Spirulina maxima Extract Ameliorates Learning and Memory Impairments via Inhibiting GSK-3β Phosphorylation Induced by Intracerebroventricular Injection of Amyloid-β 1–42 in Mice
Abstract
:1. Introduction
2. Results
2.1. SM70EE Ameliorates Learning and Memory Impairments via Inhibiting Aβ Accumulation Induced by I.C.V. Injection of Aβ1–42 in Mice
2.2. SM70EE Suppresses Hippocampal Oxidative Stress via Upregulating Antioxidant Enzymes Reduced by I.C.V. Injection of Aβ1–42
2.3. SM70EE Inhibits Phosphorylation of GSK-3β in Mouse Hippocampus via Promoting the Activation of the BDNF/PI3K/Akt Signaling Pathways Reduced by I.C.V. Injection of Aβ1–42
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Animals and Experimental Design
4.3. I.C.V. Injection of Aβ1–42
4.4. Passive Avoidance Test
4.5. Morris Water Maze Test
4.6. Biochemical Analysis
4.7. Western Blot Analysis
4.8. Statistical Analysis
5. Conclusions
Author Contributions
Conflicts of Interest
References
- Ross, C.A.; Poirier, M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 2004, 10, S10–S17. [Google Scholar] [CrossRef] [PubMed]
- Mattson, M.P. Pathways towards and away from Alzheimer’s disease. Nature 2004, 430, 631–639. [Google Scholar] [CrossRef] [PubMed]
- Van Oijen, M.; Hofman, A.; Soares, H.D.; Koudstaal, P.J.; Breteler, M.M. Plasma Aβ1–40 and Aβ1–42 and the risk of dementia: A prospective case-cohort study. Lancet Neurol. 2006, 5, 655–660. [Google Scholar] [CrossRef]
- Ly, P.T.; Wu, Y.; Zou, H.; Wang, R.; Zhou, W.; Kinoshita, A.; Zhang, M.; Yang, Y.; Cai, F.; Woodgett, J.; et al. Inhibition of GSK3β-mediated BACE1 expression reduces alzheimer-associated phenotypes. J. Clin. Investig. 2013, 123, 224–235. [Google Scholar] [CrossRef] [PubMed]
- Jhoo, J.H.; Kim, H.C.; Nabeshima, T.; Yamada, K.; Shin, E.J.; Jhoo, W.K.; Kim, W.; Kang, K.S.; Jo, S.A.; Woo, J.I. β-amyloid (1–42)-induced learning and memory deficits in mice: Involvement of oxidative burdens in the hippocampus and cerebral cortex. Behav. Brain Res. 2004, 155, 185–196. [Google Scholar] [CrossRef] [PubMed]
- Lambert, M.P.; Barlow, A.K.; Chromy, B.A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T.E.; Rozovsky, I.; Trommer, B.; Viola, K.L.; et al. Diffusible, nonfibrillar ligands derived from Aβ1–42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 1998, 95, 6448–6453. [Google Scholar] [CrossRef] [PubMed]
- Castro, A.; Martinez, A. Targeting β-amyloid pathogenesis through acetylcholinesterase inhibitors. Curr. Pharm. Des. 2006, 12, 4377–4387. [Google Scholar] [CrossRef] [PubMed]
- Bartus, R.T.; Dean, R.L.; Beer, B.; Lippa, A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982, 217, 408–414. [Google Scholar] [CrossRef] [PubMed]
- Hu, W.; Gray, N.W.; Brimijoin, S. Amyloid-β increases acetylcholinesterase expression in neuroblastoma cells by reducing enzyme degradation. J. Neurochem. 2003, 86, 470–478. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.; Kumar, A. Microglial inhibitory mechanism of coenzyme Q10 against Aβ1–42 induced cognitive dysfunctions: Possible behavioral, biochemical, cellular, and histopathological alterations. Front. Pharmacol. 2015, 6, 268. [Google Scholar] [CrossRef] [PubMed]
- Martin, J.B. Molecular basis of the neurodegenerative disorders. N. Engl. J. Med. 1999, 340, 1970–1980. [Google Scholar] [CrossRef] [PubMed]
- Huang, W.J.; Zhang, X.; Chen, W.W. Role of oxidative stress in Alzheimer’s disease. Biomed. Rep. 2016, 4, 519–522. [Google Scholar] [CrossRef] [PubMed]
- Balazs, L.; Leon, M. Evidence of an oxidative challenge in the Alzheimer’s brain. Neurochem. Res. 1994, 19, 1131–1137. [Google Scholar] [CrossRef] [PubMed]
- Embi, N.; Rylatt, D.B.; Cohen, P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Eur. J. Biochem. 1980, 107, 519–527. [Google Scholar] [CrossRef] [PubMed]
- Takashima, A. GSK-3 is essential in the pathogenesis of Alzheimer’s disease. J. Alzheimers Dis. 2006, 9, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Hetman, M.; Cavanaugh, J.E.; Kimelman, D.; Xia, Z. Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 2000, 20, 2567–2574. [Google Scholar] [PubMed]
- Ryder, J.; Su, Y.; Ni, B. Akt/GSK3β serine/threonine kinases: Evidence for a signalling pathway mediated by familial Alzheimer’s disease mutations. Cell Signal. 2004, 16, 187–200. [Google Scholar] [CrossRef] [PubMed]
- Brunet, A.; Datta, S.R.; Greenberg, M.E. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 2001, 11, 297–305. [Google Scholar] [CrossRef]
- Kitagishi, Y.; Nakanishi, A.; Ogura, Y.; Matsuda, S. Dietary regulation of PI3K/Akt/GSK-3β pathway in Alzheimer’s disease. Alzheimers Res. Ther. 2014, 6, 35. [Google Scholar] [CrossRef] [PubMed]
- Poo, M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2001, 2, 24–32. [Google Scholar] [CrossRef] [PubMed]
- Thaakur, S.R.; Jyothi, B. Effect of spirulina maxima on the haloperidol induced tardive dyskinesia and oxidative stress in rats. J. Neural. Transm. 2007, 114, 1217–1225. [Google Scholar] [CrossRef] [PubMed]
- Salazar, M.; Martinez, E.; Madrigal, E.; Ruiz, L.E.; Chamorro, G.A. Subchronic toxicity study in mice fed spirulina maxima. J. Ethnopharmacol. 1998, 62, 235–241. [Google Scholar] [CrossRef]
- Rodriguez-Hernandez, A.; Ble-Castillo, J.L.; Juarez-Oropeza, M.A.; Diaz-Zagoya, J.C. Spirulina maxima prevents fatty liver formation in CD-1 male and female mice with experimental diabetes. Life Sci. 2001, 69, 1029–1037. [Google Scholar] [CrossRef]
- Deng, R.; Chow, T.J. Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae spirulina. Cardiovasc. Ther. 2010, 28, e33–e45. [Google Scholar] [CrossRef] [PubMed]
- Koh, E.J.; Seo, Y.J.; Choi, J.; Lee, H.Y.; Kang, D.H.; Kim, K.J.; Lee, B.Y. Spirulina maxima extract prevents neurotoxicity via promoting activation of BDNF/CREB signaling pathways in neuronal cells and mice. Molecules 2017, 22, 1363. [Google Scholar] [CrossRef] [PubMed]
- Morrow, B.A.; Roth, R.H.; Elsworth, J.D. TMT, a predator odor, elevates mesoprefrontal dopamine metabolic activity and disrupts short-term working memory in the rat. Brain Res. Bull. 2000, 52, 519–523. [Google Scholar] [CrossRef]
- Sharma, A.C.; Kulkarni, S.K. Evidence for GABA-BZ receptor modulation in short-term memory passive avoidance task paradigm in mice. Methods. Find. Exp. Clin. Pharmacol. 1990, 12, 175–180. [Google Scholar] [PubMed]
- Selkoe, D.J.; Schenk, D. Alzheimer’s disease: Molecular understanding predicts amyloid-based therapeutics. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 545–584. [Google Scholar] [CrossRef] [PubMed]
- Alkadhi, K.A.; Alzoubi, K.H.; Srivareerat, M.; Tran, T.T. Elevation of BACE in an Aβ rat model of Alzheimer’s disease: Exacerbation by chronic stress and prevention by nicotine. Int. J. Neuropsychopharmacol. 2012, 15, 223–233. [Google Scholar] [CrossRef] [PubMed]
- Badshah, H.; Kim, T.H.; Kim, M.O. Protective effects of anthocyanins against amyloid β-induced neurotoxicity in vivo and in vitro. Neurochem. Int. 2015, 80, 51–59. [Google Scholar] [CrossRef] [PubMed]
- Everitt, B.J.; Robbins, T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 1997, 48, 649–684. [Google Scholar] [CrossRef] [PubMed]
- Cavallucci, V.; D’Amelio, M.; Cecconi, F. Aβ toxicity in Alzheimer’s disease. Mol. Neurobiol. 2012, 45, 366–378. [Google Scholar] [CrossRef] [PubMed]
- Behl, C. Alzheimer’s disease and oxidative stress: Implications for novel therapeutic approaches. Prog. Neurobiol. 1999, 57, 301–323. [Google Scholar] [CrossRef]
- Holmquist, L.; Stuchbury, G.; Berbaum, K.; Muscat, S.; Young, S.; Hager, K.; Engel, J.; Munch, G. Lipoic acid as a novel treatment for Alzheimer’s disease and related dementias. Pharmacol. Ther. 2007, 113, 154–164. [Google Scholar] [CrossRef] [PubMed]
- Numakawa, T.; Matsumoto, T.; Numakawa, Y.; Richards, M.; Yamawaki, S.; Kunugi, H. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J. Toxicol. 2011, 2011, 405194. [Google Scholar] [CrossRef] [PubMed]
- Holsinger, R.M.; McLean, C.A.; Beyreuther, K.; Masters, C.L.; Evin, G. Increased expression of the amyloid precursor β-secretase in Alzheimer’s disease. Ann. Neurol. 2002, 51, 783–786. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.B.; Lindholm, K.; Yan, R.; Citron, M.; Xia, W.; Yang, X.L.; Beach, T.; Sue, L.; Wong, P.; Price, D.; et al. Elevated β-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 2003, 9, 3–4. [Google Scholar] [CrossRef] [PubMed]
- Talesa, V.N. Acetylcholinesterase in Alzheimer’s disease. Mech. Ageing Dev. 2001, 122, 1961–1969. [Google Scholar] [CrossRef]
- Prasansuklab, A.; Tencomnao, T. Amyloidosis in Alzheimer’s disease: The toxicity of amyloid β (Aβ), mechanisms of its accumulation and implications of medicinal plants for therapy. Evid. Based Complement. Alternat. Med. 2013, 2013, 413808. [Google Scholar] [CrossRef] [PubMed]
- Park, S.K.; Ha, J.S.; Kim, J.M.; Kang, J.Y.; Lee du, S.; Guo, T.J.; Lee, U.; Kim, D.O.; Heo, H.J. Antiamnesic effect of broccoli (brassica oleracea var. Italica) leaves on amyloid β Aβ1–42-induced learning and memory impairment. J. Agric. Food. Chem. 2016, 64, 3353–3361. [Google Scholar] [CrossRef] [PubMed]
- Calabrese, V.; Sultana, R.; Scapagnini, G.; Guagliano, E.; Sapienza, M.; Bella, R.; Kanski, J.; Pennisi, G.; Mancuso, C.; Stella, A.M.; et al. Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer’s disease. Antioxid. Redox. Signal. 2006, 8, 1975–1986. [Google Scholar] [CrossRef] [PubMed]
- Inestrosa, N.C.; Arenas, E. Emerging roles of wnts in the adult nervous system. Nat. Rev. Neurosci. 2010, 11, 77–86. [Google Scholar] [CrossRef] [PubMed]
- Murphy, K.E.; Park, J.J. Can co-activation of Nrf2 and neurotrophic signaling pathway slow Alzheimer’s disease? Int. J. Mol. Sci. 2017, 18, 1168. [Google Scholar] [CrossRef] [PubMed]
- Weon, J.B.; Yun, B.R.; Lee, J.; Eom, M.R.; Kim, J.S.; Lee, H.Y.; Park, D.S.; Chung, H.C.; Chung, J.Y.; Ma, C.J. The ameliorating effect of steamed and fermented codonopsis lanceolata on scopolamine-induced memory impairment in mice. Evid. Based Complement. Alternat. Med. 2013, 2013, 464576. [Google Scholar] [CrossRef] [PubMed]
- Vorhees, C.V.; Williams, M.T. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1, 848–858. [Google Scholar] [CrossRef] [PubMed]
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Koh, E.-J.; Kim, K.-J.; Song, J.-H.; Choi, J.; Lee, H.Y.; Kang, D.-H.; Heo, H.J.; Lee, B.-Y. Spirulina maxima Extract Ameliorates Learning and Memory Impairments via Inhibiting GSK-3β Phosphorylation Induced by Intracerebroventricular Injection of Amyloid-β 1–42 in Mice. Int. J. Mol. Sci. 2017, 18, 2401. https://doi.org/10.3390/ijms18112401
Koh E-J, Kim K-J, Song J-H, Choi J, Lee HY, Kang D-H, Heo HJ, Lee B-Y. Spirulina maxima Extract Ameliorates Learning and Memory Impairments via Inhibiting GSK-3β Phosphorylation Induced by Intracerebroventricular Injection of Amyloid-β 1–42 in Mice. International Journal of Molecular Sciences. 2017; 18(11):2401. https://doi.org/10.3390/ijms18112401
Chicago/Turabian StyleKoh, Eun-Jeong, Kui-Jin Kim, Ji-Hyeon Song, Jia Choi, Hyeon Yong Lee, Do-Hyung Kang, Ho Jin Heo, and Boo-Yong Lee. 2017. "Spirulina maxima Extract Ameliorates Learning and Memory Impairments via Inhibiting GSK-3β Phosphorylation Induced by Intracerebroventricular Injection of Amyloid-β 1–42 in Mice" International Journal of Molecular Sciences 18, no. 11: 2401. https://doi.org/10.3390/ijms18112401
APA StyleKoh, E. -J., Kim, K. -J., Song, J. -H., Choi, J., Lee, H. Y., Kang, D. -H., Heo, H. J., & Lee, B. -Y. (2017). Spirulina maxima Extract Ameliorates Learning and Memory Impairments via Inhibiting GSK-3β Phosphorylation Induced by Intracerebroventricular Injection of Amyloid-β 1–42 in Mice. International Journal of Molecular Sciences, 18(11), 2401. https://doi.org/10.3390/ijms18112401