Host sirtuin 1 regulates mycobacterial immunopathogenesis and represents a therapeutic target against tuberculosis

Science Immunology

Volumn 2, Issue 9, 2017, Pages

  Cheng, Catherine Y ^a   Gutierrez, Nuria M ^b   Marzuki, Mardiana B ^a   Lu, Xiaohua ^a   Foreman, Taylor W ^c   Paleja, Bhairav ^a   Lee, Bernett ^a   Balachander, Akhila ^a   Chen, Jinmiao ^a   Tsenova, Liana ^d,e   Kurepina, Natalia ^d   Teng, Karen W W ^a   West, Kim ^b   Mehra, Smriti ^f   Zolezzi, Francesca ^a,h   Poidinger, Michael ^a   Kreiswirth, Barry ^d   Kaushal, Deepak ^c   Kornfeld, Hardy ^b   Newell, Evan W ^a   Singhal, Amit ^a,g   more..

^a AGENCY FOR SCIENCE   (Singapore)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e NEW YORK CITY COLLEGE OF TECHNOLOGY   (United States)

^f LOUISIANA STATE UNIVERSITY   (United States)

^g NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^h Galderma R and D   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85032750306     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aaj1789     Document Type: Article

References (54)

1. C. J. Cambier, S. Falkow, L. Ramakrishnan, Host evasion and exploitation schemes of Mycobacterium tuberculosis. Cell 159, 1497–1509 (2014).
2. M. Uhlin, J. Andersson, A. Zumla, M. Maeurer, Adjunct immunotherapies for tuberculosis. J. Infect. Dis. 205, S325–S334 (2012).
3. R. S. Wallis, R. Hafner, Advancing host-directed therapy for tuberculosis. Nat. Rev. Immunol. 15, 255–263 (2015).
4. A. O’Garra, P. S. Redford, F. W. McNab, C. I. Bloom, R. J. Wilkinson, M. P. R. Berry, The immune response in tuberculosis. Annu. Rev. Immunol. 31, 475–527 (2013).
5. K. Ganeshan, A. Chawla, Metabolic regulation of immune responses. Annu. Rev. Immunol. 32, 609–634 (2014).
6. T. Weichhart, M. Hengstschläger, M. Linke, Regulation of innate immune cell function by mTOR. Nat. Rev. Immunol. 15, 599–614 (2015).
7. B. Viollet, F. Andreelli, AMP-activated protein kinase and metabolic control. Handb. Exp. Pharmacol. 203, 303–330 (2011).
8. H.-C. Chang, L. Guarente, SIRT1 and other sirtuins in metabolism. Trends Endocrinol. Metab. 25, 138–145 (2014).
9. D. Kumar, L. Nath, M. A. Kamal, A. Varshney, A. Jain, S. Singh, K. V. S. Rao, Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140, 731–743 (2010).
10. D. Kumar, K. V. S. Rao, Regulation between survival, persistence, and elimination of intracellular mycobacteria: A nested equilibrium of delicate balances. Microbes Infect. 13, 121–133 (2011).
11. M. G. Gutierrez, S. S. Master, S. B. Singh, G. A. Taylor, M. I. Colombo, V. Deretic, Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766 (2004).
12. A. Singhal, L. Jie, P. Kumar, G. S. Hong, M. K.-S. Leow, B. Paleja, L. Tsenova, N. Kurepina, J. Chen, F. Zolezzi, B. Kreiswirth, M. Poidinger, C. Chee, G. Kaplan, Y. T. Wang, G. De Libero, Metformin as adjunct antituberculosis therapy. Sci. Transl. Med. 6, 263ra159 (2014).
13. D. Herranz, M. Muñoz-Martin, M. Cañamero, F. Mulero, B. Martinez-Pastor, O. Fernandez-Capetillo, M. Serrano, Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nat. Commun. 1, 3 (2010).
14. L. Guarente, Calorie restriction and sirtuins revisited. Genes Dev. 27, 2072–2085 (2013).
15. E. Koyuncu, H. G. Budayeva, Y. V. Miteva, D. P. Ricci, T. J. Silhavy, T. Shenk, I. M. Cristea, Sirtuins are evolutionarily conserved viral restriction factors. mBio 5, e02249–14 (2014).
16. A. F. Karim, P. Chandra, A. Chopra, Z. Siddiqui, A. Bhaskar, A. Singh, D. Kumar, Express path analysis identifies a tyrosine kinase Src-centric network regulating divergent host responses to Mycobacterium tuberculosis infection. J. Biol. Chem. 286, 40307–40319 (2011).
17. M. P. R. Berry, C. M. Graham, F. W. McNab, Z. Xu, S. A. A. Bloch, T. Oni, K. A. Wilkinson, R. Banchereau, J. Skinner, R. J. Wilkinson, C. Quinn, D. Blankenship, R. Dhawan, J. J. Cush, A. Mejias, O. Ramilo, O. M. Kon, V. Pascual, J. Banchereau, D. Chaussabel, A. O’Garra, An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466, 973–977 (2010).
18. C. I. Bloom, C. M. Graham, M. P. R. Berry, K. A. Wilkinson, T. Oni, F. Rozakeas, Z. Xu, J. Rossello-Urgell, D. Chaussabel, J. Banchereau, V. Pascual, M. Lipman, R. J. Wilkinson, A. O’Garra, Detectable changes in the blood transcriptome are present after two weeks of antituberculosis therapy. PLOS ONE 7, e46191 (2012).
19. N. T. Thuong, S. J. Dunstan, T. T. H. Chau, V. Thorsson, C. P. Simmons, N. T. H. Quyen, G. E. Thwaites, N. Thi Ngoc Lan, M. Hibberd, Y. Y. Teo, M. Seielstad, A. Aderem, J. J. Farrar, T. R. Hawn, Identification of tuberculosis susceptibility genes with human macrophage gene expression profiles. PLOS Pathog. 4, e1000229 (2008).
20. Y. Cai, Q. Yang, Y. Tang, M. Zhang, H. Liu, G. Zhang, Q. Deng, J. Huang, Z. Gao, B. Zhou, C. G. Feng, X. Chen, Increased complement C1q level marks active disease in human tuberculosis. PLOS ONE 9, e92340 (2014).
21. N. Dawany, L. C. Showe, A. V. Kossenkov, C. Chang, P. Ive, F. Conradie, W. Stevens, I. Sanne, L. Azzoni, L. J. Montaner, Identification of a 251 gene expression signature that can accurately detect M. tuberculosis in patients with and without HIV co-infection. PLOS ONE 9, e89925 (2014).
22. M. Kaforou, V. J. Wright, T. Oni, N. French, S. T. Anderson, N. Bangani, C. M. Banwell, A. J. Brent, A. C. Crampin, H. M. Dockrell, B. Eley, R. S. Heyderman, M. L. Hibberd, F. Kern, P. R. Langford, L. Ling, M. Mendelson, T. H. Ottenhoff, F. Zgambo, R. J. Wilkinson, L. J. Coin, M. Levin, Detection of tuberculosis in HIV-infected and -uninfected African adults using whole blood RNA expression signatures: A case-control study. PLOS Med. 10, e1001538 (2013).
23. J. C. Milne, P. D. Lambert, S. Schenk, D. P. Carney, J. J. Smith, D. J. Gagne, L. Jin, O. Boss, R. B. Perni, C. B. Vu, J. E. Bemis, R. Xie, J. S. Disch, P. Y. Ng, J. J. Nunes, A. V. Lynch, H. Yang, H. Galonek, K. Israelian, W. Choy, A. Iffland, S. Lavu, O. Medvedik, D. A. Sinclair, J. M. Olefsky, M. R. Jirousek, P. J. Elliott, C. H. Westphal, Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450, 712–716 (2007).
24. M. T. Borra, B. C. Smith, J. M. Denu, Mechanism of human SIRT1 activation by resveratrol. J. Biol. Chem. 280, 17187–17195 (2005).
25. J. R. Revollo, X. Li, The ways and means that fine tune Sirt1 activity. Trends Biochem. Sci. 38, 160–167 (2013).
26. T. Yang, A. A. Sauve, NAD metabolism and sirtuins: Metabolic regulation of protein deacetylation in stress and toxicity. AAPS J. 8, E632–E643 (2006).
27. L. Bai, W.-J. Pang, Y.-J. Yang, G.-S. Yang, Modulation of Sirt1 by resveratrol and nicotinamide alters proliferation and differentiation of pig preadipocytes. Mol. Cell. Biochem. 307, 129–140 (2008).
28. A. Zumla, M. Rao, S. K. Parida, S. Keshavjee, G. Cassell, R. Wallis, R. Axelsson-Robertsson, M. Doherty, J. Andersson, M. Maeurer, Inflammation and tuberculosis: Host-directed therapies. J. Intern. Med. 277, 373–387 (2015).
29. S.-R. Yang, J. Wright, M. Bauter, K. Seweryniak, A. Kode, I. Rahman, Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-B in macrophages in vitro and in rat lungs in vivo: Implications for chronic inflammation and aging. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L567–L576 (2007).
30. T. T. Schug, Q. Xu, H. Gao, A. Peres-da-Silva, D. W. Draper, M. B. Fessler, A. Purushotham, X. Li, Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol. Cell. Biol. 30, 4712–4721 (2010).
31. M.-S. Koo, C. Manca, G. Yang, P. O’Brien, N. Sung, L. Tsenova, S. Subbian, D. Fallows, G. Muller, S. Ehrt, G. Kaplan, Phosphodiesterase 4 inhibition reduces innate immunity and improves isoniazid clearance of Mycobacterium tuberculosis in the lungs of infected mice. PLOS ONE 6, e17091 (2011).
32. I. V. Lyadova, E. B. Eruslanov, S. V. Khaidukov, V. V. Yeremeev, K. B. Majorov, A. V. Pichugin, B. V. Nikonenko, T. K. Kondratieva, A. S. Apt, Comparative analysis of T lymphocytes recovered from the lungs of mice genetically susceptible, resistant, and hyperresistant to Mycobacterium tuberculosis-triggered disease. J. Immunol. 165, 5921–5931 (2000).
33. dim cells in the lungs. PLOS ONE 5, e10469 (2010).
34. D. R. Bandura, V. I. Baranov, O. I. Ornatsky, A. Antonov, R. Kinach, X. Lou, S. Pavlov, S. Vorobiev, J. E. Dick, S. D. Tanner, Mass cytometry: Technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry. Anal. Chem. 81, 6813–6822 (2009).
35. B. Becher, A. Schlitzer, J. Chen, F. Mair, H. R. Sumatoh, K. W. W. Teng, D. Low, C. Ruedl, P. Riccardi-Castagnoli, M. Poidinger, M. Greter, F. Ginhoux, E. W. Newell, High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15, 1181–1189 (2014).
36. V. Desquiret-Dumas, N. Gueguen, G. Leman, S. Baron, V. Nivet-Antoine, S. Chupin, A. Chevrollier, E. Vessiéres, A. Ayer, M. Ferré, D. Bonneau, D. Henrion, P. Reynier, V. Procaccio, Resveratrol induces a mitochondrial complex I-dependent increase in NADH oxidation responsible for sirtuin activation in liver cells. J. Biol. Chem. 288, 36662–36675 (2013).
37. C. D. Cote, B. A. Rasmussen, F. A. Duca, M. Zadeh-Tahmasebi, J. A. Baur, M. Daljeet, D. M. Breen, B. M. Filippi, T. K. Lam, Resveratrol activates duodenal Sirt1 to reverse insulin resistance in rats through a neuronal network. Nat. Med. 21, 498–505 (2015).
38. J. Sun, A. Siroy, R. K. Lokareddy, A. Speer, K. S. Doornbos, G. Cingolani, M. Niederweis, The tuberculosis necrotizing toxin kills macrophages by hydrolyzing NAD. Nat. Struct. Mol. Biol. 22, 672–678 (2015).
39. I. H. Lee, L. Cao, R. Mostoslavsky, D. B. Lombard, J. Liu, N. E. Bruns, M. Tsokos, F. W. Alt, T. Finkel, A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. U.S.A. 105, 3374–3379 (2008).
40. Y. Wang, Y. Liang, P. M. Vanhoutte, SIRT1 and AMPK in regulating mammalian senescence: A critical review and a working model. FEBS Lett. 585, 986–994 (2011).
41. M. M. Mihaylova, R. J. Shaw, The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 13, 1016–1023 (2011).
42. A. Salminen, J. M. T. Hyttinen, K. Kaarniranta, AMP-activated protein kinase inhibits NF-B signaling and inflammation: Impact on healthspan and lifespan. J. Mol. Med. 89, 667–676 (2011).
43. H. Yang, W. Zhang, H. Pan, H. G. Feldser, E. Lainez, C. Miller, S. Leung, Z. Zhong, H. Zhao, S. Sweitzer, T. Considine, T. Riera, V. Suri, B. White, J. L. Ellis, G. P. Vlasuk, C. Loh, SIRT1 activators suppress inflammatory responses through promotion of p65 deacetylation and inhibition of NF-B activity. PLOS ONE 7, e46364 (2012).
44. L. R. V. Antonelli, A. Gigliotti Rothfuchs, R. Goncalves, E. Roffê, A. W. Cheever, A. Bafica, A. M. Salazar, C. G. Feng, A. Sher, Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/ macrophage population. J. Clin. Invest. 120, 1674–1682 (2010).
45. C. M. McClean, D. M. Tobin, Macrophage form, function and phenotype in mycobacterial infection: Lessons from tuberculosis and other diseases. Pathog. Dis. 74, ftw068 (2016).
46. N. V. Serbina, E. G. Pamer, Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311–317 (2006).
47. S. Srivastava, J. D. Ernst, L. Desvignes, Beyond macrophages: The diversity of mononuclear cells in tuberculosis. Immunol. Rev. 262, 179–192 (2014).
48. M. Samsami-Kor, N. E. Daryani, P. R. Asl, A. Hekmatdoost, Anti-inflammatory effects of resveratrol in patients with ulcerative colitis: A randomized, double-blind, placebo-controlled pilot study. Arch. Med. Res. 46, 280–285 (2015).
49. S. K. Chakrabarti, J. C. James, R. G. Mirmira, Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding. J. Biol. Chem. 277, 13286–13293 (2002).
50. E. W. Newell, N. Sigal, N. Nair, B. A. Kidd, H. B. Greenberg, M. M. Davis, Combinatorial tetramer staining and mass cytometry analysis facilitate T-cell epitope mapping and characterization. Nat. Biotechnol. 31, 623–629 (2013).
51. B. M. Bolstad, R. A. Irizarry, M. Astrand, T. P. Speed, A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185–193 (2003).
52. G. K. Smyth, Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
53. S. Mehra, X. Alvarez, P. J. Didier, L. A. Doyle, J. L. Blanchard, A. A. Lackner, D. Kaushal, Granuloma correlates of protection against tuberculosis and mechanisms of immune modulation by Mycobacterium tuberculosis. J. Infect. Dis. 207, 1115–1127 (2013).
54. D. Kaushal, T. W. Foreman, U. S. Gautam, X. Alvarez, T. Adekambi, J. Rangel-Moreno, N. A. Golden, A.-M. F. Johnson, B. L. Phillips, M. H. Ahsan, K. E. Russell-Lodrigue, L. A. Doyle, C. J. Roy, P. J. Didier, J. L. Blanchard, J. Rengarajan, A. A. Lackner, S. A. Khader, S. Mehra, Mucosal vaccination with attenuated Mycobacterium tuberculosis induces strong central memory responses and protects against tuberculosis. Nat. Commun. 6, 8533 (2015).