Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Antioxidant Activity, Macamide B Content and Muscle Cell Protection of Maca (Lepidium meyenii) Extracted Using Ultrasonification-Assisted Extraction

  • Received : 2019.11.19
  • Accepted : 2019.12.05
  • Published : 2020.06.28
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Abstract

This study aims to evaluate the efficacy of the Ultrasonication-Assisted (UA) extraction on the functionality of the herbaceous biennial plant maca (Lepidium meyenii). The specific objectives include comparison of the antioxidant activities among various maca extracts, determination of the macamide B content of the extracts, and in vitro evaluation of maca on cell viability and creatine kinase (CK) activity. The antioxidant activities of the water, ethanol, and UA extracts were compared by determining the total phenolic and flavonoid contents, the 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activities, and the ferric reducing antioxidant power (FRAP) of the extracts. The macamide B content of maca extracts were analyzed by HPLC. The effects of the extracts on muscle cell viability and creatine kinase activity were also determined using C2C12 myoblasts. UA extraction significantly increased the total phenolic content (2.90 GAE ㎍/mg, p < 0.05), without affecting the flavonoid content. DPPH radical scavenging activity did not exhibit any statistical difference among the extracts. The ethanol and UA extracts exhibited significantly higher FRAP than the water extract (p < 0.05). The macamide B content of ethanol and UA extracts were 0.087 and 0.083 ㎍/mg, respectively. The water and UA extracts exhibited higher C2C12 muscle cell viability than the ethanol extract, and both extracts resulted in a significantly lower CK level than the H2O2-treated control group. This research suggests that the maca extract can protect muscle cells and serve as an antifatigue agent under oxidative stress conditions.

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References

  1. Chen L, Li J, Fan L. 2017. The nutritional composition of maca in hypocotyls (Lepidium meyenii Walp.) cultivated in different regions of China. J. Food Qual. 2017: 1-8.
  2. Zhou Y, Li P, Brantner A, Wang H, Shu X, Yang J, et al. 2017. Chemical profiling analysis of Maca using UHPLC-ESI-Orbitrap MS coupled with UHPLC-ESI-QqQ MS and the neuroprotective study on its active ingredients. Sci. Rep. 7: 44660. https://doi.org/10.1038/srep44660
  3. Tang W, Jin L, Xie L, Huang J, Wang N, Chu B, et al. 2017. Structural characterization and antifatigue effect in vivo of maca (Lepidium meyenii Walp) polysaccharide. J. Food Sci. 82: 757-764. https://doi.org/10.1111/1750-3841.13619
  4. McCollom MM, Villinski JR, McPhail KL, Craker LE, Gafner S. 2005. Analysis of macamides in samples of Maca (Lepidium meyenii) by HPLC-UV-MS/MS. Phytochem. Anal. 16: 463-469. https://doi.org/10.1002/pca.871
  5. Zhang L, Li G, Wang S, Yao W, Zhu F. 2017. Physicochemical properties of maca starch. Food Chem. 218: 56-63. https://doi.org/10.1016/j.foodchem.2016.08.123
  6. Chen J-J, Zhao Q-S, Liu Y-I, Gong P-F, Cao L-L, Wang X-D, et al. 2017. Macamides present in the commercial maca (Lepidium meyenii) products and the macamide biosynthesis affected by postharvest conditions. Int. J. Food Prop. 20: 3112-3123. https://doi.org/10.1080/10942912.2016.1274905
  7. Chain FE, Grau A, Martins J, Catalan CAN. 2014. Macamides from wild Maca, Lepidium meyenii Walpers (Brassicaceae). Phytochem. Lett. 8: 145-148. https://doi.org/10.1016/j.phytol.2014.03.005
  8. Xia C, Deng J, Chen J, Zhu Y, Song Y, Zhang Y, et al. 2019. Simultaneous determination of macaenes and macamides in maca using an HPLC method and analysis using a chemometric method (HCA) to distinguish maca origin. Rev. Bras. Farmacogn. 6: 702-709.
  9. Chen S-X, Li K-K, Pubu D, Jiang S-P, Chen B, Chen L-R, et al. 2017. Optimization of ultrasound-assisted extraction, HPLC and UHPLC-Q-TOF-MS/MS analysis of main macamides and macaenes from maca (Cultivars of Lepidium meyenii Walp). Molecules 22: 2196. https://doi.org/10.3390/molecules22122196
  10. Berlowski A, Zawada K, Wawer I, Paradowska K. 2013. Antioxidant properties of medicinal plants from Peru. Food Nutr. Sci. 4: 71-77.
  11. Li J, Chen L, Li J, Duan Z, Zhu S, Fan L. 2017. The composition analysis of Maca (Lepidium meyenii Walp.) from xinjiang and its antifatigue activity. J. Food Qual. 2017: 2904951.
  12. Wang S, Zhu F. 2019. Chemical composition and health effects of maca (Lepidium meyenii). Food Chem. 288: 422-443. https://doi.org/10.1016/j.foodchem.2019.02.071
  13. Rodriguez-Huaman A, Casimiro-Gonzales S, Chavez-Perez JA, Gonzales-Arimborgo C, Cisneros-Fernandez R, Aguilar-Mendoza LA, et al. 2016. Antioxidant and neuroprotector effect of Lepidium meyenii (maca) methanol leaf extract against 6-hydroxy dopamine (6-OHDA)-induced toxicity in PC12 cells. Toxicol. Mech. Methods 27: 279-285. https://doi.org/10.1080/15376516.2016.1275908
  14. Choi EH, Kang JI, Cho JY, Lee SH, Kim TS, Yeo IH, et al. 2012. Supplementation of standardized lipid-soluble extract from maca (Lepidium meyenii) increases swimming endurance capacity in rats. J. Funct. Foods 4: 568-573. https://doi.org/10.1016/j.jff.2012.03.002
  15. Li S, Hao L, Kang Q, Cui Y, Jiang H, Liu X. 2017. Purification, characterization and biological activities of a polysaccharide from Lepidium meyenii leaves. Int. J. Biol. Macromol. 103: 1302-1310. https://doi.org/10.1016/j.ijbiomac.2017.05.165
  16. Tang W, Jin L, Xie L, Huang J, Wang N, Chu B, et al. 2017. Structural characterization and antifatigue effect in vivo of maca (Lepidium meyenii Walp) polysaccharide. J. Food Sci. 82: 757-764. https://doi.org/10.1111/1750-3841.13619
  17. Zhang Y, Liu C, Qi Y, Li S, Pan Y, Li Y. 2015. Circulating ultrasound-assisted extraction, countercurrent chromatography, and liquid chromatography for the simultaneous extraction, isolation, and analysis of the constituents of Uncaria tomentosa. J. Chromatogr. A. 1388: 36-42. https://doi.org/10.1016/j.chroma.2015.02.028
  18. Chavan Y, Singhal RS. 2013. Ultrasound-assisted extraction (UAE) of bioactives from arecanut (Areca catechu L.) and optimization study using response surface methodology. Innov. Food Sci. Emerg. 17: 106-113. https://doi.org/10.1016/j.ifset.2012.10.001
  19. Lo KM, Cheung PCK. 2005. Antioxidant activity of extracts from the fruiting bodies of Agrocybe aegerita var. alba. Food Chem. 89: 533-539. https://doi.org/10.1016/j.foodchem.2004.03.006
  20. Hwang ES, Thi ND. 2014. Antioxidant contents and antioxidant activities of hot-water extracts of aronia (Aronia melancocarpa) with different drying methods. Korean J. Food Sci. Technol. 46: 303-308. https://doi.org/10.9721/KJFST.2014.46.3.303
  21. Brand-Williams W, Cuvelier ME, Berset C. 1995. Use of a free radical method to evaluate antioxidant activity. Food Sci. Technol. 28: 25-30.
  22. Wang KJ, Zhang YJ, Yang CR. 2005. Antioxidant phenolic compounds from rhizomes of Polygonum paleaceum. J. Ethnopharmacol. 96: 483-487. https://doi.org/10.1016/j.jep.2004.09.036
  23. Lee YK, Chang YH. 2019. Physicochemical and antioxidant properties of methanol extract from Maca (Lepidium meyenii Walp.) leaves and roots. Food Sci. Technol. 39: 278-286. https://doi.org/10.1590/fst.03818
  24. Iris F, Benzie F, Strain JJ. 1996. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal. Biochem. 239: 70-76. https://doi.org/10.1006/abio.1996.0292
  25. Lee MH, Jang MH, Kim EK, Han SW, Cho SY, Kim CJ. 2005. Nitric oxide induces apoptosis in mouse C2C12 myoblast cells. J. Pharmacol. Sci. 97: 369-376. https://doi.org/10.1254/jphs.FPJ04017X
  26. Bosutti A, Degens H. 2015. The impact of resveratrol and hydrogen peroxide on muscle cell plasticity shows a dose-dependent interaction. Sci. Rep. 5: 8093. https://doi.org/10.1038/srep08093
  27. Kwon Y-S, Jeon In-S, Hwang J-H, Lim D-M, Kang Y-S, Chung H-J. 2009. Biological activities of maca (Lepidium meyenii) extracts. J. Korean Soc. Food Sci. Nutr. 38: 817-823. https://doi.org/10.3746/jkfn.2009.38.7.817
  28. Park S-J, Kwon S-P, Rha Y-A. 2017. Enhanacement of antioxidant activities of Crataegus pinnatifida bunge fruit by ultrasonification extraction processes. J. Korean Soc. Food Sci. Nutr. 46: 891-895. https://doi.org/10.3746/jkfn.2017.46.7.891
  29. Park S-J, Kim O-L, Rha Y-A. 2017. Component analysis and antioxidant activity of Maca. Culi. Sci. Hos. Res. 23: 137-144. https://doi.org/10.20878/cshr.2017.23.3.013013013
  30. Sandoval M, Okuhama NN, Angeles FM, Melchor VV, Condezo LA, Lao J, et al. 2002. Antioxidant activity of the cruciferous vegetable Maca (Lepidium meyenii). Food Chem. 79: 207-213. https://doi.org/10.1016/S0308-8146(02)00133-4
  31. Gan J, Feng Y, He Z, Li X, Zhang H. 2017. Correlations between antioxidant activity and alkaloids and phenols of maca (Lepidium meyenii). J. Food Qual. 2017: 3185945.
  32. Caicai K, Limin H, Liming Z, Zhiqiang Z, Yongwu Y. 2018. Isolation, purification and antioxidant activity of polysaccharides from the leaves of maca (Lepidium meyenii). Int. J. Biol. Macromol. 107: 2611-2619. https://doi.org/10.1016/j.ijbiomac.2017.10.139
  33. Droge W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82: 47-95. https://doi.org/10.1152/physrev.00018.2001
  34. Bergamini CM, Gambetti S, Dondi A, Cervellati C. 2004. Oxygen, reactive oxygen species and tissue damage. Curr. Pharm. Des. 10: 1611-1626. https://doi.org/10.2174/1381612043384664
  35. Siu PM, Wang Y, Alway SE. 2009. Apoptotic signaling induced by $H_2O_2$-mediated oxidative stress in differentiated C2C12 myotubes. Life Sci. 84: 468-481. https://doi.org/10.1016/j.lfs.2009.01.014
  36. Perry CG, Heigenhauser GJ, Bonen A, Spriet LL. 2008. High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl. Physiol. Nutr. Metab. 33: 1112-1123. https://doi.org/10.1139/H08-097
  37. Ydfors M, Hughes MC, Laham R, Schlattner U, Norrbom J, Perry CG. 2016. Modelling in vivo creatine/phosphocreatine in vitro reveals divergent adaptations in human muscle mitochondrial respiratory control by ADP after acute and chronic exercise. J. Physiol. 594: 3127-3140. https://doi.org/10.1113/JP271259
  38. An H, Seo S, Sim K, Kim J, Kim E, Lee M, et al. 2006. Antifatigue effect of chlorella vulgaris in mice. Korean J. Food Nutr. 19: 169-175.
  39. Wang J, Li S, Fan Y, Chen Y, Liu D, Cheng H, et al. 2010. Anti-fatigue activity of the water-soluble polysaccharides isolated from Panax ginseng CA Meyer. J. Ethnopharmacol. 130: 421-423. https://doi.org/10.1016/j.jep.2010.05.027
  40. Xu C, Lv J, Lo YM, Cui SW, Hu X, Fan M. 2013. Effects of oat $\beta$-glucan on endurance exercise and its anti-fatigue properties in trained rats. Carbohydr. Polym. 92: 1159-1165. https://doi.org/10.1016/j.carbpol.2012.10.023
  41. Huang Y, Wang Y, Li W, Zhan J, Lei J, Li N, et al. 2019. Evaluation of anti-fatigue property of Porphyridium cruentum in mice. Trop. J. Pharm. Res. 18: 579-584.
  42. Yang Q, Jin W, Lv X, Dai P, Ao Y, Wu M, et al. 2016. Effects of macamides on endurance capacity and anti-fatigue property in prolonged swimming mice. Pharm. Biol. 54: 827-834. https://doi.org/10.3109/13880209.2015.1087036
  43. Li J, Sun Q, Meng Q, Wang L, Xiong W, Zhang L. 2017. Anti-fatigue activity of polysaccharide fractions from Lepidium meyenii Walp (maca). Int. J. Biol. Macromol. 95: 1305-1311. https://doi.org/10.1016/j.ijbiomac.2016.11.031
  44. Tang W, Jin L, Xie L, Huang J, Wang N, Chu B, et al. 2017. Structural characterization and antifatigue effect in vivo of maca (Lepidium meyenii Walp) polysaccharide. J. Food Sci. 82: 757-764. https://doi.org/10.1111/1750-3841.13619