Metabolic characterization of Leishmania major infection in activated and nonactivated macrophages.

Journal of Proteome Research

Volumn 11, Issue 8, 2012, Pages 4211-4222

  Lamour, Sabrina D ^a   Choi, Beak San ^a   Keun, Hector C ^a   Müller, Ingrid ^a   Saric, Jasmina ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

1H NMR spectroscopy; Leishmania major; macrophage activation; metabolic profiling; metabolomics; multivariate data analysis

Indexed keywords

ACETIC ACID; ARGINASE; GLUCOSE; NITRIC OXIDE; SUCCINIC ACID;

ARTICLE; BIOMASS; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; LEISHMANIA; LEISHMANIASIS; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLOME; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL MARKERS; CELL EXTRACTS; CELLS, CULTURED; FEMALE; GLUCOSE; HOST-PARASITE INTERACTIONS; LEAST-SQUARES ANALYSIS; LEISHMANIA MAJOR; LEISHMANIASIS; MACROPHAGE ACTIVATION; MACROPHAGES; METABOLOME; MICE; MICE, INBRED BALB C; MULTIVARIATE ANALYSIS; PRINCIPAL COMPONENT ANALYSIS;

LEISHMANIA MAJOR;

EID: 84864591348     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3003358     Document Type: Article

References (45)

1. WHO The world health report 2004; WHO, 2004.
2. McConville, M. J.; de Souza, D.; Saunders, E.; Likic, V. A.; Naderer, T. Living in a phagolysosome; metabolism of Leishmania amastigotes Trends Parasitol. 2007, 23 (8) 368
3. Oliveira, F.; Jochim, R. C.; Valenzuela, J. G.; Kamhawi, S. Sand flies, Leishmania, and transcriptome-borne solutions Parasitol. Int. 2009, 58 (1) 1
4. Reithinger, R.; Dujardin, J. C.; Louzir, H.; Pirmez, C.; Alexander, B.; Brooker, S. Cutaneous leishmaniasis Lancet Infect. Dis. 2007, 7 (9) 581
5. Dedet, J. P. P., F. In Manson's tropical diseases; Cook, G. C. Z.; A., I., Ed. 2009.
6. Rosenthal, E.; Marty, P.; del Giudice, P.; Pradier, C.; Ceppi, C.; Gastaut, J. A.; Le Fichoux, Y.; Cassuto, J. P. HIV and Leishmania coinfection: a review of 91 cases with focus on atypical locations of Leishmania Clin. Infect. Dis. 2000, 31 (4) 1093
7. Beil, W. J.; Meinardus-Hager, G.; Neugebauer, D. C.; Sorg, C. Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice J. Leukoc. Biol. 1992, 52 (2) 135
8. Louis, J.; Moedder, E.; Behin, R.; Engers, H. Recognition of protozoan parasite antigens by murine T lymphocytes. I. Induction of specific T lymphocyte-dependent proliferative response to Leishmania tropica Eur. J. Immunol. 1979, 9 (11) 841
9. Mitchell, G. F.; Curtis, J. M.; Scollay, R. G.; Handman, E. Resistance and abrogation of resistance to cutaneous leishmaniasis in reconstituted BALB/c nude mice Aust. J. Exp. Biol. Med. Sci. 1981, 59 (Pt 5) 539
10. Howard, J. G.; Hale, C.; Chan-Liew, W. L. Immunological regulation of experimental cutaneous leishmaniasis. 1. Immunogenetic aspects of susceptibility to Leishmania tropica in mice Parasite Immunol. 1980, 2 (4) 303
11. Mosmann, T. R.; Coffman, R. L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties Annu. Rev. Immunol. 1989, 7145
12. Tato, C. M.; Laurence, A.; O'Shea, J. J. Helper T cell differentiation enters a new era: le roi est mort; vive le roi! J. Exp. Med. 2006, 203 (4) 809
13. O'Shea, J. J.; Paul, W. E. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells Science 2010, 327 (5969) 1098
14. Murphy, K. M.; Stockinger, B. Effector T cell plasticity: flexibility in the face of changing circumstances Nat. Immunol. 2010, 11 (8) 674
15. Noel, W.; Raes, G.; Hassanzadeh Ghassabeh, G.; De Baetselier, P.; Beschin, A. Alternatively activated macrophages during parasite infections Trends Parasitol. 2004, 20 (3) 126
16. Kropf, P.; Fuentes, J. M.; Fahnrich, E.; Arpa, L.; Herath, S.; Weber, V.; Soler, G.; Celada, A.; Modolell, M.; Muller, I. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo FASEB J. 2005, 19 (8) 1000
17. Alberati-Giani, D.; Malherbe, P.; Ricciardi-Castagnoli, P.; Kohler, C.; Denis-Donini, S.; Cesura, A. M. Differential regulation of indoleamine 2,3-dioxygenase expression by nitric oxide and inflammatory mediators in IFN-gamma-activated murine macrophages and microglial cells J. Immunol. 1997, 159 (1) 419
18. Li, P.; Yin, Y. L.; Li, D.; Kim, S. W.; Wu, G. Amino acids and immune function Br. J. Nutr. 2007, 98 (2) 237
19. Wu, G.; Meininger, C. J. Regulation of nitric oxide synthesis by dietary factors Annu. Rev. Nutr. 2002, 2261
20. Choi, B. S.; Martinez-Falero, I. C.; Corset, C.; Munder, M.; Modolell, M.; Muller, I.; Kropf, P. Differential impact of L-arginine deprivation on the activation and effector functions of T cells and macrophages J. Leukoc. Biol. 2009, 85 (2) 268
21. Kropf, P.; Baud, D.; Marshall, S. E.; Munder, M.; Mosley, A.; Fuentes, J. M.; Bangham, C. R.; Taylor, G. P.; Herath, S.; Choi, B. S.; Soler, G.; Teoh, T.; Modolell, M.; Muller, I. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy Eur. J. Immunol. 2007, 37 (4) 935
22. Modolell, M.; Choi, B. S.; Ryan, R. O.; Hancock, M.; Titus, R. G.; Abebe, T.; Hailu, A.; Muller, I.; Rogers, M. E.; Bangham, C. R.; Munder, M.; Kropf, P. Local suppression of T cell responses by arginase-induced L-arginine depletion in nonhealing leishmaniasis PLoS Negl. Trop. Dis. 2009, 3 (7) e480
23. Saric, J.; Li, J. V.; Wang, Y.; Keiser, J.; Veselkov, K.; Dirnhofer, S.; Yap, I. K.; Nicholson, J. K.; Holmes, E.; Utzinger, J. Panorganismal metabolic response modeling of an experimental Echinostoma caproni infection in the mouse J. Proteome Res. 2009, 8 (8) 3899
24. Wang, Y.; Utzinger, J.; Saric, J.; Li, J. V.; Burckhardt, J.; Dirnhofer, S.; Nicholson, J. K.; Singer, B. H.; Brun, R.; Holmes, E. Global metabolic responses of mice to Trypanosoma brucei brucei infection Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (16) 6127
25. Saric, J.; Li, J. V.; Swann, J. R.; Utzinger, J.; Calvert, G.; Nicholson, J. K.; Dirnhofer, S.; Dallman, M. J.; Bictash, M.; Holmes, E. Integrated cytokine and metabolic analysis of pathological responses to parasite exposure in rodents J. Proteome Res. 2010, 9 (5) 2255
26. Saric, J.; Li, J. V.; Utzinger, J.; Wang, Y.; Keiser, J.; Dirnhofer, S.; Beckonert, O.; Sharabiani, M. T.; Fonville, J. M.; Nicholson, J. K.; Holmes, E. Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain Mol. Syst. Biol. 2010, 6396
27. Birungi, G.; Chen, S. M.; Loy, B. P.; Ng, M. L.; Li, S. F. Metabolomics approach for investigation of effects of dengue virus infection using the EA.hy926 cell line J. Proteome Res. 2010, 9 (12) 6523
28. Ellis, J. K.; Chan, P. H.; Doktorova, T.; Athersuch, T. J.; Cavill, R.; Vanhaecke, T.; Rogiers, V.; Vinken, M.; Nicholson, J. K.; T, M. D. E.; Keun, H. C. Effect of the histone deacetylase inhibitor trichostatin a on the metabolome of cultured primary hepatocytes J. Proteome Res. 2010, 9 (1) 413
29. Ellis, J. K.; Athersuch, T. J.; Cavill, R.; Radford, R.; Slattery, C.; Jennings, P.; McMorrow, T.; Ryan, M. P.; Ebbels, T. M.; Keun, H. C. Metabolic response to low-level toxicant exposure in a novel renal tubule epithelial cell system Mol. Biosyst. 2011, 7 (1) 247
30. 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
31. Meiboom, S. G. D. Modified spin-echo method for measuring nuclear relaxation times Rev. Sci. Instrum. 1958, 29688
32. 1H NMR data sets Anal. Chem. 2005, 77 (5) 1282
33. Veselkov, K. A.; Vingara, L. K.; Masson, P.; Robinette, S. L.; Want, E.; Li, J. V.; Barton, R. H.; Boursier-Neyret, C.; Walther, B.; Ebbels, T. M.; Pelczer, I.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Optimized preprocessing of ultra-performance liquid chromatography/mass spectrometry urinary metabolic profiles for improved information recovery Anal. Chem. 2011, 83 (15) 5864
34. 1H NMR metabonomics Anal. Chem. 2006, 78 (13) 4281
35. Eriksson, L.; Antti, H.; Gottfries, J.; Holmes, E.; Johansson, E.; Lindgren, F.; Long, I.; Lundstedt, T.; Trygg, J.; Wold, S. Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics (gpm) Anal. Bioanal. Chem. 2004, 380 (3) 419
36. Trygg, J.; Holmes, E.; Lundstedt, T. Chemometrics in metabonomics J. Proteome Res. 2007, 6 (2) 469
37. 1H NMR spectroscopic metabonomic studies Anal. Chem. 2005, 77 (2) 517
38. Trygg, J. W. S. Orthogonal projections to latent structures (O-PLS) J. Chemom. 2002, 16 (3) 119
39. Munder, M.; Eichmann, K.; Modolell, M. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype J. Immunol. 1998, 160 (11) 5347
40. Opperdoes, F. R.; Coombs, G. H. Metabolism of Leishmania: proven and predicted Trends Parasitol. 2007, 23 (4) 149
41. Li, Z.; Vance, D. E. Phosphatidylcholine and choline homeostasis J. Lipid Res. 2008, 49 (6) 1187
42. Wyss, M.; Kaddurah-Daouk, R. Creatine and creatinine metabolism Physiol. Rev. 2000, 80 (3) 1107
43. Naderer, T.; McConville, M. J. The Leishmania -macrophage interaction: a metabolic perspective Cell Microbiol. 2008, 10 (2) 301
44. Garedew, A.; Henderson, S. O.; Moncada, S. Activated macrophages utilize glycolytic ATP to maintain mitochondrial membrane potential and prevent apoptotic cell death Cell Death Differ. 2010, 17 (10) 1540
45. Zeisel, S. H.; Mar, M. H.; Howe, J. C.; Holden, J. M. Concentrations of choline-containing compounds and betaine in common foods J. Nutr. 2003, 133 (5) 1302