Issue

Vol. 8 No. 1 (2016)

Bovine Serum Albumin-Conjugated Ferrimagnetic Iron Oxide Nanoparticles to Enhance the Biocompatibility and Magnetic Hyperthermia Performance

https://doi.org/10.1007/s40820-015-0065-1
Viveka Kalidasan
Department of Materials Science and Engineering, Faculty of Engineering, National University of Singapore, 7 Engineering Drive 1, Singapore 117574, Singapore
Xiao Li Liu
Department of Materials Science and Engineering, Faculty of Engineering, National University of Singapore, 7 Engineering Drive 1, Singapore 117574, Singapore
Tun Seng Herng
Department of Materials Science and Engineering, Faculty of Engineering, National University of Singapore, 7 Engineering Drive 1, Singapore 117574, Singapore
Yong Yang
Department of Materials Science and Engineering, Faculty of Engineering, National University of Singapore, 7 Engineering Drive 1, Singapore 117574, Singapore
Jun Ding
Department of Materials Science and Engineering, Faculty of Engineering, National University of Singapore, 7 Engineering Drive 1, Singapore 117574, Singapore

Corresponding Author: Jun Ding

msedingj@nus.edu.sg

Nano-Micro Letters, Vol. 8 No. 1 (2016), Article Number: 80-93

Abstract

Magnetic hyperthermia is a fast emerging, non-invasive cancer treatment method which is used synergistically with the existing cancer therapeutics. We have attempted to address the current challenges in clinical magnetic hyperthermia-improved biocompatibility and enhanced heating characteristics, through a single combinatorial approach. Both superparamagnetic iron oxide nanoparticles (SPIONs) of size 10 nm and ferrimagnetic iron oxide nanoparticles (FIONs) of size 30 nm were synthesized by thermal decomposition method for comparison studies. Two different surface modifying agents, viz, Cetyl Trimethyl Ammonium Bromide and 3-Aminopropyltrimethoxysilane, were used to conjugate Bovine Serum Albumin (BSA) over the iron oxide nanoparticles via two different methods—surface charge adsorption and covalent amide bonding, respectively. The preliminary haemolysis and cell viability experiments show that BSA conjugation mitigates the haemolytic effect of the iron oxide nanoparticles on erythrocytes and is non-cytotoxic to the healthy Baby Hamster Kidney cells. It was observed from the results that due to better colloidal stability, the SAR value of the BSA-iron oxide nanoparticles is higher than the iron oxide nanoparticles without BSA, irrespective of the size of the iron oxide nanoparticles and method of conjugation. The BSA-FIONs seem to show improved biocompatibility, as the haemolytic index is less than 2 % and cell viability is up to 120 %, when normalized with the control. The SAR value of BSA-FIONs is 2300 W g−1 when compared to 1700 W g−1 of FIONs without BSA conjugation. Thus, we report here that BSA conjugation over FIONs (with a high saturation magnetization of 87 emu g−1) provide a single combinatorial approach to improve the biocompatibility and enhance the SAR value for magnetic hyperthermia, thus addressing both the current challenges of the same.

Keywords

Magnetic hyperthermia Ferrimagnetic iron oxide nanoparticles Bovine serum albumin Haemolysis Cell viability Specific absorption rate
Kalidasan, Viveka, Xiao Li Liu, Tun Seng Herng, Yong Yang, and Jun Ding. 2015. “Bovine Serum Albumin-Conjugated Ferrimagnetic Iron Oxide Nanoparticles to Enhance the Biocompatibility and Magnetic Hyperthermia Performance”. Nano-Micro Letters 8 (1):80-93. https://doi.org/10.1007/s40820-015-0065-1.
Download Citation
Endnote/Zotero/Mendeley (RIS)
BibTeX
References
  1. H. Mamiya, B. Jeyadevan, Hyperthermic effects of dissipative structures of magnetic nanoparticles in large alternating magnetic fields. Sci. Rep. 1, 1–7 (2011). doi:10.1038/srep00157
  2. R. Siegal, J. Ma, Z. Zou, A. Jemal, Cancer statistics, 2014. CA-Cancer J. Clin. 64(1), 9–29 (2014). doi:10.3322/caac.21208
  3. A.J. Guistini, A.A. Petryk, S.M. Cassim, J.A. Tate, I. Baker, P.J. Hookes, Magnetic nanoparticles hyperthermia in cancer treatment. Nano Life 17(1), 17–32 (2010). doi:10.1142/S1793984410000067
  4. T. Kobayashi, Cancer hyperthermia using magnetic nanoparticles. Biotechnol. J. 6(11), 1342–1347 (2011). doi:10.1002/biot.201100045
  5. A.K. Gupta, M. Gupta, Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26(18), 3995–4021 (2005). doi:10.1016/j.biomaterials.2004.10.012
  6. M. Chastellain, A. Petri, A. Gupta, K.V. Rao, H. Hofmann, Superparamagnetic silica–iron oxide nanocomposites for application in hyperthermia. Adv. Eng. Mater. 6(4), 235–241 (2004). doi:10.1002/adem.200300574
  7. S. Laurent, D. Forge, M. Port, A. Roch, C. Robic, L.V. Elst, R.N. Muller, Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physiochemical characterizations, and biological applications. Chem. Rev. 108(6), 2064–2110 (2008). doi:10.1021/cr068445e
  8. H. Yousef, B. al-Ramadi, B. Issa, S.Qadri1, S. Hayek, H. Hijaze, Multifunctional nanoparticles for imaging guided interventions. Available from Nature Precedings http://hdl.handle.net/10101/npre.2008.2190.1 (2008)
  9. A. Itoa, M. Shinkaib, H. Hondaa, T. Kobayashi, Medical application of functionalized magnetic nanoparticles. J. Biosci. Bioeng. 100(1), 1–11 (2005). doi:10.1263/jbb.100.1
  10. M. Mitsumori, M. Hiraoka, T. Shibata, Y. Okuno, Y. Nagata, Y. Nishimura, M. Abe, M. Hasegawa, H. Nagae, Targeted hyperthermia using dextran magnetite complex: a new treatment modality for liver tumors. Hepato Gastroenterology 43(12), 1431–1437 (1996)
  11. Robert W. Rand, Harold D. Snow, David G. Elliott, Melvin Snyder, Thermomagnetic surgery for cancer. Appl. Biochem. Biotechnol. 6(4), 265 (1981). doi:10.1007/BF02798277
  12. G.L. DeNardo, S.J. DeNardo, Update: turning the heat on cancer. Cancer Biother. Radiopharm. 23(6), 671–679 (2008). doi:10.1089/cbr.2008.0591
  13. F. Herranz, J. Ruiz-Cabello, M.P. Morales, A.G. Roca, R. Vilar, Superparamagnetic nanoparticles for atherosclerosis imaging. Contrast Media Mol. Imaging 3, 215–222 (2008). doi:10.1002/cmmi.254
  14. F. Herranz, C.B. Schmidt-Weber, M.H. Shamji, A. Narkus, J. Ruiz-Cabello, R. Vilar, Superparamagnetic iron oxide nanoparticles conjugated to a grass pollen allergen and an optical probe. Contrast Media Mol. Imaging 7, 435–439 (2012). doi:10.1002/cmmi.1466
  15. B. Salinas, J. Ruiz Cabello, M.P. Morales, F. Herranz, Olefin metathesis for the functionalization of superparamagnetic nanoparticles. Bioinspired Biomim. Nanobiomater. 1, 166–172 (2012). doi:10.1680/bbn.12.00001
  16. Y. Sahoo, H. Pizem, T. Fried, D. Golodnitsky, L. Burstein, C.N. Sukenik, G. Markovich, Alkyl phosphonate/phosphate coating on magnetite nanoparticles: a comparison with fatty acids. Langmuir 17, 7907–7911 (2001). doi:10.1021/la010703+
  17. L.M. Bronstein, E.V. Shtykova, A. Malyutin, J.C. Dyke, E. Gunn, X. Gao, B. Stein et al., Hydrophilization of magnetic nanoparticles with modified alternating copolymers. Part 1: the influence of the grafting. J. Phys. Chem. C 114(50), 21900–21907 (2010). doi:10.1021/jp107283w
  18. H. Su, Y. Liu, D. Wang, C. Wu, C. Xia, Q. Gong, B. Song, H. Ai, Amphiphilic starlike dextran wrapped superparamagnetic iron oxide nanoparticle clsuters as effective magnetic resonance imaging probes. Biomaterials 34(4), 1193–1203 (2013). doi:10.1016/j.biomaterials.2012.10.056
  19. C.L. Dennis, A.J. Jackson, J.A. Borchers, P.J. Hoopes, R. Strawbridge, A.R. Foreman, J. van Lierop, C. Grüttner, R. Ivkov, Nearly complete regression of tumors via collective behavior of magnetic nanoparticles hyperthermia. Nanotechnology 20(39), 395103 (2009). doi:10.1088/0957-4484/20/39/395103
  20. E.L. Verde, G.T. Landi, M.S. Carrião, A.L. Drummond, J.A. Gomes, E.D. Vieira, M.H. Sousa, A.F. Bakuzis, Field dependent transition to the non-linear regime in magnetic hyperthermia experiments: comparison between maghemite, copper, zinc, nickel and cobalt ferrite nanoparticles of similar sizes. AIP Advances 2(3), 032120–032142 (2012). doi:10.1063/1.4739533
  21. J. Carrey, B. Mehdaoui, M. Respaud, Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: application to magnetic hyperthermia optimization. J. Appl. Phys. 109, 083921–083937 (2011). doi:10.1063/1.3551582
  22. A. Attaluri, R. Ma, Y. Qiu, W. Li, L. Zhu, Nanoparticle distribution and temperature elevations in prostatic tumours in mice during magnetic nanoparticle hyperthermia. Int. J. Hyperthermia 27(5), 491–502 (2011). doi:10.3109/02656736.2011.584856
  23. P. Guardia, R.D. Corato, L. Lartigue, C. Wilhelm, A. Espinosa, M.G. Hernandez, F. Gazeau, L. Manna, T. Pellegrino, Water-soluble iron oxide nanocubes with high values of specific absorption rate for cancer cell hyperthermia treatment. ACS Nano 6(4), 3080–3091 (2012). doi:10.1021/nn2048137
  24. S. Patra, E. Roy, P. Karfa, S. Kumar, R. Madhuri, P.K. Sharma, Dual-responsive polymer coated superparamagnetic nanoparticle for targeted drug delivery and hyperthermia treatment. ACS Appl. Mater. Interfaces 7(17), 9235–9246 (2015). doi:10.1021/acsami.5b01786
  25. L. Lartigue, C. Innocenti, T. Kalaivani, A. Awwad, M. del Mar Sanchez Duque et al., Water-dispersible sugar-coated iron oxide nanoparticles. an evaluation of their relaxometric and magnetic hyperthermia properties. JACS 133(27), 10459–10472 (2011). doi:10.1021/ja111448t
  26. P. Businova, J. Chomoucka, J. Prasek, R. Hrdy, J. Drbohlavov, P. Sedlacek, J. Hubalek, Polymer coated iron oxide magnetic nanoparticles: preparation and characterization. Nanocon 9, 21–23 (2011)
  27. K.M. Seemann, B. Kuhn, Multi-photon excited luminescence of magnetic FePt core–shell nanoparticles. Biomedical Optics Express 5(7), 2446–2457 (2014). doi:10.1364/BOE.5.002446
  28. K.M. Seemann, M. Luysberg, Z. Révay, P. Kudejova, B. Sanz et al., Magnetic heating properties and neutron activation of tungsten-oxide coated biocompatible FePt core–shell nanoparticles. J. Control. Release 197, 131–137 (2015). doi:10.1016/j.jconrel.2014.11.007
  29. Y. Liu, M.J. Welch, Nanoparticles labeled with positron emitting nuclides: advantages, methods, and applications. Bioconjug. Chem. 23, 671–682 (2012). doi:10.1021/bc200264c
  30. Y.-H. Deng, C.-C. Wang, J.-H. Hu, W.L. Yang, S.-K. Fu, Investigation of formation of silica-coated magnetite nanoparticles via sol–gel approach. Colloids Surf. Physicochem. Eng. Asp. 262, 87–93 (2005). doi:10.1016/j.colsurfa.2005.04.009
  31. S.M. Moghimi, A.C. Hunter, J.C. Murray, Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 53(2), 283–318 (2005)
  32. J. Hankins, The role of albumin in fluid and electrolyte balance. J. Infusion Nursing 29(5), 260–265 (2009). doi:10.1097/00129804-200609000-00004
  33. K. Hirayama, S. Akashi, M. Furuya, K. Fukuhara, K, Rapid confirmation and revision of the primary structure of bovine serum albumin by ESIMS and Frit-FAB LC/MS. Biochem. Biophys. Res. Commun. 173(2), 639–646 (1990). doi:10.1016/S0006291X(05)80083-X
  34. P. Green, A.E. Woglom, P. Genereux, B. Daneault, J.M. Paradis et al., The impact of frailty status on survival after transcatheter. JACC Cardiovasc. Interv. 5(9), 974–981 (2012). doi:10.1016/j.jcin.2012.06.011
  35. S. Ge, K. Kojio, A. Takahara, T. Kajiyama, Bovine serum albumin adsorption onto immobilized organotrichlorosilane surface: influence of the phase separation on protein adsorption patterns. J. Biomater. Sci. Polym. E 9(2), 131–150 (1998). doi:10.1163/156856298X00479
  36. A. Juríková, K. Csach, J. Miškuf, M. Koneracká, V. Závišová, P. Kopčanský, Thermal analysis of magnetic polymer nanospheres for drug targeting. Acta Phys. Pol. A 118(5), 990–992 (2010)
  37. M. Keshavarz, Z. Ghasemi, Coating of iron oxide nanoparticles with human and bovine serum albumins: a thermodynamic approach. J. Phys. Theor. Chem. IAU Iran 8(2), 85–95 (2011)
  38. B. Samanta, H. Yan, N.O. Fischer, J. Shi, D.J. Jerry, V.M. Rotelloa, Protein-passivated Fe3O4 nanoparticles: low toxicity and rapid heating for thermal therapy. J. Mater. Chem. 18(11), 1204–1208 (2008). doi:10.1039/b718745a
  39. J.-H. Lee, J.-T. Jang, J.-S. Choi, S.-H. Moon, S.-H. Noh et al., Exchange-coupled magnetic nanoparticles for efficient heat induction. Nat. Nanotechnol. 6, 418–422 (2011). doi:10.1038/nnano.2011.95
  40. L.C. Branquinho, M.S. Carrião, A.S. Costa, N. Zufelato, M.H. Sousa, R. Miotto, R. Ivkov, A.F. Bakuzis, Effect of magnetic dipolar interactions on nanoparticle heating efficiency: implications for cancer hyperthermia. Sci. Rep. 3, 2887 (2013). doi:10.1038/srep02887
  41. C.M. Boubeta, K. Simeonidis, A. Makridis, M. Angelakeris, O. Iglesias et al., Learning from nature to improve the heat generation of iron-oxide nanoparticles for magnetic hyperthermia applications. Sci. Rep. 3, 1652 (2013). doi:10.1038/srep01652
  42. M. Hu, J.-S. Jiang, F.-X. Bu, X.-L. Cheng, C.-C. Lin, Y. Zeng, Hierarchical magnetic iron (III) oxides prepared by solid-state thermal decomposition of coordination polymers. RSC Adv. 2, 4782–4786 (2012). doi:10.1039/C2RA01190E
  43. W. Baaziz, B.P. Pichon, S. Fleutot, Y. Liu, C. Lefevre, J.-M. Greneche, M. Toumi, T. Mhiri, S.B. Colin, Magnetic iron oxide nanoparticles: reproducible tuning of the size and nanosized-dependent composition, defects, and spin canting. J. Phys. Chem. C 118(7), 3795–3810 (2014). doi:10.1021/jp411481p
  44. P. Guardia, A. Labarta, X. Batlle, Tuning the size, the shape, and the magnetic properties of iron oxide nanoparticles. J. Phys. Chem. C 115, 390 (2010). doi:10.1021/jp1084982
  45. R. Hufschmid, H. Arami, R.M. Ferguson, M. Gonzales, E. Teeman, L.N. Brush, N.D. Browning, K.M. Krishnan, Synthesis of phase-pure and monodisperse iron oxide nanoparticles by thermal decomposition. Nanoscale 7, 11142–11154 (2015). doi:10.1039/C5NR01651G
  46. W. Wu, Z. Wu, T. Yu, C. Jiang, W.S. Kim, Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci. Technol. Adv. Mater. (2015). doi:10.1088/1468-6996/16/2/023501
  47. R. Qiao, C. Yang, M. Gao, Superparamagnetic iron oxide nanoparticles: from preparations to in vivo MRI applications. J. Mater. Chem. 19, 6274–6293 (2009). doi:10.1039/b902394a
  48. G. Kim, M. Wutzler, H.J. Radusch, G.H. Michler, P. Simon, R.A. Sperling, W.J. Parak, One-dimensional arrangement of gold nanoparticles by electrospinning. Chem. Mater. 17, 4949–4957 (2005). doi:10.1021/cm0508120
  49. X.M. Lin, A.C.S. Samia, Synthesis, assembly and physical properties of magnetic nanoparticles. J. Magn. Magn. Mater. 305(1), 100–109 (2006). doi:10.1016/j.jmmm.2005.11.042
  50. J. Huang, L. Wang, R. Lin, A.Y. Wang, L. Yang, M. Kuang, W. Qian, H. Mao, Casein-coated iron oxide nanoparticles for high MRI contrast enhancement and efficient cell targeting. ACS Appl. Mater. Interfaces 5(11), 4632–4639 (2013). doi:10.1021/am400713j
  51. M.-H. Liao, D-H. Chen, Immobilization of yeast alcohol dehydrogenase on magnetic nanoparticles for improving its stability. Biotechnol. Lett. 23(20), 1723–1727 (2001). doi:10.1023/A:1012485221802
  52. H. Huang, R. Christmann, R. Ulber, V. Schünemann, Mössbauer spectroscopy of protein-passivated iron oxide nanoparticles. Hyperfine Interactions 205(1–3), 121–124 (2012). doi:10.1007/s10751-011-0502-6
  53. S. Pathak, S.K. Choi, N. Arnheim, M.E. Thompson, Hydroxylated quantum dots as luminescent probes for in situ hybridization. JACS 123(17), 4103–4104 (2001). doi:10.1021/ja0058334
  54. F. Shamsipour, A.H. Zarnani, R. Ghods, M. Chamankhah, F. Forouzesh et al., Conjugation of monoclonal antibodies to super paramagnetic iron oxide nanoparticles for detection of her2/neu antigen on breast cancer cell lines. Avicenna J. Med. Biotechnol. 1(1), 27–31 (2009)
  55. C.L. Priya, G. Kumar, L. Karthik, K.V.B. Rao, Phytochemical composition and in vitro antioxidant activity of achyranthes aspera linn (amaranthaceae) leaf extracts. Int. J. Agric. Technol. 8, 143–156 (2012)
  56. M. Nakaya, R. Nishida, A. Muramatsu, Size control of magnetite nanoparticles in excess ligands as a function of reaction temperature and time. Molecules 19(8), 11395–11403 (2014). doi:10.3390/molecules190811395
  57. D. Ling, N. Lee, T. Hyeon, Chemical synthesis and assembly of uniformly sized iron oxide nanoparticles for medical applications. Acc. Chem. Res. 48(5), 1276–1285 (2015). doi:10.1021/acs.accounts.5b00038
  58. A. Hu, A. Apblett, Nanotechnology for Water Treatment and Purification. Lecture Notes in Nanoscale Science and Technology, vol. 22. (Springer, New York, 2014)
  59. A. Mitra, J. Mohapatra, S.S. Meena, C.V. Tomy, M. Aslam, Verwey transition in ultrasmall-sized octahedral Fe3O4 nanoparticles. J. Phys. Chem. C 118, 19356–19362 (2014). doi:10.1021/jp501652e
  60. K. Šliužienė, V. Lisauskas, R. Butkutė, B. Vengalis, S. Tamulevicius, M. Andrulevicius, Growth and investigation of p-n structures based on Fe3O4 thin films. J. Phys. Conf. Ser. 100(8), 082028 (2008). doi:10.1088/1742-6596/100/8/082028
  61. A. Nemati, S. Shadpourab, H. Khalafbeygia, M. Barkhi, Hydrothermal synthesis and size control of Fe3O4 nanoparticles in the presence of 2,2′,2″,2″′-(ethane-1,2-diylbis(azanetriyl))tetraacetohydrazide. Syn. React. Inorg. Metal- Org. Nano-Metal Chem. 44(8), 1161–1165 (2014). doi:10.1080/15533174.2013.797443
  62. G.K. Kouassi, J. Irudayaraj, Magnetic and gold-coated magnetic nanoparticles as a DNA sensor. Anal. Chem. 78, 3234–3241 (2006). doi:10.1021/ac051621j
  63. J.F. Sun, X. Liu, Y. Chen, Y. Zhang, N. Gu, Exploiting BSA to inhibit the fibrous aggregation of magnetic nanoparticles under an alternating magnetic field. Int. J. Mol. Sci. 14(3), 5775–5783 (2013). doi:10.3390/ijms14035775
  64. M.L. Etheridge, K.R. Hurley, J. Zhang, S. Jeon, H.L. Ring, C. Hogan, C.L. Haynes, M. Garwood, J.C. Bischof, Accounting for biological aggregation in heating and imaging of magnetic nanoparticles. Technology (Singap. World Sci.) 2(3), 214–228 (2014). doi:10.1142/S2339547814500198
Read More
Author biographies are not available.
Download this PDF file
PDF
Statistic
Read Counter : 4111 Download : 3125

Most read articles by the same author(s)