Abstract
Cancer therapy triggered by various cell death pathways has attracted widespread attention to improve therapeutic efficiency. Herein, an immunomodulatory polysaccharide (galactoxyloglucan) coated iron oxide nanoconjugate, with a diameter of about 10 nm, is made-up to intracellularly trigger the Fenton reaction and achieve cell death. The nanoconjugate based on iron oxide nanoparticles (PIONPs) exhibits excellent biocompatibility, stability and can be used as an imaging agent. Moreover, importantly it can effectively generate reactive oxygen species (ROS) for tumor eradication with no systemic toxicity. In vitro and In vivo experiments reveal that the PIONPs can intratumorally accumulate and serves as an excellent MRI contrast agent.
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G.-Q. Chen, et al. (2019). Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis. Cell Death Differ. 27, 242–254.
Y. Mou, et al. (2019). Ferroptosis, a new form of cell death: opportunities and challenges in cancer. J. Hematol. Oncol. 12 (1), 34.
S. M. Dadfar, et al. (2019). Iron oxide nanoparticles: diagnostic, therapeutic and theranostic applications. Adv. Drug Deliv. Rev. 138, 302–325.
Y. Bao, J. Sherwood, and Z. Sun (2018). Magnetic iron oxide nanoparticles as T 1 contrast agents for magnetic resonance imaging. J. Mater. Chem. C 6 (6), 1280–1290.
J. M. Richards, et al. (2012). In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: feasibility and safety in humans. Circulation 5 (4), 509–517.
M. G. Harisinghani, et al. (2003). Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N. Engl. J. Med. 348 (25), 2491–2499.
Y.-X.J. Wang, S. M. Hussain, and G. P. Krestin (2001). Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur. Radiol. 11 (11), 2319–2331.
H. Unterweger, et al. (2018). Dextran-coated superparamagnetic iron oxide nanoparticles for magnetic resonance imaging: evaluation of size-dependent imaging properties, storage stability and safety. Int. J. Nanomed. 13, 1899.
A. Frtús, et al. (2020). Analyzing the mechanisms of iron oxide nanoparticles interactions with cells: A road from failure to success in clinical applications. J. Control. Rel. 328, 59–77.
Y. X. J. Wáng and J.-M. Idée (2017). A comprehensive literature update of clinical researches of superparamagnetic resonance iron oxide nanoparticles for magnetic resonance imaging. Quant. Imaging Med. Surg. 7 (1), 88.
Y.-X.J. Wang (2011). Superparamagnetic iron oxide based MRI contrast agents: current status of clinical application. Quant. Imaging Med. Surg 1 (1), 35.
H. Nosrati, et al. (2019). New insight about biocompatibility and biodegradability of iron oxide magnetic nanoparticles: stereological and in vivo MRI monitor. Sci. Rep. 9 (1), 7173.
X. Qian, et al. (2019). Nanocatalysts-augmented Fenton chemical reaction for nanocatalytic tumor therapy. Biomaterials 211, 1–13.
H.-J. Chung, H.-J. Kim, and S.-T. Hong (2019). Iron-dextran as a thermosensitizer in radiofrequency hyperthermia for cancer treatment. Appl. Biol. Chem. 62 (1), 24.
I. Cicha et al (2018) P6481 Novel dextran-coated ultrasmall superparamagnetic iron oxide nanoparticles (USPIOs)-a safe contrast agent for magnetic resonance imaging of atherosclerosis. Eur. Heart J. 39(1):ehy566. P6481.
M. B. Mulder, et al. (2019). Comparison of hypersensitivity reactions of intravenous iron: iron isomaltoside-1000 (Monofer®) versus ferric carboxy-maltose (Ferinject®). A single center, cohort study. Br. J. Clin. Pharmacol. 85 (2), 385–392.
Ö. Özdemir and M. Büyükavcı (2018). Development of hypersensitivity reactions after using different oral iron preparations. Istanbul Med. J. 19 (2), 168–171.
B. Unnikrishnan, et al. (2019). Fabrication of fluorescein labeled galactoxyloglucan polysaccharide for tumor and macrophage tagging. J. Drug Deliv. Sci. Technol. 52, 863–869.
S. Aravind, et al. (2015). TRAIL-based tumor sensitizing galactoxyloglucan, a novel entity for targeting apoptotic machinery. Int. J. Biochem. Cell Biol. 59, 153–166.
P. Rao, T. Ghosh, and S. Krishna (1946). Extraction and purification of tamarind seed polysaccharide. J. Sci. Ind. Res. 4, 705.
N. Remya, et al. (2016). Toxicity, toxicokinetics and biodistribution of dextran stabilized iron oxide nanoparticles for biomedical applications. Int. J. Pharm. 511 (1), 586–598.
A. K. Hauser, et al. (2015). The effects of synthesis method on the physical and chemical properties of dextran coated iron oxide nanoparticles. Mater. Chem. Phys. 160, 177–186.
A. Saraswathy, et al. (2014). Synthesis and characterization of dextran stabilized superparamagnetic iron oxide nanoparticles for in vivo MR imaging of liver fibrosis. Carbohydr. Polym. 101, 760–768.
M. M. Joseph, et al. (2013). PST-Gold nanoparticle as an effective anticancer agent with immunomodulatory properties. Colloids Surf. 104, 32–39.
M. M. Joseph, et al. (2017). Exploration of biogenic nano-chemobiotics fabricated by silver nanoparticle and galactoxyloglucan with an efficient biodistribution in solid tumor investigated by SERS fingerprinting. ACS Appl. Mater. Interfaces 9 (23), 19578–19590.
M.-B. Troadec, et al. (2006). Hepatocyte iron loading capacity is associated with differentiation and repression of motility in the HepaRG cell line. Genomics 87 (1), 93–103.
M. Calero, et al. (2015). Characterization of interaction of magnetic nanoparticles with breast cancer cells. J. Nanobiotechnol. 13 (1), 16.
M. Rosário, et al. (2008). Effect of storage xyloglucans on peritoneal macrophages. Phytochemistry 69 (2), 464–472.
M. M. T. do Rosário, et al. (2011). Storage xyloglucans: potent macrophages activators. Chem.-Biol. Interact. 189 (12), 127–133.
M. M. Joseph, et al. (2014). Antitumor activity of galactoxyloglucan-gold nanoparticles against murine ascites and solid carcinoma. Colloids Surf. B 116, 219–227.
C. Pardo-Castaño and G. Bolaños (2019). Solubility of chitosan in aqueous acetic acid and pressurized carbon dioxide-water: experimental equilibrium and solubilization kinetics. J. Supercrit. Fluids 151, 63–74.
S. L. Easo and P. Mohanan (2015). In vitro hematological and in vivo immunotoxicity assessment of dextran stabilized iron oxide nanoparticles. Colloids Surf. B 134, 122–130.
S. Ahmad, S. Shankar, and A. Mishra (2019). Ferromagnetic xyloglucan–Fe 3 O 4 green nanocomposites: sonochemical synthesis, characterization and application in removal of methylene blue from water. Environ. Sustain. 3, 15–22.
C. Fang, et al. (2009). Functionalized nanoparticles with long-term stability in biological media. Small 5 (14), 1637–1641.
T. Cedervall, et al. (2007). Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. 104 (7), 2050–2055.
S. Linse, et al. (2007). Nucleation of protein fibrillation by nanoparticles. Proc. Natl. Acad. Sci. 104 (21), 8691–8696.
C. Röcker, et al. (2009). A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat. Nanotechnol. 4 (9), 577–580.
A. E. Nel, et al. (2009). Understanding biophysicochemical interactions at the nano–bio interface. Nat. Mater. 8 (7), 543–557.
A. Lesniak, et al. (2010). Serum heat inactivation affects protein corona composition and nanoparticle uptake. Biomaterials 31 (36), 9511–9518.
S. Bhattacharjee (2016). DLS and zeta potential–what they are and what they are not? J. Control. Rel. 235, 337–351.
S. Xie, et al. (2015). Superparamagnetic iron oxide nanoparticles coated with different polymers and their MRI contrast effects in the mouse brains. Appl. Surf. Sci. 326, 32–38.
C. Hui, et al. (2008). Large-scale Fe 3O 4 nanoparticles soluble in water synthesized by a facile method. J. Phys. Chem. C 112 (30), 11336–11339.
M. Peng, et al. (2015). Dextran-coated superparamagnetic nanoparticles as potential cancer drug carriers in vivo. Nanoscale 7 (25), 11155–11162.
J. A. Pellicer, et al. (2019). Adsorption properties of β-and hydroxypropyl-β-cyclodextrins cross-linked with epichlorohydrin in aqueous solution. A sustainable recycling strategy in textile dyeing process. Polymers 11 (2), 252.
V. Silva, et al. (2013). Synthesis and characterization of Fe3O4 nanoparticles coated with fucan polysaccharides. J. Magn. Magn. Mater. 343, 138–143.
O. Lemine, et al. (2012). Sol–gel synthesis of 8 nm magnetite (Fe3O4) nanoparticles and their magnetic properties. Superlattices Microstruct. 52 (4), 793–799.
Y. Cao, et al. (2010). Self-assembled nanoparticle drug delivery systems from galactosylated polysaccharide–doxorubicin conjugate loaded doxorubicin. Int. J. Biol. Macromol. 46 (2), 245–249.
X. Xie, et al. (2016). Targeted nanoparticles from xyloglucan–doxorubicin conjugate loaded with doxorubicin against drug resistance. RSC Adv. 6 (31), 26137–26146.
L. Bhumarkar, A. Arkhel, and S. Ramteke (2014). Formulation design and evaluation of xyloglucan microsphere of silymarin. Pharma Innov. 3 (4), 92.
A. D. Springer and S. F. Dowdy (2018). GalNAc-siRNA conjugates: leading the way for delivery of RNAi therapeutics. Nucleic Ther. 28 (3), 109–118.
G. Huang, et al. (2013). Superparamagnetic iron oxide nanoparticles: amplifying ROS stress to improve anticancer drug efficacy. Theranostics 3 (2), 116.
X. Lin, et al. (2020). The mechanism of ferroptosis and applications in tumor treatment. Front. Pharmacol. 11, 1061.
K. Levada, et al. (2020). Progressive lysosomal membrane permeabilization induced by iron oxide nanoparticles drives hepatic cell autophagy and apoptosis. Nano Converg. 7 (1), 1–17.
T. Yin, et al. (2017). In vivo targeted therapy of gastric tumors via the mechanical rotation of a flower-like Fe 3 O 4@ Au nanoprobe under an alternating magnetic field. NPG Asia Mater. 9 (7), e408.
G. Baldi, et al. (2014). In vivo anticancer evaluation of the hyperthermic efficacy of anti-human epidermal growth factor receptor-targeted PEG-based nanocarrier containing magnetic nanoparticles. Int. J. Nanomed. 9, 3037.
M. Costa da Silva, et al. (2017). Iron induces anti-tumor activity in tumor-associated macrophages. Front. Immunol. 8, 1479.
A. Carobene, et al. (2013). A systematic review of data on biological variation for alanine aminotransferase, aspartate aminotransferase and γ-glutamyl transferase. Clin. Chem. Labor. Med. 51 (10), 1997–2007.
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Authors UBS, and PGU thanks University Grants Commission (UGC), Govt. of India for the research fellowships. Authors acknowledge Mr.Udayakumar KR, Radiodiagnosis Department for MRI.
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Unnikrishnan, B.S., Preethi, G.U., Anitha, S. et al. Impact of Galactoxyloglucan Coated Iron Oxide Nanoparticles on Reactive Oxygen Species Generation and Magnetic Resonance Imaging for Tumor Management. J Clust Sci 33, 361–374 (2022). https://doi.org/10.1007/s10876-020-01971-9
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DOI: https://doi.org/10.1007/s10876-020-01971-9