Radiolabeling of Biogenic Magnetic Nanoparticles with Rhenium-188 as a Novel Agent for Targeted Radiotherapy

  • Somayeh Akbari-Karadeh
  • Seyed Mahmoud Reza AghamiriEmail author
  • Parisa Tajer-Mohammad-GhazviniEmail author
  • Saeid Ghorbanzadeh-Mashkani


Use of nanoparticles as carriers of anticancer drugs is a suitable way for targeted drug delivery and reduction of the side effects. This research focuses on a novel drug carrier for therapeutic goals by the bacterial magnetic nanoparticles (magnetosomes). The unique characteristics of magnetosomes make them ideal nanobiotechnological materials. In this study, magnetic nanoparticles of Alphaproteobacterium MTB-KTN90 were labeled with the radioisotope rhenium-188 and optimized the factors affecting the labeling efficiency. The results showed that the labeling efficiency of magnetosomes with rhenium-188 was more than 96%. The optimum concentration of bacterial nanoparticles was 133 mg/ml and the best time for maximum efficiency labeling was 60 min. The labeling stability showed that the 188Re-nanoparticle complexes have good stability in 29 h. The results of magnetic nanoparticles bacterial cytotoxicity on cancer cells AsPC1 did not show significant toxicity to concentration of 100 μg/μl. Finally, the biogenic magnetic nanoparticles labeled with rhenium-188 can be introduced as a valuable candidate for the targeted therapy of tumor with reducing radiation to surrounding healthy tissues.


Drug delivery Magnetosomes Magnetotactic bacteria Nanobiotechnology Targeted therapy 



This manuscript was a part of the MSc. thesis by S. Akbari-Karadeh, under the supervision of Dr. S.M.R. Aghamiri and Dr. P. Tajer-Mohammad-Ghazvini; and advisory of S. Ghorbanzadeh-Mashkani. The authors would like to thank Department of Medical Radiation Engineering, Shahid Beheshti University and also Materials and Nuclear Fuel Research School, Nuclear Science and Technology Research Institute, Tehran, Iran for the supports through this study. The authors are grateful to Dr. Reza Dabbagh and Dr. Behrooz Alirezapour for their valuable contributions to this project.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Aghamiri, S. M. R., Akbari-Karadeh, S., Tajer-Mohammad-Ghazvini, P., & Ghorbanzadeh-Mashkani, S. (2018). Effect of temperature and reducing agent on labeling of magnetosomes with 188Re and biodistribution study of labeled magnetic nanoparticles. Modares Journal of Biotechnology, 9, 179–185.Google Scholar
  2. 2.
    Alphandéry, E. (2014). Applications of magnetosomes synthesized by magnetotactic bacteria in medicine. Frontiers in Bioengineering and Biotechnology, 2, 5.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Alphandéry, E., Guyot, F., & Chebbi, I. (2012). Preparation of chains of magnetosomes, isolated from Magnetospirillum magneticum strain AMB-1 magnetotactic bacteria, yielding efficient treatment of tumors using magnetic hyperthermia. International Journal of Pharmaceutics, 434(1-2), 444–452.CrossRefPubMedGoogle Scholar
  4. 4.
    Bazylinski, D. A., Lefèvre, C. T., & Schüler, D. (2013). In E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, & F. Thompson (Eds.), The prokaryotes (pp. 453–494). Berlin: Springer.CrossRefGoogle Scholar
  5. 5.
    Bouziotis, P., Psimadas, D., Tsotakos, T., Stamopoulos, D., & Tsoukalas, C. (2012). Radiolabeled iron oxide nanoparticles as dual-modality SPECT/MRI and PET/MRI agents. Current Topics in Medicinal Chemistry, 12(23), 2694–2702.CrossRefPubMedGoogle Scholar
  6. 6.
    Chunfu, Z., Jinquan, C., Duanzhi, Y., Yongxian, W., Yanlin, F., & Jiajü, T. (2004). Preparation and radiolabeling of human serum albumin (HSA)-coated magnetite nanoparticles for magnetically targeted therapy. Applied Radiation and Isotopes, 61(6), 1255–1259.CrossRefPubMedGoogle Scholar
  7. 7.
    Elcey, C., Kuruvilla, A. T., & Thomas, D. (2014). Synthesis of magnetite nanoparticles from optimized iron reducing bacteria isolated from iron ore mining sites. International Journal of Current Microbiology and Applied Sciences, 3, 408–417.Google Scholar
  8. 8.
    Erdal, E., Demirbilek, M., Yeh, Y., Akbal, Ö., Ruff, L., Bozkurt, D., Cabuk, A., Senel, Y., Gumuskaya, B., Algın, O., Colak, S., Esener, S., & Denkbas, E. B. (2018). A comparative study of receptor-targeted magnetosome and HSA-coated Iron oxide nanoparticles as MRI contrast-enhancing agent in animal cancer model. Applied Biochemistry and Biotechnology, 185(1), 91–113.CrossRefPubMedGoogle Scholar
  9. 9.
    Fernandez-Fernandez, A., Manchanda, R., & McGoron, A. J. (2011). Theranostic applications of nanomaterials in cancer: drug delivery, image-guided therapy, and multifunctional platforms. Applied Biochemistry and Biotechnology, 165(7-8), 1628–1651.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ghorbanzadeh-Mashkani, S., Tajer-Mohammad-Ghazvini, P., Nozad-Golikand, A., Kasra-Kermanshahi, R., & Davarpanah, M.-R. (2013). Synthesis of sterile and pyrogen free biogenic magnetic nanoparticles: biotechnological potential of magnetotactic bacteria for production of nanomaterials. World Academy of Science, Engineering and Technology- International Journal of Biological, Biomolecular, Agricultural, Food and Biotechnological Engineering, World Academy of Science, Engineering and Technology, 7, 133–137.Google Scholar
  11. 11.
    Grünberg, K., Wawer, C., Tebo, B. M., & Schüler, D. (2001). A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Applied and Environmental Microbiology, 67(10), 4573–4582.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Häfeli, U., Pauer, G., Failing, S., & Tapolsky, G. (2001). Radiolabeling of magnetic particles with rhenium-188 for cancer therapy. Journal of Magnetism and Magnetic Materials, 225(1-2), 73–78.CrossRefGoogle Scholar
  13. 13.
    Huang, F. Y., Lee, T. W., Chang, C. H., Chen, L. C., Hsu, W. H., Chang, C. W., & Lo, J. M. (2015). Evaluation of 188Re-labeled PEGylated nanoliposome as a radionuclide therapeutic agent in an orthotopic glioma-bearing rat model. International Journal of Nanomedicine, 10, 463–473.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Jain, R. (2001). New approaches for the treatment of cancer. Advanced Drug Delivery Reviews, 46(1-3), 149–168.CrossRefPubMedGoogle Scholar
  15. 15.
    Koo, O. M., Rubinstein, I., & Onyuksel, H. (2005). Role of nanotechnology in targeted drug delivery and imaging: a concise review. Nanomedicine: nanotechnology, biology and medicine, 1(3), 193–212.CrossRefGoogle Scholar
  16. 16.
    Laan, A. C., Santini, C., Jennings, L., de Jong, M., Bernsen, M. R., & Denkova, A. G. (2016). Radiolabeling polymeric micelles for in vivo evaluation: a novel, fast, and facile method. EJNMMI Research, 6(1), 12–12.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Liang, S., Wang, Y., Yu, J., Zhang, C., Xia, J., & Yin, D. (2007). Surface modified superparamagnetic iron oxide nanoparticles: as a new carrier for bio-magnetically targeted therapy. Journal of Materials Science: Materials in Medicine, 18(12), 2297–2302.PubMedGoogle Scholar
  18. 18.
    Liu, G., & Hnatowich, D. J. (2007). Labeling biomolecules with radiorhenium: a review of the bifunctional chelators. Anticancer Agents in Medicinal Chemistry, 7(3), 367–377.CrossRefGoogle Scholar
  19. 19.
    Loudos, G., Kagadis, G. C., & Psimadas, D. (2011). Current status and future perspectives of in vivo small animal imaging using radiolabeled nanoparticles. European Journal of Radiology, 78(2), 287–295.CrossRefPubMedGoogle Scholar
  20. 20.
    Mathuriya, A. S. (2015). Magnetotactic bacteria for cancer therapy. Biotechnology Letters, 37(3), 491–498.CrossRefPubMedGoogle Scholar
  21. 21.
    Matsunaga, T., Suzuki, T., Tanaka, M., & Arakaki, A. (2007). Molecular analysis of magnetotactic bacteria and development of functional bacterial magnetic particles for nano-biotechnology. Trends in Biotechnology, 25(4), 182–188.CrossRefPubMedGoogle Scholar
  22. 22.
    Phillips, W. T., Bao, A., Brenner, A. J., & Goins, B. A. (2014). Image-guided interventional therapy for cancer with radiotherapeutic nanoparticles. Advanced Drug Delivery Reviews, 76, 39–59.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Sun, J.-B., Duan, J.-H., Dai, S.-L., Ren, J., Zhang, Y.-D., Tian, J.-S., & Li, Y. (2007). In vitro and in vivo antitumor effects of doxorubicin loaded with bacterial magnetosomes (DBMs) on H22 cells: The magnetic bio-nanoparticles as drug carriers. Cancer Letters, 258(1), 109–117.CrossRefPubMedGoogle Scholar
  24. 24.
    Sun, J., Tang, T., Duan, J., Xu, P.-X., Wang, Z., Zhang, Y., Wu, L., & Li, Y. (2010). Biocompatibility of bacterial magnetosomes: acute toxicity, immunotoxicity and cytotoxicity. Nanotoxicology, 4(3), 271–283.CrossRefPubMedGoogle Scholar
  25. 25.
    Tajer Mohammad Ghazvini, P. (2014). Isolation of magnetic nanoparticles producer bacteria for evaluation in bioremediation processes, PhD thesis, Alzahra University. Google Scholar
  26. 26.
    Tajer Mohammad Ghazvini, P., Kasra Kermanshahi, R., Nozad Golikand, A., & Sadeghizadeh, M. (2014). Isolation and characterization of a novel magnetotactic bacterium from Iran: Iron uptake and producing magnetic nanoparticles in Alphaproteobacterium MTB-KTN90. Jundishapur journal of microbiology, 7, e19343.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Truong, N. P., Whittaker, M. R., Mak, C. W., & Davis, T. P. (2015). The importance of nanoparticle shape in cancer drug delivery. Expert Opinion on Drug Delivery, 12(1), 129–142.CrossRefPubMedGoogle Scholar
  28. 28.
    Wu, Y., Chu, M., Shi, B., & Li, Z. (2011). A novel magneto-fluorescent nano-bioprobe for cancer cell targeting, imaging and collection. Applied Biochemistry and Biotechnology, 163(7), 813–825.CrossRefPubMedGoogle Scholar
  29. 29.
    Xiang, L., Bin, W., Huali, J., Wei, J., Jiesheng, T., Feng, G., & Ying, L. (2007). Bacterial magnetic particles (BMPs)-PEI as a novel and efficient non-viral gene delivery system. The Journal of Gene Medicine, 9(8), 679–690.CrossRefPubMedGoogle Scholar
  30. 30.
    Xiang, L., Wei, J., Jianbo, S., Guili, W., Feng, G., & Ying, L. (2007). Purified and sterilized magnetosomes from Magnetospirillum gryphiswaldense MSR-1 were not toxic to mouse fibroblasts in vitro. Letters in Applied Microbiology, 45(1), 75–81.CrossRefPubMedGoogle Scholar
  31. 31.
    Yan, L., Zhang, S., Chen, P., Liu, H., Yin, H., & Li, H. (2012). Magnetotactic bacteria, magnetosomes and their application. Microbiological Research, 167(9), 507–519.CrossRefPubMedGoogle Scholar
  32. 32.
    Yeong, C.-H., Cheng, M.-H., & Ng, K.-H. (2014). Therapeutic radionuclides in nuclear medicine: current and future prospects. Journal of Zhejiang University Science B, 15(10), 845–863.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Zhang, L., Chen, H., Wang, L., Liu, T., Yeh, J., Lu, G., Yang, L., & Mao, H. (2010). Delivery of therapeutic radioisotopes using nanoparticle platforms: potential benefit in systemic radiation therapy. Nanotechnology, Science and Applications, 3, 159–170.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Zhou, W., Zhang, Y., Ding, X., Liu, Y., Shen, F., Zhang, X., Deng, S., Xiao, H., Yang, G., & Peng, H. (2012). Magnetotactic bacteria: promising biosorbents for heavy metals. Applied Microbiology and Biotechnology, 95(5), 1097–1104.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Somayeh Akbari-Karadeh
    • 1
  • Seyed Mahmoud Reza Aghamiri
    • 1
    Email author
  • Parisa Tajer-Mohammad-Ghazvini
    • 2
    Email author
  • Saeid Ghorbanzadeh-Mashkani
    • 3
  1. 1.Department of Medical Radiation EngineeringShahid Beheshti UniversityTehranIran
  2. 2.Materials and Nuclear Fuel Research SchoolNuclear Science and Technology Research InstituteTehranIran
  3. 3.Nuclear Science and Technology Research InstituteTehranIran

Personalised recommendations