- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Annual Issues
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
Clinical and Developmental Immunology
Volume 2012 (2012), Article ID 950503, 11 pages
The 19 kDa Mycobacterium tuberculosis Lipoprotein (LpqH) Induces Macrophage Apoptosis through Extrinsic and Intrinsic Pathways: A Role for the Mitochondrial Apoptosis-Inducing Factor
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México,
Circuito Escolar S/N, Ciudad Universitaria, 04510 México, DF, Mexico
Received 17 September 2012; Revised 7 November 2012; Accepted 20 November 2012
Academic Editor: Maciej Cedzynski
Copyright © 2012 Alejandro Sánchez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- J. Keane, H. G. Remold, and H. Kornfeld, “Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages,” Journal of Immunology, vol. 164, no. 4, pp. 2016–2020, 2000.
- A. Spira, J. D. Carroll, G. Liu et al., “Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor,” American Journal of Respiratory Cell and Molecular Biology, vol. 29, no. 5, pp. 545–551, 2003.
- J. Maertzdorf, D. Repsilber, S. K. Parida et al., “Human gene expression profiles of susceptibility and resistance in tuberculosis,” Genes and Immunity, vol. 12, no. 1, pp. 15–22, 2011.
- K. Velmurugan, B. Chen, J. L. Miller et al., “Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells,” PLoS Pathogens, vol. 3, no. 7, article e110, 2007.
- M. Oddo, T. Renno, A. Attinger, T. Bakker, H. R. MacDonald, and P. R. A. Meylan, “Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis,” Journal of Immunology, vol. 160, no. 11, pp. 5448–5454, 1998.
- A. Molloy, P. Laochumroonvorapong, and G. Kaplan, “Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin,” Journal of Experimental Medicine, vol. 180, no. 4, pp. 1499–1509, 1994.
- S. M. Behar, C. J. Martin, M. G. Booty et al., “Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis,” Mucosal Immunology, vol. 4, no. 3, pp. 279–287, 2011.
- F. Winau, G. Hegasy, S. H. E. Kaufmann, and U. E. Schaible, “No life without death—apoptosis as prerequisite for T cell activation,” Apoptosis, vol. 10, no. 4, pp. 707–715, 2005.
- J. Hinchey, S. Lee, B. Y. Jeon et al., “Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis,” Journal of Clinical Investigation, vol. 117, no. 8, pp. 2279–2288, 2007.
- J. Keane, M. K. Balcewicz-Sablinska, H. G. Remold et al., “Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis,” Infection and Immunity, vol. 65, no. 1, pp. 298–304, 1997.
- S. C. Derrick and S. L. Morris, “The ESAT6 protein of Mycobacterium tuberculosis induces apoptosis of macrophages by activating caspase expression,” Cellular Microbiology, vol. 9, no. 6, pp. 1547–1555, 2007.
- M. Chen, H. Gan, and H. G. Remold, “A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis,” Journal of Immunology, vol. 176, no. 6, pp. 3707–3716, 2006.
- L. Duan, H. Gan, D. E. Golan, and H. G. Remold, “Critical role of mitochondrial damage in determining outcome of macrophage infection with Mycobacterium tuberculosis,” Journal of Immunology, vol. 169, no. 9, pp. 5181–5187, 2002.
- H. H. Choi, D. M. Shin, G. Kang et al., “Endoplasmic reticulum stress response is involved in Mycobacterium tuberculosis protein ESAT-6-mediated apoptosis,” FEBS Letters, vol. 584, no. 11, pp. 2445–2454, 2010.
- J. Lee, H. G. Remold, M. H. Ieong, and H. Kornfeld, “Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway,” Journal of Immunology, vol. 176, no. 7, pp. 4267–4274, 2006.
- A. Ciaramella, A. Martino, R. Cicconi, V. Colizzi, and M. Fraziano, “Mycobacterial 19-kDa lipoprotein mediates Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages at early stages of infection,” Cell Death and Differentiation, vol. 7, no. 12, pp. 1270–1272, 2000.
- M. López, L. M. Sly, Y. Luu, D. Young, H. Cooper, and N. E. Reiner, “The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through toll-like receptor-2,” Journal of Immunology, vol. 170, no. 5, pp. 2409–2416, 2003.
- S. Basu, S. K. Pathak, A. Banerjee et al., “Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by toll-like receptor 2-dependent release of tumor necrosis factor-α,” Journal of Biological Chemistry, vol. 282, no. 2, pp. 1039–1050, 2007.
- A. Sanchez, P. Espinosa, M. A. Esparza, M. Colon, G. Bernal, and R. Mancilla, “Mycobacterium tuberculosis 38-kDa lipoprotein is apoptogenic for human monocyte-derived macrophages,” Scandinavian Journal of Immunology, vol. 69, no. 1, pp. 20–28, 2009.
- J. L. Herrmann, P. O'Gaora, A. Gallagher, J. E. R. Thole, and D. B. Young, “Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis,” EMBO Journal, vol. 15, no. 14, pp. 3547–3554, 1996.
- H. Diaz-Silvestre, P. Espinosa-Cueto, A. Sanchez-Gonzalez et al., “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,” Microbial Pathogenesis, vol. 39, no. 3, pp. 97–107, 2005.
- E. H. Noss, R. K. Pai, T. J. Sellati et al., “Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis,” Journal of Immunology, vol. 167, no. 2, pp. 910–918, 2001.
- S. A. Susin, N. Zamzami, M. Castedo et al., “The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis,” Journal of Experimental Medicine, vol. 186, no. 1, pp. 25–37, 1997.
- A. O. Aliprantis, R. B. Yang, D. S. Weiss, P. Godowski, and A. Zychlinsky, “The apoptotic signaling pathway activated by Toll-like receptor-2,” EMBO Journal, vol. 19, no. 13, pp. 3325–3336, 2000.
- R. Haase, C. J. Kirschning, A. Sing et al., “A dominant role of toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages,” Journal of Immunology, vol. 171, no. 8, pp. 4294–4303, 2003.
- N. Kayagaki, A. Kawasaki, T. Ebata et al., “Metalloproteinase-mediated release of human Fas ligand,” Journal of Experimental Medicine, vol. 182, no. 6, pp. 1777–1783, 1995.
- H. Wajant, K. Pfizenmaier, and P. Scheurich, “Tumor necrosis factor signaling,” Cell Death and Differentiation, vol. 10, no. 1, pp. 45–65, 2003.
- M. Fotin-Mleczek, F. Henkler, D. Samel et al., “Apoptotic crosstalk of TNF receptors: TNF-R2-induces depletion of TRAF2 and IAP proteins and accelerates TNF-R1-dependent activation of caspase-8,” Journal of Cell Science, vol. 115, no. 13, pp. 2757–2770, 2002.
- P. Li, D. Nijhawan, I. Budihardjo et al., “Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade,” Cell, vol. 91, no. 4, pp. 479–489, 1997.
- P. X. Petit, H. Lecoeur, E. Zorn, C. Dauguet, B. Mignotte, and M. L. Gougeon, “Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis,” Journal of Cell Biology, vol. 130, no. 1, pp. 157–167, 1995.
- B. Dallaporta, P. Marchetti, M. A. De Pablo et al., “Plasma membrane potential in thymocyte apoptosis,” Journal of Immunology, vol. 162, no. 11, pp. 6534–6542, 1999.
- E. Hangen, K. Blomgren, P. Bénit, G. Kroemer, and N. Modjtahedi, “Life with or without AIF,” Trends in Biochemical Sciences, vol. 35, no. 5, pp. 278–287, 2010.
- S. A. Susin, H. K. Lorenzo, N. Zamzami et al., “Molecular characterization of mitochodrial apoptosis-inducing factor,” Nature, vol. 397, no. 6718, pp. 441–446, 1999.
- P. Schneider, N. Holler, J. L. Bodmer et al., “Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity,” Journal of Experimental Medicine, vol. 187, no. 8, pp. 1205–1213, 1998.
- T. Mustafa, S. Phyu, R. Nilsen, G. Bjune, and R. Jonsson, “Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis?” Inflammation, vol. 23, no. 6, pp. 507–521, 1999.
- A. O. Aliprantis, R. B. Yang, M. R. Mark et al., “Cell activation and apoptosis by bacterial lipoproteins through Toll- like receptor-2,” Science, vol. 285, no. 5428, pp. 736–739, 1999.
- K. M. Heiskanen, M. B. Bhat, H. W. Wang, J. Ma, and A. L. Nieminen, “Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells,” Journal of Biological Chemistry, vol. 274, no. 9, pp. 5654–5658, 1999.
- H. Li, H. Zhu, C. J. Xu, and J. Yuan, “Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis,” Cell, vol. 94, no. 4, pp. 491–501, 1998.
- S. P. Cregan, V. L. Dawson, and R. S. Slack, “Role of AIF in caspase-dependent and caspase-independent cell death,” Oncogene, vol. 23, no. 16, pp. 2785–2796, 2004.
- N. Joza, S. A. Susin, E. Daugas et al., “Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death,” Nature, vol. 410, no. 6828, pp. 549–554, 2001.
- S. W. Yu, H. Wang, M. F. Poitras et al., “Mediation of poty(ADP-ribose) polymerase-1—dependent cell death by apoptosis-inducing factor,” Science, vol. 297, no. 5579, pp. 259–263, 2002.
- H. K. Lorenzo and S. A. Susin, “Therapeutic potential of AIF-mediated caspase-independent programmed cell death,” Drug Resistance Updates, vol. 10, no. 6, pp. 235–255, 2007.
- K. F. Ferri, E. Jacotot, J. Blanco et al., “Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex: role of mitochondria and caspases,” Journal of Experimental Medicine, vol. 192, no. 8, pp. 1081–1092, 2000.
- L. Sarmento, T. Tseggai, V. Dhingra, and Z. F. Fu, “Rabies virus-induced apoptosis involves caspase-dependent and caspase-independent pathways,” Virus Research, vol. 121, no. 2, pp. 144–151, 2006.
- D. J. Favreau, M. Meessen-Pinard, M. Desforges, and P. J. Talbot, “Human coronavirus-induced neuronal programmed cell death is cyclophilin d dependent and potentially caspase dispensable,” Journal of Virology, vol. 86, no. 1, pp. 81–93, 2012.
- H. Ashktorab, R. H. Dashwood, M. M. Dashwood et al., “H. pylori-induced apoptosis in human gastric cancer cells mediated via the release of apoptosis-inducing factor from mitochondria,” Helicobacter, vol. 13, no. 6, pp. 506–517, 2008.
- J. S. Braun, R. Novak, P. J. Murray et al., “Apoptosis-inducing factor mediates microglial and neuronal apoptosis caused by pneumococcus,” Journal of Infectious Diseases, vol. 184, no. 10, pp. 1300–1309, 2001.
- Y. Zhang, G. Zhang, L. R. Hendrix, V. L. Tesh, and J. E. Samuel, “Coxiella burnetii induces apoptosis during early stage infection via a caspase-independent pathway in human monocytic THP-1 cells,” PLoS ONE, vol. 7, no. 1, Article ID e30841, 2012.
- J. Zhang, B. Sun, Y. Huang et al., “IFN- γ promotes THP- 1 cell apoptosis during early infection with Mycobacterium bovis by activating different apoptotic signaling,” FEMS Immunology and Medical Microbiology, vol. 60, no. 3, pp. 191–198, 2010.
- X. Vega-Manriquez, Y. López-Vidal, J. Moran, L. G. Adams, and J. A. Gutiérrez-Pabello, “Apoptosis-inducing factor participation in bovine macrophage Mycobacterium bovis-induced caspase-independent cell death,” Infection and Immunity, vol. 75, no. 3, pp. 1223–1228, 2007.