APOE and the regulation of microglial nitric oxide production: A link between genetic risk and oxidative stress

Neurobiology of Aging

Volumn 23, Issue 5, 2002, Pages 777-785

  Colton, Carol A ^a   Brown, Candice M ^a   Cook, Danielle ^a   Needham, Leila K ^a   Xu, Qing ^a   Czapiga, Meggan ^a   Saunders, Ann M ^a   Schmechel, Donald E ^a   Rasheed, Karima ^a   Vitek, Michael P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Apolipoprotein E; Arginine transport; Human macrophages; Microglia; Nitric oxide

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; ARGININE; ISOENZYME; MESSENGER RNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ALLELE; ALZHEIMER DISEASE; AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INDUCTION; ENZYME SPECIFICITY; GENE EXPRESSION; GENETIC RISK; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOREGULATION; MICROGLIA; MONOCYTE; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; ARGININE; CELLS, CULTURED; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MACROPHAGES, PERITONEAL; MICE; MICROGLIA; NITRIC OXIDE; OXIDATIVE STRESS; RISK FACTORS;

EID: 0036752024     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-4580(02)00016-7     Document Type: Article

References (82)

1. Akiyama H. Inflammatory response in Alzheimer's disease. Tohoku J. Exp. Med. 174:1994;295-303.
2. Alberts M., Grafagnino C., McClenny C., DeLong D., Strittmatter W., Saunders A.M.et al. ApoE genotype and survival from intracerebral hemorrhage. Lancet. 346:1995;8974-8977.
3. Bal-Price A., Brown G. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21:2001;6480-6491.
4. Barger S., Harmon A. Microglial activation by Alzheimer amyloid precursor protein and modulation by apolipoprotein E. Nature. 388:1997;878-881.
5. Bogle R.G., Baydoun A., Pearson J.D., Moncada S., Mann G. L-arginine transport is increased in macrophages generating nitric oxide. Biochem. J. 284:1992;15-18.
6. Boschert U., Merlo-Pich E., Higgins G., Ropses A., Catsicas S. Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol. Dis. 6:1999;508-514.
7. Bredt D. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Rad. Res. 31:1999;577-596.
8. Breitner J.C., Jarvik G., Plassman B.L., Saunders A.M., Welsh K.A. Risk of Alzheimer disease with the epsilon4 allele for apolipoprotein E in a population based study of men aged 62-73 years. Alzheimer Dis. Assoc. Disord. 12:1998;40-44.
9. Butterfield D. Alzheimer's disease: a disorder of oxidative stress. Alzheimer's Dis. Rev. 1:1996;68-70.
10. Chao C., Hu S., Molitor T., Shaskan E., Peterson P. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 149:1992;2736-2741.
11. Closs E., Scheld J., Sharafi M., Forstermann U. Substrate supply for nitric oxide synthase in macrophages and endothelial cells: role of cationic amino acid transporters. Mol. Pharmacol. 57:2000;68-74.
12. Cohen G, Werner P. Free radicals, oxidative stress and neurodegeneration. In: Calne D, editor. Neurodegenerative diseases. Philadelphia: Saunders, 1996. p. 139-61.
13. Colton C.A., Abel C., Patchett J., Keri J., Yao J. Lectin staining of cultured CNS microglia. J. Histochem. Cytochem. 40:1992;505-512.
14. Colton C.A., Chernyshev O., Gilbert D., Vitek M.P. Microglial contribution to oxidative stress in Alzheimer's disease. Ann. NY Acad. Sci. 899:2000;292-301.
15. Colton CA, Snell J, Cherynshev O, Gilbert D. Induction of superoxide anion and nitric oxide production in cultured microglia. In: Chieuh C, Gilbert D, Colton CA, editors. The neurobiology of NO and OH. New York: Annals of the New York Academy of Sciences, 1994. p. 54-63.
16. Colton CA, Yao J, Keri J, Gilbert D. Regulation of microglial function by interferons. J Neuroimmunol 1992;30:89-98.
17. Colton C.A., Czapiga M., Snell-Callanan J., Cherynshev O., Vitek M.P. Apolipoprotein E acts to increase NO production in macrophages by stimulating arginine transport. Biochem. Biophys. Acta. 1535:2001;134-144.
18. Denis M. Human monocytes/macrophages: NO or no NO? J. Leukocyte Biol. 55:1994;682-684.
19. Deves R., Boyd C.A. Transporters for cationic amino acids in animal cells: discovery, structure and function. Physiol. Rev. 78:1998;487-545.
20. Dugas N., Lacroix C., Kilchnerr E., Deitcaissy J., Tardieu M. Role of CD23 in astrocytes inflammatory reaction during HIV-1 related encephalitis. Cytokine. 15:2001;96-107.
21. Egensperger R., Kosel S., Von Eitzen U., Graeber M.B. Microglial activation in Alzheimer's disease: association with APOE genotype. Mol. Neuropathol. 8:1919;439-447.
22. Eikelenboom P., Rosemuller J.M., Van Muiswinkel F. Inflammation and Alzheimer's disease: relationships between pathogenic mechanisms and clinical expression. Exp. Neurol. 154:1998;89-98.
23. Floyd R Neuroinflammatory processes are important in neurodegenerative diseases: an hypothesis to explain the increased formation of reactive oxygen and nitrogen species as major factors involved in neurodegenerative disease development. Free Rad. Biol. Med. 26:1999;1346-1355.
24. Friedman G., Froom P., Sazbon L., Grinblatt I., Shochina M., Tsenter J.et al. Apolipoprotein E-epsilon4 genotype predicts a poor outcome in survivors of traumatic brain injury. Neurology. 52:1999;244-248.
25. Giulian D., Baker T. Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6:1986;2163-2178.
26. Goodwin J., Uemura E., Cunnick J.E. Microglial release of nitric oxide by the synergistic action of β-amyloid and IFN-γ Brain Res. 692:1995;207-214.
27. Griffin W.S.T., Sheng J., Royston M., Gentleman S., McKenzie J., Graham D.et al. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol. 8:1998;65-72.
28. Griffin W.S.T., Stanley L., Ling C., White L., MacLeod C., Perrot L.et al. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Nat. Acad. Sci. USA. 86:1989;7611-7615.
29. Grootendorst J., Mulder M., Haasdijk E., deKloet E., Jaarsma D. Presence of apolipoprotein E immunoreactivity in degenerating neurones of mice is dependent on the severity of kainic acid induced lesions. Brain Res. 868:2000;165-175.
30. Hibbs J.B. Jr., Vavrin Z., Taintor R. L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J. Immunol. 138:1987;550-565.
31. Horsburgh K., McCulloch J., Nilsen M., Roses A., Nicoll J. Increased neuronal damage and apoE immunoreactivity in human apolipoprotein E, E4 isoform-specific transgenic mice after global ischemia. Eur. J. Neurosci. 12:2000;4309-4317.
32. Ii M., Sunamoto M., Ohnishi K., Ichimori Y. β-amyloid protein dependent nitric oxide production from microglial cells and neurotoxicity. Brain Res. 720:1996;93-100.
33. Jordan B., Relkin N., Ravdin L., Jacobs A., Bennett A., Gandy S. Apolipoprotein E-epsilon4 associated with chronic traumatic brain injury in boxing. J. Am. Med. Soc. 278:1997;2143-2145.
34. Kakuda D., Sweet M.J., MacLeod C., Hume D., Markovich D. CAT2-mediated L-arginine transport and nitric oxide production in activated macrophages. Biochem. J. 340:1999;549-553.
35. Kalmar B., Kittel A., Lemmens R., Kornyei Z., Madarasz E. Cultured astrocytes react to LPS with increased cyclooxygenase activity and phagocytosis. Neurochem. Int. 38:2001;453-461.
36. Klegeris A., McGeer P. β-amyloid protein enhances macrophage production of oxygen free radicals and glutamate. J. Neurosci. Res. 49:1997;229-235.
37. Kutner K., Erlanger D., Tsai J., Jordan B., Relkin N. Lower cognitive performance of older football players possessing apolipoprotein E-epsilon4. Neurosurgery. 47:2000;651-657.
38. Lau L., Yu A. Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon gamma following traumatic and metabolic injury. J. Neurotrauma. 18:2001;351-359.
39. Lerma J., Herranz A.S., Herreras O., Abraira V., Martin Del Rio R. In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res. 384:1986;145-155.
40. Lichtman S., Seliger G., Tycki B., Marder K. Apolipoprotein E and functional recovery from brain injury following post-acute rehabilitation. Neurology. 55:2000;1536-1539.
41. Lu F., Selak M., O'Connor J., Croul S., Lorenzana C., Butunoi C.et al. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J. Neurol. Sci. 177:2000;95-103.
42. MacLeod C. Regulation of cationic amino acid transporter (CAT) gene expression. Biochem. Soc. Trans. 24:1996;846-852.
43. MacLeod C., Finley K., Kakuda D. y+-Type cationic amino acid transport: expression and regulation of the mCAT genes. J. Exp. Biol. 196:1994;109-121.
44. Mahley R.W., Huang Y. Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr. Opin. Lipidol. 10:1999;207-217.
45. Maneerat Y., Viriyavejakul P., Punpoowang B., Jones M., Wilairatana P., Pongponratn E.et al. Inducible nitric oxide expression is increased in the brain in fatal cerebra malaria. Histopathology. 37:2000;269-277.
46. McGeer P., Itagaki S., Tago H., McGeer E. Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci. Lett. 79:1987;195-200.
47. Meda L., Cassatella M., Szendrel G., Otvos L., Baron P., Villalba M.et al. Activation of microglial cells by β-amyloid protein and interferon-γ Nature. 374:1995;647-650.
48. Miles A., Bohle S., Glassbrenner P., Hansert B., Wink D., Grisham M. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J. Biol. Chem. 271:1996;40-47.
49. Miyata M., Smith J. Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and β-amyloid peptides. Nature Genetics. 14:1996;55-61.
50. Moncada S., Higgs E. Endogenous nitric oxide: physiology, pathology and clinical relevance. Eur. J. Clin. Invest. 21:1991;361-374.
51. Nicholson B., Manner C., Kleeman J., MacLeod C. Sustained NO production in macrophages requires the arginine transporter. J. Biol. Chem. 273:2001;15881-15883.
52. Ohm T.G., Scharnagl H., Marz W., Bohl J. Apolipoprotein E isoforms and the development of low and high Braak stages of Alzheimer's disease-related lesions. Acta Neuropathol. (Berlin). 98:1999;273-280.
53. Piani D., Constram D., Frei K., Fontana A. Macrophages in the brain: friends or enemies? NIPS. 9:1994;80-84.
54. Pitas R., Boyles J., Lee S., Foss D., Mahley R. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotin E-containing lipoproteins. Biochim. Biophys. Acta. 917:1987;148-161.
55. Poirier J., Davignon J., Bouthillier D., Kogan S., Bertrand P., Gauthier S. Apolipoprotein E polymorphism and Alzheimer's disease. Lancet. 342:1993;697-699.
56. Practico D., Delanty N. Oxidative injury in diseases of the central nervous system: focus on Alzheimer's disease. Am. J. Med. 109:2000;577-585.
57. Praprotnik D., Smith M., Richey P., Vinters H., Perry G. Plasma membrane fragility in dystrophic neurites in senile plaques of Alzheimer's disease: an index of oxidative stress. Acta Neuropathol. 91:1996;1-5.
58. Roses A.D. Apolipoprotein E, a gene with complex biological interactions in the aging brain. Neurobiol. Dis. 4:1997;170-185.
59. Sabo T., Lomnitski L., Nyska A., Beni S., Maronpot R., Shohami E.et al. Susceptibility of transgenic mice expressing human apolipoprotein E to closed head injury: the allele E3 is neuroprotective whereas E4 increases fatalities. Neuroscience. 101:2000;879-884.
60. Samatovicz R. Genetics and brain injury: apolipoprotein E. J. Head Trauma Rehabil. 15:2000;869-874.
61. Sato H., Ishii T., Sugita Y., Bannai S. Induction of cationic amino acid transport activity in mouse peritoneal macrophages by lipopolysaccharide. Biochem. Biophys. Acta. 1069:1991;46-52.
62. Saunders A.M. Apolipoprotein E and Alzheimer's disease: an update on genetic and functional analyses. J. Neuropathol. Exp. Neurol. 59:2000;751-758.
63. Schmechel D.E., Saunders A.M., Strittmatter W., Crain B., Hulette C., Joo S.et al. Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA. 90:1996;9649-9653.
64. Sheng H., Laskowitz D., Bennett E., Schmechel D.E., Bart R., Saunders A.M.et al. Apolipoprotein E isoform-specific differences in outcome from focal ischemia in transgenic mice. J. Cereb. Blood Flow Metab. 18:1998;361-366.
65. Sheng J., Mrak R., Griffin W.S.T. Neuritic plaque evolution in Alzheimer's disease is accompanied by transition of activated microglia from primed to enlarged to phagocytic. Acta Neuropathol. 94:1997;1-5.
66. Smith M., Harris P., Sayre L., Perry G. Iron accumulation in Alzheimer disease is a source of redox generated free radicals. Proc. Natl. Acad. Sci. USA. 94:1997;9866-9868.
67. Smith M., Hirai K., Hsiao K., Pappolla M., Harris P., Siedlak S.et al. Amyloid-β deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem. 70:2001;2212-2215.
68. Snell J.C., Chernyshev O., Gilbert D., Colton C.A. Polyribonucleotides induce nitric oxide production by human monocyte-derived macrophages. J. Leukocyte Biol. 62:1997;369-373.
69. Stevens B.R., Kakuda D., Yu K., Waters M., Vo C., Raizada M. Induced nitric oxide synthesis is dependent on induced alternatively spliced CAT-2 encoding L-arginine transport in brain astrocytes. J. Biol. Chem. 271:1996;24017-24022.
70. Streit W., Colton C.A. The Brain's immune system. Sci. Am. 273:1995;38.
71. Styren S., Kamboh M.I., Dekosky S. Expression of differential immune factors in temporal cortex and cerebellum: the role of a-1-antichymotrypsin, apolipoprotein E and reactive glia in the progression of Alzheimer's disease. J. Comp. Neurol. 396:1998;511-520.
72. Sullivan P., Mezour H., Quarfordt S.H., Maeda N. Type III hyperlipoproteinemia and spontaneous athersclerosis in mice resulting from gene replacement of mouse apoe with human apoe2. J. Clin. Invest. 102:1998;130-135.
73. Van Muiswinkel F., Veerhuis R. Amyloid β protein primes cultured rat microglial cells for an enhanced phorbol 12-myristate 13-acetate induced respiratory burst activity. J. Neurochem. 66:1996;2468-2476.
74. Vitek M.P., Snell J., Chernyshev O., Colton C.A. Modulation of nitric oxide production in human macrophages by apolipoprotein E and amyloid beta peptide. Biophys. Biochem Res. Comm. 240:1997;391-394.
75. Vodovotz Y., Lucia S., Flanders K., Chesler L., Xie Q.-W., Smith T.et al. Inducible nitric oxide synthase in tangle bearing neurons of patients with Alzheimer's disease. J. Exp. Med. 184:1996;1425-1433.
76. Wallace M., Geddes J., Farquhar D., Masson M. Nitric oxide synthase in reactive astrocytes adjacent to β-amyloid plaques. Exp. Neurol. 144:1997;266-272.
77. Weinberg J.B., Misukonis M.A., Shami P.J., Mason S.N., Sauls D.L., Dittman W.A.et al. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood. 86(3):1995;1184-1195.
78. White F., Nicoll J., Roses A., Horsburgh K. Impaired neuronal plasticity in transgenic mice expressing human apolipoprotein e4 compared to e3 in a model of entorhinal cortex lesion. Neurobiol. Dis. 8:2001;611-625.
79. Wiesinger H. Arginine metabolism and the synthesis of nitric oxide in the nervous system. Prog. Neurobiol. 64:2001;365-391.
80. Wink DA, Feelisch M, Vodovotz Y, Fukuto J, Grisham MB. The chemical biology of nitric oxide. In: Gilbert DL, Colton CA, editors. Reactive oxygen species in biological systems: an interdisciplinary approach. New York: Kluwer, 1999. p. 245-91.
81. Wu G., Morris S.M. Jr. Arginine metabolism: nitric oxide and beyond. Biochem. J. 336:1998;1-17.
82. Xu P., Schmechel D.E., Rothrock-Christian T., Burkart S., Qiu H.-L., Popko B. Human apolipoprotein E2, E3 and E4 isoform-specific transgenic mice: human like pattern of glial and neuronal imunoreactivity in central nervous system not observed in wild-type mice. Neurobiol. Dis. 3:1996;229-245.