Metabolic profiling of lung granuloma in Mycobacterium tuberculosis infected guinea pigs: Ex vivo 1H magic angle spinning NMR studies

Journal of Proteome Research

Volumn 10, Issue 9, 2011, Pages 4186-4195

  Somashekar, B S ^a   Amin, Anita G ^a   Rithner, Christopher D ^a   Troudt, Jolynn ^a   Basaraba, Randall ^a   Izzo, Angelo ^a   Crick, Dean C ^a   Chatterjee, Delphi ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

guinea pig lung; HRMAS NMR; metabolic pathways; metabolomics; Mtb granulomas

Indexed keywords

ACETIC ACID; ALANINE; ASPARTIC ACID; BETAINE; CREATINE; DIHYDROXYACETONE; GLUTAMIC ACID; GLUTATHIONE; GLYCEROPHOSPHORYLCHOLINE; INOSITOL; LACTIC ACID; PHOSPHORYLCHOLINE; TRIMETHYLAMINE OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CITRIC ACID CYCLE; CLINICAL FEATURE; CONTROLLED STUDY; DOWN REGULATION; ENERGY RESOURCE; EX VIVO STUDY; FEMALE; GLYCOLYSIS; GUINEA PIG; HIGH RESOLUTION MAGIC ANGLE SPINNING NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; HYPOXIA; LUNG GRANULOMA; METABOLISM; METABOLITE; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; UPREGULATION;

ANIMALS; CELL HYPOXIA; DISEASE MODELS, ANIMAL; GRANULOMA; GUINEA PIGS; HISTOCYTOCHEMISTRY; LIPOLYSIS; LUNG; LUNG DISEASES; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MULTIVARIATE ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATIVE STRESS; PRINCIPAL COMPONENT ANALYSIS; TUBERCULOSIS;

CAVIA; MYCOBACTERIUM TUBERCULOSIS;

EID: 80052496075     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2003352     Document Type: Article

References (52)

1. WHO Global tuberculosis control: epidemiology, strategy, financing.; Publication no. WHO/HTM/TB/2009.411,; Geneva, 2009.
2. Flynn, J. L.; Chan, J. Tuberculosis: Latency and Reactivation Infect. Immun. 2001, 69 (7) 4195-201 (Pubitemid 32574413)
3. Munoz-Elias, E. J.; Upton, A. M.; Cherian, J.; McKinney, J. D. Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence Mol. Microbiol. 2006, 60 (5) 1109-22
4. Shi, L.; Sohaskey, C. D.; Kana, B. D.; Dawes, S.; North, R. J.; Mizrahi, V.; Gennaro, M. L. 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. 2005, 102 (43) 15629-34 (Pubitemid 41528107)
5. Talaat, A. M.; Ward, S. K.; Wu, C. W.; Rondon, E.; Tavano, C.; Bannantine, J. P.; Lyons, R.; Johnston, S. A. Mycobacterial bacilli are metabolically active during chronic tuberculosis in murine lungs: insights from genome-wide transcriptional profiling J. Bacteriol. 2007, 189 (11) 4265-74 (Pubitemid 46847375)
6. McKinney, J. D.; Honer zu Bentrup, K.; Munoz-Elias, E. J.; Miczak, A.; Chen, B.; Chan, W. T.; Swenson, D.; Sacchettini, J. C.; Jacobs, W. R., Jr.; Russell, D. G. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase Nature 2000, 406 (6797) 735-8
7. Bryk, R.; Gold, B.; Venugopal, A.; Singh, J. R. S.; Pupek, K.; Cao, H.; Carmen, P.; Gurney, M.; Srinivas, H.; Cherian, J.; Rhee, K. Y.; Lyn, L.; Converse, P. J.; Ehrt, S.; Vandal, O.; Jiang, X.; Schneider, J.; Lin, G.; Nathan, C. Selective Killing of Nonreplicating Mycobacteria Cell Host Microbe 2008, 3 (3) 137-45 (Pubitemid 351325759)
8. Idle, J. R.; Gonzalez, F. J. Metabolomics Cell Metab. 2007, 6 (5) 348-51 (Pubitemid 350012005)
9. Lindon, J. C.; Beckonert, O. P.; Holmes, E.; Nicholson, J. K. High-resolution magic angle spinning NMR spectroscopy: Application to biomedical studies Prog. Nucl. Magn. Reson. Spectrosc. 2009, 55, 79-100
10. Beckonert, O.; Coen, M.; Keun, H. C.; Wang, Y.; Ebbels, T. M.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues Nat. Protoc. 2010, 5 (6) 1019-32
11. Cheng, L. L.; Ma, M. J.; Becerra, L.; Ptak, T.; Tracey, I.; Lackner, A.; Gonzalez, R. G. Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (12) 6408-13 (Pubitemid 27270698)
12. Turner, O. C.; Basaraba, R. J.; Orme, I. M. Immunopathogenesis of pulmonary granulomas in the guinea pig after infection with Mycobacterium tuberculosis Infect. Immun. 2003, 71 (2) 864-71 (Pubitemid 36150782)
13. Grover, A.; Taylor, J.; Troudt, J.; Keyser, A.; Arnett, K.; Izzo, L.; Rholl, D.; Izzo, A. Kinetics of the immune response profile in guinea pigs after vaccination with Mycobacterium bovis BCG and infection with Mycobacterium tuberculosis Infect. Immun. 2009, 77 (11) 4837-46
14. Tugnoli, V.; Schenetti, L.; Mucci, A.; Parenti, F.; Cagnoli, R.; Righi, V.; Trinchero, A.; Nocetti, L.; Toraci, C.; Mavilla, L.; Trentini, G.; Zunarelli, E.; Tosi, M. R. Ex vivo HR-MAS MRS of human meningiomas: a comparison with in vivo 1H MR spectra Int. J. Mol. Med. 2006, 18 (5) 859-69
15. Ordway, D.; Palanisamy, G.; Henao-Tamayo, M.; Smith, E. E.; Shanley, C.; Orme, I. M.; Basaraba, R. J. The cellular immune response to Mycobacterium tuberculosis infection in the guinea pig J. Immunol. 2007, 179 (4) 2532-41
16. Dannenberg, A. M. Pathogenesis of human pulmonary tuberculosis: Insights from rabbit model; ASM Press: Washington, D.C., 2006.
17. De Backer, D. Lactic acidosis Intensive Care Med. 2003, 29 (5) 699-702 (Pubitemid 36609559)
18. Kandler, O. Carbohydrate metabolism in lactic acid bacteria Antonie Van Leeuwenhoek 1983, 49 (3) 209-24 (Pubitemid 13015417)
19. 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.; Lee, E. G.; Park, S. K.; Raleigh, J. A.; Cho, S. N.; McMurray, D. N.; Flynn, J. L.; Barry, C. E., 3rd Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates Infect. Immun. 2008, 76 (6) 2333-40
20. Aly, S.; Wagner, K.; Keller, C.; Malm, S.; Malzan, A.; Brandau, S.; Bange, F. C.; Ehlers, S. Oxygen status of lung granulomas in Mycobacterium tuberculosis-infected mice J. Pathol. 2006, 210 (3) 298-305 (Pubitemid 44660508)
21. Tsai, M. C.; Chakravarty, S.; Zhu, G. F.; Xu, J. Y.; Tanaka, K.; Koch, C. e. a. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension Cell Microbiol. 2006, 8, 218-32 (Pubitemid 43356045)
22. Neely, J. R.; Feuvray, D. Metabolic products and myocardial ischemia Am. J. Path. 1981, 102 (2) 282-91 (Pubitemid 12190467)
23. Proskuryakov, S. Y.; Konoplyannikov, A. G.; Gabai, V. L. Necrosis: a specific form of programmed cell death? Exp. Cell Res. 2003, 283 (1) 1-16 (Pubitemid 36259891)
24. Cheng, L. L.; Chang, I. W.; Smith, B. L.; Gonzalez, R. G. Evaluating human breast ductal carcinomas with high-resolution magic-angle spinning proton magnetic resonance spectroscopy J. Magn. Reson. 1998, 135 (1) 194-202 (Pubitemid 128450704)
25. Zhivotovsky, B.; Orrenius, S. The Warburg Effect returns to the cancer stage Semin. Cancer Biol. 2009, 19 (1) 1-3
26. Béard, E.; Braissant, O. Synthesis and transport of creatine in the CNS: importance of cerebral functions J. Neurochem. 2010, 15 (2) 297-313
27. Wallimann, T.; Wyss, M.; Brdiczka, D.; Nicolay, K.; Eppenberger, H. M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis Biochem. J. 1992, 281 (Pt 1) 21-40
28. Lane, M.; Gardner, D. K. Mitochondrial malate-aspartate shuttle regulates mouse embryo nutrient consumption J. Biol. Chem. 2005, 280 (18) 18361-7 (Pubitemid 41389084)
29. Sitter, B.; Sonnewald, U.; Spraul, M.; Fjosne, H. E.; Gribbestad, I. S. High-resolution magic angle spinning MRS of breast cancer tissue NMR Biomed. 2002, 15 (5) 327-37 (Pubitemid 34960100)
30. Benveniste, H.; Drejer, J.; Schousboe, A.; Diemer, N. H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis J. Neurochem. 1984, 43 (5) 1369-74 (Pubitemid 15205893)
31. Phillis, J. W.; O'Regan, M. H. Mechanisms of glutamate and aspartate release in the ischemic rat cerebral cortex Brain Res. 1996, 730 (1-2) 150-64 (Pubitemid 26305335)
32. Rahman, I.; MacNee, W. Oxidative stress and regulation of glutathione in lung inflammation Eur. Respir. J. 2000, 16 (3) 534-54
33. Brigham, K. L. Oxidant stress and adult respiratory distress syndrome Eur. Respir. J. Suppl. 1990, 11, 482s-4s
34. Brown, D. M.; Drost, E.; Donaldson, K.; MacNee, W. Deformability and CD11/CD18 expression of sequestered neutrophils in normal and inflamed lungs Am. J. Respir. Cell Mol. Biol. 1995, 13 (5) 531-9
35. Meister, A.; Anderson, M. E. Glutathione Annu. Rev. Biochem. 1983, 52, 711-60 (Pubitemid 13030692)
36. Li, X. Y.; Donaldson, K.; Rahman, I.; MacNee, W. An investigation of the role of glutathione in increased epithelial permeability induced by cigarette smoke in vivo and in vitro Am. J. Respir. Crit. Care Med. 1994, 149 (6) 1518-25 (Pubitemid 24175969)
37. Lannan, S, D. K.; Brown, D; MacNee, W Effect of cigarette smoke and its condensates on alveolar epithelial cell injury in vitro Am. J. Physiol. 1994, 266 (1 (Pt 1)) L92-100
38. Venketaraman, V.; Dayaram, Y. K.; Talaue, M. T.; Connell, N. D. Glutathione and nitrosoglutathione in macrophage defense against Mycobacterium tuberculosis Infect. Immun. 2005, 73 (3) 1886-9 (Pubitemid 40470782)
39. Venketaraman, V.; Millman, A.; Salman, M.; Swaminathan, S.; Goetz, M.; Lardizabal, A.; David, H.; Connell, N. D. Glutathione levels and immune responses in tuberculosis patients Microb. Pathog. 2008, 44 (3) 255-61 (Pubitemid 351163525)
40. Griffin, J. L.; Mann, C. J.; Scott, J.; Shoulders, C. C.; Nicholson, J. K. Choline containing metabolites during cell transfection: an insight into magnetic resonance spectroscopy detectable changes FEBS Lett. 2001, 509 (2) 263-6 (Pubitemid 34015954)
41. Vogel, F. S. A lipolytic enzyme in reactive histocytes of Guinea pigs with experimental Encephalomyelitis.; 1950; Plates 18 and 19.
42. Green, A.; Dobias, S. B.; Walters, D. J.; Brasier, A. R. Tumor necrosis factor increases the rate of lipolysis in primary cultures of adipocytes without altering levels of hormone-sensitive lipase Endocrinology 1994, 134 (6) 2581-8 (Pubitemid 24170874)
43. Goldman, D. S. Enzyme Systems in the Mycobacteria. Xv. Initial Steps in the Metabolism of Glycerol J. Bacteriol. 1963, 86, 30-7
44. Le Rudulier, D.; Strom, A. R.; Dandekar, A. M.; Smith, L. T.; Valentine, R. C. Molecular biology of osmoregulation Science 1984, 224 (4653) 1064-8
45. Strom, A. R.; Le Rudulier, D.; Jakowec, M. W.; Bunnell, R. C.; Valentine, R. C. Osmoregulatory (Osm) genes and osmoprotective compounds. In Genetic engineering of plants; T. Kosuge, C. M.; Hollaender, A., Eds.; Plenum Publishing Corp: New York, 1983; pp 39-59.
46. Iles, R. A. Nuclear magnetic resonance spectroscopy and genetic disorders Curr. Med. Chem. 2008, 15 (1) 15-36 (Pubitemid 351234625)
47. Delgado-Reyes, C. V.; Garrow, T. A. High sodium chloride intake decreases betaine-homocysteine S-methyltransferase expression in guinea pig liver and kidney Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288 (1) R182-7
48. Kempf, B.; Bremer, E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments Arch. Microbiol. 1998, 170 (5) 319-30 (Pubitemid 28458129)
49. Boch, J.; Kempf, B.; Bremer, E. Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline J. Bacteriol. 1994, 176 (17) 5364-71 (Pubitemid 24273524)
50. Boncompagni, E.; Osteras, M.; Poggi, M. C.; le Rudulier, D. Occurrence of choline and glycine betaine uptake and metabolism in the family rhizobiaceae and their roles in osmoprotection Appl. Environ. Microbiol. 1999, 65 (5) 2072-7
51. Price, C. T.; Bukka, A.; Cynamon, M.; Graham, J. E. Glycine betaine uptake by the ProXVWZ ABC transporter contributes to the ability of Mycobacterium tuberculosis to initiate growth in human macrophages J. Bacteriol. 2008, 190 (11) 3955-61 (Pubitemid 351732875)
52. 1H-NMR-based Metabolomic Profiling in Mice Infected with Mycobacterium tuberculosis J. Proteome Res. 2011, 10 (5) 2238-47