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Catuaba (Trichilia catigua) Prevents Against Oxidative Damage Induced by In Vitro Ischemia–Reperfusion in Rat Hippocampal Slices

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Abstract

Oxidative stress is implicated in brain damage associated with ischemia–reperfusion. Natural antioxidants found in some plants used in folk medicine have been indicated as potential neuroprotective agents. Here we investigated whether Trichilia catigua, a traditional Brazilian herbal medicine alleged to exhibit a variety of neuropharmacological properties (antidepressant, anti-neurasthenic, anti-inflammatory etc.), could have neuroprotective properties in rat hippocampal slices subjected to 2 h oxygen and glucose deprivation (OGD) followed by 1 h reperfusion. Ischemia–reperfusion (I/R) significantly decreased mitochondrial viability, increased dichlorofluorescein oxidation above control both in the incubation medium and slices homogenates, increased lactate dehydrogenase into the incubation medium and decreased non-protein thiols. T. catigua (40–100 μg/mL) protected slices from the deleterious effects of OGD when present before OGD and during the reperfusion periods. Oxidative stress in the medium was also determined under different conditions and the results demonstrated that T. catigua could not protect slices from I/R when it was added to the medium after ischemic insult. Although the translation to a real in vivo situation of I/R is difficult to be done, the results indicated that T. catigua should be used as preventive and not as a curative agent against brain damage.

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References

  1. Acker T, Acker H (2004) Cellular oxygen sensing need in CNS function: physiological and pathological implications. J Exp Biol 207:3171–3188

    Article  PubMed  CAS  Google Scholar 

  2. Rodrigo J, Fernández AP, Serrano J, Peinado MA, Martínez A (2005) The role of free radicals in cerebral hypoxia and ischemia. Free Radic Biol Med 39:26–50

    Article  PubMed  CAS  Google Scholar 

  3. Bolaños JP, Moro MA, Lizasoain I, Almeida A (2009) Mitochondria and reactive oxygen and nitrogen species in neurological disorders and stroke: therapeutic implications. Adv Drug Deliv Rev 61:1299–1315

    Article  PubMed  Google Scholar 

  4. Endres M, Dirnagl U, Moskowitz MA (2009) The ischemic cascade and mediators of ischemic injury. Handb Clin Neurol 92:31–41

    Article  PubMed  Google Scholar 

  5. Nicholls DG (2009) Mitochondrial calcium function and dysfunction in the central nervous system. Biochim Biophys Acta 1787:1416–1424

    Article  PubMed  CAS  Google Scholar 

  6. Cross JL, Meloni BP, Bakker AJ, Lee S, Knuckey NM (2010) Modes of neuronal calcium entry and homeostasis following cerebral ischemia. Stroke Res Treat. doi:10.4061/2010/316862

    PubMed  Google Scholar 

  7. Sara-Pérez A, Planas AM, Núñes-O′Mara A, Berra E, García-Villoria J, Ribes A, Santalucía T (2010) Extended ischemia prevents HIF-1α degradation at reoxygenation by impairing prolyl-hydroxylation: role of krebs cycle metabolites. J Biol Chem 285:18217–18224

    Article  Google Scholar 

  8. Yu CH, Moon CT, Sur JH, Chun YI, Choi WH, Yhee JY (2011) Serial expression of hypoxia inducible factor-1α and neuronal apoptosis in hippocampus of rats with chronic ischemic brain. J Korean Neurosurg Soc 50:481–485

    Article  PubMed  CAS  Google Scholar 

  9. Mc-Cord JM (1985) Oxygen-derivated free radicals in post-ischemic tissue injury. New Engl J Med 312:159–163

    Article  CAS  Google Scholar 

  10. Oka H, Kanemitsu H, Nihei H, Nakayama H, Tamura A, Sano K (1992) Change of xanthine dehydrogenase and xanthine oxidase activities in rat brain following complete ischaemia. Neurol Res 14:321–324

    PubMed  CAS  Google Scholar 

  11. Fellman V, Raivio KO (1997) Reperfusion injury as the mechanism of brain damage after perinatal asphyxia. Pediatr Res 41:599–606

    Article  PubMed  CAS  Google Scholar 

  12. Battelli MG, Buonamici L, Virgili M, Abbondanza A (1998) Simulated ischemia-reperfusion conditions increase dehydrogenase and oxidase activities in rat brain slices. Neurochem Int 32:17–21

    Article  PubMed  CAS  Google Scholar 

  13. Ghoneim AI, Abdel-Naim AB, Khalifa AE, El-Denshary ES (2002) Protective effects of curcumin against ischaemia/reperfusion insult in rat forebrain. Pharmacol Res 46:273–279

    Article  PubMed  CAS  Google Scholar 

  14. Berthet C, Lei H, Thenevet J, Gruetter R, Magistretti PJ, Hirt L (2009) Neuroprotective role of lactate after cerebral ischemia. J Cereb Blood Flow Metab 29:1780–1789

    Article  PubMed  CAS  Google Scholar 

  15. Kuang P, Tao Y, Tian Y (1996) Effect of radix Salviae miltiorrhizae on nitric oxide in cerebral ischemic-reperfusion injury. J Tradit Chin Med 16:224–227

    PubMed  CAS  Google Scholar 

  16. Thiyagarajan M, Sharma SS (2004) Neuroprotective effect of curcumin in middle cerebral ischemia in rats. Life Sci 74:969–985

    Article  PubMed  CAS  Google Scholar 

  17. Cai F, Li CR, Wu JL, Chen JG, Liu C, Min Q, Yu W, Ouyang CH, Chen JH (2006) Theaflavin ameliorates cerebral ischemia-reperfusion injury in rats through its anti-inflammatory effect and modulation of STAT-1. Mediators Inflamm. doi:10.1155/MI/2006/30490

    PubMed  Google Scholar 

  18. Wu P, Zhang Z, Wang F, Chen J (2010) Natural compounds from traditional medicinal herbs in the treatment of cerebral ischemia/reperfusion injury. Acta Pharmacol Sin 31:1523–1531

    Article  PubMed  CAS  Google Scholar 

  19. Bora KS, Sharma A (2011) Evaluation of antioxidant and cerebroprotective effect of Medicago sativum Linn. against ischemia and reperfusion insult. Evid Based Complement Alternat Med. doi:10.1093/ecam/neq019

    PubMed  Google Scholar 

  20. Wattanathorn J, Jittiwat J, Tongun T, Muchimapura S, Ingkaninan K (2011) Zingiber officinale mitigates brain damage and improves memory impairment in focal cerebral ischemic rat. Evid Based Complement Alternat Med. doi:10.1155/2011/429505

    Google Scholar 

  21. Sreelatha S, Padma PR (2009) Antioxidant activity and total phenolic content of Moringaoleifera leaves in two stages of maturity. Plant Foods Hum Nutr 64:303–311

    Article  PubMed  CAS  Google Scholar 

  22. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295

    PubMed  CAS  Google Scholar 

  23. Pereira RP, Fachinetto R, de Souza Prestes A, Puntel RL, Santos da Silva GN, Heinzmann BM, Boschetti TK, Athayde ML, Bürger ME, Morel AF, Morsch VM, Rocha JB (2009) Antioxidant effects of different extracts from Melissa officinalis, Matricaria recutita and Cymbopogon citratus. Neurochem Res 34:973–983

    Article  PubMed  CAS  Google Scholar 

  24. Sudati JH, Fachinetto R, Pereira RP, Boligon AA, Athayde ML, Soares FA, Barbosa NV, Rocha JB (2009) In vitro antioxidant activity of Valeriana officinalis against different neurotoxic agents. Neurochem Res 34:1372–1379

    Article  PubMed  CAS  Google Scholar 

  25. Wagner C, Vargas AP, Roos DH, Morel AF, Farina M, Nogueira CW, Aschner M, Rocha JB (2010) Comparative study of quercetin and its two glycoside derivatives quercitrin and rutin against methylmercury (MeHg)-induced ROS production in rat brain slices. Arch Toxicol 84:89–97

    Article  PubMed  CAS  Google Scholar 

  26. Ahmad S, Khan MB, Hoda MN, Bhatia K, Haque R, Fazili IS, Jamal A, Khan JS, Katare DP (2012) Neuroprotective effect of sesame seed oil in 6-Hydroxydopamine induced neurotoxicity in mice model: cellular, biochemical and neurochemical evidence. Neurochem Res 37:516–526

    Article  PubMed  CAS  Google Scholar 

  27. Essa MM, Vijayan RK, Castellano-Gonzalez G, Memon MA, Braidy N, Guillemin GJ (2012) Neuroprotective effect of natural product against Alzeimer′s disease. Neurochem Res. doi:10.1007/s11064-012-0799-9

    PubMed  Google Scholar 

  28. Viana AF, Maciel IS, Motta EM, Leal PC, Pianowski L, Campos MM, Calixto JB (2009) Antinociceptive activity of Trichilia catigua hydroalcoholic extract: new evidence on its dopaminergic effects. Evid Based Complement Alternat Med. doi:10.1093/ecam/nep144

    Google Scholar 

  29. Mendes FR, Carlini EA (2007) Brazilian plants as possible adaptogens: an ethnopharmacological survey of books edited in Brazil. J Ethnopharmacol 109:493–500

    Article  PubMed  Google Scholar 

  30. Antunes E, Gordo WM, de Oliveira JF, Teixeira CE, Hyslop S, De Nucci G (2001) The relaxation of isolated rabbit corpus cavernosum by the herbal medicine Catuama and its constituents. Phytother Res 15:416–421

    Article  PubMed  CAS  Google Scholar 

  31. Brighente IMC, Dias M, Verdi LG, Pizzolatti MG (2007) Antioxidant activity and total phenolic content of some Brazilian species. Pharmaceut Biol 45:156–161

    Article  CAS  Google Scholar 

  32. Pizzolattia MG, Vensona AF, Júnior AS, Smânia EFA, Braz-Filho R (2002) Two epimeric flavalignans from Trichilia catigua (Meliaceae) with antimicrobial activity. Z Naturforsch 57c:483–488

    Google Scholar 

  33. Campos MM, Fernandes ES, Ferreira J, Santos AR, Calixto JB (2005) Antidepressant-like effects of Trichilia catigua (Catuaba) extract: evidence for dopaminergic-mediated mechanisms. Psychopharmacol 182:45–53

    Article  CAS  Google Scholar 

  34. Chassot JM, Longhini R, Gazarini L, Mello JC, de Oliveira RM (2011) Preclinical evaluation of Trichilia catigua extracts on the central nervous system of mice. J Ethnopharmacol 137:1143–1148

    Article  PubMed  Google Scholar 

  35. Taciany BV, Micheli CJ, Longhini R, Milani H, Mello JC, de Oliveira RM (2012) Subchronic administration of Trichilia catigua ethyl-acetate fraction promotes antidepressant-like effects and increases hippocampal cell proliferation in mice. J Ethnopharmacol. doi:10.1016/j.ep.2012.06.021

    Google Scholar 

  36. Quintão NLM, Ferreira J, Beirith A, Campos MM, Calixto JB (2008) Evaluation of the effects of the herbal product catuama in inflammatory and neuropathic models of nociception in rats. Phytomedicine 15:245–252

    Article  PubMed  Google Scholar 

  37. Laghari AH, Memon S, Nelofar A, Khan KM, Yasmin A (2011) Determination of free phenolic acids and antioxidant activity of methanolic extracts obtained from fruits and leaves of Chenopodium album. Food Chem 126:1850–1855

    Article  CAS  Google Scholar 

  38. Pérez-Severiano P, Rodríguez-Pérez M, Pedraza-Chaverrí J, Maldonado PD, Medina Campos ON, Ortíz-Plata A, Sánchez-García A, Villeda-Hernández J, Galván-Arzate S, Aguilera P, Santamaría A (2004) S-allylcysteine, a garlic-derived antioxidant, ameliorates quinolinic acid-induced neurotoxicity and oxidative damage in rats. Neurochem Int 45:1175–1183

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  40. Siqueira I, Cimarosti H, Fochesatto C, Nunes D, Salbego C, Netto C (2004) Neuroprotective effects of Ptychopetalum olacoides Bentham (Olacaceae) on oxygen and glucose deprivation induced damage in rat hippocampal slices. Life Sci 75:1897–1906

    Article  PubMed  CAS  Google Scholar 

  41. David HN, Haelewyn B, Rouillon C, Lecoq M, Chazalviel L, Apiou G, Risso J, Lemaire M, Abraini JH (2008) Neuroprotective effects of xenon: a therapeutic window of opportunity in rats subjected to transient cerebral ischemia. FASEB J 22:1275–1286

    Article  PubMed  Google Scholar 

  42. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem 82:70–77

    Article  PubMed  CAS  Google Scholar 

  43. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  44. Kamdem JP, Stefanello ST, Boligon AA, Wagner C, Kade IJ, Pereira RP, Souza Preste A, Roos DH, Waczuck EP, Appel AS, Athayde ML, Souza DO, Rocha JBT (2012) In vitro antioxidant activity of stem bark of Trichilia catigua Adr. Juss (Meliaceae). Acta Pharm 62. doi:10.2478/v10007-012-0026-x

  45. Moro MA, De Alba J, Leza JC, Lorenzo P, Fernández AP, Bentura ML, Boscá L, Rodrigo J, Lizasoain I (1998) Neuronal expression of inducible nitric oxide synthase after oxygen and glucose deprivation in rat forebrain slices. Eur J Neurosci 10:445–456

    Article  PubMed  CAS  Google Scholar 

  46. De Alba J, Cárdenas A, Moro MA, Leza JC, Lorenzo P, Lizasoain I (1999) Use of brain slices in the study of pathogenic role of inducible nitric oxide synthase in cerebral ischemia-reperfusion. Gen Pharmacol 32:577–581

    Article  PubMed  Google Scholar 

  47. Rawal AK, Nath DK, Biswas SK (2008) Plausible mechanism of antioxidant action of Fagonia cretica linn, Rubia cordifolia and Tinospora cordifolia during ischemic reperfusion injury in rat hippocampus. Int J Applied Res Nat Prod 1:16–25

    Google Scholar 

  48. Li DQ, Li Y, Bao YM, Hu B, An LJ (2008) Catalpol prevents the loss of CA1 hippocampal neurons and reduces working errors in gerbils after ischemia-reperfusion injury. Toxicon 46:845–851

    Article  Google Scholar 

  49. Konrath EL, Santin K, Nassif M, Latini A, Heniriques A, Salbego C (2008) Antioxidant and pro-oxidant properties of boldine on hippocampal slices exposed to oxygen-glucose deprivation in vitro. Neurotoxicology 29:1136–1140

    Google Scholar 

  50. Simão F, Matté A, Matté C, Soares FMS, Wyse ATS, Netto CA, Salbego CG (2011) Resveratrol prevents oxidative stress and inhibition of Na+K+-ATPase activity induced by transient global cerebral ischemia in rats. J Nutr Biochem 22:921–928

    Article  PubMed  Google Scholar 

  51. Koh J, Choi D (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20:83–90

    Article  PubMed  CAS  Google Scholar 

  52. Candelario-Jalil E, Mhadu N, Al-Dalain S, Martinez G, León O (2001) Time course of oxidative damage in different brain regions following transient cerebral ischemia in gerbils. Neurosci Res 41:233–241

    Article  PubMed  CAS  Google Scholar 

  53. Venkateshappa C, Harish G, Mahadevan A, Srinivas Bharath MM, Shankar SK (2012) Elevated oxidative stress and decreased antioxidant function in the human hippocampus and frontal cortex with increasing age: implications for neurodegeneration in Alzheimer’s disease. Neurochem Res 37:1601–1614

    Article  PubMed  CAS  Google Scholar 

  54. Taylor JM, Crack PJ (2004) Impact of oxidative stress on neuronal survival. Cli Exp Pharmacol Physiol 31:397–406

    Article  CAS  Google Scholar 

  55. Gerich FJ, Hepp S, Probst I, Müller M (2006) Mitochondrial inhibition prior to oxygen-withdrawal facilitates the occurrence of hypoxia-induced spreading depression in rat hippocampal slices. J Neurophysiol 96:492–504

    Article  PubMed  Google Scholar 

  56. Reynolds A, Laurie C, Mosley RL, Gendelman HE (2007) Oxidative stress and the pathogenesis of neurodegenerative disorders. Int Rev Neurobiol 82:297–325

    Article  PubMed  CAS  Google Scholar 

  57. Jassem W, Heaton ND (2004) The role of mitochondria in ischemia/reperfusion injury in organ transplantation. Kidney Int 66:514–517

    Article  PubMed  CAS  Google Scholar 

  58. Korge P, Ping P, Weiss JN (2008) Reactive oxygen species production in energized cardiac mitochondria during hypoxia/reoxygenation: modulation by nitric oxide. Circulation Res 103:873–880

    Article  PubMed  CAS  Google Scholar 

  59. Pandya JD, Sullivan PG, Pettigrew LC (2011) Focal cerebral ischemia and mitochondrial dysfunction in the TNFα-transgenic rat. Brain Res 1384:151–160

    Article  PubMed  CAS  Google Scholar 

  60. Thomas JA, Poland B, Honzatko R (1995) Protein sulfhydryls and their role in the antioxidant function of protein s-thiolation. Arch Biochem Biophys 319:1–9

    Article  PubMed  CAS  Google Scholar 

  61. Chauhan A, Audhya T, Chauhan V (2012) Brain region-specific glutathione redox imbalance in autism. Neurochem Res 37:1681–1689

    Article  PubMed  CAS  Google Scholar 

  62. Tang W, Hioki H, Harada K, Kubo M, Fukuyama Y (2007) Antioxidant phenylpropanoid-substituted epicatechins from Trichilia catigua. J Nat Prod 70:2010–2013

    Article  PubMed  CAS  Google Scholar 

  63. Jeremy PES (2009) Flavonoids and brain health: multiple effects underpinned by common mechanisms. Genes Nutr 4:243–250

    Article  Google Scholar 

  64. Campos-Esparza MR, Torres-Ramos MA (2010) Neuroprotection by natural polyphenols: molecular mechanisms. Cent Nerv Syst Agents Med Chem 10:269–277

    Article  CAS  Google Scholar 

  65. Ahmad A, Khan MM, Hoda MN, Raza SS, Khan MB, Javed H, Ishrat T, Ashafaq M, Ahmad ME, Safhi MM, Islam F (2011) Quercetin protects against oxidative stress associated damages in a rat model of transient focal cerebral ischemia and reperfusion. Neurochem Res 36:1360–1371

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

JPK would like to thanks specially CNPq-TWAS for financial support. JPK is a beneficiary of the TWAS-CNPq postgraduate (Doctoral) fellowship. Work supported by CNPq, CAPES, FAPERGS, FAPERGS-PRONEX-CNPq, VITAE Fundation, Rede Brasileira de Neurociências (IBNET-FINEP), FINEP-CTINFRA and INCT for excitotoxicity and neuroprotection-CNPQ.

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The authors declare no conflict of interest with any person or other organization.

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Authors and Affiliations

  1. Departamento de Química, Programa de Pós-Graduação em Bioquímica Toxicológica, Universidade Federal de Santa Maria, Santa Maria, RS, CEP 97105-900, Brazil

    Jean Paul Kamdem, Ige Joseph Kade & João Batista Teixeira Rocha

  2. Department of Biochemistry, Federal University of Technology, Akure, PMB 704, Ondo State, Nigeria

    Ige Joseph Kade

  3. Universidade Federal do Pampa, Campus Caçapava do Sul, Caçapava do Sul, RS, CEP 96570-000, Brazil

    Caroline Wagner

  4. Departamento de Farmácia Industrial, Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Federal de Santa Maria, Santa Maria, RS, 97105-900, Brazil

    Aline Augusti Boligon & Margareth Linde Athayde

  5. Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Jean Paul Kamdem & Diogo Onofre Souza

  6. Universidade Federal do Pampa, UNIPAMPA, Uruguaina, RS 97500-970, Brazil

    Emily Pansera Waczuk

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  1. Jean Paul Kamdem
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  8. João Batista Teixeira Rocha
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Kamdem, J.P., Waczuk, E.P., Kade, I.J. et al. Catuaba (Trichilia catigua) Prevents Against Oxidative Damage Induced by In Vitro Ischemia–Reperfusion in Rat Hippocampal Slices. Neurochem Res 37, 2826–2835 (2012). https://doi.org/10.1007/s11064-012-0876-0

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