In vitro inhibition of glucose gastro-intestinal enzymes and antioxidant activity of hydrolyzed collagen peptides from different species
Ana Lais Andrade Gaspardi
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorDaniele Cristina da Silva
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorLuis Gustavo Saboia Ponte
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorFabiana Galland
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorVera Sonia Nunes da Silva
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorFernando Moreira Simabuco
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorRosângela Maria Neves Bezerra
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorCorresponding Author
Maria Teresa Bertoldo Pacheco
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Correspondence
Maria Teresa Bertoldo Pacheco, Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), PO Box 139, 13070-178, Campinas, SP, Brazil.
Email: [email protected]
Search for more papers by this authorAna Lais Andrade Gaspardi
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorDaniele Cristina da Silva
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorLuis Gustavo Saboia Ponte
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorFabiana Galland
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorVera Sonia Nunes da Silva
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Search for more papers by this authorFernando Moreira Simabuco
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorRosângela Maria Neves Bezerra
Laboratório Multidisciplinar em Alimentos e Saúde (LABMAS), Faculdade de Ciências Aplicadas (FCA), Universidade de Campinas (UNICAMP), Limeira, Brazil
Search for more papers by this authorCorresponding Author
Maria Teresa Bertoldo Pacheco
Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil
Correspondence
Maria Teresa Bertoldo Pacheco, Centro de Ciência e Qualidade de Alimentos (CCQA), Instituto de Tecnologia de Alimentos (ITAL), PO Box 139, 13070-178, Campinas, SP, Brazil.
Email: [email protected]
Search for more papers by this authorAbstract
The growing value of industrial collagen by-products has given rise to interest in extracting them from different species of animals. Intrinsic protein structure variation of collagen sources and its hydrolysis can bring about different bioactivities. This study aimed to characterize and evaluate the differences in vitro biological potential of commercial bovine (BH), fish (FH), and porcine hydrolysates (PH) regarding their antioxidant and hypoglycemic activities. All samples showed percentages above 90% of protein content, with high levels of amino acids (glycine, proline, and hydroxyproline), responsible for the specific structure of collagen. The BH sample showed a higher degree of hydrolysis (DH) (8.7%) and a higher percentage of smaller than 2 kDa peptides (74.1%). All collagens analyzed in vitro showed inhibition of pancreatic enzymes (α-amylase and α-glucosidase), with the potential to prevent diabetes mellitus. The PH sample showed higher antioxidant activities measured by ORAC (67.08 ± 4.23 μmol Trolox Eq./g) and ABTS radical scavenging (65.69 ± 3.53 μmol Trolox Eq./g) methods. For the first time, DNA protection was analyzed to hydrolyzed collagen peptides, and the FH sample showed a protective antioxidant action to supercoiled DNA both in the presence (39.51%) and in the absence (96.36%) of AAPH (reagent 2,2′-azobis(2-amidinopropane)). The results confirmed that the source of native collagen reflects on the bioactivity of hydrolyzed collagen peptides, probably due to its amino acid composition.
Practical applications
Our data provide new application for collagen hydrolysates with hypoglycemiant and antioxidant activity. These data open discussion for future studies on the additional benefits arising from collagen peptide consumption for the prevention of aging complications or hyperglycemic conditions as observed in chronic diseases such as diabetes mellitus type II (DM 2). The confirmation of these results can open new market areas for the use of collagen with pharmacological applications or to produce new supplements. Furthermore, provides a solution for waste collagen from meat industries and adds value to the product.
CONFLICT OF INTEREST
The authors declared that they have no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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Appendix S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Abesundara, K. J., Matsui, T., & Matsumoto, K. (2004). α-Glucosidase inhibitory activity of some Sri Lanka plant extracts, one of which, Cassia auriculata, exerts a strong antihyperglycemic effect in rats comparable to the therapeutic drug acarbose. Journal of Agricultural and Food Chemistry, 52, 2541–2545. https://doi.org/10.1021/jf035330s
- Ahmed, A. S., El-Bassiony, T., Elmalt, L. M., & Ibrahim, H. R. (2015). Identification of potent antioxidant bioactive peptides from goat milk proteins. Food Research International, 74, 80–88. https://doi.org/10.1016/j.foodres.2015.04.032
- Alemán, A., Giménez, B., Montero, P., & Gómez-Guillén, M. C. (2011). Antioxidant activity of several marine skin gelatins. LWT—Food Science and Technology, 44, 407–413. https://doi.org/10.1016/j.lwt.2010.09.003
- Al-Duais, M., Müller, L., Böhm, V., & Jetschke, G. (2009). Antioxidant capacity and total phenolics of Cyphostemma digitatum before and after processing: Use of different assays. European Food Research and Technology, 228, 813–821. https://doi.org/10.1007/s00217-008-0994-8
- Ao, J., & Li, B. (2012). Amino acid composition and antioxidant activities of hydrolysates and peptide fractions from porcine collagen. Food Science and Technology International, 18, 425–434. https://doi.org/10.1177/1082013211428219
- AOAC International. (2012). Official Methods of Analysis of AOAC International. (19th ed.). https://www.techstreet.com/standards/official-methods-83 of-analysis-of-aoac-international-19th-edition-2012?product_id=1881941
- Apostolidis, E., Kwon, Y. I., Ghaedian, R., & Shetty, K. (2007). Fermentation of milk and soymilk by Lactobacillus bulgaricus and Lactobacillus acidophilus enhances functionality for potential dietary management of hyperglycemia and hypertension. Food Biotechnology, 21, 217–236. https://doi.org/10.1080/08905430701534032
- Bawn, C. S. H. (1987). Encyclopedia of polymer science and engineering. Polymer, 28, 1234. https://doi.org/10.1016/0032-3861(87)90274-6
10.1016/0032?3861(87)90274?6 Google Scholar
- Bello, A. E., & Oesser, S. (2006). Collagen hydrolysate for the treatment of osteoarthritis and other joint disorders: A review of the literature. Current Medical Research and Opinion, 22, 2221–2232. https://doi.org/10.1185/030079906X148373
- Bezerra, T. K. A., De Araujo, A. R. R., Do Nascimento, E. S., De Matos Paz, J. E., Gadelha, C. A., Gadelha, T. S., Pacheco, M. T. B., Do Egypto Queiroga, R. D. C. R., De Oliveira, M. E. G., & Madruga, M. S. (2016). Proteolysis in goat “coalho” cheese supplemented with probiotic lactic acid bacteria. Food Chemistry, 196, 359–366. https://doi.org/10.1016/j.foodchem.2015.09.066
- Bezerra, T., Estévez, M., Lacerda, J. T., Dias, M., Juliano, M., Mendes, M. A., Morgano, M., Pacheco, M. T., & Madruga, M. (2020). Chicken combs and wattles as sources of bioactive peptides: Optimization of hydrolysis, identification by LC-ESI-MS2 and bioactivity assessment. Molecules, 25, 1698. https://doi.org/10.3390/molecules25071698
- Brand-Williams, W., Cuvelier, M. E., & Berset, C. L. W. T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT—Food Science and Technology, 28, 25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
- Chakrabarti, S., Jahandideh, F., & Wu, J. (2014). Food-derived bioactive peptides on inflammation and oxidative stress. BioMed Research International, 2014, 1–11. https://doi.org/10.1155/2014/608979
- Chalamaiah, M., Hemalatha, R., & Jyothirmayi, T. (2012). Fish protein hydrolysates: Proximate composition, amino acid composition, antioxidant activities and applications: A review. Food Chemistry, 135, 3020–3038. https://doi.org/10.1016/j.foodchem.2012.06.100
- Chi, C. F., Cao, Z. H., Wang, B., Hu, F. Y., Li, Z. R., & Zhang, B. (2014). Antioxidant and functional properties of collagen hydrolysates from Spanish mackerel skin as influenced by average molecular weight. Molecules, 19, 11211–11230. https://doi.org/10.3390/molecules190811211
- Chiou, B. S., Avena-Bustillos, R. J., Shey, J., Yee, E., Bechtel, P. J., Imam, S. H., Glenn, G. M., & Orts, W. (2006). Rheological and mechanical properties of cross-linked fish gelatins. Polymer, 47, 6379–6386. https://doi.org/10.1016/j.polymer.2006.07.004
- Chisté, R. C., Mercadante, A. Z., Gomes, A., Fernandes, E., Lima, J. L. F. D. C., & Bragagnolo, N. (2011). In vitro scavenging capacity of annatto seed extracts against reactive oxygen and nitrogen species. Food Chemistry, 127, 419–426. https://doi.org/10.1016/j.foodchem.2010.12.139
- Chotphruethipong, L., Sukketsiri, W., Aluko, R. E., Sae-leaw, T., & Benjakul, S. (2021). Effect of hydrolyzed collagen from defatted Asian sea bass (Lates calcarifer) skin on fibroblast proliferation, migration and antioxidant activities. Journal of Food Science and Technology, 58, 541–551. https://doi.org/10.1007/s13197-020-04566-4
- Church, F. C., Swaisgood, H. E., Porter, D. H., & Catignani, G. L. (1983). Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in Milk and isolated Milk proteins. Journal of Dairy Science, 66, 1219–1227. https://doi.org/10.3168/jds.S0022-0302(83)81926-2
- Damodaran, S., Parkin, K. L., & Fennema, O. R. (2018). Fenema's Food Chemistry. (5th ed.). CRC Press
- de Souza, R. S. C., Tonon, R. V., Stephan, M. P., Silva, C. M., Penteado, A. L., Cabral, L. M. C., & Kurozawa, L. E. (2019). Evaluation of the antioxidant potential of whey protein concentrated by ultrafiltration and hydrolyzed by different commercial proteases. Brazilian Journal of Food Technology, 22, e2018021. https://doi.org/10.1590/1981-6723.02118
10.1590/1981?6723.02118 Google Scholar
- Feng, M., & Betti, M. (2017). Transepithelial transport efficiency of bovine collagen hydrolysates in a human Caco-2 cell line model. Food Chemistry, 224, 242–250. https://doi.org/10.1016/j.foodchem.2016.12.044
- Ferreira, A. M., Gentile, P., Chiono, V., & Ciardelli, G. (2012). Collagen for bone tissue regeneration. Acta Biomaterialia, 8, 3191–3200. https://doi.org/10.1016/j.actbio.2012.06.014
- Hagen, S. R., Frost, B., & Augustin, J. (1989). Precolumn phenylisothiocyanate derivatization and liquid chromatography of amino acids in food. Journal—Association of Official Analytical Chemists., 72, 912–916. https://doi.org/10.1093/jaoac/72.6.912
- Hansen, P. R., & Oddo, A. (2015). Fmoc solid-phase peptide synthesis. In Houen G. (eds), Methods in Molecular Biology. Humana Press. https://doi.org/10.1007/978-1-4939-2999-3_5
- Hema, G. S., Joshy, C. G., Shyni, K., Chatterjee, N. S., Ninan, G., & Suseela, M. (2017). Optimization of process parameters for the production of collagen peptides from fish skin (Epinephelus malabaricus) using response surface methodology and its characterization. Journal of Food Science Technology, 54, 488–496. https://doi.org/10.1007/s13197-017-2490-2
- Hernández-Ledesma, B., Dávalos, A., Bartolomé, B., & Amigo, L. (2005). Preparation of antioxidant enzymatic hydrolysates from α-lactalbumin and β-lactoglobulln. Identification of active peptides by HPLC-MS/MS. Journal of Agricultural and Food Chemistry, 53, 588–593. https://doi.org/10.1021/jf048626m
- Jamdar, S. N., Rajalakshmi, V., Pednekar, M. D., Juan, F., Yardi, V., & Sharma, A. (2010). Influence of degree of hydrolysis on functional properties, antioxidant activity and ACE inhibitory activity of peanut protein hydrolysate. Food Chemistry, 121, 178–184. https://doi.org/10.1016/j.foodchem.2009.12.027
- Khiari, Z., Ndagijimana, M., & Betti, M. (2014). Low molecular weight bioactive peptides derived from the enzymatic hydrolysis of collagen after isoelectric solubilization/precipitation process of Turkey by-products. Poultry Science, 93, 2347–2362. https://doi.org/10.3382/ps.2014-03953
- Kim, M. J., Lee, S. B., Lee, H. S., Lee, S. Y., Baek, J. S., Kim, D., Moon, T. W., Robyt, J. F., & Park, K. H. (1999). Comparative study of the inhibition of α-glucosidase, α-amylase, and cyclomaltodextrin glucanosyltransferase by acarbose, isoacarbose, and acarviosine-glucose. Archives of Biochemistry and Biophysics, 371, 277–283. https://doi.org/10.1006/abbi.1999.1423
- Kim, Y. M., Jeong, Y. K., Wang, M. H., Lee, W. Y., & Rhee, H. I. (2005). Inhibitory effect of pine extract on α-glucosidase activity and postprandial hyperglycemia. Nutrition, 21, 756–761. https://doi.org/10.1016/j.nut.2004.10.014
- Klüver, E. & Meyer, M.T. (2013). Preparation , processing, and rheology of thermoplastic collagen. Journal of Applied Polymer Science, 128, 4201–4211.
- Koch, E. R., & Deo, P. (2016). Nutritional supplements modulate fluorescent protein-bound advanced glycation endproducts and digestive enzymes related to type 2 diabetes mellitus. BMC Complementary and Alternative Medicine, 16, 338. https://doi.org/10.1186/s12906-016-1329-0
- Lee, W. K., Wong, L. L., Loo, Y. Y., Kasapis, S., & Huang, D. (2010). Evaluation of different teas against starch digestibility by mammalian glycosidases. Journal of Agricultural and Food Chemistry, 58, 148–154. https://doi.org/10.1021/jf903011g
- Legay, C., Popineau, Y., Bérot, S., & Guéguen, J. (1997). Comparative study of enzymatichydrolysis of α/β- and γ-gliadins. Food/Nahrung, 41, 201–207. https://doi.org/10.1002/food.19970410404
- Li, Y. W., Li, B., He, J., & Qian, P. (2011). Quantitative structure–activity relationship study of antioxidative peptide by using different sets of amino acids descriptors. Journal of Molecular Structure, 998, 53–61. https://doi.org/10.1016/j.molstruc.2011.05.011
- Liu, D., Liang, L., Regenstein, J. M., & Zhou, P. (2012). Extraction and characterisation of pepsin-solubilised collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis). Food Chemistry, 133, 1441–1448. https://doi.org/10.1016/j.foodchem.2012.02.032
- Magro, A. E. A., Silva, L. C., Rasera, G. B., & de Castro, R. J. S. (2019). Solid-state fermentation as an efficient strategy for the biotransformation of lentils: Enhancing their antioxidant and antidiabetic potentials. Bioresources and Bioprocessing, 6, 38. https://doi.org/10.1186/s40643-019-0273-5
- Martin, B. W., Marques, M., Gouveia, M., Leal, I., Lee, I. M., Shiroma, E. J., Lobelo, F., Puska, P., Blair, S. N., Katzmarzyk, P. T., Alkandari, J. R., Andersen, L. B., Bauman, A. E., Brownson, R. C., Bull, F. C., Craig, C. L., Ekelund, U., Goenka, S., Guthold, R., … Luiz, C. (2005). Envelhecimento ativo: Uma política de saúde/World Health Organization. The Lancet, 366, 275–276.
- McDougall, G. J., Shpiro, F., Dobson, P., Smith, P., Blake, A., & Stewart, D. (2005). Different polyphenolic components of soft fruits inhibit α-amylase and α-glycosidase. Journal of Agricultural and Food Chemistry, 53, 2760–2766. https://doi.org/10.1021/jf0489926
- Mizuno, S., Nishimura, S., Matsuura, K., Gotou, T., & Yamamoto, N. J. J. O. D. S. (2004). Release of short and proline-rich antihypertensive peptides from casein hydrolysate with an Aspergillus oryzae protease. Journal of Dairy Science, 87, 3183–3188. https://doi.org/10.3168/jds.S0022-0302(04)73453-0
- Moskowitz, R. W. (2000). Role of collagen hydrolysate in bone and joint disease. Seminars in Arthritis and Rheumatism, 30, 87–99. https://doi.org/10.1053/sarh.2000.9622
- Muyonga, J. H., Cole, C. G. B., & Duodu, K. G. (2004). Characterisation of acid soluble collagen from skins of young and adult Nile perch (Lates niloticus). Food Chemistry, 85, 81–89. https://doi.org/10.1016/j.foodchem.2003.06.006
- Nielsen, P. M., Petersen, D., & Dambmann, C. (2001). Improved method for determining food protein degree of hydrolysis. Journal of Food Science, 66, 642–646. https://doi.org/10.1111/j.1365-2621.2001.tb04614.x
- Nuñez, S. M., Cárdenas, C., Pinto, M., Valencia, P., Cataldo, P., Guzmán, F., & Almonacid, S. (2020). Bovine skin gelatin hydrolysates as potential substitutes for polyphosphates: The role of degree of hydrolysis and pH on water-holding capacity. Journal of Food Science, 85, 1988–1996. https://doi.org/10.1111/1750-3841.15299
- Ohara, A., Cason, V. G., Nishide, T. G., Miranda de Matos, F., & de Castro, R. J. S. (2021). Improving the antioxidant and antidiabetic properties of common bean proteins by enzymatic hydrolysis using a blend of proteases. Biocatalysis and Biotransformation, 39, 100–108. https://doi.org/10.1080/10242422.2020.1789114
- Park, P. J., Jung, W. K., Nam, K. S., Shahidi, F., & Kim, S. K. (2001). Purification and characterization of antioxidative peptides from protein hydrolysate of lecithin-free egg yolk. Journal of the American Oil Chemists' Society, 78, 651–656. https://doi.org/10.1007/s11746-001-0321-0
- Perfetti, R., Barnett, P. S., Mathur, R., Egan, J. M. (1998). Novel therapeutic strategies for the treatment of type 2 diabetes. Diabetes/Metabolism Reviews, 14, 207–250.
10.1002/(SICI)1099-0895(1998090)14:3<207::AID-DMR214>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- Peña-Ramos, E. A., Xiong, Y. L., & Arteaga, G. E. (2004). Fractionation and characterisation for antioxidant activity of hydrolysed whey protein. Journal of the Science of Food and Agriculture, 84, 1908–1918. https://doi.org/10.1002/jsfa.1886
- Porfírio, E., & Fanaro, G. B. (2016). Suplementação com colágeno como terapia complementar na prevenção e tratamento de osteoporose e osteoartrite: uma revisão sistemática. Revista Brasileira de Geriatria e Gerontologia, 19, 153–164.
10.1590/1809-9823.2016.14145 Google Scholar
- Pownall, T. L., Udenigwe, C. C., & Aluko, R. E. (2010). Amino acid composition and antioxidant properties of pea seed (Pisum sativum L.) enzymatic protein hydrolysate fractions. Journal of Agricultural and Food Chemistry, 58, 4712–4718. https://doi.org/10.1021/jf904456r
- Rabiei, S., Rezaei, M., Asgharzade, S., Nikoo, M., & Rafieia-Kopai, M. (2019). Antioxidant and cytotoxic properties of protein hydrolysates obtained from enzymatic hydrolysis of Klunzinger's mullet (Liza klunzingeri) muscle. Brazilian Journal of Pharmaceutical Sciences, 55, 1–10. https://doi.org/10.1590/s2175-97902019000218304
- Ranilla, L. G., Kwon, Y. I., Genovese, M. I., Lajolo, F. M., & Shetty, K. (2010). Effect of thermal treatment on phenolic compounds and functionality linked to type 2 diabetes and hypertension management of peruvian and brazilian bean cultivars (Phaseolus Vulgaris L.) using in vitro methods. Journal of Food Biochemistry, 34, 329–355. https://doi.org/10.1111/j.1745-4514.2009.00281.x
- Saiga, A. I., Tanabe, S., & Nishimura, T. (2003). Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. Journal of Agricultural and Food Chemistry, 51, 3661–3667. https://doi.org/10.1021/jf021156g
- Sarmadi, B. H., & Ismail, A. (2010). Antioxidative peptides from food proteins: A review. Peptides, 31, 1949–1956. https://doi.org/10.1016/j.peptides.2010.06.020
- Savoie, L., Agudelo, R. A., Gauthier, S. F., Marin, J., & Pouliot, Y. (2005). In vitro determination of the release kinetics of peptides and free amino acids during the digestion of food proteins. Journal of AOAC International, 88, 935–948. https://doi.org/10.1093/jaoac/88.3.935
- Sgarbieri, V. C., Pacheco, M. T. B., Gibrin, N. F., de Oliveira, D. A. G., & Silva, M. E. C. (2020). Importance of diet, genetic and lifestyle on human aging, health and cognition (pp. 135–147). Book Publisher International. https://doi.org/10.9734/bpi/mono/978-93-90516-73-5
10.9734/bpi/mono/978?93?90516?73?5 Google Scholar
- Shazly, A. B., Mu, H., Liu, Z., El-Aziz, M. A., Zeng, M., Qin, F., Zhang, S., He, Z., & Chen, J. (2019). Release of antioxidant peptides from buffalo and bovine caseins: Influence of proteases on antioxidant capacities. Food Chemistry, 274, 261–267. https://doi.org/10.1016/j.foodchem.2018.08.137
- Shinde, J., Taldone, T., Barletta, M., Kunaparaju, N., Hu, B., Kumar, S., Placido, J., & Zito, S. W. (2008). α-Glucosidase inhibitory activity of Syzygium cumini (Linn.) Skeels seed kernel in vitro and in Goto-Kakizaki (GK) rats. Carbohydrate Research, 343, 1278–1281. https://doi.org/10.1016/j.carres.2008.03.003
- Singh, B. N., Singh, B. R., Singh, R. L., Prakash, D., Dhakarey, R., Upadhyay, G., & Singh, H. B. (2009). Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera. Food and Chemical Toxicology, 47, 1109–1116. https://doi.org/10.1016/j.fct.2009.01.034
- Sisconeto Bisinotto, M., da Silva, D. C., de Carvalho Fino, L., Moreira Simabuco, F., Neves Bezerra, R. M., Costa Antunes, A. E., & Bertoldo Pacheco, M. T. (2021). Bioaccessibility of cashew nut kernel flour compounds released after simulated in vitro human gastrointestinal digestion. Food Research International., 139, 109906. https://doi.org/10.1016/j.foodres.2020.109906
- Sun, S., Gao, Y., Chen, J., & Liu, R. (2022). Identification and release kinetics of peptides from tilapia skin collagen during alcalase hydrolysis. Food Chemistry, 378, 132089. https://doi.org/10.1016/j.foodchem.2022.132089
- Truscheit, E., Hillebrand, I., Junge, B., Müller, L., Puls, W., & Schmidt, D. (1988). Microbial α-glucosidase inhibitors: Chemistry, biochemistry, and therapeutic potential. In Drug Concentration Monitoring Microbial Alpha-Glucosidase Inhibitors Plasminogen Activators. Progress in Clinical Biochemistry and Medicine (Vol 7, pp. 83). Springer. https://doi.org/10.1007/978-3-642-73461-8_2
10.1007/978?3?642?73461?8_2 Google Scholar
- Walrand, S., Chiotelli, E., Noirt, F., Mwewa, S., & Lassel, T. (2008). Consumption of a functional fermented milk containing collagen hydrolysate improves the concentration of collagen-specific amino acids in plasma. Journal of Agricultural and Food Chemistry, 56, 7790–7795. https://doi.org/10.1021/jf800691f
- Wang, L., Jiang, Y., Wang, X., Zhou, J., Cui, H., Xu, W., He, Y., Ma, H., & Gao, R. (2018). Effect of oral administration of collagen hydrolysates from Nile tilapia on the chronologically aged skin. Journal of Functional Foods, 44, 112–117. https://doi.org/10.1016/j.jff.2018.03.005
- Wang, J., Luo, D., Liang, M., Zhang, T., Yin, X., Zhang, Y., Yang, X., & Liu, W. (2018). Spectrum-effect relationships between high-performance liquid chromatography (HPLC) fingerprints and the antioxidant and anti-inflammatory activities of collagen peptides. Molecules, 23, 3257. https://doi.org/10.3390/molecules23123257
- Wang, L. L., & Xiong, Y. L. (2005). Inhibition of lipid oxidation in cooked beef patties by hydrolyzed potato protein is related to its reducing and radical scavenging ability. Journal of Agricultural and Food Chemistry, 53(23), 9186–9192. https://doi.org/10.1021/jf051213g
- White, J. A., Hart, R. J., & Fry, J. C. (1986). An evaluation of the waters Pico-tag system for the amino-acid analysis of food materials. Journal of Automatic Chemistry, 8, 170–177. https://doi.org/10.1155/S1463924686000330
- Xie, N., Wang, B., Jiang, L., Liu, C., & Li, B. (2015). Hydrophobicity exerts different effects on bioavailability and stability of antioxidant peptide fractions from casein during simulated gastrointestinal digestion and Caco-2 cell absorption. Food Research International, 76, 518–526. https://doi.org/10.1016/j.foodres.2015.06.025
- Yarnpakdee, S., Benjakul, S., Kristinsson, H. G., & Bakken, H. E. (2015). Preventive effect of Nile tilapia hydrolysate against oxidative damage of HepG2 cells and DNA mediated by H2O2 and AAPH. Journal of Food Science and Technology, 52, 6194–6205. https://doi.org/10.1007/s13197-014-1672-4
- Yoon, S. H., & Robyt, J. F. (2003). Study of the inhibition of four alpha amylases by acarbose and its 4IV-alpha-maltohexaosyl and 4IV-alpha-maltododecaosyl analogues. Carbohydrate Research, 338, 1969–1980. https://doi.org/10.1016/s0008-6215(03)00293-3
- Yu, Z., Yin, Y., Zhao, W., Liu, J., & Chen, F. (2012). Anti-diabetic activity peptides from albumin against α-glucosidase and α-amylase. Food Chemistry, 135, 2078–2085. https://doi.org/10.1016/j.foodchem.2012.06.088
- Zhang, M., Mu, T. H., & Sun, M. J. (2014). Purification and identification of antioxidant peptides from sweet potato protein hydrolysates by Alcalase. Journal of Functional Foods, 7, 191–200. https://doi.org/10.1016/j.jff.2014.02.012
- Zou, T. B., He, T. P., Li, H. B., Tang, H. W., & Xia, E. Q. (2016). The structure-activity relationship of the antioxidant peptides from natural proteins. Molecules, 21, 72. https://doi.org/10.3390/molecules21010072
