Proteomic characterization of a natural host-pathogen interaction: Repertoire of in vivo expressed bacterial and host surface-associated proteins

Journal of Proteome Research

Volumn 14, Issue 1, 2015, Pages 120-132

  Rees, Megan A ^a   Kleifeld, Oded ^a   Crellin, Paul K ^a   Ho, Bosco ^a   Stinear, Timothy P ^a,b   Smith, A Ian ^a   Coppel, Ross L ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Corynebacterium pseudotuberculosis; Mycobacterium; Proteomics; surface proteins

Indexed keywords

ALPHA 1 ANTITRYPSIN; ANGIOTENSINOGEN; ASPARAGINASE; BACTERIAL PROTEIN; BETA N ACETYLGLUCOSAMINYLGLYCOPEPTIDE BETA 1,4 GALACTOSYLTRANSFERASE; CARBONATE DEHYDRATASE II; CARNITINE; CATHELICIDIN; CERULOPLASMIN; CHITINASE; COMPLEMENT COMPONENT C3; ENOLASE; FETUIN A; FRUCTOSE BISPHOSPHATASE; GLUCOSE TRANSPORTER 3; HEAT SHOCK PROTEIN 70; LACTATE DEHYDROGENASE; LACTOFERRIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; OSTEOPONTIN; PEPTIDE FRAGMENT; PROTEIN ARGININE DEIMINASE; PROTHROMBIN; PYRIDOXAL KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERUM ALBUMIN; SERUM AMYLOID A; SOMATOMEDIN BINDING PROTEIN 6; UBIQUITIN; OUTER MEMBRANE PROTEIN; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BACTERIUM CULTURE; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONTROLLED STUDY; CORYNEBACTERIUM PSEUDOTUBERCULOSIS; CULTURE MEDIUM; HOST PATHOGEN INTERACTION; IN VIVO STUDY; LYMPH NODE; LYMPHADENITIS; NATURAL HOST; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; SHEEP; SPECIES IDENTIFICATION; TUBERCULOSIS; ANIMAL; CORYNEBACTERIUM INFECTION; DOMESTIC SHEEP; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SHEEP DISEASE; VETERINARY;

BACTERIA (MICROORGANISMS); CORYNEBACTERIUM PSEUDOTUBERCULOSIS; MYCOBACTERIUM; OVIS ARIES;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CORYNEBACTERIUM INFECTIONS; CORYNEBACTERIUM PSEUDOTUBERCULOSIS; HOST-PATHOGEN INTERACTIONS; LYMPH NODES; PROTEOME; PROTEOMICS; SHEEP; SHEEP DISEASES; SHEEP, DOMESTIC;

EID: 84920275448     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5010086     Document Type: Article

References (80)

1. Poetsch, A.; Wolters, D. Bacterial membrane proteomics Proteomics 2008, 8, 4100-4122
2. Tjalsma, H.; Lambooy, L.; Hermans, P. W.; Swinkels, D. W. Shedding & shaving: disclosure of proteomic expressions on a bacterial face Proteomics 2008, 8, 1415-1428
3. Benachour, A.; Morin, T.; Hebert, L.; Budin-Verneuil, A.; Le Jeune, A.; Auffray, Y.; Pichereau, V.; Benachour, A.; Morin, T.; Hebert, L.; Budin-Verneuil, A.; Le Jeune, A.; Auffray, Y.; Pichereau, V. Identification of secreted and surface proteins from Enterococcus faecalis Can. J. Microbiol. 2009, 55, 967-974
4. Desvaux, M.; Dumas, E.; Chafsey, I.; Hebraud, M. Protein cell surface display in Gram-positive bacteria: from single protein to macromolecular protein structure FEMS Microbiol. Lett. 2006, 256, 1-15
5. Jeffery, C. J. Moonlighting proteins-an update Mol. BioSyst. 2009, 5, 345-350
6. Olaya-Abril, A.; Jiménez-Munguía, I.; Gómez-Gascón, L.; Obando, I.; Rodríguez-Ortega, M. J. Identification of potential new protein vaccine candidates through pan-surfomic analysis of pneumococcal clinical isolates from adults PLoS One 2013, 8, e70365
7. Cordwell, S. J.; Cordwell, S. J. Technologies for bacterial surface proteomics Curr. Opin. Microbiol. 2006, 9, 320-329
8. Navarre, W. W.; Schneewind, O. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope Microbiol. Mol. Biol. Rev. 1999, 63, 174-229
9. Fischer, F.; Wolters, D.; Rogner, M.; Poetsch, A. Toward the complete membrane proteome: high coverage of integral membrane proteins through transmembrane peptide detection Mol. Cell. Proteomics 2006, 5, 444-453
10. Rabilloud, T. Membrane proteins and proteomics: love is possible, but so difficult Electrophoresis 2009, 30, S174-S180
11. Rodriguez-Ortega, M. J.; Norais, N.; Bensi, G.; Liberatori, S.; Capo, S.; Mora, M.; Scarselli, M.; Doro, F.; Ferrari, G.; Garaguso, I.; Maggi, T.; Neumann, A.; Covre, A.; Telford, J. L.; Grandi, G. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome Nat. Biotechnol. 2006, 24, 191-197
12. Walters, M. S.; Mobley, H. L.; Walters, M. S.; Mobley, H. L. T. Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics J. Microbiol. Methods 2009, 78, 131-135
13. Newton, V.; McKenna, S. L.; De Buck, J. Presence of PPE proteins in Mycobacterium avium subsp. paratuberculosis isolates and their immunogenicity in cattle Vet. Microbiol. 2009, 135, 394-400
14. He, Z.; De Buck, J. Cell wall proteome analysis of Mycobacterium smegmatis strain MC2 155 BMC Microbiol. 2010, 10, 121
15. Hernáez, M. L.; Ximénez-Embún, P.; Martínez-Gomariz, M.; Gutiérrez-Blázquez, M. D.; Nombela, C.; Gil, C. Identification of Candida albicans exposed surface proteins in vivo by a rapid proteomic approach J. Proteomics 2010, 73, 1404-1409
16. Dreisbach, A.; van der Kooi-Pol, M. M.; Otto, A.; Gronau, K.; Bonarius, H. P. J.; Westra, H.; Groen, H.; Becher, D.; Hecker, M.; van Dijl, J. M. Surface shaving as a versatile tool to profile global interactions between human serum proteins and the Staphylococcus aureus cell surface Proteomics 2011, 11, 2921-2930
17. Westermann, A. J.; Gorski, S. A.; Vogel, J. Dual RNA-seq of pathogen and host Nat. Rev. Microbiol. 2012, 10, 618-630
18. Schmidt, F.; Völker, U. Proteome analysis of host-pathogen interactions: investigation of pathogen responses to the host cell environment Proteomics 2011, 11, 3203-3211
19. Soares, S. C.; Silva, A.; Trost, E.; Blom, J.; Ramos, R.; Carneiro, A.; Ali, A.; Santos, A. R.; Pinto, A. C.; Diniz, C.; Barbosa, E. G. V.; Dorella, F. A.; Aburjaile, F.; Rocha, F. S.; Nascimento, K. K. F.; Guimarães, L. C.; Almeida, S.; Hassan, S. S.; Bakhtiar, S. M.; Pereira, U. P.; Abreu, V. A. C.; Schneider, M. P. C.; Miyoshi, A.; Tauch, A.; Azevedo, V. The pan-genome of the animal pathogen Corynebacterium pseudotuberculosis reveals differences in genome plasticity between the Biovar ovis and equi strains PLoS One 2013, 8, e53818
20. Peel, M. M.; Palmer, G. G.; Stacpoole, A. M.; Kerr, T. G. Human lymphadenitis due to Corynebacterium pseudotuberculosis: report of ten cases from Australia and review Clin. Infect. Dis. 1997, 24, 185-191
21. Fontanilla, J. M.; Barnes, A.; Von Reyn, C. F. Current diagnosis and management of peripheral tuberculous Lymphadenitis Clin. Infect. Dis. 2011, 53, 555-562
22. Dover, L. G.; Alderwick, L. J.; Brown, A. K.; Futterer, K.; Besra, G. S. Regulation of cell wall synthesis and growth Curr. Mol. Med. 2007, 7, 247-276
23. Dorella, F. A.; Pacheco, L. G.; Seyffert, N.; Portela, R. W.; Meyer, R.; Miyoshi, A.; Azevedo, V. Antigens of Corynebacterium pseudotuberculosis and prospects for vaccine development Expert Rev. Vaccines 2009, 8, 205-213
24. Barh, D.; Jain, N.; Tiwari, S.; Parida, B. P.; D'Afonseca, V.; Li, L.; Ali, A.; Santos, A. R.; Guimaraes, L. C.; de Castro Soares, S.; Miyoshi, A.; Bhattacharjee, A.; Misra, A. N.; Silva, A.; Kumar, A.; Azevedo, V. A novel comparative genomics analysis for common drug and vaccine targets in Corynebacterium pseudotuberculosis and other CMN group of human pathogens Chem. Biol. Drug Des. 2011, 78, 73-84
25. Ruiz, J. C.; D'Afonseca, V.; Silva, A.; Ali, A.; Pinto, A. C.; Santos, A. R.; Rocha, A. A. M. C.; Lopes, D. O.; Dorella, F. A.; Pacheco, L. G. C.; Costa, M. P.; Turk, M. Z.; Seyffert, N.; Moraes, P. M. R. O.; Soares, S. C.; Almeida, S. S.; Castro, T. L. P.; Abreu, V. A. C.; Trost, E.; Baumbach, J.; Tauch, A.; Schneider, M. P. C.; McCulloch, J.; Cerdeira, L. T.; Ramos, R. T. J.; Zerlotini, A.; Dominitini, A.; Resende, D. M.; Coser, E. M.; Oliveira, L. M.; Pedrosa, A. L.; Vieira, C. U.; Guimaraes, C. T.; Bartholomeu, D. C.; Oliveira, D. M.; Santos, F. R.; Rabelo, E. M.; Lobo, F. P.; Franco, G. R.; Costa, A. F.; Castro, I. M.; Dias, S. R. C.; Ferro, J. A.; Ortega, J. M.; Paiva, L. V.; Goulart, L. R.; Almeida, J. F.; Ferro, M. I. T.; Carneiro, N. P.; Falcao, P. R. K.; Grynberg, P.; Teixeira, S. M. R.; Brommonschenkel, S.; Oliveira, S. C.; Meyer, R.; Moore, R. J.; Miyoshi, A.; Oliveira, G. C.; Azevedo, V. Evidence for reductive genome evolution and lateral acquisition of virulence functions in two Corynebacterium pseudotuberculosis strains PLoS One 2011, 6, e18551
26. Pacheco, L. G. C.; Slade, S. E.; Seyffert, N.; Santos, A. R.; Castro, T. L. P.; Silva, W. M.; Santos, A. V.; Santos, S. G.; Farias, L. M.; Carvalho, M. A. R.; Pimenta, A. M. C.; Meyer, R.; Silva, A.; Scrivens, J. H.; Oliveira, S. C.; Miyoshi, A.; Dowson, C. G.; Azevedo, V. A combined approach for comparative exoproteome analysis of Corynebacterium pseudotuberculosis BMC Microbiol. 2011, 11, 12
27. Moura-Costa, L. F.; Bahia, R. C.; Carminati, R.; Vale, V. L. C.; Paule, B. J. A.; Portela, R. W.; Freire, S. M.; Nascimento, I.; Schaer, R.; Barreto, L. M. S.; Meyer, R. Evaluation of the humoral and cellular immune response to different antigens of. in Caninde goats and their potential protection against caseous lymphadenitis Vet. Immunol. Immunopathol. 2008, 126, 131-141
28. McNamara, P. J.; Bradley, G. A.; Songer, J. G. Targeted mutagenesis of the phospholipase D gene results in decreased virulence of Corynebacterium pseudotuberculosis Mol. Microbiol. 1994, 12, 921-930
29. Meyer, R.; Regis, L.; Vale, V.; Paule, B.; Carminati, R.; Bahia, R.; Moura-Costa, L.; Schaer, R.; Nascimento, I.; Freire, S. In vitro IFN-gamma production by goat blood cells after stimulation with somatic and secreted Corynebacterium pseudotuberculosis antigens Vet. Immunol. Immunopathol. 2005, 107, 249-254
30. D'Afonseca, V.; Moraes, P. M.; Dorella, F. A.; Pacheco, L. G. C.; Meyer, R.; Portela, R. W.; Miyoshi, A.; Azevedo, V. A description of genes of Corynebacterium pseudotuberculosis useful in diagnostics and vaccine applications Genet. Mol. Res. 2008, 7, 252-260
31. Trost, E.; Ott, L.; Schneider, J.; Schroder, J.; Jaenicke, S.; Goesmann, A.; Husemann, P.; Stoye, J.; Dorella, F. A.; Rocha, F. S.; Soares, S. d. C.; D'Afonseca, V.; Miyoshi, A.; Ruiz, J.; Silva, A.; Azevedo, V.; Burkovski, A.; Guiso, N.; Join-Lambert, O. F.; Kayal, S.; Tauch, A. The complete genome sequence of Corynebacterium pseudotuberculosis FRC41 isolated from a 12-year-old girl with necrotizing lymphadenitis reveals insights into gene-regulatory networks contributing to virulence BMC Genomics 2010, 11, 728
32. 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, 2411-2419
33. Perry, A. J.; Ho, B. K. Inmembrane, a bioinformatic workflow for annotation of bacterial cell-surface proteomes Source Code Biol. Med. 2013, 8, 9
34. Remm, M.; Storm, C. E.; Sonnhammer, E. L. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons J. Mol. Biol. 2001, 314, 1041-1052
35. Tatusov, R. L.; Natale, D. A.; Garkavtsev, I. V.; Tatusova, T. A.; Shankavaram, U. T.; Rao, B. S.; Kiryutin, B.; Galperin, M. Y.; Fedorova, N. D.; Koonin, E. V. The COG database: new developments in phylogenetic classification of proteins from complete genomes Nucleic Acids Res. 2001, 29, 22-28
36. Rumble, S. M.; Lacroute, P.; Dalca, A. V.; Fiume, M.; Sidow, A.; Brudno, M. SHRiMP: Accurate mapping of short color-space reads PLoS Comput. Biol. 2009, 5, e1000386
37. Khamis, A.; Raoult, D.; La Scola, B. Comparison between rpoB and 16S rRNA gene sequencing for molecular identification of 168 clinical isolates of Corynebacterium J. Clin. Microbiol. 2005, 43, 1934-1936
38. Dorella, F. A.; Pacheco, L. G. C.; Oliveira, S. C.; Miyoshi, A.; Azevedo, V. Corynebacterium pseudotuberculosis: microbiology, biochemical properties, pathogenesis and molecular studies of virulence Vet. Res. 2006, 37, 201-218
39. Daffe, M.; Draper, P. The envelope layers of mycobacteria with reference to their pathogenicity Adv. Microb. Physiol. 1998, 39, 131-203
40. Silva, W. M.; Seyffert, N.; Ciprandi, A.; Santos, A. V.; Castro, T. L. P.; Pacheco, L. G. C.; Barh, D.; Le Loir, Y.; Pimenta, A. M. C.; Miyoshi, A.; Silva, A.; Azevedo, V. Differential exoproteome analysis of two Corynebacterium pseudotuberculosis Biovar ovis strains isolated from goat (1002) and sheep (C231) Curr. Microbiol. 2013, 1-6
41. Sassetti, C. M.; Boyd, D. H.; Rubin, E. J. Genes required for mycobacterial growth defined by high density mutagenesis Mol. Microbiol. 2003, 48, 77-84
42. 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, 855-861
43. 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, 1284-1296
44. Gunawardena, H. P.; Feltcher, M. E.; Wrobel, J. A.; Gu, S.; Braunstein, M.; Chen, X. Comparison of the membrane proteome of virulent Mycobacterium tuberculosis and the attenuated Mycobacterium bovis BCG vaccine strain by label-free quantitative proteomics J. Proteome Res. 2013, 12, 5463-5474
45. Sherman, D. R.; Mdluli, K.; Hickey, M. J.; Barry, C. E., III; Stover, C. K. AhpC, oxidative stress and drug resistance in Mycobacterium tuberculosis Biofactors 1999, 10, 211-217
46. Tatusov, R. L.; Koonin, E. V.; Lipman, D. J. A genomic perspective on protein families Science 1997, 278, 631-637
47. Silva, C. A. M.; Danelishvili, L.; McNamara, M.; Berredo-Pinho, M.; Bildfell, R.; Biet, F.; Rodrigues, L. S.; Oliveira, A. V.; Bermudez, L. E.; Pessolani, M. C. V. Interaction of Mycobacterium leprae with human airway epithelial cells: adherence, entry, survival, and identification of potential adhesins by surface proteome analysis Infect. Immun. 2013, 81, 2645-2659
48. DesJardin, L. E.; Kaufman, T. M.; Potts, B.; Kutzbach, B.; Yi, H.; Schlesinger, L. S. Mycobacterium tuberculosis -infected human macrophages exhibit enhanced cellular adhesion with increased expression of LFA-1 and ICAM-1 and reduced expression and/or function of complement receptors, FcγRII and the mannose receptor Microbiology 2002, 148, 3161-3171
49. Ramanathan, B.; Davis, E. G.; Ross, C. R.; Blecha, F. Cathelicidins: Microbicidal activity, mechanisms of action, and roles in innate immunity Microbes Infect. 2002, 4, 361-372
50. Cash, P. Investigating pathogen biology at the level of the proteome Proteomics 2011, 11, 3190-3202
51. Malen, H.; De Souza, G. A.; Pathak, S.; Softeland, T.; Wiker, H. G. Comparison of membrane proteins of Mycobacterium tuberculosis H37Rv and H37Ra strains BMC Microbiol. 2011, 11, 18
52. Albrethsen, J.; Agner, J.; Piersma, S. R.; Højrup, P.; Pham, T. V.; Weldingh, K.; Jimenez, C. R.; Andersen, P.; Rosenkrands, I. Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems Mol. Cell. Proteomics 2013, 12, 1180-1191
53. Kruh, N. A.; Troudt, J.; Izzo, A.; Prenni, J.; Dobos, K. M. Portrait of a pathogen: the Mycobacterium tuberculosis proteome in vivo PLoS One 2010, 5, e13938
54. Fontaine, M. C.; Baird, G. J. Caseous lymphadenitis Small Ruminant Res. 2008, 76, 42-48
55. McNamara, M.; Tzeng, S. C.; Maier, C.; Wu, M.; Bermudez, L. E. Surface-exposed proteins of pathogenic mycobacteria and the role of cu-zn superoxide dismutase in macrophages and neutrophil survival Proteome Sci. 2013, 11, 45
56. Jani, C.; Eoh, H.; Lee, J. J.; Hamasha, K.; Sahana, M. B.; Han, J.-S.; Nyayapathy, S.; Lee, J.-Y.; Suh, J.-W.; Lee, S. H.; Rehse, S. J.; Crick, D. C.; Kang, C.-M. Regulation of polar peptidoglycan biosynthesis by Wag31 phosphorylation in mycobacteria BMC Microbiol. 2010, 10, 327
57. Mukherjee, P.; Sureka, K.; Datta, P.; Hossain, T.; Barik, S.; Das, K. P.; Kundu, M.; Basu, J. Novel role of Wag31 in protection of mycobacteria under oxidative stress Mol. Microbiol. 2009, 73, 103-119
58. Chang, G.; Spencer, R. H.; Lee, A. T.; Barclay, M. T.; Rees, D. C. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel Science 1998, 282, 2220-2226
59. Barh, D.; Gupta, K.; Jain, N.; Khatri, G.; León-Sicairos, N.; Canizalez-Roman, A.; Tiwari, S.; Verma, A.; Rahangdale, S.; Shah Hassan, S.; Rodrigues Dos Santos, A.; Ali, A.; Carlos Guimarães, L.; Thiago Jucá Ramos, R.; Devarapalli, P.; Barve, N.; Bakhtiar, M.; Kumavath, R.; Ghosh, P.; Miyoshi, A.; Silva, A.; Kumar, A.; Narayan Misra, A.; Blum, K.; Baumbach, J.; Azevedo, V. Conserved host-pathogen PPIs: Globally conserved inter-species bacterial PPIs based conserved host-pathogen interactome derived novel target in C. pseudotuberculosis, C. diphtheriae, M. tuberculosis, C. ulcerans, Y. pestis, and E. coli targeted by Piper betel compounds Integr. Biol. 2013, 5, 495-509
60. Zhang, Y.; Amzel, L. M. Tuberculosis drug targets Curr. Drug Targets 2002, 3, 131-154
61. Muckle, C. A.; Menzies, P. I.; Li, Y.; Hwang, Y. T.; van Wesenbeeck, M. Analysis of the immunodominant antigens of Corynebacterium pseudotuberculosis Vet. Microbiol. 1992, 30, 47-58
62. Walker, J.; Jackson, H. J.; Eggleton, D. G.; Meeusen, E. N.; Wilson, M. J.; Brandon, M. R. Identification of a novel antigen from Corynebacterium pseudotuberculosis that protects sheep against caseous lymphadenitis Infect. Immun. 1994, 62, 2562-2567
63. Paule, B. J. A.; Meyer, R.; Moura-Costa, L. F.; Bahia, R. C.; Carminati, R.; Regis, L. F.; Vale, V. L. C.; Freire, S. M.; Nascimento, I.; Schaer, R.; Azevedo, V. Three-phase partitioning as an efficient method for extraction/concentration of immunoreactive excreted-secreted proteins of Corynebacterium pseudotuberculosis Protein Expression Purif. 2004, 34, 311-316
64. Olaya-Abril, A.; Jiménez-Munguía, I.; Gómez-Gascón, L.; Rodríguez-Ortega, M. J. Surfomics: shaving live organisms for a fast proteomic identification of surface proteins J. Proteomics 2013, 31, 164-176
65. Sardana, G.; Jung, K.; Stephan, C.; Diamandis, E. P. Proteomic analysis of conditioned media from the PC3, LNCaP, and 22Rv1 prostate cancer cell lines: discovery and validation of candidate prostate cancer biomarkers J. Proteome Res. 2008, 7, 3329-3338
66. Solis, N.; Larsen, M. R.; Cordwell, S. J. Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control Proteomics 2010, 10, 2037-2049
67. Bendz, M.; Skwark, M.; Nilsson, D.; Granholm, V.; Cristobal, S.; Käll, L.; Elofsson, A. Membrane protein shaving with thermolysin can be used to evaluate topology predictors Proteomics 2013, 13, 1467-1480
68. Kunert, A.; Losse, J.; Gruszin, C.; Huhn, M.; Kaendler, K.; Mikkat, S.; Volke, D.; Hoffmann, R.; Jokiranta, T. S.; Seeberger, H.; Moellmann, U.; Hellwage, J.; Zipfel, P. F. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein J. Immunol. 2007, 179, 2979-2988
69. Dreisbach, A.; van Dijl, J. M.; Buist, G. The cell surface proteome of Staphylococcus aureus Proteomics 2011, 11, 3154-3168
70. Prados-Rosales, R.; Baena, A.; Martinez, L. R.; Luque-Garcia, J.; Kalscheuer, R.; Veeraraghavan, U.; Camara, C.; Nosanchuk, J. D.; Besra, G. S.; Chen, B.; Jimenez, J.; Glatman-Freedman, A.; Jacobs, W. R., Jr.; Porcelli, S. A.; Casadevall, A. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice J. Clin. Invest. 2011, 121, 1471-1483
71. McNamara, M.; Tzeng, S. C.; Maier, C.; Zhang, L.; Bermudez, L. E. Surface proteome of " Mycobacterium avium subsp. hominissuis" during the early stages of macrophage infection Infect. Immun. 2012, 80, 1868-1880
72. Brown, C. C.; Olander, H. J.; Alves, S. F. Synergistic hemolysis-inhibition titers associated with caseous lymphadenitis in a slaughterhouse survey of goats and sheep in Northeastern Brazil Can. J. Vet. Res. 1987, 51, 46-49
73. Boleij, A.; Laarakkers, C. M.; Gloerich, J.; Swinkels, D. W.; Tjalsma, H. Surface-affinity profiling to identify host-pathogen interactions Infect. Immun. 2011, 79, 4777-4783
74. Veldhuizen, E. J. A.; Brouwer, E. C.; Schneider, V. A. F.; Fluit, A. C. Chicken cathelicidins display antimicrobial activity against multiresistant bacteria without inducing strong resistance PLoS One 2013, 8, e61964
75. Struyf, S.; Gouwy, M.; Dillen, C.; Proost, P.; Opdenakker, G.; Van Damme, J. Chemokines synergize in the recruitment of circulating neutrophils into inflamed tissue Eur. J. Immunol. 2005, 35, 1583-1591
76. Shi, C.; Pamer, E. G. Monocyte recruitment during infection and inflammation Nat. Rev. Immunol. 2011, 11, 762-774
77. Schlesinger, L. S. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors J. Immunol. 1993, 150, 2920-2930
78. Cywes, L.; Hoppe, H. C.; Daffé, M.; Ehlers, M. R. W. Nonopsonic binding of Mycobacterium tuberculosis to complement receptor type 3 is mediated by capsular polysaccharides and is strain dependent Infect. Immun. 1997, 65, 4258-4266
79. Weigoldt, M.; Meens, J.; Doll, K.; Fritsch, I.; Mobius, P.; Goethe, R.; Gerlach, G. F. Differential proteome analysis of Mycobacterium avium subsp. paratuberculosis grown in vitro and isolated from cases of clinical Johne's disease Microbiology 2011, 157, 557-565
80. Krogh, A.; Larsson, B.; von Heijne, G.; Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 2001, 305, 567-580