Chlorogenic acid-rich Solanum melongena extract has protective potential against rotenone-induced neurotoxicity in PC-12 cells.
Solanum melongena
PC-12 cell
apoptosis
chlorogenic acid
neuroprotection
oxidative stress
rotenone
Journal
Journal of food biochemistry
ISSN: 1745-4514
Titre abrégé: J Food Biochem
Pays: United States
ID NLM: 7706045
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
09
01
2019
revised:
13
06
2019
accepted:
12
07
2019
pubmed:
2
8
2019
medline:
22
9
2020
entrez:
2
8
2019
Statut:
ppublish
Résumé
Neurodegenerative diseases are major threats to human health. Here, through fluorescence, colorimetric, immunoblotting, spectroscopy, and laser scanning confocal microscopic techniques, we investigated the neuroprotective properties of chlorogenic acid-rich Solanum melongena extracts (SM extract) in rotenone-induced PC-12 cell death. The results showed that rotenone caused apoptosis to PC-12 cells by elevating Bax/Bcl-2 ratio and increasing caspase-3 activity. Rotenone also increased ROS in cells while suppressing SOD and catalase activities. This resulted in the depletion of ATP in cells by blocking mitochondria complex I activity. Pretreatment of the cells with SM extract at concentrations of 100, 250, and 500 μg/ml before incubation for 24 hr with rotenone significantly prevented apoptosis, decreased ROS, and increased ATP production in the cells. SM extract upregulated SOD and catalase activities in the cells. These results unveil evidence that SM extract content neuroprotective properties that can be exploited to prevent and treat neurodegenerative diseases. PRACTICAL APPLICATIONS: Solanum melongena eggplant is a popular ingredient in many traditional recipes and is well known in Asia for its medicinal benefits. Despite numerous scientific reports of the potential health benefits of this plant, reports on its effects in neurodegenerative diseases is still lacking. This pilot study demonstrates that S. melongena eggplant can protect against neurotoxicity in neurodegenerative diseases. The results of this research serves as a base for further research on eggplant that will result in its usage on a larger scale as functional food materials.
Substances chimiques
Plant Extracts
0
Rotenone
03L9OT429T
Chlorogenic Acid
318ADP12RI
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12999Informations de copyright
© 2019 Wiley Periodicals, Inc.
Références
Batandier, C., Fontaine, E., Keriel, C., & Leverve, X. M. (2002). Determination of mitochondrial reactive oxygen species: Methodological aspects. Journal of Cellular and Molecular Medicine, 6, 175-187. https://doi.org/10.1111/j.1582-4934.2002.tb00185.x
Cannon, J. R., & Greenamyre, J. T. (2010). Neurotoxic in vivo models of parkinson's disease recent advances. Progress in Brain Research, 184, 17-33. https://doi.org/10.1016/S0079-6123(10)84002-6
Cho, B. O., Che, D. N., Yin, H. H., & Jang, S. I. (2017). Gamma irradiation enhances biological activities of mulberry leaf extract. Radiation Physics and Chemistry, 133, 21-27. https://doi.org/10.1016/j.radphyschem.2016.11.013
Cregan, S. P., Maclaurin, J. G., Craig, C. G., Robertson, G. S., Nicholson, D. W., Park, D. S., & Slack, R. S. (1999). Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. The Journal of Neuroscience, 19, 7860-7869. https://doi.org/10.1523/JNEUROSCI.19-18-07860.1999
Dauer, W., & Przedborski, S. (2003). Parkinson's disease: Mechanisms and models. Neuron, 39, 889-909. https://doi.org/10.1016/S0896-6273(03)00568-3
Di Sotto, A., Di Giacomo, S., Amatore, D., Locatelli, M., Vitalone, A., Toniolo, C., … Nencioni, L. (2018). A polyphenol rich extract from Solanum melongena L. DR2 peel exhibits antioxidant properties and anti-herpes simplex virus type 1 activity In Vitro. Molecules, 23, 2066.
Du, H., & Yan, S. S. (2010). Mitochondrial medicine for neurodegenerative diseases. The International Journal of Biochemistry & Cell Biology, 42, 560-572. https://doi.org/10.1016/j.biocel.2010.01.004
Gebhardt, C. (2016). The historical role of species from the Solanaceae plant family in genetic research. TAG. Theoretical and applied genetics. Theoretische und Angewandte Genetik, 129, 2281-2294. https://doi.org/10.1007/s00122-016-2804-1
Gitler, A. D., Dhillon, P., & Shorter, J. (2017). Neurodegenerative disease: Models, mechanisms, and a new hope. Disease Models & Mechanisms, 10, 499-502. https://doi.org/10.1242/dmm.030205
Heinz, S., Freyberger, A., Lawrenz, B., Schladt, L., Schmuck, G., & Ellinger-Ziegelbauer, H. (2017). Mechanistic investigations of the mitochondrial complex I inhibitor rotenone in the context of pharmacological and safety evaluation. Scientific Reports, 7, 45465-45465. https://doi.org/10.1038/srep45465
Im, A.-R., Kim, Y.-H., Uddin, M. R., Chae, S., Lee, H. W., Kim, Y. H., … Lee, M.-Y. (2013b). Betaine protects against rotenone-induced neurotoxicity in PC12 cells. Cellular and Molecular Neurobiology, 33, 625-635. https://doi.org/10.1007/s10571-013-9921-z
Im, A. R., Kim, Y. H., Uddin, M. R., Chae, S., Lee, H. W., Kim, Y. S., & Lee, M. Y. (2013a). Neuroprotective effects of Lycium chinense Miller against rotenone-induced neurotoxicity in PC12 cells. The American Journal of Chinese Medicine, 41, 1343-1359.
Im, K., Lee, J. Y., Byeon, H., Hwang, K. W., Kang, W., Whang, W. K., & Min, H. (2016). In Vitro antioxidative and anti-inflammatory activities of the ethanol extract of eggplant (Solanum melongena) stalks in macrophage RAW 264.7 cells. Food and Agricultural Immunology, 27, 758-771.
Kim, H. Y., Jeon, H., Kim, H., Koo, S., & Kim, S. (2018). Sophora flavescens Aiton decreases MPP(+)-induced mitochondrial dysfunction in SH-SY5Y cells. Frontiers in Aging Neuroscience, 10, 119. https://doi.org/10.3389/fnagi.2018.00119
Kim, J. Y., & Park, J. H. (2003). ROS-dependent caspase-9 activation in hypoxic cell death. FEBS Letters, 549, 94-98. https://doi.org/10.1016/S0014-5793(03)00795-6
Kim, K. H., Lee, D., Lee, H. L., Kim, C. E., Jung, K., & Kang, K. S. (2018). Beneficial effects of panax ginseng for the treatment and prevention of neurodegenerative diseases: Past findings and future directions. Journal of Ginseng Research, 42, 239-247. https://doi.org/10.1016/j.jgr.2017.03.011
King, T. D., Bijur, G. N., & Jope, R. S. (2001). Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium. Brain Research, 919, 106-114.
Kirkinezos, I. G., & Moraes, C. T. (2001). Reactive oxygen species and mitochondrial diseases. Seminars in Cell & Developmental Biology, 12, 449-457. https://doi.org/10.1006/scdb.2001.0282
Lee, J., Song, K., Huh, E., Oh, M. S., & Kim, Y. S. (2018). Neuroprotection against 6-OHDA toxicity in PC12 cells and mice through the Nrf2 pathway by a sesquiterpenoid from Tussilago farfara. Redox Biology, 18, 6-15. https://doi.org/10.1016/j.redox.2018.05.015
Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J. A., & Robinson, J. P. (2003). Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. The Journal of Biological Chemistry, 278, 8516-8525. https://doi.org/10.1074/jbc.M210432200
Martin, L. J. (2001). Neuronal cell death in nervous system development, disease, and injury (Review). International Journal of Molecular Medicine, 7, 455-478. https://doi.org/10.3892/ijmm.7.5.455
Mennella, G., Lo Scalzo, R., Fibiani, M., D'Alessandro, A., Francese, G., Toppino, L., … Rotino, G. L. (2012). Chemical and bioactive quality traits during fruit ripening in eggplant (S. melongena L.) and allied species. Journal of Agricultural and Food Chemistry, 60, 11821-11831.
Moreira, P. I., Carvalho, C., Zhu, X., Smith, M. A., & Perry, G. (2010). Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology. Biochimica et Biophysica Acta, 1802, 2-10. https://doi.org/10.1016/j.bbadis.2009.10.006
Quintanilla, R. A., & Johnson, G. V. W. (2009). Role of mitochondrial dysfunction in the pathogenesis of Huntington's disease. Brain Research Bulletin, 80, 242-247. https://doi.org/10.1016/j.brainresbull.2009.07.010
Sadilova, E., Stintzing, F. C., & Carle, R. (2006). Anthocyanins, colour and antioxidant properties of eggplant (Solanum melongena L.) and violet pepper (Capsicum annuum L.) peel extracts. Journal of Biosciences, 61, 527-535.
Salakou, S., Kardamakis, D., Tsamandas, A. C., Zolota, V., Apostolakis, E., Tzelepi, V., … Dougenis, D. (2007). Increased Bax/Bcl-2 ratio up-regulates caspase-3 and increases apoptosis in the thymus of patients with myasthenia gravis. In Vivo, 21, 123-132.
Shin, D. Y., Kim, G. Y., Li, W., Choi, B. T., Kim, N. D., Kang, H. S., & Choi, Y. H. (2009). Implication of intracellular ROS formation, caspase-3 activation and Egr-1 induction in platycodon D-induced apoptosis of U937 human leukemia cells. Biomedicine & Pharmacotherapy, 63, 86-94. https://doi.org/10.1016/j.biopha.2008.08.001
Strasser, A., O'connor, L., & Dixit, V. M. (2000). Apoptosis signaling. Annual Review of Biochemistry, 69, 217-245.
Sun, J., Gu, Y.-F., Su, X.-Q., Li, M.-M., Huo, H.-X., Zhang, J., … Tu, P.-F. (2014). Anti-inflammatory lignanamides from the roots of Solanum melongena L. Fitoterapia, 98, 110-116. https://doi.org/10.1016/j.fitote.2014.07.012
Sun, J., Song, Y. L., Zhang, J., Huang, Z., Huo, H. X., Zheng, J., … Tu, P. F. (2015). Characterization and quantitative analysis of phenylpropanoid amides in eggplant (Solanum melongena L.) by high performance liquid chromatography coupled with diode array detection and hybrid ion trap time-of-flight mass spectrometry. Journal of Agricultural and Food Chemistry, 63, 3426-3436.
Umamageswari, M. S., Karthikeyan, T. M., & Maniyar, Y. A. (2017). Antidiabetic activity of aqueous extract of Solanum nigrum Linn Berries in alloxan induced diabetic wistar albino rats. Journal of Clinical and Diagnostic Research, 11, FC16-FC19. https://doi.org/10.7860/JCDR/2017/26563.10312
Villegas, R., Martinez, N. W., Lillo, J., Pihan, P., Hernandez, D., Twiss, J. L., & Court, F. A. (2014). Calcium release from intra-axonal endoplasmic reticulum leads to axon degeneration through mitochondrial dysfunction. The Journal of Neuroscience, 34, 7179-7189. https://doi.org/10.1523/JNEUROSCI.4784-13.2014
Westerink, R. H. S., & Ewing, A. G. (2008). The PC12 cell as model for neurosecretion. Acta Physiologica, 192, 273-285. https://doi.org/10.1111/j.1748-1716.2007.01805.x
William, E.-P. (2018, December 14). Nervous system disease. Retrieved from https://www.britannica.com/science/human-nervous-system-disease/Localization-of-neurological-disease
Yang, B., Johnson, T. S., Thomas, G. L., Watson, P. F., Wagner, B., Furness, P. N., … A.M., (2002). A shift in the Bax/Bcl-2 balance may activate caspase-3 and modulate apoptosis in experimental glomerulonephritis. Kidney International, 62, 1301-1313. https://doi.org/10.1111/j.1523-1755.2002.kid587.x
Yao, Z., & Wood, N. W. (2009). Cell death pathways in Parkinson's disease: Role of mitochondria. Antioxidants & Redox Signaling, 11, 2135-2149. https://doi.org/10.1089/ars.2009.2624
Zhang, Y., Dawson, V. L., & Dawson, T. M. (2000). Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiology of Disease, 7, 240-250. https://doi.org/10.1006/nbdi.2000.0319
Zorova, L. D., Popkov, V. A., Plotnikov, E. Y., Silachev, D. N., Pevzner, I. B., Jankauskas, S. S., … Zorov, D. B. (2018). Mitochondrial membrane potential. Analytical Biochemistry, 552, 50-59. https://doi.org/10.1016/j.ab.2017.07.009