Skip to main content

Advertisement

SpringerLink
Log in

Investigation of effects of transferrin-conjugated gold nanoparticles on hippocampal neuronal activity and anxiety behavior in mice

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Gold nanoparticles (GNPs) have been widely used in medicine such as imaging, drug delivery and therapeutics due to their multifunctional properties. Alterations in neuronal function may contribute to various neurological diseases. Transferrin plays a primary role in iron transportation and delivery and has recently been utilized for drug delivery to the brain. We have investigated effects of transferrin-conjugated GNPs (Tf-GNPs) on anxiety and locomotor behavior in vivo and also hippocampal neuronal activity ex vivo. Electrophysiological effects of Tf-GNP on hippocampal neurons were determined by patch clamp method. Fifteen male young adult C57BL/6 mice were randomly divided into three groups as control (200 µL PBS), GNP (bare GNP; 2.2 μg/g in PBS) and Tf-GNPs (2.2 μg/g Tf-GNP). Animals intraperitoneally received the respective treatments for seven consecutive days and were subjected to elevated plus maze (EPM) and open field tests (OFT). Ex vivo, firing frequency of the neurons significantly increased by GNP treatment (p < 0.001). In vivo, animals in Tf-GNP group showed significantly longer distance in open arms but significantly lower number of entries to the open arms in EPM (p < 0.05). Mice received bare GNPs had significantly higher locomotor activity in OFT (p < 0.05), while Tf-GNP did not alter the locomotor activity significantly (p = 0.051). Animals in Tf-GNP group spent significantly longer time in the peripheral zone in OFT (p < 0.05). The present findings have shown that Tf-GNP induces anxiety-like behavior without altering spontaneous firing rate of hippocampal neurons. We suggest that neurobiological effects of Tf-GNP should be pre-determined before using in medical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

Not applicable.

References

  1. Singh P, Pandit S, Mokkapati V, Garg A, Ravikumar V, Mijakovic I (2018) Gold nanoparticles in diagnostics and therapeutics for human cancer. Int J Mol Sci. https://doi.org/10.3390/ijms19071979

    Article  PubMed  PubMed Central  Google Scholar 

  2. Wang S and Lu G (2018) Applications of gold nanoparticles in cancer imaging and treatment. In: Seehra MS, Bristow AD (eds) Noble and precious metals—properties, nanoscale effects and applications. pp 291–309

  3. Siddique S, Chow JCL (2020) Application of nanomaterials in biomedical imaging and cancer therapy. Nanomaterials (Basel). https://doi.org/10.3390/nano10091700

    Article  PubMed  PubMed Central  Google Scholar 

  4. Emami T, Madani R, Golchinfar F, Shoushtary A, Amini SM (2015) Comparison of gold nanoparticle conjugated secondary antibody with non-gold secondary antibody in an ELISA kit model. Monoclon Antib Immunodiagn Immunother 34:366–370. https://doi.org/10.1089/mab.2015.0021

    Article  CAS  PubMed  Google Scholar 

  5. Davatgaran Taghipour Y, Kharrazi S, Amini SM (2018) Antibody conjugated gold nanoparticles for detection of small amounts of antigen based on surface plasmon resonance (SPR) spectra. Nanomed Res J 3:102–108

    Google Scholar 

  6. Fatemi F, Amini SM, Kharrazi S, Rasaee MJ, Mazlomi MA, Asadi-Ghalehni M, Rajabibazl M, Sadroddiny E (2017) Construction of genetically engineered M13K07 helper phage for simultaneous phage display of gold binding peptide 1 and nuclear matrix protein 22 ScFv antibody. Colloids Surf B 159:770–780. https://doi.org/10.1016/j.colsurfb.2017.08.034

    Article  CAS  Google Scholar 

  7. Rezaeian A, Amini SM, Najafabadi MRH, Farsangi ZJ, Samadian H (2022) Plasmonic hyperthermia or radiofrequency electric field hyperthermia of cancerous cells through green-synthesized curcumin-coated gold nanoparticles. Lasers Med Sci 37:1333–1341. https://doi.org/10.1007/s10103-021-03399-7

    Article  PubMed  Google Scholar 

  8. Amini SM, Kharrazi S, Rezayat SM, Gilani K (2018) Radiofrequency electric field hyperthermia with gold nanostructures: role of particle shape and surface chemistry. Artif Cell Nanomedi Biotechnol 46:1452–1462

    Article  CAS  Google Scholar 

  9. Vines JB, Yoon J-H, Ryu N-E, Lim D-J, Park H (2019) Gold nanoparticles for photothermal cancer therapy. Front Chem 7:167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chen Y, Yang J, Fu S, Wu J (2020) Gold nanoparticles as radiosensitizers in cancer radiotherapy. Int J Nanomed 15:9407–9430. https://doi.org/10.2147/ijn.S272902

    Article  CAS  Google Scholar 

  11. Haume K, Rosa S, Grellet S, Śmiałek MA, Butterworth KT, Solov’yov AV, Prise KM, Golding J, Mason NJ (2016) Gold nanoparticles for cancer radiotherapy: a review. Cancer Nanotechnol 7:8. https://doi.org/10.1186/s12645-016-0021-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cheng Y, A CS, Meyers JD, Panagopoulos I, Fei B and Burda C, (2008) Highly efficient drug delivery with gold nanoparticle vectors for in vivo photodynamic therapy of cancer. J Am Chem Soc 130:10643–10647. https://doi.org/10.1021/ja801631c

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tao Y, Li M, Ren J, Qu X (2015) Metal nanoclusters: novel probes for diagnostic and therapeutic applications. Chem Soc Rev 44:8636–8663. https://doi.org/10.1039/c5cs00607d

    Article  CAS  PubMed  Google Scholar 

  14. Stafstrom CE, Carmant L (2015) Seizures and epilepsy: an overview for neuroscientists. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a022426

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wada A (2006) Roles of voltage-dependent sodium channels in neuronal development, pain, and neurodegeneration. J Pharmacol Sci 102:253–268. https://doi.org/10.1254/jphs.crj06012x

    Article  CAS  PubMed  Google Scholar 

  16. Imbrici P, Camerino DC, Tricarico D (2013) Major channels involved in neuropsychiatric disorders and therapeutic perspectives. Front Genet 4:76. https://doi.org/10.3389/fgene.2013.00076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yilmaz B, Gilmore D, Wilson C (1996) Inhibition of the pre-ovulatory LH surge in the rat by central noradrenergic mediation: involvement of an anaesthetic (urethane) and opioid receptor agonists. Biog Amin 12:423–435

    CAS  Google Scholar 

  18. Kutlu S, Yilmaz B, Canpolat S, Sandal S, Ozcan M, Kumru S, Kelestimur H (2004) Mu opioid modulation of oxytocin secretion in late pregnant and parturient rats. Involv Noradrenergic Neurotransm Neuroendocrinol 79:197–203. https://doi.org/10.1159/000078101

    Article  CAS  Google Scholar 

  19. Ozcan M, Yilmaz B, King WM, Carpenter DO (2004) Hippocampal long-term potentiation (LTP) is reduced by a coplanar PCB congener. Neurotoxicology 25:981–988. https://doi.org/10.1016/j.neuro.2004.03.014

    Article  CAS  PubMed  Google Scholar 

  20. Taskin IC, Sen O, Emanet M, Culha M, Yilmaz B (2020) Hexagonal boron nitrides reduce the oxidative stress on cells. Nanotechnology 31:215101. https://doi.org/10.1088/1361-6528/ab6fdc

    Article  CAS  PubMed  Google Scholar 

  21. Paviolo C, Stoddart PR (2017) Gold nanoparticles for modulating neuronal behavior. Nanomaterials (Basel). https://doi.org/10.3390/nano7040092

    Article  PubMed  Google Scholar 

  22. Upadhyay RK (2014) Drug delivery systems, CNS protection, and the blood brain barrier. Biomed Res Int 2014:869269. https://doi.org/10.1155/2014/869269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jones AR, Shusta EV (2007) Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res 24:1759–1771. https://doi.org/10.1007/s11095-007-9379-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kutlu S, Aydin M, Alcin E, Ozcan M, Bakos J, Jezova D, Yilmaz B (2010) Leptin modulates noradrenaline release in the paraventricular nucleus and plasma oxytocin levels in female rats: a microdialysis study. Brain Res 1317:87–91. https://doi.org/10.1016/j.brainres.2009.12.044

    Article  CAS  PubMed  Google Scholar 

  25. Kawabata H (2019) Transferrin and transferrin receptors update. Free Radic Biol Med 133:46–54. https://doi.org/10.1016/j.freeradbiomed.2018.06.037

    Article  CAS  PubMed  Google Scholar 

  26. Pulgar VM (2018) Transcytosis to cross the blood brain barrier. New Adv Chall Front Neurosci 12:1019. https://doi.org/10.3389/fnins.2018.01019

    Article  Google Scholar 

  27. Funabashi T, Suyama K, Uemura T, Hirose M, Hirahara F, Kimura F (2001) Immortalized gonadotropin-releasing hormone neurons (GT1-7 cells) exhibit synchronous bursts of action potentials. Neuroendocrinology 73:157–165. https://doi.org/10.1159/000054632

    Article  CAS  PubMed  Google Scholar 

  28. Strober W (2001) Trypan blue exclusion test of cell viability. Curr Protoc Immunol Appendix. https://doi.org/10.1002/0471142735.ima03bs21

    Article  Google Scholar 

  29. Aklan I, Sayar Atasoy N, Yavuz Y, Ates T, Coban I, Koksalar F, Filiz G, Topcu IC, Oncul M, Dilsiz P, Cebecioglu U, Alp MI, Yilmaz B, Davis DR, Hajdukiewicz K, Saito K, Konopka W, Cui H, Atasoy D (2020) NTS catecholamine neurons mediate hypoglycemic hunger via medial hypothalamic feeding pathways. Cell Metab 31:313-326.e5. https://doi.org/10.1016/j.cmet.2019.11.016

    Article  CAS  PubMed  Google Scholar 

  30. Lezak KR, Missig G, Carlezon WA Jr (2017) Behavioral methods to study anxiety in rodents. Dialogues Clin Neurosci 19:181–191. https://doi.org/10.31887/DCNS.2017.19.2/wcarlezon

    Article  PubMed  PubMed Central  Google Scholar 

  31. Seibenhener ML, Wooten MC (2015) Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp. https://doi.org/10.3791/52434

    Article  PubMed  PubMed Central  Google Scholar 

  32. Amini SM, Kharrazi S, Hadizadeh M, Fateh M, Saber R (2013) Effect of gold nanoparticles on photodynamic efficiency of 5-aminolevolenic acid photosensitiser in epidermal carcinoma cell line: an in vitro study. IET Nanobiotechnol 7:151–156. https://doi.org/10.1049/iet-nbt.2013.0021

    Article  CAS  PubMed  Google Scholar 

  33. Badirzadeh A, Alipour M, Najm M, Vosoogh A, Vosoogh M, Samadian H, Hashemi AS, Farsangi ZJ, Amini SM (2022) Potential therapeutic effects of curcumin coated silver nanoparticle in the treatment of cutaneous leishmaniasis due to Leishmania major in-vitro and in a murine model. J Drug Deliv Sci Technol 74:103576. https://doi.org/10.1016/j.jddst.2022.103576

    Article  CAS  Google Scholar 

  34. Repar N, Li H, Aguilar JS, Li QQ, Drobne D, Hong Y (2018) Silver nanoparticles induce neurotoxicity in a human embryonic stem cell-derived neuron and astrocyte network. Nanotoxicology 12:104–116. https://doi.org/10.1080/17435390.2018.1425497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Engin AB, Engin A (2019) Nanoparticles and neurotoxicity: dual response of glutamatergic receptors. Prog Brain Res 245:281–303. https://doi.org/10.1016/bs.pbr.2019.03.005

    Article  PubMed  Google Scholar 

  36. Yousef MI, Abuzreda AA, Kamel MA (2019) Neurotoxicity and inflammation induced by individual and combined exposure to iron oxide nanoparticles and silver nanoparticles. J Taibah Univ Sci 13:570–578. https://doi.org/10.1080/16583655.2019.1602351

    Article  Google Scholar 

  37. Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde RR, Sastry M (2005) Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir 21:10644–10654. https://doi.org/10.1021/la0513712

    Article  CAS  PubMed  Google Scholar 

  38. Adewale OB, Davids H, Cairncross L, Roux S (2019) Toxicological behavior of gold nanoparticles on various models: influence of physicochemical properties and other factors. Int J Toxicol 38:357–384. https://doi.org/10.1177/1091581819863130

    Article  CAS  PubMed  Google Scholar 

  39. Flora SJS (2017) Chapter 8—the applications, neurotoxicity, and related mechanism of gold nanoparticles. In: Jiang X, Gao H (eds) Neurotoxicity of nanomaterials and nanomedicine. Academic Press, pp 179–203

    Chapter  Google Scholar 

  40. Velasco-Aguirre C, Morales F, Gallardo-Toledo E, Guerrero S, Giralt E, Araya E, Kogan MJ (2015) Peptides and proteins used to enhance gold nanoparticle delivery to the brain: preclinical approaches. Int J Nanomed 10:4919–4936. https://doi.org/10.2147/ijn.s82310

    Article  CAS  Google Scholar 

  41. Dante S, Petrelli A, Petrini EM, Marotta R, Maccione A, Alabastri A, Quarta A, De Donato F, Ravasenga T, Sathya A, Cingolani R, Proietti Zaccaria R, Berdondini L, Barberis A, Pellegrino T (2017) Selective targeting of neurons with inorganic nanoparticles: revealing the crucial role of nanoparticle surface charge. ACS Nano 11:6630–6640. https://doi.org/10.1021/acsnano.7b00397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Salinas K, Kereselidze Z, DeLuna F, Peralta XG, Santamaria F (2014) Transient extracellular application of gold nanostars increases hippocampal neuronal activity. J Nanobiotechnology 12:31. https://doi.org/10.1186/s12951-014-0031-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tuna BG, Yavuz Y, Kuku G, Maharramov A, Yilmaz B, Saricam M, Ercan M, Culha M, Dogan S (2019) The effect of modified gold nanoparticles on the function of neurons of mice hippocampal brain slices. Mersin Univ Saglık Bilim Derg 12:328–340

    Article  Google Scholar 

  44. Tuna BG, Yesilay G, Yavuz Y, Yilmaz B, Culha M, Maharramov A, Dogan S (2020) Electrophysiological effects of polyethylene glycol modified gold nanoparticles on mouse hippocampal neurons. Heliyon 6:e05824. https://doi.org/10.1016/j.heliyon.2020.e05824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Soe ZC, Kwon JB, Thapa RK, Ou W, Nguyen HT, Gautam M, Oh KT, Choi HG, Ku SK, Yong CS, Kim JO (2019) Transferrin-conjugated polymeric nanoparticle for receptor-mediated delivery of doxorubicin in doxorubicin-resistant breast cancer cells. Pharmaceutics. https://doi.org/10.3390/pharmaceutics11020063

    Article  PubMed  PubMed Central  Google Scholar 

  46. Lopes Rodrigues R, Xie F, Porter AE, Ryan MP (2020) Geometry-induced protein reorientation on the spikes of plasmonic gold nanostars. Nanoscale Adv 2:1144–1151. https://doi.org/10.1039/c9na00584f

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Li JL, Wang L, Liu XY, Zhang ZP, Guo HC, Liu WM, Tang SH (2009) In vitro cancer cell imaging and therapy using transferrin-conjugated gold nanoparticles. Cancer Lett 274:319–326. https://doi.org/10.1016/j.canlet.2008.09.024

    Article  CAS  PubMed  Google Scholar 

  48. De Jong WH, Hagens WI, Krystek P, Burger MC, Sips AJ, Geertsma RE (2008) Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials 29:1912–1919. https://doi.org/10.1016/j.biomaterials.2007.12.037

    Article  CAS  PubMed  Google Scholar 

  49. Semmler-Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A, Takenaka S, Schmid G, Brandau W (2008) Biodistribution of 1.4- and 18-nm gold particles in rats. Small 4:2108–2111. https://doi.org/10.1002/smll.200800922

    Article  CAS  PubMed  Google Scholar 

  50. Sonavane G, Tomoda K, Makino K (2008) Biodistribution of colloidal gold nanoparticles after intravenous administration: effect of particle size. Colloids Surf B 66:274–280. https://doi.org/10.1016/j.colsurfb.2008.07.004

    Article  CAS  Google Scholar 

  51. Lasagna-Reeves C, Gonzalez-Romero D, Barria MA, Olmedo I, Clos A, Sadagopa Ramanujam VM, Urayama A, Vergara L, Kogan MJ, Soto C (2010) Bioaccumulation and toxicity of gold nanoparticles after repeated administration in mice. Biochem Biophys Res Commun 393:649–655. https://doi.org/10.1016/j.bbrc.2010.02.046

    Article  CAS  PubMed  Google Scholar 

  52. Hirn S, Semmler-Behnke M, Schleh C, Wenk A, Lipka J, Schäffler M, Takenaka S, Möller W, Schmid G, Simon U, Kreyling WG (2011) Particle size-dependent and surface charge-dependent biodistribution of gold nanoparticles after intravenous administration. Eur J Pharm Biopharm 77:407–416. https://doi.org/10.1016/j.ejpb.2010.12.029

    Article  CAS  PubMed  Google Scholar 

  53. Takeuchi I, Onaka H, Makino K (2018) Biodistribution of colloidal gold nanoparticles after intravenous injection: effects of PEGylation at the same particle size. Biomed Mater Eng 29:205–215. https://doi.org/10.3233/bme-171723

    Article  CAS  PubMed  Google Scholar 

  54. Terentyuk GS, Maslyakova GN, Suleymanova LV, Khlebtsov BN, Kogan BY, Akchurin GG, Shantrocha AV, Maksimova IL, Khlebtsov NG, Tuchin VV (2009) Circulation and distribution of gold nanoparticles and induced alterations of tissue morphology at intravenous particle delivery. J Biophotonics 2:292–302. https://doi.org/10.1002/jbio.200910005

    Article  CAS  PubMed  Google Scholar 

  55. Pan Y, Leifert A, Ruau D, Neuss S, Bornemann J, Schmid G, Brandau W, Simon U, Jahnen-Dechent W (2009) Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 5:2067–2076. https://doi.org/10.1002/smll.200900466

    Article  CAS  PubMed  Google Scholar 

  56. Simpson CA, Salleng KJ, Cliffel DE, Feldheim DL (2013) In vivo toxicity, biodistribution, and clearance of glutathione-coated gold nanoparticles. Nanomedicine 9:257–263. https://doi.org/10.1016/j.nano.2012.06.002

    Article  CAS  PubMed  Google Scholar 

  57. Papastefanaki F, Jakovcevski I, Poulia N, Djogo N, Schulz F, Martinovic T, Ciric D, Loers G, Vossmeyer T, Weller H, Schachner M, Matsas R (2015) Intraspinal delivery of polyethylene glycol-coated gold nanoparticles promotes functional recovery after spinal cord injury. Mol Ther 23:993–1002. https://doi.org/10.1038/mt.2015.50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lin YL, Jen JC, Hsu SH, Chiu IM (2008) Sciatic nerve repair by microgrooved nerve conduits made of chitosan-gold nanocomposites. Surg Neurol 70(S1):9–18. https://doi.org/10.1016/j.surneu.2008.01.057

    Article  Google Scholar 

  59. Jung S, Bang M, Kim BS, Lee S, Kotov NA, Kim B, Jeon D (2014) Intracellular gold nanoparticles increase neuronal excitability and aggravate seizure activity in the mouse brain. PLoS ONE 9:e91360. https://doi.org/10.1371/journal.pone.0091360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Xie Y, Wang Y, Zhang T, Ren G, Yang Z (2012) Effects of nanoparticle zinc oxide on spatial cognition and synaptic plasticity in mice with depressive-like behaviors. J Biomed Sci 19:14. https://doi.org/10.1186/1423-0127-19-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Torabi M, Kesmati M, Harooni HE, Varzi HN (2013) Effects of nano and conventional zinc oxide on anxiety-like behavior in male rats. Indian J Pharmacol 45:508–512. https://doi.org/10.4103/0253-7613.117784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kesmati M, Torabi M, Teymuri Zamaneh H, Malekshahi Nia H (2014) Interaction between anxiolytic effects of magnesium oxide nanoparticles and exercise in adult male rat. Nanomed J 1:324–330. https://doi.org/10.7508/nmj.2015.05.006

    Article  Google Scholar 

  63. Li X, Liu X, Li T, Li X, Feng D, Kuang X, Xu J, Zhao X, Sun M, Chen D, Zhang Z, Feng X (2017) SiO2 nanoparticles cause depression and anxiety-like behavior in adult zebrafish. RSC Adv 7:2953–2963. https://doi.org/10.1039/C6RA24215D

    Article  CAS  Google Scholar 

  64. Martin EI, Ressler KJ, Binder E, Nemeroff CB (2009) The neurobiology of anxiety disorders: brain imaging, genetics, and psychoneuroendocrinology. Psychiatr Clin North Am 32:549–575. https://doi.org/10.1016/j.psc.2009.05.004

    Article  PubMed  PubMed Central  Google Scholar 

  65. Duval ER, Javanbakht A, Liberzon I (2015) Neural circuits in anxiety and stress disorders: a focused review. Ther Clin Risk Manag 11:115–126. https://doi.org/10.2147/tcrm.s48528

    Article  PubMed  PubMed Central  Google Scholar 

  66. McHugh SB, Deacon RM, Rawlins JN, Bannerman DM (2004) Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci 118:63–78. https://doi.org/10.1037/0735-7044.118.1.63

    Article  CAS  PubMed  Google Scholar 

  67. Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV, Abrous DN (2009) Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 14:959–967. https://doi.org/10.1038/mp.2009.15

    Article  PubMed  Google Scholar 

  68. Jimenez JC, Su K, Goldberg AR, Luna VM, Biane JS, Ordek G, Zhou P, Ong SK, Wright MA, Zweifel L, Paninski L, Hen R, Kheirbek MA (2018) Anxiety cells in a hippocampal-hypothalamic circuit. Neuron 97:670-683.e6. https://doi.org/10.1016/j.neuron.2018.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Adhikari A, Topiwala MA, Gordon JA (2011) Single units in the medial prefrontal cortex with anxiety-related firing patterns are preferentially influenced by ventral hippocampal activity. Neuron 71:898–910. https://doi.org/10.1016/j.neuron.2011.07.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kim SY, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS, Lo M, Pak S, Mattis J, Lim BK, Malenka RC, Warden MR, Neve R, Tye KM, Deisseroth K (2013) Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496:219–223. https://doi.org/10.1038/nature12018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Adhikari A (2014) Distributed circuits underlying anxiety. Front Behav Neurosci 8:112. https://doi.org/10.3389/fnbeh.2014.00112

    Article  PubMed  PubMed Central  Google Scholar 

  72. Ahrens S, Wu MV, Furlan A, Hwang GR, Paik R, Li H, Penzo MA, Tollkuhn J, Li B (2018) A central extended amygdala circuit that modulates anxiety. J Neurosci 38:5567–5583. https://doi.org/10.1523/jneurosci.0705-18.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

None.

Funding

This study did not receive any grants from any third parties.

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, Yeditepe University, Istanbul, Turkey

    Yavuz Yavuz, Cihan Suleyman Erdogan & Bayram Yilmaz

  2. Department of Molecular Biology and Genetics, Hamidiye Institute of Health Sciences, University of Health Sciences-Turkey, Istanbul, Turkey

    Gamze Yesilay

  3. Department of Biophysics, Faculty of Medicine, Yeditepe University, Istanbul, Turkey

    Bilge Guvenc Tuna & Akif Maharramov

  4. Department of Chemistry and Physics, Augusta University, Augusta, GA, USA

    Mustafa Culha

  5. Nanotechnology Research and Application Center (SUNUM), Sabanci University, Istanbul, Turkey

    Mustafa Culha

  6. Department of Biophysics, School of Medicine, Marmara University, Istanbul, Turkey

    Gunseli Ayse Garip

Authors
  1. Yavuz Yavuz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gamze Yesilay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bilge Guvenc Tuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akif Maharramov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mustafa Culha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cihan Suleyman Erdogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gunseli Ayse Garip
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bayram Yilmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YY performed behavioral experiments and electrophysiological recordings; GY performed synthesis of gold nanoparticles and characterization; BGT performed characterization of gold nanoparticles, analyzed, and interpret the data; BGT, GAG, AM, and MC provided technical support, reagents, and instrumentation; BY conceived experiments, analyzed data, prepared figures, and wrote the paper.

Corresponding author

Correspondence to Bayram Yilmaz.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Yeditepe University on Experimental Animal Research (Date. 17/03/2017 /No: 599).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yavuz, Y., Yesilay, G., Guvenc Tuna, B. et al. Investigation of effects of transferrin-conjugated gold nanoparticles on hippocampal neuronal activity and anxiety behavior in mice. Mol Cell Biochem 478, 1813–1824 (2023). https://doi.org/10.1007/s11010-022-04632-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-022-04632-9

Keywords

Search

Navigation