Fol. Biol. 2022, 68, 16-24

https://doi.org/10.14712/fb2022068010016

C-Phycocyanin Suppresses Cell Proliferation and Promotes Apoptosis by Regulating the AMPK Pathway in NCL-H292 Non-Small Cell Lung Cancer Cells

He Chaowen, H. Dongxuan, H. Dongsheng, P. Jianfeng, Y. Fan, C. Yahui, L. Xiaohua

Department of Pulmonary and Critical Care Medicine, Shenzhen Longhua District Central Hospital, Shenzhen, China

Received October 2021
Accepted December 2021

References

1. Abd El-Baky, H. H., El-Baroty, G. S. (2012) Characterization and bioactivity of phycocyanin isolated from Spirulina maxima grown under salt stress. Food Funct. 3, 381-388. <https://doi.org/10.1039/c2fo10194g>
2. Bai, J., Xu, J., Zhao, J., Zhang, R. (2020) LncRNA NBR2 suppresses migration and invasion of colorectal cancer cells by downregulating miRNA-21. Hum. Cell 33, 98-103. <https://doi.org/10.1007/s13577-019-00265-1>
3. Basha, O. M., Hafez, R. A., El-Ayouty, Y. M., Mahrous, K. F., Bareedy, M. H., Salama, A. M. (2008) C-Phycocyanin inhibits cell proliferation and may induce apoptosis in human HepG2 cells. Egypt. J. Immunol. 15, 161-167.
4. Baudelet, P. H., Gagez, A. L., Berard, J. B., Juin, C., Bridiau, N., Kaas, R., Thiery, V., Cadoret, J. P., Picot, L. (2013) Antiproliferative activity of Cyanophora paradoxa pigments in melanoma, breast and lung cancer cells. Mar. Drugs 11, 4390-4406. <https://doi.org/10.3390/md11114390>
5. Bingula, R., Dupuis, C., Pichon, C., Berthon, J. Y., Filaire, M., Pigeon, L., Filaire, E. (2016) Study of the effects of betaine and/or C-phycocyanin on the growth of lung cancer A549 cells in vitro and in vivo. J. Oncol. 2016, 8162952. <https://doi.org/10.1155/2016/8162952>
6. Brozos-Vazquez, E. M., Diaz-Pena, R., Garcia-Gonzalez, J., Leon-Mateos, L., Mondelo-Macia, P., Pena-Chilet, M., Lopez-Lopez, R. (2020) Immunotherapy in nonsmall-cell lung cancer: current status and future prospects for liquid biopsy. Cancer Immunol. Immunother. 70, 1177-1188. <https://doi.org/10.1007/s00262-020-02752-z>
7. Cian, R. E., Lopez-Posadas, R., Drago, S. R., de Medina, F. S., Martinez-Augustin, O. (2012) Immunomodulatory properties of the protein fraction from Phorphyra columbina. J. Agric. Food Chem. 60, 8146-8154. <https://doi.org/10.1021/jf300928j>
8. Deng, H., Gao, X., Peng, H., Wang, J., Hou, X., Xu, H., Yang, F. (2018) Effect of liposome-mediated HSP27 transfection on collagen synthesis in alveolar type II epithelial cells. Mol. Med. Rep. 17, 7319-7324.
9. Dimitrov, S. D., Matouskova, E., Forejt, J. (2001) Expression of BRCA1, NBR1 and NBR2 genes in human breast cancer cells. Folia Biol. (Praha) 47, 120-127.
10. Gao, Y. P., Li, Y., Li, H. J., Zhao, B. (2019) LncRNA NBR2 inhibits EMT progression by regulating Notch1 pathway in NSCLC. Eur. Rev. Med. Pharmacol. Sci. 23, 7950-7958.
11. Hamouri, S., Alrabadi, N., Syaj, S., Abushukair, H., Ababneh, O., Al-Kraimeen, L., Al-Sous, M., Hecker, E. (2022) Atrial resection for T4 non-small cell lung cancer with left atrium involvement: a systematic review and meta-analysis of survival. Surg. Today, online ahead of print. <https://doi.org/10.1007/s00595-021-02446-8>
12. Hao, S., Li, S., Wang, J., Zhao, L., Yan, Y., Wu, T., Zhang, J., Wang, C. (2019) C-Phycocyanin suppresses the in vitro proliferation and migration of non-small-cell lung cancer cells through reduction of RIPK1/NF-κB activity. Mar. Drugs 17, 362. <https://doi.org/10.3390/md17060362>
13. Huang, C. Y., Ju, D. T., Chang, C. F., Muralidhar Reddy, P., Velmurugan, B. K. (2017) A review on the effects of current chemotherapy drugs and natural agents in treating non-small cell lung cancer. Biomedicine (Taipei) 7, 23. <https://doi.org/10.1051/bmdcn/2017070423>
14. Inoki, K., Kim, J., Guan, K. L. (2012) AMPK and mTOR in cellular energy homeostasis and drug targets. Annu. Rev. Pharmacol. Toxicol. 52, 381-400. <https://doi.org/10.1146/annurev-pharmtox-010611-134537>
15. Ji, H., Liu, G., Han, J., Zhu, F., Dong, X., Li, B. (2020) C-phycocyanin inhibits epithelial-to-mesenchymal transition in Caski cells. Cancer Cell Int. 20, 292. <https://doi.org/10.1186/s12935-020-01384-8>
16. Jiang, L., Wang, Y., Liu, G., Liu, H., Zhu, F., Ji, H., Li, B. (2018) C-Phycocyanin exerts anti-cancer effects via the MAPK signaling pathway in MDA-MB-231 cells. Cancer Cell Int. 18, 12. <https://doi.org/10.1186/s12935-018-0511-5>
17. Kaur, P., Dhandayuthapani, S., Venkatesan, T., Gantor, M., Rathinavelu, A. (2020) Molecular mechanism of C-phycocyanin induced apoptosis in LNCaP cells. Bioorg. Med. Chem. 28, 115272. <https://doi.org/10.1016/j.bmc.2019.115272>
18. Li, H. B., Chen, J. K., Su, Z. X., Jin, Q. L., Deng, L. W., Huang, G., Shen, J. N. (2021) Cordycepin augments the chemosensitivity of osteosarcoma to cisplatin by activating AMPK and suppressing the AKT signaling pathway. Cancer Cell Int. 21, 706. <https://doi.org/10.1186/s12935-021-02411-y>
19. Liu, X., Xiao, Z. D., Han, L., Zhang, J., Lee, S. W., Wang, W., Lee, H., Zhuang, L., Chen, J., Lin, H. K., Wang, J., Liang, H., Gan, B. (2016) LncRNA NBR2 engages a metabolic checkpoint by regulating AMPK under energy stress. Nat. Cell Biol. 18, 431-442. <https://doi.org/10.1038/ncb3328>
20. Liu, Z., Cao, H., Shi, Y., Yang, R. (2019) KIAA1211 plays an oncogenic role in human non-small cell lung cancer. J. Cancer 10, 6747-6753. <https://doi.org/10.7150/jca.35951>
21. Lu, W., Zhang, H., Niu, Y., Wu, Y., Sun, W., Li, H., Kong, J., Ding, K., Shen, H. M., Wu, H., Xia, D., Wu, Y. (2017) Long non-coding RNA linc00673 regulated non-small cell lung cancer proliferation, migration, invasion and epithelial mesenchymal transition by sponging miR-150-5p. Mol. Cancer 16, 118. <https://doi.org/10.1186/s12943-017-0685-9>
22. Miller, K. D., Nogueira, L., Mariotto, A. B., Rowland, J. H., Yabroff, K. R., Alfano, C. M., Jemal, A., Kramer, J. L., Siegel, R. L. (2019) Cancer treatment and survivorship statistics, 2019. CA Cancer J. Clin. 69, 363-385. <https://doi.org/10.3322/caac.21565>
23. Mitra, S., Siddiqui, W. A., Khandelwal, S. (2015) C-Phycocyanin protects against acute tributyltin chloride neurotoxicity by modulating glial cell activity along with its anti-oxidant and anti-inflammatory property: a comparative efficacy evaluation with N-acetyl cysteine in adult rat brain. Chem. Biol. Interact. 238, 138-150. <https://doi.org/10.1016/j.cbi.2015.06.016>
24. Nussinov, R., Tsai, C. J., Jang, H. (2021) Anticancer drug resistance: an update and perspective. Drug Resist. Updat. 59, 100796. <https://doi.org/10.1016/j.drup.2021.100796>
25. Pandya, G., Kirtonia, A., Sethi, G., Pandey, A. K., Garg, M. (2020) The implication of long non-coding RNAs in the diagnosis, pathogenesis and drug resistance of pancreatic ductal adenocarcinoma and their possible therapeutic potential. Biochim. Biophys. Acta Rev. Cancer 1874, 188423. <https://doi.org/10.1016/j.bbcan.2020.188423>
26. Piao, J., Chen, L., Quan, T., Li, L., Quan, C., Piao, Y., Jin, T., Lin, Z. (2016) Superior efficacy of co-treatment with the dual PI3K/mTOR inhibitor BEZ235 and histone deacetylase inhibitor Trichostatin A against NSCLC. Oncotarget 7, 60169-60180. <https://doi.org/10.18632/oncotarget.11109>
27. Rao, X., Huang, X., Zhou, Z., Lin, X. (2013) An improvement of the 2^(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinforma. Biomath. 3, 71-85.
28. Ren, Z., Xie, Z., Cao, D., Gong, M., Yang, L., Zhou, Z., Ou, Y. (2018) C-Phycocyanin inhibits hepatic gluconeogenesis and increases glycogen synthesis via activating Akt and AMPK in insulin resistance hepatocytes. Food Funct. 9, 2829-2839. <https://doi.org/10.1039/C8FO00257F>
29. Rio, D. C., Ares, M. Jr., Hannon, G. J., Nilsen, T. W. (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb. Protoc. 2010, pdb.prot5439.
30. Schmidt, L. H., Görlich, D., Spieker, T., Rohde, C., Schuler, M., Mohr, M., Humberg, J., Sauer, T., Thoenissen, N. H., Huge, A., Voss, R., Marra, A., Faldum, A., Müller-Tidow, C., Berdel, W. E., Wiewrodt, R. (2014) Prognostic impact of Bcl-2 depends on tumor histology and expression of MALAT-1 lncRNA in non-small-cell lung cancer. J. Thorac. Oncol. 9, 1294-1304. <https://doi.org/10.1097/JTO.0000000000000243>
31. Schutt, M., Kern, W., Zimmermann, A., Busch, P., Kerner, W., Voll, A., Wagner, C., Kann, P. H., Dapp, A., Holl, R. W.; DPV initiative; German BMBF Competence Network Diabetes mellitus (2010) Association of antidiabetic therapies to glycemic control and to body weight in type 2 diabetes: a German multicenter analysis on 9294 patients. Exp. Clin. Endocrinol. Diabetes 118, 490-495. <https://doi.org/10.1055/s-0030-1249024>
32. Sonani, R. R., Patel, S., Bhastana, B., Jakharia, K., Chaubey, M. G., Singh, N. K., Madamwar, D. (2017) Purification and antioxidant activity of phycocyanin from Synechococcus sp. R42DM isolated from industrially polluted site. Bioresour. Technol. 245, 325-331. <https://doi.org/10.1016/j.biortech.2017.08.129>
33. Ulitsky, I., Bartel, D. P. (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154, 26-46. <https://doi.org/10.1016/j.cell.2013.06.020>
34. Wang, H., Liu, Y., Gao, X., Carter, C. L., Liu, Z. R. (2007) The recombinant beta subunit of C-phycocyanin inhibits cell proliferation and induces apoptosis. Cancer Lett. 247, 150-158. <https://doi.org/10.1016/j.canlet.2006.04.002>
35. Wang, P., Liu, X. M., Ding, L., Zhang, X. J., Ma, Z. L. (2018) mTOR signaling-related microRNAs and cancer involvement. J. Cancer 9, 667-673. <https://doi.org/10.7150/jca.22119>
36. Xu, C. F., Brown, M. A., Nicolai, H., Chambers, J. A., Griffiths, B. L., Solomon, E. (1997) Isolation and characterisation of the NBR2 gene which lies head to head with the human BRCA1 gene. Hum. Mol. Genet. 6, 1057-1062. <https://doi.org/10.1093/hmg/6.7.1057>
37. Xue, L., Li, J., Lin, Y., Liu, D., Yang, Q., Jian, J., Peng, J. (2020) m6 A transferase METTL3-induced lncRNA ABHD11-AS1 promotes the Warburg effect of non-small-cell lung cancer. J. Cell. Physiol. 236, 2649-2658. <https://doi.org/10.1002/jcp.30023>
38. Yang, W., Zheng, Z., Yi, P., Wang, S., Zhang, N., Ming, J., Tan, J., Guo, H. (2020) LncRNA NBR2 inhibits the malignancy of thyroid cancer, associated with enhancing the AMPK signaling. Front. Oncol. 10, 956. <https://doi.org/10.3389/fonc.2020.00956>
39. Yang, Y., Kuang, L., Li, L., Wu, Y., Zhong, B., Huang, X. (2021) Distinct mitochondria-mediated T-cell apoptosis responses in children and adults with coronavirus disease 2019. J. Infect. Dis. 224, 1333-1344. <https://doi.org/10.1093/infdis/jiab400>
40. Yang, Y., Wu, Y., Meng, X., Wang, Z., Younis, M., Liu, Y., Wang, P., Huang, X. (2022) SARS-CoV-2 membrane protein causes the mitochondrial apoptosis and pulmonary edema via targeting BOK. Cell Death Diff. 29, 1395-1408. <https://doi.org/10.1038/s41418-022-00928-x>
41. Yuan, Y. G., Gurunathan, S. (2017) Combination of graphene oxide-silver nanoparticle nanocomposites and cisplatin enhances apoptosis and autophagy in human cervical cancer cells. Int. J. Nanomedicine 12, 6537-6558. <https://doi.org/10.2147/IJN.S125281>
42. Zhang, L., Wang, Y., Xia, S., Yang, L., Wu, D., Zhou, Y., Lu, J. (2020a) Long noncoding RNA PANDAR inhibits the development of lung cancer by regulating autophagy and apoptosis pathways. J. Cancer 11, 4783-4790. <https://doi.org/10.7150/jca.45291>
43. Zhang, X. Z., Liu, H., Chen, S. R. (2020b) Mechanisms of long non-coding RNAs in cancers and their dynamic regulations. Cancers (Basel) 12, 1245. <https://doi.org/10.3390/cancers12051245>
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