Systemic lupus erythematosus, the brain, and anti-NR2 antibodies

Journal of Neurology

Volumn 259, Issue 4, 2012, Pages 622-629

  Lauvsnes, Maria B ^a   Omdal, Roald ^a,b  

^a STAVANGER UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

Anti NR2 antibodies; Cognitive impairment; SLE

Indexed keywords

ADRENALIN; ANTI N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A ANTIBODY; ANTI N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B ANTIBODY; ANTIBODY; DIZOCILPINE; DNA ANTIBODY; GLUTAMIC ACID; GLYCINE; KETAMINE; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; PHENCYCLIDINE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; ZINC;

AMINO ACID SEQUENCE; AMYGDALOID NUCLEUS; ANTIBODY BLOOD LEVEL; APOPTOSIS; BINDING SITE; BLOOD BRAIN BARRIER; BRAIN ATROPHY; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; COGNITIVE DEFECT; DEPRESSION; DISEASE ASSOCIATION; EMOTIONAL DISORDER; EXCITOTOXICITY; FOLLOW UP; HIPPOCAMPUS; HUMAN; IMMUNIZATION; LEARNING; MEMORY DISORDER; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NECROSIS; NEUROPSYCHIATRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPSE; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; BRAIN; HUMANS; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MICE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84862022860     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-011-6232-5     Document Type: Review

References (79)

1. Abbott NJ, Mendonca LL, Dolman DE (2003) The blood-brain barrier in systemic lupus erythematosus. Lupus 12:908-915 (Pubitemid 38082086)
2. Abreu MR, Jakosky A, Folgerini M, Brenol JC, Xavier RM, Kapczinsky F (2005) Neuropsychiatric systemic lupus erythematosus: correlation of brain MR imaging, CT, and SPECT. Clin Imaging 29:215-221 (Pubitemid 40602808)
3. ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomenclature (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599-608
4. Ainiala H, Dastidar P, Loukkola J, Lehtimaki T, Korpela M, Peltola J, Hietaharju A (2005) Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: a population-based study. Scand J Rheumatol 34:376-382 (Pubitemid 41545911)
5. Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A (2001) The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 57:496-500 (Pubitemid 32757599)
6. Alcocer-Varela J, Aleman-Hoey D, Alarcon-Segovia D (1992) Interleukin-1 and interleukin-6 activities are increased in the cerebrospinal fluid of patients with CNS lupus erythematosus and correlate with local late T-cell activation markers. Lupus 1:111-117
7. Appenzeller S, Cendes F, Costallat LT (2009) Cognitive impairment and employment status in systemic lupus erythematosus: a prospective longitudinal study. Arthritis Rheum 61:680-687
8. Arinuma Y, Yanagida T, Hirohata S (2008) Association of cerebrospinal fluid anti-NR2 glutamate receptor antibodies with diffuse neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 58:1130-1135 (Pubitemid 351564016)
9. Brey RL, Holliday SL, Saklad AR, Navarrete MG, Hermosillo-Romo D, Stallworth CL, Valdez CR, Escalante A, del Rincon I, Gronseth G, Rhine CB, Padilla P, McGlasson D (2002) Neuropsychiatric syndromes in lupus: prevalence using standardized definitions. Neurology 58:1214-1220 (Pubitemid 34411865)
10. Carbotte RM, Denburg SD, Denburg JA (1986) Prevalence of cognitive impairment in systemic lupus erythematosus. J Nerv Ment Dis 174:357-364 (Pubitemid 16084918)
11. Carlomagno S, Migliaresi S, Ambrosone L, Sannino M, Sanges G, Di Iorio G (2000) Cognitive impairment in systemic lupus erythematosus: a follow-up study. J Neurol 247:273-279 (Pubitemid 30223964)
12. Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659-1673 (Pubitemid 43999401)
13. Deapen D, Escalante A, Weinrib L, Horwitz D, Bachman B, Roy-Burman P, Walker A, Mack TM (1992) A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis Rheum 35:311-318
14. DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B (2001) A subset of lupus anti-DNA antibodies crossreacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 7:1189-1193 (Pubitemid 33063773)
15. Dellalibera-Joviliano R, Dos Reis ML, Cunha Fde Q, Donadi EA (2003) Kinins and cytokines in plasma and cerebrospinal fluid of patients with neuropsychiatric lupus. J Rheumatol 30:485-492 (Pubitemid 36301939)
16. Devinsky O, Petito CK, Alonso DR (1988) Clinical and neuropathological findings in systemic lupus erythematosus: the role of vasculitis, heart emboli, and thrombotic thrombocytopenic purpura. Ann Neurol 23:380-384 (Pubitemid 18098245)
17. Edworthy S (2004) Clinical manifestations of systemic lupus erythematosus. In: Harris ED, Budd RC, Firestein GS, Genovese MC, Sergent JS, Ruddy S, Sledge CB (eds) Kelley's textbook of rheumatology, 7th edn. Elsevier Saunders, pp 1204-1215
18. Eilertsen GO, Becker-Merok A, Nossent JC (2009) The influence of the 1997 updated classification criteria for systemic lupus erythematosus: epidemiology, disease presentation, and patient management. J Rheumatol 36:552-559
19. Ellis SG, VerityMA (1979) Central nervous system involvement in systemic lupus erythematosus: a review of neuropathologic findings in 57 cases, 1955-1977. Semin Arthritis Rheum 8:212-221 (Pubitemid 9104125)
20. Ellison G (1995) The N-methyl-D-aspartate antagonists phencyclidine, ketamine and dizocilpine as both behavioral and anatomical models of the dementias. Brain Res Brain Res Rev 20:250-267
21. Faust TW, Chang EH, Kowal C, Berlin R, Gazaryan IG, Bertini E, Zhang J, Sanchez-Guerrero J, Fragoso-Loyo HE, Volpe BT, Diamond B, Huerta PT (2010) Neurotoxic lupus autoantibodies alter brain function through two distinct mechanisms. Proc Natl Acad Sci USA 107:18569-18574
22. Fragoso-Loyo H, Cabiedes J, Orozco-Narvaez A, Davila-Maldonado L, Atisha-Fregoso Y, Diamond B, Llorente L, Sanchez-Guerrero J (2008) Serum and cerebrospinal fluid autoantibodies in patients with neuropsychiatric lupus erythematosus. Implications for diagnosis and pathogenesis. PLoS ONE 3(10):e3347
23. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, Ortmann W, Kosoy R, Ferreira RC, Nordmark G, Gunnarsson I, Svenungsson E, Padyukov L, Sturfelt G, Jonsen A, Bengtsson AA, Rantapaa-Dahlqvist S, Baechler EC, Brown EE, Alarcon GS, Edberg JC, Ramsey-Goldman R, McGwin G Jr., Reveille JD, Vila LM, Kimberly RP, Manzi S, Petri MA, Lee A, Gregersen PK, Seldin MF, Ronnblom L, Criswell LA, Syvanen AC, Behrens TW, Graham RR (2009) A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41:1228-1233
24. Goff DC, Coyle JT (2001) The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am J Psychiatry 158:1367-1377 (Pubitemid 32847232)
25. Gono T, Kawaguchi Y, Kaneko H, Nishimura K, Hanaoka M, Kataoka S, Okamoto Y, Katsumata Y, Yamanaka H (2011) Anti-NR2A antibody as a predictor for neuropsychiatric systemic lupus erythematosus. Rheumatology (Oxford) 50:1578-1585
26. Graham RR, Ortmann WA, Langefeld CD, Jawaheer D, Selby SA, Rodine PR, Baechler EC, Rohlf KE, Shark KB, Espe KJ, Green LE, Nair RP, Stuart PE, Elder JT, King RA, Moser KL, Gaffney PM, Bugawan TL, Erlich HA, Rich SS, Gregersen PK, Behrens TW (2002) Visualizing human leukocyte antigen class II risk haplotypes in human systemic lupus erythematosus. Am J Hum Genet 71:543-553 (Pubitemid 34970125)
27. Hanly JG, Hong C, Smith S, Fisk JD (1999) A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis Rheum 42:728-734 (Pubitemid 29171993)
28. Hanly JG, McCurdy G, Fougere L, Douglas JA, Thompson K (2004) Neuropsychiatric events in systemic lupus erythematosus: attribution and clinical significance. J Rheumatol 31:2156-2162 (Pubitemid 39453234)
29. Hanly JG, Robichaud J, Fisk JD (2006) Anti-NR2 glutamate receptor antibodies and cognitive function in systemic lupus erythematosus. J Rheumatol 33:1553-1558 (Pubitemid 44168826)
30. Hanly JG, Urowitz MB, Sanchez-Guerrero J, Bae SC, Gordon C, Wallace DJ, Isenberg D, Alarcon GS, Clarke A, Bernatsky S, Merrill JT, Petri M, Dooley MA, Gladman D, Fortin PR, Steinsson K, Bruce I, Manzi S, Khamashta M, Zoma A, Aranow C, Ginzler E, Van Vollenhoven R, Font J, Sturfelt G, Nived O, Ramsey-Goldman R, Kalunian K, Douglas J, Thompson K, Farewell V, Systemic Lupus International Collaborating C (2007) Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: an international inception cohort study. Arthritis Rheum 56:265-273 (Pubitemid 46106200)
31. Hanly JG, Urowitz MB, Siannis F, Farewell V, Gordon C, Bae SC, Isenberg D, Dooley MA, Clarke A, Bernatsky S, Gladman D, Fortin PR, Manzi S, Steinsson K, Bruce IN, Ginzler E, Aranow C, Wallace DJ, Ramsey-Goldman R, van Vollenhoven R, Sturfelt G, Nived O, Sanchez-Guerrero J, Alarcon GS, Petri M, Khamashta M, Zoma A, Font J, Kalunian K, Douglas J, Qi Q, Thompson K, Merrill JT, Systemic Lupus International Collaborating C (2008) Autoantibodies and neuropsychiatric events at the time of systemic lupus erythematosus diagnosis: results from an international inception cohort study. Arthritis Rheum 58:843-853
32. Hanly JG, Walsh NM, Sangalang V (1992) Brain pathology in systemic lupus erythematosus. J Rheumatol 19:732-741
33. Harboe E, Tjensvoll AB, Maroni S, Goransson LG, Greve OJ, Beyer MK, Herigstad A, Kvaloy JT, Omdal R (2009) Neuropsychiatric syndromes in patients with systemic lupus erythematosus and primary Sjogren syndrome: a comparative population-based study. Ann Rheum Dis 68:1541-1546
34. Harris EN, Gharavi AE, Boey ML, Patel BM, Mackworth-Young CG, Loizou S, Hughes GR (1983) Anticardiolipin antibodies: detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet 2:1211-1214 (Pubitemid 14229783)
35. Harrison MJ, Ravdin LD, Lockshin MD (2006) Relationship between serum NR2a antibodies and cognitive dysfunction in systemic lupus erythematosus. Arthritis Rheum 54:2515-2522 (Pubitemid 44205012)
36. Hirohata S, Arinuma Y, Takayama M, Yoshio T (2007) Association of cerebrospinal fluid anti-ribosomal P protein antibodies with diffuse psychiatric/neuropsychological syndromes in systemic lupus erythematosus. Arthritis Res Ther 9:R44
37. Hirohata S, Miyamoto T (1990) Elevated levels of interleukin-6 in cerebrospinal fluid from patients with systemic lupus erythematosus and central nervous system involvement. Arthritis Rheum 33:644-649 (Pubitemid 20166565)
38. Hossain M, Sathe T, Fazio V, Mazzone P, Weksler B, Janigro D, Rapp E, Cucullo L (2009) Tobacco smoke: a critical etiological factor for vascular impairment at the blood-brain barrier. Brain Res 1287:192-205
39. Huerta PT, Kowal C, DeGiorgio LA, Volpe BT, Diamond B (2006) Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci USA 103:678-683 (Pubitemid 43153085)
40. Husebye ES, Sthoeger ZM, Dayan M, Zinger H, Elbirt D, Levite M, Mozes E (2005) Autoantibodies to a NR2A peptide of the glutamate/NMDA receptor in sera of patients with systemic lupus erythematosus. Ann Rheum Dis 64:1210-1213 (Pubitemid 41113359)
41. Isshi K, Hirohata S (1996) Association of anti-ribosomal P protein antibodies with neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 39:1483-1490 (Pubitemid 26314981)
42. Isshi K, Hirohata S (1998) Differential roles of the anti-ribosomal P antibody and antineuronal antibody in the pathogenesis of central nervous system involvement in systemic lupus erythematosus. Arthritis Rheum 41:1819-1827 (Pubitemid 28465536)
43. Johnson RT, Richardson EP (1968) The neurological manifestations of systemic lupus erythematosus. Medicine (Baltimore) 47:337-369
44. Karassa FB, Afeltra A, Ambrozic A, Chang DM, De Keyser F, Doria A, Galeazzi M, Hirohata S, Hoffman IE, Inanc M, Massardo L, MathieuA,Mok CC,Morozzi G, Sanna G, Spindler AJ, Tzioufas AG, Yoshio T, Ioannidis JP (2006) Accuracy of anti-ribosomal P protein antibody testing for the diagnosis of neuropsychiatric systemic lupus erythematosus: an international meta-analysis. Arthritis Rheum 54:312-324 (Pubitemid 43122215)
45. Kowal C, Degiorgio LA, Lee JY, Edgar MA, Huerta PT, Volpe BT, Diamond B (2006) Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc Natl Acad Sci U S A 103:19854-19859 (Pubitemid 46037520)
46. Kowal C, DeGiorgio LA, Nakaoka T, Hetherington H, Huerta PT, Diamond B, Volpe BT (2004) Cognition and immunity; antibody impairs memory. Immunity 21:179-188 (Pubitemid 39094048)
47. Kozora E, Arciniegas DB, Zhang L, West S (2007) Neuropsychological patterns in systemic lupus erythematosus patients with depression. Arthritis Res Ther 9:R48
48. Kozora E, West SG, Maier SF, Filley CM, Arciniegas DB, Brown M, Miller D, Grimm A, Zhang L (2010) Antibodies against N-methyl-D-aspartate receptors in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. J Neurol Sci 295:87-91
49. Lapteva L, Nowak M, Yarboro CH, Takada K, Roebuck-Spencer T, Weickert T, Bleiberg J, Rosenstein D, Pao M, Patronas N, Steele S, Manzano M, van der Veen JW, Lipsky PE, Marenco S, Wesley R, Volpe B, Diamond B, Illei GG (2006) Anti-N-methyl-D-aspartate receptor antibodies, cognitive dysfunction, and depression in systemic lupus erythematosus. Arthritis Rheum 54:2505-2514 (Pubitemid 44205011)
50. Lau A, Tymianski M (2010) Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 460:525-542
51. Martel MA, Wyllie DJ, Hardingham GE (2009) In developing hippocampal neurons, NR2B-containing N-methyl-D-aspartate receptors (NMDARs) can mediate signaling to neuronal survival and synaptic potentiation, as well as neuronal death. Neuroscience 158:334-343
52. Matus S, Burgos PV, Bravo-Zehnder M, Kraft R, Porras OH, Farias P, Barros LF, Torrealba F, Massardo L, Jacobelli S, Gonzalez A (2007) Antiribosomal-P autoantibodies from psychiatric lupus target a novel neuronal surface protein causing calcium influx and apoptosis. J Exp Med 204:3221-3234
53. Mayer ML, Vyklicky L, Sernagor E (1989) A physiologist's view of the N-methyl-D-Aspartate receptor: an allosteric ion channel with multiple regulatory sites. Drug Dev Res 17:263-280 (Pubitemid 19209590)
54. McLaurin EY, Holliday SL, Williams P, Brey RL (2005) Predictors of cognitive dysfunction in patients with systemic lupus erythematosus. Neurology 64:297-303
55. McLean BN, Miller D, Thompson EJ (1995) Oligoclonal banding of IgG in CSF, blood-brain barrier function, and MRI findings in patients with sarcoidosis, systemic lupus erythematosus, and Behcet's disease involving the nervous system. J Neurol Neurosurg Psychiatry 58:548-554
56. Menon S, Jameson-Shortall E, Newman SP, Hall-Craggs MR, Chinn R, Isenberg DA (1999) A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum 42:735-741 (Pubitemid 29171994)
57. Moore PM (1999) Neuropsychiatric systemic lupus erythematosus. In: LR G (ed) Systemic lupus erythematosus. Academic press, San Diego, pp 575-578
58. Olazaran J, Lopez-Longo J, Cruz I, Bittini A, Carreno L (2009) Cognitive dysfunction in systemic lupus erythematosus: prevalence and correlates. Eur Neurol 62:49-55
59. Omdal R, Brokstad K, Waterloo K, Koldingsnes W, Jonsson R, Mellgren SI (2005) Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur J Neurol 12:392-398 (Pubitemid 40524182)
60. Ozawa S, Kamiya H, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581-618 (Pubitemid 28123327)
61. Perez-Otano I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ, Heinemann SF (2001) Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J Neurosci 21:1228-1237 (Pubitemid 32128767)
62. Petri M, Naqibuddin M, Carson KA, Wallace DJ, Weisman MH, Holliday SL, Sampedro M, Padilla PA, Brey RL (2010) Depression and cognitive impairment in newly diagnosed systemic lupus erythematosus. J Rheumatol 37:2032-2038
63. Qi X, Inagaki K, Sobel RA, Mochly-Rosen D (2008) Sustained pharmacological inhibition of deltaPKC protects against hypertensive encephalopathy through prevention of blood-brain barrier breakdown in rats. J Clin Invest 118:173-182
64. Rogoz Z, Skuza G, Maj J, Danysz W (2002) Synergistic effect of uncompetitive NMDA receptor antagonists and antidepressant drugs in the forced swimming test in rats. Neuropharmacology 42:1024-1030 (Pubitemid 34790257)
65. Sheng M, Pak DT (2000) Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu Rev Physiol 62:755-778 (Pubitemid 30618281)
66. Shiozawa S, Kuroki Y, Kim M, Hirohata S, Ogino T (1992) Interferon-alpha in lupus psychosis. Arthritis Rheum 35:417-422
67. Sorrells SF, Caso JR, Munhoz CD, Sapolsky RM (2009) The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64:33-39
68. Stahl-Hallengren C, Jonsen A, Nived O, Sturfelt G (2000) Incidence studies of systemic lupus erythematosus in Southern Sweden: increasing age, decreasing frequency of renal manifestations and good prognosis. J Rheumatol 27:685-691 (Pubitemid 30151347)
69. Steup-Beekman G, Steens S, van Buchem M, Huizinga T (2007) Anti-NMDA receptor autoantibodies in patients with systemic lupus erythematosus and their first-degree relatives. Lupus 16:329-334 (Pubitemid 47074834)
70. Svenungsson E, Andersson M, Brundin L, van Vollenhoven R, Khademi M, Tarkowski A, Greitz D, Dahlstrom M, Lundberg I, Klareskog L, Olsson T (2001) Increased levels of proinflammatory cytokines and nitric oxide metabolites in neuropsychiatric lupus erythematosus. Ann Rheum Dis 60:372-379 (Pubitemid 32242751)
71. Trysberg E, Nylen K, Rosengren LE, Tarkowski A (2003) Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum 48:2881-2887 (Pubitemid 37280617)
72. Tymianski M, Charlton MP, Carlen PL, Tator CH (1993) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 13:2085-2104 (Pubitemid 23113418)
73. Utset TO, Fink J, Doninger NA (2006) Prevalence of neurocognitive dysfunction and other clinical manifestations in disabled patients with systemic lupus erythematosus. J Rheumatol 33:531-538 (Pubitemid 43334576)
74. Waterloo K, Omdal R, Husby G, Mellgren SI (2002) Neuropsychological function in systemic lupus erythematosus: a five-year longitudinal study. Rheumatology (Oxford) 41:411-415 (Pubitemid 34537839)
75. Waterloo K, Omdal R, Sjoholm H, Koldingsnes W, Jacobsen EA, Sundsfjord JA, Husby G, Mellgren SI (2001) Neuropsychological dysfunction in systemic lupus erythematosus is not associated with changes in cerebral blood flow. J Neurol 248:595-602 (Pubitemid 32695802)
76. West SG, Emlen W, Wener MH, Kotzin BL (1995) Neuropsychiatric lupus erythematosus: a 10-year prospective study on the value of diagnostic tests. Am J Med 99:153-163
77. Winfield JB, Shaw M, Silverman LM, Eisenberg RA, Wilson HA 3rd, Koffler D (1983) Intrathecal IgG synthesis and blood-brain barrier impairment in patients with systemic lupus erythematosus and central nervous system dysfunction. Am J Med 74:837-844 (Pubitemid 13080128)
78. Yoshio T, Hirata D, Onda K, Nara H, Minota S (2005) Antiribosomal P protein antibodies in cerebrospinal fluid are associated with neuropsychiatric systemic lupus erythematosus. J Rheumatol 32:34-39 (Pubitemid 40092587)
79. Yoshio T, Onda K, Nara H, Minota S (2006) Association of IgG anti-NR2 glutamate receptor antibodies in cerebrospinal fluid with neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 54:675-678 (Pubitemid 43228647)