Inducible nitric oxide synthase and nitrotyrosine in the central nervous system of mice chronically infected with Trypanosoma brucei brucei

Experimental Parasitology

Volumn 95, Issue 1, 2000, Pages 19-27

  Keita, Mahamane ^a   Vincendeau, Philippe ^b   Buguet, Alain ^c   Cespuglio, Raymond ^d   Vallat, Jean Michel ^a   Dumas, Michel ^a   Bouteille, Bernard ^e  

^a UNIVERSITY OF LIMOGES   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c CENTRE DE RECHERCHES   (France)

^d UNIVERSITÉ LYON 1   (France)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE;

AFRICAN TRYPANOSOMIASIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; FEMALE; MENINGOENCEPHALITIS; MOUSE; NERVE CELL LESION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI; TRYPANOSOMIASIS;

ANIMALIA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI BRUCEI;

EID: 0034047508     PISSN: 00144894     EISSN: None     Source Type: Journal    
DOI: 10.1006/expr.2000.4505     Document Type: Article

References (74)

1. Adams J. H., Haller L., Boa F. Y., Doua F., Dago H., Konian K. Human African trypanosomiasis (T. b. gambiense): A study of fatal cases of sleeping sickness with some observations on acute reactive arsenical encephalopathy. Neuropathology and Applied Neurobiology. 12:1986;81-94.
2. Akaike T., Noguchi Y., Ijiri S., Setoguchi K., Suga M., Zheng Y. M., Dietzschold B., Maeda H. Pathogenesis of influenza virus-induced pneumonia: Involvement of both nitric oxide and oxygen radicals. Proceedings of the National Academy of Sciences of the United States of America. 93:1996;2448-2453.
3. Albina J. E., Cui S., Mateo R. B., Reichner J. S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. Journal of Immunology. 150:1993;5080-5085.
4. Amin N., Pearce B. Peroxynitrite-induced toxicity in cultured astrocytes. Brain Research. 773:1997;227-230.
5. Basarga O., Michaels F. H., Zheng Y. M., Borboski L. E., Spitsin S. V., Fu Z. F., Tawardos R., Koprowski H. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proceedings of the National Academy of Sciences of the United States of America. 92:1995;12041-12045.
6. Beckman J. S., Beckman T. W., Chen J., Marshall P. A., Freeman B. A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences of the United States of America. 87:1990;1620-1624.
7. Beckman J. S., Ye Y. Z., Anderson P. G., Chen J., Accavitti M. A., Tarpey M. M., White C. R. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biological Chemistry Hoppe Seyler. 375:1994;81-88.
8. Bentivoglio M., Grassi-Zucconi G., Olsson T., Kristensson K. Trypanosoma brucei and the nervous system. Trends in Neuroscience. 17:1994;325-329.
9. Blaylock M. G., Cuthbertson B. H., Galley H. F., Ferguson N. R., Webster N. R. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radical Biology and Medicine. 25:1998;748-752.
10. Bouloumie A., Bauersachs J., Linz W., Scholkens B. A., Wiemer G., Flemming I., Busse R. Endothelial dysfunction coincides with an enhanced nitric oxide synthase expression and superoxide anion production. Hypertension. 30:1997;934-941.
11. Brenner T., Broke S., Szafer F., Sobel R. A., Parkinson J. F., Perez D. H., Steinman L. Inhibition of nitric oxide synthase for treatment of experimental autoimmune encephalomyelitis. Journal of Immunology. 158:1997;2940-2946.
12. Buguet A. Is sleeping sickness a circadian disorder? The serotonergic hypothesis. Chronobiology International. 16:1999;477-489.
13. Buguet A., Cespuglio R. Sleeping sickness: A disease of clock with nitric oxide involvement. Dumas M., Bouteille B., Buguet A. Progress in Human African Trypanosomiasis, Sleeping Sickness. 1999;191-201 Springer-Verlag, Paris.
14. Buguet A., Bert J., Tapie P., Tabaraud F., Doua F., Lonsdorfer J., Bogui P., Dumas M. Sleep-wake cycle in human African trypanosomiasis. Journal of Clinical Neurophysiology. 10:1993;190-196.
15. Buguet A., Burlet S., Auzelle F., Montmayeur A., Jouvet M., Cespuglio R. Dualité d'action du monoxyde d'azote (NO) dans la trypanosomose africaine expérimentale. Comptes Rendus de l'Académie des Sciences de Paris. 319:1996;201-207.
16. Carreras M. C., Pargament G. A., Catz S. D., Poderoso J., Boveris A. Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Letters. 341:1994;65-68.
17. Cobbs C. S., Brenman J. E., Aldape K. D., Bredt D. S., Israel M. A. Expression of nitric oxide synthase in human central nervous system tumors. Cancer Research. 55:1995;727-730.
18. Estévez A. G., Radi R., Barbeito L., Shin J. T., Thompson J. A., Beckman J. S. Peroxynitrite-induced cytotoxicity in PC12 cells: Evidence for an apoptotic mechanism differentially modulated by neurotrophic factors. Journal of Neurochemistry. 65:1995;1543-1550.
19. Ferrante R. J., Hantraye P., Brouillet E., Beal M. F. Increased nitrotyrosine immunoreactivity in substantia nigra neurons in MPTP treated baboons is blocked by inhibition of neuronal nitric oxide synthase. Brain Research. 823:1999;177-182.
20. Ferro T. J., Gertzberg N., Selden L., Neumann P., Johnson A. Endothelial barrier dysfunction and p42 oxidation induced by TNF-alpha are mediated by nitric oxide. American Journal of Physiology. 272:1997;979-988.
21. Giorgio S., Linares E., Capurro M. de L., De Bianchi A. G., Augusto O. Formation of nitrosyl hemoglobin and nitrotyrosine during murine leishmaniasis. Photochemistry and Photobiology. 63:1996;750-754.
22. Globus M. Y. T., Prado R., Busto P. Ischemia-induced changes in extracellular levels of striatal cyclic GMP: Role of nitric oxide. Neuro Report. 6:1995;1909-1912.
23. Good P. F., Werner P., Hsu A., Olanow C. W., Perl D. P. Evidence for neuronal oxidative damage in Alzheimer's disease. American Journal of Pathology. 149:1996;21-28.
24. Grosskinsky C. M., Ezekowitz R. A. B., Berton G., Gordon S., Askonas B. A. Macrophage activation in murine African trypanosomiasis. Infection and Immunity. 39:1983;1080-1086.
25. Haddad I. Y., Pataki G., Hu P., Galliani C., Beckman J. S., Matalon S. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. Journal of Clinical Investigations. 94:1994;2407-2413.
26. 2 and sleep. Annals of the New York Academy of Sciences. 559:1989;374-381.
27. Hu J., Ferreira A., van Eldik L. J. S100beta induces neuronal cell death through nitric oxide release from astrocytes. Journal of Neurochemistry. 69:1997;2294-2301.
28. Hunter C. A., Gows J. W., Kennedy P. G. E., Jennings F. W., Murray M. Immunopathology of experimental African sleeping sickness: Detection of cytokine mRNA in brains of Trypanosoma b. brucei infected mice. Infection and Immunity. 53:1991;4636-4640.
29. Ischiropoulos H. Biological tyrosine nitration: A pathophysiological function of nitric oxide and reactive oxygen species. Archives of Biochemistry and Biophysics. 356:1998;1-11.
30. Ischiropoulos H., Al-Mehdi A. B. Peroxynitrite-mediated oxidative proteins modifications. FEBS Letters. 364:1995;279-282.
31. Ischiropoulos H., Al-Mehdi A. B., Fisher A. B. Reactive species in ischemic rat lung injury: Contribution of peroxynitrite. American Journal of Physiology. 269:1995;L158-L164.
32. Kaur H., Halliwell B. Evidence for nitric oxide-mediated oxidative damage in chronic inflammation. Nitrotyrosine in serum and synovial fluid from rheumatoid patients. FEBS Letters. 350:1994;9-12.
33. Keita M., Bouteille B., Enanga B., Vallat J. M., Dumas M. Trypanosoma brucei brucei: A long-term model of human African trypanosomiasis in mice, meningo-encephalitis, astrocytosis, and neurological disorders. Experimental Parasitology. 85:1997;183-192.
34. Keller J. N., Kindy M. S., Holtsberg F. W., St Clair D. K., Yen H. C., Germeyer A., Steiner S. M., Bruce Keller A. J., Hutchins J. B., Mattson M. P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: Suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. Journal of Neurosciences. 18:1998;687-697.
35. Kooy N. W., Lewis S. J., Royall J. A., Ye Y. Z., Kelly D. R., Beckman J. S. Extensive tyrosine nitration in human myocardial inflammation: Evidence for the presence of peroxynitrite. Critical Care Medicine. 25:1997;812-819.
36. Kooy N. W., Royall J. A., Ye Y. Z., Kelly D. R., Beckman J. S. Evidence for in vivo peroxynitrite production in human acute lung injury. American Journal of Respiratory and Critical Care Medicine. 151:1995;1250-1254.
37. Landino L. M., Crews B. C., Timmons M. D., Morrow J. D., Marnett L. J. Peroxynitrite, the coupling product of nitric oxide and superoxide, activates prostaglandins biosynthesis. Proceedings of the National Academy of Sciences of the United States of America. 93:1996;15069-15074.
38. Leist M., Fava E., Monteccucco C., Nicotera P. Peroxynitrite and nitric oxide donors induce neuronal apoptosis by eliciting autocrine excitotoxicity. European Journal of Neuroscience. 9:1997;1488-1498.
39. Lorsbach R. B., Murphy W. J., Loweinstein C. J., Sneyder S. H., Russell S. W. Expression of nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-gamma and lipopolysaccharide. Journal of Biological Chemistry. 268:1993;1908-1913.
40. Mayhan W. G. Effect of lipopolysaccharide on the permeability and reactivity of the cerebral microcirculation: Role of inducible nitric oxide synthase. Brain Research. 792:1998;353-357.
41. Mésenge C., Charriaut Marlangue C., Verrecchia C., Allix M., Boulu R. R., Plotkine M. Reduction of tyrosine nitration after N(omega)-nitro-l-arginine-methylester treatment of mice with traumatic brain injury. European Journal of Pharmacology. 353:1998;53-57.
42. Moncada S. D., Higgs E. A. Endogenous nitric oxide: Physiology and clinical relevance. European Journal of Clinical Investigation. 21:1991;361-374.
43. Moncada S. D., Higgs E. A. The l-arginine-nitric oxide pathway. New England Journal of Medicine. 329:1993;2002-2012.
44. Nathan C. F. Nitric oxide as secretory product of mammalian cells. FASEB Journal. 6:1992;3051-3064.
45. Nussler A. K., Billiar T. R. Inflammation, immunoregulation and inducible nitric oxide synthase. Journal of Leukocyte Biology. 54:1993;171-178.
46. 2 is selectively elevated in cerebrospinal fluid of advanced sleeping sickness patients. Transactions of the Royal Society of Tropical Medicine and Hygiene. 84:1990;795-799.
47. Pryor W. A., Squadrito G. L. The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. American Journal of Physiology. 168:1995;L699-L722.
48. Reist M., Marshall K. A., Jenner P., Halliwell B. Toxic effect of sulphite in combination with peroxynitrite on neuronal cells. Journal of Neurochemistry. 71:1998;2431-2438.
49. Roldán E., Rodriguez C., Navas G., Parra C., Brieva J. A. Cytokine network regulating terminal maturation of human bone marrow B cells capable of spontaneous and high rate Ig secretion in vitro. Journal of Immunology. 149:1992;2367-2371.
50. Sandoval M., Zhang X. J., Liu X., Mannick E. E., Clark D. A., Miller M. J. Peroxynitrite-induced apoptosis in T84 and RAW 264.7 cells: Attenuation by l-ascorbic acid. Free Radical Biology and Medicine. 22:1997;489-495.
51. Schultz J. B., Matthews R. T., Jenkins B. G., Ferrante R. J., Siwek D., Henshaw D. R., Cipollini P. B., Mecocci P., Kowall N. W., Rosen B. R., Beal M. F. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. Journal of Neurosciences. 15:1995;8419-8429.
52. Segal A., Abo A. The biochemical basis of the NADPH oxidase of phagocytes. Trends in Biochemical Sciences. 18:1993;43-47.
53. Setoguchi K., Takeya M., Akaike T., Suga M., Hattori R., Maeda H., Ando M., Takahashi K. Expression of inducible nitric oxide synthase and its involvement in pulmonary granulomatous inflammation in rats. American Journal of Pathology. 149:1996;2005-2022.
54. Shibata M., Araki N., Hamada J., Sasaki T., Shimazu K., Fukuuchi Y. Brain nitrite production during ischemia and reperfusion: An in vivo microdyalisis study. Brain Research. 734:1996;86-90.
55. Souza-Filho M. V. P., Lima M. V. A., Pompeu M. M. L., Ballajo G., Cunha F. Q., Ribeiro R. de A. Involvement of nitric oxide in the pathogenesis of cyclophosphamide-induced hemorrhagic cystitis. American Journal of Pathology. 150:1997;247-256.
56. Sternberg J. M. Elevated serum nitrate in Trypanosoma brucei rhodesiense infections: Evidence for inducible nitric oxide synthesis in trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene. 90:1996;395.
57. Sternberg J. M., Mc Guignan F. Nitric oxide mediates suppression of T cell response in murine Trypanosoma brucei infection. European Journal of Immunology. 22:1992;2741-2744.
58. Sternberg J. M., Njogu Maina N., Gickhuki C. W., Ndung'U J. M. Nitric oxide production in vervet monkeys (Cercopithecus aethiops) infected with Trypanosoma brucei. Parasite Immunology. 20:1998;395-397.
59. Stojkovic T., Colin C., Le Saux F., Jacque C. Specific pattern of nitric oxide synthase expression in glial cells after hippocampal injury. Glia. 22:1998;329-337.
60. Szabo C. The pathophysiological role of peroxynitrite in shock, inflammation, and ischemia-reperfusion. Shock. 6:1996;79-88.
61. Szabo C., Cuzzocrea S., Zingarelli B., O'Connor M., Salzman A. L. Endothelial dysfunction in a rat model of endotoxic shock: Importance of activation of Poly (ADP-ribose) synthetase by peroxynitrite. Journal of Clinical Investigation. 100:1997;723-735.
62. Szabo C., Salzman A. L., Ischiropoulos H. Endotoxin triggers the expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in the rat aorta in vivo. FEBS Letters. 363:1995;235-238.
63. Takahashi M., Fukuda K., Ohata T., Sigimura T., Wakabayashi K. Increased expression of inducible and endothelial constitutive nitric oxide synthases in rat colon tumors induced by azoxymethane. Cancer Research. 57:1997;1233-1237.
64. Tayeh M. A., Marletta M. A. Macrophage oxydation of l-arginine to nitric oxide, nitrite, and nitrate: Tetrahydropterin is required as cofactor. Journal of Biological Chemistry. 264:1989;19654-19658.
65. Van der Veen R. C., Hinton D. R., Incardonna F., Hofman F. M. Extensive peroxynitrite activity during progressive stages of central nervous system inflammation. Journal of Neuroimmunology. 77:1997;1-7.
66. Van der Vliet A., O'neill C. A., Halliwell B., Cross C. E., Kaur H. Aromatic hydroxylation and nitration of phenylalanine and tyrosine by peroxynitrite: Evidence for hydroxyl radical production from peroxynitrite. FEBS Letters. 339:1994;89-92.
67. Vincendeau P., Daulouède S., Veyret B., Dardé M. L., Bouteille B., Lemesre J. L. Nitric oxide mediated cytostatic activity on Trypanosoma brucei gambiense and Trypanosoma brucei brucei. Experimental Parasitology. 75:1992;353-360.
68. Vincent S. R. Modern methods and applications. Panula P., Paivarinta H., Soinila S. Neurohistochemistry. 1986;375-396 A. R. Liss, New York.
69. Vincent S. R. Nitric oxide: A radical neurotransmitter in the central nervous system. Progress in Neurobiology. 42:1994;129-160.
70. Virag L., Scott G. S., Cuzzocrea S., Marmer D., Salzman A. L., Szabo C. Peroxynitrite-induced thymocyte apoptosis: The role of caspases and poly (ADP-ribose) synthase (PARS) activation. Immunology. 94:1998;345-355.
71. Vray B., de Baetselier P., Auaissi A., Carlier Y. Trypanosoma cruzi but not Trypanosoma brucei fails to induce a chemiluminescent signal in a macrophage hybridoma cell line. Infection and Immunity. 59:1991;3303-3308.
72. Wizemann T. M., Gardner C. R., Laskin J. D., Quinones S., Durham S. K., Goller N. L., Ohnishi S. T., Laskin D. L. Production of nitric oxide and peroxynitrite in the lung during acute endotoxemia. Journal of Leukocyte Biology. 56:1994;759-768.
73. Xie Q.-W., Cho H. J., Calaycay J., Mumford R. A., Swiderek K. M., Lee T. D., Ding A., Troso T., Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science. 256:1992;225-228.
74. Zhao W., Tilton R. G., Corbett J. A., McDaniel M. L., Misko T. P., Williamson J. R, Cross A. H., Hickey W. F. Experimental allergic encephalomyelitis in the rat is inhibited by aminoguanidine, an inhibitor of nitric oxide synthase. Journal of Neuroimmunology. 64:1996;123-133.