Chronic overexpression of proinflammatory cytokines and histopathology in the brains of rats infected with Trypanosoma brucei

Journal of Comparative Neurology

Volumn 414, Issue 1, 1999, Pages 114-130

  Quan, Ning ^a,c   Mhlanga, Jama D M ^a   Whiteside, Michael B ^a   McCoy, Allison N ^a   Kristensson, Krister ^b   Herkenham, Miles ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Glial acidic fibrillary protein; Interleukin 1; Neurotoxicity; Nuclear factor B; Parasite infection; Tumor necrosis factor

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROSTAGLANDIN SYNTHASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTORADIOGRAPHY; CHOROID PLEXUS; HISTOCHEMISTRY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SILVER STAINING; TRYPANOSOMA BRUCEI; TRYPANOSOMIASIS;

ANIMALS; APOPTOSIS; ASTROCYTES; BRAIN; CYTOKINES; GENE EXPRESSION REGULATION; I-KAPPA B PROTEINS; IN SITU HYBRIDIZATION; INFLAMMATION; MALE; NERVE DEGENERATION; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 0033536947     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19991108)414:1<114::AID-CNE9>3.0.CO;2-G     Document Type: Article

References (57)

1. Akassoglou K, Probert L, Kontogeorgos G, Kollias G. 1997. Astrocyte-specific but not neuron-specific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J Immunol 158:438-445.
2. Angelov DN, Walther M, Streppel M, Guntinas-Lichius, O Neiss WF. 1998. The cerebral perivascular cells. Adv Anat Embryol Cell Biol 147:1-87.
3. Bentivoglio M, Grassi-Zucconi G, Olsson T, Kristensson K. 1994. Trypanosoma brucei and the nervous system. Trends Neurosci 17:325-329.
4. Bertrand I, Banlet J, Cicé A. 1935. Lésions histologiques des centres nerveux dans la trypanosomiase humaine. Ann Inst Pasteur 54:91-144.
5. Breder CD, Hazuka C, Ghayur T, Klug C, Huginin M, Yasuda K, Teng M, Saper CB. 1994. Regional induction of tumor necrosis factor α expression in the mouse brain after systemic lipopolysaccharide administration. Proc Natl Acad Sci USA 91:11393-11397.
6. Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP. 1996. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nature Med 2:788-794.
7. Buttini M, Boddeke H. 1995. Peripheral lipopolysaccharide stimulation induces interleukin-1 beta messenger RNAin rat brain microglial cells. Neuroscience 65:523-530.
8. Campbell IL. 1995. Neuropathogenic actions of cytokines assessed in transgenic mice. Int J Dev Neurosci 13:275-284.
9. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L. 1993. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA 90:10061-10065.
10. Cao C, Matsumura K, Yamagata K, Watanabe Y. 1995. Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain; its possible role in the febrile response. Brain Res 697:187-196.
11. Cao C, Matsumura K, Ozaki M, Watanabe Y. 1999. Lipopolysaccharide injected into the cerebral ventricle evokes fever through induction of cyclooxygenase-2 in brain endothelial cells. J Neurosci 19:716-725.
12. DeOlmos JS, Ingram WR. 1971. An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res 33:523-529.
13. Ghersi-Egea JF, Finnegan W, Chen JL, Fenstermacher JD. 1996. Rapid distribution of intraventricularly administered sucrose into cerebrospinal fluid cisterns via subarachnoid velae in rat. Neuroscience 75:1271-1288.
14. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzie JE, Graham DI, Roberts GW, Mrak RE. 1998. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol 8:65-72.
15. Hansen MK, Taishi P, Chen Z, Krueger JM. 1998. Vagotomy blocks the induction of interleukin-1β (IL-1β) mRNA in the brain of rats in response to systemic IL-1β. J Neurosci 18:2247-2253.
16. Hisahara S, Shoji S, Okano H, Miura M. 1997. ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J Neurochem 69:10-20.
17. Hunter CA, Gow JW, PG Kennedy, Jennings FW, Murray M. 1991. Immunopathology of experimental African sleeping sickness: detection of cytokine mRNAin the brains of Trypanosoma brucei brucei-infected mice. Infect Immunol 59:4636-4640.
18. Hunter CA, Jennings FW, Kennedy PG, Murray M. 1992. Astrocyte activation correlates with cytokine production in central nervous system of Trypanosoma brucei brucei-infected mice. Lab Invest 67:635-642.
19. Khurgel M, Koo AC, Ivy GO. 1996. Selective ablation of astrocytes by intracerebral injections of α-aminoadipate. Glia 16:351-358.
20. Klein MA, Moller JC, Jones LL, Bluethmann H, Kreutzberg GW, Raivich G. 1997. Impaired neuroglial activation in interleukin-6 deficient mice. Glia 19:227-233.
21. Konsman JP, Kelley K, Dantzer R. 1999. Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-1Β and inducible nitric oxide synthase in rat brain. Neuroscience 89:535-548.
22. Kopp E, Ghosh S. 1994. Inhibition of NF-κB by sodium salicylate and aspirin. Science 265:956-959.
23. Lacroix S, Rivest S. 1998. Effect of acute systemic inflammatory response and cytokines on the transcription of the genes encoding cyclooxygenase enzymes (COX-1 and COX-2) in the rat brain. J Neurochem 70:452-466.
24. Mabbott NA, Sutherland IA, Sternberg JM. 1994. Trypanosoma brucei is protected from the cytostatic effects of nitric oxide under in vivo conditions. Parasitol Res 80:687-690.
25. Mabbott NA, Sutherland IA, Sternberg JM. 1995. Suppressor macrophages in Trypanosoma brucei infection: nitric oxide is related to both suppressive activity and lifespan in vivo. Parasite Immunol 17:143-150.
26. Magez S, Lucas R, Darji A, Songa EB, Hamers R, De Baetselier P. 1993. Murine tumour necrosis factor plays a protective role during the initial phase of the experimental infection with Trypanosoma brucei brucei. Parasite Immunol 15:635-641.
27. Maimone D, Guazzi GC, Annunziata P. 1997. IL-6 detection in multiple sclerosis brain. J Neurol Sci 146:59-65.
28. McCann SM. 1997. The nitric oxide hypothesis of brain aging. Exp Gerontol 32:431-440.
29. Miyamoto S, Verma IM. 1995. Rel/NF-κB/IκB story. Adv Cancer Res 66:255-292.
30. Mog M, Harada M, Narabayashi H, Inagaki H, Minami M, Nagatsu T. 1996. Interleukin (IL)-1β, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease. Neurosci Lett 211:13-16.
31. Nadeau S, Rivest S. 1999. Regulation of the gene encoding tumor necrosis factor alpha (TNF-α) in the rat brain and pituitary in response in different models of systemic immune challenge. J Neuropathol Exp Neurol 58:61-77.
32. Nicotera P, Bonfoco E, Brune B. 1995. Mechanisms for nitric oxide-induced cell death: involvement of apoptosis. Adv Neuroimmunol 5:411-420.
33. + T cells: a trypanosome-released factor triggers interferon-γ production that stimulates parasite growth. Eur J Immunol 21:2447-2454.
34. Pasinetti GM. 1998. Cyclooxygenase and inflammation in Alzheimer's disease: experimental approaches and clinical interventions. J Neurosci Res 54:1-6.
35. Pentreath VW. 1995. Trypanosomiasis and the nervous system. Pathology and immunology. Trans Roy Soc Trop Med Hyg 89:9-15.
36. Pentreath VW, Baugh PJ, Lavin DR. 1994. Sleeping sickness and the central nervous system. Onderstepoort J Vet Res 61:369-377.
37. Plata-Salaman CR, Sonti G, Borkoski JP, Wilson CD, French-Mullen JM. 1996. Anorexia induced by chronic central administration of cytokines at estimated pathophysiological concentrations. Physiol Behav 60:867-875.
38. 14C]inulin in rat. Neuroscience (in press).
39. Quan N, Whiteside M, Kim L, Herkenham M. 1997. Induction of inhibitory factor κBα mRNA in the central nervous system after peripheral lipopolysaccharide administration: an in situ hybridization histochemistry study in the rat. Proc Natl Acad Sci USA 94:10985-10990.
40. Quan N, Whiteside M, Herkenham M. 1998a. Cyclooxygenase 2 mRNA expression in rat brain after peripheral injection of lipopolysaccharide. Brain Res 802:189-197.
41. Quan N, Whiteside M, Herkenham M. 1998b. Time course and localization patterns of interleukin-1β messenger RNA expression in brain and pituitary after peripheral administration of lipopolysaccharide. Neuroscience 83:281-293.
42. Quan N, Mhlanga JDM, Whiteside MB, Kristensson K, Herkenham M. 1999a. Chronic sodium salicylate treatment exacerbates brain neurodegeneration in rats infected with Trypanosoma brucei. Neuroscience (in press).
43. Quan N, Stern EL, Whiteside MB, Herkenham M. 1999b. Induction of pro-inflammatory cytokine mRNAs in the brain after peripheral injection of subseptic doses of lipopolysaccharide in the rat. J Neuroimmunol 93:72-80.
44. Schultzberg M, Ambatsis M, Samuelsson E-B, Kristensson K, van Meirvenne N. 1988. Spread of Trypanosoma brucei to the nervous system: early attack on circumventricular organs and sensory ganglia. J Neurosci Res 21:56-61.
45. Sternberg JM, Mabbott NA. 1996. Nitric oxide-mediated suppression of T cell responses during Trypanosoma brucei infection: soluble trypanosome products and interferon-γ are synergistic inducers of nitric oxide synthase. Eur J Immunol 26:539-543.
46. Strijbos PJ, Rothwell NJ. 1995. Interleukin-1β attenuates excitatory amino acid-induced neurodegeneration in vitro: involvement of nerve growth factor. J Neurosci 15:3468-3474.
47. Thea DM, Porat R, Nagimbi K, Baangi M, St Louis ME, Kaplan G, Dinarello CA, Keusch GT. 1996. Plasma cytokines, cytokine antagonists, and disease progression in African women infected with HIV-1. Ann Intern Med 124:757-762.
48. Tizard I, Nielsen KH, Seed JR, Hall JE. 1978. Biologically active products from African trypanosomes. Microbiol Rev 42:661-681.
49. Vaidya T, Bakhiet M, Hill KL, Olsson T, Kristensson K, Donelson JE. 1997. The gene for a T lymphocyte triggering factor from African trypanosomes. J Exp Med 186:433-438.
50. Vallières L, Rivest S. 1997. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1β. J Neurochem 69:1668-1683.
51. Vallières L, Lacroix S, Rivest S. 1997. Influence of interleukin-6 on neural activity and transcription of the gene encoding corticotrophin-releasing factor in the rat brain: an effect depending upon the route of administration. Eur J Neurosci 9:1461-1472.
52. van Bogaert L, Janssen P. 1957. Contribution á l'etude de la neurologie et neuropathologie de la trypanosomiase humaine. Ann Soc Belg Med Trop 37:379-426.
53. Vincendeau P, Daulouede S, Veyret B, Darde ML, Bouteille B, Lemesre JL. 1992. Nitric oxide-mediated cytostatic activity on Trypanosoma brucei gambiense and Trypanosoma brucei brucei. Exp Parasitol 75:353-360.
54. Whitfield HJ Jr, Brady LS, Smith MA, Mamalaki E, Fox, RJ Herkenham M. 1990. Optimization of cRNA probe in situ hybridization methodology for localization of glucocorticoid receptor mRNA in rat brain: a detailed protocol. Cell Mol Neurobiol 10:145-157.
55. Williams KC, Zhao RW, Ueno K, Hickey WF. 1996. PECAM-1 (CD31) expression in the central nervous system and its role in experimental allergic encephalomyelitis in the rat. J Neurosci Res 45:747-757.
56. Wong M-L, Bongiorno PB, Rettori V, McCann SM, Licinio J. 1997. Interleukin (IL) 1β, IL-1 receptor antagonist, IL-10, and IL-13 gene expression in the central nervous system and anterior pituitary during systemic inflammation: pathophysiological implications. Proc Natl Acad Sci USA 94:227-232.
57. Wong ML, Rettori V, al-Shekhlee A, Bongiorno PB, Canteros G, McCann SM, Gold PW, Licinio J. 1996. Inducible nitric oxide synthase gene expression in the brain during systemic inflammation. Nature Med 2:581-584.