Bioactive Peptides Derived from Phycobiliprotein: A Review

doi:10.11924/j.issn.1000-6850.casb2021-0005

Abstract

Abstract:

The purpose of this study is to provide references for discovery and structure-activity relationship characterization of phycobiliprotein-derived bioactive peptides, and promote the development and application of phycobiliprotein-derived bioactive peptides. In this paper, phycobiliprotein-derived bioactive peptides with different biological activities, including antioxidant peptides, antihypertensive peptides, immunomodulatory peptides, hypoglycemic peptides, antibacterial peptides and anti-inflammatory peptides, were reviewed. The sources, preparation, structure, function, and structure-activity relationship of phycobiliprotein-derived bioactive peptides were summarized. Finally, it was pointed out that there was certain blindness in the research and development of bioactive peptides using traditional methods, however, the combination of bioinformatics and traditional methods was conducive to efficient exploring of novel bioactive peptides, and the study could provide a new approach for the development of phycobiliprotein-derived bioactive peptides.

Key words: phycobiliprotein, bioactive peptide, preparation, function, structure, structure-activity relationship

CLC Number:

S188

Li Fuqiang, Zhang Tingxin, Li Xiaojie, Zhu Liping, Yan Shigan. Bioactive Peptides Derived from Phycobiliprotein: A Review[J]. Chinese Agricultural Science Bulletin, 2021, 37(27): 70-76.

Figures/Tables 1

References 62

[1]	Pagels F, Guedes A C, Amaro H M, et al. Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications[J]. Biotechnology advances, 2019, 37(3):422-443. doi: 10.1016/j.biotechadv.2019.02.010 URL
[2]	Görgüç A, Gençdağ E, Yılmaz F M. Bioactive peptides derived from plant origin by-products: Biological activities and techno-functional utilizations in food developments-A review[J]. Food Research International, 2020, 136:109504. doi: S0963-9969(20)30529-9 pmid: 32846583
[3]	范敏. 钝顶螺旋藻藻蓝蛋白及其酶解产物的抗肿瘤活性研究[D]. 呼和浩特:内蒙古农业大学, 2008.
[4]	马莹, 胡志和, 薛璐, 等. 双酶水解螺旋藻藻胆蛋白制备ACE抑制肽的工艺优化[J]. 食品工业科技, 2019, 40(12):178-185.
[5]	Martínez-Palma N, Martínez-Ayala A, Dávila-Ortiz G. Determination of antioxidant and chelating activity of protein hydrolysates from Spirulina (Arthrospira maxima) obtained by simulated gastrointestinal digestion[J]. Revista Mexicana de Ingeniera Quimica, 2015, 14(1):25-34.
[6]	Admassu H, Gasmalla M A A, Yang R, et al. Bioactive Peptides Derived from Seaweed Protein and Their Health Benefits: Antihypertensive, Antioxidant, and Antidiabetic Properties[J]. Journal of Food Science, 2018, 83(1):6-16. doi: 10.1111/1750-3841.14011 URL
[7]	Nwachukwu I D, Aluko R E. Structural and functional properties of food protein-derived antioxidant peptides[J]. Journal of Food Biochemistry, 2019, 43(1):e12761. doi: 10.1111/jfbc.12761 URL
[8]	Yaribeygi H, Atkin S L, Sahebkar A. A review of the molecular mechanisms of hyperglycemia-induced free radical generation leading to oxidative stress[J]. Journal of cellular physiology, 2019, 234(2):1300-1312. doi: 10.1002/jcp.27164 pmid: 30146696
[9]	Park P J, Jung W K, Nam K S, et al. Purification and characterization of antioxidative peptides from protein hydrolysate of lecithin-free egg yolk[J]. Journal of the American Oil Chemists Society, 2001, 78(6):651-656. doi: 10.1007/s11746-001-0321-0 URL
[10]	Rajapakse N, Mendis E, Byun H G, et al. Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems[J]. Journal of Nutritional Biochemistry, 2005, 16(9):562-569. pmid: 16115545
[11]	Sannasimuthu A, Arockiaraj J. Intracellular free radical scavenging activity and protective role of mammalian cells by antioxidant peptide from thioredoxin disulfide reductase of Arthrospira platensis[J]. Journal of Functional Foods, 2019, 61:103513. doi: 10.1016/j.jff.2019.103513 URL
[12]	Chen H, Wang S, Zhou A, et al. A novel antioxidant peptide purified from defatted round scad (Decapterus maruadsi) protein hydrolysate extends lifespan in Caenorhabditis elegans[J]. Journal of Functional Foods, 2020, 68:103907. doi: 10.1016/j.jff.2020.103907 URL
[13]	Sheng J, Yang X, Chen J, et al. Antioxidative effects and mechanism study of bioactive peptides from defatted walnut (Juglans regia L.) meal hydrolysate[J]. Journal of agricultural and food chemistry, 2019, 67(12):3305-3312. doi: 10.1021/acs.jafc.8b05722 URL
[14]	Indiano-Romacho P, Fernández-Tomé S, Amigo L, et al. Multifunctionality of lunasin and peptides released during its simulated gastrointestinal digestion[J]. Food Research International, 2019, 125:108513. doi: S0963-9969(19)30384-9 pmid: 31554062
[15]	Brabakaran A, Venkatesan S, Jayappriyan K R, et al. Antioxidant Properties of R-Phycoerythrin from Red Alga Spyridia filamentosa (Wulfen) Harvey Collected on the Pudumadam Coast[J]. Advanced Science, Engineering and Medicine, 2020, 12(4):489-498. doi: 10.1166/asem.2020.2562 URL
[16]	Dewi N, Santoso J, Setyaningsih I, et al. Extraction of phycoerythrin from Kappaphycus alvarezii seaweed using ultrasonication[J] Earth and Environmental Science. 2020, 414(1):012028.
[17]	Ganesan A R, Shanmugam M. Isolation of phycoerythrin from Kappaphycus alvarezii: a potential natural colourant in ice cream[J]. Journal of Applied Phycology, 2020, 32(6):4221-4233. doi: 10.1007/s10811-020-02214-0 URL
[18]	Zang F, Qin S, Ma C, et al. Structure, function and applications of phycoerythrin: a unique light harvesting protein in algae[J]. Chinese Science Bulletin, 2020, 65(7):565-576.
[19]	Ferraro G, Imbimbo P, Marseglia A, et al. A thermophilic C-phycocyanin with unprecedented biophysical and biochemical properties[J]. International Journal of Biological Macromolecules, 2020, 150:38-51. doi: 10.1016/j.ijbiomac.2020.02.045 URL
[20]	Nowruzi B Anvar S A A Ahari H. Extraction, purification and evaluation of antimicrobial and antioxidant properties of phycoerythrin from terrestrial cyanobacterium Nostoc sp. FA1[J]. Journal of Microbial World, 2020, 13(2):138-153.
[21]	Hsieh-Lo M, Castillo G, Ochoa-Becerra M A, et al. Phycocyanin and phycoerythrin: Strategies to improve production yield and chemical stability[J]. Algal Research, 2019, 42:101600. doi: 10.1016/j.algal.2019.101600 URL
[22]	Osman A, Abd-Elaziz S, Salama A, et al. Health protective actions of phycocyanin obtained from an Egyptian isolate of Spirulina platensis on albino rats[J]. EurAsian Journal of BioSciences, 2019, 13(1):105-112.
[23]	Kim E Y, Choi Y H, Nam T J. Identification and antioxidant activity of synthetic peptides from phycobiliproteins of Pyropia yezoensis[J]. International Journal of Molecular Medicine, 2018, 42(2):789-798.
[24]	Yu J, Hu Y, Xue M, et al. Purification and Identification of Antioxidant Peptides from Enzymatic Hydrolysate of Spirulina platensis[J]. Journal of Microbiology and Biotechnology, 2016, 26(7):1216-1223. doi: 10.4014/jmb.1601.01033 URL
[25]	Mysliwa-Kurdziel B, Solymosi K. Phycobilins and phycobiliproteins used in food industry and medicine[J]. Mini Reviews in Medicinal Chemistry, 2017, 17(13):1173-1193. doi: 10.2174/1389557516666160912180155 pmid: 27633748
[26]	Yéprémian C, Demay J, Halary S, et al. Anti-inflammatory, antioxidant and wound healing properties of cyanobacteria from thermal mud of Balaruc-les-Bains, France: a multi-approach study[J]. Preprints, 2020, 11(1):28.
[27]	Lee D, Nishizawa M, Shimizu Y, et al. Anti-inflammatory effects of dulse (Palmaria palmata) resulting from the simultaneous water-extraction of phycobiliproteins and chlorophyll a[J]. Food Research International, 2017, 100(1):514-521. doi: 10.1016/j.foodres.2017.06.040 URL
[28]	Li Y, Lammi C, Boschin G, et al. Recent Advances in Microalgae Peptides: Cardiovascular Health Benefits and Analysis[J]. Journal of Agricultural & Food Chemistry, 2019, 67(43):11825-11838.
[29]	Mirzaei M, Mirdamadi S, Safavi M. Structural analysis of ACE-inhibitory peptide (VL-9) derived from Kluyveromyces marxianus protein hydrolysate[J]. Journal of Molecular Structure, 2020, 1213:128199. doi: 10.1016/j.molstruc.2020.128199 URL
[30]	Obaroakpo J U, Liu L, Zhang S, et al. α-Glucosidase and ACE dual inhibitory protein hydrolysates and peptide fractions of sprouted quinoa yoghurt beverages inoculated with Lactobacillus casei[J]. Food chemistry, 2019, 299:124985. doi: 10.1016/j.foodchem.2019.124985 URL
[31]	Wu Q, Cai Q F, Yoshida A, et al. Purification and characterization of two novel angiotensin I-converting enzyme inhibitory peptides derived from R-phycoerythrin of red algae (Bangia fusco-purpurea)[J]. European Food Research & Technology, 2017, 243(5):779-789.
[32]	Kitade Y, Miyabe Y, Yamamoto Y, et al. Structural characteristics of phycobiliproteins from red alga Mazzaella japonica[J]. Journal of Food Biochemistry, 2018, 42(1):e12436. doi: 10.1111/jfbc.2018.42.issue-1 URL
[33]	Furuta T, Miyabe Y, Yasui H, et al. Angiotensin I Converting Enzyme Inhibitory Peptides Derived from Phycobiliproteins of Dulse Palmaria palmata[J]. Marine Drugs, 2016, 14(2):32. doi: 10.3390/md14020032 URL
[34]	Suetsuna K. Purification and identification of angiotensin I-converting enzyme inhibitors from the red alga Porphyra yezoensis[J]. Journal of Marine Biotechnology, 1998, 6(3):163-167.
[35]	Suetsuna K, Maekawa K, Chen J R. Antihypertensive effects of Undaria pinnatifida (wakame) peptide on blood pressure in spontaneously hypertensive rats[J]. Journal of Nutritional Biochemistry, 2004, 15(5):267-272. pmid: 15135150
[36]	Munawaroh H S H, Gumilar G G, Nurjanah F, et al. In-vitro molecular docking analysis of microalgae extracted phycocyanin as an anti-diabetic candidate[J]. Biochemical Engineering Journal, 2020, 161(15):107666. doi: 10.1016/j.bej.2020.107666 URL
[37]	Li Y, Aiello G, Bollati C, et al. Phycobiliproteins from Arthrospira Platensis (Spirulina): A New Source of Peptides with Dipeptidyl Peptidase-IV Inhibitory Activity[J]. Nutrients, 2020, 12(3):794. doi: 10.3390/nu12030794 URL
[38]	Cermeño M, Stack J, Tobin P R, et al. Peptide identification from a Porphyra dioica protein hydrolysate with antioxidant, angiotensin converting enzyme and dipeptidyl peptidase IV inhibitory activities[J]. Food & Function, 2019, 10(6):3421-3429.
[39]	Jiang Y, Guo F, Chen L, et al. The antitumor activity of naturally occurring chromones: A review[J]. Fitoterapia, 2019, 135(6):114-129. doi: 10.1016/j.fitote.2019.04.012 URL
[40]	Sharma P, Kaur H, Kehinde B A, et al. Food-derived anticancer peptides: A review[J]. International Journal of Peptide Research and Therapeutics, 2020: 1-16.
[41]	Liu Z, Fu X, Huang W, et al. Photodynamic effect and mechanism study of selenium-enriched phycocyanin from Spirulina platensis against liver tumours[J]. Journal of Photochemistry and Photobiology B: Biology, 2018, 180:89-97. doi: 10.1016/j.jphotobiol.2017.12.020 URL
[42]	Jiang L, Wang Y, Liu G, et al. C-Phycocyanin exerts anti-cancer effects via the MAPK signaling pathway in MDA-MB-231 cells[J]. Cancer Cell International, 2018, 18(1):1-14. doi: 10.1186/s12935-017-0498-3 URL
[43]	Pan R, Lu R, Zhang Y, et al. Spirulina phycocyanin induces differential protein expression and apoptosis in SKOV-3 cells[J]. International journal of biological macromolecules, 2015, 81:951-959. doi: 10.1016/j.ijbiomac.2015.09.039 URL
[44]	Saini M K, Sanyal S N. Targeting angiogenic pathway for chemoprevention of experimental colon cancer using C-phycocyanin as cyclooxygenase-2 inhibitor[J]. Biochemistry and Cell Biology, 2014, 92(3):206-218. doi: 10.1139/bcb-2014-0016 URL
[45]	Hao S, Li S, Wang J, et al. Phycocyanin Exerts Anti-Proliferative Effects through Down-Regulating TIRAP/NF-κB Activity in Human Non-Small Cell Lung Cancer Cells[J]. Cells, 2019, 8(6):588. doi: 10.3390/cells8060588 URL
[46]	Baudelet P H, Gagez A L, Bérard J B, et al. Antiproliferative activity of Cyanophora paradoxa pigments in melanoma, breast and lung cancer cells[J]. Marine Drugs, 2013, 11(11):4390-4406. doi: 10.3390/md11114390 URL
[47]	Subhashini J, Mahipal S V K, Reddy M C, et al. Molecular mechanisms in C-Phycocyanin induced apoptosis in human chronic myeloid leukemia cell line-K562.[J]. Biochemical Pharmacology, 2004, 68(3):453-462. pmid: 15242812
[48]	Fan X, Bai L, Mao X, et al. Novel peptides with anti-proliferation activity from the Porphyra haitanesis hydrolysate[J]. Process Biochemistry, 2017, 60:98-107. doi: 10.1016/j.procbio.2017.05.018 URL
[49]	Mao X, Bai L, Fan X, et al. Anti-proliferation peptides from protein hydrolysates of Pyropia haitanensis[J]. Journal of Applied Phycology, 2017, 29(3):1623-1633. doi: 10.1007/s10811-016-1037-7 URL
[50]	Mahmoud S, Ali O, Abdel G, et al. Antibacterial phycocyanin from Anabaena oryzae SOS13[J]. International Journal of Applied Research in Natural Products, 2016, 8(4):27-36.
[51]	Shanmugam A, Sigamani S, Venkatachalam H, et al. Antibacterial activity of extracted phycocyanin from Oscillatoria sp.[J]. Journal of Applied Pharmaceutical Science, 2017, 7(3):62-67.
[52]	Mohamed S A, Osman A, Abo Eita A, et al. Estimation of antibacterial and antioxidant activities of phycocyanin isolated from Spirulina[J]. Zagazig Journal of Agricultural Research, 2018, 45(2):657-666. doi: 10.21608/zjar.2018.49187 URL
[53]	孙宜君. 螺旋藻抗菌肽的纯化鉴定及其抑菌机理的研究[D]. 北京:北京林业大学, 2016.
[54]	付云, 赵谋明, 卢美杉, 等. 枯草芽孢杆菌YA215发酵螺旋藻渣产抑菌活性的工艺[J]. 食品与发酵工业, 2020, 46:146-152.
[55]	付云, 赵谋明, 庞一扬, 等. 源自螺旋藻渣枯草芽孢杆菌发酵抗菌肽SP-AP-1和Iturin A对金黄色葡萄球菌抑菌机制对比研究[J]. 食品科学, 2020, 41(5):1-13.
[56]	Rahiman S S F, Morgan M, Gray P, et al. Inhibitory effects of dynorphin 3-14 on the lipopolysaccharide-induced toll-like receptor 4 signalling pathway[J]. Peptides, 2017, 90:48-54. doi: 10.1016/j.peptides.2017.02.004 URL
[57]	Xiao M, Ding L, Yang W, et al. St20, a new venomous animal derived natural peptide with immunosuppressive and anti-inflammatory activities[J]. Toxicon, 2017, 127:37-43. doi: S0041-0101(17)30008-9 pmid: 28077339
[58]	Hou H, Fan Y, Wang S, et al. Immunomodulatory activity of Alaska pollock hydrolysates obtained by glutamic acid biosensor-Artificial neural network and the identification of its active central fragment[J]. Journal of Functional Foods, 2016, 24:37-47. doi: 10.1016/j.jff.2016.03.033 URL
[59]	Díaz Domínguez G Marsán Suárez V del Valle Pérez L O. Main immunomodulatory and anti-inflamatory properties of phycobiliproteins C-phycocyanin[J]. Revista Cubana de Hematología, Inmunología y Hemoterapia, 2016, 32(4):447-454.
[60]	Taniguchi M, Kuda T, Shibayama J, et al. In vitro antioxidant, anti-glycation and immunomodulation activities of fermented blue-green algae Aphanizomenon flos-aquae[J]. Molecular biology reports, 2019, 46(2):1775-1786. doi: 10.1007/s11033-019-04628-7 pmid: 30694455
[61]	杨磊. 螺旋藻活性肽的制备及其免疫调节功能研究[D]. 桂林:广西大学, 2009.
[62]	頡宇, 胡锦灵, 赵宏飞, 等. 基于生物信息学定向制备柠条籽蛋白抗氧化肽的工艺优化[J]. 食品科学, 2019, 41(20):278-284.

活性肽的名称	活性肽的结构	活性肽的藻来源	文献
抗氧化肽	RYVSYALLAGDPSVLEDRC	条斑紫菜	[23]
抗氧化肽	PNN	螺旋藻	[24]
抗氧化肽	DYYKR	紫菜	[38]
抗炎肽	LRDGEIILRY	掌状红皮藻	[27]
降血压肽	AILAGDPSVLEDR	红藻	[31]
降血压肽	VVGGTGPVDEWGIAGAR	红藻	[31]
降血压肽	YRD	日本掌状红皮藻	[32,33]
降血压肽	LDY	日本掌状红皮藻	[32,33]
降血压肽	LRY	日本掌状红皮藻	[32,33]
降血压肽	LF	日本条斑紫菜	[32,34]
降血压肽	VY	日本裙带菜	[32,35]
降血压肽	FY	日本裙带菜	[32,35]
降血压肽	TYIA	紫菜	[38]
降血糖肽	YLVA	紫菜	[38]
抗肿瘤肽	VPGTPKNLDSPR	坛紫菜	[48]
抗肿瘤肽	MPAPSCALPRSVVPPR	坛紫菜	[48]
抗肿瘤肽	QTDDNHSNVLWAGFSR	坛紫菜	[49]
抗肿瘤肽	QTDDNHSNVLWAGFSR	坛紫菜	[49]
抗菌肽	KLVDASHIRLATGDVAVRA	螺旋藻	[53]
抗菌肽	ATHDNCCLRQS	螺旋藻渣	[54,55]

活性肽的名称	活性肽的结构	活性肽的藻来源	文献
抗氧化肽	RYVSYALLAGDPSVLEDRC	条斑紫菜	[23]
抗氧化肽	PNN	螺旋藻	[24]
抗氧化肽	DYYKR	紫菜	[38]
抗炎肽	LRDGEIILRY	掌状红皮藻	[27]
降血压肽	AILAGDPSVLEDR	红藻	[31]
降血压肽	VVGGTGPVDEWGIAGAR	红藻	[31]
降血压肽	YRD	日本掌状红皮藻	[32,33]
降血压肽	LDY	日本掌状红皮藻	[32,33]
降血压肽	LRY	日本掌状红皮藻	[32,33]
降血压肽	LF	日本条斑紫菜	[32,34]
降血压肽	VY	日本裙带菜	[32,35]
降血压肽	FY	日本裙带菜	[32,35]
降血压肽	TYIA	紫菜	[38]
降血糖肽	YLVA	紫菜	[38]
抗肿瘤肽	VPGTPKNLDSPR	坛紫菜	[48]
抗肿瘤肽	MPAPSCALPRSVVPPR	坛紫菜	[48]
抗肿瘤肽	QTDDNHSNVLWAGFSR	坛紫菜	[49]
抗肿瘤肽	QTDDNHSNVLWAGFSR	坛紫菜	[49]
抗菌肽	KLVDASHIRLATGDVAVRA	螺旋藻	[53]
抗菌肽	ATHDNCCLRQS	螺旋藻渣	[54,55]