Hydrolysates and bioactive peptides generated from chicken protein hydrolysis: A systematic review of antihypertensive effects in rats
DOI:
https://doi.org/10.33448/rsd-v11i11.33353Keywords:
Protein hydrolysates; Bioactive peptides; Chicken protein; Antihypertensive activity; Enzymatic hydrolysis; Spontaneously hypertensive rats.Abstract
In recent years, obtaining protein hydrolysates and peptides from food proteins has been widely studied in order to better understand not only their nutritional and functional properties, but also the possibility of their use as ingredients in functional foods. It is known that many dietary proteins have, in their primary structure, peptide sequences that, when released, can be absorbed by enterocytes and modulate specific physiological functions, in addition to providing essential amino acids and contributing to energy metabolism. Therefore, this review aims to carry out a systematic review to assess the effectiveness of these bioactive compounds in controlling blood pressure in rats. In addition, the methodological quality of the published articles was evaluated. Searches in Scopus, ScienceDirect, ISI Web of Science and PubMed databases were focused on studies on the use of hydrolysates and peptides obtained from the enzymatic hydrolysis of various chicken tissues in rats. It was possible to verify that the positive antihypertensive effects were mainly dependent on the enzymatic conditions and enzymatic hydrolysis and the monitoring of vital organ functions is essential for the regulation of blood pressure. Due to their effectiveness and low cost, chicken protein hydrolysates could be an interesting alternative for biotechnology applications. Administration of hydrolysates and peptides derived from chicken proteins to spontaneously hypertensive rats (SHR) exhibit potential antihypertensive activity with likely cardiac protective effects against target organ damage.
References
Aluko, R. E. (2015). Antihypertensive peptides from food proteins. Annual Review of Food Science and Technology, 6(1), 235–262. https://doi.org/10.1146/annurev-food-022814-015520
Andrade, E. F., Lobato, R. V., Araújo, T. V., Zangerônimo, M. G., Sousa, R. V., & Pereira, L. J. (2015). Effect of beta-glucans in the control of blood glucose levels of diabetic patients : a systematic review. Nutrición Hospitalaria, 31(1), 170–177. https://doi.org/10.3305/nh.2015.31.1.7597
Bhat, Z. F., Mason, S., Morton, J. D., Bekhit, A. E. A., & Bhat, H. F. (2018). Antihypertensive Peptides from Animal Proteins. In J.-M. Mérillon & K. G. Ramawat (Eds.), Bioactive Molecules in Food. Reference Series in Phytochemistry (pp. 1–36). Cham: Springe. https://doi.org/10.1007/978-3-319-54528-8_18-1
Callegaro, K., Welter, N., & Daroit, D. J. (2018). Feathers as bioresource: Microbial conversion into bioactive protein hydrolysates. Process Biochemistry, 75, 1–9. https://doi.org/10.1016/j.procbio.2018.09.002
Chay, S. Y., Tan, W. K., & Saari, N. (2015). Preparation and characterisation of nanoliposomes containing winged bean seeds bioactive peptides. Journal of Microencapsulation, 32(5), 488–495. https://doi.org/10.3109/02652048.2015.1057250
Cheng, F.-Y., Wan, T.-C., Liu, Y.-T., Lai, K.-M., Lin, L.-C., & Sakata, R. (2008). A study of in vivo antihypertensive properties of enzymatic hydrolysate from chicken leg bone protein. Animal Science Journal, 79(5), 614–619. https://doi.org/10.1111/j.1740-0929.2008.00571.x
Cushman, D. W., & Cheung, H. S. (1971). Spectrophotometric assay and properties of the angiotensin I-converting enzyme of rabbit lung. Biochemical Pharmacology, 20, 1637–1648. https://doi.org/10.1016/0006-2952(71)90292-9
Deng, Z., Liu, Y., Wang, J., Wu, S., Geng, L., Sui, Z., & Zhang, Q. (2018). Antihypertensive effects of two novel angiotensin I-converting enzyme (ACE) nhibitory peptides from Gracilariopsis lemaneiformis (Rhodophyta) in spontaneously hypertensive rats (SHRs). Marine Drugs, 16(9), 299. https://doi.org/10.3390/md16090299
Fagundes, D. J., & Taha, M. O. (2004). Animal disease model: choice’s criteria and current animals specimens. Acta Cirúrgica Brasileira, 19(1), 59–65.
Ferreira, M. S. S., Garbossa, C. A. P., Oberlender, G., Pereira, L. J., Zangeronimo, M. G., Sousa, R. V., & Cantarelli, V. de S. (2013). Effect of Ractopamine on Lipid Metabolism in vivo – a Systematic Review. Brazilian Archives of Biology and Technology, 56(1), 35–43.
Fontoura, R., Daroit, D. J., Correa, A. P. F., Meira, S. M. M., Mosquera, M., & Brandelli, A. (2014). Production of feather hydrolysates with antioxidant, angiotensin-I converting enzyme- and dipeptidyl peptidase-IV-inhibitory activities. New Biotechnology, 31(5), 506–513. https://doi.org/10.1016/j.nbt.2014.07.002
Fontoura, R., Daroit, D. J., Corrêa, A. P. F., Moresco, K. S., Santi, L., Beys-da-Silva, W. O., … Brandelli, A. (2018). Characterization of a novel antioxidant peptide from feather keratin hydrolysates. New Biotechnology. https://doi.org/10.1016/j.nbt.2018.09.003
Fukada, Y., Mizutani, S., Nomura, S., Hara, W., Matsui, R., Nagai, K., … Terashima, M. (2016). Antioxidant activities of a peptide derived from chicken dark meat. Journal of Food Science and Technology, 53(5), 2476–2481. https://doi.org/10.1007/s13197-016-2233-9
Girgih, A. T., Alashi, A., He, R., Malomo, S., & Aluko, R. E. (2013). Preventive and treatment effects of a hemp seed (Cannabis sativa L.) meal protein hydrolysate against high blood pressure in spontaneously hypertensive rats. European Journal of Nutrition, 53, 1237–1246. https://doi.org/10.1007/s00394-013-0625-4
Greenhalgh, T. (1997). How to read a paper: Assessing the methodological quality of published papers. British Medical Journal, 315, 305–308. https://doi.org/10.1136/bmj.315.7103.305
Herregods, G., Van Camp, J., Morel, N., Ghesquière, B., Gevaert, K., Vercruysse, L., & Smagghe, G. (2011). Angiotensin I-converting enzyme inhibitory activity of gelatin hydrolysates and identification of bioactive peptides. Journal of Agricultural and Food Chemistry, 59(2), 552–558. https://doi.org/10.1021/jf1037823
Huang, J., Liu, Q., Xue, B., Chen, L., Wang, Y., Ou, S., & Peng, X. (2016). Angiotensin-I-Converting Enzyme Inhibitory Activities and In Vivo Antihypertensive Effects of Sardine Protein Hydrolysate. Journal of Food Science, 81(11), H2831–H2840. https://doi.org/10.1111/1750-3841.13508
Inoue, N., Hamasaki, A., Hidaka, S., Miura, N., Fukahori, M., Maruyama, M., & Muguruma, M. (2013). Analysis of the Components of Porcine Liver Hydrolysate and Examination of the Antioxidant Activity and Angiotensin Converting Enzyme ( ACE ) -inhibiting Activity. YAKUGAKU ZASSHI, 133(1), 107–115.
Iwai, K., Zhang, Y., Kouguchi, T., Saiga-Egusa, A., Shimizu, M., Ohmori, T., & Morimatsu, F. (2009). Blood Concentration of Food-Derived Peptides following Oral Intake of Chicken Collagen Hydrolysate and its Angiotensin-Converting Enzyme Inhibitory Activity in Healthy Volunteers. Nippon Shokuhin Kagaku Kogaku Kaishi, 56(6), 326–330.
Iwaniak, A., Minkiewicz, P., & Darewicz, M. (2014). Food-originating ACE inhibitors, including antihypertensive peptides, as preventive food components in blood pressure reduction. Comprehensive Reviews in Food Science and Food Safety, 13(2), 114–134. https://doi.org/10.1111/1541-4337.12051
Jahandideh, F., Majumder, K., Chakrabarti, S., Morton, J. S., Panahi, S., Kaufman, S., & Wu, J. (2014). Beneficial effects of simulated gastro-intestinal digests of fried egg and its fractions on blood pressure, plasma lipids and oxidative stress in spontaneously hypertensive rats. PloS One, 9(12), e115006. https://doi.org/10.1371/journal.pone.0115006
Jäkälä, P., & Vapaatalo, H. (2010). Antihypertensive peptides from milk proteins. Pharmaceuticals, 3(1), 251–272. https://doi.org/10.3390/ph3010251
Jamdar, S. N., Rajalakshmi, V., & Sharma, A. (2012). Antioxidant and ACE inhibitory properties of poultry viscera protein hydrolysate and its peptide fractions. Journal of Food Biochemistry, 36(4), 494–501. https://doi.org/10.1111/j.1745-4514.2011.00562.x
Jao, C.-L., Huang, S.-L., & Hsu, K.-C. (2012). Angiotensin I-converting enzyme inhibitory peptides: Inhibition mode, bioavailability, and antihypertensive effects. BioMedicine, 2(4), 130–136. https://doi.org/http://dx.doi.org/10.1016/j.biomed.2012.06.005
Kurozawa, L. E., Park, K. J., & Hubinger, M. D. (2009). Influence of process conditions on enzymatic hydrolysis kinetics of chicken meat. Ciência e Tecnologia de Alimentos, 29(3), 557–566. https://doi.org/10.1590/S0101-20612009000300017
Lau, C. C., Abdullah, N., & Shuib, A. S. (2013). Novel angiotensin I-converting enzyme inhibitory peptides derived from an edible mushroom, Pleurotus cystidiosus O.K. Miller identified by LC-MS/MS. BMC Complementary and Alternative Medicine, 13(313), 1–10. https://doi.org/https://doi.org/10.1186/1472-6882-13-313
Lee, S. J., Kim, E. K., Hwang, J. W., Oh, H. J., Cheong, S. H., Moon, S. H., & Park, P. J. (2010). Purification and characterisation of an antioxidative peptide from enzymatic hydrolysates of duck processing by-products. Food Chemistry, 123, 216–220. https://doi.org/10.1016/j.foodchem.2010.04.001
Lee, S. J., Kim, Y. S., Hwang, J. W., Kim, E. K., Moon, S. H., Jeon, B. T., & Park, P. J. (2012). Purification and characterization of a novel antioxidative peptide from duck skin by-products that protects liver against oxidative damage. Food Research International, 49, 285–295. https://doi.org/10.1016/j.foodres.2012.08.017
Lee, S. Y., & Hur, S. J. (2017). Angiotensin Converting Enzyme Inhibitory and Antioxidant Activities of Enzymatic Hydrolysates of Korean Native Cattle (Hanwoo) Myofibrillar Protein. BioMed Research International, 2017. https://doi.org/10.1155/2017/5274637
Lemes, A. C., Sala, L., Ores, J. da C., Braga, A. R. C., Egea, M. B., & Fernandes, K. F. (2016). A Review of the Latest Advances in Encrypted Bioactive Peptides from Protein-Rich Waste. International Journal of Molecular Sciences, 17(6). https://doi.org/10.3390/ijms17060950
Liu, R., Xing, L., Fu, Q., Zhou, G., & Zhang, W. (2016). A Review of antioxidant peptides derived from meat muscle and by-products. Antioxidants, 5(4), 32. https://doi.org/10.3390/antiox5030032
Mane, S., & Jamdar, S. N. (2017). Purification and identification of ACE-inhibitory peptides from poultry viscera protein hydrolysate. Journal of Food Biochemistry, 41(2), 1–10. https://doi.org/10.1111/jfbc.12275
Mas-Capdevila, A., Pons, Z., Aleixandre, A., Bravo, F. I., & Muguerza, B. (2018). Dose-related antihypertensive properties and the corresponding mechanisms of a chicken foot hydrolysate in hypertensive rats. Nutrients, 10(1), 1295. https://doi.org/10.3390/nu10091295
Mendoza-Jiménez, Y. L., Eusebio-Moreno, J. C., Álvarez-García, R., Abreu-Corona, A., Vargas-Hernández, G., Téllez-Jurado, A., & Tovar-Jiménez, X. (2018). Antioxidant activity of protein hydrolysates from common bean (Phaseolus vulgaris L.) varieties “Negro Primavera-28” and “Flor de Durazno.” Revista de Ciencias Biológicas y de La Salud, 20(2), 25–30.
Nakade, K., Kamishima, R., Inoue, Y., Ahhmed, A., Kawahara, S., Nakayama, T., & Muguruma, M. (2008). Identification of an antihypertensive peptide derived from chicken bone extract. Animal Science Journal, 79(6), 710–715. https://doi.org/10.1111/j.1740-0929.2008.00584.x
Neves, R. A. M. das, Campos, T., & Marquez, U. M. L. (2006). Modulation of arterial pressure by protein hydrolysates. Brazilian Journal of Food Technology, 1(1), 81–86.
Nie, X., Xu, D., Zhao, L., & Meng, X. (2017). Antioxidant activities of chicken bone peptide fractions and their Maillard reaction products: Effects of different molecular weight distributions. International Journal of Food Properties, 20(1), S457–S466. https://doi.org/10.1080/10942912.2017.1299176
Nobre, F., Coelho, E. B., Lopes, P. C., & Geleilete, T. J. M. (2013). Essential Arterial Hypertension. Medicina (Brazil), 46(3), 256–272.
Onuh, J. O., Girgih, A. T., Aluko, R. E., & Aliani, M. (2013). Inhibitions of renin and angiotensin converting enzyme activities by enzymatic chicken skin protein hydrolysates. Food Research International, 53(1), 260–267. https://doi.org/10.1016/j.foodres.2013.05.010
Onuh, J. O., Girgih, A. T., Malomo, S. A., Aluko, R. E., & Aliani, M. (2015). Kinetics of in vitro renin and angiotensin converting enzyme inhibition by chicken skin protein hydrolysates and their blood pressure lowering effects in spontaneously hypertensive rats. Journal of Functional Foods, 14, 133–143. https://doi.org/10.1016/j.jff.2015.01.031
Onuh, J. O., Girgih, A. T., Nwachukwu, I., Ievari-Shariati, S., Raj, P., Netticadan, T., & Aliani, M. (2016). A metabolomics approach for investigating urinary and plasma changes in spontaneously hypertensive rats (SHR) fed with chicken skin protein hydrolysates diets. Journal of Functional Foods, 22, 20–33. https://doi.org/10.1016/j.jff.2016.01.010
Pereira, U. P., Oliveira, D. G. S., Mesquita, L. R., Costa, G. M., & Pereira, L. J. (2011). Efficacy of Staphylococcus aureus vaccines for bovine mastitis: A systematic review. Veterinary Microbiology, 148(2–4), 117–124. https://doi.org/10.1016/j.vetmic.2010.10.003
Sahay, M., & Sahay, R. K. (2012). Low renin hypertension. Indian J Endocrinol Metab., 16(5), 728–739. https://doi.org/10.4103/2230
Saiga, A., Iwai, K., Hayakawa, T., Takahata, Y., Kitamura, S., Nishimura, T., & Morimatsu, F. (2008). Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. Journal of Agricultural and Food Chemistry, 56(20), 9586–9591.
Saiga, A., Okumura, T., Makihara, T., Katsuda, S.-I., Morimatsu, F., & Nishimura, T. (2006). Action mechanism of an angiotensin I-converting enzyme inhibitory peptide derived from chicken breast muscle. Journal of Agricultural and Food Chemistry, 54(3), 942–945. https://doi.org/10.1021/jf0508201
Saiga, A., Okumura, T., Makihara, T., Katsuta, S., Shimizu, T., Yamada, R., & Nishimura, T. (2003). Angiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chicken breast muscle extract. Journal of Food and Agricultural Chemistry, 51(6), 1741–1745. Retrieved from http://pubs.acs.org/doi/abs/10.1021/jf020604h
Sampaio, R. F., & Mancini, M. C. (2007). Systematic review studies: a guide for careful synthesis of the scientific evidence. Revista Brasileira de Fisioterapia, 11(1), 83–89. https://doi.org/10.1590/S1413-35552007000100013
Sánchez, A., & Vázquez, A. (2017). Bioactive peptides: A review. Food Quality and Safety, 1(1), 29–46. https://doi.org/10.1093/fqs/fyx006
Sangsawad, P., Roytrakul, S., & Yongsawatdigul, J. (2017). Angiotensin converting enzyme (ACE) inhibitory peptides derived from the simulated in vitro gastrointestinal digestion of cooked chicken breast. Journal of Functional Foods, 29, 77–83. https://doi.org/10.1016/j.jff.2016.12.005
Sarbon, N. M., Badii, F., & Howell, N. K. (2018). Purification and characterization of antioxidative peptides derived from chicken skin gelatin hydrolysate. Food Hydrocolloids, 85, 311–320. https://doi.org/10.1016/j.foodhyd.2018.06.048
Sharma, S., Singh, R., & Rana, S. (2011). Bioactive Peptides: A Review. International Journal Bioautomation, 15(4), 223–250.
Silva, R. R. (2018). Enzymatic synthesis of protein hydrolysates from animal proteins: Exploring microbial peptidases. Frontiers in Microbiology, 9(735), 1–5. https://doi.org/10.3389/fmicb.2018.00735
Silva, V. D. O., Foureaux, R. D. C., Araujo, T. S., Peconick, A. P., Zangeronimo, M. G., & Pereira, L. J. (2012). Effect of Probiotic Administration on the Immune Response : A Systematic Review of Experimental Models in Rats. Brazilian Archives of Biology and Technology, 55(5), 685–694.
Sparks, M. A., Crowley, S. D., Gurley, S. B., Mirotsou, M., & Coffman, T. M. (2014). Classical Renin-Angiotensin system in kidney physiology. Comprehensive Physiology, 4(3), 1201–1228. https://doi.org/10.1002/cphy.c130040
Terashima, M., Baba, T., Ikemoto, N., Katayama, M., Morimoto, T., & Matsumura, S. (2010). Novel angiotensin-converting enzyme (ACE) inhibitory peptides derived from boneless chicken leg meat. Journal of Agricultural and Food Chemistry, 58(12), 7432–7436. https://doi.org/10.1021/jf100977z
Udenigwe, C. C., Girgih, A. T., Mohan, A., Gong, M., Malomo, S. A., & Aluko, R. E. (2017). Antihypertensive and bovine plasma oxidation-inhibitory activities of spent hen meat protein hydrolysates. Journal of Food Biochemistry, 41(4), e12378. https://doi.org/10.1111/jfbc.12378
Udenigwe, C. C., Lin, Y.-S., Hou, W.-C., & Aluko, R. E. (2009). Kinetics of the inhibition of renin and angiotensin I-converting enzyme by flaxseed protein hydrolysate fractions. Journal of Functional Foods, 1(2), 199–207. https://doi.org/10.1016/j.jff.2009.01.009
Wang, D., & Shahidi, F. (2018). Protein hydrolysate from turkey meat and optimization of its antioxidant potential by response surface methodology. Poultry Science, 97(5), 1824–1831. https://doi.org/10.3382/ps/pex457
Wang, L.-S., Huang, J.-C., Chen, Y.-L., Huang, M., & Zhou, G.-H. (2015). Identification and characterization of antioxidant peptides from enzymatic hydrolysates of duck meat. Journal of Agricultural and Food Chemistry, 63(13), 3437–3444. https://doi.org/10.1021/jf506120w
Wang, L., Li, X., Li, Y., Liu, W., Jia, X., Qiao, X., & Wang, S. (2018). Antioxidant and angiotensin I-converting enzyme inhibitory activities of Xuanwei ham before and after cooking and in vitro simulated gastrointestinal digestion. Royal Society Open Science, 5(180876), 1–13. https://doi.org/http://dx.doi.org/10.1098/rsos.180276
Yu, Z., Yin, Y., Zhao, W., Chen, F., & Liu, J. (2014). Antihypertensive effect of angiotensin-converting enzyme inhibitory peptide RVPSL on spontaneously hypertensive rats by regulating gene expression of the renin-angiotensin system. Journal of Agricultural and Food Chemistry, 62(4), 912–917. https://doi.org/10.1021/jf405189y
Zhuang, Y., Sun, L., Zhang, Y., & Liu, G. (2012). Antihypertensive effect of long-term oral administration of jellyfish (Rhopilema esculentum) collagen peptides on renovascular hypertension. Marine Drugs, 10(2), 417–426. https://doi.org/10.3390/md10020417
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Copyright (c) 2022 Thiago Santos Araujo; Leandro Paes de Brito; José Manoel Wanderley Duarte Neto; Maria Carolina de Albuquerque Wanderley; Wendell Wagner Campos Albuquerque; Polyanna Nunes Herculano; Lorenzo Pastrana ; Maria Taciana Cavalcanti Vieira Soares ; Ana Lúcia Figueiredo Porto
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