The effect of starter cultures on peptide profiles identified in camel milk cheese
Main Article Content
Keywords
camel milk cheese; starter cultures; biologically active peptides; chemometric 24 analysis; peptide identification
Abstract
Cheese contains a lot of biologically active compounds; among them, peptides with functional properties are important assembles. In this study, camel milk cheese samples are studied. The camel milk was fermented by mesophilic and thermophilic cultures. Cheese samples were ripened for 30 days, and the peptides released from casein were analyzed using liquid chromatography–tandem mass spectrometry. Identified peptides were analyzed by applying chemometrics. Furthermore, peptides from camel milk cheeses (β-CN- and α-CN-derived) were identified using the milk bioactive peptides database (MBPDB) and Peptide Ranker. A total of 52 peptides were identified. In all, 21 peptides were identified from β-CN in cheeses using mesophilic culture and five peptides from α-CN besides 17 peptides from β-CN and nine peptides from α-CN in cheeses using thermophilic culture. From a biological point of view, the peptides identified in camel milk cheese were homologous to sequences that were previously reported in the literature to exhibit angiotensin-converting enzyme inhibitory, antioxidant, antimicrobial,and dipeptidyl-peptidase IV inhibitory activities based on peptide sequence databases.
References
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Baptista, D.P., Negrão, F., Eberlin, M.N. and Gigante, M.L. 2020. Peptide profile and angiotensin-converting enzyme inhibitory activity of prato cheese with salt reduction and Lactobacillus helveticus as an adjunct culture. Food Research International 133: 109190. https://doi.org/10.1016/j.foodres.2020.109190
Bhat, M.Y., Dar, T.A. and Singh, L.R. 2016. Casein proteins: structural and functional aspects. In: Gigli, I. (ed.) Milk Proteins – From Structure to Biological Properties and Health Aspects [Internet]. InTech Open. https://doi.org/10.5772/64187
Cebo, C. and Saadaoui, B. 2015. Analyse des Protéines du Lait des Camélidés par Approches Protéomique et Moléculaire. Thèse, Sciences du Vivant [q-bio]. Ecole Superieure des Sciences et Techniques de Tunis, Université de Tunis, Tunis.
Chourasia, R., Abedin, M.M., Chiring Phukon, L., Sahoo, D., Singh, S.P. and Rai, A.K. 2021. Biotechnological approaches for the production of designer cheese with improved functionality. Comprehensive Reviews in Food Science and Food Safety 20(1): 960–979. https://doi.org/10.1111/1541-4337.12680
Daliri, E., Oh, D. and Lee, B. 2017. Bioactive peptides. Foods 6(5): 32. https://doi.org/10.3390/foods6050032
El Hatmi, H., Jrad, Z., Khorchani, T., Jardin, J., Poirson, C., Perrin, C., Cakir-Kiefer, C. and Girardet, J.-M. 2016. Identification of bioactive peptides derived from caseins, glycosylation-dependent cell adhesion molecule-1 (GlyCAM-1), and peptidoglycan recognition protein-1 (PGRP-1) in fermented camel milk. International Dairy Journal 56: 159–168. https://doi.org/10.1016/j.idairyj.2016.01.021.
Erhardt, G., Shuiep, E. T. S., Lisson, M., Weimann, C., Wang, Z., El Zubeir, I. E. Y. M., and Pauciullo, A. 2016. Alpha S1-casein polymorphisms in camel (Camelus dromedarius) and descriptions of biological active peptides and allergenic epitopes. Tropical Animal Health and Production. 48(5): 879–887. https://doi.org/10.1007/s11250-016-0997-6
Fan, M., Guo, T., Li, W., Chen, J., Li, F., Wang, C., Shi, Y., Li, X. and Zhang, S. 2019. Isolation and identification of novel casein-derived bioactive peptides and potential functions in fermented casein with Lactobacillus helveticus. Food Science and Human Wellness 8(2): 156–176. https://doi.org/10.1016/j.fshw.2019.03.010
Faye, B., Alhaj, O.A. and Agrawal, R.P. 2020. Manufacturing camel dairy products: challenges and opportunities. In: Faye, B., Alhaj, O.A. and Agrawal, R.P. (eds.) Handbook of Research on Health and Environmental Benefits of Camel Products. IGI Global, Hershey, PA, pp. 139–158. https://doi.org/10.4018/978-1-7998-6736-4.ch007
Fernández-Esplá, M.D. and Rul, F. 1999. PepS from streptococcus thermophilus. A new member of the aminopeptidase T family of thermophilic bacteria. European Journal of Biochemistry 263(2): 502–510. https://doi.org/10.1046/j.1432-1327.1999.00528.x
Gómez-Ruiz, J.Á., Taborda, G., Amigo, L., Recio, I. and Ramos, M. 2006. Identification of ACE-inhibitory peptides in different Spanish cheeses by tandem mass spectrometry. European Food Research and Technology 223(5): 595–601. https://doi.org/10.1007/s00217-005-0238-0
Gupta, A., Mann, B., Kumar, R., and Sangwan, R.B. 2009. Antioxidant activity of cheddar cheeses at different stages of ripening. International Journal of Dairy Technology 62(3): 339–347. https://doi.org/10.1111/j.1471-0307.2009.00509.x
Helal, A. and Tagliazucchi, D. 2023. Peptidomics profile, bioactive peptides identification and biological activities of six different cheese varieties. Biology 12(1): 78. https://doi.org/10.3390/biology12010078
Kohmura, M., Nio, N., Kubo, K., Minoshima, Y., Munekata, E. and Ariyoshi, Y. 1989. Inhibition of angiotensin-converting enzyme by synthetic peptides of human β-casein. Agricultural and Biological Chemistry 53(8): 2107–2114. https://doi.org/10.1080/00021369.1989.10869621
Konuspayeva, G., Al-Ghadan, M.M., Alzuraik, F. and Faye, B. 2023. Some factors influencing the freezing point of camel milk. Animals 13(10): 1657. https://doi.org/10.3390/ani13101657
Korhonen, H. and Pihlanto, A. 2006. Bioactive peptides: production and functionality. International Dairy Journal 16(9): 945–960. https://doi.org/10.1016/j.idairyj.2005.10.012
Kurbanova, M., Voroshilin, R., Kozlova, O. and Atuchin, V. 2022. Effect of Lactobacteria on bioactive peptides and their sequence identification in mature cheese. Microorganisms 10(10): 2068. https://doi.org/10.3390/microorganisms10102068
Makhammajanov, Z., Kabayeva, A., Auganova, D. Tarlykov, P., Bukasov, R., Turebekov, D., Kanbay, M., Molnar, M. Z., Kovesdy, C. P., Abidi, S. H., and Gaipov, A . 2024. Candidate protein biomarkers in chronic kidney disease: a proteomics study. Scientific Reports 14: 14014. https://doi.org/10.1038/s41598-024-64833-8
McSweeney, P.L.H. 2017. Biochemistry of cheese ripening: introduction and overview. In: McSweeney, P.L.H., Fox, P.F., Cotter, P., Everett, D.W. (eds.) Cheese: Chemistry, Physics and Microbiology. 4th edition. Academic Press, London, 2017, pp. 379–387. https://doi.org/10.1016/B978-0-12-417012-4.00014-4
Mohamed, A. and El Zubeir, I.E.M. 2021. Cheese making from camel milk: a review. Advances in Animal and Veterinary Sciences 9(6): 852–860. https://doi.org/10.17582/journal.aavs/2021/9.6.852.860
Mooney, C., Haslam, N.J., Pollastri, G. and Shields, D.C. 2012. Towards the improved discovery and design of functional peptides: common features of diverse classes permit generalized prediction of bioactivity. PLOS ONE 7(10): e45012. https://doi.org/10.1371/journal.pone.0045012
Moslehishad, M., Ehsani, M.R., Salami, M., Mirdamadi, S., Ezzatpanah, H., Naslaji, A.N. and Moosavi-Movahedi, A.A. 2013. The comparative assessment of fermented camel and bovine milk on the rheological properties and ACE-inhibitory and antioxidant activities of their peptide fractions. Dairy Science & Technology 93(5): 487–499. https://doi.org/10.1007/s13594-013-0121-3
Murali, C., Mudgil, P., Gan, C.-Y., Tarazi, H., El-Awady, R., Abdalla, Y., Amin, A. and Maqsood, S. 2021. Camel whey protein hydrolysates induced G2/M cell cycle arrest in human colorectal carcinoma. Scientific Reports 11(1): 7062. https://doi.org/10.1038/s41598-021-86391-z
Nielsen, S.D., Beverly, R.L., Qu, Y. and Dallas, D.C. 2017. Milk bioactive peptide database: a comprehensive database of milk protein-derived bioactive peptides and novel visualization. Food Chemistry 232: 673–682. https://doi.org/10.1016/j.foodchem.2017.04.056
Nongonierma, A.B., Paolella, S., Mudgil, P., Maqsood, S., and FitzGerald, R.J. 2018. Identification of novel dipeptidyl peptidase IV (DPP-IV) inhibitory peptides in camel milk protein hydrolysates. Food Chemistry. 244: 340–348. https://doi.org/10.1016/j.foodchem.2017.10.033
Norris, R., Poyarkov, A., O’Keeffe, M.B., and Fitz Gerald, R.J. 2014. Characterisation of the hydrolytic specificity of Aspergillus niger derived prolyl endoproteinase on bovine β-casein and determination of ACE inhibitory activity. Food Chemistry 156: 29–36. https://doi.org/10.1016/j.foodchem.2014.01.056
Öztürk, H.İ. and Akın, N. 2021. Effect of ripening time on peptide dynamics and bioactive peptide composition in Tulum cheese. Journal of Dairy Science 104(4): 3832–3852. https://doi.org/10.3168/jds.2020-19494
Parastouei, K., Jabbari, M., Javanmardi, F., Barati, M., Mahmoudi, Y., Khalili-Moghadam, S., Ahmadi, H., Davoodi, S.H., and Mousavi Khaneghah, A. 2023. Estimation of bioactive peptide content of milk from different species using an in silico method. Amino Acids. 55(10): 1261–1278. https://doi.org/10.1007/s00726-022-03152-6
Suetsuna, K., Ukeda, H., and Ochi, H. 2000. Isolation and characterization of free radical scavenging activities peptides derived from casein. The Journal of Nutritional Biochemistry. 11(3): 128–131. https://doi.org/10.1016/S0955-2863(99)00083-2
Tagliazucchi, D., Shamsia, S., and Conte, A. 2016. Release of angiotensin converting enzyme-inhibitory peptides during in vitro gastro-intestinal digestion of camel milk. International Dairy Journal. 56: 119–128. https://doi.org/10.1016/j.idairyj.2016.01.009
Tarapoulouzi, M., Kokkinofta, R., and Theocharis, C.R. 2020. Chemometric analysis combined with FTIR spectroscopy of milk and Halloumi cheese samples according to species’ origin. Journal of the Science of Food and Agriculture. 100(3): 1218–1226. https://doi.org/10.1002/jsfa.10120
Théolier, J., Hammami, R., Fliss, I. and Jean, J.. 2014. Antibacterial and antifungal activity of water-soluble extracts from Mozzarella, Gouda, Swiss, and Cheddar commercial cheeses produced in Canada. Dairy Science & Technology 94: 427–438. https://doi.org/10.1007/s13594-014-0170-9
Toldrá, F., Reig, M. and Mora, L. 2021. Proteomics and peptidomics in food, by-products and bioactive peptides. Journal of Proteomics 241: 104229. https://doi.org/10.1016/j.jprot.2021.104229
Weimann, C., Meisel, H., and Erhardt, G. 2009. Short communication: Bovine κ-casein variants result in different angiotensin I converting enzyme (ACE) inhibitory peptides. Journal of Dairy Science. 92(5): 1885–1888. https://doi.org/10.3168/jds.2008-1671
Baptista, D.P., Negrão, F., Eberlin, M.N. and Gigante, M.L. 2020. Peptide profile and angiotensin-converting enzyme inhibitory activity of prato cheese with salt reduction and Lactobacillus helveticus as an adjunct culture. Food Research International 133: 109190. https://doi.org/10.1016/j.foodres.2020.109190
Bhat, M.Y., Dar, T.A. and Singh, L.R. 2016. Casein proteins: structural and functional aspects. In: Gigli, I. (ed.) Milk Proteins – From Structure to Biological Properties and Health Aspects [Internet]. InTech Open. https://doi.org/10.5772/64187
Cebo, C. and Saadaoui, B. 2015. Analyse des Protéines du Lait des Camélidés par Approches Protéomique et Moléculaire. Thèse, Sciences du Vivant [q-bio]. Ecole Superieure des Sciences et Techniques de Tunis, Université de Tunis, Tunis.
Chourasia, R., Abedin, M.M., Chiring Phukon, L., Sahoo, D., Singh, S.P. and Rai, A.K. 2021. Biotechnological approaches for the production of designer cheese with improved functionality. Comprehensive Reviews in Food Science and Food Safety 20(1): 960–979. https://doi.org/10.1111/1541-4337.12680
Daliri, E., Oh, D. and Lee, B. 2017. Bioactive peptides. Foods 6(5): 32. https://doi.org/10.3390/foods6050032
El Hatmi, H., Jrad, Z., Khorchani, T., Jardin, J., Poirson, C., Perrin, C., Cakir-Kiefer, C. and Girardet, J.-M. 2016. Identification of bioactive peptides derived from caseins, glycosylation-dependent cell adhesion molecule-1 (GlyCAM-1), and peptidoglycan recognition protein-1 (PGRP-1) in fermented camel milk. International Dairy Journal 56: 159–168. https://doi.org/10.1016/j.idairyj.2016.01.021.
Erhardt, G., Shuiep, E. T. S., Lisson, M., Weimann, C., Wang, Z., El Zubeir, I. E. Y. M., and Pauciullo, A. 2016. Alpha S1-casein polymorphisms in camel (Camelus dromedarius) and descriptions of biological active peptides and allergenic epitopes. Tropical Animal Health and Production. 48(5): 879–887. https://doi.org/10.1007/s11250-016-0997-6
Fan, M., Guo, T., Li, W., Chen, J., Li, F., Wang, C., Shi, Y., Li, X. and Zhang, S. 2019. Isolation and identification of novel casein-derived bioactive peptides and potential functions in fermented casein with Lactobacillus helveticus. Food Science and Human Wellness 8(2): 156–176. https://doi.org/10.1016/j.fshw.2019.03.010
Faye, B., Alhaj, O.A. and Agrawal, R.P. 2020. Manufacturing camel dairy products: challenges and opportunities. In: Faye, B., Alhaj, O.A. and Agrawal, R.P. (eds.) Handbook of Research on Health and Environmental Benefits of Camel Products. IGI Global, Hershey, PA, pp. 139–158. https://doi.org/10.4018/978-1-7998-6736-4.ch007
Fernández-Esplá, M.D. and Rul, F. 1999. PepS from streptococcus thermophilus. A new member of the aminopeptidase T family of thermophilic bacteria. European Journal of Biochemistry 263(2): 502–510. https://doi.org/10.1046/j.1432-1327.1999.00528.x
Gómez-Ruiz, J.Á., Taborda, G., Amigo, L., Recio, I. and Ramos, M. 2006. Identification of ACE-inhibitory peptides in different Spanish cheeses by tandem mass spectrometry. European Food Research and Technology 223(5): 595–601. https://doi.org/10.1007/s00217-005-0238-0
Gupta, A., Mann, B., Kumar, R., and Sangwan, R.B. 2009. Antioxidant activity of cheddar cheeses at different stages of ripening. International Journal of Dairy Technology 62(3): 339–347. https://doi.org/10.1111/j.1471-0307.2009.00509.x
Helal, A. and Tagliazucchi, D. 2023. Peptidomics profile, bioactive peptides identification and biological activities of six different cheese varieties. Biology 12(1): 78. https://doi.org/10.3390/biology12010078
Kohmura, M., Nio, N., Kubo, K., Minoshima, Y., Munekata, E. and Ariyoshi, Y. 1989. Inhibition of angiotensin-converting enzyme by synthetic peptides of human β-casein. Agricultural and Biological Chemistry 53(8): 2107–2114. https://doi.org/10.1080/00021369.1989.10869621
Konuspayeva, G., Al-Ghadan, M.M., Alzuraik, F. and Faye, B. 2023. Some factors influencing the freezing point of camel milk. Animals 13(10): 1657. https://doi.org/10.3390/ani13101657
Korhonen, H. and Pihlanto, A. 2006. Bioactive peptides: production and functionality. International Dairy Journal 16(9): 945–960. https://doi.org/10.1016/j.idairyj.2005.10.012
Kurbanova, M., Voroshilin, R., Kozlova, O. and Atuchin, V. 2022. Effect of Lactobacteria on bioactive peptides and their sequence identification in mature cheese. Microorganisms 10(10): 2068. https://doi.org/10.3390/microorganisms10102068
Makhammajanov, Z., Kabayeva, A., Auganova, D. Tarlykov, P., Bukasov, R., Turebekov, D., Kanbay, M., Molnar, M. Z., Kovesdy, C. P., Abidi, S. H., and Gaipov, A . 2024. Candidate protein biomarkers in chronic kidney disease: a proteomics study. Scientific Reports 14: 14014. https://doi.org/10.1038/s41598-024-64833-8
McSweeney, P.L.H. 2017. Biochemistry of cheese ripening: introduction and overview. In: McSweeney, P.L.H., Fox, P.F., Cotter, P., Everett, D.W. (eds.) Cheese: Chemistry, Physics and Microbiology. 4th edition. Academic Press, London, 2017, pp. 379–387. https://doi.org/10.1016/B978-0-12-417012-4.00014-4
Mohamed, A. and El Zubeir, I.E.M. 2021. Cheese making from camel milk: a review. Advances in Animal and Veterinary Sciences 9(6): 852–860. https://doi.org/10.17582/journal.aavs/2021/9.6.852.860
Mooney, C., Haslam, N.J., Pollastri, G. and Shields, D.C. 2012. Towards the improved discovery and design of functional peptides: common features of diverse classes permit generalized prediction of bioactivity. PLOS ONE 7(10): e45012. https://doi.org/10.1371/journal.pone.0045012
Moslehishad, M., Ehsani, M.R., Salami, M., Mirdamadi, S., Ezzatpanah, H., Naslaji, A.N. and Moosavi-Movahedi, A.A. 2013. The comparative assessment of fermented camel and bovine milk on the rheological properties and ACE-inhibitory and antioxidant activities of their peptide fractions. Dairy Science & Technology 93(5): 487–499. https://doi.org/10.1007/s13594-013-0121-3
Murali, C., Mudgil, P., Gan, C.-Y., Tarazi, H., El-Awady, R., Abdalla, Y., Amin, A. and Maqsood, S. 2021. Camel whey protein hydrolysates induced G2/M cell cycle arrest in human colorectal carcinoma. Scientific Reports 11(1): 7062. https://doi.org/10.1038/s41598-021-86391-z
Nielsen, S.D., Beverly, R.L., Qu, Y. and Dallas, D.C. 2017. Milk bioactive peptide database: a comprehensive database of milk protein-derived bioactive peptides and novel visualization. Food Chemistry 232: 673–682. https://doi.org/10.1016/j.foodchem.2017.04.056
Nongonierma, A.B., Paolella, S., Mudgil, P., Maqsood, S., and FitzGerald, R.J. 2018. Identification of novel dipeptidyl peptidase IV (DPP-IV) inhibitory peptides in camel milk protein hydrolysates. Food Chemistry. 244: 340–348. https://doi.org/10.1016/j.foodchem.2017.10.033
Norris, R., Poyarkov, A., O’Keeffe, M.B., and Fitz Gerald, R.J. 2014. Characterisation of the hydrolytic specificity of Aspergillus niger derived prolyl endoproteinase on bovine β-casein and determination of ACE inhibitory activity. Food Chemistry 156: 29–36. https://doi.org/10.1016/j.foodchem.2014.01.056
Öztürk, H.İ. and Akın, N. 2021. Effect of ripening time on peptide dynamics and bioactive peptide composition in Tulum cheese. Journal of Dairy Science 104(4): 3832–3852. https://doi.org/10.3168/jds.2020-19494
Parastouei, K., Jabbari, M., Javanmardi, F., Barati, M., Mahmoudi, Y., Khalili-Moghadam, S., Ahmadi, H., Davoodi, S.H., and Mousavi Khaneghah, A. 2023. Estimation of bioactive peptide content of milk from different species using an in silico method. Amino Acids. 55(10): 1261–1278. https://doi.org/10.1007/s00726-022-03152-6
Suetsuna, K., Ukeda, H., and Ochi, H. 2000. Isolation and characterization of free radical scavenging activities peptides derived from casein. The Journal of Nutritional Biochemistry. 11(3): 128–131. https://doi.org/10.1016/S0955-2863(99)00083-2
Tagliazucchi, D., Shamsia, S., and Conte, A. 2016. Release of angiotensin converting enzyme-inhibitory peptides during in vitro gastro-intestinal digestion of camel milk. International Dairy Journal. 56: 119–128. https://doi.org/10.1016/j.idairyj.2016.01.009
Tarapoulouzi, M., Kokkinofta, R., and Theocharis, C.R. 2020. Chemometric analysis combined with FTIR spectroscopy of milk and Halloumi cheese samples according to species’ origin. Journal of the Science of Food and Agriculture. 100(3): 1218–1226. https://doi.org/10.1002/jsfa.10120
Théolier, J., Hammami, R., Fliss, I. and Jean, J.. 2014. Antibacterial and antifungal activity of water-soluble extracts from Mozzarella, Gouda, Swiss, and Cheddar commercial cheeses produced in Canada. Dairy Science & Technology 94: 427–438. https://doi.org/10.1007/s13594-014-0170-9
Toldrá, F., Reig, M. and Mora, L. 2021. Proteomics and peptidomics in food, by-products and bioactive peptides. Journal of Proteomics 241: 104229. https://doi.org/10.1016/j.jprot.2021.104229
Weimann, C., Meisel, H., and Erhardt, G. 2009. Short communication: Bovine κ-casein variants result in different angiotensin I converting enzyme (ACE) inhibitory peptides. Journal of Dairy Science. 92(5): 1885–1888. https://doi.org/10.3168/jds.2008-1671
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