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References

  1. Ayehunie S, Belay A, Baba TW, Ruprecht RM. 1998. Inhibition of HIV-1 replication by an aqueous extract of Spirulina platensis (Arthrospira platensis). J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18: 7-12.
    Pubmed CrossRef
  2. Baek M, Choy J-H, Choi S-J. 2012. Montmorillonite intercalated with glutathione for antioxidant delivery: synthesis, characterization, and bioavailability evaluation. Int. J. Pharm. 425: 29-34.
    Pubmed CrossRef
  3. Cai L, Wu X, Zhang Y, Li X, Ma S, Li J. 2015. Purification and characterization of three antioxidant peptides from protein hydrolysate of grass carp (Ctenopharyngodon idella) skin. J. Funct. Foods 16: 234-242.
    CrossRef
  4. Chen N, Yang H, Sun Y, Niu J, Liu S. 2012. Purification and identification of antioxidant peptides from walnut (Juglans regia L.) protein hydrolysates. Peptides 38: 344-349.
    Pubmed CrossRef
  5. Chen X-M, Yang F, Bai Y, Zhou Y-H, Zheng W-J. 2008. Effects of tellurium stress on the growth and antioxidase system of Spirulina platensis and S. maximum. Acta Hydrobiol. Sin. 32: 148-153.
    CrossRef
  6. Chi C-F, Hu F-Y, Wang B, Li Z-R, Luo H-Y. 2015. Influence of amino acid compositions and peptide profiles on antioxidant capacities of two protein hydrolysates from skipjack tuna (Katsuwonus pelamis) dark muscle. Mar. Drugs 13: 2580-2601.
    Pubmed PMC CrossRef
  7. Corrêa APF, Daroit DJ, Fontoura R, Meira SMM, Segalin J, Brandelli A. 2014. Hydrolysates of sheep cheese whey as a source of bioactive peptides with antioxidant and angiotensinconverting enzyme inhibitory activities. Peptides 61: 48-55.
    Pubmed CrossRef
  8. Elias RJ, Kellerby SS, Decker EA. 2008. Antioxidant activity of proteins and peptides. Crit. Rev. Food Sci. 48: 430-441.
    Pubmed CrossRef
  9. Escudero E, Mora L, Fraser PD, Aristoy M-C, Toldrá F. 2013. Identification of novel antioxidant peptides generated in Spanish dry-cured ham. Food Chem. 138: 1282-1288.
    Pubmed CrossRef
  10. Fan J, He J, Zhuang Y, Sun L. 2012. Purification and identification of antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) frame protein. Molecules 17: 12836-12850.
    Pubmed CrossRef
  11. Girgih AT, He R, Hasan FM, Udenigwe CC, Gill TA, Aluko RE. 2015. Evaluation of the in vitro antioxidant properties of a cod (Gadus morhua) protein hydrolysate and peptide fractions. Food Chem. 173: 652-659.
    Pubmed CrossRef
  12. Gonzalez-Burgos E, Carretero ME, Gomez-Serranillos MP. 2013. Kaurane diterpenes from Sideritis spp. exert a cytoprotective effect against oxidative injury that is associated with modulation of the Nrf2 system. Phytochemistry 93: 116-123.
    Pubmed CrossRef
  13. Hernández-Ledesma B, Dávalos A, Bartolomé B, Amigo L. 2005. Preparation of antioxidant enzymatic hydrolysates from α-lactalbumin and β-lactoglobulin. Identification of active peptides by HPLC-MS/MS. J. Agric. Food Chem. 53: 588-593.
    Pubmed CrossRef
  14. Ji K, Jang N, Kim Y. 2015. Isolation of lactic acid bacteria showing antioxidative and probiotic activities from kimchi and infant feces. J. Microbiol. Biotechnol. 25: 1568-1577.
    Pubmed CrossRef
  15. Karthikeyan R, Manivasagam T, Anantharaman P, Balasubramanian T, Somasundaram S. 2011. Chemopreventive effect of Padina boergesenii extracts on ferric nitrilotriacetate (Fe-NTA)-induced oxidative damage in Wistar rats. J. Appl. Phycol. 23: 257-263.
    CrossRef
  16. Khan M, Shobha JC, Mohan IK, Naidu MUR, Sundaram C, Singh S, et al. 2005. Protective effect of Spirulina against doxorubicin-induced cardiotoxicity. Phytother. Res. 19: 1030-1037.
    Pubmed CrossRef
  17. Konickova R, Vankova K, Vanikova J, Vanova K, Muchova L, Subhanova I, et al. 2014. Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann. Hepatol. 13: 273-283.
    Pubmed
  18. Kou X, Gao J, Xue Z, Zhang Z, Wang H, Wang X. 2013. Purification and identification of antioxidant peptides from chickpea (Cicer arietinum L.) albumin hydrolysates. LWT Food Sci. Technol. 50: 591-598.
    CrossRef
  19. Kulshreshtha A, Zacharia JA, Jarouliya U, Bhadauriya P, Prasad G, Bisen PS. 2008. Spirulina in health care management. Curr. Pharm. Biotechnol. 9: 400-405.
    Pubmed CrossRef
  20. Lee JK, Li-Chan EC, Byun H-G. 2015. Characterization of βsecretase inhibitory peptide purified from skate skin protein hydrolysate. Eur. Food Res. Technol. 240: 129-136.
    CrossRef
  21. Li Y, Jiang B, Zhang T, Mu W, Liu J. 2008. Antioxidant and free radical-scavenging activities of chickpea protein hydrolysate (CPH). Food Chem. 106: 444-450.
    CrossRef
  22. Liu J, Jin Y, Lin S, Jones GS, Chen F. 2015. Purification and identification of novel antioxidant peptides from egg white protein and their antioxidant activities. Food Chem. 175: 258266.
    Pubmed CrossRef
  23. Lopez-Barrios L, Gutierrez-Uribe JA, Serna-Saldivar SO. 2014. Bioactive peptides and hydrolysates from pulses and their potential use as functional ingredients. J. Food Sci. 79:R273-R283.
    Pubmed CrossRef
  24. Moure A, Domínguez H, Parajó JC. 2006. Antioxidant properties of ultrafiltration-recovered soy protein fractions from industrial effluents and their hydrolysates. Process Biochem. 41: 447-456.
    CrossRef
  25. Rajapakse N, Mendis E, Byun HG, Kim SK. 2005. Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. J. Nutr. Biochem. 16: 562-569.
    Pubmed CrossRef
  26. Remirez D, González R, Merino N, Rodriguez S, Ancheta O. 2002. Inhibitory effects of Spirulina in zymosan-induced arthritis in mice. Mediat. Inflamm. 11: 75-79.
    Pubmed PMC CrossRef
  27. Sarmadi BH, Ismail A. 2010. Antioxidative peptides from food proteins: a review. Peptides 31: 1949-1956.
    Pubmed CrossRef
  28. Shimamatsu H. 2004. Mass production of Spirulina, an edible microalga, pp. 39-44. Asian Pacific Phycology in the 21st Century: Prospects and Challenges. Springer, Berlin.
  29. Stadtman ER. 2006. Protein oxidation and aging. Free Radic. Res. 40: 1250-1258.
    Pubmed CrossRef
  30. Tümay M, Hatungil R, Berköz M, Yalin S, Erdogan S. 2013. Role of free radicals on retinitis pigmentosa. Asian J. Chem. 25: 1561.
  31. Tayag CM, Lin YC, Li CC, Liou CH, Chen JC. 2010. Administration of the hot-water extract of Spirulina platensis enhanced the immune response of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immun. 28: 764-773.
    Pubmed CrossRef
  32. Tobon-Velasco JC, Palafox-Sanchez V, Mendieta L, Garcia E, Santamaria A, Chamorro-Cevallos G, Limon ID. 2013. Antioxidant effect of Spirulina (Arthrospira) maxima in a neurotoxic model caused by 6-OHDA in the rat striatum. J. Neural Transm. 120: 1179-1189.
    Pubmed CrossRef
  33. Torres-Durán P, Miranda-Zamora R, Paredes-Carbajal M, Mascher D, Blé-Castillo J, Dýaz-Zagoya J, Juárez-Oropeza M. 1999. Studies on the preventive effect of Spirulina maxima on fatty liver development induced by carbon tetrachloride, in the rat. J. Ethnopharmacol. 64: 141-147.
    CrossRef
  34. Wang L-S, Huang J-C, Chen Y-L, Huang M, Zhou G-H. 2015. Identification and characterization of antioxidant peptides from enzymatic hydrolysates of duck meat. J. Agric. Food Chem. 63: 3437-3444.
    Pubmed CrossRef
  35. Yang F, Wong KH, Yang YF, Li XL, Jiang J, Zheng WJ, et al. 2014. Purification and in vitro antioxidant activities of tellurium-containing phycobiliproteins from tellurium-enriched Spirulina platensis. Drug Des. Dev. Ther. 8: 1789-1800.
    Pubmed PMC
  36. Zhang T, Li Y, Miao M, Jiang B. 2011. Purification and characterisation of a new antioxidant peptide from chickpea (Cicer arietium L.) protein hydrolysates. Food Chem. 128: 28-33.
    Pubmed CrossRef
  37. Zhang Y, Duan X, Zhuang Y. 2012. Purification and characterization of novel antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) skin gelatin. Peptides 38: 13-21.
    Pubmed CrossRef
  38. Zheng XF, Sun XJ, Xia ZF. 2011. Hydrogen resuscitation, a new cytoprotective approach. Clin. Exp. Pharmacol. Physiol. 38: 155-163.
    Pubmed CrossRef
  39. Zhuang H, Tang N, Yuan Y. 2013. Purification and identification of antioxidant peptides from corn gluten meal. J. Funct. Foods 5: 1810-1821.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(7): 1216-1223

Published online July 28, 2016 https://doi.org/10.4014/jmb.1601.01033

Copyright © The Korean Society for Microbiology and Biotechnology.

Purification and Identification of Antioxidant Peptides from Enzymatic Hydrolysate of Spirulina platensis

Jie Yu 1, 2, Yuanliang Hu 1, 2, Mingxiong Xue 3, Yaohao Dun 2, Shenao Li 2, Nan Peng 2, Yunxiang Liang 2, 4 and Shumao Zhao 2, 4*

1Hubei Key Laboratory of Edible Wild Plants Conservation & Utilization, College of Life Sciences, Hubei Normal University, Huangshi 435002, P.R. China, 2State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, P.R. China, 3Beihai Shengbada Biotech Co., Ltd, Beihai 536000, P.R. China, 4Hubei Collaborative Innovation Center for Industrial Fermentation, Wuhan 430068, P.R. China

Received: January 15, 2016; Accepted: April 10, 2016

Abstract

The aim of this study was to isolate antioxidant peptides from an enzymatic hydrolysate of
Spirulina platensis. A novel antioxidant peptide was obtained by ultrafiltration, gel filtration
chromatography, and reverse-phase high-performance liquid chromatography, with the 1,1-
diphenyl-2-picrylhydrazyl (DPPH) radical scavenging assay used to measure the antioxidant
activity, and the sequence was determined to be Pro-Asn-Asn (343.15 Da) by electrospray
ionization tandem mass spectrometry. This peptide was synthesized to confirm its antioxidant
properties, and it exhibited 81.44 ± 0.43% DPPH scavenging activity at 100 μg/ml, which was
similar to that of glutathione (82.63 ± 0.56%). Furthermore, the superoxide anion and hydroxyl
free-radical scavenging activities and the SOD activity of the peptide were 47.84 ± 0.49%, 54.01
± 0.82%, and 12.55 ± 0.75%, respectively, at 10 mg/ml. These results indicate that S. platensis is
a good source of antioxidant peptides, and that its hydrolysate may have important
applications in the pharmaceutical and food industries.

Keywords: Antioxidant peptide, free radical-scavenging activity, mass spectrometry, purification, Spirulina platensis

References

  1. Ayehunie S, Belay A, Baba TW, Ruprecht RM. 1998. Inhibition of HIV-1 replication by an aqueous extract of Spirulina platensis (Arthrospira platensis). J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18: 7-12.
    Pubmed CrossRef
  2. Baek M, Choy J-H, Choi S-J. 2012. Montmorillonite intercalated with glutathione for antioxidant delivery: synthesis, characterization, and bioavailability evaluation. Int. J. Pharm. 425: 29-34.
    Pubmed CrossRef
  3. Cai L, Wu X, Zhang Y, Li X, Ma S, Li J. 2015. Purification and characterization of three antioxidant peptides from protein hydrolysate of grass carp (Ctenopharyngodon idella) skin. J. Funct. Foods 16: 234-242.
    CrossRef
  4. Chen N, Yang H, Sun Y, Niu J, Liu S. 2012. Purification and identification of antioxidant peptides from walnut (Juglans regia L.) protein hydrolysates. Peptides 38: 344-349.
    Pubmed CrossRef
  5. Chen X-M, Yang F, Bai Y, Zhou Y-H, Zheng W-J. 2008. Effects of tellurium stress on the growth and antioxidase system of Spirulina platensis and S. maximum. Acta Hydrobiol. Sin. 32: 148-153.
    CrossRef
  6. Chi C-F, Hu F-Y, Wang B, Li Z-R, Luo H-Y. 2015. Influence of amino acid compositions and peptide profiles on antioxidant capacities of two protein hydrolysates from skipjack tuna (Katsuwonus pelamis) dark muscle. Mar. Drugs 13: 2580-2601.
    Pubmed KoreaMed CrossRef
  7. Corrêa APF, Daroit DJ, Fontoura R, Meira SMM, Segalin J, Brandelli A. 2014. Hydrolysates of sheep cheese whey as a source of bioactive peptides with antioxidant and angiotensinconverting enzyme inhibitory activities. Peptides 61: 48-55.
    Pubmed CrossRef
  8. Elias RJ, Kellerby SS, Decker EA. 2008. Antioxidant activity of proteins and peptides. Crit. Rev. Food Sci. 48: 430-441.
    Pubmed CrossRef
  9. Escudero E, Mora L, Fraser PD, Aristoy M-C, Toldrá F. 2013. Identification of novel antioxidant peptides generated in Spanish dry-cured ham. Food Chem. 138: 1282-1288.
    Pubmed CrossRef
  10. Fan J, He J, Zhuang Y, Sun L. 2012. Purification and identification of antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) frame protein. Molecules 17: 12836-12850.
    Pubmed CrossRef
  11. Girgih AT, He R, Hasan FM, Udenigwe CC, Gill TA, Aluko RE. 2015. Evaluation of the in vitro antioxidant properties of a cod (Gadus morhua) protein hydrolysate and peptide fractions. Food Chem. 173: 652-659.
    Pubmed CrossRef
  12. Gonzalez-Burgos E, Carretero ME, Gomez-Serranillos MP. 2013. Kaurane diterpenes from Sideritis spp. exert a cytoprotective effect against oxidative injury that is associated with modulation of the Nrf2 system. Phytochemistry 93: 116-123.
    Pubmed CrossRef
  13. Hernández-Ledesma B, Dávalos A, Bartolomé B, Amigo L. 2005. Preparation of antioxidant enzymatic hydrolysates from α-lactalbumin and β-lactoglobulin. Identification of active peptides by HPLC-MS/MS. J. Agric. Food Chem. 53: 588-593.
    Pubmed CrossRef
  14. Ji K, Jang N, Kim Y. 2015. Isolation of lactic acid bacteria showing antioxidative and probiotic activities from kimchi and infant feces. J. Microbiol. Biotechnol. 25: 1568-1577.
    Pubmed CrossRef
  15. Karthikeyan R, Manivasagam T, Anantharaman P, Balasubramanian T, Somasundaram S. 2011. Chemopreventive effect of Padina boergesenii extracts on ferric nitrilotriacetate (Fe-NTA)-induced oxidative damage in Wistar rats. J. Appl. Phycol. 23: 257-263.
    CrossRef
  16. Khan M, Shobha JC, Mohan IK, Naidu MUR, Sundaram C, Singh S, et al. 2005. Protective effect of Spirulina against doxorubicin-induced cardiotoxicity. Phytother. Res. 19: 1030-1037.
    Pubmed CrossRef
  17. Konickova R, Vankova K, Vanikova J, Vanova K, Muchova L, Subhanova I, et al. 2014. Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann. Hepatol. 13: 273-283.
    Pubmed
  18. Kou X, Gao J, Xue Z, Zhang Z, Wang H, Wang X. 2013. Purification and identification of antioxidant peptides from chickpea (Cicer arietinum L.) albumin hydrolysates. LWT Food Sci. Technol. 50: 591-598.
    CrossRef
  19. Kulshreshtha A, Zacharia JA, Jarouliya U, Bhadauriya P, Prasad G, Bisen PS. 2008. Spirulina in health care management. Curr. Pharm. Biotechnol. 9: 400-405.
    Pubmed CrossRef
  20. Lee JK, Li-Chan EC, Byun H-G. 2015. Characterization of βsecretase inhibitory peptide purified from skate skin protein hydrolysate. Eur. Food Res. Technol. 240: 129-136.
    CrossRef
  21. Li Y, Jiang B, Zhang T, Mu W, Liu J. 2008. Antioxidant and free radical-scavenging activities of chickpea protein hydrolysate (CPH). Food Chem. 106: 444-450.
    CrossRef
  22. Liu J, Jin Y, Lin S, Jones GS, Chen F. 2015. Purification and identification of novel antioxidant peptides from egg white protein and their antioxidant activities. Food Chem. 175: 258266.
    Pubmed CrossRef
  23. Lopez-Barrios L, Gutierrez-Uribe JA, Serna-Saldivar SO. 2014. Bioactive peptides and hydrolysates from pulses and their potential use as functional ingredients. J. Food Sci. 79:R273-R283.
    Pubmed CrossRef
  24. Moure A, Domínguez H, Parajó JC. 2006. Antioxidant properties of ultrafiltration-recovered soy protein fractions from industrial effluents and their hydrolysates. Process Biochem. 41: 447-456.
    CrossRef
  25. Rajapakse N, Mendis E, Byun HG, Kim SK. 2005. Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. J. Nutr. Biochem. 16: 562-569.
    Pubmed CrossRef
  26. Remirez D, González R, Merino N, Rodriguez S, Ancheta O. 2002. Inhibitory effects of Spirulina in zymosan-induced arthritis in mice. Mediat. Inflamm. 11: 75-79.
    Pubmed KoreaMed CrossRef
  27. Sarmadi BH, Ismail A. 2010. Antioxidative peptides from food proteins: a review. Peptides 31: 1949-1956.
    Pubmed CrossRef
  28. Shimamatsu H. 2004. Mass production of Spirulina, an edible microalga, pp. 39-44. Asian Pacific Phycology in the 21st Century: Prospects and Challenges. Springer, Berlin.
  29. Stadtman ER. 2006. Protein oxidation and aging. Free Radic. Res. 40: 1250-1258.
    Pubmed CrossRef
  30. Tümay M, Hatungil R, Berköz M, Yalin S, Erdogan S. 2013. Role of free radicals on retinitis pigmentosa. Asian J. Chem. 25: 1561.
  31. Tayag CM, Lin YC, Li CC, Liou CH, Chen JC. 2010. Administration of the hot-water extract of Spirulina platensis enhanced the immune response of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immun. 28: 764-773.
    Pubmed CrossRef
  32. Tobon-Velasco JC, Palafox-Sanchez V, Mendieta L, Garcia E, Santamaria A, Chamorro-Cevallos G, Limon ID. 2013. Antioxidant effect of Spirulina (Arthrospira) maxima in a neurotoxic model caused by 6-OHDA in the rat striatum. J. Neural Transm. 120: 1179-1189.
    Pubmed CrossRef
  33. Torres-Durán P, Miranda-Zamora R, Paredes-Carbajal M, Mascher D, Blé-Castillo J, Dýaz-Zagoya J, Juárez-Oropeza M. 1999. Studies on the preventive effect of Spirulina maxima on fatty liver development induced by carbon tetrachloride, in the rat. J. Ethnopharmacol. 64: 141-147.
    CrossRef
  34. Wang L-S, Huang J-C, Chen Y-L, Huang M, Zhou G-H. 2015. Identification and characterization of antioxidant peptides from enzymatic hydrolysates of duck meat. J. Agric. Food Chem. 63: 3437-3444.
    Pubmed CrossRef
  35. Yang F, Wong KH, Yang YF, Li XL, Jiang J, Zheng WJ, et al. 2014. Purification and in vitro antioxidant activities of tellurium-containing phycobiliproteins from tellurium-enriched Spirulina platensis. Drug Des. Dev. Ther. 8: 1789-1800.
    Pubmed KoreaMed
  36. Zhang T, Li Y, Miao M, Jiang B. 2011. Purification and characterisation of a new antioxidant peptide from chickpea (Cicer arietium L.) protein hydrolysates. Food Chem. 128: 28-33.
    Pubmed CrossRef
  37. Zhang Y, Duan X, Zhuang Y. 2012. Purification and characterization of novel antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) skin gelatin. Peptides 38: 13-21.
    Pubmed CrossRef
  38. Zheng XF, Sun XJ, Xia ZF. 2011. Hydrogen resuscitation, a new cytoprotective approach. Clin. Exp. Pharmacol. Physiol. 38: 155-163.
    Pubmed CrossRef
  39. Zhuang H, Tang N, Yuan Y. 2013. Purification and identification of antioxidant peptides from corn gluten meal. J. Funct. Foods 5: 1810-1821.
    CrossRef