مروری جامع بر ساختار، خواص و کاربرد رنگ‌دانه فیکوسیانین
محورهای موضوعی : علوم و صنایع غذایی
رضا صفری
1
(استادیار، پژوهشکده اکولوژی دریای خزر، مؤسسه تحقیقات علوم شیلاتی کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، ساری، ایران)
سهیل ریحانی پول
2
(دانش‌آموخته دکتری تخصصی، گروه فرآوری محصولات شیلاتی، دانشکده شیلات و محیط زیست، دانشگاه علوم کشاورزی و منابع طبیعی گرگان، گرگان، ایران)
سکینه یگانه
3
(استاد، گروه شیلات، دانشکده علوم دامی و شیلات، دانشگاه علوم کشاورزی و منابع طبیعی ساری، ساری، ایران)
کلید واژه: فیکوسیانین, خواص دارویی, ساختار شیمیایی, روش‌های استخراج, فعالیت ضد باکتریایی و آنتی‌اکسیدانی,
چکیده مقاله :
هدف از مطالعه مروری حاضر، ارزیابی خصوصیات ذاتی و کاربردهای مختلف رنگ‌دانه فیکوسیانین در صنایع غذایی و دارویی است. ضمن این‌که، در هر بخش سابقه کاملی از تحقیقات انجام یافته در زمینه فیکوسیانین ارائه شده است. فیکوسیانین، رنگ‌دانه آبی، گیرنده نور با خاصیت آنتی اکسیدانی و فلورسنت در سیانوباکتری ها و دو جلبک از جنس رودوفیت ها و کریپتوفیت ها است. رنگ‌دانه فیکوسیانین از دو زیر واحد نسبتاً مشابهα وβ تشکیل شده است. زنجیره آلفا شامل یک فیکوسیانوبیلین متصل به سیستئین 89 و زنجیره بتا شامل دو فیکوسیانوبیلین متصل به سیستئین های 84 و 155 است. فیکوسیانین به شکل تجاری از اسپیرولینا پلاتنسیس، در قالب کشت های فتواتوتروف و در محیط های باز در حوضچه های بزرگ یا استخر های نقاط گرمسیری و نیمه گرمسیری در حواشی اقیانوس ها تولید می‌شود. این رنگ‌دانه با استفاده از تکنیک های مختلف از جمله روش آنزیمی، اولتراسوند، انجماد-انجمادزدایی، حلال معدنی، هموژنیزاسیون، استرس و شوک اسمزی، فشار هیدرواستاتیک بالا، اولتراسانتریفوژ و اولتراهموژنیزاسیون از جلبک مذکور قابل استخراج است. بسته به شرایط استخراج، هر روش دارای مزایا و معایبی است؛ اما دو روش آنزیمی و اولتراسوند نسبت به سایر روش ها کارائی بیشتری دارند. فیکوسیانین دارای خواص دارویی و درمانی متعددی از جمله ضدسرطان و ضدالتهاب است؛ ضمن این‌که تأثیر مثبت این رنگ‌دانه بر سلول های عصبی، کلیه و دستگاه ایمنی تائید شده است. فیکوسیانین با دارا بودن سه خاصیت رنگ دهندگی، آنتی اکسیدانی و ضدمیکروبی پتانسل بالقوه ای جهت استفاده در فرمولاسیون مواد غذایی مختلف از جمله ماست، پنیر، بستنی و غیره دارد که این موارد در تحقیقات مختلف ثابت شده است.
چکیده انگلیسی:
This review aims to evaluate the intrinsic properties and different applications of phycocyanin pigment in the food and pharmaceutical industries. In addition, in each section, a detailed history of the research conducted in the field of phycocyanin is presented. Phycocyanin is a blue pigment, a light receiver with antioxidant and fluorescent properties in cyanobacteria, and two algae from the genus rhodophytes and cryptophytes. Phycocyanin pigment consists of two relatively similar subunits α and β. The alpha chain contains one phycocyanobilin attached to cysteine 89 and the beta chain contains two phycocyanobilins attached to cysteines 84 and 155. Phycocyanin is commercially produced from spirulina algae (spirulina platensis), in the form of photoautotrophic cultures, and open environments in large ponds or pools in tropical or subtropical areas at the edges of oceans. This pigment can be extracted from the mentioned algae by using different techniques such as enzymatic method, ultrasound, freezing-defrosting, mineral solvent, homogenization, stress and osmotic shock, high hydrostatic pressure, ultracentrifuge, and ultra homogenization. Depending on the extraction conditions, each method has its advantages and disadvantages, but the enzymatic and ultrasound methods are more efficient than other methods. Phycocyanin has many medicinal and therapeutic properties, including anti-cancer and anti-inflammatory; In addition, the positive effect of this pigment on nerve cells, kidneys, and the immune system has been confirmed. Phycocyanin, having three colorings, antioxidant and antimicrobial properties, has the potential to be used in various food formulations, such as yogurt, cheese, ice cream, etc., which have been proven in various research.
منابع و مأخذ:
Apt, K. E., Collier, J. L. and Grossman, A. R. (1995). Evolution of the phycobiliproteins. Journal of Molecular Biology, 248(1): 79-96.
Abalde, J., Betancourt, L., Torres, E., Cid, A. and Barwell, C. (1998). Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus IO9201. Plant Science, 136(1): 109-120.
Agustini, T. W., Ma’ruf, W. F. and Wibowo, B. A. (2017). Study on the effect of different concentration of Spirulina platensis paste added into dried noodle to its quality characteristics. In IOP Conference Series: Earth and Environmental Science (Vol. 55, No. 1, p. 012068). IOP Publishing.
Barberan F. A. (1997). Determination of authenticity of fruit jams by HPLC analysis of anthocyanins. Journal of the Science of Food and Agriculture, 73(2): 207-213.
Barbarino, E. and Lourenço, S. O. (2005). An evaluation of methods for extraction and quantification of protein from marine macro-and microalgae. Journal of Applied Phycology, 17(5): 447-460.
Bermejo, P., Piñero, E. and Villar, Á. M. (2008). Iron-chelating ability and antioxidant properties of phycocyanin isolated from a protean extract of Spirulina platensis. Food Chemistry, 110(2): 436-445.
Bingula, R., Dupuis, C., Pichon, C., Berthon, J. Y., Filaire, M., Pigeon, L. and 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. Journal of Oncology, 1-12.
Bleakley, S. and Hayes, M. (2017). Algal proteins: extraction, application, and challenges concerning production. Foods, 6(5): 1-34.
Chattopadhyay, P., Chatterjee, S., and Sen, S. K. (2008). Biotechnological potential of natural food grade biocolorants. African Journal of Biotechnology, 7(17): 2972-2985.
Chaiklahan, R., Chirasuwan, N. and Bunnag, B. (2012). Stability of phycocyanin extracted from Spirulina sp.: Influence of temperature, pH and preservatives. Process Biochemistry, 47(4): 659-664.
Coustets, M., Al-Karablieh, N., Thomsen, C. and Teissié, J. (2013). Flow process for electroextraction of total proteins from microalgae. Journal of Membrane Biology, 246(10): 751-760.
Deng, R. and Chow, T. J. (2010). Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovascular Therapeutics, 28(4): 33-45.
Dewi, E. N., Purnamayati, L. and Kurniasih, R. A. (2016). Antioxidant activities of phycocyanin microcapsules using maltodextrin and carrageenan as coating materials. Jurnal Teknologi, 78(4-2): 45-50
Estrada, J. P., Bescós, P. B. and Del Fresno, A. V. (2001). Antioxidant activity of different fractions of Spirulina platensis protean extract. II Farmaco, 56(5-7): 497-500.
Eriksen, N. T. (2008). Production of phycocyanin—a pigment with applications in biology, biotechnology, foods and medicine. Applied Microbiology and Biotechnology, 80(1): 1-14.
El-Baz, F. K., El-Senousy, W. M., El-Sayed, A. B. and Kamel, M. M. (2013). In vitro antiviral and antimicrobial activities of Spirulina platensis extract. Journal of Applied Pharmaceutical Science, 3(12): 52-56.
Filimon, R. (2010). Plants pigments with therapeutic potential from horticultural products. Seria Agro, 52 (1): 668-673.
Graverholt, O. S. and Eriksen, N. T. (2007). Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Applied Microbiology and Biotechnology, 77(1): 69-75.
Gantar, M., Dhandayuthapani, S. and Rathinavelu, A. (2012). Phycocyanin induces apoptosis and enhances the effect of topotecan on prostate cell line LNCaP. Journal of Medicinal Food, 15(12): 1091-1095.
Goettel, M., Eing, C., Gusbeth, C., Straessner, R. and Frey, W. (2013). Pulsed electric field assisted extraction of intracellular valuables from microalgae. Algal Research, 2(4): 401-408.
Hsiao, G., Chou, P. H., Shen, M. Y., Chou, D. S., Lin, C. H. and Sheu, J. R. (2005). C-phycocyanin, a very potent and novel platelet aggregation inhibitor from Spirulina platensis. Journal of Agricultural and Food Chemistry, 53(20): 7734-7740.
Higuera-Ciapara, I., Felix-Valenzuela, L. and Goycoolea, F. M. (2006). Astaxanthin: a review of its chemistry and applications. Critical Reviews in Food Science and Nutrition, 46(2): 185-196.
Hosseini, S., Shahbazizadeh, S., Khosravi-Darani, K. and Reza Mozafari, M. (2013). Spirulina paltensis: Food and function. Current Nutrition and Food Science, 9(3): 189-193.
Harnedy, P. A. and FitzGerald, R. J. (2013). Extraction of protein from the macroalga Palmaria palmata. LWT-Food Science and Technology, 51(1): 375-382.
Ismaiel, M., El-Ayouty, Y. M. and Piercey-Normore, M. D. (2014). Antioxidants characterization in selected cyanobacteria. Annals of Microbiology, 64(3): 1223-1230.
Jespersen, L., Strømdahl, L. D., Olsen, K. and Skibsted, L. H. (2005). Heat and light stability of three natural blue colorants for use in confectionery and beverages. European Food Research and Technology, 220(3): 261-266.
Janczyk, P., Wolf, C. and Souffrant, W. B. (2005). Evaluation of nutritional value and safety of the green microalgae Chlorella vulgaris treated with novel processing methods. Arch Zootech, 8 (1): 132-147.
Joubert, Y. and Fleurence, J. (2008). Simultaneous extraction of proteins and DNA by an enzymatic treatment of the cell wall of Palmaria palmata (Rhodophyta). Journal of Applied Phycology, 20(1): 55-61.
Jaswir, I., Noviendri, D., Hasrini, R. F. and Octavianti, F. (2011). Carotenoids: Sources, medicinal properties and their application in food and nutraceutical industry. Journal of Medicinal Plants Research, 5(33): 7119-7131.
Joventino, I. P., Alves, H. G., Neves, L. C., Pinheiro-Joventino, F., Leal, L. K. A., Neves, S. A. and Viana, G. B. (2012). The microalga Spirulina platensis presents anti-inflammatory action as well as hypoglycemic and hypolipidemic properties in diabetic rats. Journal of Complementary and Integrative Medicine: 9(1): 1-24.
Jerley, A. and Prabu, M. (2015) Purification, characterization and antioxidant properties of C-Phycocyanin from Spirulina platensis. Scrutiny International Research Journal of Agriculture, Plant Biotechnology and Bio Products, 2(1): 7-15.
Kleinegris, D. M., Janssen, M., Brandenburg, W. A. and Wijffels, R. H. (2011). Continuous production of carotenoids from Dunaliella salina. Enzyme and Microbial Technology, 48(3): 253-259.
(2011). Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound. Journal of Medicinal Plants Research, 5(32): 7043-7048.
Kuddus, M., Singh, P., Thomas, G. and Al-Hazimi, A. (2013). Recent developments in production and biotechnological applications of C-phycocyanin. BioMed Research International, 1-9.
Li, B., Chu, X., Gao, M. and Li, W. (2010). Apoptotic mechanism of MCF-7 breast cells in vivo and in vitro induced by photodynamic therapy with C-phycocyanin. Acta Biochimica et Biophysica Sinica, 42(1): 80-89.
Li, B., Gao, M. H., Chu, X. M., Teng, L., Lv, C. Y., Yang, P. and Yin, Q. F. (2015). The synergistic antitumor effects of all-trans retinoic acid and C-phycocyanin on the lung cancer A549 cells in vitro and in vivo. European Journal of Pharmacology, 749: 107-114.
McClements, D. J. (1995). Advances in the application of ultrasound in food analysis and processing. Trends in Food Science and Technology, 6(9): 293-299.
Mishra, S. K., Shrivastav, A. and Mishra, S. (2008). Effect of preservatives for food grade C-PC from Spirulina platensis. Process Biochemistry, 43(4): 339-345.
Mala, R., Sarojini, M., Saravanababu, S. and Umadevi, G. (2009). Screening for antimicrobial activity of crude extracts of Spirulina platensis. Journal of Cell and Tissue Research, 9(3): 1951-1955
Moraes, C. C., Sala, L., Cerveira, G. P. and Kalil, S. J. (2011). C-phycocyanin extraction from Spirulina platensis wet biomass. Brazilian Journal of Chemical Engineering, 28 (1): 45-49.
Moorhead, K., Capelli, B. and Cysewski, G. R. (2011). Spirulina: Nature's superfood. Cyanotech Corporation.
Muthulakshmi, M., Saranya, A., Sudha, M. and Selvakumar, G. (2012). Extraction, partial purification, and antibacterial activity of phycocyanin from Spirulina isolated from fresh water body against various human pathogens. Journal of Algal Biomass Utilization, 3(3): 7-11.
Martelli, G., Folli, C., Visai, L., Daglia, M. and Ferrari, D. (2014). Thermal stability improvement of blue colorant C-Phycocyanin from Spirulina platensis for food industry applications. Process Biochemistry, 49(1): 154-159.
Mohite, Y. S., Shrivastava, N. D. and Sahu, D. G. (2015). Antimicrobial activity of C-phycocyanin from Arthrospira platensis isolated from extreme haloalkaline environment of Lonar Lake. Journal of Environmental Science, Toxicology and Food Technology, 1(4): 40-45.
Mazinani, S., Fadaie, V. and Khosravi-Darani., K. (2015). Viability of Lactobacillus acidophilus in sinbiotic ultrafiltration white cheese containing powdered menthe longifolia L. and Spirulina platensis. Iranian Journal of Nutrition Sciences and Food Technology, 9(4): 109-116 [In Persian].
Minato, T., Teramoto, T., Adachi, N., Hung, N. K., Yamada, K., Kawasaki, M. and Yoon, K. S. (2021). Non-conventional octameric structure of C-phycocyanin. Communications Biology, 4(1): 1-10.
Norton, R. A. (1997). Effect of carotenoids on aflatoxin B1 synthesis by Aspergillus flavus. Phytopathology, 87(8): 814-821.
Nagaraj, M., Sunitha, S. and Varalakshmi, P. (2000). Effect of lupeol, a pentacyclic triterpene, on the lipid peroxidation and antioxidant status in rat kidney after chronic cadmium exposure. Journal of Applied Toxicology: an international journal, 20(5): 413-417.
Nemoto-Kawamura, C., Hirahashi, T., Nagai, T., Yamada, H., Katoh, T. and HAYAsHI, O. (2004). Phycocyanin enhances secretary IgA antibody response and suppresses allergic IgE antibody response in mice immunized with antigen-entrapped biodegradable microparticles. Journal of Nutritional Science and Vitaminology, 50(2): 129-136.
Nagpal, N., Munjal, N. and Chatterjee, S. (2011). Microbial pigments with health benefits-a mini review. Trend in Biosciences, 4 (1): 157-160.
Nuhu, A. A. (2013). Spirulina (Arthrospira): An important source of nutritional and medicinal compounds. Journal of Marine Biology, 1-8.
Pulz, O. and Gross, W. (2004). Valuable products from biotechnology of microalgae. Applied Microbiology and Biotechnology, 65(6): 635-648.
Patel, A., Mishra, S. and Ghosh, P. K. (2006). Antioxidant potential of C-phycocyanin isolated from cyanobacterial species Lyngbya, Phormidium and Spirulina spp. Indian Journal of Biochemistry and Biophysics, 43 (1): 25-31.
Patil, G., Chethana, S., Madhusudhan, M. C. and Raghavarao, K. S. M. S. (2008). Fractionation and purification of the phycobiliproteins from Spirulina platensis. Bioresource Technology, 99(15): 7393-7396.
Pentón-Rol, G., Marín-Prida, J., Pardo-Andreu, G., Martínez-Sánchez, G., Acosta-Medina, E. F., Valdivia-Acosta, A. and Pentón-Arias, E. (2011). C-Phycocyanin is neuroprotective against global cerebral ischemia/reperfusion injury in gerbils. Brain Research Bulletin, 86(1-2): 42-52.
Prabakaran, P. and Ravindran, A. D. (2013). Efficacy of different extraction methods of phycocyanin from Spirulina platensis. International Journal of Research in Pharmacy and Life Sciences, 1(1): 15-20.
Parniakov, O., Barba, F. J., Grimi, N., Marchal, L., Jubeau, S., Lebovka, N. and Vorobiev, E. (2015). Pulsed electric field assisted extraction of nutritionally valuable compounds from microalgae Nannochloropsis spp. using the binary mixture of organic solvents and water. Innovative Food Science and Emerging Technologies, 27 (1): 79-85.
Pan, R., Lu, R., Zhang, Y., Zhu, M., Zhu, W., Yang, R. and Bao, Q. (2015). Spirulina phycocyanin induces differential protein expression and apoptosis in SKOV-3 cells. International Journal of Biological Macromolecules, 81 (1): 951-959.
Romay, C. H., Gonzalez, R., Ledon, N., Remirez, D. and Rimbau, V. (2003). C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Current Protein and Peptide Science, 4(3): 207-216.
Rostagno, M. A., Palma, M. and Barroso, C. G. (2003). Ultrasound-assisted extraction of soy isoflavones. Journal of Chromatography A, 1012(2): 119-128.
Rymbai, H., Sharma, R. R. and Srivastav, M. (2011). Bio-colorants and its implications in health and food industry–a review. International Journal of Pharmacological Research, 3(4): 2228-2244.
Shotipruk, A., Kaufman, P. B., and Wang, H. Y. (2001). Feasibility study of repeated harvesting of menthol from biologically viable menthaxpiperata using ultrasonic extraction. Biotechnology Progress, 17(5): 924-928.
Saleem, M., Afaq, F., Adhami, V. M. and Mukhtar, H. (2004). Lupeol modulates NF-κB and PI3K/Akt pathways and inhibits skin cancer in CD-1 mice. Oncogene, 23(30): 5203-5214.
Spolaore, P., Joannis-Cassan, C., Duran, E. and Isambert, A. (2006). Commercial applications of microalgae. Journal of Bioscience and Bioengineering, 101(2): 87-96.
Saini, M. K., Sanyal, S. N. and Vaiphei, K. (2012). Piroxicam and C-phycocyanin mediated apoptosis in 1, 2-dimethylhydrazine dihydrochloride induced colon carcinogenesis: exploring the mitochondrial pathway. Nutrition and Cancer, 64(3): 409-418.
Salehifar, M., Shahbazizadeh, S., Khosravi- Darani., K., Behmadi, H. and Ferdowsi, R. (2013). Possibility of using microalgae Spirulina platensis powder in industrial production of Iranian traditional cookies. Iranian Journal of Nutrition Sciences and Food Technology, 7(4): 63-72 [In Persian].
Saranraj, P. and Sivasakthi, S. (2014). Spirulina platensis–food for future: a review. Asian Journal of Pharmaceutical Science and Technology, 4(1): 26-33.
Sivasankari, S. and Ravindran, D. (2014). Comparison of different extraction methods for phycocyanin extraction and yield from Spirulina platensis. International Journal of Current Microbiology and Applied Sciences, 3(8): 904-909.
Sonani, R. R., Singh, N. K., Kumar, J., Thakar, D. and Madamwar, D. (2014). Concurrent purification and antioxidant activity of phycobiliproteins from Lyngbya sp. A09DM: An antioxidant and anti-aging potential of phycoerythrin in Caenorhabditis elegans. Process Biochemistry, 49(10): 1757-1766.
Sitohy, M., Osman, A., Ghany, A. G. A. and Salama, A. (2015). Antibacterial phycocyanin from Anabaena oryzae SOS13. International Journal of Applied Research in Natural Products, 8(4): 27-36.
Suzery, M., Majid, D., Setyawan, D. and Sutanto, H. (2017). Improvement of stability and antioxidant activities by using phycocyanin-chitosan encapsulation technique. In IOP Conference Series: Earth and Environmental Science (Vol. 55, No. 1, p. 012052). IOP Publishing.
Safari, R., Raftani Amiri, Z. and Esmailzadeh Kenari, R. (2018). Optimizing the extraction of phycocyanin pigment from Spirulina platensis algae and investigating the qualitative properties of the microcoated pigment. Ph.D. Thesis, Sari Agricultural Sciences and Natural Resources University [In Persian].
Safari, R., Raftani Amiri, Z. and Esmaeilzadeh Kenari, R. (2020). Antioxidant and antibacterial activities of C-phycocyanin from common name Spirulina platensis. Iranian Journal of Fisheries Sciences, 19(4): 1911-1927.
Safari, R., Raftani Amiri, Z., Reyhani Poul, S. and Ghaffari, H. (2022a). Nanoencapsulation of phycocyanin extracted from the alga Spirulina (Spirulina platensis) and use of resulting nanoparticles in ice cream formulation. Iranian Journal of Food Science and Technology, 123 (19): 145-159 [In Persian].
Safari, R., Raftani Amiri, Z., Reyhani Poul, S. and Esmaeilzadeh Kenari, R. (2022b). Evaluation and comparison of antioxidant and antibacterial properties of phycocyanin extracted from spirulina microalgae (Spirulina Platensis) in both pure and nanoencasulated forms with maltodextrin-sodium caseinate combination coating. Iranian Journal of Food Science and Technology, 127 (19): 1-15 [In Persian].
Tantirapan, P. and Suwanwong, Y. (2014). Anti-proliferative effects of C-phycocyanin on a human leukemic cell line and induction of apoptosis via the PI3K/AKT pathway. Journal of Chemical and Pharmaceutical Research, 6(5): 1295-1301.
Vinatoru, M. (2001). An overview of the ultrasonically assisted extraction of bioactive principles from herbs. Ultrasonics Sonochemistry, 8(3): 303-313.
Wu, Z., Duangmanee, P., Zhao, P., Juntawong, N. and Ma, C. (2016). The effects of light, temperature, and nutrition on growth and pigment accumulation of three Dunaliella salina strains isolated from saline soil. Jundishapur Journal of Microbiology, 9(1): 1-9.
Ying, Z., Han, X. and Li, J. (2011). Ultrasound-assisted extraction of polysaccharides from mulberry leaves. Food Chemistry, 127(3): 1273-1279.
Yu, P., Wu, Y., Wang, G., Jia, T. and Zhang, Y. (2017). Purification and bioactivities of phycocyanin. Critical Reviews in Food Science and Nutrition, 57(18): 3840-3849.
Zbinden, M. D. A., Sturm, B. S., Nord, R. D., Carey, W. J., Moore, D., Shinogle, H. and Stagg‐Williams, S. M. (2013). Pulsed electric field (PEF) as an intensification pretreatment for greener solvent lipid extraction from microalgae. Biotechnology and Bioengineering, 110(6): 1605-1615.
Zheng, J., Inoguchi, T., Sasaki, S., Maeda, Y., McCarty, M. F., Fujii, M. and Takayanagi, R. (2013). Phycocyanin and phycocyanobilin from Spirulina platensis protect against diabetic nephropathy by inhibiting oxidative stress. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 304(2): 110-120.
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Apt, K. E., Collier, J. L. and Grossman, A. R. (1995). Evolution of the phycobiliproteins. Journal of Molecular Biology, 248(1): 79-96.
Abalde, J., Betancourt, L., Torres, E., Cid, A. and Barwell, C. (1998). Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus IO9201. Plant Science, 136(1): 109-120.
Agustini, T. W., Ma’ruf, W. F. and Wibowo, B. A. (2017). Study on the effect of different concentration of Spirulina platensis paste added into dried noodle to its quality characteristics. In IOP Conference Series: Earth and Environmental Science (Vol. 55, No. 1, p. 012068). IOP Publishing.
Barberan F. A. (1997). Determination of authenticity of fruit jams by HPLC analysis of anthocyanins. Journal of the Science of Food and Agriculture, 73(2): 207-213.
Barbarino, E. and Lourenço, S. O. (2005). An evaluation of methods for extraction and quantification of protein from marine macro-and microalgae. Journal of Applied Phycology, 17(5): 447-460.
Bermejo, P., Piñero, E. and Villar, Á. M. (2008). Iron-chelating ability and antioxidant properties of phycocyanin isolated from a protean extract of Spirulina platensis. Food Chemistry, 110(2): 436-445.
Bingula, R., Dupuis, C., Pichon, C., Berthon, J. Y., Filaire, M., Pigeon, L. and 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. Journal of Oncology, 1-12.
Bleakley, S. and Hayes, M. (2017). Algal proteins: extraction, application, and challenges concerning production. Foods, 6(5): 1-34.
Chattopadhyay, P., Chatterjee, S., and Sen, S. K. (2008). Biotechnological potential of natural food grade biocolorants. African Journal of Biotechnology, 7(17): 2972-2985.
Chaiklahan, R., Chirasuwan, N. and Bunnag, B. (2012). Stability of phycocyanin extracted from Spirulina sp.: Influence of temperature, pH and preservatives. Process Biochemistry, 47(4): 659-664.
Coustets, M., Al-Karablieh, N., Thomsen, C. and Teissié, J. (2013). Flow process for electroextraction of total proteins from microalgae. Journal of Membrane Biology, 246(10): 751-760.
Deng, R. and Chow, T. J. (2010). Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovascular Therapeutics, 28(4): 33-45.
Dewi, E. N., Purnamayati, L. and Kurniasih, R. A. (2016). Antioxidant activities of phycocyanin microcapsules using maltodextrin and carrageenan as coating materials. Jurnal Teknologi, 78(4-2): 45-50
Estrada, J. P., Bescós, P. B. and Del Fresno, A. V. (2001). Antioxidant activity of different fractions of Spirulina platensis protean extract. II Farmaco, 56(5-7): 497-500.
Eriksen, N. T. (2008). Production of phycocyanin—a pigment with applications in biology, biotechnology, foods and medicine. Applied Microbiology and Biotechnology, 80(1): 1-14.
El-Baz, F. K., El-Senousy, W. M., El-Sayed, A. B. and Kamel, M. M. (2013). In vitro antiviral and antimicrobial activities of Spirulina platensis extract. Journal of Applied Pharmaceutical Science, 3(12): 52-56.
Filimon, R. (2010). Plants pigments with therapeutic potential from horticultural products. Seria Agro, 52 (1): 668-673.
Graverholt, O. S. and Eriksen, N. T. (2007). Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Applied Microbiology and Biotechnology, 77(1): 69-75.
Gantar, M., Dhandayuthapani, S. and Rathinavelu, A. (2012). Phycocyanin induces apoptosis and enhances the effect of topotecan on prostate cell line LNCaP. Journal of Medicinal Food, 15(12): 1091-1095.
Goettel, M., Eing, C., Gusbeth, C., Straessner, R. and Frey, W. (2013). Pulsed electric field assisted extraction of intracellular valuables from microalgae. Algal Research, 2(4): 401-408.
Hsiao, G., Chou, P. H., Shen, M. Y., Chou, D. S., Lin, C. H. and Sheu, J. R. (2005). C-phycocyanin, a very potent and novel platelet aggregation inhibitor from Spirulina platensis. Journal of Agricultural and Food Chemistry, 53(20): 7734-7740.
Higuera-Ciapara, I., Felix-Valenzuela, L. and Goycoolea, F. M. (2006). Astaxanthin: a review of its chemistry and applications. Critical Reviews in Food Science and Nutrition, 46(2): 185-196.
Hosseini, S., Shahbazizadeh, S., Khosravi-Darani, K. and Reza Mozafari, M. (2013). Spirulina paltensis: Food and function. Current Nutrition and Food Science, 9(3): 189-193.
Harnedy, P. A. and FitzGerald, R. J. (2013). Extraction of protein from the macroalga Palmaria palmata. LWT-Food Science and Technology, 51(1): 375-382.
Ismaiel, M., El-Ayouty, Y. M. and Piercey-Normore, M. D. (2014). Antioxidants characterization in selected cyanobacteria. Annals of Microbiology, 64(3): 1223-1230.
Jespersen, L., Strømdahl, L. D., Olsen, K. and Skibsted, L. H. (2005). Heat and light stability of three natural blue colorants for use in confectionery and beverages. European Food Research and Technology, 220(3): 261-266.
Janczyk, P., Wolf, C. and Souffrant, W. B. (2005). Evaluation of nutritional value and safety of the green microalgae Chlorella vulgaris treated with novel processing methods. Arch Zootech, 8 (1): 132-147.
Joubert, Y. and Fleurence, J. (2008). Simultaneous extraction of proteins and DNA by an enzymatic treatment of the cell wall of Palmaria palmata (Rhodophyta). Journal of Applied Phycology, 20(1): 55-61.
Jaswir, I., Noviendri, D., Hasrini, R. F. and Octavianti, F. (2011). Carotenoids: Sources, medicinal properties and their application in food and nutraceutical industry. Journal of Medicinal Plants Research, 5(33): 7119-7131.
Joventino, I. P., Alves, H. G., Neves, L. C., Pinheiro-Joventino, F., Leal, L. K. A., Neves, S. A. and Viana, G. B. (2012). The microalga Spirulina platensis presents anti-inflammatory action as well as hypoglycemic and hypolipidemic properties in diabetic rats. Journal of Complementary and Integrative Medicine: 9(1): 1-24.
Jerley, A. and Prabu, M. (2015) Purification, characterization and antioxidant properties of C-Phycocyanin from Spirulina platensis. Scrutiny International Research Journal of Agriculture, Plant Biotechnology and Bio Products, 2(1): 7-15.
Kleinegris, D. M., Janssen, M., Brandenburg, W. A. and Wijffels, R. H. (2011). Continuous production of carotenoids from Dunaliella salina. Enzyme and Microbial Technology, 48(3): 253-259.
(2011). Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound. Journal of Medicinal Plants Research, 5(32): 7043-7048.
Kuddus, M., Singh, P., Thomas, G. and Al-Hazimi, A. (2013). Recent developments in production and biotechnological applications of C-phycocyanin. BioMed Research International, 1-9.
Li, B., Chu, X., Gao, M. and Li, W. (2010). Apoptotic mechanism of MCF-7 breast cells in vivo and in vitro induced by photodynamic therapy with C-phycocyanin. Acta Biochimica et Biophysica Sinica, 42(1): 80-89.
Li, B., Gao, M. H., Chu, X. M., Teng, L., Lv, C. Y., Yang, P. and Yin, Q. F. (2015). The synergistic antitumor effects of all-trans retinoic acid and C-phycocyanin on the lung cancer A549 cells in vitro and in vivo. European Journal of Pharmacology, 749: 107-114.
McClements, D. J. (1995). Advances in the application of ultrasound in food analysis and processing. Trends in Food Science and Technology, 6(9): 293-299.
Mishra, S. K., Shrivastav, A. and Mishra, S. (2008). Effect of preservatives for food grade C-PC from Spirulina platensis. Process Biochemistry, 43(4): 339-345.
Mala, R., Sarojini, M., Saravanababu, S. and Umadevi, G. (2009). Screening for antimicrobial activity of crude extracts of Spirulina platensis. Journal of Cell and Tissue Research, 9(3): 1951-1955
Moraes, C. C., Sala, L., Cerveira, G. P. and Kalil, S. J. (2011). C-phycocyanin extraction from Spirulina platensis wet biomass. Brazilian Journal of Chemical Engineering, 28 (1): 45-49.
Moorhead, K., Capelli, B. and Cysewski, G. R. (2011). Spirulina: Nature's superfood. Cyanotech Corporation.
Muthulakshmi, M., Saranya, A., Sudha, M. and Selvakumar, G. (2012). Extraction, partial purification, and antibacterial activity of phycocyanin from Spirulina isolated from fresh water body against various human pathogens. Journal of Algal Biomass Utilization, 3(3): 7-11.
Martelli, G., Folli, C., Visai, L., Daglia, M. and Ferrari, D. (2014). Thermal stability improvement of blue colorant C-Phycocyanin from Spirulina platensis for food industry applications. Process Biochemistry, 49(1): 154-159.
Mohite, Y. S., Shrivastava, N. D. and Sahu, D. G. (2015). Antimicrobial activity of C-phycocyanin from Arthrospira platensis isolated from extreme haloalkaline environment of Lonar Lake. Journal of Environmental Science, Toxicology and Food Technology, 1(4): 40-45.
Mazinani, S., Fadaie, V. and Khosravi-Darani., K. (2015). Viability of Lactobacillus acidophilus in sinbiotic ultrafiltration white cheese containing powdered menthe longifolia L. and Spirulina platensis. Iranian Journal of Nutrition Sciences and Food Technology, 9(4): 109-116 [In Persian].
Minato, T., Teramoto, T., Adachi, N., Hung, N. K., Yamada, K., Kawasaki, M. and Yoon, K. S. (2021). Non-conventional octameric structure of C-phycocyanin. Communications Biology, 4(1): 1-10.
Norton, R. A. (1997). Effect of carotenoids on aflatoxin B1 synthesis by Aspergillus flavus. Phytopathology, 87(8): 814-821.
Nagaraj, M., Sunitha, S. and Varalakshmi, P. (2000). Effect of lupeol, a pentacyclic triterpene, on the lipid peroxidation and antioxidant status in rat kidney after chronic cadmium exposure. Journal of Applied Toxicology: an international journal, 20(5): 413-417.
Nemoto-Kawamura, C., Hirahashi, T., Nagai, T., Yamada, H., Katoh, T. and HAYAsHI, O. (2004). Phycocyanin enhances secretary IgA antibody response and suppresses allergic IgE antibody response in mice immunized with antigen-entrapped biodegradable microparticles. Journal of Nutritional Science and Vitaminology, 50(2): 129-136.
Nagpal, N., Munjal, N. and Chatterjee, S. (2011). Microbial pigments with health benefits-a mini review. Trend in Biosciences, 4 (1): 157-160.
Nuhu, A. A. (2013). Spirulina (Arthrospira): An important source of nutritional and medicinal compounds. Journal of Marine Biology, 1-8.
Pulz, O. and Gross, W. (2004). Valuable products from biotechnology of microalgae. Applied Microbiology and Biotechnology, 65(6): 635-648.
Patel, A., Mishra, S. and Ghosh, P. K. (2006). Antioxidant potential of C-phycocyanin isolated from cyanobacterial species Lyngbya, Phormidium and Spirulina spp. Indian Journal of Biochemistry and Biophysics, 43 (1): 25-31.
Patil, G., Chethana, S., Madhusudhan, M. C. and Raghavarao, K. S. M. S. (2008). Fractionation and purification of the phycobiliproteins from Spirulina platensis. Bioresource Technology, 99(15): 7393-7396.
Pentón-Rol, G., Marín-Prida, J., Pardo-Andreu, G., Martínez-Sánchez, G., Acosta-Medina, E. F., Valdivia-Acosta, A. and Pentón-Arias, E. (2011). C-Phycocyanin is neuroprotective against global cerebral ischemia/reperfusion injury in gerbils. Brain Research Bulletin, 86(1-2): 42-52.
Prabakaran, P. and Ravindran, A. D. (2013). Efficacy of different extraction methods of phycocyanin from Spirulina platensis. International Journal of Research in Pharmacy and Life Sciences, 1(1): 15-20.
Parniakov, O., Barba, F. J., Grimi, N., Marchal, L., Jubeau, S., Lebovka, N. and Vorobiev, E. (2015). Pulsed electric field assisted extraction of nutritionally valuable compounds from microalgae Nannochloropsis spp. using the binary mixture of organic solvents and water. Innovative Food Science and Emerging Technologies, 27 (1): 79-85.
Pan, R., Lu, R., Zhang, Y., Zhu, M., Zhu, W., Yang, R. and Bao, Q. (2015). Spirulina phycocyanin induces differential protein expression and apoptosis in SKOV-3 cells. International Journal of Biological Macromolecules, 81 (1): 951-959.
Romay, C. H., Gonzalez, R., Ledon, N., Remirez, D. and Rimbau, V. (2003). C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Current Protein and Peptide Science, 4(3): 207-216.
Rostagno, M. A., Palma, M. and Barroso, C. G. (2003). Ultrasound-assisted extraction of soy isoflavones. Journal of Chromatography A, 1012(2): 119-128.
Rymbai, H., Sharma, R. R. and Srivastav, M. (2011). Bio-colorants and its implications in health and food industry–a review. International Journal of Pharmacological Research, 3(4): 2228-2244.
Shotipruk, A., Kaufman, P. B., and Wang, H. Y. (2001). Feasibility study of repeated harvesting of menthol from biologically viable menthaxpiperata using ultrasonic extraction. Biotechnology Progress, 17(5): 924-928.
Saleem, M., Afaq, F., Adhami, V. M. and Mukhtar, H. (2004). Lupeol modulates NF-κB and PI3K/Akt pathways and inhibits skin cancer in CD-1 mice. Oncogene, 23(30): 5203-5214.
Spolaore, P., Joannis-Cassan, C., Duran, E. and Isambert, A. (2006). Commercial applications of microalgae. Journal of Bioscience and Bioengineering, 101(2): 87-96.
Saini, M. K., Sanyal, S. N. and Vaiphei, K. (2012). Piroxicam and C-phycocyanin mediated apoptosis in 1, 2-dimethylhydrazine dihydrochloride induced colon carcinogenesis: exploring the mitochondrial pathway. Nutrition and Cancer, 64(3): 409-418.
Salehifar, M., Shahbazizadeh, S., Khosravi- Darani., K., Behmadi, H. and Ferdowsi, R. (2013). Possibility of using microalgae Spirulina platensis powder in industrial production of Iranian traditional cookies. Iranian Journal of Nutrition Sciences and Food Technology, 7(4): 63-72 [In Persian].
Saranraj, P. and Sivasakthi, S. (2014). Spirulina platensis–food for future: a review. Asian Journal of Pharmaceutical Science and Technology, 4(1): 26-33.
Sivasankari, S. and Ravindran, D. (2014). Comparison of different extraction methods for phycocyanin extraction and yield from Spirulina platensis. International Journal of Current Microbiology and Applied Sciences, 3(8): 904-909.
Sonani, R. R., Singh, N. K., Kumar, J., Thakar, D. and Madamwar, D. (2014). Concurrent purification and antioxidant activity of phycobiliproteins from Lyngbya sp. A09DM: An antioxidant and anti-aging potential of phycoerythrin in Caenorhabditis elegans. Process Biochemistry, 49(10): 1757-1766.
Sitohy, M., Osman, A., Ghany, A. G. A. and Salama, A. (2015). Antibacterial phycocyanin from Anabaena oryzae SOS13. International Journal of Applied Research in Natural Products, 8(4): 27-36.
Suzery, M., Majid, D., Setyawan, D. and Sutanto, H. (2017). Improvement of stability and antioxidant activities by using phycocyanin-chitosan encapsulation technique. In IOP Conference Series: Earth and Environmental Science (Vol. 55, No. 1, p. 012052). IOP Publishing.
Safari, R., Raftani Amiri, Z. and Esmailzadeh Kenari, R. (2018). Optimizing the extraction of phycocyanin pigment from Spirulina platensis algae and investigating the qualitative properties of the microcoated pigment. Ph.D. Thesis, Sari Agricultural Sciences and Natural Resources University [In Persian].
Safari, R., Raftani Amiri, Z. and Esmaeilzadeh Kenari, R. (2020). Antioxidant and antibacterial activities of C-phycocyanin from common name Spirulina platensis. Iranian Journal of Fisheries Sciences, 19(4): 1911-1927.
Safari, R., Raftani Amiri, Z., Reyhani Poul, S. and Ghaffari, H. (2022a). Nanoencapsulation of phycocyanin extracted from the alga Spirulina (Spirulina platensis) and use of resulting nanoparticles in ice cream formulation. Iranian Journal of Food Science and Technology, 123 (19): 145-159 [In Persian].
Safari, R., Raftani Amiri, Z., Reyhani Poul, S. and Esmaeilzadeh Kenari, R. (2022b). Evaluation and comparison of antioxidant and antibacterial properties of phycocyanin extracted from spirulina microalgae (Spirulina Platensis) in both pure and nanoencasulated forms with maltodextrin-sodium caseinate combination coating. Iranian Journal of Food Science and Technology, 127 (19): 1-15 [In Persian].
Tantirapan, P. and Suwanwong, Y. (2014). Anti-proliferative effects of C-phycocyanin on a human leukemic cell line and induction of apoptosis via the PI3K/AKT pathway. Journal of Chemical and Pharmaceutical Research, 6(5): 1295-1301.
Vinatoru, M. (2001). An overview of the ultrasonically assisted extraction of bioactive principles from herbs. Ultrasonics Sonochemistry, 8(3): 303-313.
Wu, Z., Duangmanee, P., Zhao, P., Juntawong, N. and Ma, C. (2016). The effects of light, temperature, and nutrition on growth and pigment accumulation of three Dunaliella salina strains isolated from saline soil. Jundishapur Journal of Microbiology, 9(1): 1-9.
Ying, Z., Han, X. and Li, J. (2011). Ultrasound-assisted extraction of polysaccharides from mulberry leaves. Food Chemistry, 127(3): 1273-1279.
Yu, P., Wu, Y., Wang, G., Jia, T. and Zhang, Y. (2017). Purification and bioactivities of phycocyanin. Critical Reviews in Food Science and Nutrition, 57(18): 3840-3849.
Zbinden, M. D. A., Sturm, B. S., Nord, R. D., Carey, W. J., Moore, D., Shinogle, H. and Stagg‐Williams, S. M. (2013). Pulsed electric field (PEF) as an intensification pretreatment for greener solvent lipid extraction from microalgae. Biotechnology and Bioengineering, 110(6): 1605-1615.
Zheng, J., Inoguchi, T., Sasaki, S., Maeda, Y., McCarty, M. F., Fujii, M. and Takayanagi, R. (2013). Phycocyanin and phycocyanobilin from Spirulina platensis protect against diabetic nephropathy by inhibiting oxidative stress. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 304(2): 110-120.
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