Abstract

Transition from latency to active tuberculosis requires Mycobacterium tuberculosis (Mtb) to penetrate the phagosomal membrane and translocate to the cytosol of the host macrophage. Quantitative two-photon fluorescence resonance energy transfer (FRET) microscopy is developed to measure cytosolic translocation using Mycobacterium marinum (Mm) as a model organism for Mtb. Macrophages were infected with Mm or non-pathogenic Mycobacterium smegmatis (Ms) as a control, then loaded with a FRET substrate. Once translocation occurs, mycobacterium-bearing β-lactamase cleaves the substrate, resulting in decrease of FRET signal. Quantification of this FRET signal change revealed that Mm, but not Ms, is capable of translocating to the cytosol.

© 2014 Optical Society of America

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References

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  1. P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
    [PubMed]
  2. N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
    [Crossref] [PubMed]
  3. R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
    [Crossref] [PubMed]
  4. D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
    [Crossref] [PubMed]
  5. C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
    [Crossref] [PubMed]
  6. D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cell. Microbiol. 10(5), 1027–1039 (2008).
    [Crossref] [PubMed]
  7. K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
    [Crossref] [PubMed]
  8. C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
    [PubMed]
  9. G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
    [Crossref] [PubMed]
  10. LiveBLAzer™ FRET — B/G Loading Kit with CCF2-AM and CCF4-AM,” http://www.lifetechnologies.com/order/catalog/product/K1029?CID=AFLBC-425-Discovery-Sciences-K1029 .
  11. W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
    [Crossref] [PubMed]
  12. M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
    [Crossref] [PubMed]
  13. H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
    [Crossref] [PubMed]
  14. C. Li, R. K. Pastila, C. Pitsillides, J. M. Runnels, M. Puoris’haag, D. Côté, and C. P. Lin, “Imaging leukocyte trafficking in vivo with two-photon-excited endogenous tryptophan fluorescence,” Opt. Express 18(2), 988–999 (2010), http://www.opticsinfobase.org/oe/abstract.cfm?uri=oe-18-2-988 .
    [Crossref] [PubMed]
  15. http://www.cellprofiler.org .
  16. N. Otsu, “A threshold selection method from gay-level histograms,” IEEE Trans. Systems, Man, and Cybernetics 9(1), 62–66 (1979).
    [Crossref]
  17. L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
    [Crossref] [PubMed]
  18. G. H. Patterson and D. W. Piston, “Photobleaching in Two-Photon Excitation Microscopy,” Biophys. J. 78(4), 2159–2162 (2000).
    [Crossref] [PubMed]
  19. A. Hopt and E. Neher, “Highly Nonlinear Photodamage in Two-Photon Fluorescence Microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
    [Crossref] [PubMed]
  20. M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
    [Crossref] [PubMed]
  21. K. König, “Cell Damage During Multi-Photon Microscopy”, in Handbook of Biological Confocal Microscopy, 3rd ed., J.B. Pawley, Editor, Springer: New York. 680–689 (2006).
  22. J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
    [Crossref] [PubMed]
  23. G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
    [Crossref] [PubMed]
  24. Z. Xia and Y. Liu, “Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes,” Biophys. J. 81(4), 2395–2402 (2001).
    [Crossref] [PubMed]
  25. C. Berney and G. Danuser, “FRET or no FRET: a quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
    [Crossref] [PubMed]
  26. A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
    [Crossref] [PubMed]

2013 (1)

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

2012 (3)

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

2010 (2)

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

C. Li, R. K. Pastila, C. Pitsillides, J. M. Runnels, M. Puoris’haag, D. Côté, and C. P. Lin, “Imaging leukocyte trafficking in vivo with two-photon-excited endogenous tryptophan fluorescence,” Opt. Express 18(2), 988–999 (2010), http://www.opticsinfobase.org/oe/abstract.cfm?uri=oe-18-2-988 .
[Crossref] [PubMed]

2008 (1)

D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cell. Microbiol. 10(5), 1027–1039 (2008).
[Crossref] [PubMed]

2007 (1)

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

2005 (1)

M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
[Crossref] [PubMed]

2004 (1)

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

2003 (5)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
[Crossref] [PubMed]

C. Berney and G. Danuser, “FRET or no FRET: a quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref] [PubMed]

2001 (2)

A. Hopt and E. Neher, “Highly Nonlinear Photodamage in Two-Photon Fluorescence Microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
[Crossref] [PubMed]

Z. Xia and Y. Liu, “Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes,” Biophys. J. 81(4), 2395–2402 (2001).
[Crossref] [PubMed]

2000 (1)

G. H. Patterson and D. W. Piston, “Photobleaching in Two-Photon Excitation Microscopy,” Biophys. J. 78(4), 2159–2162 (2000).
[Crossref] [PubMed]

1999 (1)

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

1998 (2)

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

1994 (1)

P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
[PubMed]

1979 (1)

N. Otsu, “A threshold selection method from gay-level histograms,” IEEE Trans. Systems, Man, and Cybernetics 9(1), 62–66 (1979).
[Crossref]

Abdallah, A. M.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Baldeón, L.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Barroso, M.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

Barth, E. E.

M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
[Crossref] [PubMed]

Bavister, B. D.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

Berney, C.

C. Berney and G. Danuser, “FRET or no FRET: a quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref] [PubMed]

Berry, G.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Bitter, W.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

Bobard, A.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Bossers-de Vries, R.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Bottai, D.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Brenner, M.

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Brosch, R.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

Brown, E. J.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Burres, N.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Caleechurn, L.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Chen, Y.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

Clair, C.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Cosma, C. L.

C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
[Crossref] [PubMed]

Côté, D.

Danckaert, A.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Danuser, G.

C. Berney and G. Danuser, “FRET or no FRET: a quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref] [PubMed]

Day, R. N.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

de Punder, K.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Demangel, C.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Dolin, P. J.

P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
[PubMed]

Ehsani, S.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Elangovan, M.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

Engel, J. N.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Enninga, J.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Feng, L.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Fluitsma, D.

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Gao, L.-Y.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Gordon, G. W.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Guo, S.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Hava, D.

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Herman, B.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Hopt, A.

A. Hopt and E. Neher, “Highly Nonlinear Photodamage in Two-Photon Fluorescence Microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
[Crossref] [PubMed]

Houben, D.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Kant, A.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Keller, C.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

Knapp, T. E.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Kochi, A.

P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
[PubMed]

Levine, B.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Li, C.

Liang, X. H.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Lin, C. P.

Lippmann, J.

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

Liu, Y.

Z. Xia and Y. Liu, “Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes,” Biophys. J. 81(4), 2395–2402 (2001).
[Crossref] [PubMed]

Majlessi, L.

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

McLaughlin, B.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Mellouk, N.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

Mere, L.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Morisaki, H.

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Negulescu, P. A.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Neher, E.

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

A. Hopt and E. Neher, “Highly Nonlinear Photodamage in Two-Photon Fluorescence Microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
[Crossref] [PubMed]

Nichols, J. A.

M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
[Crossref] [PubMed]

Nichols, M. G.

M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
[Crossref] [PubMed]

Otsu, N.

N. Otsu, “A threshold selection method from gay-level histograms,” IEEE Trans. Systems, Man, and Cybernetics 9(1), 62–66 (1979).
[Crossref]

Pastila, R. K.

Patterson, G. H.

G. H. Patterson and D. W. Piston, “Photobleaching in Two-Photon Excitation Microscopy,” Biophys. J. 78(4), 2159–2162 (2000).
[Crossref] [PubMed]

Paz-Haftel, I.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Perez, J.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Periasamy, A.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

Peters, P. J.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Pierson, J.

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Piston, D. W.

G. H. Patterson and D. W. Piston, “Photobleaching in Two-Photon Excitation Microscopy,” Biophys. J. 78(4), 2159–2162 (2000).
[Crossref] [PubMed]

Pitsillides, C.

Ponimaskin, E. G.

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

Puoris’haag, M.

Ramakrishnan, L.

D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cell. Microbiol. 10(5), 1027–1039 (2008).
[Crossref] [PubMed]

C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
[Crossref] [PubMed]

Raviglione, M. C.

P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
[PubMed]

Ray, K.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Roemer, K.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Runnels, J. M.

Sansonetti, P.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Sherman, D. R.

C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
[Crossref] [PubMed]

Simeone, R.

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

Squirrell, J. M.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

Stanley, M.

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

Tang, C.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Tobin, D. M.

D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cell. Microbiol. 10(5), 1027–1039 (2008).
[Crossref] [PubMed]

Tran, G. V.

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

Tsien, R. Y.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

van der Laan, T.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

van der Wel, N.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

van Ingen, J.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

van Soolingen, D.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

van Zon, M.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Wallrabe, H.

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

White, J. G.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

Whitney, M.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Willemsen, P.

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Woehler, A.

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

Wokosin, D. L.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

Xia, Z.

Z. Xia and Y. Liu, “Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes,” Biophys. J. 81(4), 2395–2402 (2001).
[Crossref] [PubMed]

Zeug, A.

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Zlokarnik, G.

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Annu. Rev. Microbiol. (1)

C. L. Cosma, D. R. Sherman, and L. Ramakrishnan, “The Secret Lives of the Pathogenic Mycobacteria,” Annu. Rev. Microbiol. 57(1), 641–676 (2003).
[Crossref] [PubMed]

Biophys. J. (6)

G. H. Patterson and D. W. Piston, “Photobleaching in Two-Photon Excitation Microscopy,” Biophys. J. 78(4), 2159–2162 (2000).
[Crossref] [PubMed]

A. Hopt and E. Neher, “Highly Nonlinear Photodamage in Two-Photon Fluorescence Microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
[Crossref] [PubMed]

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref] [PubMed]

Z. Xia and Y. Liu, “Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes,” Biophys. J. 81(4), 2395–2402 (2001).
[Crossref] [PubMed]

C. Berney and G. Danuser, “FRET or no FRET: a quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref] [PubMed]

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches-a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref] [PubMed]

Bull. World Health Organ. (1)

P. J. Dolin, M. C. Raviglione, and A. Kochi, “Global tuberculosis incidence and mortality during 1990-2000,” Bull. World Health Organ. 72(2), 213–220 (1994).
[PubMed]

Cell (1)

N. van der Wel, D. Hava, D. Houben, D. Fluitsma, M. van Zon, J. Pierson, M. Brenner, and P. J. Peters, “M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells,” Cell 129(7), 1287–1298 (2007).
[Crossref] [PubMed]

Cell. Microbiol. (3)

D. Houben, C. Demangel, J. van Ingen, J. Perez, L. Baldeón, A. M. Abdallah, L. Caleechurn, D. Bottai, M. van Zon, K. de Punder, T. van der Laan, A. Kant, R. Bossers-de Vries, P. Willemsen, W. Bitter, D. van Soolingen, R. Brosch, N. van der Wel, and P. J. Peters, “ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria,” Cell. Microbiol. 14(8), 1287–1298 (2012).
[Crossref] [PubMed]

D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cell. Microbiol. 10(5), 1027–1039 (2008).
[Crossref] [PubMed]

K. Ray, A. Bobard, A. Danckaert, I. Paz-Haftel, C. Clair, S. Ehsani, C. Tang, P. Sansonetti, G. V. Tran, and J. Enninga, “Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time,” Cell. Microbiol. 12(4), 545–556 (2010).
[Crossref] [PubMed]

IEEE Trans. Systems, Man, and Cybernetics (1)

N. Otsu, “A threshold selection method from gay-level histograms,” IEEE Trans. Systems, Man, and Cybernetics 9(1), 62–66 (1979).
[Crossref]

J. Biomed. Opt. (1)

H. Wallrabe, M. Stanley, A. Periasamy, and M. Barroso, “One- and two-photon fluorescence resonance energy transfer microscopy to establish a clustered distribution of receptor-ligand complexes in endocytic membranes,” J. Biomed. Opt. 8(3), 339–346 (2003).
[Crossref] [PubMed]

J. Vis. Exp. (1)

C. Keller, N. Mellouk, A. Danckaert, R. Simeone, R. Brosch, J. Enninga, and A. Bobard, “Single Cell Measurements of Vacuolar Rupture Caused by Intracellular Pathogens,” J. Vis. Exp. 76(76), e50116 (2013).
[PubMed]

Methods (1)

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref] [PubMed]

Mol. Microbiol. (1)

L.-Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown, “A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion,” Mol. Microbiol. 53(6), 1677–1693 (2004).
[Crossref] [PubMed]

Nat. Biotechnol. (2)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol. 17(8), 763–767 (1999).
[Crossref] [PubMed]

Opt. Express (1)

Photochem. Photobiol. (1)

M. G. Nichols, E. E. Barth, and J. A. Nichols, “Reduction in DNA Synthesis During Two-photon Microscopy of Intrinsic Reduced Nicotinamide Adenine Dinucleotide Fluorescence,” Photochem. Photobiol. 81(2), 259–269 (2005).
[Crossref] [PubMed]

PLoS Pathog. (1)

R. Simeone, A. Bobard, J. Lippmann, W. Bitter, L. Majlessi, R. Brosch, and J. Enninga, “Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death,” PLoS Pathog. 8(2), e1002507 (2012).
[Crossref] [PubMed]

Science (1)

G. Zlokarnik, P. A. Negulescu, T. E. Knapp, L. Mere, N. Burres, L. Feng, M. Whitney, K. Roemer, and R. Y. Tsien, “Quantitation of Transcription and Clonal Selection of Single Living Cells with β-Lactamase as Reporter,” Science 279(5347), 84–88 (1998).
[Crossref] [PubMed]

Other (3)

LiveBLAzer™ FRET — B/G Loading Kit with CCF2-AM and CCF4-AM,” http://www.lifetechnologies.com/order/catalog/product/K1029?CID=AFLBC-425-Discovery-Sciences-K1029 .

K. König, “Cell Damage During Multi-Photon Microscopy”, in Handbook of Biological Confocal Microscopy, 3rd ed., J.B. Pawley, Editor, Springer: New York. 680–689 (2006).

http://www.cellprofiler.org .

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Figures (7)

Fig. 1
Fig. 1 Two-photon FRET microscope setup (a, b, & c: dichroic beam splitters; d, e, & f: band-pass filters).
Fig. 2
Fig. 2 Image processing and cell identification. (a) Original RGB image. (b) Grayscale image from red channel. (c) Grayscale image from green channel. (d) Grayscale image from blue channel. (e) Binary image with identified cells. (f) Cells with demarcated boundaries (g) RGB image with calculated B/G ratio displayed. (bar: 50 μm)
Fig. 3
Fig. 3 Overview of the experimental procedure.
Fig. 4
Fig. 4 Cellular autofluorescence backgrounds are minimal in blue (a) & (d), green (b) & (d), and red (c) & (f) channels from the uninfected or the Mm-infected cells. (g) Histograms of blue/green ratio for the uninfected (red) and Mm-infected cells (blue) at 96 h post-infection. The total counted Mm-infected cells are 9430, and the total counted uninfected cells are 16010. (bar: 20 µm)
Fig. 5
Fig. 5 CCF4 fluorescence background of the macrophages shows that the blue intensity is on the same level of cellular autofluorescence (a), while green intensity is much higher (b), indicating efficient loading of CCF4-AM into cells. (bar: 20 µm)
Fig. 6
Fig. 6 At 96 h post-infection, the cells infected with Mm show higher blue (d) and red (j) intensity than the cells infected with Ms ((e)-(k)), and the cells infected with MmΔc10/e6 ((f)-(l)) respectively. (bar: 20 µm)
Fig. 7
Fig. 7 Quantification of blue vs. green fluorescence intensity from cells infected with Mm, Ms and MmΔc10/e6, respectively. (a) Histograms of blue/green ratio for the Mm- and Ms-infected cells at 48 h post-infection. The histogram of the Mm-infected cells is enlarged by 2 times. Total counted Mm-infected cells are 5141, and total counted Ms-infected cells are 3498. (b) Histograms of blue/green ratio for the Mm- and Ms-infected cells at 96 h post-infection. Total counted Mm-infected cells are 17593, and total counted Ms-infected cells are 6664. (c) Histograms of blue/green ratio for the Mm- and MmΔc10/e6-infected cells at 96 h post-infection. Total counted Mm-infected cells are 17593, and total counted MmΔc10/e6-infected cells are 11294.

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