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Therapeutic and Protective Potency of Bee Pollen Against Neurotoxic Effects Induced by Prenatal Exposure of Rats to Methyl Mercury

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Abstract

MeHg is a widely distributed environmental toxicant with harmful effects on the developing and adult nervous system. This study aimed to evaluate the therapeutic and protective efficacy of pollen grain in improving the toxic effects of MeHg, through the measurement of selected biochemical parameters linked to oxidative stress, energy metabolism, and neurotransmission in brain homogenates of male pups’ neonates. Forty healthy pregnant female rats were randomly divided into five groups, and after delivery, each group was consisting of 10 male neonates: (1) neonates delivered by control mothers, (2) neonates delivered by bee pollen treated mothers who received bee pollen at the dose of 200-mg/kg body weight from postnatal day 0 for 4 weeks, (3) neonates delivered by MeHg-treated mothers who received MeHg at the dose of 0.5 mg/kg/day via drinking water from gestational day 7 till postnatal day 7 of delivery, (4) therapeutic group: neonates delivered by MeHg-treated mothers followed by bee pollen treatment who received bee pollen at the dose of 200-mg/kg body weight from postnatal day 0 for 4 weeks, and (5) protective group: neonates delivered by MeHg and bee pollen-treated mothers. Mothers continued receiving the bee pollen at the same dose until day 21. Biochemical parameters linked to oxidative stress and energy metabolism and neurotransmission were investigated in brain homogenates of neonates from all the five groups. MeHg treatment showed an increase in oxidative stress markers like lipid peroxidation and catalase activity coupled with a non-significant decrease in glutathione level. Impaired energy metabolism was ascertained via the inhibition of creatine kinase and lactate dehydrogenase activities. Dramatic decrease of Mg2+ and K+ concentrations confirmed the neurotransmission defect. Interestingly, the bee pollen treatment was highly effective in restoring the catalase, lactate dehydrogenase, and creatine kinase activities in addition to normalizing the levels of Mg2+, K+, lipid peroxidation, and glutathione. Overall, the exposure to MeHg during the developing brain stages was highly effective to show signs and symptoms of neuronal toxicity. Furthermore, it has been concluded that bee pollen can be used safely to ameliorate oxidative stress, poor detoxification as well as metal ion defects, and neuronal death as a critical mechanisms involved in the etiology of numerous neurological disorders.

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References

  • Aaseth J, Ajsuvakova OP, Skalny AV, Skalnaya MG, Tinkov AA (2018) Chelator combination as therapeutic strategy in mercury and lead poisonings. Coord Chem Rev 358:1–12

    Article  CAS  Google Scholar 

  • Al-Daihan S, Ben Bacha A El-Ansary A, Bhat RS (2018) Prenatal Bee Pollen Treatment Improves The Neurotoxicity In New Born Rats During Chronic Fluorides Exposure In Relation To Propionic Acid -Induced Rodent Models Of Autism Fluoride (in press)

  • Al-Dbass AM (2014) N-Acetylcysteine reduces the neurotoxic effects of propionic acid in rat pups. Journal of King Saud University - Science 26(4):254–260

    Article  Google Scholar 

  • Almaraz-Abarca N, Campos MDG, Ávila-Reyes JA, Naranjo-Jiménez N, Herrera-Corral J, González-Valdez LS (2004) Variability of antioxidant activity among honeybee-collected pollen of different botanical origin. Interciencia 29(10):574–578

    Google Scholar 

  • Amador E, Dorfman LE, Wacker WE (1963) Serum lactic dehydrogenase activity: an analytical assessment of current assays. Clin Chem 12:391–399

    PubMed  CAS  Google Scholar 

  • Ares AM, Valverde S, Bernal JL (2018) Extraction and determination of bioactive compounds from bee pollen. J Pharm Biomed Anal 147:110–124

    Article  PubMed  CAS  Google Scholar 

  • Aschner M, Farina M, Rocha JBT (2013) Mercury neurotoxicity. In: Kretsinger RH, Uversky VN, Permyakov EA (eds) Encycl. Meth. Springer, New York, pp 1362–1367

    Google Scholar 

  • Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    PubMed  CAS  Google Scholar 

  • Bjørklund G (2015) Selenium as an antidote in the treatment of mercury intoxication. Biometals 28:605–614

    Article  PubMed  CAS  Google Scholar 

  • Bjørklund G, Aaseth J, Ajsuvakova OP, Nikonorov AA, Anatoly V, Skalny AV, Skalnaya MG, Tinkov AA (2017a) Molecular interaction between mercury and selenium in neurotoxicity. Coord Chem Rev 332:30–37

    Article  CAS  Google Scholar 

  • Bjørklund G, Dadarb M, Mutterc J, Aaseth J (2017b) The toxicology of mercury: current research and emerging trends. Environ Res 159:545–554

    Article  PubMed  CAS  Google Scholar 

  • Bojes HK, Suresh PK, Mills EM, Spitz DR, Sim JE, Kehrer JP (1998) Bcl-2 and Bcl-xL in peroxide-resistant A549 and U87MG cells. Toxicol Sci 42(2):109–116

    PubMed  CAS  Google Scholar 

  • Chan HM, Scheuhammer AM, Ferran A, Loupelle C, Holloway J, Weech S (2010) Impacts of mercury on freshwater fish-eating wildlife and humans. Hum Ecol Risk Assess 9:867–883

    Article  Google Scholar 

  • Denisow B, Denisow-Pietrzyk M (2016) Biological and therapeutic properties of bee pollen: a review. J Sci Food Agric 96:4303–4309

    Article  PubMed  CAS  Google Scholar 

  • El-Ansary AK, Al-Daihan S, Ben Bacha A, Shaker GH, Al-Ayadhi LY (2013) Comparative study on the protective effect of carnosine and carnitine against pro-inflammatory/pro-oxidant effects of clindamycin and propionic acid administrations to hamsters. Afr J Microbiol Res 7(2):103–114

    Article  CAS  Google Scholar 

  • El-Ansary A, Al-Ayadhi L (2014) GABAergic/glutamatergic imbalance relative to excessive neuroinflammation in autism spectrum disorders. J Neuroinflammation 11:189

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El-Ansary A, Bhat RS, Al-Daihan S, Al Dbass AM (2015) The neurotoxic effects of ampicillin-associated gut bacterial imbalances compared to those of orally administered propionic acid in the etiology of persistent autistic features in rat pups: effects of various dietary regimens. Gut Pathog 7(1):7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El-Ansary A, Al-Salem HS, Asma A, Al-Dbass A (2017) Glutamate excitotoxicity induced by orally administered propionic acid, a short chain fatty acid can be ameliorated by bee pollen. Lipids Health Dis 16(1):96

    Article  PubMed  PubMed Central  Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal induced oxidative damage. Curr Top Med Chem 1:529–539

    Article  PubMed  CAS  Google Scholar 

  • Ferreira D, Unfer TC, Rocha HC, Kreutz LC, Koakoski G, Barcellos LJG (2012) Antioxidant activity of bee products added to water in tebuconazole-exposed fish. Neotrop Ichthyol 10(1):215–220

    Article  Google Scholar 

  • Frei B (1994) Reactive oxygen species and antioxidant vitamins: mechanisms of action. Am J Med 97:S5–S13

    Article  Google Scholar 

  • Galland L (1993) Magnesium, stress and neuropsychiatric disorders. Magnesium Trace Elem 10:287–287

    Google Scholar 

  • Geret F, Serafim A, Barreira L, Bebianno MJ (2002) Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus. Biomarkers 7(3):242–256

    Article  PubMed  CAS  Google Scholar 

  • Glaser V, Leipnitz G, Straliotto MR, Oliveira J, dos Santos VV, Wannmacher CM, de Bem AF, Rocha JB, Farina M, Latini A (2010) Oxidative stress-mediated inhibition of brain creatine kinase activity by methylmercury. Neurotoxicology 31(5):454–460

    Article  PubMed  CAS  Google Scholar 

  • Grandjean P, Pichery C, Bellanger M, Budtz-Jørgensen E (2012) Calculation of mercury’s effects on neurodevelopment. Environ Health Perspect 120(12):a452

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haley BE, Mutter J (2013) Mercury and Alzheimer’s disease. In: Kretsinger RH, Uversky VN, Permyakov EA (eds) Encycl. Met. Springer, New York, pp 1317–1324

    Google Scholar 

  • Hosseini SM, Vakili Azghandi M, Ahani S, Nourmohammadi R (2016) Effect of bee pollen and propolis (bee glue) on growth performance and biomarkers of heat stress in broiler chickens reared under high ambient temperature. J Anim Feed Sci 25(1):45–51

    Article  Google Scholar 

  • Hyslop PA, Zhang Z, Pearson DV, Phebus LA (1995) Measurement of striatal H2O2 by microdialysis following global forebrain ischemia and reperfusion in the rat: correlation with the cytotoxic potential of H2O2 in vitro. Brain Res 671(2):181–186

    Article  PubMed  CAS  Google Scholar 

  • Jafri AJA, Arfuzir NNN, Lambuk L, Iezhitsa I, Agarwal R, Agarwal P, Razali N, Krasilnikova A, Kharitonova M, Demidov V, Serebryansky E, Skalny A, Spasov A, Yusof APM, Ismail NM (2017) Protective effect of magnesium acetyltaurate against NMDA-induced retinal damage involves restoration of minerals and trace elements homeostasis. J Trace Elem Med Biol 39:147–154

    Article  PubMed  CAS  Google Scholar 

  • Khan MA, Wang F (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem 28(8):1567–77

    Article  PubMed  CAS  Google Scholar 

  • Komosinska-Vassev K, Olczyk P, Kaźmierczak J, Mencner L, Olczyk K (2015) Bee pollen: chemical composition and therapeutic application. Evid Based Complement Alternat Med 2015:297425

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroyer H (2001) Evaluation of bioactive properties of pollen extracts as functional dietary food supplement. Innovative Food Sci Emerg Technol 2(3):171–174

    Article  CAS  Google Scholar 

  • Krupp EM, Milne BF, Mestrot A, Meharg AA, Feldmann J (2008) Investigation into mercury bound to biothiols: structural identification using ESI–ion-trap MS and introduction of a method for their HPLC separation with simultaneous detection by ICP-MS and ESI–MS. Anal Bioanal Chem 390(7):1753–1764

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leonhardt R, Haas H, Büsselberg D (1996) Methyl mercury reduces voltage activated currents of rat dorsal root ganglion neurons. Naunyn Schmiedeberg’s Arch Pharmacol 354(4):532–538

    Article  CAS  Google Scholar 

  • Lin Y, Vogt R, Larssen T (2012) Environmental mercury in China: a review. Environ Toxicol Chem 31:2431–2444

    Article  PubMed  CAS  Google Scholar 

  • Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424

    PubMed  CAS  Google Scholar 

  • Marrero-Rosado B, Fox SM, Hannon HE, Atchison WD (2013) Mercury and lead, effects on voltage-gated calcium channel function. In: Kretsinger RH, Uversky VN, Permyakov EA (eds) Encycl meth. Springer, New York, pp 1336–1346

    Google Scholar 

  • Mieiro CL, Pereira E, Duarte AC, Pardal MA (2015) Mercury biomagnification in a contaminated estuary food web: effects of age and trophic position using stable isotope analyses. Mar Pollut Bull 97:488–493

    Article  PubMed  CAS  Google Scholar 

  • Nabi S, Ara A, Rizvi SJ (2011) Methylmercury chloride coaxed oxidative stress in rats. Iran J Pharmacol Ther 10(2):52–60

    CAS  Google Scholar 

  • Nutile-McMenemy N, Elfenbein A, Deleo JA (2007) Minocycline decreases in vitro microglial motility, beta1-integrin, and Kv1.3 channel expression. J Neurochem 103:2035–2046

    Article  PubMed  CAS  Google Scholar 

  • Pascoal A, Rodrigues S, Teixeira A, Feas X, Estev-inho LM (2014) Biological activities of commercial bee pollens: antimicrobial, antimutagenic, antioxidant and anti-inflammatory. Food Chem Toxicol 63:233–239

    Article  PubMed  CAS  Google Scholar 

  • Pletz J, Sánchez-Bayo F, Tennekes HA (2016) Dose–response analysis indicating time-dependent neurotoxicity caused by organic and inorganic mercuryimplications for toxic effects in the developing brain. Toxicology 347–349:1–5

    Article  PubMed  CAS  Google Scholar 

  • Puerto N, Prieto G, Castro R (2015) Chemical composition and antioxidant activity of pollen. Chilean J Agric Anim Sci 31:115–126

    Google Scholar 

  • Reyes RC, Brennan AM, Shen Y, Baldwin Y, Swanson RA (2012) Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes. J Neurosci 32:12973–12978

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ruiz-larrea B, Leal AM, Liza M, Lacort M, De Groot H (1994) Antioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsomes. Steroid 59:383–388

    Article  CAS  Google Scholar 

  • Sagara Y, Dargusch R, Chambers D, Davis J, Schubert D, Maher P (1998) Cellular mechanisms of resistance to chronic oxidative stress. Free Radic Biol Med 24(9):1375–1389

    Article  PubMed  CAS  Google Scholar 

  • Sattler JAG, de Melo AAM, do Nascimento KS, de Melo ILP, Mancini-Filho J, Sattler A, de Almeida-Muradian LB (2016) Essential minerals and inorganic contaminants (barium, cadmium, lithium, lead and vanadium) in dried bee pollen produced in Rio Grande do Sul state, Brazil. Food Sci Technol 36:505–509

    Article  Google Scholar 

  • Sen AP, Gulati A (2010) Use of magnesium in traumatic brain injury. Neurotherapeutics 7(1):91–99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Serefko A, Szopa A, Wlaź P, Nowak G, Radziwoń-Zaleska M, Skalski M, Poleszak E (2013) Magnesium in depression. Pharmacol Rep 65(3):547–554

    Article  PubMed  CAS  Google Scholar 

  • Sucher NJ, Lipton SA, Dreyer EB (1997) Molecular basis of glutamate toxicity in retinal ganglion cells. Vis Res 37:3483–3493

    Article  PubMed  CAS  Google Scholar 

  • Szasz G, Gruber W, Bernt E (1976) Creatine kinase in serum: 1. Determination of optimum reaction conditions. Clin Chem 22:650–656

    PubMed  CAS  Google Scholar 

  • Szczesna T (2007) Concentration of selected elements in honeybee-collected pollen. J Apic Sci 51(1):5–13

    Google Scholar 

  • Yang YM, Wang W, Fedchyshyn MJ, Zhou Z, Ding J, Wang LY (2014) Enhancing the fidelity of neurotransmission by activity dependent facilitation of presynaptic potassium currents. Nat Commun 5:4564

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This research project was supported by a grant from the Research Center of the Center for Female Scientific and Medical Colleges in King Saud University.

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Authors and Affiliations

  1. Department of Biochemistry, College of Science, King Saud University, P.O Box 22452, Riyadh, 11495, Saudi Arabia

    May Al-Osaimi, Sooad Al-Daihan, Ramesa Shafi Bhat & Abir Ben Bacha

  2. Central Laboratory, King Saud University, P.O Box 22452, Riyadh, 11495, Saudi Arabia

    Afaf El-Ansary

  3. Laboratory of Plant Biotechnology Applied to Crop Improvement, Faculty of Science of Sfax, University of Sfax, 3038, Sfax, Tunisia

    Abir Ben Bacha

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  1. May Al-Osaimi
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  2. Afaf El-Ansary
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  3. Sooad Al-Daihan
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  4. Ramesa Shafi Bhat
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  5. Abir Ben Bacha
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Contributions

MO and RB carried out the experimental work, AE and AB designed the study and draft the manuscript, and SD contributed to the interpretation of the results and the English polishing. All authors have read and agreed on this manuscript.

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Correspondence to Abir Ben Bacha.

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The authors declare that they have no conflict of interest.

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Significance Statement

Thanks to its antioxidative properties,bee pollen could be sugested as a protective and therapeutic strategy in case of MeHg neurotoxicity as an etiological factor linked to neurological disorders.

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Al-Osaimi, M., El-Ansary, A., Al-Daihan, S. et al. Therapeutic and Protective Potency of Bee Pollen Against Neurotoxic Effects Induced by Prenatal Exposure of Rats to Methyl Mercury. J Mol Neurosci 65, 327–335 (2018). https://doi.org/10.1007/s12031-018-1107-1

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  • DOI: https://doi.org/10.1007/s12031-018-1107-1

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