Conserved immune recognition hierarchy of mycobacterial PE/PPE proteins during infection in natural hosts

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Vordermeier, H Martin ^a   Hewinson, R Glyn ^a   Wilkinson, Robert J ^b,c,d   Wilkinson, Katalin A ^b,c   Gideon, Hannah P ^b   Young, Douglas B ^c,d   Sampson, Samantha L ^d  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GAMMA INTERFERON; GLUTAMIC ACID; PROLINE;

ADULT; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; BACTERIAL GENOME; CONTROLLED STUDY; COW; CROSS REACTION; CROSS-SECTIONAL STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE POOL; HOST CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOGENICITY; INTERFERON GAMMA RELEASE ASSAY; INTERFERON PRODUCTION; MALE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NATURAL HOST; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF;

ADULT; ANIMALS; BACTERIAL PROTEINS; CATTLE; FEMALE; HUMANS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; MALE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS, BOVINE;

BOS; BOVINAE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84864762781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040890     Document Type: Article

References (52)

1. Dye C, Williams BG, (2010) The population dynamics and control of tuberculosis. Science 328: 856-861.
2. DEFRA website. Available: http://www.defra.gov.uk/statistics/foodfarm/landuselivestock/cattletb/. Accessed 2012 Jun 23.
3. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
4. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, et al. (2003) The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci U S A 100: 7877-7882.
5. Strong M, Sawaya MR, Wang S, Phillips M, Cascio D, et al. (2006) Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 103: 8060-8065.
6. Rengarajan J, Bloom BR, Rubin EJ, (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102: 8327-8332.
7. Sassetti CM, Boyd DH, Rubin EJ, (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
8. Sassetti CM, Rubin EJ, (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100: 12989-12994.
9. Barbour A (2002) Antigenic variation by relapsing fever Borrelia species and other bacterial pathogens. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II. Washington, D.C.: ASM Press. 972-994.
10. Sampson SL, (2011) Mycobacterial PE/PPE proteins at the host-pathogen interface. Clin Dev Immunol 2011: 497203.
11. Ramakrishnan L, Federspiel NA, Falkow S, (2000) Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439.
12. Brennan MJ, Delogu G, (2002) The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol 10: 246-249.
13. Koh KW, Lehming N, Seah GT, (2009) Degradation-resistant protein domains limit host cell processing and immune detection of mycobacteria. Mol Immunol 46: 1312-1318.
14. Bansal K, Elluru SR, Narayana Y, Chaturvedi R, Patil SA, et al. (2010) PE_PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. Journal of Immunology 184: 3495-3504.
15. Bansal K, Sinha AY, Ghorpade DS, Togarsimalemath SK, Patil SA, et al. (2010) SH3-interacting domain of Rv1917c of Mycobacterium tuberculosis induces selective maturation of human dendritic cells by regulating PI3K-MAPK-NF-{kappa}B signaling and drives Th2 immune responses. Journal of Biological Chemistry 285: 36511-36522.
16. Basu S, Pathak SK, Banerjee A, Pathak S, Bhattacharyya A, et al. (2007) Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-alpha. Journal of Biological Chemistry 282: 1039-1050.
17. Nair S, Ramaswamy PA, Ghosh S, Joshi DC, Pathak N, et al. (2009) The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage. Journal of Immunology 183: 6269-6281.
18. Iantomasi R, Sali M, Cascioferro A, Palucci I, Zumbo A, et al. (2012) PE_PGRS30 is required for the full virulence of Mycobacterium tuberculosis. Cell Microbiol 14: 356-367.
19. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD, et al. (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evolutionary Biology 6: 95.
20. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, et al. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proceedings of the National Academy of Sciences U S A 100: 12420-12425.
21. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST, (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Molecular Microbiology 46: 709-717.
22. Stanley SA, Raghavan S, Hwang WW, Cox JS, (2003) Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proceedings of the National Academy of Sciences U S A 100: 13001-13006.
23. Abdallah AM, Verboom T, Hannes F, Safi M, Strong M, et al. (2006) A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Molecular Microbiology 62: 667-679.
24. Abdallah AM, Verboom T, Weerdenburg EM, Gey van Pittius NC, Mahasha PW, et al. (2009) PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Molecular Microbiology 73: 329-340.
25. Daleke MH, Cascioferro A, de Punder K, Ummels R, Abdallah AM, 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: 19024-19034.
26. Bottai D, Di Luca M, Majlessi L, Frigui W, Simeone R,et al. (2012) Disruption of the ESX-5 system of Mycobacterium tuberculosis causes loss of PPE protein secretion, reduction of cell wall integrity and strong attenuation. Mol Microbiol.
27. Leroux-Roels I, Leroux-Roels G, Ofori-Anyinam O, Moris P, De Kock E, et al. (2010) Evaluation of the safety and immunogenicity of two antigen concentrations of the Mtb72F/AS02(A) candidate tuberculosis vaccine in purified protein derivative-negative adults. Clin Vaccine Immunol 17: 1763-1771.
28. Reed SG, Coler RN, Dalemans W, Tan EV, DeLa Cruz EC, et al. (2009) Defined tuberculosis vaccine, Mtb72F/AS02A, evidence of protection in cynomolgus monkeys. Proc Natl Acad Sci U S A 106: 2301-2306.
29. Tsenova L, Harbacheuski R, Moreira AL, Ellison E, Dalemans W, et al. (2006) Evaluation of the Mtb72F polyprotein vaccine in a rabbit model of tuberculous meningitis. Infect Immun 74: 2392-2401.
30. Von Eschen K, Morrison R, Braun M, Ofori-Anyinam O, De Kock E, et al. (2009) The candidate tuberculosis vaccine Mtb72F/AS02A: Tolerability and immunogenicity in humans. Hum Vaccin 5: 475-482.
31. Dean GS, Rhodes SG, Coad M, Whelan AO, Wheeler P, et al. (2008) Isoniazid treatment of Mycobacterium bovis in cattle as a model for human tuberculosis. Tuberculosis (Edinb) 88: 586-594.
32. Whelan AO, Wright DC, Chambers MA, Singh M, Hewinson RG, et al. (2008) Evidence for enhanced central memory priming by live Mycobacterium bovis BCG vaccine in comparison with killed BCG formulations. Vaccine 26: 166-173.
33. Golby P, Hatch KA, Bacon J, Cooney R, Riley P, et al. (2007) Comparative transcriptomics reveals key gene expression differences between the human and bovine pathogens of the Mycobacterium tuberculosis complex. Microbiology 153: 3323-3336.
34. Rehren G, Walters S, Fontan P, Smith I, Zarraga AM, (2007) Differential gene expression between Mycobacterium bovis and Mycobacterium tuberculosis. Tuberculosis (Edinb) 87: 347-359.
35. Voskuil MI, Schnappinger D, Rutherford R, Liu Y, (2004) Schoolnik GK (2004) Regulation of the Mycobacterium tuberculosis PE/PPE genes. Tuberculosis (Edinb) 84: 256-262.
36. Rachman H, Strong M, Ulrichs T, Grode L, Schuchhardt J, et al. (2006) Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis. Infect Immun 74: 1233-1242.
37. Talaat AM, Lyons R, Howard ST, Johnston SA, (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci U S A 101: 4602-4607.
38. Talaat AM, Ward SK, Wu CW, Rondon E, Tavano C, et al. (2007) Mycobacterial bacilli are metabolically active during chronic tuberculosis in murine lungs: insights from genome-wide transcriptional profiling. J Bacteriol 189: 4265-4274.
39. 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.
40. Jones GJ, Hewinson RG, Vordermeier HM, (2010) Screening of predicted secreted antigens from Mycobacterium bovis identifies potential novel differential diagnostic reagents. Clin Vaccine Immunol 17: 1344-1348.
41. Jones GJ, Gordon SV, Hewinson RG, Vordermeier HM, (2010) Screening of predicted secreted antigens from Mycobacterium bovis reveals the immunodominance of the ESAT-6 protein family. Infect Immun 78: 1326-1332.
42. Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D, et al. (2006) Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74: 88-98.
43. Millington KA, Innes JA, Hackforth S, Hinks TS, Deeks JJ, et al. (2007) Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J Immunol 178: 5217-5226.
44. Comas I, Chakravartti J, Small PM, Galagan J, Niemann S, et al. (2010) Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat Genet 42: 498-503.
45. Hermans PW, van Soolingen D, van Embden JD, (1992) Characterization of a major polymorphic tandem repeat in Mycobacterium tuberculosis and its potential use in the epidemiology of Mycobacterium kansasii and Mycobacterium gordonae. J Bacteriol 174: 4157-4165.
46. Karboul A, Gey van Pittius NC, Namouchi A, Vincent V, Sola C, et al. (2006) Insights into the evolutionary history of tubercle bacilli as disclosed by genetic rearrangements within a PE_PGRS duplicated gene pair. BMC Evol Biol 6: 107.
47. Talarico S, Zhang L, Marrs CF, Foxman B, Cave MD, et al. (2008) Mycobacterium tuberculosis PE_PGRS16 and PE_PGRS26 genetic polymorphism among clinical isolates. Tuberculosis (Edinb) 88: 283-294.
48. Delogu G, Brennan MJ, (2001) Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69: 5606-5611.
49. Pirson C, Vipond J, Hall Y, Williams A, Vordermeier HM, (2011) Vaccines designed to protect against Mycobacterium tuberculosis infection may aid the identification of novel vaccine constructs and diagnostic antigens for bovine tuberculosis. Vet Microbiol 148: 232-237.
50. Flynn JL, Chan J, (2005) What's good for the host is good for the bug. Trends Microbiol 13: 98-102.
51. Vordermeier HM, Whelan A, Cockle PJ, Farrant L, Palmer N, et al. (2001) Use of synthetic peptides derived from the antigens ESAT-6 and CFP-10 for differential diagnosis of bovine tuberculosis in cattle. Clin Diagn Lab Immunol 8: 571-578.
52. European Economic Community, (1980) EEC directive 80/219, amending directive 64/432 annexe B. Official J. L047: 25-32.