Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

A proteomic approach reveals the differential protein expression in Drosophila melanogaster treated with red ginseng extract (Panax ginseng)

  • Liu, Qing-Xiu (Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Wei (Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences) ;
  • Wang, Jia (Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences) ;
  • Hou, Wei (Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences) ;
  • Wang, Ying-Ping (Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences)
  • Received : 2016.12.27
  • Accepted : 2017.04.17
  • Published : 2018.07.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Red ginseng is a popularly used traditional medicine with antiaging effects in Asian countries. The present study aimed to explore the changes in protein expression underlying the mechanisms of life span extension and antiaging caused by red ginseng extract (RGE) in Drosophila melanogaster. Methods: A proteomic approach of two-dimensional polyacrylamide gel electrophoresis (2-DE) was used to identify the differential abundance of possible target proteins of RGE in D. melanogaster. The reliability of the 2-DE results was confirmed via Western blotting to measure the expression levels of selected proteins. Proteins altered at the expression level after RGE treatment (1 mg/mL) were identified by matrix-assisted laser desorption/ionization-time of flight tandem mass spectrometry and by searching against the National Center for Biotechnology nonredundant and Uniprot protein databases. The differentially expressed proteins were analyzed using bioinformatics methods. Results: The average survival life span of D. melanogaster was significantly extended by 12.60% with RGE treatment (1 mg/mL) compared to untreated flies. This followed increased superoxide dismutase level and decreased methane dicarboxylic aldehyde content. Based on the searching strategy, 23 differentially expressed proteins were identified (16 up-regulated and 7 down-regulated) in the RGE-treated D. melanogaster. Transduction pathways were identified using the Kyoto Encyclopedia of Genes and Genomes database, and included the hippo and oxidative phosphorylation pathways that play important roles in life span extension and antiaging process of D. melanogaster. Conclusion: Treatment with RGE in D. melanogaster demonstrated that mechanisms of life span extension and antiaging are regulated by multiple factors and complicated signal pathways.

Keywords

References

  1. Ghimire S, Kim MS. Jujube (Ziziphus Jujuba Mill.) fruit feeding extends lifespan and increases tolerance to environmental stresses by regulating agingassociated gene expression in Drosophila. Biogerontology 2017;18:263-73. https://doi.org/10.1007/s10522-017-9686-8
  2. Ahangarpour A, Lamoochi Z, Fathi Moghaddam H, Mansouri SM. Effects of Portulaca oleracea ethanolic extract on reproductive system of aging female mice. Int J Reprod Biomed (Yazd) 2016;14:205-12. https://doi.org/10.29252/ijrm.14.3.205
  3. Peleg S, Feller C, Forne I, Schiller E, Sevin DC, Schauer T, Regnard C, Straub T, Prestel M, Klima C, et al. Life span extension by targeting a link between metabolism and histone acetylation in Drosophila. EMBO Rep 2016;17:455-69. https://doi.org/10.15252/embr.201541132
  4. Ghimire S, Kim MS. Defensive behavior against noxious heat stimuli is declined with aging due to decreased pain-associated gene expression in Drosophila. Biomol Ther (Seoul) 2015;23:290-5. https://doi.org/10.4062/biomolther.2014.147
  5. Ong WY, Farooqui T, Koh HL, Farooqui AA, Ling EA. Protective effects of ginseng on neurological disorders. Front Aging Neurosci 2015;7:129.
  6. Kim GN, Lee JS, Song JH, Oh CH, Kwon YI, Jang HD. Heat processing decreases Amadori products and increases total phenolic content and antioxidant activity of Korean Red Ginseng. J Med Food 2010;13:1478-84. https://doi.org/10.1089/jmf.2010.1076
  7. Lee Y, Oh S. Administration of red ginseng ameliorates memory decline in aged mice. J Ginseng Res 2015;39:250-6. https://doi.org/10.1016/j.jgr.2015.01.003
  8. Kim MS. Korean Red Ginseng tonic extends lifespan in D. melanogaster. Biomol Ther (Seoul) 2013;21:241-5. https://doi.org/10.4062/biomolther.2013.024
  9. Park S, Kim CS, Min J, Lee SH, Jung YS. A high-fat diet increases oxidative renal injury and protein glycation in D-galactose-induced aging rats and its prevention by Korea red ginseng. J Nutr Sci Vitaminol (Tokyo) 2014;60:159-66. https://doi.org/10.3177/jnsv.60.159
  10. Kang TH, Park HM, Kim YB, Kim H, Kim N, Do JH, Kang C, Cho Y, Kim SY. Effects of red ginseng extract on UVB irradiation-induced skin aging in hairless mice. J Ethnopharmacol 2009;123:446-51. https://doi.org/10.1016/j.jep.2009.03.022
  11. Han J, Li P, Cai W, Shao X. Fast determination of ginsenosides in ginseng by high-performance liquid chromatography with chemometric resolution. J Sep Sci 2014;37:2126-30. https://doi.org/10.1002/jssc.201400403
  12. Huang X, Wang X, Lv Y, Xu L, Lin J, Diao Y. Protection effect of kallistatin on carbon tetrachloride-induced liver fibrosis in rats via antioxidative stress. PLoS One 2014;9:e88498. https://doi.org/10.1371/journal.pone.0088498
  13. Dong Z, Ba H, Zhang W, Coates D, Li C. iTRAQ-based quantitative proteomic analysis of the potentiated and dormant antler stem cells. Int J Mol Sci 2016;17. pii: E1778.
  14. Erd}o F, Denes L, de Lange E. Age-associated physiological and pathological changes at the bloodebrain barrier: a review. J Cereb Blood Flow Metab 2016. pii: 0271678X16679420.
  15. Pfeffer M, Plenzig S, Gispert S, Wada K, Korf HW, Von Gall C. Disturbed sleep/wake rhythms and neuronal cell loss in lateral hypothalamus and retina of mice with a spontaneous deletion in the ubiquitin carboxyl-terminal hydrolase L1 gene. Neurobiol Aging 2012;33:393-403. https://doi.org/10.1016/j.neurobiolaging.2010.02.019
  16. Ohrfelt A, Johansson P, Wallin A, Andreasson U, Zetterberg H, Blennow K, Svensson J. Increased cerebrospinal fluid levels of ubiquitin carboxyl-terminal hydrolase L1 in patients with Alzheimer's disease. Dement Geriatr Cogn Dis Extra 2016;6:283-94. https://doi.org/10.1159/000447239
  17. Khan AT, Dobson RJ, Sattlecker M, Kiddle SJ. Alzheimer's disease: are blood and brain markers related? A systematic review. Ann Clin Transl Neurol 2016;3:455-62. https://doi.org/10.1002/acn3.313
  18. Marzban G, Grillari J, Reisinger E, Hemetsberger T, Grabherr R, Katinger H. Age-related alterations in the protein expression profile of C57BL/6J mouse pituitaries. Exp Gerontol 2002;37:1451-60. https://doi.org/10.1016/S0531-5565(02)00117-1
  19. Zhang M, Cai F, Zhang S, Zhang S, Song W. Overexpression of ubiquitin carboxyl-terminal hydrolase L1 (UCHL1) delays Alzheimer's progression in vivo. Sci Rep 2014;4:7298.
  20. Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, Chin LS, Li L. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J Biol Chem 2004;279:13256-64. https://doi.org/10.1074/jbc.M314124200
  21. Tsai YC, Lee YM, Lam KK, Lin JF, Wang JJ, Yen MH, Cheng PY. The role of heat shock protein 70 in the protective effect of YC-1 on ${\beta}$-amyloid-induced toxicity in differentiated PC12 cells. PLoS One 2013;8:e69320. https://doi.org/10.1371/journal.pone.0069320
  22. Fu Y, Zhao D, Pan B, Wang J, Cui Y, Shi F, Wang C, Yin X, Zhou X, Yang L. Proteomic analysis of protein expression throughout disease progression in a mouse model of Alzheimer's disease. J Alzheimers Dis 2015;47:915-26. https://doi.org/10.3233/JAD-150312
  23. Martinez de Toda I, De la Fuente M. The role of Hsp70 in oxi-inflamm-aging and its use as a potential biomarker of lifespan. Biogerontology 2015;16:709-21. https://doi.org/10.1007/s10522-015-9607-7
  24. Di Domenico F, Coccia R, Cocciolo A, Murphy MP, Cenini G, Head E, Butterfield DA, Giorgi A, Schinina ME, Mancuso C, et al. Impairment of proteostasis network in Down syndrome prior to the development of Alzheimer's disease neuropathology: redox proteomics analysis of human brain. Biochim Biophys Acta 2013;1832:1249-59. https://doi.org/10.1016/j.bbadis.2013.04.013
  25. Broome CS, Kayani AC, Palomero J, Dillmann WH, Mestril R, Jackson MJ, Mc Ardle A. Effect of lifelong overexpression of HSP70 in skeletal muscle on agerelated oxidative stress and adaptation after nondamaging contractile activity. FASEB J 2006;20:1549-51. https://doi.org/10.1096/fj.05-4935fje
  26. Bittles AH, Fulder SJ, Grant EC, Nicholls MR. The effect of ginseng on lifespan and stress responses in mice. Gerontology 1979;25:125-31. https://doi.org/10.1159/000212330
  27. Goren P, Reznick AZ, Reiss U, Gershon D. Isoelectric properties of nematode aldolase and rat liver superoxide dismutase from young and old animals. FEBS Lett 1977;84:83-6. https://doi.org/10.1016/0014-5793(77)81062-4
  28. Choi S, Park KA, Lee HJ, Park MS, Lee JH, Park KC, Kim M, Lee SH, Seo JS, Yoon BW. Expression of Cu/Zn SOD protein is suppressed in hsp 70.1 knockout mice. J Biochem Mol Biol 2005;38:111-4.
  29. Coulombe J, Gamage P, Gray MT, Zhang M, Tang MY, Woulfe J, Saffrey MJ, Gray DA. Loss of UCHL1 promotes age-related degenerative changes in the enteric nervous system. Front Aging Neurosci 2014;6:129.
  30. Zhu J, Mu X, Zeng J, Xu C, Liu J, Zhang M, Li C, Chen J, Li T, Wang Y. Ginsenoside Rg1 prevents cognitive impairment and hippocampus senescence in a rat model of D-galactose-induced aging. PLoS One 2014;9:e101291. https://doi.org/10.1371/journal.pone.0101291
  31. Mortensen CJ, Choi YH, Ing NH, Kraemer DC, Vogelsang MM, Hinrichs K. Heat shock protein 70 gene expression in equine blastocysts after exposure of oocytes to high temperatures in vitro or in vivo after exercise of donor mares. Theriogenology 2010;74:374-83. https://doi.org/10.1016/j.theriogenology.2010.02.020
  32. Reeg S, Jung T, Castro JP, Davies KJ, Henze A, Grune T. The molecular chaperone Hsp70 promotes the proteolytic removal of oxidatively damaged proteins by the proteasome. Free Radic Biol Med 2016;99:153-66. https://doi.org/10.1016/j.freeradbiomed.2016.08.002
  33. Bobkova NV, Evgen'ev M, Garbuz DG, Kulikov AM, Morozov A, Samokhin A, Velmeshev D, Medvinskaya N, Nesterova I, Pollock A, et al. Exogenous Hsp70 delays senescence and improves cognitive function in aging mice. Proc Natl Acad Sci USA 2015;112:16006-11. https://doi.org/10.1073/pnas.1516131112
  34. Andreeva NV, Zatsepina OG, Garbuz DG, Evgen'ev MB, Belyavsky AV. Recombinant HSP70 and mild heat shock stimulate growth of aged mesenchymal stem cells. Cell Stress Chaperones 2016;21:727-33. https://doi.org/10.1007/s12192-016-0691-7
  35. Zhang G, Liu A, Zhou Y, San X, Jin T, Jin Y. Panax ginseng ginsenoside-Rg2 protects memory impairment via anti-apoptosis in a rat model with vascular dementia. J Ethnopharmacol 2008;115:441-8. https://doi.org/10.1016/j.jep.2007.10.026
  36. Pesce M, Messina E, Chimenti I, Beltrami AP. Cardiac mechano-perception: a life-long story from early beats to aging and failure. Stem Cells Dev 2017;26:77-90. https://doi.org/10.1089/scd.2016.0206
  37. Yu F-X, Zhao B, Guan K-L. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 2015;163:811-28. https://doi.org/10.1016/j.cell.2015.10.044
  38. Schroeder MC, Halder G. Regulation of the Hippo pathway by cell architecture and mechanical signals. Semin Cell Dev Biol 2012;23:803-11. https://doi.org/10.1016/j.semcdb.2012.06.001
  39. Zhou Q, Li L, Zhao B, Guan KL. The Hippo pathway in heart development, regeneration, and diseases. Circ Res 2015;116:1431-47. https://doi.org/10.1161/CIRCRESAHA.116.303311
  40. Yang D, Lian T, Tu J, Gaur U, Mao X, Fan X, Li D, Li Y, Yang M. Lnc RNA mediated regulation of aging pathways in Drosophila melanogaster during dietary restriction. Aging (Albany NY) 2016;8:2182-203.
  41. Forgac M. Vacuolar ATPases: rotary protonpumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2006;8:917-29.
  42. Numoto N, Hasegawa Y, Takeda K, Miki K. Inter-subunit interaction and quaternary rearrangement defined by the central stalk of prokaryotic V1-ATPase. EMBO Rep 2009;10:1228-34. https://doi.org/10.1038/embor.2009.202
  43. Skorokhod OA, Davalos-Schafler D, Gallo V, Valente E, Ulliers D, Notarpietro A, Mandili G, Novelli F, Persico M, Taglialatela-Scafati O, et al. Oxidative stress-mediated antimalarial activity of plakortin, a natural endoperoxide from the tropical sponge Plakortis simplex. Free Radic Biol Med 2015;89:624-37. https://doi.org/10.1016/j.freeradbiomed.2015.10.399

Cited by

  1. Differential proteomics for studying action mechanisms of traditional Chinese medicines vol.14, pp.None, 2018, https://doi.org/10.1186/s13020-018-0223-8
  2. Anti‐ageing effects of red ginseng on female Drosophila melanogaster vol.24, pp.6, 2018, https://doi.org/10.1111/jcmm.15029
  3. Hesperidin modulates the rhythmic proteomic profiling in Drosophila melanogaster under oxidative stress vol.105, pp.3, 2020, https://doi.org/10.1002/arch.21738