Time course and nature of brain atrophy in the MRL mouse model of central nervous system lupus

Arthritis and Rheumatism

Volumn 60, Issue 6, 2009, Pages 1764-1774

  Sled, John G ^a   Spring, Shoshana ^a   Van Eede, Matthijs ^a   Lerch, Jason P ^a   Ullal, Sangeeta ^b   Sakic, Boris ^b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BRAIN ATROPHY; BRAIN CORTEX; BRAIN REGION; BRAIN VENTRICLE; CENTRAL NERVOUS SYSTEM DISEASE; CENTRAL NERVOUS SYSTEM LUPUS; CEREBELLUM; CEREBROSPINAL FLUID; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; EMOTION; FEMALE; HIPPOCAMPUS; LIMBIC SYSTEM; LUPUS ERYTHEMATOSUS; MALE; MESENCEPHALON; MORPHOMETRICS; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PERIAQUEDUCTAL GRAY MATTER; PONS; PRIORITY JOURNAL; SUPERIOR COLLICULUS; SYSTEMIC LUPUS ERYTHEMATOSUS; TEMPORAL CORTEX;

ANIMALS; ATROPHY; BEHAVIOR, ANIMAL; BRAIN; CEREBELLUM; CEREBRAL CORTEX; CEREBRAL VENTRICLES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HIPPOCAMPUS; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED MRL LPR; TIME FACTORS;

EID: 66449134778     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.24523     Document Type: Article

References (50)

1. Brooks WM, Sabet A, Sibbitt WL, Barker PB, van Zijl PC, Duyn JH, et al. Neurochemistry of brain lesions determined by spectroscopic imaging in systemic lupus erythematosus. J Rheumatol 1997;24:2323-2329 (Pubitemid 28005130)
2. Jennings JE, Sundgren PC, Attwood J, McCune J, Maly P. Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 2004;46:15-21. (Pubitemid 38248036)
3. Lopez-Longo FJ, Carol N, Almoguera MI, Olazaran J, Alonso-Farto JC, Ortega A, et al. Cerebral hypoperfusion detected by SPECT in patients with systemic lupus erythematosus is related to clinical activity and cumulative tissue damage. Lupus 2003;12:813-819 (Pubitemid 37463097)
4. Yoshida A, Shishido F, Kato K, Watanabe H, Seino O. Evaluation of cerebral perfusion in patients with neuropsychiatric systemic lupus erythematosus using 123I-IMP SPECT. Ann Nucl Med 2007;21:151-158 (Pubitemid 47216694)
5. Waterloo K, Omdal R, Jacobsen EA, Klow NE, Husby G, Torbergsen T, et al. Cerebral computed tomography and electroencephalography compared with neuropsychological findings in systemic lupus erythematosus. J Neurol 1999;246:706-711 (Pubitemid 29417854)
6. Trysberg E, Nylen K, Rosengren LE, Tarkowski A. Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum 2003;48:2881-2887 (Pubitemid 37280617)
7. Welsh RC, Rahbar H, Foerster B, Thurnher M, Sundgren PC. Brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus with new acute neurological symptoms. J Magn Reson Imaging 2007;26:541-551 (Pubitemid 350194574)
8. Alexander JJ, Quigg RJ. Systemic lupus erythematosus and the brain: what mice are telling us. Neurochem Int 2007;50:5-11. (Pubitemid 44879681)
9. Sakic B, Szechtman H, Talangbayan H, Denburg SD, Carbotte RM, Denburg JA. Behaviour and immune status of MRL mice in the postweaning period. Brain Behav Immun 1994;8:1-13. (Pubitemid 24163516)
10. Sakic B, Szechtman H, Denburg JA. Neurobehavioral alteration in autoimmune mice. Neurosci Biobehav Rev 1997;21:327-340
11. Sakic B, Szechtman H, Denburg JA, Gorny G, Kolb B, Whishaw IQ. Progressive atrophy of pyramidal neuron dendrites in autoimmune MRL/lpr mice. J Neuroimmunol 1998;87:162-170 (Pubitemid 28319857)
12. Sakic B, Kolb B, Whishaw IQ, Gorny G, Szechtman H, Denburg JA. Immunosuppression prevents neuronal atrophy in lupus-prone mice: evidence for brain damage induced by autoimmune disease? J Neuroimmunol 2000;111:93-101.
13. Sakic B, Maric I, Koeberle PD, Millward JM, Szechtman H, Maric D, et al. Increased TUNEL-staining in brains of autoimmune Fas-deficient mice. J Neuroimmunol 2000;104:147-154 (Pubitemid 30125405)
14. Ballok DA, Millward JM, Sakic B. Neurodegeneration in autoimmune MRL/lpr mice as revealed by Fluoro Jade B staining. Brain Res 2003;964:200-210 (Pubitemid 36165144)
15. Ballok DA, Woulfe J, Sur M, Cyr M, Sakic B. Hippocampal damage in mouse and human forms of systemic autoimmune disease. Hippocampus 2004;14:649-661 (Pubitemid 39107018)
16. Denenberg VH, Sherman GF, Rosen GD, Morrison L, Behan PO, Galaburda AM. A behavior profile of the MRL/Mp lpr/lpr mouse and its association with hydrocephalus. Brain Behav Immun 1992;6:40-49
17. Sakic B, Hanna SE, Millward JM. Behavioral heterogeneity in an animal model of neuropsychiatric lupus. Biol Psychiatry 2005;57:679-687 (Pubitemid 40409708)
18. Sakic B, Szechtman H, Talangbayan H, Denburg SD, Carbotte RM, Denburg JA. Disturbed emotionality in autoimmune MRL-lpr mice. Physiol Behav 1994;56:609-617 (Pubitemid 24269588)
19. Ballok DA, Earls AM, Krasnik C, Hoffman SA, Sakic B. Autoimmune-induced damage of the midbrain dopaminergic system in lupus-prone mice. J Neuroimmunol 2004;152:83-97. (Pubitemid 38829706)
20. Sakic B, Denburg JA, Denburg SD, Szechtman H. Blunted sensitivity to sucrose in autoimmune MRL/lpr mice: a curve-shift study. Brain Res Bull 1996;41:305-311 (Pubitemid 26398576)
21. Maric D, Millward JM, Ballok DA, Szechtman H, Barker JL, Denburg JA, et al. Neurotoxic properties of cerebrospinal fluid from behaviorally impaired autoimmune mice. Brain Res 2001;920:183-193 (Pubitemid 33086792)
22. Vogelweid CM, Johnson GC, Besch-Williford CL, Basler J, Walker SE. Inflammatory central nervous system disease in lupus-prone MRL/lpr mice: comparative histologic and immunohistochemical findings. J Neuroimmunol 1991;35:89-99.
23. Dorr AE, Lerch JP, Spring S, Kabani N, Henkelman RM. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 2008;42:60-69
24. Lerch JP, Carroll JB, Dorr A, Spring S, Evans AC, Hayden MR, et al. Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. Neuroimage 2008;41:243-251
25. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995;57:289-300.
26. Nieman BJ, Flenniken AM, Adamson SL, Henkelman RM, Sled JG. Anatomical phenotyping in the brain and skull of a mutant mouse by magnetic resonance imaging and computed tomography. Physiol Genomics 2006;24:154-162
27. Zar JH. Biostatistical analysis. 4th ed. New York: Prentice-Hall; 1999.
28. Sakic B, Kirkham DL, Ballok DA, Mwanjewe J, Fearon IM, Macri J, et al. Proliferating brain cells are a target of neurotoxic CSF in systemic autoimmune disease. J Neuroimmunol 2005;169:68-85. (Pubitemid 41527093)
29. Park C, Sakamaki K, Tachibana O, Yamashima T, Yamashita J, Yonehara S. Expression of Fas antigen in the normal mouse brain. Biochem Biophys Res Commun 1998;252:623-628 (Pubitemid 28556826)
30. Ishimura R, Martin GR, Ackerman SL. Loss of apoptosis-inducing factor results in cell-type-specific neurogenesis defects. J Neurosci 2008;28:4938-4948
31. Tang B, Matsuda T, Akira S, Nagata N, Ikehara S, Hirano T, et al. Age-associated increase in interleukin 6 in MRL/lpr mice. Int Immunol 1991;3:273-278
32. Vallieres L, Campbell IL, Gage FH, Sawchenko PE. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 2002;22:486-492 (Pubitemid 34049087)
33. Prendiville JS, Cabral DA, Poskitt KJ, Au S, Sargent MA. Central nervous system involvement in neonatal lupus erythematosus. Pediatr Dermatol 2003;20:60-67 (Pubitemid 37047175)
34. Denenberg VH, Mobraaten LE, Sherman GF, Morrison L, Schrott LM, Waters NS, et al. Effects of the autoimmune uterine/maternal environment upon cortical ectopias, behavior and autoimmunity. Brain Res 1991;563:114-122
35. Lee JY, Huerta PT, Zhang J, Kowal C, Bertini E, Volpe BT, et al. Neurotoxic autoantibodies mediate congenital cortical impairment of offspring in maternal lupus. Nat Med 2009;15:91-96
36. Nadler DM, Klein NW, Aramli LA, Chambers BJ, Mayes M, Wener MH. The direct embryotoxicity of immunoglobulin G fractions from patients with systemic lupus erythematosus. Am J Reprod Immunol 1995;34:349-355
37. Ross G, Sammaritano L, Nass R, Lockshin M. Effects of mothers' autoimmune disease during pregnancy on learning disabilities and hand preference in their children. Arch Pediatr Adolesc Med 2003;157:397-402. (Pubitemid 36443714)
38. DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 2001;7:1189-1193 (Pubitemid 33063773)
39. lpr mice. J Autoimmun 2000;14:325-333
40. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 2000;57:925-935
41. Sakic B, Gurunlian L, Denburg SD. Reduced aggressiveness and low testosterone levels in autoimmune MRL/lpr males. Physiol Behav 1998;63:305-309 (Pubitemid 28034084)
42. Sakic B, Szechtman H, Denburg SD, Carbotte RM, Denburg JA. Spatial learning during the course of autoimmune disease in MRL mice. Behav Brain Res 1993;54:57-66. (Pubitemid 23134666)
43. Chun S, McEvilly R, Foster JA, Sakic B. Proclivity to self-injurious behavior in MRL/lpr mice: implications for autoimmunity-induced damage in the dopaminergic system. Mol Psychiatry 2008;13:1043-1053
44. Bosma GP, Rood MJ, Zwinderman AH, Huizinga TW, van Buchem MA. Evidence of central nervous system damage in patients with neuropsychiatric systemic lupus erythematosus, demonstrated by magnetization transfer imaging. Arthritis Rheum 2000;43:48-54. (Pubitemid 30368212)
45. Huizinga TW, Steens SC, van Buchem MA. Imaging modalities in central nervous system systemic lupus erythematosus. Curr Opin Rheumatol 2001;13:383-388 (Pubitemid 32929867)
46. Csepany T, Bereczki D, Kollar J, Sikula J, Kiss E, Csiba L. MRI findings in central nervous system systemic lupus erythematosus are associated with immunoserological parameters and hypertension. J Neurol 2003;250:1348-1354 (Pubitemid 37456896)
47. Zhang L, Harrison M, Heier LA, Zimmerman RD, Ravdin L, Lockshin M, et al. Diffusion changes in patients with systemic lupus erythematosus. Magn Reson Imaging 2007;25:399-405. (Pubitemid 46413649)
48. Chinn RJ, Wilkinson ID, Hall-Craggs MA, Paley MN, Shorthall E, Carter S, et al. Magnetic resonance imaging of the brain and cerebral proton spectroscopy in patients with systemic lupus erythematosus. Arthritis Rheum 1997;40:36-46. (Pubitemid 27044034)
49. Sibbitt WL Jr, Haseler LJ, Griffey RH, Hart BL, Sibbitt RR, Matwiyoff NA. Analysis of cerebral structural changes in systemic lupus erythematosus by proton MR spectroscopy. AJNR Am J Neuroradiol 1994;15:923-928 (Pubitemid 24153783)
50. 13C] NMR spectroscopy. Neurochem Int 2005;47:143-151