Nanomedicine: Nanotechnology, Biology and Medicine
Volume 4, Issue 4 , Pages 318-329 , December 2008

Nanoimmunoliposome delivery of superparamagnetic iron oxide markedly enhances targeting and uptake in human cancer cells in vitro and in vivo

  • Chengli Yang, PhD

      Affiliations

    • Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC
    • ,
  • Antonina Rait, PhD

      Affiliations

    • Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC
    • ,
  • Kathleen F. Pirollo, PhD

      Affiliations

    • Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC
    • ,
  • John A. Dagata, PhD

      Affiliations

    • National Institute of Standards and Technology, Gaithersburg, MD, USA
    • ,
  • Natalia Farkas, PhD

      Affiliations

    • National Institute of Standards and Technology, Gaithersburg, MD, USA
    • ,
  • Esther H. Chang, PhD

      Affiliations

    • Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC
    • Corresponding Author InformationCorresponding author. Department of Oncology, Lombardi Comprehensive Cancer Center TRB/E420, Georgetown University Medical Center, Washington, DC, USA.

Received 29 September 2007 ,Accepted 20 May 2008.

References 

  1. Fortin JP, Wilhelm C, Servais J, Menager C, Bacri JC, Gazeau F. Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. J Am Chem Soc. 2007;129:2628–2635
  2. Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials. 2005;26:3995–4021
  3. Plank C, Scherer F, Schillinger U, Bergemann C, Anton M. Magnetofection: enhancing and targeting gene delivery with superparamagnetic nanoparticles and magnetic fields. J Lip Res. 2003;13:29–32
  4. Arbab AS, Pandit SD, Anderson SA, Yocum GT, Bur M, Frenkel V, et al. Magnetic resonance imaging and confocal microscopy studies of magnetically labeled endothelial progenitor cells trafficking to sites of tumor angiogenesis. Stem Cells. 2006;24:671–678
  5. Hirao K, Sugita T, Kubo T, Igarashi K, Tanimoto K, Murakami T, et al. Targeted gene delivery to human osteosarcoma cells with magnetic cationic liposomes under a magnetic field. Int J Oncol. 2003;22:1065–1071
  6. Leuschner C, Kumar CS, Hansel W, Soboyejo W, Zhou J, Hormes J. LHRH-conjugated magnetic iron oxide nanoparticles for detection of breast cancer metastases. Breast Cancer Res Treat. 2006;99:163–176
  7. Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L. Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology. 1990;175:489–493
  8. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H, et al. Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology. 2003;229:838–846
  9. Thorek DL, Chen AK, Czupryna J, Tsourkas A. Superparamagnetic iron oxide nanoparticle probes for molecular imaging. Ann Biomed Eng. 2006;34:23–38
  10. Wang YX, Hussain SM, Krestin GP. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur Radiol. 2001;11:2319–2331
  11. Modo M, Hoehn M, Bulte JW. Cellular MR imaging. Mol Imaging. 2005;4:143–164
  12. Gupta AK, Gupta M. Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials. 2005;26:1565–1573
  13. Bruce IJ, Sen T. Surface modification of magnetic nanoparticles with alkoxysilanes and their application in magnetic bioseparations. Langmuir. 2005;21:7029–7035
  14. Wang SF, Tan YM. A novel amperometric immunosensor based on Fe3O4 magnetic nanoparticles/chitosan composite film for determination of ferritin. Anal Bioanal Chem. 2007;387:703–708
  15. Martina MS, Nicolas V, Wilhelm C, Ménager C, Barratt G, Lesieur S. The in vitro kinetics of the interactions between PEG-ylated magnetic-fluid-loaded liposomes and macrophages. Biomaterials. 2007;28:4143–4153
  16. Lu CW, Hung Y, Hsiao JK, Yao M, Chung TH, Lin YS, et al. Bifunctional magnetic silica nanoparticles for highly efficient human stem cell labeling. Nano Lett. 2007;7:149–154
  17. Harisinghani MG, Dixon WT, Saksena MA, Brachtel E, Blezek DJ, Dhawale PJ, et al. MR lymphangiography: imaging strategies to optimize the imaging of lymph nodes with ferumoxtran-10. Radiographics. 2004;24:867–878
  18. MR-TIP.com. MR-Technology Information Portal [homepage on the Internet]. Mattoon, IL: Design Solutions. Softways (c) 2003–2008. [updated 2008 June 23]. Available from: http://www.mr-tip.com.
  19. Zhang Y, Kohler N, Zhang M. Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials. 2002;23:1553–1561
  20. Suwa T, Ozawa S, Ueda M, Ando N, Kitajima M. Magnetic resonance imaging of esophageal squamous cell carcinoma using magnetite particles coated with anti-epidermal growth factor receptor antibody. Int J Cancer. 1998;75:626–634
  21. Tatsushi S, Soji O, Masakazu U, Nobutoshi A, Masaki K. Magnetic resonance imaging of esophageal squamous cell carcinoma using magnetic particles coated with anti-epidermal growth factor receptor antibody. Int J Cancer. 1998;75:626–634
  22. Xu L, Pirollo K, Tang W, Rait A, Chang EH. Transferrin-liposome-mediated systemic p53 gene therapy in combination with radiation results in regression of human head and neck cancer xenografts. Hum Gene Ther. 1999;10:2941–2952
  23. Xu L, Huang CC, Huang WQ, Tang WH, Rait A, Yin Y, et al. Systemic tumor-targeted gene delivery by anti-transferrin receptor scFv-immunoliposomes. Mol Cancer Ther. 2002;1:337–346
  24. Rait AS, Pirollo KF, Xiang L, Ulick D, Chang EH. Tumor-targeting, systemically delivered antisense HER-2 chemosensitizes human breast cancer xenografts irrespective of HER-2 levels. Mol Med. 2002;8:475–486
  25. Pirollo KF, Dagata J, Wang P, Freedman M, Vladar A, Fricke S, et al. A tumor-targeted nanodelivery system to improve early MRI detection of cancer. Mol Imaging. 2006;5:41–52
  26. Pirollo KF, Rait A, Zhou Q, Hwang SH, Dagata JA, Zon G, et al. Materializing the potential of small interfering RNA via a tumor-targeting nanodelivery system. Cancer Res. 2007;67:2938–2943
  27. Ponka P, Lok CN. The transferrin receptor: role in health and disease. Int J Biochem Cell Biol. 1999;31:1111–1137
  28. Liu XQ, Liu HZ, Xing JM, Guan YP, Ma ZY, Shan GB, et al. Preparation and characterization of superparamagnetic functional polymeric microparticles. Chin Particuol. 2003;1:76–79
  29. Yang CL, Xing JM, Guan YP, Liu JG, Shan GB, An ZT, et al. Preparation of magnetic polystyrene microspheres with a narrow size distribution. AIChE J. 2005;51:2011–2015
  30. Ma M, Zhang Y, Yu W, Shen H, Zhang H, Gu N. Preparation and characterization of magnetite nanoparticles coated by amino silane. Colloids Surf A: Physicochem Eng Aspects. 2003;212:219–226
  31. Pan BF, Gao F, Gu HC. Dendrimer modified magnetite nanoparticles for protein immobilization. J Colloid Interface Sci. 2005;284:1–6
  32. Yang C, Xing J, Guan Y, Liu H. Superparamagnetic poly(methyl methacrylate) beads for nattokinase purification from fermentation broth. Appl Microbiol Biotechnol. 2006;72:616–622
  33. Won J, Kim M, Yi YW, Kim YH, Jung N, Kim TK. A magnetic nanoprobe technology for detecting molecular interactions in live cells. Science. 2005;309:121–125
  34. Yu W, Pirollo KF, Yu B, Rait A, Xiang L, Huang W, et al. Enhanced transfection efficiency of a systemically delivered tumor-targeting immunolipoplex by inclusion of a pH-sensitive histidylated oligolysine peptide. Nucleic Acids Res. 2004;32:e48
  35. Leuschner PJ, Ameres SL, Kueng S, Martinez J. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 2006;7:314–320
  36. Xu L, Frederick P, Pirollo K, Tang W, Rait A, Xiang L, et al. Self-assembly of a virus-mimicking nanostructure system for efficient tumor-targeted gene delivery. Hum Gene Ther. 2002;13:469–481
  37. Kohler N, Sun C, Wang J, Zhang M. Methotrexate-modified superparamagnetic nanoparticles and their intracellular uptake into human cancer cells. Langmuir. 2005;21:8858–8864
  38. Ohnishi T, Muroi M, Tanamoto K. MD-2 is necessary for the toll-like receptor 4 protein to undergo glycosylation essential for its translocation to the cell surface. Clin Diag Lab Immunol. 2003;10:405–410
  39. Pirollo KF, Zon G, Rait A, Zhou Q, Yu W, Hogrefe R, et al. Tumor-targeting nanoimmunoliposome complex for short interfering RNA delivery. Hum Gene Ther. 2006;17:117–124
  40. Xu L, Pirollo K, Chang EH, Murray A. Systemic p53 gene therapy in combination with radiation results in human tumor regression. Tumor Targeting. 1999;4:92–104
  41. Daniels TR, Delgado T, Rodriguez JA, Helguera G, Penichet ML. The transferrin receptor part I: biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin Immunol. 2006;121:144–158
  42. Hudgins PA, Anzai Y, Morris MR, Lucas MA. Ferumoxtran-10, a superparamagnetic iron oxide as a magnetic resonance enhancement agent for imaging lymph nodes: a phase 2 dose study. AJNR Am J Neuroradiol. 2002;23:649–656
  43. Mack MG, Balzer JO, Straub R, Eichler K, Vogl TJ. Superparamagnetic iron oxideenhanced MR imaging of head and neck lymph nodes. Radiology. 2002;222:239–244
  44. Michel ML, Mancini-Bourgine M. Therapeutic vaccination against chronic hepatitis B virus infection. J Clin Virol. 2005;34:S108–S114
  45. Tanimoto A, Yuasa Y, Shinmoto H, Jinzaki M, Imai Y, Okuda S, et al. Superparamagnetic iron oxide-mediated hepatic signal intensity change in patients with and without cirrhosis: pulse sequence effects and Kupffer cell function. Radiology. 2002;222:661–666
  46. Kim JH, Kim MJ, Suh SH, Chung JJ, Yoo HS, Lee JT. Characterization of focal hepatic lesions with ferumoxides-enhanced MR imaging: utility of T1-weighted spoiled gradient recalled echo images using different echo times. J Magn Reson Imaging. 2002;15:573–583
  47. Ward J, Chen F, Guthrie JA, Wilson D, Lodge JP, Wyatt JI, et al. Hepatic lesion detection after superparamagnetic iron oxide enhancement: comparison of five T2-weighted sequences at 1.0 T by using alternative-free response receiver operating characteristic analysis. Radiology. 2000;214:159–166
  48. Jordan A, Scholz R, Wust P, Fahling H, Krause J, Wlodarczyk W, et al. Effects of magnetic fluid hyperthermia (MFH) on C3H mammary carcinoma in vivo. Int J Hyperthermia. 1997;13:587–605
  49. Ito A, Tanaka K, Honda H, Abe S, Yamaguchi H, Kobayashi T. Complete regression of mouse mammary carcinoma with a size greater than 15 mm by frequent repeated hyperthermia using magnetite nanoparticles. J Biosci Bioeng. 2003;96:364–369
  50. Maier-Hauff K, Rothe R, Scholz R, Gneveckow U, Wust P, Thiesen B, et al. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. J Neurooncol. 2007;81:53–60
  51. Lee H, Lee E, Kim DK, Jang NK, Jeong YY, Jon S. Antibiofouling polymer-coated superparamagnetic iron oxide nanoparticles as potential magnetic resonance contrast agents for in vivo cancer imaging. J Am Chem Soc. 2006;128:7383–7389
  52. Ito A, Kuga Y, Honda H, Kikkawa H, Horiuchi A, Watanabe Y, et al. Magnetite nanoparticle-loaded anti-HER2 immunoliposomes for combination of antibody therapy with hyperthermia. Cancer Lett. 2004;212:167–175

 This work was supported by a National Cancer Institute (NCI) grant 5R01CA132012-02 (E.H.C.) and a research grant from SynerGene Therapeutics, Inc. (SGT) (K.F.P.). These studies were conducted in part using the Microscopy and Imaging, Histopathology and Tissue, and Animal Core Facilities supported by NCI Cancer Center Support grant and US Public Health Service grant 2P30-CA-51008 and 1 S10 RR 15768-01. This investigation was performed in part in a facility constructed with support from Research Facilities Improvement grant C06RR14567 from the National Center for Research Resources, National Institutes of Health. A.R. is a consultant for SGT; E.H.C. is a consultant for SGT, in which she has significant personal financial interest. SGT had no involvement in study design; in the collection, analysis, or interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

PII: S1549-9634(08)00085-3

doi: 10.1016/j.nano.2008.05.004

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 4, Issue 4 , Pages 318-329 , December 2008

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