Experimental selection of long-term intracellular mycobacteria

Cellular Microbiology

Volumn 16, Issue 9, 2014, Pages 1425-1440

  Vázquez, Cristina L ^a   Lerner, Thomas R ^b   Kasmapour, Bahram ^a   Pei, Gang ^a   Gronow, Achim ^a   Bianco, Maria V ^c   Blanco, Federico C ^c   Bleck, Christopher K E ^d   Geffers, Robert ^a   Bigi, Fabiana ^c   Abraham, Wolf Rainer ^a   Gutierrez, Maximiliano G ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c CICVyA   (Argentina)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; PHENOLIC GLYCOLIPID; SUCROSE; GLYCOLIPID;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIUM CULTURE; BIOACCUMULATION; CARBON SOURCE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HOST CELL; INTRACELLULAR BACTERIUM; LIPOGENESIS; MACROPHAGE; MOUSE; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; REINFECTION; STRESS; SURVIVAL; ANIMAL; BAGG ALBINO MOUSE; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MYCOBACTERIOSIS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MUS; MYCOBACTERIUM;

ANIMALS; FEMALE; GLYCOLIPIDS; MACROPHAGES; MICE; MICE, INBRED BALB C; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM INFECTIONS;

EID: 84906791378     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12303     Document Type: Article

References (47)

1. Alvarez, H.M., and Steinbuchel, A. (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60: 367-376.
2. An, F.Q., Folarin, H.M., Compitello, N., Roth, J., Gerson, S.L., McCrae, K.R., etal. (2006) Long-term-infected telomerase-immortalized endothelial cells: a model for Kaposi's sarcoma-associated herpesvirus latency in vitro and in vivo. J Virol 80: 4833-4846.
3. Beaumont, H.J., Gallie, J., Kost, C., Ferguson, G.C., and Rainey, P.B. (2009) Experimental evolution of bet hedging. Nature 462: 90-93.
4. Betts, J.C., Lukey, P.T., Robb, L.C., McAdam, R.A., and Duncan, K. (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43: 717-731.
5. Bianconi, I., Milani, A., Cigana, C., Paroni, M., Levesque, R.C., Bertoni, G., and Bragonzi, A. (2011) Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting airways chronic infection. PLoS Pathog 7: e1001270.
6. Boshoff, H.I., and Barry, C.E., 3rd (2005) Tuberculosis - metabolism and respiration in the absence of growth. Nat Rev Microbiol 3: 70-80.
7. Brown, K.M., Landry, C.R., Hartl, D.L., and Cavalieri, D. (2008) Cascading transcriptional effects of a naturally occurring frameshift mutation in Saccharomyces cerevisiae. Mol Ecol 17: 2985-2997.
8. Casadevall, A. (2008) Evolution of intracellular pathogens. Annu Rev Microbiol 62: 19-33.
9. Chan, K., Knaak, T., Satkamp, L., Humbert, O., Falkow, S., and Ramakrishnan, L. (2002) Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc Natl Acad Sci USA 99: 3920-3925.
10. Cosma, C.L., Humbert, O., and Ramakrishnan, L. (2004) Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol 5: 828-835.
11. Dannenberg, A.M., Jr (2003) Macrophage turnover, division and activation within developing, peak and 'healed' tuberculous lesions produced in rabbits by BCG. Tuberculosis (Edinb) 83: 251-260.
12. Eisenreich, W., Dandekar, T., Heesemann, J., and Goebel, W. (2010) Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8: 401-412.
13. Elena, S.F., and Lenski, R.E. (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469.
14. Ensminger, A.W., Yassin, Y., Miron, A., and Isberg, R.R. (2012) Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Pathog 8: e1002731.
15. Estelmann, S., Hugler, M., Eisenreich, W., Werner, K., Berg, I.A., Ramos-Vera, W.H., etal. (2011) Labeling and enzyme studies of the central carbon metabolism in Metallosphaera sedula. J Bacteriol 193: 1191-1200.
16. Flannagan, R.S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
17. Ford, C.B., Lin, P.L., Chase, M.R., Shah, R.R., Iartchouk, O., Galagan, J., etal. (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43: 482-486.
18. Fritz, C., Maass, S., Kreft, A., and Bange, F.C. (2002) Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infect Immun 70: 286-291.
19. Gotz, A., Eylert, E., Eisenreich, W., and Goebel, W. (2010) Carbon metabolism of enterobacterial human pathogens growing in epithelial colorectal adenocarcinoma (Caco-2) cells. PLoS ONE 5: e10586.
20. Gupta, R.K., Srivastava, B.S., and Srivastava, R. (2010) Comparative expression analysis of rpf-like genes of Mycobacterium tuberculosis H37Rv under different physiological stress and growth conditions. Microbiology 156: 2714-2722.
21. Gutierrez, M.G., Master, S.S., Singh, S.B., Taylor, G.A., Colombo, M.I., and Deretic, V. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
22. Homerova, D., Sevcikova, B., Rezuchova, B., and Kormanec, J. (2012) Regulation of an alternative sigma factor sigmaI by a partner switching mechanism with an anti-sigma factor PrsI and an anti-anti-sigma factor ArsI in Streptomyces coelicolor A3(2). Gene 492: 71-80.
23. Honer Bentrup, K., and Russell, D.G. (2001) Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol 9: 597-605.
24. Hsu, T., Hingley-Wilson, S.M., Chen, B., Chen, M., Dai, A.Z., Morin, P.M., etal. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci 100 (21): 12420-12425.
25. Kasmapour, B., Gronow, A., Bleck, C.K., Hong, W., and Gutierrez, M.G. (2012) Size-dependent mechanism of cargo sorting during lysosome-phagosome fusion is controlled by Rab34. Proc Natl Acad Sci USA 109: 20485-20490.
26. Lawley, T.D., Chan, K., Thompson, L.J., Kim, C.C., Govoni, G.R., and Monack, D.M. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
27. Lee, J.H., Ammerman, N.C., Nolan, S., Geiman, D.E., Lun, S., Guo, H., and Bishai, W.R. (2012) Isoniazid resistance without a loss of fitness in Mycobacterium tuberculosis. Nat Commun 3: 753.
28. Leversen, N.A., Sviland, L., Wiker, H.G., and Mustafa, T. (2012) Long-term persistence of BCG Pasteur in lungs of C57BL/6 mice following intranasal infection. Scand J Immunol 75: 489-499.
29. Martin, C.J., Booty, M.G., Rosebrock, T.R., Nunes-Alves, C., Desjardins, D.M., Keren, I., etal. (2012) Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 12: 289-300.
30. Monack, D.M., Mueller, A., and Falkow, S. (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
31. Moyed, H.S., and Bertrand, K.P. (1983) hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 155: 768-775.
32. Moyed, H.S., and Broderick, S.H. (1986) Molecular cloning and expression of hipA, a gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 166: 399-403.
33. Nguyen, D., and Singh, P.K. (2006) Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci USA 103: 8305-8306.
34. Pang, J.M., Layre, E., Sweet, L., Sherrid, A., Moody, D.B., Ojha, A., and Sherman, D.R. (2012) The polyketide Pks1 contributes to biofilm formation in Mycobacterium tuberculosis. J Bacteriol 194: 715-721.
35. Ramakrishnan, L. (2012) Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12: 352-366.
36. Reed, M.B., Domenech, P., Manca, C., Su, H., Barczak, A.K., Kreiswirth, B.N., etal. (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431: 84-87.
37. Reed, M.B., Gagneux, S., Deriemer, K., Small, P.M., and Barry, C.E., 3rd (2007) The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189: 2583-2589.
38. Rohde, K.H., Veiga, D.F., Caldwell, S., Balazsi, G., and Russell, D.G. (2012) Linking the transcriptional profiles and the physiological states of Mycobacterium tuberculosis during an extended intracellular infection. PLoS Pathog 8: e1002769.
39. Shell, S.S., Prestwich, E.G., Baek, S.H., Shah, R.R., Sassetti, C.M., Dedon, P.C., and Fortune, S.M. (2013) DNA methylation impacts gene expression and ensures hypoxic survival of Mycobacterium tuberculosis. PLoS Pathog 9: e1003419.
40. Sinsimer, D., Huet, G., Manca, C., Tsenova, L., Koo, M.S., Kurepina, N., etal. (2008) The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76: 3027-3036.
41. Stewart, G.R., Robertson, B.D., and Young, D.B. (2003) Tuberculosis: a problem with persistence. Nat Rev Microbiol 1: 97-105.
42. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., etal. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263: 678-681.
43. Tabouret, G., Astarie-Dequeker, C., Demangel, C., Malaga, W., Constant, P., Ray, A., etal. (2010) Mycobacterium leprae phenolglycolipid-1 expressed by engineered M. bovis BCG modulates early interaction with human phagocytes. PLoS Pathog 6: e1001159.
44. Vandal, O.H., Pierini, L.M., Schnappinger, D., Nathan, C.F., and Ehrt, S. (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14: 849-854.
45. Vandal, O.H., Roberts, J.A., Odaira, T., Schnappinger, D., Nathan, C.F., and Ehrt, S. (2009) Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J Bacteriol 191: 625-631.
46. Via, L.E., Fratti, R.A., McFalone, M., Pagan-Ramos, E., Deretic, D., and Deretic, V. (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 (Part 7): 897-905.
47. Wang, L., and Damania, B. (2008) Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res 68: 4640-4648.