Skip to main content
SpringerLink
Log in

Effects of heat and pH treatments and in vitro digestion on the biological activity of protein hydrolysates of Amaranthus hypochondriacus L. grain

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

The aim of this work was to assess the effects of temperature (T), time (t) and pH treatments and an in vitro digestion on the stability of the angiotensin I-converting-enzyme-inhibitory activity (ACEIA) and antithrombotic activity (ATA; assessed as inhibition of platelet aggregation) of selected protein hydrolysates of amaranth named Alb1H103 and GloH88 and GluH24 with dipeptidyl peptidase IV inhibitory activity (DPPIVIA). Heat treatment (40–100 °C) for 1 h showed no significant differences among ACEIA, DPPIVIA and ATA of the heated hydrolysates at pH 4 and 7. There was no statistically significant loss of any bioactivity under heat treatment for 3 h at pH 4.0. Alb1H103 and GluH24 maintained the inhibitory activity of ACE and ATA at pH 7.0 for 3 h, whereas GloH88 maintained ACEIA and ATA for 2.0 h at pH 7.0. The pH effect on hydrolysates bioactivity was assessed in the range of 2.0–12.0. This was negligible on ACEIA, ATA and DPPIVIA. The in vitro digestion was performed using pepsin, trypsin (T) and α-chymotrypsin (C). A previous treatment of hydrolysates with pepsin improved the proteolytic activities of T and C. The hydrolysates kept at 100 °C for 1 h at pH 4.0, showed a significant increase in bioactivity. Conversely, a treatment at pH 7.0 showed no significant difference (p < 0.05) in the hydrolysates bioactivities after their digestion. Thus, biological activity of hydrolysates may be preserved or enhanced, depending on their processing conditions.

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
Fig. 4

Similar content being viewed by others

References

  • Akilliioglu H, Karakaya S (2009) Effects of treatment and in vitro digestion on the angiotensin converting enzyme inhibitory activity of some legume species. Eur Food Res Technol 229:915–921

    Article  Google Scholar 

  • AOAC (2010) Official methods of analysis. Association of Official Analytical Chemist, Rockville

    Google Scholar 

  • Barba de la Rosa AP, Barba Montoya A, Martínez-Cuevas P. Hernández-Ledesma B, León-Galván MF, De León-Rodríguez A, González C (2010) Tryptic amaranth glutelin digest induce endothelial nitric oxide production through inhibition of ACE: antihypertensive role of amarant peptides. Nitric Oxide 23:106–111

  • Bloom KA, Huang FR, Bencharitiwong R, Bardina L, Ross A, Sampson HA, Nowak-Wegrzyn A (2015) Effect of heat treatment on milk and egg proteins allergenicity. Pediatr Allergy Immunol 25:740–746

    Article  Google Scholar 

  • Chen J, Wanga Y, Zhong Q, Wua Y, Xiaa W (2012) Purification and characterization of a novel angiotensin-I converting enzyme (ACE) inhibitory peptide derived from enzymatic hydrolysate of grass carp Protein. Peptides 33:52–58

    Article  Google Scholar 

  • Condés MC, Scilingo AA, Añón MC (2009) Characterization of amaranth proteins modified by tripsin proteolysis: structural and functional changes. Food Sci Technol 42:963–970

    Google Scholar 

  • De la Peña A, Baños G, Izaguirre R, Mandoki JJ, Fernández-G JM (1993) Comparative effect of synthetic amino-estrogens with estradiol on platelet aggregation. Steroids 58:407–409

    Article  Google Scholar 

  • Dexter AF, Middelberg PJ (2008) Peptides as functional surfactants. Ind Eng Chem Res 47:6391–6398

    Article  CAS  Google Scholar 

  • Domínguez-González K, Cruz-Guerrero A, González-Márquez H, Gómez-Ruiz L, García-Garibay M, Jiménez-Guzmán J, Rodríguez-Serrano G (2014) Antihypertensive and antithrombotic activities of a commercial fermented milk product made with Lactobacillus casei Shirota and Streptococcus thermophillus. Int J Dairy Technol 67:358–362

    Article  Google Scholar 

  • Flores-Garcia M, Fernández-G JM, León-Martínez M, Hernández-Ortega S (2012) The structures and inhibitory effects of Buame [N-(3-hydroxy-1,3,5(10)-estratrien-17β-yl)-butylamine] and Diebud [N,N 0-bis-(3-hydroxy-1,3,5(10)-estratrien-17β-yl)-1,4-butanediamine] on platelet aggregation. Steroids 77:512–520

    Article  CAS  Google Scholar 

  • Fritz M, Vecchi B, Rinaldi G, Añón MC (2011) Amaranth seed protein hydrolysates have in vivo and in vitro antihypertensive activity. Food Chem 126:878–884

    Article  CAS  Google Scholar 

  • Fu Y, Young JF, Dalsgaard TK, Therkildsen M (2015) Separation of angiotensin I-converting enzyme inhibitory peptides from bovine connective tissue and their stability towards temperature, pH and digestive enzymes. Int J Food Sci Technol 50:1234–1243

    Article  CAS  Google Scholar 

  • González G, Alvarado-Vasquez N, Fernández-G JM, Cruz-Robles D, del Valle L, Pinzón E, Torres I, Rodríguez E, Zapata E, Gómez-Vidales V, Montaño LF, de la Peña A (2010) The antithrombotic effect of the aminoestrogen prolame (N-(3-hydroxy-1,3,5(10)-estratrien-17B-YL)-3-hydroxypropylamine) is linked to an increase in nitric oxide production by platelets and endothelial cells. Atherosclerosis 208:62–68

    Article  Google Scholar 

  • Hayakari M, Kondo Y, Izumi H (1978) A rapid and simple spectrophotometric assay of angiotensin-converting enzyme. Anal Biochem 84:361–369

    Article  CAS  Google Scholar 

  • Hejgaard J, Dam J, Petersen LC, Bjorn SE (1994) Primary structure and specificity of the major serine proteinase inhibitor of amaranth (Amaranthus caudatus L.) seeds. Biochim Biophys Acta 1204:68–74

    Article  CAS  Google Scholar 

  • Huang SL, Jao CL, Ho KP, Hsu KC (2012) Dipetidyl-peptidase IV activity of peptides derived from tuna cooking juice hydrolysates. Peptides 35:114–121

    Article  CAS  Google Scholar 

  • Hwang JS (2010) Impact of processing on stability of angiotensin I-converting enzyme (ACE) inhibitory peptides obtained from tuna cooking juice. Food Res Int 43:902–906

    Article  CAS  Google Scholar 

  • Kojima K, Ham T, Kato T (1980) Rapid chromatographic purification of dipeptidyl peptidase IV in human submaxillary gland. J Chromatogr A 189:233–240

    Article  CAS  Google Scholar 

  • Kristinsson HG, Hultin HO (2003) Effect of low and high pH treatment on the functional properties of cod muscle proteins. J Agric Food Chem 51:5103–5110

    Article  CAS  Google Scholar 

  • Li GH, Le GW, Shi YH, Sherstha S (2004) Angiotensin I-converting enzyme inhibitory peptides derived from food proteins and their physiological and pharmacological effects. Nutr Res 24:469–486

    Article  CAS  Google Scholar 

  • Madureira AR, Tavares T, Gomes AMP, Pintado ME, Malcata FX (2010) Physiological properties of bioactive peptides obtained from whey proteins. J Dairy Sci 93:437–455

    Article  CAS  Google Scholar 

  • Montoya-Rodriguez A, Gómez-Favela MA, Reyes-Moreno C, Milán-Carrillo J, González de Mejía E (2015) Identification of bioactive peptide sequences from amaranth (Amaranthus hypochondriacus) seed proteins and their potential role in the prevention of chronic diseases. Compr Rev Food Sci Saf 14:139–156

    Article  CAS  Google Scholar 

  • Orsini DMC, Tironi VA, Añón MC (2011) Antioxidant activity of amaranth protein or their hydrolysates under simulated gastrointestinal digestion. Food Sci Technol 44(1752):1760

    Google Scholar 

  • Rao S, Sun J, Liu Y, Zeng H, Su Y, Yan Y (2012) ACE inhibitory peptides and antioxidant peptides derived from in vitro digestion hydrolysate of hen egg white lysozyme. Food Chem 135:1245–1252

    Article  CAS  Google Scholar 

  • Rui X (2012) Angiotensin I-converting enzyme inhibitory properties of Phaseolus vulgaris bean hydrolysates: Effects of different thermal and enzymatic digestion treatments. Food Res Int 49:739–746

    Article  CAS  Google Scholar 

  • Sabione AC, Scilingo A, Añon MC (2015) Potential antithrombotic in amaranth proteins and its hydrolysates. Food Sci Technol 60:171–177

    Google Scholar 

  • Sheih IC, Fang TJ, Wub TK (2009) Isolation and characterization of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chem 115:279–284

    Article  CAS  Google Scholar 

  • Shevkani K, Singh N (2015) Relationship between protein characteristics and film-forming properties of kidney bean, field pea and amaranth protein isolates. Intl J Food Sci Technol 50:1033–1043

    Article  CAS  Google Scholar 

  • Shevkani K, Singh N, Kaur A, Rana JC (2014a) Physicochemical, pasting, and functional properties of amaranth seed flours: effects of lipid removal. J Food Sci 79:C1271–C1277

    Article  CAS  Google Scholar 

  • Shevkani K, Singh N, Rana JC, Kaur A (2014b) Relationship between physicochemical and functional properties of amaranth (Amaranthus hypochondriacus) protein isolates. Food Sci Technol 49:541–550

    Article  CAS  Google Scholar 

  • Soriano-Santos J, Escalona-Buendía HB (2015) Angiotensin I-converting enzyme inhibitory and antioxidant activities and surfactant properties of protein hydrolysates as obtained of Amaranthus hypochondriacus L. grain. J Food Sci Technol 52:2073–2082

    Article  CAS  Google Scholar 

  • Soriano-Santos J, Reyes-Bautista R, Guerrero-Legarreta I, Ponce-Alquicira E, Escalona-Buendía HB, Almanza-Pérez JC, Díaz-Godínez G, Román-Ramos R (2015) Dipeptidyl peptidase IV inhibitory activity of protein hydrolyzates from Amaranthus hypochondriacus L. grain and their influence on postprandial glycemia in streptozotocin-induced diabetic mice. Afr J Tradit Complement Altern Med 12:90–98

    Google Scholar 

  • Tavares T, Contreras M, Amorim M, Pintado M (2011) Novel whey-derived peptides with inhibitory effect against angiotensin-converting enzyme: In vitro effect and stability to gastrointestinal enzymes. Peptides 32:1013–1019

    Article  CAS  Google Scholar 

  • Tovar-Pérez EG, Guerrero-Legarreta I, Farrés-González AN, Soriano-Santos J (2009) Angiotensin I-converting enzyme-inhibitory peptide fractions from albumin 1 and globulin as obtained of amaranth grain. Food Chem 116:437–444

    Article  Google Scholar 

  • Valdes-Rodriguez S, Segura Nieto M, Chagolla-Lopez A, Verver-y Vargas-Cortina A, Martinez-Gallardo N, Blanco-Labra A (1993) Purification, characterization, and complete amino acid sequence of a trypsin inhibitor from Amaranth (Amaranthus hypochondriacus) seeds. Plant Physiol 103:1407–1412

    Article  CAS  Google Scholar 

  • Velarde-Salcedo AJ, Barrera-Pacheco A, Lara-González S, Montero-Morín G, Díaz-Gois González, de Mejía E, Barba de la Rosa AP (2013) In vitro inhibition of dipeptidyl peptidase IV by peptides derived from the hydrolysis of amaranth (Amaranthus hypochondriacus L.) proteins. Food Chem 136:758–764

    Article  CAS  Google Scholar 

  • Wu J, Ding X (2002) Characterization of inhibition and stability of soy protein derived angiotensin I-converting enzyme inhibitory peptides. Food Res Int 35:367–375

    Article  CAS  Google Scholar 

  • Wu W, Feng-yang Z, Hong-xia CH, Zhan-mei J (2014) Stability and cytotoxicity of angiotensin-I-converting enzyme inhibitory peptides derived from bovine casein. J Zhejiang Univ-Sci B 2:143–152

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. Abraham Avendaño-Martínez for proofreading and translating the manuscript.

Author information

Authors and Affiliations

  1. Departamento de Biotecnología, Universidad Autónoma Metropolitana, Campus Iztapalapa, Av. San Rafael Atlixco No. 186, Col. Vicentina, Ap. P. 55-535, Deleg. Iztapalapa, 09340, Mexico City, Mexico

    J. López-Sánchez, E. Ponce-Alquicira & J. Soriano-Santos

  2. Departamento de Ingeniería y Ciencias Químicas, Universidad Iberoamericana, Prolongación Paseo de la Reforma 880, Lomas de Santa Fe, 01219, Mexico City, Mexico

    R. Pedroza-Islas

  3. Departamento de Farmacología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Escolar, Ciudad Universitaria, Coyoacán, 04510, Mexico City, Mexico

    A. de la Peña-Díaz

Authors
  1. J. López-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Ponce-Alquicira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Pedroza-Islas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. de la Peña-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Soriano-Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Soriano-Santos.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López-Sánchez, J., Ponce-Alquicira, E., Pedroza-Islas, R. et al. Effects of heat and pH treatments and in vitro digestion on the biological activity of protein hydrolysates of Amaranthus hypochondriacus L. grain. J Food Sci Technol 53, 4298–4307 (2016). https://doi.org/10.1007/s13197-016-2428-0

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-016-2428-0

Keywords

Search

Navigation