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Published in: NeuroMolecular Medicine 3/2016

01-09-2016 | Original Paper

Neuroprotective Effects of Germinated Brown Rice in Rotenone-Induced Parkinson’s-Like Disease Rats

Authors: Supin Chompoopong, Sunit Jarungjitaree, Tideeporn Punbanlaem, Thanaporn Rungruang, Sukumal Chongthammakun, Aikkarach Kettawan, Thongchai Taechowisan

Published in: NeuroMolecular Medicine | Issue 3/2016

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Abstract

The effects of germinated brown rice (GBR) on the motor deficits and the dopaminergic (DA) cell death were investigated in Parkinson’s-like disease (PD) rats. Reactive oxidative species generated by chronic subcutaneous injection of rotenone (RT) lead to neuronal apoptosis particularly in the nigrostriatal DA system and produce many features of PD, bradykinesis, postural instability and rigidity. In this study, 4-phenylbutyric acid (4-PBA), previously reported to inhibit RT-induced DA cell death, was used as the positive control. Results show that pretreatment with GBR as well as 4-PBA significantly enhanced the motor activity after RT injection, and GBR affected significantly in open field test, only in the ambulation but not the mobility duration, and ameliorated the time to orient down (t-turn) and total time to descend the pole (t-total) in pole test as compared to RT group, but significantly lowered both t-turn and t-total only in 4-PBA group. The percentage of apoptotic cells in brain measured by flow cytometry and the inflammatory effect measured by ELISA of TNF-α showed significant increase in RT group as compared to the control (CT) group at P < 0.05. Apoptotic cells in RT group (85.98 %) showed a significant (P < 0.05) increase versus CT group (17.50 %), and this effect was attenuated in GBR+RT group by decreasing apoptotic cells (79.32 %), whereas, increased viable cells (17.94 %) versus RT group (10.79 %). GBR in GBR + RT group could decrease TNF-α both in the serum and in brain. In summary, GBR showed a neuroprotective effect in RT-induced PD rats, and it may be useful as a value-added functional food to prevent neurodegenerative disease or PD.
Literature
go back to reference Azmi, N. H., Ismail, N., Imam, M. U., & Ismail, M. (2013). Ethyl acetate extract of germinated brown rice attenuates hydrogen peroxide-induced oxidative stress in human SH-SY5Y neuroblastoma cells: role of anti-apoptotic, pro-survival and antioxidant genes. BMC Complement Altern Med, 13, 177.CrossRefPubMedPubMedCentral Azmi, N. H., Ismail, N., Imam, M. U., & Ismail, M. (2013). Ethyl acetate extract of germinated brown rice attenuates hydrogen peroxide-induced oxidative stress in human SH-SY5Y neuroblastoma cells: role of anti-apoptotic, pro-survival and antioxidant genes. BMC Complement Altern Med, 13, 177.CrossRefPubMedPubMedCentral
go back to reference Ballesteros, I., Cuartero, M. I., Moraga, A., de la Parra, J., Lizasoain, I., & Moro, M. A. (2014). Stereological and flow cytometry characterization of leukocyte subpopulations in models of transient or permanent cerebral ischemia. Journal of Visualized Experiments. doi:10.3791/52031. Ballesteros, I., Cuartero, M. I., Moraga, A., de la Parra, J., Lizasoain, I., & Moro, M. A. (2014). Stereological and flow cytometry characterization of leukocyte subpopulations in models of transient or permanent cerebral ischemia. Journal of Visualized Experiments. doi:10.​3791/​52031.
go back to reference Beal, M. F. (2001). Experimental models of Parkinson’s disease. Nature Reviews Neuroscience, 2(5), 325–334.CrossRefPubMed Beal, M. F. (2001). Experimental models of Parkinson’s disease. Nature Reviews Neuroscience, 2(5), 325–334.CrossRefPubMed
go back to reference Betarbet, R., Sherer, T. B., MacKenzie, G., Garcia-Osuna, M., Panov, A. V., & Greenamyre, J. T. (2000). Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nature Neuroscience, 3(12), 1301–1306.CrossRefPubMed Betarbet, R., Sherer, T. B., MacKenzie, G., Garcia-Osuna, M., Panov, A. V., & Greenamyre, J. T. (2000). Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nature Neuroscience, 3(12), 1301–1306.CrossRefPubMed
go back to reference Carducci, M. A., Gilbert, J., Bowling, M. K., Noe, D., Eisenberger, M. A., Sinibaldi, V., et al. (2001). A Phase I clinical and pharmacological evaluation of sodium phenylbutyrate on an 120-h infusion schedule. Clinical Cancer Research, 7(10), 3047–3055.PubMed Carducci, M. A., Gilbert, J., Bowling, M. K., Noe, D., Eisenberger, M. A., Sinibaldi, V., et al. (2001). A Phase I clinical and pharmacological evaluation of sodium phenylbutyrate on an 120-h infusion schedule. Clinical Cancer Research, 7(10), 3047–3055.PubMed
go back to reference Cho, D. H., & Lim, S. T. (2016). Germinated brown rice and its bio-functional compounds. Food Chemistry, 196, 259–271.CrossRefPubMed Cho, D. H., & Lim, S. T. (2016). Germinated brown rice and its bio-functional compounds. Food Chemistry, 196, 259–271.CrossRefPubMed
go back to reference Collins, A. F., Pearson, H. A., Giardina, P., McDonagh, K. T., Brusilow, S. W., & Dover, G. J. (1995). Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: A clinical trial. Blood, 85(1), 43–49.PubMed Collins, A. F., Pearson, H. A., Giardina, P., McDonagh, K. T., Brusilow, S. W., & Dover, G. J. (1995). Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: A clinical trial. Blood, 85(1), 43–49.PubMed
go back to reference de Jong, P. J., Lakke, J. P., & Teelken, A. W. (1984). CSF GABA levels in Parkinson’s disease. Advances in Neurology, 40, 427–430.PubMed de Jong, P. J., Lakke, J. P., & Teelken, A. W. (1984). CSF GABA levels in Parkinson’s disease. Advances in Neurology, 40, 427–430.PubMed
go back to reference Gardian, G., Browne, S. E., Choi, D. K., Klivenyi, P., Gregorio, J., Kubilus, J. K., et al. (2005). Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington’s disease. Journal of Biological Chemistry, 280(1), 556–563.CrossRefPubMed Gardian, G., Browne, S. E., Choi, D. K., Klivenyi, P., Gregorio, J., Kubilus, J. K., et al. (2005). Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington’s disease. Journal of Biological Chemistry, 280(1), 556–563.CrossRefPubMed
go back to reference Gardian, G., Yang, L., Cleren, C., Calingasan, N. Y., Klivenyi, P., & Beal, M. F. (2004). Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity. Neuromolecular Med, 5(3), 235–241.CrossRefPubMed Gardian, G., Yang, L., Cleren, C., Calingasan, N. Y., Klivenyi, P., & Beal, M. F. (2004). Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity. Neuromolecular Med, 5(3), 235–241.CrossRefPubMed
go back to reference Gorell, J. M., Johnson, C. C., Rybicki, B. A., Peterson, E. L., & Richardson, R. J. (1998). The risk of Parkinson’s disease with exposure to pesticides, farming, well water, and rural living. Neurology, 50(5), 1346–1350.CrossRefPubMed Gorell, J. M., Johnson, C. C., Rybicki, B. A., Peterson, E. L., & Richardson, R. J. (1998). The risk of Parkinson’s disease with exposure to pesticides, farming, well water, and rural living. Neurology, 50(5), 1346–1350.CrossRefPubMed
go back to reference Hirata, Y., Suzuno, H., Tsuruta, T., Oh-hashi, K., & Kiuchi, K. (2008). The role of dopamine transporter in selective toxicity of manganese and rotenone. Toxicology, 244(2–3), 249–256.CrossRefPubMed Hirata, Y., Suzuno, H., Tsuruta, T., Oh-hashi, K., & Kiuchi, K. (2008). The role of dopamine transporter in selective toxicity of manganese and rotenone. Toxicology, 244(2–3), 249–256.CrossRefPubMed
go back to reference Ho, J. N., Son, M. E., Lim, W. C., Lim, S. T., & Cho, H. Y. (2012). Anti-obesity effects of germinated brown rice extract through down-regulation of lipogenic genes in high fat diet-induced obese mice. Bioscience, Biotechnology, and Biochemistry, 76(6), 1068–1074.CrossRefPubMed Ho, J. N., Son, M. E., Lim, W. C., Lim, S. T., & Cho, H. Y. (2012). Anti-obesity effects of germinated brown rice extract through down-regulation of lipogenic genes in high fat diet-induced obese mice. Bioscience, Biotechnology, and Biochemistry, 76(6), 1068–1074.CrossRefPubMed
go back to reference Inden, M., Kitamura, Y., Takeuchi, H., Yanagida, T., Takata, K., Kobayashi, Y., et al. (2007). Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. Journal of Neurochemistry, 101(6), 1491–1504.CrossRefPubMed Inden, M., Kitamura, Y., Takeuchi, H., Yanagida, T., Takata, K., Kobayashi, Y., et al. (2007). Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. Journal of Neurochemistry, 101(6), 1491–1504.CrossRefPubMed
go back to reference Inden, M., Taira, T., Kitamura, Y., Yanagida, T., Tsuchiya, D., Takata, K., et al. (2006). PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson’s disease rat model. Neurobiology of Diseases, 24(1), 144–158.CrossRef Inden, M., Taira, T., Kitamura, Y., Yanagida, T., Tsuchiya, D., Takata, K., et al. (2006). PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson’s disease rat model. Neurobiology of Diseases, 24(1), 144–158.CrossRef
go back to reference Ismail, N., Ismail, M., Fathy, S. F., Musa, S. N., Imam, M. U., Foo, J. B., et al. (2012). Neuroprotective effects of germinated brown rice against hydrogen peroxide induced cell death in human SH-SY5Y cells. International Journal of Molecular Sciences, 13(8), 9692–9708.CrossRefPubMedPubMedCentral Ismail, N., Ismail, M., Fathy, S. F., Musa, S. N., Imam, M. U., Foo, J. B., et al. (2012). Neuroprotective effects of germinated brown rice against hydrogen peroxide induced cell death in human SH-SY5Y cells. International Journal of Molecular Sciences, 13(8), 9692–9708.CrossRefPubMedPubMedCentral
go back to reference Iwatsubo, T., Yamaguchi, H., Fujimuro, M., Yokosawa, H., Ihara, Y., Trojanowski, J. Q., et al. (1996). Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. American Journal of Pathology, 148(5), 1517–1529.PubMedPubMedCentral Iwatsubo, T., Yamaguchi, H., Fujimuro, M., Yokosawa, H., Ihara, Y., Trojanowski, J. Q., et al. (1996). Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. American Journal of Pathology, 148(5), 1517–1529.PubMedPubMedCentral
go back to reference Kim, H. S., Lee, E. J., Lim, S. T., & Han, J. A. (2015). Self-enhancement of GABA in rice bran using various stress treatments. Food Chemistry, 172, 657–662.CrossRefPubMed Kim, H. S., Lee, E. J., Lim, S. T., & Han, J. A. (2015). Self-enhancement of GABA in rice bran using various stress treatments. Food Chemistry, 172, 657–662.CrossRefPubMed
go back to reference Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., et al. (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392(6676), 605–608.CrossRefPubMed Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., et al. (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392(6676), 605–608.CrossRefPubMed
go back to reference Leroy, E., Boyer, R., Auburger, G., Leube, B., Ulm, G., Mezey, E., et al. (1998). The ubiquitin pathway in Parkinson’s disease. Nature, 395(6701), 451–452.CrossRefPubMed Leroy, E., Boyer, R., Auburger, G., Leube, B., Ulm, G., Mezey, E., et al. (1998). The ubiquitin pathway in Parkinson’s disease. Nature, 395(6701), 451–452.CrossRefPubMed
go back to reference Lin, Y. T., Pao, C. C., Wu, S. T., & Chang, C. Y. (2015). Effect of different germination conditions on antioxidative properties and bioactive compounds of germinated brown rice. Biomed Res Int, 2015, 608761.PubMedPubMedCentral Lin, Y. T., Pao, C. C., Wu, S. T., & Chang, C. Y. (2015). Effect of different germination conditions on antioxidative properties and bioactive compounds of germinated brown rice. Biomed Res Int, 2015, 608761.PubMedPubMedCentral
go back to reference Maestri, N. E., Brusilow, S. W., Clissold, D. B., & Bassett, S. S. (1996). Long-term treatment of girls with ornithine transcarbamylase deficiency. New England Journal of Medicine, 335(12), 855–859.CrossRefPubMed Maestri, N. E., Brusilow, S. W., Clissold, D. B., & Bassett, S. S. (1996). Long-term treatment of girls with ornithine transcarbamylase deficiency. New England Journal of Medicine, 335(12), 855–859.CrossRefPubMed
go back to reference Mamiya, T., Kise, M., Morikawa, K., Aoto, H., Ukai, M., & Noda, Y. (2007). Effects of pre-germinated brown rice on depression-like behavior in mice. Pharmacology, Biochemistry and Behavior, 86(1), 62–67.CrossRefPubMed Mamiya, T., Kise, M., Morikawa, K., Aoto, H., Ukai, M., & Noda, Y. (2007). Effects of pre-germinated brown rice on depression-like behavior in mice. Pharmacology, Biochemistry and Behavior, 86(1), 62–67.CrossRefPubMed
go back to reference Marey-Semper, I., Gelman, M., & Levi-Strauss, M. (1995). A selective toxicity toward cultured mesencephalic dopaminergic neurons is induced by the synergistic effects of energetic metabolism impairment and NMDA receptor activation. Journal of Neuroscience, 15(9), 5912–5918.PubMed Marey-Semper, I., Gelman, M., & Levi-Strauss, M. (1995). A selective toxicity toward cultured mesencephalic dopaminergic neurons is induced by the synergistic effects of energetic metabolism impairment and NMDA receptor activation. Journal of Neuroscience, 15(9), 5912–5918.PubMed
go back to reference Marino, M. J., Wittmann, M., Bradley, S. R., Hubert, G. W., Smith, Y., & Conn, P. J. (2001). Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection neurons in the substantia nigra pars reticulata. Journal of Neuroscience, 21(18), 7001–7012.PubMed Marino, M. J., Wittmann, M., Bradley, S. R., Hubert, G. W., Smith, Y., & Conn, P. J. (2001). Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection neurons in the substantia nigra pars reticulata. Journal of Neuroscience, 21(18), 7001–7012.PubMed
go back to reference Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C. E., Benazzouz, A., et al. (2005). Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain, 128(Pt 10), 2372–2382.CrossRefPubMed Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C. E., Benazzouz, A., et al. (2005). Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain, 128(Pt 10), 2372–2382.CrossRefPubMed
go back to reference Menegon, A., Board, P. G., Blackburn, A. C., Mellick, G. D., & Le Couteur, D. G. (1998). Parkinson’s disease, pesticides, and glutathione transferase polymorphisms. Lancet, 352(9137), 1344–1346.CrossRefPubMed Menegon, A., Board, P. G., Blackburn, A. C., Mellick, G. D., & Le Couteur, D. G. (1998). Parkinson’s disease, pesticides, and glutathione transferase polymorphisms. Lancet, 352(9137), 1344–1346.CrossRefPubMed
go back to reference Mercuri, E., Bertini, E., Messina, S., Pelliccioni, M., D’Amico, A., Colitto, F., et al. (2004). Pilot trial of phenylbutyrate in spinal muscular atrophy. Neuromuscular Disorders, 14(2), 130–135.CrossRefPubMed Mercuri, E., Bertini, E., Messina, S., Pelliccioni, M., D’Amico, A., Colitto, F., et al. (2004). Pilot trial of phenylbutyrate in spinal muscular atrophy. Neuromuscular Disorders, 14(2), 130–135.CrossRefPubMed
go back to reference Mogi, M., Harada, M., Riederer, P., Narabayashi, H., Fujita, K., & Nagatsu, T. (1994). Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neuroscience Letters, 165(1–2), 208–210.CrossRefPubMed Mogi, M., Harada, M., Riederer, P., Narabayashi, H., Fujita, K., & Nagatsu, T. (1994). Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neuroscience Letters, 165(1–2), 208–210.CrossRefPubMed
go back to reference Mogi, M., Togari, A., Ogawa, M., Ikeguchi, K., Shizuma, N., Fan, D., et al. (1998). Effects of repeated systemic administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) to mice on interleukin-1beta and nerve growth factor in the striatum. Neuroscience Letters, 250(1), 25–28.CrossRefPubMed Mogi, M., Togari, A., Ogawa, M., Ikeguchi, K., Shizuma, N., Fan, D., et al. (1998). Effects of repeated systemic administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) to mice on interleukin-1beta and nerve growth factor in the striatum. Neuroscience Letters, 250(1), 25–28.CrossRefPubMed
go back to reference Mogi, M., Togari, A., Tanaka, K., Ogawa, N., Ichinose, H., & Nagatsu, T. (1999). Increase in level of tumor necrosis factor (TNF)-alpha in 6-hydroxydopamine-lesioned striatum in rats without influence of systemic L-DOPA on the TNF-alpha induction. Neuroscience Letters, 268(2), 101–104.CrossRefPubMed Mogi, M., Togari, A., Tanaka, K., Ogawa, N., Ichinose, H., & Nagatsu, T. (1999). Increase in level of tumor necrosis factor (TNF)-alpha in 6-hydroxydopamine-lesioned striatum in rats without influence of systemic L-DOPA on the TNF-alpha induction. Neuroscience Letters, 268(2), 101–104.CrossRefPubMed
go back to reference Mohd Esa, N., Abdul Kadir, K. K., Amom, Z., & Azlan, A. (2013). Antioxidant activity of white rice, brown rice and germinated brown rice (in vivo and in vitro) and the effects on lipid peroxidation and liver enzymes in hyperlipidaemic rabbits. Food Chemistry, 141(2), 1306–1312.CrossRefPubMed Mohd Esa, N., Abdul Kadir, K. K., Amom, Z., & Azlan, A. (2013). Antioxidant activity of white rice, brown rice and germinated brown rice (in vivo and in vitro) and the effects on lipid peroxidation and liver enzymes in hyperlipidaemic rabbits. Food Chemistry, 141(2), 1306–1312.CrossRefPubMed
go back to reference Ng, L. T., Huang, S. H., Chen, Y. T., & Su, C. H. (2013). Changes of tocopherols, tocotrienols, gamma-oryzanol, and gamma-aminobutyric acid levels in the germinated brown rice of pigmented and nonpigmented cultivars. Journal of Agriculture and Food Chemistry, 61(51), 12604–12611.CrossRef Ng, L. T., Huang, S. H., Chen, Y. T., & Su, C. H. (2013). Changes of tocopherols, tocotrienols, gamma-oryzanol, and gamma-aminobutyric acid levels in the germinated brown rice of pigmented and nonpigmented cultivars. Journal of Agriculture and Food Chemistry, 61(51), 12604–12611.CrossRef
go back to reference Oh, C. H., & Oh, S. H. (2004). Effects of germinated brown rice extracts with enhanced levels of GABA on cancer cell proliferation and apoptosis. Journal of Medicinal Food, 7(1), 19–23.CrossRefPubMed Oh, C. H., & Oh, S. H. (2004). Effects of germinated brown rice extracts with enhanced levels of GABA on cancer cell proliferation and apoptosis. Journal of Medicinal Food, 7(1), 19–23.CrossRefPubMed
go back to reference Online document Mahmoud, S. M., Abdel Moneim, A. E. (2013). The Protective Effect of Pomegranate (Punica granatum) Juice against Carbon Tetrachloride-Induced Oxidative Stress in Brain Tissue of Adult Male Albino Rats. Resource document Life Science Journal, 10(1), 151-158. (ISSN:1097-8135), http://www.lifesciencesite.com. 22. doi:10.7537/marslsj100113.22. Online document Mahmoud, S. M., Abdel Moneim, A. E. (2013). The Protective Effect of Pomegranate (Punica granatum) Juice against Carbon Tetrachloride-Induced Oxidative Stress in Brain Tissue of Adult Male Albino Rats. Resource document Life Science Journal, 10(1), 151-158. (ISSN:1097-8135), http://​www.​lifesciencesite.​com. 22. doi:10.​7537/​marslsj100113.​22.
go back to reference Ono, K., Ikemoto, M., Kawarabayashi, T., Ikeda, M., Nishinakagawa, T., Hosokawa, M., et al. (2009). A chemical chaperone, sodium 4-phenylbutyric acid, attenuates the pathogenic potency in human alpha-synuclein A30P+A53T transgenic mice. Parkinsonism Relat Disord, 15(9), 649–654.CrossRefPubMed Ono, K., Ikemoto, M., Kawarabayashi, T., Ikeda, M., Nishinakagawa, T., Hosokawa, M., et al. (2009). A chemical chaperone, sodium 4-phenylbutyric acid, attenuates the pathogenic potency in human alpha-synuclein A30P+A53T transgenic mice. Parkinsonism Relat Disord, 15(9), 649–654.CrossRefPubMed
go back to reference Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., et al. (2006). Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science, 313(5790), 1137–1140.CrossRefPubMedPubMedCentral Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., et al. (2006). Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science, 313(5790), 1137–1140.CrossRefPubMedPubMedCentral
go back to reference Park, H. J., Han, E. S., Park, D. K., Lee, C., & Lee, K. W. (2010). An extract of Phellinus linteus grown on germinated brown rice inhibits inflammation markers in RAW264.7 macrophages by suppressing inflammatory cytokines, chemokines, and mediators and up-regulating antioxidant activity. Journal of Medicinal Food, 13(6), 1468–1477.CrossRefPubMed Park, H. J., Han, E. S., Park, D. K., Lee, C., & Lee, K. W. (2010). An extract of Phellinus linteus grown on germinated brown rice inhibits inflammation markers in RAW264.7 macrophages by suppressing inflammatory cytokines, chemokines, and mediators and up-regulating antioxidant activity. Journal of Medicinal Food, 13(6), 1468–1477.CrossRefPubMed
go back to reference Parker, W. D, Jr., Boyson, S. J., & Parks, J. K. (1989). Abnormalities of the electron transport chain in idiopathic Parkinson’s disease. Ann Neurol, 26(6), 719–723.CrossRefPubMed Parker, W. D, Jr., Boyson, S. J., & Parks, J. K. (1989). Abnormalities of the electron transport chain in idiopathic Parkinson’s disease. Ann Neurol, 26(6), 719–723.CrossRefPubMed
go back to reference Patil, S. B., & Khan, M. K. (2011). Germinated brown rice as a value added rice product: A review. Journal of Food Science and Technology, 48(6), 661–667.CrossRefPubMedPubMedCentral Patil, S. B., & Khan, M. K. (2011). Germinated brown rice as a value added rice product: A review. Journal of Food Science and Technology, 48(6), 661–667.CrossRefPubMedPubMedCentral
go back to reference Pober, Z., & Calhoun, W. K. (1975). Effect of oxethazaine HCl on control of food and water intake in the rat. Pharmacology, Biochemistry and Behavior, 3(1), 69–74.CrossRefPubMed Pober, Z., & Calhoun, W. K. (1975). Effect of oxethazaine HCl on control of food and water intake in the rat. Pharmacology, Biochemistry and Behavior, 3(1), 69–74.CrossRefPubMed
go back to reference Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., et al. (1997). Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science, 276(5321), 2045–2047.CrossRefPubMed Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., et al. (1997). Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science, 276(5321), 2045–2047.CrossRefPubMed
go back to reference Ren, Y., Liu, W., Jiang, H., Jiang, Q., & Feng, J. (2005). Selective vulnerability of dopaminergic neurons to microtubule depolymerization. Journal of Biological Chemistry, 280(40), 34105–34112.CrossRefPubMed Ren, Y., Liu, W., Jiang, H., Jiang, Q., & Feng, J. (2005). Selective vulnerability of dopaminergic neurons to microtubule depolymerization. Journal of Biological Chemistry, 280(40), 34105–34112.CrossRefPubMed
go back to reference Ryu, H., Smith, K., Camelo, S. I., Carreras, I., Lee, J., Iglesias, A. H., et al. (2005). Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. Journal of Neurochemistry, 93(5), 1087–1098.CrossRefPubMed Ryu, H., Smith, K., Camelo, S. I., Carreras, I., Lee, J., Iglesias, A. H., et al. (2005). Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. Journal of Neurochemistry, 93(5), 1087–1098.CrossRefPubMed
go back to reference Schapira, A. H. (1994). Mitochondrial function and neurotoxicity. Current Opinion in Neurology, 7(6), 531–534.CrossRefPubMed Schapira, A. H. (1994). Mitochondrial function and neurotoxicity. Current Opinion in Neurology, 7(6), 531–534.CrossRefPubMed
go back to reference Schapira, A. H., Cooper, J. M., Dexter, D., Clark, J. B., Jenner, P., & Marsden, C. D. (1990). Mitochondrial complex I deficiency in Parkinson’s disease. Journal of Neurochemistry, 54(3), 823–827.CrossRefPubMed Schapira, A. H., Cooper, J. M., Dexter, D., Clark, J. B., Jenner, P., & Marsden, C. D. (1990). Mitochondrial complex I deficiency in Parkinson’s disease. Journal of Neurochemistry, 54(3), 823–827.CrossRefPubMed
go back to reference Sherer, T. B., Betarbet, R., Kim, J. H., & Greenamyre, J. T. (2003a). Selective microglial activation in the rat rotenone model of Parkinson’s disease. Neuroscience Letters, 341(2), 87–90.CrossRefPubMed Sherer, T. B., Betarbet, R., Kim, J. H., & Greenamyre, J. T. (2003a). Selective microglial activation in the rat rotenone model of Parkinson’s disease. Neuroscience Letters, 341(2), 87–90.CrossRefPubMed
go back to reference Sherer, T. B., Betarbet, R., Testa, C. M., Seo, B. B., Richardson, J. R., Kim, J. H., et al. (2003b). Mechanism of toxicity in rotenone models of Parkinson’s disease. Journal of Neuroscience, 23(34), 10756–10764.PubMed Sherer, T. B., Betarbet, R., Testa, C. M., Seo, B. B., Richardson, J. R., Kim, J. H., et al. (2003b). Mechanism of toxicity in rotenone models of Parkinson’s disease. Journal of Neuroscience, 23(34), 10756–10764.PubMed
go back to reference Sherer, T. B., Kim, J. H., Betarbet, R., & Greenamyre, J. T. (2003c). Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Experimental Neurology, 179(1), 9–16.CrossRefPubMed Sherer, T. B., Kim, J. H., Betarbet, R., & Greenamyre, J. T. (2003c). Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Experimental Neurology, 179(1), 9–16.CrossRefPubMed
go back to reference Shimohama, S., Sawada, H., Kitamura, Y., & Taniguchi, T. (2003). Disease model: Parkinson’s disease. Trends Mol Med, 9(8), 360–365.CrossRefPubMed Shimohama, S., Sawada, H., Kitamura, Y., & Taniguchi, T. (2003). Disease model: Parkinson’s disease. Trends Mol Med, 9(8), 360–365.CrossRefPubMed
go back to reference Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997). Alpha-synuclein in Lewy bodies. Nature, 388(6645), 839–840.CrossRefPubMed Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997). Alpha-synuclein in Lewy bodies. Nature, 388(6645), 839–840.CrossRefPubMed
go back to reference Swarnkar, S., Goswami, P., Kamat, P. K., Gupta, S., Patro, I. K., Singh, S., et al. (2012a). Rotenone-induced apoptosis and role of calcium: A study on Neuro-2a cells. Archives of Toxicology, 86(9), 1387–1397.CrossRefPubMed Swarnkar, S., Goswami, P., Kamat, P. K., Gupta, S., Patro, I. K., Singh, S., et al. (2012a). Rotenone-induced apoptosis and role of calcium: A study on Neuro-2a cells. Archives of Toxicology, 86(9), 1387–1397.CrossRefPubMed
go back to reference Swarnkar, S., Singh, S., Goswami, P., Mathur, R., Patro, I. K., & Nath, C. (2012b). Astrocyte activation: A key step in rotenone induced cytotoxicity and DNA damage. Neurochemical Research, 37(10), 2178–2189.CrossRefPubMed Swarnkar, S., Singh, S., Goswami, P., Mathur, R., Patro, I. K., & Nath, C. (2012b). Astrocyte activation: A key step in rotenone induced cytotoxicity and DNA damage. Neurochemical Research, 37(10), 2178–2189.CrossRefPubMed
go back to reference Taechowisan, T., Lu, C., Shen, Y., & Lumyong, S. (2007a). In vitro anti-inflammatory activity of 4-arylcoumarins from endophytic Streptomyces aureofaciens CMUAc130 in murine macrophage RAW 264.7 cells. Natural Product Research, 21(12), 1104–1113.CrossRefPubMed Taechowisan, T., Lu, C., Shen, Y., & Lumyong, S. (2007a). In vitro anti-inflammatory activity of 4-arylcoumarins from endophytic Streptomyces aureofaciens CMUAc130 in murine macrophage RAW 264.7 cells. Natural Product Research, 21(12), 1104–1113.CrossRefPubMed
go back to reference Taechowisan, T., Tuntiwachwuttikul, P., Lu, C., Shen, Y., Lumyong, S., & Taylor, W. C. (2007b). Anti-inflammatory activity of 4-arylcoumarins from endophytic Streptomyces aureofaciens CMUAc130 in murine macrophage RAW 264.7 cells. Immunological Investigations, 36(2), 203–211.CrossRefPubMed Taechowisan, T., Tuntiwachwuttikul, P., Lu, C., Shen, Y., Lumyong, S., & Taylor, W. C. (2007b). Anti-inflammatory activity of 4-arylcoumarins from endophytic Streptomyces aureofaciens CMUAc130 in murine macrophage RAW 264.7 cells. Immunological Investigations, 36(2), 203–211.CrossRefPubMed
go back to reference Tansey, M. G., & Goldberg, M. S. (2010). Neuroinflammation in Parkinson’s disease: Its role in neuronal death and implications for therapeutic intervention. Neurobiology of Diseases, 37(3), 510–518.CrossRef Tansey, M. G., & Goldberg, M. S. (2010). Neuroinflammation in Parkinson’s disease: Its role in neuronal death and implications for therapeutic intervention. Neurobiology of Diseases, 37(3), 510–518.CrossRef
go back to reference Wu, F., Yang, N., Toure, A., Jin, Z., & Xu, X. (2013). Germinated brown rice and its role in human health. Critical Reviews in Food Science and Nutrition, 53(5), 451–463.CrossRefPubMed Wu, F., Yang, N., Toure, A., Jin, Z., & Xu, X. (2013). Germinated brown rice and its role in human health. Critical Reviews in Food Science and Nutrition, 53(5), 451–463.CrossRefPubMed
go back to reference Yam, G. H., Gaplovska-Kysela, K., Zuber, C., & Roth, J. (2007). Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Investigative Ophthalmology and Visual Science, 48(4), 1683–1690.CrossRefPubMed Yam, G. H., Gaplovska-Kysela, K., Zuber, C., & Roth, J. (2007). Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Investigative Ophthalmology and Visual Science, 48(4), 1683–1690.CrossRefPubMed
go back to reference Yamada, C., Izumi, H., Hirano, J., Mizukuchi, A., Kise, M., Matsuda, T., et al. (2005). Degradation of soluble proteins including some allergens in brown rice grains by endogenous proteolytic activity during germination and heat-processing. Bioscience, Biotechnology, and Biochemistry, 69(10), 1877–1883.CrossRefPubMed Yamada, C., Izumi, H., Hirano, J., Mizukuchi, A., Kise, M., Matsuda, T., et al. (2005). Degradation of soluble proteins including some allergens in brown rice grains by endogenous proteolytic activity during germination and heat-processing. Bioscience, Biotechnology, and Biochemistry, 69(10), 1877–1883.CrossRefPubMed
go back to reference Zaitone, S. A., Abo-Elmatty, D. M., & Elshazly, S. M. (2012). Piracetam and vinpocetine ameliorate rotenone-induced Parkinsonism in rats. Indian J Pharmacol, 44(6), 774–779.CrossRefPubMedPubMedCentral Zaitone, S. A., Abo-Elmatty, D. M., & Elshazly, S. M. (2012). Piracetam and vinpocetine ameliorate rotenone-induced Parkinsonism in rats. Indian J Pharmacol, 44(6), 774–779.CrossRefPubMedPubMedCentral
Metadata
Title
Neuroprotective Effects of Germinated Brown Rice in Rotenone-Induced Parkinson’s-Like Disease Rats
Authors
Supin Chompoopong
Sunit Jarungjitaree
Tideeporn Punbanlaem
Thanaporn Rungruang
Sukumal Chongthammakun
Aikkarach Kettawan
Thongchai Taechowisan
Publication date
01-09-2016
Publisher
Springer US
Published in
NeuroMolecular Medicine / Issue 3/2016
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI
https://doi.org/10.1007/s12017-016-8427-5

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