Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis

Journal of Steroid Biochemistry and Molecular Biology

Volumn 107, Issue 3-5, 2007, Pages 228-237

  Garay, Laura ^a,b   Deniselle, Maria Claudia Gonzalez ^a,b   Lima, Analia ^a   Roig, Paulina ^a   De Nicola, Alejandro F ^a,b,c  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Argentina   (Argentina)

Author keywords

EAE; Multiple sclerosis; Myelination; Neuroprotection; Progesterone

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); FREUND ADJUVANT; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; MYELIN PROTEIN; PROGESTERONE; PROTEOLIPID PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; FEMALE; IMMUNIZATION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOTONEURON; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PROTEIN EXPRESSION; SPINAL CORD;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA PRIMERS; FEMALE; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; PROGESTERONE; SPINAL CORD;

MUS;

EID: 34548537675     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2007.03.040     Document Type: Article

References (65)

1. Jones K.J., Drengler S.M., and Oblinger M.M. Gonadal steroid regulation of growth-associated protein GAP-43 mRNA expression in axotomized hamster facial motor neurons. Neurochem. Res. 22 (1997) 1367-1374
2. Roof R., and Hall E. Gender differences in acute CNS trauma and stroke: Neuroprotective effects and progesterone. J. Neurotrauma 17 (2000) 367-388
3. Stein D.G., and Fulop Z.L. Progesterone and recovery after traumatic brain injury: an overview. Neuroscientist 4 (1998) 435-442
4. Labombarda F., Gonzalez S., Gonzalez Deniselle M.C., Guennoun R., Schumacher M., and De Nicola A.F. Cellular basis for progesterone neuroprotection in the injured spinal cord. J. Neurotrauma 19 (2002) 343-355
5. Ogata T., Nakamura Y., Tsuji K., Shibata T., and Kataoka K. Steroid hormones protect spinal cord neurons from glutamate toxicity. Neuroscience 55 (1993) 445-449
6. Thomas A., Nockels R., Pan H., Shaffrey C., and Chop M. Progesterone is neuroprotective after acute experimental spinal cord trauma in rats. Spine 24 (1999) 2134-2138
7. Gonzalez Deniselle M.C., Lopez Costa J.J., Gonzalez S.L., Labombarda F., Garay L., Guennoun R., Schumacher M., and De Nicola A.F. Basis of progesterone protection in spinal cord neurodegeneration. J. Steroid. Biochem. Mol. Biol. 83 (2002) 199-209
8. Gonzalez Deniselle M.C., Garay L., Gonzalez S.L., Guennoun R., Schumacher M., and De Nicola A.F. Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease. Exp. Neurol. 195 (2005) 518-523
9. Desarnaud F., Do Thi A.N., Brown A.M., Lemke G., Suter U., Baulieu E.E., and Schumacher M. Progesterone stimulates the activity of the promoters of peripheral myelin protein-22 and protein zero genes in Schwann cells. J. Neurochem. 71 (1998) 1765-1768
10. Melcangi R.V., Magnaghi V., and Martini L. Aging in peripheral nerves: regulation of myelin protein genes by steroid hormones. Prog. Neurobiol. 60 (2000) 291-308
11. Schumacher M., Guennoun R., Robert F., Carelli C., Gago N., Ghoumari A., Gonzalez Deniselle M.C., Gonzalez S.L., Ibanez C., Labombarda F., Coirini H., Baulieu E.E., and De Nicola A.F. Local synthesis and dual actions of progesterone in the nervous system: neuroprotection and myelination. Growth Horm. IGF Res. 14 (2004) S18-S33
12. Ibanez C., Shields S.A., El-Etr M., Leonelli E., Magnaghi V., Li W., Sim F.J., Baulieu E.E., Melcangi R.C., Schumacher M., and Franklin R.J. Steroids and the reversal of age-associated changes in myelination and remyelination. Prog. Neurobiol. 71 (2003) 49-56
13. Labombarda F., Gonzalez S., Gonzalez Deniselle M.C., Garay L., Guennoun R., Schumacher M., and De Nicola A.F. Progesterone increases the expression of myelin basic protein and the number of cells showing NG2 immunostaining in the lesioned spinal cord. J. Neurotrauma 23 (2006) 181-192
14. Gago N., Akwa Y., Sananes N., Guennoun R., Baulieu E.E., El-Etr M., and Schumacher M. Progesterone and the oligodendroglial lineage: stage-dependent biosynthesis and metabolism. Glia 36 (2001) 295-308
15. Labombarda F., González S.L., Gonzalez Deniselle M.C., Vinson V.P., Schumacher M., De Nicola A.F., and Guennoun R. Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-DX expression in the rat spinal cord. J. Neurochem. 87 (2003) 902-913
16. Druckmann R., and Druckmann M.A. Progesterone and the immunology of pregnancy. J. Steroid. Biochem. Mol. Biol. 97 (2005) 389-396
17. El-Etr M., Vukusic S., Gignoux L., Durand-Dubief F., Achiti I., Baulieu E.E., and Confavreux C. Steroid hormones in multiple sclerosis. J. Neurol. Sci. 233 (2005) 49-54
18. Piccinni M.P., Giudizi M.G., Biagiotti R., Beloni L., Giannarini L., Sampognaro S., Parronchi P., Manetti R., Annunziato F., and Livi C. Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J. Immunol. 155 (1995) 128-133
19. Szekeres-Bartho J., and Wegmann T.G. A progesterone-dependent immunomodulatory protein alters the Th1/Th2 balance. J. Reprod. Immunol. 31 (1986) 81-95
20. Gibson C.L., Constantin D., Prior M.J., Bath P.M., and Murphy S.P. Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp. Neurol. 193 (2005) 522-530
21. Pettus E.H., Wright D.W., Stein D.G., and Hoffman S.W. Progesterone treatment inhibits the inflammatory agents that accompany traumatic brain injury. Brain. Res. 1049 (2005) 112-119
22. Kornek B., Storch M.K., Weissert R., Wallstroem E., Stefferl A., Olsson T., Linington C., Schmidbauer M., and Lassmann H. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am. J. Pathol. 157 (2000) 267-276
23. Svensson L., Abdul-Majid K.B., Bauer J., Lassmann H., Harris R.A., and Holmdahl R. A comparative analysis of B cell-mediated myelin oligodendrocyte glycoprotein-experimental autoimmune encephalomyelitis pathogenesis in B cell-deficient mice reveals an effect on demyelination. Eur. J. Immunol. 32 (2002) 1939-1946
24. Wujek R., Bjartmar C., Richer E., Ransohoff R.M., Yu M., Tuohy V.K., and Trapp B.D. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J. Neuropathol. Exp. Neurol. 61 (2002) 23-32
25. Onuki M., Ayers M.M., Bernard C.C., and Orian J.M. Axonal degeneration is an early pathological feature in autoimmune-mediated demyelination in mice. Microsc. Res. Tech. 52 (2001) 731-739
26. Ayers M.M., Hazelwood L.J., Catmull D.V., Wang D., McKormack Q., Bernard C.C., and Orian J.M. Early glial responses in murine models of multiple sclerosis. Neurochem. Int. 45 (2004) 409-419
27. Garay L., González Deniselle M.C., Villa A.M., Garcea O., Sica R.E.P., and De Nicola A.F. Immunohistopathological changes in myelin oligodendrocyte glycoprotein 40-54 induced experimental autoimmune encephalomyelitis. Multiple Sclerosis 11 (2005) 43-52
28. Papadopoulos D., Pham-Dinh D., and Reynolds R. Axon loss is responsible for chronic neurological deficit following inflammatory demyelination in the rat. Exp. Neurol. 197 (2006) 373-385
29. Penkowa M., and Hidalgo J. Treatment with metallothionein prevents demyelination and axonal damage and increases oligodendrocyte precursors and tissue repair during experimental autoimmune encephalomyelitis. J. Neurosci. Res. 72 (2003) 574-586
30. + MOG-specific T cells on oligomeric MHC class I molecules. Int. Immunol. 15 (2003) 261-268
31. Gonzalez-Rey E., Fernandez-Martin A., Chorny A., Martin J., Pozo D., Ganea D., and Delgado M. Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am. J. Pathol. 168 (2006) 1179-1188
32. Liu Y., Liu J., Tetzlaff W., Paty C.D., and Cynader M.S. Biliverdin reductase, a major physiologic cytoprotectant, suppresses experimental autoimmune encephalomyelitis. Free Rad. Biol. Med. 40 (2006) 960-967
33. Li X.B., and Schluesener H.J. Therapeutic effects of cisplatin on rat experimental autoimmune encephalomyelitis. Arch. Immunol. Ther. Exp. 54 (2006) 51-53
34. Prud'homme G.J., and Vanier L.E. Cyclosporine, tolerance, and autoimmunity. Clin. Immunol. Immunopathol. 66 (1993) 185-192
35. Schilling S., Goelz S., Linker R., Luehder F., and Gold R. Fumaric acid esters are effective in chronic experimental autoimmune encephalomyelitis and suppress macrophage infiltration. Clin. Exp. Immunol. 145 (2006) 101-107
36. Mason D., MacPhee I., and Antoni F. The role of the neuroendocrine system in determining genetic susceptibility to experimental allergic encephalomyelitis in the rat. Immunology. 70 (1999) 1-5
37. Bebo B.F., Fyfe-Johnson A., Adlard K., Beam A.G., Vandenbark A.A., and Offner H. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J. Immunol. 166 (2001) 2080-2089
38. Elloso M.M., Phiel K., Henderson R.A., Harris H.A., and Adelman S.J. Suppression of experimental autoimmune encephalomyelitis using estrogen receptor-selective ligands. J. Endocrinol. 185 (2005) 243-252
39. Kim S., Liva S.M., Dalal M.A., Verity M.A., and Voskuhl R.R. Estriol ameliorates autoimmune demyelinating disease: implications for multiple sclerosis. Neurology 52 (1999) 1230-1238
40. Morales L.B.J., Loo K.K., Liu H., Peterson C., Tiwari-Woodruff S., and Voskuhl R.R. Treatment with an estrogen receptor α ligand is neuroprotective in experimental autoimmune encephalomyelitis. J. Neurosci. 26 (2006) 6823-6833
41. Offner H., Adlard K., Zamora A., and Vandenbark A.A. Estrogen potentiates treatment with T-cell receptor protein of female mice with experimental encephalomyelitis. J. Clin. Invest. 105 (2000) 1465-1472
42. Hughes M.D. Multiple sclerosis and pregnancy. Neurol. Clin. 22 (2004) 757-769
43. Elliot G.A., Gibbons A.J., and Greig M.E. A comparison of the effects of melengestrol acetate with a combination of hydrocortisone acetate and medrohyprogesterone acetate and with other steroids in the treatment of experimental allergic encephalomyelitis in Wistar rats. Acta Neuropathol. 23 (1973) 95-104
44. Hoffman G.E., Le W.W., Murphy A.Z., and Koski C.L. Divergent effects of ovarian steroids on neuronal survival during experimental allergic encephalitis in Lewis rats. Exp. Neurol. 171 (2001) 272-284
45. Vizioli N.M., Carducci C.N., Pena C., and Guzman N.A. Monitoring the purity of a synthetic peptide by capillary electrophoresis: utilization of an on-line preconcentration method for improved separation and detection sensitivity. J. Capillary. Electrophor. 6 (1999) 109-118
46. Cowden W.B., Cullen F.A., Staykova M.A., and Willemborg D.O. Nitric oxide is a potential down-regulating molecule in autoimmune disease: inhibition of nitric oxide production renders PVG rats highly susceptible to EAE. J. Neuroimmunol. 88 (1998) 1-8
47. Kim J.H., Budde M.D., Liang H.F., Klein R.S., Russell J.H., Cross A.H., and Song S.K. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol. Dis. 21 (2006) 626-632
48. Ferrini M., Lima A., and De Nicola A.F. Estradiol abolishes autologous down regulation of glucocorticoid receptors in brain. Life Sci. 57 (1995) 2403-2412
49. Mathisen P., Kawczak M., Yu M., Johnson J., and Tuohy V. Differential DM20 mRNA expression distinguishes two distinct patterns of spontaneous recovery from murine autoimmune encephalomyelitis. J. Neurosci. Res. 64 (2001) 542-551
50. +-ATPase in some spinal cord neurones after cord transection. Neuroreport. 10 (1996) 1041-1044
51. Sim F.J., Hinks G.L., and Franklin R.J. The re-expression of the homeodomain transcription factor Gtx during remyelination of experimentally induced demyelinating lesions in young and old rat brain. Neuroscience 100 (2000) 131-139
52. +) ATPase alpha 3 and beta 1 subunits in rat brain measured by in situ hybridization. Brain. Res. 657 (1994) 83-91
53. Palazynski K., Liu H., Loo K., and Voskuhl R. Estriol treatment ameliorates disease in males with experimental autoimmune encephalomyelitis: implications for multiple sclerosis. J. Neuroimmunol. 149 (2004) 84-89
54. Giardino L., Giuliani A., Fernandez M., and Calza L. Spinal motoneuron distress during experimental allergic encephalomyelitis. Neuropathol. Appl. Neurobiol. 30 (2004) 522-531
55. Nicot A., Ratnakar P.V., Ron Y., Chen C.C., and Elkabes S. Regulation of gene expression in experimental autoimmune encephalomyelitis indicates early neuronal dysfunction. Brain 126 (2003) 398-412
56. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1983), Academic Press, New York
57. Merrill J.E., and Scolding N.J. Mechanisms of damage to myelin and oligodendrocytes and their relevance to disease. Neuropathol. Appl. Neurobiol. 25 (1999) 435-458
58. Ghoumari A.M., Baulieu E.E., and Schumacher M. Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures. Neuroscience 135 (2005) 47-58
59. Jung-Testas I., Renoir M., Bugnard H., Greene G.L., and Baulieu E.E. Demonstration of steroid hormone receptors and steroid action in primary cultures of rat glial cells. J. Steroid. Biochem. Mol. Biol. 41 (1993) 621-631
60. Lees G.J., and Leong W. Brain lesions induced by specific and non-specific inhibitors of sodium-potassium ATPase. Brain. Res. 649 (1994) 225-233
61. +)-ATPase: function, structure, and conformations. Ann. Neurol. 16l (1984) 121-127
62. + ATPase alpha subunit mutants. J. Neurosci. 23 (2003) 1276-1286
63. Levine J.M., Reynolds R., and Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24 (2001) 39-47
64. Prineas J.W., Barnard R.O., Kwon E.E., Sharer L.R., and Cho E.S. Multiple sclerosis: remyelination of nascent lesions. Ann. Neurol. 33 (1993) 137-151
65. Raine C.S., and Wu E. Multiple sclerosis: remyelination in acute lesions. J. Neuropathol. Exp. Neurol. 52 (1993) 199-204