Neuroimmunopathology in a murine model of neuropsychiatric lupus

Brain Research Reviews

Volumn 54, Issue 1, 2007, Pages 67-79

  Ballok, David A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Autoimmunity; Behavioral dysfunction; Corticosteroids; Dopamine; Impaired neurogenesis; MRL mice; Neurodegeneration; Neuroinflammation

Indexed keywords

CORTICOSTEROID;

AUTOIMMUNITY; BEHAVIOR DISORDER; BRAIN ATROPHY; DISEASE MODEL; IMMUNOPATHOGENESIS; INFLAMMATION; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; BRAIN; CELL DEATH; DELIRIUM, DEMENTIA, AMNESTIC, COGNITIVE DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE; ENCEPHALITIS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; NEURODEGENERATIVE DISEASES;

EID: 33947696072     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2006.12.003     Document Type: Review

References (174)

1. Abbott N.J., Mendonca L.L., and Dolman D.E. The blood-brain barrier in systemic lupus erythematosus. Lupus 12 (2003) 908-915
2. Abbott N.J., Ronnback L., and Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev., Neurosci. 7 (2006) 41-53
3. Adelman D.C., Saltiel E., and Klinenberg J.R. The neuropsychiatric manifestations of systemic lupus erythematosus: an overview. Semin. Arthritis Rheum. 15 (1986) 185-199
4. Ainiala H., Dastidar P., Loukkola J., Lehtimaki T., Korpela M., Peltola J., and Hietaharju A. Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: a population-based study. Scand. J. Rheumatol. 34 (2005) 376-382
5. Alexander E.L., and Alexander G.E. Aseptic meningoencephalitis in primary Sjogren's syndrome. Neurology 33 (1983) 593-598
6. Alexander E.L., Murphy E.D., Roths J.B., and Alexander G.E. Congenic autoimmune murine models of central nervous system disease in connective tissue disorders. Ann. Neurol. 14 (1983) 242-248
7. Alexander J.J., Bao L., Jacob A., Kraus D.M., Holers V.M., and Quigg R.J. Administration of the soluble complement inhibitor, Crry-Ig, reduces inflammation and aquaporin 4 expression in lupus cerebritis. Biochim. Biophys. Acta 1639 (2003) 169-176
8. Alexander J.J., Jacob A., Bao L., Macdonald R.L., and Quigg R.J. Complement-dependent apoptosis and inflammatory gene changes in murine lupus cerebritis. J. Immunol. 175 (2005) 8312-8319
9. Alexander J.J., Zwingmann C., and Quigg R. MRL/lpr mice have alterations in brain metabolism as shown with [(1)H-(13)C] NMR spectroscopy. Neurochem. Int. 47 (2005) 143-151
10. Anderson K.K., Ballok D.A., Prasad N., Szechtman H., and Sakic B. Impaired response to amphetamine and neuronal degeneration in the nucleus accumbens of autoimmune MRL-lpr mice. Behav. Brain Res. 166 (2006) 32-38
11. Andrews B.S., Eisenberg R.A., Theofilopoulos A.N., Izui S., Wilson C.B., McConahey P.J., Murphy E.D., Roths J.B., and Dixon F.J. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J. Exp. Med. 148 (1978) 1198-1215
12. Asanuma M., Miyazaki I., and Ogawa N. Dopamine- or l-DOPA-induced neurotoxicity: the role of dopamine quinone formation and tyrosinase in a model of Parkinson's disease. Neurotox. Res. 5 (2003) 165-176
13. Auer R.N., Wieloch T., Olsson Y., and Siesjo B.K. The distribution of hypoglycemic brain damage. Acta Neuropathol. (Berl.) 64 (1984) 177-191
14. Ballok D.A., Millward J.M., and Sakic B. Neurodegeneration in autoimmune MRL-lpr mice as revealed by Fluoro Jade B staining. Brain Res. 964 (2003) 200-210
15. Ballok D.A., Earls A.M., Krasnik C., Hoffman S.A., and Sakic B. Autoimmune-induced damage of the midbrain dopaminergic system in lupus-prone mice. J. Neuroimmunol. 152 (2004) 83-97
16. Ballok D.A., Woulfe J., Sur M., Cyr M., and Sakic B. Hippocampal damage in mouse and human forms of systemic autoimmune disease. Hippocampus 14 (2004) 649-661
17. Ballok D.A., Ma X., Denburg J.A., Arsenault L., and Sakic B. Ibuprofen fails to prevent brain pathology in a model of neuropsychiatric lupus. J. Rheumatol. 33 (2006) 2199-2213
18. Baraczka K., Nekam K., Pozsonyi T., Jakab L., Szongoth M., and Sesztak M. Concentration of soluble adhesion molecules (sVCAM-1, sICAM-1 and sL-selectin) in the cerebrospinal fluid and serum of patients with multiple sclerosis and systemic lupus erythematosus with central nervous involvement. Neuroimmunomodulation 9 (2001) 49-54
19. Bluestein H.G. The central nervous system in systemic lupus erythematosus. Systemic Lupus Erythematosus. 2 ed. (1992), Churchill Livingstone, New York 639-655
20. Bluestein H.G., and Zvaifler N.J. Antibodies reactive with central nervous system antigens. Hum. Pathol. 14 (1983) 424-428
21. Bluestein H.G., Williams G.W., and Steinberg A.D. Cerebrospinal fluid antibodies to neuronal cells: association with neuropsychiatric manifestations of systemic lupus erythematosus. Am. J. Med. 70 (1981) 240-246
22. Blum D., Torch S., Lambeng N., Nissou M., Benabid A.L., Sadoul R., and Verna J.M. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog. Neurobiol. 65 (2001) 135-172
23. Bresnihan B., Hohmeister R., Cutting J., Travers R.L., Waldburger M., Black C., Jones T., and Hughes G.R. The neuropsychiatric disorder in systemic lupus erythematosus: evidence for both vascular and immune mechanisms. Ann. Rheum. Dis. 38 (1979) 301-306
24. Brey R.L., Cote S., Barohn R., Jackson C., Crawley R., and Teale J.M. Model for the neuromuscular complications of systemic lupus erythematosus. Lupus 4 (1995) 209-212
25. Brey R.L., Amato A.A., Kagan-Hallet K., Rhine C.B., and Stallworth C.L. Anti-intercellular adhesion molecule-1 (ICAM-1) antibody treatment prevents central and peripheral nervous system disease in autoimmune-prone mice. Lupus 6 (1997) 645-651
26. Brey R.L., Sakic B., Szechtman H., and Denburg J.A. Animal models for nervous system disease in systemic lupus erythematosus. Ann. N. Y. Acad. Sci. 823 (1997) 97-106
27. Brooks W.M., Sabet A., Sibbitt W.L., Barker P.B., van Zijl P.C., Duyn J.H., and Moonen C.T. Neurochemistry of brain lesions determined by spectroscopic imaging in systemic lupus erythematosus. J. Rheumatol. 24 (1997) 2323-2329
28. Cabanas F., Pellicer A., Valverde E., Morales C., and Quero J. Central nervous system vasculopathy in neonatal lupus erythematosus. Pediatr. Neurol. 15 (1996) 124-126
29. Chida Y., Sudo N., and Kubo C. Social isolation stress exacerbates autoimmune disease in MRL/lpr mice. J. Neuroimmunol. 158 (2005) 138-144
30. Chinn R.J., Wilkinson I.D., Hall-Craggs M.A., Paley M.N., Shortall E., Carter S., Kendall B.E., Isenberg D.A., Newman S.P., and Harrison M.J. Magnetic resonance imaging of the brain and cerebral proton spectroscopy in patients with systemic lupus erythematosus. Arthritis Rheum. 40 (1997) 36-46
31. Colamussi P., Giganti M., Cittanti C., Dovigo L., Trotta F., Tola M.R., Tamarozzi R., Lucignani G., and Piffanelli A. Brain single-photon emission tomography with Tc-99m-HMPAO in neuropsychiatric systemic lupus erythematosus: relations with EEG and MRI findings and clinical manifestations. Eur. J. Nucl. Med. 22 (1995) 17-24
32. Crimando J., and Hoffman S.A. Detection of brain-reactive autoantibodies in the sera of autoimmune mice using ELISA. J. Immunol. Methods 149 (1992) 87-95
33. DeGiorgio L.A., Konstantinov K.N., Lee S.C., Hardin J.A., Volpe B.T., and Diamond B. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 7 (2001) 1189-1193
34. del R.A., and Besedovsky H.O. The cytokine-HPA axis circuit contributes to prevent or moderate autoimmune processes. Z. Rheumatol. 59 Suppl. 2 (2000) II/31-II/35
35. Del Bigio M.R. Neuropathological changes caused by hydrocephalus. Acta Neuropathol. (Berl.) 85 (1993) 573-585
36. Denburg S.D., Carbotte R.M., Long A.A., and Denburg J.A. Neuropsychological correlates of serum lymphocytotoxic antibodies in systemic lupus erythematosus. Brain Behav. Immun. 2 (1988) 222-234
37. Denenberg V.H., Mobraaten L.E., Sherman G.F., Morrison L., Schrott L.M., Waters N.S., Rosen G.D., Behan P.O., and Galaburda A.M. Effects of the autoimmune uterine/maternal environment upon cortical ectopias, behavior and autoimmunity. Brain Res. 563 (1991) 114-122
38. Denenberg V.H., Sherman G.F., Rosen G.D., Morrison L., Behan P.O., and Galaburda A.M. A behavior profile of the MRL/Mp lpr/lpr mouse and its association with hydrocephalus. Brain Behav. Immun. 6 (1992) 40-49
39. Diederichsen H., and Pyndt I.C. Antibodies against neurons in a patient with systemic lupus erythematosus, cerebral palsy, and epilepsy. Brain 93 (1970) 407-412
40. Dixon F.J., Andrews B.S., Eisenberg R.A., McConahey P.J., Theofilopoulos A.N., and Wilson C.B. Etiology and pathogenesis of a spontaneous lupus-like syndrome in mice. Arthritis Rheum. 21 (1978) S64-S67
41. Elouaai F., Lule J., Benoist H., Appolinaire-Pilipenko S., Atanassov C., Muller S., and Fournie G.J. Autoimmunity to histones, ubiquitin, and ubiquitinated histone H2A in NZB × NZW and MRL-lpr/lpr mice. Anti-histone antibodies are concentrated in glomerular eluates of lupus mice. Nephrol. Dial. Transplant. 9 (1994) 362-366
42. Farrell M., Sakic B., Szechtman H., and Denburg J.A. Effect of cyclophosphamide on leucocytic infiltration in the brain of MRL/lpr mice. Lupus 6 (1997) 268-274
43. Freeman M.E., Kanyicska B., Lerant A., and Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80 (2000) 1523-1631
44. Fujioka M., Okuchi K., Hiramatsu K.I., Sakaki T., Sakaguchi S., and Ishii Y. Specific changes in human brain after hypoglycemic injury. Stroke 28 (1997) 584-587
45. Gerber J., Raivich G., Wellmer A., Noeske C., Kunst T., Werner A., Bruck W., and Nau R. A mouse model of Streptococcus pneumoniae meningitis mimicking several features of human disease. Acta Neuropathol. (Berl.) 101 (2001) 499-508
46. Giuliani F., Goodyer C.G., Antel J.P., and Yong V.W. Vulnerability of human neurons to T cell-mediated cytotoxicity. J. Immunol. 171 (2003) 368-379
47. Gonzalez-Scarano F., Lisak R.P., Bilaniuk L.T., Zimmerman R.A., Atkins P.C., and Zweiman B. Cranial computed tomography in the diagnosis of systemic lupus erythematosus. Ann. Neurol. 5 (1979) 158-165
48. Greenwood D.L., Gitlits V.M., Alderuccio F., Sentry J.W., and Toh B.H. Autoantibodies in neuropsychiatric lupus. Autoimmunity 35 (2002) 79-86
49. Guo Q., Sayeed I., Baronne L.M., Hoffman S.W., Guennoun R., and Stein D.G. Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats. Exp. Neurol. 198 (2006) 469-478
50. Gwag B.J., Koh J.Y., Demaro J.A., Ying H.S., Jacquin M., and Choi D.W. Slowly triggered excitotoxicity occurs by necrosis in cortical cultures. Neuroscience 77 (1997) 393-401
51. Hafler D.A., and Weiner H.L. MS: a CNS and systemic autoimmune disease. Immunol. Today 10 (1989) 104-107
52. Hampton D.W., Seitz A., Chen P., Heber-Katz E., and Fawcett J.W. Altered CNS response to injury in the MRL/MpJ mouse. Neuroscience 127 (2004) 821-832
53. Handa R., Sahota P., Kumar M., Jagannathan N.R., Bal C.S., Gulati M., Tripathi B.M., and Wali J.P. In vivo proton magnetic resonance spectroscopy (MRS) and single photon emission computerized tomography (SPECT) in systemic lupus erythematosus (SLE). Magn. Reson. Imaging 21 (2003) 1033-1037
54. Hanly J.G. Neuropsychiatric lupus. Curr. Rheumatol. Rep. 3 (2001) 205-212
55. Hanly J.G., Robichaud J., and Fisk J.D. Anti-NR2 glutamate receptor antibodies and cognitive function in systemic lupus erythematosus. J. Rheumatol. 33 (2006) 1553-1558
56. Hansen M.K., and Krueger J.M. Subdiaphragmatic vagotomy blocks the sleep- and fever-promoting effects of interleukin-1 beta. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 42 (1997) R1246-R1253
57. Harbeck R.J., Hoffman A.A., Hoffman S.A., Shucard D.W., and Carr R.I. A naturally occurring antibody in New Zealand mice cytotoxic to dissociated cerebellar cells. Clin. Exp. Immunol. 31 (1978) 313-320
58. Hayley S., Merali Z., and Anisman H. Stress and cytokine-elicited neuroendocrine and neurotransmitter sensitization: implications for depressive illness. Stress 6 (2003) 19-32
59. Hess D.C. Cerebral lupus vasculopathy. Mechanisms and clinical relevance. Ann. N. Y. Acad. Sci. 823 (1997) 154-168
60. Hess D.C., Taormina M., Thompson J., Sethi K.D., Diamond B., Rao R., and Feldman D.S. Cognitive and neurologic deficits in the MRL/lpr mouse: a clinicopathologic study. J. Rheumatol. 20 (1993) 610-617
61. Hirohata S., Hirose S., and Miyamoto T. Cerebrospinal fluid IgM, IgA, and IgG indexes in systemic lupus erythematosus. Their use as estimates of central nervous system disease activity. Arch. Intern. Med. 145 (1985) 1843-1846
62. Hoffman S.A., and Harbeck R.J. CNS lupus and the blood-brain barrier. Implications of the Blood-Brain Barrier and Its Manipulation (1989), Plenum Medical Book Co., New York 469-494
63. Hoffman S.A., and Madsen C.S. Brain specific autoantibodies in murine models of systemic lupus erythematosus. J. Neuroimmunol. 30 (1990) 229-237
64. Hoffman S.A., Hoffman A.A., Shucard D.W., and Harbeck R.J. Antibodies to dissociated cerebellar cells in New Zealand mice as demonstrated by immunofluorescence. Brain Res. 142 (1978) 477-486
65. Hoffman S.A., Arbogast D.N., Day T.T., Shucard D.W., and Harbeck R.J. Permeability of the blood-cerebrospinal fluid barrier during acute immune complex disease. J. Immunol. 130 (1983) 1695-1698
66. Hoffman S.A., Arbogast D.N., Ford P.M., Shucard D.W., and Harbeck R.J. Brain-reactive autoantibody levels in the sera of ageing autoimmune mice. Clin. Exp. Immunol. 70 (1987) 74-83
67. Hoffman S.A., Narendran A., Shucard D.W., and Harbeck R.J. Autoantibodies, immune complexes, and behavioral disorders: neuropsychiatric involvement in systemic lupus erythematosus. Drug Dev. Res. 15 (1988) 237-251
68. Hu Y., Dietrich H., Herold M., Heinrich P.C., and Wick G. Disturbed immuno-endocrine communication via the hypothalamo-pituitary-adrenal axis in autoimmune disease. Int. Arch. Allergy Immunol. 102 (1993) 232-241
69. Huang W.S., Chiu P.Y., Tsai C.H., Kao A., and Lee C.C. Objective evidence of abnormal regional cerebral blood flow in patients with systemic lupus erythematosus on Tc-99m ECD brain SPECT. Rheumatol. Int. 22 (2002) 178-181
70. Huerta P.T., Kowal C., DeGiorgio L.A., Volpe B.T., and Diamond B. Immunity and behavior: antibodies alter emotion. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 678-683
71. Isenberg D., Bacon P., Bombardier C., Gladman D., Goldsmith C.H., Kalunian K., Liang M., Maddison P., Nived O., Richter M., et al. Criteria for assessing disease activity in systemic lupus erythematosus. J. Rheumatol. 16 (1989) 1395-1396
72. Jara L.J., Vera-Lastra O., Miranda J.M., Alcala M., and varez-Nemegyei J. Prolactin in human systemic lupus erythematosus. Lupus 10 (2001) 748-756
73. Jennekens F.G., and Kater L. The central nervous system in systemic lupus erythematosus: Part 2. Pathogenetic mechanisms of clinical syndromes: a literature investigation. Rheumatology (Oxford) 41 (2002) 619-630
74. Jongen P.J., Boerbooms A.M., Lamers K.J., Raes B.C., and Vierwinden G. Diffuse CNS involvement in systemic lupus erythematosus: intrathecal synthesis of the 4th component of complement. Neurology 40 (1990) 1593-1596
75. Kaell A.T., Shetty M., Lee B.C., and Lockshin M.D. The diversity of neurologic events in systemic lupus erythematosus. Prospective clinical and computed tomographic classification of 82 events in 71 patients. Arch. Neurol. 43 (1986) 273-276
76. Kelly M.C., and Denburg J.A. Cerebrospinal fluid immunoglobulins and neuronal antibodies in neuropsychiatric systemic lupus erythematosus and related conditions. J. Rheumatol. 14 (1987) 740-744
77. Komatsu N., Kodama K., Yamanouchi N., Okada S., Noda S., Nawata Y., Takabayashi K., Iwamoto I., Saito Y., Uchida Y., Ito H., Yoshikawa K., and Sato T. Decreased regional cerebral metabolic rate for glucose in systemic lupus erythematosus patients with psychiatric symptoms. Eur. Neurol. 42 (1999) 41-48
78. Kovac A.D., Grammig J., Mahlo J., Steiner B., Roth K., Nitsch R., and Bechmann I. Comparison of neuronal density and subfield sizes in the hippocampus of CD95L-deficient (gld), CD95-deficient (lpr) and nondeficient mice. Eur. J. Neurosci. 16 (2002) 159-163
79. Kowal C., DeGiorgio L.A., Nakaoka T., Hetherington H., Huerta P.T., Diamond B., and Volpe B.T. Cognition and immunity; antibody impairs memory. Immunity 21 (2004) 179-188
80. Kyttaris V.C., Katsiari C.G., Juang Y.T., and Tsokos G.C. New insights into the pathogenesis of systemic lupus erythematosus. Curr. Rheumatol. Rep. 7 (2005) 469-475
81. Lawson L.J., Perry V.H., Dri P., and Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39 (1990) 151-170
82. Layfield R., Alban A., Mayer R.J., and Lowe J. The ubiquitin protein catabolic disorders. Neuropathol. Appl. Neurobiol. 27 (2001) 171-179
83. Lechner O., Dietrich H., Oliveira dos S.A., Wiegers G.J., Schwarz S., Harbutz M., Herold M., and Wick G. Altered circadian rhythms of the stress hormone and melatonin response in lupus-prone MRL/MP-fas(Ipr) mice. J. Autoimmun. 14 (2000) 325-333
84. Long A.A., Denburg S.D., Carbotte R.M., Singal D.P., and Denburg J.A. Serum lymphocytotoxic antibodies and neurocognitive function in systemic lupus erythematosus. Ann. Rheum. Dis. 49 (1990) 249-253
85. Lopez-Longo F.J., Carol N., Almoguera M.I., Olazaran J., onso-Farto J.C., Ortega A., Monteagudo I., Gonzalez C.M., and Carreno L. Cerebral hypoperfusion detected by SPECT in patients with systemic lupus erythematosus is related to clinical activity and cumulative tissue damage. Lupus 12 (2003) 813-819
86. Lorton D., Lubahn C., and Bellinger D.L. Potential use of drugs that target neural-immune pathways in the treatment of rheumatoid arthritis and other autoimmune diseases. Curr. Drug Targets Inflamm. Allergy 2 (2003) 1-30
87. Ma X., Foster J., and Sakic B. Distribution and prevalence of leukocyte phenotypes in brains of lupus-prone mice. J. Neuroimmunol. 179 (2006) 26-36
88. Maric D., Millward J.M., Ballok D.A., Szechtman H., Barker J.L., Denburg J.A., and Sakic B. Neurotoxic properties of cerebrospinal fluid from behaviorally impaired autoimmune mice. Brain Res. 920 (2001) 183-193
89. Marshall D., Dangerfield J.P., Bhatia V.K., Larbi K.Y., Nourshargh S., and Haskard D.O. MRL/lpr lupus-prone mice show exaggerated ICAM-1-dependent leucocyte adhesion and transendothelial migration in response to TNF-alpha. Rheumatology (Oxford) 42 (2003) 929-934
90. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22 (1999) 105-122
91. McGuire S.O., Ling Z.D., Lipton J.W., Sortwell C.E., Collier T.J., and Carvey P.M. Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons. Exp. Neurol. 169 (2001) 219-230
92. McHale J.F., Harari O.A., Marshall D., and Haskard D.O. TNF-alpha and IL-1 sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice. J. Immunol. 163 (1999) 3993-4000
93. McIntyre K.R., Ayer-LeLievre C., and Persson H. Class II major histocompatibility complex (MHC) gene expression in the mouse brain is elevated in the autoimmune MRL/Mp-lpr/lpr strain. J. Neuroimmunol. 28 (1990) 39-52
94. McLean B.N., Miller D., and Thompson E.J. 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 (1995) 548-554
95. McMurray R., Keisler D., Kanuckel K., Izui S., and Walker S.E. Prolactin influences autoimmune disease activity in the female B/W mouse. J. Immunol. 147 (1991) 3780-3787
96. Mcnicholl J.M., Glynn D., Mongey A.B., Hutchinson M., and Bresnihan B. Prospective study of neurophysiologic, neurologic and immunologic abnormalities in systemic lupus erythematosus. J. Rheumatol. 21 (1994) 1061-1066
97. Meroni P.L., Tincani A., Sepp N., Raschi E., Testoni C., Corsini E., Cavazzana I., Pellegrini S., and Salmaggi A. Endothelium and the brain in CNS lupus. Lupus 12 (2003) 919-928
98. Miguel E.C., Pereira R.M., Pereira C.A., Baer L., Gomes R.E., de Sa L.C., Hirsch R., de Barros N.G., de Navarro J.M., and Gentil V. Psychiatric manifestations of systemic lupus erythematosus: clinical features, symptoms, and signs of central nervous system activity in 43 patients. Medicine 73 (1994) 224-232
99. Miller E. Immunosuppression-An overview. Semin. Vet. Med. Surg. (Small Anim.) 12 (1997) 144-149
100. Minagar A., and Alexander J.S. Blood-brain barrier disruption in multiple sclerosis. Mult. Scler. 9 (2003) 540-549
101. Mirescu C., and Gould E. Stress and adult neurogenesis. Hippocampus 16 (2006) 233-238
102. Nagata S. Mutations in the Fas antigen gene in lpr mice. Semin. Immunol. 6 (1994) 3-8
103. Nagata S., and Suda T. Fas and Fas ligand: lpr and gld mutations. Immunol. Today 16 (1995) 39-43
104. Narendran A., and Hoffman S.A. Identification of autoantibody reactive integral brain membrane antigens-A two dimensional analysis. J. Immunol. Methods 114 (1988) 227-234
105. Narendran A., and Hoffman S.A. Characterization of brain-reactive autoantibodies in murine models of systemic lupus erythematosus. J. Neuroimmunol. 24 (1989) 113-123
106. Navarrete M.G., and Brey R.L. Neuropsychiatric systemic lupus erythematosus. Curr. Treat. Options Neurol. 2 (2000) 473-485
107. O'Sullivan F.X., Vogelweid C.M., Beschwilliford C.L., and Walker S.E. Differential effects of CD4(+) T cell depletion on inflammatory central nervous system disease, arthritis and sialadenitis in MRL/lpr mice. J. Autoimmun. 8 (1995) 163-175
108. Omdal R., Selseth B., Klow N.E., Husby G., and Mellgren S.I. Clinical neurological, electrophysiological, and cerebral CT scan findings in systemic lupus erythematosus. Scand. J. Rheumatol. 18 (1989) 283-289
109. Omdal R., Brokstad K., Waterloo K., Koldingsnes W., Jonsson R., and Mellgren S.I. Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur. J. Neurol. 12 (2005) 392-398
110. Peress N.S., Roxburgh V.A., and Gelfand M.C. Binding sites for immune components in human choroid plexus. Arthritis Rheum. 24 (1981) 520-526
111. Prendiville J.S., Cabral D.A., Poskitt K.J., Au S., and Sargent M.A. Central nervous system involvement in neonatal lupus erythematosus. Pediatr. Dermatol. 20 (2003) 60-67
112. Quismorio F.P., and Friou G.J. Antibodies reactive with neurons in SLE patients with neuropsychiatric manifestations. Int. Arch. Allergy Appl. Immunol. 43 (1972) 740-748
113. Reilly C.M., Oates J.C., Cook J.A., Morrow J.D., Halushka P.V., and Gilkeson G.S. Inhibition of mesangial cell nitric oxide in MRL/lpr mice by prostaglandin J2 and proliferator activation receptor-gamma agonists. J. Immunol. 164 (2000) 1498-1504
114. Resnick-Silverman L., and Manfredi J.J. Gene-specific mechanisms of p53 transcriptional control and prospects for cancer therapy. J. Cell. Biochem. 99 (2006) 679-689
115. Rice J.S., Kowal C., Volpe B.T., DeGiorgio L.A., and Diamond B. Molecular mimicry: anti-DNA antibodies bind microbial and nonnucleic acid self-antigens. Curr. Top. Microbiol. Immunol. 296 (2005) 137-151
116. Rivest S., Torres G., and Rivier C. Differential effects of central and peripheral injection of interleukin-1 beta on brain c-fos expression and neuroendocrine functions. Brain Res. 587 (1992) 13-23
117. Rivier C., and Rivest S. Mechanisms mediating the effects of cytokines on neuroendocrine functions in the rat. Corticotropin-Releasing Factor (1993), John Wiley & Sons, Chichester 204-225
118. Rocca M.A., Agosta F., Mezzapesa D.M., Ciboddo G., Falini A., Comi G., and Filippi M. An fMRI study of the motor system in patients with neuropsychiatric systemic lupus erythematosus. NeuroImage 30 (2006) 478-484
119. Rolls E.T., and Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Prog. Neurobiol. 79 (2006) 1-48
120. Sakic B., Szechtman H., Keffer M., Talangbayan H., Stead R., and Denburg J.A. A behavioral profile of autoimmune lupus-prone MRL mice. Brain Behav. Immun. 6 (1992) 265-285
121. Sakic B., Szechtman H., Denburg S.D., Carbotte R.M., and Denburg J.A. Brain-reactive antibodies and behavior of autoimmune MRL-lpr mice. Physiol. Behav. 54 (1993) 1025-1029
122. Sakic B., Szechtman H., Denburg S.D., Carbotte R.M., and Denburg J.A. Spatial learning during the course of autoimmune disease in MRL mice. Behav. Brain Res. 54 (1993) 57-66
123. Sakic B., Szechtman H., Talangbayan H., Denburg S.D., Carbotte R.M., and Denburg J.A. Disturbed emotionality in autoimmune MRL-lpr mice. Physiol. Behav. 56 (1994) 609-617
124. Sakic B., Szechtman H., Denburg S.D., and Denburg J.A. Immunosuppressive treatment prevents behavioral deficit in autoimmune MRL-lpr mice. Physiol. Behav. 58 (1995) 797-802
125. Sakic B., Denburg J.A., Denburg S.D., and Szechtman H. Blunted sensitivity to sucrose in autoimmune MRL-lpr mice: a curve-shift study. Brain Res. Bull. 41 (1996) 305-311
126. Sakic B., Szechtman H., Stead R., and Denburg J.A. Joint pathology and behavioral performance in autoimmune MRL-lpr mice. Physiol. Behav. 60 (1996) 901-905
127. Sakic B., Szechtman H., and Denburg J.A. Neurobehavioral alteration in autoimmune mice. Neurosci. Biobehav. Rev. 21 (1997) 327-340
128. Sakic B., Gurunlian L., and Denburg S.D. Reduced aggressiveness and low testosterone levels in autoimmune MRL-lpr males. Physiol. Behav. 63 (1998) 305-309
129. Sakic B., Szechtman H., Denburg J.A., Gorny G., Kolb B., and Whishaw I.Q. Progressive atrophy of pyramidal neuron dendrites in autoimmune MRL-lpr mice. J. Neuroimmunol. 87 (1998) 162-170
130. Sakic B., Laflamme N., Crnic L.S., Szechtman H., Denburg J.A., and Rivest S. Reduced corticotropin-releasing factor and enhanced vasopressin gene expression in brains of mice with autoimmunity-induced behavioral dysfunction. J. Neuroimmunol. 96 (1999) 80-91
131. Sakic B., Kolb B., Whishaw I.Q., Gorny G., Szechtman H., and Denburg J.A. Immunosuppression prevents neuronal atrophy in lupus-prone mice: evidence for brain damage induced by autoimmune disease?. J. Neuroimmunol. 111 (2000) 93-101
132. Sakic B., Maric I., Koeberle P.D., Millward J.M., Szechtman H., Maric D., and Denburg J.A. Increased TUNEL-staining in brains of autoimmune Fas-deficient mice. J. Neuroimmunol. 104 (2000) 147-154
133. Sakic B., Lacosta S., Denburg J., and Szechtman H. Altered neurotransmission in brains of autoimmune mice: pharmacological and neurochemical evidence. J. Neuroimmunol. 129 (2002) 84-96
134. Sakic B., Hanna S.E., and Millward J.M. Behavioral heterogeneity in an animal model of neuropsychiatric lupus. Biol. Psychiatry 57 (2005) 679-687
135. Sakic B., Kirkham D.L., Ballok D.A., Mwanjewe J., Fearon I.M., Macri J., Yu G., Sidor M.M., Denburg J.A., Szechtman H., Lau J., Ball A.K., and Doering L.C. Proliferating brain cells are a target of neurotoxic CSF in systemic autoimmune disease. J. Neuroimmunol. 169 (2005) 68-85
136. Sayeed I., Guo Q., Hoffman S.W., and Stein D.G. Allopregnanolone, a progesterone metabolite, is more effective than progesterone in reducing cortical infarct volume after transient middle cerebral artery occlusion. Ann. Emerg. Med. 47 (2006) 381-389
137. Schwartz M.M., and Roberts J.L. Membranous and vascular choroidopathy: two patterns of immune deposits in systemic lupus erythematosus. Clin. Immunol. Immunopathol. 29 (1983) 369-380
138. Scolding N.J., and Joseph F.G. The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathol. Appl. Neurobiol. 28 (2002) 173-189
139. Shanks N., Moore P.M., Perks P., and Lightman S.L. Alterations in hypothalamic-pituitary-adrenal function correlated with the onset of murine SLE in MRL+/+ and lpr/lpr mice. Brain Behav. Immun. 13 (1999) 348-360
140. Shear D.A., Galani R., Hoffman S.W., and Stein D.G. Progesterone protects against necrotic damage and behavioral abnormalities caused by traumatic brain injury. Exp. Neurol. 178 (2002) 59-67
141. Sherman G.F., Galaburda A.M., Behan P.O., and Rosen G.D. Neuroanatomical anomalies in autoimmune mice. Acta Neuropathol. (Berl.) 74 (1987) 239-242
142. Sherman G.F., Morrison L., Rosen G.D., Behan P.O., and Galaburda A.M. Brain abnormalities in immune defective mice. Brain Res. 532 (1990) 25-33
143. Sibbitt W.L., and Sibbitt R.R. Magnetic resonance spectroscopy and positron emission tomography scanning in neuropsychiatric systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 19 (1993) 851-868
144. Sibbitt W.L., Haseler L.J., Griffey R.H., Hart B.L., Sibbitt R.R., and Matwiyoff N.A. Analysis of cerebral structural changes in systemic lupus erythematosus by proton MR spectroscopy. AJNR Am. J. Neuroradiol. 15 (1994) 923-928
145. Sidor M.M., Sakic B., Malinowski P.M., Ballok D.A., Oleschuk C.J., and Macri J. Elevated immunoglobulin levels in the cerebrospinal fluid from lupus-prone mice. J. Neuroimmunol. 165 (2005) 104-113
146. Singer G.G., Carrera A.C., Marshakrothstein A., Martineza C., and Abbas A.K. Apoptosis, fas and systemic autoimmunity: the MRL-Ipr/Ipr model. Curr. Opin. Immunol. 6 (1994) 913-920
147. Spangelo B.L., and Gorospe W.C. Role of the cytokines in the neuroendocrine-immune system axis. Front. Neuroendocrinol. 16 (1995) 1-22
148. Suh S.W., Fan Y., Hong S.M., Liu Z., Matsumori Y., Weinstein P.R., Swanson R.A., and Liu J. Hypoglycemia induces transient neurogenesis and subsequent progenitor cell loss in the rat hippocampus. Diabetes 54 (2005) 500-509
149. Svenungsson E., Andersson M., Brundin L., van Vollenhoven R., Khademi M., Tarkowski A., Greitz D., Dahlstrom M., Lundberg I., Klareskog L., and Olsson T. Increased levels of proinflammatory cytokines and nitric oxide metabolites in neuropsychiatric lupus erythematosus. Ann. Rheum. Dis. 60 (2001) 372-379
150. Szechtman H., Sakic B., and Denburg J.A. Behaviour of MRL mice: an animal model of disturbed behaviour in systemic autoimmune disease. Lupus 6 (1997) 223-229
151. Theofilopoulos A.N. Murine models of lupus. Systemic Lupus Erythematosus. 2nd ed. (1992), Churchill Livingstone, New York 121-194
152. Tincani A., Brey R., Balestrieri G., Vitali C., Doria A., Galeazzi M., Meroni P.L., Migliorini P., Neri R., Tavoni A., and Bombardieri S. International survey on the management of patients with SLE: 2. The results of a questionnaire regarding neuropsychiatric manifestations. Clin. Exp. Rheumatol. 14 (1996) S23-S29
153. Tomita M., Holman B.J., and Santoro T.J. Aberrant cytokine gene expression in the hippocampus in murine systemic lupus erythematosus. Neurosci. Lett. 302 (2001) 129-132
154. Tomita M., Holman B.J., Williams L.S., Pang K.C., and Santoro T.J. Cerebellar dysfunction is associated with overexpression of proinflammatory cytokine genes in lupus. J. Neurosci. Res. 64 (2001) 26-33
155. 2 and autoantibodies in patients with neuropsychiatric systemic lupus erythematosus and central nervous system infections. Scand. J. Rheumatol. 23 (1994) 57-63
156. Valesini G., Alessandri C., Celestino D., and Conti F. Anti-endothelial antibodies and neuropsychiatric systemic lupus erythematosus. Ann. N. Y. Acad. Sci. 1069 (2006) 118-128
157. van Dam A.P. Diagnosis and pathogenesis of CNS lupus. Rheumatol. Int. 11 (1991) 1-11
158. Vincent A., Dalton P., Clover L., Palace J., and Lang B. Antibodies to neuronal targets in neurological and psychiatric diseases. Ann. N. Y. Acad. Sci. 992 (2003) 48-55
159. Vogelweid C.M., Johnson G.C., Besch-Williford C.L., Basler J., and Walker S.E. Inflammatory central nervous system disease in lupus-prone MRL/lpr mice: comparative histologic and immunohistochemical findings. J. Neuroimmunol. 35 (1991) 89-99
160. Volkow N.D., Warner N., McIntyre R., Valentine A., Kulkarni M., Mullani N., and Gould L. Cerebral involvement in systemic lupus erythematosus. Am. J. Physiol. Imaging 3 (1988) 91-98
161. Walker S.E. Bromocriptine treatment of systemic lupus erythematosus. Lupus 10 (2001) 762-768
162. Walker S.E. Impaired hypothalamic function, prolactinomas, and autoimmune diseases. J. Rheumatol. 33 (2006) 1036-1037
163. Walker S.E., Smarr K.L., Parker J.C., Weidensaul D.N., Nelson W., and McMurray R.W. Mood states and disease activity in patients with systemic lupus erythematosus treated with bromocriptine. Lupus 9 (2000) 527-533
164. Waterloo K., Omdal R., Jacobsen E.A., Klow N.E., Husby G., Torbergsen T., and Mellgren S.I. Cerebral computed tomography and electroencephalography compared with neuropsychological findings in systemic lupus erythematosus. J. Neurol. 246 (1999) 706-711
165. Weller R.O., Mitchell J., Griffin R.L., and Gardner M.J. The effects of hydrocephalus upon the developing brain. Histological and quantitative studies of the ependyma and subependyma in hydrocephalic rats. J. Neurol. Sci. 36 (1978) 383-402
166. Winfield J.B., Shaw M., Silverman L.M., Eisenberg R.A., Wilson III H.A., and Koffler D. Intrathecal IgG synthesis and blood-brain barrier impairment in patients with systemic lupus erythematosus and central nervous system dysfunction. Am. J. Med. 74 (1983) 837-844
167. Woolley C.S., Gould E., and McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531 (1990) 225-231
168. Yamashita T., Ninomiya M., Hernandez A.P., Garcia-Verdugo J.M., Sunabori T., Sakaguchi M., Adachi K., Kojima T., Hirota Y., Kawase T., Araki N., Abe K., Okano H., and Sawamoto K. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 26 (2006) 6627-6636
169. Yamauchi H., Fukuyama H., Ogawa M., Ouchi Y., and Kimura J. Callosal atrophy in patients with lacunar infarction and extensive leukoaraiosis. An indicator of cognitive impairment. Stroke 25 (1994) 1788-1793
170. Yanase K., and Madaio M.P. Nuclear localizing anti-DNA antibodies enter cells via caveoli and modulate expression of caveolin and p53. J. Autoimmun. 24 (2005) 145-151
171. Yoshio T., Hirata D., Onda K., Nara H., and Minota S. Antiribosomal P protein antibodies in cerebrospinal fluid are associated with neuropsychiatric systemic lupus erythematosus. J. Rheumatol. 32 (2005) 34-39
172. Zameer A., and Hoffman S.A. Immunoglobulin binding to brain in autoimmune mice. J. Neuroimmunol. 120 (2001) 10-18
173. Zameer A., and Hoffman S.A. Increased ICAM-1 and VCAM-1 expression in the brains of autoimmune mice. J. Neuroimmunol. 142 (2003) 67-74
174. Zhao M., Momma S., Delfani K., Carlen M., Cassidy R.M., Johansson C.B., Brismar H., Shupliakov O., Frisen J., and Janson A.M. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7925-7930