Journal of Applied Biological Chemistry

  • Volume 66
  • /
  • Pages.408-415
  • /
  • 2023
  • /
  • 1976-0442(pISSN)
  • /
  • 2234-7941(eISSN)
The Korean Society for Applied Biological Chemistry (한국응용생명화학회)
권호 표지
DOI QR코드

DOI QR Code

Populus tomentiglandulosa protects against amyloid-beta25-35-induced neuronal damage in SH-SY5Y cells

  • Yu Ri Kwon (Department of Food Science and Nutrition, Pusan National University) ;
  • Ji-Hyun Kim (Department of Food Science and Nutrition, Pusan National University) ;
  • Sanghyun Lee (Department of Plant Science and Technology, Chung-Ang University) ;
  • Hyun Young Kim (Department of Food Science and Nutrition, Gyeongsang National University) ;
  • Eun Ju Cho (Department of Food Science and Nutrition, Pusan National University)
  • Received : 2023.08.23
  • Accepted : 2023.10.13
  • Published : 2023.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Alzheimer's disease constitutes a large proportion of all neurodegenerative diseases and is mainly caused by excess aggregation of amyloid beta (Aβ), which results in oxidative stress, inflammation, and apoptosis in the neurons. Populus tomentiglandulosa belongs to the Salicaceae family and is widely distributed in Korea; the antioxidant activities of the extract and fractions from P. tomentiglandulosa have been demonstrated in previous studies. Specifically, the ethyl acetate (EtOAc) fraction of P. tomentiglandulosa (EtOAc-PT) shows the most powerful antioxidative activity. Therefore, the present study investigates the protective effects of EtOAc-PT against neuronal damage in Aβ25-35-stimulated SH-SY5Y cells. EtOAc-PT restored cell viability significantly as well as inhibited the levels of reactive oxygen species and lactate dehydrogenase release compared to the Aβ25-35-induced control group. Furthermore, the inflammation- and apoptosis-related protein expressions were investigated to demonstrate its neuroprotective mechanism. EtOAc-PT downmodulated the expressions of inducible nitric oxide synthase, cyclooxygenase-2, B-cell lymphoma 2 associated X, and B-cell lymphoma 2. Thus, the findings show that EtOAc-PT has protective effects against Aβ25-35 by suppressing oxidative stress, inflammation, and apoptosis.

Keywords

Acknowledgement

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. 2019R1F1A1054676).

References

  1. Cao Q, Tan C-C, Xu W, Hu H, Cao X-P, Dong Q, Tan L, Yu J-T (2020) The prevalence of dementia: a systematic review and meta-analysis. J Alzheimers Dis 73(3): 1157-1166. doi: 10.3233/JAD-191092
  2. Association As (2023) 2023 Alzheimer's disease facts and figures. Alzheimer's Dement 19(4): 1598-1695. doi: 10.1002/alz.13016
  3. Edwards FA (2019) A unifying hypothesis for Alzheimer's disease: from plaques to neurodegeneration. Trends Neurosci 42(5): 310-322. doi: 10.1016/j.tins.2019.03.003
  4. Castellani RJ, Rolston RK, Smith MA (2010) Alzheimer disease. Dis Mon 56(9): 484-546. doi: 10.1016/j.disamonth.2010.06.001
  5. Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol Med 8: 595-608. doi: 10.15252/emmm.201606210
  6. Xie H-r, Hu L-s, Li G-y (2010) SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson's disease. Chin Med J 123(8): 1086-1092. doi: 10.3760/cma.j.issn.0366-6999.2010.08.021
  7. Debbache-Benaida N, Atmani-Kilani D, Schini-Keirth VB, Djebbli N, Atmani D (2013) Pharmacological potential of Populus nigra extract as antioxidant, anti-inflammatory, cardiovascular and hepatoprotective agent. Asian Pac J Trop Biomed 3(9): 697-704. doi: 10.1016/S2221-1691(13)60141-0
  8. Dudonne S, Poupard P, Coutiere P, Woillez M, Richard T, Merillon J-M, Vitrac X (2011) Phenolic composition and antioxidant properties of Poplar bud (Populus nigra) extract: individual antioxidant contribution of phenolics and transcriptional effect on skin aging. J Agric Food Chem 59(9): 4527-4536. doi: 10.1021/jf104791t
  9. Kwak J, Oh Y (2003) Evaluation of populus alba × glandulosa as raw material of particleboard. J Korean For Soc 92: 140-144
  10. Choi S-I, Hwang S-J, Lee O-H, Kim JD (2020) Antioxidant activity and component analysis of Populus tomentiglandulosa extract. Korean J Food Sci Technol 52(2): 119-124. doi: 10.9721/KJFST.2020.52.2.119
  11. Lee T-K, Park JH, Ahn JH, Kim H, Song M, Lee J-C, Kim JD, Jeon YH, Choi JH, Lee CH, Hwang IK, YAN B-C, Won M-H, Kang IJ (2019) Pretreatment of Populus tomentiglandulosa protects hippocampal CA1 pyramidal neurons from ischemia-reperfusion injury in gerbils via increasing SODs expressions and maintaining BDNF and IGF-I expressions. Chin J Nat Med 17(6): 424-434. doi: 10.1016/S1875-5364(19)30050-0
  12. Kwon YR, Kim JH, Lee S, Cho EJ, Kim HY (2020) Protective role of Populus tomentiglandulosa against hydrogen peroxide-induced oxidative stress in SH-SY5Y neuronal cells. J Appl Biol Chem 63(4): 357-363. doi: 10.3839/jabc.2020.047
  13. Park JH, Lee TK, Ahn JH, Shin BN, Cho JH, Kim IH, Lee JC, Kim JD, Lee YJ, Kang IJ, Hong S, Kim YH, Jeon YH, Lee YL, Won M-H (2017) Pre-treated Populus tomentiglandulosa extract inhibits neuronal loss and alleviates gliosis in the gerbil hippocampal CA1 area induced by transient global cerebral ischemia. Anat Cell Biol 50(4): 284-292. doi: 10.5115/acb.2017.50.4.284
  14. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1-2): 55-63. doi: 10.1016/0022-1759(83)90303-4
  15. Cathcart R, Schwiers E, Ames BN (1983) Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal Biochem 134(1): 111-116. doi: 10.1016/0003-2697(83)90270-1
  16. Shanmugam G, Polavarapu PL (2004) Structure of Aβ (25-35) peptide in different environments. Biophy J 87(1): 622-630. doi: 10.1529/biophysj.104.040907
  17. Millucci L, Ghezzi L, Bernardini G, Santucci A (2010) Conformations and biological activities of amyloid beta peptide 25-35. Curr Protein Pept Sci 11(1): 54-67. doi: 10.2174/138920310790274626
  18. Wang K, Zhu L, Zhu X, Zhang K, Huang B, Zhang J, Zhang Y, Zhu L, Zhou B, Zhou F (2014) Protective effect of paeoniflorin on Aβ25-35-induced SH-SY5Y cell injury by preventing mitochondrial dysfunction. Cell Mol Neurobiol 34: 227-234. doi: 10.1007/s10571-013-0006-9
  19. Mairuae N, Connor JR, Buranrat B, Lee SY (2019) Oroxylum indicum (L.) extract protects human neuroblastoma SH-SY5Y cells against β-amyloid-induced cell injury. Mol Med Rep 20(2): 1933-1942. doi: 10.3892/mmr.2019.10411
  20. Choi SI, Hwang SJ, Lee OH, Kim JD (2020) Antioxidant activity and component analysis of Populus tomentiglandulosa extract. Korean J Food Sci Technol 52: 119-124. doi: 10.9721/KJFST.2020.52.2.119
  21. Lee T-K, Lee J-C, Kim J-D, Kim D-W, Ahn J-H, Park J-H, Kim H-I, Cho J-H, Choi S-Y, Won M-H, Kang I-J (2021) Populus tomentiglandulosa extract is rich in polyphenols and protects neurons, astrocytes, and the blood-brain barrier in gerbil striatum following ischemia-reperfusion injury. Molecules 26: 5430. doi: 10.3390/molecules26185430
  22. Lee C-H, Park JH, Ahn JH, Kim JD, Cho JH, Lee T-K, Won M-H (2019) Stronger antioxidant enzyme immunoreactivity of Populus tomentiglandulosa extract than ascorbic acid in rat liver and kidney. Iran J Basic Med Sci 22: 963-967. doi: 10.22038/ijbms.2019.34926.8296
  23. Kwon YR, Kim J-H, Lee S, Kim HY, Cho EJ (2022) Protective effects of Populus tomentiglandulosa against cognitive impairment by regulating oxidative stress in an amyloid beta25-35-induced Alzheimer's disease mouse model. Nutr Res Pract 16(2): 173-193. doi: 10.4162/nrp.2022.16.2.173
  24. Kong CS, Kim KH, Choi JS, Kim JE, Park C, Jeong JW (2014) Salicin, an extract from white willow bark, inhibits angiogenesis by blocking the ROS-ERK pathways. Phytother Res 28(8): 1246-1251. doi: 10.1002/ptr.5126
  25. Gao F, Zhang S (2019) Salicin inhibits AGE-induced degradation of type II collagen and aggrecan in human SW1353 chondrocytes: therapeutic potential in osteoarthritis. Artif Cells Nanomed Biotechnol 47(1): 1043-1049. doi: 10.1080/21691401.2019.1591427
  26. Sabaa M, ELFayoumi HM, Elshazly S, Youns M, Barakat W (2017) Anticancer activity of salicin and fenofibrate. N Schmied Arch Pharmacol 390: 1061-1071. doi: 10.1007/s00210-017-1407-y
  27. Park J-H, Lee T-K, Kim D-W, Sim H, Lee J-C, Kim J-D, Ahn J-H, Lee C-H, Kim Y-M, Won M-H, Choi S-Y (2021) Neuroprotective effects of salicin in a gerbil model of transient forebrain ischemia by attenuating oxidative stress and activating PI3K/Akt/GSK3beta pathway. Antioxidants 10(1): 62. doi: 10.3390/antiox10010062
  28. Awasthi A, Matsunaga Y, Yamada T (2005) Amyloid-beta causes apoptosis of neuronal cells via caspase cascade, which can be prevented by amyloid-beta-derived short peptides. Exp Neurol 196(2): 282-289. doi: 10.1016/j.expneurol.2005.08.001
  29. Walsh DM, Teplow DB (2012) Alzheimer's disease and the amyloid βprotein. Prog Mol Biol Transl Sci 107: 101-124. doi: 10.1016/B978-0-12-385883-2.00012-6
  30. Green KN, LaFerla FM (2008) Linking calcium to Aβ and Alzheimer's disease. Neuron 59(2): 190-194. doi: 10.1016/j.neuron.2008.07.013
  31. Oguchi T, Ono R, Tsuji M, Shozawa H, Somei M, Inagaki M, Mori Y, Yasumoto T, Ono K, Kiuchi Y (2017) Cilostazol suppresses Aβ-induced neurotoxicity in SH-SY5Y cells through inhibition of oxidative stress and MAPK signaling pathway. Front Aging Neurosci 9: 337. doi: 10.3389/fnagi.2017.00337
  32. Wang Y, Fu X-t, Li D-w, Wang K, Wang X-z, Li Y, Sun B-l, Yang X-y, Zheng Z-c, Cho NC (2016) Cyanidin suppresses amyloid beta-induced neurotoxicity by inhibiting reactive oxygen species-mediated DNA damage and apoptosis in PC12 cells. Neural Regen Res 11(5): 795-800. doi: 10.4103/1673-5374.182707
  33. Jiang S, Zhao Y, Zhang T, Lan J, Yang J, Yuan L, Zhang Q, Pan K, Zhang K (2018) Galantamine inhibits β-amyloid-induced cytostatic autophagy in PC 12 cells through decreasing ROS production. Cell Prolif 51(3): e12427. doi: 10.1111/cpr.12427
  34. Pathak J, Chatterjee A, Singh SP, Sinha RP (2017) Detection of reactive oxygen species (ROS) in cyanobacteria using the oxidant-sensing probe 2',7'-dichlorodihydrofluorescein diacetate (DCFH-DA). Bio Protoc 7(17): e2545. doi: 10.21769/BioProtoc.2545
  35. Zhang L, Yu H, Zhao X, Lin X, Tan C, Cao G, Wang Z (2010) Neuroprotective effects of salidroside against beta-amyloid-induced oxidative stress in SH-SY5Y human neuroblastoma cells. Neurochem Int 57(5): 547-555. doi: 10.1016/j.neuint.2010.06.021
  36. El-Hussein A, Mfouo-Tynga I, Abdel-Harith M, Abrahamse H (2015) Comparative study between the photodynamic ability of gold and silver nanoparticles in mediating cell death in breast and lung cancer cell lines. J Photochem Photobiol B 153: 67-75. doi: 10.1016/j.jphotobiol.2015.08.028
  37. Kimura M, Komatsu H, Ogura H, Sawada K (2005) Comparison of donepezil and memantine for protective effect against amyloid-beta (1-42) toxicity in rat septal neurons. Neurosci Lett 391(1-2): 17-21. doi: 10.1016/j.neulet.2005.08.036
  38. Mei Z, Yan P, Situ B, Mou Y, Liu P (2012) Cryptotanshinione inhibits β-amyloid aggregation and protects damage from β-amyloid in SH-SY5Y cells. Neurochem Res 37(3):622-628. doi: 10.1007/s11064-011-0652-6
  39. Ayasolla K, Khan M, Singh AK, Singh I (2004) Inflammatory mediator and β-amyloid (25-35)-induced ceramide generation and iNOS expression are inhibited by vitamin E. Free Radic Biol Med 37(3): 325-338. doi: 10.1016/j.freeradbiomed.2004.04.007
  40. Kaur D, Sharma V, Deshmukh R (2019) Activation of microglia and astrocytes: a roadway to neuroinflammation and Alzheimer's disease. Inflammopharmacology 27(4): 663-677. doi: 10.1007/s10787-019-00580-x
  41. Law A, Gauthier S, Quirion R (2001) Say NO to Alzheimer's disease: the putative links between nitric oxide and dementia of the Alzheimer's type. Brain Res Rev 35(1): 73-96. doi: 10.1016/S0165-0173(00)00051-5
  42. Kotilinek LA, Westerman MA, Wang Q, Panizzon K, Lim GP, Simonyi A, Lesne S, Falinska A, Younkin LH, Younkin SG (2008) Cyclooxygenase-2 inhibition improves amyloid-β-mediated suppression of memory and synaptic plasticity. Brain 131(3): 651-664. doi: 10.1093/brain/awn008
  43. Guan P-P, Liang Y-Y, Cao L-L, Yu X, Wang P (2019) Cyclooxygenase-2 induced the β-amyloid protein deposition and neuronal apoptosis via upregulating the synthesis of prostaglandin E2 and 15-deoxy- Δ12, 14-prostaglandin J2. Neurotherapeutics 16(4): 1255-1268. doi: 10.1007/s13311-019-00770-z
  44. Xu J, Wu W, Zhang H, Yang L (2018) Berberine alleviates amyloid β25-35-induced inflammatory response in human neuroblastoma cells by inhibiting proinflammatory factors. Exp Ther Med 16(6): 4865-4872. doi: 10.3892/etm.2018.6749
  45. Garcia-Saez A (2012) The secrets of the Bcl-2 family. Cell Death Differ 19(11): 1733-1740. doi: 10.1038/cdd.2012.105
  46. Jiang Z, Zhang H, Bockmann RA (2016) Allostery in BAX protein activation. J Biomol Struct Dyn 34(11): 2469-2480. doi: 10.1080/07391102.2015.1119731
  47. Pena-Blanco A, Garcia-Saez AJ (2018) Bax, Bak and beyond-mitochondrial performance in apoptosis. FEBS J 285(3): 416-431. doi: 10.1111/febs.14186
  48. Clementi M, Pezzotti M, Orsini F, Sampaolese B, Mezzogori D, Grassi C, Giardina B, Misiti F (2006) Alzheimer's amyloid β-peptide (1-42) induces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35. Biochem Biophys Res Commun 342(1): 206-213. doi: 10.1016/j.bbrc.2006.01.137
  49. Zhang Y, Jiao G, Song C, Gu S, Brown RE, Zhang J, Zhang P, Gagnon J, Locke S, Stefanova R, Pelletier C, Zhang Y, Lu H (2017) An extract from shrimp processing by-products protects SH-SY5Y cells from neurotoxicity induced by Aβ25-35. Mar Drugs 15(3): 83. doi: 10.3390/md15030083