Korean Journal of Acupuncture

Society for Meridian and Acupoint (경락경혈학회)
권호 표지
DOI QR코드

DOI QR Code

Proteomic Analysis for Neuroprotective Effect of Gastrodia elata Blume in the Substantia Nigra of Mice

천마의 흑질 내 도파민성 신경세포 보호 효과에 대한 단백체학적 분석

  • Chang-Hwan, Bae (Department of Korean Medical Science, School of Korean Medicine, Pusan National University) ;
  • Hee-Young, Kim (Healthy Aging Korean Medical Research Center, Pusan National University) ;
  • Hanul, Lee (Department of Korean Medical Science, School of Korean Medicine, Pusan National University) ;
  • Ji Eun, Seo (Department of Korean Medical Science, School of Korean Medicine, Pusan National University) ;
  • Dong Hak, Yoon (KyungHee YDH Oriental Clinic) ;
  • Seungtae, Kim (Department of Korean Medical Science, School of Korean Medicine, Pusan National University)
  • 배창환 (부산대학교 한의학전문대학원 한의과학과) ;
  • 김희영 (부산대학교 건강노화한의과학연구센터) ;
  • 이한울 (부산대학교 한의학전문대학원 한의과학과) ;
  • 서지은 (부산대학교 한의학전문대학원 한의과학과) ;
  • 윤동학 (경희윤동학한의원) ;
  • 김승태 (부산대학교 한의학전문대학원 한의과학과)
  • Received : 2022.11.24
  • Accepted : 2022.12.05
  • Published : 2022.12.27
Download PDF
⟨ Previous Next ⟩

Abstract

Objectives : Parkinson's disease (PD) is a neurodegenerative disorder threatening the quality of life and highly occurred in over 65 years old. Gastrodia elata Blume (GEB), a traditional medicine used for the treatment of headache and convulsion, has been reported to have neuroprotective effect. This study was designed to investigate the neuroprotective effect of GEB and the proteomic changes in the substantia nigra (SN) of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Methods : Male eleven-week-old C57BL/6 mice were intraperitoneally injected with 30 mg/kg of MPTP at 24-h intervals for 5 days. Two hours after the daily MPTP injection, the mice were orally administered 800 mg/kg of GEB extract, which continued for 7 days beyond the MPTP injections, for a total of 12 consecutive days. Two hours after the final GEB administration, the brain samples were collected, and dopaminergic neuronal death and proteomic changes in the SN were evaluated. Results : GEB prevented the MPTP-induced dopaminergic neuronal death and regulated the expression of 11 proteins including thimet oligopeptidase, T-complex protein 1, glycine tRNA ligase, and pyruvate kinase isozymes M1. Conclusions : GEB prevents MPTP-induced dopaminergic neuronal death by regulating the proteins in the SN.

Keywords

Acknowledgement

This study was supported by a research grant of the Health Fellowship Foundation.

References

  1. Tysnes OB, Storstein A. Epidemiology of Parkinson's disease. J Neural Transm (Vienna). 2017 ; 124(8) : 901-5. https://doi.org/10.1007/s00702-017-1686-y
  2. Dorszewska J, Kowalska M, Prendecki M, Piekut T, Kozlowska J, Kozubski W. Oxidative stress factors in Parkinson's disease. Neural Regen Res. 2021 ; 16(7) : 1383-91. https://doi.org/10.4103/1673-5374.300980
  3. Padilla-Godinez FJ, Ramos-Acevedo R, Martinez-Becerril HA, Bernal-Conde LD, Garrido-Figueroa JF, Hiriart M, et al. Protein misfolding and aggregation: the relatedness between Parkinson's disease and hepatic endoplasmic reticulum storage disorders. Int J Mol Sci. 2021 ; 22(22) : 12467. https://doi.org/10.3390/ijms222212467
  4. Calabresi P, Di Filippo M, Ghiglieri V, Tambasco N, Picconi B. Levodopa-induced dyskinesias in patients with Parkinson's disease: filling the bench-to-bedside gap. Lancet Neurol. 2010 ; 9(11) : 1106-17. https://doi.org/10.1016/S1474-4422(10)70218-0
  5. Tambasco N, Romoli M, Calabresi P. Levodopa in Parkinson's disease: current status and future developments. Curr Neuropharmacol. 2018 ; 16(8) : 1239-52. https://doi.org/10.2174/ 1570159X15666170510143821
  6. Armstrong MJ, Okun MS. Diagnosis and treatment of Parkinson disease: a review. JAMA. 2020 ; 323(6) : 548-60. https://doi.org/10.1001/jama.2019.22360
  7. Ntetsika T, Papathoma PE, Markaki I. Novel targeted therapies for Parkinson's disease. Mol Med. 2021 ; 27(1) : 17. https://doi.org/10.1186/s10020-021-00279-2
  8. Kim HS, Lee SI, Jeong JK. Systemic review on the research trend of Gastrodiae rhizoma and relationship between the herbology and KCD-code. Kor. J. Herbology. 2016 ; 31 (2) : 21-37. https://doi.org/10.6116/kjh.2016.31.2.21.
  9. Hsieh CL, Lin JJ, Chiang SY, Su SY, Tang NY, Lin GG, et al. Gastrodia elata modulated activator protein 1 via c-Jun N-terminal kinase signaling pathway in kainic acid-induced epilepsy in rats. J Ethnopharmacol. 2007 ; 109(2) : 241-7. https://doi. org/10.1016/j.jep.2006.07.024
  10. Lee JY, Jang YW, Kang HS, Moon H, Sim SS, Kim CJ. Anti-inflammatory action of phenolic compounds from Gastrodia elata root. Arch Pharm Res. 2006 ; 29(10) : 849-58. https://doi.org/10.1007/BF02973905
  11. Kim IS, Choi DK, Jung HJ. Neuroprotective effects of vanillyl alcohol in Gastrodia elata Blume through suppression of oxidative stress and anti-apoptotic activity in toxin-induced dopaminergic MN9D cells. Molecules. 2011 ; 16(7) : 5349-61. https:// doi.org/10.3390/molecules16075349
  12. Zhou B, Tan J, Zhang C, Wu Y. Neuroprotective effect of polysaccharides from Gastrodia elata blume against corticosterone-induced apoptosis in PC12 cells via inhibition of the endoplasmic reticulum stress-mediated pathway. Mol Med Rep. 2018 ; 17(1) : 1182-90. https://doi.org/10.3892/mmr.2017.7948
  13. Doo AR, Kim SN, Hahm DH, Yoo HH, Park JY, Lee H, et al. Gastrodia elata Blume alleviates L-DOPA-induced dyskinesia by normalizing FosB and ERK activation in a 6-OHDA-lesioned Parkinson's disease mouse model. BMC Complement Altern Med. 2014 ; 14 : 107. https://doi.org/10.1186/1472-6882-14-107
  14. He J, Li X, Yang S, Li Y, Lin X, Xiu M, et al. Gastrodin extends the lifespan and protects against neurodegeneration in the drosophila PINK1 model of Parkinson's disease. Food Funct. 2021 ; 12(17) : 7816-24. https://doi.org/10.1039/d1fo00847a
  15. Kumar H, Kim IS, More SV, Kim BW, Bahk YY, Choi DK. Gastrodin protects apoptotic dopaminergic neurons in a toxin-induced Parkinson's disease model. Evid Based Complement Alternat Med. 2013 ; 2013 : 514095. https://doi.org/10.1155/2013/514095
  16. Icimoto MY, Ferreira JC, Yokomizo CH, Bim LV, Marem A, Gilio JM, et al. Redox modulation of thimet oligopeptidase activity by hydrogen peroxide. FEBS Open Bio. 2017 ; 7(7) : 1037-50. https://doi.org/10.1002/2211-5463.12245
  17. Valenzuela R, Costa-Besada MA, Iglesias-Gonzalez J, PerezCostas E, Villar-Cheda B, Garrido-Gil P, et al. Mitochondrial angiotensin receptors in dopaminergic neurons. Role in cell protection and aging-related vulnerability to neurodegeneration. Cell Death Dis. 2016 ; 7(10) : e2427. https://doi.org/10.1038/cddis.2016.327
  18. Seebauer L, Schneider Y, Drobny A, Plotz S, Koudelka T, Tholey A, et al. Interaction of alpha synuclein and microtubule organization is linked to impaired neuritic integrity in Parkinson's patient-derived neuronal cells. Int J Mol Sci. 2022 ; 23(3) : 1812. https://doi.org/10.3390/ijms23031812
  19. Hu S, Hu M, Liu J, Zhang B, Zhang Z, Zhou FH, et al. Phosphorylation of Tau and α-synuclein induced neurodegeneration in MPTP mouse model of Parkinson's disease. Neuropsychiatr Dis Treat. 2020 ; 16 ; 651-63. https://doi.org/10.2147/NDT.S235562
  20. Sarkar S, Olsen AL, Sygnecka K, Lohr KM, Feany MB. α-Synuclein impairs autophagosome maturation through abnormal actin stabilization. PLoS Genet. 2021 ; 17(2) : e1009359. https://doi.org/10.1371/journal.pgen.1009359
  21. Cuellar J, Vallin J, Svanstrom A, Maestro-Lopez M, BuenoCarrasco MT, Ludlam WG, et al. The molecular chaperone CCT sequesters gelsolin and protects it from cleavage by caspase-3. J Mol Biol. 2022 ; 434(5) : 167399. https://doi.org/10.1016/j.jmb.2021.167399
  22. Yu M, Luo C, Huang X, Chen D, Li S, Qi H, et al. Amino acids stimulate glycyl-tRNA synthetase nuclear localization for mammalian target of rapamycin expression in bovine mammary epithelial cells. J Cell Physiol. 2019 ; 234(5) : 7608-21. https://doi.org/10.1002/jcp.27523
  23. Kato Y, Maeda T, Suzuki A, Baba Y. Cancer metabolism: new insights into classic characteristics. Jpn Dent Sci Rev. 2018 ; 54(1) : 8-21. https://doi.org/10.1016/j.jdsr.2017.08.003
  24. Jiang P, Gan M, Ebrahim AS, Castanedes-Casey M, Dickson DW, Yen SH. Adenosine monophosphate-activated protein kinase overactivation leads to accumulation of α-synuclein oligomers and decrease of neurites. Neurobiol Aging. 2013 ; 34(5) : 1504-15. https://doi.org/10.1016/j.neurobiolaging.2012.11.001
  25. Morita M, Sato T, Nomura M, Sakamoto Y, Inoue Y, Tanaka R, et al. PKM1 confers metabolic advantages and promotes cell-autonomous tumor cell growth. Cancer Cell. 2018 ; 33(3) : 355-67. https://doi.org/10.1016/j.ccell.2018.02.004
  26. Li J, Chen L, Qin Q, Wang D, Zhao J, Gao H, et al. Upregulated hexokinase 2 expression induces the apoptosis of dopaminergic neurons by promoting lactate production in Parkinson's disease. Neurobiol Dis. 2022 ; 163 : 105605. https://doi.org/10.1016/j.nbd.2021.105605
  27. Loeffler DA, Klaver AC, Coffey MP, Aasly JO, LeWitt PA. Age-related decrease in heat shock 70-kDa protein 8 in cerebrospinal fluid is associated with increased oxidative stress. Front Aging Neurosci. 2016 ; 8 : 178. https://doi.org/10.3389/fnagi.2016.00178
  28. Niu M, Dai X, Zou W, Yu X, Teng W, Chen Q, et al. Autophagy, endoplasmic reticulum stress and the unfolded protein response in intracerebral hemorrhage. Transl Neurosci. 2017 ; 8 : 37-48. https://doi.org/10.1515/tnsci-2017-0008
  29. Plowey ED, Cherra SJ 3rd, Liu YJ, Chu CT. Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. J Neurochem. 2008 ; 105(3) : 1048-56. https://doi.org/10.1111/j.1471-4159.2008.05217.x
  30. Stafa K, Tsika E, Moser R, Musso A, Glauser L, Jones A, et al. Functional interaction of Parkinson's disease-associated LRRK2 with members of the dynamin GTPase superfamily. Hum Mol Genet. 2014 ; 23(8) : 2055-77. https://doi.org/10.1093/hmg/ddt600
  31. Berner AK, Brouwers O, Pringle R, Klaassen I, Colhoun L, McVicar C, et al. Protection against methylglyoxal-derived AGEs by regulation of glyoxalase 1 prevents retinal neuroglial and vasodegenerative pathology. Diabetologia. 2012 ; 55(3) : 845-54. https://doi.org/10.1007/s00125-011-2393-0
  32. Antognelli C, Palumbo I, Aristei C, Talesa VN. Glyoxalase I inhibition induces apoptosis in irradiated MCF-7 cells via a novel mechanism involving Hsp27, p53 and NF-κB. Br J Cancer. 2014 ; 111(2) : 395-406. https://doi.org/10.1038/bjc.2014.280
  33. Taoufik E, Kouroupi G, Zygogianni O, Matsas R. Synaptic dysfunction in neurodegenerative and neurodevelopmental diseases: an overview of induced pluripotent stem-cell-based disease models. Open Biol. 2018 ; 8(9) : 180138. https://doi.org/10.1098/rsob.180138
  34. Nakos K, Radler MR, Spiliotis ET. Septin 2/6/7 complexes tune microtubule plus-end growth and EB1 binding in a concentration- and filament-dependent manner. Mol Biol Cell. 2019 ; 30(23) : 2913-28. https://doi.org/10.1091/mbc.E19-07-0362
  35. Bowen JR, Hwang D, Bai X, Roy D, Spiliotis ET. Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J Cell Biol. 2011 ; 194(2) : 187-97. https://doi.org/10.1083/jcb.201102076
  36. Kuck U, Radchenko D, Teichert I. STRIPAK, a highly conserved signaling complex, controls multiple eukaryotic cellular and developmental processes and is linked with human diseases. Biol Chem. 2019 ; 400(8) : 1005-22. https://doi.org/10.1515/hsz2019-0173
  37. Neisch AL, Neufeld TP, Hays TS. A STRIPAK complex mediates axonal transport of autophagosomes and dense core vesicles through PP2A regulation. J Cell Biol. 2017 ; 216(2) : 441-61. https://doi.org/10.1083/jcb.201606082
  38. Wilkinson KD, Lee KM, Deshpande S, Duerksen-Hughes P, Boss JM, Pohl J. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science. 1989 ; 246(4930) : 670-3. https://doi.org/10.1126/science.2530630
  39. Reinicke AT, Laban K, Sachs M, Kraus V, Walden M, Damme M, et al. Ubiquitin C-terminal hydrolase L1 (UCH-L1) loss causes neurodegeneration by altering protein turnover in the first postnatal weeks. Proc Natl Acad Sci U S A. 2019 ; 116(16) : 7963-72. https://doi.org/10.1073/pnas.1812413116
  40. Huynh TKT, Mai TTT, Huynh MA, Yoshida H, Yamaguchi M, Dang TTP. Crucial roles of ubiquitin carboxy-terminal hydrolase L1 in motor neuronal health by Drosophila Model. Antioxid Redox Signal. 2022 ; 37(4-6) : 257-73. https://doi.org/10.1089/ars.2021.0057