Progesterone effects on the oligodendrocyte linage: all roads lead to the progesterone receptor
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摘要
A new role has emerged for progesterone after discovering its potent actions away from reproduction in both the central and the peripheral nervous system. The aim of the present report is to discuss progesterone's mechanisms of action involved in myelination, remyelination and neuroinflammation. The pivotal role of the classic progesterone receptor is described and evidence is compiled about progesterone's direct effects on oligodendrocyte linage and its indirect effects on oligodendrocyte precursor cell differentiation by decreasing the neuroinflammatory environment.
A new role has emerged for progesterone after discovering its potent actions away from reproduction in both the central and the peripheral nervous system. The aim of the present report is to discuss progesterone's mechanisms of action involved in myelination, remyelination and neuroinflammation. The pivotal role of the classic progesterone receptor is described and evidence is compiled about progesterone's direct effects on oligodendrocyte linage and its indirect effects on oligodendrocyte precursor cell differentiation by decreasing the neuroinflammatory environment.
A new role has emerged for progesterone after discovering its potent actions away from reproduction in both the central and the peripheral nervous system. The aim of the present report is to discuss progesterone's mechanisms of action involved in myelination, remyelination and neuroinflammation. The pivotal role of the classic progesterone receptor is described and evidence is compiled about progesterone's direct effects on oligodendrocyte linage and its indirect effects on oligodendrocyte precursor cell differentiation by decreasing the neuroinflammatory environment.
引文
Aryanpour R,Pasbakhsh P,Zibara K,Namjoo Z,Beigi Boroujeni F,Shahbeigi S,Kashani IR,Beyer C,Zendehdel A(2017)Progesterone therapy induces an M1 to M2 switch in microglia phenotype and suppresses NLRP3 inflammasome in a cuprizone-induced demyelination mouse model.Int Immunopharmacol 51:131-139.
Azcoitia I,Leonelli E,Magnaghi V,Veiga S,Garcia-Segura LM,Melcangi RC(2003)Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats.Neurobiol Aging 24:853-860.
Bracchi-Ricard V,Lambertsen KL,Ricard J,Nathanson L,Karmally S,Johnstone J,Ellman DG,Frydel B,McTigue DM,Bethea JR(2013)Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury.J Neuroinflammation 10:92.
Brinton RD(2013)Neurosteroids as regenerative agents in the brain:therapeutic implications.Nat Rev Endocrinol 9:241-250.
Chan JR,Phillips LJ 2nd,Glaser M(1998)Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation.Proc Natl Acad Sci U S A 95:10459-10464.
Chavez-Delgado ME,Gomez-Pinedo U,Feria-Velasco A,Huerta-Viera M,Castaneda SC,Toral FA,Parducz A,Anda SL,Mora-Galindo J,Garcia-Estrada J(2005)Ultrastructural analysis of guided nerve regeneration using progesterone-and pregnenolone-loaded chitosan prostheses.J Biomed Mater Res B Appl Biomater 74:589-600.
Chesik D,De Keyser J(2010)Progesterone and dexamethasone differentially regulate the IGF-system in glial cells.Neurosci Lett 468:178-182.
De Leon-Nava MA,Nava K,Soldevila G,Lopez-Griego L,Chavez-Rios JR,Vargas-Villavicencio JA,Morales-Montor J(2009)Immune sexual dimorphism:effect of gonadal steroids on the expression of cytokines,sex steroid receptors,and lymphocyte proliferation.J Steroid Biochem Mol Biol 113:57-64.
De Nicola AF,Garay LI,Meyer M,Guennoun R,Sitruk-Ware R,Schumacher M,Gonzalez Deniselle MC(2018)Neurosteroidogenesis and progesterone anti-inflammatory/neuroprotective effects.JNeuroendocrinol doi:10.1111/jne.12502.
El-Etr M,Rame M,Boucher C,Ghoumari AM,Kumar N,Liere P,Pianos A,Schumacher M,Sitruk-Ware R(2015)Progesterone and nestorone promote myelin regeneration in chronic demyelinating lesions of corpus callosum and cerebral cortex.Glia 63:104-117.
Fancy SP,Chan JR,Baranzini SE,Franklin RJ,Rowitch DH(2011)Myelin regeneration:a recapitulation of development?Annu Rev Neurosci 34:21-43.
Gago N,Akwa Y,Sananes N,Guennoun R,Baulieu EE,El-Etr M,Schumacher M(2001)Progesterone and the oligodendroglial lineage:stage-dependent biosynthesis and metabolism.Glia 36:295-308.
Gago N,El-Etr M,Sananes N,Cadepond F,Samuel D,Avellana-Adalid V,Baron-Van Evercooren A,Schumacher M(2004)3alpha,5alpha-Tetrahydroprogesterone(allopregnanolone)and gamma-aminobutyric acid:autocrine/paracrine interactions in the control of neonatal PSA-NCAM+progenitor proliferation.J Neurosci Res 78:770-783.
Garay LI,Gonzalez Deniselle MC,Brocca ME,Lima A,Roig P,De Nicola AF(2012)Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis.Neuroscience 226:40-50.
Ghoumari AM,Baulieu EE,Schumacher M(2005)Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures.Neuroscience 135:47-58.
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.
Guennoun R,Benmessahel Y,Delespierre B,Gouezou M,Rajkowski KM,Baulieu EE,Schumacher M(2001)Progesterone stimulates Krox-20 gene expression in Schwann cells.Brain Res Mol Brain Res90:75-82.
Huang H,Zhao XF,Zheng K,Qiu M(2013)Regulation of the timing of oligodendrocyte differentiation:mechanisms and perspectives.Neurosci Bull 29:155-164.
Hussain R,El-Etr M,Gaci O,Rakotomamonjy J,Macklin WB,Kumar N,Sitruk-Ware R,Schumacher M,Ghoumari AM(2011)Progesterone and Nestorone facilitate axon remyelination:a role for progesterone receptors.Endocrinology 152:3820-3831.
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.
Jones LA,Anthony JP,Henriquez FL,Lyons RE,Nickdel MB,Carter KC,Alexander J,Roberts CW(2008)Toll-like receptor-4-mediated macrophage activation is differentially regulated by progesterone via the glucocorticoid and progesterone receptors.Immunology 125:59-69.
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.
Jure I,De Nicola AF,Labombarda F(2019)Progesterone effects on oligodendrocyte differentiation in injured spinal cord.Brain Res1708:36-46
Khan KN,Masuzaki H,Fujishita A,Kitajima M,Sekine I,Matsuyama T,Ishimaru T(2005)Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis.Hum Reprod 20:2004-2013.
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.
Labombarda F,Gonzalez SL,Deniselle MC,Vinson GP,Schumacher M,De Nicola AF,Guennoun R(2003)Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord.J Neurochem 87:902-913.
Labombarda F,Gonzalez S,Gonzalez Deniselle MC,Garay L,Guennoun R,Schumacher M,De Nicola AF(2006)Progesterone increases the expression of myelin basic protein and the number of cells showing NG2 immunostaining in the lesioned spinal cord.J Neurotrauma23:181-192.
Labombarda F,Gonzalez 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.
Labombarda F,Gonzalez S,Lima A,Roig P,Guennoun R,Schumacher M,De Nicola AF(2011)Progesterone attenuates astro-and microgliosis and enhances oligodendrocyte differentiation following spinal cord injury.Exp Neurol 231:135-146.
Labombarda F,Jure I,Gonzalez S,Lima A,Roig P,Guennoun R,Schumacher M,De Nicola AF(2015)A functional progesterone receptor is required for immunomodulation,reduction of reactive gliosis and survival of oligodendrocyte precursors in the injured spinal cord.J Steroid Biochem Mol Biol 154:274-284.
Labombarda F,Meffre D,Delespierre B,Krivokapic-Blondiaux S,Chastre A,Thomas P,Pang Y,Lydon JP,Gonzalez SL,De Nicola AF,Schumacher M,Guennoun R(2010)Membrane progesterone receptors localization in the mouse spinal cord.Neuroscience 166:94-106.
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.
Lambert JJ,Belelli D,Harney SC,Peters JA,Frenguelli BG(2001)Modulation of native and recombinant GABA(A)receptors by endogenous and synthetic neuroactive steroids.Brain Res Brain Res Rev37:68-80.
Liu J,Casaccia P(2010)Epigenetic regulation of oligodendrocyte identity.Trends Neurosci 33:193-201.
Magnaghi V,Cavarretta I,Galbiati M,Martini L,Melcangi RC(2001)Neuroactive steroids and peripheral myelin proteins.Brain Res Brain Res Rev 37:360-371.
Melcangi RC,Panzica GC(2014)Allopregnanolone:state of the art.Prog Neurobiol 113:1-5.
Melcangi RC,Magnaghi V,Cavarretta I,Zucchi I,Bovolin P,D’Urso D,Martini L(1999)Progesterone derivatives are able to influence peripheral myelin protein 22 and P0 gene expression:possible mechanisms of action.J Neurosci Res 56:349-357.
Melcangi RC,Giatti S,Pesaresi M,Calabrese D,Mitro N,Caruso D,Garcia-Segura LM(2011)Role of neuroactive steroids in the peripheral nervous system.Front Endocrinol(Lausanne)2:104.
Mercier G,Turque N,Schumacher M(2001)Early activation of transcription factor expression in Schwann cells by progesterone.Brain Res Mol Brain Res 97:137-148.
Miron VE,Franklin RJ(2014)Macrophages and CNS remyelination.JNeurochem 130:165-171.
Palazuelos J,Klingener M,Aguirre A(2014)TGFbeta signaling regulates the timing of CNS myelination by modulating oligodendrocyte progenitor cell cycle exit through SMAD3/4/FoxO1/Sp1.J Neurosci34:7917-7930.
Rupprecht R,Hauser CA,Trapp T,Holsboer F(1996)Neurosteroids:molecular mechanisms of action and psychopharmacological significance.J Steroid Biochem Mol Biol 56:163-168.
Schumacher M,Hussain R,Gago N,Oudinet JP,Mattern C,Ghoumari AM(2012)Progesterone synthesis in the nervous system:implications for myelination and myelin repair.Front Neurosci 6:10.
Sierra A,Gottfried-Blackmore A,Milner TA,McEwen BS,Bulloch K(2008)Steroid hormone receptor expression and function in microglia.Glia 56:659-674.
Sofroniew MV(2009)Molecular dissection of reactive astrogliosis and glial scar formation.Trends Neurosci 32:638-647.
Szekeres-Bartho J,Halasz M,Palkovics T(2009)Progesterone in pregnancy;receptor-ligand interaction and signaling pathways.J Reprod Immunol 83:60-64.
Vukusic S,Ionescu I,El-Etr M,Schumacher M,Baulieu EE,Cornu C,Confavreux C,Prevention of Post-Partum Relapses with P,Estradiol in Multiple Sclerosis Study G(2009)The prevention of post-partum relapses with progestin and estradiol in multiple sclerosis(PO-PART’MUS)trial:rationale,objectives and state of advancement.JNeurol Sci 286:114-118.
Wang JM,Johnston PB,Ball BG,Brinton RD(2005)The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression.J Neurosci 25:4706-4718.
Yates MA,Li Y,Chlebeck P,Proctor T,Vandenbark AA,Offner H(2010)Progesterone treatment reduces disease severity and increases IL-10in experimental autoimmune encephalomyelitis.J Neuroimmunol220:136-139.
Yu HJ,Fei J,Chen XS,Cai QY,Liu HL,Liu GD,Yao ZX(2010)Progesterone attenuates neurological behavioral deficits of experimental autoimmune encephalomyelitis through remyelination with nucleus-sublocalized Olig1 protein.Neurosci Lett 476:42-45.
Zhou X,He X,Ren Y(2014)Function of microglia and macrophages in secondary damage after spinal cord injury.Neural Regen Res 9:1787-1795.
Azcoitia I,Leonelli E,Magnaghi V,Veiga S,Garcia-Segura LM,Melcangi RC(2003)Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats.Neurobiol Aging 24:853-860.
Bracchi-Ricard V,Lambertsen KL,Ricard J,Nathanson L,Karmally S,Johnstone J,Ellman DG,Frydel B,McTigue DM,Bethea JR(2013)Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury.J Neuroinflammation 10:92.
Brinton RD(2013)Neurosteroids as regenerative agents in the brain:therapeutic implications.Nat Rev Endocrinol 9:241-250.
Chan JR,Phillips LJ 2nd,Glaser M(1998)Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation.Proc Natl Acad Sci U S A 95:10459-10464.
Chavez-Delgado ME,Gomez-Pinedo U,Feria-Velasco A,Huerta-Viera M,Castaneda SC,Toral FA,Parducz A,Anda SL,Mora-Galindo J,Garcia-Estrada J(2005)Ultrastructural analysis of guided nerve regeneration using progesterone-and pregnenolone-loaded chitosan prostheses.J Biomed Mater Res B Appl Biomater 74:589-600.
Chesik D,De Keyser J(2010)Progesterone and dexamethasone differentially regulate the IGF-system in glial cells.Neurosci Lett 468:178-182.
De Leon-Nava MA,Nava K,Soldevila G,Lopez-Griego L,Chavez-Rios JR,Vargas-Villavicencio JA,Morales-Montor J(2009)Immune sexual dimorphism:effect of gonadal steroids on the expression of cytokines,sex steroid receptors,and lymphocyte proliferation.J Steroid Biochem Mol Biol 113:57-64.
De Nicola AF,Garay LI,Meyer M,Guennoun R,Sitruk-Ware R,Schumacher M,Gonzalez Deniselle MC(2018)Neurosteroidogenesis and progesterone anti-inflammatory/neuroprotective effects.JNeuroendocrinol doi:10.1111/jne.12502.
El-Etr M,Rame M,Boucher C,Ghoumari AM,Kumar N,Liere P,Pianos A,Schumacher M,Sitruk-Ware R(2015)Progesterone and nestorone promote myelin regeneration in chronic demyelinating lesions of corpus callosum and cerebral cortex.Glia 63:104-117.
Fancy SP,Chan JR,Baranzini SE,Franklin RJ,Rowitch DH(2011)Myelin regeneration:a recapitulation of development?Annu Rev Neurosci 34:21-43.
Gago N,Akwa Y,Sananes N,Guennoun R,Baulieu EE,El-Etr M,Schumacher M(2001)Progesterone and the oligodendroglial lineage:stage-dependent biosynthesis and metabolism.Glia 36:295-308.
Gago N,El-Etr M,Sananes N,Cadepond F,Samuel D,Avellana-Adalid V,Baron-Van Evercooren A,Schumacher M(2004)3alpha,5alpha-Tetrahydroprogesterone(allopregnanolone)and gamma-aminobutyric acid:autocrine/paracrine interactions in the control of neonatal PSA-NCAM+progenitor proliferation.J Neurosci Res 78:770-783.
Garay LI,Gonzalez Deniselle MC,Brocca ME,Lima A,Roig P,De Nicola AF(2012)Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis.Neuroscience 226:40-50.
Ghoumari AM,Baulieu EE,Schumacher M(2005)Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures.Neuroscience 135:47-58.
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.
Guennoun R,Benmessahel Y,Delespierre B,Gouezou M,Rajkowski KM,Baulieu EE,Schumacher M(2001)Progesterone stimulates Krox-20 gene expression in Schwann cells.Brain Res Mol Brain Res90:75-82.
Huang H,Zhao XF,Zheng K,Qiu M(2013)Regulation of the timing of oligodendrocyte differentiation:mechanisms and perspectives.Neurosci Bull 29:155-164.
Hussain R,El-Etr M,Gaci O,Rakotomamonjy J,Macklin WB,Kumar N,Sitruk-Ware R,Schumacher M,Ghoumari AM(2011)Progesterone and Nestorone facilitate axon remyelination:a role for progesterone receptors.Endocrinology 152:3820-3831.
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.
Jones LA,Anthony JP,Henriquez FL,Lyons RE,Nickdel MB,Carter KC,Alexander J,Roberts CW(2008)Toll-like receptor-4-mediated macrophage activation is differentially regulated by progesterone via the glucocorticoid and progesterone receptors.Immunology 125:59-69.
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.
Jure I,De Nicola AF,Labombarda F(2019)Progesterone effects on oligodendrocyte differentiation in injured spinal cord.Brain Res1708:36-46
Khan KN,Masuzaki H,Fujishita A,Kitajima M,Sekine I,Matsuyama T,Ishimaru T(2005)Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis.Hum Reprod 20:2004-2013.
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.
Labombarda F,Gonzalez SL,Deniselle MC,Vinson GP,Schumacher M,De Nicola AF,Guennoun R(2003)Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord.J Neurochem 87:902-913.
Labombarda F,Gonzalez S,Gonzalez Deniselle MC,Garay L,Guennoun R,Schumacher M,De Nicola AF(2006)Progesterone increases the expression of myelin basic protein and the number of cells showing NG2 immunostaining in the lesioned spinal cord.J Neurotrauma23:181-192.
Labombarda F,Gonzalez 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.
Labombarda F,Gonzalez S,Lima A,Roig P,Guennoun R,Schumacher M,De Nicola AF(2011)Progesterone attenuates astro-and microgliosis and enhances oligodendrocyte differentiation following spinal cord injury.Exp Neurol 231:135-146.
Labombarda F,Jure I,Gonzalez S,Lima A,Roig P,Guennoun R,Schumacher M,De Nicola AF(2015)A functional progesterone receptor is required for immunomodulation,reduction of reactive gliosis and survival of oligodendrocyte precursors in the injured spinal cord.J Steroid Biochem Mol Biol 154:274-284.
Labombarda F,Meffre D,Delespierre B,Krivokapic-Blondiaux S,Chastre A,Thomas P,Pang Y,Lydon JP,Gonzalez SL,De Nicola AF,Schumacher M,Guennoun R(2010)Membrane progesterone receptors localization in the mouse spinal cord.Neuroscience 166:94-106.
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.
Lambert JJ,Belelli D,Harney SC,Peters JA,Frenguelli BG(2001)Modulation of native and recombinant GABA(A)receptors by endogenous and synthetic neuroactive steroids.Brain Res Brain Res Rev37:68-80.
Liu J,Casaccia P(2010)Epigenetic regulation of oligodendrocyte identity.Trends Neurosci 33:193-201.
Magnaghi V,Cavarretta I,Galbiati M,Martini L,Melcangi RC(2001)Neuroactive steroids and peripheral myelin proteins.Brain Res Brain Res Rev 37:360-371.
Melcangi RC,Panzica GC(2014)Allopregnanolone:state of the art.Prog Neurobiol 113:1-5.
Melcangi RC,Magnaghi V,Cavarretta I,Zucchi I,Bovolin P,D’Urso D,Martini L(1999)Progesterone derivatives are able to influence peripheral myelin protein 22 and P0 gene expression:possible mechanisms of action.J Neurosci Res 56:349-357.
Melcangi RC,Giatti S,Pesaresi M,Calabrese D,Mitro N,Caruso D,Garcia-Segura LM(2011)Role of neuroactive steroids in the peripheral nervous system.Front Endocrinol(Lausanne)2:104.
Mercier G,Turque N,Schumacher M(2001)Early activation of transcription factor expression in Schwann cells by progesterone.Brain Res Mol Brain Res 97:137-148.
Miron VE,Franklin RJ(2014)Macrophages and CNS remyelination.JNeurochem 130:165-171.
Palazuelos J,Klingener M,Aguirre A(2014)TGFbeta signaling regulates the timing of CNS myelination by modulating oligodendrocyte progenitor cell cycle exit through SMAD3/4/FoxO1/Sp1.J Neurosci34:7917-7930.
Rupprecht R,Hauser CA,Trapp T,Holsboer F(1996)Neurosteroids:molecular mechanisms of action and psychopharmacological significance.J Steroid Biochem Mol Biol 56:163-168.
Schumacher M,Hussain R,Gago N,Oudinet JP,Mattern C,Ghoumari AM(2012)Progesterone synthesis in the nervous system:implications for myelination and myelin repair.Front Neurosci 6:10.
Sierra A,Gottfried-Blackmore A,Milner TA,McEwen BS,Bulloch K(2008)Steroid hormone receptor expression and function in microglia.Glia 56:659-674.
Sofroniew MV(2009)Molecular dissection of reactive astrogliosis and glial scar formation.Trends Neurosci 32:638-647.
Szekeres-Bartho J,Halasz M,Palkovics T(2009)Progesterone in pregnancy;receptor-ligand interaction and signaling pathways.J Reprod Immunol 83:60-64.
Vukusic S,Ionescu I,El-Etr M,Schumacher M,Baulieu EE,Cornu C,Confavreux C,Prevention of Post-Partum Relapses with P,Estradiol in Multiple Sclerosis Study G(2009)The prevention of post-partum relapses with progestin and estradiol in multiple sclerosis(PO-PART’MUS)trial:rationale,objectives and state of advancement.JNeurol Sci 286:114-118.
Wang JM,Johnston PB,Ball BG,Brinton RD(2005)The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression.J Neurosci 25:4706-4718.
Yates MA,Li Y,Chlebeck P,Proctor T,Vandenbark AA,Offner H(2010)Progesterone treatment reduces disease severity and increases IL-10in experimental autoimmune encephalomyelitis.J Neuroimmunol220:136-139.
Yu HJ,Fei J,Chen XS,Cai QY,Liu HL,Liu GD,Yao ZX(2010)Progesterone attenuates neurological behavioral deficits of experimental autoimmune encephalomyelitis through remyelination with nucleus-sublocalized Olig1 protein.Neurosci Lett 476:42-45.
Zhou X,He X,Ren Y(2014)Function of microglia and macrophages in secondary damage after spinal cord injury.Neural Regen Res 9:1787-1795.
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