The Mycobacterium tuberculosis PE Proteins Rv0285 and Rv1386 Modulate Innate Immunity and Mediate Bacillary Survival in Macrophages

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Tiwari, Bhavana Mishra ^a   Kannan, Nisha ^a   Vemu, Lakshmi ^b   Raghunand, Tirumalai R ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b NIZAM'S INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BACTERIAL PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P70; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN PE15; PROTEIN PE5; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL COUNT; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; DRUG TARGETING; ENZYME PHOSPHORYLATION; GENE FUNCTION; GENETIC CONSERVATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PE15 GENE; PE5 GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UPREGULATION;

AMINO ACID SEQUENCE; APOPTOSIS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINES; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; TUBERCULOSIS; VIRULENCE;

MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84871299970     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051686     Document Type: Article

References (51)

1. Lin PL, Flynn JL, (2010) Understanding latent tuberculosis: a moving target. J Immunol 185: 15-22.
2. Akhter Y, Ehebauer MT, Mukhopadhyay S, Hasnain SE, (2012) The PE/PPE multigene family codes for virulence factors and is a possible source of mycobacterial antigenic variation: perhaps more? Biochimie 94: 110-116.
3. 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 Evol Biol 6: 95.
4. Tundup S, Pathak N, Ramanadham M, Mukhopadhyay S, Murthy KJ, et al. (2008) The co-operonic PE25/PPE41 protein complex of Mycobacterium tuberculosis elicits increased humoral and cell mediated immune response. PLoS One 3: e3586.
5. Riley R, Pellegrini M, Eisenberg D, (2008) Identifying cognate binding pairs among a large set of paralogs: the case of PE/PPE proteins of Mycobacterium tuberculosis. PLoS Comput Biol 4: e1000174.
6. Banu S, Honore N, Saint-Joanis B, Philpott D, Prevost MC, et al. (2002) Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol Microbiol 44: 9-19.
7. Brennan MJ, Delogu G, (2002) The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol 10: 246-249.
8. Brennan MJ, Delogu G, Chen Y, Bardarov S, Kriakov J, et al. (2001) Evidence that mycobacterial PE_PGRS proteins are cell surface constituents that influence interactions with other cells. Infect Immun 69: 7326-7333.
9. Cascioferro A, Delogu G, Colone M, Sali M, Stringaro A, et al. (2007) PE is a functional domain responsible for protein translocation and localization on mycobacterial cell wall. Mol Microbiol 66: 1536-1547.
10. Cascioferro A, Daleke MH, Ventura M, Dona V, Delogu G, et al. (2011) Functional dissection of the PE domain responsible for translocation of PE_PGRS33 across the mycobacterial cell wall. PLoS One 6: e27713.
11. Campuzano J, Aguilar D, Arriaga K, Leon JC, Salas-Rangel LP, et al. (2007) The PGRS domain of Mycobacterium tuberculosis PE_PGRS Rv1759c antigen is an efficient subunit vaccine to prevent reactivation in a murine model of chronic tuberculosis. Vaccine 25: 3722-3729.
12. Chaitra MG, Hariharaputran S, Chandra NR, Shaila MS, Nayak R, (2005) Defining putative T cell epitopes from PE and PPE families of proteins of Mycobacterium tuberculosis with vaccine potential. Vaccine 23: 1265-1272.
13. Delogu G, Brennan MJ, (2001) Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69: 5606-5611.
14. 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.
15. Balaji KN, Goyal G, Narayana Y, Srinivas M, Chaturvedi R, et al. (2007) Apoptosis triggered by Rv1818c, a PE family gene from Mycobacterium tuberculosis is regulated by mitochondrial intermediates in T cells. Microbes Infect 9: 271-281.
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. J Biol Chem 282: 1039-1050.
17. 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.
18. Dheenadhayalan V, Delogu G, Sanguinetti M, Fadda G, Brennan MJ, (2006) Variable expression patterns of Mycobacterium tuberculosis PE_PGRS genes: evidence that PE_PGRS16 and PE_PGRS26 are inversely regulated in vivo. J Bacteriol 188: 3721-3725.
19. 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.
20. Sambrook J, Fritsch, E. F. & Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn.: Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
21. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
22. Hofmann K, W Stoffel, (1993) TMbasc-a database of membrane spanning protein segments. Biol Chem Hoppe-Seyler 374: 166.
23. Kyte J, Doolittle RF, (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
24. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
25. Spratt JM, Ryan AA, Britton WJ, Triccas JA, (2005) Epitope-tagging vectors for the expression and detection of recombinant proteins in mycobacteria. Plasmid 53: 269-273.
26. Stover CK, de la Cruz VF, Fuerst TR, Burlein JE, Benson LA, et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
27. McEvoy CR, Cloete R, Muller B, Schurch AC, van Helden PD, et al. (2012) Comparative analysis of Mycobacterium tuberculosis pe and ppe genes reveals high sequence variation and an apparent absence of selective constraints. PLoS One 7: e30593.
28. Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, et al. (2010) The multifunctional PE_PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J Biol Chem 285: 30389-30403.
29. Daim S, Kawamura I, Tsuchiya K, Hara H, Kurenuma T, et al. (2011) Expression of the Mycobacterium tuberculosis PPE37 protein in Mycobacterium smegmatis induces low tumour necrosis factor alpha and interleukin 6 production in murine macrophages. J Med Microbiol 60: 582-591.
30. Huang Y, Wang Y, Bai Y, Wang ZG, Yang L, et al. (2010) Expression of PE_PGRS 62 protein in Mycobacterium smegmatis decrease mRNA expression of proinflammatory cytokines IL-1beta, IL-6 in macrophages. Mol Cell Biochem 340: 223-229.
31. Singh PP, Parra M, Cadieux N, Brennan MJ, (2008) A comparative study of host response to three Mycobacterium tuberculosis PE_PGRS proteins. Microbiology 154: 3469-3479.
32. 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. J Immunol 183: 6269-6281.
33. Delogu G, Pusceddu C, Bua A, Fadda G, Brennan MJ, et al. (2004) Rv1818c-encoded PE_PGRS protein of Mycobacterium tuberculosis is surface exposed and influences bacterial cell structure. Mol Microbiol 52: 725-733.
34. Dheenadhayalan V, Delogu G, Brennan MJ, (2006) Expression of the PE_PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes Infect 8: 262-272.
35. Sampson SL, Lukey P, Warren RM, van Helden PD, Richardson M, et al. (2001) Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis (Edinb) 81: 305-317.
36. Anes E, Peyron P, Staali L, Jordao L, Gutierrez MG, et al. (2006) Dynamic life and death interactions between Mycobacterium smegmatis and J774 macrophages. Cell Microbiol 8: 939-960.
37. Gupta D, Sharma S, Singhal J, Satsangi AT, Antony C, et al. (2010) Suppression of TLR2-induced IL-12, reactive oxygen species, and inducible nitric oxide synthase expression by Mycobacterium tuberculosis antigens expressed inside macrophages during the course of infection. J Immunol 184: 5444-5455.
38. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, et al. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198: 705-713.
39. Flynn JL, Chan J, (2001) Immunology of tuberculosis. Annu Rev Immunol 19: 93-129.
40. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181.
41. 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.
42. Tundup S, Akhter Y, Thiagarajan D, Hasnain SE, (2006) Clusters of PE and PPE genes of Mycobacterium tuberculosis are organized in operons: evidence that PE Rv2431c is co-transcribed with PPE Rv2430c and their gene products interact with each other. FEBS Lett 580: 1285-1293.
43. Singh A, Mai D, Kumar A, Steyn AJ, (2006) Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 103: 11346-11351.
44. Mukhopadhyay S, Balaji KN, (2011) The PE and PPE proteins of Mycobacterium tuberculosis. Tuberculosis (Edinb) 91: 441-447.
45. Malen H, Berven FS, Fladmark KE, Wiker HG, (2007) Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv. Proteomics 7: 1702-1718.
46. Dinarello CA, (2000) Proinflammatory cytokines. Chest 118: 503-508.
47. Opal SM, DePalo VA, (2000) Anti-inflammatory cytokines. Chest 117: 1162-1172.
48. Redpath S, Ghazal P, Gascoigne NR, (2001) Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol 9: 86-92.
49. Murray PJ, Young RA, (1999) Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect Immun 67: 3087-3095.
50. Sampson SL, (2011) Mycobacterial PE/PPE proteins at the host-pathogen interface. Clin Dev Immunol 2011: 497203.
51. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CM,et al. General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci U S A 109: 11342-11347.