Immune oxysterols: Role in mycobacterial infection and inflammation

Journal of Steroid Biochemistry and Molecular Biology

Volumn 169, Issue , 2017, Pages 152-163

  Bah, Saikou Y ^a,c   Dickinson, Paul ^a   Forster, Thorsten ^a   Kampmann, Beate ^c,d   Ghazal, Peter ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c MRC Unit   (Gambia)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

25 hydroxycholesterol; Cholesterol; Immunity; Infection; Oxysterols; Tuberculosis; Vitamin D

Indexed keywords

25 HYDROXYCHOLESTEROL; COLECALCIFEROL; ERGOCALCIFEROL; OXYSTEROL; 1,25-DIHYDROXYVITAMIN D; 25-HYDROXYCHOLESTEROL; ANTIINFECTIVE AGENT; CHOLESTEROL; CHOLESTEROL DERIVATIVE; VITAMIN D;

ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; BONE MARROW CELL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DISEASE SEVERITY; FATTY ACID METABOLISM; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; INFLAMMATION; LIPOGENESIS; LYMPHOCYTE; MACROPHAGE; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX; PATHOGENESIS; REVIEW; TUBERCULOSIS; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; IMMUNE SYSTEM; IMMUNOLOGY; INNATE IMMUNITY; MYCOBACTERIOSIS; MYCOBACTERIUM; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-BACTERIAL AGENTS; CHOLESTEROL; DRUG RESISTANCE, BACTERIAL; HOMEOSTASIS; HUMANS; HYDROXYCHOLESTEROLS; IMMUNE SYSTEM; IMMUNITY, INNATE; INFLAMMATION; LYMPHOCYTES; MACROPHAGES; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; OXYSTEROLS; SIGNAL TRANSDUCTION; VITAMIN D;

EID: 84970021108     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2016.04.015     Document Type: Review

References (89)

1. [1] Fessler, M.B., Parks, J.S., Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J. Immunol. 187 (2011), 1529–1535.
2. [2] Mazein, A., Griffiths, W., Freeman, T., Ghazal, P., Watterson, S., Gibbs, H., et al. Regulation and feedback of cholesterol metabolism. Nat. Preced., 2011, 10.1038/npre.2011.6315.1.
3. [3] Blanc, M., Hsieh, W.Y., Robertson, K.A., Kropp, K.A., Forster, T., Shui, G., et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity 38 (2013), 106–118.
4. [4] Liu, S.-Y., Aliyari, R., Chikere, K., Li, G., Marsden, M.D., Smith, J.K., et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity 38 (2013), 92–105, 10.1016/j.immuni.2012.11.005.
5. [5] Chan, T.Y.K., Vitamin D deficiency and susceptibility to tuberculosis. Calcif. Tissue Int. 66 (2000), 476–478, 10.1007/s002230010095.
6. [6] Talat, N., Perry, S., Parsonnet, J., Dawood, G., Hussain, R., Vitamin D deficiency and tuberculosis progression. Emerg. Infect. Dis. 16 (2010), 853–855, 10.3201/eid1605.091693.
7. [7] Cyster, J.G., Dang, E.V., Reboldi, A., Yi, T., 25-Hydroxycholesterols in innate and adaptive immunity. Nat. Rev. Immunol. 14 (2014), 731–743, 10.1038/nri3755.
8. [8] Spann, N.J., Glass, C.K., Sterols and oxysterols in immune cell function. Nat. Immunol. 14 (2013), 893–900 http://www.ncbi.nlm.nih.gov/pubmed/23959186.
9. [9] Murray, C.J., Ortblad, K.F., Guinovart, C., Lim, S.S., Wolock, T.M., Roberts, D.A., et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet, 2014, 10.1016/S0140-6736(14)60844-8.
10. [10] WHO, Global Tuberculosis Report 2015 (2015), http://apps.who.int/iris/bitstream/10665/191102/1/9789241565059_eng.pdf?ua=1.
11. [11] Rodrigues, L.C., Diwan, V.K., Wheeler, J.G., Protective effect of BCG against tuberculous meningitis and miliary tuberculosis: a meta-analysis. Int. J. Epidemiol. 22 (1993), 1154–1158.
12. [12] Colditz, G.A., Brewer, T.F., Berkey, C.S., Wilson, M.E., Burdick, E., Fineberg, H.V., et al. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 271 (1994), 698–702, 10.1001/jama.1994.03510330076038.
13. [13] Gandhi, N.R.N.N.R., Nunn, P., Dheda, K., Schaaf, H.S., Zignol, M., van Soolingen, D., et al. Multidrug-resistant and extensively drug-resistant tuberculosis: a threat to global control of tuberculosis. Lancet 375 (2010), 1830–1843, 10.1016/S0140-6736(10)60410-2.
14. [14] Lee, W., VanderVen, B.C., Fahey, R.J., Russell, D.G., Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 288 (2013), 6788–6800, 10.1074/jbc.M112.445056.
15. [15] Lovewell, R.R., Sassetti, C.M., VanderVen, B.C., Chewing the fat: lipid metabolism and homeostasis during M. tuberculosis infection. Curr. Opin. Microbiol. 29 (2015), 30–36, 10.1016/j.mib.2015.10.002.
16. [16] Macrae, D.E., The use of calciferol in tuberculous conditions. Lancet 1 (1947), 135–136 http://bf4dv7zn3u.search.serialssolutions.com.myaccess.library.utoronto.ca/?url_ver=Z39.88-2004&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rfr_id=info:sid/Ovid:emcl1&rft.genre=article&rft_id=info:doi/&rft_id=info:pmid/&rft.issn=0140-6736&rft.volume=1&rft.is.
17. [17] Dowling, G.B., Gauvain, S., Macrae, D.E., Vitamin D in treatment of cutaneous tuberculosis. Br. Med. J. 1 (1948), 430–435 http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2090361&tool=pmcentrez&rendertype=abstract (accessed 12.01.16).
18. [18] Bornman, L., Campbell, S.J., Fielding, K., Bah, B., Sillah, J., Gustafson, P., et al. Vitamin D receptor polymorphisms and susceptibility to tuberculosis in West Africa: a case-control and family study. J. Infect. Dis. 190 (2004), 1631–1641 http://www.ncbi.nlm.nih.gov/pubmed/15478069\n http://jid.oxfordjournals.org/content/190/9/1631.full.pdf\n http://jid.oxfordjournals.org/content/190/9/1631.long.
19. [19] Mazein, A., Watterson, S., Hsieh, W.Y., Griffiths, W.J., Ghazal, P., A comprehensive machine-readable view of the mammalian cholesterol biosynthesis pathway. Biochem. Pharmacol. 86 (2013), 56–66, 10.1016/j.bcp.2013.03.021.
20. [20] Le Novère, N., Hucka, M., Mi, H., Moodie, S., Schreiber, F., Sorokin, A., et al. The systems biology graphical notation. Nat. Biotechnol. 27 (2009), 735–741.
21. [21] Gold, E.S., Diercks, A.H., Podolsky, I., Podyminogin, R.L., Askovich, P.S., Treuting, P.M., et al. 25-Hydroxycholesterol acts as an amplifier of inflammatory signaling. Proc. Natl. Acad. Sci. U. S. A., 6, 2014, 10.1073/pnas.1404271111.
22. [22] Reboldi, A., Dang, E.V., McDonald, J.G., Liang, G., Russell, D.W., Cyster, J.G., 25-Hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon. Science 345 (2014), 679–684 http://www.sciencemag.org/cgi/doi/10.1126/science.1254790.
23. [23] Yi, T., Wang, X., Kelly, L.M., An, J., Xu, Y., Sailer, A.W., et al. Oxysterol gradient generation by lymphoid stromal cells guides activated B cell movement during humoral responses. Immunity 37 (2012), 535–548.
24. [24] Honda, A., Miyazaki, T., Ikegami, T., Iwamoto, J., Maeda, T., Hirayama, T., et al. Cholesterol 25-hydroxylation activity of CYP3A. J. Lipid Res. 52 (2011), 1509–1516.
25. [25] Russell, D.W., Oxysterol biosynthetic enzymes. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1529 (2000), 126–135.
26. [26] Prosser, D.E., Jones, G., Enzymes involved in the activation and inactivation of vitamin D. Trends Biochem. Sci. 29 (2004), 664–673.
27. [27] Cheng, J.B., Levine, M.A., Bell, N.H., Mangelsdorf, D.J., Russell, D.W., Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 7711–7715.
28. [28] Bauman, D.R., Bitmansour, A.D., McDonald, J.G., Thompson, B.M., Liang, G., Russell, D.W., 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16764–16769, 10.1073/pnas.0909142106.
29. [29] Diczfalusy, U., Olofsson, K.E., Carlsson, A.-M., Gong, M., Golenbock, D.T., Rooyackers, O., et al. Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide. J. Lipid Res. 50 (2009), 2258–2264, 10.1194/jlr.M900107-JLR200.
30. [30] Park, K., Scott, A.L., Cholesterol 25-hydroxylase production by dendritic cells and macrophages is regulated by type I interferons. J. Leukoc. Biol. 88 (2010), 1081–1087, 10.1189/jlb.0610318.
31. [31] Gold, E.S., Ramsey, S.A., Sartain, M.J., Selinummi, J., Podolsky, I., Rodriguez, D.J., et al. ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation. J. Exp. Med. 209 (2012), 807–817 http://www.ncbi.nlm.nih.gov/pubmed/22473958.
32. [32] Lu, H., Talbot, S., Robertson, K.A., Watterson, S., Forster, T., Roy, D., et al. Rapid proteasomal elimination of 3-hydroxy-3-methylglutaryl-CoA reductase by interferon-gamma in primary macrophages requires endogenous 25-hydroxycholesterol synthesis. Steroids, 2015, 10.1016/j.steroids.2015.02.022.
33. [33] Van Etten, E., Mathieu, C., Immunoregulation by 1,25-dihydroxyvitamin D3: basic concepts. J. Steroid Biochem. Mol. Biol., 2005, 93–101.
34. [34] Stoffels, K., Overbergh, L., Giulietti, A., Verlinden, L., Bouillon, R., Mathieu, C., Immune regulation of 25-hydroxyvitamin-D3-1alpha-hydroxylase in human monocytes. J. Bone Miner. Res. 21 (2006), 37–47.
35. [35] Edfeldt, K., Liu, P.T., Chun, R., Fabri, M., Schenk, M., Wheelwright, M., et al. T-cell cytokines differentially control human monocyte antimicrobial responses by regulating vitamin D metabolism. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 22593–22598.
36. [37] York, A.G., Williams, K.J., Argus, J.P., Zhou, Q.D., Brar, G., Vergnes, L., et al. Limiting cholesterol biosynthetic flux spontaneously engages type i IFN signaling. Cell 163 (2015), 1716–1729.
37. [38] Hannedouche, S., Zhang, J., Yi, T., Shen, W., Nguyen, D., Pereira, J.P., et al. Oxysterols direct immune cell migration via EBI2. Nature 475 (2011), 524–527.
38. [39] Kelly, L.M., Pereira, J.P., Yi, T., Xu, Y., Cyster, J.G., EBI2 guides serial movements of activated B cells and ligand activity is detectable in lymphoid and nonlymphoid tissues. J. Immunol. 187 (2011), 3026–3032.
39. [40] Chalmin, F., Rochemont, V., Lippens, C., Clottu, A., Sailer, A.W., Merkler, D., et al. Oxysterols regulate encephalitogenic CD4+ T cell trafficking during central nervous system autoimmunity. J. Autoimmun. 56 (2015), 45–55.
40. [41] Janowski, B.A., Willy, P.J., Devi, T.R., Falck, J.R., Mangelsdorf, D.J., An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383 (1996), 728–731, 10.1038/383728a0.
41. [42] Ito, A., Hong, C., Rong, X., Zhu, X., Tarling, E.J., Hedde, P.N., et al. LXRs link metabolism to inflammation through Abca1-dependent regulation of membrane composition and TLR signaling. Elife, 4, 2015.
42. [43] Karlic, H., Varga, F., Impact of vitamin D metabolism on clinical epigenetics. Clin. Epigenet. 2 (2011), 55–61.
43. [44] Takeuchi, A., Reddy, G.S., Kobayashi, T., Okano, T., Park, J., Sharma, S., Nuclear factor of activated T cells (NFAT) as a molecular target for 1alpha,25-dihydroxyvitamin D3-mediated effects. J. Immunol. 160 (1998), 209–218.
44. [45] Bar-Shavit, Z., Teitelbaum, S.L., Reitsma, P., Hall, A., Pegg, L.E., Trial, J., et al. Induction of monocytic differentiation and bone resorption by 1,25-dihydroxyvitamin D3. Proc. Natl. Acad. Sci. U. S. A. 80 (1983), 5907–5911.
45. [46] Rigby, W.F., Shen, L., Ball, E.D., Guyre, P.M., Fanger, M.W., Differentiation of a human monocytic cell line by 1,25-dihydroxyvitamin D3 (calcitriol): a morphologic, phenotypic, and functional analysis. Blood 64 (1984), 1110–1115.
46. [47] Xu, H., Soruri, A., Gieseler, R.K.H., Peters, J.H., 1,25-Dihydroxyvitamin D3 exerts opposing effects to IL-4 on MHC class-II antigen expression, accessory activity, and phagocytosis of human monocytes. Scand. J. Immunol. 38 (1993), 535–540.
47. [48] Kassebaum, N.J., Bertozzi-Villa, A., Coggeshall, M.S., Shackelford, K.A., Steiner, C., Heuton, K.R., et al. Global, regional, and national levels and causes of maternal mortality during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 6736 (2014), 1–25, 10.1016/S0140-6736(14)60696-6.
48. [49] Oberg, F., Botling, J., Nilsson, K., Functional antagonism between vitamin D3 and retinoic acid in the regulation of CD14 and CD23 expression during monocytic differentiation of U-937 cells. J. Immunol. 150 (1993), 3487–3495.
49. [50] Wang, T.-T., Tavera-Mendoza, L.E., Laperriere, D., Libby, E., MacLeod, N.B., Nagai, Y., et al. Large-scale in silico and microarray-based identification of direct 1,25-dihydroxyvitamin D3 target genes. Mol. Endocrinol. 19 (2005), 2685–2695.
50. [51] Wang, T.-T., Nestel, F.P., Bourdeau, V., Nagai, Y., Wang, Q., Liao, J., et al. Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J. Immunol. 173 (2004), 2909–2912.
51. [52] Gombart, A.F., Borregaard, N., Koeffler, H.P., Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J. 19 (2005), 1067–1077.
52. [53] Liu, P.T., Stenger, S., Li, H., Wenzel, L., Tan, B.H., Krutzik, S.R., et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311 (2006), 1770–1773.
53. [54] Lowry, M.B., Guo, C., Borregaard, N., Gombart, A.F., Regulation of the human cathelicidin antimicrobial peptide gene by 1α,25-dihydroxyvitamin D3 in primary immune cells. J. Steroid Biochem. Mol. Biol. 143C (2014), 183–191 http://www.ncbi.nlm.nih.gov/pubmed/24565560.
54. [55] Sow, F.B., Florence, W.C., Satoskar, A.R., Schlesinger, L.S., Zwilling, B.S., Lafuse, W.P., Expression and localization of hepcidin in macrophages: a role in host defense against tuberculosis. J. Leukoc. Biol. 82 (2007), 934–945.
55. [56] Bacchetta, J., Zaritsky, J.J., Sea, J.L., Chun, R.F., Lisse, T.S., Zavala, K., et al. Suppression of iron-regulatory hepcidin by vitamin D. J. Am. Soc. Nephrol., 2013, 1–9 http://www.ncbi.nlm.nih.gov/pubmed/24204002.
56. [57] Cohen-Lahav, M., Shany, S., Tobvin, D., Chaimovitz, C., Douvdevani, A., Vitamin D decreases NFkappaB activity by increasing IkappaBalpha levels. Nephrol. Dial. Transplant. 21 (2006), 889–897, 10.1093/ndt/gfi254.
57. [58] Matilainen, J.M., Räsänen, A., Gynther, P., Väisänen, S., The genes encoding cytokines IL-2 IL-10 and IL-12B are primary 1α,25(OH)2D3 target genes. J. Steroid Biochem. Mol. Biol. 121 (2010), 142–145.
58. [59] Adorini, L., Penna, G., Dendritic cell tolerogenicity in immunomodulation by vitamin D receptor agonists. Hum. Immunol., 2009, 10.1016/j.humimm.2009.01.016 S0198-8859(09)00021-4 [pii].
59. [60] Cippitelli, M., Santoni, A., Vitamin D3: a transcriptional modulator of the interferon-gamma gene. Eur. J. Immunol. 28 (1998), 3017–3030, 10.1002/(SICI)1521-4141(199810)28:10<3017:AID-IMMU3017>3.0.CO;2-6.
60. [61] Baeke, F., Korf, H., Overbergh, L., van Etten, E., Verstuyf, A., Gysemans, C., et al. Human T lymphocytes are direct targets of 1,25-dihydroxyvitamin D3 in the immune system. J. Steroid Biochem. Mol. Biol. 121 (2010), 221–227.
61. [62] Boonstra, A., Barrat, F.J., Crain, C., Heath, V.L., Savelkoul, H.F., O'Garra, A., 1alpha,25-Dihydroxyvitamin d3 has a direct effect on naive CD4(+) T cells to enhance the development of Th2 cells. J. Immunol. 167 (2001), 4974–4980 http://www.ncbi.nlm.nih.gov/pubmed/11673504.
62. [63] D'Ambrosio, D., Cippitelli, M., Cocciolo, M.G., Mazzeo, D., Di Lucia, P., Lang, R., et al. Inhibition of IL-12 production by 1,25-dihydroxyvitamin D3. Involvement of NF-κB downregulation in transcriptional repression of the p40 gene. J. Clin. Investig. 101 (1998), 252–262.
63. [64] Ferrara, G., Bleck, B., Richeldi, L., Reibman, J., Fabbri, L.M., Rom, W.N., et al. Mycobacterium tuberculosis induces CCL18 expression in human macrophages. Scand. J. Immunol. 68 (2008), 668–674.
64. [65] Nguyen, L., Pieters, J., The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages. Trends Cell Biol. 15 (2005), 269–276.
65. [66] Yang, Z., Kong, Y., Wilson, F., Foxman, B., Fowler, A.H., Marrs, C.F., et al. Identification of risk factors for extrapulmonary tuberculosis. Clin. Infect. Dis. 38 (2004), 199–205, 10.1086/380644.
66. [67] Sharma, S.K., Mohan, A., Sharma, A., Mitra, D.K., Miliary tuberculosis: new insights into an old disease. Lancet Infect. Dis. 5 (2005), 415–430, 10.1016/S1473-3099(05)70163-8.
67. [68] Harding, C.V., Boom, W.H., Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat. Rev. Microbiol. 8 (2010), 296–307.
68. [69] Bean, A.G., Roach, D.R., Briscoe, H., France, M.P., Korner, H., Sedgwick, J.D., et al. 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 (1999), 3504–3511, 10.4049/jimmunol.173.6.4066.
69. [70] Bonecini-Almeida, M.G., Ho, J.L., Boéchat, N., Huard, R.C., Chitale, S., Doo, H., et al. Down-modulation of lung immune responses by interleukin-10 and transforming growth factor beta (TGF-beta) and analysis of TGF-beta receptors I and II in active tuberculosis. Infect. Immun. 72 (2004), 2628–2634, 10.1128/IAI.72.5.2628.
70. [71] Peyron, P., Vaubourgeix, J., Poquet, Y., Levillain, F., Botanch, C., Bardou, F., et al. Foamy macrophages from tuberculous patients’ granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog., 4, 2008.
71. [72] Cole, S.T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 (1998), 537–544.
72. [73] Nesbitt, N.M., Yang, X., Fontán, P., Kolesnikova, I., Smith, I., Sampson, N.S., et al. A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect. Immun. 78 (2010), 275–282, 10.1128/IAI.00893-09.
73. [74] Griffin, J.E., Gawronski, J.D., DeJesus, M.A., Ioerger, T.R., Akerley, B.J., Sassetti, C.M., High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog., 7, 2011.
74. [75] Pandey, A.K., Sassetti, C.M., Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 4376–4380.
75. [76] Joshi, S.M., Pandey, A.K., Capite, N., Fortune, S.M., Rubin, E.J., Sassetti, C.M., Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 11760–11765.
76. [77] Yang, X., Dubnau, E., Smith, I., Sampson, N.S., Rv1106c from Mycobacterium tuberculosis is a 3beta-hydroxysteroid dehydrogenase. Biochemistry 46 (2007), 9058–9067.
77. [78] Brzostek, A., Pawelczyk, J., Rumijowska-Galewicz, A., Dziadek, B., Dziadek, J., Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J. Bacteriol. 191 (2009), 6584–6591, 10.1128/JB.00488-09.
78. [79] Capyk, J.K., D'Angelo, I., Strynadka, N.C., Eltis, L.D., Characterization of 3-ketosteroid 9beta-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J. Biol. Chem. 284 (2009), 9937–9946.
79. [80] Astarie-Dequeker, C., Le Guyader, L., Malaga, W., Seaphanh, F.K., Chalut, C., Lopez, A., et al. Phthiocerol dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog., 5, 2009.
80. [81] Capyk, J.K., Kalscheuer, R., Stewart, G.R., Liu, J., Kwon, H., Zhao, R., et al. Mycobacterial cytochrome P450 125 (Cyp125) catalyzes the terminal hydroxylation of C27 steroids. J. Biol. Chem. 284 (2009), 35534–35542.
81. [82] Chang, J.C., Harik, N.S., Liao, R.P., Sherman, D.R., Identification of Mycobacterial genes that alter growth and pathology in macrophages and in mice. J. Infect. Dis. 196 (2007), 788–795.
82. [83] Slayden, R.A., Lee, R.E., Barry, C.E., Isoniazid affects multiple components of the type II fatty acid synthase system of Mycobacterium tuberculosis. Mol. Microbiol. 38 (2000), 514–525.
83. [84] Rawat, R., Whitty, A., Tonge, P.J., The isoniazid-NAD adduct is a slow, tight-binding inhibitor of InhA, the Mycobacterium tuberculosis enoyl reductase: adduct affinity and drug resistance. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 13881–13886.
84. [85] Gande, R., Gibson, K.J.C., Brown, A.K., Krumbach, K., Dover, L.G., Sahm, H., et al. Acyl-CoA carboxylases (accD2 and accD3), together with a unique polyketide synthase (Cg-pks), are key to mycolic acid biosynthesis in Corynebacterianeae such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J. Biol. Chem. 279 (2004), 44847–44857, 10.1074/jbc.M408648200.
85. [86] Parihar, S.P., Guler, R., Khutlang, R., Lang, D.M., Hurdayal, R., Mhlanga, M.M., et al. Statin therapy reduces the Mycobacterium tuberculosis burden in human macrophages and in mice by enhancing autophagy and phagosome maturation. J. Infect. Dis. 209 (2014), 754–763.
86. [87] Lobato, L.S., Rosa, P.S., Ferreira, J.D.S., Neumann, A.D.S., Da Silva, M.G., Do Nascimento, D.C., et al. Statins increase rifampin mycobactericidal effect. Antimicrob. Agents Chemother. 58 (2014), 5766–5774, 10.1128/AAC.01826-13.
87. [88] Salamon, H., Bruiners, N., Lakehal, K., Shi, L., Ravi, J., Yamaguchi, K.D., et al. Cutting edge: vitamin D regulates lipid metabolism in Mycobacterium tuberculosis infection. J. Immunol. 193 (2014), 30–34 http://www.ncbi.nlm.nih.gov/pubmed/24899504.
88. [89] Ferrari, G., Langen, H., Naito, M., Pieters, J., A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97 (1999), 435–447.
89. [90] Anand, P.K., Kaul, D., Sharma, M., Synergistic action of vitamin D and retinoic acid restricts invasion of macrophages by pathogenic mycobacteria. J. Microbiol. Immunol. Infect. 41 (2008), 17–25.