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Research Articles

A highly purified C-phycocyanin from thermophilic cyanobacterium Thermosynechococcus elongatus and its cytotoxic activity assessment using an in vitro cell-based approach

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Pages 1218-1225 | Received 02 Apr 2020, Accepted 13 Aug 2020, Published online: 29 Aug 2020

References

  • MacColl R. Cyanobacterial phycobilisomes. J Struct Biol. 1998;124:311–334. doi:10.1006/jsbi.1998.4062.
  • Lauceri R, Chini Zittelli G, Maserti B, et al. Purification of phycocyanin from Arthrospira platensis by hydrophobic interaction membrane chromatography. Algal Res. 2018;35:333–340. doi:10.1016/j.algal.2018.09.003.
  • Chaiklahan R, Chirasuwan N, Loha V, et al. Separation and purification of phycocyanin from Spirulina sp. using a membrane process. Bioresour Technol. 2011; 102:7159–7164. doi:10.1016/j.biortech.2011.04.067.
  • Patil G, Raghavarao KSMS. Aqueous two phase extraction for purification of C-phycocyanin. Biochem Eng J. 2007;34:156–164. doi:10.1016/j.bej.2006.11.026.
  • Liu Q, Huang Y, Zhang R, et al. Medical application of Spirulina platensis derived C-phycocyanin. Evid Based Complement Alternat Med. 2016;2016:1–14. doi:10.1155/2016/7803846.
  • Wu Q, Liu L, Miron A, et al. The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch Toxicol. 2016;90:1817–1840. doi:10.1007/s00204-016-1744-5.
  • Yu P, Wu Y, Wang G, et al. Purification and bioactivities of phycocyanin. Crit Rev Food Sci Nutr. 2017;57:3840–3849. doi:10.1080/10408398.2016.1167668.
  • Bharathiraja S, Seo H, Manivasagan P, et al. In vitro photodynamic effect of phycocyanin against breast cancer cells. Molecules. 2016;21:1470), doi:10.3390/molecules21111470.
  • Bingula R, Dupuis C, Pichon C, et al. 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;2016:1–11. doi:10.1155/2016/8162952.
  • Hao S, Li S, Wang J, et al. 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. 2019;17:362), oi:10.3390/md17060362.
  • Jiang L, Wang Y, Liu G, et al. C-Phycocyanin exerts anti-cancer effects via the MAPK signaling pathway in MDA-MB-231 cells. Cancer Cell Int. 2018;18:1–14. doi:10.1186/s12935-018-0511-5. doi: 10.1186/s12935-017-0498-3
  • Ravi M, Tentu S, Baskar G, et al. Molecular mechanism of anti-cancer activity of phycocyanin in triple-negative breast cancer cells. BMC Cancer. 2015;15:768), doi:10.1186/s12885-015-1784-x.
  • Soni B, Kalavadia B, Trivedi U, et al. Extraction, purification and characterization of phycocyanin from Oscillatoria quadripunctulata isolated from the rocky shores of Bet-Dwarka, Gujarat, India. Process Biochem. 2006;41:2017–2023. doi:10.1016/j.procbio.2006.04.018.
  • Santiago-Santos MC, Ponce-Noyola T, Olvera-Ram´ırez R, et al. Extraction and purification of phycocyanin from Calothrix sp. Process Biochem. 2004;39:2047–2052. doi:10.1016/j.procbio.2003.10.007.
  • Hao S, Yan Y, Li S, et al. The in vitro anti-tumor activity of phycocyanin against non-small cell lung cancer cells. Mar Drugs. 2018;16:178), doi:10.3390/md16060178.
  • Singh NK, Parmar A, Madamwar D. Optimization of medium components for increased production of C-phycocyanin from Phormidium ceylanicum and its purification by single step process. Bioresour Technol. 2009;100:1663–1669. doi:10.1016/j.biortech.2008.09.021.
  • Ramos A, Acién FG, Fernàndez-Sevilla JM, et al. Development of a process for large-scale purification of C-phycocyanin from Synechocystis aquatilis using expanded bed adsorption chromatography. J Chromatogr B. 2011;879:511–519. doi:10.1016/j.jchromb.2011.01.013.
  • Bermejo R, Ramos A. Pilot scale recovery of phycocyanin from Spirulina platensis using expanded bed adsorption chromatography. Chromatographia. 2012;75:195–204. doi:10.1007/s10337-012-2200-1.
  • Minkova K, Tchorbadjieva M, Tchernov A, et al. Improved procedure for separation and purification of Arthronema africanum phycobiliproteins. Biotechnol Lett. 2007;29:647–651. doi:10.1007/s10529-006-9274-5.
  • Moraes CC, Kalil SJ. Strategy for a protein purification design using C-phycocyanin extract. Bioresour Technol. 2009;100:5312–5317. doi:10.1016/j.biortech.2009.05.026.
  • Muthukumar S, Muralikrishnan T, Mendhe R, et al. Economic benefits of membrane chromatography versus packed bed column purification of therapeutic proteins expressed in microbial and mammalian hosts. J Chem Technol Biotechnol. 2017;92:59–68. doi:10.1002/jctb.5064.
  • Soni B, Trivedi U, Madamwar D. A novel method of single step hydrophobic interaction chromatography for the purification of phycocyanin from Phormidium fragile and its characterization for antioxidant property. Bioresour Technol. 2008;99:188–194. doi:10.1016/j.biortech.2006.11.010.
  • Yan SG, Zhu LP, Su HN, et al. Single step chromatography for simultaneous purification of C-phycocyanin and allophycocyanin with high purity and recovery from Spirulina (Arthrospira) platensis. J Appl Phycol. 2011;23:1–6. doi:10.1007/s10811-010-9525-7.
  • Rippka R, Deruelles J, Waterbury JB, et al. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol. 1979;111:1–61. doi:10.1099/00221287-111-1-1.
  • Prodöhl A, Ambill M, El-Mohsnawy E, et al. Modular device for hydrogen production: Optimization of (individual) components. In: Miyake J, Igarashi Y, Rögner M, editors. Biohydrogen III. Amsterdam: Elsevier; 2004. p. 171–177.
  • El-Mohsnawy E, Kopczak MJ, Schlodder E, et al. Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry. 2010;49:4740–4751. doi:10.1021/bi901807p.
  • Schägger H, von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987;166:368–379. doi:10.1016/0003-2697(87)90587-2.
  • Bennett A, Bogorad L. Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol. 1973;58:419–435. doi:10.1083/jcb.58.2.419.
  • Repetto G, del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc. 2008;3:1125–1131. doi:10.1038/nprot.2008.75.
  • Gupta A, Sainis JK. Isolation of C-phycocyanin from Synechococcus sp., (Anacystis nidulans BD1). J Appl Phycol. 2010;22:231–233. doi:10.1007/s10811-009-9449-2.
  • Kumar D, Dhar DW, Pabbi S, et al. Extraction and purification of C-phycocyanin from Spirulina platensis (CCC540). Ind J Plant Physiol. 2014;19:184–188. doi:10.1007/s40502-014-0094-7.
  • Uday Bhaskar S, Gopalaswamy G, Raghu R. A simple method for efficient extraction and purification of C-phycocyanin from Spirulina platensis Geitler. Indian J Exp Biol. 2005;43:277–279.
  • Abalde J, Betancourt L, Torres E, et al. Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus sp. IO9201. Plant Sci. 1998;136:109–120. doi:10.1016/S0168-9452(98)00113-7.
  • Patil G, Chethana S, Sridevi AS, et al. Method to obtain C-phycocyanin of high purity. J Chromatogr A. 2006;1127:76–81. doi:10.1016/j.chroma.2006.05.073.
  • Manna A, Saha P, Sarkar A, et al. Malabaricone-A induces a redox imbalance that mediates apoptosis in U937 cell line. PLoS ONE. 2012;7:e36938), doi:10.1371/journal.pone.0036938.
  • Pagels F, Guedes AC, Amaro HM, et al. Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol Adv. 2019;37:422–443. doi:10.1016/j.biotechadv.2019.02.010.
  • de Jesus Raposo MF, de Morais RM, de Morais AM. Health applications of bioactive compounds from marine microalgae. Life Sci. 2013;93:479–486. doi:10.1016/j.lfs.2013.08.002.
  • Pleonsil P, Soogarun S, Suwanwong Y. Anti-oxidant activity of holo- and apo-c-phycocyanin and their protective effects on human erythrocytes. Int J Biol Macromol. 2013;60:393–398. doi:10.1016/j.ijbiomac.2013.06.016.
  • Jiang L, Wang Y, Yin Q, et al. Phycocyanin: a potential drug for cancer treatment. J Cancer. 2017;8:3416–3429. doi:10.7150/jca.21058.
  • Zhu C, Ling Q, Cai Z, et al. Selenium-containing phycocyanin from Se-enriched Spirulina platensis reduces inflammation in dextran sulfate sodium-induced colitis by inhibiting NF-kB activation. J Agric Food Chem. 2016;64:5060–5070. doi:10.1021/acs.jafc.6b01308.
  • Chen HW, Yang TS, Chen MJ, et al. Purification and immunomodulating activity of C-phycocyanin from Spirulina platensis cultured using power plant flue gas. Process Biochem. 2014;49:1337–1344. doi:10.1016/j.procbio.2014.05.006.
  • Nemoto-Kawamura C, Hirahashi T, Nagai T, et al. Phycocyanin enhances secretary IgA antibody response and suppresses allergic IgE antibody response in mice immunized with antigen-entrapped biodegradable microparticles. J Nutr Sci Vitaminol. 2004;50:129–136. doi:10.3177/jnsv.50.129.
  • Gardeva E, Toshkova R, Yossifova L, et al. Antitumor activity of c-phycocyanin from Arthronema africanum (Cyanophyceae). Braz Arch Biol Technol. 2014;57:675–684. doi:10.1590/S1516-89132014005000018.
  • Gantar M, Dhandayuthapani S, Rathinavelu A. Phycocyanin induces apoptosis and enhances the effect of topotecan on prostate cell line LNCaP. J Med Food. 2012;15:1091–1095. doi:10.1089/jmf.2012.0123.
  • Safaei M, Maleki H, Soleimanpour H, et al. Development of a novel method for the purification of C-phycocyanin pigment from a local cyanobacterial strain Limnothrix sp. NS01 and evaluation of its anticancer properties. Sci Rep. 2019;9:1–16. doi:10.1038/s41598-019-45905-6. doi: 10.1038/s41598-018-37186-2
  • Zhang LX, Cai CE, Guo TT, et al. Anti-cancer effects of polysaccharide and phycocyanin from Porphyra yezoensis. J Mar Sci Technol. 2011;19:377–382.
  • Yufeng L, Lizhi X, Chengwu Z. The inhibition of phycocyanin from Porphyra haitanensis on the growth of human leukemia HL-60 cells. Chin J Mar Drugs. 2000;19:20–24.
  • Liao G, Gao B, Gao Y, et al. Phycocyanin inhibits tumorigenic potential of pancreatic cancer cells: role of apoptosis and autophagy. Sci Rep. 2016;6:34564), doi:10.1038/srep3456. doi: 10.1038/srep34564
  • Deniz I, Ozen MO, Yesil-Celiktas O. Supercritical fluid extraction of phycocyanin and investigation of cytotoxicity on human lung cancer cells. J Supercrit Fluids. 2016;108:13–18. doi:10.1016/j.supflu.2015.10.015.
  • Pan R, Lu R, Zhang Y, et al. Spirulina phycocyanin induces differential protein expression and apoptosis in SKOV-3 cells. Int J Biol Macromol. 2015;81:951–959. doi:10.1016/j.ijbiomac.2015.09.039.