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Protein & Peptide Letters

Author(s): Guizhu Feng , Jing Wu, Hai-Long Yang* and Lixian Mu*

DOI: 10.2174/0929866528666210907145634

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Discovery of Antioxidant Peptides from Amphibians: A Review

Page: [1220 - 1229] Pages: 10

  • * (Excluding Mailing and Handling)

Abstract

In recent years, bioactive peptide drugs have attracted growing attention due to the increasing difficulty in developing new drugs with novel chemical structures. In addition, many diseases are linked to excessive oxidation in the human body. Therefore, the role of peptides with antioxidant activity in counteracting diseases related to oxidative stress is worth exploring. Amphibians are a major repository for bioactive peptides that protect the skin from biotic and abiotic stresses, such as microbial infection and radiation injury. We characterized the first amphibian- derived gene-encoded antioxidant peptides in 2008. Since then, a variety of antioxidant peptides have been detected in different amphibian species. In this work, the physicochemical properties of antioxidant peptides identified from amphibians are reviewed for the first time, particularly acquisition methods, amino acid characteristics, antioxidant mechanisms, and application prospects. This review should provide a reference for advancing the identification, structural analysis, and potential therapeutic value of natural antioxidant peptides.

Keywords: Amphibians, antioxidant peptides, antioxidant, peptide drugs, bioactive peptide drugs, abiotic stresses.

Graphical Abstract

[1]
Fransen, M.; Nordgren, M.; Wang, B.; Apanasets, O. Role of peroxisomes in ROS/RNS-metabolism: implications for human disease. Biochim. Biophys. Acta, 2012, 1822(9), 1363-1373.
[http://dx.doi.org/10.1016/j.bbadis.2011.12.001] [PMID: 22178243]
[2]
Shindo, Y.; Witt, E.; Packer, L.; Packer, L. Antioxidant defense mechanisms in murine epidermis and dermis and their responses to ultraviolet light. J. Invest. Dermatol., 1993, 100(3), 260-265.
[http://dx.doi.org/10.1111/1523-1747.ep12469048] [PMID: 8440901]
[3]
Kohen, R.; Gati, I. Skin low molecular weight antioxidants and their role in aging and in oxidative stress. Toxico., 2000, 148(2-3), 149-157.
[http://dx.doi.org/10.1016/S0300-483X(00)00206-7] [PMID: 10962134]
[4]
Yang, H.; Wang, X.; Liu, X.; Wu, J.; Liu, C.; Gong, W.; Zhao, Z.; Hong, J.; Lin, D.; Wang, Y.; Lai, R. Antioxidant peptidomics reveals novel skin antioxidant system. Mol. Cell. Proteomics, 2009, 8(3), 571-583.
[http://dx.doi.org/10.1074/mcp.M800297-MCP200] [PMID: 19028675]
[5]
Xu, X.; Lai, R. The chemistry and biological activities of peptides from amphibian skin secretions. Chem. Rev., 2015, 115(4), 1760-1846.
[http://dx.doi.org/10.1021/cr4006704] [PMID: 25594509]
[6]
Adebiyi, A.P.; Adebiyi, A.O.; Ogawa, T.; Muramoto, K. Purification and characterisation of antioxidative peptides from unfractionated rice bran protein hydrolysates. Int. J. Food Sci. Technol., 2008, 43(1), 35-43.
[http://dx.doi.org/10.1111/j.1365-2621.2006.01379.x]
[7]
Kudo, K.; Onodera, S.; Takeda, Y.; Benkeblia, N.; Shiomi, N. Antioxidative activities of some peptides isolated from hydrolyzed potato protein extract. J. Funct. Foods, 2009, 1(2), 170-176.
[http://dx.doi.org/10.1016/j.jff.2009.01.006]
[8]
Kim, E.K.; Lee, S.J.; Jeon, B.T.; Moon, S.H.; Kim, B.K.; Park, T.K.; Han, J.S.; Park, P.J. Purification and characterisation of antioxidative peptides from enzymatic hydrolysates of venison protein. Food Chem., 2009, 114(4), 1365-1370.
[http://dx.doi.org/10.1016/j.foodchem.2008.11.035]
[9]
Shanmugam, V.P.; Kapila, S.; Sonfack, T.K.; Kapila, R. Antioxidative peptide derived from enzymatic digestion of buffalo casein. Int. Dairy J., 2015, 42, 1-5.
[http://dx.doi.org/10.1016/j.idairyj.2014.11.001]
[10]
Lee, S.J.; Kim, E.K.; Hwang, J.W.; Oh, H.J.; Cheong, S.H.; Moon, S.H.; Jeon, B.T.; Sang, M.L.; Park, P.J. Purification and characterisation of an antioxidative peptide from enzymatic hydrolysates of duck processing by-products. Food Chem., 2010, 123(2), 216-220.
[http://dx.doi.org/10.1016/j.foodchem.2010.04.001]
[11]
Je, J.Y.; Qian, Z.J.; Lee, S.H.; Byun, H.G.; Kim, S.K. Purification and antioxidant properties of bigeye tuna (Thunnus obesus) dark muscle peptide on free radical-mediated oxidative systems. J. Med. Food, 2008, 11(4), 629-637.
[http://dx.doi.org/10.1089/jmf.2007.0114] [PMID: 19053853]
[12]
Qian, Z.J.; Jung, W.K.; Kim, S.K. Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresour. Technol., 2008, 99(6), 1690-1698.
[http://dx.doi.org/10.1016/j.biortech.2007.04.005] [PMID: 17512726]
[13]
Olivares-Galván, S.; Marina, M.L.; García, M.C. Extraction and characterization of antioxidant peptides from fruit residues. Foods, 2020, 9(8), 1018-1047.
[http://dx.doi.org/10.3390/foods9081018] [PMID: 32751284]
[14]
Chai, T.T.; Law, Y.C.; Wong, F.C.; Kim, S.K. Enzyme-assisted discovery of antioxidant peptides from edible marine invertebrates: A review. Mar. Drugs, 2017, 15(2), 42-67.
[http://dx.doi.org/10.3390/md15020042] [PMID: 28212329]
[15]
Chalamaiah, M.; Dinesh Kumar, B.; Hemalatha, R.; Jyothirmayi, T. Fish protein hydrolysates: proximate composition, amino acid composition, antioxidant activities and applications: a review. Food Chem., 2012, 135(4), 3020-3038.
[http://dx.doi.org/10.1016/j.foodchem.2012.06.100] [PMID: 22980905]
[16]
Agier, J.; Efenberger, M.; Brzezińska-Błaszczyk, E. Cathelicidin impact on inflammatory cells. Cent. Eur. J. Immunol., 2015, 40(2), 225-235.
[http://dx.doi.org/10.5114/ceji.2015.51359] [PMID: 26557038]
[17]
Wang, G.; Mishra, B.; Lau, K.; Lushnikova, T.; Golla, R.; Wang, X. Antimicrobial peptides in 2014. Pharmaceuticals (Basel), 2015, 8(1), 123-150.
[http://dx.doi.org/10.3390/ph8010123] [PMID: 25806720]
[18]
Wake, D.B.; Koo, M.S. Amphibians. Curr. Biol., 2018, 28(21), R1237-R1241.
[http://dx.doi.org/10.1016/j.cub.2018.09.028] [PMID: 30399342]
[19]
Clarke, B.T. The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biol. Rev. Camb. Philos. Soc., 1997, 72(3), 365-379.
[http://dx.doi.org/10.1017/S0006323197005045] [PMID: 9336100]
[20]
Lai, R.; Liu, H.; Hui Lee, W.; Zhang, Y. A novel bradykinin-related peptide from skin secretions of toad Bombina maxima and its precursor containing six identical copies of the final product. Biochem. Biophys. Res. Commun., 2001, 286(2), 259-263.
[http://dx.doi.org/10.1006/bbrc.2001.5359] [PMID: 11500030]
[21]
Wang, X.; Song, Y.; Li, J.; Liu, H.; Xu, X.; Lai, R.; Zhang, K. A new family of antimicrobial peptides from skin secretions of Rana pleuraden. Peptides, 2007, 28(10), 2069-2074.
[http://dx.doi.org/10.1016/j.peptides.2007.07.020] [PMID: 17764786]
[22]
Ren, L.; Yu, Z.; Ming, Y.D.; Zha, H.G.; Hui, L.W.; Yun, Z. Comparative study of the biological activities of the skin secretions from six common chinese amphibians. Zool. Res., 2002, 23(2), 113-119.
[http://dx.doi.org/10.3321/j.issn:0254-5853.2002.02.003]
[23]
Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3), 238-250.
[http://dx.doi.org/10.1038/nrmicro1098] [PMID: 15703760]
[24]
Lindley, B.D. Nerve stimulation and electrical properties of frog skin. J. Gen. Physiol., 1969, 53(4), 427-449.
[http://dx.doi.org/10.1085/jgp.53.4.427] [PMID: 5778317]
[25]
Tyler, M.J.; Stone, D.J.M.; Bowie, J.H. A novel method for the release and collection of dermal, glandular secretions from the skin of frogs. J. Pharmacol. Toxicol. Methods, 1992, 28(4), 199-200.
[http://dx.doi.org/10.1016/1056-8719(92)90004-K] [PMID: 1296824]
[26]
Delfino, G.; Nosi, D.; Giachi, F. Secretory granule-cytoplasm relationships in serous glands of anurans: ultrastructural evidence and possible functional role. Toxicon, 2001, 39(8), 1161-1171.
[http://dx.doi.org/10.1016/S0041-0101(00)00253-1] [PMID: 11306126]
[27]
Conlon, J.M.; Leprince, J. Identification and analysis of bioactive peptides in amphibian skin secretions. Methods Mol. Biol., 2010, 615, 145-157.
[http://dx.doi.org/10.1007/978-1-60761-535-4_12] [PMID: 20013207]
[28]
Hao, X.; Yang, H.; Wei, L.; Yang, S.; Zhu, W.; Ma, D.; Yu, H.; Lai, R. Amphibian cathelicidin fills the evolutionary gap of cathelicidin in vertebrate. Amino Acids, 2012, 43(2), 677-685.
[http://dx.doi.org/10.1007/s00726-011-1116-7] [PMID: 22009138]
[29]
Wang, G.; Wang, Y.; Ma, D.; Liu, H.; Li, J.; Zhang, K.; Yang, X.; Lai, R.; Liu, J. Five novel antimicrobial peptides from the Kuhl’s wart frog skin secretions, Limnonectes kuhlii. Mol. Biol. Rep., 2013, 40(2), 1097-1102.
[http://dx.doi.org/10.1007/s11033-012-2152-4] [PMID: 23054029]
[30]
Meng, P.; Wei, L.; Yang, S.; Liu, H.; Liu, R.; Lai, R. A novel frog skin peptide containing function to induce muscle relaxation. Biochimie, 2012, 94(12), 2508-2513.
[http://dx.doi.org/10.1016/j.biochi.2012.06.029] [PMID: 22771463]
[31]
Yan, H.; Liu, Y.; Tang, J.; Mo, G.; Song, Y.; Yan, X.; Wei, L.; Lai, R. A novel antimicrobial peptide from skin secretions of the tree frog Theloderma kwangsiensis. Zool. Sci., 2013, 30(9), 704-709.
[http://dx.doi.org/10.2108/zsj.30.704] [PMID: 24004075]
[32]
Wu, J.; Yang, J.; Wang, X.; Wei, L.; Mi, K.; Shen, Y.; Liu, T.; Yang, H.; Mu, L. A frog cathelicidin peptide effectively promotes cutaneous wound healing in mice. Biochem. J., 2018, 475(17), 2785-2799.
[http://dx.doi.org/10.1042/BCJ20180286] [PMID: 30045878]
[33]
Simmaco, M.; De Biase, D.; Severini, C.; Aita, M.; Erspamer, G.F.; Barra, D.; Bossa, F. Purification and characterization of bioactive peptides from skin extracts of Rana esculenta. Biochim. Biophys. Acta, 1990, 1033(3), 318-323.
[http://dx.doi.org/10.1016/0304-4165(90)90140-R] [PMID: 2317508]
[34]
Conlon, J.M.; Aronsson, U. Multiple bradykinin-related peptides from the skin of the frog, Rana temporaria. Peptides, 1997, 18(3), 361-365.
[http://dx.doi.org/10.1016/S0196-9781(96)00339-7] [PMID: 9145421]
[35]
Duda, T.F., Jr; Vanhoye, D.; Nicolas, P. Roles of diversifying selection and coordinated evolution in the evolution of amphibian antimicrobial peptides. Mol. Biol. Evol., 2002, 19(6), 858-864.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a004143] [PMID: 12032242]
[36]
Lai, R.; Zheng, Y.T.; Shen, J.H.; Liu, G.J.; Liu, H.; Lee, W.H.; Tang, S.Z.; Zhang, Y. Antimicrobial peptides from skin secretions of Chinese red belly toad Bombina maxima. Peptides, 2002, 23(3), 427-435.
[http://dx.doi.org/10.1016/S0196-9781(01)00641-6] [PMID: 11835991]
[37]
Conlon, J.M.; Kolodziejek, J.; Nowotny, N. Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim. Biophys. Acta, 2004, 1696(1), 1-14.
[http://dx.doi.org/10.1016/j.bbapap.2003.09.004] [PMID: 14726199]
[38]
Lee, W.H.; Li, Y.; Lai, R.; Li, S.; Zhang, Y.; Wang, W. Variety of antimicrobial peptides in the Bombina maxima toad and evidence of their rapid diversification. Eur. J. Immunol., 2005, 35(4), 1220-1229.
[http://dx.doi.org/10.1002/eji.200425615] [PMID: 15770703]
[39]
Li, J.; Liu, T.; Xu, X.; Wang, X.; Wu, M.; Yang, H.; Lai, R. Amphibian tachykinin precursor. Biochem. Biophys. Res. Commun., 2006, 350(4), 983-986.
[http://dx.doi.org/10.1016/j.bbrc.2006.09.150] [PMID: 17045570]
[40]
Lu, Y.; Li, J.; Yu, H.; Xu, X.; Liang, J.; Tian, Y.; Ma, D.; Lin, G.; Huang, G.; Lai, R. Two families of antimicrobial peptides with multiple functions from skin of rufous-spotted torrent frog, Amolops loloensis. Peptides, 2006, 27(12), 3085-3091.
[http://dx.doi.org/10.1016/j.peptides.2006.08.017] [PMID: 17000029]
[41]
Zhou, M.; Chen, T.; Walker, B.; Shaw, C. Lividins: novel antimicrobial peptide homologs from the skin secretion of the Chinese Large Odorous frog, Rana (Odorrana) livida. Identification by “shotgun” cDNA cloning and sequence analysis. Peptides, 2006, 27(9), 2118-2123.
[http://dx.doi.org/10.1016/j.peptides.2006.04.007] [PMID: 16713657]
[42]
Li, J.; Xu, X.; Xu, C.; Zhou, W.; Zhang, K.; Yu, H.; Zhang, Y.; Zheng, Y.; Rees, H.H.; Lai, R.; Yang, D.; Wu, J. Anti-infection peptidomics of amphibian skin. Mol. Cell. Proteomics, 2007, 6(5), 882-894.
[http://dx.doi.org/10.1074/mcp.M600334-MCP200] [PMID: 17272268]
[43]
Liu, X.; Wang, Y.; Cheng, L.; Song, Y.; Lai, R. Isolation and cDNA cloning of cholecystokinin from the skin of Rana nigrovittata. Peptides, 2007, 28(8), 1540-1544.
[http://dx.doi.org/10.1016/j.peptides.2007.07.006] [PMID: 17698250]
[44]
Wang, X.; Ren, S.; Guo, C.; Zhang, W.; Zhang, X.; Zhang, B.; Li, S.; Ren, J.; Hu, Y.; Wang, H. Identification and functional analyses of novel antioxidant peptides and antimicrobial peptides from skin secretions of four East Asian frog species. Acta Biochim. Biophys. Sin. (Shanghai), 2017, 49(6), 550-559.
[http://dx.doi.org/10.1093/abbs/gmx032] [PMID: 28402481]
[45]
Hsu, K.C.; Lu, G.H.; Jao, C.L. Antioxidative properties of peptides prepared from tuna cooking juice hydrolysates with orientase (Bacillus subtilis). Food Res. Int., 2009, 42(5-6), 647-652.
[http://dx.doi.org/10.1016/j.foodres.2009.02.014]
[46]
Elias, R.J.; Kellerby, S.S.; Decker, E.A. Antioxidant activity of proteins and peptides. Crit. Rev. Food Sci. Nutr., 2008, 48(5), 430-441.
[http://dx.doi.org/10.1080/10408390701425615] [PMID: 18464032]
[47]
Wu, R.; Wu, C.; Liu, D.; Yang, X.; Huang, J.; Zhang, J.; Liao, B.; He, H.; Li, H. Overview of antioxidant peptides derived from marine resources: the sources, characteristic, purification, and evaluation methods. Appl. Biochem. Biotechnol., 2015, 176(7), 1815-1833.
[http://dx.doi.org/10.1007/s12010-015-1689-9] [PMID: 26041057]
[48]
Jiang, H.; Tong, T.; Sun, J.; Xu, Y.; Zhao, Z.; Liao, D. Purification and characterization of antioxidative peptides from round scad (Decapterus maruadsi) muscle protein hydrolysate. Food Chem., 2014, 154, 158-163.
[http://dx.doi.org/10.1016/j.foodchem.2013.12.074] [PMID: 24518328]
[49]
Power, O.; Jakeman, P.; FitzGerald, R.J. Antioxidative peptides: enzymatic production, in vitro and in vivo antioxidant activity and potential applications of milk-derived antioxidative peptides. Amino Acids, 2013, 44(3), 797-820.
[http://dx.doi.org/10.1007/s00726-012-1393-9] [PMID: 22968663]
[50]
Lu, Z.; Zhai, L.; Wang, H.; Che, Q.; Wang, D.; Feng, F.; Zhao, Z.; Yu, H. Novel families of antimicrobial peptides with multiple functions from skin of Xizang plateau frog, Nanorana parkeri. Biochimie, 2010, 92(5), 475-481.
[http://dx.doi.org/10.1016/j.biochi.2010.01.025] [PMID: 20153801]
[51]
Guo, C.; Hu, Y.; Li, J.; Liu, Y.; Li, S.; Yan, K.; Wang, X.; Liu, J.; Wang, H. Identification of multiple peptides with antioxidant and antimicrobial activities from skin and its secretions of Hylarana taipehensis, Amolops lifanensis, and Amolops granulosus. Biochimie, 2014, 105, 192-201.
[http://dx.doi.org/10.1016/j.biochi.2014.07.013] [PMID: 25066917]
[52]
Liu, C.; Hong, J.; Yang, H.; Wu, J.; Ma, D.; Li, D.; Lin, D.; Lai, R. Frog skins keep redox homeostasis by antioxidant peptides with rapid radical scavenging ability. Free Radic. Biol. Med., 2010, 48(9), 1173-1181.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.01.036] [PMID: 20138142]
[53]
Yang, X.; Lee, W.H.; Zhang, Y. Extremely abundant antimicrobial peptides existed in the skins of nine kinds of Chinese odorous frogs. J. Proteome Res., 2012, 11(1), 306-319.
[http://dx.doi.org/10.1021/pr200782u] [PMID: 22029824]
[54]
Wang, Y.; Cao, X.; Fu, Z.; Wang, S.; Li, X.; Liu, N.; Feng, Z.; Yang, M.; Tang, J.; Yang, X. Identification and characterization of a novel gene-encoded antioxidant peptide obtained from amphibian skin secretions. Nat. Prod. Res., 2020, 34(6), 754-758.
[http://dx.doi.org/10.1080/14786419.2018.1499635] [PMID: 30470149]
[55]
Ling, G.; Li, L.; Gao, J.; Yu, H.; Zhou, J. Geographically distinct expression profile of host defense peptides in the skin of the Chinese odorous frog, Odorrana margaretae. Asian Herpetol. Res., 2013, 000(4), 288-297.
[http://dx.doi.org/10.3724/SP.J.1245.2013.00288]
[56]
Zhang, X.; Feng, C.; Wang, S.; Wang, Y.; Fu, Z.; Zhang, Y.; Sun, H.; Xie, C.; Fu, Y.; Tao, J.; Luo, M.; Yang, X. A novel amphibian-derived peptide alleviated ultraviolet B-induced photodamage in mice. Biomed. Pharmacother., 2021, 136(9), 111258.
[http://dx.doi.org/10.1016/j.biopha.2021.111258] [PMID: 33482615]
[57]
Cao, X.; Wang, Y.; Wu, C.; Li, X.; Fu, Z.; Yang, M.; Bian, W.; Wang, S.; Song, Y.; Tang, J.; Yang, X. Cathelicidin-OA1, a novel antioxidant peptide identified from an amphibian, accelerates skin wound healing. Sci. Rep., 2018, 8(1), 943-957.
[http://dx.doi.org/10.1038/s41598-018-19486-9] [PMID: 29343843]
[58]
Cao, X.; Tang, J.; Fu, Z.; Feng, Z.; Wang, S.; Yang, M.; Wu, C.; Wang, Y.; Yang, X. Identification and characterization of a novel gene-encoded antioxidant peptide from Odorous Frog Skin. Protein Pept. Lett., 2019, 26(3), 160-169.
[http://dx.doi.org/10.2174/0929866525666181114153136] [PMID: 30430935]
[59]
Wang, Y.; Ouyang, J.; Luo, X.; Zhang, M.; Jiang, Y.; Zhang, F.; Zhou, J.; Wang, Y. Identification and characterization of novel bi-functional cathelicidins from the black-spotted frog (Pelophylax nigromaculata) with both anti-infective and antioxidant activities. Dev. Comp. Immunol., 2021, 116, 103928.
[http://dx.doi.org/10.1016/j.dci.2020.103928] [PMID: 33242568]
[60]
Yang, X.; Wang, Y.; Zhang, Y.; Lee, W.H.; Zhang, Y. Rich diversity and potency of skin antioxidant peptides revealed a novel molecular basis for high-altitude adaptation of amphibians. Sci. Rep., 2016, 6, 19866.
[http://dx.doi.org/10.1038/srep19866] [PMID: 26813022]
[61]
Aluko, R.E.; Monu, E. Functional and bioactive properties of quinoa seed protein hydrolysates. J. Food Sci., 2006, 68(4), 1254-1258.
[http://dx.doi.org/10.1111/j.1365-2621.2003.tb09635.x]
[62]
Akerström, B.; Maghzal, G.J.; Winterbourn, C.C.; Kettle, A.J. The lipocalin alpha1-microglobulin has radical scavenging activity. J. Biol. chem., 2007, 282(43), 31493-31503.
[http://dx.doi.org/10.1074/jbc.M702624200] [PMID: 17766242]
[63]
Matsudaira, P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem., 1987, 262(21), 10035-10038.
[http://dx.doi.org/10.1016/S0021-9258(18)61070-1] [PMID: 3611052]
[64]
Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med., 1999, 26(9-10), 1231-1237.
[http://dx.doi.org/10.1016/S0891-5849(98)00315-3] [PMID: 10381194]
[65]
Zhang, C.; Zhou, Y.; Yang, G.Y.; Li, S. Biomimetic peptides protect cells from oxidative stress. Am. J. Transl. Res., 2017, 9(12), 5518-5527.
[PMID: 29312503]
[66]
Qin, D.; Lee, W.H.; Gao, Z.; Zhang, W.; Peng, M.; Sun, T.; Gao, Y. Protective effects of antioxidin-RL from Odorrana livida against ultraviolet B-irradiated skin photoaging. Peptides, 2018, 101, 124-134.
[http://dx.doi.org/10.1016/j.peptides.2018.01.009] [PMID: 29341894]
[67]
Yin, S.; Wang, Y.; Liu, N.; Yang, M.; Hu, Y.; Li, X.; Fu, Y.; Luo, M.; Sun, J.; Yang, X. Potential skin protective effects after UVB irradiation afforded by an antioxidant peptide from Odorrana andersonii. Biomed. Pharmacother., 2019, 120, 109535.
[http://dx.doi.org/10.1016/j.biopha.2019.109535] [PMID: 31610428]
[68]
Krueger, J.S.; Keshamouni, V.G.; Atanaskova, N.; Reddy, K.B. Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion. Oncogene, 2001, 20(31), 4209-4218.
[http://dx.doi.org/10.1038/sj.onc.1204541] [PMID: 11464287]
[69]
Krishnan, N.; Dickman, M.B.; Becker, D.F. Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic. Biol. Med., 2008, 44(4), 671-681.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.10.054] [PMID: 18036351]
[70]
Sun, L. Peptide-based drug development. Mod.Chem. Appl., 2013, 01(01), 100-103.
[http://dx.doi.org/10.4172/2329-6798.1000e103] [PMID: 23584997]
[71]
Craik, D.J.; Fairlie, D.P.; Liras, S.; Price, D. The future of peptide-based drugs. Chem. Biol. Drug Des., 2013, 81(1), 136-147.
[http://dx.doi.org/10.1111/cbdd.12055] [PMID: 23253135]
[72]
Du, Q.S.; Xie, N.Z.; Huang, R.B. Recent development of peptide drugs and advance on theory and methodology of peptide inhibitor design. Med. Chem., 2015, 11(3), 235-247.
[http://dx.doi.org/10.2174/1573406411666141229163355] [PMID: 25548931]
[73]
Xu, L.; Yu, Y.; Sang, R.; Li, J.; Ge, B.; Zhang, X. Protective effects of taraxasterol against ethanol-induced liver injury by regulating CYP2E1/Nrf2/HO-1 and NF-κB signaling pathways in mice. Oxid. Med. Cell. Longev., 2018, 2018, 8284107.
[http://dx.doi.org/10.1155/2018/8284107] [PMID: 30344887]
[74]
Soboloff, J.; Rothberg, B.S.; Madesh, M.; Gill, D.L. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol., 2012, 13(9), 549-565.
[http://dx.doi.org/10.1038/nrm3414] [PMID: 22914293]
[75]
Collins, H.E.; Zhu-Mauldin, X.; Marchase, R.B.; Chatham, J.C. STIM1/Orai1-mediated SOCE: current perspectives and potential roles in cardiac function and pathology. Am. J. Physiol. Heart Circ. Physiol., 2013, 305(4), H446-H458.
[http://dx.doi.org/10.1152/ajpheart.00104.2013] [PMID: 23792674]
[76]
Xie, Y.; Xiao, M.; Ni, Y.; Jiang, S.; Feng, G.; Sang, S.; Du, G. Alpinia oxyphylla Miq. Extract prevents diabetes in mice by modulating gut microbiota. J. Diabetes Res., 2018, 2018, 4230590.
[http://dx.doi.org/10.1155/2018/4230590] [PMID: 29967794]
[77]
Wang, P.; Han, J.; Wei, M.; Xu, Y.; Zhang, G.; Zhang, H.; Shi, L.; Liu, X.; Hamblin, M.R.; Wang, X. Remodeling of dermal collagen in photoaged skin using low-dose 5-aminolevulinic acid photodynamic therapy occurs via the transforming growth factor-β pathway. J. Biophotonics, 2018, 11(6), e201700357.
[http://dx.doi.org/10.1002/jbio.201700357] [PMID: 29431281]