Chewing the fat: Lipid metabolism and homeostasis during M. tuberculosis infection

Current Opinion in Microbiology

Volumn 29, Issue , 2016, Pages 30-36

  Lovewell, Rustin R ^a   Sassetti, Christopher M ^a,b   VanderVen, Brian C ^c  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; FATTY ACID; LIPID; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; MYCOLIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOLIPID; POLYKETIDE; POLYKETIDE SYNTHASE; TREHALOSE; FAT DROPLET;

BACTERIAL METABOLISM; CHOLESTEROL METABOLISM; FATTY ACID METABOLISM; FOAM CELL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNITY; LIPID HOMEOSTASIS; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; MACROPHAGE; NONHUMAN; REVIEW; TUBERCULOSIS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; MICROBIOLOGY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; FATTY ACIDS; FOAM CELLS; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPID DROPLETS; LIPID METABOLISM; MACROPHAGES; METABOLIC NETWORKS AND PATHWAYS; MICE; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84946098498     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2015.10.002     Document Type: Review

References (73)

1. Bloch H., Segal W. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 1956, 72:132-141.
2. McKinney J.D., zu Bentrup K.H., Munoz-Elias E.J., Miczak A., Chen B., Chan W.-T., Swenson D., Sacchettini J.C., Jacobs W.R., Russell D.G. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000, 406:735-738.
3. Pandey A.K., Sassetti C.M. Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci 2008, 105:4376-4380.
4. Schnappinger D., Ehrt S., Voskuil M.I., Liu Y., Mangan J.A., Monahan I.M., Dolganov G., Efron B., Butcher P.D., Nathan C., et al. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 2003, 198:693-704.
5. Van der Geize R., Yam K., Heuser T., Wilbrink M.H., Hara H., Anderton M.C., Sim E., Dijkhuizen L., Davies J.E., Mohn W.W., et al. A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci 2007, 104:1947-1952.
6. Daniel J., Maamar H., Deb C., Sirakova T.D., Kolattukudy P.E. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 2011, 7:e1002093.
7. Trivedi O.A., Arora P., Sridharan V., Tickoo R., Mohanty D., Gokhale R.S. Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 2004, 428:441-445.
8. Quadri L.E. Biosynthesis of mycobacterial lipids by polyketide synthases and beyond. Crit Rev Biochem Mol Biol 2014, 49:179-211.
9. Marrakchi H., Laneelle M.A., Daffe M. Mycolic acids: structures, biosynthesis, and beyond. Chem Biol 2014, 21:67-85.
10. Odriozola J.M., Ramos J.A., Bloch K. Fatty acid synthetase activity in Mycobacterium smegmatis. Characterization of the acyl carrier protein-dependent elongating system. Biochim Biophys Acta 1977, 488:207-217.
11. Portevin D., De Sousa-D'Auria C., Houssin C., Grimaldi C., Chami M., Daffe M., Guilhot C. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci U S A 2004, 101:314-319.
12. Daniel J., Deb C., Dubey V.S., Sirakova T.D., Abomoelak B., Morbidoni H.R., Kolattukudy P.E. Induction of a novel class of diacylglycerol acyltransferases and triacylglycerol accumulation in Mycobacterium tuberculosis as it goes into a dormancy-like state in culture. J Bacteriol 2004, 186:5017-5030.
13. Baek S.H., Li A.H., Sassetti C.M. Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol 2011, 9:e1001065.
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 2013, 288:6788-6800.
15. Singh A., Crossman D.K., Mai D., Guidry L., Voskuil M.I., Renfrow M.B., Steyn A.J. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 2009, 5:e1000545.
16. 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 2007, 196:788-795.
17. Hu Y., van der Geize R., Besra G.S., Gurcha S.S., Liu A., Rohde M., Singh M., Coates A. 3-Ketosteroid 9alpha-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis. Mol Microbiol 2010, 75:107-121.
18. Nesbitt N.M., Yang X., Fontan P., Kolesnikova I., Smith I., Sampson N.S., Dubnau E. A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect Immun 2010, 78:275-282.
19. VanderVen B.C., Fahey R.J., Lee W., Liu Y., Abramovitch R.B., Memmott C., Crowe A.M., Eltis L.D., Perola E., Deininger D.D., et al. Novel inhibitors of cholesterol degradation in Mycobacterium tuberculosis reveal how the bacterium's metabolism is constrained by the intracellular environment. PLoS Pathog 2015, 11:e1004679.
20. Yam K.C., D'Angelo I., Kalscheuer R., Zhu H., Wang J.X., Snieckus V., Ly L.H., Converse P.J., Jacobs W.R., Strynadka N., et al. Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS Pathog 2009, 5:e1000344.
21. Wipperman M.F., Sampson N.S., Thomas S.T. Pathogen roid rage: cholesterol utilization by Mycobacterium tuberculosis. Crit Rev Biochem Mol Biol 2014, 49:269-293.
22. Yam K.C., Okamoto S., Roberts J.N., Eltis L.D. Adventures in Rhodococcus-from steroids to explosives. Can J Microbiol 2011, 57:155-168.
23. Capyk J.K., Casabon I., Gruninger R., Strynadka N.C., Eltis L.D. Activity of 3-ketosteroid 9alpha-hydroxylase (KshAB) indicates cholesterol side chain and ring degradation occur simultaneously in Mycobacterium tuberculosis. J Biol Chem 2011, 286:40717-40724.
24. Capyk J.K., D'Angelo I., Strynadka N.C., Eltis L.D. Characterization of 3-ketosteroid 9{alpha}-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J Biol Chem 2009, 284:9937-9946.
25. Capyk J.K., Kalscheuer R., Stewart G.R., Liu J., Kwon H., Zhao R., Okamoto S., Jacobs W.R., Eltis L.D., Mohn W.W. Mycobacterial cytochrome p450 125 (cyp125) catalyzes the terminal hydroxylation of c27 steroids. J Biol Chem 2009, 284:35534-35542.
26. Casabon I., Crowe A.M., Liu J., Eltis L.D. FadD3 is an acyl-CoA synthetase that initiates catabolism of cholesterol rings C and D in actinobacteria. Mol Microbiol 2013, 87:269-283.
27. Casabon I., Swain K., Crowe A.M., Eltis L.D., Mohn W.W. Actinobacterial acyl coenzyme A synthetases involved in steroid side-chain catabolism. J Bacteriol 2014, 196:579-587.
28. Casabon I., Zhu S.H., Otani H., Liu J., Mohn W.W., Eltis L.D. Regulation of the KstR2 regulon of Mycobacterium tuberculosis by a cholesterol catabolite. Mol Microbiol 2013, 89:1201-1212.
29. Dresen C., Lin L.Y., D'Angelo I., Tocheva E.I., Strynadka N., Eltis L.D. A flavin-dependent monooxygenase from Mycobacterium tuberculosis involved in cholesterol catabolism. J Biol Chem 2010, 285:22264-22275.
30. Driscoll M.D., McLean K.J., Levy C., Mast N., Pikuleva I.A., Lafite P., Rigby S.E., Leys D., Munro A.W. Structural and biochemical characterization of Mycobacterium tuberculosis CYP142: evidence for multiple cholesterol 27-hydroxylase activities in a human pathogen. J Biol Chem 2010, 285:38270-38282.
31. Frank D.J., Madrona Y., Ortiz de Montellano P.R. Cholesterol ester oxidation by mycobacterial cytochrome P450. J Biol Chem 2014, 289:30417-30425.
32. 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 2011, 7.
33. Griffin J.E., Pandey A.K., Gilmore S.A., Mizrahi V., McKinney J.D., Bertozzi C.R., Sassetti C.M. Cholesterol catabolism by Mycobacterium tuberculosis requires transcriptional and metabolic adaptations. Chem Biol 2012, 19:218-227.
34. Lack N.A., Yam K.C., Lowe E.D., Horsman G.P., Owen R.L., Sim E., Eltis L.D. Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J Biol Chem 2010, 285:434-443.
35. Ouellet H., Guan S., Johnston J.B., Chow E.D., Kells P.M., Burlingame A.L., Cox J.S., Podust L.M., De Montellano P.R.O. Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol Microbiol 2010, 77:730-742.
36. Thomas S.T., VanderVen B.C., Sherman D.R., Russell D.G., Sampson N.S. Pathway Profiling in Mycobacterium tuberculosis: elucidation of a cholesterol-derived catabolite and the enzymes that catalyze its metabolism. J Biol Chem 2011, 286:43668-43678.
37. Yang X., Nesbitt N.M., Dubnau E., Smith I., Sampson N.S. Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis. Biochemistry 2009, 48:3819-3821.
38. Kim M.J., Wainwright H.C., Locketz M., Bekker L.G., Walther G.B., Dittrich C., Visser A., Wang W., Hsu F.F., Wiehart U., et al. Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2010, 2:258-274.
39. Peyron P., Vaubourgeix J., Poquet Y., Levillain F., Botanch C., Bardou F., Daffe M., Emile J.F., Marchou B., Cardona P.J., et al. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 2008, 4:e1000204.
40. Graham A., Allen A.M. Mitochondrial function and regulation of macrophage sterol metabolism and inflammatory responses. World J Cardiol 2015, 7:277-286.
41. Philips J.A., Rubin E.J., Perrimon N. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 2005, 309:1251-1253.
42. Orme I.M., Basaraba R.J. The formation of the granuloma in tuberculosis infection. Semin Immunol 2014, 26:601-609.
43. Gouzy A., Larrouy-Maumus G., Wu T.D., Peixoto A., Levillain F., Lugo-Villarino G., Guerquin-Kern J.L., de Carvalho L.P., Poquet Y., Neyrolles O. Mycobacterium tuberculosis nitrogen assimilation and host colonization require aspartate. Nat Chem Biol 2013, 9:674-676.
44. Marrero J., Trujillo C., Rhee K.Y., Ehrt S. Glucose phosphorylation is required for Mycobacterium tuberculosis persistence in mice. PLoS Pathog 2013, 9:e1003116.
45. Puckett S., Trujillo C., Eoh H., Marrero J., Spencer J., Jackson M., Schnappinger D., Rhee K., Ehrt S. Inactivation of fructose-1,6-bisphosphate aldolase prevents optimal co-catabolism of glycolytic and gluconeogenic carbon substrates in Mycobacterium tuberculosis. PLoS Pathog 2014, 10:e1004144.
46. Speer A., Sun J., Danilchanka O., Meikle V., Rowland J.L., Walter K., Buck B.R., Pavlenok M., Holscher C., Ehrt S., et al. Surface hydrolysis of sphingomyelin by the outer membrane protein Rv0888 supports replication of Mycobacterium tuberculosis in macrophages. Mol Microbiol 2015, 97:881-897.
47. Trujillo C., Blumenthal A., Marrero J., Rhee K.Y., Schnappinger D., Ehrt S. Triosephosphate isomerase is dispensable in vitro yet essential for Mycobacterium tuberculosis to establish infection. MBio 2014, 5:e00085.
48. Russell D.G., Cardona P.-J., Kim M.-J., Allain S., Altare F. Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 2009, 10:943-948.
49. Saka H.A., Valdivia R. Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu Rev Cell Dev Biol 2012, 28:411-437.
50. Bensinger S.J., Tontonoz P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 2008, 454:470-477.
51. Almeida P.E., Silva A.R., Maya-Monteiro C.M., Torocsik D., D'Avila H., Dezso B., Magalhaes K.G., Castro-Faria-Neto H.C., Nagy L., Bozza P.T. Mycobacterium bovis bacillus Calmette-Guerin infection induces TLR2-dependent peroxisome proliferator-activated receptor gamma expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J Immunol 2009, 183:1337-1345.
52. Almeida P.E., Carneiro A.B., Silva A.R., Bozza P.T. PPARgamma expression and function in mycobacterial infection: roles in lipid metabolism, immunity, and bacterial killing. PPAR Res 2012, 2012:383829.
53. Rajaram M.V., Brooks M.N., Morris J.D., Torrelles J.B., Azad A.K., Schlesinger L.S. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J Immunol 2010, 185:929-942.
54. Eisele N.A., Ruby T., Jacobson A., Manzanillo P.S., Cox J.S., Lam L., Mukundan L., Chawla A., Monack D.M. Salmonella require the fatty acid regulator PPARdelta for the establishment of a metabolic environment essential for long-term persistence. Cell Host Microbe 2013, 14:171-182.
55. Xavier M.N., Winter M.G., Spees A.M., den Hartigh A.B., Nguyen K., Roux C.M., Silva T.M., Atluri V.L., Kerrinnes T., Keestra A.M., et al. PPARgamma-mediated increase in glucose availability sustains chronic Brucella abortus infection in alternatively activated macrophages. Cell Host Microbe 2013, 14:159-170.
56. Salamon H., Bruiners N., Lakehal K., Shi L., Ravi J., Yamaguchi K.D., Pine R., Gennaro M.L. Cutting edge: vitamin D regulates lipid metabolism in Mycobacterium tuberculosis infection. J Immunol 2014, 193:30-34.
57. Mahajan S., Dkhar H.K., Chandra V., Dave S., Nanduri R., Janmeja A.K., Agrewala J.N., Gupta P. Mycobacterium tuberculosis modulates macrophage lipid-sensing nuclear receptors PPARgamma and TR4 for survival. J Immunol 2012, 188:5593-5603.
58. Singh V., Jamwal S., Jain R., Verma P., Gokhale R., Rao K.V. Mycobacterium tuberculosis-driven targeted recalibration of macrophage lipid homeostasis promotes the foamy phenotype. Cell Host Microbe 2012, 12:669-681.
59. Martens G.W., Arikan M.C., Lee J., Ren F., Vallerskog T., Kornfeld H. Hypercholesterolemia impairs immunity to tuberculosis. Infect Immun 2008, 76:3464-3472.
60. Martens G.W., Vallerskog T., Kornfeld H. Hypercholesterolemic LDL receptor-deficient mice mount a neutrophilic response to tuberculosis despite the timely expression of protective immunity. J Leukoc Biol 2012, 91:849-857.
61. Han M., Liang L., Liu L.R., Yue J., Zhao Y.L., Xiao H.P. Liver X receptor gene polymorphisms in tuberculosis: effect on susceptibility. PLoS One 2014, 9:e95954.
62. Korf H., Vander Beken S., Romano M., Steffensen K.R., Stijlemans B., Gustafsson J.A., Grooten J., Huygen K. Liver X receptors contribute to the protective immune response against Mycobacterium tuberculosis in mice. J Clin Invest 2009, 119:1626-1637.
63. Russell D.G., VanderVen B.C., Lee W., Abramovitch R.B., Kim M.-J., Homolka S., Niemann S., Rohde K.H. Mycobacterium tuberculosis wears what it eats. Cell Host Microbe 2010, 8:68-76.
64. Singh R., Kaushik S., Wang Y., Xiang Y., Novak I., Komatsu M., Tanaka K., Cuervo A.M., Czaja M.J. Autophagy regulates lipid metabolism. Nature 2009, 458:1131-1135.
65. Gutierrez M.G., Master S.S., Singh S.B., Taylor G.A., Colombo M.I., Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004, 119:753-766.
66. Shin D.M., Jeon B.Y., Lee H.M., Jin H.S., Yuk J.M., Song C.H., Lee S.H., Lee Z.W., Cho S.N., Kim J.M., et al. Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 2010, 6:e1001230.
67. Sandhu G.K. Tuberculosis: current situation, challenges and overview of its control programs in India. J Glob Infect Dis 2011, 3:143-150.
68. Eoh H., Rhee K.Y. Methylcitrate cycle defines the bactericidal essentiality of isocitrate lyase for survival of Mycobacterium tuberculosis on fatty acids. Proc Natl Acad Sci U S A 2014, 111:4976-4981.
69. Savvi S., Warner D.F., Kana B.D., McKinney J.D., Mizrahi V., Dawes S.S. Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J Bacteriol 2008, 190:3886-3895.
70. Upton A.M., McKinney J.D. Role of the methylcitrate cycle in propionate metabolism and detoxification in Mycobacterium smegmatis. Microbiology 2007, 153:3973-3982.
71. Parihar S.P., Guler R., Khutlang R., Lang D.M., Hurdayal R., Mhlanga M.M., Suzuki H., Marais A.D., Brombacher F. Statin therapy reduces the Mycobacterium tuberculosis burden in human macrophages and in mice by enhancing autophagy and phagosome maturation. J Infect Dis 2014, 209:754-763.
72. Kang Y.A., Choi N.K., Seong J.M., Heo E.Y., Koo B.K., Hwang S.S., Park B.J., Yim J.J., Lee C.H. The effects of statin use on the development of tuberculosis among patients with diabetes mellitus. Int J Tuberc Lung Dis 2014, 18:717-724.
73. Lobato L.S., Rosa P.S., Ferreira Jda S., Neumann Ada S., da Silva M.G., do Nascimento D.C., Soares C.T., Pedrini S.C., Oliveira D.S., Monteiro C.P., et al. Statins increase rifampin mycobactericidal effect. Antimicrob Agents Chemother 2014, 58:5766-5774.