, S. Kahlert, V. Goede, B. Hemmerlein, K. H. Plate, H. G. Augustin, Cancer Res. 2000, 60, 1388–1393;
- 13cE. R. Horak, R. Leek, N. Klenk, S. Lejeune, K. Smith, N. Stuart, M. Greenall, K. Stepniewska, A. L. Harris, Lancet 1992, 340, 1120–1124.
- 14W. Jiang, B. Y. S. Kim, J. T. Rutka, W. C. W. Chan, Nat. Nanotechnol. 2008, 3, 145–150.
- 15C. K. E. Wong, B. Namdarian, J. Chua, X. Chin, R. Speirs, T. Nguyen, M. Fankhauser, J. Pedersen, A. J. Costello, N. M. Corcoran, C. M. Hovens, Br. J. Cancer 2012, 107, 1564–1573.
- 16C. Zhou, C. Sun, M. Yu, Y. Qin, J. Wang, M. Kim, J. Zheng, J. Phys. Chem. C 2010, 114, 7727–7732.
- 17M. X. Yu, C. Zhou, J. B. Liu, J. D. Hankins, J. Zheng, J. Am. Chem. Soc. 2011, 133, 11014–11017.
- 18
- 18aR. J. Gillies, Z. Liu, Z. Bhujwalla, Am. J. Physiol. 1994, 267, C 195–C203;
- 18bX. M. Zhang, Y. X. Lin, R. J. Gillies, J. Nucl. Med. 2010, 51, 1167–1170;
- 18cJ. W. Hugg, G. B. Matson, D. B. Twieg, A. A. Maudsley, D. Sappeymarinier, M. W. Weiner, Magn. Reson. Imaging 1992, 10, 227–243.
- 19A. L. Vavere, G. B. Biddlecombe, W. M. Spees, J. R. Garbow, D. Wijesinghe, O. A. Andreev, D. M. Engelman, Y. K. Reshetnyak, J. S. Lewis, Cancer Res. 2009, 69, 4510–4516.
- 20
- 20aH. Maeda, H. Nakamura, J. Fang, Adv. Drug Delivery Rev. 2013, 65, 71–79;
- 20bJ. Fang, H. Nakamura, H. Maeda, Adv. Drug Delivery Rev. 2011, 63, 136–151;
- 20cA. K. Iyer, G. Khaled, J. Fang, H. Maeda, Drug Discovery Today 2006, 11, 812–818.
- 21H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kimura, Y. Terada, M. R. Kano, K. Miyazono, M. Uesaka, N. Nishiyama, K. Kataoka, Nat. Nanotechnol. 2011, 6, 815–823.
- 22C. A. Boswell, D. B. Tesar, K. Mukhyala, F. P. Theil, P. J. Fielder, L. A. Khawli, Bioconjugate Chem. 2010, 21, 2153–2163.
- 23P. Caliceti, F. M. Veronese, Adv. Drug Delivery Rev. 2003, 55, 1261–1277.
- 24S. D. Perrault, C. Walkey, T. Jennings, H. C. Fischer, W. C. W. Chan, Nano Lett. 2009, 9, 1909–1915.
- 25E. A. Sykes, Q. Dai, C. D. Sarsons, J. Chen, J. V. Rocheleau, D. M. Hwang, G. Zheng, D. T. Cramb, K. D. Rinker, W. C. W. Chan, Proc. Natl. Acad. Sci. USA 2016, 113, E 1142–E1151.
- 26R. Gutmann, M. Leunig, J. Feyh, A. E. Goetz, K. Messmer, E. Kastenbauer, R. K. Jain, Cancer Res. 1992, 52, 1993–1995.
- 27S. Ohta, D. Glancy, W. C. W. Chan, Science 2016, 351, 841–845.
Citing Literature
This is the
German version
of Angewandte Chemie.
Note for articles published since 1962:
Do not cite this version alone.
Take me to the International Edition version with citable page numbers, DOI, and citation export.
We apologize for the inconvenience.