Skip to main content

Proteomics

  • Chapter
  • First Online:
Molecular Parasitology
  • 1471 Accesses

Abstract

Systems biology integrates high-throughput molecular sciences such as genomics, proteomics, metabolomics and glycomics to advance our understanding on pathways, functional nodules and large-scale organisation (Oltvai and Barabasi, Science. 298(5594):763–764, 2002). Developed in the late 1990s, proteomics is now established as one of the pillars of ‘systems biology’. Strategies to characterise the abundance, stability and modification status of proteins, the functional molecules of the cell, are of great interest to enhance our understanding of how cells function and communicate. Proteomic approaches have been exploited extensively by the protozoan parasitology field. In this chapter, we review the present state of proteomic research in protozoan parasites and discuss how various proteomic platforms combined with advanced bioinformatic tools have been used to enhance our understanding of specific biological questions in host-parasite interaction systems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abay ET, van der Westhuizen JH, Swart KJ, Gibhard L, Tukulula M, Chibale K, Wiesner L (2014) The development and validation of an LC-MS/MS method for the determination of a new anti-malarial compound (TK900D) in human whole blood and its application to pharmacokinetic studies in mice. Malar J 13:42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 422(6928):198–207

    Article  CAS  PubMed  Google Scholar 

  • Altelaar AF, Munoz J, Heck AJ (2013) Next-generation proteomics: towards an integrative view of proteome dynamics. Nat Rev Genet 14(1):35–48

    Article  CAS  PubMed  Google Scholar 

  • Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, Carrington M, Depledge DP, Fischer S, Gajria B, Gao X, Gardner MJ, Gingle A, Grant G, Harb OS, Heiges M, Hertz-Fowler C, Houston R, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Logan FJ, Miller JA, Mitra S, Myler PJ, Nayak V, Pennington C, Phan I, Pinney DF, Ramasamy G, Rogers MB, Roos DS, Ross C, Sivam D, Smith DF, Srinivasamoorthy G, Stoeckert CJ Jr, Subramanian S, Thibodeau R, Tivey A, Treatman C, Velarde G, Wang H (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38(Database issue):D457–D462

    Article  CAS  PubMed  Google Scholar 

  • Attwood TK, Bradley P, Flower DR, Gaulton A, Maudling N, Mitchell AL, Moulton G, Nordle A, Paine K, Taylor P, Uddin A, Zygouri C (2003) PRINTS and its automatic supplement, prePRINTS. Nucleic Acids Res 31(1):400–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atwood JA 3rd, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, Tarleton RL (2005) The Trypanosoma cruzi proteome. Science 309(5733):473–476

    Article  CAS  PubMed  Google Scholar 

  • Aurrecoechea C, Brestelli J, Brunk BP, Carlton JM, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Morrison HG, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ Jr, Sullivan S, Treatman C, Wang H (2009a) GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res 37(Database issue):D526–D530

    Article  CAS  PubMed  Google Scholar 

  • Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ Jr, Treatman C, Wang H (2009b) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37(Database issue):D539–D543

    Article  CAS  PubMed  Google Scholar 

  • Aurrecoechea C, Brestelli J, Brunk BP, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer ET, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Srinivasamoorthy G, Stoeckert CJ Jr, Thibodeau R, Treatman C, Wang H (2010) EuPathDB: a portal to eukaryotic pathogen databases. Nucleic Acids Res 38(Database issue):D415–D419

    Article  CAS  PubMed  Google Scholar 

  • Baxt LA, Baker RP, Singh U, Urban S (2008) An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion. Genes Dev 22(12):1636–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck M, Claassen M, Aebersold R (2011) Comprehensive proteomics. Curr Opin Biotechnol 22:3–8

    Article  CAS  PubMed  Google Scholar 

  • Bender A, van Dooren GG, Ralph SA, McFadden GI, Schneider G (2003) Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol Biochem Parasitol 132(2):59–66

    Article  CAS  PubMed  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340(4):783–795

    Article  PubMed  CAS  Google Scholar 

  • Bertsch A, Jung S, Zerck A, Pfeifer N, Nahnsen S, Henneges C, Nordheim A, Kohlbacher O (2010) Optimal de novo design of MRM experiments for rapid assay development in targeted proteomics. J Proteome Res 9(5):2696–2704

    Article  CAS  PubMed  Google Scholar 

  • Bradley PJ, Ward C, Cheng SJ, Alexander DL, Coller S, Coombs GH, Dunn JD, Ferguson DJ, Sanderson SJ, Wastling JM, Boothroyd JC (2005) Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J Biol Chem 280(40):34245–34258

    Article  CAS  PubMed  Google Scholar 

  • Briolant S, Almeras L, Belghazi M, Boucomont-Chapeaublanc E, Wurtz N, Fontaine A, Granjeaud S, Fusaï T, Rogier C, Pradines B (2010) Plasmodium falciparum proteome changes in response to doxycycline treatment. Malar J 9:141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brownridge P, Beynon RJ (2011) The importance of the digest: proteolysis and absolute quantification in proteomics. Methods 54(4):351–360

    Article  CAS  PubMed  Google Scholar 

  • Butter F, Bucerius F, Michel M, Cicova Z, Mann M, Janzen CJ (2013) Comparative proteomics of two life cycle stages of stable isotope-labeled Trypanosoma brucei reveals novel components of the parasite’s host adaptation machinery. Mol Cell Proteomics 12(1):172–179

    Article  PubMed  CAS  Google Scholar 

  • Caspi R, Altman T, Dreher K, Fulcher CA, Subhraveti P, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Ong Q, Paley S, Pujar A, Shearer AG, Travers M, Weerasinghe D, Zhang P, Karp PD (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42(Database issue):D459–D471

    Article  CAS  PubMed  Google Scholar 

  • Chawla B, Jhingran A, Panigrahi A, Stuart KD, Madhubala R (2011) Paromomycin affects translation and vesicle-mediated trafficking as revealed by proteomics of paromomycin -susceptible -resistant Leishmania donovani. PLoS One 6, e26660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Che FY, Madrid-Aliste C, Burd B, Zhang H, Nieves E, Kim K, Fiser A, Angeletti RH, Weiss LM (2011) Comprehensive proteomic analysis of membrane proteins in Toxoplasma gondii. Mol Cell Proteomics 10(1):M110 000745

    Article  PubMed  CAS  Google Scholar 

  • Choe L, D’Ascenzo M, Relkin NR, Pappin D, Ross P, Williamson B, Guertin S, Pribil P, Lee KH (2007) 8-plex quantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer’s disease. Proteomics 7(20):3651–3660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen AM, Rumpel K, Coombs GH, Wastling JM (2002) Characterisation of global protein expression by two-dimensional electrophoresis and mass spectrometry: proteomics of Toxoplasma gondii. Int J Parasitol 32(1):39–51

    Article  CAS  PubMed  Google Scholar 

  • Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26(12):1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Cox J, Mann M (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 80:273–299

    Article  CAS  PubMed  Google Scholar 

  • Craig R, Cortens JP, Beavis RC (2004) Open source system for analyzing, validating, and storing protein identification data. J Proteome Res 3(6):1234–1242

    Article  CAS  PubMed  Google Scholar 

  • Croft D, O’Kelly G, Wu G, Haw R, Gillespie M, Matthews L, Caudy M, Garapati P, Gopinath G, Jassal B, Jupe S, Kalatskaya I, Mahajan S, May B, Ndegwa N, Schmidt E, Shamovsky V, Yung C, Birney E, Hermjakob H, D’Eustachio P, Stein L (2011) Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res 39(Database issue):D691–D697

    Article  CAS  PubMed  Google Scholar 

  • de Godoy LMF, Olsen JV, Cox J, Nielsen ML, Hubner NC, Fröhlich F, Walther TC, Mann M (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455:1251–1254

    Article  PubMed  CAS  Google Scholar 

  • de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C (2009) Global signatures of protein and mRNA expression levels. Mol Biosyst 5(12):1512–1526

    PubMed  Google Scholar 

  • Desiere F, Deutsch EW, King NL, Nesvizhskii AI, Mallick P, Eng J, Chen S, Eddes J, Loevenich SN, Aebersold R (2006) The PeptideAtlas project. Nucleic Acids Res 34(Database issue):D655–D658

    Article  CAS  PubMed  Google Scholar 

  • Doherty MK, Hammond DE, Clague MJ, Gaskell SJ, Beynon RJ (2009) Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J Proteome Res 8(1):104–112

    Article  CAS  PubMed  Google Scholar 

  • Doliwa C, Xia D, Escotte-Binet S, Newsham EL, Sanya JS, Aubert D, Randle N, Wastling JM, Villena I (2013) Identification of differentially expressed proteins in sulfadiazine resistant and sensitive strains of Toxoplasma gondii using difference-gel electrophoresis (DIGE). Int J Parasitol Drugs Drug Resist 3:35–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Dowse TJ, Soldati D (2005) Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature. Trends Parasitol 21(6):254–258

    Article  CAS  PubMed  Google Scholar 

  • Dybas JM, Madrid-Aliste CJ, Che FY, Nieves E, Rykunov D, Angeletti RH, Weiss LM, Kim K, Fiser A (2008) Computational analysis and experimental validation of gene predictions in Toxoplasma gondii. PLoS One 3(12), e3899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emery SJ, Lacey E, Haynes PA (2015) Quantitative proteomic analysis of Giardia duodenalis assemblage A: A baseline for host, assemblage, and isolate variation. Proteomics 15(13):2281–2285

    Article  CAS  PubMed  Google Scholar 

  • Emmer BT, Nakayasu ES, Souther C, Choi H, Sobreira TJ, Epting CL, Nesvizhskii AI, Almeida IC, Engman DM (2011) Global analysis of protein palmitoylation in African trypanosomes. Eukaryot Cell 10(3):455–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyford BA, Sakurai T, Smith D, Loveless B, Hertz-Fowler C, Donelson JE, Inoue N, Pearson TW (2011) Differential protein expression throughout the life cycle of Trypanosoma congolense, a major parasite of cattle in Africa. Mol Biochem Parasitol 177:116–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J, Saha S, Barker G, Heesom KJ, Ghali F, Jones AR, Matthews DA, Bessant C (2015) Galaxy Integrated Omics: web-based standards-compliant workflows for proteomics informed by transcriptomics. Mol Cell Proteomics 14(11):3087–3093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farrah T, Deutsch EW, Kreisberg R, Sun Z, Campbell DS, Mendoza L, Kusebauch U, Brusniak MY, Huttenhain R, Schiess R, Selevsek N, Aebersold R, Moritz RL (2012) PASSEL: the PeptideAtlas SRMexperiment library. Proteomics 12(8):1170–1175

    Article  CAS  PubMed  Google Scholar 

  • Faso C, Bischof S, Hehl AB (2013) The proteome landscape of Giardia lamblia encystation. PLoS One 8(12), e83207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fauquenoy S, Morelle W, Hovasse A, Bednarczyk A, Slomianny C, Schaeffer C, Van Dorsselaer A, Tomavo S (2008) Proteomics and glycomics analyses of N-glycosylated structures involved in Toxoplasma gondii – host cell interactions. Mol Cell Proteomics 7(5):891–910

    Article  CAS  PubMed  Google Scholar 

  • Ferella M, Nilsson D, Darban H, Rodrigues C, Bontempi EJ, Docampo R, Andersson B (2008) Proteomics in Trypanosoma cruzi – localization of novel proteins to various organelles. Proteomics 8(13):2735–2749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36(Database issue):D281–D288

    CAS  PubMed  Google Scholar 

  • Fleckenstein MC, Reese ML, Konen-Waisman S, Boothroyd JC, Howard JC, Steinfeldt T (2012) A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol 10(7), e1001358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florens L, Liu X, Wang Y, Yang S, Schwartz O, Peglar M, Carucci DJ, Yates JR 3rd, Wu Y (2004) Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol Biochem Parasitol 135(1):1–11

    Article  CAS  PubMed  Google Scholar 

  • Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419(6906):520–526

    Article  CAS  PubMed  Google Scholar 

  • Fritz HM, Bowyer PW, Bogyo M, Conrad PA, Boothroyd JC (2012) Proteomic analysis of fractionated Toxoplasma oocysts reveals clues to their environmental resistance. PLoS One 7(1), e29955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, Gao X, Heiges M, Iodice J, Kissinger JC, Mackey AJ, Pinney DF, Roos DS, Stoeckert CJ Jr, Wang H, Brunk BP (2008) ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Res 36(Database issue):D553–D556

    CAS  PubMed  Google Scholar 

  • Ghali F, Krishna R, Perkins S, Collins A, Xia D, Wastling J, Jones AR (2014) ProteoAnnotator – open source proteogenomics annotation software supporting PSI standards. Proteomics 14(23-24):2731–2741

    Article  CAS  PubMed  Google Scholar 

  • Gierasch LM (1989) Signal sequences. Biochemistry 28(3):923–930

    Article  CAS  PubMed  Google Scholar 

  • Goecks J, Nekrutenko A, Taylor J, Galaxy T (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11(8):R86

    Article  PubMed  PubMed Central  Google Scholar 

  • Grossmann J, Roschitzki B, Panse C, Fortes C, Barkow-Oesterreicher S, Rutishauser D, Schlapbach R (2010) Implementation and evaluation of relative and absolute quantification in shotgun proteomics with label-free methods. J Proteomics 73(9):1740–1746

    Article  CAS  PubMed  Google Scholar 

  • Guther ML, Urbaniak MD, Tavendale A, Prescott A, Ferguson MA (2014) High-confidence glycosome proteome for procyclic form Trypanosoma brucei by epitope-tag organelle enrichment and SILAC proteomics. J Proteome Res 13(6):2796–2806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17(10):994–999

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hakimi MA, Deitsch KW (2007) Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr Opin Microbiol 10(4):357–362

    Article  CAS  PubMed  Google Scholar 

  • Heiges M, Wang H, Robinson E, Aurrecoechea C, Gao X, Kaluskar N, Rhodes P, Wang S, He CZ, Su Y, Miller J, Kraemer E, Kissinger JC (2006) CryptoDB: a Cryptosporidium bioinformatics resource update. Nucleic Acids Res 34(Database issue):D419–D422

    Article  CAS  PubMed  Google Scholar 

  • Hem S, Gherardini PF, Osorio y Fortéa J, Hourdel V, Morales MA, Watanabe R, Pescher P, Kuzyk MA, Smith D, Borchers CH, Zilberstein D, Helmer-Citterich M, Namane A, Späth GF (2010) Identification of Leishmania-specific protein phosphorylation sites by LC-ESI-MS/MS and comparative genomics analyses. Proteomics 10:3868–3883

    Article  CAS  PubMed  Google Scholar 

  • Hu K, Johnson J, Florens L, Fraunholz M, Suravajjala S, DiLullo C, Yates J, Roos DS, Murray JM (2006) Cytoskeletal components of an invasion machine – the apical complex of Toxoplasma gondii. PLoS Pathog 2(2), e13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huhn C, Ruhaak LR, Wuhrer M, Deelder AM (2011) Hexapeptide library as a universal tool for sample preparation in protein glycosylation analysis. J Proteomics

    Google Scholar 

  • Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4(9):1265–1272

    Article  CAS  PubMed  Google Scholar 

  • Jackson AP, Goyard S, Xia D, Foth BJ, Sanders M, Wastling JM, Minoprio P, Berriman M (2015) Global gene expression profiling through the complete life cycle of trypanosoma vivax. PLoS Negl Trop Dis 9(8), e0003975

    Article  PubMed  PubMed Central  Google Scholar 

  • Jackson AP, Otto TD, Darby A, Ramaprasad A, Xia D, Echaide IE, Farber M, Gahlot S, Gamble J, Gupta D, Gupta Y, Jackson L, Malandrin L, Malas TB, Moussa E, Nair M, Reid AJ, Sanders M, Sharma J, Tracey A, Quail MA, Weir W, Wastling JM, Hall N, Willadsen P, Lingelbach K, Shiels B, Tait A, Berriman M, Allred DR, Pain A (2014) The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction. Nucleic Acids Res 42(11):7113–7131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jedelský PL, Doležal P, Rada P, Pyrih J, Smíd O, Hrdý I, Sedinová M, Marcinčiková M, Voleman L, Perry AJ, Beltrán NC, Lithgow T, Tachezy J (2011) The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One 6, e17285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiao X, Sherman BT, Huang da W, Stephens R, Baseler MW, Lane HC, Lempicki RA (2012) DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics 28(13):1805–1806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones P, Cote RG, Martens L, Quinn AF, Taylor CF, Derache W, Hermjakob H, Apweiler R (2006) PRIDE: a public repository of protein and peptide identifications for the proteomics community. Nucleic Acids Res 34(Database issue):D659–D663

    Article  CAS  PubMed  Google Scholar 

  • Jortzik E, Wang L, Becker K (2011) Thiol-based posttranslational modifications in parasites. Antioxid Redox Signal 17(4):657–673

    Article  CAS  Google Scholar 

  • Jovanovic M, Rooney MS, Mertins P, Przybylski D, Chevrier N, Satija R, Rodriguez EH, Fields AP, Schwartz S, Raychowdhury R, Mumbach MR, Eisenhaure T, Rabani M, Gennert D, Lu D, Delorey T, Weissman JS, Carr SA, Hacohen N, Regev A (2015) Immunogenetics. Dynamic profiling of the protein life cycle in response to pathogens. Science 347(6226):1259038

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Pevzner PA (2014) MS-GF+ makes progress towards a universal database search tool for proteomics. Nat Commun 5:5277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kooij TW, Janse CJ, Waters AP (2006) Plasmodium post-genomics: better the bug you know? Nat Rev Microbiol 4(5):344–357

    Article  CAS  PubMed  Google Scholar 

  • Krishna R, Xia D, Sanderson S, Shanmugasundram A, Vermont S, Bernal A, Daniel-Naguib G, Ghali F, Brunk BP, Roos DS, Wastling JM, Jones AR (2015) A large-scale proteogenomics study of apicomplexan pathogens-Toxoplasma gondii and Neospora caninum. Proteomics 15(15):2618–2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krogh A, Brown M, Mian IS, Sjolander K, Haussler D (1994) Hidden Markov models in computational biology. Applications to protein modeling. J Mol Biol 235(5):1501–1531

    Article  CAS  PubMed  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580

    Article  CAS  PubMed  Google Scholar 

  • Kuss C, Gan CS, Gunalan K, Bozdech Z, Sze SK, Preiser PR (2011) Quantitative proteomics reveals new insights into erythrocyte invasion by Plasmodium falciparum. Mol Cell Proteomics MCP 11:M111.010645-

    Article  PubMed  CAS  Google Scholar 

  • LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, Schoenfeld LW, Ota I, Sahasrabudhe S, Kurschner C, Fields S, Hughes RE (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438:103–107

    Article  CAS  PubMed  Google Scholar 

  • Lange V, Picotti P, Domon B, Aebersold R (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4:222

    Article  PubMed  PubMed Central  Google Scholar 

  • Lasonder E, Ishihama Y, Andersen JS, Vermunt AM, Pain A, Sauerwein RW, Eling WM, Hall N, Waters AP, Stunnenberg HG, Mann M (2002) Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419(6906):537–542

    Article  CAS  PubMed  Google Scholar 

  • Le Roch KG, Johnson JR, Florens L, Zhou Y, Santrosyan A, Grainger M, Yan SF, Williamson KC, Holder AA, Carucci DJ, Yates JR 3rd, Winzeler EA (2004) Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res 14(11):2308–2318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lees J, Yeats C, Perkins J, Sillitoe I, Rentzsch R, Dessailly BH, Orengo C (2012) Gene3D: a domain-based resource for comparative genomics, functional annotation and protein network analysis. Nucleic Acids Res 40(Database issue):D465–D471

    Article  CAS  PubMed  Google Scholar 

  • Lefevre T, Thomas F, Schwartz A, Levashina E, Blandin S, Brizard J-P, Le Bourligu L, Demettre E, Renaud F, Biron DG (2007) Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host. Proteomics 7:1908–1915

    Article  CAS  PubMed  Google Scholar 

  • Lepenies B, Seeberger PH (2010) The promise of glycomics, glycan arrays and carbohydrate-based vaccines. Immunopharmacol Immunotoxicol 32:196–207

    Article  CAS  PubMed  Google Scholar 

  • Leykauf K, Treeck M, Gilson PR, Nebl T, Braulke T, Cowman AF, Gilberger TW, Crabb BS (2010) Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite. PLoS Pathog 6, e1000941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li JJ, Bickel PJ, Biggin MD (2014) System wide analyses have underestimated protein abundances and the importance of transcription in mammals. Peer J 2, e270

    Article  PubMed  PubMed Central  Google Scholar 

  • Li JJ, Biggin MD (2015) Gene expression. Statistics requantitates the central dogma. Science 347(6226):1066–1067

    Article  CAS  PubMed  Google Scholar 

  • Lonardi E, Balog CI, Deelder AM, Wuhrer M (2010) Natural glycan microarrays. Expert Rev Proteomics 7:761–774

    Article  CAS  PubMed  Google Scholar 

  • Lorestani A, Ivey FD, Thirugnanam S, Busby MA, Marth GT, Cheeseman IM, Gubbels MJ (2012) Targeted proteomic dissection of Toxoplasma cytoskeleton sub-compartments using MORN1. Cytoskeleton (Hoboken) 69(12):1069–1085

    Article  CAS  Google Scholar 

  • Lu P, Vogel C, Wang R, Yao X, Marcotte EM (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 25(1):117–124

    Article  CAS  PubMed  Google Scholar 

  • Magnuson ML, Owens JH, Kelty CA (2000) Characterization of Cryptosporidium parvum by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl Environ Microbiol 66(11):4720–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier T, Guell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583(24):3966–3973

    Article  CAS  PubMed  Google Scholar 

  • Mallick P, Kuster B (2010) Proteomics: a pragmatic perspective. Nat Biotechnol 28(7):695–709

    Article  CAS  PubMed  Google Scholar 

  • Marugán-Hernández V, Alvarez-García G, Risco-Castillo V, Regidor-Cerrillo J, Ortega-Mora LM (2010) Identification of Neospora caninum proteins regulated during the differentiation process from tachyzoite to bradyzoite stage by DIGE. Proteomics 10:1740–1750

    Article  PubMed  CAS  Google Scholar 

  • Marx V (2013) Targeted proteomics. Nat Methods 10(1):19–22

    Article  CAS  PubMed  Google Scholar 

  • McAlister GC, Huttlin EL, Haas W, Ting L, Jedrychowski MP, Rogers JC, Kuhn K, Pike I, Grothe RA, Blethrow JD, Gygi SP (2012) Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses. Anal Chem 84(17):7469–7478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mi H, Guo N, Kejariwal A, Thomas PD (2007) PANTHER version 6: protein sequence and function evolution data with expanded representation of biological pathways. Nucleic Acids Res 35(Database issue):D247–D252

    Article  CAS  PubMed  Google Scholar 

  • Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Paabo S, Mann M (2011) Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol 7:548

    Article  PubMed  PubMed Central  Google Scholar 

  • Nebl T, Prieto JH, Kapp E, Smith BJ, Williams MJ, Yates JR, Cowman AF, Tonkin CJ (2011) Quantitative in vivo analyses reveal calcium-dependent phosphorylation sites and identifies a novel component of the toxoplasma invasion motor complex. PLoS Pathog 7, e1002222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson MM, Jones AR, Carmen JC, Sinai AP, Burchmore R, Wastling JM (2008) Modulation of the host cell proteome by the intracellular apicomplexan parasite Toxoplasma gondii. Infect Immun 76(2):828–844

    Article  CAS  PubMed  Google Scholar 

  • Nesvizhskii AI (2014) Proteogenomics: concepts, applications and computational strategies. Nat Methods 11(11):1114–1125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nett IR, Martin DM, Miranda-Saavedra D, Lamont D, Barber JD, Mehlert A, Ferguson MA (2009) The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol Cell Proteomics 8(7):1527–1538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes MC, Okada M, Scheidig-Benatar C, Cooke BM, Scherf A (2010) Plasmodium falciparum FIKK kinase members target distinct components of the erythrocyte membrane. PLoS One 5, e11747

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Donnell RA, Hackett F, Howell SA, Treeck M, Struck N, Krnajski Z, Withers-Martinez C, Gilberger TW, Blackman MJ (2006) Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 174(7):1023–1033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oates ME, Stahlhacke J, Vavoulis DV, Smithers B, Rackham OJ, Sardar AJ, Zaucha J, Thurlby N, Fang H, Gough J (2015) The SUPERFAMILY 1.75 database in 2014: a doubling of data. Nucleic Acids Res 43(Database issue):D227–D233

    Article  PubMed  Google Scholar 

  • Olsen JV, Mann M (2013) Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol Cell Proteomics 12(12):3444–3452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oltvai ZN, Barabasi AL (2002) Systems biology. Life’s complexity pyramid. Science 298(5594):763–764

    Article  CAS  PubMed  Google Scholar 

  • Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1(5):376–386

    Article  CAS  PubMed  Google Scholar 

  • Palagi PM, Walther D, Quadroni M, Catherinet S, Burgess J, Zimmermann-Ivol CG, Sanchez JC, Binz PA, Hochstrasser DF, Appel RD (2005) MSight: an image analysis software for liquid chromatography-mass spectrometry. Proteomics 5(9):2381–2384

    Article  CAS  PubMed  Google Scholar 

  • Pawar H, Renuse S, Khobragade SN, Chavan S, Sathe G, Kumar P, Mahale KN, Gore K, Kulkarni A, Dixit T, Raju R, Prasad TS, Harsha HC, Patole MS, Pandey A (2014) Neglected tropical diseases and omics science: proteogenomics analysis of the promastigote stage of Leishmania major parasite. OMICS 18(8):499–512

    Article  CAS  PubMed  Google Scholar 

  • Perez-Riverol Y, Alpi E, Wang R, Hermjakob H, Vizcaino JA (2015) Making proteomics data accessible and reusable: current state of proteomics databases and repositories. Proteomics 15(5-6):930–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20(18):3551–3567

    Article  CAS  PubMed  Google Scholar 

  • Peterson AC, Russell JD, Bailey DJ, Westphall MS, Coon JJ (2012) Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol Cell Proteomics 11(11):1475–1488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pierce A, Unwin RD, Evans CA, Griffiths S, Carney L, Zhang L, Jaworska E, Lee CF, Blinco D, Okoniewski MJ, Miller CJ, Bitton DA, Spooncer E, Whetton AD (2008) Eight-channel iTRAQ enables comparison of the activity of six leukemogenic tyrosine kinases. Mol Cell Proteomics 7(5):853–863

    Article  CAS  PubMed  Google Scholar 

  • Pineyro MD, Parodi-Talice A, Portela M, Arias DG, Guerrero SA, Robello C (2011) Molecular characterization and interactome analysis of Trypanosoma cruzi tryparedoxin 1. J Proteomics 74(9):1683–1692

    Article  CAS  PubMed  Google Scholar 

  • Prieto JH, Koncarevic S, Park SK, Yates J, Becker K (2008) Large-scale differential proteome analysis in Plasmodium falciparum under drug treatment. PLoS One 3, e4098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rebello KM, Barros JSL, Mota EM, Carvalho PC, Perales J, Lenzi HL, Neves-Ferreira AGC (2011) Comprehensive proteomic profiling of adult Angiostrongylus costaricensis, a human parasitic nematode. J Proteomics 74:1545–1559

    Article  CAS  PubMed  Google Scholar 

  • Robertson G, Schein J, Chiu R, Corbett R, Field M, Jackman SD, Mungall K, Lee S, Okada HM, Qian JQ, Griffith M, Raymond A, Thiessen N, Cezard T, Butterfield YS, Newsome R, Chan SK, She R, Varhol R, Kamoh B, Prabhu AL, Tam A, Zhao Y, Moore RA, Hirst M, Marra MA, Jones SJ, Hoodless PA, Birol I (2010) De novo assembly and analysis of RNA-seq data. Nat Methods 7(11):909–912

    Article  CAS  PubMed  Google Scholar 

  • Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3(12):1154–1169

    Article  CAS  PubMed  Google Scholar 

  • Rukmangadachar LA, Kataria J, Hariprasad G, Samantaray JC, Srinivasan A (2011) Two-dimensional difference gel electrophoresis (DIGE) analysis of sera from visceral leishmaniasis patients. Clin Proteomics 8:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sam-Yellowe TY, Florens L, Wang T, Raine JD, Carucci DJ, Sinden R, Yates JR 3rd (2004) Proteome analysis of rhoptry-enriched fractions isolated from Plasmodium merozoites. J Proteome Res 3(5):995–1001

    Article  CAS  PubMed  Google Scholar 

  • Sanderson SJ, Xia D, Prieto H, Yates J, Heiges M, Kissinger JC, Bromley E, Lal K, Sinden RE, Tomley F, Wastling JM (2008) Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 8(7):1398–1414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473(7347):337–342

    Article  PubMed  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shock JL, Fischer KF, DeRisi JL (2007) Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol 8(7):R134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, Pagni M, Bairoch A, Bucher P (2002) PROSITE: a documented database using patterns and profiles as motif descriptors. Brief Bioinform 3(3):265–274

    Article  CAS  PubMed  Google Scholar 

  • Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, Foster LJ, Reiner NE (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9(2):R35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silvestrini F, Lasonder E, Olivieri A, Camarda G, van Schaijk B, Sanchez M, Younis Younis S, Sauerwein R, Alano P (2010) Protein export marks the early phase of gametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics MCP 9:1437–1448

    Article  CAS  PubMed  Google Scholar 

  • Smith LM, Kelleher NL, P. Consortium for Top Down (2013) Proteoform: a single term describing protein complexity. Nat Methods 10(3):186–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snelling WJ, Lin Q, Moore JE, Millar BC, Tosini F, Pozio E, Dooley JS, Lowery CJ (2007) Proteomics analysis and protein expression during sporozoite excystation of Cryptosporidium parvum (Coccidia, Apicomplexa). Mol Cell Proteomics 6(2):346–355

    Article  CAS  PubMed  Google Scholar 

  • Southworth PM, Hyde JE, Sims PFG (2011) A mass spectrometric strategy for absolute quantification of Plasmodium falciparum proteins of low abundance. Malar J 10:315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein LD, Mungall C, Shu S, Caudy M, Mangone M, Day A, Nickerson E, Stajich JE, Harris TW, Arva A, Lewis S (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12(10):1599–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturm M, Bertsch A, Gropl C, Hildebrandt A, Hussong R, Lange E, Pfeifer N, Schulz-Trieglaff O, Zerck A, Reinert K, Kohlbacher O (2008) OpenMS - an open-source software framework for mass spectrometry. BMC Bioinform 9:163

    Article  CAS  Google Scholar 

  • Surget-Groba Y, Montoya-Burgos JI (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res 20(10):1432–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemae H, Sugi T, Kobayashi K, Gong H, Ishiwa A, Recuenco FC, Murakoshi F, Iwanaga T, Inomata A, Horimoto T, Akashi H, Kato K (2013) Characterization of the interaction between Toxoplasma gondii rhoptry neck protein 4 and host cellular beta-tubulin. Sci Rep 3:3199

    Article  PubMed  PubMed Central  Google Scholar 

  • Thezenas ML, Huang H, Njie M, Ramaprasad A, Nwakanma DC, Fischer R, Digleria K, Walther M, Conway DJ, Kessler BM, Casals-Pascual C (2013) PfHPRT: a new biomarker candidate of acute Plasmodium falciparum infection. J Proteome Res 12(3):1211–1222

    Article  CAS  PubMed  Google Scholar 

  • Thompson A, Schafer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, Hamon C (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75(8):1895–1904

    Article  CAS  PubMed  Google Scholar 

  • Tiberti N, Hainard A, Lejon V, Robin X, Ngoyi DM, Turck N, Matovu E, Enyaru J, Ndung’u JM, Scherl A, Dayon L, Sanchez JC (2010) Discovery and verification of osteopontin and Beta-2-microglobulin as promising markers for staging human African trypanosomiasis. Mol Cell Proteomics 9(12):2783–2795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran JC, Zamdborg L, Ahlf DR, Lee JE, Catherman AD, Durbin KR, Tipton JD, Vellaichamy A, Kellie JF, Li M, Wu C, Sweet SM, Early BP, Siuti N, LeDuc RD, Compton PD, Thomas PM, Kelleher NL (2011) Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 480(7376):254–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treeck M, Sanders JL, Elias JE, Boothroyd JC (2011) The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites’ boundaries. Cell Host Microbe 10(4):410–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwin B, Conover D, Kalbfleisch T, Vijayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403(6770):623–627

    Article  CAS  PubMed  Google Scholar 

  • UniProt C (2015) UniProt: a hub for protein information. Nucleic Acids Res 43(Database issue):D204–D212

    Google Scholar 

  • Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18(11):2071–2077

    Article  CAS  PubMed  Google Scholar 

  • Urbaniak MD, Guther ML, Ferguson MA (2012) Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS One 7(5), e36619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma R, Tiwari A, Kaur S, Varshney GC, Raghava GP (2008) Identification of proteins secreted by malaria parasite into erythrocyte using SVM and PSSM profiles. BMC Bioinform 9:201

    Article  CAS  Google Scholar 

  • Villegas EN, Glassmeyer ST, Ware MW, Hayes SL, Schaefer FW 3rd (2006) Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry-based analysis of Giardia lamblia and Giardia muris. J Eukaryot Microbiol 53(Suppl 1):S179–S181

    Article  PubMed  Google Scholar 

  • Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O’Kelly G, Schoenegger A, Ovelleiro D, Perez-Riverol Y, Reisinger F, Rios D, Wang R, Hermjakob H (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41(Database issue):D1063–D1069

    Article  CAS  PubMed  Google Scholar 

  • von Heijne G (1990) The signal peptide. J Membr Biol 115(3):195–201

    Article  Google Scholar 

  • Wasinger VC, Cordwell SJ, Cerpa-Poljak A, Yan JX, Gooley AA, Wilkins MR, Duncan MW, Harris R, Williams KL, Humphery-Smith I (1995) Progress with gene-product mapping of the Mollicutes: mycoplasma genitalium. Electrophoresis 16(7):1090–1094

    Article  CAS  PubMed  Google Scholar 

  • Wastling JM, Xia D, Sohal A, Chaussepied M, Pain A, Langsley G (2009) Proteomes and transcriptomes of the Apicomplexa – where’s the message? Int J Parasitol 39(2):135–143

    Article  CAS  PubMed  Google Scholar 

  • Werner T, Becher I, Sweetman G, Doce C, Savitski MM, Bantscheff M (2012) High-resolution enabled TMT 8-plexing. Anal Chem 84(16):7188–7194

    Article  CAS  PubMed  Google Scholar 

  • Wiens O, Xia D, von Schubert C, Wastling JM, Dobbelaere DA, Heussler VT, Woods KL (2014) Cell cycle-dependent phosphorylation of Theileria annulata schizont surface proteins. PLoS One 9(7), e103821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkins MR (1994) 2D electrophoresis: from protein maps to genomes. First Siena conference, Siena

    Google Scholar 

  • Wilkins MR, Sanchez JC, Gooley AA, Appel RD, Humphery-Smith I, Hochstrasser DF, Williams KL (1996) Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev 13:19–50

    Article  CAS  PubMed  Google Scholar 

  • Wilson D, Madera M, Vogel C, Chothia C, Gough J (2007) The SUPERFAMILY database in 2007: families and functions. Nucleic Acids Res 35(Database issue):D308–D313

    Google Scholar 

  • Wu Y, Nelson MM, Quaile A, Xia D, Wastling JM, Craig A (2009) Identification of phosphorylated proteins in erythrocytes infected by the human malaria parasite Plasmodium falciparum. Malar J 8:105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia D, Sanderson SJ, Jones AR, Prieto JH, Yates JR, Bromley E, Tomley FM, Lal K, Sinden RE, Brunk BP, Roos DS, Wastling JM (2008) The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol 9(7):R116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yates JR 3rd, Eng JK, McCormack AL, Schieltz D (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67(8):1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Yeh YM, Huang KY, Richie Gan RC, Huang HD, Wang TC, Tang P (2013) Phosphoproteome profiling of the sexually transmitted pathogen Trichomonas vaginalis. J Microbiol Immunol Infect 46(5):366–373

    Article  CAS  PubMed  Google Scholar 

  • Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ (2008) Global protein stability profiling in mammalian cells. Science 322(5903):918–923

    Article  CAS  PubMed  Google Scholar 

  • Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26(13):1608–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Xin L, Shan B, Chen W, Xie M, Yuen D, Zhang W, Zhang Z, Lajoie GA, Ma B (2012) PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol Cell Proteomics 11(4):M111 010587

    Article  PubMed  CAS  Google Scholar 

  • Zhou XW, Blackman MJ, Howell SA, Carruthers VB (2004) Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex. Mol Cell Proteomics 3(6):565–576

    Article  CAS  PubMed  Google Scholar 

  • Zhou XW, Kafsack BF, Cole RN, Beckett P, Shen RF, Carruthers VB (2005) The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J Biol Chem 280(40):34233–34244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res 5(9):2339–2347

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are indebted to members of the Wastling laboratory for helpful comments in particular to Dr S. D. Armstrong for his critical review of the manuscript. JMW is supported by funding from the BBSRC and the Wellcome Trust.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan Wastling .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer-Verlag Wien

About this chapter

Cite this chapter

Wastling, J., Xia, D. (2016). Proteomics. In: Walochnik, J., Duchêne, M. (eds) Molecular Parasitology. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1416-2_2

Download citation

Publish with us

Policies and ethics