Generic placeholder image

Current Molecular Medicine

Editor-in-Chief

ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Review Article

Understanding Mass Spectrometry-based Global Mycobacterial Lipidomics

Author(s): Zeeshan Fatima*, Shiv Nandan and Saif Hameed*

Volume 20, Issue 8, 2020

Page: [607 - 623] Pages: 17

DOI: 10.2174/1566524020666200206120840

Price: $65

Abstract

Tuberculosis (TB) is the foremost cause of mortality from single infectious agent Mycobacterium tuberculosis (MTB). Current therapeutic regimes suffer from several problems, including side effects, costs and emergence of multidrug resistance (MDR). Moreover, conventional diagnostic methods are either too slow, or lack accurate and robust biomarkers. Under such circumstances, identification of rapid metabolite based biomarkers as novel drug targets could be a potential approach to circumvent MDR. In the era of “OMIC” sciences, lipidomics has gained significant attention to unravel the complexity of lipid-loaded Mycobacterium species. Lipidomics is a subbranch of metabolomics with extreme atomic diversity between the metabolites. There is no single principle on which the metabolite diversity can be defined, unlike other biomolecules viz. nucleic acid, proteins or carbohydrates. MTB encodes 10% of the genome for lipid metabolism and lipids account for 60% of its dry weight. Mycobacterium harbor a wide spectra of lipid repertoire ranging from highly apolar to highly polar lipids, adding complexity to their identification and analysis. Compared to targeted approaches, untargeted or global lipidomics of MTB is still more challenging. This review describes recent advances in lipidomics technology with regard to chromatography, detection methods and assessment on the existing mass spectrometry-based lipidomics tools to study the untargeted or global MTB lipidomics. It also identifies the limitations associated with present technologies as well as explores solutions to practical challenges concurrent with the establishment of MTB lipidome. Together we endorse that the emerging tools of lipidomics have provided a broader vision to comprehend the role of lipid molecules in MTB pathogenesis and the need for further improvements.

Keywords: Tuberculosis, lipids, LCMS, TLC, lipid database, lipidomics.

[1]
Global tuberculosis report Geneva: WHO 2018.
[2]
Vilchèze C, Hartman T, Weinrick B, Jacobs WR Jr. Mycobacterium tuberculosis is extraordinarily sensitive to killing by a vitamin C-induced Fenton reaction. Nat Commun 2013; 4: 1881.
[http://dx.doi.org/10.1038/ncomms2898] [PMID: 23695675]
[3]
Pal R, Hameed S, Fatima Z. Altered drug efflux under iron deprivation unveils MmpL3 driven abrogated mycolic acid transport and fluidity in mycobacteria. Biometals 2019; 32(1): 49-6.
[http://dx.doi.org/10.1007/s10534-018-0157-8] [PMID: 30430296]
[4]
Crellin PK, Luo CY, Morita YS. Metabolism of Plasma Membrane Lipids in Mycobacteria and Corynebacteria. Lipid Metabolism, Rodrigo ValenzuelaBaez, IntechOpen 2013.
[5]
Layre E, Sweet L, Hong S, et al. A comparative lipidomics platform for chemotaxonomic analysis of Mycobacterium tuberculosis. Chem Biol 2011; 18(12): 1537-49.
[http://dx.doi.org/10.1016/j.chembiol.2011.10.013] [PMID: 22195556]
[6]
Sud M, Fahy E, Cotter D, et al. LMSD: LIPID MAPS structure database. Nucleic Acids Res 2007; 35(Database issue): D527-32.
[http://dx.doi.org/10.1093/nar/gkl838] [PMID: 17098933]
[7]
Jackson M. The mycobacterial cell envelope-lipids. Cold Spring Harb Perspect Med 2014; 4(10)a021105
[http://dx.doi.org/10.1101/cshperspect.a021105] [PMID: 25104772]
[8]
Daffé M, Lacave C, Lanéelle MA, Lanéelle G. Structure of the major triglycosyl phenol-phthiocerol of Mycobacterium tuberculosis (strain Canetti). Eur J Biochem 1987; 167(1): 155-60.
[http://dx.doi.org/10.1111/j.1432-1033.1987.tb13317.x] [PMID: 3113946]
[9]
Daniel J, Deb C, Dubey VS, et al. 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(15): 5017-30.
[http://dx.doi.org/10.1128/JB.186.15.5017-5030.2004] [PMID: 15262939]
[10]
Fahy E, Subramaniam S, Murphy RC, et al. Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res 2009; 50(Suppl.): S9-S14.
[http://dx.doi.org/10.1194/jlr.R800095-JLR200] [PMID: 19098281]
[11]
Bach D, Wachtel E. Phospholipid/cholesterol model membranes: formation of cholesterol crystallites. Biochim Biophys Acta 2003; 1610(2): 187-97.
[http://dx.doi.org/10.1016/S0005-2736 (03)00017-8] [PMID: 12648773]
[12]
Devlin TM. Textbook of Biochemistry: With Clinical Correlations. 4th ed. Chichester: John Wiley & Sons 1997.
[13]
Fahy E, Subramaniam S, Brown HA, et al. A comprehensive classification system for lipids. J Lipid Res 2005; 46(5): 839-61.
[http://dx.doi.org/10.1194/jlr.E400004-JLR200] [PMID: 15722563]
[14]
Caffrey P, Aparicio JF, Malpartida F, Zotchev SB. Biosynthetic engineering of polyene macrolides towards generation of improved antifungal and antiparasitic agents. Curr Top Med Chem 2008; 8(8): 639-53.
[http://dx.doi.org/10.2174/156802608784221479] [PMID: 18473889]
[15]
Sartain MJ, Dick DL, Rithner CD, Crick DC, Belisle JT. Lipidomic analyses of Mycobacterium tuberculosis based on accurate mass measurements and the novel “Mtb LipidDB”. J Lipid Res 2011; 52(5): 861-72.
[http://dx.doi.org/10.1194/jlr.M010363] [PMID: 21285232]
[16]
Singh P, Sinha R, Tandon R, et al. revisiting a protocol for extraction of mycobacterial lipids. Int J Mycobacteriol 2014; 3(3): 168-72.
[http://dx.doi.org/10.1016/j.ijmyco.2014.07.008] [PMID: 26786484]
[17]
Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226(1): 497-509.
[PMID: 13428781]
[18]
Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37(8): 911-7.
[http://dx.doi.org/10.1139/o59-099] [PMID: 13671378]
[19]
Chandramouli V, Venkitasubramanian TA. Effect of age on the lipids of mycobacteria. Indian J Chest Dis 1974; 16(Suppl.): 199-207.
[PMID: 4442929]
[20]
Chang TY, Li BL, Chang CC, Urano Y. Acyl-coenzyme A: cholesterol acyltransferases. Am J Physiol Endocrinol Metab 2009; 297(1): E1-9.
[http://dx.doi.org/10.1152/ajpendo.90926.2008] [PMID: 19141679]
[21]
Pandey AK, Sassetti CM. Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 2008; 105(11): 4376-80.
[http://dx.doi.org/10.1073/pnas.0711159105] [PMID: 18334639]
[22]
Pal R, Hameed S, Kumar P, Singh S, Fatima Z. Understanding lipidomic basis of iron limitation induced chemosensitization of drug-resistant Mycobacterium tuberculosis 2019. 3 Biotech(9): 122.
[23]
McMahon A, Lu H, Butovich IA. The spectrophotometric sulfo-phospho-vanillin assessment of total lipids in human meibomian gland secretions. Lipids 2013; 48(5): 513-25.
[http://dx.doi.org/10.1007/s11745-013-3755-9] [PMID: 23345137]
[24]
Chabrol E, Charonnat R. Une nouvelle reaction pour l’études des lipides: l’oleidemie. Presse Med 1937; 45: 1713-4.
[25]
Johnson KR, Ellis G, Toothill C. The sulfophosphovanillin reaction for serum lipids: a reappraisal. Clin Chem 1977; 23(9): 1669-78.
[http://dx.doi.org/10.1093/clinchem/23.9.1669] [PMID: 556319]
[26]
Cheng YS, Zheng Y, VanderGheynst JS. Rapid quantitative analysis of lipids using a colorimetric method in a microplate format. Lipids 2011; 46(1): 95-103.
[http://dx.doi.org/10.1007/s11745-010-3494-0] [PMID: 21069472]
[27]
Knight JA, Anderson S, Rawle JM. Chemical basis of the sulfo-phospho-vanillin reaction for estimating total serum lipids. Clin Chem 1972; 18(3): 199-202.
[http://dx.doi.org/10.1093/clinchem/18.3.199] [PMID: 5020813]
[28]
Frings CS, Fendley TW, Dunn RT, Queen CA. Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 1972; 18(7): 673-4.
[http://dx.doi.org/10.1093/clinchem/18.7.673] [PMID: 5037917]
[29]
Khanuja SPS, Srivastava S, Kumar TRS, Shasany AK. A quick and sensitive method of quantifying mycolic acid. US Patent USOO6833249B2 2004.
[30]
Hameed S, Fatima Z. Lipidomics: Tool to redefine lipids. In: Biotechnology: Progress and prospects. LLC, USA: Studium Press Paul Khurana SM, Singh Machiavelli. In: 2015; pp. 302-12.
[31]
Jandera P. Liquid chromatography—normal phase Encyclopedia of analytical science. 2nd ed. Oxford: Elsevier 2005; pp. 142-52.
[http://dx.doi.org/10.1016/B0-12-369397-7/00324-1]
[32]
Abreu S, Solgadi A, Chaminade P. 2017.Optimization of normal phase chromatographic conditions for lipid analysis and comparison of associated detection techniques
[http://dx.doi.org/10.1016/j.chroma.2017.07.063]
[33]
Olsson P, Holmbäck J, Nilsson U, Herslöf B. Separation and identification of lipid classes by normal phase LC‐ESI/MS/MS on a cyanopropyl column. Eur J Lipid Sci Technol 2014; 116: 653-8.
[http://dx.doi.org/10.1002/ejlt.201300291]
[34]
Triebl A, Trötzmüller M, Hartler J, Stojakovic T, Köfeler HC. Lipidomics by ultrahigh performance liquid chromatography-high resolution mass spectrometry and its application to complex biological samples. J Chromatogr B Analyt Technol Biomed Life Sci 2017; 1053(1053): 72-80.
[http://dx.doi.org/10.1016/j.jchromb.2017.03.027] [PMID: 28415015]
[35]
Buszewski B, Noga S. Hydrophilic interaction liquid chromatography (HILIC)--a powerful separation technique. Anal Bioanal Chem 2012; 402(1): 231-47.
[http://dx.doi.org/10.1007/s00216-011-5308-5] [PMID: 21879300]
[36]
Rabel F, Olsen BA. Advances in hydrophilic interaction chromatography (HILIC) for biochemical applications Hydrophil Interact Chromatogr 2013; 195-217.
[37]
Knittelfelder OL, Weberhofer BP, Eichmann TO, Kohlwein SD, Rechberger GN. A versatile ultra-high performance LC-MS method for lipid profiling. J Chromatogr B Analyt Technol Biomed Life Sci 2014; 951-952: 119-28.
[http://dx.doi.org/10.1016/j.jchromb.2014.01.011] [PMID: 24548922]
[38]
Fauland A, Köfeler H, Trötzmüller M, et al. A comprehensive method for lipid profiling by liquid chromatography-ion cyclotron resonance mass spectrometry. J Lipid Res 2011; 52(12): 2314-22.
[http://dx.doi.org/10.1194/jlr.D016550] [PMID: 21960706]
[39]
Murphy RC, Axelsen PH. Mass spectrometric analysis of long-chain lipids. Mass Spectrom Rev 2011; 30(4): 579-99.
[http://dx.doi.org/10.1002/mas.20284] [PMID: 21656842]
[40]
Murphy RC, Gaskell SJ. New applications of mass spectrometry in lipid analysis. J Biol Chem 2011; 286(29): 25427-33.
[http://dx.doi.org/10.1074/jbc.R111.233478] [PMID: 21632539]
[41]
Vestal ML, Campbell JM. Tandem time-of-flight mass spectrometry. Methods Enzymol 2005; 402: 79-108.
[http://dx.doi.org/10.1016/S0076-6879(05)02003-3] [PMID: 16401507]
[42]
Perry RH, Cooks RG, Noll RJ. Orbitrap mass spectrometry: instrumentation, ion motion and applications. Mass Spectrom Rev 2008; 27(6): 661-99.
[http://dx.doi.org/10.1002/mas.20186] [PMID: 18683895]
[43]
Shibayama N, Lomax SQ, Sutherland K, Rene de la Rie E. Atmospheric Pressure Chemical Ionization Liquid Chromatography Mass Spectrometry and its application to conservation: Analysis of Triacylglycerols. Stud Conserv 1999; 44: 253-68.
[44]
Byrdwell WC. Critical Ratios for Structural Analysis of Triacylglycerols Using Mass Spectrometry. Lipid Technol 2015; 27: 258-61.
[http://dx.doi.org/10.1002/lite.201500054]
[45]
Allen M R. Atmospheric pressurei onization-masss pectrometryde tection for liquid chromatographayn d capillary electrophoresisL C -GC 11 1993; 112-24.
[46]
Robb DB, Covey TR, Bruins AP. Atmospheric pressure photoionization: an ionization method for liquid chromatography-mass spectrometry. Anal Chem 2000; 72(15): 3653-9.
[http://dx.doi.org/10.1021/ac0001636] [PMID: 10952556]
[47]
Hanold KA, Fischer SM, Cormia PH, Miller CE, Syage JA. Atmospheric pressure photoionization. 1. General properties for LC/MS. Anal Chem 2004; 76(10): 2842-51.
[http://dx.doi.org/10.1021/ac035442i] [PMID: 15144196]
[48]
Hsieh Y, Merkle K, Wang G, Brisson JM, Korfmacher WA. High-performance liquid chromatography-atmospheric pressure photoionization/tandem mass spectrometric analysis for small molecules in plasma. Anal Chem 2003; 75(13): 3122-7.
[http://dx.doi.org/10.1021/ac0300082] [PMID: 12964760]
[49]
Takino M, Yamaguchi K, Nakahara T. Determination of carbamate pesticide residues in vegetables and fruits by liquid chromatography-atmospheric pressure photoionization-mass spectrometry and atmospheric pressure chemical ionization-mass spectrometry. J Agric Food Chem 2004; 52(4): 727-35.
[http://dx.doi.org/10.1021/jf0343377] [PMID: 14969523]
[50]
Cai SS, Syage JA. Comparison of atmospheric pressure photoionization, atmospheric pressure chemical ionization, and electrospray ionization mass spectrometry for analysis of lipids. Anal Chem 2006; 78(4): 1191-9.
[http://dx.doi.org/10.1021/ac0515834] [PMID: 16478111]
[51]
Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. Electrospray ionization for mass spectrometry of large biomolecules. Science 1989; 246(4926): 64-71.
[http://dx.doi.org/10.1126/science.2675315] [PMID: 2675315]
[52]
Karas M, Hillenkamp F. Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal Chem 1988; 60(20): 2299-301.
[http://dx.doi.org/10.1021/ac00171a028] [PMID: 3239801]
[53]
Peng IX, Shiea J, Ogorzalek Loo RR, Loo JA. Electrospray-assisted laser desorption/ionization and tandem mass spectrometry of peptides and proteins. Rapid Commun Mass Spectrom 2007; 21(16): 2541-6.
[http://dx.doi.org/10.1002/rcm.3154] [PMID: 17639579]
[54]
Bouslimani A, Sanchez LM, Garg N, Dorrestein PC. Mass spectrometry of natural products: current, emerging and future technologies. Nat Prod Rep 2014; 31(6): 718-29.
[http://dx.doi.org/10.1039/c4np00044g] [PMID: 24801551]
[55]
Köfeler HC, Fauland A, Rechberger GN, Trötzmüller M. Mass spectrometry based lipidomics: an overview of technological platforms. Metabolites 2012; 2(1): 19-38.
[http://dx.doi.org/10.3390/metabo2010019] [PMID: 24957366]
[56]
Quehenberger O, Armando AM, Dennis EA. High sensitivity quantitative lipidomics analysis of fatty acids in biological samples by gas chromatography-mass spectrometry. Biochim Biophys Acta 2011; 1811(11): 648-56.
[http://dx.doi.org/10.1016/j.bbalip.2011.07.006] [PMID: 21787881]
[57]
Siuzdak G. An Introduction to Mass Spectrometry Ionization: An Excerpt from The Expanding Role of Mass Spectrometry in Biotechnology. 2nd ed. San Diego: MCC Press 2004; p. 9.
[58]
Nie H, Liu R, Yang Y, et al. Lipid profiling of rat peritoneal surface layers by online normal- and reversed-phase 2D LC QToF-MS. J Lipid Res 2010; 51(9): 2833-44.
[http://dx.doi.org/10.1194/jlr.D007567] [PMID: 20526000]
[59]
Karpievitch YV, Polpitiya AD, Anderson GA, Smith RD, Dabney AR. Liquid Chromatography Mass Spectrometry-Based Proteomics: Biological and Technological Aspects. Ann Appl Stat 2010; 4(4): 1797-823.
[http://dx.doi.org/10.1214/10-AOAS341] [PMID: 21593992]
[60]
Wang M, Wang C, Han X. Selection of internal standards for accurate quantification of complex lipid species in biological extracts by electrospray ionization mass spectrometry-What, how and why? Mass Spectrom Rev 2017; 36(6): 693-714.
[http://dx.doi.org/10.1002/mas.21492] [PMID: 26773411]
[61]
Burla B, Arita M, Arita M, et al. MS-based lipidomics of human blood plasma: a community-initiated position paper to develop accepted guidelines. J Lipid Res 2018; 59(10): 2001-17.
[http://dx.doi.org/10.1194/jlr.S087163] [PMID: 30115755]
[62]
Sabareesh V, Singh G. Mass spectrometry based lipid(ome) analyzer and molecular platform: a new software to interpret and analyze electrospray and/or matrix-assisted laser desorption/ionization mass spectrometric data of lipids: a case study from Mycobacterium tuberculosis. J Mass Spectrom 2013; 48(4): 465-77.
[http://dx.doi.org/10.1002/jms.3163] [PMID: 23584940]
[63]
Herzog R, Schuhmann K, Schwudke D, et al. LipidXplorer: a software for consensual cross-platform lipidomics. PLoS One 2012; 7(1)e29851
[http://dx.doi.org/10.1371/journal.pone.0029851] [PMID: 22272252]
[64]
Herzog R, Schwudke D, Schuhmann K, et al. A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol 2011; 12(1): R8.
[http://dx.doi.org/10.1186/gb-2011-12-1-r8] [PMID: 21247462]
[65]
Bird SS, Marur VR, Sniatynski MJ, Greenberg HK, Kristal BS. Serum lipidomics profiling using LC-MS and high-energy collisional dissociation fragmentation: focus on triglyceride detection and characterization. Anal Chem 2011; 83(17): 6648-57.
[http://dx.doi.org/10.1021/ac201195d] [PMID: 21774539]
[66]
Seppänen-Laakso T, Oresic MJ. Mol Endocrinol 2009; 42(3): 185-90.
[http://dx.doi.org/10.1677/JME-08-0150]
[67]
Han X, Yang K, Gross RW. Mass Spectrom Rev 2012; 31(1): 134-78.
[http://dx.doi.org/10.1002/mas.20342] [PMID: 21755525]
[68]
Li L, Han J, Wang Z, et al. Mass spectrometry methodology in lipid analysis. Int J Mol Sci 2014; 15(6): 10492-507.
[http://dx.doi.org/10.3390/ijms150610492] [PMID: 24921707]
[69]
Pal R, Hameed S, Kumar P, Singh S, Fatima Z. Comparative lipidomics of drug sensitive and resistant Mycobacteriumtuberculosis reveals altered lipid imprints. 3 Biotech 2017; 7: 325.
[70]
Pal R, Hameed S, Sabareesh V, Kumar P, Singh S, Fatima Z. Investigations into isoniazid treated Mycobacterium tuberculosis by electrospray mass spectrometry reveals new insights into its lipid composition. J Pathogens 2018.20181454316
[http://dx.doi.org/10.1155/2018/1454316] [PMID: 30018826]
[71]
Herzog R, Schuhmann K, Schwudke D. LipidXplorer: Software for Quantitative Shotgun Lipidomics Compatible with Multiple Mass Spectrometry Platforms. Curr Protoc Bioinformatics 2013; 43: 14.12.1-.
[72]
Song H, Hsu FF, Ladenson J, Turk J. Algorithm for processing raw mass spectrometric data to identify and quantitate complex lipid molecular species in mixtures by data-dependent scanning and fragment ion database searching. J Am Soc Mass Spectrom 2007; 18(10): 1848-58.
[http://dx.doi.org/10.1016/j.jasms.2007.07.023] [PMID: 17720531]
[73]
Taguchi R, Ishikawa M. Precise and global identification of phospholipid molecular species by an Orbitrap mass spectrometer and automated search engine Lipid Search. J Chromatogr A 2010; 1217(25): 4229-39.
[http://dx.doi.org/10.1016/j.chroma.2010.04.034] [PMID: 20452604]
[75]
Hein EM, Bödeker B, Nolte J, Hayen H. Software tool for mining liquid chromatography/multi-stage mass spectrometry data for comprehensive glycerophospholipid profiling. Rapid Commun Mass Spectrom 2010; 24(14): 2083-92.
[http://dx.doi.org/10.1002/rcm.4614] [PMID: 20552715]
[76]
Schmelzer K, Fahy E, Subramaniam S, Dennis EA. The lipid maps initiative in lipidomics. Methods Enzymol 2007; 432: 171-83.
[http://dx.doi.org/10.1016/S0076-6879(07)32007-7] [PMID: 17954217]
[77]
Hartler J, Tharakan R, Köfeler HC, Graham DR, Thallinger GG. Bioinformatics tools and challenges in structural analysis of lipidomics MS/MS data. Brief Bioinform 2013; 14(3): 375-90.
[http://dx.doi.org/10.1093/bib/bbs030] [PMID: 22764120]
[78]
Koelmel JP, Kroeger NM, Ulmer CZ, et al. LipidMatch: an automated workflow for rule-based lipid identification using untargeted high-resolution tandem mass spectrometry data. BMC Bioinformatics 2017; 18(1): 331.
[http://dx.doi.org/10.1186/s12859-017-1744-3] [PMID: 28693421]
[79]
Tsugawa H, Cajka T, Kind T, et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods 2015; 12(6): 523-6.
[http://dx.doi.org/10.1038/nmeth.3393] [PMID: 25938372]
[80]
Watanabe K, Yasugi E, Oshima M. How to search the glycolipid data in LIPIDBANK for Web: the newly developed lipid database. Jpn Trend Glycosci Glycotechnol 2000; 12: 175-84.
[http://dx.doi.org/10.4052/tigg.12.175]
[81]
Merril AH Jr. SphinGOMAP--a web-based biosynthetic pathway map of sphingolipids and glycosphingolipids. Glycobiology 2005; 15(6): 15G.
[http://dx.doi.org/10.1093/glycob/cwi070] [PMID: 15938018]
[82]
Christie WW, Han X. Lipid Analysis - Isolation, Separation, Identification and Lipidomic Analysis. 4th ed. Elsevier 2010; p. 446.
[83]
James Hutton Institute. (and Mylnefield Lipid Analysis), Invergowrie, Dundee (DD2 5DA), Scotland
[84]
Pal R, Hameed S, Fatima Z. Lipidomics: Novel Strategy to Conquer Antimicrobial Resistance. In: Mendez-Vilas A, Ed. Antimicrobial Research: Novel bioknowledge and educational programsSpain: Formatex Res Center In: 2017; 6: pp. 644-650.b.
[85]
Sharma S, Hameed S, Fatima Z. Spain: Formatex Research Center Mycobacterial lipids as potential drug target to combat Tuberculosis. In: Mendez-Vilas A, Ed. Understanding Microbial Pathogens: Current Knowledge and Educational Ideas on Antimicrobial Research In: 2018; 7: pp. 644-50.
[86]
Daffé M, Draper P. The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 1998; 39: 131-203.
[http://dx.doi.org/10.1016/S0065-2911(08)60016-8] [PMID: 9328647]
[87]
Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 2008; 105(10): 3963-7.
[http://dx.doi.org/10.1073/pnas.0709530105] [PMID: 18316738]
[88]
Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffé M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 2008; 190(16): 5672-80.
[http://dx.doi.org/10.1128/JB.01919-07] [PMID: 18567661]
[89]
Adams KN, Takaki K, Connolly LE, et al. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 2011; 145(1): 39-53.
[http://dx.doi.org/10.1016/j.cell.2011.02.022] [PMID: 21376383]
[90]
Kondo E, Kanai K. The lethal effect of long-chain fatty acids on mycobacteria. Jpn J Med Sci Biol 1972; 25(1): 1-13.
[http://dx.doi.org/10.7883/yoken1952.25.1] [PMID: 4625006]
[91]
Rustad TR, Harrell MI, Liao R, Sherman DR. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 2008; 3(1)e1502
[http://dx.doi.org/10.1371/journal.pone.0001502] [PMID: 18231589]
[92]
Singh A, Crossman DK, Mai D, et al. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 2009; 5(8)e1000545
[http://dx.doi.org/10.1371/journal.ppat.1000545] [PMID: 19680450]
[93]
Raman S, Puyang X, Cheng TY, Young DC, Moody DB, Husson RN. Mycobacterium tuberculosis SigM positively regulates Esx secreted protein and nonribosomal peptide synthetase genes and down regulates virulence-associated surface lipid synthesis. J Bacteriol 2006; 188(24): 8460-8.
[http://dx.doi.org/10.1128/JB.01212-06] [PMID: 17028284]
[94]
Homolka S, Niemann S, Russell DG, Rohde KH. Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog 2010; 6(7)e1000988
[http://dx.doi.org/10.1371/journal.ppat.1000988] [PMID: 20628579]
[95]
Rohde KH, Abramovitch RB, Russell DG. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2007; 2(5): 352-64.
[http://dx.doi.org/10.1016/j.chom.2007.09.006] [PMID: 18005756]
[96]
Schnappinger D, Ehrt S, Voskuil MI, et al. Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 2003; 198(5): 693-704.
[http://dx.doi.org/10.1084/jem.20030846] [PMID: 12953091]
[97]
Wolfe LM, Mahaffey SB, Kruh NA, Dobos KM. Proteomic definition of the cell wall of Mycobacterium tuberculosis. J Proteome Res 2010; 9(11): 5816-26.
[http://dx.doi.org/10.1021/pr1005873] [PMID: 20825248]
[98]
de Carvalho LP, Fischer SM, Marrero J, Nathan C, Ehrt S, Rhee KY. Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 2010; 17(10): 1122-31.
[http://dx.doi.org/10.1016/j.chembiol.2010.08.009] [PMID: 21035735]
[99]
Marrero J, Rhee KY, Schnappinger D, Pethe K, Ehrt S. Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc Natl Acad Sci USA 2010; 107(21): 9819-24.
[http://dx.doi.org/10.1073/pnas.1000715107] [PMID: 20439709]
[100]
Matsunaga I, Bhatt A, Young DC, et al. Mycobacterium tuberculosis pks12 produces a novel polyketide presented by CD1c to T cells. J Exp Med 2004; 200(12): 1559-69.
[http://dx.doi.org/10.1084/jem.20041429] [PMID: 15611286]
[101]
Jain M, Petzold CJ, Schelle MW, et al. Lipidomics reveals control of Mycobacterium tuberculosis virulence lipids via metabolic coupling. Proc Natl Acad Sci USA 2007; 104(12): 5133-8.
[http://dx.doi.org/10.1073/pnas.0610634104] [PMID: 17360366]
[102]
Mahrous EA, Lee RB, Lee RE. A rapid approach to lipid profiling of mycobacteria using 2D HSQC NMR maps. J Lipid Res 2008; 49(2): 455-63.
[http://dx.doi.org/10.1194/jlr.M700440-JLR200] [PMID: 17982136]
[103]
Madigan CA, Martinot AJ, Wei JR, et al. Lipidomic analysis links mycobactin synthase K to iron uptake and virulence in M. tuberculosis. PLoS Pathog 2015; 11(3)e1004792
[http://dx.doi.org/10.1371/journal.ppat.1004792] [PMID: 25815898]
[104]
Yang Y, Liang Y, Yang J, Ye F, Zhou T, Gongke L. Advances of supercritical fluid chromatography in lipid profiling. J Pharm Anal 2019; 9(1): 1-8.
[http://dx.doi.org/10.1016/j.jpha.2018.11.003] [PMID: 30740251]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy