Mycobacterial WhiB6 Differentially Regulates ESX-1 and the Dos Regulon to Modulate Granuloma Formation and Virulence in Zebrafish

Cell Reports

Volumn 16, Issue 9, 2016, Pages 2512-2524

  Chen, Zhenkang ^a,d   Hu, Yangbo ^a   Cumming, Bridgette M ^b   Lu, Pei ^a   Feng, Lipeng ^a   Deng, Jiaoyu ^a   Steyn, Adrie J C ^b,c   Chen, Shiyun ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b AFRICA HEALTH RESEARCH INSTITUTE   (South Africa)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MYCOBACTERIAL WHIB6; NITRIC OXIDE; UNCLASSIFIED DRUG; 1-HYDROXY-2-OXO-3,3-BIS(2-AMINOETHYL)-1-TRIAZENE; IRON SULFUR PROTEIN; NITRIC OXIDE DONOR; PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTOME; TRIAZENE DERIVATIVE;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; BACTERIAL VIRULENCE; CELL DIVISION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DOS REGULON; ESPE GENE; ESX 1 REGULON; ESXA GENE; ESXB GENE; FE S CLUSTER; GENE CLUSTER; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GRANULOMA; METABOLIC REGULATION; MOLECULAR DYNAMICS; MYCOBACTERIOSIS; MYCOBACTERIUM MARINUM; NONHUMAN; OPEN READING FRAME; OPERON; PE35 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULON; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ZEBRA FISH; AMINO ACID SEQUENCE; ANAEROBIC GROWTH; ANIMAL; ATYPICAL MYCOBACTERIOSIS; CHEMISTRY; DRUG EFFECTS; FISH DISEASE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; VETERINARY; VIRULENCE;

AEROBIOSIS; AMINO ACID SEQUENCE; ANAEROBIOSIS; ANIMALS; BACTERIAL PROTEINS; FISH DISEASES; GENE EXPRESSION REGULATION, BACTERIAL; GRANULOMA; HOST-PATHOGEN INTERACTIONS; IRON-SULFUR PROTEINS; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; MYCOBACTERIUM MARINUM; NITRIC OXIDE; NITRIC OXIDE DONORS; PROTEIN KINASES; REGULON; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRIAZENES; VIRULENCE; ZEBRAFISH;

EID: 84989961111     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.07.080     Document Type: Article

References (65)

1. Abdallah, A.M., Bestebroer, J., Savage, N.D.L., de Punder, K., van Zon, M., Wilson, L., Korbee, C.J., van der Sar, A.M., Ottenhoff, T.H.M., van der Wel, N.N., et al. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J. Immunol. 187 (2011), 4744–4753.
2. Alam, M.S., Garg, S.K., Agrawal, P., Studies on structural and functional divergence among seven WhiB proteins of Mycobacterium tuberculosis H37Rv. FEBS J. 276 (2009), 76–93.
3. Balaban, N.Q., Gerdes, K., Lewis, K., McKinney, J.D., A problem of persistence: still more questions than answers?. Nat. Rev. Microbiol. 11 (2013), 587–591.
4. Boon, C., Dick, T., How Mycobacterium tuberculosis goes to sleep: the dormancy survival regulator DosR a decade later. Future Microbiol. 7 (2012), 513–518.
5. Boshoff, H.I.M., Xu, X., Tahlan, K., Dowd, C.S., Pethe, K., Camacho, L.R., Park, T.-H., Yun, C.-S., Schnappinger, D., Ehrt, S., et al. Biosynthesis and recycling of nicotinamide cofactors in mycobacterium tuberculosis. An essential role for NAD in nonreplicating bacilli. J. Biol. Chem. 283 (2008), 19329–19341.
6. Burian, J., Yim, G., Hsing, M., Axerio-Cilies, P., Cherkasov, A., Spiegelman, G.B., Thompson, C.J., The mycobacterial antibiotic resistance determinant WhiB7 acts as a transcriptional activator by binding the primary sigma factor SigA (RpoV). Nucleic Acids Res. 41 (2013), 10062–10076.
7. Cambier, C.J., Falkow, S., Ramakrishnan, L., Host evasion and exploitation schemes of Mycobacterium tuberculosis. Cell 159 (2014), 1497–1509.
8. Casonato, S., Cervantes Sánchez, A., Haruki, H., Rengifo González, M., Provvedi, R., Dainese, E., Jaouen, T., Gola, S., Bini, E., Vicente, M., et al. WhiB5, a transcriptional regulator that contributes to Mycobacterium tuberculosis virulence and reactivation. Infect. Immun. 80 (2012), 3132–3144.
9. Champion, M.M., Williams, E.A., Pinapati, R.S., Champion, P.A.D., Correlation of phenotypic profiles using targeted proteomics identifies mycobacterial esx-1 substrates. J. Proteome Res. 13 (2014), 5151–5164.
10. Chan, J., Xing, Y., Magliozzo, R.S., Bloom, B.R., Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175 (1992), 1111–1122.
11. Chan, J., Tanaka, K., Carroll, D., Flynn, J., Bloom, B.R., Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect. Immun. 63 (1995), 736–740.
12. Chawla, M., Parikh, P., Saxena, A., Munshi, M., Mehta, M., Mai, D., Srivastava, A.K., Narasimhulu, K.V., Redding, K.E., Vashi, N., et al. Mycobacterium tuberculosis WhiB4 regulates oxidative stress response to modulate survival and dissemination in vivo. Mol. Microbiol. 85 (2012), 1148–1165.
13. Cumming, B.M., Steyn, A.J., Metabolic plasticity of central carbon metabolism protects mycobacteria. Proc. Natl. Acad. Sci. USA 112 (2015), 13135–13136.
14. Davis, J.M., Ramakrishnan, L., The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136 (2009), 37–49.
15. Dutta, N.K., Karakousis, P.C., Latent tuberculosis infection: myths, models, and molecular mechanisms. Microbiol. Mol. Biol. Rev. 78 (2014), 343–371.
16. Ehrt, S., Schnappinger, D., Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell. Microbiol. 11 (2009), 1170–1178.
17. Ellett, F., Pase, L., Hayman, J.W., Andrianopoulos, A., Lieschke, G.J., mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117 (2011), e49–e56.
18. Flannagan, R.S.C., Cosío, G., Grinstein, S., Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7 (2009), 355–366.
19. Gao, L.-Y., Guo, S., McLaughlin, B., Morisaki, H., Engel, J.N., Brown, E.J., A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol. Microbiol. 53 (2004), 1677–1693.
20. Geiman, D.E., Raghunand, T.R., Agarwal, N., Bishai, W.R., Differential gene expression in response to exposure to antimycobacterial agents and other stress conditions among seven Mycobacterium tuberculosis whiB-like genes. Antimicrob. Agents Chemother. 50 (2006), 2836–2841.
21. Gengenbacher, M., Kaufmann, S.H., Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol. Rev. 36 (2012), 514–532.
22. Goodsmith, N., Guo, X.V., Vandal, O.H., Vaubourgeix, J., Wang, R., Botella, H., Song, S., Bhatt, K., Liba, A., Salgame, P., et al. Disruption of an M. tuberculosis membrane protein causes a magnesium-dependent cell division defect and failure to persist in mice. PLoS Pathog., 11, 2015, e1004645.
23. Hartman, T., Weinrick, B., Vilchèze, C., Berney, M., Tufariello, J., Cook, G.M., Jacobs, W.R. Jr., Succinate dehydrogenase is the regulator of respiration in Mycobacterium tuberculosis. PLoS Pathog., 10, 2014, e1004510.
24. Homolka, S., Niemann, S., Russell, D.G., Rohde, K.H., Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog., 6, 2010, e1000988.
25. Houben, D., Demangel, C., van Ingen, J., Perez, J., Baldeón, L., Abdallah, A.M., Caleechurn, L., Bottai, D., van Zon, M., de Punder, K., et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell. Microbiol. 14 (2012), 1287–1298.
26. Hurley, J.K., Weber-Main, A.M., Hodges, A.E., Stankovich, M.T., Benning, M.M., Holden, H.M., Cheng, H., Xia, B., Markley, J.L., Genzor, C., et al. Iron-sulfur cluster cysteine-to-serine mutants of Anabaena -2Fe-2S- ferredoxin exhibit unexpected redox properties and are competent in electron transfer to ferredoxin:NADP+ reductase. Biochemistry 36 (1997), 15109–15117.
27. Joshi, S.A., Ball, D.A., Sun, M.G., Carlsson, F., Watkins, B.Y., Aggarwal, N., McCracken, J.M., Huynh, K.K., Brown, E.J., EccA1, a component of the Mycobacterium marinum ESX-1 protein virulence factor secretion pathway, regulates mycolic acid lipid synthesis. Chem. Biol. 19 (2012), 372–380.
28. Karakousis, P.C., Williams, E.P., Bishai, W.R., Altered expression of isoniazid-regulated genes in drug-treated dormant Mycobacterium tuberculosis. J. Antimicrob. Chemother. 61 (2008), 323–331.
29. Kassa, D., Ran, L., Geberemeskel, W., Tebeje, M., Alemu, A., Selase, A., Tegbaru, B., Franken, K.L.M.C., Friggen, A.H., van Meijgaarden, K.E., et al. Analysis of immune responses against a wide range of Mycobacterium tuberculosis antigens in patients with active pulmonary tuberculosis. Clin. Vaccine Immunol. 19 (2012), 1907–1915.
30. Konar, M., Alam, M.S., Arora, C., Agrawal, P., WhiB2/Rv3260c, a cell division-associated protein of Mycobacterium tuberculosis H37Rv, has properties of a chaperone. FEBS J. 279 (2012), 2781–2792.
31. Kumar, A., Toledo, J.C., Patel, R.P., Lancaster, J.R. Jr., Steyn, A.J., Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. USA 104 (2007), 11568–11573.
32. Kumar, A., Deshane, J.S., Crossman, D.K., Bolisetty, S., Yan, B.-S., Kramnik, I., Agarwal, A., Steyn, A.J.C., Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J. Biol. Chem. 283 (2008), 18032–18039.
33. Langenau, D.M., Zon, L.I., The zebrafish: a new model of T-cell and thymic development. Nat. Rev. Immunol. 5 (2005), 307–317.
34. Larsen, M.H., Vilchèze, C., Kremer, L., Besra, G.S., Parsons, L., Salfinger, M., Heifets, L., Hazbon, M.H., Alland, D., Sacchettini, J.C., Jacobs, W.R. Jr., Overexpression of inhA, but not kasA, confers resistance to isoniazid and ethionamide in Mycobacterium smegmatis, M. bovis BCG and M. tuberculosis. Mol. Microbiol. 46 (2002), 453–466.
35. Larsson, C., Luna, B., Ammerman, N.C., Maiga, M., Agarwal, N., Bishai, W.R., Gene expression of Mycobacterium tuberculosis putative transcription factors whiB1-7 in redox environments. PLoS ONE, 7, 2012, e37516.
36. Leistikow, R.L., Morton, R.A., Bartek, I.L., Frimpong, I., Wagner, K., Voskuil, M.I., The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from nonrespiring dormancy. J. Bacteriol. 192 (2010), 1662–1670.
37. McLaughlin, B., Chon, J.S., MacGurn, J.A., Carlsson, F., Cheng, T.L., Cox, J.S., Brown, E.J., A mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog., 3, 2007, e105.
38. Mehra, S., Foreman, T.W., Didier, P.J., Ahsan, M.H., Hudock, T.A., Kissee, R., Golden, N.A., Gautam, U.S., Johnson, A.-M., Alvarez, X., et al. The DosR regulon modulates adaptive immunity and is essential for Mycobacterium tuberculosis persistence. Am. J. Respir. Crit. Care Med. 191 (2015), 1185–1196.
39. Ohno, H., Zhu, G., Mohan, V.P., Chu, D., Kohno, S., Jacobs, W.R. Jr., Chan, J., The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell. Microbiol. 5 (2003), 637–648.
40. Pagán, A.J., Ramakrishnan, L., Immunity and immunopathology in the tuberculous granuloma. Cold Spring Harb. Perspect. Med., 5, 2014, a018499.
41. Pagán, A.J., Yang, C.-T., Cameron, J., Swaim, L.E., Ellett, F., Lieschke, G.J., Ramakrishnan, L., Myeloid growth factors promote resistance to Mycobacterial infection by curtailing granuloma necrosis through macrophage replenishment. Cell Host Microbe 18 (2015), 15–26.
42. Parikka, M., Hammarén, M.M., Harjula, S.K., Halfpenny, N.J., Oksanen, K.E., Lahtinen, M.J., Pajula, E.T., Iivanainen, A., Pesu, M., Rämet, M., Mycobacterium marinum causes a latent infection that can be reactivated by gamma irradiation in adult zebrafish. PLoS Pathog., 8, 2012, e1002944.
43. Philips, J.A., Ernst, J.D., Tuberculosis pathogenesis and immunity. Annu. Rev. Pathol. 7 (2012), 353–384.
44. Ramakrishnan, L., Revisiting the role of the granuloma in tuberculosis. Nat. Rev. Immunol. 12 (2012), 352–366.
45. Rao, S.P.S., Alonso, S., Rand, L., Dick, T., Pethe, K., The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 105 (2008), 11945–11950.
46. Rodriguez, J.G., Burbano, C.S., Nuñez, C., González, C.E., Zambrano, M.M., García, M.J., Del Portillo, P., Rv3134c/devR/devS operon of Mycobacterium bovis BCG is differentially transcribed under “in vitro” stress conditions. Tuberculosis (Edinb.) 88 (2008), 273–282.
47. Rustad, T.R., Harrell, M.I., Liao, R., Sherman, D.R., The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE, 3, 2008, e1502.
48. Rustad, T.R., Sherrid, A.M., Minch, K.J., Sherman, D.R., Hypoxia: a window into Mycobacterium tuberculosis latency. Cell. Microbiol. 11 (2009), 1151–1159.
49. Saini, V., Farhana, A., Glasgow, J.N., Steyn, A.J.C., Iron sulfur cluster proteins and microbial regulation: implications for understanding tuberculosis. Curr. Opin. Chem. Biol. 16 (2012), 45–53.
50. Saini, V., Farhana, A., Steyn, A.J.C., Mycobacterium tuberculosis WhiB3: a novel iron-sulfur cluster protein that regulates redox homeostasis and virulence. Antioxid. Redox Signal. 16 (2012), 687–697.
51. Schnappinger, D., Ehrt, S., Voskuil, M.I., Liu, Y., Mangan, J.A., Monahan, I.M., Dolganov, G., Efron, B., Butcher, P.D., Nathan, C., Schoolnik, G.K., Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198 (2003), 693–704.
52. Shiloh, M.U., Manzanillo, P., Cox, J.S., Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3 (2008), 323–330.
53. Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R., Enninga, J., Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog., 8, 2012, e1002507.
54. Singh, A., Guidry, L., Narasimhulu, K.V., Mai, D., Trombley, J., Redding, K.E., Giles, G.I., Lancaster, J.R. Jr., Steyn, A.J., Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc. Natl. Acad. Sci. USA 104 (2007), 11562–11567.
55. Singh, A., Crossman, D.K., Mai, D., Guidry, L., Voskuil, M.I., Renfrow, M.B., Steyn, A.J.C., Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog., 5, 2009, e1000545.
56. Smith, L.J., Stapleton, M.R., Fullstone, G.J., Crack, J.C., Thomson, A.J., Le Brun, N.E., Hunt, D.M., Harvey, E., Adinolfi, S., Buxton, R.S., Green, J., Mycobacterium tuberculosis WhiB1 is an essential DNA-binding protein with a nitric oxide-sensitive iron-sulfur cluster. Biochem. J. 432 (2010), 417–427.
57. Solans, L., Aguiló, N., Samper, S., Pawlik, A., Frigui, W., Martín, C., Brosch, R., Gonzalo-Asensio, J., A specific polymorphism in Mycobacterium tuberculosis H37Rv causes differential ESAT-6 expression and identifies WhiB6 as a novel ESX-1 component. Infect. Immun. 82 (2014), 3446–3456.
58. Solans, L., Gonzalo-Asensio, J., Sala, C., Benjak, A., Uplekar, S., Rougemont, J., Guilhot, C., Malaga, W., Martín, C., Cole, S.T., The PhoP-dependent ncRNA Mcr7 modulates the TAT secretion system in Mycobacterium tuberculosis. PLoS Pathog., 10, 2014, e1004183.
59. Spiro, S., Regulators of bacterial responses to nitric oxide. FEMS Microbiol. Rev. 31 (2007), 193–211.
60. Stanley, S.A., Raghavan, S., Hwang, W.W., Cox, J.S., Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl. Acad. Sci. USA 100 (2003), 13001–13006.
61. Tobin, D.M., Vary, J.C. Jr., Ray, J.P., Walsh, G.S., Dunstan, S.J., Bang, N.D., Hagge, D.A., Khadge, S., King, M.-C., Hawn, T.R., et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140 (2010), 717–730.
62. Via, L.E., Lin, P.L., Ray, S.M., Carrillo, J., Allen, S.S., Eum, S.Y., Taylor, K., Klein, E., Manjunatha, U., Gonzales, J., et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect. Immun. 76 (2008), 2333–2340.
63. Volkman, H.E., Clay, H., Beery, D., Chang, J.C.W., Sherman, D.R., Ramakrishnan, L., Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol., 2, 2004, e367.
64. Voskuil, M.I., Schnappinger, D., Visconti, K.C., Harrell, M.I., Dolganov, G.M., Sherman, D.R., Schoolnik, G.K., Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198 (2003), 705–713.
65. Zhang, Y., Garbe, T., Young, D., Transformation with katG restores isoniazid-sensitivity in Mycobacterium tuberculosis isolates resistant to a range of drug concentrations. Mol. Microbiol. 8 (1993), 521–524.