Proclivity to self-injurious behavior in MRL-lpr mice: Implications for autoimmunity-induced damage in the dopaminergic system

Molecular Psychiatry

Volumn 13, Issue 11, 2008, Pages 1043-1053

  Chun, S ^a   McEvilly, R ^a   Foster, J A ^a,b   Sakic, B ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b Brain Body Institute   (Canada)

Author keywords

Dopamine; MRL mice; Neuropsychiatric lupus; Quinpirole; Self injurious behavior; Sensitization

Indexed keywords

DOPAMINE 2 RECEPTOR; MESSENGER RNA; QUINPIROLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; AUTOMUTILATION; BEHAVIOR; BEHAVIOR DISORDER; BITE; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; GROOMING; IMMUNE STATUS; IN SITU HYBRIDIZATION; LUPUS LIKE SYNDROME; MALE; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; SPLENOMEGALY; STEREOTYPY; SUBSTANTIA NIGRA; THORAX; WOUND;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; AUTOIMMUNITY; BODY WEIGHT; DOPAMINE; DOPAMINE AGONISTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXPLORATORY BEHAVIOR; GROOMING; MALE; MICE; MICE, INBRED MRL LPR; ORGAN SIZE; QUINPIROLE; REACTION TIME; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; RNA, MESSENGER; SELF-INJURIOUS BEHAVIOR;

EID: 54249125420     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/sj.mp.4002078     Document Type: Article

References (65)

1. Baum KA, Hopf U, Nehrig C, Stover M, Schorner W. Systemic lupus erythematosus: neuropsychiatric signs and symptoms related to cerebral MRI findings. Clin Neurol Neurosurg 1993; 95: 29-34.
2. Bosma GP, Middelkoop HA, Rood MJ, Bollen EL, Huizinga TW, van Buchem MA. Association of global brain damage and clinical functioning in neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 2002; 46: 2665-2672.
3. 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.
4. Oda K, Matsushima E, Okubo Y, Ohta K, Murata Y, Koike R et al. Abnormal regional cerebral blood flow in systemic lupus erythematosus patients with psychiatric symptoms. J Clin Psychiatry 2005; 66: 907-913.
5. 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.
6. Trysberg E, Tarkowski A. Cerebral inflammation and degeneration in systemic lupus erythematosus. Curr Opin Rheumatol 2004; 16: 527-533.
7. Theofilopoulos AN. Murine models of lupus. In: Lahita RG (ed). Systemic Lupus Erythematosus, 2 edn. Churchill Livingstone: New York, 1992, pp 121-194.
8. Alexander EL, Murphy ED, Roths JB, Alexander GE. Congenic autoimmune murine models of central nervous system disease in connective tissue disorders. Ann Neurol 1983; 14: 242-248.
9. Sakic B, Szechtman H, Denburg JA. Neurobehavioral alteration in autoimmune mice. Neurosci Biobehav Rev 1997; 21: 327-340.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
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.
16. 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.
17. Elhwuegi AS. Central monoamines and their role in major depression. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 435-451.
18. Sakic B, Lacosta S, Denburg J, Szechtman H. Altered neurotransmission in brains of autoimmune mice: pharmacological and neurochemical evidence. J Neuroimmunol 2002; 129: 84-96.
19. Wagner GC, Avena N, Kita T, Nakashima T, Fisher H, Halladay AK. Risperidone reduction of amphetamine-induced self-injurious behavior in mice. Neuropharmacology 2004; 46: 700-708.
20. Mori T, Ito S, Kita T, Narita M, Suzuki T, Sawaguchi T. Effects of mu-, delta- and kappa-opioid receptor agonists on methamphetamine-induced self-injurious behavior in mice. Eur J Pharmacol 2006; 532: 81-87.
21. Saito Y, Takashima S. Neurotransmitter changes in the pathophysiology of Lesch-Nyhan syndrome. Brain Dev 2000; 22(Suppl 1): S122-S131.
22. Breese GR, Knapp DJ, Criswell HE, Moy SS, Papadeas ST, Blake BL. The neonate-6-hydroxydopamine-lesioned rat: a model for clinical neuroscience and neurobiological principles. Brain Res Brain Res Rev 2005; 48: 57-73.
23. Deutsch SI, Long KD, Rosse RB, Mastropaolo J, Eller J. Hypothesized deficiency of guanine-based purines may contribute to abnormalities of neurodevelopment, neuromodulation, and neurotransmission in Lesch-Nyhan syndrome. Clin Neuropharmacol 2005; 28: 28-37.
24. 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.
25. Anderson KK, Ballok DA, Prasad N, Szechtman H, Sakic B. Impaired response to amphetamine and neuronal degeneration in the nucleus accumbens of autoimmune MRL-lpr mice. Behav Brain Res 2006; 166: 32-38.
26. Zhou LW, Qin ZH, Weiss B. Downregulation of stereotyped behavior and production of latent locomotor behaviors in mice treated continuously with quinpirole. Neuropsychopharmacology 1991; 4: 47-55.
27. Yokoyama C, Okamura H. Self-injurious behavior and dopaminergic neuron system in neonatal 6-hydroxydopamine-lesioned rat: 1. Dopaminergic neurons and receptors. J Pharmacol Exp Ther 1997; 280: 1016-1030.
28. Whitaker NG, Lindstrom TD. Disposition and biotransformation of quinpirole, a new D-2 dopamine agonist antihypertensive agent, in mice, rats, dogs, and monkeys. Drug Metab Dispos 1987; 15: 107-113.
29. Akhisaroglu M, Kurtuncu M, Manev H, Uz T. Diurnal rhythms in quinpirole-induced locomotor behaviors and striatal D2/D3 receptor levels in mice. Pharmacol Biochem Behav 2005; 80: 371-377.
30. Shishido T, Watanabe Y, Kato K, Horikoshi R, Niwa SI. Effects of dopamine, NMDA, opiate, and serotonin-related agents on acute methamphetamine-induced self-injurious behavior in mice. Pharmacol Biochem Behav 2000; 66: 579-583.
31. 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.
32. 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.
33. Sakic B, Szechtman H, Keffer M, Talangbayan H, Stead R, Denburg JA. A behavioral profile of autoimmune lupus-prone MRL mice. Brain Behav Immun 1992; 6: 265-285.
34. Sakic B, Laflamme N, Crnic LS, Szechtman H, Denburg JA, Rivest S. Reduced corticotropin-releasing factor and enhanced vasopressin gene expression in brains of mice with autoimmunity-induced behavioral dysfunction. J Neuroimmunol 1999; 96: 80-91.
35. Cooper JR, Bloom FE, Roth RH. Dopamine. In: Cooper JR, Bloom FE, Robert RH, (eds). The Biochemical Basis of Neuropharmacology, 8th edn. Oxford University Press Inc.: New York, 2002 pp 293-351.
36. Petitto JM, Huang Z, Lo J, Beck RD, Rinker C, Hartemink DA. Relationship between the development of autoimmunity and sensorimotor gating in MRL-lpr mice with reduced IL-2 production. Neurosci Lett 2002; 328: 304-308.
37. Peng RY, Mansbach RS, Braff DL, Geyer MA. A D2 dopamine receptor agonist disrupts sensorimotor gating in rats. Implications for dopaminergic abnormalities in schizophrenia. Neuropsychopharmacology 1990; 3: 211-218.
38. Tsao CW, Lin YS, Cheng JT. Effect of dopamine on immune cell proliferation in mice. Life Sci 1997; 61: L-71.
39. Ilani T, Strous RD, Fuchs S. Dopaminergic regulation of immune cells via D3 dopamine receptor: a pathway mediated by activated T cells. FASEB J 2004; 18: 1600-1602.
40. Delfs JM, Kelley AE. The role of D1 and D2 dopamine receptors in oral stereotypy induced by dopaminergic stimulation of the ventrolateral striatum. Neuroscience 1990; 39: 59-67.
41. Neal-Beliveau BS, Joyce JN. Timing: a critical determinant of the functional consequences of neonatal 6-OHDA lesions. Neurotoxicol Teratol 1999; 21: 129-140.
42. Kostrzewa RM. Dopamine receptor supersensitivity. Neurosci Biobehav Rev 1995; 19: 1-17.
43. Sakic B, Hanna SE, Millward JM. Behavioral heterogeneity in an animal model of neuropsychiatric lupus. Biol Psychiatry 2005; 57: 679-687.
44. Lechner O, Dietrich H, Oliveira dos SA, Wiegers GJ, Schwarz S, Harbutz M et al. Altered circadian rhythms of the stress hormone and melatonin response in lupus-prone MRL/MP-fas(Ipr) mice. J Autoimmun 2000; 14: 325-333.
45. Wrobel A, Zebrowska-Lupina I, Wielosz M. Dexamethasone reduces locomotor stimulation induced by dopamine agonists in mice. Pharmacol Rep 2005; 57: 451-457.
46. 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.
47. 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.
48. Anisman H, Merali Z, Hayley S. Sensitization associated with stressors and cytokine treatments. Brain Behav Immun 2003; 17: 86-93.
49. Tepper JM, Sun BC, Martin LP, Creese I. Functional roles of dopamine D2 and D3 autoreceptors on nigrostriatal neurons analyzed by antisense knockdown in vivo. J Neurosci 1997; 17: 2519-2530.
50. Stanwood GD, Lucki I, McGonigle P. Differential regulation of dopamine D2 and D3 receptors by chronic drug treatments. J Pharmacol Exp Ther 2000; 295: 1232-1240.
51. Kostrzewa RM, Kostrzewa JP, Nowak P, Kostrzewa RA, Brus R. Dopamine D2 agonist priming in intact and dopamine-lesioned rats. Neurotox Res 2004; 6: 457-462.
52. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 2000; 20: 6309-6316.
53. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990; 39: 151-170.
54. Ballok DA, Ma X, Denburg JA, Arsenault L, Sakic B. Ibuprofen fails to prevent brain pathology in a model of neuropsychiatric lupus. J Rheumatol 2006; 33: 2199-2213.
55. Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 2002; 202: 13-23.
56. Graham DG. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol Pharmacol 1978; 14: 633-643.
57. Asanuma M, Miyazaki I, 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 2003; 5: 165-176.
58. Blum D, Torch S, Lambeng N, Nissou M, Benabid AL, Sadoul R et al. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 2001; 65: 135-172.
59. Faber-Elmann A, Eilat E, Zinger H, Mozes E. A peptide based on an anti-DNA autoantibody downregulates matrix metalloproteinases in murine models of lupus. Clin Immunol 2002; 105: 223-232.
60. Teismann P, Vila M, Choi DK, Tieu K, Wu DC, Jackson-Lewis V et al. COX-2 and neurodegeneration in Parkinson's disease. Ann N YAcad Sci 2003; 991: 272-277.
61. Lal H, Forster MJ. Autoimmunity and age-associated cognitive decline. Neurobiol Aging 1988; 9: 733-742.
62. Zameer A, Hoffman SA. Immunoglobulin binding to brain in autoimmune mice. J Neuroimmunol 2001; 120: 10-18.
63. Sidor MM, Sakic B, Malinowski PM, Ballok DA, Oleschuk CJ, Macri J. Elevated immunoglobulin levels in the cerebrospinal fluid from lupus-prone mice. J Neuroimmunol 2005; 165: 104-113.
64. 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.
65. Alexander JJ, Zwingmann C, Quigg R. MRL/lpr mice have alterations in brain metabolism as shown with [(1)H-(13)C] NMR spectroscopy. Neurochem Int 2005; 47: 143-151.