Surface proteome of "Mycobacterium avium subsp. hominissuis" during the early stages of macrophage infection

Infection and Immunity

Volumn 80, Issue 5, 2012, Pages 1868-1880

  McNamara, Michael ^a   Tzeng, Shin Cheng ^a   Maier, Claudia ^a   Zhang, Li ^a   Bermudez, Luiz E ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; ADENOSYLHOMOCYSTEINASE; ALDEHYDE DEHYDROGENASE; BACTERIAL PROTEIN; ELONGATION FACTOR G; ELONGATION FACTOR TU; ENOLASE; FATTY ACID SYNTHASE; GLUTAMATE AMMONIA LIGASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCEROL KINASE; HU PROTEIN; ISOCITRATE DEHYDROGENASE (NADP); ISOCITRATE LYASE; KETOL ACID REDUCTOISOMERASE; MALATE DEHYDROGENASE; OXIDOREDUCTASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHOSPHOGLYCERATE KINASE; PROLINE RICH PROTEIN; PROTEIN DNAK; PROTEOME; RNA POLYMERASE BETA SUBUNIT; SUPEROXIDE DISMUTASE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; ATYPICAL MYCOBACTERIOSIS; CELL CULTURE; CONTROLLED STUDY; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM AVIUM SUBSPECIES HOMINISSUIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BIOTINYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; MICE; MYCOBACTERIUM AVIUM; PROTEOME;

EID: 84861149869     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.06151-11     Document Type: Article

References (88)

1. Abdallah AM, et al. 2008. The ESX-5 secretion system of Mycobacterium marinum modulates the macrophage response. J. Immunol. 181:7166-7175.
2. Abdallah AM, et al. 2009. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol. Microbiol. 73:329-340.
3. Bahk YY, et al. 2004. Antigens secreted from Mycobacterium tuberculosis: identification by proteomics approach and test for diagnostic marker. Proteomics 4:99-3307.
4. Beatty WL, Russell DG. 2000. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 68:6997-7002.
5. Beck HC, et al. 2009. Proteomic analysis of cell surface-associated proteins from probiotic Lactobacillus plantarum. FEMS Microbiol. Lett. 297: 61-66.
6. Bermudez LE, Petrofsky M, Goodman J. 1997. Exposure to low oxygen tension and increased osmolarity enhance the ability of Mycobacterium avium to enter intestinal epithelial (HT-29) cells. Infect. Immun. 65: 3768-3773.
7. Bermudez LE, Shelton K, Young LS. 1995. Comparison of the ability of Mycobacterium avium, M. smegmatis and M. tuberculosis to invade and replicate within HEp-2 epithelial cells. Tuber. Lung Dis. 76:240-247.
8. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43:717-731.
9. Bigi F, et al. 2004. The knockout of the lprG-Rv1410 operon produces strong attenuation of Mycobacterium tuberculosis. Microbes Infect. 6:182-187.
10. Bott M, Niebisch A. 2003. The respiratory chain of Corynebacterium glutamicum. J. Biotechnol. 104:129-153.
11. Brodt HR, Enzensberger R, Kamps BS, Keul HG, Helm EB. 1997. Impact of disseminated Mycobacterium avium-complex infection on survival of HIV-infected patients. Eur. J. Med. Res. 2:106-110.
12. Cho D, Shin SJ, Collins MT. 2010. B-cell epitope specificity of carboxy terminus of Mycobacterium paratuberculosis ModD. J. Immunoassay Immunochem. 31:181-192.
13. Daleke MH, et al. 2011. Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via the ESX-5 pathway. J. Biol. Chem. 286:024-19034.
14. Dallo SF, Kannan TR, Blaylock MW, Baseman JB. 2002. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol. Microbiol. 46:1041-1051.
15. Danelishvili L, et al. 2007. Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection. Proc. Natl. Acad. Sci. U. S. A. 104:038-11043.
16. de Lima CS, et al. 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.
17. de Miguel N, et al. 2010. Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol. Cell Proteomics 9:1554-1566.
18. Drage MG, et al. 2010. Mycobacterium tuberculosis lipoprotein LprG (Rv1411c) binds triacylated glycolipid agonists of Toll-like receptor 2. Nat. Struct. Mol. Biol. 17:1088-1095.
19. Early J, Bermudez LE. 2011. Mimicry of the pathogenic mycobacterium vacuole in vitro elicits the bacterial intracellular phenotype, including early-onset macrophage death. Infect. Immun. 79:2412-2422.
20. Elia G. 2008. Biotinylation reagents for the study of cell surface proteins. Proteomics 8:4012-4024.
21. Farrow MF, Rubin EJ. 2008. Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein. J. Bacteriol. 190:1783-1791.
22. Fontan P, Aris V, Ghanny S, Soteropoulos P, Smith I. 2008. Global transcriptional profile of Mycobacterium tuberculosis during THP-1 human macrophage infection. Infect. Immun. 76:717-725.
23. Galli G, Ghezzi P, Mascagni P, Marcucci F, Fratelli M. 1996. Mycobacterium tuberculosis heat shock protein 10 increases both proliferation and death in mouse P19 teratocarcinoma cells. In Vitro Cell Dev. Biol. Anim. 32:446-450.
24. Garcia J, et al. 2009. Comprehensive profiling of the cell surface proteome of Sy5Y neuroblastoma cells yields a subset of proteins associated with tumor differentiation. J. Proteome Res. 8:3791-3796.
25. Gehring AJ, Dobos KM, Belisle JT, Harding CV, Boom WH. 2004. Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J. Immunol. 173:2660-2668.
26. Gioffre A, et al. 2009. Characterization of the Apa antigen from M. avium subsp. paratuberculosis: a conserved Mycobacterium antigen that elicits a strong humoral response in cattle. Vet. Immunol. Immunopathol. 132: 199-208.
27. Gonzalez-Zamorano M, et al. 2009. Mycobacterium tuberculosis glycoproteomics based on ConA-lectin affinity capture of mannosylated proteins. J. Proteome Res. 8:721-733.
28. Granato D, et al. 2004. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect. Immun. 72:2160-2169.
29. Griffiths TA, Rioux K, De Buck J. 2008. Sequence polymorphisms in a surface PPE protein distinguish types I, II, and III of Mycobacterium avium subsp. paratuberculosis. J. Clin. Microbiol. 46:1207-1212.
30. Gu S, et al. 2003. Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain. Mol. Cell Proteomics 2:1284-1296.
31. He Z, De Buck J. 2010. Cell wall proteome analysis of Mycobacterium smegmatis strain MC2 155. BMC Microbiol. 10:121.
32. He Z, De Buck J. 2010. Localization of proteins in the cell wall of Mycobacterium avium subsp. paratuberculosis K10 by proteomic analysis. Proteome Sci. 8:21.
33. Hempel K, et al. 2010. Quantitative cell surface proteome profiling for SigB-dependent protein expression in the human pathogen Staphylococcus aureus via biotinylation approach. J. Proteome Res. 9:1579-1590.
34. Henderson B, Lund PA, Coates AR. 2010. Multiple moonlighting functions of mycobacterial molecular chaperones. Tuberculosis 90:119-124.
35. Holub M, et al. 2010. Comparative study of the life cycle dependent post-translation modifications of protein synthesis elongation factor Tu present in the membrane proteome of streptomycetes and mycobacteria. Folia Microbiol. 55:203-210.
36. Honer Zu Bentrup K, Miczak A, Swenson DL, Russell DG. 1999. Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis. J. Bacteriol. 181:7161-7167.
37. Hughes V, et al. 2008. Immunogenicity of proteome-determined Mycobacterium avium subsp. paratuberculosis-specific proteins in sheep with paratuberculosis. Clin. Vaccine Immunol. 15:1824-1833.
38. Jagusztyn-Krynicka EK, Roszczenko P, Grabowska A. 2009. Impact of proteomics on anti-Mycobacterium tuberculosis (MTB) vaccine development. Pol. J. Microbiol. 58:281-287.
39. Katsube T, et al. 2007. Control of cell wall assembly by a histone-like protein in mycobacteria. J. Bacteriol. 189:8241-8249.
40. Kruh NA, Troudt J, Izzo A, Prenni J, Dobos KM. 2010. Portrait of a pathogen: the Mycobacterium tuberculosis proteome in vivo. PLoS One 5:e13938.
41. Kumar P, Amara RR, Challu VK, Chadda VK, Satchidanandam V. 2003. The Apa protein of Mycobacterium tuberculosis stimulates gamma interferon-secreting CD4+ and CD8+ T cells from purified protein derivative-positive individuals and affords protection in a guinea pig model. Infect. Immun. 71:1929-1937.
42. Kunnath-Velayudhan S, et al. 2010. Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc. Natl. Acad. Sci. U. S. A. 107:14703-14708.
43. Laqueyrerie A, et al. 1995. Cloning, sequencing, and expression of the apa gene coding for the Mycobacterium tuberculosis 45/47-kilodalton secreted antigen complex. Infect. Immun. 63:4003-4010.
44. Lew JM, Kapopoulou A, Jones LM, Cole ST. 2011. TubercuList-10 years after. Tuberculosis 91:1-7.
45. Li Y, et al. 2010. A proteome-scale identification of novel antigenic proteins in Mycobacterium tuberculosis toward diagnostic and vaccine development. J. Proteome Res. 9:4812-4822.
46. Li YJ, Danelishvili L, Wagner D, Petrofsky M, Bermudez LE. 2010. Identification of virulence determinants of Mycobacterium avium that impact on the ability to resist host killing mechanisms. J. Med. Microbiol. 59:8-16.
47. Lin J, Huang S, Zhang Q. 2002. Outer membrane proteins: key players for bacterial adaptation in host niches. Microbes Infect. 4:325-331.
48. Lindahl G, Stalhammar-Carlemalm M, Areschoug T. 2005. Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin. Microbiol. Rev. 18:102-127.
49. Lu B, McClatchy DB, Kim JY, Yates JR III. 2008. Strategies for shotgun identification of integral membrane proteins by tandem mass spectrometry. Proteomics 8:3947-3955.
50. Mahfoud M, Sukumaran S, Hulsmann P, Grieger K, Niederweis M. 2006. Topology of the porin MspA in the outer membrane of Mycobacterium smegmatis. J. Biol. Chem. 281:5908-5915.
51. Malen H, Berven FS, Fladmark KE, Wiker HG. 2007. Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv. Proteomics 7:1702-1718.
52. Marques MA, Chitale S, Brennan PJ, Pessolani MC. 1998. Mapping and identification of the major cell wall-associated components of Mycobacterium leprae. Infect. Immun. 66:2625-2631.
53. Master SS, et al. 2002. Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology 148:3139-3144.
54. Mawuenyega KG, et al. 2005. Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol. Biol. Cell 16:396-404.
55. McGarvey J, Bermudez LE. 2002. Pathogenesis of nontuberculous mycobacteria infections. Clin. Chest Med. 23:569-583.
56. McKinney JD, et al. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735-738.
57. Mitra K, et al. 2005. Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438:318-324.
58. Monahan IM, Betts J, Banerjee DK, Butcher PD. 2001. Differential expression of mycobacterial proteins following phagocytosis by macrophages. Microbiology 147:459-471.
59. Munoz-Elias EJ, McKinney JD. 2005. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11:638-644.
60. Murphy DJ, Brown JR. 2008. Novel drug target strategies against Mycobacterium tuberculosis. Curr. Opin. Microbiol. 11:422-427.
61. Newton V, McKenna SL, De Buck J. 2009. Presence of PPE proteins in Mycobacterium avium subsp. paratuberculosis isolates and their immunogenicity in cattle. Vet. Microbiol. 135:394-400.
62. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. 2010. Mycobacterial outer membranes: in search of proteins. Trends Microbiol. 18:109-116.
63. Ojha A, et al. 2005. GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123: 861-873.
64. Olsen I, Reitan LJ, Holstad G, Wiker HG. 2000. Alkyl hydroperoxide reductases C and D are major antigens constitutively expressed by Mycobacterium avium subsp. paratuberculosis. Infect. Immun. 68:801-808.
65. Olsen I, Wiker HG, Johnson E, Langeggen H, Reitan LJ. 2001. Elevated antibody responses in patients with Crohn's disease against a 14-kDa secreted protein purified from Mycobacterium avium subsp. paratuberculosis. Scand. J. Immunol. 53:198-203.
66. O'Toole R, Williams HD. 2003. Universal stress proteins and Mycobacterium tuberculosis. Res. Microbiol. 154:387-392.
67. Peake P, Gooley A, Britton WJ. 1993. Mechanism of interaction of the 85B secreted protein of Mycobacterium bovis with fibronectin. Infect. Immun. 61:4828-4834.
68. Prasad R, Yadav G. 2001. Identification of a 75 kDa highly immunodominant antigen from Mycobacterium smegmatis and cross-reactivity with other species. Indian J. Exp. Biol. 39:255-262.
69. Qamra R, Mande SC, Coates AR, Henderson B. 2005. The unusual chaperonins of Mycobacterium tuberculosis. Tuberculosis 85:385-394.
70. Qiu H, Wang Y. 2008. Quantitative analysis of surface plasma membrane proteins of primary and metastatic melanoma cells. J. Proteome Res. 7:1904-1915.
71. Ragas A, Roussel L, Puzo G, Riviere M. 2007. The Mycobacterium tuberculosis cell-surface glycoprotein apa as a potential adhesin to colonize target cells via the innate immune system pulmonary C-type lectin surfactant protein A. J. Biol. Chem. 282:5133-5142.
72. Rinke de Wit TF, et al. 1992. Mycobacteria contain two groEL genes: the second Mycobacterium leprae groEL gene is arranged in an operon with groES. Mol. Microbiol. 6:1995-2007.
73. Sabarth N, et al. 2002. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and twodimensional gel electrophoresis. J. Biol. Chem. 277:27896-27902.
74. Sani M, et al. 2010. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog. 6:e1000794.
75. Schilstra MJ, et al. 1984. Immunocytochemical localization of the elongation factor Tu in E. coli cells. FEBS Lett. 165:175-179.
76. Sharma V, Sharma S, KHoener zu Bentrup McKinney JD, Russell DG, Jacobs WR, Jr, Sacchettini JC. 2000. Structure of isocitrate lyase, a persistence factor of Mycobacterium tuberculosis. Nat. Struct. Biol. 7:663-668.
77. Sherman DR, et al. 1996. Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272:1641-1643.
78. Souza GS, et al. 2011. Apa antigen of Mycobacterium avium subsp. paratuberculosis as a target for species-specific immunodetection of the bacteria in infected tissues of cattle with paratuberculosis. Vet. Immunol. Immunopathol. 143:75-82.
79. Spence JM, Clark VL. 2000. Role of ribosomal protein L12 in gonococcal invasion of Hec1B cells. Infect. Immun. 68:5002-5010.
80. Tjalsma H, Lambooy L, Hermans PW, Swinkels DW. 2008. Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 8:1415-1428.
81. Verbelen C, Dufrene YF. 2009. Direct measurement of Mycobacteriumfibronectin interactions. Integr. Biol. 1:296-300.
82. Walters MS, Mobley HL. 2009. Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics. J. Microbiol. Methods 78:131-135.
83. Wang J, et al. 2009. Evaluation of a recombinant BCG expressing antigen Ag85B and PPE protein Rv3425 from DNA segment RD11 of Mycobacterium tuberculosis in C57BL/6 mice. Med. Microbiol. Immunol. 198:5-11.
84. Weigoldt M, et al. 2011. Differential proteome analysis of Mycobacterium avium subsp. paratuberculosis grown in vitro and isolated from cases of clinical Johne's disease. Microbiology 157:557-565.
85. Wiker HG, Tomazella GG, de Souza GA. 2011. A quantitative view on Mycobacterium leprae antigens by proteomics. J. Proteomics 74:1711-1719.
86. Wilson T, de Lisle GW, Marcinkeviciene JA, Blanchard JS, Collins DM. 1998. Antisense RNA to ahpC, an oxidative stress defence gene involved in isoniazid resistance, indicates that AhpC of Mycobacterium bovis has virulence properties. Microbiology 144:2687-2695.
87. Windle HJ, Brown PA, Kelleher DP. 2010. Proteomics of bacterial pathogenicity: therapeutic implications. Proteomics Clin. Appl. 4:215-227.
88. Yamazaki Y, et al. 2006. The ability to form biofilm influences Mycobacterium avium invasion and translocation of bronchial epithelial cells. Cell Microbiol. 8:806-814.