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Antioxidant effect of Spirulina (Arthrospira) maxima in a neurotoxic model caused by 6-OHDA in the rat striatum

  • Translational Neurosciences - Original Article
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Abstract

There is evidence to support that an impaired energy metabolism and the excessive generation of reactive oxygen species (ROS) contribute to brain injury in neurodegenerative disorders such as Parkinson’s disease (PD), whereas diets enriched in foods with an antioxidant action may modulate its progression. Several studies have proved that the antioxidant components produced by Spirulina, a microscopic blue-green alga, might prevent cell death by decreasing free radicals, inhibiting lipoperoxidation and upregulating the antioxidant enzyme systems. In our study, we investigated the protective effect of the Spirulina maxima (S. maxima) against the 6-OHDA-caused toxicity in the rat striatum. The S. maxima (700 mg/kg/day, vo) was administered for 40 days before and 20 days after a single injection of 6-OHDA (16 μg/2 μL) into the dorsal striatum. At 20-day postsurgery, the brain was removed and the striatum was obtained to evaluate the indicators of toxicity, such as nitric oxide levels, ROS formation, lipoperoxidation, and mitochondrial activity. These variables were found significantly stimulated in 6-OHDA-treated rats and were accompanied by declines in dopamine levels and motor activity. In contrast, the animals that received the chronic treatment with S. maxima had a restored locomotor activity, which is associated with the decreased levels of nitric oxide, ROS, and lipoperoxidation in the striatum, although mitochondrial functions and dopamine levels remained preserved. These findings suggest that supplementation with antioxidant phytochemicals (such as contained in S. maxima) represents an effective neuroprotective strategy against 6-OHDA-caused neurotoxicity vía free radical production to preserve striatal dopaminergic neurotransmission in vivo.

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References

  • Beckman JS (1996) Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9(5):836–844

    Article  CAS  PubMed  Google Scholar 

  • Belay A (2002) The potential application of Spirulina (Arthrospira) as a nutritional and therapeutic supplement in health management. J Am Nutr Assoc 5:27–48

    Google Scholar 

  • Blandini F, Armentero MT, Martignoni E (2008) The 6-hydroxydopamine model: news from the past. Parkinsonism Relat Disord 14:S124–S129

    Article  PubMed  Google Scholar 

  • Blum D, Torch S, Lambeng N, Nissou MF, Benabid AL, Sadoul R, Verna JM (2001) Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson’s disease. Prog Neurobiol 65:135–172

    Article  CAS  PubMed  Google Scholar 

  • Chamorro G, Salazar M, Araújo KG, dos Santon CP, Ceballos G, Castillo LF (2002) Update on the pharmacology of Spirulina (Arthrospira), an unconventional food. Arch Latinoam Nutr 52:232–240

    PubMed  Google Scholar 

  • Chamorro G, Perez-Albatier M, Serrano-Garcia N, Mares-Samano JJ, Rojas P (2006) Spirulina maxima pretreatment partially protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Nutr Neurosc 9:207–212

    Article  Google Scholar 

  • Chopra K, Bishnoi M (2008) Antioxidant profile of Spirulina: a blue-green microalga. In: Spirulina in human nutrition and health. CRC press, Boca Raton, pp 101–118

  • Cools AR, Brachten R, Heeren D, Willemen A, Ellenbroek B (1990) Search after neurobiological profile of individual-specific features of Wistar rats. Brain Res Bull 24:49–69

    Article  CAS  PubMed  Google Scholar 

  • Costa G, Abin-Carriquiry JA, Dajas F (2001) Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra. Brain Res 888(2):336–342

    Article  CAS  PubMed  Google Scholar 

  • Dauer W, Przedborski S (2009) Parkinson’s disease: mechanisms and models. Neuron 39:889–909

    Article  Google Scholar 

  • Gandhi S, Wood NW (2005) Molecular pathogenesis of Parkinson’s disease. Hum Mol Genet 14:2749–2755

    Article  Google Scholar 

  • Garcia E, Rios C, Sotelo J (1992) Ventricular injection of nerve growth factor increases dopamine content in the striata of MPTP-treated mice. Neurochem Res 17(10):972–982

    Article  Google Scholar 

  • Garcia E, Limon D, Perez-de la Cruz V, Giordano M, Diaz-Muños M, Maldonado PD, Herrera-Mundo MN, Pedraza-Chaverrí J, Santamaría A (2008) Lipid peroxidation, mitocondrial dysfunction and neurochemical and behavioural déficits in different neurotoxic models: protective role of S-allylcysteine. Free Radic Res 42(10):892–902

    Article  CAS  PubMed  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and (15) nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  PubMed  Google Scholar 

  • Greenamyre JT, Hastings TG (2004) Biomedicine. Parkinson’s divergent causes, convergent mechanisms. Science 304:1120–1122

    Article  CAS  PubMed  Google Scholar 

  • Grünblatt E, Mandel S, Youdim MB (2000) MPTP and 6-hydroxydopamine-induced neurodegeneration as models for Parkinson’s disease: neuroprotective strategies. J Neurol 247(2):II95–II102

    PubMed  Google Scholar 

  • Haleagrahara N, Siew CJ, Mitra NK, Kumari M (2011) Neuroprotective effect of bioflavonoid quercetin in 6-hydroxydopamine-induced oxidative stress biomarkers in the rat striatum. Neurosci Lett 500:139–143

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Guo BJ, Wong RNS, Jiang Y (2007) Characterization and antioxidant activity of selenium-containing phycocyanin isolated from Spirulina platensis. Food Chem 100:1137–1143

    Article  CAS  Google Scholar 

  • Hudson JL, van Horne CG, Strômberg I, Brock S, Clayton J, Masserano J, Hoffer BJ, Gerhardt GA (1993) Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res 626(1–2):167–174

    Article  CAS  PubMed  Google Scholar 

  • Karadeniz A, Yildirim A, Simsek N, Kalkan Y, Celebi F (2008) Spirulina platensis protects against gentamicin-induced nephrotoxicity in rats. Phytother Res 22:1506–1510

    Article  PubMed  Google Scholar 

  • Karadeniz A, Cemek M, Simsek N (2009) The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats. Ecotoxicol Environ Saf 72:231–235

    Article  CAS  PubMed  Google Scholar 

  • Kulshreshtha A, Zacharia AJ, Jarouliya U, Bhadauriya P, Prasad GB, Bisen PS (2008) Spirulina in health care management. Curr Pharm Biotechnol 9:400–405

    Article  CAS  PubMed  Google Scholar 

  • Lang AE, Lozano AM (1998a) Parkinson’s disease. First of two parts. N Engl J Med 339:1044–1053

    Article  CAS  PubMed  Google Scholar 

  • Lang AE, Lozano AM (1998b) Parkinson’s disease. Second of two parts. N Engl J Med 339:1130–1143

    Article  CAS  PubMed  Google Scholar 

  • Liberatore GT, Finkelstein DI, Wong JY, Horne MK, Porrit MJ, Donnan GA, Howells DW (1999) Sprouting of dopaminergic axons after striatal injury: confirmation by markers not dependent on dopamine metabolism. Exp Neurol 159(2):565–573

    Article  CAS  PubMed  Google Scholar 

  • Limon ID, Mendieta L, Díaz A, Chamorro G, Espinosa B, Zenteno E, Guevara J (2009) Neuroprotective effect of alpha-asarone on spatial memory and nitric oxide levels in rats injected with amyloid-beta ((25–35)). Neurosci Lett 453:98–103

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Middelton FA, Strick PL (2000) Basal ganglia and cerebellar loops motor and cognitive circuit. Brain Res 31:236–250

    Article  Google Scholar 

  • Miller RL, James-Kracke M, Sun GY, Sun AY (2009) Oxidative and inflammatory pathways in Parkinson’s disease. Neurochem Res 34:55–65

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  PubMed  Google Scholar 

  • Ottoni EB (2000) EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Methods Instrum Comput 32:446–449

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, USA

    Google Scholar 

  • Ponce-Canchihuaman JC, Perez-Mendez O, Hernandez-Munoz R, Torres-Duran PV, Juarez-Oropeza MA (2010) Protective effects of Spirulina maxima on hyperlipidaemia and oxidative-stress induced by lead acetate in the liver and kidney. Lipids Health Dis 9:35

    Article  PubMed  Google Scholar 

  • Reddy CM, Bhat VB, Kiranmai G, Reddy MN, Reddanna P, Madyastha KM (2000) Selective inhibition of cyclooxygenase-2 by C-phycocyanin, a biliprotein from Spirulina platensis. Biochem Biophys Res Commun 277:599–603

    Article  CAS  PubMed  Google Scholar 

  • Rimbau V, Camins A, Romav C, Gonzalez R, Pallas M (1999) Protective effect of c-phycocyanin against kainic acid induced neural damage in rat hippocampus. Neurosci Lett 276:75–78

    Article  CAS  PubMed  Google Scholar 

  • Robinson TE, Mocsary Z, Camp DM, Whishaw IQ (1994) Time course of recovery of extracellular dopamine following partial damage to the nigrostriatal dopamine system. J Neurosci 14(5 Pt 1):2687–2696

    CAS  PubMed  Google Scholar 

  • Romay Ch, Gonzalez R, Ledon N, Remirez D, Rimbau V (2003) C-Phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4:207–216

    Article  CAS  PubMed  Google Scholar 

  • Santamaría A, Flores-Escartín A, Martínez JC, Osorio L, Galván-Arzate S, Pedraza-Chaverrí J, Maldonado PD, Medina-Campos ON, Jiménez-Capdeville ME, Manjarrez J, Ríos C (2003) Copper blocks quinolinic acid neurotoxicity in rats: contribution of antioxidant systems. Free Radic Biol Med 35:418–427

    Article  PubMed  Google Scholar 

  • Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39:777–787

    Article  CAS  PubMed  Google Scholar 

  • Simola N, Morelli M, Carta AR (2007) The 6-hydroxydopamine model of Parkinson’s disease. Neurotox Res 11:151–167

    Article  CAS  PubMed  Google Scholar 

  • Strömberg I, Gemma C, Vila J, Bickford PC (2005) Blueberry- and Spirulina-enriched diets enhance striatal dopamine recovery and induce a rapid, transient microglia activation after injury of the rat nigrostriatal dopamine system. Exp Neurol 196:298–307

    Article  PubMed  Google Scholar 

  • Thaakur SR, Jyothi B (2007) Effect of Spirulina maxima on the haloperidol induced tardive dyskinesia and oxidative stress in rats. J Neural Transm 114:1217–1225

    Article  CAS  PubMed  Google Scholar 

  • Tobón-Velasco JC, Carmona-Aparicio L, Ali SF, Santamaría A (2010) Biomarkers of cell damage induced by oxidative stress in Parkinson’s disease and related models. Cent Nerv Syst Agents Med Chem 10:278–286

    Article  PubMed  Google Scholar 

  • Ungerstedt U, Arbuthnott GW (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24:485–493

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Chen T, Jiang J, Wong YS, Yang F, Zheng W (2011) Selenium-containing allophycocyanin purified from selenium-enriched Spirulina platensis attenuates AAPH-induced oxidative stress in human erythrocytes through inhibition of ROS generation. J Agric Food Chem 59:8683–8690

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partially supported by (LNAB1-08-11), VIEP-BUAP NAT 2010-2012 and CONACYT (169023-2011) given to D.L. The authors of this article declare no conflict of interest. Thanks to Dr. Ellis Glazier for editing this English-language text.

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Authors and Affiliations

  1. Laboratorio de Neurofarmacología, Departamento de Farmacia, Edificio 105 C, Facultad de Ciencias Químicas, Benemérita Universidad Autónoma de Puebla, 72570, Puebla, Mexico

    J. C. Tobón-Velasco, Victoria Palafox-Sánchez, Liliana Mendieta & I. Daniel Limón

  2. Laboratorio de Neuroinmunología, Instituto Nacional de Neurología y Neurocirugía, Manuel Velasco Suárez, SSA, 14264, Mexico, DF, Mexico

    E. García

  3. Laboratorio de Aminoácidos Excitadores, Instituto Nacional de Neurología y Neurocirugía, Manuel Velasco Suárez, SSA, 14264, Mexico, DF, Mexico

    J. C. Tobón-Velasco & A. Santamaría

  4. Laboratorio de Toxicología Pre-clínica, Departamento de Farmacia, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Av. Wilfrido Massieu s/n. Adolfo López Mateos Del. Gustavo A. Madero, 07738, Mexico, DF, Mexico

    G. Chamorro-Cevallos

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  1. J. C. Tobón-Velasco
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  2. Victoria Palafox-Sánchez
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  7. I. Daniel Limón
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Correspondence to I. Daniel Limón.

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J.C. Tobón-Velasco and V. Palafox-Sanchez contributed equally to this study and both are considered like first author.

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Tobón-Velasco, J.C., Palafox-Sánchez, V., Mendieta, L. et al. Antioxidant effect of Spirulina (Arthrospira) maxima in a neurotoxic model caused by 6-OHDA in the rat striatum. J Neural Transm 120, 1179–1189 (2013). https://doi.org/10.1007/s00702-013-0976-2

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  • DOI: https://doi.org/10.1007/s00702-013-0976-2

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