Post-Translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber)
Abstract
:1. Introduction
2. Results
2.1. PAD Homologues in Naked Mole-Rat Plasma
2.2. Deiminated Protein Profiles of Naked Mole-Rat Plasma and Plasma-Derived EVs
2.3. Characterisation of Extracellular Vesicles in Naked Mole-Rat Plasma
2.4. MicroRNA Analysis of Naked Mole-Rat EVs
3. Discussion
4. Materials and Methods
4.1. Sampling of Naked Mole-Rat Plasma
4.2. Extracellular Vesicle Isolation and Nanoparticle Tracking Analysis (NTA)
4.3. Transmission Electron Microscopy (TEM)
4.4. Western Blotting Analysis
4.5. Immunoprecipitation and Protein Identification
4.6. MicroRNA Analysis
4.7. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
BSA | Bovine Serum Albumin |
CD63 | CD63 antigen; granulophysin; lysosomal-associated membrane protein 3 |
CNS | Central Nervous System |
ECL | Enhanced Chemiluminescence |
EVs | Extracellular Vesicles |
F95 | Pan-deimination/citrullination antibody |
FBS | Foetal Bovine Serum |
Flot-1 | Flotillin-1 |
HIF | Hypoxia-inducible Factor |
KEGG | Kyoto Encyclopedia of Genes and Genomes |
kDa | Kilodalton |
LC-MS/MS | Liquid Chromatography Mass Spectrometry |
miR | microRNA |
NTA | Nanoparticle Tracking Analysis |
PAD | Peptidylarginine Deiminase |
SDS-PAGE | Sodium Dodecyl Sulfate Polyacrylamide Gel Electrophoresis |
TBS | Tris Buffered Saline |
TEM | Transmission Electron Microscopy |
WB | Western Blotting |
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Protein Name | Symbol | Total Score (p < 0.05) # |
---|---|---|
Apolipoprotein B-100 | G5AZB7_HETGA | 6077 |
Alpha-2-macroglobulin | G5BPM1_HETGA | 4974 |
Complement C3 | G5C0N5_HETGA | 4300 |
Serotransferrin | G5BQA9_HETGA | 4058 |
Serum albumin | G5B5P2_HETGA | 3394 |
Fibronectin | G5BHR4_HETGA | 3333 |
Fibrinogen beta chain | G5BML3_HETGA | 2638 |
Kininogen-1 | G5BT86_HETGA | 2276 |
Fibrinogen alpha chain | G5BML2_HETGA | 2094 |
Ceruloplasmin | G5BSL1_HETGA | 2022 |
Histidine-rich glycoprotein | G5BT87_HETGA | 1851 |
Complement C4-A | G5C3H6_HETGA | 1759 |
Complement factor H | G5BM71_HETGA | 1646 |
Plasminogen | G5BC53_HETGA | 1548 |
Inter-alpha-trypsin inhibitor heavy chain H4 | G5BUN4_HETGA | 1455 |
Fibrinogen gamma chain | G5BML1_HETGA | 1338 |
Complement factor B | G5C3H1_HETGA | 1313 |
Plasma kallikrein | G5BNV2_HETGA | 1167 |
Antithrombin-III | G5ARS6_HETGA | 1093 |
Coagulation factor V | G5CB46_HETGA | 1092 |
Complement C5 | G5AXS5_HETGA | 1002 |
Hemoglobin subunit beta | G5BS33_HETGA | 941 |
Transcobalamin-2 isoform 1 | G5AVP0_HETGA | 913 |
Hemopexin | G5BBR0_HETGA | 899 |
Coagulation factor XIII B chain | G5BM72_HETGA | 821 |
Protein AMBP | G5B1Y4_HETGA | 817 |
N-acetylmuramoyl-L-alanine amidase | G5BYP3_HETGA | 812 |
Coagulation factor XII | G5BQ09_HETGA | 802 |
Apolipoprotein A-I | APOA1_HETGA | 798 |
Hemoglobin subunit alpha | G5BXY1_HETGA | 784 |
Coagulation factor XIII A chain | G5BAS8_HETGA | 779 |
Hemoglobin subunit beta | G5BYJ8_HETGA | 759 |
Alpha-1-antiproteinase S | G5B496_HETGA | 724 |
Inter-alpha-trypsin inhibitor heavy chain H3 | G5BUN3_HETGA | 682 |
Vitronectin | G5BVN8_HETGA | 652 |
Complement factor I | G5AQM1_HETGA | 647 |
Hemoglobin subunit epsilon-1 | G5BS35_HETGA | 642 |
Inter-alpha-trypsin inhibitor heavy chain H2 | G5AXV8_HETGA | 584 |
Apolipoprotein E | G5CBM7_HETGA | 581 |
Inhibitor of carbonic anhydrase | G5BQB0_HETGA | 537 |
Inter-alpha-trypsin inhibitor heavy chain H1 | G5BUN2_HETGA | 482 |
Four and a half LIM domains protein 1 | G5CA61_HETGA | 469 |
Haptoglobin | G5B5U6_HETGA | 464 |
C4b-binding protein | G5BP10_HETGA | 438 |
L-lactate dehydrogenase | G5AKA3_HETGA | 437 |
Insulin-like growth factor-binding protein complex acid labile chain | G5BY64_HETGA | 403 |
Catalase | G5AXV0_HETGA | 382 |
Fetuin-B | G5BT88_HETGA | 347 |
Alpha-2-HS-glycoprotein | G5BT89_HETGA | 337 |
Selenoprotein P | G5APA7_HETGA | 328 |
Vitamin D-binding protein | G5BE53_HETGA | 317 |
Adiponectin | G5BT83_HETGA | 283 |
von Willebrand factor | G5CAN6_HETGA | 274 |
Beta-2-glycoprotein 1 | G5BGY7_HETGA | 268 |
Basement membrane-specific heparan sulfate proteoglycan core protein | G5BI06_HETGA | 267 |
Gelsolin | G5AXS0_HETGA | 259 |
Aspartyl aminopeptidase | G5AKJ4_HETGA | 256 |
Complement C1q subcomponent subunit A | G5BHZ8_HETGA | 246 |
Ficolin-3 | G5AUT5_HETGA | 241 |
Mannan-binding lectin serine protease 1 | G5BTD5_HETGA | 228 |
Alpha-1-antichymotrypsin | G5B491_HETGA | 228 |
Carboxypeptidase N catalytic chain | G5AYP3_HETGA | 210 |
Complement C1q subcomponent subunit C | G5BHZ7_HETGA | 191 |
Mannan-binding lectin serine protease 2 | G5C521_HETGA | 188 |
Prothrombin | G5ATC4_HETGA | 177 |
Complement C1q tumour necrosis factor-related protein 3 | G5BQ97_HETGA0 | 177 |
Nucleoside diphosphate kinase | G5C4L3_HETGA | 168 |
L-lactate dehydrogenase | G5BEG2_HETGA | 167 |
Alpha-2-antiplasmin | G5BCV1_HETGA | 164 |
Keratin, type II cytoskeletal 6B | G5ALS1_HETGA | 152 |
Carbonic anhydrase 2 | G5ATW7_HETGA | 143 |
Proprotein convertase subtilisin/kexin type 9 | G5APQ4_HETGA | 137 |
Angiotensinogen | G5BQI5_HETGA | 121 |
6-phosphogluconate dehydrogenase, decarboxylating | G5C530_HETGA | 91 |
Nesprin-1 | G5C0E1_HETGA | 87 |
Complement C1q subcomponent subunit B | G5BHZ6_HETGA | 87 |
Angiopoietin-related protein 6 | G5B341_HETGA | 85 |
Hepatocyte growth factor activator | G5BZF5_HETGA | 84 |
Calpain-1 catalytic subunit | G5B6L3_HETGA | 84 |
Sulfhydryl oxidase | G5AYL7_HETGA | 80 |
Keratin, type II cytoskeletal 5 | G5ALS3_HETGA | 76 |
Profilin | G5BH50_HETGA | 75 |
40S ribosomal protein S27a | G5B8W4_HETGA | 68 |
Xanthine dehydrogenase/oxidase | G5B3Z0_HETGA | 68 |
Plasma protease C1 inhibitor | G5BLJ5_HETGA | 67 |
Collectin-11 | G5C7L1_HETGA | 66 |
Extracellular matrix protein 1 | G5BH40_HETGA | 64 |
Actin, gamma-enteric smooth muscle | G5AXH0_HETGA | 61 |
Collectin-10 | G5C9R8_HETGA | 61 |
Keratin, type I cytoskeletal 17 | G5B0M4_HETGA | 58 |
Contactin-1 | G5BGJ6_HETGA | 55 |
Dynein heavy chain 1, axonemal | G5BUL8_HETGA | 50 |
Leucine-rich repeat-containing protein 15 | G5ALE6_HETGA | 43 |
Transcriptional regulator ATRX | G5C0I5_HETGA | 42 |
Transmembrane protein 127 | G5BMW1_HETGA | 41 |
TRAF3-interacting protein 1 | G5BHH8_HETGA | 41 |
Mannose-binding protein A | G5C4H7_HETGA | 40 |
Hyaluronan-binding protein 2 | G5BKD5_HETGA | 39 |
Fer3-like protein | G5BZJ1_HETGA | 38 |
Complement component C7 | G5C4R4_HETGA | 38 |
PITH domain-containing protein | G5BHY3_HETGA | 38 |
1,4-alpha-glucan-branching enzyme | G5BA56_HETGA | 37 |
tRNA pseudouridine synthase | G5BB54_HETGA | 37 |
SRRM2-like protein | G5BG61_HETGA | 34 |
Putative carboxypeptidase PM20D1 | G5BX50_HETGA | 34 |
Olfactory receptor | G5C741_HETGA | 33 |
Protein CASC5 | G5BLZ4_HETGA | 33 |
Conserved oligomeric Golgi complex subunit 1 | G5B5M3_HETGA | 32 |
Small G protein signalling modulator 1 | G5BGN5_HETGA | 32 |
Eukaryotic translation initiation factor 3 subunit E | G5BD61_HETGA | 31 |
HEAT repeat-containing protein 2 | G5AZ15_HETGA | 31 |
Proline-rich protein 11 | G5AXY5_HETGA | 31 |
Peroxiredoxin-1 | G5ARW1_HETGA | 30 |
Pre-mRNA-processing factor 17 | G5B0Y2_HETGA | 30 |
Ribonucleoside-diphosphate reductase | G5B9C2_HETGA | 30 |
Protein Name | Symbol | Total Score (p < 0.05) # |
---|---|---|
Alpha-2-macroglobulin | G5BPM1_HETGA | 2978 |
Serum albumin | G5B5P2_HETGA | 2570 |
Serotransferrin | G5BQA9_HETGA | 1976 |
Keratin, type II cytoskeletal 6B | G5ALS1_HETGA | 1459 |
Complement C3 | G5C0N5_HETGA | 1440 |
Keratin, type II cytoskeletal 5 | G5ALS3_HETGA | 1211 |
Kininogen-1 | G5BT86_HETGA | 1196 |
Histidine-rich glycoprotein | G5BT87_HETGA | 1186 |
Keratin, type I cytoskeletal 10 | G5AX66_HETGA | 1130 |
Keratin, type I cytoskeletal 14 | G5B0M6_HETGA | 1038 |
Keratin, type II cytoskeletal 1 | G5ALS8_HETGA | 1011 |
Fibrinogen beta chain | G5BML3_HETGA | 974 |
Fibrinogen alpha chain | G5BML2_HETGA | 956 |
Apolipoprotein B-100 | G5AZB7_HETGA | 834 |
Keratin, type I cytoskeletal 13 | G5B0N0_HETGA | 701 |
Keratin, type I cytoskeletal 17 | G5B0M4_HETGA | 673 |
Desmoplakin | G5BAT4_HETGA | 670 |
Hemoglobin subunit alpha | G5BXY1_HETGA | 591 |
Hemoglobin subunit beta | G5BS33_HETGA | 581 |
Complement C4-A | G5C3H6_HETGA | 571 |
Hemoglobin subunit beta | G5BYJ8_HETGA | 568 |
Apolipoprotein A-I | APOA1_HETGA | 499 |
Keratin, type II cytoskeletal 79 | G5BJ37_HETGA | 468 |
Actin, cytoplasmic 1 | G5BI78_HETGA | 444 |
Keratin, type II cytoskeletal 4 | G5BJ36_HETGA | 443 |
Fibrinogen gamma chain | G5BML1_HETGA | 382 |
Ceruloplasmin | G5BSL1_HETGA | 350 |
Apolipoprotein E | G5CBM7_HETGA | 338 |
Inter-alpha-trypsin inhibitor heavy chain H4 | G5BUN4_HETGA | 332 |
Protein AMBP | G5B1Y4_HETGA | 280 |
Inhibitor of carbonic anhydrase | G5BQB0_HETGA | 244 |
Hemopexin | G5BBR0_HETGA | 239 |
Histone H4 | G5BKL3_HETGA | 238 |
Plasminogen | G5BC53_HETGA | 232 |
Alpha-1-antiproteinase S | G5B496_HETGA | 217 |
Hemoglobin subunit epsilon-1 | G5BS35_HETGA | 213 |
Junction plakoglobin | G5B0M0_HETGA | 202 |
N-acetylmuramoyl-L-alanine amidase | G5BYP3_HETGA | 190 |
Inter-alpha-trypsin inhibitor heavy chain H3 | G5BUN3_HETGA | 190 |
Keratin, type II cytoskeletal 7 | G5BL96_HETGA | 182 |
Fibronectin | G5BHR4_HETGA | 164 |
Glyceraldehyde-3-phosphate dehydrogenase | G5CAP7_HETGA | 154 |
Coagulation factor XII | G5BQ09_HETGA | 152 |
Antithrombin-III | G5ARS6_HETGA | 150 |
Catenin beta-1 | G5ALX2_HETGA | 126 |
Plakophilin-1 | G5B3A4_HETGA | 120 |
Annexin | G5AWC0_HETGA | 119 |
Keratin, type II cytoskeletal 3 | G5ALT2_HETGA | 118 |
40S ribosomal protein S27a | G5B8W4_HETGA | 116 |
Inter-alpha-trypsin inhibitor heavy chain H2 | G5AXV8_HETGA | 106 |
Alpha-2-antiplasmin | G5BCV1_HETGA | 86 |
Complement factor B | G5C3H1_HETGA | 81 |
Elongation factor 1-alpha | G5ALK7_HETGA | 78 |
Angiotensinogen | G5BQI5_HETGA | 77 |
Histone H2B | G5BH20_HETGA | 77 |
Plasma kallikrein | G5BNV2_HETGA | 72 |
Beta-enolase | G5BW96_HETGA | 70 |
Vitamin D-binding protein | G5BE53_HETGA | 57 |
Alpha-1-antichymotrypsin | G5B491_HETGA | 55 |
Keratin, type II cytoskeletal 80 | G5BL95_HETGA | 53 |
Heat shock cognate 71 kDa protein | G5B170_HETGA | 51 |
Leucine-rich repeat-containing protein KIAA1731 | G5C3Y1_HETGA | 50 |
Cathepsin D | G5C2G1_HETGA | 49 |
Basement membrane-specific heparan sulfate proteoglycan core protein | G5BI06_HETGA | 47 |
Skin-specific protein 32 | G5BUY9_HETGA | 46 |
Desmocollin-1 | G5C312_HETGA | 46 |
Protein-arginine deiminase type-6 | G5BZN1_HETGA | 46 |
Cryptochrome-1 | G5C454_HETGA | 45 |
Complement C1q subcomponent subunit C | G5BHZ7_HETGA | 45 |
p2Y purinoceptor 12 | G5C102_HETGA | 44 |
Alpha-1B-glycoprotein | G5B7K8_HETGA | 44 |
Exportin-1 | G5C1Y9_HETGA | 44 |
Putative hexokinase HKDC1 | G5B183_HETGA | 43 |
Transcriptional regulator ATRX | G5C0I5_HETGA | 42 |
Coiled-coil domain-containing protein 57 | G5BJ98_HETGA | 42 |
Microtubule plus-end tracking protein TIP150 | G5ATU1_HETGA | 40 |
Tubulin alpha-1C chain | G5AQ00_HETGA | 38 |
Fer3-like protein | G5BZJ1_HETGA | 38 |
Amino acid transporter | G5BYQ9_HETGA | 36 |
Ventricular zone-expressed PH domain-containing protein-like protein 1 | G5B253_HETGA | 35 |
SRRM2-like protein | G5BG61_HETGA | 35 |
N6-adenosine-methyltransferase 70 kDa subunit | G5BFU9_HETGA | 33 |
Proline-rich protein 11 | G5AXY5_HETGA | 33 |
Carbonic anhydrase 2 | G5ATW7_HETGA | 32 |
26S proteasome non-ATPase regulatory subunit 3 | G5BRY1_HETGA | 31 |
Serine/threonine-protein kinase LATS1 | G5BMD1_HETGA | 31 |
Transmembrane gamma-carboxyglutamic acid protein 1 | G5C418_HETGA | 31 |
Collagen alpha-2(I) chain | G5ANK8_HETGA | 31 |
Bcl-2-associated transcription factor 1 | G5C1A7_HETGA | 30 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
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Pamenter, M.E.; Uysal-Onganer, P.; Huynh, K.W.; Kraev, I.; Lange, S. Post-Translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber). Int. J. Mol. Sci. 2019, 20, 5378. https://doi.org/10.3390/ijms20215378
Pamenter ME, Uysal-Onganer P, Huynh KW, Kraev I, Lange S. Post-Translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber). International Journal of Molecular Sciences. 2019; 20(21):5378. https://doi.org/10.3390/ijms20215378
Chicago/Turabian StylePamenter, Matthew E., Pinar Uysal-Onganer, Kenny W. Huynh, Igor Kraev, and Sigrun Lange. 2019. "Post-Translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber)" International Journal of Molecular Sciences 20, no. 21: 5378. https://doi.org/10.3390/ijms20215378