Top

Published in:

2020 | OriginalPaper | Chapter

8. Analytical Protocols in Phycobiliproteins Analysis

Authors : Milan R. Nikolic, Simeon Minic, Mirjana Macvanin, Dragana Stanic-Vucinic, Tanja Cirkovic Velickovic

Published in: Pigments from Microalgae Handbook

Publisher: Springer International Publishing

Activate our intelligent search to find suitable subject content or patents.

search-config

AI-assisted search

Off

Abstract

The aim of this chapter is to review and discuss methodology and protocols in the analysis of phycobiliproteins (phycocyanins, allophycocyanins, and phycoerythrins) and their chromophores. Due to the presence of multiple covalently bound open-chain tetrapyrrole chromophores, phycobiliproteins are colored and strongly fluorescent molecules, with high absorption coefficients (10⁵ to 10⁶) and excellent fluorescent quantum yield (0.51 up to 0.98). Therefore, a vast number of methods for phycobiliproteins analysis is based on these spectral characteristics, whereas assessment of their bioactivity is related to their exceptional redox and metal-chelating properties. This chapter is dedicated to methods used for isolation and purification, structure analysis, physicochemical properties and stability characterization, quantification, as well as in vitro and in vivo biological activities evaluation. In addition, emerging approaches related to phycobiliproteins analysis are also reviewed including interactions with other biomolecules and ions and identification of phycobiliprotein (chromo)peptides by mass spectrometry.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

inform now

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

inform now

previous chapter Analytical Protocols in Carotenoid Analysis

next chapter Analytical Protocols in Antioxidant Capacity Measurement

Adir, N., Vainer, R., & Lerner, N. (2002). Refined structure of c-phycocyanin from the cyanobacterium Synechococcus vulcanus at 1.6 angstrom: Insights into the role of solvent molecules in thermal stability and co-factor structure. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1556, 168–174.

Aghtar, M., Strumpfer, J., Olbrich, C., Schulten, K., & Kleinekathofer, U. (2014). Different types of vibrations interacting with electronic excitations in phycoerythrin 545 and Fenna-Matthews-Olson Antenna systems. The Journal of Physical Chemistry Letters, 5, 3131–3137.PubMed

Almog, R., Marsilio, F., & Berns, D. S. (1988). Interaction of C-phycocyanin with lipid monolayers under nitrogen and in the presence of air. Archives of Biochemistry and Biophysics, 260, 28–36.PubMed

Angeleri, M., Muth-Pawlak, D., Aro, E. M., & Battchikova, N. (2016). Study of O-phosphorylation sites in proteins involved in photosynthesis-related processes in synechocystis sp strain PCC 6803: Application of the SRM approach. Journal of Proteome Research, 15, 4638–4652.PubMed

Anwer, K., Sonani, R., Madamwar, D., Singh, P., Khan, F., Bisetty, K., et al. (2015). Role of N-terminal residues on folding and stability of C-phycoerythrin: Simulation and urea-induced denaturation studies. Journal of Biomolecular Structure & Dynamics, 33, 121–133.

Beer, S., & Eshel, A. (1985). Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Australian Journal of Marine and Freshwater Research, 36, 785–793.

Bellissent-Funel, M. C. (2004). Internal motions in proteins: A combined neutron scattering and molecular modelling approach. Pramana – Journal of Physics, 63, 91–97.

Benedetti, S., Benvenuti, F., Pagliarani, S., Francogli, S., Scoglio, S., & Canestrari, F. (2004). Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sciences, 75, 2353–2362.PubMed

Bennett, A., & Borogad, L. (1973). Complementary chromatic adaptation in a filamentous bluegreen alga. Journal of Cell Biology, 58, 419–435.PubMed

Berkelman, T. R., & Lagarias, J. C. (1986). Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Analytical Biochemistry, 156, 194–201.PubMed

Berns, D. S., & MacColl, R. (1989). Phycocyanin in Physical-Chemical Studies. Chemical Reviews, 89, 807–825.

Bhattacharya, S., Bhayani, K., Ghosh, T., Bajaj, S., Trivedi, N., & Mishra, S. (2018). Stability of phycobiliproteins using natural preservative ε-Polylysine (ε-PL). Journal of Fermentation TechnologyJournal of Fermentation Technology, 7, 149.

Bhayani, K., Mitra, M., Ghosh, T., & Mishra, S. (2016). C-Phycocyanin as a potential biosensor for heavy metals like Hg2+ in aquatic systems. RSC Advances, 6, 111599–111605.

Blau, S. M., Bennett, D. I. G., Kreisbeck, C., Scholes, G. D., & Aspuru-Guzik, A. (2018). Local protein solvation drives direct down-conversion in phycobiliprotein PC645 via incoherent vibronic transport. Proceedings of the National Academy of Sciences of the United States of America, 115, E3342–E3350.PubMedPubMedCentral

Bleakley, S., Hayes, M., 2017. Algal proteins: Extraction, application, and challenges concerning production. Foods 6, pii: E33.

Braga, A. R. C., da Silva Figueira, F., da Silveira, J. T., de Morais, M. G., Costa, J. A. V., & Kalil, V. S. J. (2016). Improvement of thermal stability of C-phycocyanin by nanofiber and preservative agents. Journal of Food Processing and Preservation, 40, 1264–1269.

Cai, C., Wang, Y., Li, C., Guo, Z., Jia, R., Wu, W., et al. (2014). Purification and photodynamic bioactivity of phycoerythrin and phycocyanin from Porphyra yezoensis Ueda. Journal of Ocean University of China, 13, 479–484.

Cervantes-Llanos, M., Lagumersindez-Denis, N., Marín-Prida, J., Pavón-Fuentes, N., Falcon-Cama, V., Piniella-Matamoros, B., et al. (2018). Beneficial effects of oral administration of C-phycocyanin and phycocyanobilin in rodent models of experimental autoimmune encephalomyelitis. Life Sciences, 194, 130–138.PubMed

Chen, T., Wong, Y. S., & Zheng, W. (2006). Purification and characterization of selenium-containing phycocyanin from selenium-enriched Spirulina platensis. Phytochemistry, 67, 2424–2430.PubMed

Chen, H., Jiang, P., Li, F., & Wu, H. (2015a). Improving production of thermostable and fluorescent holo-beta-allophycocyanin by metabolically engineered Escherichia coli using response surface methodology. Preparative Biochemistry & Biotechnology, 45, 730–741.

Chen, Z., Zhan, J., Chen, Y., Yang, M., He, C., Ge, F., et al. (2015b). Effects of Phosphorylation of beta subunits of phycocyanins on state transition in the model cyanobacterium Synechocystis sp. PCC 6803. Plant & Cell Physiology, 56, 1997–2013.

Cherdkiatikul, T., & Suwanwong, Y. (2014). Production of the alpha and beta subunits of Spirulina allophycocyanin and C-phycocyanin in Escherichia coli: A comparative study of their antioxidant activities. Journal of Biomolecular Screening, 19, 959–965.PubMed

Cole, W. J., Chapman, D. J., & Siegelman, H. W. (1967). Structure of phycocyanobilin. Journal of the American Chemical Society, 89, 3643–3645.

Combet, S., & Zanotti, J. M. (2012). Further evidence that interfacial water is the main “driving force” of protein dynamics: A neutron scattering study on perdeuterated C-phycocyanin. Physical Chemistry Chemical Physics: PCCP, 14, 4927–4934.PubMed

Deschoenmaeker, F., Facchini, R., Leroy, B., Badri, H., Zhang, C. C., & Wattiez, R. (2014). Proteomic and cellular views of Arthrospira sp. PCC 8005 adaptation to nitrogen depletion. Microbiology, 160, 1224–1236.PubMed

Dufossé, L. (2018). Microbial pigments from bacteria, yeasts, fungi, and microalgae for the food and feed industries. In: A. Grumezescu, A.M. Holban (Eds.), Natural and artificial flavoring agents and food dyes. Handbook of food bioengineering, VII (pp. 113–132). Elsevier.

Dumay, J., Clement, N., Morancais, M., & Fleurence, J. (2013). Optimization of hydrolysis conditions of Palmaria palmata to enhance R-phycoerythrin extraction. Bioresource technology, 131, 21–27.PubMed

Eisenberg, I., Harris, D., Levi-Kalisman, Y., Yochelis, S., Shemesh, A., Ben-Nissan, G., et al. (2017). Concentration-based self-assembly of phycocyanin. Photosynthesis Research, 134, 39–49.PubMed

Elgabarty, H., Schmieder, P., & Sebastiani, D. (2013). Unraveling the existence of dynamic water channels in light-harvesting proteins: Alpha-C-phycocyanobilin in vitro. Chemical Science, 4, 755–763.

Farooq, S. M., Asokan, D., Kalaiselvi, P., Sakthivel, R., & Varalakshmi, P. (2004). Prophylactic role of phycocyanin: a study of oxalate mediated renal cell injury. Chemico-Biological Interactions, 149, 1–7.PubMed

Fu, E., Friedman, L. F. L., & Siegelman, H. W. (1979). Mass-spectral identification and purification of phycoerythrobilin and phycocyanobilin. Biochemical Journal, 179, 1–6.PubMedPubMedCentral

Fuszard, M.A., Ow, S. Y., Gan, C. S., Noirel, J., Ternan, N. G., McMullan, G., Biggs, C. A. et al. (2013). The quantitative proteomic response of Synechocystis sp. PCC6803 to phosphate acclimation. Aquatic Biosystems, 9, 5.

Galland-Irmouli, A. V., Pons, L., Lucon, M., Villaume, C., Mrabet, N. T., Gueant, J. L., et al. (2000). One-step purification of R-phycoerythrin from the red macroalga Palmaria palmata using preparative polyacrylamide gel electrophoresis. Journal of Chromatography B: Biomedical Sciences and Applications, 739, 117–123.PubMed

Gelagutashvili, E. (2013). Binding of heavy metals with C-phycocyanin: A comparison between equilibrium dialysis, fluorescence and absorption titration. American Journal of Biomedical and Life Sciences, 1, 12–16.

Golub, M., Combet, S., Wieland, D. C. F., Soloviov, D., Kuklin, A., Lokstein, H., et al. (2017). Solution structure and excitation energy transfer in phycobiliproteins of Acaryochloris marina investigated by small angle scattering. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1858, 318–324.

González, R., Rodríguez, S., Romay, C., Ancheta, O., González, A., Armesto, J., et al. (1999). Anti-inflammatory activity of phycocyanin extract in acetic acid-induced colitis in rats. Pharmacological Research, 39, 55–59.PubMed

González-Ramírez, E., Andújar-Sánchez, M., Ortiz-Salmerón, E., Bacarizo, J., Cuadri, C., Mazzuca-Sobczuk, T., et al. (2014). Thermal and pH stability of the B-phycoerythrin from the red algae Porphyridium cruentum. Food Biophysics, 9, 184–192.

Gwizdala, M., Kruger, T. P. J., Wahadoszamen, M., Gruber, J. M., & van Grondelle, R. (2018). Phycocyanin: one complex, two states, two functions. The Journal of Physical Chemistry Letters, 9, 1365–1371.PubMed

Hahn, J., Kuhne, R., & Schmieder, P. (2007). Solution-state (15)N NMR spectroscopic study of alpha-C-phycocyanin: Implications for the structure of the chromophore-binding pocket of the cyanobacterial phytochrome Cph1. ChemBioChem, 8, 2249–2255.PubMed

Hao, S., Yan, Y., Li, S., Zhao, L., Zhang, C., Liu, L., & Wang, C., (2018). The in vitro anti-tumor activity of phycocyanin against non-small cell lung cancer cells. Marine Drugs, 16, pii: E178.

Hermanson, G. (2013). Bioconjugate techniques (3rd ed.). Academic Press.

Herrera-Salgado, P., Leyva-Castillo, L. E., Rios-Castro, E., & Gomez-Lojero, C. (2018). Complementary chromatic and far-red photoacclimations in Synechococcus ATCC 29403 (PCC 7335). I: The phycobilisomes, a proteomic approach. Photosynthesis Research, 138, 39–56.PubMed

Isailovic, D., Li, H. W., & Yeung, E. S. (2004). Isolation and characterization of R-phycoerythrin subunits and enzymatic digests. Journal of Chromatography A, 1051, 119–130.PubMed

Isailovic, D., Sultana, I., Phillips, G. J., & Yeung, E. S. (2006). Formation of fluorescent proteins by the attachment of phycoerythrobilin to R-phycoerythrin alpha and beta apo-subunits. Analytical Biochemistry, 358, 38–50.PubMedPubMedCentral

Jiang, T., Zhang, J. P., Chang, W. R., & Liang, D. C. (2001). Crystal structure of R-phycocyanin and possible energy transfer pathways in the phycobilisome. Biophysical Journal, 81, 1171–1179.PubMedPubMedCentral

Jiang, L., Wang, Y., Liu, G., Liu, H., Zhu, F., Ji, H., et al. (2018). C-Phycocyanin exerts anti-cancer effects via the MAPK signaling pathway in MDA-MB-231 cells. Cancer Cell International, 18, 12.PubMedPubMedCentral

Kathiravan, A., Chandramohan, M., Renganathan, R., & Sekar, S. (2009). Spectroscopic studies on the interaction between phycocyanin and bovine serum albumin. Journal of Molecular Structure, 919, 210–214.

Kenny, O., Brunton, N. P., & Smyth, T. J. (2015). In vitro protocols for measuring the antioxidant capacity of algal extracts. In: D. Stengel & S. Connan (Eds.), Natural products from marine algae (pp. 375–402). Methods in molecular biology. New York: Humana Press, 1308.

Khan, M., Varadharaj, S., Shobha, J. C., Naidu, M. U., Parinandi, N. L., Kutala, V. K., et al. (2006). C-phycocyanin ameliorates doxorubicin-induced oxidative stress and apoptosis in adult rat cardiomyocytes. Journal of Cardiovascular Pharmacology, 47, 9–20.PubMed

Kieselbach, T., Cheregi, O., Green, B. R., & Funk, C. (2018). Proteomic analysis of the phycobiliprotein antenna of the cryptophyte alga Guillardia theta cultured under different light intensities. Photosynthesis Research, 135, 149–163.PubMed

Kim, E. Y., Choi, Y. H., & Nam, T. J. (2018). Identification and antioxidant activity of synthetic peptides from phycobiliproteins of Pyropia yezoensis. International Journal of Molecular Medicine, 42, 789–798.PubMedPubMedCentral

Koeper, I., Combet, S., Petry, W., & Bellissent-Funel, M. C. (2008). Dynamics of C-phycocyanin in various deuterated trehalose/water environments measured by quasielastic and elastic neutron scattering. European Biophysics Journal With Biophysics Letters, 37, 739–748.

Kumari, N., Narayan, O. P., & Rai, L. C. (2009). Understanding butachlor toxicity in Aulosira fertilissima using physiological, biochemical and proteomic approaches. Chemosphere, 77, 1501–1507.PubMed

Kumari, R. P., Sivakumar, J., Thankappan, B., & Anbarasu, K. (2013). C-phycocyanin modulates selenite-induced cataractogenesis in rats. Biological Trace Element Research, 151, 59–67.PubMed

Kursar, T. A., Vander, M. J., & Alberte, R. S. (1983). Light-harvesting system of the red alga Gracilaria tikvahiae. I Biochemical analysis of pigment mutations. Plant Physiology, 73, 353–360.PubMedPubMedCentral

Leney, A. C., Tschanz, A., & Heck, A. J. R. (2018). Connecting color with assembly in the fluorescent B-phycoerythrin protein complex. FEBS Journal, 285, 178–187.PubMed

Li, P., Ying, J., Chang, Q., Zhu, W., Yang, G., Xu, T., et al. (2016). Effects of phycoerythrin from Gracilaria lemaneiformis in proliferation and apoptosis of SW480 cells. Oncology Reports, 36, 3536–3544.PubMed

Li, W., Su, H. N., Pu, Y., Chen, J., Liu, L. N., Liu, Q., et al. (2019). Phycobiliproteins: Molecular structure, production, applications, and prospects. Biotechnology Advances, 37, 340–353.PubMed

Liao, G., Gao, B., Gao, Y., Yang, X., Cheng, X., & Ou, Y. (2016). Phycocyanin inhibits tumorigenic potential of pancreatic cancer cells: Role of apoptosis and autophagy. Scientific Reports, 6, 34564.PubMedPubMedCentral

Liu, L. N., Su, H. N., Yan, S. G., Shao, S. M., Xie, B. B., Chen, X. L., et al. (2009). Probing the pH sensitivity of R-phycoerythrin: Investigations of active conformational and functional variation. Biochimica et Biophysica Acta, 1787, 939–946.PubMed

MacColl, R., Eisele, L. E., & Menikh, A. (2003). Allophycocyanin: Trimers, monomers, subunits, and homodimers. Biopolymers, 72, 352–365.PubMed

Mackey, K. R. M., Post, A. F., McIlvin, M. R., & Saito, M. A. (2017). Physiological and proteomic characterization of light adaptations in marine Synechococcus. Environmental Microbiology, 19, 2348–2365.PubMed

Madamwar, D., Patel, D. K., Desai, S. N., Upadhyay, K. K., & Devkar, R. V. (2015). Apoptotic potential of C-phycoerythrin from Phormidium sp. A27DM and Halomicronema sp. A32DM on human lung carcinoma cells. EXCLI JournalEXCLI Journal, 14, 527–539.

Matallana-Surget, S., Derock, J., Leroy, B., Badri, H., Deschoenmaeker, F., & Wattiez, R. (2014). Proteome-wide analysis and diel proteomic profiling of the cyanobacterium Arthrospira platensis PCC 8005. PLoS ONE, 9, e99076.PubMedPubMedCentral

McGregor, A., Klartag, M., David, L., & Adir, N. (2008). Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. Journal of Molecular Biology, 384, 406–421.PubMed

Minic, S. L., Milcic, M., Stanic-Vucinic, D., Radibratovic, M., Sotiroudis, T. G., Nikolic, M. R., et al. (2015). Phycocyanobilin, a bioactive tetrapyrrolic compound of blue-green alga Spirulina, binds with high affinity and competes with bilirubin for binding on human serum albumin. RSC Advances, 5, 61787–61798.

Minic, S. L., Stanic-Vucinic, D., Mihailovic, J., Krstic, M., Nikolic, M. R., & Cirkovic Velickovic, T. (2016). Digestion by pepsin releases biologically active chromopeptides from C-phycocyanin, a blue-colored biliprotein of microalga Spirulina. Journal of Proteomics, 147, 132–139.PubMed

Minic, S., Radomirovic, M., Radibratovic, M., Milcic, M., Stanic-Vucinic, D., Nikolic, M., et al. (2018a). Characterization and effects of binding of food-derived bioactive phycocyanobilin to bovine serum albumin. Food Chemistry, 239, 1090–1099.PubMed

Minic, S., Radomirovic, M., Savkovic, N., Radibratovic, M., Mihailovic, J., Vasovic, T., et al. (2018b). Covalent binding of food-derived blue pigment phycocyanobilin to bovine beta-lactoglobulin under physiological conditions. Food Chemistry, 269, 43–52.PubMed

Mroginski, M. A., Mark, F., Thiel, W., & Hildebrandt, P. (2007). Quantum mechanics/molecular mechanics calculation of the Raman spectra of the phycocyanobilin chromophore in alpha-c-phycocyanin. Biophysical Journal, 93, 1885–1894.PubMedPubMedCentral

Muller, K., Engesser, R., Timmer, J., Nagy, F., Zurbriggen, M. D., & Weber, W. (2013). Synthesis of phycocyanobilin in mammalian cells. Chemical Communications (Cambridge, England), 49, 8970–8972.

Nair, D., Krishna, J. G., Panikkar, M. V. N., Nair, B. G., Pai, J. G., & Nair, S. S. (2018). Identification, purification, biochemical and mass spectrometric characterization of novel phycobiliproteins from a marine red alga, Centroceras clavulatum. International Journal of Biological Macromolecules, 114, 679–691.PubMed

Nikolova, D., Weber, D., Scholz, M., Bald, T., Scharsack, J. P., & Hippler, M. (2017). Temperature-induced remodeling of the photosynthetic machinery tunes photosynthesis in the thermophilic alga Cyanidioschyzon merolae. Plant Physiology, 174, 35–46.PubMedPubMedCentral

Niu, J. F., Wang, G. C., & Tseng, C. K. (2006). Method for large-scale isolation and purification of R-phycoerythrin from red alga Polysiphonia urceolata Grev. Protein Expression and Purification, 49, 23–31.PubMed

Oh, J. H., Kim, E. Y., & Nam, T. J. (2018). Phycoerythrin-derived tryptic peptide of a red Alga Pyropia yezoensis attenuates glutamate-induced ER stress and neuronal senescence in primary rat hippocampal neurons. Molecular Nutrition & Food Research, 62, e1700469.

Ovando, C. A., de Carvalho, J. C., Pereira, G. V. D., Jacques, P., Soccol, V. T., & Soccol, C. R. (2018). Functional properties and health benefits of bioactive peptides derived from Spirulina: A review. Food Reviews International, 34, 34–51.

Pan, Q., Chen, M., Li, J., Wu, Y., Zhen, C., & Liang, B. (2013). Antitumor function and mechanism of phycoerythrin from Porphyra haitanensis. Biological Research, 46, 87–95.PubMed

Pandey, G., Fatma, T., Cowsik, S. M., & Komath, S. S. (2009a). Specific interaction of jacalin with phycocyanin, a fluorescent phycobiliprotein. Journal of Photochemistry and Photobiology B, 97, 87–93.

Pandey, G., Fatma, T., & Komath, S. S. (2009b). Specific Interaction of the legume lectins, concanavalin A and peanut agglutinin, with phycocyanin. Photochemistry and Photobiology, 85, 1126–1133.PubMed

Paswan, M. B., Chudasama, M. M., Mitra, M., Bhayani, K., George, B., Chatterjee, S., et al. (2016). Fluorescence quenching property of C-phycocyanin from Spirulina platensis and its binding efficacy with viable cell components. Journal of Fluorescence, 26, 577–583.PubMed

Pleonsil, P., Soogarun, S., & Suwanwong, Y. (2013). Anti-oxidant activity of holo- and apo-c-phycocyanin and their protective effects on human erythrocytes. International Journal of Biological Macromolecules, 60, 393–398.PubMed

Puangploy, P., Oaew, S., & Surareungchai, W. (2015). Development of fluorescent phycocyanin-Cu²⁺ chemosensor for detection of homocysteine. International Journal of Bioscience, Biochemistry and Bioinformatics, 5, 241–248.

Purnamayati, L., Dewi, E. N., & Kurniasih, R. A. (2018). Phycocyanin stability in microcapsules processed by spray drying method using different inlet temperature. IOP Conference Series: Earth and Environmental Science, 116, 012076.

Rabier, J., & Vijayalakshmi, M. (1983). Affinity of phycocyanin chromopeptides to histidyl-sepharose gels: A model for histidine-tetrapyrrol-interactions in biliproteins. Zeitschrift für Naturforschung C, 38, 230–236.

Radibratovic, M., Minic, S., Stanic-Vucinic, D., Nikolic, M., Milcic, M., & Cirkovic Velickovic, T. (2016). Stabilization of human serum albumin by the binding of phycocyanobilin, a bioactive chromophore of blue-green alga Spirulina: Molecular dynamics and experimental Study. PLoS ONE, 11, e0167973.PubMedPubMedCentral

Rahman, D. Y., Sarian, F. D., van Wijk, A., Martinez-Garcia, M., & van der Maarel, M. J. E. C. (2017). Thermostable phycocyanin from the red microalga Cyanidioschyzon merolae, a new natural blue food colorant. Journal of Applied Phycology, 29, 1233–1239.PubMed

Ravi, M., Tentu, S., Baskar, G., Rohan Prasad, S., Raghavan, S., Jayaprakash, P., et al. (2015). Molecular mechanism of anti-cancer activity of phycocyanin in triple-negative breast cancer cells. BMC Cancer, 15, 768.PubMedPubMedCentral

Rimbau, V., Camins, A., Romay, C., González, R., & Pallàs, M. (1999). Protective effects of C-phycocyanin against kainic acid-induced neuronal damage in rat hippocampus. Neuroscience Letters, 276, 75–78.PubMed

Riss, J., Décordé, K., Sutra, T., Delage, M., Baccou, J. C., Jouy, N., et al. (2007). Phycobiliprotein C-phycocyanin from Spirulina platensis is powerfully responsible for reducing oxidative stress and NADPH oxidase expression induced by an atherogenic diet in hamsters. Journal of Agriculture and Food Chemistry, 55, 7962–7967.

Roda-Serrat, M. C., Christensen, K. V., El-Houri, R. B., Frette, X., & Christensen, L. P. (2018). Fast cleavage of phycocyanobilin from phycocyanin for use in food colouring. Food Chemistry, 240, 655–661.PubMed

Sampath-Wiley, P., & Neefus, C. (2007). An improved method for estimating R-phycoerythrin and R-phycocyanin contents from crude aqueous extracts of Porphyra (Bangiales, Rhodophyta). Journal of Applied Phycology, 19, 123–129.PubMed

Sathyasaikumar, K. V., Swapna, I., Reddy, P. V., Murthy, Ch R, Roy, K. R., Dutta Gupta, A., et al. (2007). Co-administration of C-phycocyanin ameliorates thioacetamide-induced hepatic encephalopathy in Wistar rats. Journal of the Neurological Sciences, 252, 67–75.PubMed

Sepúlveda-Ugarte, J., Brunet, J. E., Matamala, A. R., Martínez-Oyanedel, J., & Bunster, M. (2011). Spectroscopic parameters of phycoerythrobilin and phycourobilin on phycoerythrin from Gracilaria chilensis. Journal of Photochemistry and Photobiology A: Chemistry, 219, 211–216.

Sheu, M. J., Hsieh, Y. Y., Lai, C. H., Chang, C. C., & Wu, C. H. (2013). Antihyperlipidemic and antioxidant effects of C-phycocyanin in Golden Syrian hamsters fed with a hypercholesterolemic diet. Journal of Traditional and Complementary Medicine, 3, 41–47.PubMedPubMedCentral

Shi, J., Chen, Y., Xu, Y., Ji, D., Chen, C., & Xie, C. (2017). Differential proteomic analysis by iTRAQ reveals the mechanism of Pyropia haitanensis responding to high temperature stress. Scientific Reports, 7, 44734.PubMedPubMedCentral

Singh, P., Kuddus, M., & Thomas, G. (2011). Isolation and binding affinity of C-phycocyanin to blood cells and genomic DNA as well as its diagnostic applications. Journal of Biotechnology and Pharmaceutical Research, 2, 001–008.

Sonani, R. R., Singh, N. K., Awasthi, A., Prasad, B., Kumar, J., & Madamwar, D. (2014a). Phycoerythrin extends life span and health span of Caenorhabditis elegans. Age (Dordr), 36, 9717.

Sonani, R. R., Singh, N. K., Kumar, J., Thakar, D., & Madamwar, D. (2014b). 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, 1757–1766.

Sonani, R. R., Rastogi, R. P., Patel, R., & Madamwar, D. (2016). Recent advances in production, purification and applications of phycobiliproteins. World Journal of Biological Chemistry, 7, 100–109.PubMedPubMedCentral

Spat, P., Klotz, A., Rexroth, S., Macek, B., & Forchhammer, K. (2018). Chlorosis as a developmental program in cyanobacteria: The proteomic fundament for survival and awakening. Molecular and Cellular Proteomics, 17, 1650–1669.PubMed

Stanic-Vucinic, D., Minic, S., Nikolic, M. R., & Cirkovic Velickovic, T. (2018). Spirulina phycobiliproteins as food components and complements. In: E. Jacob-Lopes, L. Q. Zepka, M. I. Queiroz (Eds.), Microalgal biotechnology (pp. 129–149). IntechOpen.

Su, H. N., Wang, Q. M., Li, C. Y., Li, K., Luo, W., Chen, B., et al. (2017). Structural insights into the cold adaptation of the photosynthetic pigment-protein C-phycocyanin from an Arctic cyanobacterium. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1858, 325–335.

Suzery, M., Hadiyanto, Sutanto, H., Soetrisnanto, D., Majid, D., Setyawan, D., & Azizah, N. (2015). The improvement of phycocyanin stability extracted from Spirulina sp using extrusion encapsulation technique. AIP Conference Proceedings, 1699, 030011.

Thoren, K. L., Connell, K. B., Robinson, T. E., Shellhamer, D. D., Tammaro, M. S., & Gindt, Y. M. (2006). The free energy of dissociation of oligomeric structure in phycocyanin is not linear with denaturant. Biochemistry, 45, 12050–12059.PubMedPubMedCentral

Thümmler, F., & Rüdiger, W. (1983). Chromopeptides from phytochrome and phycocyanin. NMR Studies of the Pfr and Pr chromophore of phytochrome and EyZ isomeric chromophores of phycocyanin. Zeitschrift für Naturforschung C, 38, 359–368.

Vadiraja, B. B., Gaikwad, N. W., & Madyastha, K. M. (1998). Hepatoprotective effect of C-phycocyanin: Protection for carbon tetrachloride and R-(+)-pulegone-mediated hepatotoxicity in rats. Biochemical and Biophysical Research Communications, 249, 428–431.PubMed

Vernès, L., Granvillain, P., Chemat, F., & Vian, M. (2015). Phycocyanin from Arthrospira platensis. Production, extraction and analysis. Current Biotechnology, 4, 481–491.

Wang, L., Wang, S., Fu, X., & Sun, L. (2015). Characteristics of an R-phycoerythrin with two gamma subunits prepared from red macroalga Polysiphonia urceolata. PLoS ONE, 10, e0120333.PubMedPubMedCentral

Watermann, T., Elgabarty, H., & Sebastiani, D. (2014). Phycocyanobilin in solution—A solvent triggered molecular switch. Physical Chemistry Chemical Physics: PCCP, 16, 6146–6152.PubMed

Wedemayer, G. J., Kidd, D. G., Wemmer, D. E., & Glazer, A. N. (1992). Phycobilins of cryptophycean algae. Occurrence of dihydrobiliverdin and mesobiliverdin in cryptomonad biliproteins. Journal of Biological Chemistry, 267, 7315–7331.PubMed

Wen, P., Hu, T. G., Wen, Y., Linhardt, R. J., Zong, M. H., Zou, Y. X., et al. (2019). Targeted delivery of phycocyanin for the prevention of colon cancer using electrospun fibers. Food Function. https://doi.org/10(4):1816-1825.CrossRefPubMed

Williams, V. P., & Glazer, A. N. (1978). Structural studies on phycobiliproteins. I. Bilin-containing peptides of C-phycocyanin. Journal of Biological Chemistry, 253, 202–211.PubMed

Wu, L. C., Lin, Y. Y., Yang, S. Y., Weng, Y. T., & Tsai, Y. T. (2011). Antimelanogenic effect of c-phycocyanin through modulation of tyrosinase expression by upregulation of ERK and downregulation of p38 MAPK signaling pathways. Journal of Biomedical Science, 18, 74.PubMedPubMedCentral

Wu, H.-L., Wang, G.-H., Xiang, W.-Z., Li, T., & He, H. (2016). Stability and antioxidant activity of food-grade phycocyanin isolated from Spirulina platensis. International Journal of Food Properties, 19, 2349–2362.

Wu, Q., Cai, Q. F., Yoshida, A., Sun, L. C., Liu, Y. X., Liu, G. M., et al. (2017). Purification and characterization of two novel angiotensin I-converting enzyme inhibitory peptides derived from R-phycoerythrin of red algae (Bangia fusco-purpurea). European Food Research and Technology, 243, 779–789.

Xu, K., Xu, Y., Ji, D. H., Xie, J., Chen, C. S., & Xie, C. T. (2016). Proteomic analysis of the economic seaweed Pyropia haitanensis in response to desiccation. Algal Research, 19, 198–206.

Xu, W. Y., Xiao, Y., Luo, P. F., & Fan, L. H. (2018). Preparation and characterization of C-phycocyanin peptide grafted N-succinyl chitosan by enzyme method. International Journal of Biological Macromolecules, 113, 841–848.PubMed

Yan, S.-G., Zhu, L.-P., Su, H.-N., Zhang, X.-Y., Chen, X.-L., Zhou, B.-C., et al. (2011). Single-step chromatography for simultaneous purification of C-phycocyanin and allophycocyanin with high purity and recovery from Spirulina (Arthrospira) platensis. Journal of Applied Phycology, 23, 1–6.

Zhang, J., Ma, J., Liu, D., Qin, S., Sun, S., Zhao, J., et al. (2017a). Structure of phycobilisome from the red alga Griffithsia pacifica. Nature, 551, 57–63.PubMed

Zhang, X.-F., Wang, X., & Luo, G.-H. (2017b). Ultrasound-assisted three phase partitioning of phycocyanin from Spirulina platensis. European Journal of Pure and Applied Chemistry, 4, 1–15.

Title: Analytical Protocols in Phycobiliproteins Analysis
Authors: Milan R. Nikolic
Simeon Minic
Mirjana Macvanin
Dragana Stanic-Vucinic
Tanja Cirkovic Velickovic
Publisher: Springer International Publishing
Book: Pigments from Microalgae Handbook
Print ISBN: 978-3-030-50970-5

Electronic ISBN: 978-3-030-50971-2

Copyright Year: 2020
DOI: https://doi.org/10.1007/978-3-030-50971-2_8