Advertisement

Kolaviron via anti-inflammatory and redox regulatory mechanisms abates multi-walled carbon nanotubes-induced neurobehavioral deficits in rats

  • Ebenezer O. FarombiEmail author
  • Ifeoluwa O. Awogbindin
  • Olatunde Owoeye
  • Ikenna C. Maduako
  • Akinola O. Ajeleti
  • Solomon E. Owumi
  • Anita K. Patlolla
  • Ebenezer O. Farombi
Original Investigation
  • 28 Downloads

Abstract

Exposure to multi-walled carbon nanotubes (MWCNTs) reportedly elicits neurotoxic effects. Kolaviron is a phytochemical with several pharmacological effects namely anti-oxidant, anti-inflammatory, and anti-genotoxic activities. The present study evaluated the neuroprotective mechanism of kolaviron in rats intraperitoneally injected with MWCNTs alone at 1 mg/kg body weight or orally co-administered with kolaviron at 50 and 100 mg/kg body weight for 15 consecutive days. Following exposure, neurobehavioral analysis using video-tracking software during trial in a novel environment indicated that co-administration of both doses of kolaviron significantly (p < 0.05) enhanced the locomotor, motor, and exploratory activities namely total distance traveled, maximum speed, total time mobile, mobile episode, path efficiency, body rotation, absolute turn angle, and negative geotaxis when compared with rats exposed to MWCNTs alone. Further, kolaviron markedly abated the decrease in the acetylcholinesterase activity and antioxidant defense system as well as the increase in oxidative stress and inflammatory biomarkers induced by MWCNT exposure in the cerebrum, cerebellum, and mid-brain of rats. The amelioration of MWCNT-induced neuronal degeneration in the brain structures by kolaviron was verified by histological and morphometrical analyses. Taken together, kolaviron abated MWCNT-induced neurotoxicity via anti-inflammatory and redox regulatory mechanisms.

Keywords

Multi-walled carbon nanotubes Kolaviron Neurotoxicity Acetylcholinesterase Oxido-inflammation 

Notes

Funding information

This research was supported in part by the National Institute of Health (NIH)-NIMHD with the grant number G12MD007581 and TETFUND National Research Fund (NRF) 2015 grant.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Abarikwu SO (2014) Kolaviron, a natural flavonoid from the seeds of Garcinia kola, reduces LPS-induced inflammation in macrophages by combined inhibition of IL-6 secretion, and inflammatory transcription factors, ERK1/2, NF-κB, p38, Akt, p-c-JUN and JNK. Biochim Biophys Acta 1840(7):2373–2381PubMedGoogle Scholar
  2. Abu Gazia M, El-Magd MA (2019) Effect of pristine and functionalized multiwalled carbon nanotubes on rat renal cortex. Acta Histochem 121(2):207–217PubMedGoogle Scholar
  3. Adedara IA, Abolaji AO, Rocha JB, Farombi EO (2016a) Diphenyl diselenide protects against mortality, locomotor deficits and oxidative stress in Drosophila melanogaster model of manganese-induced neurotoxicity. Neurochem Res 41:1430–1438PubMedGoogle Scholar
  4. Adedara IA, Rosemberg DB, de Souza D, Farombi EO, Aschner M, Souza DO, Rocha JBT (2016b) Neurobehavioral and biochemical changes in Nauphoeta cinerea following dietary exposure to chlorpyrifos. Pestic Biochem Physiol 130:22–30PubMedGoogle Scholar
  5. Adedara IA, Abolaji AO, Idris UF, Olabiyi BF, Onibiyo EM, Ojuade TD, Farombi EO (2017) Neuroprotective influence of taurine on fluoride-induced biochemical and behavioral deficits in rats. Chem Biol Interact 261:1–10PubMedGoogle Scholar
  6. Adedara IA, Anao OO, Forcados GE, Awogbindin IO, Agbowo A, Ola-Davies OE, Patlolla AK, Tchounwou PB, Farombi EO (2018) Low doses of multi-walled carbon nanotubes elicit hepatotoxicity in rats with markers of oxidative stress and induction of pro-inflammatory cytokines. Biochem Biophys Res Commun 503(4):3167–3173PubMedGoogle Scholar
  7. Akinmoladun AC, Akinrinola BL, Olaleye MT, Farombi EO (2015) Kolaviron, a Garcinia kola biflavonoid complex, protects against ischemia/reperfusion injury: pertinent mechanistic insights from biochemical and physical evaluations in rat brain. Neurochem Res 40(4):777–787PubMedGoogle Scholar
  8. Antúnez-Flores W, Valenzuela-Muñiz AM, Amézaga-Madrid P, Alonso-Nuñez G, Verde Y, Martínez-Sánchez R, Miki-Yoshida M (2008) Simplified route to multi-walled carbon nanotube synthesis by aerosol assisted chemical vapor deposition. J Nanosci Nanotechnol 8(12):6451–6455PubMedGoogle Scholar
  9. Aratani Y (2018) Myeloperoxidase: its role for host defense, inflammation, and neutrophil function. Arch Biochem Biophys 640:47–52PubMedGoogle Scholar
  10. Aschberger K, Johnston HJ, Stone V, Aitken RJ, Hankin SM, Peters SA, Tran CL, Christensen FM (2010) Review of carbon nanotubes toxicity and exposure--appraisal of human health risk assessment based on open literature. Crit Rev Toxicol 40(9):759–790PubMedGoogle Scholar
  11. Bancroft JD, Gamble M (2008) Theory and practice of histology techniques, 6th edn. Churchill Livingstone Elsevier, Philadelphia (PA), pp 83–134Google Scholar
  12. Baud V, Karin M (2001) Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 11(9):372–377PubMedGoogle Scholar
  13. Belyanskaya L, Weigel S, Hirsch C, Tobler U, Krug HF, Wick P (2009) Effects of carbon nanotubes on primary neurons and glial cells. Neurotoxicology 30:702–711PubMedGoogle Scholar
  14. Bianco A, Kostarelos K, Partidos CD, Prato M (2005) Biomedical applications of functionalised carbon nanotubes. Chem Commun 7:571–577Google Scholar
  15. Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralGoogle Scholar
  16. Brunauer S, Emmett PH, Teller E (1938) Adsorption of gases in multi-molecular layers. J Am Chem Soc 60:309–319Google Scholar
  17. Chen T, Yang J, Ren G, Yang Z, Zhang T (2013) Multi-walled carbon nanotube increases the excitability of hippocampal CA1 neurons through inhibition of potassium channels in rat's brain slices. Toxicol Lett 217:121–128PubMedGoogle Scholar
  18. Chen T, Yang J, Zhang H, Ren G, Yang Z, Zhang T (2014) Multi-walled carbon nanotube inhibits CA1 glutamatergic synaptic transmission in rat's hippocampal slices. Toxicol Lett 229:423–429PubMedGoogle Scholar
  19. Claiborne A (1995) Catalase activity. In: Greewald AR (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 237–242Google Scholar
  20. Day J, Damsma G, Fibiger HC (1991) Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav 38:723–729PubMedGoogle Scholar
  21. De Marchi L, Neto V, Pretti C, Figueira E, Chiellini F, Morelli A, Soares AMVM, Freitas R (2018) Toxic effects of multi-walled carbon nanotubes on bivalves: comparison between functionalized and non-functionalized nanoparticles. Sci Total Environ 622-623:1532–1542PubMedGoogle Scholar
  22. Dong J, Ma Q (2016) Suppression of basal and carbon nanotube-induced oxidative stress, inflammation and fibrosis in mouse lungs by Nrf2. Nanotoxicology. 10(6):699–709PubMedGoogle Scholar
  23. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95PubMedGoogle Scholar
  24. Farombi EO, Nwaokeafor IA (2005) Anti-oxidant mechanisms of kolaviron: studies on serum lipoprotein oxidation, metal chelation and oxidative membrane damage in rats. Clin Exp Pharmacol Physiol 32(8):667–674PubMedGoogle Scholar
  25. Farombi EO, Tahnteng JG, Agboola AO, Nwankwo JO, Emerole GO (2000) Chemoprevention of 2-acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron-a Garcinia kola seed extract. Food Chem Toxicol 38:535–541PubMedGoogle Scholar
  26. Farombi EO, Adedara IA, Forcados GE, Anao OO, Agbowo A, Patlolla AK (2016) Responses of testis, epididymis, and sperm of pubertal rats exposed to functionalized multiwalled carbon nanotubes. Environ Toxicol 31:543–551PubMedGoogle Scholar
  27. Farombi EO, Awogbindin IO, Farombi TH, Oladele JO, Izomoh ER, Aladelokun OB, Ezekiel IO, Adebambo OI, Abah VO (2019) Neuroprotective role of kolaviron in striatal redo-inflammation associated with rotenone model of Parkinson's disease. Neurotoxicology 73:132–141PubMedGoogle Scholar
  28. Gao J, Zhang X, Yu M, Ren G, Yang Z (2015) Cognitive deficits induced by multi-walled carbon nanotubes via the autophagic pathway. Toxicology 337:21–29PubMedGoogle Scholar
  29. Gorny JH, Gorny B, Wallace DG, Whishaw IQ (2002) Fimbria-fornix lesions disrupt the dead reckoning (homing) component of exploratory behavior in mice. Learn Mem 9(6):387–394PubMedPubMedCentralGoogle Scholar
  30. Granell S, Gironella M, Bulbena O, Panés J, Mauri M, Sabater L, Aparisi L, Gelpí E, Closa D (2003) Heparin mobilizes xanthine oxidase and induces lung inflammation in acute pancreatitis. Crit Care Med 31:525–530PubMedGoogle Scholar
  31. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and [15N] nitrate in biological fluids. Anal Biochem 126:131–138PubMedGoogle Scholar
  32. Grochowski C, Litak J, Kamieniak P, Maciejewski R (2018) Oxidative stress in cerebral small vessel disease. Role of reactive species. Free Radic Res 52(1):1–13PubMedGoogle Scholar
  33. Guzik TJ, Korbut R, Adamek-Guzik T (2003) Nitric oxide and superoxide in inflammation and immune regulation. J Physiol Pharmacol 54:469–487PubMedGoogle Scholar
  34. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  35. Han YG, Xu J, Li ZG, Ren GG, Yang Z (2012) In vitro toxicity of multi-walled carbon nanotubes in C6 rat glioma cells. Neurotoxicology 33:1128–1134PubMedGoogle Scholar
  36. Hayes JD, Strange RC (2000) Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology. 61:154–166PubMedGoogle Scholar
  37. Ishola IO, Adamson FM, Adeyemi OO (2017) Ameliorative effect of kolaviron, a biflavonoid complex from Garcinia kola seeds against scopolamine-induced memory impairment in rats: role of antioxidant defense system. Metab Brain Dis 32(1):235–245PubMedGoogle Scholar
  38. Iwu MM (1985) Antihepatoxic constituents of Garcinia kola seeds. Experientia 41(5):699–700PubMedGoogle Scholar
  39. Jacobs CB, Peairs MJ, Venton BJ (2010) Review: carbon nanotube based electrochemical sensors for biomolecules. Anal Chim Acta 662:105–127PubMedGoogle Scholar
  40. Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene induced liver necrosis: protective role of glutathione and evidence for 3,4 bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169PubMedGoogle Scholar
  41. Kamran U, Heo YJ, Lee JW, Park SJ (2019) Functionalized carbon materials for electronic devices: a review. Micromachines (Basel) 10(4).  https://doi.org/10.3390/mi10040234 PubMedCentralGoogle Scholar
  42. Kumar R, Dhanawat M, Kumar S, Singh BN, Pandit JK, Sinha VR (2014) Carbon nanotubes: a potential concept for drug delivery applications. Rec Patents Drug Deliv Formulat 8:12–26Google Scholar
  43. Lin Y, Taylor S, Li H, Shiral Fernando KA, Qu L, Wang W, Gu L, Zhou B, Ping Sun Y (2004) Advances toward bioapplications of carbon nanotubes. J Mater Chem 14:527–541Google Scholar
  44. Malarkey EB, Parpura V (2007) Applications of carbon nanotubes in neurobiology. Neurodegener Dis 4(4):292–299PubMedGoogle Scholar
  45. Misra HP, Fridovich I (1972) The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175PubMedGoogle Scholar
  46. Motz BA, Alberts JR (2005) The validity and utility of geotaxis in young rodents. Neurotoxicol Teratol 27(4):529–533PubMedGoogle Scholar
  47. Ndrepepa G (2019) Myeloperoxidase - a bridge linking inflammation and oxidative stress with cardiovascular disease. Clin Chim Acta 493:36–51PubMedGoogle Scholar
  48. Nel AE (2013) Implementation of alternative test strategies for the safety assessment of engineered nanomaterials. J Intern Med 274(6):561–577PubMedPubMedCentralGoogle Scholar
  49. Nwankwo JO, Tahnteng JG, Emerole GO (2000) Inhibition of aflatoxin B1 genotoxicity in human liver-derived HepG2 cells by kolaviron biflavonoids and molecular mechanisms of action. Eur J Cancer Prev 9(5):351–361PubMedGoogle Scholar
  50. Ojo OB, Amoo ZA, Saliu IO, Olaleye MT, Farombi EO, Akinmoladun AC (2019) Neurotherapeutic potential of kolaviron on neurotransmitter dysregulation, excitotoxicity, mitochondrial electron transport chain dysfunction and redox imbalance in 2-VO brain ischemia/reperfusion injury. Biomed Pharmacother 111:859–872PubMedGoogle Scholar
  51. Olajide OJ, Asogwa NT, Moses BO, Oyegbola CB (2017) Multidirectional inhibition of cortico-hippocampal neurodegeneration by kolaviron treatment in rats. Metab Brain Dis 32(4):1147–1161PubMedGoogle Scholar
  52. Onasanwo SA, Rotu RA (2016) Antinociceptive and anti-inflammatory potentials of kolaviron: mechanisms of action. J Basic Clin Physiol Pharmacol 27(4):363–370PubMedGoogle Scholar
  53. Osuagwu FC, Owoeye O, Avwioro OG, Oluwadara OO, Imosemi IO, Ajani RS, Ogunleye AA, Oladejo OW (2007) Reduction of hippocampal CA 1 neurons in Wistar rats following the administration of phenytoin for seven days. Afr J Med Med Sci 36:103–108PubMedGoogle Scholar
  54. Patlolla AK, Berry A, Tchounwou PB (2011) Study of hepatotoxicity and oxidative stress in male Swiss-Webster mice exposed to functionalized multi-walled carbon nanotubes. Mol Cell Biochem 358:189–199PubMedPubMedCentralGoogle Scholar
  55. Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ, Valko M (2017) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38(7):592–607PubMedGoogle Scholar
  56. Reddy AR, Rao MV, Krishna DR, Himabindu V, Reddy YN (2011) Evaluation of oxidative stress and anti-oxidant status in rat serum following exposure of carbon nanotubes. Regul Toxicol Pharmacol 59(2):251–257PubMedGoogle Scholar
  57. Riemann BL, Lephart SM (2002) The sensorimotor system, part I: the physiologic basis of functional joint stability. J Athl Train 37:71–79PubMedPubMedCentralGoogle Scholar
  58. Rode A, Sharma S, Mishra DK (2018) Carbon nanotubes: classification, method of preparation and pharmaceutical application. Curr Drug Deliv 15(5):620–629PubMedGoogle Scholar
  59. Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590PubMedGoogle Scholar
  60. Shichiri M (2014) The role of lipid peroxidation in neurological disorders. J Clin Biochem Nutr 54(3):151–160PubMedPubMedCentralGoogle Scholar
  61. Tsukahara T, Matsuda Y, Haniu H (2014) The role of autophagy as a mechanism of toxicity induced by multi-walled carbon nanotubes in human lung cells. Int J Mol Sci 16(1):40–48PubMedPubMedCentralGoogle Scholar
  62. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84PubMedGoogle Scholar
  63. Wang J, Schlagenhauf L, Setyan A (2017) Transformation of the released asbestos, carbon fibers and carbon nanotubes from composite materials and the changes of their potential health impacts. J Nanobiotechnol 15(1):15.  https://doi.org/10.1186/s12951-017-0248-7 CrossRefGoogle Scholar
  64. Zhao X, Chang S, Long J, Li J, Li X, Cao Y (2019) The toxicity of multi-walled carbon nanotubes (MWCNTs) to human endothelial cells: the influence of diameters of MWCNTs. Food Chem Toxicol 126:169–177PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  • Ebenezer O. Farombi
    • 1
    Email author
  • Ifeoluwa O. Awogbindin
    • 1
  • Olatunde Owoeye
    • 2
  • Ikenna C. Maduako
    • 1
  • Akinola O. Ajeleti
    • 3
  • Solomon E. Owumi
    • 4
  • Anita K. Patlolla
    • 5
  • Ebenezer O. Farombi
    • 1
  1. 1.Drug Metabolism and Toxicology Research Laboratories, Department of Biochemistry, College of MedicineUniversity of IbadanIbadanNigeria
  2. 2.Department of Anatomy, College of MedicineUniversity of IbadanIbadanNigeria
  3. 3.Department of Anatomy, College of MedicineBowen UniversityIwoNigeria
  4. 4.Cancer Research and Molecular Biology Laboratory, Department of Biochemistry, College of MedicineUniversity of IbadanIbadanNigeria
  5. 5.College of Science Engineering and Technology, NIH-RCMI Center for Environmental HealthJackson State UniversityJacksonUSA

Personalised recommendations