Advertisement

Tupistra nutans Wall. root extract, rich in phenolics, inhibits microbial growth and α-glucosidase activity, while demonstrating strong antioxidant potential

  • Ill-Min Chung
  • Ramachandran Chelliah
  • Deog-Hwan Oh
  • Seung-Hyun Kim
  • Chang Yeon Yu
  • Bimal Kumar GhimireEmail author
Original Article
  • 13 Downloads

Abstract

The current study was performed to determine the phenolic compounds composition, antioxidant and antimicrobial activity, and α-glucosidase inhibitory effect of the root extract of Tupistra nutans Wall., in order to validate its use in traditional medicine. HPLC–MS/MS analysis showed the presence of ferulic acid, protocatechuic acid, p-hydroxybenzoic acid, p-coumaric acid, salicylic acid, chlorogenic acid, caffeic acid, l-phenylalanine as the predominant phenolic compounds. The antioxidant potentials of T. nutans were determined in different solvent extract and found to vary in a concentration-dependent manner. Ethyl acetate-soluble fraction exhibited the highest amount of phenolic acids, flavonoids, antioxidant activity against the DPPH, reduced Fe3+/ferric cyanide complexes to the ferrous form and inhibitory effect on α-glucosidase. Butanol fraction showed the strongest ABTS radical scavenging ability. Methanolic root extract showed higher reduction capability of ferric ions than the other solvent fractions. A significant and higher positive correlation was found between total phenolic content and total flavonoid content with α-glucosidase inhibition and DPPH using ethyl acetate solvent than the other solvent fractions. All the tested microorganisms: Staphylococcus aureus Rosenback (ATCC13150), Salmonella enterica typhimurium Kauffmann and Edwads (ATCC14028), Escherichia coli Castllani and Chalmers (ATCC35150), and fungi: Candida albicans Robin and Berkhout (KTCC7965), Aspergillus fumigatus Fresenius (KTCC6145), A. flavus var. flavus Link ex Fries (KTCC6143), A. niger van Tieghem (KTCC6317) were susceptible to the root extracts at a concentration of 0.12–0.25 mg mL−1. This study may allow us to understand indigenous medicinal values of T. nutans. Furthermore, these results showed that T. nutans is a good source of antioxidants along with antimicrobial and antidiabetic activities and could be used as an important bioresource for the pharmaceutical and food industries.

Keywords

Diabetes mellitus Flavonoids Microbial growth Nakima Phenolics Phytochemicals Tupistra nutans 

Notes

Acknowledgements

This study was supported by the KU Research Professor program.

Author contributions

BKG performed designing of experiment and writing of manuscript. CYY supervised the experiment. RC and D-HO performed the antimicrobial activities. S-HK and I-MC performed the phytochemical determination, analysis and editing of manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ademiluyi AO, Oboh G (2013) Soybean phenolic-rich extracts inhibit key-enzymes linked to type 2 diabetes (α-amylase and α-glucosidase) and hypertension (angiotensin I converting enzyme) in vitro. Exp Toxicol Pathol 65:305–309CrossRefGoogle Scholar
  2. Amalan V, Vijayakumar N (2015) Antihyperglycemic effect of p-coumaric acid on streptozotocin induced diabetic rats. Indian J Appl Res 5:10–13Google Scholar
  3. Andrade-Cetto A, Becerra-Jimenez J, Cardenas-Vazquez R (2008) α-glucosidase inhibiting activity of some Mexican plants used in the treatment of type 2 diabetes. J Ethnopharmacol 116:27–32CrossRefGoogle Scholar
  4. Arulmozhi P, Vijayakumar S, Kumar T (2018) Phytochemical analysis and antimicrobial activity of some medicinal plants against selected pathogenic microorganisms. Microb Pathog 123:219–226CrossRefGoogle Scholar
  5. Asayama K (1990) Free radicals and diabetes mellitus. Mod Med 45:1736–1742Google Scholar
  6. Barros L, Ferreira MJ, Queiros B, Ferreira IC, Bapista P (2007) Total phenols, ascorbic acid, β-carotene and lycopene in Portuguese wild edible mushrooms and their antioxidant activities. Food Chem 103:413–419CrossRefGoogle Scholar
  7. Benzie IFF, Strain JJ (1996) Ferric reducing ability of plasma (FRAP) a measure of antioxidant power: the FRAP assay. Anal Biochem 239:70–76CrossRefGoogle Scholar
  8. Brul S, Klis FM (1999) Mechanistic and mathematical inactivation studies of food spoilage fungi. Fungal Genet Biol 27:199–208CrossRefGoogle Scholar
  9. Brumfitt W, Hamilton-Miller JMT, Franklin I (1990) Antibiotic activity of natural products. I. Propolis. Microbios 62:19–22Google Scholar
  10. Campos FM, Coouto JA, Figueiredo AR, Toth IV, Rangel AOSS, Hogg TA (2009) Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol 135:144–151CrossRefGoogle Scholar
  11. Chaichana N (2018) Nutritional composition, antioxidant activity and phytochemical composition of Tupistra albiflora K. Larsen’s flowers. Walailak J Sci Technol 15:305–311Google Scholar
  12. Chakrabarti R, Rajagopalan R (2002) Diabetes and insulin resistance associated disorders: disease and the therapy. Curr Sci 83:1533–1538Google Scholar
  13. Chandra H, Bishnoi P, Yadav A, Patni B, Mishra AP, Nautiyal AR (2017) Antimicrobial resistance and the alternative resources with special emphasis on plant-based antimicrobials: a review. Plants 6:16CrossRefGoogle Scholar
  14. Charpentier G, Riveline JP, Varroud-Vial M (2002) Management of drugs affecting blood glucose in diabetic patients with renal failure. Diabetes Metab 26:73–85Google Scholar
  15. Chettri DR, Parajuli P, Subba GC (2005) Antidiabetic plants used by Sikkim and Darjeeling Himalayan tribes, India. J Ethnopharmacol 99:199–202CrossRefGoogle Scholar
  16. Coniff R, Krol A (1997) A review of US clinical experience. Clin Ther 19:16–26CrossRefGoogle Scholar
  17. de Brum TF, Camponogara C, Jesus RDS, Belke BV, Piana M, Boligon AA, Pires FB, Oliveira SM, da Rosa MB, de Freitas BL (2016) Ethnopharmacological study and topical anti-inflammatory activity of crude extract from Poikilacanthus glandulosus (Nees) Ariza leaves. J Ethnopharmacol 193:60–67CrossRefGoogle Scholar
  18. Decker EA, Welch B (1990) Role of ferritin as a lipid oxidation catalyst in muscle food. J Agric Food Chem 38:674–677CrossRefGoogle Scholar
  19. Dewanto X, Wu K, Adom K, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014CrossRefGoogle Scholar
  20. Edward-Jones V (2013) Alternative antimicrobial approaches to fighting multidrug resistant infections. In: Rai M, Kon K (eds) Fighting multidrug resistance with herbal extracts, essential oils and their components, vol 1. Academic Press, Amsterdam, pp 1–8Google Scholar
  21. Ghimire BK, Yu CY, Chung IM (2017) Assessment of the phenolic profile, antimicrobial activity and oxidative stability of transgenic Perilla frutescens L. overexpressing tocopherol methyltransferase (g-tmt) gene. Plant Physiol Biochem 118:77–87CrossRefGoogle Scholar
  22. Hendra R, Ahmad S, Sukari A, Yunus Shukor M, Oskoueian E (2011) Flavonoid analyses and antimicrobial activity of various parts of Phaleria macrocarpa (Scheff.) Boerl Fruit. Int J Mol Sci 12:3422–3431CrossRefGoogle Scholar
  23. Hussain S, Hore DK (2007) Collection and conservation of major medicinal plants of Darjeeling and Sikkim Himalayas. Indian J Tradit Knowl 6:352–357Google Scholar
  24. Inzucchi SE (2002) Oral antihyperglycemic therapy for type 2 diabetes: scientific review. JAMA 287:360–372CrossRefGoogle Scholar
  25. Ji HF, Li XJ, Zhang HY (2009) Natural products and drug discovery. EMBO Rep 10:194–200CrossRefGoogle Scholar
  26. Kala CP (2005) Current status of medicinal plants used by traditional Vaidyas in Uttaranchal state of India. Ethnobot Res Appl 3:267–278CrossRefGoogle Scholar
  27. Khanna VG, Kannabiran K (2008) Antimicrobial activity of saponin fractions of the leaves of Gymnema sylvestre and Eclipta prostrata. World J Microbiol Biotechnol 24:2737–2740CrossRefGoogle Scholar
  28. Khatoon U, Sharma L, Manivannan S, Muddarsu V (2018) Proximate analysis, elemental profiling and antioxidant activities of Tupistra nutans wall grown in Sikkim Hills, India. J Pharmacogn Phytochem 7:3630–3633Google Scholar
  29. Kim YM, Jeong YK, Wang MH, Lee WY, Rhee H (2005) Inhibitory effect of pine extract on α-glucosidase activity and postprandial hyperglycemia. Nutrition 2:756–761CrossRefGoogle Scholar
  30. Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrović P, Niksic M, Vrvic MM, van Griensven L (2015) Antioxidants of edible mushrooms. Molecules 20:19489–19525CrossRefGoogle Scholar
  31. Kozyra M, Komsta L, Wojtanowski K (2019) Analysis of phenolic compounds and antioxidant activity of methanolic extracts from inflorescences of Carduus sp. Phytochem Lett 31:256–262CrossRefGoogle Scholar
  32. Kumarappan CT, Mandal SC (2008) Polyphenolic extract of Ichnocarpus frutescens attenuates diabetic complications in streptozotocin-treated diabetic rats. Ren Fail 30:307–322CrossRefGoogle Scholar
  33. Li HB, Wong CC, Cheng KW, Chen F (2008) Antioxidant properties in vitro and total phenolic contents in methanol extracts from medicinal plants. LWT Food Sci Technol 41:385–390CrossRefGoogle Scholar
  34. Li X, Wang X, Chen D, Chen S (2011) Antioxidant activity and mechanism of protocatechuic acid in vitro. FFHD 7:232–244Google Scholar
  35. Liu X, Dong M, Chen X, Jiang M, Lv X, Yan G (2007) Antioxidant activity and phenolics of an endophytic Xylaria sp. from Gingko biloba. Food Chem 105:548–554CrossRefGoogle Scholar
  36. Liu CX, Guo ZY, Xue YH, Cheng J, Huang NY, Zhou Y, Cheng F, Zou K (2012) Five new furostanol saponins from the rhizomes of Tupistra chinensis. Fitoterapia 83:323–328CrossRefGoogle Scholar
  37. Lou Z, Wang H, Zhu S, Ma C, Wang Z (2011) Antibacterial activity and mechanism of action of chlorogenic acid. J Food Sci 76:M398–M403CrossRefGoogle Scholar
  38. Martins N, Barros L, Henriques M, Silva S, Ferreira ICFR (2015) Activity of phenolic compounds from plant origin against Candida species. Ind Crop Prod 74:648–670CrossRefGoogle Scholar
  39. Masek A, Chrzescijanska E, Latos M (2016) Determination of antioxidant activity of caffeic acid and p-coumaric acid by using electrochemical and spectrophotometric assays. Int J Electrochem Sci 11:10644–10658CrossRefGoogle Scholar
  40. Moreno MIN, Isla MI, Sampietro AR, Vattuone MA (2000) Comparison of the free radical-scavenging activity of propolis from several regions of Argentina. J Ethnopharmacol 7:109–114CrossRefGoogle Scholar
  41. Narasimhan A, Chinnaiyan M, Karundevi B (2015) Ferulic acid exerts its antidiabetic effect by modulating insulin-signalling molecules in the liver of high-fat diet and fructose-induced type-2 diabetic adult male rat. Appl Physiol Nutr Metab 40:769–781CrossRefGoogle Scholar
  42. Negi PS, Jayaprakash GK, Jena BS (2003) Antioxidant and antimutagenic activities of pomegranate peel extracts. Food Chem 80:393–397CrossRefGoogle Scholar
  43. Oboh G, Agunloye OM, Adefegha SA, Akinyemi AJ, Ademiluyi AO (2015) Caffeic and chlorogenic acids inhibit key enzymes linked to type-2 diabetes (in vitro): a comparative study. J Basic Clin Physiol Pharmacol 26:165–170CrossRefGoogle Scholar
  44. Ota A, Abramovic H, Abram V, Poklar UN (2011) Interactions of p-coumaric, caffeic and ferulic acids and their styrenes with model lipid membranes. Food Chem 125:1256–1261CrossRefGoogle Scholar
  45. Oyaizu M (1986) Studies on products of browning reactions: antioxidative activities of products of browning reaction prepared from glucosamine. Jpn J Nutr Diet 44:307–315CrossRefGoogle Scholar
  46. Pan WB, Wei LM, Wei LL, Wu YC (2006) Chemical constituents of Tupistra chinensis rhizomes. Chem Pharm Bull 54:954–958CrossRefGoogle Scholar
  47. Pan ZH, Li Y, Liu JL, Ning DS, Li DP, Wu XD, Wen YX (2012) A cytotoxic cardenolide and a saponin from the rhizomes of Tupistra chinensis. Fitoterapia 83:1489–1493CrossRefGoogle Scholar
  48. Paphitou NI (2013) Antimicrobial resistance: action to combat the rising microbial challenges. Int J Antimicrob Agent 42:S25–S28CrossRefGoogle Scholar
  49. Pereira FD, Cazarolli LH, Lavado C, Mengatto V, Figueiredo MS, Guedes A, Pizzolatti MG, Silva FR (2011) Effects of flavonoids on α-glucosidase activity: potential targets for glucose homeostasis. Nutrition 27:1161–1167CrossRefGoogle Scholar
  50. Rios JL, Recio MC (2005) Medicinal plants and antimicrobial activity. J Ethnopharmacol 4:80–100CrossRefGoogle Scholar
  51. Rizvi SI, Zaid MA, Anis R, Mishra N (2005) Protective role of tea catechins against oxidation-induced damage of type 2 diabetic erythrocytes. Clin Exp Pharmacol Physiol 32:70–75CrossRefGoogle Scholar
  52. Rubilar M, Jara C, Poo Y, Acevedo F, Gutierrez C, Sineiro J, Shene C (2011) Extracts of Maqui (Aristotelia chilensis) and Murta (Ugni molinae Turcz.): sources of antioxidant compounds and α-glucosidase/α-amylase inhibitors. J Agric Food Chem 59:1630–1637CrossRefGoogle Scholar
  53. Safer AM, Al-Nughamish AJ (1999) Hepatotoxicity induced by the antioxidant food additive butylated hydroxytoluene (BHT) in rats: an electron microscopical study. Histol Histopathol 14:391–406Google Scholar
  54. Semaming Y, Kukongviriyapan U, Kongyingyoes B, Thukhammee W, Pannangpetch P (2015) Protocatechuic acid restores vascular responses in rats with chronic diabetes induced by streptozotocin. Phytother Res 30:227–233CrossRefGoogle Scholar
  55. Sineiro J, Domínguez H, Nunez MJ, Lema JM (1996) Ethanol extraction of polyphenols in an immersion extractor. Effect of pulsing flow. J Am Oil Chem Soc 73:1121–1125CrossRefGoogle Scholar
  56. Singh R, Parihar P, Singh S, Mishra RK, Singh VP, Prasad SM (2017) Reactive oxygen species signaling and stomatal movement: current updates and future perspectives. Redox Biol 11:213–218CrossRefGoogle Scholar
  57. Singleton VL, Rossi JA Jr (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  58. Song X, Li Y, Zhang D, Jiang Y, Wang W, Song B, Tang Z, Cui J, Yue Z (2015) Two new spirostanol saponins from the roots and rhizomes of Tupistra chinensis. Phytochem Lett 13:6–10CrossRefGoogle Scholar
  59. SPSS (2011) IBM SPSS statistics base 20. SPSS Inc., ChicagoGoogle Scholar
  60. Thaipong K, Boonprakob U, Crosby K, Cisneros-Zevallos L, Hawkins Byrne D (2006) Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J Food Compos Anal 19:669–675CrossRefGoogle Scholar
  61. Verma S, Nath LK (2016) Analytical standards for the flowers of Tupistra Nutans Wall. a rare medicinal plant of Sikkim Himalayan Region. Pharm Lett 8:48–56Google Scholar
  62. Vilioglu YS, Mazza G, Gao L, Oomah BD (1998) Antioxidant activity and total phenolics in selected fruits, vegetables and grain products. J Agric Food Chem 46:4113–4117CrossRefGoogle Scholar
  63. Wongsa P, Chaiwarit J, Zamaludien A (2012) In vitro screening of phenolic compounds, potential inhibition against α-amylase and α-glucosidase of culinary herbs in Thailand. Food Chem 131:964–971CrossRefGoogle Scholar
  64. Xiang J, Apea-Bah F, Ndolo VU, Katundu MC, Beta T (2019) Profile of phenolic compounds and antioxidant activity of finger millet varieties. Food Chem 275:361–368CrossRefGoogle Scholar
  65. Xing Q, Kadota S, Tadata T, Namba T (1996) Antioxidant effect of phenylethanoids from Cistanche deserticola. Biol Pharm Bull 19:1580–1585CrossRefGoogle Scholar
  66. Yang QX, Zhang YJ, Li HZ, Yang CR (2005) Polyhydroxylated steroidal constituents from the fresh rhizomes of Tupistra yunnanensis. Steroids 70:732–737CrossRefGoogle Scholar
  67. Yonzone R, Rai S, Bhujel RB (2011) Genetic diversity of ethnobotanical and medicinal plants resources of Darjeeling district, West Engal, India. Int J Adv Pharm Res 3:713–729Google Scholar
  68. Zahin M, Aqil F, Ahmad I (2010) Broad spectrum antimutagenic activity of antioxidant active fraction of Punica granatum L. peel extract. Mutat Res 703:99–107CrossRefGoogle Scholar

Copyright information

© Botanical Society of Sao Paulo 2019

Authors and Affiliations

  • Ill-Min Chung
    • 1
  • Ramachandran Chelliah
    • 3
  • Deog-Hwan Oh
    • 3
  • Seung-Hyun Kim
    • 1
  • Chang Yeon Yu
    • 2
  • Bimal Kumar Ghimire
    • 1
    Email author
  1. 1.Department of Applied Life ScienceKonkuk UniversitySeoulSouth Korea
  2. 2.Bioherb Research InstituteKangwon National UniversityChuncheonSouth Korea
  3. 3.Department of Food Science and Biotechnology, College of Agriculture and Life SciencesKangwon National UniversityChuncheonSouth Korea

Personalised recommendations