Proteomic definition of the cell wall of mycobacterium tuberculosis

Journal of Proteome Research

Volumn 9, Issue 11, 2010, Pages 5816-5826

  Wolfe, Lisa M ^a   Mahaffey, Spencer B ^a   Kruh, Nicole A ^a   Dobos, Karen M ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

Author keywords

cell wall; mass spectrometry; Mycobacterium tuberculosis; proteome

Indexed keywords

CHLORIDE; DODECYL SULFATE SODIUM; GUANIDINE; LIPID BINDING PROTEIN; ORGANIC SOLVENT; TRITON X 114;

ALGORITHM; ARTICLE; BACTERIAL SURVIVAL; BIOSYNTHESIS; CELL WALL; CHROMATOGRAPHY; COVALENT BOND; EXTRACTION; MACROMOLECULE; MASS SPECTROMETRY; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIAL PROTEINS; CELL WALL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MASS SPECTROMETRY; MYCOBACTERIUM TUBERCULOSIS; PROTEOMICS; SOLUBILITY; SOLVENTS;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 78149386742     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr1005873     Document Type: Article

References (58)

1. Flynn, J. L.; Chan, J. Immunology of tuberculosis Annu. Rev. Immunol. 2001, 19, 93-129
2. Szczepan, J.; Andrzej, S.; Katarzyna, K. How Mycobacterium tuberculosis subverts host immune responses BioEssays 2008, 30 (10) 943-954
3. Brennan, P. J. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis Tuberculosis 2003, 83 (1-3) 91-97
4. Briken, V.; Porcelli, S. A.; Besra, G. S.; Kremer, L. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response Mol. Microbiol. 2004, 53 (2) 391-403
5. Jackson, M.; Stadthagen, G.; Gicquel, B. Long-chain multiple methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis: biosynthesis, transport, regulation and biological activities Tuberculosis 2007, 87 (2) 78-86
6. Neyrolles, O.; Gould, K.; Gares, M. P.; Brett, S.; Janssen, R.; O'Gaora, P.; Herrmann, J. L.; Prevost, M. C.; Perret, E.; Thole, J. E.; Young, D. Lipoprotein access to MHC class I presentation during infection of murine macrophages with live mycobacteria J. Immunol. 2001, 166 (1) 447-457
7. Sutcliffe, I. C.; Harrington, D. J. Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components FEMS Microbiol. Rev. 2004, 28 (5) 645-659
8. Young, D. B.; Garbe, T. R. Lipoprotein antigens of Mycobacterium tuberculosis Res. Microbiol. 1991, 142 (1) 55-65
9. Brightbill, H. D.; Libraty, D. H.; Krutzik, S. R.; Yang, R. B.; Belisle, J. T.; Bleharski, J. R.; Maitland, M.; Norgard, M. V.; Plevy, S. E.; Smale, S. T.; Brennan, P. J.; Bloom, B. R.; Godowski, P. J.; Modlin, R. L. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors Science 1999, 285 (5428) 732-736
10. Gehring, A. J.; Dobos, K. M.; Belisle, J. T.; Harding, C. V.; Boom, W. H. Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing J. Immunol. 2004, 173 (4) 2660-2668
11. Pecora, N. D.; Gehring, A. J.; Canaday, D. H.; Boom, W. H.; Harding, C. V. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function J. Immunol. 2006, 177 (1) 422-4229
12. Hertz, C. J.; Kiertscher, S. M.; Godowski, P. J.; Bouis, D. A.; Norgard, M. V.; Roth, M. D.; Modlin, R. L. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2 J. Immunol. 2001, 166 (4) 2444-2450
13. Sanchez, A.; Espinosa, P.; Esparza, M. A.; Colon, M.; Bernal, G.; Mancilla, R. Mycobacterium tuberculosis 38-kDa lipoprotein is apoptogenic for human monocyte-derived macrophages Scand. J. Immunol. 2009, 69 (1) 20-28
14. Malen, H.; Softeland, T.; Wiker, H. G. Antigen analysis of Mycobacterium tuberculosis H37Rv culture filtrate proteins Scand. J. Immunol. 2008, 67 (3) 245-252
15. Malen, H.; Berven, F. S.; Softeland, T.; Arntzen, M. O.; D'Santos, C. S.; De Souza, G. A.; Wiker, H. G. Membrane and membrane-associated proteins in Triton X-114 extracts of Mycobacterium bovis BCG identified using a combination of gel-based and gel-free fractionation strategies Proteomics 2008, 8 (9) 1859-1870
16. Malen, H.; Berven, F. S.; Fladmark, K. E.; Wiker, H. G. Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv Proteomics 2007, 7 (10) 1702-1718
17. Urquhart, B. L.; Atsalos, T. E.; Roach, D.; Basseal, D. J.; Bjellqvist, B.; Britton, W. L.; Humphery-Smith, I. 'Proteomic contigs' of Mycobacterium tuberculosis and Mycobacterium bovis (BCG) using novel immobilised pH gradients Electrophoresis 1997, 18 (8) 1384-1392
18. Urquhart, B. L.; Cordwell, S. J.; Humphery-Smith, I. Comparison of predicted and observed properties of proteins encoded in the genome of Mycobacterium tuberculosis H37Rv Biochem. Biophys. Res. Commun. 1998, 253 (1) 70-79
19. Rosenkrands, I.; King, A.; Weldingh, K.; Moniatte, M.; Moertz, E.; Andersen, P. Towards the proteome of Mycobacterium tuberculosis Electrophoresis 2000, 21 (17) 3740-3756
20. Jungblut, P. R.; Muller, E. C.; Mattow, J.; Kaufmann, S. H. Proteomics reveals open reading frames in Mycobacterium tuberculosis H37Rv not predicted by genomics Infect. Immun. 2001, 69 (9) 5905-5907
21. Mattow, J.; Jungblut, P. R.; Schaible, U. E.; Mollenkopf, H. J.; Lamer, S.; Zimny-Arndt, U.; Hagens, K.; Muller, E. C.; Kaufmann, S. H. Identification of proteins from Mycobacterium tuberculosis missing in attenuated Mycobacterium bovis BCG strains Electrophoresis 2001, 22 (14) 2936-2946
22. Gu, S.; Chen, J.; Dobos, K. M.; Bradbury, E. M.; Belisle, J. T.; Chen, X. Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain Mol. Cell. Proteomics 2003, 2 (12) 1284-1296
23. Schmidt, F.; Donahoe, S.; Hagens, K.; Mattow, J.; Schaible, U. E.; Kaufmann, S. H.; Aebersold, R.; Jungblut, P. R. Complementary analysis of the Mycobacterium tuberculosis proteome by two-dimensional electrophoresis and isotope-coded affinity tag technology Mol. Cell. Proteomics 2004, 3 (1) 24-42
24. Mawuenyega, K. G.; Forst, C. V.; Dobos, K. M.; Belisle, J. T.; Chen, J.; Bradbury, E. M.; Bradbury, A. R.; Chen, X. Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling Mol. Biol. Cell 2005, 16 (1) 396-404
25. Xiong, Y.; Chalmers, M. J.; Gao, F. P.; Cross, T. A.; Marshall, A. G. Identification of Mycobacterium tuberculosis H37Rv integral membrane proteins by one-dimensional gel electrophoresis and liquid chromatography electrospray ionization tandem mass spectrometry J. Proteome Res. 2005, 4 (3) 855-861
26. Sinha, S.; Kosalai, K.; Arora, S.; Namane, A.; Sharma, P.; Gaikwad, A. N.; Brodin, P.; Cole, S. T. Immunogenic membrane-associated proteins of Mycobacterium tuberculosis revealed by proteomics Microbiology 2005, 151 (Pt 7) 2411-2419
27. Rosenkrands, I.; Weldingh, K.; Jacobsen, S.; Hansen, C. V.; Florio, W.; Gianetri, I.; Andersen, P. Mapping and identification of Mycobacterium tuberculosis proteins by two-dimensional gel electrophoresis, microsequencing and immunodetection Electrophoresis 2000, 21 (5) 935-948
28. Takayama, K.; Schnoes, H. K.; Armstrong, E. L.; Boyle, R. W. Site of inhibitory action of isoniazid in the synthesis of mycolic acids in Mycobacterium tuberculosis J. Lipid Res. 1975, 16 (4) 308-317
29. Hirschfield, G. R.; McNeil, M.; Brennan, P. J. Peptidoglycan-associated polypeptides of Mycobacterium tuberculosis J. Bacteriol. 1990, 172 (2) 1005-1013
30. Konigsberg, W. H.; Henderson, L. Removal of sodium dodecyl sulfate from proteins by ion-pair extraction Methods Enzymol. 1983, 91, 254-259
31. Radolf, J. D.; Chamberlain, N. R.; Clausell, A.; Norgard, M. V. Identification and localization of integral membrane proteins of virulent Treponema pallidum subsp. pallidum by phase partitioning with the nonionic detergent triton X-114 Infect. Immun. 1988, 56 (2) 490-498
32. Hellman, U.; Wernstedt, C.; Gonez, J.; Heldin, C. H. Improvement of an "in-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing Anal. Biochem. 1995, 224 (1) 451-455
33. Rosenfeld, J.; Capdevielle, J.; Guillemot, J. C.; Ferrara, P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis Anal. Biochem. 1992, 203 (1) 173-179
34. Turner, J.; Dobos, K. M.; Keen, M. A.; Frank, A. A.; Ehlers, S.; Orme, I. M.; Belisle, J. T.; Cooper, A. M. A limited antigen-specific cellular response is sufficient for the early control of Mycobacterium tuberculosis in the lung but is insufficient for long-term survival Infect. Immun. 2004, 72 (7) 3759-3768
35. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-5392
36. Searle, B. C. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies Proteomics 10 (6) 1265-1269
37. Bendtsen, J. D.; Nielsen, H.; von Heijne, G.; Brunak, S. Improved prediction of signal peptides: SignalP 3.0 J. Mol. Biol. 2004, 340 (4) 783-795
38. Nielsen, H.; Engelbrecht, J.; Brunak, S.; von Heijne, G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Protein Eng. 1997, 10 (1) 1-6
39. Nielsen, H.; Krogh, A. Prediction of signal peptides and signal anchors by a hidden Markov model Proc. Int. Conf. Intell. Syst. Mol. Biol. 1998, 6, 122-130
40. Mawuenyega, K. G.; Kaji, H.; Yamuchi, Y.; Shinkawa, T.; Saito, H.; Taoka, M.; Takahashi, N.; Isobe, T. Large-scale identification of Caenorhabditis elegans proteins by multidimensional liquid chromatography-tandem mass spectrometry J. Proteome Res. 2003, 2 (1) 23-35
41. Isobe, T.; Uchida, K.; Taoka, M.; Shinkai, F.; Manabe, T.; Okuyama, T. Automated two-dimensional liquid chromatographic system for mapping proteins in highly complex mixtures J. Chromatogr. 1991, 588 (1-2) 115-123
42. Mollenkopf, H. J.; Jungblut, P. R.; Raupach, B.; Mattow, J.; Lamer, S.; Zimny-Arndt, U.; Schaible, U. E.; Kaufmann, S. H. A dynamic two-dimensional polyacrylamide gel electrophoresis database: the mycobacterial proteome via Internet Electrophoresis 1999, 20 (11) 2172-2180
43. Juncker, A. S.; Willenbrock, H.; Von Heijne, G.; Brunak, S.; Nielsen, H.; Krogh, A. Prediction of lipoprotein signal peptides in Gram-negative bacteria Protein Sci. 2003, 12 (8) 1652-1662
44. Sartain, M. J.; Slayden, R. A.; Singh, K. K.; Laal, S.; Belisle, J. T. Disease state differentiation and identification of tuberculosis biomarkers via native antigen array profiling Mol. Cell. Proteomics 2006, 5 (11) 2102-2113
45. Sartain, M. J.; Belisle, J. T. N-Terminal clustering of the O-glycosylation sites in the Mycobacterium tuberculosis lipoprotein SodC Glycobiology 2009, 19 (1) 38-51
46. Gonzalez-Zamorano, M.; Mendoza-Hernandez, G.; Xolalpa, W.; Parada, C.; Vallecillo, A. J.; Bigi, F.; Espitia, C. Mycobacterium tuberculosis glycoproteomics based on ConA-lectin affinity capture of mannosylated proteins J. Proteome Res. 2009, 8 (2) 721-733
47. Driessen, A. J.; Manting, E. H.; van der Does, C. The structural basis of protein targeting and translocation in bacteria Nat. Struct. Biol. 2001, 8 (6) 492-498
48. Mattow, J.; Schaible, U. E.; Schmidt, F.; Hagens, K.; Siejak, F.; Brestrich, G.; Haeselbarth, G.; Muller, E. C.; Jungblut, P. R.; Kaufmann, S. H. Comparative proteome analysis of culture supernatant proteins from virulent Mycobacterium tuberculosis H37Rv and attenuated M. bovis BCG Copenhagen Electrophoresis 2003, 24 (19-20) 3405-3420
49. Dobos, K. M.; Spencer, J. S.; Orme, I. M.; Belisle, J. T. Proteomic approaches to antigen discovery Methods Mol. Med. 2004, 94, 3-17
50. Mehaffy, C.; Hess, A.; Prenni, J. E.; Mathema, B.; Kreiswirth, B.; Dobos, K. M. Descriptive proteomic analysis shows protein variability between closely related clinical isolates of Mycobacterium tuberculosis Proteomics 2010, 10 (10) 1966-1984
51. Young, D.; Garbe, T.; Lathigra, R.; Abou-Zeid, C.; Zhang, Y. Characterization of prominent protein antigens from mycobacteria Bull. Int. Union Tuberc. Lung Dis. 1991, 66 (1) 47-51
52. Sonnenberg, M. G.; Belisle, J. T. Definition of Mycobacterium tuberculosis culture filtrate proteins by two-dimensional polyacrylamide gel electrophoresis, N-terminal amino acid sequencing, and electrospray mass spectrometry Infect. Immun. 1997, 65 (11) 4515-24
53. Mattow, J.; Jungblut, P. R.; Muller, E. C.; Kaufmann, S. H. Identification of acidic, low molecular mass proteins of Mycobacterium tuberculosis strain H37Rv by matrix-assisted laser desorption/ionization and electrospray ionization mass spectrometry Proteomics 2001, 1 (4) 494-507
54. Ciaramella, A.; Cavone, A.; Santucci, M. B.; Garg, S. K.; Sanarico, N.; Bocchino, M.; Galati, D.; Martino, A.; Auricchio, G.; D'Orazio, M.; Stewart, G. R.; Neyrolles, O.; Young, D. B.; Colizzi, V.; Fraziano, M. Induction of apoptosis and release of interleukin-1 beta by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection J. Infect. Dis. 2004, 190 (6) 1167-1176
55. Farrow, M. F.; Rubin, E. J. Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein J. Bacteriol. 2008, 190 (5) 1783-1791
56. Drage, M. G.; Pecora, N. D.; Hise, A. G.; Fabbraio, M.; Silverstein, R. L.; Golenbock, D. T.; Boom, W. H.; Harding, C. V. TLR2 and its co-receptors determine responses of macrophages and dendritic cells to lipoproteins of Mycobacterium tuberculosis Cellular Immunology 2009, 258, 29-37
57. Sulzenbacher, G.; Canaan, S.; Bordat, Y.; Neyrolles, O.; Stadthagen, G.; Roig-Zamboni, V.; Rauzier, J.; Maurin, D.; Laval, F.; Daffe, M.; Cambillau, C.; Gicquel, B.; Bourne, Y.; Jackson, M. LppX is a lipoprotein required for the translocation of phthiocerol dimycocerosates to the surface of Mycobacterium tuberculosis EMBO J. 2006, 25 (7) 1436-1444
58. Farrow, M. F.; Rubin, E. J. Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein J. Bacteriol. 2008, 190 (5) 1783-1791