Galbanic Acid-Coated Fe3O4 Magnetic Nanoparticles with Enhanced Cytotoxicity to Prostate Cancer Cells

Leila Mohtashami; Narjes Ghows; Zahra Tayarani-Najaran; Mehrdad Iranshahi

doi:10.1055/a-0721-1886

Planta Medica, Table of Contents

Planta Med 2019; 85(02): 169-178
DOI: 10.1055/a-0721-1886

Formulation and Delivery Systems of Natural Products

Original Papers

Georg Thieme Verlag KG Stuttgart · New York

Galbanic Acid-Coated Fe₃O₄ Magnetic Nanoparticles with Enhanced Cytotoxicity to Prostate Cancer Cells

Leila Mohtashami

¹Department of Pharmacognosy, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

,

Narjes Ghows

²Sonochemical Research Center, Department of Chemistry, Ferdowsi University of Mashhad, Mashhad, Iran

,

Zahra Tayarani-Najaran

³Department of Pharmacodynamics and Toxicology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

,

Mehrdad Iranshahi

⁴Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

› Author Affiliations

Abstract

Galbanic acid is a natural sesquiterpene coumarin compound with different biological activities, particularly cytotoxicity against LNCaP (an androgen-dependent prostate cancer cell line). Galbanic acid induces apoptosis in LNCaP via down-regulation of androgen receptor. However, the poor water-solubility of galbanic acid limits further in vitro and in vivo studies. In this study we present the synthesis of galbanic acid-coated Fe₃O₄ magnetic nanoparticles and their cytotoxicity evaluation on three prostate cancer cell lines, including PC3 (an androgen-independent cell line), LNCaP, and DU145 (an androgen-independent cell line). The synthesized nanoparticles were characterized by X-ray diffraction spectroscopy, Fourier transform infrared spectroscopy, transmission electron microscopy, scattering electron microscopy, energy-dispersive X-ray spectroscopy, dynamic light scattering, and vibrating sample magnetometry. Our cytotoxicity evaluation demonstrated that galbanic acid was cytotoxic only against LNCaP cells, while the galbanic acid-coated Fe₃O₄ nanoparticles showed cytotoxicity on all tested cells, including androgen-dependent and -independent cell lines. This indicates that other mechanisms are involved in the cytotoxicity of galbanic acid in addition to androgen receptor down-regulation. In conclusion, the loading of galbanic acid on the surface of Fe₃O₄ magnetic nanoparticles turned out to be a successful approach to enhance the solubility and cytotoxicity of this compound.

Key words

Ferula assa-foetida - Apiaceae - galbanic acid - prostate cancer - Fe₃O₄ magnetic nanoparticles - cytotoxicity

Full Text

References

References
1 Attard G, Parker C, Eeles RA, Schröder F, Tomlins SA, Tannock I, Drake CG, de Bono JS. Prostate cancer. Lancet 2016; 387: 70-82
2 Xu J, Zheng SL, Komiya A, Mychaleckyj JC, Isaacs SD, Hu JJ, Sterling D, Lange EM, Hawkins GA, Turner A, Ewing CM, Faith DA, Johnson JR, Suzuki H, Bujnovszky P, Wiley KE, DeMarzo AM, Bova GS, Chang B, Hall MC, McCullough DL, Partin AW, Kassabian VS, Carpten JD, Bailey-Wilson JE, Trent JM, Ohar J, Bleecker ER, Walsh PC, Isaacs WB, Meyers DA. Germline mutations and sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Nat Genet 2002; 32: 321-325
3 Nelson WG, De Marzo AM, Isaacs WB. Prostate cancer. N Engl J Med 2003; 349: 366-381
4 Kung HJ, Evans CP. Oncogenic activation of androgen receptor. Urol Oncol 2009; 27: 48-52
5 Zhang Y, Kim KH, Zhang W, Guo Y, Kim SH, Lü J. Galbanic acid decreases androgen receptor abundance and signaling and induces G₁ arrest in prostate cancer cells. Int J Cancer 2012; 130: 200-212
6 Kasaian J, Iranshahy M, Iranshahi M. Synthesis, biosynthesis and biological activities of galbanic acid – A review. Pharm Biol 2013; 52: 524-531
7 Shahverdi AR, Fakhimi A, Zarrini G, Dehghan G, Iranshahi M. Galbanic acid from Ferula szowitsiana enhanced the antibacterial activity of penicillin G and cephalexin against Staphylococcus aureus . Biol Pharm Bull 2007; 30: 1805-1807
8 Lee CL, Chiang LC, Cheng LH, Liaw CC, Abd El-Razek MH, Chang FR, Wu YC. Influenza A (H(1)N(1)) antiviral and cytotoxic agents from Ferula assa-foetida . J Nat Prod 2009; 72: 1568-1572
9 Kimura Y. Prevention of Cancer Chemotherapy drug-induced adverse Reaction, antitumor and antimetastatic Activities by natural Products. In: Atta-ur-Rahman. ed. Studies in natural Products Chemistry. Amsterdam: Elsevier; 2003: 559-586
10 Kimura Y. Antitumor and vascular physiological Effects of natural Products. In: Atta-ur-Rahman. ed. Studies in natural Products Chemistry. Amsterdam: Elsevier; 2005: 55-78
11 Kimura Y. Antitumor and antimetastatic Actions of various natural Products. In: Atta-ur-Rahman. ed. Studies in natural Products Chemistry. Amsterdam: Elsevier; 2008: 35-76
12 Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005; 26: 3995-4021
13 Chastellain M, Petri A, Hofmann H. Superparamagnetic silica-iron oxide nanocomposites for application in hyperthermia. Adv Eng Mater 2004; 6: 235-241
14 Valdiglesias V, Fernández-Bertólez N, Kiliç G, Costa C, Costa S, Fraga S, Bessa MJ, Pásaro E, Teixeira JP, Laffon B. Are iron oxide nanoparticles safe? Current knowledge and future perspectives. J Trace Elem Med Biol 2016; 38: 53-63
15 Maccarini M, Atrei A, Innocenti C, Barbucci R. Interactions at the CMC/magnetite interface: Implications for the stability of aqueous dispersions and the magnetic properties of magnetite nanoparticles. Colloids Surf A Physicochem Eng Asp 2014; 462: 107-114
16 Yazdani F, Seddigh M. Magnetite nanoparticles synthesized by co-precipitation method: The effects of various iron anions on specifications. Mater Chem Phys 2016; 184: 318-323
17 Hedayati K, Goodarzi M, Ghanbari D. Hydrothermal synthesis of Fe₃O₄ nanoparticles and flame resistance magnetic poly styrene nanocomposite. J Nanostruct 2017; 7: 32-39
18 Xu J, Yang H, Fu W, Du K, Sui Y, Chen J, Zeng Y, Li M, Zou G. Preparation and magnetic properties of magnetite nanoparticles by sol–gel method. J Magn Magn Mater 2007; 309: 307-311
19 Lemine OM, Omri K, Zhang B, El Mir L, Sajieddine M, Alyamani A, Bououdina M. Sol–gel synthesis of 8 nm magnetite (Fe₃O₄) nanoparticles and their magnetic properties. Superlattices Microstruct 2012; 52: 793-799
20 Salazar-Alvarez G, Muhammed M, Zagorodni AA. Novel flow injection synthesis of iron oxide nanoparticles with narrow size distribution. Chem Eng Sci 2006; 61: 4625-4633
21 Pascal C, Pascal JL, Favier F, Elidrissi Moubtassim ML, Payen C. Electrochemical synthesis for the control of γ-Fe₂O₃ nanoparticle size. Morphology, microstructure, and magnetic behavior. Chem Mater 1999; 11: 141-147
22 Wu W, He Q, Chen H, Tang J, Nie L. Sonochemical synthesis, structure and magnetic properties of air-stable Fe₃O₄/Au nanoparticles. Nanotechnology 2007; 18: 145609
23 Hachani R, Lowdell M, Birchall M, Hervault A, Mertz D, Begin-Colin S, Thanh NT. Polyol synthesis, functionalisation, and biocompatibility studies of superparamagnetic iron oxide nanoparticles as potential MRI contrast agents. Nanoscale 2016; 8: 3278-3287
24 Strobel R, Pratsinis SE. Direct synthesis of maghemite, magnetite and wustite nanoparticles by flame spray pyrolysis. Adv Powder Technol 2009; 20: 190-194
25 Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, Muller RN. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 2008; 108: 2064-2110
26 Nosrati H, Salehiabar M, Davaran S, Danafar H, Kheiri Manjili H. Methotrexate-conjugated L-lysine coated iron oxide magnetic nanoparticles for inhibition of MCF-7 breast cancer cells. Drug Dev Ind Pharm 2018; 44: 886-894
27 Nosrati H, Salehiabar M, Attari E, Davaran S, Danafar H, Kheiri Manjili H. Green and one-pot surface coating of iron oxide magnetic nanoparticles with natural amino acids and biocompatibility investigation. Appl Organomet Chem 2018; 32: e4069
28 Nosrati H, Rashidi N, Danafar H, Kheiri Manjili H. Anticancer activity of tamoxifen loaded tyrosine decorated biocompatible Fe₃O₄ magnetic nanoparticles against breast cancer cell lines. J Inorg Organomet Polym Mater 2018; 28: 1178-1186
29 Nosrati H, Salehiabar M, Kheiri Manjili H, Danafar H, Davaran S. Preparation of magnetic albumin nanoparticles via a simple and one-pot desolvation and co-precipitation method for medical and pharmaceutical applications. Int J Biol Macromol 2018; 108: 909-915
30 Khandhar AP, Keselman P, Kemp SJ, Ferguson RM. Evaluation of PEG-coated iron oxide nanoparticles as blood pool tracers for preclinical magnetic particle imaging. Nanoscale 2017; 9: 1299-1306
31 Nadeem M, Ahmad M, Akhtar MS, Shaari A, Riaz S, Naseem S, Masood M, Saeed MA. Magnetic properties of polyvinyl alcohol and doxorubicine loaded iron oxide nanoparticles for anticancer drug delivery applications. PLoS One 2016; 11: e0158084
32 Wulandari IO, Mardila VD, Santjojo DJDH, Sabarudin A. Preparation and characterization of chitosan-coated Fe₃O₄ nanoparticles using ex-situ co-precipitation method and tripolyphosphate/sulphate as dual crosslinkers. IOP Conference Series: Mater Sci Eng 2018; 299: 012064.
33 Kim DK, Mikhaylova M, Zhang Y, Muhammed M. Protective coating of superparamagnetic iron oxide nanoparticles. Chem Mater 2003; 15: 1617-1627
34 Lakay EM. Superparamagnetic Iron Oxide based Nanoparticles for the Separation and Recovery of precious Metals from Solution [Dissertation]. Stellenbosch: University of Stellenbosch; 2009
35 Khosroshahi ME, Ghazanfari L. Preparation and characterization of silica-coated iron oxide bionanoparticles under N₂ gas. Physica E Low Dimens Syst Nanostruct 2010; 42: 1824-1829
36 Haw CY, Chia CH, Zakaria S, Mohamed F, Radiman S, Teh CH, Khiew PS, Chiu WS, Huang NM. Morphological studies of randomized dispersion magnetite nanoclusters coated with silica. Ceram Int 2011; 37: 451-464
37 Salopek B, Krasić D, Filipović S. Measurement and application of zeta potential. Rudarsko-geoloSko-naftni zbornik 1992; 4: 147-151
38 Kumar SR, Priyatharshni S, Babu VN, Mangalaraj D, Viswanathan C, Kannan S, Ponpandian N. Quercetin conjugated superparamagnetic magnetite nanoparticles for in vitro analysis of breast cancer cell lines for chemotherapy applications. J Colloid Interface Sci 2014; 436: 234-242
39 Fu W, Yang H, Hari B, Liu S, Li M, Zou G. Preparation and characteristics of core–shell structure cobalt/silica nanoparticles. Mater Chem Phys 2006; 100: 246-250
40 Sato A, Itcho N, Ishiguro H, Okamoto D, Kobayashi N, Kawai K, Kasai H, Kurioka D, Uemura H, Kubota Y, Watanabe M. Magnetic nanoparticles of Fe₃O₄ enhance docetaxel-induced prostate cancer cell death. Int J Nanomedicine 2013; 8: 3151-3160
41 Khorramizadeh MR, Esmail-Nazari Z, Zarei-Ghaane Z, Shakibaie M, Mollazadeh-Moghaddam K, Iranshahi M, Shahverdi AR. Umbelliprenin-coated Fe₃O₄ magnetite nanoparticles: Antiproliferation evaluation on human Fibrosarcoma cell line (HT-1080). Mater Sci Eng C 2010; 30: 1038-1042
42 Yallapu MM, Othman SF, Curtis ET, Bauer NA, Chauhan N, Kumar D, Jaggi M, Chauhan SC. Curcumin-loaded magnetic nanoparticles for breast cancer therapeutics and imaging applications. Int J Nanomedicine 2012; 7: 1761-1779
43 Yallapu MM, Ebeling MC, Khan S, Sundram V, Chauhan N, Gupta BK, Puumala SE, Jaggi M, Chauhan SC. Novel curcumin-loaded magnetic nanoparticles for pancreatic cancer treatment. Mol Cancer Ther 2013; 12: 1471-1480
44 Helmi Rashid Farimani M, Shahtahmassebi N, Rezaee Roknabadi M, Ghows N. Synthesis and study of structural and magnetic properties of superparamagnetic Fe₃O₄@SiO₂ core/shell nanocomposite for biomedical applications. Nanomed J 2013; 1: 71-78

Supplementary Material

Supporting Information