Ins and outs of Mycobacterium tuberculosis PPE family in pathogenesis and implications for novel measures against tuberculosis

Journal of Cellular Biochemistry

Volumn 113, Issue 4, 2012, Pages 1087-1095

  Deng, Wanyan ^a   Xie, Jianping ^a  

^a SOUTHWEST UNIVERSITY   (China)

Author keywords

IMMUNE EVASION; M. tuberculosis; PATHOGENESIS; PPE FAMILY; VACCINE

Indexed keywords

BACTERIAL ANTIGEN; BIOLOGICAL MARKER; TRIACYLGLYCEROL LIPASE; VACCINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CELLULAR IMMUNITY; FATTY ACID METABOLISM; GENE EXPRESSION; HUMAN; INNATE IMMUNITY; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SERODIAGNOSIS; TUBERCULOSIS;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IMMUNE EVASION; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 84857620233     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23449     Document Type: Article

References (77)

1. Abdallah AM, Verboom T, Hannes F, Safi M, Strong M, Eisenberg D, Musters RJ, Vandenbroucke-Grauls CM, Appelmelk BJ, Luirink J, Bitter W,. 2006. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol Microbiol 62 (3): 667-679.
2. Adindla S, Guruprasad L,. 2003. Sequence analysis corresponding to the PPE and PE proteins in Mycobacterium tuberculosis and other genomes. J Biosci 28 (2): 169-179.
3. Baldwin SL, Bertholet S, Kahn M, Zharkikh I, Ireton GC, Vedvick TS, Reed SG, Coler RN,. 2009. Intradermal immunization improves protective efficacy of a novel TB vaccine candidate. Vaccine 27 (23): 3063-3071.
4. Bansal K, Sinha AY, Ghorpade DS, Togarsimalemath SK, Patil SA, Kaveri SV, Balaji KN, Bayry J,. 2010. Src homology 3-interacting domain of Rv1917c of Mycobacterium tuberculosis induces selective maturation of human dendritic cells by regulating PI3K-MAPK-NF-kappaB signaling and drives Th2 immune responses. J Biol Chem 285 (47): 36511-36522.
5. Bertholet S, Ireton GC, Kahn M, Guderian J, Mohamath R, Stride N, Laughlin EM, Baldwin SL, Vedvick TS, Coler RN, Reed SG,. 2008. Identification of human T cell antigens for the development of vaccines against Mycobacterium tuberculosis. J Immunol 181 (11): 7948-7957.
6. 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 (3): 717-731.
7. Bonanni D, Rindi L, Lari N, Garzelli C,. 2005. Immunogenicity of mycobacterial PPE44 (Rv2770c) in Mycobacterium bovis BCG-infected mice. J Med Microbiol 54 (Pt 5): 443-448.
8. Bottai D, Brosch R,. 2009. Mycobacterial PE, PPE and ESX clusters: Novel insights into the secretion of these most unusual protein families. Mol Microbiol 73 (3): 325-328.
9. Brennan MJ, Delogu G,. 2002. The PE multigene family: A 'molecular mantra' for mycobacteria. Trends Microbiol 10 (5): 246-249.
10. Brodin P, Rosenkrands I, Andersen P, Cole ST, Brosch R,. 2004. ESAT-6 proteins: Protective antigens and virulence factors? Trends Microbiol 12 (11): 500-508.
11. Brodin P, Poquet Y, Levillain F, Peguillet I, Larrouy-Maumus G, Gilleron M, Ewann F, Christophe T, Fenistein D, Jang J, Jang MS, Park SJ, Rauzier J, Carralot JP, Shrimpton R, Genovesio A, Gonzalo-Asensio JA, Puzo G, Martin C, Brosch R, Stewart GR, Gicquel B, Neyrolles O,. 2010. High content phenotypic cell-based visual screen identifies Mycobacterium tuberculosis acyltrehalose-containing glycolipids involved in phagosome remodeling. PLoS Pathog 6 (9): e1001100.
12. Caruso AM, Serbina N, Klein E, Triebold K, Bloom BR, Flynn JL,. 1999. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-gamma, yet succumb to tuberculosis. J Immunol 162 (9): 5407-5416.
13. Cerdeno-Tarraga AM, Efstratiou A, Dover LG, Holden MT, Pallen M, Bentley SD, Besra GS, Churcher C, James KD, De Zoysa A, Chillingworth T, Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, Jagels K, Moule S, Quail MA, Rabbinowitsch E, Rutherford KM, Thomson NR, Unwin L, Whitehead S, Barrell BG, Parkhill J,. 2003. The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res 31 (22): 6516-6523.
14. Chakhaiyar P, Nagalakshmi Y, Aruna B, Murthy KJ, Katoch VM, Hasnain SE,. 2004. Regions of high antigenicity within the hypothetical PPE major polymorphic tandem repeat open-reading frame, Rv2608, show a differential humoral response and a low T cell response in various categories of patients with tuberculosis. J Infect Dis 190 (7): 1237-1244.
15. Choudhary RK, Mukhopadhyay S, Chakhaiyar P, Sharma N, Murthy KJR, Katoch VM, Hasnain SE,. 2003. PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect Immun 71 (11): 6338-6343.
16. Choudhary RK, Pullakhandam R, Ehtesham NZ, Hasnain SE,. 2004. Expression and characterization of Rv2430c, a novel immunodominant antigen of Mycobacterium tuberculosis. Protein Expr Purif 36 (2): 249-253.
17. Cole ST,. 1999. Learning from the genome sequence of Mycobacterium tuberculosis H37Rv. FEBS Lett 452 (1-2): 7-10.
18. Cole ST, Barrell BG,. 1998. Analysis of the genome of Mycobacterium tuberculosis H37Rv. Novartis Found Symp 217: 160-172 (discussion 172-167).
19. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG,. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 (6685): 537-544.
20. Cuccu B, Freer G, Genovesi A, Garzelli C, Rindi L,. 2011. Identification of a human immunodominant T-cell epitope of Mycobacterium tuberculosis antigen PPE44. BMC Microbiol 11 (1): 167.
21. Daim S, Kawamura I, Tsuchiya K, Hara H, Kurenuma T, Shen Y, Dewamitta SR, Sakai S, Nomura T, Qu H, Mitsuyama M,. 2011. Expression of the Mycobacterium tuberculosis PPE37 protein in Mycobacterium smegmatis induces low TNF-{alpha} and IL-6 production in murine macrophages. J Med Microbiol 60 (Pt5): 582-591.
22. Daleke MH, Cascioferro A, de Punder K, Ummels R, Abdallah AM, van der Wel N, Peters PJ, Luirink J, Manganelli R, Bitter W,. 2011. Conserved PE and PPE protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via ESX-5. J Biol Chem 286 (21): 19024-19034.
23. Deb C, Daniel J, Sirakova TD, Abomoelak B, Dubey VS, Kolattukudy PE,. 2006. A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J Biol Chem 281 (7): 3866-3875.
24. DiGiuseppe Champion PA, Champion MM, Manzanillo P, Cox JS,. 2009. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol Microbiol 73 (5): 950-962.
25. Dillon DC, Alderson MR, Day CH, Lewinsohn DM, Coler R, Bement T, Campos-Neto A, Skeiky YA, Orme IM, Roberts A, Steen S, Dalemans W, Badaro R, Reed SG,. 1999. Molecular characterization and human T-cell responses to a member of a novel Mycobacterium tuberculosis mtb39 gene family. Infect Immun 67 (6): 2941-2950.
26. Doran TJ, Hodgson AL, Davies JK, Radford AJ,. 1992. Characterisation of a novel repetitive DNA sequence from Mycobacterium bovis. FEMS Microbiol Lett 75 (2-3): 179-185.
27. Flynn JL, Goldstein MM, Triebold KJ, Koller B, Bloom BR,. 1992. Major histocompatibility complex class I-restricted T cells are required for resistance to Mycobacterium tuberculosis infection. Proc Natl Acad Sci USA 89 (24): 12013-12017.
28. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG,. 2003. The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 100 (13): 7877-7882.
29. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD,. 2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2 (10): RESEARCH0044.
30. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD, Warren RM,. 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.
31. Goldstone RM, Goonesekera SD, Bloom BR, Sampson SL,. 2009. The transcriptional regulator Rv0485 modulates the expression of a pe and ppe gene pair and is required for Mycobacterium tuberculosis virulence. Infect Immun 77 (10): 4654-4667.
32. Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE, Lewinsohn DM, Smith S, Sherman DR,. 2004. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 51 (2): 359-370.
33. 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 (12): 4157-4165.
34. Ishikawa J, Yamashita A, Mikami Y, Hoshino Y, Kurita H, Hotta K, Shiba T, Hattori M,. 2004. The complete genomic sequence of Nocardia farcinica IFM 10152. Proc Natl Acad Sci USA 101 (41): 14925-14930.
35. Jain SK, Paul-Satyaseela M, Lamichhane G, Kim KS, Bishai WR,. 2006. Mycobacterium tuberculosis invasion and traversal across an in vitro human blood-brain barrier as a pathogenic mechanism for central nervous system tuberculosis. J Infect Dis 193 (9): 1287-1295.
36. Jha SS, Danelishvili L, Wagner D, Maser J, Li Y-j, Moric I, Vogt S, Yamazaki Y, Lai B, Bermudez LE,. 2010. Virulence-related Mycobacterium avium subsp hominissuis MAV-2928 gene is associated with vacuole remodeling in macrophages. BMC Microbiol 10 (1): 100.
37. Khan N, Alam K, Nair S, Valluri VL, Murthy KJ, Mukhopadhyay S,. 2008. Association of strong immune responses to PPE protein Rv1168c with active tuberculosis. Clin Vaccine Immunol 15 (6): 974-980.
38. Le Moigne V, Robreau G, Borot C, Guesdon JL, Mahana W,. 2005. Expression, immunochemical characterization and localization of the Mycobacterium tuberculosis protein p27. Tuberculosis (Edinb) 85 (4): 213-219.
39. Li Y, Miltner E, Wu M, Petrofsky M, Bermudez LE,. 2005. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol 7 (4): 539-548.
40. Luthi B, Diacon AH,. 2011. [Tuberculosis and HIVâFeatures of the co-infection]. Ther Umsch 68 (7): 389-394.
41. Manganelli R, Voskuil MI, Schoolnik GK, Smith I,. 2001. The Mycobacterium tuberculosis ECF sigma factor sigmaE: Role in global gene expression and survival in macrophages. Mol Microbiol 41 (2): 423-437.
42. Manganelli R, Voskuil MI, Schoolnik GK, Dubnau E, Gomez M, Smith I,. 2002. Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45 (2): 365-374.
43. Mishra KC, de Chastellier C, Narayana Y, Bifani P, Brown AK, Besra GS, Katoch VM, Joshi B, Balaji KN, Kremer L,. 2008. Functional role of the PE domain and immunogenicity of the Mycobacterium tuberculosis triacylglycerol hydrolase LipY. Infect Immun 76 (1): 127-140.
44. Nair S, Ramaswamy PA, Ghosh S, Joshi DC, Pathak N, Siddiqui I, Sharma P, Hasnain SE, Mande SC, Mukhopadhyay S,. 2009. The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage. J Immunol 183 (10): 6269-6281.
45. Nair S, Pandey AD, Mukhopadhyay S,. 2011. The PPE18 protein of Mycobacterium tuberculosis inhibits NF-{kappa}B/rel-mediated proinflammatory cytokine production by upregulating and phosphorylating suppressor of cytokine signaling 3 protein. J Immunol 186 (9): 5413-5424.
46. Okkels LM, Brock I, Follmann F, Agger EM, Arend SM, Ottenhoff TH, Oftung F, Rosenkrands I, Andersen P,. 2003. PPE protein (Rv3873) from DNA segment RD1 of Mycobacterium tuberculosis: Strong recognition of both specific T-cell epitopes and epitopes conserved within the PPE family. Infect Immun 71 (11): 6116-6123.
47. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR,. 2003. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48 (3): 833-843.
48. Poulet S, Cole ST,. 1995. Characterization of the highly abundant polymorphic GC-rich-repetitive sequence (PGRS) present in Mycobacterium tuberculosis. Arch Microbiol 163 (2): 87-95.
49. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I,. 2002. ideR, An essential gene in Mycobacterium tuberculosis: Role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70 (7): 3371-3381.
50. Romano M, Rindi L, Korf H, Bonanni D, Adnet PY, Jurion F, Garzelli C, Huygen K,. 2008. Immunogenicity and protective efficacy of tuberculosis subunit vaccines expressing PPE44 (Rv2770c). Vaccine 26 (48): 6053-6063.
51. Sampson SL, Lukey P, Warren RM, van Helden PD, Richardson M, Everett MJ,. 2001. Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis (Edinb) 81 (5-6): 305-317.
52. Samten B, Wang X, Barnes PF,. 2009. Mycobacterium tuberculosis ESX-1 system-secreted protein ESAT-6 but not CFP10 inhibits human T-cell immune responses. Tuberculosis (Edinb) 89 (Suppl 1): S74-76.
53. Sani M, Houben EN, Geurtsen J, Pierson J, de Punder K, van Zon M, Wever B, Piersma SR, Jimenez CR, Daffe M, Appelmelk BJ, Bitter W, van der Wel N, Peters PJ,. 2010. Direct visualization by cryo-EM of the mycobacterial capsular layer: A labile structure containing ESX-1-secreted proteins. PLoS Pathog 6 (3): e1000794.
54. Sassetti CM, Rubin EJ,. 2003. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100 (22): 12989-12994.
55. Sassetti CM, Boyd DH, Rubin EJ,. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48 (1): 77-84.
56. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK,. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: Insights into the phagosomal environment. J Exp Med 198 (5): 693-704.
57. Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M, Cheng TY, Siddiqi N, Fortune SM, Moody DB, Rubin EJ,. 2009. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci USA 106 (44): 18792-18797.
58. Singh KK, Dong Y, Patibandla SA, McMurray DN, Arora VK, Laal S,. 2005. Immunogenicity of the Mycobacterium tuberculosis PPE55 (Rv3347c) protein during incipient and clinical tuberculosis. Infect Immun 73 (8): 5004-5014.
59. Skeiky YA, Ovendale PJ, Jen S, Alderson MR, Dillon DC, Smith S, Wilson CB, Orme IM, Reed SG, Campos-Neto A,. 2000. T cell expression cloning of a Mycobacterium tuberculosis gene encoding a protective antigen associated with the early control of infection. J Immunol 165 (12): 7140-7149.
60. Soldini S, Palucci I, Zumbo A, Sali M, Ria F, Manganelli R, Fadda G, Delogu G,. 2011. PPE-MPTR genes are differentially expressed by Mycobacterium tuberculosis in vivo. Tuberculosis (Edinb) 91 (6): 563-568.
61. Srivastava R, Kumar D, Waskar MN, Sharma M, Katoch VM, Srivastava BS,. 2006. Identification of a repetitive sequence belonging to a PPE gene of Mycobacterium tuberculosis and its use in diagnosis of tuberculosis. J Med Microbiol 55 (Pt 8): 1071-1077.
62. Stewart GR, Patel J, Robertson BD, Rae A, Young DB,. 2005. Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog 1 (3): 269-278.
63. Strong M, Sawaya MR, Wang S, Phillips M, Cascio D, Eisenberg D,. 2006. Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103 (21): 8060-8065.
64. Sultana R, Tanneeru K, Guruprasad L,. 2011. The PE-PPE domain in mycobacterium reveals a serine alpha/beta hydrolase fold and function: An in-silico analysis. PLoS One 6 (2): e16745.
65. Talarico S, Zhang L, Marrs CF, Foxman B, Cave MD, Brennan MJ, Yang Z,. 2008. Mycobacterium tuberculosis PE-PGRS16 and PE-PGRS26 genetic polymorphism among clinical isolates. Tuberculosis (Edinb) 88 (4): 283-294.
66. Tian C, Jian-Ping X,. 2010. Roles of PE-PGRS family in Mycobacterium tuberculosis pathogenesis and novel measures against tuberculosis. Microb Pathog 49 (6): 311-314.
67. Trinchieri G,. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3 (2): 133-146.
68. 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 (5): 1285-1293.
69. Tundup S, Pathak N, Ramanadham M, Mukhopadhyay S, Murthy KJ, Ehtesham NZ, Hasnain SE,. 2008. The co-operonic PE25/PPE41 protein complex of Mycobacterium tuberculosis elicits increased humoral and cell mediated immune response. PLoS One 3 (10): e3586.
70. Venkatesh KK, Swaminathan S, Andrews JR, Mayer KH,. 2011. Tuberculosis and HIV co-infection: Screening and treatment strategies. Drugs 71 (9): 1133-1152.
71. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK,. 2003. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198 (5): 705-713.
72. Voskuil MI, Schnappinger D, Rutherford R, Liu Y, Schoolnik GK,. 2004a. Regulation of the Mycobacterium tuberculosis PE/PPE genes. Tuberculosis (Edinb) 84 (3-4): 256-262.
73. Voskuil MI, Visconti KC, Schoolnik GK,. 2004b. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84 (3-4): 218-227.
74. Wang J, Qie Y, Zhang H, Zhu B, Xu Y, Liu W, Chen J, Wang H,. 2008. PPE protein (Rv3425) from DNA segment RD11 of Mycobacterium tuberculosis: A novel immunodominant antigen of Mycobacterium tuberculosis induces humoral and cellular immune responses in mice. Microbiol Immunol 52 (4): 224-230.
75. Wang J, Qie Y, Zhu B, Zhang H, Xu Y, Wang Q, Chen J, Liu W, Wang H,. 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 (1): 5-11.
76. Yu X, Sun Z, Zhou C, Wen Z, Chen J, Sun Q, Wang H, Zhang S,. 2010. [Expression, purification, and characterization Mycobacterium tuberculosis Rv1168c]. Wei Sheng Wu Xue Bao 50 (7): 931-936.
77. Zhang H, Wang J, Lei J, Zhang M, Yang Y, Chen Y, Wang H,. 2007. PPE protein (Rv3425) from DNA segment RD11 of Mycobacterium tuberculosis: A potential B-cell antigen used for serological diagnosis to distinguish vaccinated controls from tuberculosis patients. Clin Microbiol Infect 13 (2): 139-145.