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Interactions between immunity and metabolism – contributions from the metabolic profiling of parasite-rodent models

Published online by Cambridge University Press:  05 July 2010

J. SARIC*
Affiliation:
Biomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, Sir Alexander Fleming Building, SW7 2AZ, London, UK
*
*Corresponding author. Dr. Jasmina Saric, Biomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, Sir Alexander Fleming Building, SW7 2AZ, London, UK, Tel.: +44 20 7594-3899; Fax: +44 20 7595-3220; E-mail: [email protected]

Summary

A combined interdisciplinary research strategy is even more crucial in immunology than in many other biological sciences in order to comprehend the closely linked interactions between cell proliferation, molecular signalling and gene rearrangements. Because of the multi-dimensional nature of the immune system, an abundance of different experimental approaches has developed, with a main focus on cellular and molecular mechanisms. The role of metabolism in immunity has been underexplored so far, and yet researchers have made important contributions in describing associations of immune processes and metabolic pathways, such as the central role of the l-arginine pathway in macrophage activation or the immune regulatory functions of the nucleotides. Furthermore, metabolite supplement studies, including nutritional administration and labelled substrates, have opened up new means of manipulating immune mechanisms. Metabolic profiling has introduced a reproducible platform for systemic assessment of changes at the small-molecule level within a host organism, and specific metabolic fingerprints of several parasitic infections have been characterized by 1H NMR spectroscopy. The application of multivariate statistical methods to spectral data has facilitated recovery of biomarkers, such as increased acute phase protein signals, and enabled direct correlation to the relative cytokine levels, which encourages further application of metabolic profiling to explore immune regulatory systems.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Alberati-Giani, D., Malherbe, P., Ricciardi-Castagnoli, P., Kohler, C., Denis-Donini, S. and Cesura, A. M. (1997). Differential regulation of indoleamine 2,3-dioxygenase expression by nitric oxide and inflammatory mediators in IFN-gamma-activated murine macrophages and microglial cells. Journal of Immunology 159, 419426.CrossRefGoogle ScholarPubMed
Arita, M., Yoshida, M., Hong, S., Tjonahen, E., Glickman, J. N., Petasis, N. A., Blumberg, R. S. and Serhan, C. N. (2005). Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proceedings of the National Academy of Sciences, USA 102, 76717676.CrossRefGoogle Scholar
Bagga, D., Wang, L., Farias-Eisner, R., Glaspy, J. A. and Reddy, S. T. (2003). Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proceedings of the National Academy of Sciences, USA 100, 17511756.CrossRefGoogle ScholarPubMed
Bansal, V. and Ochoa, J. B. (2003). Arginine availability, arginase, and the immune response. Current Opinion in Clinical Nutrition and Metabolic Care 6, 223228.CrossRefGoogle ScholarPubMed
Barbul, A., Lazarou, S. A., Efron, D. T., Wasserkrug, H. L. and Efron, G. (1990). Arginine enhances wound healing and lymphocyte immune responses in humans. Surgery 108, 331336; discussion 336–337.Google ScholarPubMed
Basso, A. S., Cheroutre, H. and Mucida, D. (2009). More stories on Th17 cells. Cell Research 19, 399411.CrossRefGoogle ScholarPubMed
Belkaid, Y., Blank, R. B. and Suffia, I. (2006). Natural regulatory T cells and parasites: a common quest for host homeostasis. Immunological Reviews 212, 287300.CrossRefGoogle ScholarPubMed
Bell, J. D., Brown, J. C., Nicholson, J. K. and Sadler, P. J. (1987 a). Assignment of resonances for 'acute-phase' glycoproteins in high resolution proton NMR spectra of human blood plasma. FEBS Letters 215, 311315.CrossRefGoogle ScholarPubMed
Bell, J. D., Sadler, P. J., Macleod, A. F., Turner, P. R. and La Ville, A. (1987 b). 1H NMR studies of human blood plasma. Assignment of resonances for lipoproteins. FEBS Letters 219, 239243.Google Scholar
Belluzzi, A., Boschi, S., Brignola, C., Munarini, A., Cariani, G. and Miglio, F. (2000). Polyunsaturated fatty acids and inflammatory bowel disease. American Journal of Clinical Nutrition 71, 339S342S.CrossRefGoogle ScholarPubMed
Bender, J. G., Van Epps, D. E. and Stewart, C. C. (1986). A model for the regulation of myelopoiesis by specific factors. Journal of Leukocyte Biology, 39, 101111.CrossRefGoogle Scholar
Benowitz, L. I., Goldberg, D. E., Madsen, J. R., Soni, D. and Irwin, N. (1999). Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proceedings of the National Academy of Sciences, USA 96, 1348613490.CrossRefGoogle ScholarPubMed
Bettelli, E., Korn, T. and Kuchroo, V. K. (2007). Th17: the third member of the effector T cell trilogy. Current Opinion in Immunology 19, 652657.CrossRefGoogle ScholarPubMed
Bogdan, C. (2001). Nitric oxide and the immune response. Nature Immunology 2, 907916.CrossRefGoogle ScholarPubMed
Bogdan, C., Rollinghoff, M. and Diefenbach, A. (2000). Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology 12, 6476.CrossRefGoogle ScholarPubMed
Bollard, M. E., Garrod, S., Holmes, E., Lindon, J. C., Humpfer, E., Spraul, M. and Nicholson, J. K. (2000). High-resolution 1H and 1H-13C magic angle spinning NMR spectroscopy of rat liver. Magnetic Resonance in Medicine 44, 201207.Google Scholar
Bollard, M. E., Contel, N. R., Ebbels, T. M., Smith, L., Beckonert, O., Cantor, G. H., Lehman-Mckeeman, L., Holmes, E. C., Lindon, J. C., Nicholson, J. K. and Keun, H. C. (2009). NMR-based metabolic profiling identifies biomarkers of liver regeneration following partial hepatectomy in the rat. Journal of Proteome Research 9, 5969.CrossRefGoogle Scholar
Bollard, M. E., Murray, A. J., Clarke, K., Nicholson, J. K. and Griffin, J. L. (2003). A study of metabolic compartmentation in the rat heart and cardiac mitochondria using high-resolution magic angle spinning 1H NMR spectroscopy. FEBS Letters 553, 7378.CrossRefGoogle Scholar
Bollard, M. E., Stanley, E. G., Lindon, J. C., Nicholson, J. K. and Holmes, E. (2005). NMR-based metabonomic approaches for evaluating physiological influences on biofluid composition. NMR Biomedicine 18, 143162.CrossRefGoogle ScholarPubMed
Calder, P. C. (2008). Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Molecular Nutrition and Food Research 52, 885897.CrossRefGoogle ScholarPubMed
Calder, P. C. (2009). Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 91, 791795.CrossRefGoogle Scholar
Carver, J. D., Cox, W. I. and Barness, L. A. (1990). Dietary nucleotide effects upon murine natural killer cell activity and macrophage activation. Journal of Parenteral and Enteral Nutrition 14, 1822.Google Scholar
Caughey, G. E., Mantzioris, E., Gibson, R. A., Cleland, L. G. and James, M. J. (1996). The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. American Journal of Clinical Nutrition 63, 116122.CrossRefGoogle ScholarPubMed
Chen, P., Goldberg, D. E., Kolb, B., Lanser, M. and Benowitz, L. I. (2002). Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proceedings of the National Academy of Sciences, USA 99, 90319036.CrossRefGoogle ScholarPubMed
Chorazy, M., Kontny, E., Marcinkiewicz, J. and Maslinski, W. (2002). Taurine chloramine modulates cytokine production by human peripheral blood mononuclear cells. Amino Acids 23, 407413.CrossRefGoogle ScholarPubMed
Cleland, L. G., Caughey, G. E., James, M. J. and Proudman, S. M. (2006). Reduction of cardiovascular risk factors with longterm fish oil treatment in early rheumatoid arthritis. Journal of Rheumatology 33, 19731979.Google ScholarPubMed
Cleland, L. G. and James, M. J. (2000). Fish oil and rheumatoid arthritis: antiinflammatory and collateral health benefits. Journal of Rheumatology 27, 23052307.Google ScholarPubMed
Cook, S. P. and McCleskey, E. W. (2002). Cell damage excites nociceptors through release of cytosolic ATP. Pain 95, 4147.CrossRefGoogle ScholarPubMed
Cloarec, O., Dumas, M. E., Trygg, J., Craig, A., Barton, R. H., Lindon, J. C., Nicholson, J. K. and Holmes, E. (2005). Evaluation of the orthogonal projection on latent structure model limitations caused by chemical shift variability and improved visualization of biomarker changes in 1H NMR spectroscopic metabonomic studies. Analytical Chemistry 77, 517526.CrossRefGoogle ScholarPubMed
Crockford, D. J., Holmes, E., Lindon, J. C., Plumb, R. S., Zirah, S., Bruce, S. J., Rainville, P., Stumpf, C. L. and Nicholson, J. K. (2006). Statistical heterospectroscopy, an approach to the integrated analysis of NMR and UPLC-MS data sets: application in metabonomic toxicology studies. Analytical Chemistry 78, 363371.CrossRefGoogle Scholar
Cummings, J. H. (1981). Short chain fatty acids in the human colon. Gut 22, 763779.CrossRefGoogle ScholarPubMed
De Jonge, W. J., Kwikkers, K. L., Te Velde, A. A., Van Deventer, S. J., Nolte, M. A., Mebius, R. E., Ruijter, J. M., Lamers, M. C. and Lamers, W. H. (2002). Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice. Journal of Clinical Investigation 110, 15391548.CrossRefGoogle Scholar
Di Virgilio, F., Chiozzi, P., Ferrari, D., Falzoni, S., Sanz, J. M., Morelli, A., Torboli, M., Bolognesi, G. and Baricordi, O. R. (2001). Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 97, 587600.CrossRefGoogle ScholarPubMed
Dooper, M. M., Wassink, L., M'rabet, L. and Graus, Y. M. (2002). The modulatory effects of prostaglandin-E on cytokine production by human peripheral blood mononuclear cells are independent of the prostaglandin subtype. Immunology 107, 152159.CrossRefGoogle ScholarPubMed
Eritsland, J., Arnesen, H., Gronseth, K., Fjeld, N. B. and Abdelnoor, M. (1996). Effect of dietary supplementation with n-3 fatty acids on coronary artery bypass graft patency. American Journal of Cardiology 77, 3136.CrossRefGoogle ScholarPubMed
Fang, Y. Z., Yang, S. and Wu, G. (2002). Free radicals, antioxidants, and nutrition. Nutrition 18, 872879.CrossRefGoogle ScholarPubMed
Fanslow, W. C., Kulkarni, A. D., Van Buren, C. T. and Rudolph, F. B. (1988). Effect of nucleotide restriction and supplementation on resistance to experimental murine candidiasis. JPEN. Journal of Parenteral and Enteral Nutrition 12, 4952.Google Scholar
Foxall, P. J., Spraul, M., Farrant, R. D., Lindon, L. C., Neild, G. H. and Nicholson, J. K. (1993). 750 MHz 1H-NMR spectroscopy of human blood plasma. Journal of Pharmaceutical and Biomedical Analysis, 11, 267276.CrossRefGoogle ScholarPubMed
Garrod, S., Humpfer, E., Spraul, M., Connor, S. C., Polley, S., Connelly, J., Lindon, J. C., Nicholson, J. K. and Holmes, E. (1999). High-resolution magic angle spinning 1H NMR spectroscopic studies on intact rat renal cortex and medulla. Magnetic Resonance in Medicine 41, 11081118.3.0.CO;2-M>CrossRefGoogle Scholar
Goldsby, R. A., Kindt, T. J. and Osborne, B. A. (2001). Kuby Immunology, W. H. Freeman and Company, New York.Google Scholar
Gordon, S. (2003). Alternative activation of macrophages. Nature reviews. Immunology 3, 2335.CrossRefGoogle ScholarPubMed
Gounaris, K. (2002). Nucleotidase cascades are catalyzed by secreted proteins of the parasitic nematode Trichinella spiralis. Infection and immunity 70, 49174924.CrossRefGoogle ScholarPubMed
Gounaris, K. and Selkirk, M. E. (2005). Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends in Parasitology 21, 1721.Google Scholar
Griffith, R. S., Norins, A. L. and Kagan, C. (1978). A multicentered study of lysine therapy in Herpes simplex infection. Dermatologica 156, 257267.CrossRefGoogle ScholarPubMed
Grimble, R. F. and Grimble, G. K. (1998). Immunonutrition: role of sulfur amino acids, related amino acids, and polyamines. Nutrition 14, 605610.CrossRefGoogle ScholarPubMed
Grohmann, U., Fallarino, F. and Puccetti, P. (2003). Tolerance, DCs and tryptophan: much ado about IDO. Trends in Immunology 24, 242248.Google Scholar
Grootveld, M., Claxson, A. W., Chander, C. L., Haycock, P., Blake, D. R. and Hawkes, G. E. (1993). High resolution proton NMR investigations of rat blood plasma. Assignment of resonances for the molecularly mobile carbohydrate side-chains of ‘acute-phase’ glycoproteins. FEBS Letters 322, 266276.CrossRefGoogle ScholarPubMed
Guarner, F. and Malagelada, J. R. (2003). Gut flora in health and disease. Lancet 361, 512519.CrossRefGoogle ScholarPubMed
Hasko, G. and Cronstein, B. N. (2004). Adenosine: an endogenous regulator of innate immunity. Trends in Immunology 25, 3339.CrossRefGoogle ScholarPubMed
Hasko, G., Kuhel, D. G., Nemeth, Z. H., Mabley, J. G., Stachlewitz, R. F., Virag, L., Lohinai, Z., Southan, G. J., Salzman, A. L. and Szabo, C. (2000). Inosine inhibits inflammatory cytokine production by a posttranscriptional mechanism and protects against endotoxin-induced shock. Journal of Immunology 164, 10131019.CrossRefGoogle ScholarPubMed
Hasko, G., Sitkovsky, M. V. and Szabo, C. (2004). Immunomodulatory and neuroprotective effects of inosine. Trends in Pharmacological Sciences 25, 152157.CrossRefGoogle ScholarPubMed
Holmes, E., Loo, R. L., Stamler, J., Bictash, M., Yap, I. K., Chan, Q., Ebbels, T., De Iorio, M., Brown, I. J., Veselkov, K. A., Daviglus, M. L., Kesteloot, H., Ueshima, H., Zhao, L., Nicholson, J. K. and Elliott, P. (2008). Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 453, 396400.Google Scholar
Holmes, E., Tsang, T. M. and Tabrizi, S. J. (2006). The application of NMR-based metabonomics in neurological disorders. NeuroRx 3, 358372.CrossRefGoogle ScholarPubMed
Hudert, C. A., Weylandt, K. H., Lu, Y., Wang, J., Hong, S., Dignass, A., Serhan, C. N. and Kang, J. X. (2006). Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proceedings of the National Academy of Sciences, USA 103, 1127611281.CrossRefGoogle Scholar
Hunter, E. A. and Grimble, R. F. (1994). Cysteine and methionine supplementation modulate the effect of tumor necrosis factor alpha on protein synthesis, glutathione and zinc concentration of liver and lung in rats fed a low protein diet. Journal of Nutrition 124, 23192328.Google Scholar
Hunter, E. A. and Grimble, R. F. (1997). Dietary sulphur amino acid adequacy influences glutathione synthesis and glutathione-dependent enzymes during the inflammatory response to endotoxin and tumour necrosis factor-alpha in rats. Clinical Science (London, England : 1979) 92, 297305.CrossRefGoogle ScholarPubMed
Joosten, S. A. and Ottenhoff, T. H. (2008). Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination. Human Immunology 69, 760770.CrossRefGoogle ScholarPubMed
Jyonouchi, H. (1994). Nucleotide actions on humoral immune responses. Journal of Nutrition 124, 138S143S.CrossRefGoogle ScholarPubMed
Keun, H. C., Athersuch, T. J., Beckonert, O., Wang, Y., Saric, J., Shockcor, J. P., Lindon, J. C., Wilson, I. D., Holmes, E. and Nicholson, J. K. (2008). Heteronuclear 19F-1H statistical total correlation spectroscopy as a tool in drug metabolism: study of flucloxacillin biotransformation. Analytical Chemistry 80, 10731079.CrossRefGoogle ScholarPubMed
King, N. J. and Thomas, S. R. (2007). Molecules in focus: indoleamine 2,3-dioxygenase. International Journal of Biochemistry and Cell Biology 39, 21672172.CrossRefGoogle ScholarPubMed
Korn, T., Oukka, M., Kuchroo, V. and Bettelli, E. (2007). Th17 cells: effector T cells with inflammatory properties. Seminars in Immunology 19, 362371.Google Scholar
Kulkarni, A. D., Fanslow, W. C., Drath, D. B., Rudolph, F. B. and Van Buren, C. T. (1986 a). Influence of dietary nucleotide restriction on bacterial sepsis and phagocytic cell function in mice. Archives of Surgery 121, 169172.CrossRefGoogle ScholarPubMed
Kulkarni, A. D., Fanslow, W. C., Rudolph, F. B. and Van Buren, C. T. (1986 b). Effect of dietary nucleotides on response to bacterial infections. Journal of Parenteral and Enteral Nutrition 10, 169171.Google Scholar
Kulkarni, A. D., Rudolph, F. B. and Van Buren, C. T. (1994). The role of dietary sources of nucleotides in immune function: a review. Journal of Nutrition 124, 1442S1446S.Google Scholar
Lenz, E. M., Bright, J., Knight, R., Westwood, F. R., Davies, D., Major, H. and Wilson, I. D. (2005). Metabonomics with 1H-NMR spectroscopy and liquid chromatography-mass spectrometry applied to the investigation of metabolic changes caused by gentamicin-induced nephrotoxicity in the rat. Biomarkers 10, 173187.CrossRefGoogle Scholar
Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K. and Serhan, C. N. (2001). Lipid mediator class switching during acute inflammation: signals in resolution. Nature Immunology 2, 612619.Google Scholar
Li, J. V., Holmes, E., Saric, J., Keiser, J., Dirnhofer, S., Utzinger, J. and Wang, Y. (2009). Metabolic profiling of a Schistosoma mansoni infection in mouse tissues using magic angle spinning-nuclear magnetic resonance spectroscopy. International Journal for Parasitology 39, 547558.Google Scholar
Li, J. V., Wang, Y., Saric, J., Nicholson, J. K., Dirnhofer, S., Singer, B. H., Tanner, M., Wittlin, S., Holmes, E. and Utzinger, J. (2008). Global metabolic responses of NMRI mice to an experimental Plasmodium berghei infection. Journal of Proteome Research 7, 39483956.CrossRefGoogle Scholar
Li, Z. and Vance, D. E. (2008). Phosphatidylcholine and choline homeostasis. Journal of Lipid Research 49, 11871194.CrossRefGoogle ScholarPubMed
Li, P., Yin, Y. L., Li, D., Kim, S. W. and Wu, G. (2007). Amino acids and immune function. British Journal of Nutrition 98, 237252.CrossRefGoogle ScholarPubMed
Liaudet, L., Mabley, J. G., Pacher, P., Virag, L., Soriano, F. G., Marton, A., Hasko, G., Deitch, E. A. and Szabo, C. (2002). Inosine exerts a broad range of antiinflammatory effects in a murine model of acute lung injury. Annals of Surgery 235, 568578.Google Scholar
Linden, J. (2001). Molecular approach to adenosine receptors: receptor-mediated mechanisms of tissue protection. Annual Review of Pharmacology and Toxicology 41, 775787.CrossRefGoogle ScholarPubMed
Loscher, T. and Saathoff, E. (2008). Eosinophilia during intestinal infection. Best Practice and Research. Clinical Gastroenterology 22, 511536.Google Scholar
Marchesi, J. R., Holmes, E., Khan, F., Kochhar, S., Scanlan, P., Shanahan, F., Wilson, I. D. and Wang, Y. (2007). Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. Journal of Proteome Research 6, 546551.CrossRefGoogle ScholarPubMed
Martin, F. P., Verdu, E. F., Wang, Y., Dumas, M. E., Yap, I. K., Cloarec, O., Bergonzelli, G. E., Corthesy-Theulaz, I., Kochhar, S., Holmes, E., Lindon, J. C., Collins, S. M. and Nicholson, J. K. (2006). Transgenomic metabolic interactions in a mouse disease model: interactions of Trichinella spiralis infection with dietary Lactobacillus paracasei supplementation. Journal of Proteome Research 5, 21852193.CrossRefGoogle Scholar
Martin, F. P., Rezzi, S., Pere-Trepat, E., Kamlage, B., Collino, S., Leibold, E., Kastler, J., Rein, D., Fay, L. B. and Kochhar, S. (2009). Metabolic effects of dark chocolate consumption on energy, gut microbiota, and stress-related metabolism in free-living subjects. Journal of Proteome Research 8, 55685579.Google Scholar
McCloskey, M. A., Fan, Y. and Luther, S. (1999). Chemotaxis of rat mast cells toward adenine nucleotides. Journal of Immunology 163, 970977.CrossRefGoogle ScholarPubMed
Melillo, G., Cox, G. W., Biragyn, A., Sheffler, L. A. and Varesio, L. (1994). Regulation of nitric-oxide synthase mRNA expression by interferon-gamma and picolinic acid. Journal of Biological Chemistry, 269, 81288133.CrossRefGoogle ScholarPubMed
Mellor, A. L. and Munn, D. H. (2004). IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nature Reviews, Immunology 4, 762774.CrossRefGoogle ScholarPubMed
Miles, E. A., Allen, E. and Calder, P. C. (2002). In vitro effects of eicosanoids derived from different 20-carbon Fatty acids on production of monocyte-derived cytokines in human whole blood cultures. Cytokine 20, 215223.CrossRefGoogle ScholarPubMed
Miossec, P., Korn, T. and Kuchroo, V. K. (2009). Interleukin-17 and type 17 helper T cells. New England Journal of Medicine 361, 888898.Google Scholar
Moffett, J. R. and Namboodiri, M. A. (2003). Tryptophan and the immune response. Immunology and Cell Biology. 81, 247265.CrossRefGoogle ScholarPubMed
Mosmann, T. R., Cherwinski, H., Bond, M. W., Giedlin, M. A. and Coffman, R. L. (1986). Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 136, 23482357.CrossRefGoogle ScholarPubMed
Munn, D. H., Shafizadeh, E., Attwood, J. T., Bondarev, I., Pashine, A. and Mellor, A. L. (1999). Inhibition of T cell proliferation by macrophage tryptophan catabolism. Journal of Experimental Medicine 189, 13631372.Google Scholar
Navarro, J., Ruiz-Bravo, A., Jimenez-Valera, M. and Gil, A. (1996). Modulation of antibody-forming cell and mitogen-driven lymphoproliferative responses by dietary nucleotides in mice. Immunology Letters 53, 141145.CrossRefGoogle ScholarPubMed
Newsholme, P. and Newsholme, E. A. (1989). Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochemical Journal 261, 211218.Google Scholar
Nicholson, J. K., Foxall, P. J., Spraul, M., Farrant, R. D. and Lindon, J. C. (1995). 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Analytical Chemistry 67, 793811.CrossRefGoogle ScholarPubMed
Nicholson, J. K., Lindon, J. C. and Holmes, E. (1999). ‘Metabonomics’: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29, 11811189.CrossRefGoogle Scholar
Noel, W.,Raes, G.,Hassanzadeh Ghassabeh, G.,De Baetselier, P. and Beschin, A. (2004). Alternatively activated macrophages during parasite infections. Trends in Parasitology 20, 126133.Google Scholar
Peterson, J. D., Herzenberg, L. A., Vasquez, K. and Waltenbaugh, C. (1998). Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proceedings of the National Academy of Sciences, USA 95, 30713076.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. and Francischetti, I. M. (2003). Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology 48, 7388.CrossRefGoogle ScholarPubMed
Rodriguez, P. C., Zea, A. H., Desalvo, J., Culotta, K. S., Zabaleta, J., Quiceno, D. G., Ochoa, J. B. and Ochoa, A. C. (2003). l-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. Journal of Immunology 171, 12321239.Google Scholar
Rudolph, F. B., Kulkarni, A. D., Fanslow, W. C., Pizzini, R. P., Kumar, S. and Van Buren, C. T. (1990). Role of RNA as a dietary source of pyrimidines and purines in immune function. Nutrition 6, 4552; discussion 59–62.Google ScholarPubMed
Salek, R. M., Maguire, M. L., Bentley, E., Rubtsov, D. V., Hough, T., Cheeseman, M., Nunez, D., Sweatman, B. C., Haselden, J. N., Cox, R. D., Connor, S. C. and Griffin, J. L. (2007). A metabolomic comparison of urinary changes in type 2 diabetes in mouse, rat, and human. Physiological Genomics 29, 99108.CrossRefGoogle ScholarPubMed
Sanni, L. A., Thomas, S. R., Tattam, B. N., Moore, D. E., Chaudhri, G., Stocker, R. and Hunt, N. H. (1998). Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. American Journal of Pathology 152, 611619.Google ScholarPubMed
Saric, J., Li, J. V., Swann, J. R., Utzinger, J., Calvert, G., Nicholson, J. K., Dirnhofer, S., Dallman, M. D., Bictash, M. and Holmes, E. (2010). Integrated cytokine and metabolic analysis of pathological responses to parasite exposure in rodents. Journal of Proteome Research 7, 22552264.CrossRefGoogle Scholar
Saric, J., Li, J. V., Wang, Y., Keiser, J., Bundy, J. G., Holmes, E. and Utzinger, J. (2008 b). Metabolic profiling of an Echinostoma caproni infection in the mouse for biomarker discovery. PLoS Neglected Tropical Diseases 2, e254.CrossRefGoogle ScholarPubMed
Saric, J., Li, J. V., Wang, Y., Keiser, J., Veselkov, K., Dirnhofer, S., Yap, I. K., Nicholson, J. K., Holmes, E. and Utzinger, J. (2009). Panorganismal metabolic response modeling of an experimental Echinostoma caproni infection in the mouse. Journal of Proteome Research 8, 38993911.CrossRefGoogle ScholarPubMed
Saric, J., Wang, Y., Li, J., Coen, M., Utzinger, J., Marchesi, J. R., Keiser, J., Veselkov, K., Lindon, J. C., Nicholson, J. K. and Holmes, E. (2008 a). Species variation in the fecal metabolome gives insight into differential gastrointestinal function. Journal of Proteome Research 7, 352360.Google Scholar
Schuller-Levis, G. B. and Park, E. (2004). Taurine and its chloramine: modulators of immunity. Neurochemical Research 29, 117126.CrossRefGoogle ScholarPubMed
Seki, H., Tani, Y. and Arita, M. (2009). Omega-3 PUFA derived anti-inflammatory lipid mediator resolvin E1. Prostaglandins and Other Lipid Mediators 89, 126130.CrossRefGoogle ScholarPubMed
Serhan, C. N., Arita, M., Hong, S. and Gotlinger, K. (2004). Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their endogenous aspirin-triggered epimers. Lipids 39, 11251132.Google Scholar
Serhan, C. N., Clish, C. B., Brannon, J., Colgan, S. P., Chiang, N. and Gronert, K. (2000). Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. Journal of Experimental Medicine 192, 11971204.Google Scholar
Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P., Devchand, P. R., Mirick, G. and Moussignac, R. L. (2002). Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. Journal of Experimental Medicine 196, 10251037.Google Scholar
Shi, W., Meininger, C. J., Haynes, T. E., Hatakeyama, K. and Wu, G. (2004). Regulation of tetrahydrobiopterin synthesis and bioavailability in endothelial cells. Cell Biochemistry and Biophysics 41, 415434.Google Scholar
Thomas, S. R., Mohr, D. and Stocker, R. (1994). Nitric oxide inhibits indoleamine 2,3-dioxygenase activity in interferon-gamma primed mononuclear phagocytes. Journal of Biological Chemistry 269, 1445714464.CrossRefGoogle ScholarPubMed
Thomas, S. R. and Stocker, R. (1999). Redox reactions related to indoleamine 2,3-dioxygenase and tryptophan metabolism along the kynurenine pathway. Redox Report: Communications in Free Radical Research 4, 199220.Google Scholar
Thomas, S. R., Terentis, A. C., Cai, H., Takikawa, O., Levina, A., Lay, P. A., Freewan, M. and Stocker, R. (2007). Post-translational regulation of human indoleamine 2,3-dioxygenase activity by nitric oxide. Journal of Biological Chemistry 282, 2377823787.CrossRefGoogle ScholarPubMed
Tilley, S. L., Wagoner, V. A., Salvatore, C. A., Jacobson, M. A. and Koller, B. H. (2000). Adenosine and inosine increase cutaneous vasopermeability by activating A(3) receptors on mast cells. Journal of Clinical Investigation 105, 361367.Google Scholar
Troseid, M., Arnesen, H., Hjerkinn, E. M. and Seljeflot, I. (2009). Serum levels of interleukin-18 are reduced by diet and n-3 fatty acid intervention in elderly high-risk men. Metabolism 58, 15431549.CrossRefGoogle ScholarPubMed
Tsang, T. M., Griffin, J. L., Haselden, J., Fish, C. and Holmes, E. (2005). Metabolic characterization of distinct neuroanatomical regions in rats by magic angle spinning 1H nuclear magnetic resonance spectroscopy. Magnetic Resonance in Medicine 53, 10181024.Google Scholar
Tsang, T. M., Haselden, J. N. and Holmes, E. (2009). Metabonomic characterization of the 3-nitropropionic acid rat model of Huntington's disease. Neurochemical Research 34, 12611271.Google Scholar
Tsang, T. M., Huang, J. T., Holmes, E. and Bahn, S. (2006). Metabolic profiling of plasma from discordant schizophrenia twins: correlation between lipid signals and global functioning in female schizophrenia patients. Journal of Proteome Research 5, 756760.CrossRefGoogle ScholarPubMed
Vachier, I., Chanez, P., Bonnans, C., Godard, P., Bousquet, J. and Chavis, C. (2002). Endogenous anti-inflammatory mediators from arachidonate in human neutrophils. Biochemical and Biophysical Research Communications 290, 219224.Google Scholar
Wanasen, N. and Soong, L. (2008). l-arginine metabolism and its impact on host immunity against Leishmania infection. Immunologic Research 41, 1525.CrossRefGoogle ScholarPubMed
Wang, Y., Holmes, E., Nicholson, J. K., Cloarec, O., Chollet, J., Tanner, M., Singer, B. H. and Utzinger, J. (2004). Metabonomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification. Proceedings of the National Academy of Sciences, USA 101, 1267612681.CrossRefGoogle ScholarPubMed
Wang, Y., Tang, H., Holmes, E., Lindon, J. C., Turini, M. E., Sprenger, N., Bergonzelli, G., Fay, L. B., Kochhar, S. and Nicholson, J. K. (2005 a). Biochemical characterization of rat intestine development using high-resolution magic-angle-spinning 1H NMR spectroscopy and multivariate data analysis. Journal of Proteome Research 4, 13241329.Google Scholar
Wang, Y., Lawler, D., Larson, B., Ramadan, Z., Kochhar, S., Holmes, E. and Nicholson, J. K. (2007). Metabonomic investigations of aging and caloric restriction in a life-long dog study. Journal of Proteome Research, 6, 18461854.Google Scholar
Wang, Y., Tang, H., Nicholson, J. K., Hylands, P. J., Sampson, J. and Holmes, E. (2005 b). A metabonomic strategy for the detection of the metabolic effects of chamomile (Matricaria recutita L.) ingestion. Journal of Agricultural and Food Chemistry 53, 191196.Google Scholar
Wang, Y., Utzinger, J., Xiao, S. H., Xue, J., Nicholson, J. K., Tanner, M., Singer, B. H. and Holmes, E. (2006). System level metabolic effects of a Schistosoma japonicum infection in the Syrian hamster. Molecular and Biochemical Parasitology 146, 19.Google Scholar
Wang, Y., Utzinger, J., Saric, J., Li, J. V., Burckhardt, J., Dirnhofer, S., Nicholson, J. K., Singer, B. H., Brun, R. and Holmes, E. (2008). Global metabolic responses of mice to Trypanosoma brucei brucei infection. Proceedings of the National Academy of Sciences, USA 105, 61276132.Google Scholar
Wang, Y., Xiao, S. H., Xue, J., Singer, B. H., Utzinger, J. and Holmes, E. (2009). Systems metabolic effects of a Necator americanus infection in Syrian hamster. Journal of Proteome Research 8, 54425450.CrossRefGoogle ScholarPubMed
Waters, N. J., Garrod, S., Farrant, R. D., Haselden, J. N., Connor, S. C., Connelly, J., Lindon, J. C., Holmes, E. and Nicholson, J. K. (2000). High-resolution magic angle spinning 1H NMR spectroscopy of intact liver and kidney: optimization of sample preparation procedures and biochemical stability of tissue during spectral acquisition. Analytical Biochemistry 282, 1623.Google Scholar
Weiss, S. J., Klein, R., Slivka, A. and Wei, M. (1982). Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. Journal of Clinical Investigation 70, 598607.Google Scholar
Williams, H. R., Cox, I. J., Walker, D. G., North, B. V., Patel, V. M., Marshall, S. E., Jewell, D. P., Ghosh, S., Thomas, H. J., Teare, J. P., Jakobovits, S., Zeki, S., Welsh, K. I., Taylor-Robinson, S. D. and Orchard, T. R. (2009). Characterization of inflammatory bowel disease with urinary metabolic profiling. American Journal of Gastroenterology 104, 14351444.Google Scholar
Wilson, M. S., Mentink-Kane, M. M., Pesce, J. T., Ramalingam, T. R., Thompson, R. and Wynn, T. A. (2007). Immunopathology of schistosomiasis. Immunology and Cell Biology 85, 148154.CrossRefGoogle ScholarPubMed
Wong, J. T., Chan, M., Lee, D., Jiang, J. Y., Skrzypczak, M. and Choy, P. C. (2000). Phosphatidylcholine metabolism in human endothelial cells: modulation by phosphocholine. Molecular and Cellular Biochemistry 207, 95100.Google Scholar
Wong, J. T., de Souza, R., Kendall, C. W., Emam, A. and Jenkins, D. J. (2006). Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology, 40, 235243.Google Scholar
Woulfe, D., Yang, J. and Brass, L. (2001). ADP and platelets: the end of the beginning. Journal of Clinical Investigation 107, 15031505.Google Scholar
Wu, G. (1998). Intestinal mucosal amino acid catabolism. Journal of Nutrition 128, 12491252.CrossRefGoogle ScholarPubMed
Wu, G. Y., Field, C. J. and Marliss, E. B. (1991). Glutamine and glucose metabolism in rat splenocytes and mesenteric lymph node lymphocytes. American Journal of Physiology 260, E141E147.Google ScholarPubMed
Wu, G. and Meininger, C. J. (2002). Regulation of nitric oxide synthesis by dietary factors. Annual Review of Nutrition 22, 6186.Google Scholar
Yan, H., Peng, X., Huang, Y., Zhao, M., Li, F. and Wang, P. (2007). Effects of early enteral arginine supplementation on resuscitation of severe burn patients. Burns 33, 179184.Google Scholar
Yap, I. K., Li, J., Saric, J., Martin, F. P., Davies, H., Wang, Y., Wilson, I. D., Nicholson, J. K., Utzinger, J., Marchesi, J. R. and Holmes, E. (2008). Metabonomic and microbiological analysis of the dynamic effect of vancomycine-induced gut microbiota modification in the mouse. Journal of Proteome Research 7, 37183728.Google Scholar
Zeisel, S. H., Mar, M. H., Howe, J. C. and Holden, J. M. (2003). Concentrations of choline-containing compounds and betaine in common foods. Journal of Nutrition 133, 13021307.Google Scholar