Brain metabolic markers reflect susceptibility status in cytokine gene knockout mice with murine cerebral malaria

International Journal for Parasitology

Volumn 36, Issue 13, 2006, Pages 1409-1418

  Parekh, Sapan B ^a   Bubb, William A ^a   Hunt, Nicholas H ^a   Rae, Caroline ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

Author keywords

Cytopathic hypoxia; Glutamine; Metabolomics; Plasmodium berghei

Indexed keywords

BIOLOGICAL MARKER; CYTOKINE; GAMMA INTERFERON; GLUCOSE; GLUTAMINE; LYMPHOTOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; TRYPTOPHAN; TUMOR NECROSIS FACTOR;

BRAIN; GENE EXPRESSION; GENETIC MARKER; MALARIA; MODEL; PARASITIC DISEASE; PATHOGENICITY; RODENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MALARIA; BRAIN METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE MODEL; FEMALE; HIGH ENERGY PHOSPHATE; INFECTION SENSITIVITY; KNOCKOUT GENE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARASITEMIA; PHOSPHORYLATION; WILD TYPE;

ANIMALS; BRAIN; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DISEASE SUSCEPTIBILITY; GLUCOSE; GLUTAMINE; MAGNETIC RESONANCE SPECTROSCOPY; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

MURINAE; PLASMODIUM BERGHEI;

EID: 33749238497     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.07.004     Document Type: Article

References (66)

1. Arsenijevic D., Garcia I., Vesin C., Vesin D., Arsenijevic Y., Seydoux J., Girardier L., Ryffel B., Dulloo A., and Richard D. Differential roles of tumor necrosis factor-alpha and interferon-gamma in mouse hypermetabolic and anorectic responses induced by LPS. Eur. Cytokine Network 11 (2000) 662-668
2. Ashwal S., Holshouser B., Tong K., Serna T., Osterdock R., Gross M., and Kido D. Proton MR spectroscopy detected glutamate/glutamine is increased in children with traumatic brain injury. J. Neurotrauma 21 (2004) 1539-1552
3. Berendt A.R., Turner G., and Newbold C. Cerebral malaria: the sequestration hypothesis. Parasitol. Today 10 (1994) 412-414
4. Berg S., Sappington P.L., Guzik L.J., Delude R.L., and Fink M.P. Proinflammatory cytokines increase the rate of glycolysis and adenosine-5′-triphosphate turnover in cultured rat enterocytes. Crit. Care Med. 31 (2003) 1203-1212
5. Broer S., and Brookes N. Transfer of glutamine between astrocytes and neurons. J. Neurochem. 77 (2001) 705-719
6. Brown H., Turner G., Rogerson S., Tembo M., Mwenechanya J., Molyneux M., and Taylor T. Cytokine expression in the brain in human cerebral malaria. J. Inf. Dis. 180 (1999) 1742-1746
7. Cabantous S., Poudiougou B., Traore A., Keita M., Cisse M.B., Doumbo O., Dessein A.J., and Marquet S. Evidence that interferon-gamma plays a protective role during cerebral malaria. J. Inf. Dis. 192 (2005) 854-860
8. Cavender D.E., Edelbaum D., and Ziff M. Endothelial cell activation induced by tumor necrosis factor and lymphotoxin. Am. J. Pathol. 134 (1989) 551-560
9. Chan-Ling T., Neill A.L., and Hunt N.H. Early microvascular changes in murine cerebral malaria detected in retinal wholemounts. Am. J. Pathol. 140 (1992) 1121-1130
10. Chen Y.W., Zhao P., Borup R., and Hoffman E.P. Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J. Cell Biol. 151 (2000) 1321-1336
11. Clark C.J., Mackay G.M., Smythe G.A., Bustamante S., Stone T.W., and Phillips R.S. Prolonged survival of a murine model of cerebral malaria by kynurenine pathway inhibition. Inf. Immun. 73 (2005) 5249-5251
12. Clark I.A., Gray K.M., Rockett E.J., Cowden W.B., Rockett K.A., Ferrante A., and Aggarwal B.B. Increased lymphotoxin in human malarial serum, and the ability of this cytokine to increase plasma interleukin-6 and cause hypoglycaemia in mice: implications for malarial pathology. Trans. R. Soc. Trop. Med. Hygiene 86 (1992) 602-607
13. Day N.P., Hien T.T., Schollaardt T., Loc P.P., Chuong L.V., Chau T.T., Mai N.T., Phu N.H., Sinh D.X., White N.J., and Ho M. The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J. Inf. Dis. 180 (1999) 1288-1297
14. de Kossodo S., and Grau G.E. Profiles of cytokine production in relation with susceptibility to cerebral malaria. J. Immunol. 151 (1993) 4811-4820
15. Dobbie M., Crawley J., Waruiru C., Marsh K., and Surtees R. Cerebrospinal fluid studies in children with cerebral malaria: an excitotoxic mechanism?. Am. J. Trop. Med. Hygiene 62 (2000) 284-290
16. Dunne V.G., Bhattachayya S., Besser M., Rae C., and Griffin J.L. Metabolites from cerebrospinal fluid in aneurysmal subarachnoid haemorrhage correlate with vasospasm and clinical outcome: a pattern-recognition 1H NMR study. NMR Biomed. 18 (2005) 24-33
17. Engwerda C.R., Mynott T.L., Sawhney S., De Souza J.B., Bickle Q.D., and Kaye P.M. Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J. Exp. Med. 195 (2002) 1371-1377
18. Franke-Fayard B., Janse C.J., Cunha-Rodrigues M., Ramesar J., Buscher P., Que I., Lowik C., Voshol P.J., den Boer M.A., van Duinen S.G., Febbraio M., Mota M.M., and Waters A.P. Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc. Natl. Acad. Sci. USA 102 (2005) 11468-11473
19. Grau G.E., and de Kossodo S. Cerebral malaria: mediators, mechanical obstruction or more?. Parasitol. Today 10 (1994) 408-409
20. Grau G.E., Heremans H., Piguet P.F., Pointaire P., Lambert P.H., Billiau A., and Vassalli P. Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc. Natl. Acad. Sci. USA 86 (1989) 5572-5574
21. Greenwood B., and Mutabingwa T. Malaria in 2002. Nature 415 (2002) 670-672
22. Hansen A.M., Ball H.J., Mitchell A.J., Miu J., Takikawa O., and Hunt N.H. Increased expression of indoleamine 2,3-dioxygenase in murine malaria infection is predominantly localised to the vascular endothelium. Int. J. Parasitol. 34 (2004) 1309-1319
23. Haslett J.N., Sanoudou D., Kho A.T., Bennett R.R., Greenberg S.A., Kohane I.S., Beggs A.H., and Kunkel L.M. Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle. Proc. Natl. Acad. Sci. USA 99 (2002) 15000-15005
24. Hearn J., Rayment N., Landon D.N., Katz D.R., and de Souza J.B. Immunopathology of cerebral malaria: morphological evidence of parasite sequestration in murine brain microvasculature. Inf. Immun. 68 (2000) 5364-5376
25. Hunt N.H., and Grau G.E. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 24 (2003) 491-499
26. Hunt N.H., Golenser J., Chan-Ling T., Parekh S.B., Rae C., Potter S., Medana I.M., Miu J., and Ball H.J. Immunopathogenesis of cerebral malaria. Int. J. Parasitol. 36 (2006) 569-582
27. Kaiser K., Texier A., Ferrandiz J., Buguet A., Meiller A., Latour C., Peyron F., Cespuglio R., and Picot S. Recombinant human erythropoietin prevents the death of mice during cerebral malaria. J. Inf. Dis. 193 (2006) 987-995
28. Kennan R.P., Machado F.S., Lee S.C., Desruisseaux M.S., Wittner M., Tsuji M., and Tanowitz H.B. Reduced cerebral blood flow and N-acetyl aspartate in a murine model of cerebral malaria. Parasitol. Res. 96 (2005) 302-307
29. Koch O., Awomoyi A., Usen S., Jallow M., Richardson A., Hull J., Pinder M., Newport M., and Kwiatkowski D. IFNGR1 gene promoter polymorphisms and susceptibility to cerebral malaria. J. Inf. Dis. 185 (2002) 1684-1687
30. Krishna S., Shoubridge E.A., White N.J., Weatherall D.J., and Radda G.K. Plasmodium yoelii: blood oxygen and brain function in the infected mouse. Exp. Parasitol. 56 (1983) 391-396
31. Kupce E., and Freeman R. Adiabatic pulses for wideband inversion and broadband decoupling. J. Magn. Reson. A 115 (1995) 273-276
32. Le Belle J.E., Harris N.G., Williams S.R., and Bhakoo K.K. A comparison of cell and tissue extraction techniques using high-resolution 1H NMR spectroscopy. NMR Biomed. 15 (2002) 37-44
33. Lou J., Lucas R., and Grau G.E. Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin. Microbiol. Rev. 14 (2001) 810-820
34. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
35. Medana I.M., Hunt N.H., and Chan-Ling T. Early activation of microglia in the pathogenesis of fatal murine cerebral malaria. Glia 19 (1997) 91-103
36. Medana I.M., Chan-Ling T., and Hunt N.H. Reactive changes of retinal microglia during fatal murine cerebral malaria: effects of dexamethasone and experimental permeabilization of the blood-brain barrier. Am. J. Pathol. 156 (2000) 1055-1065
37. Medana I.M., Day N.P., Salahifar-Sabet H., Stocker R., Smythe G., Bwanaisa L., Njobvu A., Kayira K., Turner G.D., Taylor T.E., and Hunt N.H. Metabolites of the kynurenine pathway of tryptophan metabolism in the cerebrospinal fluid of Malawian children with malaria. J. Inf. Dis. 188 (2003) 844-849
38. Medana I.M., Hien T.T., Day N.P., Phu N.H., Mai N.T., Chu'ong L.V., Chau T.T., Taylor A., Salahifar H., Stocker R., Smythe G., Turner G.D., Farrar J., White N.J., and Hunt N.H. The clinical significance of cerebrospinal fluid levels of kynurenine pathway metabolites and lactate in severe malaria. J. Inf. Dis. 185 (2002) 650-656
39. 2+ exchange activity by interferon-γ in cultured rat microglia. J. Neurochem. 90 (2004) 784-791
40. Naressi A., Couturier C., Devos J.M., Janssen M., Mangeat C., de Beer R., and Graveron-Demilly D. Java-based graphical user interface for the MRUI quantitation package. Magma 12 (2001) 141-152
41. Neill A.L., and Hunt N.H. Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology 105 (1992) 165-175
42. Penet M.F., Viola A., Confort-Gouny S., Le Fur Y., Duhamel G., Kober F., Ibarrola D., Izquierdo M., Coltel N., Gharib B., Grau G.E., and Cozzone P.J. Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J. Neurosci. 25 (2005) 7352-7358
43. Perkmann T., Winkler H., Graninger W., Kremsner P.G., and Winkler S. Circulating levels of the interleukin (IL)-4 receptor and of IL-18 in patients with Plasmodium falciparum malaria. Cytokine 29 (2005) 153-158
44. Planche T., Dzeing A., Emmerson A.C., Onanga M., Kremsner P.G., Engel K., Kombila M., Ngou-Milama E., and Krishna S. Plasma glutamine and glutamate concentrations in Gabonese children with Plasmodium falciparum infection. Quart. J. Med. 95 (2002) 89-97
45. Rae C., Moussa C.E.-H., Griffin J.L., Parekh S.B., Bubb W.A., Hunt N.H., and Balcar V.J. A metabolomic approach to ionotropic glutamate receptor subtype function: a nuclear magnetic resonance in vitro investigation. J. Cerebral Blood Flow Metab. 14 (2006) 2006 26, 1005-1017
46. Renia L., Potter S., Mauduit M., Rosa D.S., Kayibanda M., Deschemin J.C., Snounou G., and Gruner A.C. Pathogenic T cells in cerebral malaria. Int. J. Parasitol. 36 (2006) 547-554
47. Rae C., Hare N., Bubb W.A., McEwan S.R., Broer A., McQuillan J.A., Balcar V.J., Conigrave A.D., and Broer S. Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: further evidence for metabolic compartmentation. J. Neurochem. 85 (2003) 503-514
48. Rae C., McQuillan J.A., Parekh S.B., Bubb W.A., Weiser S., Balcar V.J., Hansen A.M., Ball H.J., and Hunt N.H. Brain gene expression, metabolism, and bioenergetics: interrelationships in murine models of cerebral and noncerebral malaria. FASEB J. 18 (2004) 499-510
49. Ringwald P., Peyron F., Vuillez J.P., Touze J.E., Le Bras J., and Deloron P. Levels of cytokines in plasma during Plasmodium falciparum malaria attacks. J. Clin. Microbiol. 29 (1991) 2076-2078
50. Sanni L.A., Rae C., Maitland A., Stocker R., and Hunt N.H. Is ischemia involved in the pathogenesis of murine cerebral malaria?. Am. J. Pathol. 159 (2001) 1105-1112
51. Sanni L.A., Thomas S.R., Tattam B.N., Moore D.E., Chaudhri G., Stocker R., and Hunt N.H. Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am. J. Pathol. 152 (1998) 611-619
52. Sanni L.A., Fu S., Dean R.T., Bloomfield G., Stocker R., Chaudhri G., Dinauer M.C., and Hunt N.H. Are reactive oxygen species involved in the pathogenesis of murine cerebral malaria?. J. Inf. Dis. 179 (1999) 217-222
53. Schwarcz A., Natt O., Watanabe T., Boretius S., Frahm J., and Michaelis T. Localized proton MRS of cerebral metabolite profiles in different mouse strains. Magn. Reson. Med. 49 (2003) 822-827
54. Shin C.Y., Choi J.W., Ryu J.R., Ryu J.H., Kim W., Kim H., and Ko K.H. Immunostimulation of rat primary astrocytes decreases intracellular ATP level. Brain Res. 902 (2001) 198-204
55. Skinner T.E., and Bendall M.R. A phase-cycling algorithm for reducing sidebands in adiabatic decoupling. J. Magn. Reson. (1997) 474-478
56. Taylor T.E., Molyneux M.E., Wirima J.J., Fletcher K.A., and Morris K. Blood glucose levels in Malawian children before and during the administration of intravenous quinine for severe falciparum malaria. New Engl. J. Med. 319 (1988) 1040-1047
57. Turner G. Cerebral malaria. Brain Pathol. 7 (1997) 569-582
58. Turner G.D., Morrison H., Jones M., Davis T.M., Looareesuwan S., Buley I.D., Gatter K.C., Newbold C.I., Pukritayakamee S., Nagachinta B., et al. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am. J. Pathol. 145 (1994) 1057-1069
59. van Hensbroek M.B., Palmer A., Onyiorah E., Schneider G., Jaffar S., Dolan G., Memming H., Frenkel J., Enwere G., Bennett S., Kwiatkowski D., and Greenwood B. The effect of a monoclonal antibody to tumor necrosis factor on survival from childhood cerebral malaria. J. Inf. Dis. 174 (1996) 1091-1097
60. Vanhamme L., van den Boogaart A., and Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 129 (1997) 35-43
61. Voza T., Vigario A.M., Belnoue E., Gruner A.C., Deschemin J.C., Kayibanda M., Delmas F., Janse C.J., Franke-Fayard B., Waters A.P., Landau I., Snounou G., and Renia L. Species-specific inhibition of cerebral malaria in mice coinfected with Plasmodium spp. Inf. Immun. 73 (2005) 4777-4786
62. Warrell D.A., White N.J., Veall N., Looareesuwan S., Chanthavanich P., Phillips R.E., Karbwang J., Pongpaew P., and Krishna S. Cerebral anaerobic glycolysis and reduced cerebral oxygen transport in human cerebral malaria. Lancet 2 (1988) 534-538
63. White N.J., Miller K.D., Brown J., Marsh K., and Greenwood B. Prognostic value of CSF lactate in cerebral malaria. Lancet 1 (1987) 1261
64. WHO, 2000. Severe falciparum malaria. Trans. R. Soc. Trop. Med. Hygiene 94, S1-S90.
65. Yanez D.M., Manning D.D., Cooley A.J., Weidanz W.P., and van der Heyde H.C. Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 157 (1996) 1620-1624
66. Yang G., Kitagawa K., Matsushita K., Mabuchi T., Yagita Y., Yanagihara T., and Matsumoto M. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Res. 752 (1997) 209-218