Effects of Astaxanthin on Learning and Memory Disorders and Oxidative Damage Induced by Ethanol in the Hippocampal Area in Mice

Hajizadeh Moghaddam, Akbar; Samei, Farhad; Khanjani Jelodar, Sedigheh; Malekzadeh Estalkhi, Fatemeh

doi:10.22034/nbr.11.2.19

Effects of Astaxanthin on Learning and Memory Disorders and Oxidative Damage Induced by Ethanol in the Hippocampal Area in Mice

Authors

Akbar Hajizadeh Moghaddam

Farhad Samei

Sedigheh Khanjani Jelodar

Fatemeh Malekzadeh Estalkhi

University of Mazandaran

https://doi.org/10.22034/nbr.11.2.19

Abstract

Long-term ethanol consumption leads to the destruction of neurons in the central nervous system and cells in the hippocampus by causing oxidative stress. Astaxanthin (ATX) is a carotenoid that serves as an antioxidant and anti-inflammatory agent. This study sought to examine the impacts of astaxanthin on learning and memory impairments and oxidative damage within the hippocampus of mice induced by ethanol. 35 mice were divided into five groups (n=7): the control group didn't receive any treatment. The positive control group received 20 mg/kg ATX. The ethanol group received 20% ethanol, and two ATX treatment groups received doses of 10 and 20 mg/kg, which first received 20% ethanol and then ATX. All treatments were done orally for 14 consecutive days. In this research, the novel object recognition test (NORT), malondialdehyde (MDA) and dopamine (DA) levels, and activities of catalase (CAT) and superoxide dismutase (SOD) were analyzed in the hippocampus of mice. Ethanol consumption decreased the discrimination index in NORT, activities of CAT and SOD, and increased the levels of DA and MDA, compared to the control group. ATX treatment led to an increase in the discrimination index in NORT, activities of CAT and SOD, and a decrease in the levels of DA and MDA, compared to the ethanol group. Results showed astaxanthin's antioxidant properties can improve ethanol-induced cognitive defects and oxidative damage. Therefore, astaxanthin can be used as a potential food and drug supplement to reduce ethanol-induced disorders.

Keywords

Astaxanthin

Ethanol

Hippocampus

Cognitive impairment

20.1001.1.24236330.1403.11.2.2.4

1. Abrahao, K. P., Salinas, A. G., & Lovinger, D. M. (2017). Alcohol and the brain: neuronal molecular targets, synapses, and circuits. Neuron, 96(6), 1223-1238. https://doi.org/10.1016/j.neuron.2017.10.032
2. Antunes, M., & Biala, G. (2012). The novel object recognition memory: neurobiology, test procedure, and its modifications. Cognitive processing, 13, 93-110. https://doi.org/10.1007/s10339-011-0430-z
3. Banerjee, N. (2014). Neurotransmitters in alcoholism: A review of neurobiological and genetic studies. Indian journal of human genetics, 20(1), 20. https://doi.org/10.4103%2F0971-6866.132750
4. Bigdeli, M. R., Rasoulian, B., & Meratan, A. A. (2009). In vivo normobaric hyperoxia preconditioning induces different degrees of antioxidant enzymes activities in rat brain tissue. European Journal of Pharmacology, 611(1-3), 22-29. https://doi.org/10.1016/j.ejphar.2009.03.034
5. Chang, M. X., & Xiong, F. (2020). Astaxanthin and its effects in inflammatory responses and inflammation-associated diseases: recent advances and future directions. Molecules, 25(22), 5342. https://doi.org/10.3390/molecules25225342
6. Chen, Q., & Hu, P. (2017). Proanthocyanidins prevent ethanol-induced cognitive impairment by suppressing oxidative and inflammatory stress in adult rat brain. Neuroreport, 28(15), 980-986. https://doi.org/10.1097/WNR.0000000000000867
7. Contreras, A., Morales, L., & Del Olmo, N. (2019). The intermittent administration of ethanol during the juvenile period produces changes in the expression of hippocampal genes and proteins and deterioration of spatial memory. Behavioural Brain Research, 372, 112033. https://doi.org/10.1016/j.bbr.2019.112033
8. Coune, F., Silvestre de Ferron, B., González‐Marín, M. C., Antol, J., Naassila, M., & Pierrefiche, O. (2017). Resistance to ethanol sensitization is associated with a loss of synaptic plasticity in the hippocampus. Synapse, 71(2), e21899. https://doi.org/10.1002/syn.21899
9. Deehan Jr, G. A., Knight, C. P., Waeiss, R. A., Engleman, E. A., Toalston, J. E., McBride, W. J., ... & Rodd, Z. A. (2016). Peripheral administration of ethanol results in a correlated increase in dopamine and serotonin within the posterior ventral tegmental area. Alcohol and Alcoholism, 51(5), 535-540. https://doi.org/10.1093/alcalc/agw037
10. Ekpe, L., Inaku, K., & Ekpe, V. (2018). Antioxidant effects of astaxanthin in various diseases—A review. J. Mol. Pathophysiol, 7(1), 1-6. 10.5455/jmp.20180627120817
11. Esterbauer, H., & Cheeseman, K. H. (1990). [42] Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. In Methods in enzymology (Vol. 186, pp. 407-421). Academic Press. https://doi.org/10.1016/0076-6879(90)86134-H
12. Fakhri, S., Yosifova Aneva, I., Farzaei, M. H., & Sobarzo-Sánchez, E. (2019). The neuroprotective effects of astaxanthin: therapeutic targets and clinical perspective. Molecules, 24(14), 2640. https://doi.org/10.3390/molecules24142640
13. Fan, M., Song, C., Wang, T., Li, L., Dong, Y., Jin, W., & Lu, P. (2015). Protective effects of lithium chloride treatment on repeated cerebral ischemia–reperfusion injury in mice. Neurological Sciences, 36, 315-321. https://doi.org/10.1007/s10072-014-1943-x
14. Fang, Q., Guo, S., Zhou, H., Han, R., Wu, P., & Han, C. (2017). Astaxanthin protects against early burn-wound progression in rats by attenuating oxidative stress-induced inflammation and mitochondria-related apoptosis. Scientific reports, 7(1), 41440. https://doi.org/10.1038/srep41440
15. Goc, Z., Szaroma, W., Kapusta, E., & Dziubek, K. (2017). Protective effects of melatonin on the activity of SOD, CAT, GSH-Px and GSH content in organs of mice after administration of SNP. Chin J Physiol, 60(1), 1-10. https://doi.org/10.4077/cjp.2017.baf435
16. Grimmig, B., Kim, S. H., Nash, K., Bickford, P. C., & Douglas Shytle, R. (2017). Neuroprotective mechanisms of astaxanthin: a potential therapeutic role in preserving cognitive function in age and neurodegeneration. Geroscience, 39, 19-32. https://doi.org/10.1007/s11357-017-9958-x
17. Hajizadeh, E., Khezri, S., & Piri, M. (2014). Influence Of Ethanol On Amnesia And State-Dependent Learning Induced By Scopolamine In Male Mouse.
18. Hernández, J. A., López-Sánchez, R. C., & Rendón-Ramírez, A. (2016). Lipids and oxidative stress associated with ethanol-induced neurological damage. Oxidative medicine and cellular longevity, 2016. https://doi.org/10.1155/2016/1543809
19. Hwa, L. S., Chu, A., Levinson, S. A., Kayyali, T. M., DeBold, J. F., & Miczek, K. A. (2011). Persistent escalation of alcohol drinking in C57BL/6J mice with intermittent access to 20% ethanol. Alcoholism: Clinical and Experimental Research, 35(11), 1938-1947.
https://doi.org/10.1111/j.1530-0277.2011.01545.x
20. Jeong, J. S., Jeon, H., Ko, K. M., Chung, B., & Choi, G. W. (2012). Production of anhydrous ethanol using various PSA (Pressure Swing Adsorption) processes in pilot plant. Renewable Energy, 42, 41-45. https://doi.org/10.1016/j.renene.2011.09.027
21. Le Dare, B., Lagente, V., & Gicquel, T. (2019). Ethanol and its metabolites: update on toxicity, benefits, and focus on immunomodulatory effects. Drug metabolism reviews, 51(4), 545-561. https://doi.org/10.1080/03602532.2019.1679169
22. Li, J., Guo, C., & Wu, J. (2020). Astaxanthin in liver health and disease: a potential therapeutic agent. Drug design, development and therapy, 2275-2285. https://doi.org/10.2147/DDDT.S230749
23. Mæhre, H. K., Dalheim, L., Edvinsen, G. K., Elvevoll, E. O., & Jensen, I. J. (2018). Protein determination—method matters. Foods, 7(1), 5. https://doi.org/10.3390/foods7010005
24. Manabe, Y., Komatsu, T., Seki, S., & Sugawara, T. (2018). Dietary astaxanthin can accumulate in the brain of rats. Bioscience, Biotechnology, and Biochemistry, 82(8), 1433-1436. https://doi.org/10.1080/09168451.2018.1459467
25. Perera, C. O., & Yen, G. M. (2007). Functional properties of carotenoids in human health. International Journal of Food Properties, 10(2), 201-230. https://doi.org/10.1080/10942910601045271
26. Pisoschi, A. M., Pop, A., Iordache, F., Stanca, L., Predoi, G., & Serban, A. I. (2021). Oxidative stress mitigation by antioxidants-an overview on their chemistry and influences on health status. European Journal of Medicinal Chemistry, 209, 112891. https://doi.org/10.1016/j.ejmech.2020.112891
27. Squeglia, L. M., Jacobus, J., & Tapert, S. F. (2014). The effect of alcohol use on human adolescent brain structures and systems. Handbook of clinical neurology, 125, 501-510. https://doi.org/10.1016/B978-0-444-62619-6.00028-8
28. Stachowiak, B., & Szulc, P. (2021). Astaxanthin for the food industry. Molecules, 26(9), 2666. https://doi.org/10.3390/molecules26092666
29. Vetreno, R. P., & Crews, F. T. (2015). Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning. Frontiers in neuroscience, 9, 35. https://doi.org/10.3389/fnins.2015.00035
30. Vetreno, R. P., & Crews, F. T. (2015). Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning. Frontiers in neuroscience, 9, 35. https://doi.org/10.3389/fnins.2015.00035
31. Wu, D., & Cederbaum, A. I. (2003). Alcohol, oxidative stress, and free radical damage. Alcohol research & health, 27(4), 277. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668865/
32. Xing, Y., & Zou, D. (2018). Ethanol-induced cognitive dysfunction is associated with alterations in the mammalian target of rapamycin signalling pathway in the hippocampus of male mice. Neuroreport, 29(14), 1230-1237. https://doi.org/10.1097/WNR.0000000000001104
33. Yang, K., Broussard, J. I., Levine, A. T., Jenson, D., Arenkiel, B. R., & Dani, J. A. (2017). Dopamine receptor activity participates in hippocampal synaptic plasticity associated with novel object recognition. European Journal of Neuroscience, 45(1), 138-146. https://doi.org/10.1111/ejn.13406
34. Zhao, Y. N., Wang, F., Fan, Y. X., Ping, G. F., Yang, J. Y., & Wu, C. F. (2013). Activated microglia are implicated in cognitive deficits, neuronal death, and successful recovery following intermittent ethanol exposure. Behavioural brain research, 236, 270-282. https://doi.org/10.1016/j.bbr.2012.08.052
35. مافی اسماعیلی, مهین, خسروی, اسماعیلی, بنانج, صولتی, & جلال. (2022). ارزیابی فعالیت ضد پارکینسونی آستاگزانتین در شرایط برون تنی ودرون تنی. مجله دانشکده پزشکی دانشگاه علوم پزشکی مشهد, 65(3), 1387-1400.‎
https://doi.org/10.22038/mjms.2022.65697.3865