ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img
RETURN TO ISSUEPREVResearch ArticleNEXT

A Versatile Carbonic Anhydrase IX Targeting Ligand-Functionalized Porous Silicon Nanoplatform for Dual Hypoxia Cancer Therapy and Imaging

View Author Information
Department of Biothermodynamics and Drug Design, Institute of Biotechnology, Vilnius University, LT-10257 Vilnius, Lithuania
Division of Pharmaceutical Chemistry and Technology, Drug Research Program, Faculty of Pharmacy, University of Helsinki, FI-00014 Helsinki, Finland
§ Laboratory of Industrial Physics, Department of Physics, University of Turku, FI-20014 Turku, Finland
Shanghai Institute of Ceramics, Chinese Academy of Sciences, Shanghai 200050, China
Department of Pharmaceutical Science, Åbo Akademi University, FI-20520 Turku, Finland
# Department of Drug chemistry, Faculty of Pharmacy, Lithuanian University of Health Sciences, LT-44307 Kaunas, Lithuania
*(H.Z.) E-mail [email protected]
*(V.P.) E-mail [email protected]
*(H.A.S.) E-mail [email protected]
Cite this: ACS Appl. Mater. Interfaces 2017, 9, 16, 13976–13987
Publication Date (Web):April 6, 2017
https://doi.org/10.1021/acsami.7b04038
Copyright © 2017 American Chemical Society

    Article Views

    1233

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (1)»

    Abstract

    Abstract Image

    Hypoxia occurs in most solid tumors, and it has been shown to be an independent prognostic indicator of a poor clinical outcome for patients with various cancers. Therefore, constructing a nanosystem specifically targeting cancer cells under hypoxia conditions is a promising approach for cancer therapy. Herein, we develop a porous silicon (PSi)-based nanosystem for targeted cancer therapy. VD11-4-2, a novel inhibitor for carbonic anhydrase IX (CA IX), is anchored on PSi particles (VD-PSi). As CA IX is mainly expressed on the cancer cell membrane under hypoxia condition, this nanocomplex inherits a strong affinity toward hypoxic human breast adenocarcinoma (MCF-7) cells; thus, a better killing efficiency for the hypoxia-induced drug resistance cancer cell is observed. Furthermore, the release of doxorubicin (DOX) from VD-PSi showed pH dependence, which is possibly due to the hydrogen-bonding interaction between DOX and VD11-4-2. The fluorescence resonance energy transfer effect between DOX and VD11-4-2 is observed and applied for monitoring the DOX release intracellularly. Protein inhibition and binding assays showed that VD-PSi binds and inhibits CA IX. Overall, we developed a novel nanosystem inheriting several advantageous properties, which has great potential for targeted treatment of cancer cells under hypoxic conditions.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.7b04038.

    • Additional experimental details (fabrication of PSi, the selection of PEG linker, quantitative conjugating efficacy, fluorescent thermal shift assay), particles size and zeta potential changes, TEM images, VD11-4-2 and DOX fluorescence spectra; FRET spectra, protein binding and inhibition, pH changes, cell viability results (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 45 publications.

    1. Gediminas Žvinys, Agne Petrosiute, Audrius Zakšauskas, Asta Zubrienė, Alvilė Ščerbavičienė, Zane Kalnina, Edita Čapkauskaitė, Vaida Juozapaitienė, Aurelija Mickevičiu̅tė, Kirill Shubin, Švitrigailė Grincevičienė, Steponas Raišys, Kaspars Tars, Jurgita Matulienė, Daumantas Matulis. High-Affinity NIR-Fluorescent Inhibitors for Tumor Imaging via Carbonic Anhydrase IX. Bioconjugate Chemistry 2024, Article ASAP.
    2. De-Xiang Zhang, Terence Tieu, Lars Esser, Marcin Wojnilowicz, Chieh-Hua Lee, Anna Cifuentes-Rius, Helmut Thissen, Nicolas H. Voelcker. Differential Surface Engineering Generates Core–Shell Porous Silicon Nanoparticles for Controlled and Targeted Delivery of an Anticancer Drug. ACS Applied Materials & Interfaces 2022, 14 (49) , 54539-54549. https://doi.org/10.1021/acsami.2c16370
    3. Agne Janoniene, Vilma Petrikaite. In Search of Advanced Tumor Diagnostics and Treatment: Achievements and Perspectives of Carbonic Anhydrase IX Targeted Delivery. Molecular Pharmaceutics 2020, 17 (6) , 1800-1815. https://doi.org/10.1021/acs.molpharmaceut.0c00180
    4. Meihua Luo, Guido Lewik, Julian Charles Ratcliffe, Chung Hang Jonathan Choi, Ermei Mäkilä, Wing Yin Tong, Nicolas H. Voelcker. Systematic Evaluation of Transferrin-Modified Porous Silicon Nanoparticles for Targeted Delivery of Doxorubicin to Glioblastoma. ACS Applied Materials & Interfaces 2019, 11 (37) , 33637-33649. https://doi.org/10.1021/acsami.9b10787
    5. Terence Tieu, Sameer Dhawan, V. Haridas, Lisa M. Butler, Helmut Thissen, Anna Cifuentes-Rius, Nicolas H. Voelcker. Maximizing RNA Loading for Gene Silencing Using Porous Silicon Nanoparticles. ACS Applied Materials & Interfaces 2019, 11 (26) , 22993-23005. https://doi.org/10.1021/acsami.9b05577
    6. Ahmed M. Shabana Marc A. Ilies . Drug Delivery to Hypoxic Tumors Targeting Carbonic Anhydrase IX. 2019, 223-252. https://doi.org/10.1021/bk-2019-1309.ch010
    7. Jitka Neburkova, Frantisek Sedlak, Jirina Zackova Suchanova, Libor Kostka, Pavel Sacha, Vladimir Subr, Tomas Etrych, Petr Simon, Jitka Barinkova, Robin Krystufek, Hana Spanielova, Jitka Forstova, Jan Konvalinka, Petr Cigler. Inhibitor–GCPII Interaction: Selective and Robust System for Targeting Cancer Cells with Structurally Diverse Nanoparticles. Molecular Pharmaceutics 2018, 15 (8) , 2932-2945. https://doi.org/10.1021/acs.molpharmaceut.7b00889
    8. Isaac S. Marks, Spencer S. Gardeen, Sarah J. Kurdziel, Sonia T. Nicolaou, J. Evan Woods, Sumith A. Kularatne, Philip S. Low. Development of a Small Molecule Tubulysin B Conjugate for Treatment of Carbonic Anhydrase IX Receptor Expressing Cancers. Molecular Pharmaceutics 2018, 15 (6) , 2289-2296. https://doi.org/10.1021/acs.molpharmaceut.8b00139
    9. Mohamed J. Saadh, Mohammed Ahmed Mustafa, Laith Yassen Qassem, Ghadir Kamil Ghadir, Mohd Alaraj, Mahmood Hasen Shuhata Alubiady, Salah Hassan Zain Al-Abdeen, Hussein Ghafel Shakier, Mohammad Y. Alshahrani, Ahmed Hussein Zwamel. Targeting hypoxic and acidic tumor microenvironment by nanoparticles: A review. Journal of Drug Delivery Science and Technology 2024, 96 , 105660. https://doi.org/10.1016/j.jddst.2024.105660
    10. Hongjian Liao, Yuchao Cao, Can Hu, Shangfeng Shen, Zhifei Zhang, Dairong Li, Yonghong Du. Oxygen-producing and pH-responsive targeted DNA nanoflowers for enhanced chemo-sonodynamic therapy of lung cancer. Materials Today Bio 2024, 25 , 101005. https://doi.org/10.1016/j.mtbio.2024.101005
    11. Xinyue Cui, Zhuang Hu, Ruihan Li, Peng Jiang, Yongchang Wei, Zilin Chen. CA IX-targeted Ag2S Quantum Dots Bioprobe for NIR-II Imaging-guided Hypoxia tumor Chemo-Photothermal Therapy. Journal of Pharmaceutical Analysis 2024, 16 , 100969. https://doi.org/10.1016/j.jpha.2024.100969
    12. Liang Chen, Shanshan Zhang, Yanqiu Duan, Xinran Song, Meiqi Chang, Wei Feng, Yu Chen. Silicon-containing nanomedicine and biomaterials: materials chemistry, multi-dimensional design, and biomedical application. Chemical Society Reviews 2024, 53 (3) , 1167-1315. https://doi.org/10.1039/D1CS01022K
    13. Jian-Shuang Guo, Juan-Juan Li, Ze-Han Wang, Yang Liu, Yu-Xin Yue, Hua-Bin Li, Xiu-He Zhao, Yuan-Jun Sun, Ya-Hui Ding, Fei Ding, Dong-Sheng Guo, Liang Wang, Yue Chen. Dual hypoxia-responsive supramolecular complex for cancer target therapy. Nature Communications 2023, 14 (1) https://doi.org/10.1038/s41467-023-41388-2
    14. Nian Liu, Qian Lin, Wenbao Zuo, Weibin Chen, Shan Huang, Yinshu Han, Xing-Jie Liang, Xuan Zhu, Shuaidong Huo. Carbonic anhydrase IX-targeted nanovesicles potentiated ferroptosis by remodeling the intracellular environment for synergetic cancer therapy. Nanoscale Horizons 2023, 8 (6) , 783-793. https://doi.org/10.1039/D2NH00494A
    15. Vilma Petrikaite, Nicola D'Avanzo, Christian Celia, Massimo Fresta. Nanocarriers overcoming biological barriers induced by multidrug resistance of chemotherapeutics in 2D and 3D cancer models. Drug Resistance Updates 2023, 68 , 100956. https://doi.org/10.1016/j.drup.2023.100956
    16. Gholamali Farzi, Maedeh Gheysipour. Encapsulation with polymers. 2023, 3-38. https://doi.org/10.1016/B978-0-12-824345-9.00010-6
    17. Muhammad Umair Amin, Sajid Ali, Muhammad Yasir Ali, Dominik C. Fuhrmann, Imran Tariq, Benjamin S. Seitz, Eduard Preis, Jana Brüßler, Bernhard Brüne, Udo Bakowsky. Co-delivery of carbonic anhydrase IX inhibitor and doxorubicin as a promising approach to address hypoxia-induced chemoresistance. Drug Delivery 2022, 29 (1) , 2072-2085. https://doi.org/10.1080/10717544.2022.2092234
    18. Siavash Shariatzadeh, Negin Moghimi, Farima Khalafi, Sepehr Shafiee, Mohsen Mehrabi, Saba Ilkhani, Foad Tosan, Pooria Nakhaei, Ali Alizadeh, Rajender S. Varma, Mohammad Taheri. Metallic Nanoparticles for the Modulation of Tumor Microenvironment; A New Horizon. Frontiers in Bioengineering and Biotechnology 2022, 10 https://doi.org/10.3389/fbioe.2022.847433
    19. Agne Janoniene, Linas Mazutis, Daumantas Matulis, Vilma Petrikaite. Inhibition of Carbonic Anhydrase IX Suppresses Breast Cancer Cell Motility at the Single-Cell Level. International Journal of Molecular Sciences 2021, 22 (21) , 11571. https://doi.org/10.3390/ijms222111571
    20. Xiaoyu Xu, Chang Liu, Yonghui Wang, Oliver Koivisto, Junnian Zhou, Yilai Shu, Hongbo Zhang. Nanotechnology-based delivery of CRISPR/Cas9 for cancer treatment. Advanced Drug Delivery Reviews 2021, 176 , 113891. https://doi.org/10.1016/j.addr.2021.113891
    21. Bárbara B. Mendes, Diana P. Sousa, João Conniot, João Conde. Nanomedicine-based strategies to target and modulate the tumor microenvironment. Trends in Cancer 2021, 7 (9) , 847-862. https://doi.org/10.1016/j.trecan.2021.05.001
    22. Edgar Pérez-Herrero, Alberto Fernández-Medarde. The reversed intra- and extracellular pH in tumors as a unified strategy to chemotherapeutic delivery using targeted nanocarriers. Acta Pharmaceutica Sinica B 2021, 11 (8) , 2243-2264. https://doi.org/10.1016/j.apsb.2021.01.012
    23. Selvaraj Kunjiappan, Parasuraman Pavadai, Sivakumar Vellaichamy, Sureshbabu Ram Kumar Pandian, Vigneshwaran Ravishankar, Ponnusamy Palanisamy, Saravanan Govindaraj, Gowshiki Srinivasan, Adhvitha Premanand, Murugesan Sankaranarayanan, Panneerselvam Theivendren. Surface receptor‐mediated targeted drug delivery systems for enhanced cancer treatment: A state‐of‐the‐art review. Drug Development Research 2021, 82 (3) , 309-340. https://doi.org/10.1002/ddr.21758
    24. Ilaria Arduino, Zehua Liu, Antti Rahikkala, Patrícia Figueiredo, Alexandra Correia, Annalisa Cutrignelli, Nunzio Denora, Hélder A. Santos. Preparation of cetyl palmitate-based PEGylated solid lipid nanoparticles by microfluidic technique. Acta Biomaterialia 2021, 121 , 566-578. https://doi.org/10.1016/j.actbio.2020.12.024
    25. Terence Tieu, Marcin Wojnilowicz, Pie Huda, Kristofer J. Thurecht, Helmut Thissen, Nicolas H. Voelcker, Anna Cifuentes-Rius. Nanobody-displaying porous silicon nanoparticles for the co-delivery of siRNA and doxorubicin. Biomaterials Science 2021, 9 (1) , 133-147. https://doi.org/10.1039/D0BM01335H
    26. Simonas Daunys, Agnė Janonienė, Indrė Januškevičienė, Miglė Paškevičiūtė, Vilma Petrikaitė. 3D Tumor Spheroid Models for In Vitro Therapeutic Screening of Nanoparticles. 2021, 243-270. https://doi.org/10.1007/978-3-030-58174-9_11
    27. Patrícia Figueiredo, Hélder A. Santos. Requirements and properties of biomaterials for biomedical applications. 2021, 195-226. https://doi.org/10.1016/B978-0-12-820303-3.00009-6
    28. Jean-Yves Winum. Nanostructures and innovative delivery systems for overcoming cancer resistance. 2021, 185-201. https://doi.org/10.1016/B978-0-12-820701-7.00002-6
    29. F. Fontana, Z. Liu, J. Hirvonen, H.A. Santos. Porous silicon materials for cancer and immunotherapy. 2021, 571-609. https://doi.org/10.1016/B978-0-12-821677-4.00020-3
    30. Yuna Jung, Youngbuhm Huh, Dokyoung Kim. Recent advances in surface engineering of porous silicon nanomaterials for biomedical applications. Microporous and Mesoporous Materials 2021, 310 , 110673. https://doi.org/10.1016/j.micromeso.2020.110673
    31. Fei Gong, Nailin Yang, Xianwen Wang, Qi Zhao, Qian Chen, Zhuang Liu, Liang Cheng. Tumor microenvironment-responsive intelligent nanoplatforms for cancer theranostics. Nano Today 2020, 32 , 100851. https://doi.org/10.1016/j.nantod.2020.100851
    32. Ulrika Jakobsson, Ermei Mäkilä, Antti Rahikkala, Surachet Imlimthan, Jarkko Lampuoti, Sanjeev Ranjan, Jouni Heino, Pasi Jalkanen, Ulli Köster, Kenichiro Mizohata, Hélder A. Santos, Jarno Salonen, Anu J. Airaksinen, Mirkka Sarparanta, Kerttuli Helariutta. Preparation and in vivo evaluation of red blood cell membrane coated porous silicon nanoparticles implanted with 155Tb. Nuclear Medicine and Biology 2020, 84-85 , 102-110. https://doi.org/10.1016/j.nucmedbio.2020.04.001
    33. Zehua Liu, Flavia Fontana, Andre Python, Jouni T. Hirvonen, Hélder A. Santos. Microfluidics for Production of Particles: Mechanism, Methodology, and Applications. Small 2020, 16 (9) https://doi.org/10.1002/smll.201904673
    34. Patrícia Figueiredo, Flavia Fontana, Hélder A. Santos. Nanomedicine Therapies. 2020, 373-400. https://doi.org/10.1002/9783527344406.ch13
    35. Jiachen Li, Weiwei Zhang, Yan Gao, Haibei Tong, Zhenyu Chen, Jisen Shi, Hélder A. Santos, Bing Xia. Near-infrared light and magnetic field dual-responsive porous silicon-based nanocarriers to overcome multidrug resistance in breast cancer cells with enhanced efficiency. Journal of Materials Chemistry B 2020, 8 (3) , 546-557. https://doi.org/10.1039/C9TB02340B
    36. De-Xiang Zhang, Lars Esser, Roshan B Vasani, Helmut Thissen, Nicolas H Voelcker. Porous Silicon Nanomaterials: Recent Advances in Surface Engineering for Controlled drug-delivery Applications. Nanomedicine 2019, 14 (24) , 3213-3230. https://doi.org/10.2217/nnm-2019-0167
    37. Patrícia Figueiredo, Mika H. Sipponen, Kalle Lintinen, Alexandra Correia, Alexandros Kiriazis, Jari Yli‐Kauhaluoma, Monika Österberg, Anne George, Jouni Hirvonen, Mauri A. Kostiainen, Hélder A. Santos. Preparation and Characterization of Dentin Phosphophoryn‐Derived Peptide‐Functionalized Lignin Nanoparticles for Enhanced Cellular Uptake. Small 2019, 15 (24) https://doi.org/10.1002/smll.201901427
    38. Jaime A Espinoza, Ismael Riquelme, Eduardo A Sagredo, Lorena Rosa, Patricia García, Carolina Bizama, María Apud‐Bell, Pamela Leal, Helga Weber, Felipe Benavente, Sergio Vargas, Diego Romero, Alexis M Kalergis, Juan Carlos Roa. Mucin 5B, carbonic anhydrase 9 and claudin 18 are potential theranostic markers of gallbladder carcinoma. Histopathology 2019, 74 (4) , 597-607. https://doi.org/10.1111/his.13797
    39. Miglė Paškevičiūtė, Vilma Petrikaitė. Overcoming transporter-mediated multidrug resistance in cancer: failures and achievements of the last decades. Drug Delivery and Translational Research 2019, 9 (1) , 379-393. https://doi.org/10.1007/s13346-018-0584-7
    40. Fengye Mo, Zhangyan Ma, Tengteng Wu, Meiling Liu, Youyu Zhang, Haitao Li, Shouzhuo Yao. Holey reduced graphene oxide inducing sensitivity enhanced detection nanoplatform for cadmium ions based on glutathione-gold nanocluster. Sensors and Actuators B: Chemical 2019, 281 , 486-492. https://doi.org/10.1016/j.snb.2018.10.133
    41. Terence Tieu, Maria Alba, Roey Elnathan, Anna Cifuentes‐Rius, Nicolas H. Voelcker. Advances in Porous Silicon–Based Nanomaterials for Diagnostic and Therapeutic Applications. Advanced Therapeutics 2019, 2 (1) https://doi.org/10.1002/adtp.201800095
    42. Jingjing Liu, Qian Chen, Liangzhu Feng, Zhuang Liu. Nanomedicine for tumor microenvironment modulation and cancer treatment enhancement. Nano Today 2018, 21 , 55-73. https://doi.org/10.1016/j.nantod.2018.06.008
    43. Zehua Liu, Yunzhan Li, Wei Li, Chen Xiao, Dongfei Liu, Chao Dong, Ming Zhang, Ermei Mäkilä, Marianna Kemell, Jarno Salonen, Jouni T. Hirvonen, Hongbo Zhang, Dawang Zhou, Xianming Deng, Hélder A. Santos. Multifunctional Nanohybrid Based on Porous Silicon Nanoparticles, Gold Nanoparticles, and Acetalated Dextran for Liver Regeneration and Acute Liver Failure Theranostics. Advanced Materials 2018, 30 (24) https://doi.org/10.1002/adma.201703393
    44. Wei Li, Zehua Liu, Flavia Fontana, Yaping Ding, Dongfei Liu, Jouni T. Hirvonen, Hélder A. Santos. Tailoring Porous Silicon for Biomedical Applications: From Drug Delivery to Cancer Immunotherapy. Advanced Materials 2018, 30 (24) https://doi.org/10.1002/adma.201703740
    45. Patrícia Figueiredo, Tomás Bauleth-Ramos, Jouni Hirvonen, Bruno Sarmento, Hélder A. Santos. The Emerging Role of Multifunctional Theranostic Materials in Cancer Nanomedicine. 2018, 1-31. https://doi.org/10.1016/B978-0-12-813339-2.00001-3

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect