Iron Oxide Nanoparticles for Visualization of Prostate Cancer in MRI
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Cell Culture
2.2. Xenograft Mouse Model and In Vivo Study Design
2.3. In Vivo MRI
2.4. Ferumoxytol as a Contrast Agent for MRI
2.5. Ferumoxytol Imaging Using T2* Weighted Sequences
2.6. MRI Measurements
2.7. Histological Analysis
2.8. Quantification of the Iron and Macrophages in Immunofluorescence
2.9. Laser Ablation-Inductively Coupled Plasma-Mass Spectroscopy (LA-ICP-MS)
2.10. Inductively Coupled Plasma-Mass Spectrometry (ICP-MS)
2.11. Western Blot
2.12. Statistical Analysis
3. Results
3.1. Characterization in T2*-Weigthed MR Imaging Using Superparamagnetic Iron-Oxide Particle
3.2. Ex Vivo Analysis
3.3. Elemental Analysis of Tumor Tissue with Specific Regard to Fe
4. Discussion
5. Limitations
6. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics, 2021. CA Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef]
- Duffy, M.J. Biomarkers for prostate cancer: Prostate-specific antigen and beyond. Clin. Chem. Lab. Med. 2020, 58, 326–339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, J.; Mangarova, D.B.; Brangsch, J.; Kader, A.; Hamm, B.; Brenner, W.; Makowski, M.R. Correlation between Intraprostatic PSMA Uptake and MRI PI-RADS of [(68)Ga] Ga-PSMA-11 PET/MRI in Patients with Prostate Cancer: Comparison of PI-RADS Version 2.0 and PI-RADS Version 2.1. Cancers 2020, 12, 3523. [Google Scholar] [CrossRef] [PubMed]
- Zhao, S.; Yu, X.; Qian, Y.; Chen, W.; Shen, J. Multifunctional magnetic iron oxide nanoparticles: An advanced platform for cancer theranostics. Theranostics 2020, 10, 6278–6309. [Google Scholar] [CrossRef] [PubMed]
- Figuerola, A.; Di Corato, R.; Manna, L.; Pellegrino, T. From iron oxide nanoparticles towards advanced iron-based inorganic materials designed for biomedical applications. Pharmacol. Res. 2010, 62, 126–143. [Google Scholar] [CrossRef]
- Gazeau, F.; Lévy, M.; Wilhelm, C. Optimizing magnetic nanoparticle design for nanothermotherapy. Nanomedicine 2008, 3, 831–844. [Google Scholar] [CrossRef]
- Gupta, A.K.; Gupta, M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26, 3995–4021. [Google Scholar] [CrossRef]
- Wang, G.; Serkova, N.J.; Groman, E.V.; Scheinman, R.I.; Simberg, D. Feraheme (Ferumoxytol) Is Recognized by Proinflammatory and Anti-inflammatory Macrophages via Scavenger Receptor Type AI/II. Mol. Pharm. 2019, 16, 4274–4281. [Google Scholar] [CrossRef]
- Lin, Y.; Xu, J.; Lan, H. Tumor-associated macrophages in tumor metastasis: Biological roles and clinical therapeutic applications. J. Hematol. Oncol. 2019, 12, 76. [Google Scholar] [CrossRef]
- Zhou, J.; Tang, Z.; Gao, S.; Li, C.; Feng, Y.; Zhou, X. Tumor-Associated Macrophages: Recent Insights and Therapies. Front. Oncol. 2020, 10, 188. [Google Scholar] [CrossRef]
- Lissbrandt, I.F.; Stattin, P.; Wikström, P.; Damber, J.-E.; Egeva, L.; Bergh, A. Tumor associated macrophages in human prostate cancer: Relation to clinicopathological variables and survival. Int. J. Oncol. 2000, 17, 445–496. [Google Scholar] [CrossRef]
- Ramanathan, R.K.; Korn, R.L.; Raghunand, N.; Sachdev, J.C.; Newbold, R.G.; Jameson, G.; Fetterly, G.J.; Prey, J.; Klinz, S.G.; Kim, J.; et al. Correlation between Ferumoxytol Uptake in Tumor Lesions by MRI and Response to Nanoliposomal Irinotecan in Patients with Advanced Solid Tumors: A Pilot Study. Clin. Cancer Res. 2017, 23, 3638–3648. [Google Scholar] [CrossRef] [Green Version]
- Harisinghani, M.; Ross, R.W.; Guimaraes, A.R.; Weissleder, R. Utility of a New Bolus-injectable Nanoparticle for Clinical Cancer Staging. Neoplasia 2007, 9, 1160–1165. [Google Scholar] [CrossRef] [Green Version]
- McConnell, H.L.; Schwartz, D.L.; Richardson, B.E.; Woltjer, R.L.; Muldoon, L.L.; Neuwelt, E.A. Ferumoxytol nanoparticle uptake in brain during acute neuroinflammation is cell-specific. Nanomedicine 2016, 12, 1535–1542. [Google Scholar] [CrossRef] [Green Version]
- Toth, G.B.; Varallyay, C.G.; Horvath, A.; Bashir, M.R.; Choyke, P.L.; Daldrup-Link, H.E.; Dosa, E.; Finn, J.P.; Gahramanov, S.; Harisinghani, M.; et al. Current and potential imaging applications of ferumoxytol for magnetic resonance imaging. Kidney Intern. 2017, 92, 47–66. [Google Scholar] [CrossRef]
- Tse, B.W.-C.; Cowin, G.J.; Soekmadji, C.; Jovanovic, L.; Vasireddy, R.S.; Ling, M.-T.; Khatri, A.; Liu, T.; Thierry, B.; Russell, P.J. PSMA-targeting iron oxide magnetic nanoparticles enhance MRI of preclinical prostate cancer. Nanomedicine 2015, 10, 375–386. [Google Scholar] [CrossRef] [Green Version]
- Bates, D.; Abraham, S.; Campbell, M.; Zehbe, I.; Curiel, L. Development and characterization of an antibody-labeled super-paramagnetic iron oxide contrast agent targeting prostate cancer cells for magnetic resonance imaging. PLoS ONE 2014, 9, e97220. [Google Scholar] [CrossRef] [Green Version]
- Zhu, Y.; Sun, Y.; Chen, Y.; Liu, W.; Jiang, J.; Guan, W.; Zhang, Z.; Duan, Y. In Vivo Molecular MRI Imaging of Prostate Cancer by Targeting PSMA with Polypeptide-Labeled Superparamagnetic Iron Oxide Nanoparticles. Int. J. Mol. Sci. 2015, 16, 9573–9587. [Google Scholar] [CrossRef] [Green Version]
- Nagesh, P.K.B.; Johnson, N.R.; Boya, V.K.N.; Chowdhury, P.; Othman, S.F.; Khalilzad-Sharghi, V.; Hafeez, B.B.; Ganju, A.; Khan, S.; Behrman, S.W.; et al. PSMA targeted docetaxel-loaded superparamagnetic iron oxide nanoparticles for prostate cancer. Colloids Surf. B Biointerfaces 2016, 144, 8–20. [Google Scholar] [CrossRef] [Green Version]
- Knobloch, G.; Colgan, T.; Wiens, C.N.; Wang, X.; Schubert, T.; Hernando, D.; Sharma, S.D.; Reeder, S.B. Relaxivity of Ferumoxytol at 1.5 T and 3.0 T. Investig. Radiol. 2018, 53, 257–263. [Google Scholar] [CrossRef]
- Brangsch, J.; Reimann, C.; Kaufmann, J.O.; Adams, L.C.; Onthank, D.C.; Thone-Reineke, C.; Robinson, S.P.; Buchholz, R.; Karst, U.; Botnar, R.M.; et al. Concurrent Molecular Magnetic Resonance Imaging of Inflammatory Activity and Extracellular Matrix Degradation for the Prediction of Aneurysm Rupture. Circ. Cardiovasc. Imaging 2019, 12, e008707. [Google Scholar] [CrossRef] [Green Version]
- Mockel, J.; Brangsch, J.; Reimann, C.; Kaufmann, J.O.; Sack, I.; Mangarova, D.B.; Kader, A.; Taupitz, M.; Adams, L.C.; Keller, S.; et al. Assessment of Albumin ECM Accumulation and Inflammation as Novel In Vivo Diagnostic Targets for Multi-Target MR Imaging. Biology 2021, 10, 964. [Google Scholar] [CrossRef]
- Reimann, C.; Brangsch, J.; Kaufmann, J.O.; Adams, L.C.; Onthank, D.C.; Thone-Reineke, C.; Robinson, S.P.; Hamm, B.; Botnar, R.M.; Makowski, M.R. Dual-probe molecular MRI for the in vivo characterization of atherosclerosis in a mouse model: Simultaneous assessment of plaque inflammation and extracellular-matrix remodeling. Sci. Rep. 2019, 9, 13827. [Google Scholar] [CrossRef] [Green Version]
- Zanganeh, S.; Hutter, G.; Spitler, R.; Lenkov, O.; Mahmoudi, M.; Shaw, A.; Pajarinen, J.S.; Nejadnik, H.; Goodman, S.; Moseley, M.; et al. Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues. Nat. Nanotechnol. 2016, 11, 986–994. [Google Scholar] [CrossRef]
- Daldrup-Link, H.E.; Golovko, D.; Ruffell, B.; Denardo, D.G.; Castaneda, R.; Ansari, C.; Rao, J.; Tikhomirov, G.A.; Wendland, M.F.; Corot, C.; et al. MRI of tumor-associated macrophages with clinically applicable iron oxide nanoparticles. Clin. Cancer Res. 2011, 17, 5695–5704. [Google Scholar] [CrossRef] [Green Version]
- Cendrowicz, E.; Sas, Z.; Bremer, E.; Rygiel, T.P. The Role of Macrophages in Cancer Development and Therapy. Cancers 2021, 13, 1946. [Google Scholar] [CrossRef]
- Serguei, V.; Galya, W.; Xin, W. Macrophages associated with tumors as potential targets and therapeutic intermediates. Nanomedicine 2014, 9, 695–707. [Google Scholar]
- Franklin, R.A.; Liao, W.; Sarkar, A.; Kim, M.V.; Bivona, M.R.; Liu, K.; Pamer, E.G.; Li, M.O. The cellular and molecular origin of tumor-associated macrophages. Science 2014, 344, 921–925. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, S.R.; Schmid, M.C. Macrophages as Key Drivers of Cancer Progression and Metastasis. Mediat. Inflamm. 2017, 2017, 9624760. [Google Scholar] [CrossRef]
- Nonomura, N.; Takayama, H.; Kawashima, A.; Mukai, M.; Nagahara, A.; Nakai, Y.; Nakayama, M.; Tsujimura, A.; Nishimura, K.; Aozasa, K.; et al. Decreased infiltration of macrophage scavenger receptor-positive cells in initial negative biopsy specimens is correlated with positive repeat biopsies of the prostate. Cancer Sci. 2010, 101, 1570–1573. [Google Scholar] [CrossRef]
- Yuri, P.; Shigemura, K.; Kitagawa, K.; Hadibrata, E.; Risan, M.; Zulfiqqar, A.; Soeroharjo, I.; Hendri, A.Z.; Danarto, R.; Ishii, A.; et al. Increased tumor-associated macrophages in the prostate cancer microenvironment predicted patients’ survival and responses to androgen deprivation therapies in Indonesian patients cohort. Prostate Int. 2020, 8, 62–69. [Google Scholar] [CrossRef]
- Lewis, C.E.; Pollard, J.W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006, 66, 605–612. [Google Scholar] [CrossRef] [Green Version]
- Wu, S.; Boyer, C.M.; Whitaker, R.S.; Berchuck, A.; Wiener, J.R.; Weinberg, J.B.; Bast, R.C. Tumor Necrosis Factor a as an Autocrine and Paracrine Growth Factor for Ovarian Cancer: Monokine Induction of Tumor Cell Proliferation and Tumor Necrosis Factor a Expression1. Cancer Res. 1993, 53, 1939–1944. [Google Scholar] [PubMed]
- Liu, R.Y.; Fan, C.; Mitchell, S.; Chen, Q.; Wu, J.; Zuckerman, K.S. The role of type I and type II tumor necrosis factor (TNF) receptors in the ability of TNF-alpha to transduce a proliferative signal in the human megakaryoblastic leukemic cell line Mo7e. Cancer Res. 1998, 58, 2217–2223. [Google Scholar]
- Adler, H.L.; McCurdy, M.A.; Kattan, M.W.; Timme, T.L.; Scardino, P.T.; Thompson, T.C. Elevated levels of circulating interleukin-6 and transforming growth factor-beta 1 in patients with metastatic prostatic carcinoma. J. Urol. 1999, 161, 182–187. [Google Scholar] [CrossRef]
- Maolake, A.; Izumi, K.; Natsagdorj, A.; Iwamoto, H.; Kadomoto, S.; Makino, T.; Naito, R.; Shigehara, K.; Kadono, Y.; Hiratsuka, K.; et al. Tumor necrosis factor-alpha induces prostate cancer cell migration in lymphatic metastasis through CCR7 upregulation. Cancer Sci. 2018, 109, 1524–1531. [Google Scholar] [CrossRef] [PubMed]
- Cassier, P.A.; Treilleux, I.; Bachelot, T.; Ray-Coquard, I.; Bendriss-Vermare, N.; Ménétrier-Caux, C.; Trédan, O.; Goddard-Léon, S.; Pin, J.-J.; Mignotte, H.; et al. Prognostic value of the expression of C-Chemokine Receptor 6 and 7 and their ligands in non-metastatic breast cancer. BMC Cancer 2011, 11, 213. [Google Scholar] [CrossRef] [Green Version]
- Du, P.; Liu, Y.; Ren, H.; Zhao, J.; Zhang, X.; Patel, R.; Hu, C.; Gan, J.; Huang, G. Expression of chemokine receptor CCR7 is a negative prognostic factor for patients with gastric cancer: A meta-analysis. Gastric Cancer 2017, 20, 235–245. [Google Scholar] [CrossRef] [Green Version]
- Peng, X.H.; Qian, X.; Mao, H.; Wang, A.Y.; Nie, S.; Shin, D.M. Targeted magnetic iron oxide nanoparticles for tumor imaging and therapy. Int. J. Nanomed. 2008, 3, 311–326. [Google Scholar]
- Israel, L.L.; Galstyan, A.; Holler, E.; Ljubimova, J.Y. Magnetic iron oxide nanoparticles for imaging, targeting and treatment of primary and metastatic tumors of the brain. J. Control. Release 2020, 320, 45–62. [Google Scholar] [CrossRef]
- Xue, X.; Bo, R.; Qu, H.; Jia, B.; Xiao, W.; Yuan, Y.; Vapniarsky, N.; Lindstrom, A.; Wu, H.; Zhang, D.; et al. A nephrotoxicity-free, iron-based contrast agent for magnetic resonance imaging of tumors. Biomaterials 2020, 257, 120234. [Google Scholar] [CrossRef] [PubMed]
- Jung, M.; Mertens, C.; Tomat, E.; Brune, B. Iron as a Central Player and Promising Target in Cancer Progression. Int. J. Mol. Sci. 2019, 20, 273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, J.Y.; Neuhouser, M.L.; Barnett, M.J.; Hong, C.C.; Kristal, A.R.; Thornquist, M.D.; King, I.B.; Goodman, G.E.; Ambrosone, C.B. Iron intake, oxidative stress-related genes (MnSOD and MPO) and prostate cancer risk in CARET cohort. Carcinogenesis 2008, 29, 964–970. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adams, L.C.; Brangsch, J.; Reimann, C.; Kaufmann, J.O.; Buchholz, R.; Karst, U.; Botnar, R.M.; Hamm, B.; Makowski, M.R. Simultaneous molecular MRI of extracellular matrix collagen and inflammatory activity to predict abdominal aortic aneurysm rupture. Sci. Rep. 2020, 10, 15206. [Google Scholar] [CrossRef]
- Cheng, K.; Shen, D.; Hensley, M.T.; Middleton, R.; Sun, B.; Liu, W.; De Couto, G.; Marban, E. Magnetic antibody-linked nanomatchmakers for therapeutic cell targeting. Nat. Commun. 2014, 5, 4880. [Google Scholar] [CrossRef]
- Zhou, M.C.A.; Kleer, C.; Lucas, P.; Rubin, M. Alpha-Methylacyl-CoA Racemase. Am. J. Surg. Pathol. 2002, 26, 926–931. [Google Scholar] [CrossRef]
- Mazaris, E.; Tsiotras, A. Molecular Pathways in Prostate Cancer. Nephro-Urol. Mon. 2013, 5, 792–800. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kader, A.; Kaufmann, J.O.; Mangarova, D.B.; Moeckel, J.; Brangsch, J.; Adams, L.C.; Zhao, J.; Reimann, C.; Saatz, J.; Traub, H.; et al. Iron Oxide Nanoparticles for Visualization of Prostate Cancer in MRI. Cancers 2022, 14, 2909. https://doi.org/10.3390/cancers14122909
Kader A, Kaufmann JO, Mangarova DB, Moeckel J, Brangsch J, Adams LC, Zhao J, Reimann C, Saatz J, Traub H, et al. Iron Oxide Nanoparticles for Visualization of Prostate Cancer in MRI. Cancers. 2022; 14(12):2909. https://doi.org/10.3390/cancers14122909
Chicago/Turabian StyleKader, Avan, Jan O. Kaufmann, Dilyana B. Mangarova, Jana Moeckel, Julia Brangsch, Lisa C. Adams, Jing Zhao, Carolin Reimann, Jessica Saatz, Heike Traub, and et al. 2022. "Iron Oxide Nanoparticles for Visualization of Prostate Cancer in MRI" Cancers 14, no. 12: 2909. https://doi.org/10.3390/cancers14122909
APA StyleKader, A., Kaufmann, J. O., Mangarova, D. B., Moeckel, J., Brangsch, J., Adams, L. C., Zhao, J., Reimann, C., Saatz, J., Traub, H., Buchholz, R., Karst, U., Hamm, B., & Makowski, M. R. (2022). Iron Oxide Nanoparticles for Visualization of Prostate Cancer in MRI. Cancers, 14(12), 2909. https://doi.org/10.3390/cancers14122909