Protective and survival efficacies of Rv0160c protein in murine model of Mycobacterium tuberculosis

Applied Microbiology and Biotechnology

Volumn 97, Issue 13, 2013, Pages 5825-5837

  Singh, Susmita K ^a   Tripathi, Dinesh K ^a   Singh, Pramod K ^a   Sharma, Sharad ^a   Srivastava, Kishore K ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Immunodominant antigen; Pathogenesis; Persistence; Rv0160c; Tuberculosis

Indexed keywords

MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PATHOGENESIS; PERSISTENCE; PULMONARY TUBERCULOSIS; RV0160C; TUBERCULOSIS; TUBERCULOSIS PATIENTS;

AMINO ACIDS; ANTIGENS; BACTERIA; MAMMALS; TUBES (COMPONENTS);

PROTEINS;

BACTERIAL PROTEIN; BCG VACCINE; INTERLEUKIN 2; INTERLEUKIN 6; PROTEIN RV0160C; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

AMINO ACID; ANTIGEN; BACTERIUM; GENE EXPRESSION; GENETIC ENGINEERING; GENOME; PATHOGENICITY; PROTEIN; PUBLIC HEALTH; RODENT; TUBERCULOSIS;

ACIDITY; ACTIVE IMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL HYPOXIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL MODEL; EXTRAPULMONARY TUBERCULOSIS; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; LUNG TUBERCULOSIS; MACROPHAGE; MAJOR CLINICAL STUDY; MOUSE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PHYSIOLOGICAL STRESS; PROTECTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SPLEEN CELL; SURVIVAL;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CYTOKINES; DISEASE MODELS, ANIMAL; HUMANS; IMMUNODOMINANT EPITOPES; MACROPHAGES; MICE; MICROBIAL VIABILITY; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS; VIRULENCE FACTORS;

CORYNEBACTERINEAE; MURINAE; MUS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84879386329     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4493-2     Document Type: Article

References (45)

1. Abou-Zeid C, Garbe T, Lathigra R, Wiker HG, Harboe M, Rook GA, Young DB (1991) Genetic and immunological analysis of Mycobacterium tuberculosis fibronectin-binding proteins. Infect Immun 59:2712-2718
2. Beatty WL, Ullrich HJ, Russell DG (2001) Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur J Cell Biol 80:31-40. doi: 10.1078/0171-9335-00131
3. 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. doi: 10.1046/j.1365-2958.2002.02779.x
4. Boon C, Li R, Qi R, Dick T (2001) Proteins of Mycobacterium bovis BCG induced in the Wayne dormancy model. J Bacteriol 183:2672-2676. doi: 10.1128/JB.183.8.2672-2676.2001
5. Brennan MJ, Delogu G, Chen Y, Bardarov S, Kriakov J, Alavi M, Jacobs WR Jr (2001) Evidence that mycobacterial PE-PGRS proteins are cell surface constituents that influence interactions with other cells. Infect Immun 69:7326-7333. doi: 10.1128/IAI.69.12.7326-7333.2001
6. Campuzano J, Aguilar D, Arriaga K, Leon JC, Salas-Rangel LP, Gonzalez-y-Merchand J, Hernandez-Pando R, Espitia C (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. doi: 10.1016/j.vaccine.2006.12.042
7. Changhong S, Hai Z, Limei W, Jiaze A, Li X, Tingfen Z, Zhikai X, Yong Z (2009) Therapeutic efficacy of a tuberculosis DNA vaccine encoding heat shock protein 65 of Mycobacterium tuberculosis and the human interleukin 2 fusion gene. Tuberculosis (Edinb) 89:54-61. doi: 10.1016/j.tube.2008.09.005
8. Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, Togarsimalemath SK, Chandra N, Mishra S, Ajitkumar P, Joshi B, Katoch VM, Patil SA, Balaji KN (2010) The multifunctional PE-PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J Biol Chem 285:30389-30403. doi: 10.1074/jbc.M110.135251
9. Chaurasiya SK, Srivastava KK (2009) Downregulation of protein kinase C-alpha enhances intracellular survival of Mycobacteria: role of PknG. BMC Microbiol 9:271-285. doi: 10.1186/1471-2180-9-271
10. Choudhary RK, Mukhopadhyay S, Chakhaiyar P, Sharma N, Murthy KJ, Katoch VM, Hasnain SE (2003) PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect Immun 71:6338-6343. doi: 10.1128/IAI.71.11. 6338-6343.2003
11. 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 393:537-544. doi: 10.1038/31159
12. Delogu G, Brennan MJ (2001) Comparative immune response to PE and PE-PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69:5606-5611. doi: 10.1128/IAI.69.9.5606-5611.2001
13. 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. doi: 10.1016/j.micinf.2005.06.021
14. 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 67:2941-2950
15. Dong D, Wang D, Li M, Wang H, Yu J, Wang C, Liu J, Gao Q (2012) PPE38 modulates the innate immune response and is required for Mycobacterium marinum virulence. Infect Immun 80:43-54. doi: 10.1128/IAI.05249-11
16. Dye C, Lonnroth K, Jaramillo E, Williams BG, Raviglione M (2009) Trends in tuberculosis incidence and their determinants in 134 countries. Bull World Health Org 87:683-691. doi: 10.2471/BLT.08.058453
17. Espitia C, Laclette JP, Mondragón-Palomino M, Amador A, Campuzano J, Martens A, Singh M, Cicero R, Zhang Y, Moreno C (1999) The PE-PGRS glycine-rich proteins of Mycobacterium tuberculosis: a new family of fibronectin-binding proteins. Microbiology 145:3487-3495
18. Fisher MA, Plikaytis BB, Shinnick TM (2002) Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. J Bacteriol 184:4025-4032. doi: 10.1128/JB.184.14.4025- 4032.2002
19. Flynn JL (2004) Immunology of tuberculosis and implications in vaccine development. Tuberculosis (Edinb) 84:93-101. doi: 10.1016/j.tube.2003.08.010
20. Flynn JL, Chan J (2001) Immunology of tuberculosis. Annu Rev Immunol 19:93-129. doi: 10.1146/annurev.immunol.19.1.93
21. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, Schreiber R, Mak TW, Bloom BR (1995) Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2:561-572. doi: 10.1016/1074-7613(95)90001-2
22. Gomase VS, Phadnis AC, Ghatak AA (2009) Immunoproteomics approach for prediction of antigenic epitope of Tertiapin from Apis mellifera. Int J Drug Discovery 1:14-17, http://www.bioinfo.in/uploadfiles/13240103061-1-3-IJDD.pdf
23. Hackam DJ, Rotstein OD, Zhang W, Gruenheid S, Gros P, Grinstein S (1998) Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J Exp Med 188:351-364. doi: 10.1084/jem.188.2.351
24. Kaufmann SH, Baumann S, Nasser-Eddine A (2006) Exploiting immunology and molecular genetics for rational vaccine design against tuberculosis. Int J Tuberc Lung Dis 10:1068-1079, http://docstore.ingenta.com/cgi-bin/ds-deliver/1/ u/d/ISIS/70114032
25. 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 15:974-980. doi: 10.1128/CVI.00485-07
26. 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. doi: 10.1016/j.molimm.2008.11.008
27. Kolaskar AS, Tongaonkar PC (1990) A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett 276:172-174. doi: 10.1016/0014-5793(90)80535-Q
28. Ladel CH, Blum C, Dreher A, Reifenberg K, Kopf M, Kaufmann SH (1997) Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect Immun 65:4843-4849
29. Narayana Y, Joshi B, Katoch VM, Mishra KC, Balaji KN (2007) Differential B-cell responses are induced by Mycobacterium tuberculosis PE antigens Rv1169c, Rv0978c, and Rv1818c. Clin Vaccine Immunol 14:1334-1341. doi: 10.1128/CVI.00181-07
30. Pajón R, Yero D, Lage A, Llanes A, Borroto CJ (2006) Computational identification of beta-barrel outer-membrane proteins in Mycobacterium tuberculosis predicted proteomes as putative vaccine candidates. Tuberculosis (Edinb) 86:290-302. doi: 10.1016/j.tube.2006.01.005
31. Pieters J (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3:399-407. doi: 10.1016/j.chom.2008.05. 006
32. 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. doi: 10.1126/science.288.5470.1436
33. 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 26:6053-6063. doi: 10.1016/j.vaccine.2008.09. 025
34. Saunders BM, Frank AA, Orme IM, Cooper AM (2000) Interleukin-6 induces early gamma interferon production in the infected lung but is not required for generation of specific immunity to Mycobacterium tuberculosis infection. Infect Immun 68:3322-3326
35. 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 198:693-704. doi: 10.1084/jem.20030846
36. 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 165:7140-7149
37. Soo PC, Horng YT, Chang KC, Wang JY, Hsueh PR, Chuang CY, Lu CC, Lai HC (2009) A simple gold nanoparticle probes assay for identification of Mycobacterium tuberculosis and Mycobacterium tuberculosis complex from clinical specimens. Mol Cell Probes 23:240-246. doi: 10.1016/j.mcp. 2009.04.006
38. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG (1994) Lack of acidification in mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678-681. doi: 10.1126/science.8303277
39. Sultana R, Tanneeru K, Guruprasad L (2011) The PE-PPE domain in mycobacterium reveals a serine α/β hydrolase fold and function: an in-silico analysis. PLoS One 6:16745. doi: 10.1371/journal.pone.0016745
40. Sweeney KA, Dao DN, Goldberg MF, Hsu T, Venkataswamy MM, Henao-Tamayo M, Ordway D, Sellers RS, Jain P, Chen B, Chen M, Kim J, Lukose R, Chan J, Orme IM, Porcelli SA, Jacobs WR Jr (2011) A recombinant Mycobacterium smegmatis induces potent bactericidal immunity against Mycobacterium tuberculosis. Nat Med 17:1261-1268. doi: 10.1038/nm.2420
41. VanHeyningen TK, Collins HL, Russell DG (1997) IL-6 produced by macrophages infected with Mycobacterium species suppresses T-cell responses. J Immunol 158:330-337, http://www.jimmunol.org/content/158/1/330.full.pdf
42. Vipond J, Vipond R, Allen-Vercoe E, Clark SO, Hatch GJ, Gooch KE, Bacon J, Hampshire T, Shuttleworth H, Minton NP, Blake K, Williams A, Marsh PD (2006) Selection of novel TB vaccine candidates and their evaluation as DNA vaccines against aerosol challenge. Vaccine 24:6340-6350. doi: 10.1016/j.vaccine.2006.05. 025
43. Voskuil MI, Schnappinger D, Rutherford R, Liu Y, Schoolnik GK (2004) Regulation of the Mycobacterium tuberculosis PE/PPE genes. Tuberculosis (Edinb) 84:256-262. doi: 10.1016/j.tube.2003.12.014
44. Wayne LG, Hayes LG (1996) An in vitro model for sequential study of shift down of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64:2062-2069
45. Wei J, Dahl JL, Moulder JW, Roberts EA, O'Gaora P, Young DB, Friedman RL (2000) Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J Bacteriol 182:377-384. doi: 10.1128/JB.182.2.377-384.2000