Mechanistic insights into corticosteroids in multiple sclerosis: War horse or chameleon?

Clinical Neurology and Neurosurgery

Volumn 119, Issue , 2014, Pages 6-16

  Krieger, Stephen ^a   Sorrells, Shawn F ^b   Nickerson, Molly ^c   Pace, Thaddeus W W ^d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Questcor Pharmaceuticals Inc   (United States)

^d UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Corticosteroids; Exacerbations; Glucocorticoids; Multiple sclerosis; Relapses

Indexed keywords

CORTICOSTEROID; GLUCOCORTICOID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CALCIUM CELL LEVEL; CLINICAL PRACTICE; COMORBIDITY; CORTICOSTEROID THERAPY; DEPRESSION; DISEASE EXACERBATION; DNA BINDING; DRUG MECHANISM; DRUG MEGADOSE; DRUG TOLERABILITY; HIPPOCAMPUS; HUMAN; IMMUNE DYSREGULATION; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; MACROPHAGE; MAJOR DEPRESSION; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL NECROSIS; PROTEIN PROTEIN INTERACTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); RELAPSE; REMYELINIZATION; T LYMPHOCYTE; TREATMENT DURATION; TREATMENT RESPONSE; UNSPECIFIED SIDE EFFECT;

CORTICOSTEROIDS; EXACERBATIONS; GLUCOCORTICOIDS; MULTIPLE SCLEROSIS; RELAPSES;

ADRENAL CORTEX HORMONES; ANTI-INFLAMMATORY AGENTS; DEPRESSIVE DISORDER, MAJOR; DISEASE PROGRESSION; HUMANS; MULTIPLE SCLEROSIS; TREATMENT OUTCOME;

EID: 84893349991     PISSN: 03038467     EISSN: 18726968     Source Type: Journal    
DOI: 10.1016/j.clineuro.2013.12.021     Document Type: Article

References (121)

1. P.S. Hench The present status of cortisone and ACTH in general medicine Proc R Soc Med 43 1950 769 773
2. G. Neeck Fifty years of experience with cortisone therapy in the study and treatment of rheumatoid arthritis Ann N Y Acad Sci 966 2002 28 38 (Pubitemid 34729158)
3. G.A. Schumacher Critique of experimental trials of therapy in multiple sclerosis Neurology 24 1974 1010 1014
4. F.D. Lublin, M. Baier, and G. Cutter Effect of relapses on development of residual deficit in multiple sclerosis Neurology 61 2003 1528 1532 (Pubitemid 37505574)
5. G.F. Wu, and E. Alvarez The immunopathophysiology of multiple sclerosis Neurol Clin 29 2011 257 278
6. E.C. Breij, B.P. Brink, R. Veerhuis, van den, R. Vloet, and R. Yan et al. Homogeneity of active demyelinating lesions in established multiple sclerosis Ann Neurol 63 2008 16 25 (Pubitemid 351240547)
7. A. Bar-Or, P.A. Calabresi, D. Arnold, C. Markowitz, S. Shafer, and L.H. Kasper et al. Rituximab in relapsing-remitting multiple sclerosis: a 72-week, open-label, phase I trial Ann Neurol 63 2008 395 400 (Pubitemid 351499869)
8. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat Neurosci 10 2007 1387 1394 (Pubitemid 350014685)
9. J.W. Peterson, L. Bo, S. Mork, A. Chang, and B.D. Trapp Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions Ann Neurol 50 2001 389 400 (Pubitemid 32848742)
10. F.D. Lublin The incomplete nature of multiple sclerosis relapse resolution J Neurol Sci 256 Suppl. 1 2007 S14 S18
11. C. Renoux Natural history of multiple sclerosis: long-term prognostic factors Neurol Clin 29 2011 293 308
12. P. Repovic, and F.D. Lublin Treatment of multiple sclerosis exacerbations Neurol Clin 29 2011 389 400
13. A.J. Thompson, C. Kennard, M. Swash, B. Summers, G.M. Yuill, and D.I. Shepherd et al. Relative efficacy of intravenous methylprednisolone and ACTH in the treatment of acute relapse in MS Neurology 39 1989 969 971 (Pubitemid 19170424)
14. ® Gel (repository corticotropin injection) [prescribing information] 2012
15. ® (methylprednisolone sodium succinate for injection, USP) [prescribing information] 2012
16. R.W. Beck, P.A. Cleary, M.M. Anderson Jr., J.L. Keltner, W.T. Shults, and D.I. Kaufman et al. A randomized, controlled trial of corticosteroids in the treatment of acute optic neuritis. The Optic Neuritis Study Group N Engl J Med 326 1992 581 588
17. M. Debono, C. Ghobadi, A. Rostami-Hodjegan, H. Huatan, M.J. Campbell, and J. Newell-Price et al. Modified-release hydrocortisone to provide circadian cortisol profiles J Clin Endocrinol Metab 94 2009 1548 1554
18. C.A. Morgan III, S. Wang, J. Mason, S.M. Southwick, P. Fox, and G. Hazlett et al. Hormone profiles in humans experiencing military survival training Biol Psychiatry 47 2000 891 901
19. T.W.W. Pace, L.T. Negi, D.D. Adame, S.P. Cole, T.I. Sivilli, and T.D. Brown et al. Effect of compassion meditation on neuroendocrine, innate immune and behavioral responses to psychosocial stress Opt Lett 34 2009 87 98
20. C.J. Needs, M. Smith, J. Boutagy, S. Donovan, D. Cosh, and M. McCredie et al. Comparison of methylprednisolone (1 g IV) with prednisolone (1 g orally) in rheumatoid arthritis: a pharmacokinetic and clinical study J Rheumatol 15 1988 224 228 (Pubitemid 18073742)
21. P.J. Hayball, D.G. Cosh, M.J. Ahern, D.W. Schultz, and P.J. Roberts-Thomson High dose oral methylprednisolone in patients with rheumatoid arthritis: pharmacokinetics and clinical response Eur J Clin Pharmacol 42 1992 85 88
22. Pavlaki AN, Magiakou MA, Chrousos GP. Chapter 14: glucocorticoid therapy and adrenal support. http://www.endotext.org/adrenal/adrenal14/adrenalframe14 [accessed 29.03.2013].
23. L. Durelli, D. Cocito, A. Riccio, C. Barile, B. Bergamasco, and G.F. Baggio et al. High-dose intravenous methylprednisolone in the treatment of multiple sclerosis: clinical-immunologic correlations Neurology 36 1986 238 243 (Pubitemid 16124215)
24. N.M. Milligan, R. Newcombe, and D.A. Compston A double-blind controlled trial of high dose methylprednisolone in patients with multiple sclerosis. 1: Clinical effects J Neurol Neurosurg Psychiatry 50 1987 511 516 (Pubitemid 17067536)
25. D. Barnes, R.A. Hughes, R.W. Morris, O. Wade-Jones, P. Brown, and T. Britton et al. Randomised trial of oral and intravenous methylprednisolone in acute relapses of multiple sclerosis Lancet 349 1997 902 906 (Pubitemid 27139818)
26. F. Sellebjerg, J.L. Frederiksen, P.M. Nielsen, and J. Olesen Double-blind, randomized, placebo-controlled study of oral, high-dose methylprednisolone in attacks of MS Neurology 51 1998 529 534 (Pubitemid 28406333)
27. R. Berkovich Treatment of acute relapses in multiple sclerosis Neurotherapeutics 10 2013 97 105
28. G. Filippini, F. Brusaferri, W.A. Sibley, A. Citterio, G. Ciucci, and R. Midgard et al. Corticosteroids or ACTH for acute exacerbations in multiple sclerosis Cochrane Database Syst Rev 4 2000 CD001331
29. D.M. Miller, B. Weinstock-Guttman, F. Bethoux, J.C. Lee, G. Beck, and V. Block et al. A meta-analysis of methylprednisolone in recovery from multiple sclerosis exacerbations Mult Scler 6 2000 267 273
30. J.M. Burton, P.W. O'Connor, M. Hohol, and J. Beyene Oral versus intravenous steroids for treatment of relapses in multiple sclerosis Cochrane Database Syst Rev 12 2012 CD006921
31. B.G. Arnason, R. Berkovich, A. Catania, R.P. Lisak, and M. Zaidi Mechanisms of action of adrenocorticotropic hormone and other melanocortins relevant to the clinical management of patients with multiple sclerosis Mult Scler J 19 2013 130 136
32. C. Pozzilli, F. Marinelli, S. Romano, and F. Bagnato Corticosteroids treatment J Neurol Sci 223 2004 47 51 (Pubitemid 38903261)
33. P. Repovic, and F.D. Lublin Treatment of multiple sclerosis exacerbations Neurol Clin 29 2011 389 400
34. A. Vasheghani-Farahani, M.A. Sahraian, L. Darabi, A. Aghsaie, and A. Minagar Incidence of various cardiac arrhythmias and conduction disturbances due to high dose intravenous methylprednisolone in patients with multiple sclerosis J Neurol Sci 309 2011 75 78
35. R. Zivadinov, R.A. Rudick, M.R. De, D. Nasuelli, M. Ukmar, and R.S. Pozzi-Mucelli et al. Effects of IV methylprednisolone on brain atrophy in relapsing-remitting MS Neurology 57 2001 1239 1247 (Pubitemid 32947383)
36. R.J. Fox, E. Fisher, J. Tkach, J.C. Lee, J.A. Cohen, and R.A. Rudick Brain atrophy and magnetization transfer ratio following methylprednisolone in multiple sclerosis: short-term changes and long-term implications Mult Scler 11 2005 140 145 (Pubitemid 40403250)
37. B.F. Then, T. Kumpfel, E. Schumann, U. Held, M. Schwan, and M. Blazevic et al. Monthly intravenous methylprednisolone in relapsing-remitting multiple sclerosis - reduction of enhancing lesions, T2 lesion volume and plasma prolactin concentrations BMC Neurol 6 2006 19
38. P.S. Sorensen, S.I. Mellgren, A. Svenningsson, I. Elovaara, J.L. Frederiksen, and A.G. Beiske et al. NORdic trial of oral methylprednisolone as add-on therapy to interferon beta-1a for treatment of relapsing-remitting multiple sclerosis (NORMIMS study): a randomised, placebo-controlled trial Lancet Neurol 8 2009 519 529
39. M. Ravnborg, P.S. Sorensen, M. Andersson, E.G. Celius, P.J. Jongen, and I. Elovaara et al. Methylprednisolone in combination with interferon beta-1a for relapsing-remitting multiple sclerosis (MECOMBIN study): a multicentre, double-blind, randomised, placebo-controlled, parallel-group trial Lancet Neurol 9 2010 672 680
40. M.C. Ysrraelit, M.I. Gaitan, A.S. Lopez, and J. Correale Impaired hypothalamic-pituitary-adrenal axis activity in patients with multiple sclerosis Neurology 71 2008 1948 1954
41. N.K. Evanson, J.P. Herman, R.R. Sakai, and E.G. Krause Nongenomic actions of adrenal steroids in the central nervous system J Neuroendocrinol 22 2010 846 861
42. E.R. De Kloet, E. Vreugdenhil, M.S. Oitzl, and M. Joels Brain corticosteroid receptor balance in health and disease Endocr Rev 19 1998 269 301 (Pubitemid 29117816)
43. J.M. Reul, and E.R. De Kloet Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation Endocrinology 117 1985 2505 2511 (Pubitemid 16194083)
44. N.C. Lan, B. Graham, F.C. Bartter, and J.D. Baxter Binding of steroids to mineralocorticoid receptors: implications for in vivo occupancy by glucocorticoids J Clin Endocrinol Metab 54 1982 332 342 (Pubitemid 12006606)
45. P.J. Barnes Anti-inflammatory actions of glucocorticoids: molecular mechanisms Clin Sci 94 1998 557 572 (Pubitemid 28269054)
46. R.H. Oakley, and J.A. Cidlowski Cellular processing of the glucocorticoid receptor gene and protein: new mechanisms for generating tissue-specific actions of glucocorticoids J Biol Chem 286 2011 3177 3184
47. L. Pujols, J. Mullol, J. Roca-Ferrer, A. Torrego, A. Xaubet, and J.A. Cidlowski et al. Expression of glucocorticoid receptor a- and b-isoforms in human cells and tissues Am J Physiol Cell Physiol 283 2002 C1324 C1331
48. S.M. Hollenberg, C. Weinberger, E.S. Ong, G. Cerelli, A. Oro, and R. Lebo et al. Primary structure and expression of a functional human glucocorticoid receptor cDNA Nature 318 1985 635 641 (Pubitemid 16172412)
49. R.H. Oakley, C.M. Jewell, M.R. Yudt, D.M. Bofetiado, and J.A. Cidlowski The dominant negative activity of the human glucocorticoid receptor b isoform. Specificity and mechanisms of action J Biol Chem 274 1999 27857 27866
50. H. Shahidi, A. Vottero, C.A. Stratakis, S.E. Taymans, M. Karl, and C.A. Longui et al. Imbalanced expression of the glucocorticoid receptor isoforms in cultured lymphocytes from a patient with systemic glucocorticoid resistance and chronic lymphocytic leukemia Biochem Biophys Res Commun 254 1999 559 565 (Pubitemid 29290505)
51. T. Kino, E. Charmandari, and G.P. Chrousos Glucocorticoid receptor: implications for rheumatic diseases Clin Exp Rheumatol 29 5 Suppl. 68 2011 S32 S41
52. T. Matsubara, H. Funato, A. Kobayashi, M. Nobumoto, and Y. Watanabe Reduced glucocorticoid receptor alpha expression in mood disorder patients and first-degree relatives Biol Psychiatry 59 2006 689 695
53. M. Matysiak, B. Makosa, A. Walczak, and K. Selmaj Patients with multiple sclerosis resisted to glucocorticoid therapy: abnormal expression of heat-shock protein 90 in glucocorticoid receptor complex Mult Scler 14 2008 919 926
54. L.I. McKay, and J.A. Cidlowski Cross-talk between nuclear factor-kB and the steroid hormone receptors: mechanisms of mutual antagonism Mol Endocrinol 12 1998 45 56 (Pubitemid 28124778)
55. F. Hu, T.W. Pace, and A.H. Miller Interferon-alpha inhibits glucocorticoid receptor-mediated gene transcription via STAT5 activation in mouse HT22 cells Brain Behav Immun 23 2009 455 463
56. X. Wang, H. Wu, and A.H. Miller Interleukin 1a (IL-1a) induced activation of p38 mitogen-activated protein kinase inhibits glucocorticoid receptor function Mol Psychiatry 9 2004 65 75 (Pubitemid 38175083)
57. T.W. Pace, and A.H. Miller Cytokines and glucocorticoid receptor signaling. Relevance to major depression Ann N Y Acad Sci 1179 2009 86 105
58. +)-ATPase Biochem Biophys Res Commun 66 1975 115 122
59. I.H. Song, and F. Buttgereit Non-genomic glucocorticoid effects to provide the basis for new drug developments Mol Cell Endocrinol 246 2006 142 146 (Pubitemid 43238408)
60. F. Buttgereit, M. Wehling, and G.R. Burmester A new hypothesis of modular glucocorticoid actions: steroid treatment of rheumatic diseases revisited Arthritis Rheum 41 1998 761 767
61. B.L. Mason, C.M. Pariante, S. Jamel, and S.A. Thomas Central nervous system (CNS) delivery of glucocorticoids is fine-tuned by saturable transporters at the blood-CNS barriers and nonbarrier regions Endocrinology 151 2010 5294 5305
62. R.M. Sapolsky, L.M. Romero, and A.U. Munck How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions Endocr Rev 21 2000 55 89 (Pubitemid 32266068)
63. J.D. Johnson, K.A. O'Connor, L.R. Watkins, and S.F. Maier The role of IL-1b in stress-induced sensitization of proinflammatory cytokine and corticosterone responses Neuroscience 127 2004 569 577 (Pubitemid 38993161)
64. F.S. Dhabhar Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology Neuroimmunomodulation 16 2009 300 317
65. S.F. Sorrells, J.R. Caso, C.D. Munhoz, and R.M. Sapolsky The stressed CNS: when glucocorticoids aggravate inflammation Neuron 64 2009 33 39
66. T. Uz, Y. Dwivedi, P.D. Savani, F. Impagnatiello, G. Pandey, and H. Manev Glucocorticoids stimulate inflammatory 5-lipoxygenase gene expression and protein translocation in the brain J Neurochem 73 1999 693 699 (Pubitemid 29339843)
67. L.F. Garcia-Fernandez, M.A. Iniguez, N. Eguchi, M. Fresno, Y. Urade, and A. Munoz Dexamethasone induces lipocalin-type prostaglandin D synthase gene expression in mouse neuronal cells J Neurochem 75 2000 460 470 (Pubitemid 30485426)
68. K. Dinkel, A. MacPherson, and R.M. Sapolsky Novel glucocorticoid effects on acute inflammation in the CNS J Neurochem 84 2003 705 716 (Pubitemid 36176929)
69. A. MacPherson, K. Dinkel, and R. Sapolsky Glucocorticoids worsen excitotoxin-induced expression of pro-inflammatory cytokines in hippocampal cultures Exp Neurol 194 2005 376 383 (Pubitemid 40966997)
70. R.M. de Pablos, R.F. Villaran, S. Arguelles, A.J. Herrera, J.L. Venero, and A. Ayala et al. Stress increases vulnerability to inflammation in the rat prefrontal cortex J Neurosci 26 2006 5709 5719 (Pubitemid 44315262)
71. C.D. Munhoz, L.B. Lepsch, E.M. Kawamoto, M.B. Malta, L.S. Lima, and M.C. Avellar et al. Chronic unpredictable stress exacerbates lipopolysaccharide- induced activation of nuclear factor-kB in the frontal cortex and hippocampus via glucocorticoid secretion J Neurosci 26 2006 3813 3820
72. C.D. Munhoz, S.F. Sorrells, J.R. Caso, C. Scavone, and R.M. Sapolsky Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner J Neurosci 30 2010 13690 13698
73. I. Harpaz, S. Abutbul, A. Nemirovsky, R. Gal, H. Cohen, and A. Monsonego Chronic exposure to stress predisposes to higher autoimmune susceptibility in C57BL/6 mice: glucocorticoids as a double-edged sword Eur J Immunol 43 2013 758 769
74. S. Wust, B.J. van den, H.M. Reichardt, and F. Luhder Preventive treatment with methylprednisolone paradoxically exacerbates experimental autoimmune encephalomyelitis Int J Endocrinol 2012 417017
75. M.G. Frank, M.V. Baratta, D.B. Sprunger, L.R. Watkins, and S.F. Maier Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses Brain Behav Immun 21 2007 47 59 (Pubitemid 44854445)
76. M.G. Frank, Z.D. Miguel, L.R. Watkins, and S.F. Maier Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide Brain Behav Immun 24 2010 19 30
77. J.D. Johnson, K.A. O'Connor, T. Deak, M. Stark, L.R. Watkins, and S.F. Maier Prior stressor exposure sensitizes LPS-induced cytokine production Brain Behav Immun 16 2002 461 476 (Pubitemid 35346208)
78. A.E. Barber, S.M. Coyle, M.A. Marano, E. Fischer, S.E. Calvano, and Y. Fong et al. Glucocorticoid therapy alters hormonal and cytokine responses to endotoxin in man J Immunol 150 1993 1999 2006 (Pubitemid 23129678)
79. G.P. Smyth, P.P. Stapleton, T.A. Freeman, E.M. Concannon, J.R. Mestre, and M. Duff et al. Glucocorticoid pretreatment induces cytokine overexpression and nuclear factor-kB activation in macrophages J Surg Res 116 2004 253 261 (Pubitemid 38175315)
80. J.J. Chiang, N.I. Eisenberger, T.E. Seeman, and S.E. Taylor Negative and competitive social interactions are related to heightened proinflammatory cytokine activity Proc Natl Acad Sci U S A 109 2012 1878 1882
81. V.H. Perry Stress primes microglia to the presence of systemic inflammation: implications for environmental influences on the brain Brain Behav Immun 21 2007 45 46 (Pubitemid 44854448)
82. E. Goujon, P. Parnet, S. Laye, C. Combe, K.W. Kelley, and R. Dantzer Stress downregulates lipopolysaccharide-induced expression of proinflammatory cytokines in the spleen, pituitary, and brain of mice Brain Behav Immun 9 1995 292 303 (Pubitemid 26039769)
83. E. Goujon, P. Parnet, S. Laye, C. Combe, and R. Dantzer Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide Brain Res Mol Brain Res 36 1996 53 62 (Pubitemid 26058875)
84. P.H. Black Stress and the inflammatory response: a review of neurogenic inflammation Brain Behav Immun 16 2002 622 653 (Pubitemid 36027055)
85. M.P. Yeager, P.M. Guyre, and A.U. Munck Glucocorticoid regulation of the inflammatory response to injury Acta Anaesthesiol Scand 48 2004 799 813 (Pubitemid 38993094)
86. A. Munck, P.M. Guyre, and N.J. Holbrook Physiological functions of glucocorticoids in stress and their relation to pharmacological actions Endocr Rev 5 1984 25 44
87. C. Hirst, G. Ingram, O. Pearson, T. Pickersgill, N. Scolding, and N. Robertson Contribution of relapses to disability in multiple sclerosis J Neurol 255 2008 280 287
88. L.M. van Winsen, J.J. Kragt, E.L. Hoogervorst, C.H. Polman, and B.M. Uitdehaag Outcome measurement in multiple sclerosis: detection of clinically relevant improvement Mult Scler 16 2010 604 610
89. A.H. Marques, M.N. Silverman, and E.M. Sternberg Glucocorticoid dysregulations and their clinical correlates. From receptors to therapeutics Ann N Y Acad Sci 1179 2009 1 18
90. R.P. Rao, S. Anilkumar, B.S. McEwen, and S. Chattarji Glucocorticoids protect against the delayed behavioral and cellular effects of acute stress on the amygdala Biol Psychiatry 72 2012 466 475
91. A. Izquierdo, C.L. Wellman, and A. Holmes Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice J Neurosci 26 2006 5733 5738 (Pubitemid 44315265)
92. A. Vyas, R. Mitra, B.S. Shankaranarayana Rao, and S. Chattarji Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons J Neurosci 22 2002 6810 6818 (Pubitemid 35386438)
93. B. Roozendaal 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation Opt Lett 25 2000 213 238 (Pubitemid 30089730)
94. S.J. Lupien, and M. Lepage Stress, memory, and the hippocampus: can't live with it, can't live without it Behav Brain Sci 127 2001 137 158 (Pubitemid 33062407)
95. R.M. Sapolsky, and W.A. Pulsinelli Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications Science 229 1985 1397 1400 (Pubitemid 16222382)
96. D. Kaufer, W.O. Ogle, Z.S. Pincus, K.L. Clark, A.C. Nicholas, and K.M. Dinkel et al. Restructuring the neuronal stress response with anti-glucocorticoid gene delivery Nat Neurosci 7 2004 947 953 (Pubitemid 39129503)
97. S.F. Sorrells, J.R. Caso, C.D. Munhoz, C.K. Hu, K.V. Tran, and Z.D. Miguel et al. Glucocorticoid signaling in myeloid cells worsens acute CNS injury and inflammation J Neurosci 33 2013 7877 7889
98. R. Diem, M. Hobom, K. Maier, R. Weissert, M.K. Storch, and R. Meyer et al. Methylprednisolone increases neuronal apoptosis during autoimmune CNS inflammation by inhibition of an endogenous neuroprotective pathway J Neurosci 23 2003 6993 7000 (Pubitemid 36975865)
99. T. Clarner, A. Parabucki, C. Beyer, and M. Kipp Corticosteroids impair remyelination in the corpus callosum of cuprizone-treated mice J Neuroendocrinol 23 2011 601 611
100. L.C. Triarhou, and R.M. Herndon The effect of dexamethasone on L-s-lysophosphatidyl choline (lysolecithin)-induced demyelination of the rat spinal cord Arch Neurol 43 1986 121 125 (Pubitemid 16124235)
101. D.M. Chari, C. Zhao, M.R. Kotter, W.F. Blakemore, and R.J. Franklin Corticosteroids delay remyelination of experimental demyelination in the rodent central nervous system J Neurosci Res 83 2006 594 605 (Pubitemid 43384853)
102. K.D. Pavelko, B.G. van Engelen, and M. Rodriguez Acceleration in the rate of CNS remyelination in lysolecithin-induced demyelination J Neurosci 18 1998 2498 2505
103. P.A. Zunszain, C. Anacker, A. Cattaneo, L.A. Carvalho, and C.M. Pariante Glucocorticoids, cytokines and brain abnormalities in depression Prog Neuropsychopharmacol Biol Psychiatry 35 2011 722 729
104. A. Feinstein Multiple sclerosis and depression Mult Scler 17 2011 1276 1281
105. R.J. Siegert, and D.A. Abernethy Depression in multiple sclerosis: a review J Neurol Neurosurg Psychiatry 76 2005 469 475 (Pubitemid 40486568)
106. L. Chwastiak, D.M. Ehde, L.E. Gibbons, M. Sullivan, J.D. Bowen, and G.H. Kraft Depressive symptoms and severity of illness in multiple sclerosis: epidemiologic study of a large community sample Am J Psychiatry 159 2002 1862 1868 (Pubitemid 35283251)
107. The IFNB Multiple Sclerosis Study Group Interferon b-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial Neurology 43 1993 655 661
108. C. Pozzilli, B. Schweikert, U. Ecari, W. Oentrich, and J.P. Bugge Quality of life and depression in multiple sclerosis patients: longitudinal results of the BetaPlus study J Neurol 259 2012 2319 2328
109. A. Feinstein, P. O'Connor, and K. Feinstein Multiple sclerosis, interferon beta-1b and depression: a prospective investigation J Neurol 249 2002 815 820 (Pubitemid 34754215)
110. D.C. Mohr, W. Likosky, P. Dwyer, W.J. Van Der, A.C. Boudewyn, and D.E. Goodkin Course of depression during the initiation of interferon beta-1a treatment for multiple sclerosis Arch Neurol 56 1999 1263 1265 (Pubitemid 29473219)
111. J. Pujol, J. Bello, J. Deus, J.L. Marti-Vilalta, and A. Capdevila Lesions in the left arcuate fasciculus region and depressive symptoms in multiple sclerosis Neurology 49 1997 1105 1110 (Pubitemid 27456095)
112. R. Bakshi, D. Czarnecki, Z.A. Shaikh, R.L. Priore, V. Janardhan, and Z. Kaliszky et al. Brain MRI lesions and atrophy are related to depression in multiple sclerosis Neuroreport 11 2000 1153 1158 (Pubitemid 30262949)
113. F.J. Eccles, and J. Simpson A review of the demographic, clinical and psychosocial correlates of perceived control in three chronic motor illnesses Disabil Rehabil 33 2011 1065 1088
114. B.E. Leonard Psychopathology of depression Drugs Today 43 2007 705 716 (Pubitemid 350220794)
115. H.S. Mayberg Modulating limbic-cortical circuits in depression: targets of antidepressant treatments Semin Clin Neuropsychiatry 7 2002 255 268
116. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat Rev Neurosci 9 2008 46 56 (Pubitemid 350295688)
117. A.H. Miller, V. Maletic, and C.L. Raison Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression Biol Psychiatry 65 2009 732 741
118. C.M. Pariante Glucocorticoid receptor function in vitro in patients with major depression Stress 7 2004 209 219 (Pubitemid 40591421)
119. P. Fitzgerald, S.M. O'Brien, P. Scully, K. Rijkers, L.V. Scott, and T.G. Dinan Cutaneous glucocorticoid receptor sensitivity and pro-inflammatory cytokine levels in antidepressant-resistant depression Psychol Med 36 2006 37 43 (Pubitemid 41825344)
120. K. Fassbender, R. Schmidt, R. Mossner, U. Kischka, J. Kuhnen, and A. Schwartz et al. Mood disorders and dysfunction of the hypothalamic-pituitary- adrenal axis in multiple sclerosis: association with cerebral inflammation Arch Neurol 55 1998 66 72 (Pubitemid 28139107)
121. S.M. Gold, S. Kruger, K.J. Ziegler, T. Krieger, K.H. Schulz, and C. Otte et al. Endocrine and immune substrates of depressive symptoms and fatigue in multiple sclerosis patients with comorbid major depression J Neurol Neurosurg Psychiatry 82 2011 814 818