A Multifunctional, Highly Biocompatible, and Double-Triggering Caramelized Nanotheranostic System Loaded with Fe₃O₄ and DOX for Combined Chemo-Photothermal Therapy and Real-Time Magnetic Resonance Imaging Monitoring of Triple Negative Breast Cancer

References

• Wilkinson L, Gathani T. Understanding breast cancer as a global health concern. Br J Radiol. 2022;95(1130):20211033. doi:10.1259/bjr.20211033
   PubMed Web of Science ®Google Scholar
• Xiao Y, Ma D, Yang YS, et al. Comprehensive metabolomics expands precision medicine for triple-negative breast cancer. Cell Res. 2022;32(5):477–490. doi:10.1038/s41422-022-00614-0
   PubMed Web of Science ®Google Scholar
• Al-Mahmood S, Sapiezynski J, Garbuzenko OB, Minko T. Metastatic and triple-negative breast cancer: challenges and treatment options. Drug Deliv Transl Res. 2018;8(5):1483–1507. doi:10.1007/s13346-018-0551-3
   PubMed Web of Science ®Google Scholar
• Lee KL, Kuo YC, Ho YS, Huang YH. Triple-negative breast cancer: current understanding and future therapeutic breakthrough targeting cancer stemness. Cancers. 2019;11(9):1334. doi:10.3390/cancers11091334
   PubMed Web of Science ®Google Scholar
• Matsen CB, Neumayer LA. Breast cancer: a review for the general surgeon. JAMA Surg. 2013;148(10):971–979. doi:10.1001/jamasurg.2013.3393
   PubMed Web of Science ®Google Scholar
• Maughan KL, Lutterbie MA, Ham PS. Treatment of breast cancer. Am Fam Physician. 2010;81(11):1339–1346.
   PubMed Web of Science ®Google Scholar
• Oh Y, Jin JO, Oh J. Photothermal-triggered control of sub-cellular drug accumulation using doxorubicin-loaded single-walled carbon nanotubes for the effective killing of human breast cancer cells. Nanotechnology. 2017;28(12):125101. doi:10.1088/1361-6528/aa5d7d
   PubMed Web of Science ®Google Scholar
• Fan X, Yuan Z, Shou C, et al. cRGD-conjugated Fe3O4@PDA-DOX multifunctional nanocomposites for MRI and antitumor chemo-photothermal therapy. Int J Nanomedicine. 2019;14:9631–9645. doi:10.2147/IJN.S222797
   PubMed Web of Science ®Google Scholar
• Suo A, Qian J, Zhang Y, Liu R, Xu W, Wang H. Comb-like amphiphilic polypeptide-based copolymer nanomicelles for co-delivery of doxorubicin and P-gp siRNA into MCF-7 cells. Mater Sci Eng C Mater Biol Appl. 2016;62:564–573. doi:10.1016/j.msec.2016.02.007
   PubMed Web of Science ®Google Scholar
• Shen S, Ding B, Zhang S, et al. Near-infrared light-responsive nanoparticles with thermosensitive yolk-shell structure for multimodal imaging and chemo-photothermal therapy of tumor. Nanomedicine. 2017;13(5):1607–1616. doi:10.1016/j.nano.2017.02.014
   PubMed Web of Science ®Google Scholar
• Yin L, Duan JJ, Bian XW, Yu SC. Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Res. 2020;22(1):61. doi:10.1186/s13058-020-01296-5
   PubMed Web of Science ®Google Scholar
• Forrai G, Kovács E, Ambrózay É, et al. Use of diagnostic imaging modalities in modern screening, diagnostics and management of breast tumours 1st central-eastern European professional consensus statement on breast cancer. Pathol Oncol Res. 2022;28:1610382. doi:10.3389/pore.2022.1610382
   PubMed Web of Science ®Google Scholar
• Mo T, Brandal SHB, Köhn-Luque A, et al. Quantification of tumor hypoxia through unsupervised modelling of consumption and supply hypoxia MR imaging in breast cancer. Cancers. 2022;14(5):1326. doi:10.3390/cancers14051326
   PubMed Web of Science ®Google Scholar
• Nian D, Shi P, Sun J, Ren L, Hao X, Han J. Application of luteinizing hormone-releasing hormone-ferrosoferric oxide nanoparticles in targeted imaging of breast tumors. J Int Med Res. 2019;47(4):1749–1757. doi:10.1177/0300060519834457
   PubMed Web of Science ®Google Scholar
• Chen Z, Wang Q, Wang H, et al. Ultrathin PEGylated W18O49 nanowires as a new 980 nm-laser-driven photothermal agent for efficient ablation of cancer cells in vivo. Adv Mater. 2013;25(14):2095–2100. doi:10.1002/adma.201204616
   PubMed Web of Science ®Google Scholar
• Melancon MP, Lu W, Zhong M, et al. Targeted multifunctional gold-based nanoshells for magnetic resonance-guided laser ablation of head and neck cancer. Biomaterials. 2011;32(30):7600–7608. doi:10.1016/j.biomaterials.2011.06.039
   PubMed Web of Science ®Google Scholar
• Khafaji M, Zamani M, Golizadeh M, Bavi O. Inorganic nanomaterials for chemo/photothermal therapy: a promising horizon on effective cancer treatment. Biophys Rev. 2019;11(3):335–352. doi:10.1007/s12551-019-00532-3
   PubMedGoogle Scholar
• Shao F, Pan Z, Long Y, et al. Nectin-4-targeted immunoSPECT/CT imaging and photothermal therapy of triple-negative breast cancer. J Nanobiotechnology. 2022;20(1):243. doi:10.1186/s12951-022-01444-3
   PubMed Web of Science ®Google Scholar
• Mishra SK, Dhadve AC, Mal A, et al. Photothermal therapy (PTT) is an effective treatment measure against solid tumors which fails to respond conventional chemo/radiation therapies in clinic. Biomater Adv. 2022;143:213153. doi:10.1016/j.bioadv.2022.213153
   PubMedGoogle Scholar
• Avila-Flores R, Medellin RA. Ecological, taxonomic, and physiological correlates of cave use by Mexican bats. J Mammal. 2004;85(4):675–687. doi:10.1644/Bos-127
   Web of Science ®Google Scholar
• Lambert TN, Andrews NL, Gerung H, et al. Water-soluble germanium(0) nanocrystals: cell recognition and near-infrared photothermal conversion properties. Small. 2007;3(4):691–699. doi:10.1002/smll.200600529
   PubMed Web of Science ®Google Scholar
• Huang X, Tang S, Liu B, Ren B, Zheng N. Enhancing the photothermal stability of plasmonic metal nanoplates by a core-shell architecture. Adv Mater. 2011;23(30):3420–3425. doi:10.1002/adma.201100905
   PubMed Web of Science ®Google Scholar
• Cheng L, Wang C, Feng L, Yang K, Liu Z. Functional nanomaterials for phototherapies of cancer. Chem Rev. 2014;114(21):10869–10939. doi:10.1021/cr400532z
   PubMed Web of Science ®Google Scholar
• Xiang Y, Li N, Guo L, et al. Biocompatible and pH-sensitive MnO-loaded carbonaceous nanospheres (MnO@CNSs): a theranostic agent for magnetic resonance imaging-guided photothermal therapy. Carbon. 2018;136:113–124. doi:10.1016/j.carbon.2018.04.058
   Web of Science ®Google Scholar
• Hong G, Diao S, Antaris AL, Dai H. Carbon nanomaterials for biological imaging and nanomedicinal therapy. Chem Rev. 2015;115(19):10816–10906. doi:10.1021/acs.chemrev.5b00008
   PubMed Web of Science ®Google Scholar
• Miao ZH, Wang H, Yang H, Li Z, Zhen L, Xu CY. Glucose-derived carbonaceous nanospheres for photoacoustic imaging and photothermal therapy. ACS Appl Mater Interfaces. 2016;8(25):15904–15910. doi:10.1021/acsami.6b03652
   PubMed Web of Science ®Google Scholar
• Wang Y, Li X, Chen P, Dong Y, Liang G, Yu Y. Enzyme-instructed self-aggregation of Fe3O4 nanoparticles for enhanced MRI T2 imaging and photothermal therapy of tumors. Nanoscale. 2020;12(3):1886–1893. doi:10.1039/c9nr09235h
   PubMed Web of Science ®Google Scholar
• Zhou Z, Huang D, Bao J, et al. A synergistically enhanced T(1) -T(2) dual-modal contrast agent. Adv Mater. 2012;24(46):6223–6228. doi:10.1002/adma.201203169
   PubMed Web of Science ®Google Scholar
• Lee N, Hyeon T. Designed synthesis of uniformly sized iron oxide nanoparticles for efficient magnetic resonance imaging contrast agents. Chem Soc Rev. 2012;41(7):2575–2589. doi:10.1039/c1cs15248c
   PubMed Web of Science ®Google Scholar
• Oh Y, Je JY, Moorthy MS, Seo H, Cho WH. pH and NIR-light-responsive magnetic iron oxide nanoparticles for mitochondria-mediated apoptotic cell death induced by chemo-photothermal therapy. Int J Pharm. 2017;531(1):1–13. doi:10.1016/j.ijpharm.2017.07.014
   PubMedGoogle Scholar
• Zhang X, Xu X, Li T, et al. Composite photothermal platform of polypyrrole-enveloped Fe3O4 nanoparticle self-assembled superstructures. ACS Appl Mater Interfaces. 2014;6(16):14552–14561. doi:10.1021/am503831m
   PubMed Web of Science ®Google Scholar
• Ge R, Li X, Lin M, et al. Fe3O4@polydopamine composite theranostic superparticles employing preassembled Fe3O4 Nanoparticles as the core. ACS Appl Mater Interfaces. 2016;8(35):22942–22952. doi:10.1021/acsami.6b07997
   PubMed Web of Science ®Google Scholar
• Tao K, Liu S, Wang L, et al. Targeted multifunctional nanomaterials with MRI, chemotherapy and photothermal therapy for the diagnosis and treatment of bladder cancer. Biomater Sci. 2019;8:342–352. doi:10.1039/c9bm01377f
   PubMed Web of Science ®Google Scholar
• Yoon J, Cho SH, Seong H. Multifunctional ultrasmall superparamagnetic iron oxide nanoparticles as a theranostic agent. Colloids Surfaces A. 2017;520:892–902. doi:10.1016/j.colsurfa.2017.02.080
   Google Scholar
• Liu B, Zhang X, Li C, et al. Magnetically targeted delivery of DOX loaded Cu9S5@mSiO2@Fe3O4-PEG nanocomposites for combined MR imaging and chemo/photothermal synergistic therapy. Nanoscale. 2016;8(25):12560–12569. doi:10.1039/c5nr06322a
   PubMed Web of Science ®Google Scholar
• Qi Y, Li W, Fang J, et al. Application and mechanism of manganese-coated caramelization nanospheres for active targeting in hepatobiliary tumors. Nanomedicine. 2019;14(22):2973–2985. doi:10.2217/nnm-2018-0272
   PubMed Web of Science ®Google Scholar
• Jin S, Deng H, Long D, et al. Facile synthesis of hierarchically structured Fe3O4/carbon micro-flowers and their application to lithium-ion battery anodes. J Power Sources. 2011;196(8):3887–3893. doi:10.1016/j.jpowsour.2010.12.078
   Web of Science ®Google Scholar
• Sun X, Li Y. Colloidal carbon spheres and their core/shell structures with noble-metal nanoparticles. Angew Chem Int Ed Engl. 2004;43(5):597–601. doi:10.1002/anie.200352386
   PubMed Web of Science ®Google Scholar
• Ostadhossein F, Vulugundam G, Misra SK, Srivastava I, Pan D. Chirality inversion on the carbon dot surface via covalent surface conjugation of cyclic α-amino acid capping agents. Bioconjug Chem. 2018;29(11):3913–3922. doi:10.1021/acs.bioconjchem.8b00736
   PubMed Web of Science ®Google Scholar
• Wei Y, Chen L, Wang J, Liu X, Yang Y, Yu S. Investigation on the chirality mechanism of chiral carbon quantum dots derived from tryptophan. RSC Adv. 2019;9(6):3208–3214. doi:10.1039/c8ra09649j
   PubMed Web of Science ®Google Scholar
• Finbloom JA, Sousa F, Stevens MM, Desai TA. Engineering the drug carrier biointerface to overcome biological barriers to drug delivery. Adv Drug Deliv Rev. 2020;167:89–108. doi:10.1016/j.addr.2020.06.007
   PubMed Web of Science ®Google Scholar
• Oladipo AO, Nkambule TTI, Mamba BB, Msagati TAM. The stimuli-responsive properties of doxorubicin adsorbed onto bimetallic Au@Pd nanodendrites and its potential application as drug delivery platform. Mater Sci Eng C. 2020;110. doi:10.1016/j.msec.2020.110696.
   PubMed Web of Science ®Google Scholar
• Guo W, Qi Y, Zhang Y, Ma L, Yu D, Zhan J. Biocompatible caramelized carbonaceous nanospheres supported paramagnetic ultrathin manganese oxide nanosheets via self-sacrificing reduction as a MRI contrast agent for liver imaging. Carbon. 2016;110:321–329. doi:10.1016/j.carbon.2016.09.030
   Web of Science ®Google Scholar
• Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015;33(9):941–951. doi:10.1038/nbt.3330
   PubMed Web of Science ®Google Scholar
• Sharifi M, Cho WC, Ansariesfahani A, et al. An updated review on EPR-based solid tumor targeting nanocarriers for cancer treatment. Cancers. 2022;14(12):2868. doi:10.3390/cancers14122868
   PubMed Web of Science ®Google Scholar
• Liu B, Li C, Yang D, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014. 2014:1906–1913.
   Google Scholar
• Wu L, Wu M, Zeng Y, et al. Multifunctional PEG modified DOX loaded mesoporous silica nanoparticle@ CuS nanohybrids as photo-thermal agent and thermal-triggered drug release vehicle for hepatocellular carcinoma treatment. Nanotechnology. 2014;26(2):025102. doi:10.1088/0957-4484/26/2/025102
   PubMed Web of Science ®Google Scholar
• Lu N, Huang P, Fan W, et al. Tri-stimuli-responsive biodegradable theranostics for mild hyperthermia enhanced chemotherapy. Biomaterials. 2017;126:39–48. doi:10.1016/j.biomaterials.2017.02.025
   PubMed Web of Science ®Google Scholar
• Qin J, Peng Z, Li B, et al. Gold nanorods as a theranostic platform for in vitro and in vivo imaging and photothermal therapy of inflammatory macrophages. Nanoscale. 2015;7(33):13991–14001. doi:10.1039/c5nr02521d
   PubMed Web of Science ®Google Scholar
• Jamalipour Soufi G, Iravani S. Eco-friendly and sustainable synthesis of biocompatible nanomaterials for diagnostic imaging: current challenges and future perspectives. Green Chem. 2020;22(9):2662–2687. doi:10.1039/d0gc00734j
   Web of Science ®Google Scholar
• Zhou Z, Sun Y, Shen J, et al. Iron/iron oxide core/shell nanoparticles for magnetic targeting MRI and near-infrared photothermal therapy. Biomaterials. 2014;35(26):7470–7478. doi:10.1016/j.biomaterials.2014.04.063
   PubMed Web of Science ®Google Scholar
• Zhang X, Chen F, Wang M. Impacts of selected dietary polyphenols on caramelization in model systems. Food Chem. 2013;141(4):3451–3458. doi:10.1016/j.foodchem.2013.06.053
   PubMed Web of Science ®Google Scholar
• Yu L, Chen Y, Wu M, et al. “Manganese extraction” strategy enables tumor-sensitive biodegradability and theranostics of nanoparticles. J Am Chem Soc. 2016;138(31):9881–9894. doi:10.1021/jacs.6b04299
   PubMed Web of Science ®Google Scholar
• Pan D, Caruthers SD, Hu G, et al. Ligand-directed nanobialys as theranostic agent for drug delivery and manganese-based magnetic resonance imaging of vascular targets. J Am Chem Soc. 2008;130(29):9186–9187. doi:10.1021/ja801482d
   PubMed Web of Science ®Google Scholar
• Chang H, Yhee JY, Jang GH, et al. Predicting the in vivo accumulation of nanoparticles in tumor based on in vitro macrophage uptake and circulation in zebrafish. J Control Release. 2016;244(Pt B):205–213. doi:10.1016/j.jconrel.2016.07.025
   PubMedGoogle Scholar
• Desai N. Challenges in development of nanoparticle-based therapeutics. Aaps j. 2012;14(2):282–295. doi:10.1208/s12248-012-9339-4
   PubMed Web of Science ®Google Scholar
• Gaumet M, Vargas A, Gurny R, Delie F. Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur J Pharm Biopharm. 2008;69(1):1–9. doi:10.1016/j.ejpb.2007.08.001
   PubMed Web of Science ®Google Scholar
• Zhang Q, Shan W, Ai C, et al. Construction of multifunctional Fe(3)O(4)-MTX@HBc nanoparticles for MR imaging and photothermal therapy/chemotherapy. Nanotheranostics. 2018;2(1):87–95. doi:10.7150/ntno.21942
   PubMedGoogle Scholar
• Estelrich J, Busquets MA. Iron oxide nanoparticles in photothermal therapy. Molecules. 2018;23(7):1567. doi:10.3390/molecules23071567
   PubMed Web of Science ®Google Scholar
• Amzulescu MS, De Craene M, Langet H, et al. Myocardial strain imaging: review of general principles, validation, and sources of discrepancies. Eur Heart J Cardiovasc Imaging. 2019;20(6):605–619. doi:10.1093/ehjci/jez041
   PubMed Web of Science ®Google Scholar
• Purschke M, Laubach H, Anderson R, Manstein D. Thermal injury causes DNA damage and lethality in unheated surrounding cells: active thermal bystander effect. J Invest Dermatol. 2010;130(1):86–92. doi:10.1038/jid.2009.205
   PubMed Web of Science ®Google Scholar
• Xie W, Gao Q, Wang D, et al. Doxorubicin-loaded Fe3O4@MoS2-PEG-2DG nanocubes as a theranostic platform for magnetic resonance imaging-guided chemo-photothermal therapy of breast cancer. Nano Res. 2018;11(5):2470–2487. doi:10.1007/s12274-017-1871-1
   Web of Science ®Google Scholar
• Caltagirone C, Bettoschi A, Garau A, Montis R. Silica-based nanoparticles: a versatile tool for the development of efficient imaging agents. Chem Soc Rev. 2015;44(14):4645–4671. doi:10.1039/c4cs00270a
   PubMed Web of Science ®Google Scholar
• Cherian AM, Nair SV, Lakshmanan VK. The role of nanotechnology in prostate cancer theranostic applications. J Nanosci Nanotechnol. 2014;14(1):841–852. doi:10.1166/jnn.2014.9052
   PubMed Web of Science ®Google Scholar
• Yang K, Wan J, Zhang S, Zhang Y, Lee ST, Liu Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano. 2011;5(1):516–522. doi:10.1021/nn1024303
   PubMed Web of Science ®Google Scholar
• Zha L, Wang B, Qian J, et al. Preparation, characterization and preliminary pharmacokinetic study of pH-sensitive Hydroxyapatite/Zein nano-drug delivery system for doxorubicin hydrochloride. J Pharm Pharmacol. 2020;72(4):496–506. doi:10.1111/jphp.13223
   PubMed Web of Science ®Google Scholar
• Lee S, George Thomas R, Ju Moon M, et al. Near-infrared heptamethine cyanine based iron oxide nanoparticles for tumor targeted multimodal imaging and photothermal therapy. Sci Rep. 2017;7(1):2108. doi:10.1038/s41598-017-01108-5
   PubMedGoogle Scholar
• Wang L, Xu X, Mu X, et al. Fe-doped copper sulfide nanoparticles for in vivo magnetic resonance imaging and simultaneous photothermal therapy. Nanotechnology. 2019;30(41):415101. doi:10.1088/1361-6528/ab2c13
   PubMed Web of Science ®Google Scholar
• Chen Y, Zhang F, Wang Q, et al. The synthesis of LA-Fe3O4@PDA-PEG-DOX for photothermal therapy-chemotherapy. Dalton Trans. 2018;47(7):2435–2443. doi:10.1039/c7dt04080f
   PubMed Web of Science ®Google Scholar