Glutamate Receptor Biology and its Clinical Significance in Neuropsychiatric Systemic Lupus Erythematosus

Rheumatic Disease Clinics of North America

Volumn 36, Issue 1, 2010, Pages 187-201

  Aranow, Cynthia ^a   Diamond, Betty ^a   Mackay, Meggan ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Anti NR2 antibody; Cognitive impairment; Emotional impairment; Neuropsychiatric SLE; NMDAR

Indexed keywords

ANTIBODY; AUTOANTIBODY; DNA ANTIBODY; GLUTAMATE RECEPTOR; INTERLEUKIN 6; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR ANTIBODY; PHOSPHOLIPID ANTIBODY; RIBOSOMAL P ANTIBODY; UNCLASSIFIED DRUG;

ANTIBODY BLOOD LEVEL; ANTIBODY TITER; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; COGNITIVE DEFECT; DISEASE CLASSIFICATION; HUMAN; MOOD DISORDER; NEUROPATHOLOGY; NEUROPSYCHIATRIC SYSTEMIC LUPUS ERYTHEMATOSUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BINDING; REVIEW; RISK FACTOR; SYMPTOMATOLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; BLOOD-BRAIN BARRIER; HUMANS; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MICE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 77349097603     PISSN: 0889857X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.rdc.2009.12.007     Document Type: Review

References (79)

1. Ginzler E.M., and Dvorkina O. Newer therapeutic approaches for systemic lupus erythematosus. Rheum Dis Clin North Am 31 2 (2005) 315-328
2. Scolding N.J., and Joseph F.G. The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathol Appl Neurobiol 28 3 (2002) 173-189
3. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42 4 (1999) 599-608
4. Hanly J.G., McCurdy G., Fougere L., et al. Neuropsychiatric events in systemic lupus erythematosus: attribution and clinical significance. J Rheumatol 31 11 (2004) 2156-2162
5. Hanly J.G., Urowitz M.B., Sanchez-Guerrero J., et al. Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: an international inception cohort study. Arthritis Rheum 56 1 (2007) 265-273
6. Molloy E.S., and Calabrese L.H. Progressive multifocal leukoencephalopathy in patients with rheumatic diseases: are patients with systemic lupus erythematosus at particular risk?. Autoimmun Rev 8 2 (2008) 144-146
7. Carson K.R., Evens A.M., Richey E.A., et al. Progressive multifocal leukoencephalopathy after rituximab therapy in HIV-negative patients: a report of 57 cases from the Research on Adverse Drug Events and Reports project. Blood 113 20 (2009) 4834-4840
8. Love P.E., and Santoro S.A. Antiphospholipid antibodies: anticardiolipin and the lupus anticoagulant in systemic lupus erythematosus (SLE) and in non-SLE disorders. Prevalence and clinical significance. Ann Intern Med 112 9 (1990) 682-698
9. Sanna G., Bertolaccini M.L., Cuadrado M.J., et al. Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies. J Rheumatol 30 5 (2003) 985-992
10. Brey R.L., Holliday S.L., Saklad A.R., et al. Neuropsychiatric syndromes in lupus: prevalence using standardized definitions. Neurology 58 8 (2002) 1214-1220
11. Ainiala H., Loukkola J., Peltola J., et al. The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 57 3 (2001) 496-500
12. Sibbitt Jr. W.L., Brandt J.R., Johnson C.R., et al. The incidence and prevalence of neuropsychiatric syndromes in pediatric onset systemic lupus erythematosus. J Rheumatol 29 7 (2002) 1536-1542
13. Brey R.L., and Petri M.A. Neuropsychiatric systemic lupus erythematosus: miles to go before we sleep. Neurology 61 1 (2003) 9-10
14. Bleiberg J., Kane R.L., Reeves D.L., et al. Factor analysis of computerized and traditional tests used in mild brain injury research. Clin Neuropsychol 14 3 (2000) 287-294
15. Menon S., Jameson-Shortall E., Newman S.P., et al. A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum 42 4 (1999) 735-741
16. McLaurin E.Y., Holliday S.L., Williams P., et al. Predictors of cognitive dysfunction in patients with systemic lupus erythematosus. Neurology 64 2 (2005) 297-303
17. Hanly J.G., Hong C., Smith S., et al. A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis Rheum 42 4 (1999) 728-734
18. Hanly J.G., Urowitz M.B., Siannis F., et al. Autoantibodies and neuropsychiatric events at the time of systemic lupus erythematosus diagnosis: results from an international inception cohort study. Arthritis Rheum 58 3 (2008) 843-853
19. Trysberg E., Nylen K., Rosengren L.E., et al. Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum 48 10 (2003) 2881-2887
20. Waterloo K., Omdal R., Sjoholm H., et al. Neuropsychological dysfunction in systemic lupus erythematosus is not associated with changes in cerebral blood flow. J Neurol 248 7 (2001) 595-602
21. Jarek M.J., West S.G., Baker M.R., et al. Magnetic resonance imaging in systemic lupus erythematosus patients without a history of neuropsychiatric lupus erythematosus. Arthritis Rheum 37 11 (1994) 1609-1613
22. Kao C.H., Lan J.L., ChangLai S.P., et al. The role of FDG-PET, HMPAO-SPET and MRI in the detection of brain involvement in patients with systemic lupus erythematosus. Eur J Nucl Med 26 2 (1999) 129-134
23. Lim M.K., Suh C.H., Kim H.J., et al. Systemic lupus erythematosus: brain MR imaging and single-voxel hydrogen 1 MR spectroscopy. Radiology 217 1 (2000) 43-49
24. Kaell A.T., Shetty M., Lee B.C., et al. The diversity of neurologic events in systemic lupus erythematosus. Prospective clinical and computed tomographic classification of 82 events in 71 patients. Arch Neurol 43 3 (1986) 273-276
25. Axford J.S., Howe F.A., Heron C., et al. Sensitivity of quantitative (1)H magnetic resonance spectroscopy of the brain in detecting early neuronal damage in systemic lupus erythematosus. Ann Rheum Dis 60 2 (2001) 106-111
26. Kozora E., Arciniegas D.B., Filley C.M., et al. Cognition, MRS neurometabolites, and MRI volumetrics in non-neuropsychiatric systemic lupus erythematosus: preliminary data. Cogn Behav Neurol 18 3 (2005) 159-162
27. Lapteva L., Nowak M., Yarboro C.H., et al. Anti-N-methyl-d-aspartate receptor antibodies, cognitive dysfunction, and depression in systemic lupus erythematosus. Arthritis Rheum 54 8 (2006) 2505-2514
28. DiFrancesco M.W., Holland S.K., Ris M.D., et al. Functional magnetic resonance imaging assessment of cognitive function in childhood-onset systemic lupus erythematosus: a pilot study. Arthritis Rheum 56 12 (2007) 4151-4163
29. Fitzgibbon B.M., Fairhall S.L., Kirk I.J., et al. Functional MRI in NPSLE patients reveals increased parietal and frontal brain activation during a working memory task compared with controls. Rheumatology (Oxford) 47 1 (2008) 50-53
30. Fragoso-Loyo H.E., and Sanchez-Guerrero J. Effect of severe neuropsychiatric manifestations on short-term damage in systemic lupus erythematosus. J Rheumatol 34 1 (2007) 76-80
31. Katsumata Y., Harigai M., Kawaguchi Y., et al. Diagnostic reliability of cerebral spinal fluid tests for acute confusional state (delirium) in patients with systemic lupus erythematosus: interleukin 6 (IL-6), IL-8, interferon-alpha, IgG index, and Q-albumin. J Rheumatol 34 10 (2007) 2010-2017
32. Hirohata S., Kanai Y., Mitsuo A., et al. Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis. A multicenter retrospective study. Clin Rheumatol 28 11 (2009) 1319-1323
33. George-Chandy A., Trysberg E., and Eriksson K. Raised intrathecal levels of APRIL and BAFF in patients with systemic lupus erythematosus: relationship to neuropsychiatric symptoms. Arthritis Res Ther 10 4 (2008) R97
34. Santer D.M., Yoshio T., Minota S., et al. Potent induction of IFN-alpha and chemokines by autoantibodies in the cerebrospinal fluid of patients with neuropsychiatric lupus. J Immunol 182 2 (2009) 1192-1201
35. Fragoso-Loyo H., Richaud-Patin Y., Orozco-Narvaez A., et al. Interleukin-6 and chemokines in the neuropsychiatric manifestations of systemic lupus erythematosus. Arthritis Rheum 56 4 (2007) 1242-1250
36. Trysberg E., Blennow K., Zachrisson O., et al. Intrathecal levels of matrix metalloproteinases in systemic lupus erythematosus with central nervous system engagement. Arthritis Res Ther 6 6 (2004) R551-R556
37. Bonfa E., Golombek S.J., Kaufman L.D., et al. Association between lupus psychosis and anti-ribosomal P protein antibodies. N Engl J Med 317 5 (1987) 265-271
38. Schneebaum A.B., Singleton J.D., West S.G., et al. Association of psychiatric manifestations with antibodies to ribosomal P proteins in systemic lupus erythematosus. Am J Med 90 1 (1991) 54-62
39. Karassa F.B., Afeltra A., Ambrozic A., et al. Accuracy of anti-ribosomal P protein antibody testing for the diagnosis of neuropsychiatric systemic lupus erythematosus: an international meta-analysis. Arthritis Rheum 54 1 (2006) 312-324
40. Isshi K., and Hirohata S. Association of anti-ribosomal P protein antibodies with neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 39 9 (1996) 1483-1490
41. Matus S., Burgos P.V., Bravo-Zehnder M., et al. Antiribosomal-P autoantibodies from psychiatric lupus target a novel neuronal surface protein causing calcium influx and apoptosis. J Exp Med 204 13 (2007) 3221-3234
42. Paul E., Manheimer-Lory A., Livneh A., et al. Pathogenic anti-DNA antibodies in SLE: idiotypic families and genetic origins. Int Rev Immunol 5 3-4 (1990) 295-313
43. Gaynor B., Putterman C., Valadon P., et al. Peptide inhibition of glomerular deposition of an anti-DNA antibody. Proc Natl Acad Sci U S A 94 5 (1997) 1955-1960
44. DeGiorgio L.A., Konstantinov K.N., Lee S.C., et al. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 7 11 (2001) 1189-1193
45. Olney J.W., and Ho O.L. Brain damage in infant mice following oral intake of glutamate, aspartate or cysteine. Nature 227 5258 (1970) 609-611
46. Chen H.S., and Lipton S.A. The chemical biology of clinically tolerated NMDA receptor antagonists. J Neurochem 97 6 (2006) 1611-1626
47. Kutsuwada T., Kashiwabuchi N., Mori H., et al. Molecular diversity of the NMDA receptor channel. Nature 358 6381 (1992) 36-41
48. Collingridge G.L., Kehl S.J., and McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334 (1983) 33-46
49. Huntley G.W., Vickers J.C., and Morrison J.H. Cellular and synaptic localization of NMDA and non-NMDA receptor subunits in neocortex: organizational features related to cortical circuitry, function and disease. Trends Neurosci 17 12 (1994) 536-543
50. Ozawa S., Kamiya H., and Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54 5 (1998) 581-618
51. Coan E.J., and Collingridge G.L. Magnesium ions block an N-methyl-d-aspartate receptor-mediated component of synaptic transmission in rat hippocampus. Neurosci Lett 53 1 (1985) 21-26
52. Choi D.W., and Rothman S.M. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 13 (1990) 171-182
53. Laube B., Hirai H., Sturgess M., et al. Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18 3 (1997) 493-503
54. Lipton S.A., and Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330 9 (1994) 613-622
55. Erdo S.L., and Schafer M. Memantine is highly potent in protecting cortical cultures against excitotoxic cell death evoked by glutamate and N-methyl-d-aspartate. Eur J Pharmacol 198 2-3 (1991) 215-217
56. Ellison G. The N-methyl-d-aspartate antagonists phencyclidine, ketamine and dizocilpine as both behavioral and anatomical models of the dementias. Brain Res Brain Res Rev 20 2 (1995) 250-267
57. Gaspar P.A., Bustamante M.L., Silva H., et al. Molecular mechanisms underlying glutamatergic dysfunction in schizophrenia: therapeutic implications. J Neurochem 111 4 (2009) 891-900
58. Kowal C., DeGiorgio L.A., Nakaoka T., et al. Cognition and immunity; antibody impairs memory. Immunity 21 2 (2004) 179-188
59. Huerta P.T., Kowal C., DeGiorgio L.A., et al. Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci U S A 103 3 (2006) 678-683
60. Sharma A., Isenberg D., and Diamond B. Studies of human polyclonal and monoclonal antibodies binding to lupus autoantigens and cross-reactive antigens. Rheumatology (Oxford) 42 3 (2003) 453-463
61. Omdal R., Brokstad K., Waterloo K., et al. Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur J Neurol 12 5 (2005) 392-398
62. Emmer B.J., van der Grond J., Steup-Beekman G.M., et al. Selective involvement of the amygdala in systemic lupus erythematosus. PLoS Med 3 12 (2006) e499
63. Hanly J.G., Robichaud J., and Fisk J.D. Anti-NR2 glutamate receptor antibodies and cognitive function in systemic lupus erythematosus. J Rheumatol 33 8 (2006) 1553-1558
64. Harrison M.J., Ravdin L.D., and Lockshin M.D. Relationship between serum NR2a antibodies and cognitive dysfunction in systemic lupus erythematosus. Arthritis Rheum 54 8 (2006) 2515-2522
65. Steup-Beekman G., Steens S., van Buchem M., et al. Anti-NMDA receptor autoantibodies in patients with systemic lupus erythematosus and their first-degree relatives. Lupus 16 5 (2007) 329-334
66. Arinuma Y., Yanagida T., and Hirohata S. Association of cerebrospinal fluid anti-NR2 glutamate receptor antibodies with diffuse neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 58 4 (2008) 1130-1135
67. Yoshio T., Onda K., Nara H., et al. Association of IgG anti-NR2 glutamate receptor antibodies in cerebrospinal fluid with neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 54 2 (2006) 675-678
68. Fragoso-Loyo H., Cabiedes J., Orozco-Narvaez A., et al. Serum and cerebrospinal fluid autoantibodies in patients with neuropsychiatric lupus erythematosus. Implications for diagnosis and pathogenesis. PLoS One 3 10 (2008) e3347
69. Kowal C., Degiorgio L.A., Lee J.Y., et al. Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc Natl Acad Sci U S A 103 52 (2006) 19854-19859
70. McAllister D.L., Kaplan B.J., Edworthy S.M., et al. The influence of systemic lupus erythematosus on fetal development: cognitive, behavioral, and health trends. J Int Neuropsychol Soc 3 4 (1997) 370-376
71. Ross G., Sammaritano L., Nass R., et al. Effects of mothers' autoimmune disease during pregnancy on learning disabilities and hand preference in their children. Arch Pediatr Adolesc Med 157 4 (2003) 397-402
72. Neri F., Chimini L., Bonomi F., et al. Neuropsychological development of children born to patients with systemic lupus erythematosus. Lupus 13 10 (2004) 805-811
73. Tincani A., Nuzzo M., Motta M., et al. Autoimmunity and pregnancy: autoantibodies and pregnancy in rheumatic diseases. Ann N Y Acad Sci 1069 (2006) 346-352
74. Lahita R.G. Systemic lupus erythematosus: learning disability in the male offspring of female patients and relationship to laterality. Psychoneuroendocrinology 13 5 (1988) 385-396
75. Lee J.Y., Huerta P.T., Zhang J., et al. Neurotoxic autoantibodies mediate congenital cortical impairment of offspring in maternal lupus. Nat Med 15 1 (2009) 91-96
76. Dalmau J., Tuzun E., Wu H.Y., et al. Paraneoplastic anti-N-methyl-d-aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol 61 1 (2007) 25-36
77. Dalmau J., Gleichman A.J., Hughes E.G., et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol 7 12 (2008) 1091-1098
78. Niehusmann P., Dalmau J., Rudlowski C., et al. Diagnostic value of N-methyl-d-aspartate receptor antibodies in women with new-onset epilepsy. Arch Neurol 66 4 (2009) 458-464
79. Ganor Y., Goldberg-Stern H., Lerman-Sagie T., et al. Autoimmune epilepsy: distinct subpopulations of epilepsy patients harbor serum autoantibodies to either glutamate/AMPA receptor GluR3, glutamate/NMDA receptor subunit NR2A or double-stranded DNA. Epilepsy Res 65 1-2 (2005) 11-22