Identification of Host-Targeted Small Molecules That Restrict Intracellular Mycobacterium tuberculosis Growth

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Stanley, Sarah A ^a,b   Barczak, Amy K ^a,c   Silvis, Melanie R ^a   Luo, Samantha S ^c   Sogi, Kimberly ^b   Vokes, Martha ^a   Bray, Mark Anthony ^a   Carpenter, Anne E ^a   Moore, Christopher B ^a   Siddiqi, Noman ^d   Rubin, Eric J ^d   Hung, Deborah T ^a,c,e  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FLUOXETINE; G PROTEIN COUPLED RECEPTOR; GEFITINIB; IMATINIB; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE P38; QUINIDINE; RIFAMPICIN; RITANSERIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BACTERIAL GROWTH; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DRUG SCREENING; GENE EXPRESSION; GROWTH INHIBITION; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; MALE; MICROSCOPY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTITUBERCULAR AGENTS; DISEASE MODELS, ANIMAL; HIGH-THROUGHPUT SCREENING ASSAYS; HOST-PATHOGEN INTERACTIONS; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; SIGNAL TRANSDUCTION; TUBERCULOSIS;

EID: 84895732971     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003946     Document Type: Article

References (63)

1. Deretic V, Singh S, Master S, Harris J, Roberts E, et al. (2006) Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cellular Microbiology 8: 719-727.
2. Malik ZA, Iyer SS, Kusner DJ, (2001) Mycobacterium tuberculosis Phagosomes Exhibit Altered Calmodulin-Dependent Signal Transduction: Contribution to Inhibition of Phagosome-Lysosome Fusion and Intracellular Survival in Human Macrophages. The Journal of Immunology 166: 3392-3401.
3. Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, et al. (2007) Survival of Mycobacteria in Macrophages Is Mediated by Coronin 1-Dependent Activation of Calcineurin. Cell 130: 37-50.
4. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM, (2010) Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 11: 751-758.
5. Chen M, Divangahi M, Gan H, Shin DSJ, Hong S, et al. (2008) Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. The Journal of Experimental Medicine 205: 2791-2801.
6. Martin CJ, Booty MG, Rosebrock TR, Nunes-Alves C, Desjardins DM, et al. (2012) Efferocytosis Is an Innate Antibacterial Mechanism. Cell Host & Microbe 12: 289-300.
7. Shin D-M, Jeon B-Y, Lee H-M, Jin HS, Yuk J-M, et al. (2010) Mycobacterium tuberculosis Eis Regulates Autophagy, Inflammation, and Cell Death through Redox-dependent Signaling. PLoS Pathog 6: e1001230.
8. Master SS, Rampini SK, Davis AS, Keller C, Ehlers S, et al. (2008) Mycobacterium tuberculosis Prevents Inflammasome Activation. Cell Host & Microbe 3: 224-232.
9. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, et al. (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathogens 4: e1000204.
10. Kumar D, Nath L, Kamal MA, Varshney A, Jain A, et al. (2010) Genome-wide Analysis of the Host Intracellular Network that Regulates Survival of Mycobacterium tuberculosis. Cell 140: 731-743.
11. Jayaswal S, Kamal MA, Dua R, Gupta S, Majumdar T, et al. (2010) Identification of Host-Dependent Survival Factors for Intracellular Mycobacterium tuberculosis through an siRNA Screen. PLoS Pathog 6: e1000839.
12. Kuijl C, Savage NDL, Marsman M, Tuin AW, Janssen L, et al. (2007) Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 450: 725-U710.
13. Tailleux L, Waddell SJ, Pelizzola M, Mortellaro A, Withers M, et al. (2008) Probing Host Pathogen Cross-Talk by Transcriptional Profiling of Both Mycobacterium tuberculosis and Infected Human Dendritic Cells and Macrophages. PLoS ONE 3: e1403.
14. Stanley SA, Hung DT, (2009) Chemical Tools for Dissecting Bacterial Physiology and Virulence. Biochemistry 48: 8776-8786.
15. Christophe T, Jackson M, Jeon HK, Fenistein D, Contreras-Dominguez M, et al. (2009) High Content Screening Identifies Decaprenyl-Phosphoribose 2′ Epimerase as a Target for Intracellular Antimycobacterial Inhibitors. PLoS Pathog 5: e1000645.
16. Pethe K, Bifani P, Jang J, Kang S, Park S, et al. (2013) Discovery of Q203, a potent clinical candidate for the treatment of tuberculosis. Nat Med advance online publication.
17. Sundaramurthy V, Barsacchi R, Samusik N, Marsico G, Gilleron J, et al. (2013) Integration of Chemical and RNAi Multiparametric Profiles Identifies Triggers of Intracellular Mycobacterial Killing. Cell Host & Microbe 13: 129-142.
18. Stanley SA, Grant SS, Kawate T, Iwase N, Shimizu M, et al. (2012) Identification of Novel Inhibitors of M. tuberculosis Growth Using Whole Cell Based High-Throughput Screening. ACS Chemical Biology 7: 1377-1384.
19. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biology pp. 7.
20. Wei X, Gao L, Zhang X, Qian H, Rowan K, et al. (2013) Introducing Bayesian Thinking to High-Throughput Screening for False-Negative Rate Estimation. Journal of Biomolecular Screening.
21. Ilouga PE, Hesterkamp T, (2012) On the Prediction of Statistical Parameters in High-Throughput Screening Using Resampling Techniques. Journal of Biomolecular Screening 17: 705-712.
22. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, et al. (2001) Tuberculosis Associated with Infliximab, a Tumor Necrosis Factor-alpha ìNeutralizing Agent. New England Journal of Medicine 345: 1098-1104.
23. Gardam MA, Keystone EC, Menzies R, Manners S, Skamene E, et al. (2003) Anti-tumour necrosis factor agents and tuberculosis risk: mechanisms of action and clinical management. The Lancet Infectious Diseases 3: 148-155.
24. Glosli H, Stray-Pedersen A, Brun AC, Holtmon LW, Tonjum T, et al. (2008) Infections Due to Various Atypical Mycobacteria in a Norwegian Multiplex Family with Dominant Interferon-gamma Receptor Deficiency. Clinical Infectious Diseases 46: e23-e27.
25. Bekker L-G, Freeman S, Murray PJ, Ryffel B, Kaplan G, (2001) TNF-alpha Controls Intracellular Mycobacterial Growth by Both Inducible Nitric Oxide Synthase-Dependent and Inducible Nitric Oxide Synthase-Independent Pathways. The Journal of Immunology 166: 6728-6734.
26. Warner-Schmidt JL, Vanover KE, Chen EY, Marshall JJ, Greengard P, (2011) Antidepressant effects of selective serotonin reuptake inhibitors (SSRIs) are attenuated by antiinflammatory drugs in mice and humans. Proceedings of the National Academy of Sciences 108: 9262-9267.
27. Harris J, Keane J, (2010) How tumour necrosis factor blockers interfere with tuberculosis immunity. Clinical & Experimental Immunology 161: 1-9.
28. Napier RJ, Rafi W, Cheruvu M, Powell KR, Zaunbrecher MA, et al. (2011) Imatinib-Sensitive Tyrosine Kinases Regulate Mycobacterial Pathogenesis and Represent Therapeutic Targets against Tuberculosis. Cell Host & Microbe 10: 475-485.
29. Bruns H, Stegelmann F, Fabri M, Döhner K, van Zandbergen G, et al. (2012) Abelson Tyrosine Kinase Controls Phagosomal Acidification Required for Killing of Mycobacterium tuberculosis in Human Macrophages. The Journal of Immunology 189: 4069-4078.
30. Zhao Z, Leister WH, Robinson RG, Barnett SF, Defeo-Jones D, et al. (2005) Discovery of 2,3,5-trisubstituted pyridine derivatives as potent Akt1 and Akt2 dual inhibitors. Bioorganic & Medicinal Chemistry Letters 15: 905-909.
31. Barnett SF, Defeo-Jones D, Fu S, Hancock PJ, Haskell KM, et al. (2005) Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem J 385: 399-408.
32. Alessi DRA, M.; Caudwell, B.; Cron, P.; Morrice, N.; Cohen, P.; Hemmings BA, (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15: 6541-6551.
33. Wong S, Witte ON, (2004) The BCR-ABL Story: Bench to Bedside and Back. Annual Review of Immunology 22: 247-306.
34. Wong S, McLaughlin J, Cheng D, Zhang C, Shokat KM, et al. (2004) Sole BCR-ABL inhibition is insufficient to eliminate all myeloproliferative disorder cell populations. Proceedings of the National Academy of Sciences of the United States of America 101: 17456-17461.
35. Eierhoff T, Hrincius ER, Rescher U, Ludwig S, Ehrhardt C, (2010) The Epidermal Growth Factor Receptor (EGFR) Promotes Uptake of Influenza A Viruses (IAV) into Host Cells. PLoS Pathog 6: e1001099.
36. Liu K, Gualano RC, Hibbs ML, Anderson GP, Bozinovski S, (2008) Epidermal Growth Factor Receptor Signaling to Erk1/2 and STATs Control the Intensity of the Epithelial Inflammatory Responses to Rhinovirus Infection. Journal of Biological Chemistry 283: 9977-9985.
37. Yan F, Cao H, Chaturvedi R, Krishna U, Hobbs SS, et al. (2009) Epidermal Growth Factor Receptor Activation Protects Gastric Epithelial Cells From Helicobacter pylori-Induced Apoptosis. Gastroenterology 136: 1297-1307.e1293.
38. Lynch T, (2003) Clinical benefit in NSCLC: the evidence for gefitinib (Iressa, ZD1839). European Journal of Cancer Supplements 1: 17-22.
39. Spangler JB, Neil JR, Abramovitch S, Yarden Y, White FM, et al. (2010) Combination antibody treatment down-regulates epidermal growth factor receptor by inhibiting endosomal recycling. Proceedings of the National Academy of Sciences 107: 13252-13257.
40. Lee MRD, (2005) C (2005) MAP kinase p38 inhibitors: Clinical results and an intimate look at their interactions with p38 alpha protein. Current Medicinal Chemistry 12: 2979-2994.
41. Webber JL, Tooze SA, (2010) Coordinated regulation of autophagy by p38-alpha MAPK through mAtg9 and p38IP. EMBO J 29: 27-40.
42. Subbian S, Tsenova L, O'Brien P, Yang G, Koo M-S, et al. (2011) Phosphodiesterase-4 Inhibition Alters Gene Expression and Improves Isoniazid-Mediated Clearance of Mycobacterium tuberculosis in Rabbit Lungs. PLoS Pathog 7: e1002262.
43. Gupta S, Salam N, Srivastava V, Singla R, Behera D, et al. (2009) Voltage Gated Calcium Channels Negatively Regulate Protective Immunity to Mycobacterium tuberculosis. PLoS ONE 4: e5305.
44. Adams KN, Takaki K, Connolly LE, Wiedenhoft H, Winglee K, et al. (2011) Drug Tolerance in Replicating Mycobacteria Mediated by a Macrophage-Induced Efflux Mechanism. Cell 145: 39-53.
45. Gupta ST, Sandeep, (2013) Almeida, Deepak V, (2013) Maiga, Mariama C, (2013) Ammerman, Nicole C, (2013) Bishai, William R, (2013) Acceleration of tuberculosis treatment by adjunctive therapy with verapamil as an efflux inhibitor. AJRCCM 10.1164/rccm.201304-0650OC.
46. Singh V, Jamwal S, Jain R, Verma P, Gokhale R, et al. (2012) Mycobacterium tuberculosis-Driven Targeted Recalibration of Macrophage Lipid Homeostasis Promotes the Foamy Phenotype. Cell Host & Microbe 12: 669-681.
47. de las Casas-Engel M, Dominguez-Soto A, Sierra-Filardi E, Bragado R, Nieto C, et al. (2013) Serotonin Skews Human Macrophage Polarization through HTR2B and HTR7. The Journal of Immunology 190: 2301-2310.
48. Gaskill PC, Loreto, (2012) Eugenin, Eliseo A, (2012) Berman, Joan W, (2012) Characterization and function of the human macrophage dopaminergic system: implications for CNS disease and drug abuse. Journal of Neuroimflammation 9: 203-216.
49. Izeboud CM, JAJ; Monshouwer, M; van Miert, ASJPAM; Witkamp RF, (1999) Participation of beta-Adrenergic Receptors on Marophages in Modulation of LPS-Induced Cytokine Release. Journal of Receptors and Signal Transduction 19: 191-202.
50. Sternberg EM, Trial J, Parker CW, (1986) Effect of serotonin on murine macrophages: suppression of Ia expression by serotonin and its reversal by 5-HT2 serotonergic receptor antagonists. The Journal of Immunology 137: 276-282.
51. Cloez-Tayarani I, Petit-Bertron A-F, Venters HD, Cavaillon J-M, (2003) Differential effect of serotonin on cytokine production in lipopolysaccharide-stimulated human peripheral blood mononuclear cells: involvement of 5-hydroxytryptamine2A receptors. International Immunology 15: 233-240.
52. Tobin DM, Roca FJ, Oh SF, McFarland R, Vickery TW, et al. (2012) Host Genotype-Specific Therapies Can Optimize the Inflammatory Response to Mycobacterial Infections. Cell 148: 434-446.
53. Roca FJ, Ramakrishnan L, (2013) TNF Dually Mediates Resistance and Susceptibility to Mycobacteria via Mitochondrial Reactive Oxygen Species. Cell 153: 521-534.
54. Koo M-S, Manca C, Yang G, O'Brien P, Sung N, et al. (2011) Phosphodiesterase 4 Inhibition Reduces Innate Immunity and Improves Isoniazid Clearance of Mycobacterium tuberculosis in the Lungs of Infected Mice. PLoS ONE 6: e17091.
55. Shubin H, Lambert RE, Heiken CA, Sokmensuer A, Glaskin A, (1959) Steroid therapy and tuberculosis. Journal of the American Medical Association 170: 1885-1890.
56. Critchley JA, Young F, Orton L, Garner P, (2013) Corticosteroids for prevention of mortality in people with tuberculosis: a systematic review and meta-analysis. The Lancet Infectious Diseases 13: 223-237.
57. Wallis RS, (2005) Reconsidering Adjuvant Immunotherapy for Tuberculosis. Clinical Infectious Diseases 41: 201-208.
58. Skerry C, Harper J, Klunk M, Bishai WR, Jain SK, (2012) Adjunctive TNF Inhibition with Standard Treatment Enhances Bacterial Clearance in a Murine Model of Necrotic TB Granulomas. PLoS ONE 7: e39680.
59. Maiga M, Agarwal N, Ammerman NC, Gupta R, Guo H, et al. (2012) Successful Shortening of Tuberculosis Treatment Using Adjuvant Host-Directed Therapy with FDA-Approved Phosphodiesterase Inhibitors in the Mouse Model. PLoS ONE 7: e30749.
60. Schwegmann A, Brombacher F, (2008) Host-Directed Drug Targeting of Factors Hijacked by Pathogens. Science Signaling 1: re8.
61. Korf H, Vander Beken S, Romano M, Steffensen KR, Stijlemans B, et al. (2009) Liver X receptors contribute to the protective immune response against Mycobacterium tuberculosis in mice. The Journal of Clinical Investigation 119: 1626-1637.
62. Lee M, Lee J, Carroll MW, Choi H, Min S, et al. (2012) Linezolid for Treatment of Chronic Extensively Drug-Resistant Tuberculosis. New England Journal of Medicine 367: 1508-1518.
63. Stanley SA, Kawate T, Iwase N, Shimizu M, Clatworthy AE, et al. (2013) Diarylcoumarins inhibit mycolic acid biosynthesis and kill Mycobacterium tuberculosis by targeting FadD32. Proceedings of the National Academy of Sciences 110: 11565-11570.