DOI: 10.1046/j.1365-2958.2002.02813.x. Are the PE‐PGRS proteins of <i>Mycobacterium tuberculosis</i> variable surface antigens?

Are the PE‐PGRS proteins of Mycobacterium tuberculosis variable surface antigens?

10.1046/j.1365-2958.2002.02813.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

Summary Mycobacterium tuberculosis H37Rv contains 67 PE‐PGRS genes, with multiple tandem repetitive sequences, encoding closely related proteins that are exceptionally rich in glycine and alanine. As no functional information was available, 10 of these genes were selected and shown to be expressed in vitro by reverse transcription–polymerase chain reaction (RT–PCR). Antibodies against five PE‐PGRS proteins, raised in mice by DNA vaccination, detected single proteins when the same plasmid constructs used for immunization were expressed in epithelial cells or in reticulocyte extracts, confirming that the PE‐PGRS proteins are antigenic. As expected from the conserved repetitive structure, the antibodies cross‐reacted with more than one PE‐PGRS protein, suggesting that different proteins share common epitopes. PE‐PGRS proteins were detected by West‐ern blotting in five different mycobacterial species (M. tuberculosis, M. bovis BCG, M. smegmatis, M. marinum and M. gordonae) and 11 clinical isolates of M. tuberculosis. Whole‐genome comparisons of M. tuberculosis predicted allelic diversity in the PE‐PGRS family, and this was confirmed by immunoblot studies as size variants were detected in clinical strains. Subcellular fractionation studies and immunoelectron microscopy localized many PE‐PGRS proteins in the cell wall and cell membrane of M. tuberculosis. The data suggest that some PE‐PGRS proteins are variable surface antigens.

Bibliography

Banu, S., HonorÃ©, N., SaintâJoanis, B., Philpott, D., PrÃ©vost, M., & Cole, S. T. (2002). Are the PEâPGRS proteins of Mycobacterium tuberculosis variable surface antigens? Molecular Microbiology, 44(1), 9â19. Portico.

Authors 6

Sayera Banu (first)
Nadine Honoré (additional)
Brigitte Saint‐Joanis (additional)
Dana Philpott (additional)
Marie‐Christine Prévost (additional)
Stewart T. Cole (additional)

References 50 Referenced 236

10.1128/iai.59.8.2712-2718.1991 / Infect Immun / Genetic and immunological analysis of Mycobacterium tuberculosis fibronectin‐binding proteins. by Abou‐Zeid C. (1991)
Bailey T.L. andElkan C.(1994)Fitting a mixture model by expectation maximization to discover motifs in biopolymers.Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology pp.28–36.
10.1093/bioinformatics/14.1.48
10.1099/00221287-146-12-3205
10.1128/IAI.66.5.2221-2229.1998 / Infect Immun / Use of a Mycobacterium tuberculosis H37Rv bacterial artificial chromosome (BAC) library for genome mapping, sequencing and comparative genomics. by Brosch R. (1998)
{'key': 'e_1_2_6_7_1', 'first-page': '19', 'volume-title': 'Molecular Genetics of Mycobacteria.', 'author': 'Brosch R.', 'year': '1800'} / Molecular Genetics of Mycobacteria. by Brosch R. (1800)
10.1128/iai.61.6.2273-2276.1993 / Infect Immun / Bacterial antigenic variation, host immune response, and pathogen–host coevolution. by Brunham R.C. (1993)
10.1099/13500872-145-2-389
10.1016/S0014-5793(99)00536-0
10.1002/0470846526.ch12
10.1038/31159
10.1093/hmg/2.11.1847
10.1128/IAI.69.9.5606-5611.2001
10.1016/0022-1759(94)90308-5
10.1111/j.1365-2958.1993.tb01111.x
10.1099/00221287-145-12-3487
10.1016/S0140-6736(95)92348-9
10.1128/IAI.66.11.5053-5059.1998 / Infect Immun / Antigenic diversity and gene polymorphisms in Haemophilus influenzae. by Gilsdorf J.R. (1998)
10.1016/S0140-6736(94)91338-2
10.1016/S0167-7799(00)01481-5
10.1128/jb.172.2.1005-1013.1990
10.1007/BF00331578
10.1038/nm0896-893
10.1046/j.1365-2958.1999.01549.x
10.1128/iai.60.5.2066-2074.1992 / Infect Immun / Characterization of the major membrane protein of virulent Myco‐bacterium tuberculosis. by Lee B.‐Y. (1992)
10.1038/375685a0
10.1073/pnas.94.23.12616
10.1128/IAI.66.5.1918-1927.1998 / Infect Immun / Comparisons between colony phase variation of Neisseria gonorrhoeae FA1090 and pilus, pilin, and S‐pilin expression. by Long C.D. (1998)
10.1128/IAI.66.10.4788-4796.1998 / Infect Immun / Immunologic and structural relationships of the minor pilus subunits among Haemophilus influenzae isolates. by McCrea K.W. (1998)
10.1146/annurev.mi.44.100190.002315
10.1089/dna.1993.12.777
{'key': 'e_1_2_6_33_1', 'first-page': '72', 'article-title': 'DNA microsatellites: agents of evolution?', 'author': 'Moxon E.R.', 'year': '1999', 'journal-title': 'Sci Am'} / Sci Am / DNA microsatellites: agents of evolution? by Moxon E.R. (1999)
10.1073/pnas.93.7.3132
10.1007/BF00381781
10.1038/44738
10.1126/science.288.5470.1436
10.1016/0168-9525(92)90325-X
10.1002/(sici)1522-2683(20000301)21:5<935::aid-elps935>3.0.co;2-p
10.1128/jcm.30.4.942-946.1992 / J Clin Microbiol / Molecular cloning of a highly repeated DNA element from Mycobacterium tuberculosis and its use as an epidemiological tool. by Ross B.C. (1992)
10.1042/0264-6021:3380753
10.1128/JB.180.14.3541-3547.1998 / J Bacteriol / Expression of a gene for a porin‐like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. by Senaratne R.H. (1998)
{'key': 'e_1_2_6_43_1', 'first-page': '95', 'volume-title': 'Vaccines.', 'author': 'Shiver J.W.', 'year': '1995'} / Vaccines. by Shiver J.W. (1995)
10.1128/IAI.69.6.4185-4191.2001
10.1128/jcm.31.8.1987-1995.1993 / J Clin Microbiol / Comparison of various repetitive DNA elements as genetic markers for strain differentiation and epidemiology of Mycobacterium tuberculosis. by Van Soolingen D. (1993)
10.1073/pnas.94.18.9869
10.1111/j.1365-2958.1987.tb00520.x
10.1054/tuld.1999.0220
10.1073/pnas.76.9.4350
10.1126/science.8456302
10.1128/IAI.66.8.3698-3704.1998 / Infect Immun / Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette‐specific, segmental gene conversion. by Zhang J.‐R. (1998)

Dates

Type	When
Created	22 years, 5 months ago (March 12, 2003, 6:43 a.m.)
Deposited	1 year, 10 months ago (Oct. 17, 2023, 2:50 p.m.)
Indexed	1 week ago (Aug. 29, 2025, 5:47 a.m.)
Issued	23 years, 5 months ago (April 1, 2002)
Published	23 years, 5 months ago (April 1, 2002)
Published Online	23 years, 4 months ago (April 20, 2002)
Published Print	23 years, 5 months ago (April 1, 2002)

Funders 0

None

BibTeX

@article{Banu_2002, title={Are the PE‐PGRS proteins of Mycobacterium tuberculosis variable surface antigens?}, volume={44}, ISSN={1365-2958}, url={http://dx.doi.org/10.1046/j.1365-2958.2002.02813.x}, DOI={10.1046/j.1365-2958.2002.02813.x}, number={1}, journal={Molecular Microbiology}, publisher={Wiley}, author={Banu, Sayera and Honoré, Nadine and Saint‐Joanis, Brigitte and Philpott, Dana and Prévost, Marie‐Christine and Cole, Stewart T.}, year={2002}, month=apr, pages={9–19} }

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      "author": "Brunham R.C.",
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