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Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye)

Yıl 2024, Cilt: 28 Sayı: 4, 1166 - 1173, 28.06.2025

Öz

In this study, we investigated the anti-microbial and anti-inflammatory activities of the cosmopolite macrolichens Usnea articulata (L.) Hoffm., Umbilicaria crustulosa (Ach.) Lamy and Bryoria fuscescens (Gyeln.) Brodo & D.Hawksw hydroalcoholic extracts to contribute the potential pharmacological uses of lichens. In vitro antimicrobial activities of ethanol extracts against Gram-negative bacteria Escherichia coli, Gram-positive bacteria Staphylococcus aureus, and the yeast Candida albicans were presented using the Broth microdilution method. The most effective lichen extract against gram-positive bacteria S. aureus was U. articulata ethanol extract with a MIC value of 0.125 mg/ml. U. articulata and B. fuscences extracts have similar anti-fungal activities despite having MIC values of 0.5 mg/ml. The anti- inflammatory effects of the extracts on Lipopolysaccharide/Interferon-gamma (LPS/IF-γ) induced macrophage-like cellular systems (BV-2 microglia and RAW 264,7 macrophages) were evaluated by measuring P38 mitogen-activated protein kinase phosphorylation (P38MAPK), cyclooxygenase 2 (COX-2) and inducible nitric oxide synthase 2 (NOS2) mRNA and protein expression. Especially, Usnea and Umbilicaria extracts also attenuated the LPS/IF-γ induced increase in P38MAPK phosphorylation, COX-2, and NOS2 expression in both macrophage-like cells without any cytotoxicity. According to the results of our study, we suggest that the anti-inflammatory mechanism of lichen extracts might result from the inhibition of P38MAPK phosphorylation through a reduction in COX-2 and NOS2 expressions.

Kaynakça

  • [1] Zambare VP, Christopher LP. Biopharmaceutical potential of lichens. Pharm Biol. 2012; 50(6): 778-798. https://doi.org/10.3109/13880209.2011.633089
  • [2] Adenubi OT, Famuyide IM, McGaw LJ, Eloff JN. Lichens: An update on their ethnopharmacological uses and potential as sources of drug leads. J Ethnopharmacol. 2022; 298: 115657. https://doi.org/10.1016/j.jep.2022.115657
  • [3] Micheletti AC, Honda NK, Ravaglia LM, Matayoshi T, Spielmann AA. Antibacterial potencial of 12 Lichen species. An Acad Bras Cienc. 2021; 93(4): S0001-37652021000700904. https://doi.org/10.1590/0001-3765202120191194
  • [4] Wethalawe AN, Alwis YV, Udukala DN, Paranagama PA. Antimicrobial compounds ısolated from Endolichenic Fungi: A Review. Molecules. 2021; 26(13): 3901. https://doi.org/10.3390/molecules26133901
  • [5] Garcia Rowe J, Garcia Gimenez MD, Saenz Rodriguez MT. Some lichen products have antimicrobial activity. Z Naturforsch C J Biosci. 1999; 54(7-8): 605-9. https://doi.org/10.1515/znc-1999-7-824
  • [6] Zindel J, Kubes P. DAMPs, PAMPs, and LAMPs in ımmunity and sterile ınflammation. Annu Rev Pathol. 2020; 15: 493-518. https://doi.org/10.1146/annurev-pathmechdis-012419-032847
  • [7] Amarante-Mendes GP, Adjemian S, Branco LM, Zanetti LC, Weinlich R, Bortoluci KR. Pattern recognition receptors and the host cell death molecular machinery. Front Immunol. 2018; 9: 2379. https://doi.org/10.3389/fimmu.2018.02379
  • [8] Li X, Jiang S, Tapping RI. Toll-like receptor signaling in cell proliferation and survival. Cytokine. 2010; 49(1): 1-9. https://doi.org/10.1016/j.cyto.2009.08.010
  • [9] Chaiwut R, Kasinrerk W. Very low concentration of lipopolysaccharide can induce the production of various cytokines and chemokines in human primary monocytes. BMC Res Notes. 2022; 15(1): 42. https://doi.org/10.1186/s13104-022-05941-4
  • [10] Salvemini D, Kim SF, Mollace V. Reciprocal regulation of the nitric oxide and cyclooxygenase pathway in pathophysiology: relevance and clinical implications. Am J Physiol Regul Integr Comp Physiol. 2013; 304(7): R473-487. https://doi.org/10.1152/ajpregu.00355.2012
  • [11] Hong JM, Kim JE, Min SK, Kim KH, Han SJ, Yim JH, Park H, Kim JH, Kim IC. Anti-ınflammatory effects of antarctic lichen Umbilicaria antarctica methanol extract in lipopolysaccharide-stimulated RAW 264.7 macrophage cells and zebrafish model. Biomed Res Int. 2021; 2021: 8812090. https://doi.org/10.1155/2021/8812090.
  • [12] Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005; 15(1): 11-18. https://doi.org/10.1038/sj.cr.7290257
  • [13] Ratajczak-Wrona W, Jablonska E, Marcinczyk M, Grabowska Z, Piotrowski L. Role of p38 MAPK pathway in induction of iNOS expression in neutrophils and peripheral blood mononuclear cells in patients with squamous cell carcinoma of the oral cavity. J Oral Maxillofac Surg. 2009; 67(11): 2354-2363. https://doi.org/10.1016/j.joms.2009.04.030
  • [14] Bhat NR, Feinstein DL, Shen Q, Bhat AN. p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. Roles of nuclear factors, nuclear factor kappa B, cAMP response element-binding protein, CCAAT/enhancer-binding protein-beta, and activating transcription factor-2. J Biol Chem. 2002; 277(33): 29584-29592. https://doi.org/10.1074/jbc.M204994200
  • [15] Hedges JC, Singer CA, Gerthoffer WT. Mitogen-activated protein kinases regulate cytokine gene expression in human airway myocytes. Am J Respir Cell Mol Biol. 2000; 23(1): 86-94. https://doi.org/10.1165/ajrcmb.23.1.4014
  • [16] Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol. 2000; 20(12): 4265-4274. https://doi.org/10.1128/MCB.20.12.4265-4274.2000
  • [17] Yang CM, Chien CS, Hsiao LD, Luo SF, Wang CC. Interleukin-1beta-induced cyclooxygenase-2 expression is mediated through activation of p42/44 and p38 MAPKS, and NF-kappaB pathways in canine tracheal smooth muscle cells. Cell Signal. 2002; 14(11): 899-911. https://doi.org/10.1016/S0898-6568(02)00037-2
  • [18] Fong CY, Pang L, Holland E, Knox AJ. TGF-beta1 stimulates IL-8 release, COX-2 expression, and PGE(2) release in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2000; 279(1): L201-207. https://doi.org/10.1152/ajplung.2000.279.1.L201
  • [19] Maier JA, Hla T, Maciag T. Cyclooxygenase is an immediate-early gene induced by interleukin-1 in human endothelial cells. J Biol Chem. 1990; 265(19): 10805-10808. https://doi.org/10.1016/S0021-9258(19)38515-1
  • [20] Perkins DJ, Kniss DA. Rapid and transient induction of cyclo-oxygenase 2 by epidermal growth factor in human amnion-derived WISH cells. Biochem J. 1997; 321 ( Pt 3): 677-681. https://doi.org/10.1042/bj3210677
  • [21] Cai ZL, Shen B, Yuan Y, Liu C, Xie QW, Hu TT, Yao Q, Wu QQ, Tang QZ. The effect of HMGA1 in LPS-induced myocardial ınflammation. Int J Biol Sci. 2020; 16(11): 1798-1810. https://doi.org/10.7150/ijbs.39947.
  • [22] Nick JA, Young SK, Brown KK, Avdi NJ, Arndt PG, Suratt BT, Janes MS, Henson PM, Worthen GS. Role of p38 mitogen-activated protein kinase in a murine model of pulmonary inflammation. J Immunol. 2000; 164(4): 2151-2159. https://doi.org/10.4049/jimmunol.164.4.2151
  • [23] Branger J, van den Blink B, Weijer S, Madwed J, Bos CL, Gupta A, Yong CL, Polmar SH, Olszyna DP, Hack CE, van Deventer SJ, Peppelenbosch MP, van der Poll T. Anti-inflammatory effects of a p38 mitogen-activated protein kinase inhibitor during human endotoxemia. J Immunol. 2002; 168(8): 4070-4077. https://doi.org/10.4049/jimmunol.168.8.4070
  • [24] Kwon IS, Yim JH, Lee HK, Pyo S. Lobaric Acid Inhibits VCAM-1 Expression in TNF-α-stimulated vascular smooth muscle cells via modulation of NF-κB and MAPK signaling pathways. Biomol Ther (Seoul). 2016; 24(1): 25-32. https://doi.org/10.4062/biomolther.2015.084
  • [25] Park B, Yim JH, Lee HK, Kim BO, Pyo S. Ramalin inhibits VCAM-1 expression and adhesion of monocyte to vascular smooth muscle cells through MAPK and PADI4-dependent NF-kB and AP-1 pathways. Biosci Biotechnol Biochem. 2015; 79(4): 539-552. https://doi.org/10.1080/09168451.2014.991681
  • [26] Kim JE, Min SK, Hong JM, Kim KH, Han SJ, Yim JH, Park H, Kim IC. Anti-inflammatory effects of methanol extracts from the Antarctic lichen, Amandinea sp. in LPS-stimulated raw 264.7 macrophages and zebrafish. Fish Shellfish Immunol. 2020; 107(Pt A): 301-308. https://doi.org/10.1016/j.fsi.2020.10.017.
  • [27] Cirillo D, Borroni E, Festoso I, Monti D, Romeo S, Mazier D, Verotta L. Synthesis and antimycobacterial activity of (+)-usnic acid conjugates. Arch Pharm(Weinheim). 2018; 351(12): e1800177. https://doi.org/10.1002/ardp.201800177
  • [28] Furmanek Ł, Czarnota P, Seaward MRD. Antifungal activity of lichen compounds against dermatophytes: A review. J Appl Microbiol. 2019; 127(2): 308-325. https://doi.org/10.1111/jam.14209
  • [29] Micheletti AC, Honda NK, Ravaglia LM, Matayoshi T, Spielmann AA. Antibacterial potencial of 12 Lichen species. An Acad Bras Cienc. 2021; 93(4): S0001-37652021000700904. https://doi.org/10.1590/0001-3765202120191194
  • [30] Wayne PA. Clinical and Laboratory Standards Institute (CLSI); 2010. Performance standards for antimicrobial susceptibility testing, 20.
  • [31] Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol. 1990; 27(2-3): 229-237. https://doi.org/10.1016/0165-5728(90)90073-v.
  • [32] Cumaoğlu A, Karatoprak GŞ, Yerer MB, Koşar M. Anti-inflammatory effects of Pelargonium endlicherianum Fenzl. extracts in lipopolysaccharide-stimulated macrophages. Turk J Pharm Sci. 2018; 15(1): 107-115. https://doi.org/10.4274/tjps.86580.
Yıl 2024, Cilt: 28 Sayı: 4, 1166 - 1173, 28.06.2025

Öz

Kaynakça

  • [1] Zambare VP, Christopher LP. Biopharmaceutical potential of lichens. Pharm Biol. 2012; 50(6): 778-798. https://doi.org/10.3109/13880209.2011.633089
  • [2] Adenubi OT, Famuyide IM, McGaw LJ, Eloff JN. Lichens: An update on their ethnopharmacological uses and potential as sources of drug leads. J Ethnopharmacol. 2022; 298: 115657. https://doi.org/10.1016/j.jep.2022.115657
  • [3] Micheletti AC, Honda NK, Ravaglia LM, Matayoshi T, Spielmann AA. Antibacterial potencial of 12 Lichen species. An Acad Bras Cienc. 2021; 93(4): S0001-37652021000700904. https://doi.org/10.1590/0001-3765202120191194
  • [4] Wethalawe AN, Alwis YV, Udukala DN, Paranagama PA. Antimicrobial compounds ısolated from Endolichenic Fungi: A Review. Molecules. 2021; 26(13): 3901. https://doi.org/10.3390/molecules26133901
  • [5] Garcia Rowe J, Garcia Gimenez MD, Saenz Rodriguez MT. Some lichen products have antimicrobial activity. Z Naturforsch C J Biosci. 1999; 54(7-8): 605-9. https://doi.org/10.1515/znc-1999-7-824
  • [6] Zindel J, Kubes P. DAMPs, PAMPs, and LAMPs in ımmunity and sterile ınflammation. Annu Rev Pathol. 2020; 15: 493-518. https://doi.org/10.1146/annurev-pathmechdis-012419-032847
  • [7] Amarante-Mendes GP, Adjemian S, Branco LM, Zanetti LC, Weinlich R, Bortoluci KR. Pattern recognition receptors and the host cell death molecular machinery. Front Immunol. 2018; 9: 2379. https://doi.org/10.3389/fimmu.2018.02379
  • [8] Li X, Jiang S, Tapping RI. Toll-like receptor signaling in cell proliferation and survival. Cytokine. 2010; 49(1): 1-9. https://doi.org/10.1016/j.cyto.2009.08.010
  • [9] Chaiwut R, Kasinrerk W. Very low concentration of lipopolysaccharide can induce the production of various cytokines and chemokines in human primary monocytes. BMC Res Notes. 2022; 15(1): 42. https://doi.org/10.1186/s13104-022-05941-4
  • [10] Salvemini D, Kim SF, Mollace V. Reciprocal regulation of the nitric oxide and cyclooxygenase pathway in pathophysiology: relevance and clinical implications. Am J Physiol Regul Integr Comp Physiol. 2013; 304(7): R473-487. https://doi.org/10.1152/ajpregu.00355.2012
  • [11] Hong JM, Kim JE, Min SK, Kim KH, Han SJ, Yim JH, Park H, Kim JH, Kim IC. Anti-ınflammatory effects of antarctic lichen Umbilicaria antarctica methanol extract in lipopolysaccharide-stimulated RAW 264.7 macrophage cells and zebrafish model. Biomed Res Int. 2021; 2021: 8812090. https://doi.org/10.1155/2021/8812090.
  • [12] Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005; 15(1): 11-18. https://doi.org/10.1038/sj.cr.7290257
  • [13] Ratajczak-Wrona W, Jablonska E, Marcinczyk M, Grabowska Z, Piotrowski L. Role of p38 MAPK pathway in induction of iNOS expression in neutrophils and peripheral blood mononuclear cells in patients with squamous cell carcinoma of the oral cavity. J Oral Maxillofac Surg. 2009; 67(11): 2354-2363. https://doi.org/10.1016/j.joms.2009.04.030
  • [14] Bhat NR, Feinstein DL, Shen Q, Bhat AN. p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. Roles of nuclear factors, nuclear factor kappa B, cAMP response element-binding protein, CCAAT/enhancer-binding protein-beta, and activating transcription factor-2. J Biol Chem. 2002; 277(33): 29584-29592. https://doi.org/10.1074/jbc.M204994200
  • [15] Hedges JC, Singer CA, Gerthoffer WT. Mitogen-activated protein kinases regulate cytokine gene expression in human airway myocytes. Am J Respir Cell Mol Biol. 2000; 23(1): 86-94. https://doi.org/10.1165/ajrcmb.23.1.4014
  • [16] Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol. 2000; 20(12): 4265-4274. https://doi.org/10.1128/MCB.20.12.4265-4274.2000
  • [17] Yang CM, Chien CS, Hsiao LD, Luo SF, Wang CC. Interleukin-1beta-induced cyclooxygenase-2 expression is mediated through activation of p42/44 and p38 MAPKS, and NF-kappaB pathways in canine tracheal smooth muscle cells. Cell Signal. 2002; 14(11): 899-911. https://doi.org/10.1016/S0898-6568(02)00037-2
  • [18] Fong CY, Pang L, Holland E, Knox AJ. TGF-beta1 stimulates IL-8 release, COX-2 expression, and PGE(2) release in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2000; 279(1): L201-207. https://doi.org/10.1152/ajplung.2000.279.1.L201
  • [19] Maier JA, Hla T, Maciag T. Cyclooxygenase is an immediate-early gene induced by interleukin-1 in human endothelial cells. J Biol Chem. 1990; 265(19): 10805-10808. https://doi.org/10.1016/S0021-9258(19)38515-1
  • [20] Perkins DJ, Kniss DA. Rapid and transient induction of cyclo-oxygenase 2 by epidermal growth factor in human amnion-derived WISH cells. Biochem J. 1997; 321 ( Pt 3): 677-681. https://doi.org/10.1042/bj3210677
  • [21] Cai ZL, Shen B, Yuan Y, Liu C, Xie QW, Hu TT, Yao Q, Wu QQ, Tang QZ. The effect of HMGA1 in LPS-induced myocardial ınflammation. Int J Biol Sci. 2020; 16(11): 1798-1810. https://doi.org/10.7150/ijbs.39947.
  • [22] Nick JA, Young SK, Brown KK, Avdi NJ, Arndt PG, Suratt BT, Janes MS, Henson PM, Worthen GS. Role of p38 mitogen-activated protein kinase in a murine model of pulmonary inflammation. J Immunol. 2000; 164(4): 2151-2159. https://doi.org/10.4049/jimmunol.164.4.2151
  • [23] Branger J, van den Blink B, Weijer S, Madwed J, Bos CL, Gupta A, Yong CL, Polmar SH, Olszyna DP, Hack CE, van Deventer SJ, Peppelenbosch MP, van der Poll T. Anti-inflammatory effects of a p38 mitogen-activated protein kinase inhibitor during human endotoxemia. J Immunol. 2002; 168(8): 4070-4077. https://doi.org/10.4049/jimmunol.168.8.4070
  • [24] Kwon IS, Yim JH, Lee HK, Pyo S. Lobaric Acid Inhibits VCAM-1 Expression in TNF-α-stimulated vascular smooth muscle cells via modulation of NF-κB and MAPK signaling pathways. Biomol Ther (Seoul). 2016; 24(1): 25-32. https://doi.org/10.4062/biomolther.2015.084
  • [25] Park B, Yim JH, Lee HK, Kim BO, Pyo S. Ramalin inhibits VCAM-1 expression and adhesion of monocyte to vascular smooth muscle cells through MAPK and PADI4-dependent NF-kB and AP-1 pathways. Biosci Biotechnol Biochem. 2015; 79(4): 539-552. https://doi.org/10.1080/09168451.2014.991681
  • [26] Kim JE, Min SK, Hong JM, Kim KH, Han SJ, Yim JH, Park H, Kim IC. Anti-inflammatory effects of methanol extracts from the Antarctic lichen, Amandinea sp. in LPS-stimulated raw 264.7 macrophages and zebrafish. Fish Shellfish Immunol. 2020; 107(Pt A): 301-308. https://doi.org/10.1016/j.fsi.2020.10.017.
  • [27] Cirillo D, Borroni E, Festoso I, Monti D, Romeo S, Mazier D, Verotta L. Synthesis and antimycobacterial activity of (+)-usnic acid conjugates. Arch Pharm(Weinheim). 2018; 351(12): e1800177. https://doi.org/10.1002/ardp.201800177
  • [28] Furmanek Ł, Czarnota P, Seaward MRD. Antifungal activity of lichen compounds against dermatophytes: A review. J Appl Microbiol. 2019; 127(2): 308-325. https://doi.org/10.1111/jam.14209
  • [29] Micheletti AC, Honda NK, Ravaglia LM, Matayoshi T, Spielmann AA. Antibacterial potencial of 12 Lichen species. An Acad Bras Cienc. 2021; 93(4): S0001-37652021000700904. https://doi.org/10.1590/0001-3765202120191194
  • [30] Wayne PA. Clinical and Laboratory Standards Institute (CLSI); 2010. Performance standards for antimicrobial susceptibility testing, 20.
  • [31] Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol. 1990; 27(2-3): 229-237. https://doi.org/10.1016/0165-5728(90)90073-v.
  • [32] Cumaoğlu A, Karatoprak GŞ, Yerer MB, Koşar M. Anti-inflammatory effects of Pelargonium endlicherianum Fenzl. extracts in lipopolysaccharide-stimulated macrophages. Turk J Pharm Sci. 2018; 15(1): 107-115. https://doi.org/10.4274/tjps.86580.
Toplam 32 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Eczacılık ve İlaç Bilimleri (Diğer)
Bölüm Articles
Yazarlar

Selçuk Sevinç 0009-0006-9216-5751

Mehmet Gökhan Halıcı 0000-0003-4797-1157

Ahmet Cumaoğlu 0000-0002-3997-7746

Yayımlanma Tarihi 28 Haziran 2025
Yayımlandığı Sayı Yıl 2024 Cilt: 28 Sayı: 4

Kaynak Göster

APA Sevinç, S., Halıcı, M. G., & Cumaoğlu, A. (2025). Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye). Journal of Research in Pharmacy, 28(4), 1166-1173.
AMA Sevinç S, Halıcı MG, Cumaoğlu A. Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye). J. Res. Pharm. Temmuz 2025;28(4):1166-1173.
Chicago Sevinç, Selçuk, Mehmet Gökhan Halıcı, ve Ahmet Cumaoğlu. “Screening of Antimicrobial and Antiinflammatory Activities of Three Lichenized Fungal Extracts Collected from Northwest Anatolia (Türkiye)”. Journal of Research in Pharmacy 28, sy. 4 (Temmuz 2025): 1166-73.
EndNote Sevinç S, Halıcı MG, Cumaoğlu A (01 Temmuz 2025) Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye). Journal of Research in Pharmacy 28 4 1166–1173.
IEEE S. Sevinç, M. G. Halıcı, ve A. Cumaoğlu, “Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye)”, J. Res. Pharm., c. 28, sy. 4, ss. 1166–1173, 2025.
ISNAD Sevinç, Selçuk vd. “Screening of Antimicrobial and Antiinflammatory Activities of Three Lichenized Fungal Extracts Collected from Northwest Anatolia (Türkiye)”. Journal of Research in Pharmacy 28/4 (Temmuz 2025), 1166-1173.
JAMA Sevinç S, Halıcı MG, Cumaoğlu A. Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye). J. Res. Pharm. 2025;28:1166–1173.
MLA Sevinç, Selçuk vd. “Screening of Antimicrobial and Antiinflammatory Activities of Three Lichenized Fungal Extracts Collected from Northwest Anatolia (Türkiye)”. Journal of Research in Pharmacy, c. 28, sy. 4, 2025, ss. 1166-73.
Vancouver Sevinç S, Halıcı MG, Cumaoğlu A. Screening of antimicrobial and antiinflammatory activities of three lichenized fungal extracts collected from Northwest Anatolia (Türkiye). J. Res. Pharm. 2025;28(4):1166-73.