Journal of Food Measurement and Characterization

, Volume 13, Issue 4, pp 3015–3024 | Cite as

Potent antiproliferative and pro-apoptotic effects of a soluble protein fraction from culinary-medicinal mushroom Lentinus tigrinus on cancer cells

  • Safoora Mohammadnejad
  • Hamid R. PourianfarEmail author
  • Ahmad Drakhshan
  • Isa Jabaleh
  • Majid Rezayi
Original Paper


Lentinus tigrinus is a culinary-medicinal mushroom that possesses nutritious substances and biological activities. This study for the first time reports the anticancer potentiality of a soluble protein fraction of L. tigrinus (designated as LTPp) precipitated with polyethylene glycol 6000 on MCF-7 and PC3 cancerous cell lines. The findings of antiproliferation assays revealed that LTPp caused significant inhibitory effects at concentrations less than 1000 µg/mL on both cell lines. Further microscopic observations confirmed obvious morphological changes caused by LTPp in both cell lines. While LTPp generated an IC50 value of 193.5 ± 25 μg/mL in MCF-7 cells, it was 33.60 ± 9.0 μg/mL in PC3 cells. In addition, the mode of cell death detected by co-staining of V-FITC/PI indicated that LTPp at 70 μg/mL killed approximately 45.00 and 70.00% of MCF-7 and PC3 cells, respectively, through inducing apoptosis in these cells after 6 h of treatment. Altogether, LTPp showed greater antiproliferative and cytotoxic activities against PC3 cells compared with MCF-7 cells (p ≤ 0.05). The data presented here suggest that the LTPp fraction may be considered as a potent anticancer compound, which promisingly warrants further studies to isolate and identify active single protein/peptides.


Lentinus tigrinus Antiproliferative activity Medicinal mushroom Pro-apoptotic effects Soluble protein Polyethylene glycol 



This research was part of the master thesis project of S Mohammadnejad in ACECR-Khorasan Razavi, Kashmar Higher Education Institute, Kashmar, Iran. The study was partially funded by an internal grant to HR Pourianfar from Industrial Fungi Biotechnology Research Department, ACECR- Khorasan Razavi Branch, Iran. The authors appreciate Dr. Alireza Majid Ansari from Motamed Cancer Institute (Breast Cancer Research Center), Tehran-Iran for his kind assistance with the apoptosis analysis.

Compliance with ethical standards

Conflict of interest

There is no conflict of interest. The authors alone are responsible for the content and writing of the paper.


  1. 1.
    S.S. Usmani, G. Bedi, J.S. Samuel, S. Singh, S. Kalra, P. Kumar, A.A. Ahuja, M. Sharma, A. Gautam, G.P. Raghava, PLoS ONE 12, 0181748 (2017)CrossRefGoogle Scholar
  2. 2.
    A. Tyagi, A. Tuknait, P. Anand, S. Gupta, M. Sharma, D. Mathur, A. Joshi, S. Singh, A. Gautam, G.P. Raghava, Nucleic Acids Res. 43, 837–843 (2014)CrossRefGoogle Scholar
  3. 3.
    R. Zhou, Z.K. Liu, Y.N. Zhang, J.H. Wong, T.B. Ng, F. Liu, Science 20(3), 196–219 (2019)Google Scholar
  4. 4.
    T.S. Ivanova, T.A. Krupodorova, V.Y. Barshteyn, A.B. Artamonova, V.A. Shlyakhovenko, Exp. Oncol. 36, 58–66 (2014)PubMedGoogle Scholar
  5. 5.
    J.S.S. Seelan, A. Justo, L.G. Nagy, E.A. Grand, S.A. Redhead, D. Hibbett, Mycologia 107, 460–474 (2015)CrossRefGoogle Scholar
  6. 6.
    B.E. Lechner, V.L. Papinutti, Process Biochem. 41, 594–598 (2006)CrossRefGoogle Scholar
  7. 7.
    R.M.R. Dulay, M.C. Arenas, S.P. Kalaw, R.G. Reyes, E.C. Cabrera, Int. J. Med. Mushrooms 16, 85–94 (2014)CrossRefGoogle Scholar
  8. 8.
    R.M.R. Dulay, S.P. Kalaw, R.G. Reyes, E.C. Cabrera, N.F. Alfonso, Philipp. Agric. Sci. 95, 278–285 (2012)Google Scholar
  9. 9.
    F.S. Reis, E. Pereira, L. Barros, M.J. Sousa, A. Martins, I.C. Ferreira, Molecules 16, 4328–4338 (2011)CrossRefGoogle Scholar
  10. 10.
    C.Y. Ragasa, M.C.S. Tan, M.E. De Castro, M. Mariquit, G.G. Oyong, C.C. Shen, Pharmacogn. J. 10, 1079–1081 (2018)CrossRefGoogle Scholar
  11. 11.
    G. Sadi, B. Emsen, A. Kaya, A. Kocabaş, S. Çınar, D.I. Kartal, Pharmacogn. Mag. 11, 6–18 (2015)CrossRefGoogle Scholar
  12. 12.
    R.M.R. Dulay, K.S. Flores, R.C. Tiniola, D.H.H. Marquez, A.G. Dela Cruz, S.P. Kalaw, R.G. Reyes, Mycosphere 6, 659–666 (2015)CrossRefGoogle Scholar
  13. 13.
    A.G. Zavarzina, A.V. Lisov, A.A. Leontievsky, J. Geophys. Res. 123, 2727–2742 (2018)CrossRefGoogle Scholar
  14. 14.
  15. 15.
    L. Xu, H. Wang, T. Ng, Biomed. Res. Int. (2012). CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    P. He, S. Wu, L. Pan, S. Sun, D. Mao, C. Xu, Food Technol. Biotechnol. 54, 290–295 (2016)CrossRefGoogle Scholar
  17. 17.
    A. Prateep, S. Sumkhemthong, M. Suksomtip, P. Chanvorachote, C. Chaotham, Pharm. Biol. 55, 1792–1799 (2017)CrossRefGoogle Scholar
  18. 18.
    K. Ghosh, J. Phys. Sci. 20, 239–252 (2015)Google Scholar
  19. 19.
    V. Pushparajah, A. Fatima, C.H. Chong, T.Z. Gambule, C.J. Chan, S.T. Ng, C.S. Tan, S.Y. Fung, S.S. Lee, N.H. Tan, R.L.H. Lim, Sci. Rep. (2016). CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    E.C. Ooi, F. Liu, Curr. Med. Chem. 7, 715–729 (2000)CrossRefGoogle Scholar
  21. 21.
    S.H. Shahtahmasebi, H.R. Pourianfar, S.H. Rezaeian, J. Janpoor, Int. J. Farm. Allied Sci. 6, 149–153 (2017)CrossRefGoogle Scholar
  22. 22.
    S.H. Shahtahmasebi, H.R. Pourianfar, V. Mahdizadeh, S.A. Fazeli, M.A. Amoozegar, S.H. Nasr, S.S. Zabihi, S.H. Rezaeian, K.H. Malekzadeh, J. Janpoor, Curr. Res. Environ. Appl. Mycol. 8, 606–623 (2018)CrossRefGoogle Scholar
  23. 23.
    A. Tarafdar, N.C. Shahi, A. Singh, R. Sirohi, J. Food Qual. (2017). CrossRefGoogle Scholar
  24. 24.
    W. Liu, Z. Huang, P. Li, J. Xia, B. Chen, J. Exp. Mar. Biol. Ecol. 418, 24–29 (2012)CrossRefGoogle Scholar
  25. 25.
    M.M. Bradford, Anal. Biochem. 72, 248–254 (1976)CrossRefGoogle Scholar
  26. 26.
    O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall, J. Biol. Chem. 193, 265–275 (1951)Google Scholar
  27. 27.
    S. Rezaeian, H.R. Pourianfar, Food Measure. 12, 2377–2384 (2019)CrossRefGoogle Scholar
  28. 28.
    H.R. Pourianfar, K. Kirk, L. Grollo, Virusdisease 25, 277–284 (2014)CrossRefGoogle Scholar
  29. 29.
    M.M. Hosseini, A. Karimi, M. Behroozaghdam, M.A. Javidi, S. Ghiasvand, A. Bereimipour, H. Aryan, F. Nassiri, E. Jangholi, World Neurosurg. 108, 94–100 (2017)CrossRefGoogle Scholar
  30. 30.
    J. Manjunathan, N. Subbulakshmi, R. Shanmugapriya, V. Kaviyarasan, Int. J. Biodivers. Conserv. 3, 386–388 (2011)Google Scholar
  31. 31.
    A. Braaksma, D.J. Schaap, Postharvest Biol. Technol. 7, 119–127 (1996)CrossRefGoogle Scholar
  32. 32.
    A.A. Fisher, Contact Dermat. 4, 135–138 (1978)CrossRefGoogle Scholar
  33. 33.
    G. Liu, Y. Li, L. Yang, Y. Wei, X. Wang, Z. Wang, L. Tao, RSC Adv. 7, 18252–18259 (2017)CrossRefGoogle Scholar
  34. 34.
    M.S. Spitzer, B.W. Thilo, A. Sierra, E. Yoeruek, S. Peters, S.H. Fahle, K.U.B. Schmidt, P. Szurman, Br. J. Ophthalmol. 90, 1316–1321 (2006)CrossRefGoogle Scholar
  35. 35.
    K. Tanaka, S. Ishikawa, Y. Matsui, T. Kawanishi, M. Tamesada, N. Harashima, M. Harada, Cancer Immunol. Immunother. 61, 2143–2152 (2012)CrossRefGoogle Scholar
  36. 36.
    B. Yuan, L. Zhao, K. Rakariyatham, Y. Han, Z. Gao, B.M. Kimatu, Q. Hu, H. Xiao, Food Funct. 8, 2175–2183 (2017)CrossRefGoogle Scholar
  37. 37.
    J.Y. Wu, C.H. Chen, W.H. Chang, K.T. Chung, Y.W. Liu, F.J. Lu, C.H. Chen, Evid. Based Complement. Altern. Med. (2011). CrossRefGoogle Scholar
  38. 38.
    L. Yu, D.G. Fernig, J.A. Smith, J.D. Milton, J.M. Rhodes, Cancer Res. 53, 4627–4632 (1993)PubMedGoogle Scholar
  39. 39.
    Y. Sun, T. Yin, X.H. Chen, G. Zhang, R.B. Curtis, Z.H. Lu, J.H. Jiang, Int. J. Med. Mushrooms 13(2), 121–130 (2011)CrossRefGoogle Scholar
  40. 40.
    S.K. Sharma, N.S. Atri, Curr. Res. Environ. Appl. Mycol. 4, 11–32 (2014)CrossRefGoogle Scholar
  41. 41.
    S. Jiang, Y. Chen, M. Wang, Y. Yin, Y. Pan, B. Gu, G. Yu, Y. Li, B.H.C. Wong, Y. Liang, H. Sun, Biochem. J. 443, 369–378 (2012)CrossRefGoogle Scholar
  42. 42.
    C.I. Ukaegbu, S.R. Shah, H.A. Hamid, Z. Normaiza, O.R. Alara, Food Measure. (2018). CrossRefGoogle Scholar
  43. 43.
    D.N. Pegler, Kew Bull Addit Ser. 10, 1–281 (1983)Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant ProtectionAcademic Center for Education, Culture and Research (ACECR)-Khorasan Razavi, Kashmar Higher Education InstituteKashmarIran
  2. 2.Industrial Fungi Biotechnology Research Department, Research Institute for Industrial BiotechnologyAcademic Center for Education, Culture and Research (ACECR)- Khorasan Razavi BranchMashhadIran
  3. 3.Medical Toxicology Research CenterMashhad University of Medical SciencesMashhadIran
  4. 4.Department of Medical Biotechnology and Nanotechnology, School of MedicineMashhad University of Medical SciencesMashhadIran

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