Mycobacterium tuberculosis adhesins: Potential biomarkers as anti-tuberculosis therapeutic and diagnostic targets

Microbiology (United Kingdom)

Volumn 160, Issue PART 9, 2014, Pages 1821-1831

  Govender, Viveshree S ^a   Ramsugit, Saiyur ^a   Pillay, Manormoney ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BIOLOGICAL MARKER; TUBERCULOSTATIC AGENT; VIRULENCE FACTOR;

BACTERIAL COLONIZATION; BIOFILM; CELL ADHESION; CELL SURFACE; DIAGNOSTIC PROCEDURE; DRUG TARGETING; HOST CELL; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INFECTION CONTROL; MICROORGANISM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; ANTAGONISTS AND INHIBITORS; DIAGNOSTIC TEST; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PROCEDURES;

ADHESINS, BACTERIAL; ANTITUBERCULAR AGENTS; BIOLOGICAL MARKERS; DIAGNOSTIC TESTS, ROUTINE; MYCOBACTERIUM TUBERCULOSIS; VIRULENCE FACTORS;

EID: 84906875855     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/MIC.0.082206-0     Document Type: Review

References (127)

1. Abebe, F., Holm-Hansen, C., Wiker, H. G. & Bjune, G. (2007). Progress in serodiagnosis of Mycobacterium tuberculosis infection. Scand J Immunol 66, 176-191.
2. Algood, H. M., Chan, J. & Flynn, J. L. (2003). Chemokines and tuberculosis. Cytokine Growth Factor Rev 14, 467-477.
3. Almeida Da Silva, P. E. & Palomino, J. C. (2011). Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. J Antimicrob Chemother 66, 1417-1430.
4. Alteri, C. J. (2005). Novel pili of Mycobacterium tuberculosis. PhD thesis, The University of Arizona.
5. Alteri, C. J., Xicohténcatl-Cortes, J., Hess, S., Caballero-Olín, G., Girón, J. A. & Friedman, R. L. (2007). Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci U S A 104, 5145-5150.
6. Armstrong, J. A. & Hart, P. D. (1971). Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134, 713-740.
7. Ashiru, O. T., Pillay, M. & Sturm, A. W. (2010). Adhesion to and invasion of pulmonary epithelial cells by the F15/LAM4/KZN and Beijing strains of Mycobacterium tuberculosis. J Med Microbiol 59, 528-533.
8. Barbosa, M. S., Báo, S. N., Andreotti, P. F., de Faria, F. P., Felipe, M. S., dos Santos Feitosa, L., Mendes-Giannini, M. J. & Soares, C. M. (2006). Glyceraldehyde-3-phosphate dehydrogenase of Paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect Immun 74, 382-389.
9. Barnhart, M. M. & Chapman, M. R. (2006). Curli biogenesis and function. Annu Rev Microbiol 60, 131-147.
10. Bergmann, S., Rohde, M., Chhatwal, G. S. & Hammerschmidt, S. (2001). α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol 40, 1273-1287.
11. Bergsten, G., Wullt, B., Schembri, M. A., Leijonhufvud, I. & Svanborg, C. (2007). Do type 1 fimbriae promote inflammation in the human urinary tract? Cell Microbiol 9, 1766-1781.
12. Bermudez, L. E. & Goodman, J. (1996). Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 64, 1400-1406.
13. Bermudez, L. E., Sangari, F. J., Kolonoski, P., Petrofsky, M. & Goodman, J. (2002). The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells. Infect Immun 70, 140-146.
14. Bodnar, K. A., Serbina, N. V. & Flynn, J. L. (2001). Fate of Mycobacterium tuberculosis within murine dendritic cells. Infect Immun 69, 800-809.
15. Boël, G., Jin, H. & Pancholi, V. (2005). Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect Immun 73, 6237-6248.
16. Bothamley, G. H., Beck, J. S., Potts, R. C., Grange, J. M., Kardjito, T. & Ivanyi, J. (1992a). Specificity of antibodies and tuberculin response after occupational exposure to tuberculosis. J Infect Dis 166, 182-186.
17. Bothamley, G. H., Rudd, R., Festenstein, F. & Ivanyi, J. (1992b). Clinical value of the measurement of Mycobacterium tuberculosis specific antibody in pulmonary tuberculosis. Thorax 47, 270-275.
18. Brennan, M. J., Delogu, G., Chen, Y., Bardarov, S., Kriakov, J., Alavi, M. & Jacobs, W. R., Jr (2001). Evidence that mycobacterial PE_PGRS proteins are cell surface constituents that influence interactions with other cells. Infect Immun 69, 7326-7333.
19. Brzuszkiewicz, E., Brüggemann, H., Liesegang, H., Emmerth, M., Olschläger, T., Nagy, G., Albermann, K., Wagner, C., Buchrieser, C. & other authors (2006). How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A 103, 12879-12884.
20. Castro-Garza, J., King, C. H., Swords, W. E. & Quinn, F. D. (2002). Demonstration of spread by Mycobacterium tuberculosis bacilli in A549 epithelial cell monolayers. FEMS Microbiol Lett 212, 145-149.
21. Cherny, I., Rockah, L., Levy-Nissenbaum, O., Gophna, U., Ron, E. Z. & Gazit, E. (2005). The formation of Escherichia coli curli amyloid fibrils is mediated by prion-like peptide repeats. J Mol Biol 352, 245-252.
22. Chhatwal, G. S. (2002). Anchorless adhesins and invasins of Grampositive bacteria: a new class of virulence factors. Trends Microbiol 10, 205-208.
23. Crandall, E. D. & Kim, K. J. (1991). Alveolar epithelial barrier properties. In The Lung: Scientific Foundations, pp. 273-287. Edited by R. G. Crystal & J. B. West. New York: Raven Press.
24. da Silva Neto, B. R., de Fátima da Silva, J., Mendes-Giannini, M. J., Lenzi, H. L., de Almeida Soares, C. M. & Pereira, M. (2009). The malate synthase of Paracoccidioides brasiliensis is a linked surface protein that behaves as an anchorless adhesin. BMC Microbiol 9, 272.
25. Danelishvili, L., McGarvey, J., Li, Y. J. & Bermudez, L. E. (2003). Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol 5, 649-660.
26. Delogu, G. & Brennan, M. J. (1999). Functional domains present in the mycobacterial hemagglutinin, HBHA. J Bacteriol 181, 7464-7469.
27. Delogu, G. & Brennan, M. J. (2001). Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69, 5606-5611.
28. Dersch, P. & Isberg, R. R. (2000). An immunoglobulin superfamilylike domain unique to the Yersinia pseudotuberculosis invasin protein is required for stimulation of bacterial uptake via integrin receptors. Infect Immun 68, 2930-2938.
29. Diaz-Silvestre, H., Espinosa-Cueto, P., Sanchez-Gonzalez, A., Esparza-Ceron, M. A., Pereira-Suarez, A. L., Bernal-Fernandez, G., Espitia, C. & Mancilla, R. (2005). The 19-kDa antigen of Mycobacterium tuberculosis is a major adhesin that binds the mannose receptor of THP-1 monocytic cells and promotes phagocytosis of mycobacteria. Microb Pathog 39, 97-107.
30. Dobos, K. M., Spotts, E. A., Quinn, F. D. & King, C. H. (2000). Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by cell permeation. Infect Immun 68, 6300-6310.
31. Dubnau, E. & Smith, I. (2003). Mycobacterium tuberculosis gene expression in macrophages. Microbes Infect 5, 629-637.
32. Dumke, R., Hausner, M. & Jacobs, E. (2011). Role of Mycoplasma pneumoniae glyceraldehyde-3-phosphate dehydrogenase (GAPDH) in mediating interactions with the human extracellular matrix. Microbiology 157, 2328-2338.
33. Dunn, M. F., Ramírez-Trujillo, J. A. & Hernández-Lucas, I. (2009). Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology 155, 3166-3175.
34. Esko, J. D. & Sharon, N. (2009). Microbial lectins: hemagglutinins, adhesins, and toxins. In Essentials of Glycobiology, 2nd edn, pp. 489-500. Edited by A. Varki, R. D. Cummings, J. D. Esko, H. H. Freeze, P. Stanley, C. R. Bertozzi, G. W. Hart & M. E. Etzler. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. Espitia, C., Rodríguez, E., Ramón-Luing, L., Echeverría-Valencia, G. & Vallecillo, A. J. (2012). Host-pathogen interactions in tuberculosis. In Understanding Tuberculosis-Analyzing the Origin of Mycobacterium Tuberculosis Pathogenicity, Chapter 3, pp. 43-76. Edited by P. Cardona. Rijeka, Croatia: InTech Open Access Publisher.
36. Esposito, C., Marasco, D., Delogu, G., Pedone, E. & Berisio, R. (2011). Heparin-binding hemagglutinin HBHA from Mycobacterium tuberculosis affects actin polymerisation. Biochem Biophys Res Commun 410, 339-344.
37. Esposito, C., Cantisani, M., D'Auria, G., Falcigno, L., Pedone, E., Galdiero, S. & Berisio, R. (2012). Mapping key interactions in the dimerization process of HBHA from Mycobacterium tuberculosis, insights into bacterial agglutination. FEBS Lett 586, 659-667.
38. Fauci, A. S., Alston, B., Barry, C. E., Augustine, A. D., Fenton, M. J., Handley, F. G., Holland, S. M., Huebner, R. E., Jacobs, G. & NIAID Tuberculosis Working Group (2008). Multidrug-resistant and extensively drug-resistant tuberculosis: the National Institute of Allergy and Infectious Diseases Research agenda and recommendations for priority research. J Infect Dis 197, 1493-1498.
39. Finlay, B. B. & Cossart, P. (1997). Exploitation of mammalian host cell functions by bacterial pathogens. Science 276, 718-725.
40. Finlay, B. B. & Falkow, S. (1997). Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61, 136-169.
41. Foster, T. J., Geoghegan, J. A., Ganesh, V. K. & Höök, M. (2014). Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12, 49-62.
42. Gerlach, R. G. & Hensel, M. (2007). Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297, 401-415.
43. Gillespie, S. H. (2002). Evolution of drug resistance in Mycobacterium tuberculosis: clinical and molecular perspective. Antimicrob Agents Chemother 46, 267-274.
44. Ginsberg, A. M. & Spigelman, M. (2007). Challenges in tuberculosis drug research and development. Nat Med 13, 290-294.
45. Goluszko, P., Goluszko, E., Nowicki, B., Nowicki, S., Popov, V. & Wang, H. Q. (2005). Vaccination with purified Dr fimbriae reduces mortality associated with chronic urinary tract infection due to Escherichia coli bearing Dr adhesin. Infect Immun 73, 627-631.
46. Gonzalez-Juarrero, M. & Orme, I. M. (2001). Characterization of murine lung dendritic cells infected with Mycobacterium tuberculosis. Infect Immun 69, 1127-1133.
47. Greenaway, C., Lienhardt, C., Adegbola, R., Brusasca, P., McAdam, K. & Menzies, D. (2005). Humoral response to Mycobacterium tuberculosis antigens in patients with tuberculosis in the Gambia. Int J Tuberc Lung Dis 9, 1112-1119.
48. Harmsen, A. G., Muggenburg, B. A., Snipes, M. B. & Bice, D. E. (1985). The role of macrophages in particle translocation from lungs to lymph nodes. Science 230, 1277-1280.
49. Henderson, B. & Martin, A. (2011). Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 79, 3476-3491.
50. Henderson, H. J., Dannenberg, A. M., Jr & Lurie, M. B. (1963). Phagocytosis of tubercle bacilli by rabbit pulmonary alveolar macrophages and its relation to native resistance to tuberculosis. J Immunol 91, 553-556.
51. Henderson, B., Lund, P. A. & Coates, A. R. (2010). Multiple moonlighting functions of mycobacterial molecular chaperones. Tuberculosis (Edinb) 90, 119-124.
52. Henderson, B., Nair, S., Pallas, J. & Williams, M. A. (2011). Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35, 147-200.
53. Hendrickson, R. C., Douglass, J. F., Reynolds, L. D., McNeill, P. D., Carter, D., Reed, S. G. & Houghton, R. L. (2000). Mass spectrometric identification of Mtb81, a novel serological marker for tuberculosis. J Clin Microbiol 38, 2354-2361.
54. Hickey, T. B., Thorson, L. M., Speert, D. P., Daffé, M. & Stokes, R. W. (2009). Mycobacterium tuberculosis Cpn60. 2 and DnaK are located on the bacterial surface, where Cpn60. 2 facilitates efficient bacterial association with macrophages. Infect Immun 77, 3389-3401.
55. Hickey, T. B., Ziltener, H. J., Speert, D. P. & Stokes, R. W. (2010). Mycobacterium tuberculosis employs Cpn60. 2 as an adhesin that binds CD43 on the macrophage surface. Cell Microbiol 12, 1634-1647.
56. Hu, Y., Henderson, B., Lund, P. A., Tormay, P., Ahmed, M. T., Gurcha, S. S., Besra, G. S. & Coates, A. R. M. (2008). A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60. 1 is viable but fails to induce an inflammatory response in animal models of infection. Infect Immun 76, 1535-1546.
57. Jackett, P. S., Bothamley, G. H., Batra, H. V., Mistry, A., Young, D. B. & Ivanyi, J. (1988). Specificity of antibodies to immunodominant mycobacterial antigens in pulmonary tuberculosis. J Clin Microbiol 26, 2313-2318.
58. Jassal, M. & Bishai, W. R. (2009). Extensively drug-resistant tuberculosis. Lancet Infect Dis 9, 19-30.
59. Jin, H., Agarwal, S., Agarwal, S. & Pancholi, V. (2011). Surface export of GAPDH/SDH, a glycolytic enzyme, is essential for Streptococcus pyogenes virulence. MBio 2, e00068-11.
60. Joh, D., Wann, E. R., Kreikemeyer, B., Speziale, P. & Höök, M. (1999). Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol 18, 211-223.
61. Kao, D. J., Churchill, M. E., Irvin, R. T. & Hodges, R. S. (2007). Animal protection and structural studies of a consensus sequence vaccine targeting the receptor binding domain of the type IV pilus of Pseudomonas aeruginosa. J Mol Biol 374, 426-442.
62. Kinhikar, A. G., Vargas, D., Li, H., Mahaffey, S. B., Hinds, L., Belisle, J. T. & Laal, S. (2006). Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol Microbiol 60, 999-1013.
63. Klemm, P. & Schembri, M. A. (2000). Bacterial adhesins: function and structure. Int J Med Microbiol 290, 27-35.
64. Kline, K. A., Fälker, S., Dahlberg, S., Normark, S. & Henriques-Normark, B. (2009). Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5, 580-592.
65. Krieger, I. V., Freundlich, J. S., Gawandi, V. B., Roberts, J. P., Gawandi, V. B., Sun, Q., Owen, J. L., Fraile, M. T., Huss, S. I. & other authors (2012). Structure-guided discovery of phenyl-diketo acids as potent inhibitors of M. tuberculosis malate synthase. Chem Biol 19, 1556-1567.
66. Kumar, S., Puniya, B. L., Parween, S., Nahar, P. & Ramachandran, S. (2013). Identification of novel adhesins of M. tuberculosis H37Rv using integrated approach of multiple computational algorithms and experimental analysis. PLoS ONE 8, e69790.
67. Langermann, S., Möllby, R., Burlein, J. E., Palaszynski, S. R., Auguste, C. G., DeFusco, A., Strouse, R., Schenerman, M. A., Hultgren, S. J. & other authors (2000). Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J Infect Dis 181, 774-778.
68. Lebrun, P., Raze, D., Fritzinger, B., Wieruszeski, J. M., Biet, F., Dose, A., Carpentier, M., Schwarzer, D., Allain, F. & other authors (2012). Differential contribution of the repeats to heparin binding of HBHA, a major adhesin of Mycobacterium tuberculosis. PLoS ONE 7, e32421.
69. Lewthwaite, J. C., Clarkin, C. E., Coates, A. R., Poole, S., Lawrence, R. A., Wheeler-Jones, C. P., Pitsillides, A. A., Singh, M. & Henderson, B. (2007). Highly homologous Mycobacterium tuberculosis chaperonin 60 proteins with differential CD14 dependencies stimulate cytokine production by human monocytes through cooperative activation of p38 and ERK1/2 mitogen-activated protein kinases. Int Immunopharmacol 7, 230-240.
70. Lim, J. H., Park, J. K., Jo, E. K., Song, C. H., Min, D., Song, Y. J. & Kim, H. J. (1999). Purification and immunoreactivity of three components from the 30/32-kilodalton antigen 85 complex in Mycobacterium tuberculosis. Infect Immun 67, 6187-6190.
71. Lipscomb, M. F. & Masten, B. J. (2002). Dendritic cells: immune regulators in health and disease. Physiol Rev 82, 97-130.
72. LoBue, P. (2009). Extensively drug-resistant tuberculosis. Curr Opin Infect Dis 22, 167-173.
73. Luetkemeyer, A. F., Getahun, H., Chamie, G., Lienhardt, C. & Havlir, D. V. (2011). Tuberculosis drug development: ensuring people living with HIV are not left behind. Am J Respir Crit Care Med 184, 1107-1113.
74. Mandlik, A., Swierczynski, A., Das, A. & Ton-That, H. (2008). Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16, 33-40.
75. Margarit, I., Rinaudo, C. D., Galeotti, C. L., Maione, D., Ghezzo, C., Buttazzoni, E., Rosini, R., Runci, Y., Mora, M. & other authors (2009). Preventing bacterial infections with pilus-based vaccines: the group B streptococcus paradigm. J Infect Dis 199, 108-115.
76. Masungi, C., Temmerman, S., Van Vooren, J. P., Drowart, A., Pethe, K., Menozzi, F. D., Locht, C. & Mascart, F. (2002). Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J Infect Dis 185, 513-520.
77. Matta, S. K., Agarwal, S. & Bhatnagar, R. (2010). Surface localized and extracellular glyceraldehyde-3-phosphate dehydrogenase of Bacillus anthracis is a plasminogen binding protein. Biochim Biophys Acta 1804, 2111-2120.
78. McDonough, K. A. & Kress, Y. (1995). Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect Immun 63, 4802-4811.
79. Mehta, P. K., King, C. H., White, E. H., Murtagh, J. J., Jr & Quinn, F. D. (1996). Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication. Infect Immun 64, 2673-2679.
80. Menozzi, F. D., Rouse, J. H., Alavi, M., Laude-Sharp, M., Muller, J., Bischoff, R., Brennan, M. J. & Locht, C. (1996). Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 184, 993-1001.
81. Menozzi, F. D., Bischoff, R., Fort, E., Brennan, M. J. & Locht, C. (1998). Molecular characterization of the mycobacterial heparinbinding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci U S A 95, 12625-12630.
82. Menozzi, F. D., Reddy, V. M., Cayet, D., Raze, D., Debrie, A. S., Dehouck, M. P., Cecchelli, R. & Locht, C. (2006). Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect 8, 1-9.
83. Mitchison, D. & Davies, G. (2012). The chemotherapy of tuberculosis: past, present and future. Int J Tuberc Lung Dis 16, 724-732.
84. Monack, D. M. & Hultgren, S. J. (2013). The complex interactions of bacterial pathogens and host defenses. Curr Opin Microbiol 16, 1-3.
85. Naidoo, N., Ramsugit, S. & Pillay, M. (2014). Mycobacterium tuberculosis pili (MTP), a putative biomarker for a tuberculosis diagnostic test. Tuberculosis (Edinb) 94, 338-345.
86. Nandakumar, S., Kannanganat, S., Dobos, K. M., Lucas, M., Spencer, J. S., Fang, S., McDonald, M. A., Pohl, J., Birkness, K. & other authors (2013). O-mannosylation of the Mycobacterium tuberculosis adhesin Apa is crucial for T cell antigenicity during infection but is expendable for protection. PLoS Pathog 9, e1003705.
87. Nguyen, L. & Pieters, J. (2005). The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages. Trends Cell Biol 15, 269-276.
88. Niemann, H. H., Schubert, W. D. & Heinz, D. W. (2004). Adhesins and invasins of pathogenic bacteria: a structural view. Microbes Infect 6, 101-112.
89. Pancholi, V. (2001). Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci 58, 902-920.
90. Pancholi, V. & Chhatwal, G. S. (2003). Housekeeping enzymes as virulence factors for pathogens. Int J Med Microbiol 293, 391-401.
91. Pethe, K., Aumercier, M., Fort, E., Gatot, C., Locht, C. & Menozzi, F. D. (2000). Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin. J Biol Chem 275, 14273-14280.
92. Pethe, K., Alonso, S., Biet, F., Delogu, G., Brennan, M. J., Locht, C. & Menozzi, F. D. (2001). The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412, 190-194.
93. Pethe, K., Bifani, P., Drobecq, H., Sergheraert, C., Debrie, A. S., Locht, C. & Menozzi, F. D. (2002). Mycobacterial heparin-binding hemagglutinin and laminin-binding protein share antigenic methyllysines that confer resistance to proteolysis. Proc Natl Acad Sci U S A 99, 10759-10764.
94. Pinkner, J. S., Remaut, H., Buelens, F., Miller, E., Åberg, V., Pemberton, N., Hedenström, M., Larsson, A., Seed, P. & other authors (2006). Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci U S A 103, 17897-17902.
95. Pizarro-Cerdá, J. & Cossart, P. (2006). Bacterial adhesion and entry into host cells. Cell 124, 715-727.
96. Purves, J., Cockayne, A., Moody, P. C. & Morrissey, J. A. (2010). Comparison of the regulation, metabolic functions, and roles in virulence of the glyceraldehyde-3-phosphate dehydrogenase homologues gapA and gapB in Staphylococcus aureus. Infect Immun 78, 5223-5232.
97. Qamra, R., Srinivas, V. & Mande, S. C. (2004). Mycobacterium tuberculosis GroEL homologues unusually exist as lower oligomers and retain the ability to suppress aggregation of substrate proteins. J Mol Biol 342, 605-617.
98. Ragas, A., Roussel, L., Puzo, G. & Rivière, M. (2007). The Mycobacterium tuberculosis cell-surface glycoprotein Apa as a potential adhesin to colonize target cells via the innate immune system pulmonary C-type lectin surfactant protein A. J Biol Chem 282, 5133-5142.
99. Raja, A., Uma Devi, K. R., Ramalingam, B. & Brennan, P. J. (2002). Immunoglobulin G, A, and M responses in serum and circulating immune complexes elicited by the 16-kilodalton antigen of Mycobacterium tuberculosis. Clin Diagn Lab Immunol 9, 308-312.
100. Raja, A., Uma Devi, K. R., Ramalingam, B. & Brennan, P. J. (2004). Improved diagnosis of pulmonary tuberculosis by detection of free and immune complex-bound anti-30 kDa antibodies. Diagn Microbiol Infect Dis 50, 253-259.
101. Ramsugit, S. & Pillay, M. (in press). Mycobacterium tuberculosis pili promote adhesion to, and invasion of THP-1 macrophages. Jpn J Infect Dis (in press).
102. Ramsugit, S., Guma, S., Pillay, B., Jain, P., Larsen, M. H., Danaviah, S. & Pillay, M. (2013). Pili contribute to biofilm formation in vitro in Mycobacterium tuberculosis. Antonie van Leeuwenhoek 104, 725-735.
103. Ratliff, T. L., McGarr, J. A., Abou-Zeid, C., Rook, G. A., Stanford, J. L., Aslanzadeh, J. & Brown, E. J. (1988). Attachment of mycobacteria to fibronectin-coated surfaces. J Gen Microbiol 134, 1307-1313.
104. Russell, D. G. (2001). TB comes to a sticky beginning. Nat Med 7, 894-895.
105. Russell, D. G., Barry, C. E., III & Flynn, J. L. (2010). Tuberculosis: what we don't know can, and does, hurt us. Science 328, 852-856.
106. Salminen, A., Loimaranta, V., Joosten, J. A., Khan, A. S., Hacker, J., Pieters, R. J. & Finne, J. (2007). Inhibition of P-fimbriated Escherichia coli adhesion by multivalent galabiose derivatives studied by a live-bacteria application of surface plasmon resonance. J Antimicrob Chemother 60, 495-501.
107. Shahar, A., Melamed-Frank, M., Kashi, Y., Shimon, L. & Adir, N. (2011). The dimeric structure of the Cpn60. 2 chaperonin of Mycobacterium tuberculosis at 2. 8 Åreveals possible modes of function. J Mol Biol 412, 192-203.
108. Singh, B., Fleury, C., Jalalvand, F. & Riesbeck, K. (2012a). Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 36, 1122-1180.
109. Singh, V. K., Syring, M., Singh, A., Singhal, K., Dalecki, A. & Johansson, T. (2012b). An insight into the significance of the DnaK heat shock system in Staphylococcus aureus. Int J Med Microbiol 302, 242-252.
110. Smith, I. (2003). Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16, 463-496.
111. Stokes, R. W., Norris-Jones, R., Brooks, D. E., Beveridge, T. J., Doxsee, D. & Thorson, L. M. (2004). The glycan-rich outer layer of the cell wall of Mycobacterium tuberculosis acts as an antiphagocytic capsule limiting the association of the bacterium with macrophages. Infect Immun 72, 5676-5686.
112. Strindelius, L., Folkesson, A., Normark, S. & Sjöholm, I. (2004). Immunogenic properties of the Salmonella atypical fimbriae in BALB/c mice. Vaccine 22, 1448-1456.
113. Strom, M. S. & Lory, S. (1993). Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 47, 565-596.
114. Tailleux, L., Neyrolles, O., Honoré-Bouakline, S., Perret, E., Sanchez, F., Abastado, J. P., Lagrange, P. H., Gluckman, J. C., Rosenzwajg, M. & Herrmann, J. L. (2003). Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J Immunol 170, 1939-1948.
115. Tascon, R. E., Soares, C. S., Ragno, S., Stavropoulos, E., Hirst, E. M. A. & Colston, M. J. (2000). Mycobacterium tuberculosis-activated dendritic cells induce protective immunity in mice. Immunology 99, 473-480.
116. Telford, J. L., Barocchi, M. A., Margarit, I., Rappuoli, R. & Grandi, G. (2006). Pili in gram-positive pathogens. Nat Rev Microbiol 4, 509-519.
117. Temmerman, S., Pethe, K., Parra, M., Alonso, S., Rouanet, C., Pickett, T., Drowart, A., Debrie, A. S., Delogu, G. & other authors (2004). Methylation-dependent T cell immunity to Mycobacterium tuberculosis heparin-binding hemagglutinin. Nat Med 10, 935-941.
118. Tunio, S. A., Oldfield, N. J., Ala'Aldeen, D. A., Wooldridge, K. G. & Turner, D. P. (2010). The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitidis adherence to human cells. BMC Microbiol 10, 280.
119. Uma Devi, K. R., Ramalingam, B. & Raja, A. (2003). Antibody response to Mycobacterium tuberculosis 30 and 16kDa antigens in pulmonary tuberculosis with human immunodeficiency virus coinfection. Diagn Microbiol Infect Dis 46, 205-209.
120. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M. & Peters, P. J. (2007). M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129, 1287-1298.
121. Velayati, A. A., Masjedi, M. R., Farnia, P., Tabarsi, P., Ghanavi, J., Ziazarifi, A. H. & Hoffner, S. E. (2009). Emergence of new forms of totally drug-resistant tuberculosis bacilli: super extensively drugresistant tuberculosis or totally drug-resistant strains in Iran. Chest 136, 420-425.
122. Vikerfors, T., Olcén, P., Wiker, H. & Watson, J. D. (1993). Serological response in leprosy and tuberculosis patients to the 18-kDa antigen of Mycobacterium leprae and antigen 85B of Mycobacterium bovis BCG. Int J Lepr Other Mycobact Dis 61, 571-580.
123. Wallis, R. S., Pai, M., Menzies, D., Doherty, T. M., Walzl, G., Perkins, M. D. & Zumla, A. (2010). Biomarkers and diagnostics for tuberculosis: progress, needs, and translation into practice. Lancet 375, 1920-1937.
124. Wellens, A., Garofalo, C., Nguyen, H., Van Gerven, N., Slättegård, R., Hernalsteens, J. P., Wyns, L., Oscarson, S., De Greve, H. & other authors (2008). Intervening with urinary tract infections using antiadhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS ONE 3, e2040.
125. World Health Organization (2013). Global tuberculosis report 2013. http://apps. who. int/iris/bitstream/10665/91355/1/9789241564656_eng. pdf.
126. Zanetti, S., Bua, A., Delogu, G., Pusceddu, C., Mura, M., Saba, F., Pirina, P., Garzelli, C., Vertuccio, C. & other authors (2005). Patients with pulmonary tuberculosis develop a strong humoral response against methylated heparin-binding hemagglutinin. Clin Diagn Lab Immunol 12, 1135-1138.
127. Zhu, H., Lee, C., Zhang, D., Wu, W., Wang, L., Fang, X., Xu, X., Song, D., Xie, J. & other authors (2013). Surface-associated GroEL facilitates the adhesion of Escherichia coli to macrophages through lectin-like oxidized low-density lipoprotein receptor-1. Microbes Infect 15, 172-180.