Tumor Biology

, Volume 36, Issue 8, pp 5727–5742 | Cite as

Folate-conjugated nanoparticles as a potent therapeutic approach in targeted cancer therapy

  • Behdokht Bahrami
  • Mousa Mohammadnia-Afrouzi
  • Peyman Bakhshaei
  • Yaghoub Yazdani
  • Ghasem Ghalamfarsa
  • Mehdi Yousefi
  • Sanam Sadreddini
  • Farhad Jadidi-Niaragh
  • Mohammad Hojjat-Farsangi
Review

Abstract

The selective and efficient drug delivery to tumor cells can remarkably improve different cancer therapeutic approaches. There are several nanoparticles (NPs) which can act as a potent drug carrier for cancer therapy. However, the specific drug delivery to cancer cells is an important issue which should be considered before designing new NPs for in vivo application. It has been shown that cancer cells over-express folate receptor (FR) in order to improve their growth. As normal cells express a significantly lower levels of FR compared to tumor cells, it seems that folate molecules can be used as potent targeting moieties in different nanocarrier-based therapeutic approaches. Moreover, there is evidence which implies folate-conjugated NPs can selectively deliver anti-tumor drugs into cancer cells both in vitro and in vivo. In this review, we will discuss about the efficiency of different folate-conjugated NPs in cancer therapy.

Keywords

Folate Folate receptor Nanoparticle Cancer therapy 

Notes

Conflicts of interest

None

References

  1. 1.
    Kazemi T, Younesi V, Jadidi-Niaragh F, Yousefi M. Immunotherapeutic approaches for cancer therapy: an updated review. Artificial Cells, Nanomed Biotechnol. 2015(0):1-11.Google Scholar
  2. 2.
    Hosseini M, Haji-Fatahaliha M, Jadidi-Niaragh F, Majidi J, Yousefi M. The use of nanoparticles as a promising therapeutic approach in cancer immunotherapy. Artif cells, Nanomed Biotechnol. 2015(0):1-11.Google Scholar
  3. 3.
    Murthy SK. Nanoparticles in modern medicine: state of the art and future challenges. Int J Nanomedicine. 2007;2(2):129–41.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Talekar M, Kendall J, Denny W, Garg S. Targeting of nanoparticles in cancer: drug delivery and diagnostics. Anti-Cancer Drugs. 2011;22(10):949–62.PubMedGoogle Scholar
  5. 5.
    Conniot J, Silva JM, Fernandes JG, Silva LC, Gaspar R, Brocchini S et al. Cancer immunotherapy: nanodelivery approaches for immune cell targeting and tracking. Frontiers Chem. 2014;2(105).Google Scholar
  6. 6.
    Parker N, Turk MJ, Westrick E, Lewis JD, Low PS, Leamon CP. Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Anal Biochem. 2005;338(2):284–93.PubMedGoogle Scholar
  7. 7.
    Mansoori GA, Brandenburg KS, Shakeri-Zadeh A. A comparative study of two folate-conjugated gold nanoparticles for cancer nanotechnology applications. Cancers. 2010;2(4):1911–28.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Ye W, Du J, Na R, Song Y, Mei Q, Zhao M. Cellular uptake and antitumor activity of DOX-hyd-PEG-FA nanoparticles. PLoS One. 2014;9(5):e97358.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Xu W, Ling P, Zhang T. Polymeric micelles, a promising drug delivery system to enhance bioavailability of poorly water-soluble drugs. J Drug Del. 2013;2013(340315).Google Scholar
  10. 10.
    Wang J, Yao K, Wang C, Tang C, Jiang X. Synthesis and drug delivery of novel amphiphilic block copolymers containing hydrophobic dehydroabietic moiety. J Mat Chem B. 2013;1(17):2324–32.Google Scholar
  11. 11.
    Khoee S, Kavand A. Preparation, co-assembling and interfacial crosslinking of photocurable and folate-conjugated amphiphilic block copolymers for controlled and targeted drug delivery: smart armored nanocarriers. Eur J Med Chem. 2014;73:18–29.PubMedGoogle Scholar
  12. 12.
    Miyata K, Christie RJ, Kataoka K. Polymeric micelles for nano-scale drug delivery. React Funct Polym. 2011;71(3):227–34.Google Scholar
  13. 13.
    Aliabadi HM, Lavasanifar A. Polymeric micelles for drug delivery. Expert Opin Drug Del. 2006;3(1):139–62.Google Scholar
  14. 14.
    Gao Z-G, Tian L, Hu J, Park I-S, Bae YH. Prevention of metastasis in a 4T1 murine breast cancer model by doxorubicin carried by folate conjugated pH sensitive polymeric micelles. J Control Release. 2011;152(1):84–9.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Rapoport N. Physical stimuli-responsive polymeric micelles for anti-cancer drug delivery. Prog Polym Sci. 2007;32(8):962–90.Google Scholar
  16. 16.
    Zhu J, Zhou Z, Yang C, Kong D, Wan Y, Wang Z. Folate-conjugated amphiphilic star-shaped block copolymers as targeted nanocarriers. J Biomed Mat Res Part A. 2011;97(4):498–508.Google Scholar
  17. 17.
    Hami Z, Amini M, Ghazi-Khansari M, Rezayat SM, Gilani K. Doxorubicin-conjugated PLA-PEG-Folate based polymeric micelle for tumor-targeted delivery: synthesis and in vitro evaluation. DARU J Pharmaceut Sci. 2014;22(1):22–30.Google Scholar
  18. 18.
    Scarano W, Duong HT, Lu H, De Souza PL, Stenzel MH. Folate conjugation to polymeric micelles via boronic acid ester to deliver platinum drugs to ovarian cancer cell lines. Biomacromolecules. 2013;14(4):962–75.PubMedGoogle Scholar
  19. 19.
    Guo X, Shi C, Wang J, Di S, Zhou S. pH-triggered intracellular release from actively targeting polymer micelles. Biomaterials. 2013;34(18):4544–54.PubMedGoogle Scholar
  20. 20.
    Wu W-C, Huang C-M, Liao P-W. Dual-sensitive and folate-conjugated mixed polymeric micelles for controlled and targeted drug delivery. React Funct Polym. 2014;81:82–90.Google Scholar
  21. 21.
    Bae Y, Jang W-D, Nishiyama N, Fukushima S, Kataoka K. Multifunctional polymeric micelles with folate-mediated cancer cell targeting and pH-triggered drug releasing properties for active intracellular drug delivery. Mol BioSyst. 2005;1(3):242–50.PubMedGoogle Scholar
  22. 22.
    Liu S-Q, Wiradharma N, Gao S-J, Tong YW, Yang Y-Y. Bio-functional micelles self-assembled from a folate-conjugated block copolymer for targeted intracellular delivery of anticancer drugs. Biomaterials. 2007;28(7):1423–33.PubMedGoogle Scholar
  23. 23.
    Song N, Ding M, Pan Z, Li J, Zhou L, Tan H, et al. Construction of targeting-clickable and tumor-cleavable polyurethane nanomicelles for multifunctional intracellular drug delivery. Biomacromolecules. 2013;14(12):4407–19.PubMedGoogle Scholar
  24. 24.
    Prabaharan M, Grailer JJ, Steeber DA, Gong S. Thermosensitive micelles based on folate conjugated poly (N-vinylcaprolactam) block-poly (ethylene glycol) for tumor targeted drug delivery. Macromol Biosci. 2009;9(8):744–53.PubMedGoogle Scholar
  25. 25.
    Syu WJ, Yu HP, Hsu CY, Rajan YC, Hsu YH, Chang YC, et al. Improved photodynamic cancer treatment by folate conjugated polymeric micelles in a KB xenografted animal model. Small. 2012;8(13):2060–9.PubMedGoogle Scholar
  26. 26.
    Fanciullino R, Ciccolini J, Milano G. Challenges, expectations and limits for nanoparticles-based therapeutics in cancer: a focus on nano-albumin-bound drugs. Criti Rev Oncol/Hematol. 2013;88(3):504–13.Google Scholar
  27. 27.
    Quinlan GJ, Martin GS, Evans TW. Albumin: biochemical properties and therapeutic potential. Hepatology. 2005;41(6):1211–9.PubMedGoogle Scholar
  28. 28.
    Lindner J, Loibl S, Denkert C, Ataseven B, Fasching P, Pfitzner B, et al. Expression of secreted protein acidic and rich in cysteine (SPARC) in breast cancer and response to neoadjuvant chemotherapy. Ann Oncol. 2014;26(1):95–100.PubMedGoogle Scholar
  29. 29.
    Zhang L, Hou S, Mao S, Wei D, Song X, Lu Y. Uptake of folate-conjugated albumin nanoparticles to the SKOV3 cells. Int J Pharm. 2004;287(1):155–62.PubMedGoogle Scholar
  30. 30.
    Zhao D, Zhao X, Zu Y, Li J, Zhang Y, Jiang R, et al. Preparation, characterization, and in vitro targeted delivery of folate-decorated paclitaxel-loaded bovine serum albumin nanoparticles. Int J Nanomedicine. 2010;20(5):669–77.Google Scholar
  31. 31.
    Hoffman RM, Bouvet M. Nanoparticle albumin-bound-paclitaxel: a limited improvement under the current therapeutic paradigm of pancreatic cancer. Expert Opin Pharmacother. 2015;16(7):943–7.PubMedGoogle Scholar
  32. 32.
    Miele E, Spinelli GP, Miele E, Tomao F, Tomao S. Albumin-bound formulation of paclitaxel (Abraxane® ABI-007) in the treatment of breast cancer. Int J Nanomedicine. 2009;4:99–105.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Ren K, Dusad A, Dong R, Quan L. Albumin as a delivery carrier for rheumatoid arthritis. J Nanomed Nanotechol. 2013;4(4):176.Google Scholar
  34. 34.
    Kratz F, Elsadek B. Clinical impact of serum proteins on drug delivery. J Control Release. 2012;161(2):429–45.PubMedGoogle Scholar
  35. 35.
    Hao H, Ma Q, Huang C, He F, Yao P. Preparation, characterization, and in vivo evaluation of doxorubicin loaded BSA nanoparticles with folic acid modified dextran surface. Int J Pharm. 2013;444(1):77–84.PubMedGoogle Scholar
  36. 36.
    Shen Z, Li Y, Kohama K, Oneill B, Bi J. Improved drug targeting of cancer cells by utilizing actively targetable folic acid-conjugated albumin nanospheres. Pharmacol Res. 2011;63(1):51–8.PubMedGoogle Scholar
  37. 37.
    Su C, Li H, Shi Y, Wang G, Liu L, Zhao L, et al. Carboxymethyl-β-cyclodextrin conjugated nanoparticles facilitate therapy for folate receptor-positive tumor with the mediation of folic acid. Int J Pharm. 2014;474(1):202–11.PubMedGoogle Scholar
  38. 38.
    Liang X, Sun Y, Liu L, Ma X, Hu X, Fan J, et al. Folate-functionalized nanoparticles for controlled ergosta-4, 6, 8 (14), 22-tetraen-3-one delivery. Int J Pharm. 2013;441(1):1–8.PubMedGoogle Scholar
  39. 39.
    Zu Y, Zhang Y, Zhao X, Zhang Q, Liu Y, Jiang R. Optimization of the preparation process of vinblastine sulfate (VBLS)-loaded folateconjugated bovine serum albumin (BSA) nanoparticles for tumor-targeted drug delivery using response surface methodology (RSM). Int J Nanomedicine. 2009;4:321.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Martínez A, Muñiz E, Teijón C, Iglesias I, Teijón J, Blanco M. Targeting tamoxifen to breast cancer xenograft tumours: preclinical efficacy of folate-attached nanoparticles based on alginate-cysteine/disulphide-bond-reduced albumin. Pharm Res. 2014;31(5):1264–74.PubMedGoogle Scholar
  41. 41.
    Yang R, An Y, Miao F, Li M, Liu P, Tang Q. Preparation of folic acid-conjugated, doxorubicin-loaded, magnetic bovine serum albumin nanospheres and their antitumor effects in vitro and in vivo. Int J Nanomedicine. 2014;9:4231–43.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Zhang L, Hou S, Zhang J, Hu W, Wang C. Preparation, characterization, and in vivo evaluation of mitoxantrone-loaded, folate-conjugated albumin nanoparticles. Arch Pharm Res. 2010;33(8):1193–8.PubMedGoogle Scholar
  43. 43.
    Akbarzadeh A, Samiei M, Davaran S. Magnetic nanoparticles: preparation, physical properties, and applications in biomedicine. Nanoscale Res Lett. 2012;7(1):1–13.Google Scholar
  44. 44.
    Jing Y, Dong-Yan H, Yousaf MZ, Yang-Long H, Song G. Magnetic nanoparticle-based cancer therapy. Chin Physics B. 2013;22(2):027506.Google Scholar
  45. 45.
    Wang J, Chen Y, Chen B, Ding J, Xia G, Gao C, et al. Pharmacokinetic parameters and tissue distribution of magnetic Fe3O4 nanoparticles in mice. Int J Nanomedicine. 2010;5:861–6.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Tang Q, An Y, Liu D, Liu P, Zhang D. Folate/NIR 797-conjugated albumin magnetic nanospheres: synthesis, characterisation, and in vitro and in vivo targeting evaluation. PLoS One. 2014;9(9):e106483.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Lu AH, Salabas EL, Schüth F. Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angew Chem Int Ed. 2007;46(8):1222–44.Google Scholar
  48. 48.
    Ito A, Shinkai M, Honda H, Kobayashi T. Medical application of functionalized magnetic nanoparticles. J Biosci Bioeng. 2005;100(1):1–11.PubMedGoogle Scholar
  49. 49.
    Majd MH, Barar J, Asgari D, Valizadeh H, Rashidi MR, Kafil V, et al. Targeted fluoromagnetic nanoparticles for imaging of breast cancer MCF-7 cells. Adv Pharmaceut Bull. 2013;3(1):189–95.Google Scholar
  50. 50.
    Ma X, Gong A, Chen B, Zheng J, Chen T, Shen Z, et al. Exploring a new SPION-based MRI contrast agent with excellent water-dispersibility, high specificity to cancer cells and strong MR imaging efficacy. Colloids Surf B: Biointerfaces. 2014;126:44–9.PubMedGoogle Scholar
  51. 51.
    Li J, Zheng L, Cai H, Sun W, Shen M, Zhang G, et al. Polyethyleneimine-mediated synthesis of folic acid-targeted iron oxide nanoparticles for in vivo tumor MR imaging. Biomaterials. 2013;34(33):8382–92.PubMedGoogle Scholar
  52. 52.
    Shi J, Wang L, Gao J, Liu Y, Zhang J, Ma R, et al. A fullerene-based multi-functional nanoplatform for cancer theranostic applications. Biomaterials. 2014;35(22):5771–84.PubMedGoogle Scholar
  53. 53.
    Wen J, Jiang S, Chen Z, Zhao W, Yi Y, Yang R, et al. Apoptosis selectively induced in BEL-7402 cells by folic acid-modified magnetic nanoparticles combined with 100 Hz magnetic field. Int J Nanomedicine. 2014;9:2043.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Majetich SA. Magnetic nanoparticles for biomedicine. Conf Proc IEEE Eng Med Biol Soc. 2009;2009:4477–8.PubMedGoogle Scholar
  55. 55.
    Varshosaz J, Hassanzadeh F, Sadeghi Aliabadi H, Nayebsadrian M, Banitalebi M, Rostami M. Synthesis and characterization of folate-targeted dextran/retinoic acid micelles for doxorubicin delivery in acute leukemia. BioMed Res Int. 2014;2014.Google Scholar
  56. 56.
    Krais A, Wortmann L, Hermanns L, Feliu N, Vahter M, Stucky S, et al. Targeted uptake of folic acid-functionalized iron oxide nanoparticles by ovarian cancer cells in the presence but not in the absence of serum. Nanomed: Nanotechnol, Biol Med. 2014;10(7):1421–31.Google Scholar
  57. 57.
    Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, et al. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev. 2008;108(6):2064–110.PubMedGoogle Scholar
  58. 58.
    Sahoo B, Devi KSP, Dutta S, Maiti TK, Pramanik P, Dhara D. Biocompatible mesoporous silica-coated superparamagnetic manganese ferrite nanoparticles for targeted drug delivery and MR imaging applications. J Colloid Interface Sci. 2014;431:31–41.PubMedGoogle Scholar
  59. 59.
    Wu W, He Q, Jiang C. Magnetic iron oxide nanoparticles: synthesis and surface functionalization strategies. Nanoscale Res Lett. 2008;3(11):397–415.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Guan Y-Q, Zheng Z, Huang Z, Li Z, Niu S, Liu J-M. Powerful inner/outer controlled multi-target magnetic nanoparticle drug carrier prepared by liquid photo-immobilization. Scientific reports. 2014;4(4990).Google Scholar
  61. 61.
    Badruddoza AZM, Rahman MT, Ghosh S, Hossain MZ, Shi J, Hidajat K, et al. β-Cyclodextrin conjugated magnetic, fluorescent silica core–shell nanoparticles for biomedical applications. Carbohydr Polym. 2013;95(1):449–57.PubMedGoogle Scholar
  62. 62.
    Erdal N, Gürgül S, Tamer L, Ayaz L. Effects of long-term exposure of extremely low frequency magnetic field on oxidative/nitrosative stress in rat liver. J Radiat Res. 2008;49(2):181–7.PubMedGoogle Scholar
  63. 63.
    Qu J, Liu G, Wang Y, Hong R. Preparation of Fe3O4–chitosan nanoparticles used for hyperthermia. Adv Powder Technol. 2010;21(4):461–7.Google Scholar
  64. 64.
    Viota J, Carazo A, Munoz-Gamez J, Rudzka K, Gómez-Sotomayor R, Ruiz-Extremera A, et al. Functionalized magnetic nanoparticles as vehicles for the delivery of the antitumor drug gemcitabine to tumor cells. Physicochemical in vitro evaluation. Mater Sci Eng C. 2013;33(3):1183–92.Google Scholar
  65. 65.
    Lee GY, Qian WP, Wang L, Wang YA, Staley CA, Satpathy M, et al. Theranostic nanoparticles with controlled release of gemcitabine for targeted therapy and MRI of pancreatic cancer. ACS Nano. 2013;7(3):2078–89.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Zhang F, Huang X, Zhu L, Guo N, Niu G, Swierczewska M, et al. Noninvasive monitoring of orthotopic glioblastoma therapy response using RGD-conjugated iron oxide nanoparticles. Biomaterials. 2012;33(21):5414–22.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Hu H, Zhang C, An L, Yu Y, Yang H, Sun J, et al. General protocol for the synthesis of functionalized magnetic nanoparticles for magnetic resonance imaging from protected metal–organic precursors. Chem-A Europ J. 2014;20(23):7160–7.Google Scholar
  68. 68.
    Sivakumar B, Aswathy RG, Sreejith R, Nagaoka Y, Iwai S, Suzuki M, et al. Bacterial exopolysaccharide based magnetic nanoparticles: a versatile nanotool for cancer cell imaging, targeted drug delivery and synergistic effect of drug and hyperthermia mediated cancer therapy. J Biomed Nanotechnol. 2014;10(6):885–99.PubMedGoogle Scholar
  69. 69.
    Fazilati M. Folate decorated magnetite nanoparticles: synthesis and targeted therapy against ovarian cancer. Cell Biol Int. 2014;38(2):154–63.PubMedGoogle Scholar
  70. 70.
    Mehrabi M, Javid A, Hashemi A, Rezaei-Zarchi S. Investigation of the effect of folic acid based iron oxide nanoparticles on human leukemic CCRF-CEM cell line. Iran J Pediatr Hematol Oncol. 2013;3(2):47–53.Google Scholar
  71. 71.
    Gunduz U, Keskin T, Tansık G, Mutlu P, Yalcın S, Unsoy G, et al. Idarubicin-loaded folic acid conjugated magnetic nanoparticles as a targetable drug delivery system for breast cancer. Biomed Pharmacotherapy. 2014;68(6):729–36.Google Scholar
  72. 72.
    An Q, Sun C, Li D, Xu K, Guo J, Wang C. Peroxidase-like activity of Fe3O4@ carbon nanoparticles enhances ascorbic acid-induced oxidative stress and selective damage to PC-3 prostate cancer cells. ACS Appl Mater Interfaces. 2013;5(24):13248–57.PubMedGoogle Scholar
  73. 73.
    Li X, Ding J, Wang X, Wei K, Weng J, Wang J. One-pot synthesis and functionalisation of Fe 2 O 3@ CNH 2 nanoparticles for imaging and therapy. Nanobiotechnol, IET. 2014;8(2):93–101.Google Scholar
  74. 74.
    Tang Z, Li D, Sun H, Guo X, Chen Y, Zhou S. Quantitative control of active targeting of nanocarriers to tumor cells through optimization of folate ligand density. Biomaterials. 2014;35(27):8015–27.PubMedGoogle Scholar
  75. 75.
    Mikhaylova M, Kim DK, Bobrysheva N, Osmolowsky M, Semenov V, Tsakalakos T, et al. Superparamagnetism of magnetite nanoparticles: dependence on surface modification. Langmuir. 2004;20(6):2472–7.PubMedGoogle Scholar
  76. 76.
    Kim J, Park S, Lee JE, Jin SM, Lee JH, Lee IS, et al. Designed fabrication of multifunctional magnetic gold nanoshells and their application to magnetic resonance imaging and photothermal therapy. Angew Chem. 2006;118(46):7918–22.Google Scholar
  77. 77.
    Wu W, Chen B, Cheng J, Wang J, Xu W, Liu L, et al. Biocompatibility of Fe3O4/DNR magnetic nanoparticles in the treatment of hematologic malignancies. Int J Nanomedicine. 2010;5:1079.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Hervault A, Thanh NTK. Magnetic nanoparticle-based therapeutic agents for thermo-chemotherapy treatment of cancer. Nanoscale. 2014;6(20):11553–73.PubMedGoogle Scholar
  79. 79.
    Sivakumar Balasubramanian ARG, Nagaoka Y, Iwai S, Suzuki M, Kizhikkilot V, Yoshida Y, et al. Curcumin and 5-Fluorouracil-loaded, folate-and transferrin-decorated polymeric magnetic nanoformulation: a synergistic cancer therapeutic approach, accelerated by magnetic hyperthermia. Int J Nanomedicine. 2014;9:437–59.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Chen B, Cheng J, Wu Y, Gao F, Xu W, Shen H, et al. Reversal of multidrug resistance by magnetic Fe3O4 nanoparticle copolymerizating daunorubicin and 5-bromotetrandrine in xenograft nude-mice. Int J Nanomedicine. 2009;4:73–8.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Chen B, Cheng J, Shen M, Gao F, Xu W, Shen H, et al. Magnetic nanoparticle of Fe3O4 and 5-bromotetrandrin interact synergistically to induce apoptosis by daunorubicin in leukemia cells. Int J Nanomedicine. 2009;4:65–71.PubMedPubMedCentralGoogle Scholar
  82. 82.
    Goya G, Grazu V, Ibarra M. Magnetic nanoparticles for cancer therapy. Curr Nanosci. 2008;4(1):1–16.Google Scholar
  83. 83.
    Safarik I, Safarikova M. Magnetically responsive nanocomposite materials for bioapplications. Solid State Phenom. 2009;151:88–94.Google Scholar
  84. 84.
    Jeong U, Teng X, Wang Y, Yang H, Xia Y. Superparamagnetic colloids: controlled synthesis and niche applications. Adv Mater. 2007;19(1):33–60.Google Scholar
  85. 85.
    Tang Q, Chen D. Study of the therapeutic effect of 188Re labeled folate targeting albumin nanoparticle coupled with cis-diamminedichloroplatinum cisplatin on human ovarian cancer. Bio-Med Mat Eng. 2014;24(1):711–22.Google Scholar
  86. 86.
    Yoo H, Moon S-K, Hwang T, Kim YS, Kim J-H, Choi S-W, et al. Multifunctional magnetic nanoparticles modified with polyethylenimine and folic acid for biomedical theranostics. Langmuir. 2013;29(20):5962–7.PubMedGoogle Scholar
  87. 87.
    Varshosaz J, Sadeghi-Aliabadi H, Ghasemi S, Behdadfar B. Use of magnetic folate-dextran-retinoic acid micelles for dual targeting of doxorubicin in breast cancer. BioMed Res Int. 2013;2013:680712.PubMedPubMedCentralGoogle Scholar
  88. 88.
    Yang H-W, Hua M-Y, Liu H-L, Huang C-Y, Wei K-C. Potential of magnetic nanoparticles for targeted drug delivery. Nanotechnol Sci Appl. 2012;5:73–86.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Franckena M, Wit RD, Ansink AC, Notenboom A, Canters RA, Fatehi D, et al. Weekly systemic cisplatin plus locoregional hyperthermia: an effective treatment for patients with recurrent cervical carcinoma in a previously irradiated area. Int J Hyperth. 2007;23(5):443–50.Google Scholar
  90. 90.
    Chen ZQ, Wen J, Tu WY, Xiao L, Fang Z. A study on early apoptosis of hepatoma Bel-7402 cells in vitro treated by altering-electric magnetic field exposure of extremely low frequency combined with magnetic nano-Fe3O4 powders. Appl Mech Mat. 2013;364:742–8.Google Scholar
  91. 91.
    Klichko Y, Liong M, Choi E, Angelos S, Nel AE, Stoddart JF, et al. Mesostructured silica for optical functionality, nanomachines, and drug delivery. J Am Ceram Soc. 2009;92(s1):S2–S10.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Slowing II, Vivero-Escoto JL, Wu C-W, Lin VS-Y. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv Drug Deliv Rev. 2008;60(11):1278–88.PubMedGoogle Scholar
  93. 93.
    Liong M, Lu J, Kovochich M, Xia T, Ruehm SG, Nel AE, et al. Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano. 2008;2(5):889–96.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Trewyn BG, Slowing II, Giri S, Chen H-T, Lin VS-Y. Synthesis and functionalization of a mesoporous silica nanoparticle based on the sol–gel process and applications in controlled release. Acc Chem Res. 2007;40(9):846–53.PubMedGoogle Scholar
  95. 95.
    Safari J, Zarnegar Z. Advanced drug delivery systems: nanotechnology of health design a review. J Saudi Chem Soc. 2014;18(2):85–99.Google Scholar
  96. 96.
    Kwon S, Singh RK, Perez RA, Neel EAA, Kim H-W, Chrzanowski W. Silica-based mesoporous nanoparticles for controlled drug delivery. J Tiss Eng. 2013;4:2041731413503357.Google Scholar
  97. 97.
    Wang S. Ordered mesoporous materials for drug delivery. Microporous Mesoporous Mater. 2009;117(1):1–9.Google Scholar
  98. 98.
    Halamová D, Zeleňák V. NSAID naproxen in mesoporous matrix MCM-41: drug uptake and release properties. J Incl Phenom Macrocycl Chem. 2012;72(1-2):15–23.Google Scholar
  99. 99.
    Ma X, Zhao Y, Ng KW, Zhao Y. Integrated hollow mesoporous silica nanoparticles for target drug/siRNA co-delivery. Chem-A Europ J. 2013;19(46):15593–603.Google Scholar
  100. 100.
    Fan J, Fang G, Wang X, Zeng F, Xiang Y, Wu S. Targeted anticancer prodrug with mesoporous silica nanoparticles as vehicles. Nanotechnology. 2011;22(45):455102.PubMedGoogle Scholar
  101. 101.
    Mohapatra S, Rout SR, Narayan R, Maiti TK. Multifunctional mesoporous hollow silica nanocapsules for targeted co-delivery of cisplatin-pemetrexed and MR imaging. Dalton Trans. 2014;43(42):15841–50.PubMedGoogle Scholar
  102. 102.
    Luo Z, Ding X, Hu Y, Wu S, Xiang Y, Zeng Y, et al. Engineering a hollow nanocontainer platform with multifunctional molecular machines for tumor-targeted therapy in vitro and in vivo. ACS Nano. 2013;7(11):10271–84.PubMedGoogle Scholar
  103. 103.
    Teng I, Chang Y-J, Wang L-S, Lu H-Y, Wu L-C, Yang C-M, et al. Phospholipid-functionalized mesoporous silica nanocarriers for selective photodynamic therapy of cancer. Biomaterials. 2013;34(30):7462–70.PubMedGoogle Scholar
  104. 104.
    Jain S, Hirst D, O’sullivan J. Gold nanoparticles as novel agents for cancer therapy. Br J Radiol. 2014;85(1010):101–13.Google Scholar
  105. 105.
    Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006;311(5761):622–7.PubMedGoogle Scholar
  106. 106.
    Lal S, Clare SE, Halas NJ. Nanoshell-enabled photothermal cancer therapy: impending clinical impact. Acc Chem Res. 2008;41(12):1842–51.PubMedGoogle Scholar
  107. 107.
    Niidome T, Yamagata M, Okamoto Y, Akiyama Y, Takahashi H, Kawano T, et al. PEG-modified gold nanorods with a stealth character for in vivo applications. J Control Release. 2006;114(3):343–7.PubMedGoogle Scholar
  108. 108.
    Llevot A, Astruc D. Applications of vectorized gold nanoparticles to the diagnosis and therapy of cancer. Chem Soc Rev. 2012;41(1):242–57.PubMedGoogle Scholar
  109. 109.
    Kim D, Jeong YY, Jon S. A drug-loaded aptamer-gold nanoparticle bioconjugate for combined CT imaging and therapy of prostate cancer. ACS Nano. 2010;4(7):3689–96.PubMedGoogle Scholar
  110. 110.
    Lin J, Zhou Z, Li Z, Zhang C, Wang X, Wang K, et al. Biomimetic one-pot synthesis of gold nanoclusters/nanoparticles for targeted tumor cellular dual-modality imaging. Nanoscale Res Lett. 2013;8(1):1–7.Google Scholar
  111. 111.
    Brown SD, Nativo P, Smith J-A, Stirling D, Edwards PR, Venugopal B, et al. Gold nanoparticles for the improved anticancer drug delivery of the active component of oxaliplatin. J Am Chem Soc. 2010;132(13):4678–84.PubMedPubMedCentralGoogle Scholar
  112. 112.
    Jain PK, Huang W, El-Sayed MA. On the universal scaling behavior of the distance decay of plasmon coupling in metal nanoparticle pairs: a plasmon ruler equation. Nano Lett. 2007;7(7):2080–8.Google Scholar
  113. 113.
    Park JH, von Maltzahn G, Ruoslahti E, Bhatia SN, Sailor MJ. Micellar hybrid nanoparticles for simultaneous magnetofluorescent imaging and drug delivery. Angew Chem. 2008;120(38):7394–8.Google Scholar
  114. 114.
    Sezgin E, Karatas ÖF, Çam D, Sur İ, Sayin İ, Avci E, et al. Interaction of gold nanoparticles with living cells. Sigma. 2008;26:227–46.Google Scholar
  115. 115.
    Chithrani BD, Ghazani AA, Chan WC. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006;6(4):662–8.PubMedGoogle Scholar
  116. 116.
    De Jong WH, Hagens WI, Krystek P, Burger MC, Sips AJ, Geertsma RE. Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials. 2008;29(12):1912–9.PubMedGoogle Scholar
  117. 117.
    Semmler‐Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A, Takenaka S, et al. Biodistribution of 1.4 and 18 nm gold particles in rats. Small. 2008;4(12):2108–11.PubMedGoogle Scholar
  118. 118.
    Pandey S, Mewada A, Thakur M, Shah R, Oza G, Sharon M. Biogenic gold nanoparticles as fotillas to fire berberine hydrochloride using folic acid as molecular road map. Mater Sci Eng C. 2013;33(7):3716–22.Google Scholar
  119. 119.
    Park J, Jeon WI, Lee SY, Ock KS, Seo JH, Park J, et al. Confocal Raman microspectroscopic study of folate receptor targeted delivery of 6 mercaptopurine embedded gold nanoparticles in a single cell. J Biomed Mat Res Part A. 2012;100(5):1221–8.Google Scholar
  120. 120.
    Ganeshkumar M, Ponrasu T, Raja MD, Subamekala MK, Suguna L. Green synthesis of pullulan stabilized gold nanoparticles for cancer targeted drug delivery. Spectrochim Acta A Mol Biomol Spectrosc. 2014;130:64–71.PubMedGoogle Scholar
  121. 121.
    Zhu J, Zheng L, Wen S, Tang Y, Shen M, Zhang G, et al. Targeted cancer theranostics using alpha-tocopheryl succinate-conjugated multifunctional dendrimer-entrapped gold nanoparticles. Biomaterials. 2014;35(26):7635–46.PubMedGoogle Scholar
  122. 122.
    Kattumuri V, Katti K, Bhaskaran S, Boote EJ, Casteel SW, Fent GM, et al. Gum arabic as a phytochemical construct for the stabilization of gold nanoparticles: in vivo pharmacokinetics and x-ray contrast imaging studies. Small. 2007;3(2):333–41.PubMedGoogle Scholar
  123. 123.
    Fent GM, Casteel SW, Kim DY, Kannan R, Katti K, Chanda N, et al. Biodistribution of maltose and gum arabic hybrid gold nanoparticles after intravenous injection in juvenile swine. Nanomed: Nanotechnol, Biol Med. 2009;5(2):128–35.Google Scholar
  124. 124.
    Triulzi RC, Dai Q, Zou J, Leblanc RM, Gu Q, Orbulescu J, et al. Photothermal ablation of amyloid aggregates by gold nanoparticles. Colloids Surf B: Biointerfaces. 2008;63(2):200–8.PubMedGoogle Scholar
  125. 125.
    Jain PK, El-Sayed IH, El-Sayed MA. Au nanoparticles target cancer. Nano Today. 2007;2(1):18–29.Google Scholar
  126. 126.
    Mehdizadeh A, Pandesh S, Shakeri-Zadeh A, Kamrava SK, Habib-Agahi M, Farhadi M, et al. The effects of folate-conjugated gold nanorods in combination with plasmonic photothermal therapy on mouth epidermal carcinoma cells. Lasers Med Sci. 2014;29(3):939–48.PubMedGoogle Scholar
  127. 127.
    Hu D, Sheng Z, Fang S, Wang Y, Gao D, Zhang P, et al. Folate receptor-targeting gold nanoclusters as fluorescence enzyme mimetic nanoprobes for tumor molecular colocalization diagnosis. Theranostics. 2014;4(2):142.PubMedPubMedCentralGoogle Scholar
  128. 128.
    Xu S, Liu J, Wang T, Li H, Miao Y, Liu Y, et al. A simple and rapid electrochemical strategy for non-invasive, sensitive and specific detection of cancerous cell. Talanta. 2013;104:122–7.PubMedGoogle Scholar
  129. 129.
    Bharali DJ, Khalil M, Gurbuz M, Simone TM, Mousa SA. Nanoparticles and cancer therapy: a concise review with emphasis on dendrimers. Int J Nanomedicine. 2009;4:1–7.PubMedPubMedCentralGoogle Scholar
  130. 130.
    Eichman JD, Bielinska AU, Kukowska-Latallo JF, Baker Jr JR. The use of PAMAM dendrimers in the efficient transfer of genetic material into cells. Pharmaceut Sci Technol. 2000;3(7):232–45.Google Scholar
  131. 131.
    Gillies ER, Frechet JM. Dendrimers and dendritic polymers in drug delivery. Drug Discov Today. 2005;10(1):35–43.PubMedGoogle Scholar
  132. 132.
    Hong S, Leroueil PR, Majoros IJ, Orr BG, Baker Jr JR, Banaszak Holl MM. The binding avidity of a nanoparticle-based multivalent targeted drug delivery platform. Chem Biol. 2007;14(1):107–15.PubMedGoogle Scholar
  133. 133.
    Myc A, Douce TB, Ahuja N, Kotlyar A, Kukowska-Latallo J, Thomas TP, et al. Preclinical antitumor efficacy evaluation of dendrimer-based methotrexate conjugates. Anti-Cancer Drugs. 2008;19(2):143–9.PubMedGoogle Scholar
  134. 134.
    Kesharwani P, Tekade RK, Jain NK. Generation dependent safety and efficacy of folic acid conjugated dendrimer based anticancer drug formulations. Pharm Res. 2014;32(4):1438–50.PubMedGoogle Scholar
  135. 135.
    Birdhariya B, Kesharwani P, Jain NK. Effect of surface capping on targeting potential of folate decorated poly (propylene imine) dendrimers. Drug Dev Indust Pharma. 2014(0):1-7.Google Scholar
  136. 136.
    Wong PT, Tang K, Coulter A, Tang S, Baker Jr JR, Choi SK. Multivalent dendrimer vectors with DNA intercalation motifs for gene delivery. Biomacromolecules. 2014;15(11):4134–45.PubMedGoogle Scholar
  137. 137.
    Arima H, Arizono M, Higashi T, Yoshimatsu A, Ikeda H, Motoyama K, et al. Potential use of folate-polyethylene glycol (PEG)-appended dendrimer (G3) conjugate with α-cyclodextrin as DNA carriers to tumor cells. Cancer Gene Ther. 2012;19(5):358–66.PubMedGoogle Scholar
  138. 138.
    Wang M, Hu H, Sun Y, Qiu L, Zhang J, Guan G, et al. A pH-sensitive gene delivery system based on folic acid-PEG-chitosan–PAMAM-plasmid DNA complexes for cancer cell targeting. Biomaterials. 2013;34(38):10120–32.PubMedGoogle Scholar
  139. 139.
    Sunoqrot S, Bugno J, Lantvit D, Burdette JE, Hong S. Prolonged blood circulation and enhanced tumor accumulation of folate-targeted dendrimer-polymer hybrid nanoparticles. J Control Release. 2014;191:115–22.PubMedPubMedCentralGoogle Scholar
  140. 140.
    Liu W, Sun S, Cao Z, Zhang X, Yao K, Lu WW, et al. An investigation on the physicochemical properties of chitosan/DNA polyelectrolyte complexes. Biomaterials. 2005;26(15):2705–11.PubMedGoogle Scholar
  141. 141.
    Sadigh-Eteghad S, Talebi M, Farhoudi M, Mahmoudi J, Reyhani B. Effects of Levodopa loaded chitosan nanoparticles on cell viability and caspase-3 expression in PC12 neural like cells. Neurosciences. 2013;18(3):281–3.PubMedGoogle Scholar
  142. 142.
    Bowman K, Leong KW. Chitosan nanoparticles for oral drug and gene delivery. Int J Nanomedicine. 2006;1(2):117–28.PubMedPubMedCentralGoogle Scholar
  143. 143.
    Xu Q, Wang C-H, Pack DW. Polymeric carriers for gene delivery: chitosan and poly (amidoamine) dendrimers. Curr Pharm Des. 2010;16(21):2350.PubMedPubMedCentralGoogle Scholar
  144. 144.
    Song H, Su C, Cui W, Zhu B, Liu L, Chen Z, et al. Folic acid-chitosan conjugated nanoparticles for improving tumor-targeted drug delivery. BioMed Res Int. 2013;2013.Google Scholar
  145. 145.
    Pramanik A, Laha D, Pramanik P, Karmakar P. A novel drug “copper acetylacetonate” loaded in folic acid-tagged chitosan nanoparticle for efficient cancer cell targeting. J Drug Target. 2013;22(1):23–33.PubMedGoogle Scholar
  146. 146.
    Zhou J, Wang J, Xu Q, Xu S, Wen J, Yu Z, et al. Folate-chitosan-gemcitabine core-shell nanoparticles targeted to pancreatic cancer. Chin J Cancer Res. 2013;25(5):527.PubMedPubMedCentralGoogle Scholar
  147. 147.
    Zheng Y, Cai Z, Song X, Yu B, Bi Y, Chen Q, et al. Receptor mediated gene delivery by folate conjugated N-trimethyl chitosan in vitro. Int J Pharm. 2009;382(1):262–9.PubMedGoogle Scholar
  148. 148.
    Lee KD, Choi S-H, Kim DH, Lee H-Y, Choi K-C. Self-organized nanoparticles based on chitosan-folic acid and dextran succinate-doxorubicin conjugates for drug targeting. Arch Pharmacal Res. 2014:1-8.Google Scholar
  149. 149.
    Gaspar VM, Costa EC, Queiroz JA, Pichon C, Sousa F, Correia IJ. Folate-targeted multifunctional amino acid-chitosan nanoparticles for improved cancer therapy. Pharm Res. 2014;1–16.Google Scholar
  150. 150.
    Jia M, Li Y, Yang X, Huang Y, Wu H, Huang Y, et al. Development of both methotrexate and mitomycin C loaded pegylated chitosan nanoparticles for targeted drug codelivery and synergistic anticancer effect. ACS Appl Mater Interfaces. 2014;6(14):11413–23.PubMedGoogle Scholar
  151. 151.
    Shi Z, Guo R, Li W, Zhang Y, Xue W, Tang Y, et al. Nanoparticles of deoxycholic acid, polyethylene glycol and folic acid-modified chitosan for targeted delivery of doxorubicin. J Mater Sci Mater Med. 2014;25(3):723–31.PubMedGoogle Scholar
  152. 152.
    Li TSC, Yawata T, Honke K. Efficient siRNA delivery and tumor accumulation mediated by ionically cross-linked folic acid–poly (ethylene glycol)–chitosan oligosaccharide lactate nanoparticles: for the potential targeted ovarian cancer gene therapy. Eur J Pharm Sci. 2014;52:48–61.PubMedGoogle Scholar
  153. 153.
    Allen TM, Brandeis E, Hansen CB, Kao GY, Zalipsky S. A new strategy for attachment of antibodies to sterically stabilized liposomes resulting in efficient targeting to cancer cells. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1995;123(2):99–108.Google Scholar
  154. 154.
    Liu Y, Li K, Pan J, Liu B, Feng S-S. Folic acid conjugated nanoparticles of mixed lipid monolayer shell and biodegradable polymer core for targeted delivery of Docetaxel. Biomaterials. 2010;31(2):330–8.PubMedGoogle Scholar
  155. 155.
    Cho K, Wang X, Nie S, Shin DM. Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res. 2008;14(5):1310–6.PubMedGoogle Scholar
  156. 156.
    Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov. 2005;4(2):145–60.PubMedGoogle Scholar
  157. 157.
    Tong R, Cheng J. Anticancer polymeric nanomedicines. J Macromol Sci Polym Rev. 2007;47(3):345–81.Google Scholar
  158. 158.
    S-s F, Huang G. Effects of emulsifiers on the controlled release of paclitaxel (Taxol®) from nanospheres of biodegradable polymers. J Control Release. 2001;71(1):53–69.Google Scholar
  159. 159.
    Wang X, Yang L, Chen ZG, Shin DM. Application of nanotechnology in cancer therapy and imaging. CA: Cancer J Clin. 2008;58(2):97–110.Google Scholar
  160. 160.
    Campbell IG, Jones TA, Foulkes WD, Trowsdale J. Folate-binding protein is a marker for ovarian cancer. Cancer Res. 1991;51(19):5329–38.PubMedGoogle Scholar
  161. 161.
    Zhang Z, Jia J, Lai Y, Ma Y, Weng J, Sun L. Conjugating folic acid to gold nanoparticles through glutathione for targeting and detecting cancer cells. Bioorg Med Chem. 2010;18(15):5528–34.PubMedGoogle Scholar
  162. 162.
    Ai J, Xu Y, Li D, Liu Z, Wang E. Folic acid as delivery vehicles: targeting folate conjugated fluorescent nanoparticles to tumors imaging. Talanta. 2012;101:32–7.PubMedGoogle Scholar
  163. 163.
    Zhu Y, Cheng L, Cheng L, Huang F, Hu Q, Li L, et al. Folate and TAT peptide co-modified liposomes exhibit receptor-dependent highly efficient intracellular transport of payload in vitro and in vivo. Pharm Res. 2014;31(12):3289–303.PubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2015

Authors and Affiliations

  • Behdokht Bahrami
    • 1
  • Mousa Mohammadnia-Afrouzi
    • 2
  • Peyman Bakhshaei
    • 3
  • Yaghoub Yazdani
    • 4
  • Ghasem Ghalamfarsa
    • 5
  • Mehdi Yousefi
    • 6
    • 7
  • Sanam Sadreddini
    • 6
  • Farhad Jadidi-Niaragh
    • 3
  • Mohammad Hojjat-Farsangi
    • 8
    • 9
  1. 1.Department of Immunology, School of MedicineShiraz University of Medical SciencesShirazIran
  2. 2.Department of Immunology and Microbiology, School of MedicineBabol University of Medical SciencesBabolIran
  3. 3.Department of Immunology, School of Public HealthTehran University of Medical SciencesTehranIran
  4. 4.Infectious Diseases Research Center and Laboratory Science Research CenterGolestan University of Medical SciencesGorganIran
  5. 5.Cellular and Molecular Research CenterYasuj University of Medical SciencesYasujIran
  6. 6.Immunology Research CenterTabriz University of Medical SciencesTabrizIran
  7. 7.Department of Immunology, Faculty of MedicineTabriz University of Medical SciencesTabrizIran
  8. 8.Department of Oncology-Pathology, Immune and Gene Therapy Lab, Cancer Center Karolinska (CCK)Karolinska University Hospital Solna and Karolinska InstituteStockholmSweden
  9. 9.Department of Immunology, School of MedicineBushehr University of Medical SciencesBushehrIran

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