Benefits of Erinacines from Different Cultivate Formulas on Cognitive Deficits and Anxiety-Like Behaviour in Mice with Trimethyltin-Induced Toxicity

Main Article Content

Yaovapa Aramsirirujiwet
Teerachart Leepasert
Danita Piamariya
Wachiryah Thong-asa

Abstract

We investigated the neurological effects of the varied erinacine composition of different mycelia cultures in mice with trimethyltin (TMT)-induced neurodegeneration. Forty male ICR mice were randomly divided into five groups of Sham-veh, TMT-veh, TMT-EME, TMT-EMR and TMT-EME/R. The TMT groups received 2.6 mg/kg one-time intraperitoneal injections of TMT. Oral dosages of 200 mg/kg erinacine combination from each Hericium erinaceus mycelia (EM) cultivated formula (100% eucalyptus wood [E], 100% rubber wood [R], or 40% eucalyptus wood/60% rubber wood [E/R]) were given for 2 weeks. Spatial learning, memory, flexibility, and anxious behaviour were evaluated alongside brain tissues’ oxidative status and histological analyses. Erinacine composition from EME/R exhibited significant positive effects on spatial learning, memory, flexibility, and anxiety (p < 0.05). These findings emerged concurrently with the significant mitigation of hippocampal lipid peroxidation, CA1 hippocampal, cortical neuron, and corpus callosum white matter degeneration (p < 0.05). These neurological benefits were associated with the EME/R composition of erinacine A, C, D, G, H, I, K and R. The best neuroprotective effect against TMT-induced neurodegeneration in mice is offered by the EME/R erinacine composition according to its anti-lipid peroxidation, its nurturing effect on neuronal and white matter, and mitigation of behavioral deficits.

Article Details

How to Cite
Benefits of Erinacines from Different Cultivate Formulas on Cognitive Deficits and Anxiety-Like Behaviour in Mice with Trimethyltin-Induced Toxicity . (2023). Tropical Life Sciences Research, 34(3), 165–183. https://doi.org/10.21315/tlsr2023.34.3.9
Section
Original Article

References

Butterfield D A, Howard B J and LaFontaine M A. (2001). Brain oxidative stress in animal models of accelerated aging and the age-related neurodegenerative disorders, Alzheimer’s disease and Huntington’s disease. Current Medicinal Chemistry 8: 815–828. https://doi.org/10.2174/0929867013373048

Chiu C -H, Chyau C -C, Chen C -C, Lee L -Y, Chen W -P, Liu J -L, Lin W -H and Mong M -C. (2018). Erinacine A-Enriched Hericium erinaceus Mycelium produces antidepressant-like effects through modulating BDNF/PI3K/Akt/GSK-3? signaling in mice. International Journal of Molecular Sciences 19: 341. https://doi.org/10.3390/ijms19020341

Chong Z Z, Li F and Maiese K. (2005). Oxidative stress in the brain: Novel cellular targets that govern survival during neurodegenerative disease Progress in Neurobiology 75(3): 207–246. https://doi.org/10.1016/j.pneurobio.2005.02.004

Darmasiwi S, Aramsirirujiwet Y and Kimkong I. (2022). Biological activities and chemical profile of Hericium erinaceus mycelium cultivated on mixed red and white jasmine rice. Food Science and Technology 42: e08022. https://doi.org/10.1590/fst.08022

Dillon G M, Qu X, Marcus J N and Dodart J C. (2008). Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiology of Learning and Memory 90(2): 426–433. https://doi.org/10.1016/j.nlm.2008.05.008

Durmus A, Durmus I, Bender O and Karatepe O. (2021). The effect of Hericium erinaceum on the prevention of chemically induced experimental colitis in rats. Korean Journal of Internal Medicine 36(Suppl. 1): S44–S52. https://doi.org/10.3904/kjim.2019.050

Geloso M C, Corvino V and Michetti F. (2011). Trimethyltin-induced hippocampal degeneration as a tool to investigate neurodegenerative processes. Neurochemistry International 58(7): 729–738. https://doi.org/10.1016/j.neuint.2011.03.009

Hiwatashi K, Kosaka Y, Suzuki N, Hata K, Mukaiyama T, Sakamoto K, Shirakawa H and Komai M. (2010). Yamabushitake mushroom (Hericium erinaceus) improved lipid metabolism in mice fed a high-fat diet. Bioscience, Biotechnology, and Biochemistry 74(7): 1447–1451. https://doi.org/10.1271/bbb.100130

Hock C, Heese K, Hulette C, Rosenberg C and Otten U (2000). Region-specific neurotrophin imbalances in Alzheimer disease: Decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurology 57(6): 846–851. https://doi.org/10.1001/archneur.57.6.846

Holahan M R and Routtenberg A. (2011). Lidocaine injections targeting CA3 hippocampus impair long-term spatial memory and prevent learning-induced mossy fiber remodeling. Hippocampus 21(5): 532–540. https://doi.org/10.1002/hipo.20786

Izquierdo A, Brigman J L, Radke A K, Rudebeck P H and Holmes A. (2016). The neural basis of reversal learning: An updated perspective. Neuroscience 345: 12–26. https://doi.org/10.1016/j.neuroscience.2016.03.021

Jeong E S, Bajgai J, You I S, Rahman M H, Fadriquela A, Sharma S, Kwon H U, Lee S Y, Kim C S and Lee K J. (2021). Therapeutic effects of hydrogen gas inhalation on trimethyltin-induced neurotoxicity and cognitive impairment in the C57BL/6 mice model. International Journal of Molecular Sciences 22(24): 13313. https://doi.org/10.3390/ijms222413313

Kawagishi H, Shimada A, Shirai R, Okamoto K, Ojima F, Sakamoto H, Ishiguro Y and Furukawa S. (1994). Erinacines A, B and C, strong stimulators of nerve growth factor (NGF)-synthesis, from the mycelia of Hericium erinaceum. Tetrahedron Letters 35(10): 1569–1572. https://doi.org/10.1016/S0040-4039(00)76760-8

Kim S, Chen J, Cheng T, Gindulyte A, He J, He S, Li Q, Shoemaker B A, Thiessen P A, Yu B, Zaslavsky L, Zhang J and Bolton E E. (2020). PubChem in 2021: New data content and improved web interfaces. Nucleic Acids Research 49(D1): D1388– D1395. https://doi.org/10.1093/nar/gkaa971

Lee E W, Shizuki K, Hosokawa S, Suzuki M, Suganuma H, Inakuma T, Li J, Ohnishi- Kameyama M, Nagata T, Furukawa S and Kawagishi H. (2000). Two novel diterpenoids, erinacines H and I from the mycelia of Hericium erinaceum. Bioscience, Biotechnology, and Biochemistry 64(11): 2402–2405. https://doi.org/10.1271/bbb.64.2402

Lee S, Yang M, Kim J, Kang S, Kim J, Kim J C, Jung C, Shin T, Kim S H and Moon C. (2016). Trimethyltin-induced hippocampal neurodegeneration: A mechanism-based review. Brain Research Bulletin 125: 187–199. https://doi.org/10.1016/j.brainresbull.2016.07.010

Lee S C, Zhao M L, Hirano A and Dickson D W. (1999). Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: Association with Hirano bodies, neurofibrillary tangles, and senile plaques. Journal of Neuropathology & Experimental Neurology 58(11): 1163–1169. https://doi.org/10.1097/00005072-199911000-00006

Li E, Kim D H, Cai M, Lee S, Kim Y, Lim E, Ryu J H, Unterman T G and Park S. (2011). Hippocampus-dependent spatial learning and memory are impaired in growth hormone-deficient spontaneous dwarf rats. Endocrine Journal 58(4): 257–267. https://doi.org/10.1507/endocrj.K11E-006

Li G, Yu K, Li F, Xu K, Li J, He S, Cao S and Tan G. (2014). Anticancer potential of Hericium erinaceus extracts against human gastrointestinal cancers. Journal of Ethnopharmacology 153(2): 521–530. https://doi.org/10.1016/j.jep.2014.03.003

Li I C, Lee L Y, Tzeng T T, Chen W P, Chen Y P, Shiao Y J and Chen C C. (2018). Neurohealth properties of Hericium erinaceus mycelia enriched with erinacines. Behavioural Neurology 2018: 5802634. https://doi.org/10.1155/2018/5802634

Ma B-J, Shen J-W, Yu H-Y, Ruan Y, Wu T-T and Zhao X. (2010). Hericenones and erinacines: Stimulators of nerve growth factor (NGF) biosynthesis in Hericium erinaceus. Mycology 1(2): 92–98. https://doi.org/10.1080/21501201003735556

Manyagasa N and Thong-asa W. (2019). The effects of p-hydroxycinnamic acid in ameliorating spatial learning and flexibility deficits in rats with chronic cerebral hypoperfusion. Sains Malaysiana 48(12): 2623–2631. https://doi.org/10.17576/jsm-2019-4812-03

Martin E I, Ressler K J, Binder E and Nemeroff C B. (2009). The neurobiology of anxiety disorders: Brain imaging, genetics, and psychoneuroendocrinology. Psychiatric Clinics of North America 32(3): 549–575. https://doi.org/10.1016/j.psc.2009.05.004

Mattila P M, Rinne J O, Helenius H and Roytta M. (1999). Neuritic degeneration in the hippocampus and amygdala in Parkinson’s disease in relation to Alzheimer pathology. Acta Neuropathologica 98: 157–164. https://doi.org/10.1007/s004010051064

Nagano M, Shimizu K, Kondo R, Hayashi C, Sato D, Kitagawa K and Ohnuki K. (2010). Reduction of depression and anxiety by 4 weeks Hericium erinaceus intake. Biomedical Research 31: 231–237. https://doi.org/10.2220/biomedres.31.231

Ogita K, Nitta Y, Watanabe M, Nakatani Y, Nishiyama N, Sugiyama C and Yoneda Y. (2004). In vivo activation of c-Jun N-terminal kinase signaling cascade prior to granule cell death induced by trimethyltin in the dentate gyrus of mice. Neuropharmacology 47: 619–630. https://doi.org/10.1016/j.neuropharm.2004.06.012

Paxinos G and Franklin K. (2008). The mouse brain in stereotaxic coordinates, 3rd ed. Elsevier.

Sakamula R and Thong-asa W. (2018). Neuroprotective effect of p-coumaric acid in mice with cerebral ischemia reperfusion injuries. Metabolic Brain Disease 33: 765–773. https://doi.org/10.1007/s11011-018-0185-7

Shi L, Adams M A, Long A, Carter C C, Bennett C, Sonntag W E, Nicolle M M, Robbins M, D’Agostino R and Brunso-Bechtold J K. (2006). Spatial learning and memory deficits after whole-brain irradiation are associated with changes in NMDA receptor subunits in the hippocampus. Radiation Research 166(6): 892–899. https://doi.org/10.1667/RR0588.1

Silvers J M, Tokunaga S, Berry R B, White A M and Matthews D B. (2003). Impairments in spatial learning and memory: Ethanol, allopregnanolone, and the hippocampus. Brain Brain Research Reviews 43(3): 275–284. https://doi.org/10.1016/j.brainresrev.2003.09.002

Somredngan S and Thong-asa W. (2017). Neurological changes in vulnerable brain areas of chronic cerebral hypoperfusion mice. Annals of Neurosciences 24: 233–242. https://doi.org/10.1159/000481789

Sze C I, Troncoso J C, Kawas C, Mouton P, Price D L and Martin L J. (1997). Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. Journal of Neuropathology & Experimental Neurology 56(8): 933–944. https://doi.org/10.1097/00005072-199708000-00011

Thong-Asa W and Bullangpoti V. (2020). Neuroprotective effects of Tiliacora triandra leaf extract in a mice model of cerebral ischemia reperfusion. Avicenna Journal of Phytomedicine 10: 202–212.

Thong-Asa W, Prasartsri S, Klomkleaw N and Thongwan N. (2020). The neuroprotective effect of betanin in trimethyltin-induced neurodegeneration in mice. Metabolic Brain Disease 35: 1395–1405. https://doi.org/10.1007/s11011-020-00615-1

Thong-Asa W, Tumkiratiwong P, Bullangpoti V, Kongnirundonsuk K and Tilokskulchai K. (2017). Tiliacora triandra (Colebr.) Diels leaf extract enhances spatial learning and learning flexibility, and prevents dentate gyrus neuronal damage induced by cerebral ischemia/reperfusion injury in mice. Avicenna Journal of Phytomedicine 7: 389–400.

Wang J C, Hu S H, Wang J T, Chen K S and Chia Y C. (2005). Hypoglycemic effect of extract of Hericium erinaceus. Journal of the Science of Food and Agriculture 85(4): 641–646. https://doi.org/10.1002/jsfa.1928

Wang M, Li B, Wang C, Chen Y and Zuo Z. (2008). The concentration-dependent induction of cell death by trimethyltin chloride in rat liver epithelial IAR20 cells. Toxicology in Vitro 22(5): 1136–1142. https://doi.org/10.1016/j.tiv.2008.02.021

Win-Shwe T T, Yamamoto S, Fujitani Y, Hirano S and Fujimaki H. (2008). Spatial learning and memory function-related gene expression in the hippocampus of mouse exposed to nanoparticle-rich diesel exhaust. Neurotoxicology 29: 940–947. https://doi.org/10.1016/j.neuro.2008.09.007

Yoneyama M, Seko K, Kawada K, Sugiyama C and Ogita K. (2009). High susceptibility of cortical neural progenitor cells to trimethyltin toxicity: Involvement of both caspases and calpain in cell death. Neurochemistry International 55(4): 257–264. https://doi.org/10.1016/j.neuint.2009.03.008