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Structure–function relationship of fermented skate skin gelatin-derived bioactive peptides: a peptidomics approach

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Abstract

In this study, we investigated the multi-functionality of bioactive peptides derived from fermented skate (Raja kenojei) skin gelatin hydrolysates. The extracted gelatin was hydrolyzed using a combination of food grade subtilisin and actinidin. The hydrolysates were then fractionated via ultrafiltration, and the fractions with the highest dipeptidyl peptidase-IV (DPP-IV) inhibitory, angiotensin-converting enzyme (ACE) inhibitory, and antibacterial proprieties were further purified via ion exchange, solid phase extraction, and reverse phase high performance liquid chromatography. Analysis of the obtained extract revealed a direct relationship between hydrolysis time, degree of hydrolysis, and biological activities. The peptides GRPGNRGE (P1) and AKDYEVDAT (P2), with a molecular weight of 841.42 and 1010.46 Da, respectively, were identified through tandem mass spectrometry. P1 had a lower ACE and DPP-IV inhibitory activity, with a half maximal inhibitory concentration [IC50] of 0.74 and 0.69 mg.mL−1, respectively, than P2 (0.52 and 0.58 mg.mL−1, respectively). Antibacterial analysis showed similar results, with a minimum inhibitory concentration of 0.52 and 0.46 mg.mL−1 against Staphylococcus aureus (highest activity) and 1.75 and 1.44 mg.mL−1 against Klebsiella pneumonia (lowest activity) for P1 and P2, respectively. Overall, this study revealed two fish gelatin-derived multifunctional peptides, exhibiting ACE inhibitory, DPP-IV inhibitory, and antibacterial activities, as natural nutraceuticals.

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References

  • Adler-Nissen J. Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. Journal of Agricultural and Food Chemistry. 27(6): 1256-1262 (1979)

    Article  CAS  Google Scholar 

  • Aissaoui N, Chobert J-M., Haertlé T, Marzouki MN, & Abidi F. Purification and biochemical characterization of a neutral serine protease from Trichoderma harzianum. Use in antibacterial peptide production from a fish by-product hydrolysate. Applied Biochemistry and Biotechnology. 182: 831-845 (2017)

    Article  CAS  Google Scholar 

  • Asoodeh A, Yazdi MM, & Chamani J. Purification and characterisation of angiotensin I converting enzyme inhibitory peptides from lysozyme hydrolysates. Food Chemistry. 131(1): 291-295 (2012)

    Article  CAS  Google Scholar 

  • Byun H-G., & Kim S-K. Purification and characterization of angiotensin I converting enzyme (ACE) inhibitory peptides from Alaska pollack (Theragra chalcogramma) skin. Process Biochemistry. 36(12): 1155-1162 (2001)

    Article  CAS  Google Scholar 

  • Cao S, Wang Y, Hao Y, Zhang W, & Zhou G. Antihypertensive effects in vitro and in vivo of novel angiotensin-converting enzyme inhibitory peptides from bovine bone gelatin hydrolysate.Journal of Agricultural and Food Chemistry. 68 : 759-768 (2019)

    Article  Google Scholar 

  • Cho S-H, Jahncke ML, Chin K-B, & Eun J-B. The effect of processing conditions on the properties of gelatin from skate (Raja kenojei) skins. Food Hydrocolloids. 20: 810–816 (2006)

    Article  CAS  Google Scholar 

  • Drucker DJ. Enhancing the action of incretin hormones: a new whey forward? Endocrinology. 147: 3171–3172 (2006)

    Article  CAS  Google Scholar 

  • Floris R, Recio I, Berkhout B, & Visser S. Antibacterial and antiviral effects of milk proteins and derivatives thereof. Current Pharmaceutical Design. 9(16): 1257-1275 (2003)

    Article  CAS  Google Scholar 

  • Gómez-Guillén M, Giménez B, López-Caballero MA, & Montero M. Functional and bioactive properties of collagen and gelatin from alternative sources: A review. Food Hydrocolloids. 25(8): 1813-1827 (2011)

    Article  Google Scholar 

  • Jang A, & Lee M. Purification and identification of angiotensin converting enzyme inhibitory peptides from beef hydrolysates. Meat Science. 69:653-661 (2005).

    Article  CAS  Google Scholar 

  • Jin R, Teng X, Shang J, Wang D, & Liu N. Identification of novel DPP–IV inhibitory peptides from Atlantic salmon (Salmo salar) skin. Food Research International. 133: 109161 (2020)

    Article  CAS  Google Scholar 

  • Lacroix IM, & Li-Chan EC. Evaluation of the potential of dietary proteins as precursors of dipeptidyl peptidase (DPP)-IV inhibitors by an in silico approach. Journal of Functional Foods. 4: 403-422 (2012)

    Article  CAS  Google Scholar 

  • Lacroix IM, & Li-Cha EC. Inhibition of dipeptidyl peptidase (DPP)-IV and α-glucosidase activities by pepsin-treated whey proteins. Journal of Agricultural and Food Chemistry. 61: 7500-7506 (2013)

    Article  CAS  Google Scholar 

  • Liu Z, Dong S, Xu J, Zeng M, Song H, & Zhao Y. Production of cysteine-rich antimicrobial peptide by digestion of oyster (Crassostrea gigas) with alcalase and bromelin Food Control. 19: 231-235 (2008)

    Article  Google Scholar 

  • Mirzapour-Kouhdasht A, Moosavi-Nasab M, Kim Y-M, & Eun J-B. Antioxidant mechanism, antibacterial activity, and functional characterization of peptide fractions obtained from barred mackerel gelatin with a focus on application in carbonated beverages. Food Chemistry. 128339 (2021)

    Article  CAS  Google Scholar 

  • Mirzapour-Kouhdasht A, Moosavi-Nasab M, Krishnaswamy K, & Khalesi M. Optimization of gelatin production from Barred mackerel by-products: Characterization and hydrolysis using native and commercial proteases. Food Hydrocolloids. 108: 105970 (2020)

    Article  CAS  Google Scholar 

  • Mirzapour-Kouhdasht A, Moosavi-Nasab M, Lee CW, Yun H, & Eun J-B. Structure–function engineering of novel fish gelatin-derived multifunctional peptides using high-resolution peptidomics and bioinformatics. Scientific Reports. 11(1), 1-15 (2021)

    Article  Google Scholar 

  • Nauck M, & El-Ouaghlidi A. The therapeutic actions of DPP-IV inhibition are not mediated by glucagon-like peptide-1. Diabetologia. 48: 608-611 (2005)

    Article  CAS  Google Scholar 

  • Ngo D-H, Vo T-S, Ryu B, & Kim S-K. Angiotensin-I-converting enzyme (ACE) inhibitory peptides from Pacific cod skin gelatin using ultrafiltration membranes. Process Biochemistry. 51(10): 1622-1628 (2016)

    Article  CAS  Google Scholar 

  • NM S, NK H, & WAN WA. Angiotensin-I converting enzyme (ACE) inhibitory peptides from chicken skin gelatin hydrolysate and its antihypertensive effect in spontaneously hypertensive rats.International Food Research Journal. 26 (3): 903-911 (2019)

  • Nongonierma AB, Mooney C, Shields DC, & FitzGerald RJ. Inhibition of dipeptidyl peptidase IV and xanthine oxidase by amino acids and dipeptides. Food Chemistry. 141 : 644-653 (2013)

    Article  CAS  Google Scholar 

  • Pan D, Cao J, Guo H, & Zhao B. Studies on purification and the molecular mechanism of a novel ACE inhibitory peptide from whey protein hydrolysate. Food Chemistry. 130(1): 121-126 (2012)

    Article  CAS  Google Scholar 

  • Patrzykat A, & Douglas SE. Antimicrobial peptides: cooperative approaches to protection. Protein and Peptide Letters. 12(1): 19-25 (2005)

    Article  CAS  Google Scholar 

  • Sha X-M, Tu Z-C, Liu W, Wang H, Shi Y, Huang T, & Man Z-Z. Effect of ammonium sulfate fractional precipitation on gel strength and characteristics of gelatin from bighead carp (Hypophthalmichthys nobilis) scale. Food Hydrocolloids. 36: 173-180 (2014)

    Article  CAS  Google Scholar 

  • Singh A-K., Jatwa R, Purohit A, & Ram H. Synthetic and phytocompounds based dipeptidyl peptidase-IV (DPP-IV) inhibitors for therapeutics of diabetes. Journal of Asian Natural Products Research. 19(10): 1036-1045 (2017)

    Article  CAS  Google Scholar 

  • Zhang Y, Chen R, Ma H, & Chen S. Isolation and identification of dipeptidyl peptidase IV-inhibitory peptides from trypsin/chymotrypsin-treated goat milk casein hydrolysates by 2D-TLC and LC–MS/MS. Journal of Agricultural and Food Chemistry. 63:8819-8828 (2015)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by Shiraz University, Iran [grant no.: GR-AGR-56], the Heilongjiang Provincial Natural Science Foundation of China [grant no. ZD2019C002], and the National Key Research and Development Program of China [grant no. 2018YFD0401101].

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Authors and Affiliations

  1. Department of Food Science and Biotechnology, Graduate School of Chonnam National University, 77 Yongbong-ro Buk-gu, Gwangju, 61186, South Korea

    Armin Mirzapour-Kouhdasht & Jong-Bang Eun

  2. Department of Chemistry, Chonnam National University, Gwangju, 61186, South Korea

    Chul Won Lee & Hyosuk Yun

  3. School of Agriculture and Food Science, University College Dublin, Belfield, 4 Dublin, Ireland

    Armin Mirzapour-Kouhdasht

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  1. Armin Mirzapour-Kouhdasht
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  2. Chul Won Lee
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  3. Hyosuk Yun
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  4. Jong-Bang Eun
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Contributions

Armin Mirzapour-Kouhdasht Conceptualization, Methodology, Software, Data curation, Writing–original draft, Visualization, Investigation, and Validation. Marzieh Moosavi-Nasab Conceptualization, Methodology, Visualization, Investigation, Software, Funding acquisition, and Supervision. Chul Won Lee Visualization, Investigation, Validation, Funding acquisition, and Supervision. Hyosuk Yun Investigation, Methodology, and Validation. Jong Bang Eun Visualization, Investigation, Methodology, Validation, Writing–review & editing, Funding acquisition, and Supervision.

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Correspondence to Jong-Bang Eun.

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Mirzapour-Kouhdasht, A., Lee, C.W., Yun, H. et al. Structure–function relationship of fermented skate skin gelatin-derived bioactive peptides: a peptidomics approach. Food Sci Biotechnol 30, 1685–1693 (2021). https://doi.org/10.1007/s10068-021-00998-6

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  • DOI: https://doi.org/10.1007/s10068-021-00998-6

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