Leccinum vulpinum Watling induces DNA damage, decreases cell proliferation and induces apoptosis on the human MCF-7 breast cancer cell line

Food and Chemical Toxicology

Volumn 90, Issue , 2016, Pages 45-54

  Reis, Filipa S ^a,b,c,d   Sousa, Diana ^a,b   Barros, Lillian ^c   Martins, Anabela ^c   Morales, Patricia ^d   Ferreira, Isabel C F R ^c   Vasconcelos, M Helena ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Antitumour potential; Apoptosis; Bioactive compounds; DNA damage; Mushrooms; Phenolic extract

Indexed keywords

4 HYDROXYBENZOIC ACID; CELL DNA; CINNAMIC ACID; FUNGAL EXTRACT; GALLIC ACID; LECCINUM VULPINUM EXTRACT; PROTOCATECHUIC ACID; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DRUG IDENTIFICATION; DRUG ISOLATION; DRUG STRUCTURE; EDIBLE MUSHROOM; HUMAN; HUMAN CELL; LECCINUM VULPINUM; MCF 7 CELL LINE; AGARICALES; BREAST NEOPLASMS; CHEMISTRY; DRUG EFFECTS; FEMALE; FRUITING BODY; MCF-7 CELL LINE;

AGARICALES; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BREAST NEOPLASMS; CELL PROLIFERATION; DNA DAMAGE; FEMALE; FRUITING BODIES, FUNGAL; HUMANS; MCF-7 CELLS;

EID: 84957628785     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2016.02.005     Document Type: Article

References (70)

1. Ahn W.S., Kim D.J., Chae G.T., Lee J.M., Bae S.M., Sin J.I., Kim Y.W., Namkoong S.E., Lee I.P. Natural killer cell activity and quality of life were improved by consumption of a mushroom extract, Agaricus blazei Murill Kyowa, in gynecological cancer patients undergoing chemotherapy. Int. J. Gynecol. Cancer 2004, 14:589-594.
2. Azevedo C.M.G., Afonso C.M.M., Sousa D., Lima R.T., Vasconcelos M.H., Pedro M., Barbosa J., Corrêa A.G., Reis S., Pinto M.M.M. Multidimensional optimization of promising antitumor xanthone derivatives. Bioorg. Med. Chem. 2013, 21:2941-2959.
3. Cancer Research UK Cancer Statistics Report - Cancer Incidence and Mortality in the UK, September 2014 (Incidence 2011, Mortality 2012) 2014, Available at:, (accessed 02.02.16.). http://www.cancerresearchuk.org/.
4. Chabner B.A., Longo D.L. Cancer chemotherapy and Biotherapy: Principles and Practice 2011, Lippincott Williams & Wilkins, Philadelphia.
5. Chaitanya G.V., Alexander J.S., Babu P.P. PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal. 2010, 8:31.
6. Charvet C., Wissler M., Brauns-Schubert P., Wang S.-J., Tang Y., Sigloch F.C., et al. Phosphorylation of Tip60 by GSK-3 determines the induction of PUMA and apoptosis by p53. Mol. Cell 2011, 42:584-596.
7. Chen D.M., Bastias B.A., Taylor A.F.S., Cairney J.W.G. Identification of laccase-like genes in ectomycorrhizal basidiomycetes and transcriptional regulation by nitrogen in Piloderma byssinum. New Phytol. 2003, 157:547-554.
8. Chen D.M., Taylor A.F.S., Burke R.M., Cairney J.W.G. Identification of genes for lignin peroxidases and manganese peroxidases in ectomycorrhizal fungi. New Phytol. 2001, 152:151-158.
9. Cheung P.C.K. The nutritional and health benefits of mushrooms. Nutr. Bull. 2010, 35:292-299.
10. dos Santos T., Oliveira M., Sousa D., Lima R.T., Martins A., Ferreira I.C.F.R., Vasconcelos M.H. Suillus luteus methanolic extract inhibits proliferation and increases expression of p-H2A.X in a non-small cell lung cancer cell line. J. Funct. Foods 2014, 6:100-106.
11. dos Santos T., Tavares C., Sousa D., Vaz J.A., Calhelha R.C., Martins A., Almeida G.M., Ferreira I.C.F.R., Vasconcelos M.H. Suillus luteus methanolic extract inhibits cell growth and proliferation of a colon cancer cell line. Food Res. Int. 2013, 53:476-481.
12. Ekmekcioglu C., Feyertag J., Marktl W. Cinnamic acid inhibits proliferation and modulates brush border membrane enzyme activities in Caco-2 cells. Cancer Lett. 1998, 128:137-144.
13. Ellis M.B., Ellis J.P. Fungi without Gills (Hymenomycetes and Gasteromycetes): an Identification Handbook 1990, Chapman and Hall, London.
14. Ferguson H.A., Marietta P.M., Van Den Berg C.L. UV-induced apoptosis is mediated independent of caspase-9 in MCF-7 cells a model for cytochrome c resistance. J. Biol. Chem. 2003, 278:45793-45800.
15. Ferreira I.C.F.R., Barros L., Abreu R.M.V. Antioxidants in wild mushrooms. Curr. Med. Chem. 2009, 16:1543-1560.
16. Ferreira I.C.F.R., Vaz J.A., Vasconcelos M.H., Martins A. Compounds from wild mushrooms with antitumor potential. Anticancer Agents Med. Chem. 2010, 10:424-436.
17. Fortes R.C., Novaes M.R., Recôva V.L., Melo A.L. Immunological, hematological, and glycemia effects of dietary supplementation with Agaricus sylvaticus on patients' colorectal cancer. Exp. Biol. Med. 2009, 234:53-62.
18. Fujita N., Nagahashi A., Nagashima K., Rokudai S., Tsuruo T. Acceleration of apoptotic cell death after the cleavage of Bcl-XL protein by caspase-3-like proteases. Oncogene 1998, 17:1295-1304.
19. Heleno S.A., Ferreira I.C.F.R., Calhelha R.C., Esteves A.P., Martins A., Queiroz M.J.R.P. Cytotoxicity of Coprinopsis atramentaria extract, organic acids and their synthesized methylated and glucuronate derivatives. Food Res. Int. 2014, 55:170-175.
20. Hong S.A., Kim K., Nam S.-J., Kong G., Kim M.K. A case-control study on the dietary intake of mushrooms and breast cancer risk among Korean women. Int. J. Cancer 2008, 122:919-923.
21. Huang Y., Hu J., Zheng J., Li J., Wei T., Zheng Z., Chen Y. Down-regulation of the PI3K/Akt signaling pathway and induction of apoptosis in CA46 Burkitt lymphoma cells by baicalin. J. Exp. Clin. Cancer Res. 2012, 31:1-9.
22. Ito K., Nakazato H., Koike A., Takagi H., Saji S., Baba S., Mai M., Sakamoto J.-i., Ohashi Y. Long-term effect of 5-fluorouracil enhanced by intermittent administration of polysaccharide K after curative resection of colon cancer. Int. J. Colorectal Dis. 2004, 19:157-164.
23. Iwański M., Rudawska M. Ectomycorrhizal colonization of naturally regenerating Pinus sylvestris L. seedlings growing in different micro-habitats in boreal forest. Mycorrhiza 2007, 17:461-467.
24. Ji B., Hsu W., Yang J., Hsia T., Lu C., Chiang J., Yang J., Lin C., Lin J., Suen L., Wood W.G., Chung J. Gallic acid induces apoptosis via caspase-3 and mitochondrion-dependent pathways in vitro and suppresses lung xenograft tumor growth in vivo. J. Agr. Food Chem. 2009, 57:7596-7604.
25. Kajstura M., Halicka H.D., Pryjma J., Darzynkiewicz Z. Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete "sub-G1" peaks on DNA content histograms. Cytom. Part A 2007, 71A:125-131.
26. Kaur M., Velmurugan B., Rajamanickam S., Agarwal R., Agarwal C. Gallic acid, an active constituent of grape seed extract, exhibits anti-proliferative, pro-apoptotic and anti-tumorigenic effects against prostate carcinoma xenograft growth in nude mice. Pharm. Res. 2009, 26:2133-2140.
27. Kirsch D.G., Doseff A., Chau B.N., Lim D.S., de Souza-Pinto N.C., Hansford R., Kastan M.B., Lazebnik Y.A., Hardwick J.M. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J. Biol. Chem. 1999, 274:21155-21161.
28. Liang Y., Nylander K.D., Yan C., Schor N.F. Role of caspase 3-dependent Bcl-2 cleavage in potentiation of apoptosis by Bcl-2. Mol. Pharmacol. 2002, 61:142-149.
29. Lima M.J., Sousa D., Lima R.T., Carvalho A.M., Ferreira I.C.F.R., Vasconcelos M.H. Flower extracts of Filipendula ulmaria (L.) maxim inhibit the proliferation of the NCI-H460 tumour cell line. Ind. Crops Prod. 2014, 59:149-153.
30. Lima R.T., Martins L.M., Guimarães J.E., Sambade C., Vasconcelos M.H. Chemosensitization effects of XIAP downregulation in K562 leukemia cells. J. Chemother. 2006, 18:98-102.
31. Lu Y., Jiang F., Jiang H., Wu K., Zheng X., Cai Y., Katakowski M., Chopp M., To S.S. Gallic acid suppresses cell viability, proliferation, invasion and angiogenesis in human glioma cells. Eur. J. Pharmacol. 2010, 641:102-107.
32. Mitomi T., Tsuchiya S., Iijima N., Aso K., Suzuki K., Nishiyama K., Amano T., Takahashi T., Murayama N., Oka H., et al. Randomized, controlled study on adjuvant immunochemotherapy with PSK in curatively resected colorectal cancer. The cooperative study group of surgical adjuvant immunochemotherapy for cancer of colon and rectum (Kanagawa). Dis. Colon Rectum 1992, 35:123-130.
33. Monks A., Scudiero D., Skehan P., Shoemaker R., Paull K., Vistica D., et al. Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumour cell lines. J. Natl. Cancer Inst. 1991, 83:757-766.
34. Nakazato H., Koike A., Saji S., Ogawa N., Sakamoto J. Efficacy of immunochemotherapy as adjuvant treatment after curative resection of gastric cancer. Study group of immunochemotherapy with PSK for gastric cancer. Lancet 1994, 343:1122-1126.
35. Neves M.P., Cidade H., Pinto M., Silva A.M., Gales L., Damas A.M., Lima R.T., Vasconcelos M.H., Nascimento M.S.J. Prenylated derivatives of baicalein and 3,7-dihydroxyflavone: synthesis and study of their effects on tumor cell lines growth, cell cycle and apoptosis. Eur. J. Med. Chem. 2011, 46:2562-2574.
36. Ohwada S., Ikeya T., Yokomori T., Kusaba T., Roppongi T., Takahashi T., Nakamura S., Kakinuma S., Iwazaki S., Ishikawa H., Kawate S., Nakajima T., Morishita Y. Adjuvant immunochemotherapy with oral Tegafur/Uracil plus PSK in patients with stage II or III colorectal cancer: a randomised controlled study. Br. J. Cancer 2004, 90:1003-1010.
37. Öztürk M., Tel-Çayan G., Muhammad A., Terzioğlu P., Duru M.E. Mushrooms: a source of exciting bioactive compounds. Studies in Natural Products Chemistry 2015, 363-456. Elsevier, Amsterdam. F.R.S. Atta-ur-Rahman (Ed.).
38. Palacios I., Lozano M., Moro C., D'Arrigo M., Rostagno M.A., Martínez J.A., García-Lafuente A., Guillamón E., Villares A. Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem. 2011, 128:674-678.
39. Palmeira A., Paiva A., Sousa E., Seca H., Almeida G.M., Lima R.T., Fernandes M.X., Pinto M., Vasconcelos M.H. Insights into the in vitro antitumor mechanism of action of a new pyranoxanthone. Chem. Biol. Drug Des. 2010, 76:43-58.
40. Patel S., Goyal A. Recent developments in mushrooms as anti-cancer therapeutics: a review. 3 Biotech 2012, 2:1-15.
41. Queiroz M.J.R.P., Peixoto D., Calhelha R.C., Soares P., Santos T., Lima R.T., Campos J.F., Abreu R.M.V., Ferreira I.C.F.R., Vasconcelos M.H. Newdi(hetero)arylethers and di(hetero)arylamines in the thieno[3,2-b] pyridineseries: synthesis, growth inhibitory activity on human tumor cell lines and non-tumor cells, effects on cell cycle and on programmed cell death. Eur. J. Med. Chem. 2013, 69:855-862.
42. Reddy T.C., Reddy D.B., Aparna A., Arunasree K.M., Gupta G., Achari C., Reddy G.V., Lakshmipathi V., Subramanyam A., Reddanna P. Anti-leukemic effects of gallic acid on human leukemia K562 cells: downregulation of COX-2, inhibition of BCR/ABL kinase and NF-kB inactivation. Toxicol. Vitro 2012, 26:396-405.
43. Reis F.S., Martins A., Barros L., Ferreira I.C.F.R. Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: a comparative study between in vivo and in vitro samples. Food Chem. Toxicol. 2012, 50:1201-1207.
44. Roos W.P., Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett. 2013, 332:237-248.
45. Roupas P., Keogh J., Noakes M., Margetts C., Taylor P. The role of edible mushrooms in health: evaluation of the evidence. J. Funct. Foods 2012, 4:687-709.
46. Saxén R., Ilus E. Transfer and behaviour of 137Cs in two Finnish lakes and their catchments. Sci. Total Environ. 2008, 394:349-360.
47. Seca H., Lima R.T., Almeida G.M., Sobrinho-Simões M., Bergantim R., Guimarães J.E., Vasconcelos M.H. Effect of miR-128 in DNA damage of HL-60 acute myeloid leukemia cells. Curr. Pharm. Biotechnol. 2014, 15:492-502.
48. Seidel C., Schnekenburger M., Dicato M., Diederich M. Antiproliferative and proapoptotic activities of 4-hydroxybenzoic acid-based inhibitors of histone deacetylases. Cancer Lett. 2014, 343:134-146.
49. Senawong T., Khaopha S., Misuna S., Komaikul J., Senawong G., Wongphakham P., Yunchalard S. Phenolic acid composition and anticancer activity against human cancer cell lines of the commercially available fermentation products of Houttuynia cordata. ScienceAsia 2014, 40:420-427.
50. Sharma V., Anderson D., Dhawan A. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 2012, 17:852-870.
51. Shin A., Kim J., Lim S.-Y., Kim G., Sung M.-K., Lee E.-S., Ro J. Dietary mushroom intake and the risk of breast cancer based on hormone receptor status. Nutr. Cancer 2010, 62:476-483.
52. Spilioti E., Jaakkola M., Tolonen T., Lipponen M., Virtanen V., Chinou I., Kassi E., Karabournioti S., Moutsatsou P. Phenolic acid composition, antiatherogenic and anticancer potential of honeys derived from various regions in Greece. PLOS One 2014, 9:e94860.
53. Torisu M., Hayashi Y., Ishimitsu T., Fujimura T., Iwasaki K., Katano M., Yamamoto H., Kimura Y., Takesue M., Kondo M., et al. Significant prolongation of disease-free period gained by oral polysaccharide K (PSK) administration after curative surgical operation of colorectal cancer. Cancer Immunol. Immunother. 1990, 31:261-268.
54. Tsujitani S., Kakeji Y., Orita H., Watanabe A., Kohnoe S., Baba H., Anai H., Maehara Y., Sugimachi K. Postoperative adjuvant immunochemotherapy and infiltration of dendritic cells for patients with advanced gastric cancer. Anticancer Res. 1992, 12:645-648.
55. Tsujitani S., Saito H., Wakatsuki T., Ikeguchi M., Shirabe K., Morita M., Kakeji Y., Yano T., Maehara Y. Relationship between expression of apoptosis-related proteins and the efficacy of postoperative chemotherapy in patients with T3 gastric cancer. Surg. Today 2012, 42:225-232.
56. Vaaramaa K., Solatie D., Aro L. Distribution of 210Pb and 210Po concentrations in wild berries and mushrooms in boreal forest ecosystems. Sci. Total Environ. 2009, 408:84-91.
57. Varaprasad K., Ravindra S., Reddy N.N., Vimala K., Raju K.M. Design and development of temperature sensitive porous poly (NIPAAm-AMPS) hydrogels for drug release of doxorubicin-a cancer chemotherapy drug. J. Appl. Polym. Sci. J. Appl. Polym. Sci. 2010, 116:3593-3602.
58. Vasconcelos M.H., Beleza S.S., Quirk C., Maia L.F., Sambade C., Guimarães J.E. Limited synergistic effect of antisense oligonucleotides against bcr-abl and transferrin receptor mRNA in leukemic cells in culture. Cancer Lett. 2000, 152:135-143.
59. Vaz J.A., Almeida G.M., Ferreira I.C.F.R., Martins A., Vasconcelos M.H. Clitocybe alexandri extract induces cell cycle arrest and apoptosis in a lung cancer cell line: identification of phenolic acids with cytotoxic potential. Food Chem. 2012, 132:482-486.
60. Vaz J.A., Ferreira I.C.F.R., Tavares C., Almeida G.M., Martins A., Vasconcelos M.H. Suillus collinitus methanolic extract increases p53 expression and causes cell cycle arrest and apoptosis in a breast cancer cell line. Food Chem. 2012, 135:596-602.
61. Vaz J.A., Heleno S.A., Martins A., Almeida G.M., Vasconcelos M.H., Ferreira I.C.F.R. Wild mushrooms Clitocybe alexandri and Lepista inversa: in vitro antioxidant activity and growth inhibition of human tumour cell lines. Food Chem. Toxicol. 2010, 48:2881-2884.
62. Vichai V., Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat. Protoc. 2006, 1:1112-1116.
63. Wasser S.P. Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Appl. Microbiol. Biotechnol. 2011, 89:1323-1332.
64. Wu H. Cell Death Mechanism and Disease 2014, Springer, New York.
65. Yang Y., Zhao S., Song J. Caspase-dependent apoptosis and -independent poly(ADP-ribose) polymerase cleavage induced by transforming growth factor beta1. Int. J. Biochem. Cell Biol. 2004, 36:223-234.
66. Yin M.C., Lin C.C., Wu H.C., Tsao S.M., Hsu C.K. Apoptotic effects of protocatechuic acid in human breast, lung, liver, cervix, and prostate cancer cells: potential mechanisms of action. J. Agric. Food Chem. 2009, 57:6468-6473.
67. Yip E.C.H., Chan A.S.L., Pang H., Tam Y.K., Wong Y.H. Protocatechuic acid induces cell death in HepG2 hepatocellular carcinoma cells through a c-Jun N-terminal kinase-dependent mechanism. Cell Biol. Toxicol. 2006, 22:293-302.
68. You B.R., Moon H.J., Han Y.H., Park W.H. Gallic acid inhibits the growth of HeLa cervical cancer cells via apoptosis and/or necrosis. Food Chem. Toxicol. 2010, 48:1334-1340.
69. Yu J., Sun R., Zhao Z., Wang Y. Auricularia polytricha polysaccharides induce cell cycle arrest and apoptosis in human lung cancer A549 cells. Int. J. Biol. Macromol. 2014, 68:67-71.
70. Zhang M., Huang J., Xie X., Holman C.D.J. Dietary intakes of mushrooms and green tea combine to reduce the risk of breast cancer in Chinese women. Int. J. Cancer 2009, 124:1404-1408.