Purine receptor antagonist modulates serology and affective behaviors in lupus-prone mice: Evidence of autoimmune-induced pain?

Brain, Behavior, and Immunity

Volumn 22, Issue 8, 2008, Pages 1208-1216

  Ballok, David A ^a   Sakic, Boris ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b Brain Body Institute   (Canada)

Author keywords

Analgesia; Anhedonia; Corticosterone; Metabolic perturbations; Neophobia; Neuronal atrophy; Nociception; P2X purine receptors; Pain related behaviors; Suramin

Indexed keywords

ANTINUCLEAR ANTIBODY; CORTICOSTERONE; PURINERGIC RECEPTOR; SUCROSE; SURAMIN;

ANALGESIA; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AUTOIMMUNITY; BRAIN ATROPHY; CHRONIC DRUG ADMINISTRATION; CHRONIC STRESS; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; DISEASE PREDISPOSITION; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUID INTAKE; FOOD INTAKE; GOLGI COMPLEX; GROUPS BY AGE; HIPPOCAMPUS; IMMUNOMODULATION; IMMUNOPATHOLOGY; INFLAMMATION; MALE; MOOD DISORDER; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NOCICEPTION; NONHUMAN; PAIN; PHOBIA; PRIORITY JOURNAL; SEROLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS; TASTE PREFERENCE; TREATMENT OUTCOME;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; AUTOANTIBODIES; AUTOIMMUNITY; BODY WEIGHT; CELL SHAPE; DENDRITES; DISEASE MODELS, ANIMAL; DRINKING; EATING; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; INFLAMMATION; INTERLEUKIN-1BETA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED MRL LPR; MICE, TRANSGENIC; NEURONS; ORGAN SIZE; PAIN; RECEPTORS, PURINERGIC P2; SPLEEN; SURAMIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 52949108812     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2008.06.002     Document Type: Article

References (106)

1. 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
2. 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
3. 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
4. Attal N., and Bouhassira D. Mechanisms of pain in peripheral neuropathy. Acta. Neurol. Scand. Suppl. 173 (1999) 12-24
5. 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
6. Ballok D.A., Szechtman H., and Sakic B. Taste responsiveness and diet preference in autoimmune MRL mice. Behav. Brain Res. 140 (2003) 119-130
7. 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
8. 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
9. 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
10. Ballok D.A. Neuroimmunopathology in a murine model of neuropsychiatric lupus. Brain Res. Rev. 54 (2007) 67-79
11. Bolles R.C., and Fanselow M.S. A perceptual-defensive-recuperative model of fear and pain. Behav. Brain Sci. 3 (1980) 291-323
12. Brebner K., Hayley S., Zacharko R., Merali Z., and Anisman H. Synergistic effects of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha: central monoamine, corticosterone, and behavioral variations. Neuropsychopharmacology 22 (2000) 566-580
13. 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
14. Burnstock G. Purine and pyrimidine receptors. Cell. Mol. Life Sci. 64 (2007) 147-183
15. Carlsten H., and Tarkowski H. Expression of heterozygous lpr gene in MRL mice. I. Defective T-cell reactivity and polyclonal B-cell activation. Scand. J. Immunol. 30 (1989) 457-462
16. Chun S., McEvilly R., Foster J.A., and Sakic B. Proclivity to self-injurious behavior in MRL-lpr mice: implications for autoimmunity-induced damage in the dopaminergic system. Mol. Psychiatry. (2007) 10.1038/sj.mp.4002078
17. Colburn K., Boucek R., Gusewitch G., Wong A., Wat P., and Weeks D. B-adrenergic receptor stimulation increases anti-DNA antibody production in MRL/1 pr mice. J. Rheumatol. 17 (1990) 138-141
18. Colburn K., Wong A.L., Weisbart R.H., and Green L.M. Antiguanosine antibodies in murine and human lupus have the internal image of G-binding proteins. J. Rheumatol. 30 (2003) 993-997
19. Czyrak A., Mackowiak M., Chocyk A., Fijal K., and Wedzony K. Role of glucocorticoids in the regulation of dopaminergic neurotransmission. Pol. J. Pharmacol. 55 (2003) 667-674
20. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann. NY Acad. Sci. 933 (2001) 222-234
21. 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
22. Denburg S.D., and Denburg J.A. Cognitive dysfunction and antiphospholipid antibodies in systemic lupus erythematosus. Lupus 12 (2003) 883-890
23. 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
24. de Vasconcellos A.P., Nieto F.B., Fontella F.U., da Rocha E.R., and Dalmaz C. The nociceptive response of stressed and lithium-treated rats is differently modulated by different flavors. Physiol. Behav. 88 (2006) 382-388
25. 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
26. Donohue H.S., Gabbott P.L., Davies H.A., Rodríguez J.J., Cordero M.I., Sandi C., Medvedev N.I., Popov V.I., Colyer F.M., Peddie C.J., and Stewart M.G. Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 140 (2006) 597-606
27. Dorfman A., and Matalon R. The mucopolysaccharidoses (a review). Proc. Natl. Acad. Sci. USA 73 (1976) 630-637
28. Eskay R.L., Grino M., and Chen H.T. Interleukins, signal transduction, and the immune system-mediated stress response. Adv. Exp. Med. Biol. 274 (1990) 331-343
29. Fairchild G.M., Leitch M., and Ingram C.D. Acute and chronic effects of corticosterone on 5-HT1A receptor-mediated autoinhibition in the rat dorsal raphe nucleus. Neuropharmacology 45 (2003) 925-934
30. Fernandes G., and Good R.A. Inhibition by restricted-calorie diet of lymphoproliferative disease and renal damage in MRL/lpr mice. Proc. Natl. Acad. Sci. USA 81 (1984) 6144-6148
31. Fiore M., Alleva E., Probert L., Kollias G., Angelucci F., and Aloe L. Exploratory and displacement behavior in transgenic mice expressing high levels of brain TNF-alpha. Physiol. Behav. 63 (1998) 571-576
32. Gibb R., and Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J. Neurosci. Methods 79 (1998) 1-4
33. Gilkeson G.S., Mudgett J.S., Seldin M.F., Ruiz P., Alexander A.A., Misukonis M.A., Pisetsky D.S., and Weinberg J.B. Clinical and serologic manifestations of autoimmune disease in MRL-lpr/lpr mice lacking nitric oxide synthase type 2. J. Exp. Med. 186 (1997) 365-373
34. Grippo A.J., Francis J., Beltz T.G., Felder R.B., and Johnson A.K. Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol. Behav. 84 (2005) 697-706
35. Gu L., Johnson M.W., and Lusis A.J. Quantitative trait locus analysis of plasma lipoprotein levels in an autoimmune mouse model. Interactions between lipoprotein metabolism, autoimmune disease, and atherogenesis. Arterioscl. Thromb. Vasc. Biol. 19 (1999) 442-453
36. Hart B.L. Behavioral adaptations to pathogens and parasites: five strategies. Neurosci. Biobehav. Rev. 14 (1990) 273-294
37. Hoffman S.A., Arbogast D.N., Ford P.M., Shucard S.W., and Harbeck R.J. Brain-reactive autoantibody levels in the sera of ageing autoimmune mice. Clin. Exp. Immunol. 70 (1987) 74-83
38. 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
39. Huber J.D., Witt K.A., Hom S., Egleton R.D., Mark K.S., and Davis T.P. Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression. Am. J. Physiol. Heart Circ. Physiol. 280 (2001) H1241-H1248
40. Huber J.D., Hau V.S., Borg L., Campos C.R., Egleton R.D., and Davis T.P. Blood-brain barrier tight junctions are altered during a 72-h exposure to lambda-carrageenan-induced inflammatory pain. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H1531-H1537
41. Huerta P.T., Kowal C., DeGiorgio L.A., Volpe B.T., and Diamond B. Immunity and behavior: antibodies alter emotion. Proc. Natl. Acad. Sci. USA 103 (2006) 678-683
42. Humphrey P.P., Buell G., Kennedy I., Khakh B.S., Michel A.D., Surprenant A., and Trezise D.J. New insights on P2X purinoceptors. Naunyn Schmiedebergs Arch. Pharmacol. 352 (1995) 585-596
43. Isenberg D., Bacon P., Bombardier C., Gladman D., Goldsmith C.H., Kalunian K., Liang M., Maddison P., Nived O., and Richter M. Criteria for assessing disease activity in systemic lupus erythematosus. J. Rheumatol. 16 (1989) 1395-1396
44. Keng T., Privalle C.T., Gilkeson G.S., and Weinberg J.B. Peroxynitrite formation and decreased catalase activity in autoimmune MRL-lpr/lpr mice. Mol. Med. 6 (2000) 779-792
45. Kim D.S., and Palmiter R.D. Interaction of dopamine and adenosine receptor function in behavior: studies with dopamine-deficient mice. Front. Biosci. 13 (2008) 2311-2318
46. Koles L., Furst S., and Illes P. Purine ionotropic (P2X) receptors. Curr. Pharm. Des. 13 (2007) 2368-2384
47. 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
48. Kowal C., DeGiorgio L.A., Lee J.Y., Edgar M.A., Huerta P.T., Volpe B.T., and Diamond B. Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc. Natl. Acad. Sci. USA 103 (2006) 19854-19859
49. Lakshmi S., and Joshi P.G. Co-activation of P2Y2 receptor and TRPV channel by ATP: implications for ATP induced pain. Cell. Mol. Neurobiol. 25 (2005) 819-832
50. Landau A.M., Luk K.C., Jones M.L., Siegrist-Johnstone R., Young Y.K., Kouassi E., Rymar V.V., Dagher A., Sadikot A.F., and Desbarats J. Defective Fas expression exacerbates neurotoxicity in a model of Parkinson's disease. J. Exp. Med. 202 (2005) 575-581
51. 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
52. Liu T., and Tracey D.J. ATP P2X receptors play little role in the maintenance of neuropathic hyperalgesia. Neuroreport 11 (2000) 1669-1672
53. 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
54. Magarinos A.M., Orchinik M., and McEwen B.S. Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res. 809 (1998) 314-318
55. Magarinos A.M., Verdugo J.M., and McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA. 94 (1997) 14002-14009
56. Maric D., Millward J.M., Ballok D.A., Szechtman H., Denburg J.A., Barkera J.L., and Sakic B. Neurotoxic properties of cerebrospinal fluid from behaviorally impaired autoimmune mice. Brain Res. 920 (2001) 183-193
57. Mattson M.P., and Kater S.B. Development and selective neurodegeneration in cell cultures from different hippocampal regions. Brain Res. 490 (1989) 110-125
58. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22 (1999) 105-122
59. McHale J.F., Harari A.O., Marshall D., and Haskard D.O. TNF-alpha and IL-1beta sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice. J. Immunol. 163 (1999) 3993-4000
60. Minor T.R., Huang Q., and Foley E.A. Cytokine-purine interactions in behavioral depression in rats. Integr. Physiol. Behav. Sci. 38 (2003) 189-202
61. Minor T.R., Huang Q., and Witt A.E. Cytokine-purine interactions in traumatic stress, behavioral depression, and sickness. CNS. Neurol. Disord. Drug Targets. 5 (2006) 547-560
62. Monleon S., D'Aquila P., Parra A., Simon V.M., Brain P.F., and Willner P. Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine. Psychopharmacology (Berlin) 117 (1995) 453-457
63. Moskowitz N. Systemic lupus erythematosus of the central nervous system: molecular theories and models for mental disease. Mt. Sinai J. Med. 56 (1989) 23-29
64. Munro G., Erichsen H.K., and Mirza N.R. Pharmacological comparison of anticonvulsant drugs in animal models of persistent pain and anxiety. Neuropharmacology 53 (2007) 609-618
65. Nakazawa K., Inoue K., Fujimori K., and Takanaka A. Effects of ATP antagonists on purinoceptor-operated inward currents in rat phaeochromocytoma cells. Pflugers Arch. 418 (1991) 214-219
66. Newsom-Davis J., Buckley C., Clover L., Hart I., Maddison P., Tuzum E., and Vincent A. Autoimmune disorders of neuronal potassium channels. Ann. NY Acad. Sci. 998 (2003) 202-210
67. Novales-Li P. Suramin exerts in vivo cytokine modulatory properties on splenocytes from experimental allergic encephalomyelitis-induced SJL mice: implications for autoimmune disease therapy. Immunopharmacology 35 (1996) 155-162
68. Pauly J.R., Ullman E.A., and Collins A.C. Adrenocortical hormone regulation of nicotine sensitivity in mice. Physiol. Behav. 44 (1988) 109-116
69. Pawlak R., Skrzypiec A., Sulkowski S., and Buczko W. Ethanol-induced neurotoxicity is counterbalanced by increased cell proliferation in mouse dentate gyrus. Neurosci. Lett. 327 (2002) 83-86
70. Phipps R.P., Spaulding M., and Szakos J. DNA is a potent immunogen for spleen cells and for guanosine-binding B lymphocytes. Cell. Immunol. 113 (1988) 202-213
71. Raine C.S., Canella B., Duijvestijn A.M., and Cross A.H. Homing to central nervous system vasculature by antigen-specific lymphocytes. Lymphocyte/endothelial cell adhesion during the initial stages of autoimmune demyelination. Lab. Invest. 63 (1990) 476-489
72. Rathbone M.P., Middlemiss P.J., Gysbers J.W., Andrew C., Herman M.A., Reed J.K., Ciccarelli R., Di Iorio P., and Caciagli F. Trophic effects of purines in neurons and glial cells. Prog. Neurobiol. 59 (1999) 663-690
73. Rees S., Constantopoulos G., Barranger J.A., and Brady R.O. Organomegaly and histopathology in an animal model of mucopolysaccharidosis induced by suramin. Naunyn Schmiedebergs Arch. Pharmacol. 319 (1982) 262-270
74. 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
75. 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
76. 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
77. 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
78. Sakic B., Szechtman H., and Denburg J.A. Neurobehavioral alterations in autoimmune mice. Neurosci. Biobehav. Rev. 21 (1997) 327-340
79. Sakic B., Szechtman H., Braciak T., Richards C., Gauldie J., and Denburg J.A. Reduced preference for sucrose in autoimmune mice: a possible role of interleukin-6. Brain Res. Bull. 44 (1997) 155-165
80. 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
81. 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
82. Sakic B., Kolb B., Whishaw I.Q., Gorny G., Szechtman H., and Denburd J.A. Immunosuppression prevents neuronal atrophy in lupus-prone mice: evidence for brain damage induced by autoimmune disease?. J. Neuroimmunol. 111 (2000) 93-101
83. Sakic B., Gauldie J., Denburg J.A., and Szechtman H. Behavioral effects of infection with IL-6 adenovector. Brain Behav. Immun. 15 (2001) 25-42
84. Sakic B., Lacosta S., Denburg J.A., and Szechtman H. Altered neurotransmission in brains of autoimmune mice: pharmacological and neurochemical evidence. J. Neuroimmunol. 129 (2002) 84-96
85. 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
86. Sanderson L., Khan A., and Thomas S. Distribution of suramin, an antitrypanosomal drug, across the blood-brain and blood-cerebrospinal fluid interfaces in wild-type and P-glycoprotein transporter-deficient mice. Antimicrob. Agents Chemother. 51 (2007) 3136-3146
87. Sapolsky R.M. Stress, glucocorticoids, and damage to the nervous system: The current state of confusion. Stress 1 (1996) 1-19
88. Schmidt A.P., Lara D.R., and Souza D.O. Proposal of a guanine-based purinergic system in the mammalian central nervous system. Pharmacol. Ther. 116 (2007) 401-416
89. Shanks N., Harbuz M.S., Jessop D.S., Perks P., Moore P.M., and Lightman S.L. Inflammatory disease as chronic stress. Ann. NY Acad. Sci. 840 (1998) 599-607
90. 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
91. 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
92. Siegfried B., Frischknecht H.R., and Nunes de Souza R.L. An ethological model for the study of activation and interaction of pain, memory and defensive systems in the attacked mouse. Role of endogenous opioids. Neurosci. Biobehav. Rev. 14 (1990) 481-490
93. Silverman M.N., Macdougall M.G., Hu F., Pace T.W., Raison C.L., and Miller A.H. Endogenous glucocorticoids protect against TNF-alpha-induced increases in anxiety-like behavior in virally infected mice. Mol. Psychiatry 12 (2007) 408-417
94. Smith L.K., Jadavji N.M., Colwell K.L., Katrina Perehudoff S., and Metz G.A. Stress accelerates neural degeneration and exaggerates motor symptoms in a rat model of Parkinson's disease. Eur. J. Neurosci. 27 (2008) 2133-2146
95. Srivastava A.K., Mohan S., Masinde G.F., Masinde L., Yu H., and Baylink D.J. Identification of quantitative trait loci that regulate obesity and serum lipid levels in MRL/MpJ x SJL/J inbred mice. J. Lip. Res. 47 (2006) 123-133
96. Strassmann G., Fong M., Freter C.E., Windsor S., D'Alessandro F., and Nordan R.P. Suramin interferes with interleukin-6 receptor binding in vitro and inhibits colon-26-mediated experimental cancer cachexia in vivo. J. Clin. Invest. 92 (1993) 2152-2159
97. 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
98. van Dam A.P., Wekking E.M., Callewaert J.A., Schipperijn A.J., Oomen H.A., de Jong J., Swaak A.J., Smeenk R.J., and Feltkamp T.E. Psychiatric symptoms before systemic lupus erythematosus is diagnosed. Rheumatol. Int. 14 (1994) 57-62
99. Vidal S., Kono D.H., and Theofilopoulos A.N. Loci predisposing to autoimmunity in MRL-Fas lpr and C57BL/6-Faslpr mice. J. Clin. Invest. 101 (1998) 696-702
100. Vogelweid C.M., Johnson C.G., 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
101. Waldron J.B., and Sawynok J. Peripheral P2X receptors and nociception: interactions with biogenic amine systems. Pain 110 (2004) 79-89
102. Wekking E.M. Psychiatric symptoms in systemic lupus erythematosus: an update. Psychosom. Med. 55 (1993) 219-228
103. Wolka A.M., Huber J.D., and Davis T.P. Pain and the blood-brain barrier: obstacles to drug delivery. Adv. Drug Deliv. Rev. 55 (2003) 987-1006
104. Wuttke T.V., Jurkat-Rott K., Paulus W., Garncarek M., Lehmann-Horn F., and Lerche H. Peripheral nerve hyperexcitability due to dominant-negative KCNQ2 mutations. Neurology 69 (2007) 2045-2053
105. Yamada K., Iida R., Miyamoto Y., Saito K., Sekikawa K., Seishima M., and Nabeshima T. Neurobehavioral alterations in mice with a targeted deletion of the tumor necrosis factor-alpha gene: implications for emotional behavior. J. Neuroimmunol. 111 (2000) 131-138
106. Zimmermann M. Pathophysiological mechanisms of fibromyalgia. Clin. J. Pain. 7 (1991) S8-S15