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Comparative analyses of antioxidant, cytotoxic, and anti-inflammatory activities of different Cladonia species and determination of fumarprotocetraric acid amounts

Year 2021, Volume: 24 Issue: 6, 1196 - 1207, 31.12.2021

Zekiye Kocakaya Mustafa Kocakaya , Gökçe Şeker Karatoprak

https://doi.org/10.18016/ksutarimdoga.vi.868927
Cited By: 3

Abstract

In traditional medicine, Cladonia lichens are used for several disorders like hypertension, headaches, dizziness, cough, and menstrual disorders. The study aimed to determine the biological activities of 70% methanol extracts of nine Cladonia species from Turkey. The chemical composition was analyzed via spectrophotometric and chromatographic (HPLC) techniques. DPPH● (1,1-diphenyl-2-picrylhydrazyl) and ABTS+● (2,2'-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) radical scavenging activities, inhibition of β-carotene/linoleic acid co-oxidation, and cytotoxicity on A549 and COLO205 cell lines were studied. Anti-inflammatory activity was assessed on the Raw 264.7 mouse macrophage cell line by determining nitric oxide (NO) levels. Among the studied Cladonia species Cladonia firma was found the most active extract in ABTS+● test system (2.58±0.07 mmol/L/Trolox) and also in the cytotoxicity and anti-inflammatory experiments. Cladonia pocillum, Cladonia rangiformis, and Cladonia foliaceae were also found to be active. Fumarprotocetraric acid amounts are between 1.89 -23.82 mg/gextract and fumarprotocetraric acid content did not show linearity with biological activities. It has been proved with this study that lichens traditionally used in treatment have as much biological activity as plants and can be evaluated in pharmaceuticals and cosmetics.

Keywords

Antioxidant Anti-inflammatory Cladonia Cytotoxicity Fumarprotocetraric acid

Project Number

6602b BMYO/17-121

References

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  • Ahti T, Stenroos S, Moberg R 2013. Nordic Lichen Flora Volume 5 Cladoniaceae, Museum of Evolution. Uppsala University.
  • Antal DS 2004. Medicinal plants with antioxidant properties from Banat region (Romania): a rich pool for the discovery of multi-target phytochemicals active in free-radical related disorders. Analele Universitatii din Oradea-Fascicula Biology 22:14-22.
  • Aslan A, Güllüce M, Sökmen M, Adιgüzel A, Şahin F, Özkan H 2006. Antioxidant and antimicrobial properties of the lichens Cladonia foliacea, Dermatocarpon miniatum, Everinia divaricata, Evernia prunastri, and Neofuscella pulla. Pharmaceutical Biology 44:247-252. https://doi.org/10.1080/13880200600713808
  • Bartak M, Hajek J, Vrablíkova H, Dubova J 2004. High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. Plant Biology 3:331-341. https://doi.org/10.1055/s-2004-820877
  • Behera BC, Verma N, Sonone A, Makhija U 2005. Antioxidant and antibacterial activities of Usnea ghattensis in vitro. Biotechnology Letters 27:991-995. https://doi.org/10.1007/s10529-005-7847-3
  • Bhattacharyya S, Deep PR, Singh S, Nayak B 2016. Lichen secondary metabolites and its biological activity. American Journal of Pharm-Tech Research 6:29-44.
  • Caviglia AM, Nicora P, Giordani P, Brunialti G, Modenesi P 2001. Oxidative stress and usnic acid content in Parmelia caperata and Parmelia soredians (lichens). II Farmaco 56:379-382. https://doi.org/10.1016/S0014-827X(01)01090-4
  • Choudhari SK, Chaudhary M, Bagde S, Gadbail AR, Joshi V 2013. Nitric oxide and cancer: a review. World Journal of Surgical Oncology 11:1. https://doi.org/10.1186/1477-7819-11-118
  • Coskun ZM, Ersoz M, Acikgoz B, Karalti I, Cobanoglu G, Sesal C 2015. Anti-Proliferative and Apoptotic Effects of Methanolic Extracts from Different Cladonia Species on Human Breast Cancer Cells. Folia Biologica (Praha) 61:97-103.
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  • Huovinen K, Ahti T 1982. Biosequential patterns for the formation of depsides, depsidones, and dibenzofurans in the genus Cladonia (lichen-forming ascomycetes). Annales Botanici Fennici 19:225-234. Avaliable at www.jstor.org/stable/23725855
  • Khansari N., Shakiba Y, Mahmoudi, M 2009. Chronic Inflammation and Oxidative Stress as a Major Cause of Age- Related Diseases and Cancer. Recent Patents on Inflammation & Allergy Drug Discovery 3:73-80. https://doi.org/10.2174/187221309787158371
  • Koparal AT, Ayaz Tüylü B, Türk H 2006. In vitro cytotoxic activities of (+)-usnic acid and (−)-usnic acid on V79, A549, and human lymphocyte cells and their non-genotoxicity on human lymphocytes. Natural Product Research 20:1300-1307. https://doi.org/10.1080/14786410601101910
  • Kosani M, Rankovi B, Stanojkovi T, Rancic A, Manojlovi N 2014. Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. Food Science and Technology 59:518-525. https://doi.org/10.1016/j.lwt.2014.04.047
  • Kosanić M, Ranković B, Vukojević J 2011. Antioxidant properties of some lichen species. Journal of Food Scıence and Technology 48:584-590. https://doi.org/10.1007/s13197-010-0174-2
  • Kosanić M, Ristić S, Stanojkovic T, Manojlovic N, Ranković B 2018. Extracts of five Cladonia lichens as sources of biologically active compounds. Farmacia 66:644-651. https://doi.org/10.31925/farmacia.2018.4.13
  • Laundon, J 1971. Fumarprotocetraric Acid in Cladonia Rangiformis. The Lichenologist 5(1-2), 175-176. https://doi.org/10.1017/S0024282971000173 Lumbsch HT, Huhndorf SM 2010. Myconet Volume 14. Part One. Outline of Ascomycota-2009. Part Two. Notes on Ascomycete Systematics. Nos. 4751-5113. Fieldiana Life and Earth Sciences 2010:4751-5113. https://doi.org/10.3158/1557.1
  • Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP et al 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98:1088-1103. https://doi.org/10.1080/15572536.2006.11832636
  • Molnár K, Farkas E 2010. Current results on biological activities of lichen secondary metabolites: a Review. Verlag der Zeitschrift für Naturforschung 65:157-173. https://doi.org/10.1515/znc-2010-3-401
  • Narendra Kumar SM, Khurana P 2019. Active Compounds and Bacteria Harbouring Capacity of Lichens and Its Medicinal Use in Bacterial and Cancer Infections. Plant Biotechnology: Progress in Genomic Era 327-348. https://doi.org/10.1007/978-981-13-8499-8_15
  • Okan OT, Varlıbaş H, Öz M, Deniz İ 2013. Antioxidant analysis methods and some non-wood forest plant products as sources of antioxidants in Eastern Black Sea Region. Kastamonu University Journal of Forestry Faculty JF 13:48-59.
  • Parejo I, Viladomat F, Bastida J, Rosas-Romero A, Flerlage N, Burillo J, Codina C 2002. Comparison between the radical scavenging activity and antioxidant activity of six distilled and nondistilled Mediterranean herbs and aromatic plants. Journal of Agricultural Food Chemistry 50:6882-6890. https://doi.org/10.1021/jf020540a
  • Paudel B, Bhattarai HD, Pandey DP, Hur JS, Hong SG, Kim C, Yim JG 2012. Antioxidant, Antibacterial activity and Brine shrimp toxicity test of some Mountainous Lichens from Nepal Biol Res. 45: 387-391. https://doi.org/10.4067/S0716-97602012000400010
  • Prokop′ev IA, Filippova GV 2019. Antioxidant Activity of Secondary Metabolites from Cladonia Lichens. Chemistry of Natural Compounds 55: 945-947. https://doi.org/10.1007/s10600-019-02855-9
  • Ramos DDBM, Gomes FS, Napoleão TH, Paiva PMG, Silva MDC, Coelho LCBB 2014. Antimicrobial activity of Cladonia verticillaris lichen preparations on bacteria and fungi of medical importance. Chinese Journal of Biology 2014:1-7. https://doi.org/10.1155/2014/219392
  • Ranković BR, Kosanić MM, Stanojković TP 2011. Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis. BMC Complementary and Alternative Medicine 11:97. https://doi.org/10.1186/1472-6882-11-97
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Farklı Cladonia türlerinin antioksidan, sitotoksik ve antienflamatuvar aktivitelerinin karşılaştırmalı analizleri ve fumarprotosetrarik asit miktarlarının belirlenmesi

Year 2021, Volume: 24 Issue: 6, 1196 - 1207, 31.12.2021

Zekiye Kocakaya Mustafa Kocakaya , Gökçe Şeker Karatoprak

https://doi.org/10.18016/ksutarimdoga.vi.868927
Cited By: 3

Abstract

Geleneksel tıpta Cladonia likenleri, hipertansiyon, baş ağrısı, baş dönmesi, öksürük ve adet bozuklukları gibi çeşitli rahatsızlıklarda kullanılır. Çalışmada, Türkiye'den 9 Cladonia türünün % 70 metanol ekstrelerinin biyolojik aktivitelerinin belirlemesi amaçlandı. Kimyasal bileşimi, spektrofotometrik ve kromatografik (HPLC) tekniklerle analiz edildi. Ekstrelerin DPPH● (1,1-difenil-2-pikrilhidrazil) ve ABTS+● (2,2'-azino-bis (3-etilbenzotiyazolin-6-sülfonik asit) radikal süpürücü aktiviteleri, β-karoten/linoleik asit birlikte oksidasyonunun inhibisyonu ve A549 ve COLO205 hücre hatlarında sitotoksisiteleri çalışıldı. Antienflamatuvar aktivite, Raw 264.7 fare makrofaj hücre hattında nitrik oksit (NO) seviyelerinin belirlenmesiyle değerlendirildi. Çalışılan Cladonia türleri arasında Cladonia firma, ABTS+●test sisteminde (2.58 ± 0.07 mmol/L/Troloks) ve ayrıca sitotoksisite ve antienflamatuvar deneylerinde en aktif ekstre olarak belirlendi. Cladonia pocillum, Cladonia rangiformis ve Cladonia foliaceae'nin de aktif olduğu bulundu. Fumarprotosetrarik asit miktarları 1.89-23.82 mg/gekstre arasında olup fumarprotosetrarik asit içeriği biyolojik aktivitelerle doğrusallık göstermedi. Geleneksel olarak tedavide kullanılan likenlerin bitkiler kadar biyolojik aktiviteye sahip olduğu ve ilaç ve kozmetikte değerlendirilebileceği bu çalışma ile kanıtlanmıştır.

Keywords

Antioksidan Antienflamatuvar Cladonia Sitotoksisite Fumarprotosetrarik asit

Supporting Institution

Bozok Üniversitesi

Project Number

6602b BMYO/17-121

References

  • Ahti T, Hammer S 2002. Cladonia. In: Nash III TH, Ryan BD, Gries C. Bungartz F, editor. Lichen Flora of the Greater Sonoran Desert Region. Arizona State University.
  • Ahti T, Stenroos S, Moberg R 2013. Nordic Lichen Flora Volume 5 Cladoniaceae, Museum of Evolution. Uppsala University.
  • Antal DS 2004. Medicinal plants with antioxidant properties from Banat region (Romania): a rich pool for the discovery of multi-target phytochemicals active in free-radical related disorders. Analele Universitatii din Oradea-Fascicula Biology 22:14-22.
  • Aslan A, Güllüce M, Sökmen M, Adιgüzel A, Şahin F, Özkan H 2006. Antioxidant and antimicrobial properties of the lichens Cladonia foliacea, Dermatocarpon miniatum, Everinia divaricata, Evernia prunastri, and Neofuscella pulla. Pharmaceutical Biology 44:247-252. https://doi.org/10.1080/13880200600713808
  • Bartak M, Hajek J, Vrablíkova H, Dubova J 2004. High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. Plant Biology 3:331-341. https://doi.org/10.1055/s-2004-820877
  • Behera BC, Verma N, Sonone A, Makhija U 2005. Antioxidant and antibacterial activities of Usnea ghattensis in vitro. Biotechnology Letters 27:991-995. https://doi.org/10.1007/s10529-005-7847-3
  • Bhattacharyya S, Deep PR, Singh S, Nayak B 2016. Lichen secondary metabolites and its biological activity. American Journal of Pharm-Tech Research 6:29-44.
  • Caviglia AM, Nicora P, Giordani P, Brunialti G, Modenesi P 2001. Oxidative stress and usnic acid content in Parmelia caperata and Parmelia soredians (lichens). II Farmaco 56:379-382. https://doi.org/10.1016/S0014-827X(01)01090-4
  • Choudhari SK, Chaudhary M, Bagde S, Gadbail AR, Joshi V 2013. Nitric oxide and cancer: a review. World Journal of Surgical Oncology 11:1. https://doi.org/10.1186/1477-7819-11-118
  • Coskun ZM, Ersoz M, Acikgoz B, Karalti I, Cobanoglu G, Sesal C 2015. Anti-Proliferative and Apoptotic Effects of Methanolic Extracts from Different Cladonia Species on Human Breast Cancer Cells. Folia Biologica (Praha) 61:97-103.
  • Dayan FE, Romagni JG 2001. Lichens as a potential source of pesticides. Pesticide Outlook 12:229-232. https://doi.org/10.1039/b110543b
  • De Barros Alves GM, de Sousa Maia MB, de Souza Franco E, Galvão AM, da Silva TG. Gomes RM, da Silva NH 2014. Expectorant and antioxidant activities of purified fumarprotocetraric acid from Cladonia verticillaris lichen in mice. Pulmonary Pharmacology & Therapeutics 27:139-143. https://doi.org/10.1016/j.pupt.2013.07.002
  • Farkas E, Biró B, Szabó K, Veres K, Csintalan ZS, Engel R 2020. The Amount of Lichen Secondary Metabolites In Cladonia foliacea (Cladoniaceae, Lichenised Ascomycota). Acta Botanica Hungarica 62:33-48. https://doi.org/10.1556/034.62.2020.1-2.4
  • Gaidhani SN, Singh A, Kumari S, Lavekar GS, Juvekar, AS, Sen S, Padhi MM 2013. Evaluation of some plant extracts for standardization and anticancer activity. Indian Journal of Traditional Knowledge 12:682-687.
  • Gyamfi MA 1999. Yonamine M, Aniya Y. Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. General Pharmacology 32:661-667. https://doi.org/10.1016/S0306-3623(98)00238-9
  • Hawrył A, Hawrył M, Hajnos-Stolarz A, Abramek J, Bogucka-Kocka A, Komsta Ł 2020. HPLC Fingerprint Analysis with the Antioxidant and Cytotoxic Activities of Selected Lichens Combined with the Chemometric Calculations Molecules 25, 4301. https://doi.org/10.3390/molecules25184301
  • Hodkinson B, Lutzoni F 2009. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163-180. https://doi.org/10.1007/s13199-009-0049-3
  • Hoshyar R, Mostafavinia SE, Zarban A, Hassanpour M, Partovfari M, Taheri A, Pouyan M 2015. Correlation of anticancer effects of 12 Iranian herbs on human breast adenocarcinoma cells with antioxidant properties. Free Radicals and Antioxidants 5:65-73. https://doi.org/10.5530/fra.2015.2.4
  • Huneck S 1999. The significance of lichens and their metabolites. Naturwissenschaften 86:559-570. https://doi.org/10.1007/s001140050676
  • Huovinen K, Ahti T 1982. Biosequential patterns for the formation of depsides, depsidones, and dibenzofurans in the genus Cladonia (lichen-forming ascomycetes). Annales Botanici Fennici 19:225-234. Avaliable at www.jstor.org/stable/23725855
  • Khansari N., Shakiba Y, Mahmoudi, M 2009. Chronic Inflammation and Oxidative Stress as a Major Cause of Age- Related Diseases and Cancer. Recent Patents on Inflammation & Allergy Drug Discovery 3:73-80. https://doi.org/10.2174/187221309787158371
  • Koparal AT, Ayaz Tüylü B, Türk H 2006. In vitro cytotoxic activities of (+)-usnic acid and (−)-usnic acid on V79, A549, and human lymphocyte cells and their non-genotoxicity on human lymphocytes. Natural Product Research 20:1300-1307. https://doi.org/10.1080/14786410601101910
  • Kosani M, Rankovi B, Stanojkovi T, Rancic A, Manojlovi N 2014. Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. Food Science and Technology 59:518-525. https://doi.org/10.1016/j.lwt.2014.04.047
  • Kosanić M, Ranković B, Vukojević J 2011. Antioxidant properties of some lichen species. Journal of Food Scıence and Technology 48:584-590. https://doi.org/10.1007/s13197-010-0174-2
  • Kosanić M, Ristić S, Stanojkovic T, Manojlovic N, Ranković B 2018. Extracts of five Cladonia lichens as sources of biologically active compounds. Farmacia 66:644-651. https://doi.org/10.31925/farmacia.2018.4.13
  • Laundon, J 1971. Fumarprotocetraric Acid in Cladonia Rangiformis. The Lichenologist 5(1-2), 175-176. https://doi.org/10.1017/S0024282971000173 Lumbsch HT, Huhndorf SM 2010. Myconet Volume 14. Part One. Outline of Ascomycota-2009. Part Two. Notes on Ascomycete Systematics. Nos. 4751-5113. Fieldiana Life and Earth Sciences 2010:4751-5113. https://doi.org/10.3158/1557.1
  • Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP et al 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98:1088-1103. https://doi.org/10.1080/15572536.2006.11832636
  • Molnár K, Farkas E 2010. Current results on biological activities of lichen secondary metabolites: a Review. Verlag der Zeitschrift für Naturforschung 65:157-173. https://doi.org/10.1515/znc-2010-3-401
  • Narendra Kumar SM, Khurana P 2019. Active Compounds and Bacteria Harbouring Capacity of Lichens and Its Medicinal Use in Bacterial and Cancer Infections. Plant Biotechnology: Progress in Genomic Era 327-348. https://doi.org/10.1007/978-981-13-8499-8_15
  • Okan OT, Varlıbaş H, Öz M, Deniz İ 2013. Antioxidant analysis methods and some non-wood forest plant products as sources of antioxidants in Eastern Black Sea Region. Kastamonu University Journal of Forestry Faculty JF 13:48-59.
  • Parejo I, Viladomat F, Bastida J, Rosas-Romero A, Flerlage N, Burillo J, Codina C 2002. Comparison between the radical scavenging activity and antioxidant activity of six distilled and nondistilled Mediterranean herbs and aromatic plants. Journal of Agricultural Food Chemistry 50:6882-6890. https://doi.org/10.1021/jf020540a
  • Paudel B, Bhattarai HD, Pandey DP, Hur JS, Hong SG, Kim C, Yim JG 2012. Antioxidant, Antibacterial activity and Brine shrimp toxicity test of some Mountainous Lichens from Nepal Biol Res. 45: 387-391. https://doi.org/10.4067/S0716-97602012000400010
  • Prokop′ev IA, Filippova GV 2019. Antioxidant Activity of Secondary Metabolites from Cladonia Lichens. Chemistry of Natural Compounds 55: 945-947. https://doi.org/10.1007/s10600-019-02855-9
  • Ramos DDBM, Gomes FS, Napoleão TH, Paiva PMG, Silva MDC, Coelho LCBB 2014. Antimicrobial activity of Cladonia verticillaris lichen preparations on bacteria and fungi of medical importance. Chinese Journal of Biology 2014:1-7. https://doi.org/10.1155/2014/219392
  • Ranković BR, Kosanić MM, Stanojković TP 2011. Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis. BMC Complementary and Alternative Medicine 11:97. https://doi.org/10.1186/1472-6882-11-97
  • Re R, Pellegrini N 1999. Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine 26:1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
  • Selbmann L, Zucconi L, Ruisi S, Grube M, Cardinale M, Onofri S 2010. Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance. Polar Biology 33:71-83. https://doi.org/10.1007/s00300-009-0686-2
  • Shahidi F, Yeo J 2018. Bioactivities of Phenolics by Focusing on Suppression of Chronic Diseases: A Review. Int J Mol Sci 19:1573. Published 2018 May 25. https://doi.org/10.3390/ijms19061573
  • Shukla P, Upreti DK, Nayaka S, Tewari P 2014. Natural dyes from Himalayan lichens. Indian Journal of Traditional Knowledge 13:195-201.
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There are 48 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section RESEARCH ARTICLE
Authors

Zekiye Kocakaya 0000-0001-5248-0462

Mustafa Kocakaya 0000-0003-2306-8094

Gökçe Şeker Karatoprak 0000-0001-5829-6914

Project Number 6602b BMYO/17-121
Publication Date December 31, 2021
Submission Date January 26, 2021
Acceptance Date March 3, 2021
Published in Issue Year 2021 Volume: 24 Issue: 6

Cite

APA Kocakaya, Z., Kocakaya, M., & Şeker Karatoprak, G. (2021). Comparative analyses of antioxidant, cytotoxic, and anti-inflammatory activities of different Cladonia species and determination of fumarprotocetraric acid amounts. Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 24(6), 1196-1207. https://doi.org/10.18016/ksutarimdoga.vi.868927

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