Skip to main content

Advertisement

SpringerLink
Log in

The in vitro biological activity of Lepidium meyenii extracts

  • Published:
Cell Biology and Toxicology Aims and scope Submit manuscript

Abstract

The biological activity of methanolic and aqueous extracts from dehydrated hypocotyls of Lepidium meyenii (Brassicaceae, vernacular name “maca”), was studied on rat hepatocytes and human breast cancer MCF-7 cells. The extracts did not exhibit cytotoxicity in hepatocyte primary cultures up to 10 mg/ml as measured by the MTT viability test, and lactate dehydrogenase (LDH) and aspartate aminotransferase (AST) leakage. Moreover, after 72 h, extracts inhibited LDH and AST leakage from the hepatocytes. When hepatocytes were intoxicated by t-butyl hydroperoxide, neither extract prevented oxidative damage. Both extracts showed weak antioxidant activity in the DPPH radical scavenging test with IC50 values of 3.46 ± 0.16 and 0.71 ± 0.10 mg/ml, for aqueous and methanolic extracts, respectively. Thus, the observed effect on spontaneous enzyme leakage is probably mediated through mechanisms other than antioxidant activity. Both methanolic and aqueous extracts have shown estrogenic activity comparable with that of silymarin in MCF-7 cell line. Maca estrogenicity was exhibited in the range from 100 to 200 μg of extract per ml. The findings in the present study show that maca does not display in vitro hepatotoxicity. In contrast, a slight cytoprotective effect, probably not mediated by antioxidant capacity, was noted. Maca extracts exhibited estrogenic activity comparably to the effect of silymarin in MCF-7 cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AST:

aspartate aminotransferase

DMEM:

Dulbecco's modified Eagle medium

DMSO:

dimethyl sulfoxide

DPPH:

1,1-diphenyl-2-picrylhydrazyl

GC-MS:

gas chromatography – mass spectrometry

IC50:

50% inhibitory concentration

LDH:

lactate dehydrogenase

MTT:

3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

TBA:

2-thiobarbituric acid

tBH:

t-butyl peroxide

References

  • Aliaga E, Aliaga R. Guia para el cultivo, aprovechamiento y conservacion de la maca, Lepidium meyenii Walpers. Santafé de Bogotá: Convenio Andres Bello; 1998.

  • Almstrup K, Fernandez MF, Petersen JH, Olea N, Skakkebaek NE, Leffers H. Dual effects of phytoestrogens result in u-shaped dose-response curves. Environ Health Perspect. 2002; 110:743–8.

    CAS  PubMed  Google Scholar 

  • Aquila S, Sisci D, Gentile M, Middea E, Catalano S, Carpino A, Rago V, Ando S. Estrogen receptor (ER) alpha and ER beta are both expressed in human ejaculated spermatozoa: evidence of their direct interaction with phosphatidylinositol-3-OH kinase/Akt pathway. J Clin Endocrinol Metab. 2004;89:1443–51.

    Article  CAS  PubMed  Google Scholar 

  • Baker VA, Hepburn PA, Kennedy SJ, Jones PA, Lea LJ, Sumpter JP, Ashby J. Safety evaluation of phytosterol esters. Part 1. Assessment of oestrogenicity using a combination of in vivo and in vitro assays. Food Chem Toxicol. 1999;37:13–22.

    CAS  PubMed  Google Scholar 

  • Balick MJ, Lee R. Maca: from traditional food crop to energy and libido stimulant. Altern Ther Health Med. 2002;8:96–8.

    Google Scholar 

  • Bergmeyer HU, Bernt E. Lactate dehydrogenase: UV-Assay with pyruvate and NADH. In: Bergmeyer HU, ed. New York: Academic Press; 1974:574–6.

  • Bergmeyer HU, Horder M. International federation of clinical chemistry. Scientific committee. Expert panel on enzymes. IFCC document stage 2, draft 1; 1979-11-19 with a view to an IFCC recommendation. IFCC methods for the measurement of catalytic concentration of enzymes. Part 3. IFCC method for alanine aminotransferase. J Clin Chem Clin Biochem. 1980; 18:521–34.

    Google Scholar 

  • Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol. 1978;52:302–10.

    CAS  PubMed  Google Scholar 

  • Bustos-Obregon E, Yucra S, Gonzales GF. Lepidium meyenii (Maca) reduces spermatogenic damage induced by a single dose of malathion in mice. Asian J Androl. 2005;7:71–6.

    PubMed  Google Scholar 

  • Canales M, Aguilar J, Prada A, Marcelo A, Huaman C, Carbajal L. Nutritional evaluation of Lepidium meyenii (MACA) in albino mice and their descendant. Archivos Latinoamericanos De Nutricion. 2000;50:126–33.

    CAS  PubMed  Google Scholar 

  • Chen WF, Huang MH, Tzang CH, Yang M, Wong MS. Inhibitory actions of genistein human breast cancer (MCF-7) cells. Biochim Biophys Acta. 2003; 1638:187–96.

    CAS  PubMed  Google Scholar 

  • Chung F, Rubio J, Gonzales C, Gasco M, Gonzales GF. Dose-response effects of Lepidium meyenii (Maca) aqueous extract on testicular function and weight of different organs in adult rats. J Ethnopharmacol. 2005;98:143–7.

    Article  PubMed  Google Scholar 

  • Cicero AF, Bandieri E, Arletti R. Lepidium meyenii Walp. improves sexual behaviour in male rats independently from its action on spontaneous locomotor activity. J Ethnopharmacol. 2001;75:225–9.

    Article  CAS  PubMed  Google Scholar 

  • Cicero AF, Piacente S, Plaza A, Sala E, Arletti R, Pizza C. Hexanic Maca extract improves rat sexual performance more effectively than methanolic and chloroformic Maca extracts. Andrologia. 2002;34:177–9.

    Article  CAS  PubMed  Google Scholar 

  • Cui B, Zheng BL, He K, Zheng QY. Imidazole alkaloids from Lepidium meyenii. J Nat Prod. 2003;66:1101–3.

    Article  CAS  PubMed  Google Scholar 

  • Cummings AM, Laws SC. Assessment of estrogenicity by using the delayed implanting rat model and examples. Reprod Toxicol. 2000;14:111–7.

    Article  CAS  PubMed  Google Scholar 

  • Dini A, Migliuolo G, Rastrelli L, Saturnino P, Shettino O. Chemical composition of Lepidium meyenii. Food Chem. 1994;49: 347–9.

    Article  CAS  Google Scholar 

  • Dini I, Tenore GC, Dini A. Glucosinolates from maca (Lepidium meyenii). Biochem Syst Ecol 2002;30:1087–90.

    CAS  Google Scholar 

  • Duda RB, Zhong Y, Navas V, Li MZ, Toy BR, Alavarez JG. American ginseng and breast cancer therapeutic agents synergistically inhibit MCF-7 breast cancer cell growth. J Surg Oncol. 1999;72:230–9.

    Article  CAS  PubMed  Google Scholar 

  • Flores H, Walker T, Guimaraes R, PalBais H, Vivanco J. Andean root and tuber crops: underground rainbows. HortScience. 2003;38:161–7.

    Google Scholar 

  • Ganzera M, Zhao J, Muhammad I, Khan IA. Chemical profiling and standardization of Lepidium meyenii (maca) by reversed phase high performance liquid chromatography. Chem Pharm Bull. 2002;50:988–91.

    Article  CAS  PubMed  Google Scholar 

  • Gonzales GF, Cordova A, Gonzales C, Chung A, Vega K, Villena A. Lepidium meyenii (Maca) improved semen parameters in adult men. Asian J Androl. 2001a;3:301–3.

    CAS  Google Scholar 

  • Gonzales GF, Ruiz A, Gonzales C, Villegas L, Cordova A. Effect of Lepidium meyenii (maca) roots on spermatogenesis of male rats. Asian J Androl. 2001b;3:231–3.

    CAS  Google Scholar 

  • Gonzales GF, Cordova A, Vega K, Chung A, Villena A, Gonez C, Castillo S. Effect of Lepidium meyenii (MACA) on sexual desire and its absent relationship with serum testosterone levels in adult healthy men. Andrologia. 2002;34:367–72.

    CAS  PubMed  Google Scholar 

  • Gonzales GF, Cordova A, Vega K, Chung A, Villena A, Gonez C. Effect of Lepidium meyenii (Maca), a root with aphrodisiac and fertility-enhancing properties, on serum reproductive hormone levels in adult healthy men. J Endocrinol. 2003a; 176: 163–8.

    Article  CAS  Google Scholar 

  • Gonzales GF, Rubio J, Chung A, Gasco M, Villegas L. Effect of alcoholic extract of Lepidium meyenii (Maca) on testicular function in male rats. Asian J Androl. 2003b;5:349–52.

    Google Scholar 

  • Gonzales GF, Miranda S, Nieto J, Fernandez G, Yucra S, Rubio J, Yi P, Gasco M. Red maca (Lepidium meyenii) reduced prostate size in rats. Reprod Biol Endocrinol. 2005;3:5.

    PubMed  Google Scholar 

  • Lee KJ, Dabrowski K, Rinchard J, Gomez C, Guz L, Vilchez C. Supplementation of maca (Lepidium meyenii) tuber meal in diets improves growth rate and survival of rainbow trout Oncorhynchus mykiss (Walbaum) alevins and juveniles. Aquacult. Res. 2004;35:215–23.

    Article  Google Scholar 

  • Lee KJ, Dabrowski K, Sandoval M, Miller MJS. Activity-guided fractionation of phytochemicals of maca meal, their antioxidant activities and effects on growth, feed utilization, and survival in rainbow trout (Oncorhynchus mykiss) juveniles. Aquaculture. 2005;244:293–301.

    Article  CAS  Google Scholar 

  • Lee YS, Park JS, Cho SD, Son JK, Cherdshewasart W, Kang KS. Requirement of metabolic activation for estrogenic activity of Pueraria mirifica. J Vet Sci. 2002;3:273–7.

    CAS  PubMed  Google Scholar 

  • Li G, Ammermann U, Quirós CF. Glucosinolate contents in maca (Lepidium peruvianum Chacón) seeds, sprouts, mature plants and several derived commercial products. Econ Bot. 2001;55:255–62.

    CAS  Google Scholar 

  • Liu Z, Yang Z, Zhu M, Huo J. Estrogenicity of black cohosh (Cimicifuga racemosa) and its effect on estrogen receptor level in human breast cancer MCF-7 cells. Wei Sheng Yan Jiu. 2001;30:77–80.

    CAS  PubMed  Google Scholar 

  • López-Fando A, Gómez-Serranillos MP, Iglesias I, Lock O, Upamayta UP, Carretero ME. Lepidium peruvianum Chacon restores homeostasis impaired by restraint stress. Phytother Res. 2004;18:471–4.

    Article  PubMed  Google Scholar 

  • Mellanen P, Petanen T, Lehtimaki J, Makela S, Bylund G, Holmbom B, Mannila E, Oikari A, Santti R. Wood-derived estrogens: studies in vitro with breast cancer cell lines and in vivo in trout. Toxicol Appl Pharmacol. 1996;136:381–8.

    Article  CAS  PubMed  Google Scholar 

  • Mensor LL, Menezes FS, Leitao GG, Reis AS, dos Santos TC, Coube CS, Leitao SG. Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytother Res. 2001;15:127–30.

    Article  CAS  PubMed  Google Scholar 

  • Moldeus P, Hogberg J, Orrenius S. Isolation and use of liver cells. Methods Enzymol. 1978;52:60–71.

    CAS  PubMed  Google Scholar 

  • Muhammad I, Zhao J, Dunbar DC, Khan IA. Constituents of Lepidium meyenii ‘maca’. Phytochemistry. 2002;59:105–10.

    Article  CAS  PubMed  Google Scholar 

  • O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev. 2001;22:289–318.

    Article  PubMed  Google Scholar 

  • Okubo T, Kano I. Studies on estrogenic activities of food additives with human breast cancer MCF-7 cells and mechanism of estrogenicity by BHA and OPP. Yakugaku Zasshi. 2003;123:443–52.

    Article  CAS  PubMed  Google Scholar 

  • Piacente S, Carbone V, Plaza A, Zampelli A, Pizza C. Investigation of the tuber constituents of maca (Lepidium meyenii Walp.). J Agric Food Chem. 2002;50:5621–5.

    Article  CAS  PubMed  Google Scholar 

  • Plíšková M, Vondráček J, Křen V, Gažák R, Sedmera P, Walterová D, Psotová J, Šimánek V, Machala M. Effects of silymarin flavonolignans and synthetic silybin derivatives on estrogen and aryl hydrocarbon receptor activation. Toxicology. 2005;215:80–9.

    PubMed  Google Scholar 

  • Popovici GC. La importancia de Lepidium peruvianum (“Maca”) en la alimentación y salud del ser humano y animal 2,00 anos antes y desputa del Cristo y en el siglo XXI. Lima: Servicios Grá Gficos “ROMERO”; 1997.

  • Psotová J, Chlopčíková S, Grambal F, Šimánek V, Ulrichová J. Influence of silymarin and its flavonolignans on doxorubicin-iron induced lipid peroxidation in rat heart microsomes and mitochondria in comparison with quercetin. Phytother Res. 2002;16 (Suppl 1) :S63–7.

    PubMed  Google Scholar 

  • Psotová J, Kolář M, Soušek J, Švagera Z, Vičar J, Ulrichová J. Biological activities of Prunella vulgaris extract. Phytother Res. 2003;17:1082–7.

    Article  PubMed  Google Scholar 

  • Quirós CF, Aliaga RC Maca. Lepidium meyenii Walp. In: Hermann M, Heller J, eds. Rome: IPGRI;1997:173–97.

  • Robertson KM, O'Donnell L, Simpson ER, Jones ME. The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology. 2002;143:2913–21.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblum ER, Stauber RE, Van Thiel DH, Campbell IM, Gavaler JS. Assessment of the estrogenic activity of phytoestrogens isolated from bourbon and beer. Alcohol Clin Exp Res. 1993;17:1207–9.

    CAS  PubMed  Google Scholar 

  • Sandoval M, Okuhama NN, Angeles FM, Melchor VV, Condezo LA, Lao J, Miller MJS. Antioxidant activity of the cruciferous vegetable Maca (Lepidium meyenii). Food Chem. 2002;79:207–13.

    Article  CAS  Google Scholar 

  • Seidlova-Wuttke D, Becker T, Christoffel V, Jarry H, Wuttke W. Silymarin is a selective estrogen receptor beta (ERbeta) agonist and has estrogenic effects in the metaphysis of the femur but no or antiestrogenic effects in the uterus of ovariectomized (ovx) rats. J Steroid Biochem Mol Biol. 2003;86:179–88.

    CAS  PubMed  Google Scholar 

  • Sieuwerts AM, Klijn JG, Peters HA, Foekens JA. The MTT tetrazolium salt assay scrutinized: how to use this assay reliably to measure metabolic activity of cell cultures in vitro for the assessment of growth characteristics, IC50-values and cell survival. Eur J Clin Chem Clin Biochem. 1995;33:813–23.

    CAS  PubMed  Google Scholar 

  • Simpson E, Rubin G, Clyne C, Robertson K, O'Donnell L, Jones M, Davis S. The role of local estrogen biosynthesis in males and females. Trends Endocrinol Metab. 2000;11:184–8.

    CAS  PubMed  Google Scholar 

  • Soto AM, Lin TM, Justicia H, Silvia RM, Sonnenschein C. An “in culture” bioassay to assess the estrogenicity of xenobitics (E-screen). In: Colborn T, Ckenent C, eds. Princeton, NJ: Princeton Scientific Publishing; 1992:295–309.

  • Tsai PS, Kessler AE, Jones JT, Wahr KB. Alteration of the hypothalamic–pituitary–gonadal axis in estrogen- and androgen-treated adult male leopard frog, Rana pipiens. Reprod Biol Endocrinol. 2005;3:2.

    Article  PubMed  Google Scholar 

  • Valentová K, Ulrichová J. Smallanthus sonchifolius and Lepidium meyenii—prospective Andean crops for the prevention of chronic diseases. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2003;147:119–30.

    PubMed  Google Scholar 

  • Valentová K, Cvak L, Muck A, Ulrichová J, Šimánek V. Antioxidant activity of extracts from the leaves of Smallanthus sonchifolius. Eur J Nutr. 2003;42:61–6.

    PubMed  Google Scholar 

  • Valentová K, Moncion A, de Waziers I, Ulrichová J. The effect of Smallanthus sonchifolius leaf extracts on rat hepatic metabolism. Cell Biol Toxicol. 2004;20:109–20.

    Article  PubMed  Google Scholar 

  • Zheng BL, He K, Kim CH, Rogers L, Shao Y, Huang ZY, Lu Y, Yan SJ, Qien LC, Zheng QY. Effect of a lipidic extract from Lepidium meyenii on sexual behavior in mice and rats. Urology. 2000;55:598–602.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Medical Chemistry and Biochemistry, Faculty of Medicine, Palacký University, Olomouc

    K. Valentová, J. Ulrichová & V. Šimánek

  2. Department of Teratology, Institute of Experimental Medicine, Czech Republic

    D. Buckiová

  3. Laboratory of Biotransformation, Institute of Microbiology, Czech Republic

    V. Křen

  4. Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Prague, Czech Republic

    J. Pěknicová

  5. Institute of Medical Chemistry and Biochemistry, Faculty of Medicine, Palacký University, Hněvotínská 3, 775 15, Olomouc, Czech Republic

    K. Valentová

Authors
  1. K. Valentová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Buckiová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Křen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Pěknicová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Ulrichová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Šimánek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Valentová.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valentová, K., Buckiová, D., Křen, V. et al. The in vitro biological activity of Lepidium meyenii extracts. Cell Biol Toxicol 22, 91–99 (2006). https://doi.org/10.1007/s10565-006-0033-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10565-006-0033-0

Keywords

Search

Navigation