Cited by 5Advanced Proteomics Techniques and ApplicationsMosquito-borne diseases and controlMass Spectrometry Techniques and Applications

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Re-mining serum proteomics data reveals extensive post-translational modifications upon Zika and dengue infection

Open access

Published version of a preprint

Abstract

Zika virus (ZIKV) and dengue virus (DENV) are two closely related flaviviruses with similar symptoms. However, due to the implications of ZIKV infections for pregnancy outcomes, understanding differences in their molecular impact on the host is of high interest. Viral infections change the host proteome, including post-translational modifications. As modifications are diverse and of low abundance, they typically require additional sample processing which is not feasible for large cohort studies. Therefore, we tested the potential of next-generation proteomics data in its ability to prioritize specific modifications for later analysis. We re-mined published mass spectra from 122 serum samples from ZIKV and DENV patients for the presence of phosphorylated, methylated, oxidized, glycosylated/glycated, sulfated, and carboxylated peptides. We identified 246 modified peptides with significantly differential abundance in ZIKV and DENV patients. Amongst these, methionine-oxidized peptides from apolipoproteins and glycosylated peptides from immunoglobulin proteins were more abundant in ZIKV patient serum and generate hypotheses on the potential roles of the modification in the infection. The results demonstrate how data-independent acquisition techniques can help prioritize future analyses of peptide modifications.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1039/d2mo00258b

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 95

  1. Subissi, 2018, Zika Virus Infection during Pregnancy and Effects on Early Childhood Development, French Polynesia, 2013–2016, Emerg. Infect. Dis., 24, 1850, 10.3201/eid2410.172079 · DOI
  2. Teo, 2015, mapDIA: preprocessing and statistical analysis of quantitative proteomics data from data independent acquisition mass spectrometry, J. Proteomics, 129, 108, 10.1016/j.jprot.2015.09.013 · DOI
  3. Eggo, 2018, Expected Duration of Adverse Pregnancy Outcomes after Zika Epidemic, Emerg. Infect. Dis., 24, 127, 10.3201/eid2401.170482 · DOI
  4. Wen, 2017, Identification of Zika virus epitopes reveals immunodominant and protective roles for dengue virus cross-reactive CD8 + T cells, Nat. Microbiol., 2, 1, 10.1038/nmicrobiol.2017.36 · DOI
  5. Ngono, 2019, Cross-Reactive T Cell Immunity to Dengue and Zika Viruses: New Insights Into Vaccine Development, Front. Immunol., 10, 1316, 10.3389/fimmu.2019.01316 · DOI
  6. Pierson, 2020, The continued threat of emerging flaviviruses, Nat. Microbiol., 5, 796, 10.1038/s41564-020-0714-0 · DOI
  7. Bhargavi, 2020, Global outbreaks of zika infection by epidemic observatory (EpiWATCH), 2016–2019, Global Biosecurity, 2
  8. Sharp, 2019, Dengue and Zika Virus Diagnostic Testing for Patients with a Clinically Compatible Illness and Risk for Infection with Both Viruses, MMWR Recomm. Rep., 68, 1, 10.15585/mmwr.rr6801a1 · DOI
  9. Tsai, 2017, Distinguishing Secondary Dengue Virus Infection From Zika Virus Infection With Previous Dengue by a Combination of 3 Simple Serological Tests, Clin. Infect. Dis., 65, 1829, 10.1093/cid/cix672 · DOI
  10. Langerak, 2019, The possible role of cross-reactive dengue virus antibodies in Zika virus pathogenesis, PLoS Pathog., 15, e1007640, 10.1371/journal.ppat.1007640 · DOI
  11. Stettler, 2016, Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection, Science, 353, 823, 10.1126/science.aaf8505 · DOI
  12. Valencia, 2022, Effect of prior Zika and dengue virus exposure on the severity of a subsequent dengue infection in adults, Sci. Rep., 12, 17225, 10.1038/s41598-022-22231-y · DOI
  13. Savidis, 2016, Identification of Zika Virus and Dengue Virus Dependency Factors using Functional Genomics, Cell Rep., 16, 232, 10.1016/j.celrep.2016.06.028 · DOI
  14. Shah, 2018, Comparative Flavivirus-Host Protein Interaction Mapping Reveals Mechanisms of Dengue and Zika Virus Pathogenesis, Cell, 175, 1931, 10.1016/j.cell.2018.11.028 · DOI
  15. Allgoewer, 2021, New Proteomic Signatures to Distinguish Between Zika and Dengue Infections, Mol. Cell. Proteomics, 20, 100052, 10.1016/j.mcpro.2021.100052 · DOI
  16. Hu, 2020, Role of Post-translational Modifications in Influenza A Virus Life Cycle and Host Innate Immune Response, Front. Microbiol., 11, 2156, 10.3389/fmicb.2020.517461 · DOI
  17. Kumar, 2020, Role of Host-Mediated Post-Translational Modifications (PTMs) in RNA Virus Pathogenesis, Int. J. Mol. Sci., 22, 323, 10.3390/ijms22010323 · DOI
  18. Johnson, 2022, Global post-translational modification profiling of HIV-1-infected cells reveals mechanisms of host cellular pathway remodeling, Cell Rep., 39, 110690, 10.1016/j.celrep.2022.110690 · DOI
  19. Macedo-da-Silva, 2020, Serum Proteomics Reveals Alterations in Protease Activity, Axon Guidance, and Visual Phototransduction Pathways in Infants With In Utero Exposure to Zika Virus Without Congenital Zika Syndrome, Front. Cell. Infect. Microbiol., 10, 577819, 10.3389/fcimb.2020.577819 · DOI
  20. Mazzon, 2009, Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation, J. Infect. Dis., 200, 1261, 10.1086/605847 · DOI
  21. Schaller, 2008, Posttranslational Modifications, pp. 75–87, 10.1002/9780470724378.ch6 · DOI
  22. Hermann, 2022, Identification and characterization of post-translational modifications: Clinical implications, Mol. Aspects Med., 86, 101066, 10.1016/j.mam.2022.101066 · DOI
  23. Hansson, 2005, Post-translational modifications in proteins involved in blood coagulation, J. Thromb. Haemostasis, 3, 2633, 10.1111/j.1538-7836.2005.01478.x · DOI
  24. Mnatsakanyan, 2018, Detecting post-translational modification signatures as potential biomarkers in clinical mass spectrometry, Expert Rev. Proteomics, 15, 515, 10.1080/14789450.2018.1483340 · DOI
  25. Doll, 2015, Mass spectrometry-based detection and assignment of protein posttranslational modifications, ACS Chem. Biol., 10, 63, 10.1021/cb500904b · DOI
  26. Rosenberger, 2014, A repository of assays to quantify 10,000 human proteins by SWATH-MS, Sci. Data, 1, 140031, 10.1038/sdata.2014.31 · DOI · Paper page
  27. Faria, 2017, A Timely Shift from Shotgun to Targeted Proteomics and How It Can Be Groundbreaking for Cancer Research, Front. Oncol., 7, 13, 10.3389/fonc.2017.00013 · DOI
  28. Yang, 2022, Data-independent acquisition proteomics methods for analyzing post-translational modifications, Proteomics, e2200046
  29. Olsen, 2013, Status of large-scale analysis of post-translational modifications by mass spectrometry, Mol. Cell. Proteomics, 12, 3444, 10.1074/mcp.O113.034181 · DOI
  30. Mi, 2019, Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0), Nat. Protoc., 14, 703, 10.1038/s41596-019-0128-8 · DOI
  31. Mi, 2021, PANTHER version 16: a revised family classification, tree-based classification tool, enhancer regions and extensive API, Nucleic Acids Res., 49, D394, 10.1093/nar/gkaa1106 · DOI · Paper page
  32. Baldensperger, 2020, Comprehensive analysis of posttranslational protein modifications in aging of subcellular compartments, Sci. Rep., 10, 7596, 10.1038/s41598-020-64265-0 · DOI
  33. Sun, 2018, Site-Specific Profiling of Serum Glycoproteins Using N-Linked Glycan and Glycosite Analysis Revealing Atypical N-Glycosylation Sites on Albumin and α-1B-Glycoprotein, Anal. Chem., 90, 6292, 10.1021/acs.analchem.8b01051 · DOI
  34. Krieg, 1998, Recognition Signal for C-Mannosylation of Trp-7 in RNase 2 Consists of Sequence Trp–x–x–Trp, MBoC, 9, 301, 10.1091/mbc.9.2.301 · DOI
  35. Chauhan, 2013, In silico Platform for Prediction of N-, O- and C-Glycosites in Eukaryotic Protein Sequences, PLoS One, 8, e67008, 10.1371/journal.pone.0067008 · DOI
  36. Hofsteenge, 1999, The four terminal components of the complement system are C-mannosylated on multiple tryptophan residues, J. Biol. Chem., 274, 32786, 10.1074/jbc.274.46.32786 · DOI
  37. Potgieter, 1997, Spontaneous oxidation of methionine: effect on the quantification of plasma methionine levels, Anal. Biochem., 248, 86, 10.1006/abio.1997.2075 · DOI
  38. Liu, 2013, Accurate Determination of Protein Methionine Oxidation by Stable Isotope Labeling and LC-MS Analysis, Anal. Chem., 85, 11705, 10.1021/ac403072w · DOI
  39. Pankhurst, 2003, Characterization of specifically oxidized apolipoproteins in mildly oxidized high density lipoprotein, J. Lipid Res., 44, 349, 10.1194/jlr.M200256-JLR200 · DOI
  40. Fukuhara, 2017, Host-derived apolipoproteins play comparable roles with viral secretory proteins Erns and NS1 in the infectious particle formation of Flaviviridae, PLoS Pathog., 13, e1006475, 10.1371/journal.ppat.1006475 · DOI
  41. Faustino, 2014, Dengue virus capsid protein interacts specifically with very low-density lipoproteins, Nanomedicine, 10, 247, 10.1016/j.nano.2013.06.004 · DOI
  42. Weigandt, 2012, Fibrin clot structure and mechanics associated with specific oxidation of methionine residues in fibrinogen, Biophys. J., 103, 2399, 10.1016/j.bpj.2012.10.036 · DOI
  43. White, 2016, Post-translational oxidative modification of fibrinogen is associated with coagulopathy after traumatic injury, Free Radical Biol. Med., 96, 181, 10.1016/j.freeradbiomed.2016.04.023 · DOI
  44. Pederson, 2019, Oxidation-induced destabilization of the fibrinogen αC-domain dimer investigated by molecular dynamics simulations, Proteins, 87, 826, 10.1002/prot.25746 · DOI
  45. Wu, 1998, Oxidized alpha2-macroglobulin (alpha2M) differentially regulates receptor binding by cytokines/growth factors: implications for tissue injury and repair mechanisms in inflammation, J. Immunol., 161, 4356, 10.4049/jimmunol.161.8.4356 · DOI
  46. Griffiths, 2002, Relationship between protein structure and methionine oxidation in recombinant human alpha 1-antitrypsin, Biochemistry, 41, 6245, 10.1021/bi025599p · DOI
  47. Taggart, 2000, Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity, J. Biol. Chem., 275, 27258, 10.1016/S0021-9258(19)61505-X · DOI · Paper page
  48. Li, 2009, Oxidized {alpha}1-antitrypsin stimulates the release of monocyte chemotactic protein-1 from lung epithelial cells: potential role in emphysema, Am. J. Physiol.: Lung Cell. Mol. Physiol., 297, L388
  49. Liu, 2013, A method for systematic mapping of protein lysine methylation identifies new functions for HP1β in DNA damage repair, Mol. Cell, 50, 723, 10.1016/j.molcel.2013.04.025 · DOI
  50. Gu, 2016, Quantitative Profiling of Post-translational Modifications by Immunoaffinity Enrichment and LC-MS/MS in Cancer Serum without Immunodepletion, Mol. Cell. Proteomics, 15, 692, 10.1074/mcp.O115.052266 · DOI
  51. Liu, 2007, Mapping the human plasma proteome by SCX-LC-IMS-MS, J. Am. Soc. Mass Spectrom., 18, 1249, 10.1016/j.jasms.2007.04.012 · DOI
  52. Sennels, 2007, Proteomic analysis of human blood serum using peptide library beads, J. Proteome Res., 6, 4055, 10.1021/pr070339l · DOI
  53. Marsden, 2021, Inhibition of Arginine Methylation Impairs Platelet Function, ACS Pharmacol Transl. Sci., 4, 1567, 10.1021/acsptsci.1c00135 · DOI
  54. Guo, 2014, Immunoaffinity enrichment and mass spectrometry analysis of protein methylation, Mol. Cell. Proteomics, 13, 372, 10.1074/mcp.O113.027870 · DOI
  55. Jones, 1983, Glycosylated serum albumin: an intermediate index of diabetic control, Diabetes Care, 6, 501, 10.2337/diacare.6.5.501 · DOI
  56. Shaklai, 1984, Nonenzymatic glycosylation of human serum albumin alters its conformation and function, J. Biol. Chem., 259, 3812, 10.1016/S0021-9258(17)43168-1 · DOI
  57. Goetze, 2012, Rates and impact of human antibody glycation in vivo, Glycobiology, 22, 221, 10.1093/glycob/cwr141 · DOI
  58. Wei, 2017, Glycation of antibodies: Modification, methods and potential effects on biological functions, MAbs., 9, 586, 10.1080/19420862.2017.1300214 · DOI
  59. Gudelj, 2018, Immunoglobulin G glycosylation in aging and diseases, Cell. Immunol., 333, 65, 10.1016/j.cellimm.2018.07.009 · DOI
  60. Karsten, 2012, Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1, Nat. Med., 18, 1401, 10.1038/nm.2862 · DOI
  61. Thulin, 2020, Maternal Anti-Dengue IgG Fucosylation Predicts Susceptibility to Dengue Disease in Infants, Cell Rep., 31, 107642, 10.1016/j.celrep.2020.107642 · DOI
  62. Spiller, 2017, Glycated lysine-141 in haptoglobin improves the diagnostic accuracy for type 2 diabetes mellitus in combination with glycated hemoglobin HbA1c and fasting plasma glucose, Clin. Proteomics, 14, 10, 10.1186/s12014-017-9145-1 · DOI
  63. Miao, 2019, Proteomics Profiling of Host Cell Response via Protein Expression and Phosphorylation upon Dengue Virus Infection, Virol. Sin., 34, 549, 10.1007/s12250-019-00131-2 · DOI
  64. Yalak, 2019, Phosphorylated fibronectin enhances cell attachment and upregulates mechanical cell functions, PLoS One, 14, e0218893, 10.1371/journal.pone.0218893 · DOI
  65. Foo, 2017, Asian Zika virus strains target CD14+ blood monocytes and induce M2-skewed immunosuppression during pregnancy, Nat. Microbiol., 2, 1558, 10.1038/s41564-017-0016-3 · DOI
  66. Nair, 2013, Role of inflammatory proteins S100A8 and S100A9 in pathophysiology of recurrent early pregnancy loss, Placenta, 34, 824, 10.1016/j.placenta.2013.06.307 · DOI
  67. Schenten, 2018, Secretion of the Phosphorylated Form of S100A9 from Neutrophils Is Essential for the Proinflammatory Functions of Extracellular S100A8/A9, Front. Immunol., 9, 447, 10.3389/fimmu.2018.00447 · DOI
  68. Oehmcke-Hecht, 2018, Interaction of the Human Contact System with Pathogens—An Update, Front. Immunol., 9, 312, 10.3389/fimmu.2018.00312 · DOI
  69. Ray, 2012, Serum proteome changes in dengue virus-infected patients from a dengue-endemic area of India: towards new molecular targets?, OMICS, 16, 10.1089/omi.2012.0037 · DOI
  70. Martin, 1992, Increased phosphate content of fibrinogen in vivo correlates with alteration in fibrinogen behaviour, Thromb. Res., 68, 467, 10.1016/0049-3848(92)90059-J · DOI
  71. de Vries, 2020, Effects of Post-Translational Modifications of Fibrinogen on Clot Formation, Clot Structure, and Fibrinolysis: A Systematic Review, Arterioscler., Thromb., Vasc. Biol., 40, 554, 10.1161/ATVBAHA.119.313626 · DOI
  72. Lee, 2011, Investigation and identification of protein γ-glutamyl carboxylation sites, BMC Bioinf., 12, S10, 10.1186/1471-2105-12-S13-S10 · DOI
  73. Li, 2010, Reversible Post-Translational Carboxylation Modulates The Enzymatic Activity Of N-Acetyl-L-Ornithine Transcarbamylase, Biochemistry, 49, 6887, 10.1021/bi1007386 · DOI
  74. Jimenez-Morales, 2013, Lysine carboxylation: unveiling a spontaneous post-translational modification, Acta Crystallogr., Sect. D: Biol. Crystallogr., 70, 48, 10.1107/S139900471302364X · DOI
  75. Bukowska, 2015, The effect of catechol on human peripheral blood mononuclear cells (in vitro study), Environ. Toxicol. Pharmacol., 39, 187, 10.1016/j.etap.2014.11.017 · DOI
  76. Choe, 2003, Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120, Cell., 114, 161, 10.1016/S0092-8674(03)00508-7 · DOI
  77. Larsen, 2006, Analysis of posttranslational modifications of proteins by tandem mass spectrometry, Biotechniques, 40, 790, 10.2144/000112201 · DOI
  78. Oriá, 2005, APOE4 Protects the Cognitive Development in Children with Heavy Diarrhea Burdens in Northeast Brazil, Pediatr. Res., 57, 310, 10.1203/01.PDR.0000148719.82468.CA · DOI
  79. Geffin, 2017, Apolipoprotein E4 Suppresses Neuronal-Specific Gene Expression in Maturing Neuronal Progenitor Cells Exposed to HIV, J. Neuroimmune Pharmacol., 12, 462, 10.1007/s11481-017-9734-9 · DOI
  80. Braga, 2010, Apolipoprotein E genotype and cerebral palsy, Dev. Med. Child Neurol., 52, 666, 10.1111/j.1469-8749.2009.03465.x · DOI
  81. Kuroda, 2007, Association of Apolipoprotein E Genotype and Cerebral Palsy in Children, Pediatrics, 119, 306, 10.1542/peds.2006-1083 · DOI
  82. Wong, 2010, Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I, Proc. Natl. Acad. Sci. U. S. A., 107, 1977, 10.1073/pnas.0910136107 · DOI
  83. Shao, 2008, Methionine oxidation impairs reverse cholesterol transport by apolipoprotein A-I, Proc. Natl. Acad. Sci. U. S. A., 105, 12224, 10.1073/pnas.0802025105 · DOI
  84. Li, 2013, Human Apolipoprotein A-I Is Associated with Dengue Virus and Enhances Virus Infection through SR-BI, PLoS One, 8, 10.1371/journal.pone.0070390 · DOI
  85. Osuna-Ramos, 2018, The Role of Host Cholesterol During Flavivirus Infection, Front. Cell. Infect. Microbiol., 8, 388, 10.3389/fcimb.2018.00388 · DOI
  86. Mellors, 2020, Viral Evasion of the Complement System and Its Importance for Vaccines and Therapeutics, Front. Immunol., 11, 1450, 10.3389/fimmu.2020.01450 · DOI
  87. Stadtman, 2003, Oxidation of Methionine Residues of Proteins: Biological Consequences, Antioxid. Redox Signaling, 5, 577, 10.1089/152308603770310239 · DOI
  88. Chen, 2020, Metabolic reprogramming by Zika virus provokes inflammation in human placenta, Nat. Commun., 11, 2967, 10.1038/s41467-020-16754-z · DOI
  89. van de Bovenkamp, 2016, The Emerging Importance of IgG Fab Glycosylation in Immunity, J. Immunology, 196, 1435, 10.4049/jimmunol.1502136 · DOI
  90. Parekh, 1985, Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG, Nature, 316, 452, 10.1038/316452a0 · DOI · Paper page
  91. Maverakis, 2015, Glycans in the immune system and The Altered Glycan Theory of Autoimmunity: a critical review, J. Autoimmun., 57, 1, 10.1016/j.jaut.2014.12.002 · DOI
  92. Henderson, 2020, Shilman, Investigation of the immunogenicity of Zika glycan loop, Virol. J., 17, 43, 10.1186/s12985-020-01313-1 · DOI
  93. Giglio, 2020, Recent Updates and Advances in the Use of Glycated Albumin for the Diagnosis and Monitoring of Diabetes and Renal, Cerebro- and Cardio-Metabolic Diseases, J. Clin. Med. Res., 9, E3634
  94. Mittal, 2017, Zika Virus: An Emerging Global Health Threat, Front. Cell. Infect. Microbiol., 7, 486, 10.3389/fcimb.2017.00486 · DOI
  95. Suwarto, 2016, Dengue score: a proposed diagnostic predictor for pleural effusion and/or ascites in adults with dengue infection, BMC Infect. Dis., 16, 322, 10.1186/s12879-016-1671-3 · DOI

Metadata

Authors
Allgoewer, K., Wu, S., Choi, H., & Vogel, C.
Affiliations
  • Humboldt-Universität zu Berlin (DE)
  • New York University (US)
  • National University of Singapore (SG)
Corresponding author
Vogel, Christine
Venue
Molecular Omics
Published
2023-02-15
Volume
19
Issue
4
Pages
308-320
ISSN
2515-4184 (ISSN-L)
OpenAlex
W4320925155
Cited by
5
References
1
Citations by year
2026: 1 · 2025: 3 · 2024: 1
FWCI
0.46
Type
journal article
Language
en
Open access
Locations
  • Molecular Omics (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of General Medical Sciences (R35GM127089)
  • National Institute of Allergy and Infectious Diseases (75N93019C00052/NH/NIH HHS/United States)
Topics
  • Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
Keywords
Zika virus, dengue virus, flavivirus infection, post-translational modification, serum proteomics, mass spectrometry, phosphorylation, methionine oxidation, glycosylation, sulfation, carboxylation, apolipoproteins, immunoglobulins, host response to viral infection
MeSH terms
Zika Virus Infection, Zika Virus, Dengue, Dengue Virus, Humans, Protein Processing, Post-Translational, Proteomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review