Impact of Simulated Gastrointestinal Digestion on the Biological Activity of an Alcalase Hydrolysate of Orange Seed (Siavaraze, Citrus sinensis) by-Products
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Productions of Orange Seed Proteins Concentrate
2.3. Optimization of Enzymatic Hydrolysis
2.4. Determination of Hydrolysis Degree
2.5. Assay of DPPH Radical Scavenging Activity Measurement
2.6. Assay of Ferric-Reducing Antioxidant Power Measurement
2.7. Assay of the ACE-Inhibitory Activity Measurement
2.8. Assay of α-Amylase-Inhibitory Activity
2.9. Assay of α-Glucosidase-Inhibitory Activity
2.10. SEC Separation of Hydrolyzed Protein
2.11. Isolation of Most Active Fractions Using RP-HPLC
2.12. Simulated in Vitro Gastrointestinal Digestion
2.13. Free Amino Acid Analysis
2.14. Identification of Peptides, Using Mass Spectrometry in Tandem
2.15. Statistical Analysis
3. Results and Discussion
3.1. Antioxidant Activity
3.2. ACE-Inhibitory Activity
3.3. α-Amylase- and α-Glucosidase-Inhibitory Activity
3.4. Fractionation of OSPH by SEC
3.5. Purification of Peptide Fractions by RP-HPLC
3.6. Free Amino Acid Composition
3.7. Influence of Simulated In Vitro Gastrointestinal Digestion on the Bioactivity of Peptides
3.8. Identification of Peptide in Most Active HPLC Fractions by MS/MS
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Amino Acid Name | Concentration (mg/g of OSPH) ± SD |
---|---|
Asp | 0.1276 |
Glu | 0.1434 |
Ser | 0.1087 |
Asn | 0.13 ± 0.0001 |
Gly | 0.0742 |
Gln | 0.1278 ± 0.0001 |
β Ala | 0.0885 ± 0.0001 |
His | 0.1616 ± 0.0001 |
Thr | 0.1172 |
Ala | 0.0871 ± 0.0003 |
Arg | 0.1682 |
Pro | 0.1103 |
Tyr | 0.1665 |
Val | 0.1158 |
Met | 0.1439 |
Ile | 0.1245 |
Leu | 0.1305 |
Phe | 0.153 |
Trp | 0.1637 |
Orn | 0.0812 |
Lys | 0.1417 |
Total | 2.6657 ± 0.001 |
Sequence | Protein | Bioactivity (Sequence Previously Described as Responsible for the Bioactivity) | MW |
---|---|---|---|
ATREQRQQQQRFQTQ | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Inhibition of prolyl endopeptidase (IHPFAQTQ) | 1933.3 |
EQEQEFQGSGD | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | ACE-inhibitory (RKSGDPLGR) | 1253.36 |
HNINDPSGA KHNINDPSGA | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Antimicrobial activities (GYVSGAVIEIPDEILDSAR) | 924.06 1052.51 |
HNINDPSGAD KHNINDPSGAD | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Celiac toxic (GWFGGADWHA) | 1039.16 1166.53 |
HNINDPSGADA | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Kinases inhibitor, (KKALRRQEAADAL) Antioxidative (LLPHHADADY) Antithrombotic, Antimicrobial (DNIADAVACAKRVVRDPQGIR) | 1110.25 |
PSGADAYNPR | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Antioxidative (PRHVFYRWFLSNPRI) | 1052.25 |
QESQQRSSESQSRSQDQHQKVR | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Antimicrobial (TKCFQWQRNMRKVRGPPVSCIKR) | 1167.35 |
QQQQRFQTQ TREQRQQQQRFQTQ | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | ACE inhibitor (QTQSLVYP) | 1047.21 1903.93 |
SSESQSRSQDQHQKVR FQSSKSQDQHQKVR | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Antimicrobial (AGRGKQGGKVRAKAKTRSSRA) ACE inhibitor (KVREGTTY) | 2644.05 1701.84 |
LRHNIDKPSHAD | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Antimicrobial (LLPHHADADY) | 1191.41 |
QDSQQQQSFQSS | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Neuropeptide (FSEFMRQYLVLSMQSSQ) | 1887.18 |
SFQSSKSQDQHQKVR | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | ACE inhibitor (KVREGTTY) | 1862.21 |
SQGGRSQGSQGSDDRRAGN SQGSQGSDDRRAGN | Citrin OS = Citrus sinensis Q39627_CITSI Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | VLKMAGNSFQEN (Celiac Toxic coeliac toxic peptide) YLAGNQ, EVMAGNYLPG, EVMAGNLYPG (ACE inhibitor) | 1918.83 1433.59 |
SQSQGGRSQGSQGSDDRRAGNL GSQGSDDGRGGNL SQGGRSQGSQGSDDGRGGNL SQSQGGRSQGSQGSDDGRGGNL | Citrin OS = Citrus sinensis Q39627_CITSI | Antimicrobial (GLFDAIGNLLGGLGLG) Antiamnestic (PEP inhibitor) (RYDWWPYGNLFGGHTFISP) | 2247.01 1218.51 1918.83 2133.91 |
VFPGCAETFQDSQQQQSFQSSKSQDQHQKVR | Uncharacterized protein OS = Penicillium digitatum tr|K9FZ18|K9FZ18_PEND1 | Antimicrobial (AGRGKQGGKVRAKAKTRSSRAGLQFPV) ACE inhibitor (KVREGTTY) | 3549.70 |
VTDITREGKQQ | Citrin OS = Citrus sinensis tr|Q39627|Q39627_CITSI | Regulating (QQQKQQQQPSSQVS) | 1790.14 |
GTQDHPHDDYAE | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Anti-inflammatory peptide (KGHYAERVG) ACE inhibitor (YAEERYPIL) | 1920.17 |
GTQDHPHDDYAEAK | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Kinases inhibitor (VTCDILSVEAKGVKLG) | 1434.59 |
AGDTHLGGED | Uncharacterized protein OS = Penicillium digitatum tr|K9FZ18|K9FZ18_PEND1 | Antithrombotic (EAGEDCDCGSPANPCCDAATCKLIPGAQCGEGLCCDQCSFIEEGTVCRIARGDDLDDYCNGRSAGCPRNPFH) | 2135.41 |
DQGNRITPS | Uncharacterized protein OS = Penicillium digitatum tr|K9FZ18|K9FZ18_PEND1 | Antimicrobial (GIFSSRKCKTPSKTFKGICTRDSNCDTSCRYEGYPAGDCKGIRRRCMCSKPC) Neuropeptide (NKLASVYALTPSLRVG) TPSPR (Alpha-glucosidase inhibitor) | 2248.59 |
SEGTEPIQSK GQKDAYVGDEAQSK | Protein disulfide-isomerase OS = Citrus limon tr|V9HXG3|V9HXG3_CITLI | Antimicrobial (FVPYNPPRPGQSKPFPSFPGHGPFNPKIQWPYPLPNPGH) | 3585.3 |
DYDKPVQQ | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Coeliac toxic peptide (QQPFVQQQQPFVQQ) | 1219.38 |
GADDSADNKSSNAPTRTY | Uncharacterized protein OS = Citrus clementina tr|V4UJF9|V4UJF9_9ROSI | Erythropoietin receptor agonist peptide (YQRRPAIAINNPYVPRTYYANPAVVRPHAQIPQRQYLPNSHPPTVVRRPNLHPSF) | 1920.2 |
GETGGPHPGYETR | Uncharacterized protein OS = Citrus clementina tr|V4SQX0|V4SQX0_9ROSI | Alpha amylase inhibitory (DETRL) | 2135.44 |
IVPRKAASSEE | Uncharacterized protein OS = Citrus clementina tr|V4S6W0|V4S6W0_9ROSI | Antioxidative (RELEELNVPGEIVESLSSSEESITR) | 1274.56 |
EVHNPATGE | Succinate-semialdehyde dehydrogenase OS = Citrus clementina tr|V4RMN0|V4RMN0_9ROSI | ACE inhibitor (VLSPPFTGE) | 1384.5 |
QDQGPMVK | Uncharacterized protein OS = Citrus unshiu tr|A0A2H5NKL3|A0A2H5NKL3_CITUN | Neuropeptide (SPTISITAPIDVLRKTWEQERARKQMVKNREFLNSLN) Membrane-active peptides (MVKSKIGSWILVLFVAMWSDVGLCKKRPKP) | 1583.78 |
GQMNEPPGAR | ATP synthase subunit beta (Fragment) OS =Poncirus trifoliata tr|Q9THW1|Q9THW1_PONTR | Antimicrobial, (GICACRRRFCPNSERFSGYCRVNGARYVRCCSRR)Opioid, (GICACRRRFCPNSERFSGYCRVNGARYVRCCSRR, YGGFTGARKSARKLANQ, FGGFTGARKSA) Neuropeptide (YGGFLGARKSARKLANQ) Antioxidative (QGAR) | 971.09 |
FYLGGNPQPQLQ | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Neuropeptide (MPRVRSLFQEQEEPEPGMEEAGEMEQKQLQ) coeliac toxic peptide (LQLQPFPQPQLPYPQPQLPYPQPQLPYPQPQPF) | 987.16 |
QQQRFQTQ | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | ACE inhibitor (QTQSLVYP) | 1075.28 |
GSAKESGDKAEQGS | ABC transporter solute-binding protein OS = Streptomyces sp. tr|A0A3L8QSZ7|A0A3L8QSZ7_9ACTN | coeliac toxic peptide, (QQQQPSSQVSFQQPLQQYPLGQGSFRPSQQNPQA, QGSFRPSQQNPQAQ, QYPLGQGSFRPS, LGQGSFRPSQQN) ACE inhibitor, (YQGS) Antioxidative (AWEEREQGSR) | 992.16 |
SQSRSQDQHQKVRQIRE | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Neuropeptide (SENFTPWAYIILNGEAPIIREVHYSPRL) | 1870.1 |
HNIDKPSHAD | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | Antioxidative (LLPHHADADY) | 1495.76 |
QSFQSSKSQDQHQKVR | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | ACE inhibitor (KVREGTTY, KVREGT) | 1357.59 |
QDSQQQQSFQS | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | Antimicrobial (GLLSRLRDFLSDRGRRLGEKIERIGQKIKDLSEFFQS) | 1186.47 |
QPAGKRGEGPPKRAGQVR | REVERSED Uncharacterized protein OS = Curtobacterium sp. RRRRRtr|A0A1E5MMN3|A0A1E5MMN3_9MICO | Celiac toxic (VQGQGHQPPQQPAQL, VQGQGIIQPQQPAQL) | 953.1 |
QKVESEAGVT | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | Antioxidative (DSGVT) | 902.15 |
VIGTVLAFALIASAESLF | Sulfate transporter OS = Streptomyces sp. tr|A0A3L8QBZ9|A0A3L8QBZ9_9ACTN | Antimicrobial (SLFSLIKAGAKFLGKNLLKQGAQYAACKVSKECG, SLFSLIKAGAKFLGKNLLKQGACYAACKASKQC) Neuropeptide (MPRVRSLFQEQEEPEPGMEEAGEMEQKQLQ) | 1056.3 |
TAAEEVLQKAEAAP | CHAD domain-containing protein OS = Methylobacterium mesophilicum tr|M7YUM6|M7YUM6_9RHIZ | Antimicrobial (WNPFKELERAGQRVRDAVISAAPAVATVGQAAAIARG) | 1361.71 |
SAEKGNLYQN | Uncharacterized protein OS = Citrus clementina tr|V4S993|V4S993_9ROSI | Regulating (EPFYQNVPD) | 1063.26 |
NALEPR | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | Peptide stimulating insulin release Antioxidative (GFGSFLGKALKA ALKIGANALGGSPQQ) | 1350.55 |
QNPANPVTLAQAIEGEPK | DNA-directed DNA polymerase OS = Methylobacterium mesophilicum tr|M7Y0I8|M7Y0I8_9RHIZ | ACE Inhibitor (EPKAIP, HSGIQSEPKAIP)Antioxidative (APIRMWYMYRKLTDMEPKPVA) | 2110.53 |
SSDTIDNVKAK | Polyubiquitin OS = Avena fatua UBIQP_AVEFA | Antimicrobial (GCASRCKAKCAGRRCJGWASASFRGRCYCKCFRC) | 1133.32 |
QSDVTTTS | Transcription factor MYB21 OS = Arabidopsis thaliana MYB21_ARATH | Antimicrobial (QLKTADLPAGRDETTSFVLV) Antioxidative (PIAAEVYEHTEGSTTSY) | 1918.29 |
DESTGTIGKR | Fructose-bisphosphate aldolase, cytoplasmic isozyme 1 OS = Pisum sativum ALF1_PEA | Neuropeptide (KRQHPGKR) | 1310.46 |
SAPKKEKSQGFLQ | Type II inositol polyphosphate 5-phosphatase 14 OS = Arabidopsis thaliana IP5PE_ARATH | ACE Inhibitor, DPP IV inhibitor (TPVVVPPFLQP, FLQP) | 1219.35 |
FASTRRRQCPQ | Lignin-forming anionic peroxidase OS = Nicotiana sylvestris PERX_NICSY | Antimicrobial (CPQLQPQNPSQQQPQEQG) | 1889.41 |
GSGAKPGTKPTKCT | Chaperone protein dnaJ A6, chloroplastic OS = Arabidopsis thaliana DNJA6_ARATH | Antimicrobial (RSVCRQIKICRRRGGCYYKCTNRPY) | 1047.27 |
TNADKATTVS | Soluble starch synthase 3, chloroplastic/amyloplastic OS = Solanum tuberosum SSY3_SOLTU | Antimicrobial (GILDTLKQFAKGVGKDLVKGAAQGVLSTVSCKLAKTC, GIFSSRKCKTVSKTFRGICTRNANC) | 1822.44 |
WTAEHSVNAALGQFE | Pyruvate, phosphate dikinase regulatory protein, chloroplastic OS = Zea mays PDRP1_MAIZE | Celiac Toxic (QQLPQFEEIRNL, GSVQPQQQLPQFEIR) | 1427.76 |
GSEEPNVEEDS | FHA domain-containing protein DDL OS = Arabidopsis thaliana DDL_ARATH | Antimicrobial (YPGPQAKEDSEGPSQGPASREK) | 1123.33 |
Sequence | Protein | Bioactivity | MW |
---|---|---|---|
SQGSQGSDDGRGGNL | Citrin OS = Citrus sinensis Q39627_CITSI | PEP inhibitor (Antiamnestic), (RYDWWPYGNLFGGHTFISP) Antibacterial, (LLPIVGNLLKSLL, GLLDMVTGLLGNLG, GLFDAIGNLLGGLGLG)Antioxidative, (QLGNLGV)ACE inhibitor (EVMAGNLYPG) | 1219.38 |
GSQGSDDGRGGNL | Citrin OS = Citrus sinensis Q39627_CITSI | PEP inhibitor (Antiamnestic), (RYDWWPYGNLFGGHTFISP)Antibacterial, (LLPIVGNLLKSLL, GLLDMVTGLLGNLG, GLFDAIGNLLGGLGLG) Antioxidative, (QLGNLGV)ACE inhibitor (EVMAGNLYPG) | 1434.62 |
GSQGSDDGRGGNL | Citrin OS = Citrus sinensis Q39627_CITSI | PEP inhibitor (Antiamnestic), (RYDWWPYGNLFGGHTFISP)Antibacterial, (LLPIVGNLLKSLL, GLLDMVTGLLGNLG, GLFDAIGNLLGGLGLG)Antioxidative, (QLGNLGV)ACE inhibitor (EVMAGNLYPG) | 1219.38 |
SQGSQGSDDRRAGN | Uncharacterized protein OS = Citrus clementina tr|V4U2L8|V4U2L8_9ROSI | Celiac Toxic, (VLKMAGNSFQEN) ACE inhibitor (YLAGNQ, EVMAGNYLPG, EVMAGNLYPG) | 1434.59 |
IDLPQPQ | Serine/threonine-protein kinase TOR OS = Arabidopsis TOR_ARATH | ACE inhibitor, (QPQPLIYP) Potential coeliac toxic peptide, (PQNPSQQQPQEQVP) Celiac Toxic, (SQPQAFP) Antibacterial (PYPQPQPF) | 1219.38 |
RLAIEEAISITTTLVAQY | Protein RETICULATA-RELATED 5, chloroplastic OS = Arabidopsis thaliana RER5_ARATH | Antibacterial, (NLLKQGAQYAACKVSKECG) ACE inhibitor (VLAQYK) | 1434.59 |
SSCPVINVD | Uncharacterized GPI-anchored protein At1g61900 OS = Arabidopsis thaliana UGPI6_ARATH | Antibacterial, (CSCRTSSCRFGERL) Natriuretic (RSSCFGGRIDRIGAC) | 810.02 |
RHSWMMN | Phosphoenolpyruvate carboxylase kinase 2 OS = Arabidopsis thaliana PPCK2_ARATH | Antibacterial, (VPMPKGRSSRGRRHS) Antioxidative (RHS) | 1992.57 |
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Mazloomi, S.N.; Mora, L.; Aristoy, M.-C.; Mahoonak, A.S.; Ghorbani, M.; Houshmand, G.; Toldrá, F. Impact of Simulated Gastrointestinal Digestion on the Biological Activity of an Alcalase Hydrolysate of Orange Seed (Siavaraze, Citrus sinensis) by-Products. Foods 2020, 9, 1217. https://doi.org/10.3390/foods9091217
Mazloomi SN, Mora L, Aristoy M-C, Mahoonak AS, Ghorbani M, Houshmand G, Toldrá F. Impact of Simulated Gastrointestinal Digestion on the Biological Activity of an Alcalase Hydrolysate of Orange Seed (Siavaraze, Citrus sinensis) by-Products. Foods. 2020; 9(9):1217. https://doi.org/10.3390/foods9091217
Chicago/Turabian StyleMazloomi, Seyadeh Narges, Leticia Mora, M-Concepción Aristoy, Alireza Sadeghi Mahoonak, Mohammad Ghorbani, Gholamreza Houshmand, and Fidel Toldrá. 2020. "Impact of Simulated Gastrointestinal Digestion on the Biological Activity of an Alcalase Hydrolysate of Orange Seed (Siavaraze, Citrus sinensis) by-Products" Foods 9, no. 9: 1217. https://doi.org/10.3390/foods9091217