Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA

IntroductionParkinson’s disease affects 2% of the population aged over 65 years and is the second most common neurodegenerative disorder in the general population. The appearance of motor symptoms is associated with the degeneration of dopaminergic neurons in the nigrostriatal pathway. Clinically si...

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Main Authors: Váldina Solimar Lopes Cardoso, Anderson Valente-Amaral, Rayan Fidel Martins Monteiro, Clarina Loius Silva Meira, Natália Silva de Meira, Milton Nascimento da Silva, João de Jesus Viana Pinheiro, Gilmara de Nazareth Tavares Bastos, João Soares Felício, Elizabeth Sumi Yamada
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2024.1351718/full
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author Váldina Solimar Lopes Cardoso
Váldina Solimar Lopes Cardoso
Anderson Valente-Amaral
Anderson Valente-Amaral
Rayan Fidel Martins Monteiro
Rayan Fidel Martins Monteiro
Clarina Loius Silva Meira
Natália Silva de Meira
Milton Nascimento da Silva
João de Jesus Viana Pinheiro
João de Jesus Viana Pinheiro
Gilmara de Nazareth Tavares Bastos
Gilmara de Nazareth Tavares Bastos
João Soares Felício
João Soares Felício
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
author_facet Váldina Solimar Lopes Cardoso
Váldina Solimar Lopes Cardoso
Anderson Valente-Amaral
Anderson Valente-Amaral
Rayan Fidel Martins Monteiro
Rayan Fidel Martins Monteiro
Clarina Loius Silva Meira
Natália Silva de Meira
Milton Nascimento da Silva
João de Jesus Viana Pinheiro
João de Jesus Viana Pinheiro
Gilmara de Nazareth Tavares Bastos
Gilmara de Nazareth Tavares Bastos
João Soares Felício
João Soares Felício
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
author_sort Váldina Solimar Lopes Cardoso
collection DOAJ
description IntroductionParkinson’s disease affects 2% of the population aged over 65 years and is the second most common neurodegenerative disorder in the general population. The appearance of motor symptoms is associated with the degeneration of dopaminergic neurons in the nigrostriatal pathway. Clinically significant nonmotor symptoms are also important for severe disability with disease progression. Pharmacological treatment with levodopa, which involves dopamine restitution, results in a temporary improvement in motor symptoms. Among the mechanisms underlying the pathogenesis of the disease are exacerbated oxidative stress, mitochondrial dysfunction, and neuroinflammation. A phytochemical prospecting study showed that the aqueous extract of the leaves from Swietenia macrophylla (Melineaceae), known as mahogany, has polyphenols with antioxidant and anti-inflammatory capacity in a significantly higher percentage than leaf extracts from other Amazonian plants. Furthermore, the antioxidant and anti-inflammatory capacity of aqueous extract of mahogany leaf has already been demonstrated in an in vitro model. In this study, we hypothesized that the aqueous extract of mahogany leaf (AEML) has a neuroprotective effect in a murine model of Parkinson’s disease induced by 6-hydroxidopamine (6-OHDA), due to antioxidant and anti-inflammatory properties of its phenolic compounds.MethodsMice were treated daily with the mahogany extract at a dose of 50 mg/kg, starting 7 days before 6-OHDA infusion until post-surgery day 7.Results and discussionThe animals from the 6-OHDA/mahogany group, which corresponds to animals injected with the toxin and treated with aqueous extract of the mahogany leaf, presented distinct behavioral phenotypes after apomorphine challenge and were therefore subdivided into 2 groups, 6-OHDA/mahogany F1 and 6-OHDA/mahogany F2. The F1 group showed a significant increase in contralateral rotations, whereas the F2 group did not show rotations after the apomorphine stimulus. In the F1 group, there was an increase, although not significant, in motor performance in the open field and elevated plus maze tests, whereas in the F2 group, there was significant improvement, which may be related to the lesser degree of injury to the nigrostriatal dopaminergic pathway. The TH+ histopathological analysis, a dopaminergic neuron marker, confirmed that the lesion to the nigrostriatal dopaminergic pathway was more pronounced in 6-OHDA/mahogany F1 than in 6-OHDA/mahogany F2. Our main result consisted of signs of improvement in the inflammatory profile in both the F1 and F2 6-OHDA/mahogany groups, such as a lower number of IBA-1+ microglial cells in the ventral striatum and substantia nigra pars compacta and a reduction in GFAP+ expression, an astrocyte marker, in the dorsal striatum. In this study, several bioactive compounds in the aqueous extract of mahogany leaf may have contributed to the observed beneficial effects. Further studies are necessary to better characterize their applicability for treating chronic degenerative diseases with inflammatory and oxidative bases, such as Parkinson’s disease.
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spelling doaj.art-087989332568491384b399adaa5215282024-02-21T04:26:06ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2024-02-011810.3389/fnins.2024.13517181351718Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDAVáldina Solimar Lopes Cardoso0Váldina Solimar Lopes Cardoso1Anderson Valente-Amaral2Anderson Valente-Amaral3Rayan Fidel Martins Monteiro4Rayan Fidel Martins Monteiro5Clarina Loius Silva Meira6Natália Silva de Meira7Milton Nascimento da Silva8João de Jesus Viana Pinheiro9João de Jesus Viana Pinheiro10Gilmara de Nazareth Tavares Bastos11Gilmara de Nazareth Tavares Bastos12João Soares Felício13João Soares Felício14Elizabeth Sumi Yamada15Elizabeth Sumi Yamada16Elizabeth Sumi Yamada17Experimental Neuropathology Laboratory, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilOncology Research Center and Graduate Program in Oncology and Medical Sciences, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilExperimental Neuropathology Laboratory, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilGraduate Program in Neuroscience and Cellular Biology, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilGraduate Program in Neuroscience and Cellular Biology, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilNeuroinflammation Laboratory, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilExperimental Neuropathology Laboratory, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilExperimental Neuropathology Laboratory, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilLiquid Chromatography Laboratory, Institute of Exact and Natural Science, Federal University of Pará, Belém, BrazilOncology Research Center and Graduate Program in Oncology and Medical Sciences, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilLaboratory of Pathological Anatomy and Immunohistochemistry, School of Dentistry, Federal University of Pará, Belém, BrazilGraduate Program in Neuroscience and Cellular Biology, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilNeuroinflammation Laboratory, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilOncology Research Center and Graduate Program in Oncology and Medical Sciences, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilEndocrinology Division, University Hospital João de Barros Barreto, Federal University of Pará, Belém, BrazilExperimental Neuropathology Laboratory, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilOncology Research Center and Graduate Program in Oncology and Medical Sciences, João de Barros Barreto University Hospital, Federal University of Pará, Belém, BrazilGraduate Program in Neuroscience and Cellular Biology, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilIntroductionParkinson’s disease affects 2% of the population aged over 65 years and is the second most common neurodegenerative disorder in the general population. The appearance of motor symptoms is associated with the degeneration of dopaminergic neurons in the nigrostriatal pathway. Clinically significant nonmotor symptoms are also important for severe disability with disease progression. Pharmacological treatment with levodopa, which involves dopamine restitution, results in a temporary improvement in motor symptoms. Among the mechanisms underlying the pathogenesis of the disease are exacerbated oxidative stress, mitochondrial dysfunction, and neuroinflammation. A phytochemical prospecting study showed that the aqueous extract of the leaves from Swietenia macrophylla (Melineaceae), known as mahogany, has polyphenols with antioxidant and anti-inflammatory capacity in a significantly higher percentage than leaf extracts from other Amazonian plants. Furthermore, the antioxidant and anti-inflammatory capacity of aqueous extract of mahogany leaf has already been demonstrated in an in vitro model. In this study, we hypothesized that the aqueous extract of mahogany leaf (AEML) has a neuroprotective effect in a murine model of Parkinson’s disease induced by 6-hydroxidopamine (6-OHDA), due to antioxidant and anti-inflammatory properties of its phenolic compounds.MethodsMice were treated daily with the mahogany extract at a dose of 50 mg/kg, starting 7 days before 6-OHDA infusion until post-surgery day 7.Results and discussionThe animals from the 6-OHDA/mahogany group, which corresponds to animals injected with the toxin and treated with aqueous extract of the mahogany leaf, presented distinct behavioral phenotypes after apomorphine challenge and were therefore subdivided into 2 groups, 6-OHDA/mahogany F1 and 6-OHDA/mahogany F2. The F1 group showed a significant increase in contralateral rotations, whereas the F2 group did not show rotations after the apomorphine stimulus. In the F1 group, there was an increase, although not significant, in motor performance in the open field and elevated plus maze tests, whereas in the F2 group, there was significant improvement, which may be related to the lesser degree of injury to the nigrostriatal dopaminergic pathway. The TH+ histopathological analysis, a dopaminergic neuron marker, confirmed that the lesion to the nigrostriatal dopaminergic pathway was more pronounced in 6-OHDA/mahogany F1 than in 6-OHDA/mahogany F2. Our main result consisted of signs of improvement in the inflammatory profile in both the F1 and F2 6-OHDA/mahogany groups, such as a lower number of IBA-1+ microglial cells in the ventral striatum and substantia nigra pars compacta and a reduction in GFAP+ expression, an astrocyte marker, in the dorsal striatum. In this study, several bioactive compounds in the aqueous extract of mahogany leaf may have contributed to the observed beneficial effects. Further studies are necessary to better characterize their applicability for treating chronic degenerative diseases with inflammatory and oxidative bases, such as Parkinson’s disease.https://www.frontiersin.org/articles/10.3389/fnins.2024.1351718/fullSwietenia macrophyllanatural productspolyphenolsParkinson’s diseaseneuroinflammation6-OHDA model
spellingShingle Váldina Solimar Lopes Cardoso
Váldina Solimar Lopes Cardoso
Anderson Valente-Amaral
Anderson Valente-Amaral
Rayan Fidel Martins Monteiro
Rayan Fidel Martins Monteiro
Clarina Loius Silva Meira
Natália Silva de Meira
Milton Nascimento da Silva
João de Jesus Viana Pinheiro
João de Jesus Viana Pinheiro
Gilmara de Nazareth Tavares Bastos
Gilmara de Nazareth Tavares Bastos
João Soares Felício
João Soares Felício
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
Elizabeth Sumi Yamada
Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
Frontiers in Neuroscience
Swietenia macrophylla
natural products
polyphenols
Parkinson’s disease
neuroinflammation
6-OHDA model
title Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
title_full Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
title_fullStr Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
title_full_unstemmed Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
title_short Aqueous extract of Swietenia macrophylla leaf exerts an anti-inflammatory effect in a murine model of Parkinson’s disease induced by 6-OHDA
title_sort aqueous extract of swietenia macrophylla leaf exerts an anti inflammatory effect in a murine model of parkinson s disease induced by 6 ohda
topic Swietenia macrophylla
natural products
polyphenols
Parkinson’s disease
neuroinflammation
6-OHDA model
url https://www.frontiersin.org/articles/10.3389/fnins.2024.1351718/full
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