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Phytochemical profile and angiotensin I converting enzyme (ACE) inhibitory activity of Limonium michelsonii Lincz

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Abstract

Members of the genus Limonium are widely used as medicinal herbs due to their health-promoting effects, such as an ability to improve blood circulation by inhibiting angiotensin I converting enzyme (ACE). While the potential of L. michelsonii Lincz. (a medicinal plant endemic to Kazakhstan) to inhibit ACE has been demonstrated, the inhibitory activities of its secondary metabolites have not been explored. In this work, the principal phenolic compounds (1–20) among these metabolites were isolated to determine the components responsible for ACE inhibition. The natural abundances of the active constituents within the target plant were characterized by UPLC-Q-TOF/MS analysis. All of the isolated compounds except for gallates 10–12 were found to significantly inhibit ACE, with IC50 values of between 7.1 and 138.4 μM. Unexpectedly, the flavonol glycosides 16–20 were observed to be more potent than the corresponding aglycones 4 and 5. For example, quercetin (4) had IC50 = 30.3 μM, whereas its glycosides (16, 17) had IC50 = 10.2 and 14.5 μM, respectively. A similar trend was observed for myricetin (5) and its glycosides (18–20). In a kinetic study, the flavonols 3–5 and 16–20 and the dihydroflavonols 8 and 9 behaved as competitive inhibitors, whereas other flavones (1, 2, 13–15) and flavanones (6, 7) performed noncompetitive inhibition.

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Abbreviations

ACE:

Angiotensin I converting enzyme

IC50 :

Inhibitor concentration that produces a 50% decrease in activity

K i :

Inhibition constant

V max :

Maximum velocity

K m :

Michaelis–Menten constant

References

  1. Baytenov MC (1963) Flora of Kazakhstan, part 7. Science Press, Almaty, p 75

  2. Compiling Groups of Countrywide Herbal Medicine of China (1996) Compilation of countrywide herbal medicine of China, part 1, 2nd edn. People’s Medical Publishing House, Beijing, pp 407–408

  3. Xu X, Bahargul K, Hang B, Jia XG (2009) Kazakh herbal medicine, part 1. The Ethnic Press, Beijing, pp 90–92

  4. Aniya Y, Miyagi C, Nakandakari A, Kamiya S, Imaizumi N, Ichiba T (2002) Free radical scavenging action of the medicinal herb Limonium wrightii from the Okinawa Islands. Phytomed 9:239–244

    Article  CAS  Google Scholar 

  5. Sihem B, Nicola M, Teresa M, Tiziana E, Rita PA, Noureddine B, Samir B, Massimiliano DA, Antonio V (2015) Phenolic compounds from Limonium pruinosum. Nat Pro Com 10:319–321

  6. Anastassiya VG, Amer HT, Galiya EZh, Nadezhda GG, Charles LC, Stephen JC, Samir AR (2015) Sulfated phenolic compounds from Limonium caspium: isolation, structural elucidation, and biological evaluation. Fitoterapia 104:80–85

    Article  Google Scholar 

  7. Tang XH, Yu F, Liu J, Gao J, Yan LF, Dong MM (2014) Isolation and identification of anti-tumor polysaccharide LSP21from Limonium sinense (Girard) Kuntze. Int J Biol Macromol 70:138–142

    Article  CAS  Google Scholar 

  8. Kazuyoshi K, Mami T, Kotaro M, Yoshishisa T (2005) A novel drime-type sesquiterpene from Limonium wrightii. J Nat Med 59(4):186–188

    Google Scholar 

  9. Faten M, Wided M, Vakhtang M, Andre P, Jean L, St-G Alexis, Riadh K (2014) Antiviral-guided fractionation and isolation of phenolic compounds from Limonium densiflorum hydroalcoholic extract. C R Chimie 19:726–732

    Google Scholar 

  10. Medini F, Fellah H, Ksouri R, Abdelly C (2014) Total phenolic, flavonoid and tannin contents and antioxidant and antimicrobial activities of organic extracts of shoots of the plant Limonium delicatulum. J Taibah Univ Sci 8(3):216–224

    Article  Google Scholar 

  11. Kandil FE, Ahmed KM, Hussieny HA, Soliman AM (2000) A new flavonoid from Limonium axillare. Arch Pharm J Pharmacol Med Chem 333:275–277

    Article  CAS  Google Scholar 

  12. Murray AP, Rodriguez S, Frontera MA, Tomas MA, Mulet MC (2004) Antioxidant metabolites from Limonium brasiliense (Boiss.) Kuntze. Z Naturforsch 59:477–480

    Article  CAS  Google Scholar 

  13. Yuh ChK, Lie ChL, Wei JT, Cheng JC, Szu HK, Yen HH (2002) Samarangenin B from Limonium sinense suppresses herpes simplex virus type 1 replication in vero cells by regulation of viral macromolecular synthesis. Antimicrob Agents Chemother 46(9):2854–2864

    Article  Google Scholar 

  14. Jallapally A, Addla D, Bagul P, Sridhar B, Banerjee SK, Kantevari S (2015) Design, synthesis and evaluation of novel 2-butyl-4-chloroimidazole derived peptidomimetics as angiotensin converting enzyme (ACE) inhibitors. Bioorg Med Chem 23:3526–3533

    Article  CAS  Google Scholar 

  15. Shukor NA, Camp JV, Gonzales GB, Staljanssens D, Struijs K, Zotti MJ, Raes K, Smagghe G (2013) Angiotensin-converting enzyme inhibitory effects by plant phenolic compounds: a study of structure activity relationships. J Agric Food Chem 61:11832–11839

    Article  Google Scholar 

  16. Felmeden DC, Lip GY (2000) The renin–angiotensin–aldosterone system and fibrinolysis. JRAAS 1(3):240–244

    Article  CAS  Google Scholar 

  17. Mitsuo M, Masayoshi H (2003) Antimutagenic activity of flavonoids from Chrysanthemum morifolium. Biosci Biotechnol Biochem 67:2091–2099

    Article  Google Scholar 

  18. Masuda T, Iritani K, Yonemori S, Oyama Y, Takeda Y (2001) Isolation and antioxidant activity of galloylflavonol glycosides from the seashore plant, Pemphis acidula. Biosc Biotechnol Biochem 65:1302–1309

    Article  CAS  Google Scholar 

  19. Movsumov IS (1996) Flavonoids of the roots of Limonium caspium. Chem Nat Compd 32(6):922

    Article  Google Scholar 

  20. Zhang XF, Hung TM, Phuong TP, Ngoc TM, Min BS, Song KS, Seong YH, Bae KH (2006) Anti-inflammatory activity of flavonoids from Populus davidiana. Arch Pharm Res 29(12):1102–1108

    Article  CAS  Google Scholar 

  21. Jeon SH, Chun W, Choi YJ, Kwon YS (2008) Cytotoxic constituents from the bark of Salix hulteni. Arch Pharm Res 31(8):978–982

    Article  CAS  Google Scholar 

  22. Trabelsi N, Oueslati S, Ksouri R, Nassra M, Marchal A, Krisa S, Abdelly C, Scharbert S, Holzmann N, Hofmann T (2004) Identification of the astringent taste compounds in black tea infusions by combining instrumental analysis and human bioresponse. J Agric Food Chem 52:3498–3508

    Article  Google Scholar 

  23. Guvenalp Z, Ozbek H, Kuruuzum-uz A, Kazaz C, Demirezer LO (2009) Secondary metabolites from Nepeta heliotropifolia. Turk J Chem 33:667–675

    CAS  Google Scholar 

  24. Lin YL, Wang ChN, Shiao YJ, Liu TY, Wang WY (2003) Benzolignanoid and polyphenols from Origanum vulgare. J Chin Chem Soc 50:1079–1083

    Article  CAS  Google Scholar 

  25. Hilbert G, Temsamani H, Bordenave L, Pedrot E, Chaher N, Cluzet S, Delaunay JC, Ollat N, Delrot S, Merillon JM, Gomes E, Richard T (2015) Flavonol profiles in berries of wild Vitis accessions using liquid chromatography coupled to mass spectrometry and nuclear magnetic resonance spectrometry. Food Chem 169:49–58

    Article  CAS  Google Scholar 

  26. Dawidar AM, Abdel-Mogib M, El-Nagga ME, Mostafa ME (2014) Isolation and characterization of Polygonum equisetiforme flavonoids and their acaricidal activity against Tetranychus urticae Koch. Res J Pharm Biol Chem Sci 5(4):140–148

    Google Scholar 

  27. Korul′kina LM, Shul′ts EE, Zhusupova GE, Abilov ZhA, Erzhanov KB, Chaudri MI (2014) Biologically active compounds from Limonium gmelinii and L. popovii. I. Chem Nat Compd 40(5):465–471

    Article  Google Scholar 

  28. Sentandreu MA, Toldrá FA (2006) A fluorescence-based protocol for quantifying angiotensin-converting enzyme activity. Nat Protoc 1(5):2423–2437

    Article  Google Scholar 

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Acknowledgements

This work was done with research funds from the Ministry of Agriculture, Food and Rural Affairs (No. 315032-04-2-SB010) and the Next-Generation BioGreen 21 program, Rural Development Administration (SSAC, No. PJ01107001), Republic of Korea. The BK21 PLUS program supported scholarships for senior researchers and all other students.

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Authors and Affiliations

  1. Division of Applied Life Science (BK21 Plus), IALS, Gyeongsang National University, Jinju, 52828, Republic of Korea

    Janar Jenis, Jeong Yoon Kim, Zia Uddin, Yeong Hun Song, Hyeong-Hwan Lee & Ki Hun Park

  2. Faculty of Chemistry and Chemical Technology, Al-Farabi Kazakh National University, Almaty, Republic of Kazakhstan

    Janar Jenis

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  1. Janar Jenis
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Correspondence to Ki Hun Park.

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Jenis, J., Kim, J.Y., Uddin, Z. et al. Phytochemical profile and angiotensin I converting enzyme (ACE) inhibitory activity of Limonium michelsonii Lincz. J Nat Med 71, 650–658 (2017). https://doi.org/10.1007/s11418-017-1095-4

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  • DOI: https://doi.org/10.1007/s11418-017-1095-4

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