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Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites

Yıl 2019, Cilt: 23 Sayı: 4, 740 - 748, 27.06.2025

Beril Kadıoğlu Yaman , Ozan Şen Aycan Salman Hande Sipahi , Norbert Kusz Judit Hohmann Hasan Kırmızıbekmez

Öz

Lycium barbarum possesses many bioactivities such as antidiabetic, antioxidant, antitumor, and immunomodulatory activities. In the present study, the MeOH extract (1 mg/mL) prepared from the leaves of L. barbarum cultivated in Turkey exerted significant anti-inflammatory activity via reducing the release of nitric oxide (NO) in LPSstimulated RAW 264.7 macrophages comparable to positive control indomethacin. Then, the extract was partitioned against CH2Cl2 and EtOAc to yield CH2Cl2, EtOAc and H2O subextracts which were also submitted to the same tests. Among the tested extracts, EtOAc (0.25 and 0.5 mg/mL), and CH2Cl2 (0.25 mg/mL) subextracts showed significant NO production inhibitory activities. The tested extracts also inhibited the production of PGE2 slightly. Successive chromatographic studies on the EtOAc subextract led to the isolation of three secondary metabolites, including chlorogenic acid, hesperidin and rutin as the potential bioactive compounds that are responsible for the in vitro antiinflammatory activity of the EtOAc subextract. The structures were elucidated based on 1D and 2D NMR spectra. Although chlorogenic acid and rutin were previously reported from leaves of L. barbarum, this is the first report of hesperidin from L. barbarum to the best of our knowledge.

Anahtar Kelimeler

Lycium barbarum anti-inflammatory activity NO inhibition flavonoid glycosides hesperidin

Kaynakça

  • [1] Davis PH. Flora of Turkey and the East Aegean Islands, sixth ed., Edinburgh University Press, Edinburgh, United Kingdom, 1979.
  • [2] Yao X, Peng Y, Xua LJ, Li L, Wu QL, Xiao PG. Phytochemical and biological studies of Lycium medicinal plants. Chem Biodivers. 2011; 8: 976-1010. [CrossRef]
  • [3] Amagase H, Farnsworth NR. A review of botanical characteristics, phytochemistry, clinical relevance in efficacy and safety of Lycium barbarum fruit (Goji). Food Res Int. 2011; 44(7): 1702-1717. [CrossRef]
  • [4] Cai H, Liu F, Zuo P, Huang G, Song Z, Wang T, Lu H, Guo F, Han C, Sun G. Practical application of antidiabetic efficacy of Lycium barbarum polysaccharide in patients with type 2 diabetes. Med Chem. 2015; 11: 383-390. [CrossRef]
  • [5] Amagase H, Sun B, Nance DM. Immunomodulatory effects of a standardized Lycium barbarum fruit juice in Chinese older healthy human subjects. J Med Food. 2009; 12(5): 1159-1165. [CrossRef]
  • [6] Amagase H, Sun B, Borek C. Lycium barbarum (goji) juice improves in vivo antioxidant biomarkers in serum of healthy adults. Nutr Res. 2009; 29(1): 19-25. [CrossRef]
  • [7] Mocan A, Vlase L, Vodnar DC, Bischin C, Hanganu D, Gheldiu AM, Oprean R, Silaghi-Dumitrescu R, Crișan G. Polyphenolic content, antioxidant and antimicrobial activities of Lycium barbarum L. and Lycium chinense Mill. leaves. Molecules. 2014; 19(7): 10056-10073. [CrossRef]
  • [8] Liu H, Fan Y, Wang W, Liu N, Zhang H, Zhu Z, Liu A. Polysaccharides from Lycium barbarum leaves: isolation, characterization and splenocyte proliferation activity. Int J Biol Macromol. 2012; 51(4): 417-22. [CrossRef]
  • [9] Dong JZ, Lu DY, Wang Y. Analysis of flavonoids from leaves of cultivated Lycium barbarum L. Plant Foods Hum Nutr. 2009; 64(3): 199-204. [CrossRef]
  • [10] Dong JZ, Gao WS, Lu DY, Wang Y. Simultaneous extraction and analysis of four polyphenols from leaves of Lycium barbarum L. J Food Biochem. 2011; 35(3): 914-931. [CrossRef]
  • [11] Wang Y, Wang Y, Zhao B, Ma HR, Aisa HA. Two new sesquiterpenoid glycosides from the leaves of Lycium barbarum. J Asian Nat Prod Res. 2016; 18(9): 871-877. [CrossRef]
  • [12] Kumar KP, Nicholls AJ, Wong CHY. Partners in crime: neutrophils and monocytes/macrophages in inflammation and disease. Cell Tissue Res. 2018; 371: 551–565. [CrossRef]
  • [13] Phan AT, Goldrath AW, Glass CK. Metabolic and epigenetic coordination of T cell and Macrophage immunity. Immunity. 2017; 46(5): 714–729. [CrossRef]
  • [14] Tsai HH, Lee WR, Wang PH, Cheng KT, Chen YC, Shen SC. Propionibacterium acnes-induced iNOS and COX-2 protein expression via ROS-dependent NF-kB and AP-1 activation in macrophages. J Dermatol Sci. 2013; 69(2): 122-131. [CrossRef]
  • [15] López-Martínez LM, Santacruz-Ortega H, Navarro RE, Sotelo-Mundo RR, González-Aguilar GA. A 1H NMR investigation of the interaction between phenolic acids found in mango (Mangifera indica cv Ataulfo) and papaya (Carica papaya cv Maradol) and 1,1-diphenyl-2-picrylhydrazyl (DPPH) Free Radicals. PLoS ONE. 2015; 10(11): 1-11. [CrossRef]
  • [16] Lahmer N, Belboukhari N, Cheriti A, Sekkoum K. Hesperidin and hesperitin preparation and purification from Citrus sinensis peels. Der Pharma Chemica. 2015; 7(2): 1-4.
  • [17] Fathiazad F, Delazar A, Amiri R, Sarker SD. Extraction of flavonoids and quantification of rutin from waste tobacco leaves. 2006; 5(3): 222-227.
  • [18] Medzhitov R. Inflammation 2010: New Adventures of an Old Flame. Cell. 2010; 140: 771-776. [CrossRef]
  • [19] Nathan C, Ding A. Nonresolving inflammation. Cell. 2010; 140: 871–882. [CrossRef]
  • [20] Handschin C, Spiegelman BM. The role of exercise and PGC1α in inflammation and chronic disease. Nature. 2008; 454(7203): 463–469. [CrossRef]
  • [21] Minihane AM, Vinoy S, Russell WR, et al. Low-grade inflammation, diet composition and health: Current research evidence and its translation. Br J Nutr. 2015; 114: 999-1012. [CrossRef]
  • [22] Bogdan C. Nitric oxide synthase in innate and adaptive immunity: An update. Trends Immunol. 2015; 36(3): 161-178. [CrossRef]
  • [23] Wang S, Suh JH, Hung WL, Zheng X, Wang Y, Ho CT. Use of UHPLC-TripleQ with synthetic standards to profile anti-inflammatory hydroxycinnamic acid amides in root barks and leaves of Lycium barbarum. J Food Drug Anal. 2018; 26: 572-582. [CrossRef]
  • [24] Lopatriello A, Previtera R, Pace S, et al. NMR-based identification of the major bioactive molecules from an Italian cultivar of Lycium barbarum. Phytochemistry. 2017; 144: 52-57. [CrossRef]
  • [25] Mocan A, Vlase L, Vodnar DC, et al. Polyphenolic content, antioxidant and antimicrobial activities of Lycium barbarum L. and Lycium chinense Mill. leaves. Molecules. 2014; 19: 10056-10073. [CrossRef]
  • [26] Mocan A, Vlase L, Vodnar DC, Gheldiu AM, Oprean R, Crișan G. Antioxidant, antimicrobial effects and phenolic profile of Lycium barbarum L. flowers. Molecules. 2015; 20: 15060-15071. [CrossRef]
  • [27] Kazłowska K, Hsu T, Hou CC, Yang WC, Tsai GJ. Anti-inflammatory properties of phenolic compounds and crude extract from Porphyra dentata. J Ethnopharmacol. 2010; 128: 123–130. [CrossRef]
  • [28] Guardia T, Rotelli AE, Juarez AO, Pelzer LE. Anti-inflammatory properties of plant flavonoids. Effects of rutin, quercetin and hesperidin on adjuvant arthritis in rat. Il Farmaco. 2001; 56: 683–687. [CrossRef]
  • [29] Liu CC, Zhang Y, Dai BL, et al. Chlorogenic acid prevents inflammatory responses in IL‑1β‑stimulated human SW‑1353 chondrocytes, a model for osteoarthritis. Mol Med Rep. 2017; 16: 1369-1375. [CrossRef]
  • [30] Parhiz H, Roohbakhsh A, Soltani F, Rezaee R, Iranshahi M. Antioxidant and anti-inflammatory properties of the citrus flavonoids hesperidin and hesperetin: An updated review of their molecular mechanisms and experimental models. Phytother Res. 2015; 29: 323–331. [CrossRef]

Yıl 2019, Cilt: 23 Sayı: 4, 740 - 748, 27.06.2025

Beril Kadıoğlu Yaman , Ozan Şen Aycan Salman Hande Sipahi , Norbert Kusz Judit Hohmann Hasan Kırmızıbekmez

Öz

Kaynakça

  • [1] Davis PH. Flora of Turkey and the East Aegean Islands, sixth ed., Edinburgh University Press, Edinburgh, United Kingdom, 1979.
  • [2] Yao X, Peng Y, Xua LJ, Li L, Wu QL, Xiao PG. Phytochemical and biological studies of Lycium medicinal plants. Chem Biodivers. 2011; 8: 976-1010. [CrossRef]
  • [3] Amagase H, Farnsworth NR. A review of botanical characteristics, phytochemistry, clinical relevance in efficacy and safety of Lycium barbarum fruit (Goji). Food Res Int. 2011; 44(7): 1702-1717. [CrossRef]
  • [4] Cai H, Liu F, Zuo P, Huang G, Song Z, Wang T, Lu H, Guo F, Han C, Sun G. Practical application of antidiabetic efficacy of Lycium barbarum polysaccharide in patients with type 2 diabetes. Med Chem. 2015; 11: 383-390. [CrossRef]
  • [5] Amagase H, Sun B, Nance DM. Immunomodulatory effects of a standardized Lycium barbarum fruit juice in Chinese older healthy human subjects. J Med Food. 2009; 12(5): 1159-1165. [CrossRef]
  • [6] Amagase H, Sun B, Borek C. Lycium barbarum (goji) juice improves in vivo antioxidant biomarkers in serum of healthy adults. Nutr Res. 2009; 29(1): 19-25. [CrossRef]
  • [7] Mocan A, Vlase L, Vodnar DC, Bischin C, Hanganu D, Gheldiu AM, Oprean R, Silaghi-Dumitrescu R, Crișan G. Polyphenolic content, antioxidant and antimicrobial activities of Lycium barbarum L. and Lycium chinense Mill. leaves. Molecules. 2014; 19(7): 10056-10073. [CrossRef]
  • [8] Liu H, Fan Y, Wang W, Liu N, Zhang H, Zhu Z, Liu A. Polysaccharides from Lycium barbarum leaves: isolation, characterization and splenocyte proliferation activity. Int J Biol Macromol. 2012; 51(4): 417-22. [CrossRef]
  • [9] Dong JZ, Lu DY, Wang Y. Analysis of flavonoids from leaves of cultivated Lycium barbarum L. Plant Foods Hum Nutr. 2009; 64(3): 199-204. [CrossRef]
  • [10] Dong JZ, Gao WS, Lu DY, Wang Y. Simultaneous extraction and analysis of four polyphenols from leaves of Lycium barbarum L. J Food Biochem. 2011; 35(3): 914-931. [CrossRef]
  • [11] Wang Y, Wang Y, Zhao B, Ma HR, Aisa HA. Two new sesquiterpenoid glycosides from the leaves of Lycium barbarum. J Asian Nat Prod Res. 2016; 18(9): 871-877. [CrossRef]
  • [12] Kumar KP, Nicholls AJ, Wong CHY. Partners in crime: neutrophils and monocytes/macrophages in inflammation and disease. Cell Tissue Res. 2018; 371: 551–565. [CrossRef]
  • [13] Phan AT, Goldrath AW, Glass CK. Metabolic and epigenetic coordination of T cell and Macrophage immunity. Immunity. 2017; 46(5): 714–729. [CrossRef]
  • [14] Tsai HH, Lee WR, Wang PH, Cheng KT, Chen YC, Shen SC. Propionibacterium acnes-induced iNOS and COX-2 protein expression via ROS-dependent NF-kB and AP-1 activation in macrophages. J Dermatol Sci. 2013; 69(2): 122-131. [CrossRef]
  • [15] López-Martínez LM, Santacruz-Ortega H, Navarro RE, Sotelo-Mundo RR, González-Aguilar GA. A 1H NMR investigation of the interaction between phenolic acids found in mango (Mangifera indica cv Ataulfo) and papaya (Carica papaya cv Maradol) and 1,1-diphenyl-2-picrylhydrazyl (DPPH) Free Radicals. PLoS ONE. 2015; 10(11): 1-11. [CrossRef]
  • [16] Lahmer N, Belboukhari N, Cheriti A, Sekkoum K. Hesperidin and hesperitin preparation and purification from Citrus sinensis peels. Der Pharma Chemica. 2015; 7(2): 1-4.
  • [17] Fathiazad F, Delazar A, Amiri R, Sarker SD. Extraction of flavonoids and quantification of rutin from waste tobacco leaves. 2006; 5(3): 222-227.
  • [18] Medzhitov R. Inflammation 2010: New Adventures of an Old Flame. Cell. 2010; 140: 771-776. [CrossRef]
  • [19] Nathan C, Ding A. Nonresolving inflammation. Cell. 2010; 140: 871–882. [CrossRef]
  • [20] Handschin C, Spiegelman BM. The role of exercise and PGC1α in inflammation and chronic disease. Nature. 2008; 454(7203): 463–469. [CrossRef]
  • [21] Minihane AM, Vinoy S, Russell WR, et al. Low-grade inflammation, diet composition and health: Current research evidence and its translation. Br J Nutr. 2015; 114: 999-1012. [CrossRef]
  • [22] Bogdan C. Nitric oxide synthase in innate and adaptive immunity: An update. Trends Immunol. 2015; 36(3): 161-178. [CrossRef]
  • [23] Wang S, Suh JH, Hung WL, Zheng X, Wang Y, Ho CT. Use of UHPLC-TripleQ with synthetic standards to profile anti-inflammatory hydroxycinnamic acid amides in root barks and leaves of Lycium barbarum. J Food Drug Anal. 2018; 26: 572-582. [CrossRef]
  • [24] Lopatriello A, Previtera R, Pace S, et al. NMR-based identification of the major bioactive molecules from an Italian cultivar of Lycium barbarum. Phytochemistry. 2017; 144: 52-57. [CrossRef]
  • [25] Mocan A, Vlase L, Vodnar DC, et al. Polyphenolic content, antioxidant and antimicrobial activities of Lycium barbarum L. and Lycium chinense Mill. leaves. Molecules. 2014; 19: 10056-10073. [CrossRef]
  • [26] Mocan A, Vlase L, Vodnar DC, Gheldiu AM, Oprean R, Crișan G. Antioxidant, antimicrobial effects and phenolic profile of Lycium barbarum L. flowers. Molecules. 2015; 20: 15060-15071. [CrossRef]
  • [27] Kazłowska K, Hsu T, Hou CC, Yang WC, Tsai GJ. Anti-inflammatory properties of phenolic compounds and crude extract from Porphyra dentata. J Ethnopharmacol. 2010; 128: 123–130. [CrossRef]
  • [28] Guardia T, Rotelli AE, Juarez AO, Pelzer LE. Anti-inflammatory properties of plant flavonoids. Effects of rutin, quercetin and hesperidin on adjuvant arthritis in rat. Il Farmaco. 2001; 56: 683–687. [CrossRef]
  • [29] Liu CC, Zhang Y, Dai BL, et al. Chlorogenic acid prevents inflammatory responses in IL‑1β‑stimulated human SW‑1353 chondrocytes, a model for osteoarthritis. Mol Med Rep. 2017; 16: 1369-1375. [CrossRef]
  • [30] Parhiz H, Roohbakhsh A, Soltani F, Rezaee R, Iranshahi M. Antioxidant and anti-inflammatory properties of the citrus flavonoids hesperidin and hesperetin: An updated review of their molecular mechanisms and experimental models. Phytother Res. 2015; 29: 323–331. [CrossRef]
Toplam 30 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Farmakognozi, Farmasotik Toksikoloji, Temel Farmakoloji
Bölüm Articles
Yazarlar

Beril Kadıoğlu Yaman

Ozan Şen

Aycan Salman

Hande Sipahi

Norbert Kusz

Judit Hohmann

Hasan Kırmızıbekmez

Yayımlanma Tarihi 27 Haziran 2025
Yayımlandığı Sayı Yıl 2019 Cilt: 23 Sayı: 4

Kaynak Göster

APA Kadıoğlu Yaman, B., Şen, O., Salman, A., Sipahi, H., vd. (2025). Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites. Journal of Research in Pharmacy, 23(4), 740-748.
AMA Kadıoğlu Yaman B, Şen O, Salman A, Sipahi H, Kusz N, Hohmann J, Kırmızıbekmez H. Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites. J. Res. Pharm. Haziran 2025;23(4):740-748.
Chicago Kadıoğlu Yaman, Beril, Ozan Şen, Aycan Salman, Hande Sipahi, Norbert Kusz, Judit Hohmann, ve Hasan Kırmızıbekmez. “Anti-Inflammatory Effects of Lycium Barbarum Leaf Extracts in Lipopolysaccharide-Induced RAW 264.7 Macrophage Cells and Isolation of Secondary Metabolites”. Journal of Research in Pharmacy 23, sy. 4 (Haziran 2025): 740-48.
EndNote Kadıoğlu Yaman B, Şen O, Salman A, Sipahi H, Kusz N, Hohmann J, Kırmızıbekmez H (01 Haziran 2025) Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites. Journal of Research in Pharmacy 23 4 740–748.
IEEE B. Kadıoğlu Yaman, O. Şen, A. Salman, H. Sipahi, N. Kusz, J. Hohmann, ve H. Kırmızıbekmez, “Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites”, J. Res. Pharm., c. 23, sy. 4, ss. 740–748, 2025.
ISNAD Kadıoğlu Yaman, Beril vd. “Anti-Inflammatory Effects of Lycium Barbarum Leaf Extracts in Lipopolysaccharide-Induced RAW 264.7 Macrophage Cells and Isolation of Secondary Metabolites”. Journal of Research in Pharmacy 23/4 (Haziran 2025), 740-748.
JAMA Kadıoğlu Yaman B, Şen O, Salman A, Sipahi H, Kusz N, Hohmann J, Kırmızıbekmez H. Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites. J. Res. Pharm. 2025;23:740–748.
MLA Kadıoğlu Yaman, Beril vd. “Anti-Inflammatory Effects of Lycium Barbarum Leaf Extracts in Lipopolysaccharide-Induced RAW 264.7 Macrophage Cells and Isolation of Secondary Metabolites”. Journal of Research in Pharmacy, c. 23, sy. 4, 2025, ss. 740-8.
Vancouver Kadıoğlu Yaman B, Şen O, Salman A, Sipahi H, Kusz N, Hohmann J, Kırmızıbekmez H. Anti-inflammatory effects of Lycium barbarum leaf extracts in lipopolysaccharide-induced RAW 264.7 macrophage cells and isolation of secondary metabolites. J. Res. Pharm. 2025;23(4):740-8.