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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Exploring the Cell Wall and Secretory Proteins of Mycobacterium leprae as Biomarkers

Author(s): Sakshi Singh, Devesh Sharma, Sakshi Gautam, Mamta Arora and Deepa Bisht*

Volume 31, Issue 1, 2024

Published on: 13 November, 2023

Page: [11 - 24] Pages: 14

DOI: 10.2174/0109298665267993231026114709

Abstract

The bacterial cell wall is composed of a wide variety of intricate proteins in addition to lipids, glycolipids, and polymers. Given the diversity of cell wall proteins among bacterial species, they are a feasible target for biomarker identification and characterization in clinical research and diagnosis of the disease. The slow growth rate of Mycobacterium leprae poses a major hurdle in the accurate diagnosis of leprosy before the onset of peripheral neuropathy. The use of biomarker- based diagnostic methods can help in preventing the spread and manifestation of leprosy. Despite many advances in research methods and techniques, there remains a knowledge gap regarding the cell wall proteomes of M. leprae that can be used as biomarkers. The cell wall and secretory proteins of M. leprae are the major focus of this review article. This article enfolds the characteristics and functions of M. leprae cell wall proteins and gives an insight into those cell wall proteins that are yet to be established as biomarkers. Tools and techniques used in cell wall extraction and biomarker identification can also be explored in this article.

Graphical Abstract

[1]
Lederer, E.; Adam, A.; Ciorbaru, R.; Petit, J.F.; Wietzerbin, J. Cell walls of mycobacteria and related organisms; Chemistry and immunostimulant properties. Mol. Cell. Biochem., 1975, 7(2), 87-104.
[http://dx.doi.org/10.1007/BF01792076] [PMID: 1095912]
[2]
Draper, P. Cell walls of Mycobacterium leprae. Int. J. Lepr. Other Mycobact. Dis., 1976, 44(1-2), 95-98.
[PMID: 776875]
[3]
Kawamoto, I.; Oka, T.; Nara, T. Cell wall composition of Micromonospora olivoasterospora, Micromonospora sagamiensis, and related organisms. J. Bacteriol., 1981, 146(2), 527-534.
[http://dx.doi.org/10.1128/jb.146.2.527-534.1981] [PMID: 7217010]
[4]
Mahapatra, S.; Crick, D.C.; McNeil, M.R.; Brennan, P.J. Unique structural features of the peptidoglycan of Mycobacterium leprae. J. Bacteriol., 2008, 190(2), 655-661.
[http://dx.doi.org/10.1128/JB.00982-07] [PMID: 18024514]
[5]
Crick, D.C.; Mahapatra, S.; Brennan, P.J. Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology, 2001, 11(9), 107R-118R.
[http://dx.doi.org/10.1093/glycob/11.9.107R] [PMID: 11555614]
[6]
Raymond, J.B.; Mahapatra, S.; Crick, D.C.; Pavelka, M.S., Jr Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J. Biol. Chem., 2005, 280(1), 326-333.
[http://dx.doi.org/10.1074/jbc.M411006200] [PMID: 15522883]
[7]
Mahapatra, S.; Scherman, H.; Brennan, P.J.; Crick, D.C. N Glycolylation of the nucleotide precursors of peptidoglycan biosynthesis of Mycobacterium spp. is altered by drug treatment. J. Bacteriol., 2005, 187(7), 2341-2347.
[http://dx.doi.org/10.1128/JB.187.7.2341-2347.2005] [PMID: 15774877]
[8]
McNeil, M.; Daffe, M.; Brennan, P.J. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J. Biol. Chem., 1990, 265(30), 18200-18206.
[http://dx.doi.org/10.1016/S0021-9258(17)44738-7] [PMID: 2211696]
[9]
McNeil, M.; Daffe, M.; Brennan, P.J. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J. Biol. Chem., 1991, 266(20), 13217-13223.
[http://dx.doi.org/10.1016/S0021-9258(18)98826-5] [PMID: 1906464]
[10]
Besra, G.S. P. J. B. The mycobacterial cell envelope: A target for novel drugs against tuberculosis. J. Pharm. Pharmacol., 1997, 49(S1), 25-30.
[11]
Barnes, P.F.; Mehra, V.; Hirschfield, G.R.; Fong, S.J.; Abou-Zeid, C.; Rook, G.A.; Hunter, S.W.; Brennan, P.J.; Modlin, R.L. Characterization of T cell antigens associated with the cell wall protein-peptidoglycan complex of Mycobacterium tuberculosis. J. Immunol., 1989, 143(8), 2656-2662.
[http://dx.doi.org/10.4049/jimmunol.143.8.2656] [PMID: 2507635]
[12]
Harboe, M.; Wiker, H.G.; Nagai, S. Protein antigens of mycobacteria studied by quantitative immunologic techniques. Clin. Infect. Dis., 1992, 14(1), 313-319.
[http://dx.doi.org/10.1093/clinids/14.1.313] [PMID: 1571446]
[13]
Løvik, M.; Closs, O. Induction of immunity against live Mycobacterium lepraemurium: A requirement for viable bacilli? Immunology, 1984, 53(1), 165-173.
[PMID: 6381292]
[14]
Melancon-Kaplan, J.; Hunter, S.W.; McNeil, M.; Stewart, C.; Modlin, R.L.; Rea, T.H.; Convit, J.; Salgame, P.; Mehra, V.; Bloom, B.R. Immunological significance of Mycobacterium leprae cell walls. Proc. Natl. Acad. Sci. USA, 1988, 85(6), 1917-1921.
[http://dx.doi.org/10.1073/pnas.85.6.1917] [PMID: 3279420]
[15]
Nagai, S.; Wiker, H.G.; Harboe, M.; Kinomoto, M. Isolation and partial characterization of major protein antigens in the culture fluid of Mycobacterium tuberculosis. Infect. Immun., 1991, 59(1), 372-382.
[http://dx.doi.org/10.1128/iai.59.1.372-382.1991] [PMID: 1898899]
[16]
Wiker, H.G.; Harboe, M.; Nagai, S.; Bennedsen, J. Quantitative and qualitative studies on the major extracellular antigen of Mycobacterium tuberculosis H37Rv and Mycobacterium bovis BCG. Am. Rev. Respir. Dis., 1990, 141(4_pt_1), 830-838.
[http://dx.doi.org/10.1164/ajrccm/141.4_Pt_1.830] [PMID: 2109556]
[17]
Andersen, P.; Askgaard, D.; Ljungqvist, L.; Bentzon, M.W.; Heron, I. T-cell proliferative response to antigens secreted by Mycobacterium tuberculosis. Infect. Immun., 1991, 59(4), 1558-1563.
[http://dx.doi.org/10.1128/iai.59.4.1558-1563.1991] [PMID: 1900811]
[18]
Mehra, V.; Bloom, B.R..; Torigian, V.K.; Mandich, D.; Reichel, M.; Young, S.M.; Salgame, P.; Convit, J.; Hunter, S.W.; McNeil, M. Characterization of Mycobacterium leprae cell wall-associated proteins with the use of T lymphocyte clones. J Immunol., 1989, 142(8), 2873-8.
[19]
Kirchheimer, W.F.; Storrs, E.E. Attempts to establish the armadillo (Dasypus novemcinctus Linn.) as a model for the study of leprosy. I. Report of lepromatoid leprosy in an experimentally infected armadillo. Int. J. Lepr. Other Mycobact. Dis., 1971, 39(3), 693-702.
[PMID: 4948218]
[20]
Gautam, S.; Sharma, D.; Singh, S.; Deo, N.; Goel, A.; Gupta, V.K. Increscent journey of anti-leprosy drug development. Curr. Sci., 2023, 125(3), 253-267.
[21]
Wallace, E.; Hendrickson, D.; Tolli, N.; Mehaffy, C.; Peña, M.; Nick, J.A. Culturing Mycobacteria. Methods Mol Biol, 2021, 2314, 1-58.
[http://dx.doi.org/10.1007/978-1-0716-1460-0_1]
[22]
Britton, W.J.; Hellqvist, L.; Basten, A.; Raison, R.L. Mycobacterium leprae antigens involved in human immune responses. I. Identification of four antigens by monoclonal antibodies. J. Immunol., 1985, 135(6), 4171-4177.
[http://dx.doi.org/10.4049/jimmunol.135.6.4171] [PMID: 2415603]
[23]
Gillis, T.P.; Buchanan, T.M. Production and partial characterization of monoclonal antibodies to Mycobacterium leprae. Infect. Immun., 1982, 37(1), 172-178.
[http://dx.doi.org/10.1128/iai.37.1.172-178.1982] [PMID: 6179876]
[24]
Kolk, A.H.; Ho, M.L.; Klatser, P.R.; Eggelte, T.A.; Kuijper, S.; de Jonge, S.; van Leeuwen, J. Production and characterization of monoclonal antibodies to Mycobacterium tuberculosis, M. bovis (BCG) and M. leprae. Clin. Exp. Immunol., 1984, 58(3), 511-521.
[PMID: 6439449]
[25]
Young, D.B.; Fohn, M.J.; Khanolkar, S.R.; Buchanan, T.M. Monoclonal antibodies to a 28,000 mol. wt protein antigen of Mycobacterium leprae. Clin. Exp. Immunol., 1985, 60(3), 546-552.
[PMID: 2410167]
[26]
Muñoz-Egea, M.C.; Akir, A.; Esteban, J. Mycobacterium biofilms. Biofilm, 2023, 5, 100107.
[http://dx.doi.org/10.1016/j.bioflm.2023.100107] [PMID: 36798742]
[27]
Snapper, S.B.; Lugosi, L.; Jekkel, A.; Melton, R.E.; Kieser, T.; Bloom, B.R.; Jacobs, W.R., Jr Lysogeny and transformation in mycobacteria: stable expression of foreign genes. Proc. Natl. Acad. Sci. USA, 1988, 85(18), 6987-6991.
[http://dx.doi.org/10.1073/pnas.85.18.6987] [PMID: 2842799]
[28]
Snapper, S.B.; Melton, R.E.; Mustafa, S.; Kieser, T.; Jr, W.R.J. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol., 1990, 4(11), 1911-1919.
[http://dx.doi.org/10.1111/j.1365-2958.1990.tb02040.x] [PMID: 2082148]
[29]
Zhang, Y.; Heym, B.; Allen, B.; Young, D.; Cole, S. The catalase—peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature, 1992, 358(6387), 591-593.
[http://dx.doi.org/10.1038/358591a0] [PMID: 1501713]
[30]
Eiglmeier, K.; Honoré, N.; Woods, S.A.; Caudron, B.; Cole, S.T. Use of an ordered cosmid library to deduce the genomic organization of Mycobacterium leprae. Mol. Microbiol., 1993, 7(2), 197-206.
[http://dx.doi.org/10.1111/j.1365-2958.1993.tb01111.x] [PMID: 8446027]
[31]
Honoré, N.; Bergh, S.; Chanteau, S.; Doucet-Populaire, F.; Eiglmeir, K.; Garnier, T.; Georges, C.; Launois, P.; Limpaiboon, T.; Newton, S.; Niang, K.; Portillo, P.; Ramesh, G.R.; Reddi, P.; Ridel, P.R.; Sittisombut, N.; Wu-Hunte, S.; Cole, S.T. Nucleotide sequence of the first cosmid from the >Mycobacterium leprae genome project: Structure and function of the Rif-Str regions. Mol. Microbiol., 1993, 7(2), 207-214.
[http://dx.doi.org/10.1111/j.1365-2958.1993.tb01112.x] [PMID: 8446028]
[32]
Clark-Curtiss, J.E.; Jacobs, W.R.; Docherty, M.A.; Ritchie, L.R.; Curtiss, R., III Molecular analysis of DNA and construction of genomic libraries of Mycobacterium leprae. J. Bacteriol., 1985, 161(3), 1093-1102.
[http://dx.doi.org/10.1128/jb.161.3.1093-1102.1985] [PMID: 3882664]
[33]
Chiaradia, L.; Lefebvre, C.; Parra, J.; Marcoux, J.; Burlet-Schiltz, O.; Etienne, G.; Tropis, M.; Daffé, M. Dissecting the mycobacterial cell envelope and defining the composition of the native mycomembrane. Sci. Rep., 2017, 7(1), 12807.
[http://dx.doi.org/10.1038/s41598-017-12718-4] [PMID: 28993692]
[34]
Bajaj, A.; Saraswat, S.; Freeke, J.; Barker, A. Method of extraction and proteome profiling of mycobacteria using liquid chromatography-high resolution mass spectrometry. SN Appl. Sci., 2020, 2(11), 1863.
[http://dx.doi.org/10.1007/s42452-020-03691-1]
[35]
Britton, W.J.; Hellqvist, L.; Garsia, R.J.; Basten, A. Dominant cell wall proteins of Mycobacterium leprae recognized by monoclonal antibodies. Clin. Exp. Immunol., 1987, 67(1), 31-42.
[PMID: 3304738]
[36]
Rambukkana, A.; Das, P.K.; Burggraaf, J.D.; Faber, W.R.; Teeling, P.; Krieg, S.; Thole, J.E.; Harboe, M. Identification and characterization of epitopes shared between the mycobacterial 65-kilodalton heat shock protein and the actively secreted antigen 85 complex: their in situ expression on the cell wall surface of Mycobacterium leprae. Infect. Immun., 1992, 60(11), 4517-4527.
[http://dx.doi.org/10.1128/iai.60.11.4517-4527.1992] [PMID: 1383151]
[37]
Rambukkana, A.; Das, P.K.; Burggraaf, J.D.; Yong, S.; Faber, W.R.; Thole, J.E.; Harboe, M. Heterogeneity of monoclonal antibody-reactive epitopes on mycobacterial 30-kilodalton-region proteins and the secreted antigen 85 complex and demonstration of antigen 85B on the Mycobacterium leprae cell wall surface. Infect. Immun., 1992, 60(12), 5172-5181.
[http://dx.doi.org/10.1128/iai.60.12.5172-5181.1992] [PMID: 1280626]
[38]
Hunter, S.W.; Rivoire, B.; Mehra, V.; Bloom, B.R.; Brennan, P.J. The major native proteins of the leprosy bacillus. J. Biol. Chem., 1990, 265(24), 14065-14068.
[http://dx.doi.org/10.1016/S0021-9258(18)77267-0] [PMID: 2201679]
[39]
Pessolani, M.C.V.; Smith, D.R.; Rivoire, B.; McCormick, J.; Hefta, S.A.; Cole, S.T.; Brennan, P.J. Purification, characterization, gene sequence, and significance of a bacterioferritin from Mycobacterium leprae. J. Exp. Med., 1994, 180(1), 319-27.
[40]
Pessolani, M.C.; Brennan, P.J. Molecular definition and identification of new proteins of Mycobacterium leprae. Infect. Immun., 1996, 64(12), 5425-5427.https://journals.asm.org/journal/iai
[http://dx.doi.org/10.1128/iai.64.12.5425-5427.1996] [PMID: 8945601]
[41]
Dhandayuthapani, S.; Banu, M.J.; Kashiwabara, Y. Cloning and sequence determination of the gene coding for the elongation factor Tu of Mycobacterium leprae. J. Biochem., 1994, 115(4), 664-669.https://academic.oup.com/jb/article-abstract/115/4/664/840056
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a124393] [PMID: 8089081]
[42]
Thangaraj, H.S.; Lamb, F.I.; Davis, E.O.; Jenner, P.J.; Jeyakumar, L.H.; Colston, M.J. Identification, sequencing, and expression of Mycobacterium leprae superoxide dismutase, a major antigen. Infect. Immun., 1990, 58(6), 1937-1942.
[http://dx.doi.org/10.1128/iai.58.6.1937-1942.1990] [PMID: 1692812]
[43]
Kim, H.J.; Brennan, P.J.; Heaslip, D.; Udey, M.C.; Modlin, R.L.; Belisle, J.T. Carbohydrate-dependent binding of langerin to SodC, a cell wall glycoprotein of Mycobacterium leprae. J. Bacteriol., 2015, 197(3), 615-625.
[http://dx.doi.org/10.1128/JB.02080-14] [PMID: 25422308]
[44]
Marques, M.A.; Chitale, S.; Brennan, P.J.; Pessolani, M.C. Mapping and identification of the major cell wall-associated components of Mycobacterium leprae. Infect. Immun., 1998, 66(6), 2625-2631.
[http://dx.doi.org/10.1128/IAI.66.6.2625-2631.1998] [PMID: 9596726]
[45]
Closs, O.; Reitan, L.J.; NEGASSl, K.; Harboe, M.; Belehu, A. In vitro stimulation of lymphocytes in leprosy patients, healthy contacts of leprosy patients, and subjects not exposed to leprosy. Comparison of an antigen fraction prepared from Mycobacterium leprae and tuberculin-purified protein derivative. Scand. J. Immunol., 1982, 16(2), 103-115.
[http://dx.doi.org/10.1111/j.1365-3083.1982.tb00704.x] [PMID: 6182610]
[46]
Jindal, S.; Dudani, A.K.; Singh, B.; Harley, C.B.; Gupta, R.S. Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen. Mol. Cell. Biol., 1989, 9(5), 2279-2283.
[PMID: 2568584]
[47]
Shinnick, T.M.; Sweetser, D.; Thole, J.; van Embden, J.; Young, R.A. The etiologic agents of leprosy and tuberculosis share an immunoreactive protein antigen with the vaccine strain Mycobacterium bovis BCG. Infect. Immun., 1987, 55(8), 1932-1935.
[http://dx.doi.org/10.1128/iai.55.8.1932-1935.1987] [PMID: 2440811]
[48]
Shinnick, T.M.; Vodkin, M.H.; Williams, J.C. The Mycobacterium tuberculosis 65-kilodalton antigen is a heat shock protein which corresponds to common antigen and to the Escherichia coli GroEL protein. Infect. Immun., 1988, 56(2), 446-451.
[http://dx.doi.org/10.1128/iai.56.2.446-451.1988] [PMID: 2892795]
[49]
Thole, J.E.; Keulen, W.J.; De Bruyn, J.; Kolk, A.H.; Groothuis, D.G.; Berwald, L.G.; Tiesjema, R.H.; Van Embden, J.D. Characterization, sequence determination, and immunogenicity of a 64-kilodalton protein of Mycobacterium bovis BCG expressed in Escherichia coli K-12. Infect. Immun., 1987, 55(6), 1466-1475.
[http://dx.doi.org/10.1128/iai.55.6.1466-1475.1987] [PMID: 3553003]
[50]
Young, D.; Lathigra, R.; Hendrix, R.; Sweetser, D.; Young, R.A. Stress proteins are immune targets in leprosy and tuberculosis. Proc. Natl. Acad. Sci. USA, 1988, 85(12), 4267-4270.
[http://dx.doi.org/10.1073/pnas.85.12.4267] [PMID: 3132709]
[51]
Cohen, I.R.; Young, D.B. Autoimmunity, microbial immunity and the immunological homunculus. Immunol. Today, 1991, 12(4), 105-110.
[http://dx.doi.org/10.1016/0167-5699(91)90093-9] [PMID: 2059311]
[52]
Hindersson, P.; Petersen, C.S.; Pedersen, N.S.; Høiby, N.; Axelsen, N.H. Immunological cross-reaction between antigen Tp-4 OF Treponema pallidum and an antigen common to a wide range of bacteria. Acta Pathol. Microbiol. Immunol. Scand. [B], 1984, 92B(1-6), 183-188.
[http://dx.doi.org/10.1111/j.1699-0463.1984.tb02818.x] [PMID: 6083697]
[53]
HøIBY, N. Cross-reactions between Pseudomonas aeruginosa and thirty-six other bacterial species. Scand. J. Immunol., 1975, 4, 187-196.
[http://dx.doi.org/10.1111/j.1365-3083.1975.tb03825.x]
[54]
Plikaytis, B.B.; Carlone, G.M.; Pau, C.P.; Wilkinson, H.W. Purified 60-kilodalton Legionella protein antigen with Legionella-specific and nonspecific epitopes. J. Clin. Microbiol., 1987, 25(11), 2080-2084.
[http://dx.doi.org/10.1128/jcm.25.11.2080-2084.1987] [PMID: 2447117]
[55]
Rambukkana, A.; Das, P.K.; Krieg, S.; Faber, W.R. Association of the mycobacterial 30-kDa region proteins with the cutaneous infiltrates of leprosy lesions. Evidence for the involvement of the major mycobacterial secreted proteins in the local immune response of leprosy. Scand. J. Immunol., 1992, 36(1), 35-48.
[http://dx.doi.org/10.1111/j.1365-3083.1992.tb02938.x] [PMID: 1615282]
[56]
Das, P.K.; Rambukkana, A.; Baas, J.G.; Groothuis, D.G.; Halperin, M. Enzyme-linked immunosorbent assay for distinguishing serological responses of lepromatous and tuberculoid leprosies to the 29/33-kilodalton doublet and 64-kilodalton antigens of Mycobacterium tuberculosis. J. Clin. Microbiol., 1990, 28(2), 379-382.
[http://dx.doi.org/10.1128/jcm.28.2.379-382.1990] [PMID: 2107205]
[57]
Espitia, C.; Sciutto, E.; Bottasso, O.; González-Amaro, R.; Hernández-Pando, R.; Mancilla, R. High antibody levels to the mycobacterial fibronectin-binding antigen of 30–31 kD in tuberculosis and lepromatous leprosy. Clin. Exp. Immunol., 2008, 87(3), 362-367.
[http://dx.doi.org/10.1111/j.1365-2249.1992.tb03003.x] [PMID: 1371953]
[58]
Harboe, M.; Wiker, H.G.; Duncan, J.R.; Garcia, M.M.; Dukes, T.W.; Brooks, B.W.; Turcotte, C.; Nagai, S. Protein G-based enzyme-linked immunosorbent assay for anti-MPB70 antibodies in bovine tuberculosis. J. Clin. Microbiol., 1990, 28(5), 913-921.
[http://dx.doi.org/10.1128/jcm.28.5.913-921.1990] [PMID: 2191012]
[59]
Pessolani, M.C.; Rumjanek, F.D.; Marques, M.A.; de Melo, F.S.; Sarno, E.N. Serological response of patients with leprosy to a 28- to 30-kilodalton protein doublet from early cultures of Mycobacterium bovis BCG. J. Clin. Microbiol., 1989, 27(10), 2184-2189.
[http://dx.doi.org/10.1128/jcm.27.10.2184-2189.1989] [PMID: 2685019]
[60]
Rumschlag, H.S.; Shinnick, T.M.; Cohen, M.L. Serological responses of patients with lepromatous and tuberculoid leprosy to 30-, 31-, and 32-kilodalton antigens of Mycobacterium tuberculosis. J. Clin. Microbiol., 1988, 26(10), 2200-2202.
[http://dx.doi.org/10.1128/jcm.26.10.2200-2202.1988] [PMID: 3141462]
[61]
Thole, J.E.R.; Schöningh, R.; Janson, A.A.M.; Garbe, T.; Cornelisse, Y.E.; Clark-Curtiss, J.E.; Kolk, A.H.J.; Ottenhoff, T.H.M.; Vries, R.R.P.; Abou-Zeid, C. Molecular and immunological analysis of a fibronectin-binding protein antigen secreted by Mycobacterium leprae. Mol. Microbiol., 1992, 6(2), 153-163.
[http://dx.doi.org/10.1111/j.1365-2958.1992.tb01996.x] [PMID: 1532043]
[62]
Turneer, M.; Van Vooren, J.P.; De Bruyn, J.; Serruys, E.; Dierckx, P.; Yernault, J.C. Humoral immune response in human tuberculosis: immunoglobulins G, A, and M directed against the purified P32 protein antigen of Mycobacterium bovis bacillus Calmette-Guérin. J. Clin. Microbiol., 1988, 26(9), 1714-1719.
[http://dx.doi.org/10.1128/jcm.26.9.1714-1719.1988] [PMID: 3053775]
[63]
Van Vooren, J.P.; Drowart, A.; De Bruyn, J.; Launois, P.; Millan, J.; Delaporte, E.; Develoux, M.; Yernault, J.C.; Huygen, K. Humoral responses against the 85A and 85B antigens of Mycobacterium bovis BCG in patients with leprosy and tuberculosis. J. Clin. Microbiol., 1992, 30(6), 1608-1610.
[http://dx.doi.org/10.1128/jcm.30.6.1608-1610.1992] [PMID: 1624586]
[64]
Wiker, H.G.; Harboe, M.; Nagai, S.; Patarroyo, M.E.; Ramirez, C.; Cruz, N. MPB59, a widely cross-reacting protein of Mycobacterium bovis BCG. Int. Arch. Allergy Immunol., 1986, 81(4), 307-314.
[http://dx.doi.org/10.1159/000234154] [PMID: 3536756]
[65]
Abou-Zeid, C.; Ratliff, T.L.; Wiker, H.G.; Harboe, M.; Bennedsen, J.; Rook, G.A. Characterization of fibronectin-binding antigens released by Mycobacterium tuberculosis and Mycobacterium bovis BCG. Infect. Immun., 1988, 56(12), 3046-3051.
[http://dx.doi.org/10.1128/iai.56.12.3046-3051.1988] [PMID: 3141278]
[66]
Borremans, M.; de Wit, L.; Volckaert, G.; Ooms, J.; de Bruyn, J.; Huygen, K.; van Vooren, J.P.; Stelandre, M.; Verhofstadt, R.; Content, J. Cloning, sequence determination, and expression of a 32-kilodalton-protein gene of Mycobacterium tuberculosis. Infect. Immun., 1989, 57(10), 3123-3130.
[http://dx.doi.org/10.1128/iai.57.10.3123-3130.1989] [PMID: 2506131]
[67]
Content, J.; de la Cuvellerie, A.; De Wit, L.; Vincent-Levy-Frébault, V.; Ooms, J.; De Bruyn, J. The genes coding for the antigen 85 complexes of Mycobacterium tuberculosis and Mycobacterium bovis BCG are members of a gene family: cloning, sequence determination, and genomic organization of the gene coding for antigen 85-C of M. tuberculosis. Infect. Immun., 1991, 59(9), 3205-3212.
[http://dx.doi.org/10.1128/iai.59.9.3205-3212.1991] [PMID: 1715324]
[68]
Matsuo, K.; Yamaguchi, R.; Yamazaki, A.; Tasaka, H.; Terasaka, K.; Yamada, T. Cloning and expression of the gene for the cross-reactive alpha antigen of Mycobacterium kansasii. Infect. Immun., 1990, 58(2), 550-556.
[http://dx.doi.org/10.1128/iai.58.2.550-556.1990] [PMID: 2404875]
[69]
Matsuo, K.; Yamaguchi, R.; Yamazaki, A.; Tasaka, H.; Yamada, T. Cloning and expression of the Mycobacterium bovis BCG gene for extracellular alpha antigen. J. Bacteriol., 1988, 170(9), 3847-3854.
[http://dx.doi.org/10.1128/jb.170.9.3847-3854.1988] [PMID: 2842287]
[70]
Wiker, H.G.; Sletten, K.; Nagai, S.; Harboe, M. Evidence for three separate genes encoding the proteins of the mycobacterial antigen 85 complex. Infect. Immun., 1990, 58(1), 272-274.
[http://dx.doi.org/10.1128/iai.58.1.272-274.1990] [PMID: 2403534]
[71]
Hunter, S.W.; McNeil, M.; Modlin, R.L.; Mehra, V.; Bloom, B.R.; Brennan, P.J. Isolation and characterization of the highly immunogenic cell wall-associated protein of Mycobacterium leprae. J. Immunol., 1989, 142(8), 2864-2872.
[http://dx.doi.org/10.4049/jimmunol.142.8.2864] [PMID: 2649561]
[72]
Parkash, O. Progress towards development of immunoassays for detection of Mycobacterium leprae infection, employing 35kDa antigen: an update. Lepr. Rev., 2002, 73(1), 9-19.
[http://dx.doi.org/10.47276/lr.73.1.9] [PMID: 11969136]
[73]
Oskam, L.; Slim, E.; Bührer-Sékula, S. Serology: recent developments, strengths, limitations and prospects: a state of the art overview. Lepr. Rev., 2003, 74(3), 196-205.
[PMID: 14577464]
[74]
Mohagheghpour, N.; Munn, M.W.; Gelber, R.H.; Engleman, E.G. Identification of an immunostimulating protein from Mycobacterium leprae. Infect. Immun., 1990, 58(3), 703-710.
[http://dx.doi.org/10.1128/iai.58.3.703-710.1990] [PMID: 2407653]
[75]
Gelber, R.H.; Brennan, P.J.; Hunter, S.W.; Munn, M.W.; Monson, J.M.; Murray, L.P.; Siu, P.; Tsang, M.; Engleman, E.G.; Mohagheghpour, N. Effective vaccination of mice against leprosy bacilli with subunits of Mycobacterium leprae. Infect. Immun., 1990, 58(3), 711-718.
[http://dx.doi.org/10.1128/iai.58.3.711-718.1990] [PMID: 2407654]
[76]
Ivanyi, J.; Sinha, S.; Aston, R.; Cussell, D.; Keen, M.; Sengupta, U. Definition of species specific and cross-reactive antigenic determinants of Mycobacterium leprae using monoclonal antibodies. Clin. Exp. Immunol., 1983, 52(3), 528-536.
[PMID: 6191891]
[77]
Britton, W.J.; Hellqvist, L.; Ivanyi, J.; Basten, A. Immunopurification of radiolabelled antigens of Mycobacterium leprae and Mycobacterium bovis (bacillus Calmette-Guerin) with monoclonal antibodies. Scand. J. Immunol., 1987, 26(2), 149-159.
[http://dx.doi.org/10.1111/j.1365-3083.1987.tb02247.x] [PMID: 3306906]
[78]
Roche, P.W.; Britton, W.J.; Failbus, S.S.; Ludwig, H.; Theuvenet, W.J.; Adiga, R.B. Heterogeneity of serological responses in paucibacillary leprosy-differential responses to protein and carbohydrate antigens and correlation with clinical parameters. Int. J. Lepr. Other Mycobact. Dis., 1990, 58(2), 319-327.
[PMID: 1695912]
[79]
Winter, N.; Triccas, J.A.; Rivoire, B.; Pessolani, M.C.V.; Eiglmeier, K.; Lim, E.M.; Hunter, S.W.; Brennan, P.J.; Britton, W.J. Characterization of the gene encoding the immunodominant 35 kDa protein of Mycobacterium leprae. Mol. Microbiol., 1995, 16(5), 865-876.
[http://dx.doi.org/10.1111/j.1365-2958.1995.tb02314.x] [PMID: 7476185]
[80]
Lee, B.Y.; Hefta, S.A.; Brennan, P.J. Characterization of the major membrane protein of virulent Mycobacterium tuberculosis. Infect. Immun., 1992, 60(5), 2066-2074.
[http://dx.doi.org/10.1128/iai.60.5.2066-2074.1992] [PMID: 1563797]
[81]
Roche, P.W.; Britton, W.J.; Failbus, S.S.; Neupane, K.D.; Theuvenet, W.J. Serological monitoring of the response to chemotherapy in leprosy patients. Int. J. Lepr. Other Mycobact. Dis., 1993, 61(1), 35-43.
[PMID: 8326179]
[82]
Sritharan, M. Iron as a candidate in virulence and pathogenesis in mycobacteria and other microorganisms. World J. Microbiol. Biotechnol., 2000, 16(8/9), 769-780.
[http://dx.doi.org/10.1023/A:1008995313232]
[83]
Grossman, M.J.; Hinton, S.M.; Minak-Bernero, V.; Slaughter, C.; Stiefel, E.I. Unification of the ferritin family of proteins. Proc. Natl. Acad. Sci. USA, 1992, 89(6), 2419-2423.
[http://dx.doi.org/10.1073/pnas.89.6.2419] [PMID: 1549605]
[84]
Andrews, S.C.; Smith, J.M.A.; Yewdall, S.J.; Guest, J.R.; Harrison, P.M. Bacterioferritins and ferritins are distantly related in evolution Conservation of ferroxidase-centre residues. FEBS Lett., 1991, 293(1-2), 164-168.
[http://dx.doi.org/10.1016/0014-5793(91)81177-A] [PMID: 1959654]
[85]
Wilson, T.M.; Collins, D.M. ahpC, a gene involved in isoniazid resistance of the Mycobacterium tuberculosis complex. Mol. Microbiol., 1996, 19(5), 1025-1034.
[http://dx.doi.org/10.1046/j.1365-2958.1996.449980.x] [PMID: 8830260]
[86]
Christman, M.F.; Storz, G.; Ames, B.N. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc. Natl. Acad. Sci. USA, 1989, 86(10), 3484-3488.
[http://dx.doi.org/10.1073/pnas.86.10.3484] [PMID: 2471187]
[87]
Storz, G. Regulation of bacterial gene expression in response to oxidative stress. In: Methods Enzymol; , 1994; pp. 196-207.
[88]
Deretic, V.; Philipp, W.; Dhandayuthapani, S.; Mudd, M.H.; Curcic, R.; Garbe, T.; Heym, B.; Via, L.E.; Cole, S.T. Mycobacterium tuberculosis is a natural mutant with an inactivated oxidative-stress regulatory gene:implications for sensitivity to isoniazid. Mol. Microbiol., 1995, 17(5), 889-900.
[http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_17050889.x] [PMID: 8596438]
[89]
Sherman, D.R.; Sabo, P.J.; Hickey, M.J.; Arain, T.M.; Mahairas, G.G.; Yuan, Y.; Barry, C.E., III; Stover, C.K. Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. Proc. Natl. Acad. Sci. USA, 1995, 92(14), 6625-6629.
[http://dx.doi.org/10.1073/pnas.92.14.6625] [PMID: 7604044]
[90]
Forman, H.J.; Thomas, M.J. Oxidant production and bactericidal activity of phagocytes. Annu. Rev. Physiol., 1986, 48(1), 669-680.
[http://dx.doi.org/10.1146/annurev.ph.48.030186.003321] [PMID: 3010830]
[91]
James, S.L.; Hibbs, J.B., Jr The role of nitrogen oxides as effector molecules of parasite killing. Parasitol. Today, 1990, 6(9), 303-305.
[http://dx.doi.org/10.1016/0169-4758(90)90261-2] [PMID: 15463371]
[92]
Laudenbach, D.E.; Ehrhardt, D.; Green, L.; Grossman, A. Isolation and characterization of a sulfur-regulated gene encoding a periplasmically localized protein with sequence similarity to rhodanese. J. Bacteriol., 1991, 173(9), 2751-2760.
[http://dx.doi.org/10.1128/jb.173.9.2751-2760.1991] [PMID: 1708376]
[93]
Lucas-Lenard, J.; Lipmann, F. Protein Biosynthesis. Annu. Rev. Biochem., 1971, 40(1), 409-448.
[http://dx.doi.org/10.1146/annurev.bi.40.070171.002205] [PMID: 4941237]
[94]
Weijland, A.; Harmark, K.; Cool, R.H.; Anborgh, P.H.; Parmeggiani, A. Elongation factor Tu: a molecular switch in protein biosynthesis. Mol. Microbiol., 1992, 6(6), 683-688.
[http://dx.doi.org/10.1111/j.1365-2958.1992.tb01516.x] [PMID: 1573997]
[95]
Hagge, D.A.; Scollard, D.M.; Ray, N.A.; Marks, V.T.; Deming, A.T.; Spencer, J.S.; Adams, L.B. IL-10 and NOS2 modulate antigen-specific reactivity and nerve infiltration by t cells in experimental leprosy. PLOS Negl Trop Dis., 2014, 8(9)
[http://dx.doi.org/10.1111/j.1365-2958.1992.tb01516.x] [PMID: 1573997]
[96]
Sela, S.; Yogev, D.; Razin, S.; Bercovier, H. Duplication of the tuf gene: a new insight into the phylogeny of eubacteria. J. Bacteriol., 1989, 171(1), 581-584.
[http://dx.doi.org/10.1128/jb.171.1.581-584.1989] [PMID: 2492503]
[97]
Landini, P.; Bandera, M.; Goldstein, B.P.; Ripamonti, F.; Soffientini, A.; Islam, K.; Denaro, M. Inhibition of bacterial protein synthesis by elongation-factor-Tu-binding antibiotics MDL 62,879 and efrotomycin. Biochem. J., 1992, 283(3), 649-652.
[http://dx.doi.org/10.1042/bj2830649] [PMID: 1590753]
[98]
Jacobson, G.R.; Rosenbusch, J.P. Abundance and membrane association of elongation factor Tu in E. coli. Nature, 1976, 261(5555), 23-26.
[http://dx.doi.org/10.1038/261023a0] [PMID: 775340]
[99]
Porcella, S.F.; Belland, R.J.; Judd, R.C. Identification of an EF-Tu protein that is periplasm-associated and processed in Neisseria gonorrhoeae. Microbiology (Reading), 1996, 142(9), 2481-2489.
[http://dx.doi.org/10.1099/00221287-142-9-2481] [PMID: 8828215]
[100]
Ji, B.; Grosset, J.H. Recent advances in the chemotherapy of leprosy. Lepr. Rev., 1990, 61(4), 313-329.
[http://dx.doi.org/10.5935/0305-7518.19900029] [PMID: 2280653]
[101]
Houghten, R.A. General method for the rapid solid-phase synthesis of large numbers of peptides: Specificity of antigen-antibody interaction at the level of individual amino acids. Proc. Natl. Acad. Sci. USA, 1985, 82(15), 5131-5135.
[http://dx.doi.org/10.1073/pnas.82.15.5131] [PMID: 2410914]
[102]
Arshady, R.; Atherton, E.; Clive, D.L.J.; Sheppard, R.C. Peptide synthesis. Part 1. Preparation and use of polar supports based on poly(dimethylacrylamide). J. Chem. Soc., Perkin Trans. 1, 1981, 1, 529-537.
[http://dx.doi.org/10.1039/p19810000529]
[103]
Parker, M.W.; Blake, C.C.F. Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures. FEBS Lett., 1988, 229(2), 377-382.
[http://dx.doi.org/10.1016/0014-5793(88)81160-8] [PMID: 3345848]
[104]
Bannister, J.V.; Bannister, W.H.; Rotilio, G. Aspects of the structure, function, and applications of superoxide dismutase. Crit. Rev. Biochem. Mol. Biol., 1987, 22(2), 111-180.
[105]
Barra, D.; Schinina, M.E.; Simmaco, M.; Bannister, J.V.; Bannister, W.H.; Rotilio, G.; Bossa, F. The primary structure of human liver manganese superoxide dismutase. J. Biol. Chem., 1984, 259(20), 12595-12601.
[http://dx.doi.org/10.1016/S0021-9258(18)90788-X] [PMID: 6386798]
[106]
Muno, D The N-terminal sequences of superoxide dismutases from the 4 mycobacterial species. Biochem. Int., 1981, 2(1), 33-42.
[107]
Khanolkar, S.R., Sr; Mackenzie, C.D.; Lucas, S.B.; Hussen, A.; Girdhar, B.K.; Katoch, K.; McAdam, K.P. Identification of Mycobacterium leprae antigens in tissues of leprosy patients using monoclonal antibodies. Int. J. Lepr. Other Mycobact. Dis., 1989, 57(3), 652-658.
[PMID: 2674303]
[108]
Sieling, P.A.; Hill, P.J.; Dobos, K.M.; Brookman, K.; Kuhlman, A.M.; Fabri, M.; Krutzik, S.R.; Rea, T.H.; Heaslip, D.G.; Belisle, J.T.; Modlin, R.L. Conserved mycobacterial lipoglycoproteins activate TLR2 but also require glycosylation for MHC class II-restricted T cell activation. J. Immunol., 2008, 180(9), 5833-5842.
[http://dx.doi.org/10.4049/jimmunol.180.9.5833] [PMID: 18424702]
[109]
Sartain, M.J.; Belisle, J.T. N-Terminal clustering of the O-glycosylation sites in the Mycobacterium tuberculosis lipoprotein SodC. Glycobiology, 2009, 19(1), 38-51.
[http://dx.doi.org/10.1093/glycob/cwn102] [PMID: 18842962]
[110]
Cole, S.T.; Eiglmeier, K.; Parkhill, J.; James, K.D.; Thomson, N.R.; Wheeler, P.R.; Honoré, N.; Garnier, T.; Churcher, C.; Harris, D.; Mungall, K.; Basham, D.; Brown, D.; Chillingworth, T.; Connor, R.; Davies, R.M.; Devlin, K.; Duthoy, S.; Feltwell, T.; Fraser, A.; Hamlin, N.; Holroyd, S.; Hornsby, T.; Jagels, K.; Lacroix, C.; Maclean, J.; Moule, S.; Murphy, L.; Oliver, K.; Quail, M.A.; Rajandream, M.A.; Rutherford, K.M.; Rutter, S.; Seeger, K.; Simon, S.; Simmonds, M.; Skelton, J.; Squares, R.; Squares, S.; Stevens, K.; Taylor, K.; Whitehead, S.; Woodward, J.R.; Barrell, B.G. Massive gene decay in the leprosy bacillus. Nature, 2001, 409(6823), 1007-1011.
[http://dx.doi.org/10.1038/35059006] [PMID: 11234002]
[111]
Geluk, A.; van Meijgaarden, K.E.; Franken, K.L.M.C.; Subronto, Y.W.; Wieles, B.; Arend, S.M.; Sampaio, E.P.; de Boer, T.; Faber, W.R.; Naafs, B.; Ottenhoff, T.H.M. Identification and characterization of the ESAT-6 homologue of Mycobacterium leprae and T-cell cross-reactivity with Mycobacterium tuberculosis. Infect. Immun., 2002, 70(5), 2544-2548.
[http://dx.doi.org/10.1128/IAI.70.5.2544-2548.2002] [PMID: 11953394]
[112]
Spencer, J.S.; Marques, M.A.M.; Lima, M.C.B.S.; Junqueira-Kipnis, A.P.; Gregory, B.C.; Truman, R.W.; Brennan, P.J. Antigenic specificity of the Mycobacterium leprae homologue of ESAT-6. Infect. Immun., 2002, 70(2), 1010-1013.
[http://dx.doi.org/10.1128/IAI.70.2.1010-1013.2002] [PMID: 11796642]
[113]
Parkash, O.; Pandey, R.; Kumar, A.; Kumar, A. Performance of recombinant ESAT-6 antigen (ML0049) for detection of leprosy patients. Lett. Appl. Microbiol., 2007, 44(5), 524-530.
[http://dx.doi.org/10.1111/j.1472-765X.2006.02099.x] [PMID: 17451520]
[114]
Mehra, V.; Bloom, B.R.; Bajardi, A.C.; Grisso, C.L.; Sieling, P.A.; Alland, D.; Convit, J.; Fan, X.D.; Hunter, S.W.; Brennan, P.J. A major T cell antigen of Mycobacterium leprae is a 10-kD heat-shock cognate protein. J. Exp. Med., 1992, 175(1), 275-284.
[http://dx.doi.org/10.1084/jem.175.1.275] [PMID: 1730920]
[115]
Harboe, M.; Closs, O.; Bjorvatn, B.; Kronvall, G.; Axelsen, N.H. Antibody response in rabbits to immunization with Mycobacterium leprae. Infect. Immun., 1977, 18(3), 792-805.
[http://dx.doi.org/10.1128/iai.18.3.792-805.1977] [PMID: 338491]
[116]
Closs, O.; Harboe, M.; Axelsen, N.H.; Bunch-Christensen, K.; Magnusson, M. The antigens of Mycobacterium bovis, strain BCG, studied by crossed immunoelectrophoresis: a reference system. Scand. J. Immunol., 1980, 12(3), 249-263.
[http://dx.doi.org/10.1111/j.1365-3083.1980.tb00065.x] [PMID: 7008186]
[117]
Reitan, L.J.; Closs, O.; Jantzen, E. Further characterization including preliminary chemical analysis of antigen MLW1 from Mycobacterium leprae. Int. Arch. Allergy Immunol., 1985, 78(3), 269-276.
[http://dx.doi.org/10.1159/000233897] [PMID: 3902662]
[118]
Parkash, O. Serological detection of leprosy employing Mycobacterium leprae derived serine-rich 45 kDa, ESAT-6, CFP-10 and PGL-I: a compilation of data from studies in Indian populations. Lepr. Rev., 2011, 82(4), 383-388.
[http://dx.doi.org/10.47276/lr.82.4.383] [PMID: 22439278]
[119]
Via, L.E.; Curcic, R.; Mudd, M.H.; Dhandayuthapani, S.; Ulmer, R.J.; Deretic, V. Elements of signal transduction in Mycobacterium tuberculosis: in vitro phosphorylation and in vivo expression of the response regulator MtrA. J. Bacteriol., 1996, 178(11), 3314-3321.
[http://dx.doi.org/10.1128/jb.178.11.3314-3321.1996] [PMID: 8655513]
[120]
Shimoji, Y.; Ng, V.; Matsumura, K.; Fischetti, V.A.; Rambukkana, A. A 21-kDa surface protein of Mycobacterium leprae binds peripheral nerve laminin-2 and mediates Schwann cell invasion. Proc. Natl. Acad. Sci. USA, 1999, 96(17), 9857-9862.www.pnas.org
[http://dx.doi.org/10.1073/pnas.96.17.9857] [PMID: 10449784]
[121]
Kaur, G.; Sharma, A.; Narang, T.; Dogra, S.; Kaur, J. Characterization of ML0314c of Mycobacterium leprae and deciphering its role in the immune response in leprosy patients. Gene, 2018, 643, 26-34.
[http://dx.doi.org/10.1016/j.gene.2017.12.001] [PMID: 29208413]
[122]
Bisht, D.; Deo, N.; Sharma, D. Gautam S and, Patil SA. Biochemical Aspects of Leprosy.IAL Textbook of Leprosy (Indian Association of Leprologists); Kar, H.K.; Kumar, B., Eds.; JayPee Publishers & Co: New Delhi, 2023.

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