Abstract
Camel milk has both nutritional value and therapeutic effects due to its bioactive components, including proteins and peptides. This study characterize endogenous peptide and potential bioactivity in both Dromedary and Bactrian camel by peptidomics techniques. In total, 622 parent protein from 8393 peptides were identified from camel milk, of which 208 proteins from Dromedary and 464 proteins from Bactrian. After filtration, 4464 endogenous peptides were quantified with 459 peptides were common in two breeds. Finally, 170 peptides were significantly different between Dromedary and Bactrian camel milk, which derived from 27 proteins, including osteopontin, lactoperoxidase up-regulated in Dromedary camel milk and butyophilin subfamily member A1, perilicin, fatty acids synthase up-regulated in Bactrian camel milk. Peptide ranker showed that 14.6% and 15.7% quantified peptides from Dromedary and Bactrian has bioactivity, which were dominated by dipeptidyl peptidase IV inhibitor (39.93%), followed by ACE inhibitor (34.85%) and anti-oxidative activity (8.69%). In sum, although Dromedary and Bactrian camel milk had significantly differences in qualitative and quantitative level of endogenous peptides, they had similarity in bioactivity including anti-diabetic, anti-hypertensive, and anti-oxidative function. The result of this study suggest that endogenous peptides may also contribute to the therapeutic benefits of camel milk.
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References
Park YW, Haenlein GFW (2013) Milk and dairy products in human nutrition: production, composition and health: chapter 26 camel milk. Wiley, Hoboken, pp 578–593
Farah MJ (1996) Is face recognition “special”? Evidence from neuropsychology. Behav Brain Res 76(1–2):181–189. https://doi.org/10.1016/0166-4328(95)00198-0
Maryniak NZ, Hansen EB (2018) Comparison of the allergenicity and immunogenicity of camel and cow’s milk—a study in brown norway rats. Nutrients. https://doi.org/10.3390/nu10121903
Ayyash M, Al-Dhaheri AS, Al Mahadin S, Kizhakkayil J, Abushelaibi A (2018) In vitro investigation of anticancer, antihypertensive, antidiabetic, and antioxidant activities of camel milk fermented with camel milk probiotic: a comparative study with fermented bovine milk. J Dairy Sci 101(2):900–911. https://doi.org/10.3168/jds.2017-13400
Ayyash M, Al-Nuaimi AK, Al-Mahadin S, Liu SQ (2018) In vitro investigation of anticancer and ACE-inhibiting activity, alpha-amylase and alpha-glucosidase inhibition, and antioxidant activity of camel milk fermented with camel milk probiotic: a comparative study with fermented bovine milk. Food Chem 239:588–597. https://doi.org/10.1016/j.foodchem.2017.06.149
el Agamy EI, Ruppanner R, Ismail A, Champagne CP, Assaf R (1992) Antibacterial and antiviral activity of camel milk protective proteins. J Dairy Res 59(2):169–175. https://doi.org/10.1017/s0022029900030417
Mudgil P, Kamal H, Yuen GC, Maqsood S (2018) Characterization and identification of novel antidiabetic and anti-obesity peptides from camel milk protein hydrolysates. Food Chem 259:46–54. https://doi.org/10.1016/j.foodchem.2018.03.082
Mirmiran P, Ejtahed HS, Angoorani P, Eslami F, Azizi F (2017) Camel milk has beneficial effects on diabetes mellitus: a systematic review. Int J Endocrinol Metab 15(2):e42150
Ayoub MA, Palakkott AR, Ashraf A, Iratni R (2018) The molecular basis of the anti-diabetic properties of camel milk. Diabetes Res Clin Pract 146:305–312. https://doi.org/10.1016/j.diabres.2018.11.006
Conesa C, Sánchez L, Rota C, Pérez MD, Calvo M, Farnaud S, Evans RW (2008) Isolation of lactoferrin from milk of different species: calorimetric and antimicrobial studies. Comp Biochem Physiol B Biochem Mol Biol 150(1):131–139. https://doi.org/10.1016/j.cbpb.2008.02.005
Almehdar HA, El-Baky NA, Alhaider AA, Almuhaideb SA, Alhaider AA, Albiheyri RS, Uversky VN, Redwan EM (2020) Bacteriostatic and bactericidal activities of camel lactoferrins against Salmonella enterica serovar typhi. Probiotics Antimicrob Proteins 12(1):18–31. https://doi.org/10.1007/s12602-019-9520-5
Ebaid H, Abdel-Salam B, Hassan I, Al-Tamimi J, Metwalli A, Alhazza I (2015) Camel milk peptide improves wound healing in diabetic rats by orchestrating the redox status and immune response. Lipids Health Dis 14:132. https://doi.org/10.1186/s12944-015-0136-9
Nongonierma AB, Cadamuro C, Le Gouic A, Mudgil P, Maqsood S, FitzGerald RJ (2019) Dipeptidyl peptidase IV (DPP-IV) inhibitory properties of a camel whey protein enriched hydrolysate preparation. Food Chem 279:70–79. https://doi.org/10.1016/j.foodchem.2018.11.142
Banting FG, Best CH, Collip JB, Campbell WR, Fletcher AA (1922) Pancreatic extracts in the treatment of diabetes mellitus. Can Med Assoc J 12:141–146
Lau JL, Dunn MK (2018) Therapeutic peptides: historical perspectives, current development trends, and future directions. Bioorg Med Chem 26(10):2700–2707. https://doi.org/10.1016/j.bmc.2017.06.052
Zhang LN, Boeren S, Smits M, van Hooijdonk T, Vervoort J, Hettinga K (2016) Proteomic study on the stability of proteins in bovine, camel, and caprine milk sera after processing. Food Res Int 82:104–111. https://doi.org/10.1016/j.foodres.2016.01.023
Yang Y, Zheng N, Wang W, Zhao X, Zhang Y, Han R, Ma L, Zhao S, Li S, Guo T, Zang C, Wang J (2016) N-glycosylation proteomic characterization and cross-species comparison of milk fat globule membrane proteins from mammals. Proteomics 16(21):2792–2800. https://doi.org/10.1002/pmic.201500361
Hinz K, O’Connor PM, Huppertz T, Ross RP, Kelly AL (2012) Comparison of the principal proteins in bovine, caprine, buffalo, equine and camel milk. J Dairy Res 79(2):185–191. https://doi.org/10.1017/s0022029912000015
Ryskaliyeva A, Henry C, Miranda G, Faye B, Konuspayeva G, Martin P (2018) Combining different proteomic approaches to resolve complexity of the milk protein fraction of dromedary, Bactrian camels and hybrids, from different regions of Kazakhstan. PLoS One 13(5):e0197026. https://doi.org/10.1371/journal.pone.0197026
Dingess KA, de Waard M, Boeren S, Vervoort J, Lambers TT, van Goudoever JB, Hettinga K (2017) Human milk peptides differentiate between the preterm and term infant and across varying lactational stages. Food Funct 8(10):3769–3782. https://doi.org/10.1039/c7fo00539c
Beverly RL, Underwood MA, Dallas DC (2019) Peptidomics analysis of milk protein-derived peptides released over time in the preterm infant stomach. J Proteome Res 18(3):912–922. https://doi.org/10.1021/acs.jproteome.8b00604
Dallas D, Nielsen SD (2018) Milk peptidomics to identify functional peptides and for quality control of dairy products. Methods Mol Biol (Clifton, NJ) 1719:223–240. https://doi.org/10.1007/978-1-4939-7537-2_15
Giacometti J, Buretić-Tomljanović A (2017) Peptidomics as a tool for characterizing bioactive milk peptides. Food Chem 230:91–98. https://doi.org/10.1016/j.foodchem.2017.03.016
Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98(9):5116–5121. https://doi.org/10.1073/pnas.091062498
Mooney C, Haslam NJ, Pollastri G, Shields DC (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
Minkiewicz P, Iwaniak A, Darewicz M (2019) BIOPEP-UWM database of bioactive peptides: current opportunities. Int J Mol Sci. https://doi.org/10.3390/ijms20235978
Dallas DC, Guerrero A, Khaldi N, Borghese R, Bhandari A, Underwood MA, Lebrilla CB, German JB, Barile D (2014) A peptidomic analysis of human milk digestion in the infant stomach reveals protein-specific degradation patterns. J Nutr 144(6):815–820. https://doi.org/10.3945/jn.113.185793
Ismail B, Nielsen SS (2010) Invited review: plasmin protease in milk: current knowledge and relevance to dairy industry. J Dairy Sci 93(11):4999–5009. https://doi.org/10.3168/jds.2010-3122
Caessens PW, Visser S, Gruppen H, Voragen AG (1999) beta-lactoglobulin hydrolysis. 1. Peptide composition and functional properties of hydrolysates obtained by the action of plasmin, trypsin, and Staphylococcus aureus V8 protease. J Agric Food Chem 47(8):2973–2979. https://doi.org/10.1021/jf981229p
Grufferty MB, Fox PF (1988) Milk alkaline proteinase. J Dairy Res 55(4):609–630. https://doi.org/10.1017/s0022029900033409
Kussendrager KD, van Hooijdonk AC (2000) Lactoperoxidase: physico-chemical properties, occurrence, mechanism of action and applications. Br J Nutr 84(Suppl 1):S19-25. https://doi.org/10.1017/s0007114500002208
Zou Z, Bauland J, Hewavitharana AK, Al-Shehri SS, Duley JA, Cowley DM, Koorts P, Shaw PN, Bansal N (2021) A sensitive, high-throughput fluorescent method for the determination of lactoperoxidase activities in milk and comparison in human, bovine, goat and camel milk. Food Chem 339:128090. https://doi.org/10.1016/j.foodchem.2020.128090
Icer MA, Gezmen-Karadag M (2018) The multiple functions and mechanisms of osteopontin. Clin Biochem 59:17–24. https://doi.org/10.1016/j.clinbiochem.2018.07.003
Nomiyama T, Perez-Tilve D, Ogawa D, Gizard F, Zhao Y, Heywood EB, Jones KL, Kawamori R, Cassis LA, Tschöp MH, Bruemmer D (2007) Osteopontin mediates obesity-induced adipose tissue macrophage infiltration and insulin resistance in mice. J Clin Investig 117(10):2877–2888. https://doi.org/10.1172/jci31986
Jayakumar A, Tai MH, Huang WY, Al-Feel W, Hsu M, Abu-Elheiga L, Chirala SS, Wakil SJ (1995) Human fatty acid synthase: properties and molecular cloning. Proc Natl Acad Sci U S A 92(19):8695–8699. https://doi.org/10.1073/pnas.92.19.8695
Suburu J, Shi L, Wu J, Wang S, Samuel M, Thomas MJ, Kock ND, Yang G, Kridel S, Chen YQ (2014) Fatty acid synthase is required for mammary gland development and milk production during lactation. Am J Physiol Endocrinol Metab 306(10):E1132-1143. https://doi.org/10.1152/ajpendo.00514.2013
Müller TD, Finan B, Bloom SR, D’Alessio D, Drucker DJ, Flatt PR, Fritsche A, Gribble F, Grill HJ, Habener JF, Holst JJ, Langhans W, Meier JJ, Nauck MA, Perez-Tilve D, Pocai A, Reimann F, Sandoval DA, Schwartz TW, Seeley RJ, Stemmer K, Tang-Christensen M, Woods SC, DiMarchi RD, Tschöp MH (2019) Glucagon-like peptide 1 (GLP-1). Mol Metab 30:72–130. https://doi.org/10.1016/j.molmet.2019.09.010
Musoev A, Numonov S, You Z, Gao H (2019) Discovery of novel DPP-IV inhibitors as potential candidates for the treatment of type 2 diabetes mellitus predicted by 3D QSAR pharmacophore models, molecular docking and de novo evolution. Molecules (Basel, Switzerland). https://doi.org/10.3390/molecules24162870
Bischoff H (1995) The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin Investig Med 18(4):303–311
Hedrington MS, Davis SN (2019) Considerations when using alpha-glucosidase inhibitors in the treatment of type 2 diabetes. Expert Opin Pharmacother 20(18):2229–2235. https://doi.org/10.1080/14656566.2019.1672660
Singh AK, Jatwa R, Purohit A, Ram H (2017) Synthetic and phytocompounds based dipeptidyl peptidase-IV (DPP-IV) inhibitors for therapeutics of diabetes. J Asian Nat Prod Res 19(10):1036–1045. https://doi.org/10.1080/10286020.2017.1307183
Uchida M, Ohshiba Y, Mogami O (2011) Novel dipeptidyl peptidase-4-inhibiting peptide derived from β-lactoglobulin. J Pharmacol Sci 117(1):63–66. https://doi.org/10.1254/jphs.11089sc
Nongonierma AB, FitzGerald RJ (2013) Dipeptidyl peptidase IV inhibitory and antioxidative properties of milk protein-derived dipeptides and hydrolysates. Peptides 39:157–163. https://doi.org/10.1016/j.peptides.2012.11.016
Kehinde BA, Sharma P (2020) Recently isolated antidiabetic hydrolysates and peptides from multiple food sources: a review. Crit Rev Food Sci Nutr 60(2):322–340. https://doi.org/10.1080/10408398.2018.1528206
Lin L, Lv S, Li B (2012) Angiotensin-I-converting enzyme (ACE) inhibitory and antihypertensive properties of squid skin gelatin hydrolysates. Food Chem 131:2225–2230
Rai AK, Sanjukta S, Jeyaram K (2017) Production of angiotensin I converting enzyme inhibitory (ACE-I) peptides during milk fermentation and their role in reducing hypertension. Crit Rev Food Sci Nutr 57(13):2789–2800. https://doi.org/10.1080/10408398.2015.1068736
Quirós A, del Mar CM, Ramos M, Amigo L, Recio I (2009) Stability to gastrointestinal enzymes and structure-activity relationship of beta-casein-peptides with antihypertensive properties. Peptides 30(10):1848–1853. https://doi.org/10.1016/j.peptides.2009.06.031
Quirós A, Hernández-Ledesma B, Ramos M, Amigo L, Recio I (2005) Angiotensin-converting enzyme inhibitory activity of peptides derived from caprine kefir. J Dairy Sci 88(10):3480–3487. https://doi.org/10.3168/jds.S0022-0302(05)73032-0
Ayyash M, Al-Nuaimi AK, Al-Mahadin S, Liu SQ (2018) In vitro investigation of anticancer and ACE-inhibiting activity, α-amylase and α-glucosidase inhibition, and antioxidant activity of camel milk fermented with camel milk probiotic: a comparative study with fermented bovine milk. Food Chem 239:588–597. https://doi.org/10.1016/j.foodchem.2017.06.149
Salami M, Moosavi-Movahedi AA, Moosavi-Movahedi F, Ehsani MR, Yousefi R, Farhadi M, Niasari-Naslaji A, Saboury AA, Chobert JM, Haertlé T (2011) Biological activity of camel milk casein following enzymatic digestion. J Dairy Res 78(4):471–478. https://doi.org/10.1017/s0022029911000628
Laudisio A, Giovannini S, Finamore P, Gemma A, Bernabei R, Incalzi RA, Zuccalà G (2018) Use of ACE-inhibitors and quality of life in an older population. J Nutr Health Aging 22(10):1162–1166. https://doi.org/10.1007/s12603-018-1135-0
Maritim AC, Sanders RA, Watkins JB 3rd (2003) Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 17(1):24–38. https://doi.org/10.1002/jbt.10058
Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet (London, England) 344(8924):721–724. https://doi.org/10.1016/s0140-6736(94)92211-x
Sah BNP, Vasiljevic T, McKechnie S, Donkor ON (2018) Antioxidative and antibacterial peptides derived from bovine milk proteins. Crit Rev Food Sci Nutr 58(5):726–740. https://doi.org/10.1080/10408398.2016.1217825
Ibrahim HR, Isono H, Miyata T (2018) Potential antioxidant bioactive peptides from camel milk proteins. Anim Nutr (Zhongguo xu mu shou yi xue hui) 4(3):273–280. https://doi.org/10.1016/j.aninu.2018.05.004
Sarmadi BH, Ismail A (2010) Antioxidative peptides from food proteins: a review. Peptides 31(10):1949–1956. https://doi.org/10.1016/j.peptides.2010.06.020
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31801463), Natural Science Foundation of Jiangsu Province (BK20180612), Innovation and Exploration Project of State Key Laboratory of Food Science and Technology (SKLF-ZZA-202104).
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LZ: Conceptualization, formal analysis, investigation, methodology, writing—original draft, funding acquisition. BH: Data curation, methodology. BL, YN, NB: Sample collection, review & editing. PZ: Supervision, writing—review & editing.
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217_2021_3952_MOESM1_ESM.tif
Figure S1 The functional distribution of potential bioactive peptides from both Dromedary and Bactrian camel milk (A) and The differences in functional distribution of potential bioactive peptides between Dromedary and Bactrian camel milk (B) (TIF 930 KB)
217_2021_3952_MOESM2_ESM.xlsx
Table S1 Identified parent proteins of Dromedary camel milk. Table S2 Identified parent proteins of Bactrian camel milk. Table S3 Identified peptides from Dromedary camel milk. Table S4 Identified peptides from Bactrian camel milk. Table S5 Quantified peptides from Dromedary camel milk. Table S6 Quantified peptides from Bactrian camel milk. Table S7 Significantly different proteins between Dromedary and Bactrian camel milk. Table S8 Potential bioactive score of significantly different peptides using peptide ranker. Table S9 The bioactivity of those potential bioactive peptides from both Dromedary and Bactrian camel using BioPEP (XLSX 1734 KB)
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Zhang, L., Han, B., Luo, B. et al. Characterization of endogenous peptides from Dromedary and Bactrian camel milk. Eur Food Res Technol 248, 1149–1160 (2022). https://doi.org/10.1007/s00217-021-03952-2
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DOI: https://doi.org/10.1007/s00217-021-03952-2