1887

Microbiology Society logo

Volume 157, Issue 2

Differential proteome analysis of subsp. grown and isolated from cases of clinical Johne's disease Free

Abstract

Bovine Johne's disease (paratuberculosis), caused by subspecies , poses a significant economic problem to the beef and dairy industry worldwide. Despite its relevance, however, pathogenesis of Johne's disease is still only partially resolved. Since mycobacterial membrane proteins expressed during infection are likely to play an important role in pathogenesis, membrane-enriched fractions, namely mucosa-derived membranes (MDM) and culture-derived membranes (CDM), of subsp. from three cows with clinical paratuberculosis were investigated. An initial analysis by 2D difference gel electrophoresis (2D DIGE) and MALDI-TOF-MS analysis revealed four differentially expressed proteins with only one predicted membrane protein. Due to this limited outcome, membrane preparations were subjected to a tube–gel trypsin digestion and investigated by using nanoflow-liquid-chromatography-coupled tandem MS. Based on this approach a total of 212 proteins were detected in MDM including 32 proteins of bovine origin; 275 proteins were detected in CDM 59 % of MDM and CDM proteins were predicted to be membrane-associated. A total of 130 of the proteins were detected in both MDM and CDM and 48 predicted membrane proteins were detected in MDM from at least two cows. Four of these proteins were not detected in CDM, implying differential expression in the host. All membrane-associated proteins, especially the four identified as being differentially expressed, might be relevant targets for further analyses into the pathogenesis of bovine paratuberculosis.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): 2D DIGE, 2D difference gel electrophoresis , CDM, culture-derived membranes , MDM, mucosa-derived membranes , MIRU-VNTR, mycobacterial interspersed repetitive unit-variable-number tandem-repeat , MLSSR, multilocus short sequence repeat and nUPLC-ESI Q-TOF-MS/MS, nanoflow-liquid-chromatography-coupled tandem MS
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.044859-0
2011-02-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/2/557.html?itemId=/content/journal/micro/10.1099/mic.0.044859-0&mimeType=html&fmt=ahah

References

  1. Aebersold R., Mann M. 2003; Mass spectrometry-based proteomics. Nature 422:198–207
     [Google Scholar]
  2. Agarwal N., Woolwifie S. C., Tyagi S., Bishai W. R. 2007; Characterization of the Mycobacterium tuberculosis sigma factor SigM by assessment of virulence and identification of SigM-dependent genes. Infect Immun 75:452–461
     [Google Scholar]
  3. Bannantine J. P., Huntley J. F. J., Miltner E., Stabel J. R., Bermudez L. E. 2003; The Mycobacterium avium subsp paratuberculosis 35 kDa protein plays a role in invasion of bovine epithelial cells. Microbiology 149:2061–2069
     [Google Scholar]
  4. Buettner F. F., Bendalla I. M., Bosse J. T., Meens J., Nash J. H., Hartig E., Langford P. R., Gerlach G. F. 2009; Analysis of the Actinobacillus pleuropneumoniae HlyX (FNR) regulon and identification of iron-regulated protein B as an essential virulence factor. Proteomics 9:2383–2398
     [Google Scholar]
  5. Camejo A., Buchrieser C., Couve E., Carvalho F., Reis O., Ferreira P., Sousa S., Cossart P., Cabanes D. 2009; In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5:e1000449
     [Google Scholar]
  6. Carsiotis M., Stocker B. A. D., Weinstein D. L., Obrien A. D. 1989; A Salmonella typhimurium virulence gene linked to flg . Infect Immun 57:3276–3280
     [Google Scholar]
  7. Chen G., Pramanik B. N. 2009; Application of LC/MS to proteomics studies: current status and future prospects. Drug Discov Today 14:465–471
     [Google Scholar]
  8. Choy E., Whittington R. J., Marsh I., Marshall J., Campbell M. T. 1998; A method for purification and characterisation of Mycobacterium avium subsp. paratuberculosis from the intestinal mucosa of sheep with Johne's disease. Vet Microbiol 64:51–60
     [Google Scholar]
  9. de Lima C. S., Marques M. A., Debrie A. S., Almeida E. C., Silva C. A., Brennan P. J., Sarno E. N., Menozzi F. D., Pessolani M. C. 2009; Heparin-binding hemagglutinin (HBHA) of Mycobacterium leprae is expressed during infection and enhances bacterial adherence to epithelial cells. FEMS Microbiol Lett 292:162–169
     [Google Scholar]
  10. Delogu G., Brennan M. J. 1999; Functional domains present in the mycobacterial hemagglutinin, HBHA. J Bacteriol 181:7464–7469
     [Google Scholar]
  11. Egan S., Lanigan M., Shiell B., Beddome G., Stewart D., Vaughan J., Michalski W. P. 2008; The recovery of Mycobacterium avium subspecies paratuberculosis from the intestine of infected ruminants for proteomic evaluation. J Microbiol Methods 75:29–39
     [Google Scholar]
  12. Gehring A. J., Dobos K. M., Belisle O. T., Harding C. V., Boom W. H. 2004; Mycobacterium tuberculosis LprG (Rv1411c): A novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J Immunol 173:2660–2668
     [Google Scholar]
  13. Gioffré A., Infante E., Aguilar D., De La Paz Santangelo M., Klepp L., Amadio A., Meikle V., Etchechoury I., Romano M. I. other authors 2005; Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect 7:325–334
     [Google Scholar]
  14. Harriff M. J., Danelishvili L., Wu M., Wilder C., McNamara M., Kent M. L., Bermudez L. E. 2009; Mycobacterium avium genes MAV_5138 and MAV_3679 are transcriptional regulators that play a role in invasion of epithelial cells, in part by their regulation of CipA, a putative surface protein interacting with host cell signaling pathways. J Bacteriol 191:1132–1142
     [Google Scholar]
  15. Harris N. B., Barletta R. G. 2001; Mycobacterium avium subsp. paratuberculosis in Veterinary Medicine. Clin Microbiol Rev 14:489–512
     [Google Scholar]
  16. Hauser A. R., Kang P. J., Engel J. N. 1998; PepA, a secreted protein of Pseudomonas aeruginosa , is necessary for cytotoxicity and virulence. Mol Microbiol 27:807–818
     [Google Scholar]
  17. He Z. G., De Buck J. 2010; Localization of proteins in the cell wall of Mycobacterium avium subsp paratuberculosis K10 by proteomic analysis. Proteome Sci 8:21
     [Google Scholar]
  18. Henningsen R., Gale B. L., Straub K. M., DeNagel D. C. 2002; Application of zwitterionic detergents to the solubilization of integral membrane proteins for two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2:1479–1488
     [Google Scholar]
  19. Hughes V., Smith S., Garcia-Sanchez A., Sales J., Stevenson K. 2007; Proteomic comparison of Mycobacterium avium subspecies paratuberculosis grown in vitro and isolated from clinical cases of ovine paratuberculosis. Microbiology 153:196–205
     [Google Scholar]
  20. Kreeger J. M. 1991; Ruminant paratuberculosis – a century of progress and frustration. J Vet Diagn Invest 3:373–382
     [Google Scholar]
  21. Lu X. N., Zhu H. N. 2005; Tube–gel digestion – a novel proteomic approach for high throughput analysis of membrane proteins. Mol Cell Proteomics 4:1948–1958
     [Google Scholar]
  22. Manning E. J., Collins M. T. 2001; Mycobacterium avium subsp. paratuberculosis : pathogen, pathogenesis and diagnosis. Rev Sci Tech 20:133–150
     [Google Scholar]
  23. Masungi C., Temmerman S., Van Vooren J. P., Drowart A., Pethe K., Menozzi F. D., Locht C., Mascart F. 2002; Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J Infect Dis 185:513–520
     [Google Scholar]
  24. Mendoza J. L., Lana R., Diaz-Rubio M. 2009; Mycobacterium avium subspecies paratuberculosis and its relationship with Crohn's disease. World J Gastroenterol 15:417–422
     [Google Scholar]
  25. Menozzi F. D., Reddy V. M., Cayet D., Raze D., Debrie A. S., Dehouck M. P., Cecchelli R., Locht C. 2006; Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect 8:1–9
     [Google Scholar]
  26. Möbius P., Fritsch I., Luyven G., Hotzel H., Kohler H. 2009; Unique genotypes of Mycobacterium avium subsp. paratuberculosis strains of Type III. Vet Microbiol 139:398–404
     [Google Scholar]
  27. Old W. M., Meyer-Arendt K., Aveline-Wolf L., Pierce K. G., Mendoza A., Sevinsky J. R., Resing K. A., Ahn N. G. 2005; Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 4:1487–1502
     [Google Scholar]
  28. Patel D., Danelishvili L., Yamazaki Y., Alonso M., Paustian M. L., Bannantine J. P., Meunier-Goddik L., Bermudez L. E. 2006; The ability of Mycobacterium avium subsp. paratuberculosis to enter bovine epithelial cells is influenced by preexposure to a hyperosmolar environment and intracellular passage in bovine mammary epithelial cells. Infect Immun 74:2849–2855
     [Google Scholar]
  29. Patton W. F. 2000; A thousand points of light: the application of fluorescence detection technologies to two-dimensional gel electrophoresis and proteomics. Electrophoresis 21:1123–1144
     [Google Scholar]
  30. Peterson Y. K., Winter-Vann A. M., Casey P. J. 2005; Icmt. UCSD-Nature Molecule Pages. Published online 8 August 2005 doi: 10.1038/mp.a001154.01
    [Google Scholar]
  31. Pethe K., Alonso S., Biet F., Delogu G., Brennan M. J., Locht C., Menozzi F. D. 2001; The heparin-binding haemagglutinin of M-tuberculosis is required for extrapulmonary dissemination. Nature 412:190–194
     [Google Scholar]
  32. Pierce E. S. 2009; Where are all the Mycobacterium avium subspecies paratuberculosis in patients with Crohn's disease?. PLoS Pathog 5:e1000234
     [Google Scholar]
  33. Quadroni M., James P. 1999; Proteomics and automation. Electrophoresis 20:664–677
     [Google Scholar]
  34. Radosevich T. J., Reinhardt T. A., Lippolis J. D., Bannantine J. P., Stabel J. R. 2007; Proteome and differential expression analysis of membrane and cytosolic proteins from Mycobacterium avium subsp. paratuberculosis strains K-10 and 187. J Bacteriol 189:1109–1117
     [Google Scholar]
  35. Reddy V. M., Kumar B. 2000; Interaction of Mycobacterium avium complex with human respiratory epithelial cells. J Infect Dis 181:1189–1193
     [Google Scholar]
  36. Santema W., Overdijk M., Barends J., Krijgsveld J., Rutten V., Koets A. 2009; Searching for proteins of Mycobacterium avium subspecies paratuberculosis with diagnostic potential by comparative qualitative proteomic analysis of mycobacterial tuberculins. Vet Microbiol 138:191–196
     [Google Scholar]
  37. Santoni V., Molloy M., Rabilloud T. 2000; Membrane proteins and proteomics: un amour impossible?. Electrophoresis 21:1054–1070
     [Google Scholar]
  38. Sechi L. A., Ahmed N., Felis G. E., Dupre I., Cannas S., Fadda G., Bua A., Zanetti S. 2006; Immunogenicity and cytoadherence of recombinant heparin binding haemagglutinin (HBHA) of Mycobacterium avium subsp paratuberculosis : functional promiscuity or a role in virulence?. Vaccine 24:236–243
     [Google Scholar]
  39. Seibert V., Wiesner A., Buschmann T., Meuer J. 2004; Surface-enhanced laser desorption ionization time-of-flight mass spectrometry (SELDI TOF-MS) and ProteinChip technology in proteomics research. Pathol Res Pract 200:83–94
     [Google Scholar]
  40. Shevchenko A., Wilm M., Vorm O., Mann M. 1996; Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68:850–858
     [Google Scholar]
  41. Stack H. M., Sleator R. D., Bowers M., Hill C., Gahan C. G. M. 2005; Role for HtrA in stress induction and virulence potential in Listeria monocytogenes . Appl Environ Microbiol 71:4241–4247
     [Google Scholar]
  42. Talaat A. M., Lyons R., Howard S. T., Johnston S. A. 2004; The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci U S A 101:4602–4607
     [Google Scholar]
  43. Talapatra A., Rouse R., Hardiman G. 2002; Protein microarrays: challenges and promises. Pharmacogenomics 3:527–536
     [Google Scholar]
  44. Xiong Y., Chalmers M. J., Gao F. P., Cross T. A., Marshall A. G. 2005; Identification of Mycobacterium tuberculosis H37Rv integral membrane proteins by one-dimensional gel electrophoresis and liquid chromatography electrospray ionization tandem mass spectrometry. J Proteome Res 4:855–861
     [Google Scholar]
  45. Zanetti S., Bua A., Delogu G., Pusceddu C., Mura M., Saba F., Pirina P., Garzelli C., Vertuccio C. other authors 2005; Patients with pulmonary tuberculosis develop a strong humoral response against methylated heparin-binding hemagglutinin. Clin Diagn Lab Immunol 12:1135–1138
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.044859-0
Loading
Differential proteome analysis of Mycobacterium avium subsp. paratuberculosis grown in vitro and isolated from cases of clinical Johne's disease
Microbiology 157, 557 (2011); https://doi.org/10.1099/mic.0.044859-0
/content/journal/micro/10.1099/mic.0.044859-0
/content/journal/micro/10.1099/mic.0.044859-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error