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Cytotechnology

, Volume 71, Issue 6, pp 1095–1108 | Cite as

Antitumor effects of seleno-short-chain chitosan (SSCC) against human gastric cancer BGC-823 cells

  • Xiao-dan Dong
  • Juan Yu
  • Fan-qi Meng
  • Ying-ying Feng
  • Hai-yu Ji
  • Anjun LiuEmail author
Original Article
  • 87 Downloads

Abstract

Seleno-short-chain chitosan (SSCC) is a derivative of chitosan. In the present study, we sought to investigate the underlying antitumor mechanism of SSCC on human gastric cancer BGC-823 cells in vitro. MTT assay suggested that SSCC exhibited a dose-dependent inhibitory effect on the proliferation of BGC-823 cells. We found the SSCC-treated cells showed typical morphological characteristics of apoptosis in a dose dependent manner by observing on microscope. Annexin V-FITC/PI double staining and cell cycle assay identified that SSCC could induce BGC-823 cells apoptosis by triggering G2/M phase arrest. Our research provided the first evidence that SSCC could effectively induce the apoptosis of BGC-823 cells via an intrinsic mitochondrial pathway, as indicated by inducing the disruption of mitochondrial membrane potential (MMP), the excessive accumulation of reactive oxidative species (ROS), the increase of Bax/Bcl-2 ratio and the activation of caspase 3, caspase 9 and cytochrome C (Cyt-C) in BGC-823 cells. These combined results clearly indicated that SSCC could induce BGC-823 cells apoptosis by the involvement of mitochondrial signaling pathway, which provided precise experimental evidence for SSCC as a potential agent in the prevention and treatment of human gastric cancer.

Keywords

SSCC Human gastric cancer Cell apoptosis Mitochondrial pathway 

Notes

Compliance with ethical standards

Conflicts of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Bano I, Arshad M, Yasin T, Ghauri MA, Younus M (2017) Chitosan: a potential biopolymer for wound management. Int J Biol Macromol 102:380–383.  https://doi.org/10.1016/j.ijbiomac.2017.04.047 CrossRefPubMedGoogle Scholar
  2. Birkinshaw RW, Czabotar PE (2017) The BCL-2 family of proteins and mitochondrial outer membrane permeabilisation. Semin Cell Dev Biol 72:152–162.  https://doi.org/10.1016/j.semcdb.2017.04.001 CrossRefPubMedGoogle Scholar
  3. Cao H, Xu H, Zhu G, Liu S (2017) Isoquercetin ameliorated hypoxia/reoxygenation-induced H9C2 cardiomyocyte apoptosis via a mitochondrial-dependent pathway. Biomed Pharmacother 95:938–943.  https://doi.org/10.1016/j.biopha.2017.08.128 CrossRefPubMedGoogle Scholar
  4. Chang CC, Hung CM, Yang YR, Lee MJ, Hsu YC (2013) Sulforaphane induced cell cycle arrest in the G2/M phase via the blockade of cyclin B1/CDC2 in human ovarian cancer cells (Article). J Ovarian Res 6:7.  https://doi.org/10.1186/1757-2215-6-41 CrossRefGoogle Scholar
  5. Chen GC, Zhang PY, Huang TT, Yu WQ, Lin J, Li P et al (2013) Polysaccharides from Rhizopus nigricans mycelia induced apoptosis and G2/M arrest in BGC-823 cells (Article). Carbohyd Polym 97:800–808.  https://doi.org/10.1016/j.carbpol.2013.05.068 CrossRefGoogle Scholar
  6. Cheng L, Chen L, Yang Q, Wang Y, Wei X (2018a) Antitumor activity of Se-containing tea polysaccharides against sarcoma 180 and comparison with regular tea polysaccharides and Se-yeast. Int J Biol Macromol 120:853–858.  https://doi.org/10.1016/j.ijbiomac.2018.08.154 CrossRefPubMedGoogle Scholar
  7. Cheng L, Chen L, Yang Q, Wang Y, Wei X (2018b) Antitumor activity of Se-containing tea polysaccharides against sarcoma 180 and comparison with regular tea polysaccharides and Se-yeast. Int J Biol Macromol.  https://doi.org/10.1016/j.ijbiomac.2018.08.154 CrossRefPubMedGoogle Scholar
  8. Cui D, Yan C, Miao J, Zhang X, Chen J, Sun L et al (2018) Synthesis, characterization and antitumor properties of selenium nanoparticles coupling with ferulic acid. Mater Sci Eng C 90:104–112.  https://doi.org/10.1016/j.msec.2018.04.048 CrossRefGoogle Scholar
  9. Endo M, Hasegawa H, Kaneko T, Kanno C, Monma T, Kano M et al (2017) Antitumor activity of selenium compounds and its underlying mechanism in human oral squamous cell carcinoma cells: a preliminary study. J Oral Maxillofac Surg Med Pathol 29:17–23.  https://doi.org/10.1016/j.ajoms.2016.08.006 CrossRefGoogle Scholar
  10. Fan S, Zhang J, Nie W, Zhou W, Jin L, Chen X et al (2017) Antitumor effects of polysaccharide from Sargassum fusiforme against human hepatocellular carcinoma HepG2 cells. Food Chem Toxicol 102:53–62.  https://doi.org/10.1016/j.fct.2017.01.020 CrossRefPubMedGoogle Scholar
  11. Gandin V, Khalkar P, Braude J, Fernandes AP (2018) Organic selenium compounds as potential chemotherapeutic agents for improved cancer treatment. Free Radical Biol Med.  https://doi.org/10.1016/j.freeradbiomed.2018.05.001 CrossRefGoogle Scholar
  12. Grela E, Kozłowska J, Grabowiecka A (2018) Current methodology of MTT assay in bacteria—a review. Acta Histochem 120:303–311.  https://doi.org/10.1016/j.acthis.2018.03.007 CrossRefPubMedGoogle Scholar
  13. He J, Wu Z, Pan D, Guo Y, Zeng X (2017) Effect of selenylation modification on antitumor activity of peptidoglycan from Lactobacillus acidophilus. Carbohyd Polym 165:344–350.  https://doi.org/10.1016/j.carbpol.2017.02.031 CrossRefGoogle Scholar
  14. Jia X, Liu Q, Zou S, Xu X, Zhang L (2015) Construction of selenium nanoparticles/β-glucan composites for enhancement of the antitumor activity. Carbohyd Polym 117:434–442.  https://doi.org/10.1016/j.carbpol.2014.09.088 CrossRefGoogle Scholar
  15. Jia Z-Q, Li S-Q, Qiao W-Q, Xu W-Z, Xing J-W, Liu J-T et al (2018) Ebselen protects mitochondrial function and oxidative stress while inhibiting the mitochondrial apoptosis pathway after acute spinal cord injury. Neurosci Lett 678:110–117.  https://doi.org/10.1016/j.neulet.2018.05.007 CrossRefPubMedGoogle Scholar
  16. Laskar K, Faisal SM, Rauf A, Ahmed A, Owais M (2017) Undec-10-enoic acid functionalized chitosan based novel nano-conjugate: an enhanced anti-bacterial/biofilm and anti-cancer potential. Carbohyd Polym 166:14–23.  https://doi.org/10.1016/j.carbpol.2017.02.082 CrossRefGoogle Scholar
  17. Lee JS, Hong EK (2010) Hericium erinaceus enhances doxorubicin-induced apoptosis in human hepatocellular carcinoma cells. Cancer Lett 297:144–154.  https://doi.org/10.1016/j.canlet.2010.05.006 CrossRefPubMedGoogle Scholar
  18. Li FN, Dong XW, Lin P, Jiang JL (2018) Regulation of Akt/FoxO3a/Skp2 axis is critically involved in berberine-induced cell cycle arrest in hepatocellular carcinoma cells (Article). Int J Mol Sci 19:13.  https://doi.org/10.3390/ijms19020327 CrossRefGoogle Scholar
  19. Liu A et al (2008) Growth inhibition and apoptosis of human leukemia K562 cells induced by seleno-short-chain chitosan. Methods Find Exp Clin Pharmacol 3:181–186CrossRefGoogle Scholar
  20. Liu Y, Sun J, Rao S, Su Y, Li J, Li C et al (2013) Antidiabetic activity of mycelia selenium-polysaccharide from Catathelasma ventricosum in STZ-induced diabetic mice. Food Chem Toxicol 62:285–291.  https://doi.org/10.1016/j.fct.2013.08.082 CrossRefPubMedGoogle Scholar
  21. Liu L, Wang D, Wang J, Ji H, Zhang Y (2015) NOAD, a novel nitric oxide donor, induces G2/M phase arrest and apoptosis in human hepatocellular carcinoma Bel-7402 cells. Toxicol In Vitro 29:1289–1297.  https://doi.org/10.1016/j.tiv.2015.05.003 CrossRefPubMedGoogle Scholar
  22. Liu WB, Xie F, Sun HQ, Meng M, Zhu ZY (2017) Anti-tumor effect of polysaccharide from Hirsutella sinensis on human non-small cell lung cancer and nude mice through intrinsic mitochondrial pathway. Int J Biol Macromol 99:258–264.  https://doi.org/10.1016/j.ijbiomac.2017.02.071 CrossRefPubMedGoogle Scholar
  23. Liu L, Chang X, Zhang Y, Wu C, Li R, Tang L et al (2018) Fluorochloridone induces primary cultured Sertoli cells apoptosis: involvement of ROS and intracellular calcium ions-mediated ERK1/2 activation. Toxicol In Vitro 47:228–237.  https://doi.org/10.1016/j.tiv.2017.12.006 CrossRefPubMedGoogle Scholar
  24. Lü H, Gao Y, Shan H, Lin Y (2014) Preparation and antibacterial activity studies of degraded polysaccharide selenide from Enteromorpha prolifera. Carbohyd Polym 107:98–102.  https://doi.org/10.1016/j.carbpol.2014.02.045 CrossRefGoogle Scholar
  25. Ma Z-J, Lu L, Yang J-J, Wang X-X, Su G, Wang Z-L et al (2018) Lariciresinol induces apoptosis in HepG2 cells via mitochondrial-mediated apoptosis pathway. Eur J Pharmacol 821:1–10.  https://doi.org/10.1016/j.ejphar.2017.12.027 CrossRefPubMedGoogle Scholar
  26. Nagappan A, Park KI, Park HS, Kim JA, Hong GE, Kang SR et al (2012) Vitamin C induces apoptosis in AGS cells by down-regulation of 14-3-3sigma via a mitochondrial dependent pathway. Food Chem 135:1920–1928.  https://doi.org/10.1016/j.foodchem.2012.06.050 CrossRefPubMedGoogle Scholar
  27. Perez MG, Fourcade L, Mateescu MA, Paquin J (2017) Neutral Red versus MTT assay of cell viability in the presence of copper compounds. Anal Biochem 535:43–46.  https://doi.org/10.1016/j.ab.2017.07.027 CrossRefGoogle Scholar
  28. Perumalsamy H, Sankarapandian K, Kandaswamy N, Balusamy SR, Periyathambi D, Raveendiran N (2017) Cellular effect of styrene substituted biscoumarin caused cellular apoptosis and cell cycle arrest in human breast cancer cells. Int J Biochem Cell Biol 92:104–114.  https://doi.org/10.1016/j.biocel.2017.09.019 CrossRefPubMedGoogle Scholar
  29. Pur MRK, Hosseini M, Faridbod F, Ganjali MR, Hosseinkhani S (2018) Early detection of cell apoptosis by a cytochrome C label-Free electrochemiluminescence aptasensor. Sens Actuators B Chem 257:87–95.  https://doi.org/10.1016/j.snb.2017.10.138 CrossRefGoogle Scholar
  30. Qiao Y, Li T, Zheng S, Wang H (2018) The Hippo pathway as a drug target in gastric cancer. Cancer Lett 420:14–25.  https://doi.org/10.1016/j.canlet.2018.01.062 CrossRefPubMedGoogle Scholar
  31. Redza-Dutordoir M, Averill-Bates DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta 1863:2977–2992.  https://doi.org/10.1016/j.bbamcr.2016.09.012 CrossRefPubMedGoogle Scholar
  32. Sawai H, Domae N (2011) Discrimination between primary necrosis and apoptosis by necrostatin-1 in Annexin V-positive/propidium iodide-negative cells. Biochem Biophys Res Commun 411:569–573.  https://doi.org/10.1016/j.bbrc.2011.06.186 CrossRefPubMedGoogle Scholar
  33. Sinha R, Ei-Bayoumy K (2004) Apoptosis is a critical cellular event in cancer chemoprevention and chemotherapy by selenium compounds (Review). Curr Cancer Drug Targets 4:13–28.  https://doi.org/10.2174/1568009043481614 CrossRefPubMedGoogle Scholar
  34. Song F, Zhang L, Yu HX, Lu RR, Bao JD, Tan C et al (2012) The mechanism underlying proliferation-inhibitory and apoptosis-inducing effects of curcumin on papillary thyroid cancer cells. Food Chem 132:43–50.  https://doi.org/10.1016/j.foodchem.2011.10.024 CrossRefPubMedGoogle Scholar
  35. Tao J, Xu J, Chen F, Xu B, Gao J, Hu Y (2018) Folate acid-Cyclodextrin/Docetaxel induces apoptosis in KB cells via the intrinsic mitochondrial pathway and displays antitumor activity in vivo. Eur J Pharm Sci 111:540–548.  https://doi.org/10.1016/j.ejps.2017.10.039 CrossRefPubMedGoogle Scholar
  36. Wang Y, Chen J, Zhang D, Zhang Y, Wen Y, Li L et al (2013) Tumoricidal effects of a selenium (Se)-polysaccharide from Ziyang green tea on human osteosarcoma U-2 OS cells. Carbohyd Polym 98:1186–1190.  https://doi.org/10.1016/j.carbpol.2013.07.022 CrossRefGoogle Scholar
  37. Xiao X, Liu H, Li X (2017) Orlistat treatment induces apoptosis and arrests cell cycle in HSC-3 oral cancer cells. Microb Pathog 112:15–19.  https://doi.org/10.1016/j.micpath.2017.09.001 CrossRefPubMedGoogle Scholar
  38. Xie P, Fujii I, Zhao J, Shinohara M, Matsukura M (2016) A novel polysaccharide derived from algae extract induces apoptosis and cell cycle arrest in human gastric carcinoma MKN45 cells via ROS/JNK signaling pathway. Int J Oncol 49:1561–1568.  https://doi.org/10.3892/ijo.2016.3658 CrossRefPubMedGoogle Scholar
  39. Ya G (2017) A Lentinus edodes polysaccharide induces mitochondrial-mediated apoptosis in human cervical carcinoma HeLa cells. Int J Biol Macromol 103:676–682.  https://doi.org/10.1016/j.ijbiomac.2017.05.085 CrossRefPubMedGoogle Scholar
  40. Zhang CG, Huang JC, Liu T, Li XY (2015) Anticancer effects of bishydroxycoumarin are mediated through apoptosis induction, cell migration inhibition and cell cycle arrest in human glioma cells. J Buon 20:1592–1600PubMedGoogle Scholar
  41. Zhang C, Powell SE, Betel D, Shah MA (2017a) The gastric microbiome and its influence on gastric carcinogenesis: current knowledge and ongoing research. Hematol Oncol Clin North Am 31:389–408.  https://doi.org/10.1016/j.hoc.2017.01.002 CrossRefPubMedGoogle Scholar
  42. Zhang RJ, Shi Y, Zheng J, Mao XM, Liu ZY, Chen QX et al (2017b) Effects of polysaccharides from abalone viscera (Haliotis discus hannai Ino) on MGC 803 cells proliferation. Int J Biol Macromol.  https://doi.org/10.1016/j.ijbiomac.2017.08.055 CrossRefPubMedGoogle Scholar
  43. Zhao Y, Zhang S, Wang P, Fu S, Wu D, Liu A (2017) Seleno-short-chain chitosan induces apoptosis in human non-small-cell lung cancer A549 cells through ROS-mediated mitochondrial pathway. Cytotechnology 69:851–863.  https://doi.org/10.1007/s10616-017-0098-z CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhou J, Zhong X, Lin J, Hong Z (2018) Qianliening capsule promotes mitochondrial pathway mediated the apoptosis of benign prostatic hyperplasia epithelial-1 cells by regulating the miRNA-181a. Int J Gerontol.  https://doi.org/10.1016/j.ijge.2018.04.002 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Xiao-dan Dong
    • 1
    • 2
  • Juan Yu
    • 1
    • 2
  • Fan-qi Meng
    • 1
    • 2
  • Ying-ying Feng
    • 1
    • 2
  • Hai-yu Ji
    • 1
    • 2
  • Anjun Liu
    • 1
    • 3
    Email author
  1. 1.Key Laboratory of Food Nutrition and Safety, Ministry of Education, College of Food Engineering and BiotechnologyTianjin University of Science and TechnologyTianjinChina
  2. 2.QingYunTang Biotech (Beijing) Co., LtdBeijingChina
  3. 3.Tianjin Key Laboratory of Food Nutrition and Safety, School of Food Engineering and Biological TechnologyTianjin University of Science and TechnologyTianjinChina

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