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Research Article | Open Access

Apoptosis of colon cancer CT-26 cells induced polysaccharide from Cyclocarya paliurus and its phosphorylated derivative via intrinsic mitochondrial passway

Liuming XieMingyue Shen( )Rong HuangXuan LiuYue YuHanyu LuJianhua Xie( )
State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang 330047, China

Peer review under responsibility of KeAi Communications Co., Ltd.

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Abstract

In this study, the antitumor properties and the possible molecular mechanisms of Cyclocarya paliurus polysaccharide (CP) and its phosphorylated derivative (P-CP) on CT-26 mouse colon carcinoma cells were investigated. Results found that CP had high inhibition ratio against CT-26 cells. The flow cytometry results found that CP treatment could cause the intracellular acidification, arrest the cell cycle in the S phase and increase reactive oxygen species generation. Additionally, CP treatment triggered mitochondrial membrane potential depolarization and Ca2+ overloading, and broke down the balance of antioxidant system, Na+/K+-ATPase and Ca2+-ATPase. Further analysis found CP induced cell apoptosis through improving the activities of caspase-3 and caspase-9, and increasing the level of cytochrome C. Furthermore, the comparative study of antitumor effect on CT-26 cells displayed that the phosphorylation enhanced antitumor activities of polysaccharides. These results suggest CP is a potential natural therapeutic agent for colon cancer and phosphorylation represents an effective method of enhancing the antitumor activity of CP.

References

[1]

F. Bray, J. Ferlay, I. Soerjomataram, et al., Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries, CA. Cancer J. Clin. 68 (2018) 394-424. https://doi.org/10.3322/caac.21492.

[2]

Y. Zheng, W. Wang, Y. Li, Antitumor and immunomodulatory activity of polysaccharide isolated from Trametes orientalis, Carbohydr. Polym. 131 (2015) 248-254. https://doi.org/10.1016/j.carbpol.2015.05.074.

[3]

L. Herszényi, Z. Tulassay, Epidemiology of gastrointestinal and liver tumors, Eur. Rev. Med. Pharmacol. Sci. 14 (2010) 249-258.

[4]

J. Wu, X. Chen, K. Qiao, et al., Purification, structural elucidation, and in vitro antitumor effects of novel polysaccharides from Bangia fuscopurpurea, Food Sci. Hum. Well. 10 (2021) 63-71. https://doi.org/10.1016/j.fshw.2020.05.003.

[5]

D. Bagchi, M. Bagchi, S. Stchs, et al., Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention, Toxicology 148 (2000) 187-197. https://doi.org/10.1016/S0300-483X(00)00210-9.

[6]

X. Chen, Y. Zhang, Y. Han, et al., Emulsifying properties of polysaccharide conjugates prepared from Chin-Brick tea, J. Agric. Food Chem. 67 (2019) 10165-10173. https://doi.org/10.1021/acs.jafc.9b03161.

[7]

R. He, Y. Zhao, R. Zhao, et al., Antioxidant and antitumor activities in vitro of polysaccharides from E. sipunculoides, Int. J. Biol. Macromol. 78 (2015) 56-61. https://doi.org/10.1016/j.ijbiomac.2015.03.030.

[8]

X. Chen, J. Xie, W. Huang, et al., Comparative analysis of physicochemical characteristics of green tea polysaccharide conjugates and its decolored fraction and their effect on HepG2 cell proliferation, Ind. Crop. Prod. 131 (2019) 243-249. https://doi.org/10.1016/j.indcrop.2019.01.061.

[9]

H. Jiang, J. Dong, S. Jiang, et al., Effect of Durio zibethinus rind polysaccharide on functional constipation and intestinal microbiota in rats, Food Res. Int. 136 (2020) 109316. https://doi.org/10.1016/j.foodres.2020.109316.

[10]

W. Qi, X. Zhou, J. Wang, et al., Cordyceps sinensis polysaccharide inhibits colon cancer cells growth by inducing apoptosis and autophagy flux blockage via mTOR signaling, Carbohydr. Polym. 237 (2020) 116113. https://doi.org/10.1016/j.carbpol.2020.116113.

[11]

X. Chen, X. Xu, L. Zhang, et al., Chain conformation and anti-tumor activities of phosphorylated (1→3)-beta-D-glucan from Poria cocos, Carbohydr. Polym. 78 (2009) 581-587. https://doi.org/10.1016/j.carbpol.2009.05.019.

[12]

H. Zhang, T. Zhao, J. Wang, et al., An amendment to the fine structure of galactoxyloglucan from Tamarind (Tamarindus indica L.) seed, Int. J. Biol. Macromol. 149 (2020) 1189-1197. https://doi.org/10.1016/j.ijbiomac.2020.01.284.

[13]

Z.J. Wang, J.H. Xie, L.J. Kan, et al., Sulfated polysaccharides from Cyclocarya paliurus reduce H2O2-induced oxidative stress in RAW264.7 cells, Int. J. Biol. Macromol. 80 (2015) 410-417. https://doi.org/10.1016/j.ijbiomac.2015.06.031.

[14]

J. Wang, A. Bao, Q. Wang, et al., Sulfation can enhance antitumor activities of Artemisia sphaerocephala polysaccharide in vitro and vivo, Int. J. Biol. Macromol. 107 (2018) 502-511. https://doi.org/10.1016/j.ijbiomac.2017.09.018.

[15]

J. Xie, X. Liu, M. Shen, et al., Purification, physicochemical characterisation and anticancer activity of a polysaccharide from Cyclocarya paliurus leaves, Food Chem. 136 (2013) 1453-1460. https://doi.org/10.1016/j.foodchem.2012.09.078.

[16]

L. Xie, M. Shen, P. Wen, et al., Preparation, characterization, antioxidant activity and protective effect against cellular oxidative stress of phosphorylated polysaccharide from Cyclocarya paliurus, Food Chem. Toxicol. 145 (2020) 111754. https://doi.org/10.1016/j.fct.2020.111754.

[17]

K. Ming, M. He, L. Su, et al., The inhibitory effect of phosphorylated Codonopsis pilosula polysaccharide on autophagosomes formation contributes to the inhibition of duck hepatitis A virus replication, Poult. Sci. 99 (2020) 2146-2156. https://doi.org/10.1016/j.psj.2019.11.060.

[18]

H.J. Kim, J.Y. Lee, T.H. Kim, et al., Radioisotope and anticancer agent incorporated layered double hydroxide for tumor targeting theranostic nanomedicine, Appl. Clay Sci. 186 (2020) 105454. https://doi.org/10.1016/j.clay.2020.105454.

[19]

J. Yang, W. Chen, B. Zhang, et al., Lon in maintaining mitochondrial and endoplasmic reticulum homeostasis, Arch. Toxicol. 92 (2018) 1913-1923. https://doi.org/10.1007/s00204-018-2210-3.

[20]

X.Y. Wang, A.N. Gao, Y.D. Jiao, et al., Antitumor effect and molecular mechanism of antioxidant polysaccharides from Salvia miltiorrhiza Bunge in human colorectal carcinoma LoVo cells, Int. J. Biol. Macromol. 108 (2018) 625-634. https://doi.org/10.1016/j.ijbiomac.2017.12.006.

[21]

K.A. Foster, F. Galeffi, F.J. Gerich, et al., Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration, Prog. Neurobiol. 79 (2006) 136-171. https://doi.org/10.1016/j.pneurobio.2006.07.001.

[22]

J. Yu, H. Ji, X. Dong, et al., Apoptosis of human gastric carcinoma MGC-803 cells induced by a novel Astragalus membranaceus polysaccharide via intrinsic mitochondrial pathways, Int. J. Biol. Macromol. 126 (2018) 811-819. https://doi.org/10.1016/j.ijbiomac.2018.12.268.

[23]

M. Jin, K. Zhao, Q. Huang, et al., Structural features and biological activities of the polysaccharides from Astragalus membranaceus, Int. J. Biol. Macromol. 64 (2014) 257-266. https://doi.org/10.1016/j.ijbiomac.2013.12.002.

[24]

Y, Liang, X. Chuan, J. Pan, et al., Structural characterization and in vitro antitumor activity of a polysaccharide from Artemisia annua L. (Huang Huahao), Carbohydr. Polym. 213 (2019) 361-369. https://doi.org/10.1016/j.carbpol.2019.02.081.

[25]

J. Wu, J. Zhou, Y. Lang, et al., A polysaccharide from Armillaria mellea exhibits strong in vitro anticancer activity via apoptosis-involved mechanisms, Int. J. Biol. Macromol. 51 (2012) 663-667. https://doi.org/10.1016/j.ijbiomac.2012.06.040.

[26]

B.E. Phillips, S. Kenneth, L. Sarah, et al., Effect of colon cancer and surgical resection on skeletal muscle mitochondrial enzyme activity in colon cancer patients: a pilot study, J. Cachexia. Sarcopenia. Muscle 4 (2013) 71-77. https://doi.org/10.1007/s13539-012-0073-7.

[27]

Y. Li, L. Liu, Y. Niu, et al., Modified apple polysaccharide prevents against tumorigenesis in a mouse model of colitis-associated colon cancer: role of galectin-3 and apoptosis in cancer prevention, Eur. J. Nutr. 51 (2012) 107-117. https://doi.org/10.1016/j.nutres.2013.06.004.

[28]

Y. Masuda, K. Ito, M. Konishi, et al., A polysaccharide extracted from Grifola frondosa enhances the anti-tumor activity of bone marrow-derived dendritic cell-based immunotherapy against murine colon cancer, Cancer Immunol. Immunother. 59 (2010) 1531-1541. https://doi.org/10.1007/s00262-010-0880-7.

[29]

N.N. Abrahim, M.S. Kanthimathi, A. Abdul-Aziz, Piper betle shows antioxidant activities, inhibits MCF-7 cell proliferation and increases activities of catalase and superoxide dismutase, BMC Complement. Altern. Med. 12 (2012) 220-231. https://doi.org/10.1186/1472-6882-12-220.

[30]

F. Kar, C. Hacioglu, S. Kacar, et al., Betaine suppresses cell proliferation by increasing oxidative stress–mediated apoptosis and inflammation in DU-145 human prostate cancer cell line, Cell Stress Chaperon. 24 (2019) 871-881. https://doi.org/10.1007/s12192-019-01022-x.

[31]

C. Wang, G. Nie, F. Yang, et al., Molybdenum and cadmium co-induce oxidative stress and apoptosis through mitochondria-mediated pathway in duck renal tubular epithelial cells, J. Hazard. Mater. 383 (2020) 121157. https://doi.org/10.1016/j.jhazmat.2019.121157.

[32]

F. Yang, R. Pei, Z. Zhang, et al., Copper induces oxidative stress and apoptosis through mitochondria-mediated pathway in chicken hepatocytes, Toxicol. In Vitro 54 (2018) 610-616. https://doi.org/10.1016/j.tiv.2018.10.017.

[33]

R. Liang, X.L. Shen, B. Zhang, et al., Apoptosis signal-regulating kinase 1 promotes Ochratoxin A-induced renal cytotoxicity, Sci. Rep. 5 (2015) 8078. https://doi.org/10.1038/srep08078.

[34]

S. Xia, Y. Miao, S. Liu, et al., Withaferin A induces apoptosis by ROS-dependent mitochondrial dysfunction in human colorectal cancer cells, Biochem. Biophys. Res. Commun. 503 (2018) 2363-2369. https://doi.org/10.1016/j.bbrc.2018.06.162.

[35]

L.Y. Jin, L. Changhee, Porcine deltacoronavirus induces caspase-dependent apoptosis through activation of the cytochrome c-mediated intrinsic mitochondrial pathway, Virus Res. 253 (2018) 112-123. https://doi.org/10.1016/j.virusres.2018.06.008.

[36]

X.J. Qin, Y.N. Li, L. Xin, et al., The dysfunction of ATPases due to impaired mitochondrial respiration in phosgene-induced pulmonary edema, Biochem. Biophys. Res. Commun. 367 (2008) 150-155. https://doi.org/10.1016/j.bbrc.2007.12.111.

[37]

L. Sousa, M.T.C. Pessoa, T.G.F. Costa, et al., Iron overload impact on P-ATPases, Ann. Hematol. 97 (2018) 377-385. https://doi.org/10.1007/s00277-017-3222-4.

[38]

A. Bogdanova, A. Makhro, J. Wang, et al., Calcium in red blood cells—a perilous balance, Int. J. Mol. Sci. 14 (2013) 9848-9872. https://doi.org/10.1007/s00277-017-3222-4.

[39]

J. Luo, C. Zhang, R. Liu, et al., Ganoderma lucidum polysaccharide alleviating colorectal cancer by alteration of special gut bacteria and regulation of gene expression of colonic epithelial cells, J. Funct. Foods 47 (2018) 127-135. https://doi.org/10.1016/j.jff.2018.05.041.

[40]

H. Liu, H. Fan, J. Zhang, et al., Isolation, purification, structural characteristic and antioxidative property of polysaccharides from A. cepa L. var. agrogatum Don, Food Sci. Hum. Well. 9 (2020) 71-79. https://doi.org/10.1016/j.fshw.2019.12.006.

[41]

L. Xie, M. Shen, Y. Hong, et al., Chemical modifications of polysaccharides and their anti-tumor activities, Carbohydr. Polym. 229 (2020) 115436. https://doi.org/10.1016/j.carbpol.2019.115436.

[42]

C. Deng, H. Fu, J. Xu, et al., Physiochemical and biological properties of phosphorylated polysaccharides from Dictyophora indusiata, Int. J. Biol. Macromol. 72 (2015) 894-899. https://doi.org/10.1016/j.ijbiomac.2014.09.053.

[43]

Q.H. Li, Y. Song, X.S. Hu, et al., Effect of phosphorylation on antioxidant activities of pumpkin (Cucurbita pepo, Lady godiva) polysaccharide, Int. J. Biol. Macromol. 81 (2015) 41-48. https://doi.org/10.1016/j.ijbiomac.2015.07.055.

Food Science and Human Wellness
Pages 1545-1556
Cite this article:
Xie L, Shen M, Huang R, et al. Apoptosis of colon cancer CT-26 cells induced polysaccharide from Cyclocarya paliurus and its phosphorylated derivative via intrinsic mitochondrial passway. Food Science and Human Wellness, 2023, 12(5): 1545-1556. https://doi.org/10.1016/j.fshw.2023.02.002

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Received: 30 March 2021
Revised: 12 April 2021
Accepted: 18 April 2021
Published: 21 March 2023
© 2023 Beijing Academy of Food Sciences.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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