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References

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    Pubmed CrossRef
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    Pubmed CrossRef
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    Pubmed CrossRef
  21. P hosri S, J angpromma N, P atramanon R, K ongyingyoes B , Mahakunakorn P, Klaynongsruang S. 2017. Protective effect of crocodile hemoglobin and whole blood against hydrogen peroxide-induced oxidative damage in human lung fibroblasts (MRC-5) and inflammation in mice. Inflammation. 40: 205-220.
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  33. Anunthawan T, de la Fuente-Núñez C, Hancock REW, Klaynongsruang S. 2015. Cationic amphipathic peptides KT2 and RT2 are taken up into bacterial cells and kill planktonic and biofilm bacteria. Biochim. Biophys. Acta 1848: 1352-1358.
    Pubmed CrossRef
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    Pubmed CrossRef
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    Pubmed CrossRef
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    Pubmed CrossRef
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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(6): 1007-1021

Published online June 28, 2018 https://doi.org/10.4014/jmb.1712.12002

Copyright © The Korean Society for Microbiology and Biotechnology.

Siamese Crocodile White Blood Cell Extract Inhibits Cell Proliferation and Promotes Autophagy in Multiple Cancer Cell Lines

Santi Phosri 1, 2, Nisachon Jangpromma 2, 3, Leng Chee Chang 4, Ghee T. Tan 4, Supakit Wongwiwatthananukit 5, Surachai Maijaroen 2, 6, Preeyanan Anwised 2, Wisarut Payoungkiattikun 2 and Sompong Klaynongsruang 2, 6*

1Office of Education, Faculty of Engineering, Burapha University, Chonburi 20131, Thailand, 2Protein and Proteomics Research Center for Commercial and Industrial Purposes (ProCCI), Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand, 3Office of the Dean, Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand, 4Department of Pharmaceutical Sciences, College of Pharmacy, University of Hawaii at Hilo, Hilo HI 96720, United States, 5Department of Pharmacy Practice, College of Pharmacy, University of Hawaii at Hilo, Hilo HI 96720, United States, 6Department of Biochemistry, Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand

Received: December 4, 2017; Accepted: March 31, 2018

Abstract

Cancer represents one of the most significant threats to human health on a global scale. Hence,
the development of effective cancer prevention strategies, as well as the discovery of novel
therapeutic agents against cancer, is urgently required. In light of this challenge, this research
aimed to evaluate the effects of several potent bioactive peptides and proteins contained in
crocodile white blood cell extract (cWBC) against LU-1, LNCaP, PC-3, MCF-7, and CaCo-2
cancer cell lines. The results demonstrate that 25, 50, 100, and 200 μg/ml cWBC exhibits a
strong cytotoxic effect against all investigated cell lines (IC50 70.34−101.0 μg/ml), while
showing no signs of cytotoxicity towards noncancerous Vero and HaCaT cells. Specifically,
cWBC treatment caused a significant reduction in the cancerous cells’ colony forming ability.
A remarkable suppression of cancerous cell migration was observed after treatment with
cWBC, indicating potent antimetastatic properties. The mechanism involved in the cancer cell
cytotoxicity of cWBC may be related to apoptosis induction, as evidenced by typical apoptotic
morphology features. Moreover, certain cWBC concentrations induced significant
overproduction of ROS and significantly inhibited the S-G2/M transition in the cancer cell. The
molecular mechanisms of cWBC in apoptosis induction were to decrease Bcl-2 and XIAP
expression levels and increase the expression levels of caspase-3, caspase-8, and p53. These led
to a decrease in the expression level of the cell cycle-associated gene cyclin-B1 and the arrest of
cell population growth. Consequently, these findings demonstrate the prospect of the use of
cWBC for cancer therapy.

Keywords: Antitumor, breast cancer, colorectal cancer, Crocodylus siamensis, lung cancer, prostate cancer

References

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    CrossRef
  2. Yach D, Hawkes C, Gould CL, Hofman KJ. 2004. The global burden of chronic diseases: overcoming impediments to prevention and control. JAMA. 291: 2616-2622.
    Pubmed CrossRef
  3. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. 2015. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136: E359-E386.
    Pubmed CrossRef
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    Pubmed
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    Pubmed CrossRef
  7. P andey S, W alpole C , Cabot P , JS haw P N, B atra J , Hewavitharana AK. 2017. Selective anti-proliferative activities of Carica papaya leaf juice extracts against prostate cancer. Biomed. Pharmacother. 89: 515-523.
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  9. Patathananone S, Thammasirirak S, Daduang J, Chung J, Temsiripong Y, Daduang S. 2016. Inhibition of HeLa cells metastasis by bioactive compounds in crocodile (Crocodylus siamensis) white blood cells extract. Environ. Toxicol. 31:1329-1336.
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  21. P hosri S, J angpromma N, P atramanon R, K ongyingyoes B , Mahakunakorn P, Klaynongsruang S. 2017. Protective effect of crocodile hemoglobin and whole blood against hydrogen peroxide-induced oxidative damage in human lung fibroblasts (MRC-5) and inflammation in mice. Inflammation. 40: 205-220.
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    Pubmed CrossRef
  23. Risso A. 2000. Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J. Leukoc. Biol. 68:785-792.
    Pubmed
  24. Mehta RG, Pezzuto JM. 2002. Discovery of cancer preventive agents from natural products: from plants to prevention. Curr. Oncol. Rep. 4: 478-486.
    Pubmed CrossRef
  25. Chen J, Zhou M, Zhang Q, Xu J, Ouyang J. 2015. Anticancer effect and apoptosis induction of gambogic acid in human leukemia cell line K562 in vitro. Med. Sci. Monit. 21: 1604-1610.
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    Pubmed CrossRef
  27. Liu E, Du X, Ge R, Liang T, Niu Q, Li Q. 2013. Comparative toxicity and apoptosis induced by diorganotins in rat
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    Pubmed CrossRef
  29. Häcker G. 2000. The morphology of apoptosis. Cell Tissue Res. 301: 5-17.
    Pubmed CrossRef
  30. Ameziane El Hassani R, Dupuy C. 2013. Detection of intracellular reactive oxygen species (CM-H2DCFDA). Bio Protoc. 3: e313.
    CrossRef
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    Pubmed CrossRef
  32. Woo CC, Loo SY, Gee V, Yap CW, Sethi G, Kumar AP, et al. 2011. Anticancer activity of thymoquinone in breast cancer cells: possible involvement of PPAR-γ pathway. Biochem. Pharmacol. 82: 464-475.
    Pubmed CrossRef
  33. Anunthawan T, de la Fuente-Núñez C, Hancock REW, Klaynongsruang S. 2015. Cationic amphipathic peptides KT2 and RT2 are taken up into bacterial cells and kill planktonic and biofilm bacteria. Biochim. Biophys. Acta 1848: 1352-1358.
    Pubmed CrossRef
  34. Barksdale SM, Hrifko EJ, van Hoek ML. 2017. Cathelicidin antimicrobial peptide from Alligator mississippiensis has antibacterial activity against multi-drug resistant Acinetobacter baumanii and Klebsiella pneumoniae. Dev. Comp. Immunol. 70:135-144.
    Pubmed CrossRef
  35. Hao J, Li Y-W, Xie M-Q, Li A-X. 2012. Molecular cloning, recombinant expression and antibacterial activity analysis of hepcidin from Simensis crocodile (Crocodylus siamensis). Comp. Biochem. Physiol. 163: 309-315.
    Pubmed CrossRef
  36. Iwasaki T, Ishibashi J, Tanaka H, Sato M, Asaoka A, Taylor D, et al. 2009. Selective cancer cell cytotoxicity of enantiomeric 9-mer peptides derived from beetle defensins depends on negatively charged phosphatidylserine on the cell surface. Peptides 30: 660-668.
    Pubmed CrossRef
  37. Brandenburg LO, Merres J, Albrecht LJ, Varoga D, Pufe T. 2012. Antimicrobial peptides: multifunctional drugs for different applications. Polymers 4: 539-560.
    CrossRef
  38. Arouri A, Dathe M, Blume A. 2009. Peptide induced demixing in PG/PE lipid mixtures: a mechanism for the specificity of antimicrobial peptides towards bacterial membranes? Biochim. Biophys. Acta 1788: 650-659.
    Pubmed CrossRef
  39. Patathananone S, Thammasirirak S, Daduang J, Chung JG, Temsiripong Y, Daduang S. 2016. Bioactive compounds from crocodile (Crocodylus siamensis) white blood cells induced apoptotic cell death in HeLa cells. Environ. Toxicol. 31: 986-997.
    Pubmed CrossRef
  40. Boohaker RJ, Lee MW, Vishnubhotla P, Perez JM, Khaled AR. 2012. The use of therapeutic peptides to target and to kill cancer cells. Curr. Med. Chem. 19: 3794-3804.
    Pubmed KoreaMed CrossRef
  41. Dia VP, Krishnan HB. 2016. BG-4, a novel anticancer peptide from bitter gourd (Momordica charantia), promotes apoptosis in human colon cancer cells. Sci. Rep. 15: 33532.
    Pubmed KoreaMed CrossRef
  42. Xiao JX, Huang GQ, Zhu CP, Ren DD, Zhang SH. 2007. Morphological study on apoptosis Hela cells induced by soyasaponins. Toxicol. In Vitro 21: 820-826.
    Pubmed CrossRef
  43. Syed Abdul Rahman SN, Abdul Wahab N, Abd Malek SN. 2013. In vitro morphological assessment of apoptosis induced by antiproliferative constituents from the rhizomes of Curcuma zedoaria. Evid. Based Complement. Alternat. Med. 2013: 257108.
    Pubmed KoreaMed CrossRef
  44. Saraste A, Pulkki K. 2000. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res. 45: 528-537.
    CrossRef
  45. Zhang L, Zheng Y, Deng H, Liang L, Peng J. 2014. Aloperine induces G2/M phase cell cycle arrest and apoptosis in HCT116 human colon cancer cells. Int. J. Mol. Med. 33: 1613-1620.
    Pubmed CrossRef
  46. Borhani N, Manoochehri M, Gargari SS, Novin MG, Mansouri A, Omrani MD. 2014. Decreased expression of proapoptotic genes Caspase-8- and BCL2-associated agonist of cell death (BAD) in ovarian cancer. Clin. Ovarian Other Gynecol. Cancer 7: 18-23.
    CrossRef
  47. Nita M, Grzybowski A. 2016. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxid. Med. Cell. Longev. 2016: 3164734.
    Pubmed KoreaMed CrossRef
  48. Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh H, Lleonart ME. 2013. Oxidative stress and cancer: an overview. Ageing Res. Rev. 12: 376-390.
    Pubmed CrossRef
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