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Cytotoxic, Genotoxic and Oxidative Effects of Cladonia furcata (Huds.) Schrad. on Human Peripheral Lymphocytes

Yıl 2018, Cilt: 39 Sayı: 1, 169 - 180, 16.03.2018
https://doi.org/10.17776/csj.405735

Öz

In
the present study, it was aimed the evaluation of activities of methanol and
water extracts (respectively, CME and CSE) obtained from
Cladonia furcata (Huds.) Schrad. on human lymphocytes. In order to test cytotoxic effect in lymphocytes, 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium
bromide and lactate dehydrogenase tests were used.
Oxidative stress and
genotoxicity changes in the cells were also examined with total oxidant status
and 8-hydroxy-2
-deoxyguanosine levels, respectively. In
addition to these assays, total antioxidant capacity (TAC) changes in
lymphocytes treated with extracts were also determined. It was revealed that
low concentrations of
CSE did not show cytotoxic effect at high levels (IC50=221,14 mg/L). Performed correlation
analyzes showed that cytotoxicity was associated with oxidative stress (p < 0,01). Considering all
applications, it was determined that CSE did not statistically (p > 0,05) cause genetic damage on
cells compared to negative control. Based on TAC in cells, it is notable that
certain concentrations of the extracts (12,5-50 mg/L) significantly increased
TAC (p < 0,05). Consequently, the
resulting data reveal that especially CSE can be a source of new therapeutic
agents due to its high antioxidant properties, without causing genotoxic and
oxidative stress on lymphocytes.

Kaynakça

  • [1] Sultana B, Anwar F, Ashraf M. Effect of extraction solvent/technique on the antioxidant activity of selected medicinal plant extracts. Molecules, 14 (2009) 2167-2180.
  • [2] Zamir R, Khalil SA, Shah ST, Ahmad N. Antioxidant activity influenced by in vivo and in vitro mutagenesis in sugarcane (Saccharum officinarum L.). African J. Biotechnol., 11 (2012) 11686-11692.
  • [3] Paper O. Cadmium-induced response of protein profile and antioxidant enzymes in aquatic macrophytes Myriophyllum spicatum and Ceratophyllum demersum. J. Environ. Stud., 7 (2011) 7: 17-23.
  • [4] Efdi M, Itoh T, Akao Y, Nozawa Y, Koketsu M, Ishihara H. The isolation of secondary metabolites and in vitro potent anti-cancer activity of clerodermic acid from Enicosanthum membranifolium. Bioorg. Med. Chem., 15 (2007) 3667-3671.
  • [5] Efferth T, Herrmann F, Tahrani A, Wink M. Cytotoxic activity of secondary metabolites derived from Artemisia annua L. towards cancer cells in comparison to its designated active constituent artemisinin. Phytomedicine, 18 (2011) 959-969.
  • [6] Markiewicz-Żukowska R, Borawska MH, Fiedorowicz A, Naliwajko SK, Sawicka D, Car H. Propolis changes the anticancer activity of temozolomide in U87MG human glioblastoma cell line. BMC Complement. Altern. Med., 13 (2013) 50.
  • [7] Khan RS, Senthi M, Rao PC, Basha A, Alvala M, Tummuri D, Masubuti H, Fujimoto Y, Begum AS. Cytotoxic constituents of Abutilon indicum leaves against U87MG human glioblastoma cells. Nat. Prod. Res., 29 (2015) 1069-1073.
  • [8] Nash TH. Lichen Biology. New York: Cambridge University Press 2008; 486.
  • [9] Öztürk A, Aslan A. Likenlerin ekonomik özellikleri ve Kuzeydoğu Anadolu’dan bazı liken türleri. Yüzüncü Yıl Üniversitesi Fen Edeb. Fakültesi Fen Bilim. Derg., 2 (1991) 27-42.
  • [10] Ari F, Ulukaya E, Oran S, Celikler S, Ozturk S, Ozel MZ. Promising anticancer activity of a lichen, Parmelia sulcata Taylor, against breast cancer cell lines and genotoxic effect on human lymphocytes. Cytotechnology, 67 (2015) 531-543.
  • [11] Singh N, Nambiar D, Kale RK, Singh RP. Usnic acid inhibits growth and induces cell cycle arrest and apoptosis in human lung carcinoma A549 cells. Nutr. Cancer, 65 (2013) 36-43.
  • [12] O’Neill MA, Mayer MM, Murray KE, Rolim-Santos HML, Santos-Magalhães NS, Thompson AM, Appleyard VCL. Does usnic acid affect microtubules in human cancer cells? Brazilian J. Biol., 70 (2010) 659–664.
  • [13] Yildirim E, Emsen B, Aslan A, Bulak Y, Ercisli S. Insecticidal activity of lichens against the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Egypt. J. Biol. Pest Control, 22 (2012) 151-156.
  • [14] Emsen B, Bulak Y, Yildirim E, Aslan A, Ercisli S. Activities of two major lichen compounds, diffractaic acid and usnic acid against Leptinotarsa decemlineata Say, 1824 (Coleoptera: Chrysomelidae). Egypt. J. Biol. Pest Control, 22 (2012) 5-10.
  • [15] Emsen B, Aslan A, Yildirim E, Ercisli S. Toxicity effects of some lichen species extracts against the colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Egypt. J. Biol. Pest Control, 23 (2013) 193-199.
  • [16] Grujičić D, Stošić I, Kosanić M, Stanojković T, Ranković B, Milošević-Djordjević O. Evaluation of in vitro antioxidant, antimicrobial, genotoxic and anticancer activities of lichen Cetraria islandica. Cytotechnology, 66 (2014) 803-813.
  • [17] Yücel O, Odabaşoǧlu F, Güllüce M, Çalik ZZ, Çakir A, Aslan A, Yazici K, Halici M. Antioxidant and antimicrobial properties of a lichen species, Cladonia rangiformis growing in Turkey. Turkish J. Pharm. Sci., 4 (2007) 101-109.
  • [18] Huneck S. The significance of lichens and their metabolites. Naturwissenschaften, 86 (1999) 559-570.
  • [19] Kirmizigul S, Koz O, Boke N. Constituents of apolar extracts including essential fatty acids of some Turkish lichens. Chem. Nat. Compd., 43 (2007) 462-464.
  • [20] Agar G, Gulluce M, Aslan A, Bozari S, Karadayi M, Orhan F. Mutation preventive and antigenotoxic potential of methanol extracts of two natural lichen. J. Med. Plants Res., 4 (2010) 2132-2137.
  • [21] Einarsdóttir E, Groeneweg J, Björnsdóttir GG, Harethardottir G, Omarsdóttir S, Ingólfsdóttir K, Ogmundsdóttir HM. Cellular mechanisms of the anticancer effects of the lichen compound usnic acid. Planta Med., 76 (2010) 969–974.
  • [22] Wirth V. Die Flechten Baden Württembergs. Württembergs, vol. 1-2. Stuttgart: Ulmer 1995; 1006.
  • [23] Purvis OW, Coppins BJ, Hawksworth DL, James PW, Moore DM. The Lichen Flora of Great Britain and Ireland. London: Natural History Museum Publications in Association with the British Lichen Society 1992; 710.
  • [24] Berridge M V, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol. Annu. Rev., 11 (2005) 127-152.
  • [25] Haslam G, Wyatt D, Kitos PA. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology, 32 (2000) 63-75.
  • [26] Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem., 37 (2004) 277–285.
  • [27] Erel O. A new automated colorimetric method for measuring total oxidant status. Clin. Biochem., 38 (2005) 1103-1111.
  • [28] Gan W, Nie B, Shi F, Xu XM, Qian JC, Takagi Y, Hayakawa H, Sekiguchi M, Cai JP. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: urinary 8-oxoguanosine as a novel biomarker of aging. Free Radic. Biol. Med., 52 (2012) 1700-1707.
  • [29] Emsen B, Turkez H, Togar B, Aslan A. Evaluation of antioxidant and cytotoxic effects of olivetoric and physodic acid in cultured human amnion fibroblasts. Hum. Exp. Toxicol., 36 (2017) 376-385.
  • [30] Bucar F, Schneider I, Ögmundsdóttir H, Ingólfsdóttir K. Anti-proliferative lichen compounds with inhibitory activity on 12(S)-HETE production in human platelets. Phytomedicine , 11 (2004) 602-606.
  • [31] Celenza G, Segatore B, Setacci D, Perilli M, Brisdelli F, Bellio P, Piovano M, Garbarino JA, Amicosante G, Nicoletti M. Antibacterial activity of selected metabolites from Chilean lichen species against methicillin-resistant staphylococci. Nat. Prod. Res., 27 (2013) 1528-1531.
  • [32] Lauinger IL, Vivas L, Perozzo R, Stairiker C, Tarun A, Zloh M, Zhang X, Xu H, Tonge PJ, Franzblau SG, Pham DH, Esguerra C V., Crawford AD, Maes L, Tasdemir D. Potential of lichen secondary metabolites against Plasmodium liver stage parasites with FAS-II as the potential target. J. Nat. Prod., 76 (2013) 1064-1070.
  • [33] Brandao LFG, Alcantara GB, Matos MDFC, Bogo D, Freitas DDS, Oyama NM, Honda NK. Cytotoxic evaluation of phenolic compounds from lichens against melanoma cells. Chem. Pharm. Bull. (Tokyo), 61 (2013) 176-183.
  • [34] Tokur O, Aksoy A. In vitro sitotoksisite testleri. Harran Üniversitesi Vet. Fakültesi Derg., 6 (2017) 112-118.
  • [35] Aydin E, Turkez H. Effects of lichenic extracts (Bryoria capillaris, Peltigera rufescens and Xanthoria elegans) on human blood cells: A cytogenetic and biochemical study. Fresenius Environ. Bull., 20 (2011) 2992-2998.
  • [36] Turkez H, Aydin E, Aslan A. Xanthoria elegans (Link) (lichen) extract counteracts DNA damage and oxidative stress of mitomycin C in human lymphocytes. Cytotechnology ,64 (2012) 679-686.
  • [37] Emsen B, Aslan A, Togar B, Turkez H. In vitro antitumor activities of the lichen compounds olivetoric, physodic and psoromic acid in rat neuron and glioblastoma cells. Pharm. Biol., 54 (2016) 1748-1762.
  • [38] Ceker S, Orhan F, Kizil HE, Alpsoy L, Gulluce M, Aslan A, Agar G. Genotoxic and antigenotoxic potentials of two Usnea species. Toxicol. Ind. Health, 32 (2015) 990-999.
  • [39] Alpsoy L, Orhan F, Nardemir G, Agar G, Gulluce M, Aslan A. Antigenotoxic potencies of a lichen species, Evernia prunastri. Toxicol. Ind. Health, 31 (2015) 153-161.
  • [40] Behera BC, Mahadik N, Morey M. Antioxidative and cardiovascular-protective activities of metabolite usnic acid and psoromic acid produced by lichen species Usnea complanata under submerged fermentation. Pharm. Biol., 50 (2012) 968-979.
  • [41] Sepulveda B, Chamy MC, Piovano M, Areche C. Lichens: Might be considered as a source of gastroprotective molecules? J. Chil. Chem. Soc., 58 (2013) 1750-1752.

Cladonia furcata (Huds.) Schrad.'nın İnsan Periferal Lenfositleri Üzerindeki Sitotoksik, Genotoksik ve Oksidatif Etkileri

Yıl 2018, Cilt: 39 Sayı: 1, 169 - 180, 16.03.2018
https://doi.org/10.17776/csj.405735

Öz

Mevcut
çalışmada, Cladonia furcata (Huds.) Schrad. 
 likeninden elde edilen metanol ve su ekstraktlarının (sırasıyla CME ve CSE) insan lenfositleri
üzerindeki aktivitelerinin değerlendirilmesi amaçlanmıştır. Lenfositlerdeki sitotoksik
etkiyi test etmek için 3-(4,5-dimetiltiazol-2-il)-2,5-difeniltetrazolyum bromür
ve laktat dehidrogenaz testleri kullanılmıştır. Ayrıca, hücrelerdeki oksidatif stres ve genotoksisite değişimleri sırasıyla toplam oksidan durum ve 8-hidroksi-2'-
deoksiguanozin seviyeleri ile incelenmiştir. Bu uygulamalara ek olarak, ekstraktlar ile muamele edilen lenfositlerdeki toplam antioksidan kapasite (TAK) değişimleri de belirlenmiştir. CSE'nin düşük konsantrasyonlarının yüksek seviyelerde sitotoksik etki göstermedikleri
ortaya çıkarılmıştır (IC50=221,14 mg/L). Gerçekleştirilen korelasyon analizleri sitotoksisitenin oksidatif stres ile ilişkili (p < 0.01) olduğunu
göstermiştir. Tüm uygulamalar göz önüne alındığında, özellikle CSE'nin negatif kontrole kıyasla hücreler üzerinde istatistiksel olarak (p >0,0,5) genetik hasar meydana getirmediği
tespit edilmiştir. Hücrelerdeki TAK temel alındığında, ekstraktların belli konsantrasyonlarının (12,5-50 mg/L) TAK'yi anlamlı derecede (p <0,05) yükselttiği dikkat çekmektedir. Sonuç olarak elde edilen veriler, özellikle CSE'nin lenfositler üzeride genotoksik ve oksidatif strese neden olmayarak, yüksek antioksidan özellikleri sayesinde yeni bir tedavi maddesi kaynağı olabileceğini ortaya çıkarmıştır.

Kaynakça

  • [1] Sultana B, Anwar F, Ashraf M. Effect of extraction solvent/technique on the antioxidant activity of selected medicinal plant extracts. Molecules, 14 (2009) 2167-2180.
  • [2] Zamir R, Khalil SA, Shah ST, Ahmad N. Antioxidant activity influenced by in vivo and in vitro mutagenesis in sugarcane (Saccharum officinarum L.). African J. Biotechnol., 11 (2012) 11686-11692.
  • [3] Paper O. Cadmium-induced response of protein profile and antioxidant enzymes in aquatic macrophytes Myriophyllum spicatum and Ceratophyllum demersum. J. Environ. Stud., 7 (2011) 7: 17-23.
  • [4] Efdi M, Itoh T, Akao Y, Nozawa Y, Koketsu M, Ishihara H. The isolation of secondary metabolites and in vitro potent anti-cancer activity of clerodermic acid from Enicosanthum membranifolium. Bioorg. Med. Chem., 15 (2007) 3667-3671.
  • [5] Efferth T, Herrmann F, Tahrani A, Wink M. Cytotoxic activity of secondary metabolites derived from Artemisia annua L. towards cancer cells in comparison to its designated active constituent artemisinin. Phytomedicine, 18 (2011) 959-969.
  • [6] Markiewicz-Żukowska R, Borawska MH, Fiedorowicz A, Naliwajko SK, Sawicka D, Car H. Propolis changes the anticancer activity of temozolomide in U87MG human glioblastoma cell line. BMC Complement. Altern. Med., 13 (2013) 50.
  • [7] Khan RS, Senthi M, Rao PC, Basha A, Alvala M, Tummuri D, Masubuti H, Fujimoto Y, Begum AS. Cytotoxic constituents of Abutilon indicum leaves against U87MG human glioblastoma cells. Nat. Prod. Res., 29 (2015) 1069-1073.
  • [8] Nash TH. Lichen Biology. New York: Cambridge University Press 2008; 486.
  • [9] Öztürk A, Aslan A. Likenlerin ekonomik özellikleri ve Kuzeydoğu Anadolu’dan bazı liken türleri. Yüzüncü Yıl Üniversitesi Fen Edeb. Fakültesi Fen Bilim. Derg., 2 (1991) 27-42.
  • [10] Ari F, Ulukaya E, Oran S, Celikler S, Ozturk S, Ozel MZ. Promising anticancer activity of a lichen, Parmelia sulcata Taylor, against breast cancer cell lines and genotoxic effect on human lymphocytes. Cytotechnology, 67 (2015) 531-543.
  • [11] Singh N, Nambiar D, Kale RK, Singh RP. Usnic acid inhibits growth and induces cell cycle arrest and apoptosis in human lung carcinoma A549 cells. Nutr. Cancer, 65 (2013) 36-43.
  • [12] O’Neill MA, Mayer MM, Murray KE, Rolim-Santos HML, Santos-Magalhães NS, Thompson AM, Appleyard VCL. Does usnic acid affect microtubules in human cancer cells? Brazilian J. Biol., 70 (2010) 659–664.
  • [13] Yildirim E, Emsen B, Aslan A, Bulak Y, Ercisli S. Insecticidal activity of lichens against the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Egypt. J. Biol. Pest Control, 22 (2012) 151-156.
  • [14] Emsen B, Bulak Y, Yildirim E, Aslan A, Ercisli S. Activities of two major lichen compounds, diffractaic acid and usnic acid against Leptinotarsa decemlineata Say, 1824 (Coleoptera: Chrysomelidae). Egypt. J. Biol. Pest Control, 22 (2012) 5-10.
  • [15] Emsen B, Aslan A, Yildirim E, Ercisli S. Toxicity effects of some lichen species extracts against the colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Egypt. J. Biol. Pest Control, 23 (2013) 193-199.
  • [16] Grujičić D, Stošić I, Kosanić M, Stanojković T, Ranković B, Milošević-Djordjević O. Evaluation of in vitro antioxidant, antimicrobial, genotoxic and anticancer activities of lichen Cetraria islandica. Cytotechnology, 66 (2014) 803-813.
  • [17] Yücel O, Odabaşoǧlu F, Güllüce M, Çalik ZZ, Çakir A, Aslan A, Yazici K, Halici M. Antioxidant and antimicrobial properties of a lichen species, Cladonia rangiformis growing in Turkey. Turkish J. Pharm. Sci., 4 (2007) 101-109.
  • [18] Huneck S. The significance of lichens and their metabolites. Naturwissenschaften, 86 (1999) 559-570.
  • [19] Kirmizigul S, Koz O, Boke N. Constituents of apolar extracts including essential fatty acids of some Turkish lichens. Chem. Nat. Compd., 43 (2007) 462-464.
  • [20] Agar G, Gulluce M, Aslan A, Bozari S, Karadayi M, Orhan F. Mutation preventive and antigenotoxic potential of methanol extracts of two natural lichen. J. Med. Plants Res., 4 (2010) 2132-2137.
  • [21] Einarsdóttir E, Groeneweg J, Björnsdóttir GG, Harethardottir G, Omarsdóttir S, Ingólfsdóttir K, Ogmundsdóttir HM. Cellular mechanisms of the anticancer effects of the lichen compound usnic acid. Planta Med., 76 (2010) 969–974.
  • [22] Wirth V. Die Flechten Baden Württembergs. Württembergs, vol. 1-2. Stuttgart: Ulmer 1995; 1006.
  • [23] Purvis OW, Coppins BJ, Hawksworth DL, James PW, Moore DM. The Lichen Flora of Great Britain and Ireland. London: Natural History Museum Publications in Association with the British Lichen Society 1992; 710.
  • [24] Berridge M V, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol. Annu. Rev., 11 (2005) 127-152.
  • [25] Haslam G, Wyatt D, Kitos PA. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology, 32 (2000) 63-75.
  • [26] Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem., 37 (2004) 277–285.
  • [27] Erel O. A new automated colorimetric method for measuring total oxidant status. Clin. Biochem., 38 (2005) 1103-1111.
  • [28] Gan W, Nie B, Shi F, Xu XM, Qian JC, Takagi Y, Hayakawa H, Sekiguchi M, Cai JP. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: urinary 8-oxoguanosine as a novel biomarker of aging. Free Radic. Biol. Med., 52 (2012) 1700-1707.
  • [29] Emsen B, Turkez H, Togar B, Aslan A. Evaluation of antioxidant and cytotoxic effects of olivetoric and physodic acid in cultured human amnion fibroblasts. Hum. Exp. Toxicol., 36 (2017) 376-385.
  • [30] Bucar F, Schneider I, Ögmundsdóttir H, Ingólfsdóttir K. Anti-proliferative lichen compounds with inhibitory activity on 12(S)-HETE production in human platelets. Phytomedicine , 11 (2004) 602-606.
  • [31] Celenza G, Segatore B, Setacci D, Perilli M, Brisdelli F, Bellio P, Piovano M, Garbarino JA, Amicosante G, Nicoletti M. Antibacterial activity of selected metabolites from Chilean lichen species against methicillin-resistant staphylococci. Nat. Prod. Res., 27 (2013) 1528-1531.
  • [32] Lauinger IL, Vivas L, Perozzo R, Stairiker C, Tarun A, Zloh M, Zhang X, Xu H, Tonge PJ, Franzblau SG, Pham DH, Esguerra C V., Crawford AD, Maes L, Tasdemir D. Potential of lichen secondary metabolites against Plasmodium liver stage parasites with FAS-II as the potential target. J. Nat. Prod., 76 (2013) 1064-1070.
  • [33] Brandao LFG, Alcantara GB, Matos MDFC, Bogo D, Freitas DDS, Oyama NM, Honda NK. Cytotoxic evaluation of phenolic compounds from lichens against melanoma cells. Chem. Pharm. Bull. (Tokyo), 61 (2013) 176-183.
  • [34] Tokur O, Aksoy A. In vitro sitotoksisite testleri. Harran Üniversitesi Vet. Fakültesi Derg., 6 (2017) 112-118.
  • [35] Aydin E, Turkez H. Effects of lichenic extracts (Bryoria capillaris, Peltigera rufescens and Xanthoria elegans) on human blood cells: A cytogenetic and biochemical study. Fresenius Environ. Bull., 20 (2011) 2992-2998.
  • [36] Turkez H, Aydin E, Aslan A. Xanthoria elegans (Link) (lichen) extract counteracts DNA damage and oxidative stress of mitomycin C in human lymphocytes. Cytotechnology ,64 (2012) 679-686.
  • [37] Emsen B, Aslan A, Togar B, Turkez H. In vitro antitumor activities of the lichen compounds olivetoric, physodic and psoromic acid in rat neuron and glioblastoma cells. Pharm. Biol., 54 (2016) 1748-1762.
  • [38] Ceker S, Orhan F, Kizil HE, Alpsoy L, Gulluce M, Aslan A, Agar G. Genotoxic and antigenotoxic potentials of two Usnea species. Toxicol. Ind. Health, 32 (2015) 990-999.
  • [39] Alpsoy L, Orhan F, Nardemir G, Agar G, Gulluce M, Aslan A. Antigenotoxic potencies of a lichen species, Evernia prunastri. Toxicol. Ind. Health, 31 (2015) 153-161.
  • [40] Behera BC, Mahadik N, Morey M. Antioxidative and cardiovascular-protective activities of metabolite usnic acid and psoromic acid produced by lichen species Usnea complanata under submerged fermentation. Pharm. Biol., 50 (2012) 968-979.
  • [41] Sepulveda B, Chamy MC, Piovano M, Areche C. Lichens: Might be considered as a source of gastroprotective molecules? J. Chil. Chem. Soc., 58 (2013) 1750-1752.
Toplam 41 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Bölüm Natural Sciences
Yazarlar

Buğrahan Emsen

Ali Aslan

Abdullah Kaya

Yayımlanma Tarihi 16 Mart 2018
Gönderilme Tarihi 12 Temmuz 2017
Kabul Tarihi 30 Kasım 2017
Yayımlandığı Sayı Yıl 2018Cilt: 39 Sayı: 1

Kaynak Göster

APA Emsen, B., Aslan, A., & Kaya, A. (2018). Cladonia furcata (Huds.) Schrad.’nın İnsan Periferal Lenfositleri Üzerindeki Sitotoksik, Genotoksik ve Oksidatif Etkileri. Cumhuriyet Science Journal, 39(1), 169-180. https://doi.org/10.17776/csj.405735