Bioactive Peptides from Fish Protein By-Products

  • Aurélien V. Le Gouic
  • Pádraigín A. Harnedy
  • Richard J. FitzGeraldEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


The interest in fish processing by-products and underutilized catch for the production of biofunctional food ingredients has increased in the last number of decades. These marine-derived components contain a significant quantity of protein, which is normally processed into low-value products such as animal feed, fishmeal, and fertilizer. However, due to the global demand for high-quality protein and the need for sustainable production and processing of landed material, the valorization of proteins and other nutrients from fish processing by-products has significantly increased. Fish processing by-products contain significant quantities of high-quality protein, which can be exploited as sources of essential nitrogenous nutrients and biologically active peptides. Bioactive peptides, including those from fish processing by-products, have been reported to possess the ability to beneficially modulate physiological processes associated with noncommunicable diseases. These short peptides, which are encrypted within the primary sequence of the parent protein and are released during food processing or gastrointestinal digestion, could have a role in the prevention and management of these diseases. This chapter reviews the recent literature on the processing and utilization of proteins and protein hydrolysates from fish processing by-products and underutilized fish species with a particular focus on their bioactive properties and peptide sequences.


By-products Proteins Hydrolysates Biofunctional properties Fish Peptides Noncommunicable diseases 



Aurélien V. Le Gouic and Pádraigín A. Harnedy were funded by the Department of Agriculture, Food and the Marine, Ireland, under grant issue 14/F/873 and 13/F/467, respectively.


  1. 1.
    Teh LCL, Sumaila UR (2013) Contribution of marine fisheries to worldwide employment. Fish Fish 14:77–88CrossRefGoogle Scholar
  2. 2.
    FAO (2016) The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. FAO, RomeGoogle Scholar
  3. 3.
    Chalamaiah M, Dinesh Kumar B, Hemalatha R et al (2012) Fish protein hydrolysates: proximate composition, amino acid composition, antioxidant activities and applications: a review. Food Chem 135:3020–3038PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Commission Delegated (20 October 2014) Regulation (EU) No 1392/2014 – establishing a discard plan for certain small pelagic fisheries in the Mediterranean Sea, BrusselsGoogle Scholar
  5. 5.
    García-Moreno PJ, Pérez-Gálvez R, Espejo-Carpio FJ et al (2017) Functional, bioactive and antigenicity properties of blue whiting protein hydrolysates: effect of enzymatic treatment and degree of hydrolysis. J Sci Food Agric 97:299–308PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Neves AC, Harnedy PA, O’Keeffe MB et al (2017) Bioactive peptides from Atlantic salmon (Salmo salar) with angiotensin converting enzyme and dipeptidyl peptidase IV inhibitory, and antioxidant activities. Food Chem 218:396–405PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Sukkhown P, Jangchud K, Lorjaroenphon Y et al (2018) Flavored-functional protein hydrolysates from enzymatic hydrolysis of dried squid by-products: effect of drying method. Food Hydrocoll 76:103–112CrossRefGoogle Scholar
  8. 8.
    Ettelaie R, Zengin A, Lishchuk SV (2017) Novel food grade dispersants: review of recent progress. Curr Opin Colloid Interface Sci 28:46–55CrossRefGoogle Scholar
  9. 9.
    Lafarga T, Hayes M (2017) Bioactive protein hydrolysates in the functional food ingredient industry: overcoming current challenges. Food Rev Int 33:217–246CrossRefGoogle Scholar
  10. 10.
    Sidhu KS (2003) Health benefits and potential risks related to consumption of fish or fish oil. Regul Toxicol Pharmacol 38:336–344PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Ross A, Vincent A, Savolainen OI et al (2017) Dietary protein sources beyond proteins and amino acids – a comparative study of the small molecular weight components of meat and fish using metabolomics. FASEB J 31:652.613Google Scholar
  12. 12.
    Pangestuti R, Kim S-K (2017) Bioactive peptide of marine origin for the prevention and treatment of non-communicable diseases. Mar Drugs 15:67PubMedCentralCrossRefGoogle Scholar
  13. 13.
    Felix M, Romero A, Rustad T et al (2017) Physicochemical, microstructure and bioactive characterization of gels made from crayfish protein. Food Hydrocoll 63:429–436CrossRefGoogle Scholar
  14. 14.
    Vidotti RM, Viegas EMM, Carneiro DJ (2003) Amino acid composition of processed fish silage using different raw materials. Anim Feed Sci Technol 105:199–204CrossRefGoogle Scholar
  15. 15.
    Villamil O, Váquiro H, Solanilla JF (2017) Fish viscera protein hydrolysates: production, potential applications and functional and bioactive properties. Food Chem 224:160–171PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Friedman M (1996) Nutritional value of proteins from different food sources. A review. J Agric Food Chem 44:6–29CrossRefGoogle Scholar
  17. 17.
    Venugopal V (2009) Seafood proteins: functional properties and protein supplements. In: Venugopal V (ed) Marine products for healthcare: functional and bioactive nutraceutical compounds from the ocean. CRC Press, Boca Raton, pp 51–102Google Scholar
  18. 18.
    Bechtel PJ (1986) Muscle development and contractile proteins. In: Muscle as food. Academic, San Diego, pp 1–35Google Scholar
  19. 19.
    Lowey S, Risby D (1971) Light chains from fast and slow muscle myosins. Nature 234:81–85PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Lanier T, Yongsawatdigul J, Carvajal-Rondanelli P (2013) Surimi gelation chemistry. In: Park J (ed) Surimi and surimi seafood, 3rd edn. CRC Press, Boca Raton, pp 101–140CrossRefGoogle Scholar
  22. 22.
    Kim S-K, Mendis E (2006) Bioactive compounds from marine processing byproducts – a review. Food Res Int 39:383–393CrossRefGoogle Scholar
  23. 23.
    Pearson AM, Young RB (1989) The connective tissues: collagen, elastin, and ground substance. In: Pearson AM (ed) Muscle and meat biochemistry. Academic, San Diego, pp 338–390CrossRefGoogle Scholar
  24. 24.
    Kristinsson HG, Lanier TC, Halldorsdottir SM et al (2013) Fish protein isolate by pH shift. In: Park J (ed) Surimi and surimi seafood, 3rd edn. CRC Press, Boca Raton, pp 169–192CrossRefGoogle Scholar
  25. 25.
    Hayes M, Mora L, Hussey K et al (2016) Boarfish protein recovery using the pH-shift process and generation of protein hydrolysates with ACE-I and antihypertensive bioactivities in spontaneously hypertensive rats. Innovative Food Sci Emerg Technol 37:253–260CrossRefGoogle Scholar
  26. 26.
    Park J, Graves D, Draves R et al (2013) Manufacture of surimi. In: Park J (ed) Surimi and surimi seafood, 3rd edn. CRC Press, Boca Raton, pp 55–100CrossRefGoogle Scholar
  27. 27.
    Nguyen E, Jones O, Kim YHB et al (2017) Impact of microwave-assisted enzymatic hydrolysis on functional and antioxidant properties of rainbow trout Oncorhynchus mykiss by-products. Fish Sci 83:317–331CrossRefGoogle Scholar
  28. 28.
    Auwal SM, Zarei M, Abdul-Hamid A et al (2017) Optimization of bromelain-aided production of angiotensin I-converting enzyme inhibitory hydrolysates from stone fish using response surface methodology. Mar Drugs 15:104PubMedCentralCrossRefGoogle Scholar
  29. 29.
    Salampessy J, Reddy N, Phillips M et al (2017) Isolation and characterization of nutraceutically potential ACE-inhibitory peptides from leatherjacket (Meuchenia sp.) protein hydrolysates. LWT Food Sci Technol 80:430–436CrossRefGoogle Scholar
  30. 30.
    Klomklao S, Benjakul S (2017) Utilization of tuna processing byproducts: protein hydrolysate from skipjack tuna (Katsuwonus pelamis) viscera. J Food Process Preserv 41:e12970CrossRefGoogle Scholar
  31. 31.
    Venkatesan J, Anil S, Kim S-K et al (2017) Marine fish proteins and peptides for cosmeceuticals: a review. Mar Drugs 15:143PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Cermeño M, FitzGerald RJ, O’Brien NM (2016) In vitro antioxidant and immunomodulatory activity of transglutaminase-treated sodium caseinate hydrolysates. Int Dairy J 63:107–114CrossRefGoogle Scholar
  33. 33.
    Jeewanthi RKC, Lee N-K, Paik H-D (2015) Improved functional characteristics of whey protein hydrolysates in food industry. Korean J Food Sci Anim Resour 35:350–359PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Adler-Nissen J (1976) Enzymatic hydrolysis of proteins for increased solubility. J Agric Food Chem 24:1090–1093PubMedCrossRefGoogle Scholar
  35. 35.
    Pacheco-Aguilar R, Mazorra-Manzano MA, Ramírez-Suárez JC (2008) Functional properties of fish protein hydrolysates from Pacific whiting (Merluccius productus) muscle produced by a commercial protease. Food Chem 109:782–789PubMedCrossRefGoogle Scholar
  36. 36.
    Guérard F, Decourcelle N, Sabourin C et al (2010) Recent developments of marine ingredients for food and nutraceutical applications: a review. J Sci Halieut Aquat 2:21–27Google Scholar
  37. 37.
    Chéret R, Delbarre-Ladrat C, de Lamballerie-Anton M et al (2007) Calpain and cathepsin activities in post mortem fish and meat muscles. Food Chem 101:1474–1479CrossRefGoogle Scholar
  38. 38.
    Busconi L, Folco EJ, Martone C et al (1984) Identification of two alkaline proteases and a trypsin inhibitor from muscle of white croaker (Micropogon opercularis). FEBS Lett 176:211–214CrossRefGoogle Scholar
  39. 39.
    Li Q, Zhang L, Lu H et al (2017) Comparison of postmortem changes in ATP-related compounds, protein degradation and endogenous enzyme activity of white muscle and dark muscle from common carp (Cyprinus carpio) stored at 4 °C. LWT Food Sci Technol 78:317–324CrossRefGoogle Scholar
  40. 40.
    Kleekayai T, Harnedy PA, O’Keeffe MB et al (2015) Extraction of antioxidant and ACE inhibitory peptides from Thai traditional fermented shrimp pastes. Food Chem 176:441–447PubMedCrossRefGoogle Scholar
  41. 41.
    Wenno MR, Suprayitno E, Aulanni’am Aulanni’am H (2016) Identification and molecular interaction, mechanism and angiotensin converting enzyme inhibitory peptide from Bakasang (fermented Skipjack tuna (Katsuwonus pelamis)). Int J PharmTech Res 9:591–598Google Scholar
  42. 42.
    Mouritsen OG, Duelund L, Calleja G et al (2017) Flavour of fermented fish, insect, game, and pea sauces: garum revisited. Int J Gastron Food Sci 9:16–28CrossRefGoogle Scholar
  43. 43.
    Kumar S, Nayak BB (2015) Health benefits of fermented fish. In: Prakash Tamang J (ed) Health Benefits of Fermented Foods and Beverages. CRC Press, Boca Raton, FL, 475–488Google Scholar
  44. 44.
    Skåra T, Axelsson L, Stefánsson G et al (2015) Fermented and ripened fish products in the northern European countries. J Ethnic Foods 2:18–24CrossRefGoogle Scholar
  45. 45.
    Wu H-C, Chen H-M, Shiau C-Y (2003) Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber australasicus). Food Res Int 36:949–957CrossRefGoogle Scholar
  46. 46.
    Wisuthiphaet N, Kongruang S, Chamcheun C (2015) Production of fish protein hydrolysates by acid and enzymatic hydrolysis. J Med Bioeng 4:466–470Google Scholar
  47. 47.
    Beddows CG (1997) Fermented fish and fish products. In: Wood BJB (ed) Microbiology of fermented foods. Springer, Boston, pp 416–440Google Scholar
  48. 48.
    Korhonen H, Pihlanto A (2006) Bioactive peptides: production and functionality. Int Dairy J 16:945–960CrossRefGoogle Scholar
  49. 49.
    Udenigwe CC, Aluko RE (2012) Food protein-derived bioactive peptides: production, processing, and potential health benefits. J Food Sci 77:R11–R24PubMedCrossRefGoogle Scholar
  50. 50.
    Bouglé D, Bouhallab S (2017) Dietary bioactive peptides: human studies. Crit Rev Food Sci Nutr 57:335–343PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Jo C, Khan FF, Khan MI et al (2017) Marine bioactive peptides: types, structures, and physiological functions. Food Rev Int 33:44–61CrossRefGoogle Scholar
  52. 52.
    Wilkins E, Wilson L, Wickramasinghe K et al (2017) European cardiovascular disease statistics 2017. European Heart Network, BrusselsGoogle Scholar
  53. 53.
    Zielińska E, Baraniak B, Karaś M (2017) Antioxidant and anti-inflammatory activities of hydrolysates and peptide fractions obtained by enzymatic hydrolysis of selected heat-treated edible insects. Nutrients 9:970PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Nongonierma AB, Lalmahomed M, Paolella S et al (2017) Milk protein isolate (MPI) as a source of dipeptidyl peptidase IV (DPP-IV) inhibitory peptides. Food Chem 231:202–211PubMedCrossRefGoogle Scholar
  55. 55.
    Vieira EF, da Silva DD, Carmo H et al (2017) Protective ability against oxidative stress of brewers’ spent grain protein hydrolysates. Food Chem 228:602–609PubMedCrossRefGoogle Scholar
  56. 56.
    Mao X, Bai L, Fan X et al (2017) Anti-proliferation peptides from protein hydrolysates of Pyropia haitanensis. J Appl Phycol 29:1623–1633CrossRefGoogle Scholar
  57. 57.
    Nongonierma AB, Hennemann M, Paolella S et al (2017) Generation of wheat gluten hydrolysates with dipeptidyl peptidase IV (DPP-IV) inhibitory properties. Food Funct 8:2249–2257PubMedCrossRefGoogle Scholar
  58. 58.
    Nongonierma AB, Paolella S, Mudgil P et al (2017) Dipeptidyl peptidase IV (DPP-IV) inhibitory properties of camel milk protein hydrolysates generated with trypsin. J Funct Foods 34:49–58CrossRefGoogle Scholar
  59. 59.
    Mojica L, Luna-Vital DA, González de Mejía E (2017) Characterization of peptides from common bean protein isolates and their potential to inhibit markers of type-2 diabetes, hypertension and oxidative stress. J Sci Food Agric 97:2401–2410PubMedCrossRefGoogle Scholar
  60. 60.
    Zhou D-Y, Liu Z-Y, Zhao J et al (2017) Antarctic krill (Euphausia superba) protein hydrolysates stimulate cholecystokinin release in STC-1 cells and its signaling mechanism. J Food Process Preserv 41:e12903CrossRefGoogle Scholar
  61. 61.
    Flaim C, Kob M, Di Pierro AM et al (2017) Effects of a whey proteins supplementation on oxidative stress, body composition and glucose metabolism among overweight people affected by diabetes mellitus or impaired fasting glucose: a pilot study. J Nutr Biochem 50:95–102PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Nobile V, Duclos E, Michelotti A et al (2016) Supplementation with a fish protein hydrolysate (Micromesistius poutassou): effects on body weight, body composition, and CCK/GLP-1 secretion. Food Nutr Res 60:29857PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Poprac P, Jomova K, Simunkova M et al (2016) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38:592–607PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Neves AC, Harnedy PA, O’Keeffe MB et al (2017) Peptide identification in a salmon gelatin hydrolysate with antihypertensive, dipeptidyl peptidase IV inhibitory and antioxidant activities. Food Res Int 100:112–120PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Li-Chan ECY, Hunag S-L, Jao C-L et al (2012) Peptides derived from Atlantic salmon skin gelatin as dipeptidyl-peptidase IV inhibitors. J Agric Food Chem 60:973–978PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Gu R-Z, Li C-Y, Liu W-Y et al (2011) Angiotensin I-converting enzyme inhibitory activity of low-molecular-weight peptides from Atlantic salmon (Salmo salar L.) skin. Food Res Int 44:1536–1540CrossRefGoogle Scholar
  67. 67.
    Ahn C-B, Cho Y-S, Je J-Y (2015) Purification and anti-inflammatory action of tripeptide from salmon pectoral fin byproduct protein hydrolysate. Food Chem 168:151–156PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Jung W-K, Karawita R, Heo S-J et al (2006) Recovery of a novel Ca-binding peptide from Alaska Pollack (Theragra chalcogramma) backbone by pepsinolytic hydrolysis. Process Biochem 41:2097–2100CrossRefGoogle Scholar
  69. 69.
    Hou H, Fan Y, Li B et al (2012) Purification and identification of immunomodulating peptides from enzymatic hydrolysates of Alaska pollock frame. Food Chem 134:821–828PubMedCrossRefGoogle Scholar
  70. 70.
    Guo L, Harnedy PA, O’Keeffe MB et al (2015) Fractionation and identification of Alaska pollock skin collagen-derived mineral chelating peptides. Food Chem 173:536–542PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Nikoo M, Benjakul S, Ehsani A et al (2014) Antioxidant and cryoprotective effects of a tetrapeptide isolated from Amur sturgeon skin gelatin. J Funct Foods 7:609–620CrossRefGoogle Scholar
  72. 72.
    Lee S-H, Qian Z-J, Kim S-K (2010) A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats. Food Chem 118:96–102CrossRefGoogle Scholar
  73. 73.
    Je J-Y, Qian Z-J, Byun H-G et al (2007) Purification and characterization of an antioxidant peptide obtained from tuna backbone protein by enzymatic hydrolysis. Process Biochem 42:840–846CrossRefGoogle Scholar
  74. 74.
    Chi C-F, Wang B, Hu F-Y et al (2015) Purification and identification of three novel antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) skin. Food Res Int 73:124–129CrossRefGoogle Scholar
  75. 75.
    Egerton S, Culloty S, Whooley J et al (2017) Characterization of protein hydrolysates from blue whiting (Micromesistius poutassou) and their application in beverage fortification. Food Chem 245:698–706PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Rochelle HDL, Courois E, Cudennec B et al (2015) Fish protein hydrolysate having a satietogenic activity, nutraceutical and pharmacological compositions comprising such a hydrolysate and method for obtaining same. Compagnie des Pêches Saint Malo Santé, Museum National D’Histoire Naturelle. US Patent 14/085,350, 22 Jan 2015Google Scholar
  77. 77.
    Harnedy PA, Parthsarathy V, McLaughlin CM et al (2018) Blue whiting (Micromesistius poutassou) muscle protein hydrolysate with in vitro and in vivo antidiabetic properties. J Funct Foods 40:137–145CrossRefGoogle Scholar
  78. 78.
    Song R, Wei R, Zhang B et al (2011) Antioxidant and antiproliferative activities of heated sterilized pepsin hydrolysate derived from half-fin anchovy (Setipinna taty). Mar Drugs 9:1142–1156PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    You L, Zhao M, Liu RH et al (2011) Antioxidant and antiproliferative activities of loach (Misgurnus anguillicaudatus) peptides prepared by papain digestion. J Agric Food Chem 59:7948–7953PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Hsu K-C, Li-Chan ECY, Jao C-L (2011) Antiproliferative activity of peptides prepared from enzymatic hydrolysates of tuna dark muscle on human breast cancer cell line MCF-7. Food Chem 126:617–622CrossRefGoogle Scholar
  81. 81.
    Huang S-L, Jao C-L, Ho K-P et al (2012) Dipeptidyl-peptidase IV inhibitory activity of peptides derived from tuna cooking juice hydrolysates. Peptides 35:114–121PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Ko J-Y, Kang N, Lee J-H et al (2016) Angiotensin I-converting enzyme inhibitory peptides from an enzymatic hydrolysate of flounder fish (Paralichthys olivaceus) muscle as a potent anti-hypertensive agent. Process Biochem 51:535–541CrossRefGoogle Scholar
  83. 83.
    Mahmoodani F, Ghassem M, Babji AS et al (2014) ACE inhibitory activity of pangasius catfish (Pangasius sutchi) skin and bone gelatin hydrolysate. J Food Sci Technol 51:1847–1856PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Kim HJ, Park KH, Shin JH et al (2011) Antioxidant and ACE inhibiting activities of the rockfish Sebastes hubbsi skin gelatin hydrolysates produced by sequential two-step enzymatic hydrolysis. Fish Aquat Sci 14:1–10Google Scholar
  85. 85.
    Chalamaiah M, Hemalatha R, Jyothirmayi T et al (2014) Immunomodulatory effects of protein hydrolysates from rohu (Labeo rohita) egg (roe) in BALB/c mice. Food Res Int 62:1054–1061CrossRefGoogle Scholar
  86. 86.
    Yang J-I, Tang J-Y, Liu Y-S et al (2016) Roe protein hydrolysates of Giant Grouper (Epinephelus lanceolatus) inhibit cell proliferation of oral cancer cells involving apoptosis and oxidative stress. Biomed Res Int 2016:12Google Scholar
  87. 87.
    Jang HL, Liceaga AM, Yoon KY (2017) Isolation and characteristics of anti-inflammatory peptides from enzymatic hydrolysates of sandfish (Arctoscopus japonicus) protein. J Aquat Food Prod Technol 26:234–244CrossRefGoogle Scholar
  88. 88.
    Senphan T, Benjakul S (2014) Antioxidative activities of hydrolysates from seabass skin prepared using protease from hepatopancreas of Pacific white shrimp. J Funct Foods 6:147–156CrossRefGoogle Scholar
  89. 89.
    Ngo D-H, Ryu B, Kim S-K (2014) Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. Food Chem 143:246–255PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Aissaoui N, Chobert J-M, Haertlé T et al (2017) Purification and biochemical characterization of a neutral serine protease from Trichoderma harzianum. Use in antibacterial peptide production from a fish by-product hydrolysate. Appl Biochem Biotechnol 182:831–845PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Karnjanapratum S, Benjakul S, O’Callaghan YC et al (2016) Purification and identification of antioxidant peptides from gelatin hydrolysates of unicorn leatherjacket skin. Ital J Food Sci 29:158–170Google Scholar
  92. 92.
    Vilas Boas LCP, de Lima LMP, Migliolo L et al (2017) Linear antimicrobial peptides with activity against Herpes simplex virus 1 and Aichi virus. Pept Sci 108:e22871CrossRefGoogle Scholar
  93. 93.
    Rajapakse N, Jung W-K, Mendis E et al (2005) A novel anticoagulant purified from fish protein hydrolysate inhibits factor XIIa and platelet aggregation. Life Sci 76:2607–2619PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Wang L, Dong C, Li X et al (2017) Anticancer potential of bioactive peptides from animal sources. Oncol Rep 38:637–651PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Ishak NH, Sarbon NM (2017) A review of protein hydrolysates and bioactive peptides deriving from wastes generated by fish processing. Food Bioprocess Technol. Scholar
  96. 96.
    Karoud W, Sila A, Krichen F et al (2017) Characterization, surface properties and biological activities of protein hydrolysates obtained from hake (Merluccius merluccius) heads. Waste Biomass Valorization. Scholar
  97. 97.
    Yesmine BH, Antoine B, da Silva Ortência Leocádia NG et al (2017) Identification of ACE inhibitory cryptides in Tilapia protein hydrolysate by UPLC–MS/MS coupled to database analysis. J Chromatogr B 1052:43–50CrossRefGoogle Scholar
  98. 98.
    Gauthier SF, Vachon C, Savoie L (1986) Enzymatic conditions of an in vitro method to study protein digestion. J Food Sci 51:960–964CrossRefGoogle Scholar
  99. 99.
    Fekete S, Veuthey J-L, Guillarme D (2012) New trends in reversed-phase liquid chromatographic separations of therapeutic peptides and proteins: theory and applications. J Pharm Biomed Anal 69:9–27PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Lemieux L, Piot J-M, Guillochon D et al (1991) Study of the efficiency of a mobile phase used in size-exclusion HPLC for the separation of peptides from a casein hydrolysate according to their hydrodynamic volume. Chromatographia 32:499–504CrossRefGoogle Scholar
  101. 101.
    Ghassem M, Arihara K, Mohammadi S et al (2017) Identification of two novel antioxidant peptides from edible bird’s nest (Aerodramus fuciphagus) protein hydrolysates. Food Funct 8:2046–2052PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    WHO (2014) Global status report on noncommunicable diseases 2014. World Health Organization, GenevaGoogle Scholar
  103. 103.
    Brieger K, Schiavone S, Miller FJ et al (2012) Reactive oxygen species: from health to disease. Swiss Med Wkly 142:w13659PubMedPubMedCentralGoogle Scholar
  104. 104.
    Machlin LJ, Bendich A (1987) Free radical tissue damage: protective role of antioxidant nutrients. FASEB J 1:441–445PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Barbour JA, Turner N (2014) Mitochondrial stress signaling promotes cellular adaptations. Int J Cell Biol 2014:156020PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Sae-Leaw T, Karnjanapratum S, O’Callaghan YC et al (2017) Purification and identification of antioxidant peptides from gelatin hydrolysate of seabass skin. J Food Biochem 41:e12350CrossRefGoogle Scholar
  107. 107.
    Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Hernández-Ledesma B, Dávalos A, Bartolomé B et al (2005) Preparation of antioxidant enzymatic hydrolysates from α-lactalbumin and β-lactoglobulin. Identification of active peptides by HPLC-MS/MS. J Agric Food Chem 53:588–593PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Murase H, Nagao A, Terao J (1993) Antioxidant and emulsifying activity of N-(long-chain-acyl) histidine and N-(long-chain-acyl) carnosine. J Agric Food Chem 41:1601–1604CrossRefGoogle Scholar
  110. 110.
    Park P-J, Jung W-K, Nam K-S et al (2001) Purification and characterization of antioxidative peptides from protein hydrolysate of lecithin-free egg yolk. J Am Oil Chem Soc 78:651–656CrossRefGoogle Scholar
  111. 111.
    Husain Z, Schwartz RA (2013) Food allergy update: more than a peanut of a problem. Int J Dermatol 52:286–294PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Pawankar R (2014) Allergic diseases and asthma: a global public health concern and a call to action. World Allergy Organ J 7:12–14PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7:131–137PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Le Y, Zhou Y, Iribarren P et al (2004) Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cell Mol Immunol 1:95–104PubMedPubMedCentralGoogle Scholar
  115. 115.
    Martin P, Leibovich SJ (2005) Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 15:599–607PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    Andersen MH, Schrama D, Thor Straten P et al (2006) Cytotoxic T cells. J Invest Dermatol 126:32–41PubMedCrossRefPubMedCentralGoogle Scholar
  118. 118.
    Portnoy JM, Van Osdol T, Williams PB (2004) Evidence-based strategies for treatment of allergic rhinitis. Curr Allergy Asthma Rep 4:439–446PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Meltzer EO (2017) Sublingual immunotherapy: a guide for primary care. J Fam Pract 66:S58–S58PubMedPubMedCentralGoogle Scholar
  120. 120.
    Reyes-Díaz A, González-Córdova AF, Hernández-Mendoza A et al (2017) Immunomodulation by hydrolysates and peptides derived from milk proteins. Int J Dairy Technol. Scholar
  121. 121.
    Tsuruki T, Kishi K, Takahashi M et al (2003) Soymetide, an immunostimulating peptide derived from soybean β-conglycinin, is an fMLP agonist. FEBS Lett 540:206–210PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Jaziri Mh, Migliore-Samour D, Casabianca-Pignède M-R et al (1992) Specific binding sites on human phagocytic blood cells for Gly-Leu-Phe and Val-Glu-Pro-Ile-Pro-Tyr, immunostimulating peptides from human milk proteins. Biochim Biophys Acta 1160:251–261CrossRefGoogle Scholar
  123. 123.
    Takahashi M, Moriguchi S, Ikeno M et al (1996) Studies on the ileum-contracting mechanisms and identification as a complement C3a receptor agonist of oryzatensin, a bioactive peptide derived from rice albumin. Peptides 17:5–12PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Cicero AFG, Fogacci F, Colletti A (2017) Potential role of bioactive peptides in prevention and treatment of chronic diseases: a narrative review. Br J Pharmacol 174:1378–1394PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Chalamaiah M, Yu W, Wu J (2018) Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: a review. Food Chem 245:205–222PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Subhan F, Kang HY, Lim Y et al (2017) Fish scale collagen peptides protect against CoCl2/TNF-α-induced cytotoxicity and inflammation via inhibition of ROS, MAPK, and NF-κB pathways in HaCaT cells. Oxid Med Cell Longev. Scholar
  127. 127.
    Elango R, Laviano A (2017) Protein and amino acids: key players in modulating health and disease. Curr Opin Clin Nutr Metab Care 20:69–70PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Li G-H, Le G-W, Shi Y-H et al (2004) Angiotensin I–converting enzyme inhibitory peptides derived from food proteins and their physiological and pharmacological effects. Nutr Res 24:469–486CrossRefGoogle Scholar
  129. 129.
    Natesh R, Schwager SLU, Sturrock ED et al (2003) Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 421:551–554PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Wu J, Aluko RE, Nakai S (2006) Structural requirements of angiotensin I-converting enzyme inhibitory peptides: quantitative structure−activity relationship study of di- and tripeptides. J Agric Food Chem 54:732–738PubMedCrossRefPubMedCentralGoogle Scholar
  131. 131.
    de Oliveira-Sales EB, Nishi EE, Boim MA et al (2010) Upregulation of AT1R and iNOS in the rostral ventrolateral medulla (RVLM) is essential for the sympathetic hyperactivity and hypertension in the 2K-1C wistar rat model. Am J Hypertens 23:708–715PubMedCrossRefGoogle Scholar
  132. 132.
    Chatterjee S, Khunti K, Davies MJ (2017) Type 2 diabetes. Lancet 389:2239–2251PubMedCrossRefGoogle Scholar
  133. 133.
    Eisenbarth GS (2007) Update in type 1 diabetes. J Clin Endocrinol Metab 92:2403–2407PubMedCrossRefGoogle Scholar
  134. 134.
    IDF (2015) IDF diabetes atlas. IDF, BrusselsGoogle Scholar
  135. 135.
    Thomas MC, Paldánius PM, Ayyagari R et al (2016) Systematic literature review of DPP-4 inhibitors in patients with type 2 diabetes mellitus and renal impairment. Diabetes Ther 7:439–454PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Mahmood N (2016) A review of α-amylase inhibitors on weight loss and glycemic control in pathological state such as obesity and diabetes. Comp Clin Pathol 25:1253–1264CrossRefGoogle Scholar
  137. 137.
    Zhang L, Chen Q, Li L et al (2016) Alpha-glucosidase inhibitors and hepatotoxicity in type 2 diabetes: a systematic review and meta-analysis. Sci Rep 6:32649PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Lacroix IME, Li-Chan ECY (2016) Food-derived dipeptidyl-peptidase IV inhibitors as a potential approach for glycemic regulation – current knowledge and future research considerations. Trends Food Sci Technol 54:1–16CrossRefGoogle Scholar
  139. 139.
    Stoimenis D, Karagiannis T, Katsoula A et al (2017) Once-weekly dipeptidyl peptidase-4 inhibitors for type 2 diabetes: a systematic review and meta-analysis. Expert Opin Pharmacother 18:843–851PubMedCrossRefGoogle Scholar
  140. 140.
    Lovshin JA (2017) Glucagon-like peptide-1 receptor agonists: a class update for treating type 2 diabetes. Can J Diabetes 41:524–535PubMedCrossRefGoogle Scholar
  141. 141.
    Gourgari E, Aroda VR, Wilhelm EE et al (2017) A comprehensive review of the FDA-approved labels of diabetes drugs: indications, safety, and emerging cardiovascular safety data. J Diabetes Complications 31:1719–1727PubMedCrossRefGoogle Scholar
  142. 142.
    Nishi T, Hara H, Tomita F (2003) Soybean β-conglycinin peptone suppresses food intake and gastric emptying by increasing plasma cholecystokinin levels in rats. J Nutr 133:352–357PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Sharara AI, Bouras EP, Misukonis MA et al (1993) Evidence for indirect dietary regulation of cholecystokinin release in rats. Am J Physiol Gastrointest Liver Physiol 265:G107–G112CrossRefGoogle Scholar
  144. 144.
    Cudennec B, Ravallec-Plé R, Courois E et al (2008) Peptides from fish and crustacean by-products hydrolysates stimulate cholecystokinin release in STC-1 cells. Food Chem 111:970–975CrossRefGoogle Scholar
  145. 145.
    Cudennec B, Fouchereau-Peron M, Ferry F et al (2012) In vitro and in vivo evidence for a satiating effect of fish protein hydrolysate obtained from blue whiting (Micromesistius poutassou) muscle. J Funct Foods 4:271–277CrossRefGoogle Scholar
  146. 146.
    Greco E, Winquist A, Lee T et al (2017) The role of source of protein in regulation of food intake, satiety, body weight and body composition. J Nutr Health Food Eng 6:00223Google Scholar
  147. 147.
    Madani Z, Sener A, Malaisse WJ et al (2015) Sardine protein diet increases plasma glucagon-like peptide-1 levels and prevents tissue oxidative stress in rats fed a high-fructose diet. Mol Med Rep 12:7017–7026PubMedPubMedCentralGoogle Scholar
  148. 148.
    Umezawa H, Aoyagi T, Ogawa K et al (1984) Diprotins A and B, inhibitors of dipeptidyl aminopeptidase IV, produced by bacteria. J Antibiot 37:422–425PubMedCrossRefPubMedCentralGoogle Scholar
  149. 149.
    Chinembiri T, du Plessis L, Gerber M et al (2014) Review of natural compounds for potential skin cancer treatment. Molecules 19:11679PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Creagh EM (2014) Caspase crosstalk: integration of apoptotic and innate immune signalling pathways. Trends Immunol 35:631–640PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Roomi MW, Shanker N, Niedzwiecki A et al (2015) Induction of apoptosis in the human prostate cancer cell line DU-145 by a novel micronutrient formulation. Open J Apoptosis 4:11CrossRefGoogle Scholar
  152. 152.
    Ding G-F, Huang F-F, Yang Z-S et al (2011) Anticancer activity of an oligopeptide isolated from hydrolysates of Sepia ink. Chin J Nat Med 9:151–155Google Scholar
  153. 153.
    Alemán A, Pérez-Santín E, Bordenave-Juchereau S et al (2011) Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Res Int 44:1044–1051CrossRefGoogle Scholar
  154. 154.
    Harnedy PA, Fitzgerald RJ (2013) Bioactive proteins and peptides from macroalgae, fish, shellfish and marine processing waste. In: Kim S-K (ed) Marine proteins and peptides. Wiley, Chichester, pp 5–39CrossRefGoogle Scholar
  155. 155.
    Minekus M, Alminger M, Alvito P et al (2014) A standardised static in vitro digestion method suitable for food – an international consensus. Food Funct 5:1113–1124PubMedCrossRefGoogle Scholar
  156. 156.
    Liu Y, Pischetsrieder M (2017) Identification and relative quantification of bioactive peptides sequentially released during simulated gastrointestinal digestion of commercial kefir. J Agric Food Chem 65:1865–1873PubMedCrossRefGoogle Scholar
  157. 157.
    Vilcacundo R, Martínez-Villaluenga C, Hernández-Ledesma B (2017) Release of dipeptidyl peptidase IV, α-amylase and α-glucosidase inhibitory peptides from quinoa (Chenopodium quinoa Willd.) during in vitro simulated gastrointestinal digestion. J Funct Foods 35:531–539CrossRefGoogle Scholar
  158. 158.
    Phongthai S, D’Amico S, Schoenlechner R et al (2018) Fractionation and antioxidant properties of rice bran protein hydrolysates stimulated by in vitro gastrointestinal digestion. Food Chem 240:156–164PubMedCrossRefGoogle Scholar
  159. 159.
    Nieva-Echevarria B, Jacobsen C, García Moreno PJ et al (2016) Evaluation of the antioxidant activity in food model system of fish peptides released during simulated gastrointestinal digestion. Paper presented at the 14th Euro Fed Lipid Congress, Ghent, 18–21 Sept 2016Google Scholar
  160. 160.
    Sanchón J, Fernández-Tomé S, Miralles B et al (2018) Protein degradation and peptide release from milk proteins in human jejunum. Comparison with in vitro gastrointestinal simulation. Food Chem 239:486–494PubMedCrossRefGoogle Scholar
  161. 161.
    Toopcham T, Mes JJ, Wichers HJ et al (2017) Bioavailability of angiotensin I-converting enzyme (ACE) inhibitory peptides derived from Virgibacillus halodenitrificans SK1-3-7 proteinases hydrolyzed tilapia muscle proteins. Food Chem 220:190–197PubMedCrossRefGoogle Scholar
  162. 162.
    Grimble GK, Keohane PP, Higgins BE et al (1986) Effect of peptide chain length on amino acid and nitrogen absorption from two lactalbumin hydrolysates in the normal human jejunum. Clin Sci 71:65–69PubMedCrossRefGoogle Scholar
  163. 163.
    Keohane PP, Grimble GK, Brown B et al (1985) Influence of protein composition and hydrolysis method on intestinal absorption of protein in man. Gut 26:907–913PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Hou H, Fan Y, Wang S et al (2016) Immunomodulatory activity of Alaska pollock hydrolysates obtained by glutamic acid biosensor – artificial neural network and the identification of its active central fragment. J Funct Foods 24:37–47CrossRefGoogle Scholar
  165. 165.
    FitzGerald RJ, Meisel H (2000) Milk protein-derived peptide inhibitors of angiotensin-I-converting enzyme. Br J Nutr 84:33–37CrossRefGoogle Scholar
  166. 166.
    Ramezanzade L, Hosseini SF, Nikkhah M (2017) Biopolymer-coated nanoliposomes as carriers of rainbow trout skin-derived antioxidant peptides. Food Chem 234:220–229PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Aurélien V. Le Gouic
    • 1
  • Pádraigín A. Harnedy
    • 1
  • Richard J. FitzGerald
    • 1
    Email author
  1. 1.Department of Biological SciencesUniversity of LimerickLimerickIreland

Personalised recommendations