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Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids pp 1–24Cite as

Mycobacterial Lipid Bodies and the Chemosensitivity and Transmission of Tuberculosis

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Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

Just over a quarter of humanity is infected with the tubercle bacillus and risks developing active disease that routinely requires 6-month treatment. The impact of this scourge cannot be underestimated, and reducing the global burden of tuberculosis is the focus of much research. In addition to the need for improved chemotherapy regimens and monitoring thereof, understanding the risk and processes involved in transmission, a critical step in the life cycle of the organism, has even greater potential to impact the burden of disease. Our chance observation that lipid bodies (LBs) were present in Mycobacterium tuberculosis in sputum, but not in growing cultures of the lab strain in vitro, led us and others to examine this phenomenon further. Transcriptional analysis of the bacilli in sputum identified that upregulation of tgs1, a triacylglycerol synthase, was likely responsible for the presence of these LBs. Strikingly, in contrast to the then established view that tubercle bacilli in sputum arose directly from rapidly replicating populations, further transcriptional and cytological analyses led us to link the M. tuberculosis sputum phenotype to slow or non-growing persisters. As a result, we and others have directed research to further understanding the biological and clinical significance of LBs and neutral lipids in mycobacteria. There is now greater insight into the biosynthetic pathways and role of neutral lipids during infection, for both growing and dormant M. tuberculosis. Links have been made between tgs1-related triacylglycerol LB accumulation and growth arrest and with antibiotic tolerance potentially underpinning the need for protracted chemotherapy. The possible clinical significance of this is reflected in the finding that sustained high frequencies of LB-positive M. tuberculosis in sputum during treatment are associated with unsatisfactory outcomes. LB-positivity may also support transmission of the organism. Greater understanding of the significance of this “fat and lazy” population will open up new approaches to the combat of this long-standing foe.

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Abbreviations

ACSL:

Long-chain acyl-CoA synthase

DAG:

Diacylglycerol

DC:

Differentially culturable

DGAT:

Diacylglycerol acyl transferase

FACS:

Fatty acyl CoA synthase

FCR:

Fatty acyl long-chain CoA reductase

ILI:

Intracellular lipophilic inclusion

LB:

Lipid body

LCFA:

Long-chain fatty acid

LD:

Lipid droplet

NO:

Nitric oxide

PBMC:

Peripheral blood mononuclear cell

RIF:

Rifampicin

TAG:

Triacylglycerol

TB:

Tuberculosis

TCA:

Tricarboxylic acid

TGS:

Triacylglycerol synthase

THL:

Tetrahydrolipstatin

WE:

Wax ester

WS:

Wax ester synthase

References

  • Alvarez HM (2016) Triacylglycerol and wax ester-accumulating machinery in prokaryotes. Biochimie 120:28–39

    Article  CAS  PubMed  Google Scholar 

  • Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RM, Adams KL, Zilisch JE, Bretl DJ, Sato H, Anderson DM, Zahrt TC (2016) Rv2744c is a PspA Ortholog that regulates lipid droplet homeostasis and nonreplicating persistence in Mycobacterium tuberculosis. J Bacteriol 198:1645–1661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacon J, James BW, Wernisch L, Williams A, Morley KA, Hatch GJ, Mangan JA, Hinds J, Stoker NG, Butcher PD, Marsh PD (2004) The influence of reduced oxygen availability on pathogenicity and gene expression in Mycobacterium tuberculosis. Tuberculosis (Edinb) 84:205–217

    Article  Google Scholar 

  • Bacon J, Dover LG, Hatch KA, Zhang Y, Gomes JM, Kendall S, Wernisch L, Stoker NG, Butcher PD, Besra GS, Marsh PD (2007) Lipid composition and transcriptional response of Mycobacterium tuberculosis grown under iron-limitation in continuous culture: identification of a novel wax ester. Microbiology 153:1435–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baek SH, Li AH, Sassetti CM (2011) Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol 9:e1001065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barer MR, Garton NJ (2010) Mycobacterial lipid bodies and the chemosensitivity and transmission of tuberculosis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg

    Google Scholar 

  • Betts JC, Lukey PT , Robb LC, McAdam RA, Duncan K (2002) Evaluation of a nutrient starvation model of persistence by gene and protein expression profiling. Molecular Microbiology 43(3):717–731

    Article  CAS  PubMed  Google Scholar 

  • Burdon KL (1946) Disparity in appearance of true Hansen’s bacilli and cultured “leprosy bacilli” when stained for fat. J Bacteriol 52:679–680

    PubMed  PubMed Central  Google Scholar 

  • Christensen H, Garton NJ, Horobin RW, Minnikin DE, Barer MR (1999) Lipid domains of mycobacteria studied with fluorescent molecular probes. Mol Microbiol 31:1561–1572

    Article  CAS  PubMed  Google Scholar 

  • Daniel J, Deb C, Dubey VS, Sirakova TD, Abomoelak B, Morbidoni HR, Kolattukudy PE (2004) 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 186:5017–5030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daniel J, Maamar H, Deb C, Sirakova TD, Kolattukudy PE (2011) Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 7:e1002093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daniel J, Kapoor N, Sirakova T, Sinha R, Kolattukudy P (2016) The perilipin-like PPE15 protein in Mycobacterium tuberculosis is required for triacylglycerol accumulation under dormancy-inducing conditions. Mol Microbiol 101:784–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Datta S, Sherman JM, Tovar MA, Bravard MA, Valencia T, Montoya R, Quino W, D'Arcy N, Ramos ES, Gilman RH, Evans CE (2017) Sputum microscopy with fluorescein diacetate predicts tuberculosis infectiousness. J Infect Dis 216:514–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Deb C, Daniel J, Sirakova TD, Abomoelak B, Dubey VS, Kolattukudy PE (2006) A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J Biol Chem 281:3866–3875

    Article  CAS  PubMed  Google Scholar 

  • Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, Sirakova TD, Pawar S, Rogers L, Kolattukudy PE (2009) A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4:e6077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhouib R, Ducret A, Hubert P, Carriere F, Dukan S, Canaan S (2011) Watching intracellular lipolysis in mycobacteria using time lapse fluorescence microscopy. Biochim Biophys Acta 1811:234–241

    Article  CAS  PubMed  Google Scholar 

  • Domenech P, Zou J, Averback A, Syed N, Curtis D, Donato S, Reed MD (2017) Unique regulation of the DosR regulon in the Beijing lineage of Mycobacterium tuberculosis. J Bacteriol 199:e00696–e00716

    Article  CAS  PubMed  Google Scholar 

  • Elamin AA, Stehr M, Spallek R, Rohde M, Singh M (2011) The Mycobacterium tuberculosis Ag85A is a novel diacylglycerol acyltransferase involved in lipid body formation. Mol Microbiol 81:1577–1592

    Article  CAS  PubMed  Google Scholar 

  • Falkinham JO 3rd (2003) Mycobacterial aerosols and respiratory disease. Emerg Infect Dis 9:763–767

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia BJ, Loxton AG, Dolganov GM, Van TT, Davis JL, de Jong BC, Voskuil MI, Leach SM, Schoolnik GK, Walzl G, Strong M, Walter ND (2016) Sputum is a surrogate for bronchoalveolar lavage for monitoring Mycobacterium tuberculosis transcriptional profiles in TB patients. Tuberculosis (Edinb) 100:89–94

    Article  CAS  Google Scholar 

  • Garton NJ, Christensen H, Minnikin DE, Adegbola RA, Barer MR (2002) Intracellular lipophilic inclusions of mycobacteria in vitro and in sputum. Microbiology 148:2951–2958

    Article  CAS  PubMed  Google Scholar 

  • Garton NJ, Waddell SJ, Sherratt AL, Lee SM, Smith RJ, Senner C, Hinds J, Rajakumar K, Adegbola RA, Besra GS, Butcher PD, Barer MR (2008) Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med 5:e75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golby P, Nunez J, Cockle PJ, Ewer K, Logan K, Hogarth P, Vordermeier HM, Hinds J, Hewinson RG, Gordon SV (2008) Characterization of two in vivo-expressed methyltransferases of the Mycobacterium tuberculosis complex: antigenicity and genetic regulation. Microbiology 154:1059–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond RJ, Baron VO, Oravcova K, Lipworth SL, Gillespie SH (2015) Phenotypic resistance in mycobacteria: is it because I am old or fat that I resist you? J Antimicrob Chemother 70:2823–2827

    Article  CAS  PubMed  Google Scholar 

  • Hector J, Anderson ST, Banda G, Kamdolozi M, Jefferys LF, Shani D, Garton NJ, Mwale A, Jobe A, Davies GR, Sloan DJ (2017) TST positivity in household contacts of tuberculosis patients: a case-contact study in Malawi. BMC Infect Dis 17:259

    Article  PubMed  PubMed Central  Google Scholar 

  • Honeyborne I, McHugh TD, Kuittinen I, Cichonska A, Evangelopoulos D, Ronacher K, van Helden PD, Gillespie SH, Fernandez-Reyes D, Walzl G, Rousu J, Butcher PD, Waddell SJ (2016) Profiling persistent tubercle bacilli from patient sputa during therapy predicts early drug efficacy. BMC Med 14:68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishige T, Tani A, Takabe K, Kawasaki K, Sakai Y, Kato N (2002) Wax ester production from n-alkanes by Acinetobacter sp. strain M-1: ultrastructure of cellular inclusions and role of acyl coenzyme A reductase. Appl Environ Microbiol 68:1192–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalscheuer R, Steinbüchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA:diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J Biol Chem 278:8075–8082

    Article  CAS  PubMed  Google Scholar 

  • Kapoor N, Pawar S, Sirakova TD, Deb C, Warren WL, Kolattukudy PE (2013) Human granuloma in vitro model, for TB dormancy and resuscitation. PLoS One 8:e53657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayigire XA, Friedrich SO, van der Merwe L, Donald PR, Diacon AH (2015) Simultaneous staining of sputum smears for acid-fast and lipid-containing Myobacterium tuberculosis can enhance the clinical evaluation of antituberculosis treatments. Tuberculosis (Edinb) 95:770–779

    Article  CAS  Google Scholar 

  • Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Annu Rev Microbiol 47:855–874

    Article  CAS  PubMed  Google Scholar 

  • Kondo E, Kanai K (1977) The relationship between the chemical structure of fatty acids and their mycobactericidal activity. Jpn J Med Sci Biol 30:171–178

    Article  CAS  PubMed  Google Scholar 

  • Kussell E, Kishony R, Balaban NQ, Leibler S (2005) Bacterial persistence: a model of survival in changing environments. Genetics 169:1807–1814

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56

    Article  CAS  PubMed  Google Scholar 

  • Lovewell RR, Sassetti CM, VanderVen BC (2016) Chewing the fat: lipid metabolism and homeostasis during Mycobacterium tuberculosis infection. Curr Opin Microbiol 29:30–36

    Article  CAS  PubMed  Google Scholar 

  • Low KL, Rao PS, Shui G, Bendt AK, Pethe K, Dick T, Wenk MR (2009) Triacylglycerol utilization is required for regrowth of in vitro hypoxic nonreplicating Mycobacterium bovis bacillus Calmette-Guerin. J Bacteriol 191:5037–5043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Low KL, Shui G, Natter K, Yeo WK, Kohlwein SD, Dick T, Rao SP, Wenk MR (2010) Lipid droplet-associated proteins are involved in the biosynthesis and hydrolysis of triacylglycerol in Mycobacterium bovis bacillus Calmette-Guerin. J Biol Chem 285:21662–21670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacEachran DP, Prophete ME, Sinskey AJ (2010) The Rhodococcus opacus PD630 heparin-binding hemagglutinin homolog TadA mediates lipid body formation. Appl Environ Microbiol 76:7217–7225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinot AJ, Farrow M, Bai L, Layre E, Cheng TY, Tsai JH, Iqbal J, Annand JW, Sullivan ZA, Hussain MM, Sacchettini J, Moody DB, Seeliger JC, Rubin EJ (2016) Mycobacterial metabolic syndrome: LprG and Rv1410 regulate triacylglyceride levels, growth rate and virulence in Mycobacterium tuberculosis. PLoS Pathog 12:e1005351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKinney JD, Honer zu Bentrup K, Munoz-Elias EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR Jr, Russell DG (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735–738

    Article  CAS  PubMed  Google Scholar 

  • Minnikin DE (1982) Lipids: complex lipids, their chemistry, biosynthesis and roles. In: Ratledge C, Stanford J (eds) The biology of the mycobacteria. Academic Press, London, pp. 95–185

    Google Scholar 

  • Minnikin DE, Lee OY, Wu HH, Nataraj V, Donoghue HD, Ridell M, Watanabe M, Alderwick L, Bhatt A, Besra GS (2015) Pathophysiological implications of cell envelope structure in Mycobacterium tuberculosis and related taxa. In: Ribón W (eds) Tuberculosis – expanding knowledge. InTech Open Access Publisher, Rijeka, pp. 145–175

    Google Scholar 

  • Mishra KC, de Chastellier C, Narayana Y, Bifani P, Brown AK, Besra GS, Katoch VM, Joshi B, Balaji KN, Kremer L (2008) Functional role of the PE domain and immunogenicity of the Mycobacterium tuberculosis triacylglycerol hydrolase LipY. Infect Immun 76:127–140

    Article  CAS  PubMed  Google Scholar 

  • Mitchison DA (1979) Basic mechanisms of chemotherapy. Chest 76(6 Suppl):771–781

    Article  CAS  PubMed  Google Scholar 

  • Mukamolova GV, Turapov O, Malkin J, Woltmann G, Barer MR (2010) Resuscitation-promoting factors reveal an occult population of tubercle bacilli in sputum. Am J Respir Crit Care Med 181:174–180

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541–585

    Article  CAS  PubMed  Google Scholar 

  • Muttucumaru DG, Roberts G, Hinds J, Stabler RA, Parish T (2004) Gene expression profile of Mycobacterium tuberculosis in a non-replicating state. Tuberculosis (Edinb) 84:239–246

    Article  Google Scholar 

  • Ofori-Anyinam B, Dolganov G, Van T, Davis JL, Walter ND, Garcia BJ, Voskuil M, Fissette K, Diels M, Driesen M, Meehan CJ, Yeboah-Manu D, Coscolla M, Gagneux S, Antonio M, Schoolnik G, Gehre F, de Jong BC (2017) Significant under expression of the DosR regulon in M. tuberculosis complex lineage 6 in sputum. Tuberculosis (Edinb) 104:58–64

    Article  CAS  Google Scholar 

  • Ortalo-Magné A, Lemassu A, Lanéelle MA, Bardou F, Silve G, Gounon P, Marchal G, Daffé M (1996) Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178:456–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandey AK, Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A 105:4376–4380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48:833–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, Bardou F, Daffe M, Emile JF, Marchou B, Cardona PJ, de Chastellier C, Altare F (2008) Foamy macrophages from tuberculous patients’ granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4:e1000204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rastogi S, Singh AK, Chandra G, Kushwaha P, Pant G, Singh K, Mitra K, Sashidhara KV, Krishnan MY (2017) The diacylglycerol acyltransferase Rv3371 of Mycobacterium tuberculosis is required for growth arrest and involved in stress-induced cell wall alterations. Tuberculosis (Edinb) 104:8–19

    Article  CAS  Google Scholar 

  • Reed MB, Gagneux S, Deriemer K, Small PM, Barry CM 3rd (2007) The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189:2583–2589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR (2004) Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem 279:23082–23087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russell DG (2007) Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5:39–47

    Article  CAS  PubMed  Google Scholar 

  • Russell DG, Cardona PJ, Kim MJ, Allain S, Altare F (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10:943–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segal W, Bloch H (1956) Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72:132–141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma S, Ryndak MB, Aggarwal AN, Yadav R, Sethi S, Masih S, Laal S, Verma I (2017) Transcriptome analysis of mycobacteria in sputum samples of pulmonary tuberculosis patients. PLoS One 12:e0173508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherratt AL (2008) Lipid bodies in mycobacteria. PhD, University of Leicester

    Google Scholar 

  • Shi L, Sohaskey CD, Kana BD, Dawes S, North RJ, Mizrahi V, Gennaro ML (2005) Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102(43):15629–15634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singer ME, Tyler SM, Finnerty WR (1985) Growth of Acinetobacter sp. strain HO1-N on n-hexadecanol: physiological and ultrastructural characteristics. J Bacteriol 162:162–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sirakova TD, Dubey VS, Deb C, Daniel J, Korotkova TA, Abomoelak B, Kolattukudy PE (2006) Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152:2717–2725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirakova TD, Deb C, Daniel J, Singh HD, Maamar H, Dubey VS, Kolattukudy PE (2012) Wax ester synthesis is required for Mycobacterium tuberculosis to enter in vitro dormancy. PLoS One 7:e51641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sloan DJ, Mwandumba HC, Garton NJ, Khoo SH, Butterworth AE, Allain TJ, Heyderman RS, Corbett EL, Barer MR, Davies GR (2015) Pharmacodynamic modeling of bacillary elimination rates and detection of bacterial lipid bodies in sputum to predict and understand outcomes in treatment of pulmonary tuberculosis. Clin Infect Dis 61:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smeulders MJ, Keer J, Speight RA, Williams HD (1999) Adaptation of Mycobacterium smegmatis to stationary phase. J Bacteriol 181:270–283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stöveken T, Kalscheuer R, Malkus U, Reichelt R, Steinbüchel A (2005) The wax ester synthase/acyl coenzyme A:diacylglycerol acyltransferase from Acinetobacter sp. strain ADP1: characterization of a novel type of acyltransferase. J Bacteriol 187:1369–1376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tientcheu LD, Bell A, Secka O, Ayorinde A, Otu J, Garton NJ, Sutherland JS, Ota MO, Antonio M, Dockrell HM, Kampmann B, Barer MR (2016) Association of slow recovery of Mycobacterium africanum-infected patients posttreatment with high content of persister-like bacilli in pretreatment sputum. Int J Mycobacteriol 5(Suppl 1):S99–S100

    Article  PubMed  Google Scholar 

  • Turapov O, O'Connor BD, Sarybaeva AA, Williams C, Patel H, Kadyrov AS, Sarybaev AS, Woltmann G, Barer MR, Mukamolova GV (2016) Phenotypically adapted Mycobacterium tuberculosis populations from sputum are tolerant to first-line drugs. Antimicrob Agents Chemother 60:2476–2483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vijay S, Hai HT, Thu DDA, Johnson E, Pielach A, Phu NH, Thwaites GE, Thuong NTT (2017) Ultrastructural analysis of cell envelope and accumulation of lipid inclusions in clinical Mycobacterium tuberculosis isolates from sputum, oxidative stress, and iron deficiency. Front Microbiol 8:2681

    Article  PubMed  Google Scholar 

  • Viljoen A, Richard M, Nguyen PC, Fourquet P, Camoin L, Paudal RR, Gnawali GR, Spilling CD, Cavalier JF, Canaan S, Blaise M, Kremer L (2018) Cyclipostins and cyclophostin analogs inhibit the antigen 85C from Mycobacterium tuberculosis both in vitro and in vivo. J Biol Chem 293(8):2755–2769

    Article  CAS  PubMed  Google Scholar 

  • Voskuil MI, Visconti KC, Schoolnik GK (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84:218–227

    Article  CAS  Google Scholar 

  • Walker RW, Barakat H, Hung JG (1970) The positional distribution of fatty acids in the phospholipids and triglycerides of Mycobacterium smegmatis and M. bovis BCG. Lipids 5:684–691

    Article  CAS  PubMed  Google Scholar 

  • Walter ND, de Jong BC, Garcia BJ, Dolganov GM, Worodria W, Byanyima P, Musisi E, Huang L, Chan ED, Van TT, Antonio M, Ayorinde A, Kato-Maeda M, Nahid P, Leung AM, Yen A, Fingerlin TE, Kechris K, Strong M, Voskuil I, Davis JL, Schoolnik GK (2016) Adaptation of Mycobacterium tuberculosis to impaired host immunity in HIV-infected patients. J Infect Dis 214(8):1205–1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walther TC, Farese RV Jr (2012) Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81:687–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wayne LG, Hayes LG (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64:2062–2069

    CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, UK

    Natalie J. Garton & Michael R. Barer

  2. Department of Clinical Microbiology, University Hospitals Leicester NHS Trust, Leicester, UK

    Michael R. Barer

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  1. Natalie J. Garton
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  2. Michael R. Barer
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Correspondence to Natalie J. Garton .

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Editors and Affiliations

  1. Dept. Microbiology, University of Pennsylvania Dept. Microbiology, PHILADELPHIA, PA, USA

    Howard Goldfine

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Garton, N.J., Barer, M.R. (2019). Mycobacterial Lipid Bodies and the Chemosensitivity and Transmission of Tuberculosis. In: Goldfine, H. (eds) Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-72473-7_6-1

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