Interaction of mycobacteria with Plasmin(ogen) affects phagocytosis and granuloma development

World Health Organization, 2017, 2017 Kukkonen, 1998, Identification of two laminin-binding fimbriae, the type 1 fimbria of Salmonella enterica serovar typhimurium and the G fimbria of Escherichia coli, as plasminogen receptors, Infect Immun, 66, 4965, 10.1128/IAI.66.10.4965-4970.1998 Bergmann, 2001, α Enolase of Streptococcus pneumoniae is a plasmin(ogen) binding protein displayed on the bacterial cell surface, Mol Microbiol, 40, 1273, 10.1046/j.1365-2958.2001.02448.x Coleman, 1995, Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers, Infect Immun, 63, 2478, 10.1128/IAI.63.7.2478-2484.1995 Vieira, 2012, Plasminogen binding proteins and plasmin generation on the surface of Leptospira spp.: the contribution to the bacteria-host interactions, J Biomed Biotechnol, 758513 Pancholi, 1998, α-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci, J Biol Chem, 273, 14503, 10.1074/jbc.273.23.14503 Fuchs, 1994, The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor, Proc Natl Acad Sci USA, 91, 12594, 10.1073/pnas.91.26.12594 Klempner, 1995, Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi, J Infect Dis, 171, 1258, 10.1093/infdis/171.5.1258 Hu, 1995, Binding of human plasminogen to Borrelia burgdorferi, Infect Immun, 63, 3491, 10.1128/IAI.63.9.3491-3496.1995 Stie, 2012, Blood–brain barrier invasion by Cryptococcus neoformans is enhanced by functional interactions with plasmin, Microbiology, 158, 240, 10.1099/mic.0.051524-0 Attali, 2008, The interaction of Streptococcus pneumoniae with plasmin mediates transmigration across endothelial and epithelial monolayers by intercellular junction cleavage, Infect Immun, 76, 5350, 10.1128/IAI.00184-08 Singh, 2015, Moraxella catarrhalis binds plasminogen to evade host innate immunity, Infect Immun, 83, 3458, 10.1128/IAI.00310-15 Chung, 2011, Bacillus anthracis interacts with plasmin(ogen) to Evade C3b-dependent innate immunity, PLoS One, 6, 10.1371/journal.pone.0018119 Monroy, 2000, Binding and activation of human plasminogen by Mycobacterium tuberculosis, Infect Immun, 68, 4327, 10.1128/IAI.68.7.4327-4330.2000 Xolalpa, 2007, Identification of novel bacterial plasminogen binding proteins in the human pathogen Mycobacterium tuberculosis, Proteomics, 7, 3332, 10.1002/pmic.200600876 Gordon, 1978, Bacille Calmette-Guerin infection in the mouse. Regulation of macrophage plasminogen activator by T lymphocytes and specific antigen, J Exp Med, 147, 1175, 10.1084/jem.147.4.1175 Schuyler, 1984, Alveolar macrophage plasminogen activator, Exp Lung Res, 6, 159, 10.3109/01902148409087903 Rodríguez-Flores, 2012, The response of the fibrinolytic system to mycobacteria infection, Tuberculosis, 92, 497, 10.1016/j.tube.2012.07.002 Lu, 2007, Fibrinolytic characteristics and their significance in malignant, tuberculous and cirrhotic pleural and ascitic fluids, Int J Lab Hematol, 29, 132, 10.1111/j.1751-553X.2006.00835.x Eugen-Olsen, 2002, The serum level of soluble urokinase receptor is elevated in tuberculosis patients and predicts mortality during treatment: a community study from Guinea-Bissau, Int J Tuberc Lung Dis, 6, 686 Rudolf, 2017, Tuberculosis case finding and mortality prediction: added value of the clinical TBscore and biomarker suPAR, Int J Tuberc Lung Dis, 21, 67, 10.5588/ijtld.16.0404 Sato, 2003, The fibrinolytic system in dissemination and matrix protein deposition during a mycobacterium infection, Am J Pathol, 163, 517, 10.1016/S0002-9440(10)63680-2 Silva-Miranda, 2015, High-content screening technology combined with a human granuloma model as a new approach to evaluate the activities of drugs against Mycobacterium tuberculosis, Antimicrob Agents Chemother, 59, 693, 10.1128/AAC.03705-14 Stephens, 1993, Plasminogen, 81 Wattiez, 1999, Human bronchoalveolar lavage fluid: two-dimensional gel electrophoresis, amino acid microsequencing and identification of major proteins, Electrophoresis, 20, 1634, 10.1002/(SICI)1522-2683(19990601)20:7<1634::AID-ELPS1634>3.0.CO;2-J Lottenberg, 1994, Capturing host plasmin(ogen): a common mechanism for invasive pathogens?, Trends Microbiol, 2, 20, 10.1016/0966-842X(94)90340-9 de la Paz Santangelo, 2011, Glycolytic and non-glycolytic functions of Mycobacterium tuberculosis fructose-1,6-bisphosphate aldolase, an essential enzyme produced by replicating and non-replicating bacilli, J Biol Chem, 46, 40219, 10.1074/jbc.M111.259440 de la Paz Santangelo M, Gest PM, Guerin ME, Coinçon M, Pham H, Ryan G, Puckett SE, Spencer JS, Gonzalez-Juarrero M, Daher R, Lenaerts AJ, Schnappinger D, Therisod M, Ehrt S, Sygusch J, Jackson M. Glycolytic and non-glycolytic functions of Mycobacterium tuberculosis fructose-1,6-bisphosphate aldolase, an essential enzyme produced by replicating and non-replicating bacilli. J Biol Chem. 201;46:40219-40231. doi: 10.1074/jbc.M111.259440. Das, 2014, Plasminogen promotes macrophage phagocytosis in mice, Blood, 124, 679, 10.1182/blood-2014-01-549659 Rooijakkers, 2005, Anti-opsonic properties of staphylokinase, Microb Infect, 7, 476, 10.1016/j.micinf.2004.12.014 Crane, 2009, A novel role for plasmin- mediated degradation of opsonizing antibody in the evasion of host immunity by virulent, but not attenuated, Francisella tularensis, J Immunol, 183, 4593, 10.4049/jimmunol.0901655 Ladel, 1997, Lethal tuberculosis in interleukin-6-deficient mutant mice, Infect Immun, 65, 4843, 10.1128/IAI.65.11.4843-4849.1997 Leal, 1999, Interleukin-6 and interleukin-12 participate in induction of a type 1 protective T-cell response during vaccination with a tuberculosis subunit vaccine, Infect Immun, 67, 5747, 10.1128/IAI.67.11.5747-5754.1999 Dutta, 2012, IL-6 inhibits IFN-γ induced autophagy in Mycobacterium tuberculosis H37Rv infected macrophages, Int J Biochem Cell Biol, 44, 942, 10.1016/j.biocel.2012.02.021 Nagabhushanam, 2003, Innate inhibition of adaptive immunity: Mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN gamma, J Immunol, 171, 4750, 10.4049/jimmunol.171.9.4750 Roach, 2002, TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection, J Immunol, 168, 4620, 10.4049/jimmunol.168.9.4620 Kaneko, 1999, Role of tumor necrosis factor-alpha in Mycobacterium-induced granuloma formation in tumor necrosis factor-alpha-deficient mice, Lab Investig, 79, 379 Bean, 1999, Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin, J Immunol, 162, 3504, 10.4049/jimmunol.162.6.3504 Gardam, 2003, Anti-tumour necrosis factor agents and tuberculosis risk: mechanisms of action and clinical management, Lancet Infect Dis, 3, 148, 10.1016/S1473-3099(03)00545-0 Clay, 2008, Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death, Immunity, 29, 284, 10.1016/j.immuni.2008.06.011 Flesch, 1990, Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor, Infect Immun, 58, 2675, 10.1128/IAI.58.8.2675-2677.1990 Engele, 2002, Induction of TNF in human alveolar macrophages as a potential evasion mechanism of virulent Mycobacterium tuberculosis, J Immunol, 168, 1328, 10.4049/jimmunol.168.3.1328 Laumonnier, 2007, Identification of the annexin A2 heterotetramer as a receptor for the plasmin-induced signaling in human peripheral monocytes, Blood, 107, 3342, 10.1182/blood-2005-07-2840 Li, 2007, Plasmin triggers cytokine induction in human monocyte-derived macrophages, Arterioscler Thromb Vasc Biol, 27, 1383, 10.1161/ATVBAHA.107.142901 Zhang, 2007, Urokinase-type plasminogen activator stimulation of monocyte matrix metalloproteinase-1 production is mediated by plasmin-dependent signaling through annexin A2 and inhibited by inactive plasmin, J Immunol, 179, 3297, 10.4049/jimmunol.179.5.3297 Haka, 2013, Plasmin promotes foam cell formation by increasing macrophage catabolism of aggregated low-density lipoprotein, Arterioscler Thromb Vasc Biol, 33, 1768, 10.1161/ATVBAHA.112.301109 Das, 2013, Macrophage gene expression and foam cell formation are regulated by plasminogen, Circulation, 127, 1209, 10.1161/CIRCULATIONAHA.112.001214 Peyron, 2008, Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence, PLoS Pathog, 4, 10.1371/journal.ppat.1000204 Boussiotis, 2000, IL-10-producing T cells suppress immune responses in anergic tuberculosis patients, J Clin Investig, 105, 1317, 10.1172/JCI9918 Gerosa, 1999, CD4(+) T cell clones producing both interferon-gamma and interleukin-10 predominate in bronchoalveolar lavages of active pulmonary tuberculosis patients, Clin Immunol, 92, 224, 10.1006/clim.1999.4752 Ranjbar, 2004, Mycobacterium tuberculosis recall antigens suppress HIV-1 replication in anergic donor cells via CD8+ T cell expansion and increased IL-10 levels, J Immunol, 172, 1953, 10.4049/jimmunol.172.3.1953 Bogdan, 1991, Macrophage deactivation by interleukin 10, J Exp Med, 174, 1549, 10.1084/jem.174.6.1549 Balcewicz-Sablinska, 1999, Interleukin 10 produced by macrophages inoculated with Mycobacterium avium attenuates mycobacteria-induced apoptosis by reduction of TNF-a activity, J Infect Dis, 180, 1230, 10.1086/315011 O'Leary, 2011, IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages, Am J Respir Cell Mol Biol, 45, 172, 10.1165/rcmb.2010-0319OC Fiorentino, 1991, IL-10 inhibits cytokine production by activated macrophages, J Immunol, 147, 3815, 10.4049/jimmunol.147.11.3815 Redford, 2010, Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung, Eur J Immunol, 40, 2200, 10.1002/eji.201040433 Richardson, 2015, Toll-like receptor 2-dependent extracellular signal-regulated kinase signaling in Mycobacterium tuberculosis-infected macrophages drives anti-inflammatory responses and inhibits Th1 polarization of responding T cells, Infect Immun, 83, 2242, 10.1128/IAI.00135-15 Luo, 2016, Mycobacterium tuberculosis Rv1265 promotes mycobacterial intracellular survival and alters cytokine profile of the infected macrophage, J Biomol Struct Dyn, 34, 585, 10.1080/07391102.2015.1046935 Deng, 2014, Mycobacterium tuberculosis PPE family protein Rv1808 manipulates cytokines profile via co-activation of MAPK and NF-κB signaling pathways, Cell Physiol Biochem, 33, 273, 10.1159/000356668 Yonekawa, 2014, Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria, Immunity, 41, 402, 10.1016/j.immuni.2014.08.005 Gideon, 2015, Variability in tuberculosis granuloma T cell responses exists, but a balance of pro- and anti-inflammatory cytokines is associated with sterilization, PLoS Pathog, 11, 10.1371/journal.ppat.1004603 Marakalala, 2016, Inflammatory signaling in human tuberculosis granulomas is spatially organized, Nat Med, 22, 531, 10.1038/nm.4073 Gerszten, 1999, MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions, Nature, 398, 718, 10.1038/19546 Mukaida, 1998, Interleukin-8 (IL-8) and monocyte chemotactic and activating factor (MCAF/MCP-1), chemokines essentially involved in inflammatory and immune reactions, Cytokine Growth Factor Rev, 9, 9, 10.1016/S1359-6101(97)00022-1 Larsen, 1995, The delayed-type hypersensitivity reaction is dependent on IL-8. Inhibition of a tuberculin skin reaction by an anti-IL-8 monoclonal antibody, J Immunol, 155, 2151, 10.4049/jimmunol.155.4.2151 Krupa, 2015, Binding of CXCL8/IL-8 to Mycobacterium tuberculosis modulates the innate immune response, Mediat Inflamm, 24762