Skip to main content
SpringerLink
Log in

Production of Dual Inhibitory Hydrolysate by Enzymatic Hydrolysis of Squid Processing By-product

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Squid processing by-product contains unutilized abundant proteins. In this study, 6 proteases (pepsin, protamex, trypsin, neutral protease, alkaline protease, and papain) were firstly employed to hydrolyze the squid processing by-product protein. The neutral protease-digested hydrolysate was found to have the most promising ACE (angiotensin-converting enzyme) inhibitory activity. Based on Box-Behnken design, the optimal hydrolysis process was determined to be: 52.4 ℃ of temperature, 5.7 h of time, pH 7.1, and 8151 U/g of enzyme. Under these conditions, the ACE inhibition rate and polypeptide content of the hydrolysate were 84.26% and 229.09 mg/g, respectively. Subsequently, ultrafiltration was performed, and the ACE and renin inhibitory activities of the filtrate (< 1 kDa) were the highest, reaching 87.48 ± 1.76% and 69.72 ± 1.16%, with IC50 values of 1.34 ± 0.12 mg/mL and 1.47 ± 0.06 mg/mL, respectively. However, these activities decreased to 35.15 ± 1.31% and 43.17% ± 1.42%, respectively, after digestion by simulated gastrointestinal juice. Nevertheless, this is the first report representing the neutral protease-digested hydrolysate of squid processing by-product as a potential source of both ACE and renin inhibitors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of Data and Material

Available as requested.

Code Availability

Not applicable.

References

  • Aleman A, Gimenez B, Perez-Santin E, Gomez-Guillen MC, Montero P (2011) Contribution of Leu and Hyp residues to antioxidant and ACE-inhibitory activities of peptide sequences isolated from squid gelatin hydrolysate. Food Chem 125:334–341

    Article  CAS  Google Scholar 

  • Aluko RE (2019) Food protein-derived renin-inhibitory peptides: in vitro and in vivo properties. J Food Biochem 43:1–12

    Article  Google Scholar 

  • Apostolidis E, Karayannakidis PD, Lee CM (2016) Recovery of bioactive peptides and omega-3 fatty acids-containing phospholipids from squid processing by-product hydrolysate. J Aquat Food Prod Technol 25:496–506

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cermeño M, Stack J, Tobin PR, O’Keeffe MB, Harnedy PA, Stengel DB, FitzGerald RJ (2019) Peptide identification from a Porphyra dioica protein hydrolysate with antioxidant, angiotensin converting enzyme and dipeptidyl peptidase IV inhibitory activities. Food Funct 10:3421–3429

    Article  PubMed  Google Scholar 

  • Coscueta ER, Brassesco ME, Pintado M (2021) Collagen-based bioactive bromelain hydrolysate from salt-cured cod skin. Applied Sciences-Basel 11(18)

  • Darewicz M, Borawska J, Vegarud GE, Minkiewicz P, Iwaniak A (2014) Angiotensin I-converting enzyme (ACE) inhibitory activity and ACE inhibitory peptides of salmon (Salmo salar) protein hydrolysates obtained by human and porcine gastrointestinal enzymes. Int J Mol Sci 15:14077–14101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Brutto OH, Mera RM, Gillman J, Castillo PR, Zambrano M, Ha JE (2016) Dietary oily fish intake and blood pressure levels: a population-based study. J Clin Hypertens 18:337–341

    Article  Google Scholar 

  • Drotningsvik A, Oterhals Å, Mjøs SA, Vikøren LA, Flesland O, Gudbrandsen OA (2021) Effects of intact and hydrolysed blue whiting proteins on blood pressure and markers of kidney function in obese Zucker fa/fa rats. Eur J Nutr 60:529–544

    Article  CAS  PubMed  Google Scholar 

  • Girgih AT, Udenigwe CC, Li H, Adebiyi AP, Aluko RE (2011) Kinetics of enzyme inhibition and antihypertensive effects of hemp seed (Cannabis sativa L.) protein hydrolysates. J Am Oil Chem Soc 88:1767–74

  • Girgih AT, Nwachukwu ID, Hasan F, Fagbemi TN, Gill T, Aluko RE (2015) Kinetics of the inhibition of renin and angiotensin I-converting enzyme by cod (Gadus morhua) protein hydrolysates and their antihypertensive efects in spontaneously hypertensive rats. Food Nutr Res 59:29788

    Article  PubMed  Google Scholar 

  • He R, Aluko RE, Ju XR (2014) Evaluating molecular mechanism of hypotensive peptides interactions with renin and angiotensin converting enzyme. PLoS One 9:e91051

  • He S, Mao X, Zhang T, Guo X, Ge Y, Ma C, Zhang X (2016) Separation and nanoencapsulation of antitumor peptides from Chinese three-striped box turtle (Cuora trifasciata). J Microencapsul 33:344–354

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim MM (2006) RAS inhibition in hypertension. J Hum Hypertens 20:101–108

    Article  CAS  PubMed  Google Scholar 

  • Je J-Y, Park P-J, Kwon YJ, Kim S-K (2004) A novel angiotensin I converting inhibitory peptide from Alaska pollack (Theraga chalcogramma) frame protein hydrolysate. J Agric Food Chem 52:7842–7845

    Article  CAS  PubMed  Google Scholar 

  • Jung WK, Mendis E, Je JY, Park PJ, Son BW, Kim HC, Choi YK, Kim SK (2006) Angiotensin I-converting enzyme inhibitory peptide from yellow-fin sole (Limanda aspera) frame protein and its antihypertensive effect on spontaneously hypertensive rats. Food Chem 94:26–32

    Article  CAS  Google Scholar 

  • Kannan A, Hettiarachchy NS, Marshall M, Raghavan S, Kristinsson H (2011) Shrimp shell peptide hydrolysates inhibit human cancer cell proliferation. J Sci Food Agric 91:1920–1924

    Article  CAS  PubMed  Google Scholar 

  • Ko S-C, Kang MC, Lee J-K et al (2011) Effect of angiotensin I-converting enzyme (ACE) inhibitory peptide purified from enzymatic hydrolysates of Styela plicata. Eur Food Res Technol 233:915–922

    Article  CAS  Google Scholar 

  • Liang PZ, Lee CM, Park E (2005) Characterization of squid-processing byproduct hydrolysate and its potential as aquaculture feed ingredient. J Agric Food Chem 53:5587–5592

    Article  Google Scholar 

  • Lin L, Lv S, Li B (2012) Angiotensin-I-converting enzyme (ACE)-inhibitory and antihypertensive properties of squid skin gelatin hydrolysates. Food Chem 131:225–230

    Article  CAS  Google Scholar 

  • Lin HC, Alashi AM, Aluko RE, Sun Pan B, Chang YW (2017) Antihypertensive properties of tilapia (Oreochromis spp.) frame and skin enzymatic protein hydrolysates. Food Nutr Res 61(1):1391666

  • Malomo SA, Onuh JO, Girgih AT, Aluko RE (2015) Structural and antihypertensive properties of enzymatic hemp seed protein hydrolysates. Nutrients 7:7616–7632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan S, Wang S, Jing L, Yao D (2016) Purification and characterisation of a novel angiotensin-I converting enzyme (ACE)-inhibitory peptide derived from the enzymatic hydrolysate of Enteromorpha clathrata protein. Food Chem 211:423–430

    Article  CAS  PubMed  Google Scholar 

  • Park SY, Je J-Y, Ahn C-B (2016) Protein hydrolysates and ultrafiltration fractions obtained from Krill (Euphausia superba): nutritional, functional, antioxidant, and ACEInhibitory characterization. J Aquat Food Prod Technol 25:1266–1277

    Article  CAS  Google Scholar 

  • Pinciroli M, Aphalo P, Nardo AE, Añón MC, Quiroga AV (2019) Broken rice as a potential functional ingredient with inhibitory activity of renin and angiotensin-converting enzyme (ACE). Plant Foods Hum Nutr 74:405–413

    Article  CAS  PubMed  Google Scholar 

  • Quiroga AV, Aphalo P, Nardo AE, Añón MC (2017) In vitro modulation of renin-angiotensin system enzymes by amaranth (Amaranthus hypochondriacus) protein-derived peptides: alternative mechanisms different from ACE inhibition. J Agric Food Chem 65:7415–7423

    Article  CAS  PubMed  Google Scholar 

  • Udenigwe CC, Lin YS, Hou WC, Aluko RE (2009) Kinetics of the inhibition of renin and angiotensin I-converting enzyme by flaxseed protein hydrolysate fractions. J Funct Foods 1:199–207

    Article  Google Scholar 

  • Wijesekara I, Qian ZJ, Ryu B, Ngo DH, Kim SK (2011) Purification and identification of antihypertensive peptides from seaweed pipefish (Syngnathus schlegeli) muscle protein hydrolysate. Food Res Int 44:703–707

    Article  CAS  Google Scholar 

  • Wang X, Zhang X (2013) Separation, antitumor activities, and encapsulation of polypeptide from Chlorella pyrenoidosa. Biotechnol Prog 29:681–687

    Article  PubMed  Google Scholar 

  • Yathisha UG, Bhat I, Karunasagar I, Mamatha BS (2019) Antihypertensive activity of fish protein hydrolysates and its peptides. Crit Rev Food Sci Nutr 59:2363–2374

    Article  CAS  Google Scholar 

  • Zhang B, Zhang X (2013) Separation and nanoencapsulation of antitumor polypeptide from Spirulina platensis. Biotechnol Prog 29:1230–1238

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was partly supported by The Program of The Department of Natural Resources of Guangdong Province, China (GDNRC [2021] 49).

Author information

Authors and Affiliations

  1. College of Food Science and Engineering, South China University of Technology, Guangzhou, China

    Qi Liu, Yushan Yao, Li Yang & Xuewu Zhang

  2. Guangzhou Institute of Modern Industrial Technology, Guangzhou, China

    Qi Liu, Li Yang & Xuewu Zhang

  3. Department of Chemistry, Faculty of Science, Minia University, Minya, Egypt

    Mahmoud A. A. Ibrahim

  4. Department of Pharmacognosy, Faculty of Pharmacy, Cairo University, Giza, Egypt

    Ali Mahmoud El Halawany

Authors
  1. Qi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yushan Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahmoud A. A. Ibrahim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ali Mahmoud El Halawany
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuewu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li Yang or Xuewu Zhang.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

All authors consent for publication.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Q., Yao, Y., Ibrahim, M.A.A. et al. Production of Dual Inhibitory Hydrolysate by Enzymatic Hydrolysis of Squid Processing By-product. Mar Biotechnol 24, 293–302 (2022). https://doi.org/10.1007/s10126-022-10104-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-022-10104-4

Keywords

Search

Navigation