Sesame Lignans Suppress Age-Related Cognitive Decline in Senescence-Accelerated Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Animals and Diets
2.3. Step-Through Passive Avoidance Task
2.4. Forced Swim Test
2.5. Measurement of Reactive Carbonyl Species
2.6. Statistical Analysis
3. Results
3.1. Body and Brain Weights, and Survival Rates
3.2. Step-Through Passive Avoidance Task
3.3. Forced Swim Test
3.4. Reactive Carbonyl Species
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Barnes, L.L.; Bennett, D.A. Alzheimer’s disease in African Americans: Risk factors and challenges for the future. Health Aff. 2014, 33, 580–586. [Google Scholar] [CrossRef] [PubMed]
- Pohanka, M. Oxidative stress in Alzheimer disease as a target for therapy. Bratisl. Lek. Listy 2018, 119, 535–543. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Floyd, R.A.; Hensley, K. Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol. Aging 2002, 23, 795–807. [Google Scholar] [CrossRef]
- Uchida, K. Role of reactive aldehyde in cardiovascular diseases. Free Radic. Biol. Med. 2000, 28, 1685–1696. [Google Scholar] [CrossRef]
- Liu, S.; Shi, W.; Li, G.; Jin, B.; Chen, Y.; Hu, H.; Liu, L.; Xie, F.; Chen, K.; Yin, D. Plasma reactive carbonyl species levels and risk of non-alcoholic fatty liver disease. J. Gastroenterol. Hepatol. 2011, 26, 1010–1015. [Google Scholar] [CrossRef] [PubMed]
- Nair, U.; Bartsch, H.; Nair, J. Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: A review of published adduct types and levels in humans. Free Radic. Biol. Med. 2007, 43, 1109–1120. [Google Scholar] [CrossRef] [PubMed]
- Tomono, S.; Miyoshi, N.; Ohshima, H. Comprehensive analysis of the lipophilic reactive carbonyls present in biological specimens by LC/ESI-MS/MS. J. Chromatogr. B 2015, 988, 149–156. [Google Scholar] [CrossRef] [PubMed]
- Onuma, W.; Tomono, S.; Miyamoto, S.; Fujii, G.; Hamoya, T.; Fujimoto, K.; Miyoshi, N.; Fukai, F.; Wakabayashi, K.; Mutoh, M. Irsogladine maleate, a gastric mucosal protectant, suppresses intestinal polyp development in Apc-mutant mice. Oncotarget 2016, 7, 8640–8652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hamoya, T.; Miyamoto, S.; Tomono, S.; Fujii, G.; Nakanishi, R.; Komiya, M.; Tamura, S.; Fujimoto, K.; Toshima, J.; Wakabayashi, K.; et al. Chemopreventive effects of a low-side-effect antibiotic drug, erythromycin, on mouse intestinal tumors. J. Clin. Biochem. Nutr. 2017, 60, 199–207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Domenico, F.; Tramutola, A.; Butterfield, D.A. Role of 4-hydroxy-2-nonenal (HNE) in the pathogenesis of alzheimer disease and other selected age-related neurodegenerative disorders. Free Radic. Biol. Med. 2017, 111, 253–261. [Google Scholar] [CrossRef]
- Bradley, M.A.; Xiong-Fister, S.; Markesbery, W.R.; Lovell, M.A. Elevated 4-hydroxyhexenal in Alzheimer’s disease (AD) progression. Neurobiol. Aging 2012, 33, 1034–1044. [Google Scholar] [CrossRef] [PubMed]
- Takeda, T.; Hosokawa, M.; Takeshita, S.; Irino, M.; Higuchi, K.; Matsushita, T.; Tomita, Y.; Yasuhira, K.; Hamamoto, H.; Shimizu, K.; et al. A new murine model of accelerated senescence. Mech. Ageing Dev. 1981, 17, 183–194. [Google Scholar] [CrossRef]
- Shimada, A.; Ohta, A.; Akiguchi, I.; Takeda, T. Inbred SAM-P/10 as a mouse model of spontaneous, inherited brain atrophy. J. Neuropathol. Exp. Neurol. 1992, 51, 440–450. [Google Scholar] [CrossRef] [PubMed]
- Shimada, A.; Ohta, A.; Akiguchi, I.; Takeda, T. Age-related deterioration in conditional avoidance task in the SAM-P/10 mouse, an animal model of spontaneous brain atrophy. Brain Res. 1993, 608, 266–272. [Google Scholar] [CrossRef]
- Miyamoto, M. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp. Gerontol. 1997, 32, 139–148. [Google Scholar] [CrossRef]
- Miyamoto, M.; Takahashi, H.; Ohta, H.; Sakamoto, J. Animal model of brain aging: Senescence-accelerated mouse (SAM). CNS Drug Rev. 1998, 4, 361–375. [Google Scholar] [CrossRef] [PubMed]
- Unno, K.; Takabayashi, F.; Yoshida, H.; Choba, D.; Fukutomi, R.; Kikunaga, N.; Kishido, T.; Oku, N.; Hoshino, M. Daily consumption of green tea catechin delays memory regression in aged mice. Biogerontology 2007, 8, 89–95. [Google Scholar] [CrossRef]
- Unno, K.; Sugiura, M.; Ogawa, K.; Takabayashi, F.; Toda, M.; Sakuma, M.; Maeda, K.; Fujitani, K.; Miyazaki, H.; Yamamoto, H.; et al. Beta-cryptoxanthin, plentiful in Japanese mandarin orange, prevents age-related cognitive dysfunction and oxidative damage in senescence-accelerated mouse brain. Biol. Pharm. Bull. 2011, 34, 311–317. [Google Scholar] [CrossRef]
- Hasegawa-Ishii, S.; Takei, S.; Chiba, Y.; Furukawa, A.; Umegaki, H.; Iguchi, A.; Kawamura, N.; Yoshikawa, K.; Hosokawa, M.; Shimada, A. Morphological impairments in microglia precede age-related neuronal degeneration in senescence-accelerated mice. Neuropathology 2011, 31, 20–28. [Google Scholar] [CrossRef]
- Hasegawa-Ishii, S.; Inaba, M.; Li, M.; Shi, M.; Umegaki, H.; Ikehara, S.; Shimada, A. Increased recruitment of bone marrow-derived cells into the brain associated with altered brain cytokine profile in senescence-accelerated mice. Brain Struct. Funct. 2016, 221, 1513–1531. [Google Scholar] [CrossRef]
- Nakai, M.; Harada, M.; Nakahara, K.; Akimoto, K.; Shibata, H.; Miki, W.; Kiso, Y. Novel antioxidative metabolites in rat liver with ingested sesamin. J. Agric. Food Chem. 2003, 51, 1666–1670. [Google Scholar] [CrossRef] [PubMed]
- Ikeda, T.; Nishijima, Y.; Shibata, H.; Kiso, Y.; Ohnuki, K.; Fushiki, T.; Moritani, T. Protective effect of sesamin administration on exercise-induced lipid peroxidation. Int. J. Sports Med. 2003, 24, 530–534. [Google Scholar] [PubMed]
- Hirata, F.; Fujita, K.; Ishikura, Y.; Hosoda, K.; Ishikawa, T.; Nakamura, H. Hypocholesterolemic effect of sesame lignan in humans. Atherosclerosis 1996, 122, 135–136. [Google Scholar] [CrossRef]
- Nakano, D.; Kwak, C.-J.; Fujii, K.; Ikemura, K.; Satake, A.; Ohkita, M.; Takaoka, M.; Ono, Y.; Nakai, M.; Tomimori, N.; et al. Sesamin metabolites induce an endothelial nitric oxide-dependent vasorelaxation through their antioxidative property-independent mechanisms: Possible involvement of the metabolites in the antihypertensive effect of sesamin. J. Pharmacol. Exp. Ther. 2006, 318, 328–335. [Google Scholar] [CrossRef] [PubMed]
- Akimoto, K.; Kitagawa, Y.; Akamatsu, T.; Hirose, N.; Sugano, M.; Shimizu, S.; Yamada, H. Protective effects of sesamin against liver damage caused by alcohol or carbon tetrachloride in rodents. Ann. Nutr. Metab. 1993, 37, 218–224. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, S.; Elsherbiny, N.M.; Haque, R.; Khan, M.B.; Ishrat, T.; Shah, Z.A.; Khan, M.M.; Ali, M.; Jamal, A.; Katare, D.P.; et al. Sesamin attenuates neurotoxicity in mouse model of ischemic brain stroke. Neurotoxicology 2014, 45, 100–110. [Google Scholar] [CrossRef] [PubMed]
- Fujikawa, T.; Kanada, N.; Shimada, A.; Ogata, M.; Suzuki, I.; Hayashi, I.; Nakashima, K. Effect of sesamin in Acanthopanax senticosus HARMS on behavioral dysfunction in rotenone-induced parkinsonian rats. Biol. Pharm. Bull. 2005, 28, 169–172. [Google Scholar] [CrossRef] [PubMed]
- Nakai, M.; Kageyama, N.; Nakahara, K.; Miki, W. Decomposition reaction of sesamin in supercritical water. Biosci. Biotechnol. Biochem. 2006, 70, 1273–1276. [Google Scholar] [CrossRef] [PubMed]
- Hamada, N.; Tanaka, A.; Fujita, Y.; Itoh, T.; Ono, Y.; Kitagawa, Y.; Tomimori, N.; Kiso, Y.; Akao, Y.; Nozawa, Y.; et al. Involvement of heme oxygenase-1 induction via Nrf2/ARE activation in protection against H2O2-induced PC12 cell death by a metabolite of sesamin contained in sesame seeds. Bioorg. Med. Chem. 2011, 19, 1959–1965. [Google Scholar] [CrossRef]
- Wentworth, P.; Nieva, J.; Takeuchi, C.; Galve, R.; Wentworth, A.D.; Dilley, R.B.; DeLaria, G.A.; Saven, A.; Babior, B.M.; Janda, K.D.; et al. Evidence for ozone formation in human atherosclerotic arteries. Science 2003, 302, 1053–1056. [Google Scholar] [CrossRef]
- Unno, K.; Takabayashi, F.; Kishido, T.; Oku, N. Suppressive effect of green tea catechins on morphologic and functional regression of the brain in aged mice with accelerated senescence (SAMP10). Exp. Gerontol. 2004, 39, 1027–1034. [Google Scholar] [CrossRef] [PubMed]
- Porsolt, R.D.; Le Pichon, M.; Jalfre, M. Depression: A new animal model sensitive to antidepressant treatments. Nature 1977, 266, 730–732. [Google Scholar] [CrossRef] [PubMed]
- Sakul, A.; Cumaoğlu, A.; Aydin, E.; Ari, N.; Dilsiz, N.; Karasu, C. Age- and diabetes-induced regulation of oxidative protein modification in rat brain and peripheral tissues: Consequences of treatment with antioxidant pyridoindole. Exp. Gerontol. 2013, 48, 476–484. [Google Scholar] [CrossRef] [PubMed]
- Kishido, T.; Unno, K.; Yoshida, H.; Choba, D.; Fukutomi, R.; Asahina, S.; Iguchi, K.; Oku, N.; Hoshino, M. Decline in glutathione peroxidase activity is a reason for brain senescence: Consumption of green tea catechin prevents the decline in its activity and protein oxidative damage in ageing mouse brain. Biogerontology 2007, 8, 423–430. [Google Scholar] [CrossRef] [PubMed]
- Walton, J.C.; Selvakumar, B.; Weil, Z.M.; Snyder, S.H.; Nelson, R.J. Neuronal nitric oxide synthase and NADPH oxidase interact to affect cognitive, affective, and social behaviors in mice. Behav. Brain Res. 2013, 256, 320–327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seo, J.-S.; Park, J.-Y.; Choi, J.; Kim, T.-K.; Shin, J.-H.; Lee, J.-K.; Han, P.-L. NADPH oxidase mediates depressive behavior induced by chronic stress in mice. J. Neurosci. 2012, 32, 9690–9699. [Google Scholar] [CrossRef] [PubMed]
- Le, T.D.; Nakahara, Y.; Ueda, M.; Okumura, K.; Hirai, J.; Sato, Y.; Takemoto, D.; Tomimori, N.; Ono, Y.; Nakai, M.; et al. Sesamin suppresses aging phenotypes in adult muscular and nervous systems and intestines in a Drosophila senescence-accelerated model. Eur. Rev. Med. Pharmacol. Sci. 2019, 23, 1826–1839. [Google Scholar] [PubMed]
- Ito, N.; Saito, H.; Seki, S.; Ueda, F.; Asada, T. Effects of Composite Supplement Containing Astaxanthin and Sesamin on Cognitive Functions in People with Mild Cognitive Impairment: A Randomized, Double-Blind, Placebo-Controlled Trial. J. Alzheimer Dis. 2018, 62, 1767–1775. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- LoPachin, R.M.; Gavin, T.; Petersen, D.R.; Barber, D.S. Molecular mechanisms of 4-hydroxy-2-nonenal and acrolein toxicity: Nucleophilic targets and adduct formation. Chem. Res. Toxicol. 2009, 22, 1499–1508. [Google Scholar] [CrossRef] [PubMed]
- Götz, M.E.; Künig, G.; Riederer, P.; Youdim, M.B. Oxidative stress: Free radical production in neural degeneration. Pharmacol. Ther. 1994, 63, 37–122. [Google Scholar] [CrossRef]
- Keller, J.N.; Pang, Z.; Geddes, J.W.; Begley, J.G.; Germeyer, A.; Waeg, G.; Mattson, M.P. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid beta-peptide: Role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 1997, 69, 273–284. [Google Scholar] [CrossRef] [PubMed]
- Mark, R.J.; Lovell, M.A.; Markesbery, W.R.; Uchida, K.; Mattson, M.P. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J. Neurochem. 1997, 68, 255–264. [Google Scholar] [CrossRef] [PubMed]
- Bowling, A.C.; Beal, M.F. Bioenergetic and oxidative stress in neurodegenerative diseases. Life Sci. 1995, 56, 1151–1171. [Google Scholar] [CrossRef]
- Keller, J.N.; Mattson, M.P. Roles of lipid peroxidation in modulation of cellular signaling pathways, cell dysfunction, and death in the nervous system. Rev. Neurosci. 1998, 9, 105–116. [Google Scholar] [CrossRef] [PubMed]
- Head, E.; Liu, J.; Hagen, T.M.; Muggenburg, B.A.; Milgram, N.W.; Ames, B.N.; Cotman, C.W. Oxidative damage increases with age in a canine model of human brain aging. J. Neurochem. 2002, 82, 375–381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Williams, T.I.; Lynn, B.C.; Markesbery, W.R.; Lovell, M.A. Increased levels of 4-hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in mild cognitive impairment and early Alzheimer’s disease. Neurobiol. Aging 2006, 27, 1094–1099. [Google Scholar] [CrossRef] [PubMed]
- Shibata, N.; Yamada, S.; Uchida, K.; Hirano, A.; Sakoda, S.; Fujimura, H.; Sasaki, S.; Iwata, M.; Toi, S.; Kawaguchi, M.; et al. Accumulation of protein-bound 4-hydroxy-2-hexenal in spinal cords from patients with sporadic amyotrophic lateral sclerosis. Brain Res. 2004, 1019, 170–177. [Google Scholar] [CrossRef] [PubMed]
- Long, E.K.; Murphy, T.C.; Leiphon, L.J.; Watt, J.; Morrow, J.D.; Milne, G.L.; Howard, J.R.H.; Picklo, M.J. Trans-4-hydroxy-2-hexenal is a neurotoxic product of docosahexaenoic (22:6; n − 3) acid oxidation. J. Neurochem. 2008, 105, 714–724. [Google Scholar] [CrossRef]
- Keller, J.N.; Hanni, K.B.; Markesbery, W.R. 4-hydroxynonenal increases neuronal susceptibility to oxidative stress. J. Neurosci. Res. 1999, 58, 823–830. [Google Scholar] [CrossRef]
- Hong, L.; Yi, W.; Liangliang, C.; Juncheng, H.; Qin, W.; Xiaoxiang, Z. Hypoglycaemic and hypolipidaemic activities of sesamin from sesame meal and its ability to ameliorate insulin resistance in KK-Ay mice. J. Sci. Food Agric. 2013, 93, 1833–1838. [Google Scholar] [CrossRef]
- D’Mello, C.; Swain, M.G. Liver-brain inflammation axis. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301, G749–G761. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rapp, M.A.; Schnaider-Beeri, M.; Wysocki, M.; Guerrero-Berroa, E.; Grossman, H.T.; Heinz, A.; Haroutunian, V. Cognitive decline in patients with dementia as a function of depression. Am. J. Geriatr. Psychiatry 2011, 19, 357–363. [Google Scholar] [CrossRef] [PubMed]
- Savva, G.M.; Zaccai, J.; Matthews, F.E.; Davidson, J.E.; McKeith, I.; Brayne, C. Medical Research Council Cognitive Function and Ageing Study. Prevalence, correlates and course of behavioural and psychological symptoms of dementia in the population. Br. J. Psychiatry 2009, 194, 212–219. [Google Scholar] [CrossRef] [PubMed]
- Ikeda, M.; Fukuhara, R.; Shigenobu, K.; Hokoishi, K.; Maki, N.; Nebu, A.; Komori, K.; Tanabe, H. Dementia associated mental and behavioural disturbances in elderly people in the community: Findings from the first Nakayama study. J. Neurol. Neurosurg. Psychiatry 2004, 75, 146–148. [Google Scholar] [PubMed]
- Ownby, R.L.; Crocco, E.; Acevedo, A.; John, V.; Loewenstein, D. Depression and risk for Alzheimer disease: Systematic review, meta-analysis, and metaregression analysis. Arch. Gen. Psychiatry 2006, 63, 530–538. [Google Scholar] [CrossRef] [PubMed]
- Shimada, A.; Tsuzuki, M.; Keino, H.; Satoh, M.; Chiba, Y.; Saitoh, Y.; Hosokawa, M. Apical vulnerability to dendritic retraction in prefrontal neurones of ageing SAMP10 mouse: A model of cerebral degeneration. Neuropathol. Appl. Neurobiol. 2006, 32, 1–14. [Google Scholar] [CrossRef] [PubMed]
YC | YS0.05 | OC | OS0.02 | OS0.05 | |
---|---|---|---|---|---|
Body weight (g) | 30.1 ± 0.3 ab | 28.8 ± 0.4 a | 30.9 ± 0.9 ab | 33.2 ± 1.5 bc | 35.0 ± 1.1 c |
Brain weight (mg) | 467.7 ± 0.3 a | 467.2 ± 0.4 a | 469.5 ± 0.4 a | 465.6 ± 0.5 a | 468.8 ± 0.3 a |
Final survival rate (%) | 90 | 85 | 64 | 75 | 64 |
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Shimoyoshi, S.; Takemoto, D.; Ono, Y.; Kitagawa, Y.; Shibata, H.; Tomono, S.; Unno, K.; Wakabayashi, K. Sesame Lignans Suppress Age-Related Cognitive Decline in Senescence-Accelerated Mice. Nutrients 2019, 11, 1582. https://doi.org/10.3390/nu11071582
Shimoyoshi S, Takemoto D, Ono Y, Kitagawa Y, Shibata H, Tomono S, Unno K, Wakabayashi K. Sesame Lignans Suppress Age-Related Cognitive Decline in Senescence-Accelerated Mice. Nutrients. 2019; 11(7):1582. https://doi.org/10.3390/nu11071582
Chicago/Turabian StyleShimoyoshi, Satomi, Daisuke Takemoto, Yoshiko Ono, Yoshinori Kitagawa, Hiroshi Shibata, Susumu Tomono, Keiko Unno, and Keiji Wakabayashi. 2019. "Sesame Lignans Suppress Age-Related Cognitive Decline in Senescence-Accelerated Mice" Nutrients 11, no. 7: 1582. https://doi.org/10.3390/nu11071582