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Differences in the neurochemical characteristics of the cortex and striatum of mice with cerebral malaria

Published online by Cambridge University Press:  13 December 2004

C. J. CLARK ,
R. S. PHILLIPS ,
R. B. McMILLAN ,
I. O. MONTGOMERY  and
T. W. STONE
C. J. CLARK
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
R. S. PHILLIPS
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
R. B. McMILLAN
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
I. O. MONTGOMERY
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
T. W. STONE
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
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Abstract

Fatal murine cerebral malaria is an encephalitis and not simply a local manifestation in the brain of a systemic process. Histopathologically, murine cerebral malaria has been characterized by monocyte adherence to the endothelium of the microvasculature, activation of microglial cells, swelling of endothelial cell nuclei, microvasculature damage, and breakdown of the blood-brain barrier with cerebral oedema. Brain parenchymal cells have been proposed to be actively involved in the pathogenesis of murine cerebral malaria. We, therefore, compared the neurochemical characteristics of Plasmodium berghei ANKA-infected mice with controls to determine whether cerebral malarial infection significantly impairs specific neuronal populations. Between 6 and 7 days after infection, we found a significant loss of neurones containing substance P, with preservation of cells containing somatostatin, neuropeptide Y and calbindin in the striatum of infected mice compared with controls. In the cortex of infected mice, we found a significant reduction in the number of cells containing substance P, somatostatin and neuropeptide Y. The number of calbindin-containing neurones was unchanged. This study found significant changes in the neurochemical characteristics of the cortex and striatum of mice infected with P. berghei ANKA, which may contribute to their cerebral symptoms.

Keywords

brain malariaimmunohistochemistrymouseneurotransmitterPlasmodium bergheiquinolinic acid
Type
Research Article
Information
Parasitology , Volume 130 , Issue 1 , January 2005 , pp. 23 - 29
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

BARLOW, C., HIROTSUNE, S., PAYLOR, R., LIYANAGE, M., ECKHAUS, M., COLLINS, F., SHILOH, Y., CRAWLEY, J. N., RIED, T., TAGLE, D. & WYNSHAW-BORIS, A. ( 1996). Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159–171.CrossRefGoogle Scholar
BEAL, M. F., KOWALL, N. W., SWARTZ, K. J., FERRANTE, R. J. & MARTIN, J. B. ( 1989). Differential sparing of somatostatin-neuropeptide Y and cholinergic neurons following striatal excitotoxin lesions. Synapse 3, 38–47.CrossRefGoogle Scholar
BEAL, M. F., FERRANTE, R. J., SWARTZ, K. J. & KOWALL, N. W. ( 1991). Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. Journal of Neuroscience 11, 1649–1659.CrossRefGoogle Scholar
BOEGMAN, R. J., SMITH, Y. & PARENT, A. ( 1987). Quinolinic acid does not spare striatal neuropeptide Y-immunoreactive neurons. Brain Research 415, 178–182.CrossRefGoogle Scholar
BOEGMAN, R. J. & PARENT, A. ( 1988). Differential sensitivity of neuropeptide Y, somatostatin and NADPH-diaphorase containing neurons in rat cortex and striatum to quinolinic acid. Brain Research 445, 358–362.CrossRefGoogle Scholar
CHANG-LING, T., NEILL, A. L. & HUNT, N. H. ( 1992). Early microvascular changes in murine cerebral malaria detected in retinal wholemounts. American Journal of Pathology 140, 1121–1130.Google Scholar
CUELLO, A. C., GALFRE, G. & MILSTEIN, C. ( 1979). Detection of substance P in the central nervous system by a monoclonal antibody. Proceedings of the National Academy of Sciences, USA 76, 3532–3536.CrossRefGoogle Scholar
DAVIES, S. W. & ROBERTS, P. J. ( 1987). No evidence for preservation of somatostatin-containing neurons after intrastriatal injections of quinolinic acid. Nature, London 327, 326–329.CrossRefGoogle Scholar
DOBBIE, M., CRAWLEY, J., WARUIRU, C., MARSH, K. & SURTEES, R. ( 2000). Cerebrospinal fluid studies in children with cerebral malaria: an excitotoxic mechanism? American Journal of Tropical Medicine and Hygiene 62, 284–290.Google Scholar
EILAM, R., PETER, Y., GRONER, Y. & SEGAL, M. ( 2003). Late degeneration of nigro-striatal neurons in ATM−/−mice. Neuroscience 121, 83–98.CrossRefGoogle Scholar
FIGUEREDO-CARDENAS, G., ANDERSON, K. D., CHEN, Q., VEENMAN, C. L. & REINER, A. ( 1994). Relative survival of striatal projection neurons and interneurons after intrastriatal injection of quinolinic acid in rats. Experimental Neurology 129, 37–56.CrossRefGoogle Scholar
FIGUEREDO-CARDENAS, G., CHEN, Q. & REINER, A. ( 1997). Age-dependent differences in survival of striatal somatostatin-NPY-NADPH-diaphorase-containing interneurons versus striatal projection neurons after intrastriatal injection of quinolinic acid in rats. Experimental Neurology 146, 444–457.CrossRefGoogle Scholar
FORLONI, G. L., ANGERETTI, N., RIZZI, M. & VEZZANI, A. ( 1992). Chronic infusion of quinolinic acid in rat striatum: effects on discrete neuronal populations. Journal of Neurological Science 108, 129–136.CrossRefGoogle Scholar
GRAU, G. E., PIGUET, P. F., ENGERS, H. D., LOUIS, J. A., VASSALLI, P. & LAMBERT, P. H. ( 1986). L3T4+ T lymphocytes play a major role in the pathogenesis of murine cerebral malaria. Journal of Immunology 137, 2348–2354.Google Scholar
HANSEN, A. M., DRIUSSI, C., TURNER, V., TAKIKAWA, O. & HUNT, N. H. ( 2000). Tissue distribution of indoleamine 2,3-dioxygenase in normal and malaria-infected tissue. Redox Report 5, 112–115.CrossRefGoogle Scholar
HUANG, Q., ZHOU, D., SAPP, E., AIZAWA, H., GE, P., BIRD, E. D., VONSATTEL, J. P. & DIFIGLIA, M. ( 1995). Quinolinic acid-induced increases in calbindin D28k immunoreactivity in rat striatal neurons in vivo and in vitro mimic the pattern seen in Huntington's disease. Neuroscience 65, 397–407.CrossRefGoogle Scholar
HUNT, N. H. & GRAU, G. E. ( 2003). Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends in Immunology 24, 491–499.CrossRefGoogle Scholar
JENNINGS, V. M., ACTOR, J. K., LAL, A. A. & HUNTER, R. L. ( 1997). Cytokine profile suggesting that murine cerebral malaria is an encephalitis. Infection and Immunity 65, 4883–4887.Google Scholar
JENNINGS, V. M., LAL, A. A. & HUNTER, R. L. ( 1998). Evidence for multiple pathologic and protective mechanisms of murine cerebral malaria. Infection and Immunity 66, 5972–5979.Google Scholar
KAWAGUCHI, Y. & SHINDOU, T. ( 1998). Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. The Journal of Neuroscience 18, 6963–6976.CrossRefGoogle Scholar
KIM, J. P. & CHOI, D. W. ( 1987). Quinolinate neurotoxicity in cortical cell culture. Neuroscience 23, 423–432.CrossRefGoogle Scholar
KOSSODO, S., MONSO, C., JUILLARD, P., VELU, T., GOLDMAN, M. & GRAU, G. E. ( 1997). Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology 91, 536–540.CrossRefGoogle Scholar
MA, N., MADIGAN, M. C., CHAN-LING, T. & HUNT, N. H. ( 1997). Compromised blood-nerve barrier, astrogliosis, and myelin disruption in optic nerves during fatal murine cerebral malaria. Glia 19, 135–151.3.0.CO;2-#>CrossRefGoogle Scholar
MATTSON, M. P., RYCHLIK, B., CHU, C. & CHRISTAKOS, S. ( 1991). Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 6, 41–51.CrossRefGoogle Scholar
MEDANA, I. M., HUNT, N. H. & CHAUDHRI, G. ( 1997). Tumor necrosis factor-alpha expression in the brain during fatal murine cerebral malaria: evidence for production by microglia and astrocytes. American Journal of Pathology 150, 1473–1486.Google Scholar
MEDANA, I. M., HIEN, T. T., DAY, N. P., PHU, N. H., MAI, N. T. H., VAN CHU'ONG, L., CHAU, T. T. H., TAYLOR, A., SALAHIFAR, H., STOCKER, R., SMYTHE, G., TURNER, G. D. H., FARRAR, J., WHITE, N. J. & HUNT, N. H. ( 2002 a). The clinical significance of cerebrospinal fluid levels of kynurenine pathway metabolites and lactate in severe malaria. Journal of Infectious Diseases 185, 650–656.Google Scholar
MEDANA, I. M., DAY, N. P., HIEN, T. T., MAI, N. T. H., BETHELL, D., PHU, N. H., FARRAR, J., ESIRI, M. M., WHITE, N. J. & TURNER, G. D. ( 2002 b). Axonal injury in cerebral malaria. American Journal of Pathology 160, 655–666.Google Scholar
MEDANA, I. M., DAY, N. P. J., SALAHIFAR-SABET, H., STOCKER, R., SMYTHE, G., BWANAISA, L., NJOBVU, A., KAYIRA, K., TURNER, G. D. H., TAYLOR, T. E. & HUNT, N. H. ( 2003). Metabolites of the kynurenine pathway of tryptophan metabolism in the cerebrospinal fluid of Malawian children with malaria. Journal of Infectious Diseases 188, 844–849.CrossRefGoogle Scholar
NEILL, A. L. & HUNT, N. H. ( 1992). Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology 105, 165–175.CrossRefGoogle Scholar
NEILL, A. L., CHANG-LING, T. & HUNT, N. H. ( 1993). Comparisons between microvascular changes in cerebral and non-cerebral malaria in mice, using the retinal whole-mount technique. Parasitology 107, 477–487.CrossRefGoogle Scholar
OO, M. M., AIKAWA, M., THAN, T., AYE, T. M., MYINT, P. T., IGARASHI, I. & SCHOENE, W. C. ( 1987). Human cerebral malaria: a pathological study. Journal of Neuropathology and Experimental Neurology 46, 223–231.CrossRefGoogle Scholar
REST, J. R. ( 1982). Cerebral malaria in inbred mice. I. A new model and its pathology. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 410–415.CrossRefGoogle Scholar
SANNI, L. A., THOMAS, S. R., TATTAM, B. N., MOORE, D. E., CHAUDHRI, G., STOCKER, R. & 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, 611–619.Google Scholar
SCHWARCZ, R., WHETSELL, W. O. & MANGANO, R. M. ( 1983). Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science 219, 316–318.CrossRefGoogle Scholar
STONE, T. W. & PERKINS, M. N. ( 1981). Quinolinic acid: a potent endogenous excitant at amino acid receptors in the CNS. European Journal of Pharmacology 72, 411–412.CrossRefGoogle Scholar
STONE, T. W. ( 1993). Neuropharmacology of quinolinic and kynurenic acids. Pharmacological Reviews 45, 309–379.Google Scholar
STONE, T. W. ( 1995). Neuropharmacology, 1st Edn. W. H. Freeman and Company Limited, Oxford.
STONE, T. W. ( 2001). Kynurenines in the CNS: from endogenous obscurity to therapeutic importance. Progress in Neurobiology 64, 185–218.CrossRefGoogle Scholar
THUMWOOD, C. M., HUNT, N. H., CLARK, I. A. & COWDEN, W. B. ( 1988). Breakdown of the blood-brain barrier in murine cerebral malaria. Parasitology 96, 579–589.CrossRefGoogle Scholar
TOHGI, H., UTSUGISAWA, K., YOSHIMURA, M., YAMAGATA, M., NAGANE, Y. & SAITOH, K. ( 1997). Reduction in the ratio of β-preprotachykinin to preproenkephalin messenger RNA expression in postmortem human putamen during aging and in patients with status lacunaris. Implications for the susceptibility to parkinsonism. Brain Research 768, 86–90.Google Scholar
WARRELL, D. A., WHITE, N. J., VEALL, N., LOOAREESUWAN, S., CHANTHAVANICH, P., PHILLIPS, R. E., KARBWANG, J., PONGPAEW, P. & KRISHNA, S. ( 1988). Cerebral anaerobic glycolysis and reduced cerebral oxygen transport in human cerebral malaria. Lancet 2, 534–538.CrossRefGoogle Scholar