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2023 Vol.41, Issue 5

Research Article

Comparison of Rutin Content, Anti-Cancer Activity, and Anti-Obesity Effect of Four Asparagus (Asparagus officinalis) Cultivars
Myoung Sun Kang1†
,
Thi Luyen Cao23†
,
Tae Heon Lee145
,
Nathan Cho6
,
Tae Gyu Yi7
,
Nam il Park7
,
Baul Ko8
,
Ho Cheol Kim145
,
Jong Hyang Bae145
,
Yang Gyu Ku145*
1Department of Horticulture Industry, Wonkwang University, Iksan 54538, Korea
2Faculty of Agriculture and Natural Resources, An Giang University, An Giang 880000, Vietnam
3Vietnam National University, Ho Chi Minh City 700000, Vietnam
4Institute of Life Science and Natural Resources, Wonkwang University, Iksan 54538, Korea
5Institute of Plant Breeding, Wonkwang University, Iksan 54538, Korea
6Kyugnong Gimje Future Agricultural Center, Gimje 54338, Korea
7Department of Plant Science, Gangneung-Wonju National University, Gangneung 25457, Korea
8Post-Doctoral Researcher, National Institute of Horticultural and Herbal Science, Wanju 55365, Korea
*Corresponding Author
†These authors contributed equally to this work.
31 October 2023. pp. 497-507
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Abstract

This study aimed to compare rutin content, anti-cancer activity against Calu-6 lung, HCT-116 colorectal, and MCF-7 breast cancer cell lines and anti-obesity activity of Jersey Giant, Jersey Supreme, NJ953, and UC157 asparagus cultivars. The rutin content in the spears of the four cultivars gradually decreased from the tip to the basal segments. In the spear tip segments, the rutin content of the Jersey Giant and UC157 cultivars was higher than that in the Jersey Supreme and NJ953 cultivars; whereas the rutin content in the basal segments of Jersey Supreme and UC157 spears was higher than that of Jersey Giant and NJ953 cultivars. The rutin content in the whole spear of the UC157 cultivar was significantly higher than that in Jersey Giant and NJ953 spears. Asparagus spears exhibited anti-cancer activity against HCT-116 colorectal cancer cells more effectively than Calu-6 lung and MCF-7 breast cancer cells, as demonstrated by the lower viability of HCT-116 colorectal cancer cells compared to the viability of the other cancer cell lines. The Jersey Giant cultivar showed higher anti-cancer activity against Calu-6 lung cancer cell line at spear extract concentrations of 400 and 800 µg·mL-1. The UC157 cultivar showed higher anti-cancer activity against HCT-116 colorectal cancer cells at spear extract concentrations from 100 to 800 µg·mL-1 compared to Jersey Giant and Jersey Supreme cultivars. The rutin content was negatively correlated with the viability of HCT-116 colorectal and MCF-7 breast cancer cells, indicating that the high rutin content of the UC157 cultivar is linked to high anti-cancer activity against HCT-116 colorectal and MCF-7 breast cancer cells. The spear extracts from the four asparagus cultivars significantly decreased lipid accumulation. There were no significant differences in the effects to 3T3-L1 preadipocyte viability and lipid accumulation among the four cultivars. These results suggest the potential of the UC157 cultivar with its high rutin content and anti-cancer activity against HCT-116 colorectal cancer cells, also suggest that the consumption of asparagus may contribute to the alleviation of obesity.

Keywords
asparagus spear
Calu-6
HCT-116
lipid accumulation
MCF-7
References
1
Abotaleb M, Liskova A, Kubatka P, Büsselberg D (2020) Therapeutic potential of plant phenolic acids in the treatment of cancer. Biomolecules 10:221. doi:10.3390/biom10020221 10.3390/biom1002022132028623PMC7072661
2
Akhtar MF, Saleem A, Rasul A, Baig MMFA, Bin-Jumah M, Daim MMA (2020) Anticancer natural medicines: An overview of cell signaling and other targets of anticancer phytochemicals. Eur J Pharmacol 888:173488. doi:10.1016/j.ejphar.2020.173488 10.1016/j.ejphar.2020.17348832805253
3
Aksorn N, Chanvorachote P (2019) Integrin as a molecular target for anti-cancer approaches in lung cancer. Anticancer Res 39:541-548. doi:10.21873/anticanres.13146 10.21873/anticanres.1314630711928
4
Alonso-Castro AJ, Domínguez F, García-Carrancá A (2013) Rutin exerts antitumor effects on nude mice bearing sw480 tumor. Arch Med Res 44:346-351. doi:10.1016/j.arcmed.2013.06.002 10.1016/j.arcmed.2013.06.00223867787
5
Benson BL (2001) Second international asparagus cultivar trial final report. Acta Hortic 589:159-166. doi:10.17660/ActaHortic.2002.589.22 10.17660/ActaHortic.2002.589.22
6
Bousserouel S, Le Grandois J, Gossé F, Werner D, Barth SW, Marchioni E, Marescaux J, Raul F (2013) Methanolic extract of white asparagus shoots activates TRAIL apoptotic death pathway in human cancer cells and inhibits colon carcinogenesis in a preclinical model. Int J Oncol 43:394-404. doi:10.3892/ijo.2013.1976 10.3892/ijo.2013.197623754197PMC3775565
7
Cao TL, Shawon AR, Cho N, Lee TH, Ko B, Kim HC, Bae JH, Ku YG (2022a) Effects of shade treatment on plant growth characteristics, phenolic content, activity of antioxidant enzymes, and antioxidant activity of male cultivar asparagus (Asparagus officinalis L.). Hortic Sci Technol 40:273-285. doi:10.7235/HORT.20220026 10.7235/HORT.20220026
8
Cao TL, Cho N, Lee TH, Ahn SJ, Lee DJ, Ku YG (2022b) Bioactive substances, antioxidant enzymes, and anti-cancer activity of Asparagus 'Atlas' grown in an open field and rain-shelter house system. Hortic Environ Biotechnol 63:809-821. doi:10.1007/s13580-022-00470-2 10.1007/s13580-022-00470-2
9
Chitrakar B, Zhang M, Adhikari B (2019) Asparagus (Asparagus officinalis): Processing effect on nutritional and phytochemical composition of spear and hard-stem byproducts. Trends Food Sci Technol 93:1-11. doi:10.1016/j.tifs.2019.08.020 10.1016/j.tifs.2019.08.020
10
Dias JS (2012) Nutritional quality and health benefits of vegetables: A review. J Food Nutr Sci 3:1354-1374. doi:10.4236/fns.2012.310179 10.4236/fns.2012.310179
11
Drinkwater JM, Tsao R, Liu R, Defelice C, Wolyn DJ (2015) Effects of cooking on rutin and glutathione concentrations and antioxidant activity of green asparagus (Asparagus officinalis) spears. J Funct Foods 12:342-353. doi:10.1016/j.jff.2014.11.013 10.1016/j.jff.2014.11.013
12
Drost D (2001) Asparagus cultivar trials in Utah. Acta Hortic 589:167-171. doi:10.17660/ActaHortic.2002.589.23 10.17660/ActaHortic.2002.589.23
13
Eichholz I, Rohn S, Gamm A, Beesk N, Herppich WB, Kroh LW, Ulrichs C, Huyskens-Keil S (2012) UV-B-mediated flavonoid synthesis in white asparagus (Asparagus officinalis L.). Food Res Int 48:196-201. doi:10.1016/j.foodres.2012.03.008 10.1016/j.foodres.2012.03.008
14
Elmer WH, LaMondia J, Taylor GS (1997) Asparagus cultivar trials in connecticut. Acta Hortic 479:189-198. doi:10.17660/ActaHortic.1999.479.26 10.17660/ActaHortic.1999.479.26
15
Eum HL, Yi TG, Hong SJ, Park NI (2020) Variations of bioactive compound contents and antioxidant capacity of asparagus seedlings in 23 varieties. Hortic Sci Technol 38:291-302. doi:10.7235/HORT.20200028 10.7235/HORT.20200028
16
González MI (2009) Results of the third international asparagus cultivar trial at Chillan, Chile. Acta Hortic 950:109-115. doi:10.17660/ActaHortic.2012.950.11 10.17660/ActaHortic.2012.950.11
17
Guo Q, Wang N, Liu H, Li Z, Lu L, Wang C (2020) The bioactive compounds and biological functions of Asparagus officinalis L.-a review. J Funct Foods 65:103727. doi:10.1016/j.jff.2019.103727 10.1016/j.jff.2019.103727
18
Haihong Y, Zeng J, Kumano T, Fujii M, Araki H (2017) New asparagus cultivars suitable for outdoor cultivation in Hokkaido, Japan. Acta Hortic 1223:25-32. doi:10.17660/ActaHortic.2018.1223.4 10.17660/ActaHortic.2018.1223.4
19
Huyskens-Keil S, Eichholz Dündar I, Hassenberg K, Herppich WB (2020) Impact of light quality (white, red, blue light and UV-C irradiation) on changes in anthocyanin content and dynamics of pal and pod activities in apical and basal spear sections of white asparagus after harvest. Postharvest Biol Technol 161:111069. doi:10.1016/j.postharvbio.2019.111069 10.1016/j.postharvbio.2019.111069
20
Jiménez-Sánchez C, Lozano-Sánchez J, Rodríguez-Pérez C, Segura-Carretero A, Fernández-Gutiérrez A (2016) Comprehensive, untargeted, and qualitative RP-HPLC-ESI-QTOF/MS2 metabolite profiling of green asparagus (Asparagus officinalis). J Food Compos Anal 46:78-87. doi:10.1016/j.jfca.2015.11.004 10.1016/j.jfca.2015.11.004
21
Kim YS, Lee YM, Kim HJ, Kim JH, Jang DS, Kim JH, Kim JS (2010) Anti-obesity effect of morus bombycis root extract: Anti-lipase activity and lipolytic effect. J Ethnopharmacol 130:621-624. doi:10.1016/j.jep.2010.05.053 10.1016/j.jep.2010.05.05320669373
22
Ku YG, Bae JH, Namieśnik J, Barasch D, Nemirovski A, Katrich E, Gorinstein S (2018a) Detection of bioactive compounds in organically and conventionally grown asparagus spears. Food Anal Methods 11:309-318. doi:10.1007/s12161-017-1074-0 10.1007/s12161-017-1074-0
23
Ku YG, Kang DH, Lee CK, Lee SY, Ryu CS, Kim DE, Polovka M, Namieśnik J, Gorinstein S (2018b) Influence of different cultivation systems on bioactivity of asparagus. Food Chem 244:349-358. doi:10.1016/j.foodchem.2017.10.044 10.1016/j.foodchem.2017.10.04429120792
24
Laura A, Moreno Escamilla JO, Rodrigo García J, Alvarez Parrilla E (2019) Phenolic compounds. In: Postharvest physiology and biochemistry of fruits and vegetables. Agric Biol Sci Elsevier, pp 253-271. doi:10.1016/B978-0-12-813278-4.00012-9 10.1016/B978-0-12-813278-4.00012-9
25
Lee EJ, Yoo KS, Patil BS (2010) Development of a rapid HPLC‐UV method for simultaneous quantification of protodioscin and rutin in white and green asparagus spears. J Food Sci 75:C703-C709. doi:10.1111/j.1750-3841.2010.01824.x 10.1111/j.1750-3841.2010.01824.x
26
Lee JA, Cho YR, Hong SS, Ahn EK (2017) Anti‐obesity activity of saringosterol isolated from Sargassum muticum (Yendo) fensholt extract in 3T3‐L1 cells. Phytother Res 31:1694-1701. doi:10.1002/ptr.5892 10.1002/ptr.589228921681
27
Lee JW, Heo BG, Bae JH, Ku YG (2015) Comparison of plant growth, dormancy breaking, yield, and biological activities of extracts in four asparagus cultivars. Horti Sci Technol 33:796-804. doi:10.7235/HORT.2015.15080 10.7235/hort.2015.15080
28
Lee JW, Lee JH, Yu IH, Gorinstein S, Bae JH, Ku YG (2014) Bioactive compounds, antioxidant and binding activities and spear yield of Asparagus officinalis L. Plant Food Hum Nutr 69:175-181. doi:10.1007/s11130-014-0418-9 10.1007/s11130-014-0418-924793354
29
Marrelli M, Russo N, Chiocchio I, Statti G, Poli F, Conforti F (2020) Potential use in the treatment of inflammatory disorders and obesity of selected wild edible plants from Calabria region (Southern Italy). South Afr J Bot 128:304-311. doi:10.1016/j.sajb.2019.11.029 10.1016/j.sajb.2019.11.029
30
Motoki S, Kitazawa H, Maeda T, Suzuki T, Chiji H, Nishihara E, Shinohara Y (2012) Effects of various asparagus production methods on rutin and protodioscin contents in spears and cladophylls. Biosci Biotechnol Biochem 76:1047-1050. doi:10.1271/bbb.120143 10.1271/bbb.12014322738987
31
Motoki S, Matsunaga K, Maeda T, Kutsuzawa T (2005) Selection of asparagus cultivars for cold areas of Japan. Acta Hortic 776:357-366. doi:10.17660/ActaHortic.2008.776.47 10.17660/ActaHortic.2008.776.47
32
Muller AG, Sarker SD, Saleem IY, Hutcheon GA (2019) Delivery of natural phenolic compounds for the potential treatment of lung cancer. Daru 27:433-449. doi:10.1007/s40199-019-00267-2 10.1007/s40199-019-00267-231115871PMC6593021
33
Ntambi JM, Kim YC (2000) Adipocyte differentiation and gene expression. J Nutr 130:3122S-3126S. doi:10.1093/jn/130.12.3122S 10.1093/jn/130.12.3122S11110885
34
Papoulias E, Siomos AS, Koukounaras A, Gerasopoulos D, Kazakis E (2009) Effects of genetic, pre-and post-harvest factors on phenolic content and antioxidant capacity of white asparagus spears. Int J Mol Sci 10:5370-5380. doi:10.3390/ijms10125370 10.3390/ijms1012537020054475PMC2801999
35
Pegiou E, Mumm R, Acharya P, de Vos RCH, Hall RD (2019) Green and white asparagus (Asparagus officinalis): A source of developmental, chemical and urinary intrigue. Metabolites 10:17. doi:10.3390/metabo10010017 10.3390/metabo1001001731881716PMC7022954
36
Rodríguez-Pérez C, Segura-Carretero A, del Mar-Contreras M (2019) Phenolic compounds as natural and multifunctional anti-obesity agents: A review. Crit Rev Food Sci Nutr 59:1212-1229. doi:10.1080/10408398.2017.1399859 10.1080/10408398.2017.139985929156939
37
Romani A, Casciano F, Stevanin C, Maietti A, Tedeschi P, Secchiero P, Marchetti N, Voltan R (2021) Anticancer activity of aqueous extracts from Asparagus officinalis L. byproduct on breast cancer cells. Molecules 26:6369. doi:10.3390/molecules26216369 10.3390/molecules2621636934770777PMC8588164
38
Romanos-Nanclares A, Sánchez-Quesada C, Gardeazábal I, Martínez-González MÁ, Gea A, Toledo E (2020) Phenolic acid subclasses, individual compounds, and breast cancer risk in a mediterranean cohort: The SUN Project. J Acad Nutr Diet 120:1002-1015. e5. doi:10.1016/j.jand.2019.11.007 10.1016/j.jand.2019.11.00731982373
39
Selvakumar P, Badgeley A, Murphy P, Anwar H, Sharma U, Lawrence K, Lakshmikuttyamma A (2020) Flavonoids and other polyphenols act as epigenetic modifiers in breast cancer. Nutrients 12:761. doi:10.3390/nu12030761 10.3390/nu1203076132183060PMC7146477
40
Shawon RA, Ha SY, Lee TH, Cao TL, Kim HC, Bae JH, Ku YG (2021) Influence of shade treatment on plant growth characteristics and spear production in five asparagus (Asparagus officinalis L.) cultivars. Hortic Sci Technol 39:37-48. doi:10.7235/HORT.20210004 10.7235/HORT.20210004
41
Siomos AS (2018) The quality of asparagus as affected by preharvest factors. Sci Hortic 233:510-519. doi:10.1016/j.scienta.2017.12.031 10.1016/j.scienta.2017.12.031
42
Sladowski D, Steer SJ, Clothier RH, Balls M (1993) An improved mit assay. J Immunol Methods 157:203-207. doi:10.1016/0022-1759(93)90088-O 10.1016/0022-1759(93)90088-O8423364
43
Trigueros L, Peña S, Ugidos AV, Sayas-Barberá E, Pérez Álvarez JA, Sendra E (2013) Food ingredients as anti-obesity agents: A review. Crit Rev Food Sci Nutr 53:929-942. doi:10.1080/10408398.2011.574215 10.1080/10408398.2011.57421523768185
44
Wang M, Tadmor Y, Wu QL, Chin CK, Garrison SA, Simon JE (2003) Quantification of protodioscin and rutin in asparagus shoots by LC/MS and HPLC methods. J Agric Food Chem 51:6132-6136. doi:10.1021/jf0344587 10.1021/jf034458714518934
45
Zhu F, Du B, Xu B (2018) Anti-inflammatory effects of phytochemicals from fruits, vegetables, and food legumes: A review. Crit Rev Food Sci Nutr 58:1260-1270. doi:10.1080/10408398.2016.1251390 10.1080/10408398.2016.125139028605204
Information
  • Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
  • Publisher(Ko) :한국원예학회
  • Journal Title :Horticultural Science and Technology
  • Journal Title(Ko) :원예과학기술지
  • Volume : 41
  • No :5
  • Pages :497-507
  • Received Date : 2023-01-31
  • Revised Date : 2023-07-08
  • Accepted Date : 2023-07-10
  • DOI :https://doi.org/10.7235/HORT.20230043
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