Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T11:51:42.325Z Has data issue: false hasContentIssue false
  • English
  • Français

Strategies to dissect parasite proteomes

Published online by Cambridge University Press:  20 February 2012

KARL BURGESS  and
RICHARD BURCHMORE
KARL BURGESS
Affiliation:
Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, G12 8QQ, UK
RICHARD BURCHMORE*
Affiliation:
Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, G12 8QQ, UK
*
*Corresponding author: Richard Burchmore, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Joseph Black Building, room B2-25, University of Glasgow, Glasgow G12 8QQ, UK. Tel: (+44) 141 330 8612. E-mail: richard.burchmore@glasgow.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Proteomes are complex and dynamic entities that are still poorly understood, but the application of proteomic technologies has become invaluable in many areas of biology, including parasitology. These technologies can be exploited to identify proteins in both complex or relatively simple samples, that formerly could only be characterized by targeted approaches such as Western blotting. Quantitative proteomic approaches can reveal modulations in protein expression that accompany phenotypes of interest. Proteomic approaches have been exploited to understand some of the molecular basis for host:parasite interactions and to elucidate phenotypes such as virulence, antigenicity and drug resistance. Many of the same technologies can also be more easily applied to targeted sub-proteomes.

Examples from several studies on pathogen proteomes and sub-proteomes, from bacteria to helminths, are presented to illustrate the potential and limitations of proteomic technologies.

Keywords

Proteomicsmass spectrometryphenotypic analysis
Type
Research Article
Information
Parasitology , Volume 139 , Issue 9: Symposia of the British Society for Parasitology Volume 48 Proteomic insights into parasite biology , August 2012 , pp. 1119 - 1130
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aggarwal, K., Choe, L. H. and Lee, K. H. (2006). Shotgun proteomics using the iTRAQ isobaric tags. Briefings in Functional Genomics and Proteomics 5, 112–120.Google Scholar
Alban, A., David, S. O., Bjorkesten, L., Andersson, C., Sloge, E., Lewis, S. and Currie, I. (2003). A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3, 36–44.Google Scholar
Appel, R. D., Hochstrasser, D. F., Funk, M., Vargas, J. R., Pellegrini, C., Muller, A. F. and Scherrer, J. R. (1991). The MELANIE project: from a biopsy to automatic protein map interpretation by computer. Electrophoresis 12, 722–735.CrossRefGoogle ScholarPubMed
Bantscheff, M., Scholten, A. and Heck, A. J. (2009). Revealing promiscuous drug-target interactions by chemical proteomics. Drug Discovery Today 14, 1021–1029.Google Scholar
Barrett, M. P., Tetaud, E., Seyfang, A., Bringaud, F. and Baltz, T. (1998). Trypanosome glucose transporters. Molecular and Biochemical Parasitology 91, 195–205.CrossRefGoogle ScholarPubMed
Bridges, D. J., Pitt, A. R., Hanrahan, O., Brennan, K., Voorheis, H. P., Herzyk, P., de Koning, H. P. and Burchmore, R. J. (2008). Characterisation of the plasma membrane subproteome of bloodstream form Trypanosoma brucei. Proteomics 8, 83–99.Google Scholar
Briolant, S., Almeras, L., Belghazi, M., Boucomont-Chapeaublanc, E., Wurtz, N., Fontaine, A., Granjeaud, S., Fusai, T., Rogier, C. and Pradines, B. (2010). Plasmodium falciparum proteome changes in response to doxycycline treatment. Malaria Journal 9, 141.Google Scholar
Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S., Hart, S. R., Portman, N., Shaw, M. K., Ginger, M. L., Gaskell, S. J., Mckean, P. G. and Gull, K. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224–227.Google Scholar
Colasante, C., Ellis, M., Ruppert, T. and Voncken, F. (2006). Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 6, 3275–3293.Google Scholar
Corthals, G. L., Wasinger, V. C., Hochstrasser, D. F. and Sanchez, J. C. (2000). The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21, 1104–1115.Google Scholar
Daneshvar, H., Wyllie, S., Phillips, S., Hagan, P. and Burchmore, R. (2012). Comparative proteomics profiling of a gentamicin-attenuated Leishmania infantum cell line identifies key changes in parasite thiol-redox metabolism. Journal of Proteomics 75, 1463–1471.Google Scholar
DeGrasse, J. A., Chait, B. T., Field, M. C. and Rout, M. P. (2008) High-yield isolation and subcellular proteomic characterization of nuclear and subnuclear structures from trypanosomes. Methods in Molecular Biology 463, 77–92.CrossRefGoogle ScholarPubMed
Foucher, A. L., McIntosh, A., Douce, G., Wastling, J., Tait, A. and Turner, C. M. (2006). A proteomic analysis of arsenical drug resistance in Trypanosoma brucei. Proteomics 6, 2726–2732.Google Scholar
Gorg, A., Weiss, W. and Dunn, M. J. (2004). Current two-dimensional electrophoresis technology for proteomics. Proteomics 4, 3665–3685.Google Scholar
Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F., Gelb, M. H. and Aebersold, R. (1999). Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nature Biotechnology 17, 994–999.Google Scholar
Gygi, S. P., Rist, B., Griffin, T. J., Eng, J. and Aebersold, R. (2002). Proteome analysis of low-abundance proteins using multidimensional chromatography and isotope-coded affinity tags. Journal of Proteome Research 1, 47–54.Google Scholar
Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T. W., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D., Churcher, C., Quail, M. A., Ormond, D., Doggett, J., Trueman, H. E., Mendoza, J., Bidwell, S. L., Rajandream, M. A., Carucci, D. J., Yates, J. R. III, Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M., Waters, A. P. and Sinden, R. E. (2005). A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82–86.Google Scholar
Hartinger, J., Stenius, K., Hogemann, D. and Jahn, R. (1996). 16-BAC/SDS-PAGE: a two-dimensional gel electrophoresis system suitable for the separation of integral membrane proteins. Analytical Biochemistry 240, 126–133.Google Scholar
Heck, A. J. and van den Heuvel, R. H. (2004). Investigation of intact protein complexes by mass spectrometry. Mass Spectrometry Reviews 23, 368–389.Google Scholar
Hernandez, P., Muller, M. and Appel, R. D. (2006). Automated protein identification by tandem mass spectrometry: issues and strategies. Mass Spectrometry Reviews 25, 235–254.Google Scholar
Hsu, J. L., Huang, S. Y. and Chen, S. H. (2006). Dimethyl multiplexed labeling combined with microcolumn separation and MS analysis for time course study in proteomics. Electrophoresis 27, 3652–3660.Google Scholar
Hsu, J. L., Huang, S. Y., Chow, N. H. and Chen, S. H. (2003). Stable-isotope dimethyl labeling for quantitative proteomics. Analytical Chemistry 75, 6843–6852.CrossRefGoogle ScholarPubMed
Johnson, K. L. and Muddiman, D. C. (2004). A method for calculating 16O/18O peptide ion ratios for the relative quantification of proteomes. Journal of the American Society for Mass Spectrometry 15, 437–445.Google Scholar
Jones, A., Faldas, A., Foucher, A., Hunt, E., Tait, A., Wastling, J. M. and Turner, C. M. (2006). Visualisation and analysis of proteomic data from the procyclic form of Trypanosoma brucei. Proteomics 6, 259–267.CrossRefGoogle ScholarPubMed
Kantawong, F., Burchmore, R., Gadegaard, N., Oreffo, R. O. and Dalby, M. J. (2008). Proteomic analysis of human osteoprogenitor response to disordered nanotopography. Journal of the Royal Society Interface 6, 1075–1086.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.Google Scholar
Mallick, P. and Kuster, B. (2010). Proteomics: a pragmatic perspective. Nature Biotechnology 28, 695–709.Google Scholar
McNamara, L. E., Dalby, M. J., Riehle, M. O. and Burchmore, R. (2010). Fluorescence two-dimensional difference gel electrophoresis for biomaterial applications. Journal of the Royal Society Interface 7 Suppl 1, S107–S118.Google Scholar
Miseta, A. and Csutora, P. (2000). Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Molecular Biology and Evolution 17, 1232–1239.CrossRefGoogle ScholarPubMed
Murphy, L., Eckersall, P. D., Bishop, S. C., Pettit, J. J., Huntley, J. F., Burchmore, R. and Stear, M. J. (2010). Genetic variation among lambs in peripheral IgE activity against the larval stages of Teladorsagia circumcincta. Parasitology 137, 1249–1260.CrossRefGoogle ScholarPubMed
Mutapi, F., Bourke, C., Harcus, Y., Midzi, N., Mduluza, T., Michael, ■., Turner, C., Burchmore, R. and Maizels, R. M. (2010). Differential recognition patterns of Schistosoma haematobium adult worm antigens by the human antibodies IgA, IgE, IgG1 and IgG4. Parasite Immunology 33, 181–192.Google Scholar
Mutapi, F., Burchmore, R., Mduluza, T., Midzi, N., Turner, C. M. and Maizels, R. M. (2008). Age-related and infection intensity-related shifts in antibody recognition of defined protein antigens in a schistosome-exposed population. Journal of Infectious Disease 198, 167–175.Google Scholar
Nelson, M. M., Jones, A. R., Carmen, J. C., Sinai, A. P., Burchmore, R. and Wastling, J. M. (2008). Modulation of the host cell proteome by the intracellular apicomplexan parasite Toxoplasma gondii. Infection and Immunity 76, 828–844.CrossRefGoogle ScholarPubMed
O'Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250, 4007–4021.Google Scholar
Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A. and Mann, M. (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular and Cellular Proteomics 1, 376–386.Google Scholar
Paape, D., Lippuner, C., Schmid, M., Ackermann, R., Barrios-Llerena, M. E., Zimny-Arndt, U., Brinkmann, V., Arndt, B., Pleissner, K. P., Jungblut, P. R. and Aebischer, T. (2008). Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Molecular and Cellular Proteomics 7, 1688–1701.Google Scholar
Palagi, P. M., Muller, M., Walther, D. and Lisacek, F. (2011). LC/MS data processing for label-free quantitative analysis. Methods in Molecular Biology 696, 369–377.Google Scholar
Palagi, P. M., Walther, D., Quadroni, M., Catherinet, S., Burgess, J., Zimmermann-Ivol, C. G., Sanchez, J. C., Binz, P. A., Hochstrasser, D. F. and Appel, R. D. (2005). MSight: an image analysis software for liquid chromatography-mass spectrometry. Proteomics 5, 2381–2384.CrossRefGoogle ScholarPubMed
Panchaud, A., Scherl, A., Shaffer, S. A., von Haller, P. D., Kulasekara, H. D., Miller, S. I. and Goodlett, D. R. (2009). Precursor acquisition independent from ion count: how to dive deeper into the proteomics ocean. Analytical Chemistry 81, 6481–6488.Google Scholar
Panigrahi, A. K., Ogata, Y., Zikova, A., Anupama, A., Dalley, R. A., Acestor, N., Myler, P. J. and Stuart, K. D. (2009). A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9, 434–450.Google Scholar
Pappin, D. J. (1997). Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods in Molecular Biology 64, 165–173.Google ScholarPubMed
Pappin, D. J., Hojrup, P. and Bleasby, A. J. (1993). Rapid identification of proteins by peptide-mass fingerprinting. Current Biology 3, 327–332.CrossRefGoogle ScholarPubMed
Pedersen, S. K., Harry, J. L., Sebastian, L., Baker, J., Traini, M. D., McCarthy, J. T., Manoharan, A., Wilkins, M. R., Gooley, A. A., Righetti, P. G., Packer, N. H., Williams, K. L. and Herbert, B. R. (2003). Unseen proteome: mining below the tip of the iceberg to find low abundance and membrane proteins. Journal of Proteome Research 2, 303–311.Google Scholar
Rosenzweig, D., Smith, D., Opperdoes, F., Stern, S., Olafson, R. W. and Zilberstein, D. (2008). Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB Journal 22, 590–602.Google Scholar
Ross, P. L., Huang, Y. N., Marchese, J. N., 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. and Pappin, D. J. (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Molecular and Cellular Proteomics 3, 1154–1169.Google Scholar
Rout, M. P. and Field, M. C. (2001). Isolation and characterization of subnuclear compartments from Trypanosoma brucei. Identification of a major repetitive nuclear lamina component. Journal of Biological Chemistry 276, 38261–38271.Google Scholar
Schagger, H. and von Jagow, G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Analytical Biochemistry 199, 223–231.Google Scholar
Schnolzer, M., Jedrzejewski, P. and Lehmann, W. D. (1996). Protease-catalyzed incorporation of 18O into peptide fragments and its application for protein sequencing by electrospray and matrix-assisted laser desorption/ionization mass spectrometry. Electrophoresis 17, 945–953.Google Scholar
Tarun, A. S., Peng, X., Dumpit, R. F., Ogata, Y., Silva-Rivera, H., Camargo, N., Daly, T. M., Bergman, L. W. and Kappe, S. H. (2008). A combined transcriptome and proteome survey of malaria parasite liver stages. Proceedings of the National Academy of Sciences, USA 105, 305–310.CrossRefGoogle ScholarPubMed
Tree, J. J., Wang, D., McInally, C., Mahajan, A., Layton, A., Houghton, I., Elofsson, M., Stevens, M. P., Gally, D. L. and Roe, A. J. (2009). Characterization of the effects of salicylidene acylhydrazide compounds on type III secretion in Escherichia coli O157:H7. Infection and Immunity 77, 4209–4220.CrossRefGoogle ScholarPubMed
Trinkle-Mulcahy, L., Boulon, S., Lam, Y. W., Urcia, R., Boisvert, F. M., Vandermoere, F., Morrice, N. A., Swift, S., Rothbauer, U., Leonhardt, H. and Lamond, A. (2008). Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. Journal of Cell Biology 183, 223–239.Google Scholar
Voorheis, H. P., Gale, J. S., Owen, M. J. and Edwards, W. (1979). The isolation and partial characterization of the plasma membrane from Trypanosoma brucei. Biochemistry Journal 180, 11–24.Google Scholar
Walker, J., Vasquez, J. J., Gomez, M. A., Drummelsmith, J., Burchmore, R., Girard, I. and Ouellette, M. (2006). Identification of developmentally-regulated proteins in Leishmania panamensis by proteome profiling of promastigotes and axenic amastigotes. Molecular and Biochemical Parasitology 147, 64–73.Google Scholar
Wang, D., Zetterstrom, C. E., Gabrielsen, M., Beckham, K. S., Tree, J. J., Macdonald, S. E., Byron, O., Mitchell, T. J., Gally, D. L., Herzyk, P., Mahajan, A., Uvell, H., Burchmore, R., Smith, B. O., Elofsson, M. and Roe, A. J. (2011). Identification of bacterial target proteins for the salicylidene acylhydrazide class of virulence-blocking compounds. Journal of Biological Chemistry 286, 29922–29931.Google Scholar
Wilkins, M. R., Pasquali, C., Appel, R. D., Ou, K., Golaz, O., Sanchez, J. C., Yan, J. X., Gooley, A. A., Hughes, G., Humphery-Smith, I., Williams, K. L. and Hochstrasser, D. F. (1996). From proteins to proteomes: large scale protein identification by two-dimensional electrophoresis and amino acid analysis. Biotechnology (NY) 14, 61–65.Google Scholar
Wolters, D. A., Washburn, M. P. and Yates, J. R. III (2001). An automated multidimensional protein identification technology for shotgun proteomics. Analytical Chemistry 73, 5683–5690.CrossRefGoogle ScholarPubMed
Xie, F., Liu, T., Qian, W. J., Petyuk, V. A. and Smith, R. D. (2011). Liquid chromatography-mass spectrometry-based quantitative proteomics 2. Journal of Biological Chemistry 286, 25443–25449.Google Scholar
Yao, X., Afonso, C. and Fenselau, ■. (2003). Dissection of proteolytic 18O labeling: endoprotease-catalyzed 16O-to-18O exchange of truncated peptide substrates. Journal of Proteome Research 2, 147–152.Google Scholar