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Original Paper Hypoxia Tolerance and Fatigue Relief Produced By _ Food Science and Technology Research, 22 (5), 611 621, 2016 Copyright © 2016, Japanese Society for Food Science and Technology doi: 10.3136/fstr.22.611 http://www.jsfst.or.jp Original paper Hypoxia Tolerance and Fatigue Relief Produced by Lepidium meyenii and its Water-soluble Polysaccharide in Mice 1 2 1 1 1 1 Xiao-Feng CHEN , Yan-Yun LIU , Min-Jie CAO , Ling-Jing ZHANG , Le-Chang SUN , Wen-Jin SU and 1* Guang-Ming LIU 1College of Food and Biological Engineering, Xiamen Key Laboratory of Marine Functional Food, Fujian Provincial, Engineering Technology Research Center of Marine Functional Food, Fujian Collaborative Innovation Center for Exploitation and Utilization of Marine Biological Resources, Jimei University, 43 Yindou Road, Xiamen, Fujian, 361021, China 2Xiamen Everbright Biotechnology Ltd, 68 Hubinbei Road, Xiamen, Fujian, 361001, China Received November 14, 2015 ; Accepted January 24, 2016 The aim of the present study was to investigate the effects of Lepidium meyenii (maca) on hypoxia tolerance and fatigue relief, and to determine its active constituents. The results showed that, in the mouse model, maca powder could significantly prolong hypoxia time (HT) and forced swim time (FST) and optimize blood sugar ratio (BSR), liver glycogen (LG), muscle glycogen (MG), blood lactic acid, and lactic dehydrogenase. Based on these results, aqueous extracts and maca water-soluble polysaccharide (MWP) were isolated. The total sugar content of MWP is 90.41 ± 2.55%, and the main monosaccharide component is glucose (79.88%). In the mouse model, HT (40.76 ± 7.97 min), FST (48.32 ± 10.76 min), BSR (4.49 ± 4.04%), LG (11.27 ± 0.61 mg/g), and MG (1.45 ± 0.17 mg/g) were all significantly enhanced in groups given maca powder compared to the control group (p < 0.05). In summary, maca is effective in improving hypoxia tolerance and relieving fatigue, and MWP is the active substance. Keywords: maca (Lepidium meyenii), maca aqueous extracts, maca water-soluble polysaccharide, relieve fatigue, hypoxia tolerance, BALB/c mice Introduction Hyung, Rogers, Shao, Huang, Lu, Qien and Zheng, 2000). Maca (Lepidium meyenii) is a plant that belongs to the Brassica Maca has been utilized for almost 2000 years (Ganzera, Zhao family, Lepidium genus (Gustavo, 2012), which is native to areas and Khan), with people mainly consuming its tubers for extra in the Andes in South America with elevations over 4000 m. It is nutrition and treating diseases (Gonzales-Castañeda, Rivera, mainly cultivated in Peru (Gonzales, Gonzales. and Gonzales, Chirinos, Evelson and Gonzales, 2011). Modern technology and 2009). In dried form, maca has abundant carbohydrates (59.0%), methods have been employed to confirm or explore the different proteins (10.2%) and lipids (2.2%) (Dini, Migliuolo, Rastrelli, kinds of bioactive effects of maca. Rubio et al. established an Saturnino and Schettino, 1993), and contains amino acids, minerals animal model via ovariectomy, and found that black maca could (Gustavo, 2012), and secondary metabolites (Zheng, He, Kim, improve experimental memory impairment induced by ovariectomy Abbreviations: BLA, blood lactic acid; BSR, blood sugar ratio; FST, forced swim time; HT, hypoxia time; LDH, lactic dehydrogenase; LG, liver glycogen: MAE, maca aqueous extracts; MG, muscle glycogen; MWP, maca water-soluble polysaccharide; *To whom correspondence should be addressed. E-mail: [email protected] 612 X.-F. CHEN et al. (Rubio, Qiong, Liu, Jiang, Dang, Chen and Gonzales, 2011). Zheng a BALB/c mouse model in which hypoxia time could be tested to et al. found that lipid extracts of maca could enhance the sexual evaluate hypoxia tolerance induced by maca, and forced swim time function of mice and rats (Zheng, He, Kim, Hyung, Rogers, Shao, (FST) could be used as the exercise index with the biochemical Huang, Lu, Qien and Zheng, 2000). Ai et al. established a mouse parameters blood sugar ratio (BSR), LG, MG, LDH, BLA, and model of chronic unpredictable mild stress (CUMS), and BUN measured to investigate the fatigue-relieving activity of demonstrated the antidepressant-like effect of the petroleum ether maca. Furthermore, the active components could be isolated by extract of maca (Ai, Cheng, Yu, Yu and Jin, 2014). Furthermore, extraction and purification, to provide theoretical support for the anti-oxidant effects (Večeřa, Orolin, Škottová, Kazdová, Oliyarnik, use of maca as a functional food. Ulrichová and Simanek, 2007), and decreases in serum IL-6 levels (Gonzales, Gasco and Lozada, 2013) produced by maca have been Materials and Methods reported. Maca Maca powder used in this study was cultivated in Muscles experience a progressive decline in performance when Lijiang city, Yunnan province, China, and was provided by used intensively, but normally recover after a period of rest. This Xiamen Everbright Biotechnology Ltd, Fujian, China reversible phenomenon is denoted muscle fatigue (Westerblad, et Chemicals and reagents Ethyl alcohol, anthrone, sulfuric acid, al. 2003). Fatigue may decrease work efficiency and reduce quality soda lime, arabinose, galactose, xylose, and glucose were of life. Available therapies in modern medicine for relieving or purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, preventing fatigue are limited; hence, more and more people are China). NaOH was purchased from Guanghua Sci-tech Co., Ltd. turning to traditional medicine (Zhang, Ren, Huang, Ding, Zhou (Shantou, Guangdong, China). Vaseline was purchased from and Liu, 2010). Methods of evaluating fatigue relief are various. Shanghai Reagent Factory (Shanghai, China). Trifluoroacetic acid, For example, the forced swim test is directly related to the capacity trichloroacetic acid, BaCl2, and K2SO4 were purchased from Xilong to relieve fatigue in mice (Wang, Yan and Cai, 2014). A previous Chemical Co., Ltd. (Shantou, Guangdong, China). Gelatin was study speculated that depletion of energy storage and accumulation purchased from Genebase Gene-tech Co., Ltd. (Shanghai, China); of metabolic products in the body may lead to fatigue (Zhang, Liu, nitrogen gas was purchased from Linder Gas (Xiamen, Fujian, Zhou, Wang and Sun, 2014). Blood sugar is the most preferred China). Cellulase was purchased from Novozymes (Tianjin, energy source that is mobilized during exercise. Extensive exercise China). often leads to a decrease in blood sugar level, and weakens exercise Animals Female BALB/c mice were purchased from Slaccas performance of the body (Kumar, Anand, Singsit, Khanum and Lab Animal Ltd. (Shanghai, China) at 6 _ 8 weeks old. Mice were Anilakumar, 2013). During extensive exercise, the body cannot get housed in a specific pathogen-free (SPF) barrier room (room enough energy via aerobic respiration only, so glycolysis becomes temperature 23 ± 2℃, relative humidity 50% _ 70%, 12/12 h light/ an important energy source. In the glycolysis pathway, lactate dark cycle), and food and water were available ad libitum. All dehydrogenase (LDH) is the key enzyme. An increase in LDH experiments were carried out following the institutional and would accelerate the glycolysis process, producing more energy as national guidelines, SCXK 2012-0005, and all animals were used well as blood lactic acid (BLA). Lactic acid may cause fatigue for academic research. according to Hill and Kupalov’s research (Hill, et al., 1929), so it Use of the BALB/c mouse model to determine hypoxia is also often detected as an indicator in anti-fatigue tests (Hao, Cao, tolerance and fatigue- relieving activities of maca powder Hao and Zhang, 2013; Xu, Lv, Lo, Cui, Hu and Fan, 2012). Mouse model design. After 1 week of adaption, 48 selected Glycogen, including liver glycogen (LG) and muscle glycogen mice were randomly divided into four groups (12 mice in each (MG), is an important energy source stored in the body. Glycogen group): a high-dose group, a medium-dose group, and a low-dose could be used to complement the consumption of blood sugar (Ren, group, which were treated with maca powder at doses of 1, 0.5, or Zhao, Wang, Cui and You, 2011; Shao, Wang and Zheng, 2013). 0.1 g/kg body weight, respectively; a control group, which was Because of its importance as an energy source, glycogen is often treated with distilled water. Maca samples were dispersed in selected as an index for evaluating relief of fatigue (Lin, Liu, Fang, distilled water and given by oral administration continuously for Yu, Xiong and Ke, 2014). Proteins and amino acids are other 30 days. Body weight was measured using an electronic balance sources of energy, and blood urea nitrogen (BUN) reflects the (Yingpai, Shanghai, China). production of proteins and amino acid metabolism (Wang, Shieh, Hypoxia tolerance test. Hypoxia tolerance was measured Kuo, Lee and Pan, 2006). It has been reported that BUN is 30 minutes after the latest treatment, following the method of Luo significantly positively correlated with exercise and endurance time (Luo, Cai and Hu, 2014), with modifications. In brief, three mice (You, Zhao, Regenstein and Ren, 2011). from each group were placed individually into a 250 mL sealable If the hypoxia tolerance and fatigue-relieving activities of maca glass bottle containing 15 g of soda lime, and vaseline was smeared could be established, then its active substances could be around the cap to enhance the seal. Each mouse remained in the determined. Therefore, the aim of the present study was to establish bottle until it succumbed to oxygen deficiency and died. The The Activities of Relieving Fatigue of Lepidium meyenii 613 survival time was recorded as the hypoxia time (HT). Because the Extraction and purification of maca water-soluble mice in HT test were expected to die after the experiment, polysaccharide A certain amount of MAE was dissolved with considering the welfare of mice, fewer mice were used in HT test distilled water, and ethyl alcohol was added to a final concentration than that in forced swim test. of 80%, with stirring for 6 h. The mixture was centrifuged Forced swim test.
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