Zinc chloride through N-Cadherin upregulation prevents the damage induced by silver nanoparticles in rat cerebellum
Source abstract
Abstract
Silver nanoparticles (AgNPs), due to their metallic nature, are increasingly used in biological, optical, and electrical applications. Some reports indicate that AgNPs can induce damage in the central nervous system (CNS), yet little is known about the physiological responses to any such damage. The goal of this work was to investigate the histological cerebellar cortex damage caused by an intraperitoneal administration of AgNPs (15 mg/kg) in rats, and if this damage could be prevented by 24 h of previous treatment with ZnCl2 (27 mg/kg), as well as to evaluate if these effects are associated with the expression of N-Cadherin in the cerebellum. We showed that AgNPs induced damage in the different layers of the cerebellum. Expression of N-Cadherin increased in the white matter after AgNPs and ZnCl2 + AgNPs treatment, and in all cerebellar cortical layers after ZnCl2 + AgNPs administration. We find that N-Cadherin is acting as a mediator of the neuroprotective process against the damage induced by AgNPs in the cerebellar cortex, and this neuroprotective role is enhanced by extracellular Zn. Graphical abstract
Source: expertdata · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Nanoparticles: synthesis and applications · Heavy Metal Exposure and Toxicity · Trace Elements in Health
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (61)
Show source-provided references
1. Specification PA (2007) Terminology for nanomaterials: British Standards Institute London. https://www.mendeley.com/catalogue/3708dfb2-946d-3ec0-99eb-49b409534225/?utm_source=desktop&utm_medium=1.19.4&utm_campaign=open_catalog&userDocumentId=%7B315720f1-1e92-489b-93d6-cc569f8d47c8%7D
2. Kolahalam LA, Kasi Viswanath IV, Diwakar BS, Govindh B, Reddy V, Murthy YLN (2019) Review on nanomaterials: synthesis and applications. Mater Today Proc 18:2182–2190. https://doi.org/10.1016/j.matpr.2019.07.37110.1016/j.matpr.2019.07.371 ↗
3. Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 17(9):1534. https://doi.org/10.3390/ijms1709153410.3390/ijms17091534 ↗
4. Wiesner MR, Lowry GV, Jones KL, Hochella MF Jr, Di Giulio RT, Casman E, Bernhardt ES (2009) Decreasing uncertainties in assessing environmental exposure, risk, and ecological implications of nanomaterials. Environ Sci Technol 43(17):6458–6462. https://doi.org/10.1021/es803621k10.1021/es803621k ↗
5. Papp T, Schiffmann D, Weiss D, Castranova V, Vallyathan V, Rahman Q (2008) Human health implications of nanomaterial exposure. Nanotoxicology 2(1):9–27. https://doi.org/10.1080/1743539070184793510.1080/17435390701847935 ↗
6. Barabadi H, Mojab F, Vahidi H, Marashi B, Talank N, Hosseini O, Saravanan M (2021) Green synthesis, characterization, antibacterial and biofilm inhibitory activity of silver nanoparticles compared to commercial silver nanoparticles. Inorg Chem Commun 129:108647. https://doi.org/10.1016/j.inoche.2021.10864710.1016/j.inoche.2021.108647 ↗
7. Barabadi H, Mostafavi E, Truong LB, Cruz DM, Vahidi H, Mahjoub MA, Hosseini O, Saravanan M (2022) Microbial nanotechnology–based approaches for wound healing and infection control. In: Handbook of Microbial Nanotechnology: Academic Press p. 1–15. https://doi.org/10.1016/B978-0-12-823426-6.00009-710.1016/B978-0-12-823426-6.00009-7 ↗
8. Barabadi H, Jounaki K, Pishgahzadeh E, Morad H, Sadeghian-Abadi S, Vahidi H, Mahjoub A, Hosseini O, Saravanan M (2022) Antiviral potential of green-synthesized silver nanoparticles. In: Handbook of Microbial Nanotechnology: Academic Press p. 285–310. https://doi.org/10.1016/B978-0-12-823426-6.00009-710.1016/B978-0-12-823426-6.00009-7 ↗
9. Talank N, Morad H, Barabadi H, Mojab F, Amidi S, Kobarfard F, Mahjoub A, Jounaki K, Mohammadi N, Salehi G, Ashrafizadeh M, Mostafavi E (2022) Bioengineering of green-synthesized silver nanoparticles: in vitro physicochemical, antibacterial, biofilm inhibitory, anticoagulant, and antioxidant performance. Talanta 243:123374. https://doi.org/10.1016/j.talanta.2022.12337410.1016/j.talanta.2022.123374 ↗
10. Barabadi H, Hosseini O, Damavandi Kamali K, Jazayeri Shoushtari F, Rashedi M, Haghi-Aminjan H, Saravanan M (2020) Emerging theranostic silver nanomaterials to combat lung cancer: a systematic review. J Clust Sci 31(1):1–10. https://doi.org/10.1007/s10876-019-01639-z10.1007/s10876-019-01639-z ↗
11. Barabadi H, Vahidi H, Damavandi Kamali K, Rashedi M, Hosseini O, Golnaraghi Ghomi AR, Saravanan M (2020) Emerging theranostic silver nanomaterials to combat colorectal cancer: a systematic review. J Clust Sci 31(2):311–321. https://doi.org/10.1007/s10876-019-01668-810.1007/s10876-019-01668-8 ↗
12. Mostafavi E, Zarepour A, Barabadi H, Zarrabi A, Truong LB, Medina-Cruz D (2022) Antineoplastic activity of biogenic silver and gold nanoparticles to combat leukemia: beginning a new era in cancer theragnostic. Biotechnol Rep 34:e00714. https://doi.org/10.1016/j.talanta.2022.12337410.1016/j.talanta.2022.123374 ↗
13. Barabadi H, Vahidi H, Rashedi M, Mahjoub MA, Nanda A, Saravanan M (2020) Recent advances in biological mediated cancer research using silver nanoparticles as a promising strategy for hepatic cancer therapeutics: a systematic review. Nanomed J 7(4):251–62. https://doi.org/10.22038/nmj.2020.07.0000110.22038/nmj.2020.07.00001 ↗
14. Liu W, Worms IAM, Herlin-Boime N, Truffier-Boutry D, Michaud-Soret I, Mintz E, Vidaud V, Rollin-Genetet F (2017) Interaction of silver nanoparticles with metallothionein and ceruloplasmin: impact on metal substitution by Ag(i), corona formation and enzymatic activity. Nanoscale 9(19):6581–6594. https://doi.org/10.1039/c7nr01075c10.1039/c7nr01075c ↗
15. Mirkatuli HA, Baghbani M, Yahyaei B (2021) Comparison of the possible histopathological changes of the rat neonatal cerebellum induced by toxic and nontoxic doses of biological silver nanoparticles with chemical silver nanoparticles. Brain Behav 11(8):e2319. https://doi.org/10.1002/brb3.231910.1002/brb3.2319 ↗
16. Salazar-García S, Silva-Ramírez AS, Ramirez-Lee MA, Rosas-Hernandez H, Rangel- López E, Castillo CG, Santamaría A, Martinez-Castañon GA, Gonzalez C (2015) Comparative effects on rat primary astrocytes and C6 rat glioma cells cultures after 24-h exposure to silver nanoparticles (AgNPs). J Nanopart Res 17(11):1–13. https://doi.org/10.1007/s11051-015-3257-110.1007/s11051-015-3257-1 ↗
17. Salazar-García S, Delgado-Buenrostro NL, Rodríguez-Escamilla JC, Davalos-Rivas G, Chirino YI, del Campo CGCM, Martínez-Castañon G, Vargas-Morales JM, Gonzalez C (2019) Zinc protects the rat brain from damage induced by 24 h exposure to silver nanoparticles. J Nanopart Res 21(8):1–13. https://doi.org/10.1007/s11051-019-4616-010.1007/s11051-019-4616-0 ↗
18. Hochmeister S, Romauch M, Bauer J, Seifert-Held T, Weissert R, Linington C, Hartung HP, Fazekas F, Storch MK (2012) Re-expression of N-cadherin in remyelinating lesions of experimental inflammatory demyelination. Exp Neurol 237(1):70–77. https://doi.org/10.1016/j.toxlet.2008.04.015.2012.06.01010.1016/j.toxlet.2008.04.015.2012.06.010 ↗
19. Heiliger E, Osmanagic A, Haase H, Golenhofen N, Grabrucker AM, Weth A, Baumgartner W (2015) N-cadherin-mediated cell adhesion is regulated by extracellular Zn2+. Metallomics 7(2):355–362. https://doi.org/10.1039/c4mt00300d10.1039/c4mt00300d ↗
20. Cerminara NL, Lang EJ, Sillitoe RV, Apps R (2015) Redefining the cerebellar cortex as an assembly of non-uniform Purkinje cell microcircuits. Nat Rev Neurosci 16(2):79–93. https://doi.org/10.1038/nrn388610.1038/nrn3886 ↗
21. Espinosa-Cristobal L, Martinez-Castanon G, Loyola-Rodriguez J, Patino-Marin N, Reyes-Macias J, Vargas-Morales J, Ruiz F (2013) Toxicity, distribution, and accumulation of silver nanoparticles in Wistar rats. J Nanopart Res 15(6):1702. https://doi.org/10.1007/s11051-013-1702-610.1007/s11051-013-1702-6 ↗
22. Zeng Z, Li D, Liu F, Zhou C, Shao Q, Ding C, Qing C, Wang X, Hu Z, Qian K (2019) Mitochondrial DNA plays an important role in lung injury induced by sepsis. J Cell Biochem 120(5):8547–8560. https://doi.org/10.1002/jcb.2814210.1002/jcb.28142 ↗
23. Cisneros-Mejorado AJ, Garay E, Ortiz-Retana J, Concha L, Moctezuma JP, Romero S, Arellano RO (2020) Demyelination-remyelination of the rat caudal cerebellar peduncle evaluated with magnetic resonance imaging. Neuroscience 439:255–267. https://doi.org/10.1016/j.neuroscience.2019.06.04210.1016/j.neuroscience.2019.06.042 ↗
24. Trivedi MK, Sethi KK, Panda P, Jana S (2017) A comprehensive physicochemical, thermal, and spectroscopic characterization of zinc (II) chloride using X-ray diffraction, particle size distribution, differential scanning calorimetry, thermogravimetric analysis/differential thermogravimetric analysis, ultraviolet-visible, and Fourier transform-infrared spectroscopy. Int J Pharm Investig 7(1):33–40. https://doi.org/10.4103/jphi.JPHI_2_1710.4103/jphi.JPHI_2_17 ↗
25. Brynestad J, Yakel H (1978) Preparation and structure of anhydrous zinc chloride. Inorg Chem 17(5):1376–1377. https://doi.org/10.1021/ic50183a05910.1021/ic50183a059 ↗
26. Wilcox RJ, Losey BP, Folmer JC, Martin JD, Zeller M, Sommer R (2015) Crystalline and liquid structure of zinc chloride trihydrate: a unique ionic liquid. Inorg Chem 54(3):1109–1119. https://doi.org/10.1021/ic502453210.1021/ic5024532 ↗
27. Thorat GM, Ho VC, Mun J (2022) Zn-based deep eutectic solvent as the stabilizing electrolyte for Zn metal anode in rechargeable aqueous batteries. Front Chem 9:825807. https://doi.org/10.3389/fchem.2021.82580710.3389/fchem.2021.825807 ↗
28. Lang W (1968) Nomarski differential interference-contrast microscopy I. Fundamentals and experimental designs. Zeiss Information 70:16–114
29. Kadowaki M, Nakamura S, Machon O, Krauss S, Radice GL, Takeichi M (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304(1):22–33. https://doi.org/10.1016/j.ydbio.2006.12.01410.1016/j.ydbio.2006.12.014 ↗
30. Sim W, Barnard RT, Blaskovich M, Ziora ZM (2018) Antimicrobial silver in medicinal and consumer applications: a patent review of the past decade (2007–2017). Antibiotics 7(4):93. https://doi.org/10.3390/antibiotics704009310.3390/antibiotics7040093 ↗
31. Barabadi H, Vahidi H, Damavandi Kamali K, Rashedi M, Saravanan M (2020) Antineoplastic biogenic silver nanomaterials to combat cervical cancer: a novel approach in cancer therapeutics. J of Clust Sci 31(4):659–672. https://doi.org/10.1007/s10876-019-01697-310.1007/s10876-019-01697-3 ↗
32. Saravanan M, Barabadi H, Vahidi H, Webster TJ, Medina-Cruz D, Mostafavi E, Vernet-Crua A, Cholula-Diaz J, Periakaruppan P (2021) Emerging theranostic silver and gold nanobiomaterials for breast cancer: present status and future prospects. In: Handbook on nanobiomaterials for therapeutics and diagnostic applications: Elsevier p. 439–56. https://doi.org/10.1016/B978-0-12-821013-0.00004-010.1016/B978-0-12-821013-0.00004-0 ↗
33. Gonzalez C, Rosas-Hernandez H, Ramirez-Lee MA, Salazar-García S, Ali SF (2016) Role of silver nanoparticles (AgNPs) on the cardiovascular system. Arch Toxicol 90(3):493–511. https://doi.org/10.1007/s00204-014-1447-810.1007/s00204-014-1447-8 ↗
34. Rosas-Hernández H, Jiménez-Badillo S, Martínez-Cuevas PP, Gracia-Espino E, Terrones H, Terrones M, Hussain SM, Ali SF, González C (2009) Effects of 45-nm silver nanoparticles on coronary endothelial cells and isolated rat aortic rings. Toxicol Lett 191(2–3):305–313. https://doi.org/10.1016/j.toxlet.2009.09.01410.1016/j.toxlet.2009.09.014 ↗
35. Ramírez-Lee MA, Rosas-Hernández H, Salazar-García S, Gutiérrez-Hernández JM, Espinosa-Tanguma R, González FJ, Ali SF, González C (2014) Silver nanoparticles induce anti-proliferative effects on airway smooth muscle cells. Role of nitric oxide and muscarinic receptor signaling pathway. Toxicol Lett 224(2):246–256. https://doi.org/10.1016/j.toxlet.2013.10.02710.1016/j.toxlet.2013.10.027 ↗
36. AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3(2):279–290. https://doi.org/10.1021/nn800596w10.1021/nn800596w ↗
37. Hsin YH, Chen CF, Huang S, Shih TS, Lai PS, Chueh PJ (2008) The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179(3):130–139. https://doi.org/10.1016/j.toxlet.2008.04.01510.1016/j.toxlet.2008.04.015 ↗
38. Krajewski S, Prucek R, Panacek A, Avci-Adali M, Nolte A, Straub A, Zboril R, Wendel HP, Kvitek L (2013) Hemocompatibility evaluation of different silver nanoparticle concentrations employing a modified Chandler-loop in vitro assay on human blood. Acta Biomater 9(7):7460–7468. https://doi.org/10.1016/j.actbio.2013.03.01610.1016/j.actbio.2013.03.016 ↗
39. Janzadeh A, Behroozi Z, Janzadeh N, Arzani H, Tanha K, Hamblin MR, Ramezani F (2021) Neurotoxicity of silver nanoparticles in the animal brain: a systematic review and meta-analysis. Forensic Toxicol 40:49–63. https://doi.org/10.1007/s11419-021-00589-410.1007/s11419-021-00589-4 ↗
40. Xu Y, Tang H, Liu JH, Wang H, Liu Y (2013) Evaluation of the adjuvant effect of silver nanoparticles both in vitro and in vivo. Toxicol Lett 219(1):42–8. https://doi.org/10.1016/j.toxlet.2013.02.01010.1016/j.toxlet.2013.02.010 ↗
41. Mohamed EM, Kattaia AAA, Abdul-Maksoud RS, Abd El-Baset SA (2020) Cellular, molecular and biochemical impacts of silver nanoparticles on rat cerebellar cortex. Cells 10(1):7. https://doi.org/10.3390/cells1001000710.3390/cells10010007 ↗
42. Sarhan OMM, Hussein RM (2014) Effects of intraperitoneally injected silver nanoparticles on histological structures and blood parameters in the albino rat. Int J Nanomedicine 24(9):1505–1517. https://doi.org/10.2147/IJN.S5672910.2147/IJN.S56729 ↗
43. Alessandrini F, Vennemann A, Gschwendtner S, Neumann AU, Rothballer M, Seher T, Wimmer M, Kublik S, Traidl-Hoffmann C, Schloter M, Wiemann M, Schmidt-Weber C (2017) Pro-inflammatory versus immunomodulatory effects of silver nanoparticles in the lung: the critical role of dose, size and surface modification. Nanomater (Basel) 7(10):300. https://doi.org/10.3390/nano710030010.3390/nano7100300 ↗
44. de Lahunta A, Glass EN, Kent M (2016) Embryonic development of the central nervous system. Vet Clin North Am Small Anim Pract 46(2):193–216. https://doi.org/10.1016/j.cvsm.2015.10.01110.1016/j.cvsm.2015.10.011 ↗
45. Ahmed MM, Hussein MM (2017) Neurotoxic effects of silver nanoparticles and the protective role of rutin. Biomed Pharmacother 90:731–739. https://doi.org/10.1016/j.biopha.2017.04.02610.1016/j.biopha.2017.04.026 ↗
46. Krawczyńska A, Dziendzikowska K, Gromadzka-Ostrowska J, Lankoff A, Herman AP, Oczkowski M, Królikowski T, Wilczak J, Wojewódzka M, Kruszewski M (2015) Silver and titanium dioxide nanoparticles alter oxidative/inflammatory response and renin-angiotensin system in brain. Food Chem Toxicol 85:96–105. https://doi.org/10.1016/j.fct.2015.08.00510.1016/j.fct.2015.08.005 ↗
47. Xu L, Shao A, Zhao Y, Wang Z, Zhang C, Sun Y, Deng J, Chou LL (2015) Neurotoxicity of silver nanoparticles in rat brain after intragastric exposure. J Nanosci Nanotechnol 15(6):4215–4223. https://doi.org/10.1166/jnn.2015.961210.1166/jnn.2015.9612 ↗
48. Wu T, Tang M (2018) The inflammatory response to silver and titanium dioxide nanoparticles in the central nervous system. Nanomedicine 13(2):233–249. https://doi.org/10.2217/nnm-2017-027010.2217/nnm-2017-0270 ↗
49. Sandstead HH (2000) Causes of iron and zinc deficiencies and their effects on brain. J Nutr 130(2):347S-349S. https://doi.org/10.1093/jn/130.2.347S10.1093/jn/130.2.347S ↗
50. Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6(6):449–462. https://doi.org/10.1038/nrn167110.1038/nrn1671 ↗
51. Kim J, Kim S, Jeon S, Hui Z, Kim Y, Im Y, Lim W, Kim C, Choi H, Kim O (2015) Anti-inflammatory effects of zinc in PMA-treated human gingival fibroblast cells. Med Oral Patol Oral Cir Bucal 20(2):e180-7. https://doi.org/10.4317/medoral10.4317/medoral ↗
52. Franciscato C, Moraes-Silva L, Duarte FA, Oliveira CS, Ineu RP, Flores EM, Dressler VL, Peixoto NC, Pereira ME (2011) Delayed biochemical changes induced by mercury intoxication are prevented by zinc pre-exposure. Ecotoxicol Environ Saf 74(3):480–486. https://doi.org/10.1016/j.ecoenv.2010.11.01110.1016/j.ecoenv.2010.11.011 ↗
53. Miyamoto Y, Sakane F, Hashimoto K (2015) N-cadherin-based adherens junction regulates the maintenance, proliferation, and differentiation of neural progenitor cells during development. Cell Adh Migr 9(3):183–192. https://doi.org/10.1080/19336918.2015.100546610.1080/19336918.2015.1005466 ↗
54. Salazar-García S, García-Rodrigo JF, Martínez-Castañón GA, Ruiz-Rodríguez VM, Portales-Pérez DP, Gonzalez C (2020) Silver nanoparticles (AgNPs) and zinc chloride (ZnCl2) exposure order determines the toxicity in C6 rat glioma cells. J Nanopart Res 22(9):1–13. https://doi.org/10.1007/s11051-020-04984-710.1007/s11051-020-04984-7 ↗
55. Strużyńska L, Skalska J (2018) Mechanisms underlying neurotoxicity of silver nanoparticles. Adv Exp Med Biol 227-250.https://doi.org/10.1007/978-3-319-72041-8_1410.1007/978-3-319-72041-8_14 ↗
56. Yin N, Zhang Y, Yun Z, Liu Q, Qu G, Zhou Q, Hu L, Jiang G (2015) Silver nanoparticle exposure induces rat motor dysfunction through decrease in expression of calcium channel protein in cerebellum. Toxicol Lett 237(2):112–120. https://doi.org/10.1016/j.toxlet.2015.06.00710.1016/j.toxlet.2015.06.007 ↗
57. Ziemińska E, Stafiej A, Strużyńska L (2014) The role of the glutamatergic NMDA receptor in nanosilver-evoked neurotoxicity in primary cultures of cerebellar granule cells. Toxicology 315:38–48. https://doi.org/10.1016/j.tox.2013.11.00810.1016/j.tox.2013.11.008 ↗
58. Romero-Isart N, Vasák M (2002) Advances in the structure and chemistry of metallothioneins. J Inorg Biochem 88(3–4):388–396. https://doi.org/10.1016/s0162-0134(01)00347-610.1016/s0162-0134(01)00347-6 ↗
59. Kanemaru K, Kubota J, Sekiya H, Hirose K, Okubo Y, Iino M (2013) Calcium-dependent N-cadherin up-regulation mediates reactive astrogliosis and neuroprotection after brain injury. Proc Natl Acad Sci U S A 110(28):11612–11617. https://doi.org/10.1073/pnas.130037811010.1073/pnas.1300378110 ↗
60. Wolf C, Weth A, Walcher S, Lax C, Baumgartner W (2018) Modeling of zinc dynamics in the synaptic cleft: implications for cadherin mediated adhesion and synaptic plasticity. Front Mol Neurosci 11:306. https://doi.org/10.3389/fnmol.2018.0030610.3389/fnmol.2018.00306 ↗
61. Schnädelbach O, Özen Í, Blaschuk OW, Gour BJ, Meyer RL, Fawcett JW (2001) N-Cadherin is involved in axon-oligodendrocyte contact and myelination. Mol Cell Neurosci 17(6):1084–1093. https://doi.org/10.1006/mcne.2001.096110.1006/mcne.2001.0961 ↗