Comparative Phosphoproteomic Analysis of Sporulated Oocysts and Tachyzoites of Toxoplasma gondii Reveals Stage-Specific Patterns
Abstract
:1. Introduction
2. Results
2.1. Phosphopeptide Profiling of Mature Oocysts and Tachyzoites of T. gondii
2.2. Identification of Differentially Expressed Phosphopeptides (DEPs)
2.3. Phosphorylation Motif Analysis for Quantitative Phosphopeptides
2.4. GO Category Analysis of DEPs
2.5. KEGG Pathway Analysis
2.6. Interaction Network of Identified Phosphoproteins
2.7. Kinase Connected Network
2.8. Potential Phosphor-Dependent Interactions
3. Discussion
3.1. Motifs
3.2. GO and KEGG Analysis
3.3. PPI Network
3.4. Kinase–Protein Interactions
4. Material and Methods
4.1. Ethics Statements
4.2. Mice, Guinea Pigs, Cats, and Parasite Strains
4.3. Preparation of Tachyzoites and Sporulated Oocysts
4.3.1. Collection and Purification of Tachyzoites
4.3.2. Collection and Purification of Sporulated Oocysts
4.4. Extraction and Digestion of Protein
4.5. IBT Labeling
4.6. Enrichment of Phosphopeptides by Affinity Chromatography
4.7. LC-MS/MS
4.8. Data Analysis
4.9. Bioinformatics
4.10. Relevance Analysis of T. gondii Protein Kinase with Phosphorylated Peptides
4.11. Forecast of Protein Coactions Activated or Inactivated by Phosphorylation
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
Abbreviations
Ab1 | Abelson kinase |
ACN | Acetonitrile |
αSNAP | Alpha soluble N-ethylmaleimide-sensitive fusion protein attachment protein |
ATM | Ataxia telangiectasia mutated kinase |
CsCl | Cesium chloride |
CDPK | Calcium dependent protein kinase |
Cam-II | Calmodulin-dependent protein kinase II |
CDC2 | Cell division cycle protein kinase p34 |
CDK | Cyclin-dependent kinase |
cis-SNARE | cis-soluble N-ethylmaleimide sensitive factor attachment protein receptor |
CKI | Casein kinase I |
CKII | Casein kinase II |
CV | Coefficient of variation |
MAPK | Cyclin-dependent kinase of mitogen-activated protein kinase |
GRAs | Dense granule proteins |
DEPs | Differentially expressed phosphopeptides |
DTT | Dithiothreitol |
EGFR | Epithelial growth factor receptor |
FDR | False-discovery rate |
FA | Formic acid |
GO | Gene ontology |
IKK | ikappab kinase |
INSR | Insulin receptor |
Jak | Janus kinase |
KEGG | Kyoto Encyclopedia of Genes and Genomes |
MAPK | Mitogen-activated protein kinase |
OG | Orthologous groups |
OWP | Oocyst wall protein |
PBS | Phosphate-buffered saline |
PKA | Camp-dependent protein kinase |
PKB | Protein kinase B |
PKC | Protein kinase C |
PKG | cGMP-dependent protein kinase |
PTM | Posttranslational modification |
ROPs | Rhoptry proteins |
RP | ribosomal protein |
STRING | Search tool for the retrieval of interacting genes/protein |
SDZ | Sulfadiazine |
SAGE | Serial analysis of gene expression |
SPF | Specific pathogen free |
Src | Sarcoma gene kinase |
Syk | Cytoplasmic tyrosine kinases |
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Motif | Kinase Classes |
---|---|
P..SP | ATM, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKC, and PKG |
E……SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, and Syk |
SP…T | Ab1, ATM, CaM-II, CDC2, CDK, CKI, IKK, INSR, MAPK, PKA, PKB, PKC, and PKG |
ASP | Ab1, ATM, CDC2, CDK, CKI, IKK, INSR, MAPK, PKA, PKB, PKC, PKG |
K……SP | ATM, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, and PKG |
SP….R | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, Jak, MAPK, PKA, PKB, PKC, and PKG |
P.SP | ATM, CaM-II, CDC2, CDK, CKI, IKK, MAPK, PKA, PKC, and PKG |
SP | Ab1, ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, Src, Syk, PKA, PKB, PKC, and PKG |
L.R..S | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
R..S | ATM, CaM-II, CDC2, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
GS | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, Jak, MAPK, PKA, PKC, PKG, Src, and Syk |
K..S | ATM, CDC2, CDK, CKI, IKK, MAPK, PKA, PKC, PKG, and Syk |
S…..K | ATM, CaM-II, CDK, CKI, CKII, IKK, INSR, Jak, MAPK, PKB, PKC, PKG, and Syk |
TP | ATM, CaM-II, CDC2, CDK, CKI, CKII, EGFR, IKK, INSR, Jak, MAPK, PKA, PKB, PKC, PKG, and Syk |
R..T | Ab1, CaM-II, CDC2, EGFR, IKK, MAPK, PKA, PKC, PKG, and Src |
K..T | CDK, IKK, MAPK, PKA, PKC, and PKG |
Motif | Kinase Classes |
---|---|
RS.SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
SP…K | ATM, PKA, CDC2, CDK, IKK, MAPK, PKC, and PKG |
A.SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, PKG, and Syk |
P.SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
Q..SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
G..SP | Ab1, ATM, CDC2, CDK, CKI, CKII, IKK, INSR, Jak, MAPK, PKB, PKC, PKG, and Syk |
E.SP | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, and PKG |
SP | Ab1, ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, Src, and Syk |
SD.E | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
L.R..S | ATM, CaM-II, CDC2,CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, and PKG |
R..S | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, Src, and Syk |
SS.D | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKC, and PKG |
SG.E | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, and Syk |
SE.E | ATM, CaM-II, CDC2, CDK, CKI, CKII, EGFR, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, and Syk |
SD | Ab1, ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, and Syk |
GS | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, PKG, Src, and Syk |
K..S | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, INSR, MAPK, PKA, PKB, PKC, and PKG |
DS | ATM, CaM-II, CDC2, CDK, CKI, CKII, EGFR, IKK, INSR, Jak, MAPK, PKA, PKC, PKC, and PKG |
S..S | ATM, CaM-II, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, PKC, and PKG |
G..TP | ATM, CDC2, CDK, CKII, IKK, MAPK, PKC, and PKG, |
TP | ATM, CDC2, CDK, CKI, CKII, IKK, MAPK, PKA, PKB, and PKG, |
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Wang, Z.-X.; Che, L.; Hu, R.-S.; Sun, X.-L. Comparative Phosphoproteomic Analysis of Sporulated Oocysts and Tachyzoites of Toxoplasma gondii Reveals Stage-Specific Patterns. Molecules 2022, 27, 1022. https://doi.org/10.3390/molecules27031022
Wang Z-X, Che L, Hu R-S, Sun X-L. Comparative Phosphoproteomic Analysis of Sporulated Oocysts and Tachyzoites of Toxoplasma gondii Reveals Stage-Specific Patterns. Molecules. 2022; 27(3):1022. https://doi.org/10.3390/molecules27031022
Chicago/Turabian StyleWang, Ze-Xiang, Liang Che, Rui-Si Hu, and Xiao-Lin Sun. 2022. "Comparative Phosphoproteomic Analysis of Sporulated Oocysts and Tachyzoites of Toxoplasma gondii Reveals Stage-Specific Patterns" Molecules 27, no. 3: 1022. https://doi.org/10.3390/molecules27031022