Nanomedicine: Nanotechnology, Biology and Medicine
Volume 3, Issue 3 , Pages 224-238 , September 2007

Attaching folic acid on gold nanoparticles using noncovalent interaction via different polyethylene glycol backbones and targeting of cancer cells

  • Resham Bhattacharya, MS, PhD

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Both the authors contributed equally to this work.
    • ,
  • Chitta Ranjan Patra, MS, PhD

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Both the authors contributed equally to this work.
    • ,
  • Alexis Earl

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Shanfeng Wang, MS, PhD

      Affiliations

    • Department of Orthopedic Surgery, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Department of Biomedical Engineering, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Aaron Katarya

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Lichun Lu, BEng, PhD

      Affiliations

    • Department of Orthopedic Surgery, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Department of Biomedical Engineering, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Jayachandran N. Kizhakkedathu, MS, PhD

      Affiliations

    • Department of Pathology and Laboratory Medicine, Centre for Blood Research, University of British Columbia, Vancouver, BC, Canada
    • ,
  • Michael J. Yaszemski, MD, PhD

      Affiliations

    • Department of Orthopedic Surgery, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Department of Biomedical Engineering, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Philip R. Greipp, BS, MD

      Affiliations

    • Division of Hematology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Debabrata Mukhopadhyay, MS, PhD

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Department of Biomedical Engineering, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • ,
  • Priyabrata Mukherjee, MS, PhD

      Affiliations

    • Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Department of Biomedical Engineering, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    • Corresponding Author InformationCorresponding author. Department of Biomedical Engineering and Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Mayo Clinic, Rochester, MN 55905, USA.

Received 29 March 2007 ,Accepted 10 July 2007.

References 

  1. Langer R. Drug delivery and targeting. Nature. 1998;392:5–10
  2. Duncan R. The dawning era of polymer therapeutics. Nat Rev Drug Discov. 2003;2:347–360
  3. Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Cancer Rev. 2005;5:161–171
  4. Zahr AS, de Villiers M, Pishko MV. Encapsulation of drug nanoparticles in self-assembled macromolecular nanoshells. Langmuir. 2005;21:403–410
  5. Kamen BA, Capdevila A. Receptor-mediated folate accumulation is regulated by the cellular folate content. Proc Natl Acad Sci U S A. 1986;83:5983–5987
  6. Mattes MJ, Major PP, Goldenberg DM, Dion AS, Hutter RV, Klein KM. Patterns of antigen distribution in human carcinomas. Cancer Res. 1990;50:880s–884s
  7. Coney LR, Tomassetti A, Carayannopoulos L, Frasca V, Kamen BA, Colnaghi M, et al. Cloning of a tumor-associated antigen: MOv18 and MOv19 antibodies recognize a folate-binding protein. Cancer Res. 1991;51:6125–6132
  8. Weitman SD, Lark RH, Coney LR, Fort DW, Frasca V, Zurawski VR, et al. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res. 1992;52:3396–3401
  9. Ross JF, Chaudhuri PK, Ratnam M. Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines. Physiologic and clinical implications. Cancer. 1994;73:2432–2443
  10. Weitman SD, Frazier KM, Kamen BA. The folate receptor in central nervous system malignancies of childhood. J Neurooncol. 1994;21:107–112
  11. Garin-Chesa P, Campbell I, Saigo PE, Lewis JL, Old LJ, Rettig WJ, et al. Trophoblast and ovarian cancer antigen LK26. Sensitivity and specificity in immunopathology and molecular identification as a folate-binding protein. J Am J Pathol. 1993;142:557–567
  12. Toffoli G, Cernigoi C, Russo A, Gallo A, Bagnoli M, Boiocchi M. Overexpression of folate binding protein in ovarian cancers. Int J Cancer. 1997;74:193–198
  13. Holm J, Hansen SI, Hoier-Madsen M, Bostad L. High-affinity folate binding in human choroid plexus. Characterization of radioligand binding, immunoreactivity, molecular heterogeneity and hydrophobic domain of the binding protein. J. Biochem. 1991;280:267–271
  14. Shen F, Ross JF, Wang X, Ratnam M. Identification of a novel folate receptor, a truncated receptor, and receptor type p in hematopoietic cells: cDNA cloning, expression, immunoreactivity, and tissue specificity. Biochemistry. 1994;33:1209–1215
  15. Sadasivan E, Rothenberg SP, da Costa M, Brink L. Characterization of multiple forms of folate-binding protein from human leukemia cells. Biochim Biophys Acta. 1986;882:311–321
  16. Sadasivan E, Rothenberg SP, da Costa M, Brink L. Purification, properties, and immunological characterization of folate-binding proteins from human leukemia cells. Biochim Biophys Acta. 1987;925:36–47
  17. Morikawa J, Li H, Kim S, Nishi K, Ueno S, Suh E, et al. Identification of signature genes by microarray for acute myeloid leukemia without maturation and acute promyelocytic leukemia with t(15;17)(q22;q12)(PML/RAR). Int J Oncol. 2003;23:617–625
  18. Kennedy MD, Jallad KN, Lu J, Low PS, Ben-Amotz D. Evaluation of folate conjugate uptake and transport by the choroid plexus of mice. Pharm Res. 2003;20:714–719
  19. Patrick TA, Kranz DM, van Dyke TA, Roy EJ. Folate receptors as potential therapeutic targets in choroid plexus tumors of SV40 transgenic mice. J Neurooncol. 1997;32:111–123
  20. Daniel MC, Astruc D. Gold nanoparticles: assembly, supramolecular chemistry, quantum-size related properties, and applications toward biology, catalysis, and nanotechnology. Chem Rev. 2004;104:293–346
  21. Antony AC. The biological chemistry of folate receptors. Blood. 1992;79:2807–2820
  22. Sabharanjak S, Mayor S. Folate receptor endocytosis and trafficking. Adv Drug Deliv Rev. 2004;56:1099–1109
  23. Kamen BA, Smith AK. A review of folate receptor alpha cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv Drug Deliv Rev. 2004;56:1085–1097
  24. Huang X, El-Sayed IH, Quan W, El-Sayed MA. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J Am Chem Soc. 2006;128:2115–2120
  25. Hainfeld JF, Slatkin DN, Focella TM, Smilowitz MH. Gold nanoparticles: a new X-ray contrast agent. Br J Radiol. 2006;79:248–253
  26. Hirsch LR, Stafford RJ, Bankson JA, Sershen SR, Rivera B, Price RE, et al. Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance. Proc Natl Acad Sci U S A. 2003;100:13549–13554
  27. Mukherjee P, Bhattacharya R, Wang P, Wang L, Basu S, Nagy JA, et al. Antiangiogenic properties of gold nanoparticles. Clin Cancer Res. 2005;11:3530–3534
  28. Chang-Cheng Y, Verma Y, Rotello VM. Engineering the nanoparticle-biomacromolecule interface. Soft Mater. 2006;2:190–204
  29. Higby GJ. Gold in medicine: a review of its use in the West before 1900. Gold Bull. 1982;15:130–140
  30. Richards DG, McMillin DL, Mein EA, Nelson CD. Gold and its relationship to neurological/glandular conditions. Int J Neurosci. 2003;112:31–53
  31. Mahdihassan S. Tan, cinnabar, as drug of longevity prior to alchemy. Am J Chin Med. 1984;12:50–54
  32. Mahdihassan S. Cinnabar-gold as the best alchemical drug of longevity, called Makaradhwaja in India. Am J Chin Med. 1985;13:93–108
  33. Fricker SP. Medicinal uses of gold compounds: past, present and future. Gold Bull. 1996;29:53–59
  34. Koch R. Über bacteriologische Forschung: Tenth International Medical Congress. Dtsch Med Wochenschr. 1890;16:756–757
  35. Shaw CF. Gold-based therapeutic agents. Chem Rev. 1999;99:2589–2600
  36. Connor EE, Mwamuka J, Gole A, Murphy CJ, Wyatt MD. Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small. 2005;1:325–327
  37. Thomas M, Klibanov AM. Conjugation to gold nanoparticles enhances polyethylenimines transfer of plasmid DNA into mammalian cells. Proc Natl Acad Sci. U S A. 2003;100:9138–9143
  38. El-Sayed IH, Huang XH, El-Sayed MA. Surface plasmon resonance scattering and absorption of anti-EGFR antibody conjugated gold nanoparticles in cancer diagnostics: applications in oral cancer. Nano Lett. 2005;5:829–834
  39. Goodman CM, McCusker CD, Yilmaz T, Rotello VM. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjug Chem. 2004;15:897–900
  40. Bhattacharya R, Mukherjee P, Xiong Z, Atala A, Soker S, Mukhopadhyay D. Gold nanoparticles inhibit VEGF165-induced proliferation of HUVEC cells. Nano Lett. 2004;4:2479–2481
  41. Esther R, Bhattacharya R, Ruan M, Bolander ME, Mukhopadhyay D, Sarkar G, et al. Gold nanoparticles do not affect the global transcriptional program of human umbilical vein endothelial cells: a DNA microarray analysis. J Biomed Nanotechnol. 2005;3:328–335
  42. Templeton AC, Wuelfing WP, Murray RW. Monolayer-protected cluster molecules. Acc Chem Res. 2000;33:27–36
  43. Boal AK, Rotello VM. Fabrication and self-optimization of multivalent receptors on nanoparticle scaffolds. J Am Chem Soc. 2000;122:734–735
  44. Srivastava S, Verma A, Frankamp BL, Rotello VM. Controlled assembly of protein nanoparticle composites through protein surface recognition. Adv Mater. 2005;17:617–621
  45. Fischer NO, McIntosh CM, Simrad JM, Rotello VM. Inhibition of chymotrypsin through surface binding using nanoparticle-based receptors. Proc Natl Acad Sci U S A. 2002;16:5018–5023
  46. Levy Y, Onuchic JN. Mechanisms of protein assembly: lessons from minimalist models. Acc Chem Res. 2006;39:135–142
  47. Takahashi T. Significant role of electrostatic interactions for stabilization of protein assemblies. Adv Biophys. 1997;34:41–54
  48. Martin B, Sainlos M, Aissaoui A, Oudrhiri N, Hauchecorne M, Vigneron JP, et al. The design of cationic lipids for gene delivery. Curr Pharm Des. 2005;11:375–394
  49. Sastry M, Rao M, Ganesh KN. Electrostatic assembly of nanoparticles and biomacromolecules. Acc Chem Res. 2002;35:847–855
  50. Lehn JM. Supramolecular chemistry—scope and perspectives molecules, supermolecules, and molecular devices. (Nobel Lecture) Angew Chem Int Ed Engl. 1988;27:89–112
  51. Lehn JM. Perspectives in supramolecular chemistry—from molecular recognition towards molecular information processing and self-organization. Angew Chem Int Ed Engl. 1990;29:1304–1319
  52. In:  Lehn JM,  Atwood JL,  Davies JED,  MacNicol DD,  Vogtle F editor. Comprehensive Supramolecular Chemistry. Oxford: Pergamon; 1996;
  53. Klaus DM, Pavel H. Noncovalent interactions: a challenge for experiment and theory. Chem Rev. 2000;100:143–168
  54. Dixit V, Bossche JV, Sherman DM, Thompson DH, Andres RP. Synthesis and grafting of thioctic acid-PEG-folate conjugates onto Au nanoparticles for selective targeting of folate receptor-positive tumor cells. Bioconjug Chem. 2006;17:603–609
  55. Kohler N, Fryxell GE, Zhang M. A bifunctional poly(ethylene glycol) silane immobilized on metallic oxide-based nanoparticles for conjugation with cell targeting agents. J Am Chem Soc. 2004;126:7206–7211
  56. Kumar A, Mandal S, Selvakannan PR, Pasricha R, Mandale AB, Sastry M. Investigation into the interaction between surface-bound alkylamines and gold nanoparticles. Langmuir. 2003;19:6277–6282
  57. Leff DV, Brandt L, Heath JR. Synthesis and characterization of hydrophobic, organically soluble gold nanocrystals functionalized with primary amines. Langmuir. 1996;12:4723–4730
  58. Terril RH, Postelwaithe TA, Chen C, Poon C, Terzis A, Chen A, et al. Monolayers in three dimensions: NMR, SAXS, thermal, and electron hopping studies of alkanethiol stabilized gold clusters. J Am Chem Soc. 1995;117:12537–12548
  59. Spurr AR. A low viscosity epoxy resin embedding for electron microscopy. J Ultrastruct Res. 1969;26:31–43
  60. Mukherjee P, Bhattacharya R, Mukhopadhyay D. Gold nanoparticles bearing functional anti-cancer drug and anti-angiogenic agent: a “2 in 1” system with potential application in cancer therapeutics. J Biomed Nanotechnol. 2005;1:224–228
  61. Templeton AC, Hostelter MJ, Kraft CT, Murray RW. Reactivity of monolayer-protected gold cluster molecules: steric effects. J Am Chem Soc. 1998;120:1906–1911
  62. Johnson SR, Evans SD, Mahon SW, Ulman A. Alkanethiol molecules containing an aromatic moiety self-assembled onto gold clusters. Langmuir. 1997;13:51–57
  63. Colin BD, Evall J, Whitesides GM. Formation of monolayers by the coadsorption of thiols on gold: variation in the head group, tail group, and solvent. J Am Chem Soc. 1989;111:7155–7164
  64. Faulk WP, Taylor GM. An immunocolloid method for the electron microscope. Immunochemistry. 1971;8:1081–1083
  65. Hayat M. Colloidal gold: principles, methods and applications. San Diego: Academic; 1989;
  66. Bhattacharya R, Patra CR, Wang S, Lu L, Yaszemski MJ, Mukhopadhyay D, et al. Assembly of gold nanoparticles in a rod-like fashion using proteins as templates. Adv Funct Mater. 2006;16:395–400
  67. Love JC, Estroff LA, Kriebel JK, Nuzzo RG, Whitesides GM. Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev. 2005;105:1103–1170
  68. Kumar A, Mukherjee P, Guha A, Adyantaya SD, Mandale AB, Kumar R, et al. Amphoterization of colloidal gold particles by capping with valine molecules and their phase transfer from water to toluene by electrostatic coordination with fatty amine molecules. Langmuir. 2000;16:9775–9783
  69. Zhang Y, Kohler N, Zhang M. Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials. 2002;23:1553–1561
  70. Hess MW, Schwendinger MG, Eskelinen E, Pfaller K, Pavelka M, Dierich MP, et al. Tracing uptake of C3dg-conjugated antigen into B cells via complement receptor type 2 (CR2, CD21). Blood. 2003;95:2617–2623

 No conflict of interest was reported by the authors of this article.

PII: S1549-9634(07)00093-7

doi: 10.1016/j.nano.2007.07.001

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 3, Issue 3 , Pages 224-238 , September 2007

Article Tools

* Image Usage & Resolution