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Exploring the Combined Effect of Exercise and Apigenin on Aluminium-Induced Neurotoxicity in Zebrafish

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Abstract

Aluminium (AL) is a strong environmental neurotoxin linked to neurodegenerative disorders. Widespread industrial use leads to its presence in water systems, causing bioaccumulation in organisms. This, in turn, results in the bioaccumulation of AL in various organisms. Several studies have highlighted the benefits of enhanced physical activity in combating neurodegenerative diseases. Meanwhile widespread presence of apigenin in aquatic environment has been largely overlooked, in terms of its potential to counter AL-induced neurotoxicity. The combined impact of exercise and apigenin in mitigating the effects of AL-induced neurotoxicity in aquatic animals remains unexplored. Hence, the objective of this study is to determine whether the combined treatment of exercise and apigenin can effectively alleviate the chronic neurotoxicity induced by AL. Zebrafish that were exposed to AL showed behaviours resembling anxiety, increased aggression, unusual swimming pattern, and memory impairment, which are typical features observed in Alzheimer’s disease (AD)–like syndrome. Combined treatment of exercise and apigenin protects zebrafish from AL-induced neurotoxicity, which was measured by improvements in memory, reduced anxiety and aggression, and increased levels of antioxidant enzymes and acetylcholinesterase (AChE) activity. Furthermore, AL exposure is associated with increased expression of genes related to neuroinflammation and AD. However, synergistic effect of exercise and apigenin counteract this effect in AL-treated zebrafish. These findings suggest that AL is involved in neurodegenerative diseases in fish, which could affect the integrity of aquatic ecosystem. Hence, there is a strong correlation between enhanced physical activity, apigenin, and the well-being of the ecosystem.

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Data Availability

The data presented in this study are available on request from the corresponding authors.

References

  1. Barabasz W, Albinska D, Jaskowska M, Lipiec J (2002) Ecotoxicology of aluminium. Pol J Environ Stud 11(3):199–204

    CAS  Google Scholar 

  2. Viaroli S, Cuoco E, Mazza R, Tedesco D (2016) Dynamics of natural contamination by aluminium and iron rich colloids in the volcanic aquifers of Central Italy. Environ Sci Pollut Res 23:19958–19977

    Article  CAS  Google Scholar 

  3. Alabi OA, Adeoluwa YM (2020) Production usage, and potential public health effects of aluminum cookware: a review. Ann Sci Technol 5(1):20–30

    Article  Google Scholar 

  4. Botté A, Zaidi M, Guery J, Fichet D, Leignel V (2022) Aluminium in aquatic environments: abundance and ecotoxicological impacts. Aquat Ecol 56(3):751–773

    Article  Google Scholar 

  5. Namieśnik J, Rabajczyk A (2010) The speciation and physico-chemical forms of metals in surface waters and sediments. Chem Speciat Bioavailab 22(1):1–24

    Article  Google Scholar 

  6. Haridevamuthu B, Raj D, Kesavan D, Muthuraman S, Kumar RS, Mahboob S, Al-Ghanim KA, Almutairi BO et al (2023) Trihydroxy piperlongumine protects aluminium induced neurotoxicity in zebrafish: behavioral and biochemical approach. Comp Biochem Physiol C: Toxicol Pharmacol 268:109600

  7. Allin C, Wilson R (2000) Effects of pre-acclimation to aluminium on the physiology and swimming behaviour of juvenile rainbow trout (Oncorhynchus mykiss) during a pulsed exposure. Aquat Toxicol 51(2):213–224

    Article  CAS  PubMed  Google Scholar 

  8. Monaco A, Grimaldi M, Ferrandino I (2017) Aluminium chloride-induced toxicity in zebrafish larvae. J Fish Dis 40(5):629–635fish rearing: a case report. Vet Med 59(11):

    Article  CAS  PubMed  Google Scholar 

  9. Slaninova A, Machova J, Svobodova Z (2014) Fish kill caused by aluminium and iron contamination in a natural pond used for fish rearing: a case report. Vet Med 59(11):573–581

  10. Rondeau V, Jacqmin-Gadda H, Commenges D, Helmer C, Dartigues J-F (2009) Aluminum and silica in drinking water and the risk of Alzheimer’s disease or cognitive decline: findings from 15-year follow-up of the PAQUID cohort. Am J Epidemiol 169(4):489–496

    Article  PubMed  Google Scholar 

  11. Maya S, Prakash T, Madhu KD, Goli D (2016) Multifaceted effects of aluminium in neurodegenerative diseases: a review. Biomed Pharmacother 83:746–754

    Article  CAS  PubMed  Google Scholar 

  12. Closset M, Cailliau K, Slaby S, Marin M (2021) Effects of aluminium contamination on the nervous system of freshwater aquatic vertebrates: a review. Int J Mol Sci 23(1):31

    Article  PubMed  PubMed Central  Google Scholar 

  13. Suryavanshi J, Prakash C, Sharma D (2022) Asiatic acid attenuates aluminium chloride-induced behavioral changes, neuronal loss and astrocyte activation in rats. Metab Brain Dis 37(6):1773–1785

    Article  CAS  PubMed  Google Scholar 

  14. Di Liegro CM, Schiera G, Proia P, Di Liegro I (2019) Physical activity and brain health. Genes 10(9):720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Cariati I, Bonanni R, Pallone G, Scimeca M, Frank C, Tancredi V, D’Arcangelo G (2021) Hippocampal adaptations to continuous aerobic training: a functional and ultrastructural evaluation in a young murine model. J Funct Morphol Kinesiol 6(4):101

    Article  PubMed  PubMed Central  Google Scholar 

  16. Müller P, Duderstadt Y, Lessmann V, Müller NG (2020) Lactate and BDNF: key mediators of exercise induced neuroplasticity? J Clin Med 9(4):1136

    Article  PubMed  PubMed Central  Google Scholar 

  17. Chang Y-K, Labban JD, Gapin JI, Etnier JL (2012) The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res 1453:87–101

    Article  CAS  PubMed  Google Scholar 

  18. Lloyd BA, Hake HS, Ishiwata T, Farmer CE, Loetz EC, Fleshner M, Bland ST, Greenwood BN (2017) Exercise increases mTOR signaling in brain regions involved in cognition and emotional behavior. Behav Brain Res 323:56–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Takei N, Inamura N, Kawamura M, Namba H, Hara K, Yonezawa K, Nawa H (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24(44):9760–9769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Martins BT, Correia da Silva M, Pinto M, Cidade H, Kijjoa A (2019) Marine natural flavonoids: chemistry and biological activities. Nat Prod Res 33(22):3260–3272

    Article  CAS  PubMed  Google Scholar 

  21. Hajibabaie F, Abedpoor N, Taghian F, Safavi K (2023) A cocktail of polyherbal bioactive compounds and regular mobility training as senolytic approaches in age-dependent Alzheimer’s: the in silico analysis, lifestyle intervention in old age. J Mol Neurosci 73(2-3):171–184

    Article  CAS  PubMed  Google Scholar 

  22. Senger MR, Seibt KJ, Ghisleni GC, Dias RD, Bogo MR, Bonan CD (2011) Aluminum exposure alters behavioral parameters and increases acetylcholinesterase activity in zebrafish (Danio rerio) brain. Cell Biol Toxicol 27:199–205

    Article  CAS  PubMed  Google Scholar 

  23. Brodeur JC, Økland F, Finstad B, Dixon DG, McKinley RS (2001) Effects of subchronic exposure to aluminium in acidic water on bioenergetics of Atlantic salmon (Salmo salar). Ecotoxicol Environ Saf 49(3):226–234

    Article  CAS  PubMed  Google Scholar 

  24. DePasquale C, Leri J (2018) The influence of exercise on anxiety-like behavior in zebrafish (Danio rerio). Behav Process 157:638–644

    Article  CAS  Google Scholar 

  25. Palstra AP, Tudorache C, Rovira M, Brittijn SA, Burgerhout E, Van den Thillart GE, Spaink HP, Planas JV (2010) Establishing zebrafish as a novel exercise model: swimming economy, swimming-enhanced growth and muscle growth marker gene expression. PLoS One 5(12):e14483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhao L, Wang J-L, Liu R, Li X-X, Li J-F, Zhang L (2013) Neuroprotective, anti-amyloidogenic and neurotrophic effects of apigenin in an Alzheimer’s disease mouse model. Molecules 18(8):9949–9965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yamanaka O, Takeuchi R (2018) UMATracker: an intuitive image-based tracking platform. J Exp Biol 221(16):jeb182469

    Article  PubMed  Google Scholar 

  28. Haridevamuthu B, Manjunathan T, Guru A, Alphonse CRW, Boopathi S, Murugan R, Gatasheh MK, Hatamleh AA et al (2022) Amelioration of acrylamide induced neurotoxicity by benzo [b] thiophene analogs via glutathione redox dynamics in zebrafish larvae. Brain Res 1788:147941

    Article  CAS  PubMed  Google Scholar 

  29. Boopathi S, Haridevamuthu B, Mendonca E, Gandhi A, Priya PS, Alkahtani S, Al-Johani NS, Arokiyaraj S et al (2023) Combined effects of a high-fat diet and polyethylene microplastic exposure induce impaired lipid metabolism and locomotor behavior in larvae and adult zebrafish. Sci Total Environ 902:165988

    Article  CAS  PubMed  Google Scholar 

  30. Boopathi S, Haridevamuthu B, Gandhi A, Nayak S, Sudhakaran G, Rajakrishnan R, Arokiyaraj S, Arockiaraj J (2023) Neurobehavioral impairments from chromium exposure: insights from a zebrafish model and drug validation. Comp Biochem Physiol Part - C: Toxicol Pharmacol 275:109780

  31. Ngoc Hieu BT, Ngoc Anh NT, Audira G, Juniardi S, Liman RAD, Villaflores OB, Lai Y-H, Chen J-R et al (2020) Development of a modified three-day T-maze protocol for evaluating learning and memory capacity of adult zebrafish. Int J Mol Sci 21(4):1464

    Article  PubMed  PubMed Central  Google Scholar 

  32. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47(3):469–474

    Article  CAS  PubMed  Google Scholar 

  33. Ganie SA, Haq E, Hamid A, Qurishi Y, Mahmood Z, Zargar BA, Masood A, Zargar MA (2011) Carbon tetrachloride induced kidney and lung tissue damages and antioxidant activities of the aqueous rhizome extract of Podophyllum hexandrum. BMC Complement Altern Med 11(1):1–10

    Article  Google Scholar 

  34. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  PubMed  Google Scholar 

  35. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  Google Scholar 

  36. Ellerby LM, Bredesen DE (2000) Measurement of cellular oxidation, reactive oxygen species, and antioxidant enzymes during apoptosis. Methods Enzymol 322:413–421

    Article  CAS  PubMed  Google Scholar 

  37. Capriello T, Felix LM, Monteiro SM, Santos D, Cofone R, Ferrandino I (2021) Exposure to aluminium causes behavioural alterations and oxidative stress in the brain of adult zebrafish. Environ Toxicol Pharmacol 85:103636

    Article  CAS  PubMed  Google Scholar 

  38. Waring C, Brown J, Collins J, Prunet P (1996) Plasma prolactin, cortisol, and thyroid responses of the brown trout (Salmo trutta) exposed to lethal and sublethal aluminium in acidic soft waters. Gen Comp Endocrinol 102(3):377–385

    Article  CAS  PubMed  Google Scholar 

  39. Monette MY, McCormick SD (2008) Impacts of short-term acid and aluminum exposure on Atlantic salmon (Salmo salar) physiology: a direct comparison of parr and smolts. Aquat Toxicol 86(2):216–226

    Article  CAS  PubMed  Google Scholar 

  40. Wang D, He Y, Liang J, Liu P, Zhuang P (2013) Distribution and source analysis of aluminum in rivers near Xi’an City, China. Environ Monit Assess 185:1041–1053

    Article  CAS  PubMed  Google Scholar 

  41. Takatsu A, Ezoe Y, Eyama S, Uchiumi A, Tsunoda K-i, Satake K (2000) Aluminum in lake water and organs of a fish Tribolodon hakonensis in strongly acidic lakes with a high aluminum concentration. Limnology 1:185–189

    Article  CAS  Google Scholar 

  42. Filipek LH, Nordstrom DK, Ficklin WH (1987) Interaction of acid mine drainage with waters and sediments of West Squaw Creek in the West Shasta Mining District. California Environ sci tech 21(4):388–396

    Article  CAS  Google Scholar 

  43. S-Y Y, Gil-Mohapel J, Christie BR, So K-F (2014) Physical exercise-induced adult neurogenesis: a good strategy to prevent cognitive decline in neurodegenerative diseases? BioMed res int 2014:1–20

  44. Liu Y, Yan T, Chu JM-T, Chen Y, Dunnett S, Ho Y-S, Wong GT-C, Chang RC-C (2019) The beneficial effects of physical exercise in the brain and related pathophysiological mechanisms in neurodegenerative diseases. Lab Investig 99(7):943–957

    Article  PubMed  Google Scholar 

  45. Sinclair EL, de Souza CRN, Ward AJ, Seebacher F (2014) Exercise changes behaviour. Funct Ecol 28(3):652–659

    Article  Google Scholar 

  46. Nabavi SF, Khan H, D'onofrio G, Šamec D, Shirooie S, Dehpour AR, Argüelles S, Habtemariam S et al (2018) Apigenin as neuroprotective agent: of mice and men. Pharmacol Res 128:359–365

    Article  PubMed  Google Scholar 

  47. Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, Elkhayat SI, Bartels BK et al (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205(1):38–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Schnörr S, Steenbergen P, Richardson M, Champagne D (2012) Measuring thigmotaxis in larval zebrafish. Behav Brain Res 228(2):367–374

    Article  PubMed  Google Scholar 

  49. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S et al (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci 108(7):3017–3022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Abedpoor N, Taghian F, Hajibabaie F (2022) Cross brain–gut analysis highlighted hub genes and LncRNA networks differentially modified during leucine consumption and endurance exercise in mice with depression-like behaviors. Mol Neurobiol 59(7):4106–4123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Faria M, Valls A, Prats E, Bedrossiantz J, Orozco M, Porta JM, Gómez-Oliván LM, Raldúa D (2019) Further characterization of the zebrafish model of acrylamide acute neurotoxicity: gait abnormalities and oxidative stress. Sci Rep 9(1):7075

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bedrossiantz J, Bellot M, Dominguez-García P, Faria M, Prats E, Gomez-Canela C, Lopez-Arnau R, Escubedo E et al (2021) A zebrafish model of neurotoxicity by binge-like methamphetamine exposure. Frontiers in pharmacology 12:770319

  53. Saverino C, Gerlai R (2008) The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav Brain Res 191(1):77–87

    Article  PubMed  PubMed Central  Google Scholar 

  54. Gerlai R (2014) Social behavior of zebrafish: from synthetic images to biological mechanisms of shoaling. J Neurosci Methods 234:59–65

    Article  PubMed  Google Scholar 

  55. Fontana BD, Stefanello FV, Mezzomo NJ, Müller TE, Quadros VA, Parker MO, Rico EP, Rosemberg DB (2018) Taurine modulates acute ethanol-induced social behavioral deficits and fear responses in adult zebrafish. J Psychiatr Res 104:176–182

    Article  PubMed  Google Scholar 

  56. Shapiro T, Hertzig ME (1991) Social deviance in autism: a central integrative failure as a model for social nonengagement. Psychiatr Clin N Am 14:19–32

  57. Gutiérrez HC, Vacca I, Schoenmacker G, Cleal M, Tochwin A, O’connor B, Young AM, Vasquez AA et al (2020) Screening for drugs to reduce zebrafish aggression identifies caffeine and sildenafil. Eur Neuropsychopharmacol 30:17–29

    Article  PubMed  Google Scholar 

  58. Exley C (2004) The pro-oxidant activity of aluminum. Free Radic Biol Med 36(3):380–387

    Article  CAS  PubMed  Google Scholar 

  59. Soreq H, Seidman S (2001) Acetylcholinesterase—new roles for an old actor. Nat Rev Neurosci 2(4):294–302

    Article  CAS  PubMed  Google Scholar 

  60. Prakash A, Kumar AJB (2009) Effect of N-acetyl cysteine against aluminium-induced cognitive dysfunction and oxidative damage in rats. Basic Clin Pharmacol Toxicol 105(2):98–104

    Article  CAS  PubMed  Google Scholar 

  61. Kaviani E, Hajibabaie F, Abedpoor N, Safavi K, Ahmadi Z, Karimy A (2023) System biology analysis to develop diagnostic biomarkers, monitoring pathological indexes, and novel therapeutic approaches for immune targeting based on maggot bioactive compounds and polyphenolic cocktails in mice with gastric cancer. Environ Res 238:117168

    Article  CAS  PubMed  Google Scholar 

  62. Gonçalves FM, Neis VB, Rieger DK, Peres TV, Lopes MW, Heinrich IA, Costa AP, Rodrigues ALS et al (2017) Glutamatergic system and mTOR-signaling pathway participate in the antidepressant-like effect of inosine in the tail suspension test. J Neural Transm 124:1227–1237

    Article  PubMed  Google Scholar 

  63. Berchtold NC, Castello N, Cotman CW (2010) Exercise and time-dependent benefits to learning and memory. Neuroscience 167(3):588–597

    Article  CAS  PubMed  Google Scholar 

  64. Prema A, Justin Thenmozhi A, Manivasagam T, Mohamed Essa M, Guillemin GJ (2017) Fenugreek seed powder attenuated aluminum chloride-induced tau pathology, oxidative stress, and inflammation in a rat model of Alzheimer’s disease. J Alzheimers Dis 60(s1):S209–S220

    Article  CAS  PubMed  Google Scholar 

  65. Shang N, Zhang P, Wang S, Chen J, Fan R, Chen J, Huang T, Wang Y et al (2020) Aluminum-induced cognitive impairment and PI3K/Akt/mTOR signaling pathway involvement in occupational aluminum workers. Neurotox Res 38:344–358

    Article  CAS  PubMed  Google Scholar 

  66. Gao X, Zhang P, Chen J, Zhang L, Shang N, Chen J, Fan R, Wang Y et al (2022) Necrostatin-1 relieves learning and memory deficits in a zebrafish model of Alzheimer’s disease induced by aluminum. Neurotox Res 40(1):198–214

    Article  CAS  PubMed  Google Scholar 

  67. Li H, Xue X, Li L, Li Y, Wang Y, Huang T, Wang Y, Meng H et al (2020) Aluminum-induced synaptic plasticity impairment via PI3K-Akt-mTOR signaling pathway. Neurotox Res 37:996–1008

    Article  CAS  PubMed  Google Scholar 

  68. Chen G-f, Xu T-h, Yan Y, Zhou Y-r, Jiang Y, Melcher K, Xu HE (2017) Amyloid beta: structure, biology and structure-based therapeutic development. Acta Pharmacol Sin 38(9):1205–1235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Herukka S-K, Hallikainen M, Soininen H, Pirttilä T (2005) CSF Aβ42 and tau or phosphorylated tau and prediction of progressive mild cognitive impairment. Neurology 64(7):1294–1297

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Researchers Supporting Project Number (RSPD2024R691), King Saud University, Riyadh, Saudi Arabia. Dr. T.T. Ajith Kumar acknowledges The Director, NBFGR, Lucknow for the support he received to complete this study.

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Authors and Affiliations

  1. Toxicology and Pharmacology Laboratory, Department of Biotechnology, Faculty of Science and Humanities, SRM Institute of Science and Technology, Kattankulathur, Tamil Nadu, Chengalpattu District, 603203, India

    Seenivasan Boopathi, Edrea Mendonca, Akash Gandhi & Jesu Arockiaraj

  2. Department of Zoology, College of Science, King Saud University, P. O. Box 2455, Riyadh, 11451, Saudi Arabia

    Ahmed Rady

  3. Biochemistry Department, Faculty of Science Ain Shams University, Abbasaya, P.O. Box, Cairo, 11566, Egypt

    Noura M. Darwish

  4. Department of Food Science & Biotechnology, Sejong University, Seoul, 05006, Korea

    Selvaraj Arokiyaraj

  5. ICAR National Bureau of Fish Genetic Resources (NBFGR), Lucknow, Uttar Pradesh, 226002, India

    Thipramalai Thankappan Ajith Kumar

  6. Department of Biotechnology, Faculty of Engineering and Technology, School of Bioengineering, SRM Institute of Science and Technology, Kattankulathur, Tamil Nadu, Chengalpattu District, 603203, India

    Raman Pachaiappan

  7. Department of Cariology, Saveetha Dental College and Hospitals, Saveetha Institute of Medical and Technical Sciences, Saveetha University, Chennai, Tamil Nadu, 600 077, India

    Ajay Guru

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  1. Seenivasan Boopathi
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Contributions

BS: conceptualisation, formal analysis, investigation, methodology, visualisation, and writing—original draft; EM and AG: formal analysis and methodology; AR, NMD, SA, TTAK, and RP: formal analysis, resources, visualisation, and writing—original draft and editing; and AG and JA: conceptualisation, formal analysis, methodology, project administration, resources, supervision, visualisation, and writing—original draft and editing

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Correspondence to Ajay Guru or Jesu Arockiaraj.

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Boopathi, S., Mendonca, E., Gandhi, A. et al. Exploring the Combined Effect of Exercise and Apigenin on Aluminium-Induced Neurotoxicity in Zebrafish. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-03913-2

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