Progesterone and nestorone facilitate axon remyelination: A role for progesterone receptors

Endocrinology

Volumn 152, Issue 10, 2011, Pages 3820-3831

  Hussain, Rashad ^a   El Etr, Martine ^a   Gaci, Ouardia ^a   Rakotomamonjy, Jennifer ^a   Macklin, Wendy B ^b   Kumar, Narender ^c   Sitruk Ware, Regine ^c   Schumacher, Michael ^a   Ghoumari, Abdel M ^a  

^a INSERM   (France)

^b UNIVERSITY OF COLORADO   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELCOMETRINE; ENHANCED GREEN FLUORESCENT PROTEIN; LYSOPHOSPHATIDYLCHOLINE; MEDROXYPROGESTERONE ACETATE; MYELIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEIN NG2; PROTEOGLYCAN; PROTEOLIPID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CELL LINEAGE; CELL MIGRATION; CEREBELLUM; COCULTURE; CONTROLLED STUDY; DEMYELINATION; DRUG MECHANISM; HAPLOINSUFFICIENCY; HETEROZYGOTE; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE REGENERATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; REMYELINIZATION; TISSUE CULTURE; WILD TYPE;

ANIMALS; AXONS; CELL MOVEMENT; MALE; MEDROXYPROGESTERONE ACETATE; MYELIN SHEATH; NORPROGESTERONES; OLIGODENDROGLIA; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PROGESTERONE;

EID: 80053156795     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1219     Document Type: Article

References (55)

1. Schumacher M, Guennoun R, Ghoumari A, Massaad C, Robert F, El-Etr M, Akwa Y, Rajkowski K, Baulieu EE 2007 Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr Rev 28:387-439 (Pubitemid 46984826)
2. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, Morgan TE, Pike CJ, Mack WJ, Stanczyk FZ, Nilsen J 2008 Progesterone receptors: form and function in brain. Front Neuroendocrinol 29:313-339
3. Stein DG 2008 Progesterone exerts neuroprotective effects after brain injury. Brain Res Rev 57:386-397 (Pubitemid 351381771)
4. Stein DG, Wright DW 2010 Progesterone in the clinical treatment of acute traumatic brain injury. Expert Opin Investig Drugs 19:847-857
5. Koenig HL, Schumacher M, Ferzaz B, Thi AN, Ressouches A, Guennoun R, Jung-Testas I, Robel P, Akwa Y, Baulieu EE 1995 Progesterone synthesis and myelin formation by Schwann cells. Science 268:1500-1503
6. Ghoumari AM, Ibanez C, El-Etr M, Leclerc P, Eychenne B, O'Malley BW, Baulieu EE, Schumacher M 2003 Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. J Neurochem 86: 848-859 (Pubitemid 36988797)
7. Ghoumari AM, Baulieu EE, Schumacher M 2005 Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures. Neuroscience 135:47-58 (Pubitemid 41219737)
8. Jung-Testas I, Hu ZY, Baulieu EE, Robel P 1989 Neurosteroids: biosynthesis of pregnenolone and progesterone in primary cultures of rat glial cells. Endocrinology 125:2083-2091 (Pubitemid 19258646)
9. Marin-Husstege M, Muggironi M, Raban D, Skoff RP, Casaccia- Bonnefil P 2004 Oligodendrocyte progenitor proliferation and maturation is differentially regulated by male and female sex steroid hormones. Dev Neurosci 26:245-254
10. Miller RH, Mi S 2007 Dissecting demyelination. Nat Neurosci 10: 1351-1354 (Pubitemid 350014684)
11. Franklin RJ, Ffrench-Constant C 2008 Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9:839-855
12. Baumann N, Pham-Dinh D 2001 Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81: 871-927 (Pubitemid 32267079)
13. Miller RH 2002 Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67:451-467 (Pubitemid 35232446)
14. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, Brosnan CF 2002 Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 8:1115-1121 (Pubitemid 35175966)
15. Arnett HA, Fancy SP, Alberta JA, Zhao C, Plant SR, Kaing S, Raine CS, Rowitch DH, Franklin RJ, Stiles CD 2004 bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 306:2111-2115 (Pubitemid 40007666)
16. Stidworthy MF, Genoud S, Li WW, Leone DP, Mantei N, Suter U, Franklin RJ 2004 Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain 127:1928-1941 (Pubitemid 39150252)
17. Ibanez C, Shields SA, El-Etr M, Baulieu EE, Schumacher M, Franklin RJ 2004 Systemic progesterone administration results in a partial reversal of the age-associated decline in CNS remyelination following toxin-induced demyelination in male rats. Neuropathol Appl Neurobiol 30:80-89 (Pubitemid 38178005)
18. Labombarda F, González SL, Lima A, Roig P, Guennoun R, Schumacher M, De Nicola AF 2009 Effects of progesterone on oligodendrocyte progenitors, oligodendrocyte transcription factors, and myelin proteins following spinal cord injury. Glia 57:884-897
19. Belelli D, Lambert JJ 2005 Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6:565-575 (Pubitemid 40942823)
20. Thomas P, Pang Y, Dong J, Groenen P, Kelder J, De Vlieg J, Zhu Y, Tubbs C 2007 Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor α subtypes and their evolutionary origins. Endocrinology 148:705-718 (Pubitemid 46143172)
21. Kumar N, Koide SS, Tsong Y, Sundaram K 2000 Nestorone: a progestin with a unique pharmacological profile. Steroids 65:629-636
22. Sitruk-Ware R 2008 Pharmacological profile of progestins. Maturitas 61:151-157
23. Liu L, Zhao L, She H, Chen S, Wang JM, Wong C, McClure K, Sitruk-Ware R, Brinton RD 2010 Clinically relevant progestins regulate neurogenic and neuroprotective responses in vitro and in vivo. Endocrinology 151:5782-5794
24. Birgbauer E, Rao TS, Webb M 2004 Lysolecithin induces demyelination in vitro in a cerebellar slice culture system. J Neurosci Res 78:157-166 (Pubitemid 39313787)
25. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, Zhang Y, Shields CB, Zhang Y, Miklasz S, Shea D, Mason J, Franklin RJ, Ji B, Shao Z, Chédotal A, Bernard F, Roulois A, Xu J, Jung V, Pepinsky B 2009 Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 65: 304-315
26. Miron VE, Ludwin SK, Darlington PJ, Jarjour AA, Soliven B, Kennedy TE, Antel JP 2010 Fingolimod (FTY720) enhances remyelination following demyelination of organotypic cerebellar slices. Am J Pathol 176:2682-2694
27. Ismail PM, Li J, DeMayo FJ, O'Malley BW, Lydon JP 2002 A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol Endocrinol 16:2475-2489 (Pubitemid 35266067)
28. Mallon BS, Shick HE, Kidd GJ, Macklin WB 2002 Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22: 876-885 (Pubitemid 34141768)
29. Ligon KL, Kesari S, Kitada M, Sun T, Arnett HA, Alberta JA, Anderson DJ, Stiles CD, Rowitch DH 2006 Development of NG2 neural progenitor cells requires Olig gene function. Proc Natl Acad Sci USA 103:7853-7858
30. Fancy SP, Zhao C, Franklin RJ 2004 Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 27:247-254 (Pubitemid 39433839)
31. Mason JL, Toews A, Hostettler JD, Morell P, Suzuki K, Goldman JE, Matsushima GK 2004 Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 164:1673-1682 (Pubitemid 38529770)
32. Acs P, Kipp M, Norkute A, Johann S, Clarner T, Braun A, Berente Z, Komoly S, Beyer C 2009 17β-estradiol and progesterone prevent cuprizone provoked demyelination of corpus callosum in male mice. Glia 57:807-814
33. Garay L, Deniselle MC, Lima A, Roig P, De Nicola AF 2007 Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis. J Steroid Biochem Mol Biol 107:228-237 (Pubitemid 47381578)
34. Garay L, Deniselle MC, Meyer M, Costa JJ, Lima A, Roig P, De Nicola AF 2009 Protective effects of progesterone administration on axonal pathology in mice with experimental autoimmune encephalomyelitis. Brain Res 1283:177-185
35. Mani SK, Blaustein JD, O'Malley BW 1997 Progesterone receptor function from a behavioral perspective. Horm Behav 31:244-255 (Pubitemid 27305722)
36. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
37. Sakamoto H, Ukena K, Tsutsui K 2001 Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J Neurosci 21:6221-6232 (Pubitemid 32737754)
38. Simons M, Trajkovic K 2006 Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J Cell Sci 119:4381-4389 (Pubitemid 44830637)
39. Jung-Testas I, Renoir JM, Gasc JM, Baulieu EE 1991 Estrogen-inducible progesterone receptor in primary cultures of rat glial cells. Exp Cell Res 193:12-19 (Pubitemid 121004329)
40. Labombarda F, Guennoun R, Gonzalez S, Roig P, Lima A, Schumacher M, De Nicola AF 2000 Immunocytochemical evidence for a progesterone receptor in neurons and glial cells of the rat spinal cord. Neurosci Lett 288:29-32 (Pubitemid 30408431)
41. Lacroix-Fralish ML, Tawfik VL, Nutile-McMenemy N, Harris BT, Deleo JA 2006 Differential regulation of neuregulin 1 expression by progesterone in astrocytes and neurons. Neuron Glia Biol 2:227-234 (Pubitemid 47074742)
42. Chesik D, De Keyser J 2010 Progesterone and dexamethasone differentially regulate the IGF-system in glial cells. Neurosci Lett 468: 178-182
43. Chan JR, Phillips 2nd LJ, Glaser M 1998 Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation. Proc Natl Acad Sci USA 95:10459-10464 (Pubitemid 28413089)
44. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K 2008 Steroid hormone receptor expression and function in microglia. Glia 56:659-674
45. Hapgood JP, Koubovec D, Louw A, Africander D 2004 Not all progestins are the same: implications for usage. Trends Pharmacol Sci 25:554-557 (Pubitemid 39371144)
46. Vukusic S, Ionescu I, El-Etr M, Schumacher M, Baulieu EE, Cornu C, Confavreux C 2009 The prevention of post-partum relapses with progestin and estradiol in multiple sclerosis (POPART'MUS) trial: rationale, objectives and state of advancement. J Neurol Sci 286: 114-118
47. Taylor HS, Manson JE 2011 Update in hormone therapy use in menopause. J Clin Endocrinol Metab 96:255-264
48. Nilsen J, Brinton RD 2002 Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology 143:205-212 (Pubitemid 34056421)
49. Nilsen J, Morales A, Brinton RD 2006 Medroxyprogesterone acetate exacerbates glutamate excitotoxicity. Gynecol Endocrinol 22: 355-361 (Pubitemid 44180261)
50. Lawson A, Ahima RS, Krozowski Z, Harlan RE 1992 Postnatal development of corticosteroid receptor immunoreactivity in the rat cerebellum and brain stem. Neuroendocrinology 55:695-707
51. Chari DM, Zhao C, Kotter MR, Blakemore WF, Franklin RJ 2006 Corticosteroids delay remyelination of experimental demyelination in the rodent central nervous system. J Neurosci Res 83:594 -605
52. El-Etr M, Ghoumari A, Sitruk-Ware R, Schumacher M 2011 Hormonal influences in multiple sclerosis: new therapeutic benefits for steroids. Maturitas 68:47-51
53. Kuhlmann T, Miron V, Cui Q, Cuo Q, Wegner C, Antel J, Brück W 2008 Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131:1749-1758 (Pubitemid 351957453)
54. Sitruk-Ware R, Small M, Kumar N, Tsong YY, Sundaram K, Jackanicz T 2003 Nestorone: clinical applications for contraception and HRT. Steroids 68:907-913 (Pubitemid 37532414)
55. Mahabadi V, Amory JK, Swerdloff RS, Bremner WJ, Page ST, Sitruk- Ware R, Christensen PD, Kumar N, Tsong YY, Blithe D, Wang C 2009 Combined transdermal testosterone gel and the progestin nestorone suppresses serum gonadotropins in men. J Clin Endocrinol Metab 94:2313-2320