Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps
Abstract
:1. Introduction
2. Results and Discussion
2.1. Major Venom Components
2.2. Minor Venom Components
2.3. Quantification of Venom Components
3. Conclusions
4. Materials and Methods
4.1. Venom Extraction and Ethics Statement
4.2. Tryptic Digestion of Crude Venom
4.3. Chromatography and Mass Spectrometry
4.3.1. One-Dimensional Sodium Dodecyl Sulfate Polyacrylamide Gel Electrophoresis (SDS-PAGE)
4.3.2. Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS) Analysis of Excised Gel Bands
4.3.3. Electrospray Mass Spectrometry of Digested Venom
4.3.4. MALDI Mass Spectrometry of Digested Venom
4.4. Data Analysis of Digested Venom
4.5. De Novo Sequencing and Similarity-Driven Analysis of Digested Venom
4.6. Protein Quantitation
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Protein Family | Protein | Accession No. | Species | Number of Peptides Matched |
---|---|---|---|---|
3FTx | Non-conventional three finger toxin isoform 1 | 294961050 | Bungarus flaviceps | 6 |
3FTx | Non-conventional three finger toxin isoform 6 | 294961060 | Bungarus flaviceps | 5 |
3FTx | Short-chain three finger toxin isoform 4 | 294961042 | Bungarus flaviceps | 4 |
3FTx | Short-chain three finger toxin isoform 7 | 294961048 | Bungarus flaviceps | 9 |
3FTx | Short-chain three finger toxin isoform 6 | 294961046 | Bungarus flaviceps | 7 |
3FTx | Short-chain three finger toxin isoform 1 | 294961036 | Bungarus flaviceps | 2 |
3FTx | κ-bungarotoxin | 809178 | Bungarus multicinctus | 1 |
3FTx | Short-chain three finger toxin isoform 3 | 294961040 | Bungarus flaviceps | 1 |
3FTx | κ-flavitoxin | 128938 | Bungarus flaviceps | 9 |
3FTx | Muscarinic toxin-like protein | 294961066 | Bungarus flaviceps | 9 |
Serine protease inhibitor | β-bungarotoxin B chain precursor | 31745053 | Bungarus flaviceps | 7 |
Serine protease inhibitor | Kunitz-type serine proteinase inhibitor isoform 5 | 294961076 | Bungarus flaviceps | 8 |
Serine protease inhibitor | Kunitz-type serine proteinase inhibitor isoform 1 | 294961068 | Bungarus flaviceps | 4 |
Acetylcholinesterase | Acetylcholinesterase | 1389604 | Bungarus flaviceps | 20 |
Acetylcholinesterase | Acetylcholinesterase DEN | 476538388 | Denisoni adevisi | 4 |
PLA2 | β-bungarotoxin A2 chain precursor | 31745049 | Bungarus flaviceps | 16 |
PLA2 | β-bungarotoxin A1 chain precursor | 31745051 | Bungarus flaviceps | 3 |
PLA2 | Phospholipase A2II precursor | 31745057 | Bungarus flaviceps | 21 |
PLA2 | Phospholipase A2 | 263083 | Bungarus fasciatus | 8 |
PLA2 | Phospholipase A2 precursor | 31745055 | Bungarus flaviceps | 23 |
PLA2 | Phospholipase A2 isoform 3 | 294961092 | Bungarus flaviceps | 5 |
PLA2 | Phospholipase A2Kbf-III | 110559306 | Bungarus fasciatus | 4 |
PLA2 | Phospholipase A2 isozyme 1 | 24638470 | Laticauda semifasciata | 1 |
PLA2 | Phospholipase A2 | 29422777 | Bungarus candidus | 2 |
PLA2 | Phospholipase A2 | 5924345 | Austrelaps superbus | 3 |
PLA2 | Phospholipase A2 | 152032644 | Bungarus fasciatus | 3 |
PLA2 | Phospholipase A2 precursor | 156257593 | Bungarus fasciatus | 1 |
PLA2 | Phospholipase A2 | 48425218 | Bungarus caeruleus | 1 |
PLA2 | Phospholipase A2 | 129428 | Laticauda colubrina | 1 |
VEGF | Hypothetical protein L345_04144 | 565318860 | Ophiophagus hannah | 4 |
Nucleotidase | Ecto-5′-nucleotidase 1 | 537444870 | Micrurus fulvius | 11 |
Snaclec | Snaclec factor IX/factor X-binding protein B chain | 398488 | Bothrops jararaca | 1 |
Snaclec | C-type lectin-like protein 1 | 13876735 | Bungarus fasciatus | 3 |
Vespryn | Ohanin precursor | 70907886 | Ophiophagus hannah | 2 |
Vespryn | Vespryn22 | 336042222 | Drysdalia coronoides | 1 |
Phosphodiesterase | Phosphodiesterase 1 | 537444868 | Micrurus fulvius | 20 |
Phosphodiesterase | Phosphodiesterase 1 | 338855302 | Crotalus adamanteus | 1 |
Hyaluronidase | Hyaluronidase | 113203681 | Bitis arietans | 4 |
VNGF | Venom nerve growth factor precursor | 266299 | Bungarus multicinctus | 4 |
LAAO | L-amino-acid oxidase | 126035653 | Bungarus fasciatus | 5 |
LAAO | L-amino acid oxidase | 126035649 | Bungarus multicinctus | 2 |
LAAO | L-amino-acid oxidase | 426205815 | Crotalus durissus cumanensis | 2 |
PLB | Phospholipase B | 537444729 | Micrurus fulvius | 3 |
CRISP | Cysteine-rich seceretory protein | 190195343 | Bungarus candidus | 3 |
CRISP | Opharin precursor | 225547744 | Ophiophagus hannah | 2 |
SVMP | Scutatease-1 (PIII) | 145982766 | Notechis scutatus | 8 |
SVMP | Metalloproteinase (PIII) | 126035640 | Bungarus multicinctus | 6 |
SVMP | Metalloproteinase MTP9 (PIII) | 336042214 | Drysdalia coronoides | 4 |
SVMP | Metalloproteinase (PIII) | 126035635 | Bungarus fasciatus | 4 |
SVMP | P-III | 633276509 | Micropechis ikaheka | 4 |
SVMP | MTP4 (PIII) | 537463069 | Micrurus fulvius | 3 |
SVMP | Atragin precursor(PIII) | 224482347 | Naja atra | 3 |
SVMP | Metalloproteinase isoform 3 (PIII) | 109254964 | Sistrurus catenatus edwardsi | 2 |
SVMP | SVMP-Hop-14, partial (PIII) | 476539284 | Hoplocephalus bungaroides | 2 |
SVMP | SVMP-Hop-46, partial(PIII) | 476539268 | Hoplocephalus bungaroides | 2 |
SVMP | SVMP 1 | 537444726 | Micrurus fulvius | 2 |
SVMP | Metalloproteinase (PII) | 82466485 | Bothrops asper | 1 |
SVMP | Fur-1, partial (PI) | 476538467 | Furinaor nata | 1 |
SVMP | jararhagin (PIII) | 62468 | Bothrops jararaca | 1 |
SVMP | Metalloproteinase (PIII) | 241995585 | Philodrya solfersii | 1 |
SVMP | Leucurolysin-B (PIII) | 223635807 | Bothrops leucurus | 1 |
SVMP | Ech-32 (PIII) | 476538400 | Echiopsis curta | 1 |
SVMP | Cobrin precursor(PIII) | 6006966 | Naja naja | 1 |
SVMP | Metalloproteinase (PII) | 297594122 | Echis pyramidum leakeyi | 1 |
SVMP | CohPH-3 (PII) | 522802426 | Crotalus oreganus helleri | 1 |
SVSP | Serine proteinase isoform 2 | 109254940 | Sistrurus catenatus edwardsi | 2 |
SVSP | SVSP 11 | 387014258 | Crotalus adamanteus | 1 |
Natriuretic peptide | Natriuretic peptide | 294961100 | Bungarus flaviceps | 1 |
Complement-depleting factor | Complement-depleting factor | 126035660 | Bungarus fasciatus | 1 |
Protein Family | Protein | Accession No. | Species | Database Sequence | Alignment Score | De Novo Sequence | ALC (%) | m/z | ppm to De Novo Derived Sequence |
---|---|---|---|---|---|---|---|---|---|
3FTx | Muscarinic toxin-like protein | 117606606 | Ophiophagus hannah | TFTCPELTPN | 64 | CGTYTCPELTPDRR | 52 | 575.9354 | 13.5 |
PLA2 | Phospholipase A2 | 9453880 | Laticauda semifasciata | VHDDCYGEAEK | 87 | VHDDCYGEAEK | 58 | 563.5938 | −1.8 |
LVQFTYLIQCANKGSRASYHYADYGCY | 84 | RLAQFACLLQCADEEVGVDLHYADYGCYNCK | 46 | 906.911 | 5.8 | ||||
Nucleotidase | Snake venom 5′-nucleotidase | 752779244 | Boiga irregularis | VVQFMNSLR | 69 | EAAAVVQFMNSLR | 51 | 479.2537 | 7.1 |
HGQGTGELLQVSGIKVVYDLS | 99 | HPQGTGELLQVSLGKVVYDLSKGAPVNK | 52 | 587.7292 | 4.2 | ||||
Snaclec | C-type lectin 2 | 537444936 | Micrurus fulvius | DHHCPSDWYSFDKFCYKFI | 105 | DNHCNADWSSFDKFCYQFLR | 52 | 653.2799 | 2 |
Vespryn | Vespryn 23 | 336042224 | Drysdalia coronoides | HFFEVK | 49 | HFFEVK | 60 | 403.7129 | −1.1 |
IVVFLDYSEGK | 68 | LVVFLDYKEGK | 60 | 437.5828 | −1.2 | ||||
IVVFLDY | 51 | LVVFLDYK | 71 | 498.791 | −1.7 | ||||
Phosphodiesterase | Phosphodiesterase | 675402318 | Protobothrops elegans | FYTLYIEEPDTTGHK | 106 | QFLPVFFTLYLEEPDTTGHK | 57 | 592.0533 | 7 |
RPDFYTLYIEEPDTTGHK | 130 | RPDFFTLYLEEPDTTGHK | 59 | 542.2665 | −2.6 | ||||
VNGF | Venom nerve growth factor | 335892638 | Bungarus fasciatus | YFFETK | 51 | AGYFFETK | 51 | 481.7344 | −0.2 |
LAAO | L-amino acid oxidase | 126035653 | Bungarus fasciatus | SYVTADYVIVCAT | 76 | LTSYVTADYLLVSATMGR | 51 | 981.0001 | −6.1 |
TADYVIVCATSR | 80 | TLSAAHTADYLLVCATSR | 52 | 650.6723 | 14.1 | ||||
LAAO | L-amino acid oxidase | 401021343 | Lachesis muta | LSAAYVLAEAGHQVTVLEASER | 105 | LSAAYVLSEKHQVTVLQASER | 52 | 583.3127 | −2.5 |
LAAO | L-amino acid oxidase | 537444909 | Micrurus fulvius | SAAYVLAEAGHKVTLLE | 103 | QLLVVQGMQDSAAYVLSEAGHKVTVLESNNK | 50 | 669.7629 | 20.9 |
AGMAGLSAAYVLAEAGHK | 116 | VKHHSVPPRVAGMAGLSAAYVLSEAGHK | 52 | 574.7169 | 10.5 | ||||
LAAO | L-amino acid oxidase | 3426324 | Crotalus adamanteus | RVVIVGAGMAGLSAAYVL | 104 | RLALVGAGMAGLSAAYVLNPSSPGVLSQLLWSR | 53 | 671.7708 | −3.1 |
LAAO | L-amino acid oxidase 1a | 537444909 | Micrurus fulvius | GMAGLSAAYVLAEAGHK | 110 | RTPVVKGMAGLSAAYVLSEAGHK | 48 | 590.3197 | −1.2 |
Phospholipase B | Phospholipase B | 537444729 | Micrurus fulvius | KGYWPSYNIPFHK | 94 | KPYWPSYNLPFHK | 56 | 559.6232 | −1.9 |
CRISP | CRISP precursor | 158262802 | Austrelaps superbus | VDKHNALR | 58 | VAAVDKHNALR | 45 | 398.5624 | −2 |
YLYVCQYCPAGNIRGSIATPYK | 84 | YLYVCQYCFRAFGAPYNNKHGSLATPYK | 43 | 847.8989 | −8.6 | ||||
CRISP | Cysteine-rich secretory protein A | 698375481 | Opheodrys aestivus | WNSNAAQNAK | 76 | EMWNSNAAQNAK | 44 | 682.3055 | −1.5 |
PAGNIVGSIATPYK | 95 | MENTQAAVCSDPAGNLVGSLATPYK | 44 | 846.4114 | 7.4 | ||||
PAGNIVGSIATPYK | 95 | LYYCMNEGQMAPAGNLVGSLATPYK | 44 | 897.7457 | −14.4 | ||||
ASCFCH | 50 | HCASCFCHGGK | 48 | 632.2381 | −10.1 | ||||
SVSP | Venom thrombin-like enzyme | 118500915 | Deinagkistrodon acutus | DECDINEHR | 72 | VVNDECDLNEHR | 51 | 500.5556 | −1.3 |
SVMP | Metalloproteinase 13b | 699236656 | Hypsiglena sp. JMG-2014 | DPDNGMVEPGTK | 82 | LNMMSSSPNACADPDEGMVEPGTK | 50 | 846.6896 | −2.9 |
SVMP | Metalloproteinase 4a | 752782853 | Boiga irregularis | YLVVDNR | 53 | LYLVVDNR | 72 | 496.282 | −0.4 |
AYEMVNILNVIFR | 81 | AYEMVNLLNTMFR | 61 | 801.3932 | −1.5 | ||||
YLVVDNR | 53 | TNTARCLTLYLKLKYQPPAYLVVDNR | 51 | 622.9447 | 4 | ||||
SPDYGMVEPGTK | 64 | DYPGHHACALEDDQLLMCSEDYGMVEPASK | 51 | 850.1182 | 11.6 | ||||
SVMP | Metalloproteinase | 172046653 | Naja mossambica | TSMVAITMAHQMGHNLGMNDDR | 122 | NTDMVAGTMAHQMGHNLGLNDHR | 52 | 841.0485 | 7.2 |
AHQMGHNLGMNDDR | 81 | EFVRQAFANALYPPWWMPKYMVPQKCKAHEMGHNLGLNDHR | 50 | 986.0939 | 12.5 | ||||
SVMP | Metalloproteinase (type III) 2a | 752782867 | Boiga irregularis | TEGMVEPGTK | 75 | QTEGMVEPGTK | 60 | 580.2688 | 0.3 |
TESFVASTMAHELGHNLGINHDR | 136 | TNPFVGSTMAHEMGHNLGLNHDR | 60 | 634.5504 | 7.2 | ||||
SVMP | Atrase B, partial | 289655973 | Naja atra | FGEWRETVLLPR | 92 | AFGEWRETVLLPR | 63 | 525.2878 | 0.2 |
SVMP | Metalloproteinase 11a | 699236668 | Hypsiglena sp. JMG-2014 | QPCQNNQGYCYNGK | 94 | GPGLQPCGNNQGYCYDGK | 44 | 964.4064 | −0.3 |
KYIEFYIVVDH | 78 | SMTKPCLMRVCDLVKYLQFYLVVDHVKSYVLCYR | 48 | 823.6322 | 11.2 |
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Chapeaurouge, A.; Silva, A.; Carvalho, P.; McCleary, R.J.R.; Modahl, C.M.; Perales, J.; Kini, R.M.; Mackessy, S.P. Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps. Toxins 2018, 10, 373. https://doi.org/10.3390/toxins10090373
Chapeaurouge A, Silva A, Carvalho P, McCleary RJR, Modahl CM, Perales J, Kini RM, Mackessy SP. Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps. Toxins. 2018; 10(9):373. https://doi.org/10.3390/toxins10090373
Chicago/Turabian StyleChapeaurouge, Alex, Andreza Silva, Paulo Carvalho, Ryan J. R. McCleary, Cassandra Marie Modahl, Jonas Perales, R. Manjunatha Kini, and Stephen P. Mackessy. 2018. "Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps" Toxins 10, no. 9: 373. https://doi.org/10.3390/toxins10090373
APA StyleChapeaurouge, A., Silva, A., Carvalho, P., McCleary, R. J. R., Modahl, C. M., Perales, J., Kini, R. M., & Mackessy, S. P. (2018). Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps. Toxins, 10(9), 373. https://doi.org/10.3390/toxins10090373