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Exploring the Contribution of Mycobacteria Characteristics in Their Interaction with Human Macrophages

Published online by Cambridge University Press:  24 June 2013

Carla Silva ,
Joao Perdigao ,
Elsa Alverca ,
António P. Alves de Matos ,
Patricia A. Carvalho ,
Isabel Portugal  and
Luisa Jordao
Carla Silva
Affiliation:
Centro de Patogénese Molecular, URIA, Faculdade de Farmácia da Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003 Lisboa, Portugal
Joao Perdigao
Affiliation:
Centro de Patogénese Molecular, URIA, Faculdade de Farmácia da Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003 Lisboa, Portugal
Elsa Alverca
Affiliation:
Instituto Nacional de Saúde Dr Ricardo Jorge (INSA), Departamento de Saúde Ambiental, Av. Padre Cruz, 1649-016 Lisboa, Portugal
António P. Alves de Matos
Affiliation:
Serviço de Anatomia Patológica, Centro Hospitalar de Lisboa Central, Hospital Curry Cabral, R. da Beneficência 8, 1069-166 Lisboa, Portugal
Patricia A. Carvalho
Affiliation:
ICEMS, Departamento de Bioengenharia, Instituto Superior Técnico, Universidade Técnica de Lisboa, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
Isabel Portugal
Affiliation:
Centro de Patogénese Molecular, URIA, Faculdade de Farmácia da Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003 Lisboa, Portugal
Luisa Jordao*
Affiliation:
INSA, Departamento de Doenças Infeciosas, Av. Padre Cruz, 1649-016 Lisboa, Portugal
*
*Corresponding author. E-mail: maria.jordao@insa.min-saude.pt
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Abstract

Tuberculosis (TB) is a major health problem. The emergence of multidrug resistant (MDR) Mycobacterium tuberculosis (Mtb) isolates confounds treatment strategies. In Portugal, cases of MDR-TB are reported annually with an increased incidence noted in Lisbon. The majority of these MDR-TB cases are due to closely related mycobacteria known collectively as the Lisboa family and Q1 cluster. Genetic determinants linked to drug resistance have been exhaustively studied resulting in the identification of family and cluster specific mutations. Nevertheless, little is known about other factors involved in development of mycobacteria drug resistance. Here, we complement genetic analysis with the study of morphological and structural features of the Lisboa family and Q1 cluster isolates by using scanning and transmission electron microscopy. This analysis allowed the identification of structural differences, such as cell envelope thickness, between Mtb clinical isolates that are correlated with antibiotic resistance. The infection of human monocyte derived macrophages allowed us to document the relative selective advantage of the Lisboa family isolates over other circulating Mtb isolates.

Keywords

Mycobacteriumtuberculosishost–pathogen interactiondrug resistanceTEMSEMMIRUScell envelope
Type
Portuguese Society for Microscopy
Information
Microscopy and Microanalysis , Volume 19 , Issue 5 , October 2013 , pp. 1159 - 1169
Copyright
Copyright © Microscopy Society of America 2013 

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References

Aderem, A. & Underhill, D.M. (1999). Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17, 593–623.Google Scholar
Alsteens, D., Verbelen, C., Dague, E., Raze, D., Baulard, A.R. & Dufrêne, Y.F. (2008). Organization of the mycobacterial cell wall: A nanoscale view. Pflugers Arch–Eur J Physiol 456, 117–125.CrossRefGoogle ScholarPubMed
Anuchin, A.M., Mulyukin, A.L., Suzina, N.E., Duda, V.I., El-Registan, G.I. & Kaprelyants, A.S. (2009). Dormant forms of Mycobacterium smegmatis with distinct morphology. Microbiology 155, 1071–1079.Google Scholar
Barkan, D., Liu, Z., Sacchettini, J.C. & Glickman, M.S. (2009). Mycolic acid cyclopropanation is essential for viability, drug resistance, and cell wall integrity of Mycobacterium tuberculosis . Chem Biol 29, 499–509.Google Scholar
Bozzola, J.J., Johnson, M.C. & Shechmeister, I.L. (1973). In situ multiple sampling of attached bacteria for scanning and transmission electron microscopy. Stain Technol 48, 317–325.Google Scholar
Brennan, P.J. (2003). Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis . Tuberculosis 83, 91–97.Google Scholar
Cade, C., Dlouhy, A.C., Medzihradszky, K.F., Salas-Castillo, S.P. & Ghilado, R.A. (2010). Isoniazid-resistance conferring mutations in Mycobacterium tuberculosis KatG: Catalase, peroxidase, and INH-NADH adduct formation activities. Protein Sci 19, 458–474.CrossRefGoogle ScholarPubMed
Cohen, J. (2013). Approval of novel TB drug celebrated—with restraint. Science 339, 130.Google Scholar
Cole, S. & Riccardi, G. (2011). New tuberculosis drugs on the horizon. Curr Opin Microbiol 14, 570–576.Google Scholar
Cunningham, A.F. & Spreadbury, C.L. (1998). Mycobacterial stationary phase induced by low oxygen tension: Cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J Bacteriol 180, 801–808.Google Scholar
Davies, J. & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74, 417–433.Google Scholar
Demangel, C., Brodin, P., Cockle, P.J., Brosch, R., Majlessi, L., Leclerc, C. & Cole, S.T. (2004). Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-kilodalton culture filtrate protein and ESAT-6. Infect Immun 72, 2170–2176.Google Scholar
Drapper, P. & Daffé, M. (2005). The cell envelope of Mycobacterium tuberculosis with special reference to the capsule and outer permeability barrier. In Tuberculosis and the Tubercle Bacillus, Cole, S.T., Eisenach, K.D., McMurray, D.N. & Jacobs, W.R. Jr. (Eds.), pp. 405–426. New York: ASM Press.Google Scholar
Ehrt, S. & Schnappinger, D. (2007). Mycobacterium tuberculosis virulence: Lipids inside and out. Nat Med 13, 284–285.Google Scholar
Farmer, P. (1997). Social scientists and the new tuberculosis. Soc Sci Med 44, 347–358.Google Scholar
Fenton, M.J., Riley, L.W. & Schlesinger, L.S. (2005). Receptor-mediated recognition of Mycobacterium tuberculosis by host cells. In Tuberculosis and the Tubercle Bacillus, Cole, S.T., Eisenach, K.D., McMurray, D.N. & Jacobs, W.R. Jr. (Eds.), pp. 405–426. New York: ASM Press.Google Scholar
Flores, A.R., Parsons, L.M. & Pavelka, M.S. Jr. (2005). Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology 151, 521–532.Google Scholar
Gagliardi, M.C., Lemassu, A., Teloni, R., Mariotti, S., Sargentini, V., Pardini, M., Daffé, M. & Nisini, R. (2007). Cell wall-associated alpha-glucan is instrumental for Mycobacterium tuberculosis to block CD1 molecule expression and disable the function of dendritic cell derived from infected monocyte. Cell Microbiol 9, 2081–2092.Google Scholar
Gagneux, S., Long, C.D., Small, P.M., Van, T., Schoolnik, G.K. & Bohannan, B.J.M. (2006). The competitive cost of antibiotic resistance in Mycobacterium tuberculosis . Science 312, 1944–1946.CrossRefGoogle ScholarPubMed
Grodzki, A.C., Giulivi, C. & Lein, P.J. (2013). Oxygen tension modulates differentiation and primary macrophage functions in the human monocytic THP-1 cell line. PLoS One 8, e54926 (doi:10.1371/journal.pone.0054926). Google Scholar
Jain, M., Petzold, C.J., Schelle, M.W., Leavell, M.D., Mougous, J.D., Bertozzi, C.R., Leary, J.A. & Cox, J.S. (2007). Lipidomics reveals control of Mycobacterium tuberculosis virulence lipids via metabolic coupling. Proc Natl Acad Sci USA 20, 5133–5138.Google Scholar
Jarlier, V. & Nikaido, H. (1994). Mycobacterial cell wall: Structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 15, 11–18.Google Scholar
Jordao, L., Bleck, C.K., Mayorga, L., Griffiths, G. & Anes, E. (2008). On the killing of mycobacteria by macrophages. Cell Microbiol 10, 529–548.Google Scholar
Jordao, L. & Vieira, O.V. (2011). Tuberculosis: New aspects of an old disease. Int J Cell Biol 2011, 403623. CrossRefGoogle ScholarPubMed
Kapur, V., Li, L.L., Iordanescu, S., Hamrick, M.R., Wanger, A., Kreiswirth, B.N. & Musser, J.M. (1994). Characterization by automated DNA sequencing of mutations in the gene (rpoB) encoding the RNA polymerase beta subunit in rifampin resistant Mycobacterium tuberculosis strains from New York City and Texas. J Clin Microbiol 32, 1095–1098.Google Scholar
Khomenko, A.G. (1987). The variability of Mycobacterium tuberculosis in patients with cavitary pulmonary tuberculosis in the course of chemotherapy. Tubercle 68, 243–253.Google Scholar
Kocagöz, T., Hackbarth, C.J., Ünsal, I., Rosenberg, E.Y., Nikaido, H. & Chambers, H.F. (1996). Gyrase mutations in laboratory-selected, fluoroquinolones-resistant mutations of Mycobacterium tuberculosis H37Ra. Antimicrob Agents Chemother 40, 1768–1774.Google Scholar
Kruuner, A., Jureen, P., Levina, K., Ghebremichael, S. & Hoffner, S. (2003). Discordant resistance to kanamycin and amikacin in drug-resistant Mycobacterium tuberculosis . Antimicrob Agents Chemother 47, 2971–2973.Google Scholar
Kusner, D.J. (2005). Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 114, 239–247.Google Scholar
Larsen, M.H., Vilcheze, C., Kremer, L., Besra, G.S., Parsons, L., Salfinger, M., Heifets, L., Alland, D., Sacchettini, J.C. & Jacobs, W.R. Jr. (2002). Overexpression of inhA, but not kasa, confers resistance to isoniazid and ethionamide in M. smegmatis, M. bovis BCG and M. tuberculosis . Mol Microbiol 46, 453–466.Google Scholar
Maus, C.E., Plikaytis, B.B. & Shinnick, T.M. (2005a). Mutation of tlyA confers capreomycin resistance in Mycobacterium tuberculosis . Antimicrob Agents Chemother 49, 571–577.Google Scholar
Maus, C.E., Plikaytis, B.B. & Shinnick, T.M. (2005b). Molecular analysis of cross-resistance to capreomycin, kanamycin, amikacin, and viomycin in Mycobacterium tuberculosis . Antimicrob Agents Chemother 49, 3192–3197.Google Scholar
Meier, A., Sander, P., Schaper, K.J., Scholz, M. & Bottger, E.C. (1996). Correlation of molecular resistance mechanisms and phenotypic resistance levels in streptomycin-resistant Mycobacterium tuberculosis . Antimicrob Agents Chemother 40, 2452–2454.Google Scholar
Mendez-Samperio, P., Ayala, H., Trejo, A. & Ramirez, F.A. (2004). Differential induction of TNF-alpha and NOS2 by mitogen-activated protein kinase signaling pathways during Mycobacterium bovis infection. J Infect 48, 66–73.Google Scholar
Perdigão, J., Macedo, R., Joao, I., Fernandes, E., Brum, L. & Portugal, I. (2008). Multidrug-resistant tuberculosis in Lisbon, Portugal: A molecular epidemiological perspective. Microbiol Drug Resist 14, 133–143.CrossRefGoogle Scholar
Perdigão, J., Macedo, R., Malaquias, A., Ferreira, A., Brum, L. & Portugal, I. (2010). Genetic analysis of extensively drug-resistant Mycobacterium tuberculosis strains in Lisbon, Portugal. J Antimicrob Chemother 65, 224–227.Google Scholar
Perdigão, J., Macedo, R., Silva, C., Machado, D., Couto, I., Viveiros, M., Jordao, L. & Portugal, I. (2013). From multidrug-resistant to extensively drug-resistant tuberculosis in Lisbon, Portugal: The stepwise mode of resistance acquisition. J Antimicrob Chemother 68, 27–33.Google Scholar
Plinke, C., Rusch-Gerdes, S. & Niemann, S. (2006). Significance of mutations in embb codon 306 for prediction of ethambutol resistance in clinical Mycobacterium tuberculosis isolates. Antimicrob Agents Chemother 50, 1900–1902.Google Scholar
Portugal, I., Covas, M.J., Brum, L., Viveiros, M., Ferrinho, P., Moniz-Pereira, J. & David, H. (1999). Outbreak of multiple drug-resistant tuberculosis in Lisbon: Detection by restriction fragment length polymorphism analysis. Int J Tuberc Lung Dis 3, 207–213.Google Scholar
Ramaswamy, S. & Musser, J.M. (1998). Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. Tuber Lung Dis 79, 3–29.Google Scholar
Rossetti, M.L., Valim, A.R., Silva, M.S. & Rodrigues, V.S. (2002). Resistant tuberculosis: A molecular review. Rev Saude Publica 36, 525–532.Google Scholar
Russell, D.G. (2001). Mycobacterium tuberculosis: Here today, and here tomorrow. Nat Rev Mol Cell Biol 2, 569–577.Google Scholar
Schlesinger, L.S. (1997). The role of mononuclear phagocytes in tuberculosis. In Lung Macrophages and Dendritic Cells in Health and Disease, Lipscomb, M.F. & Russell, S.W. (Eds.), pp. 437–480. New York: Dekker.Google Scholar
Sreevatsan, S., Pan, X., Stockbauer, K.E., Williams, D.L., Kreiswirth, B.N. & Musser, J.M. (1996). Characterization of rpsl and rrs mutations in streptomycin-resistant Mycobacterium tuberculosis isolates from diverse geographic localities. Antimicrob Agents Chemother 40, 1024–1026.Google Scholar
Sreevatsan, S., Pan, X., Zhang, Y., Kreiswirth, B.N. & Musser, J.M. (1997). Mutations associated with pyrazinamide resistance in pncA of Mycobacterium tuberculosis complex organisms. Antimicrob Agents Chemother 41, 636–640.Google Scholar
Supply, P., Allix, C., Lesjean, S., Cardoso-Oelemann, M., Rüsch-Gerdes, S., Willery, E., Savine, E., Haas, P., van Deutekom, H., Roring, S., Bifani, P., Kurepina, N., Kreiswirth, B., Sola, C., Rastogi, N., Vatin, V., Gutierrez, M.C., Fauville, M., Niemann, S., Skuce, R., Kremer, K., Locht, C. & van Soolingen, D. (2006). Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis . J Clin Microbiol 44, 4498–4510.Google Scholar
Swanson, J.A. (2008). Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9, 639–649.Google Scholar
Torrelles, J.B., Sieling, P.A., Zhang, N., Keen, M.A., McNeil, M.R., Belisle, J.T., Modlin, R.L., Brennan, P.J. & Chatterjee, D. (2012). Isolation of a distinct Mycobacterium tuberculosis mannose-capped lipoarabinomannan isoform responsible for recognition by CD1b-restricted T cells. Glycobiology 22, 1118–1127 Google Scholar
Velayati, A.A., Farnia, P., Ibrahim, T.A., Haroun, R.Z., Kuan, H.O., Ghanavi, J., Farnia, P., Kabarei, A.N., Tabarsi, P., Omar, A.R., Varahram, M. & Masjedi, M.R. (2009). Differences in cell wall thickness between resistant and non-resistant strains of Mycobacterium tuberculosis: Using transmission electron microscopy. Chemotherapy 55, 303–307.Google Scholar
Velayati, A.A., Farnia, P., Merza, M.A., Zhavnerko, G.K., Tabarsi, P., Titov, L.P., Ghanavei, J., Farnia, P., Setare, M., Poleschuyk, N.N., Owlia, P., Sheikolslami, M., Ranjbar, R. & Masjedi, M.R. (2010). New insight into extremely drug-resistant tuberculosis: Using atomic force microscopy. Eur Respir J 36, 1490–1493.Google Scholar
Via, L.E., Lin, P.L., Ray, S.M., Carrillo, J., Allen, S.S., Eum, S.Y., Taylor, K., Klein, E., Manjunatha, U., Gonzales, J., Lee, E.G., Park, S.K., Raleigh, J.A., Cho, S.N., McMurray, D.N., Flynn, J.L. & Barry, C.E. 3rd (2008). Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76, 2333–2340.Google Scholar
Vizcaíno, C., Restrepo-Montoya, D., Rodríguez, D., Niño, L.F., Ocampo, M., Vanegas, M., Reguero, M.T., Martínez, N.L., Patarroyo, M.E. & Patarroyo, M.A. (2010). Computational prediction and experimental assessment of secreted/surface proteins from Mycobacterium tuberculosis H37Rv. PLoS Comput Biol 6, e1000824. Google Scholar
Wayne, L.G. & Sohaskey, C.D. (2001). Nonreplicating persistence of Mycobacterium tuberculosis . Annu Rev Microbiol 55, 139–163.Google Scholar
Weniger, T., Krawczyk, J., Supply, P., Niemann, S. & Harmsen, D. (2010). MIRU-VNTRplus: A web tool for polyphasic genotyping of Mycobacterium tuberculosis complex bacteria. Nucl Acid Res 38, 326–331.Google Scholar
World Health Organization (WHO) (2011). 2011/2012 tuberculosis global facts. http://www.who.int/tb/publications/2011/factsheet_tb_2011.pdf (accessed February 1, 2013).Google Scholar
World Health Organization (WHO) (2012). Global tuberculosis report 2012. http://apps.who.int/iris/bitstream/10665/75938/1/9789241564502_eng.pdf (accessed February 1, 2013).Google Scholar
Zaunbrecher, M.A., Sikes, R.D., Metchock, B., Shinnick, T.M. & Posey, J.E. (2009). Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 106, 20004–20009.Google Scholar