Cited by 92Spinal Cord Injury ResearchNerve injury and regenerationMultiple Sclerosis Research Studies

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Progesterone Treatment of Spinal Cord Injury: Effects on Receptors, Neurotrophins, and Myelination

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De Nicola, Alejandro F., Gonzalez, Susana L., Labombarda, Florencia, Deniselle, Maria Claudia González, Garay, Laura, Guennoun, Rachida, Schumacher, Michael·2006·Journal of Molecular Neuroscience

DOI 10.1385/jmn:28:1:3

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Abstract

In addition to its traditional role in reproduction, progesterone (PROG) has demonstrated neuroprotective and promyelinating effects in lesions of the peripheral and central nervous systems, including the spinal cord. The latter is a target of PROG, as nuclear receptors, as well as membrane receptors, are expressed by neurons and/or glial cells. When spinal cord injury (SCI) is produced at the thoracic level, several genes become sensitive to PROG in the region caudal to the lesion site. Although the cellular machinery implicated in PROG neuroprotection is only emerging, neurotrophins, their receptors, and signaling cascades might be part of the molecules involved in this process. In rats with SCI, a 3-d course of PROG treatment increased the mRNA of brain-derived neurotrophic factor (BDNF) and BDNF immunoreactivity in perikaryon and processes of motoneurons, whereas chromatolysis was strongly prevented. The increased expression of BDNF correlated with increased immunoreactivity for the BDNF receptor TrkB and for phosphorylated cAMP-responsive element binding in motoneurons. In the same SCI model, PROG restored myelination, according to measurements of myelin basic protein (MBP) and mRNA levels, and further increased the density of NG2+-positive oligodendrocyte progenitors. These cells might be involved in remyelination of the lesioned spinal cord. Interestingly, similarities in the regulation of molecular parameters and some cellular events attributed to PROG and BDNF (i.e., choline acetyltransferase, Na,K-ATPase, MBP, chromatolysis) suggest that BDNF and PROG might share intracellular pathways. Furthermore, PROG-induced BDNF might regulate, in a paracrine or autocrine fashion, the function of neurons and glial cells and prevent the generation of damage.

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Translational regulation by steroids. Identification of a steroid modulatory element in the 5'-untranslated region of the myelin basic protein messenger RNA
Verdi, J. M., & Campagnoni, A. T. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)30506-9 · Cited by 77
Basis of progesterone protection in spinal cord neurodegeneration
Deniselle, M. C. G., Costa, J. J. L., González, S. L., Labombarda, F., Garay, L. I., Guennoun, R., Schumacher, M., & Nicola, A. F. D. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00262-5 · Cited by 77
Self-citation
Progesterone as a neurosteroid: synthesis and actions in rat glial cellsProceedings of Xth International Congress on Hormonal Steroids, Quebec, Canada, 17–21 June 1998.
Jung‐Testas, I., Thi, A. D., Koenig, H. L., Désarnaud, F., Shazand, K., Schumacher, M., & Baulieu, E. E. (1999) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00149-6 · Cited by 73 · cited 2×
“The latter are fundamental players in this scenario, as they are sensitive to PROG and also take up and produce BDNF (Jung-Testas et al., 1999; Dougherty et al., 2000; McTigue et al., 1998; Schumacher et al., 2000).”
Self-citation
Estrogen stimulates brain‐derived neurotrophic factor expression in embryonic mouse midbrain neurons through a membrane‐mediated and calcium‐dependent mechanism
Ivanova, T., Küppers, E., Engele, J., & Beyer, C. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1214 · Cited by 72 · cited 8×
“BDNF is a key regulator of myelin proteins in the PNS and the CNS (Chan et al., 2001; Du et al., 2003; Tolwani et al., 2004), and this property also applies to the contused spinal cord, in which MBP expression is highly enhanced by BDNF treatment (McTigue et al., 1998; Ikeda et al., 2002).”
Influential
Increase of oligodendrocyte progenitor cells after spinal cord injury
Ishii, K., Toda, M., Nakai, Y., Asou, H., Watanabe, M., Nakamura, M., Yato, Y., Fujimura, Y., Kawakami, Y., Toyama, Y., et al. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1180 · Cited by 71 · cited 2×
“NG2 and OPC cells labeled with other markers are able to migrate, proliferate, and differentiate into mature oligodendrocytes and, as already pointed out, can express several myelin constituents (Nishiyama et al., 1999; Ishii et al., 2001; McTigue et al., 1998; Ye et al., 2003; Li and Blakemore, 2004).”
Manganese uptake into rat brain during development and aging
Takeda, A., Ishiwatari, S., & Okada, S. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990401)56:1 · Cited by 69
Identification of the rat adrenal zona fasciculata/reticularis specific protein, inner zone antigen (IZAg), as the putative membrane progesterone receptor
Raza, F. S., Takemori, H., Tojo, H., Okamoto, M., & Vinson, G. P. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02096.x · Cited by 67
Immunocytochemical evidence for a progesterone receptor in neurons and glial cells of the rat spinal cord
Labombarda, F., Guennoun, R., González, S. L., Roig, P., Lima, A. E., Schumacher, M., & Nicola, A. F. D. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01191-5 · Cited by 67 · cited 6×
“As pointed out in the Introduction, an estrogeninsensitive PR recently has been demonstrated in the rat spinal cord by immunocytochemistry (Labombarda et al., 2000b).”
InfluentialSelf-citation
Survival of motoneurons following axotomy is enhanced by lactation or by progesterone treatment
Yu, W.-H. A. (1989) · Brain Research · doi:10.1016/0006-8993(89)90075-9 · Cited by 67
The re-expression of the homeodomain transcription factor Gtx during remyelination of experimentally induced demyelinating lesions in young and old rat brain
Sim, F. J., Hinks, G. L., & Franklin, R. J. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00252-9 · Cited by 64 · cited 1×
“To investigate if changes in MBP immunostaining were also reflected at the mRNA level, ISH was carried out using a probe specific for MBP exon1 mRNA (Sim et al., 2000).”
Progesterone stimulates Krox-20 gene expression in Schwann cells
Guennoun, R., Benmessahel, Y., Delespierre, B., Gouézou, M., Rajkowski, K. M., Baulieu, E. E., & Schumacher, M. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00094-8 · Cited by 63 · cited 2×
“…the presence of a membrane receptor for PROG in the spinal cord, called 25-Dx (Labombarda et al., 2003), and PROG metabolism to reduced derivatives (Guennoun et al., 2001), which modulate the activity of neurotransmitter receptors (Majewska et al., 1986; Rupprecht et al., 1996), further supports…”
Self-citation
The neurosteroid progesterone increases the expression of myelin proteins (MBP and CNPase) in rat oligodendrocytes in primary culture
Jung‐Testas, I., Schumacher, M., Röbel, P., & Baulieu, E. E. (1996) · Cellular and Molecular Neurobiology · doi:10.1007/bf02088110 · Cited by 62 · cited 2×
“Considering that MBP expression responded to PROG treatment in several experimental models (Jung-Testas et al., 1996; Ghoumari et al., 2003; Ibanez et al., 2004), we studied if PROG prevented SCI-induced demyelination.”
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A quantitative analysis of rat central nervous system myelination using the immunohistochemical method for MBP
Hamano, K., Iwasaki, N., Takeya, T., & Takita, H. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00025-9 · Cited by 58 · cited 1×
“MBP is a component of central myelin, which provides a reliable method for assessing the process of myelination in the brain (Hamano et al., 1996; Muse et al., 2001).”
Effect of cyclic AMP on the expression of myelin basic protein species and myelin proteolipid protein in committed oligodendrocytes: Differential involvement of the transcription factor CREB
Afshari, F. S., Chu, A. K., & Sato‐Bigbee, C. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1195 · Cited by 56
Structural changes of anterior horn neurons and their synaptic input caudal to a low thoracic spinal cord hemisection in the adult rat: a light and electron microscopic study
Nacimiento, W., Sappok, T., Brook, G. A., T�th, L., Schoen, S. W., Noth, J., & Kreutzberg, G. W. (1995) · Acta Neuropathologica · doi:10.1007/bf00318567 · Cited by 55 · cited 2×
“SCI was accompanied by typical signs of chromatolysis (Nacimiento et al., 1995; Young, 1966; Tanridag et al., 1999), a feature of incipient motoneuron degeneration that culminates in cell dysfunction and death (Eidelberg et al., 1989; Wakayama, 1992; Grossman et al., 2001).”
Non target-derived roles of the neurotrophins
Acheson, A. L., & Lindsay, R. M. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0037 · Cited by 52 · cited 1×
“Detection of BDNF mRNAand protein in motoneurons (Dreyfus et al., 1999; Buck et al., 2000), coupled with the beneficial effects of this neurotrophin on damaged motoneurons, indicates that locally synthesized BDNF might be an autocrine/paracrine regulator of neuronal functions (Miranda et al., 1993; Acheson and Linsday…”
Background
Paracrine and autocrine actions of neurotrophic factors
Davies, A. M. (1996) · Neurochemical Research · doi:10.1007/bf02532296 · Cited by 50
Mouse NG2+Oligodendrocyte Precursors Express mRNA for Proteolipid Protein But Not Its DM-20 Variant: A Study of Laser Microdissection-Captured NG2+Cells
Ye, P., Bagnell, R. C., & D’Ercole, A. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04401.2003 · Cited by 47 · cited 4×
“NG2 and OPC cells labeled with other markers are able to migrate, proliferate, and differentiate into mature oligodendrocytes and, as already pointed out, can express several myelin constituents (Nishiyama et al., 1999; Ishii et al., 2001; McTigue et al., 1998; Ye et al., 2003; Li and Blakemore, 2004).”
Influential
Modulation of NADPH-diaphorase and glial fibrillary acidic protein by progesterone in astrocytes from normal and injured rat spinal cord
Labombarda, F., Gonzalez, S., Roig, P., Lima, A. E., Guennoun, R., Schumacher, M., & Nicola, A. F. D. (2000) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(00)00064-9 · Cited by 45 · cited 6×
“As pointed out in the Introduction, an estrogeninsensitive PR recently has been demonstrated in the rat spinal cord by immunocytochemistry (Labombarda et al., 2000b).”
InfluentialSelf-citation
Steroid Effects on Glial Cells
Nicola, A. F. D., Labombarda, F., González, S. L., Deniselle, M. C. G., Guennoun, R., & Schumacher, M. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.030 · Cited by 40 · cited 2×
“…neuronal BDNF expression, reversion of severe chromatolysis, and stimulation of key features of neuronal and glial cell function (Labombarda et al., 2002; De Nicola et al., 2003) suggest that PROG provides local trophic support and represents a new approach to prevent neuronal death after injury.”
Self-citation
Ciliary Neurotrophic Factor Receptor α in Spinal Motoneurons is Regulated by Gonadal Hormones
Forger, N. G., Wagner, C. K., Contois, M., Bengston, L., & MacLennan, A. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08720.1998 · Cited by 40 · cited 1×
“Recent data indicate that steroid hormones interplay with neurotrophins in the CNS (Forger et al., 1998; Ianova et al., 2001; Solum and Handa, 2002).”
Cloning and Expression of VEMA: A Novel Ventral Midline Antigen in the Rat CNS
Runko, E., Wideman, C., & Kaprielian, Z. (1999) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1999.0794 · Cited by 35 · cited 9×
“BDNF is a key regulator of myelin proteins in the PNS and the CNS (Chan et al., 2001; Du et al., 2003; Tolwani et al., 2004), and this property also applies to the contused spinal cord, in which MBP expression is highly enhanced by BDNF treatment (McTigue et al., 1998; Ikeda et al., 2002).”
Influential
Morphological and histochemical studies of partially and totally deafferented spinal cord segments
Young, I. J. (1966) · Experimental Neurology · doi:10.1016/0014-4886(66)90009-4 · Cited by 33
Expression of neurotrophin receptors trkB and trkC and their ligands in rat adrenal gland and the intermediolateral column of the spinal cord
Schober, A., Wolf, N. I., Kahane, N., Kalcheim, C., KRIEGLSTEIN, K. G., & Unsicker, K. (1999) · Cell and Tissue Research · doi:10.1007/s004410051288 · Cited by 28 · cited 3×
“Neurotrophic factors and their receptors are present not only in developing but also in adult spinal cord neurons (Dreyfus et al., 1999; Schober et al., 1999, Buck et al., 2000), indicating that they might play an important role in neuronal survival (Thoenen et al., 1995) and axonal regeneration…”
Estrogen-Inducible Progesterone Receptors in the Rat Lumbar Spinal Cord: Regulation by Ovarian Steroids and Fluctuation across the Estrous Cycle
Monks, D. A., Arciszewska, G., & Watson, N. V. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1717 · Cited by 28
Neurotrophic Factors Attenuate Alterations in Spinal Cord Evoked Potentials and Edema Formation Following Trauma to the Rat Spinal Cord
Winkler, T., Sharma, H. S., Stålberg, E., & Badgaiyan, R. D. (2000) · Springer eBooks · doi:10.1007/978-3-7091-6346-7_60 · Cited by 26 · cited 2×
“Additionally, BDNF administration decreases edema formation (Winkler et al., 2000) and promotes the recovery of myelin-basic protein (MBP) after compression-induced SCI (Ikeda et al.”
Review : Progesterone and Recovery after Traumatic Brain Injury: An Overview
Stein, D., & Fulop, Z. (1998) · The Neuroscientist · doi:10.1177/107385849800400615 · Cited by 25
Motor neuron degeneration due to aluminium deposition in the spinal cord: a light microscopical study
Tanrıdağ, T., Coşkun, T., Hürdağ, C., Arbak, S., Aktan, S., & Yeğen, B. Ç. (1999) · Acta Histochemica · doi:10.1016/s0065-1281(99)80018-x · Cited by 19 · cited 2×
“SCI was accompanied by typical signs of chromatolysis (Nacimiento et al., 1995; Young, 1966; Tanridag et al., 1999), a feature of incipient motoneuron degeneration that culminates in cell dysfunction and death (Eidelberg et al., 1989; Wakayama, 1992; Grossman et al., 2001).”
Morphometry of spinal motor neurons in amyotrophic lateral sclerosis with special reference to chromatolysis and intracytoplasmic inclusion bodies
WAKAYAMA, I. (1992) · Brain Research · doi:10.1016/0006-8993(92)91365-l · Cited by 18 · cited 2×
“SCI was accompanied by typical signs of chromatolysis (Nacimiento et al., 1995; Young, 1966; Tanridag et al., 1999), a feature of incipient motoneuron degeneration that culminates in cell dysfunction and death (Eidelberg et al., 1989; Wakayama, 1992; Grossman et al., 2001).”
The Number of Cells Expressing the Myelin-Supporting Oligodendrocyte Marker PLP-Exon 3b Remains Unchanged in Wallerian Degeneration
Li, G., & Blakemore, W. F. (2004) · Journal of Neurotrauma · doi:10.1089/0897715041651015 · Cited by 8 · cited 3×
“These cells were practically absent in control rats receiving vehicle or PROG treatment but in agreement with others (Nishiyama et al., 1999; Levine et al., 2001; Hubbard, 2003); SCI alone stimulated NG2 + cell number over controls in white matter and gray matter.”
BackgroundResultInfluential
Mouse NG2 + Oligodendrocyte Precursors Express mRNA for Proteolipid Protein But Not Its DM-20 Variant: A Study of Laser Microdissection-Captured NG2 + Cells
Ye, P., D’Ercole, A. J., & Bagnell, R. C. (2021) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/37wt-ep51 · Cited by 4
Structural changes of anterior horn neurons and their synaptic input caudal to a low thoracic spinal cord hemisection in the adult rat: a light and electron microscopic study
Nacimiento, W., Sappok, T., Brook, G. A., et al. (1995) · Acta Neuropathologica · doi:10.1007/s004010050369 · Cited by 3

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Authors: De Nicola, A. F., Gonzalez, S. L., Labombarda, F., Deniselle, M. C. G., Garay, L., Guennoun, R., & Schumacher, M.
Affiliations: Universidad de Buenos Aires (AR)
Inserm (FR)
ORCID: Labombarda, Florencia
Garay, Laura
Guennoun, Rachida
Venue: Journal of Molecular Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2006
Volume: 28
Issue: 1
Pages: 3-16
ISSN: 0895-8696 (ISSN-L)
DOI: 10.1385/jmn:28:1:3
OpenAlex: W153328306
Semantic Scholar: 8ca69c844ba5b9c038c308d3f8e1aa7ece651fa0
Cited by: 92
References: 93
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 4 · 2018: 3 · 2017: 6 · 2016: 6 · 2015: 3 · 2014: 2 · 2013: 7 · 2012: 5
FWCI: 8.39
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: cc-by-nc-sa
Locations: Journal of Molecular Neuroscience (publishedVersion)
PubMed (publishedVersion)
CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
Funders: Consejo Nacional de Investigaciones Científicas y Técnicas
Universidad de Buenos Aires (CONICET)
Fondo para la Investigación Científica y Tecnológica
Topics: Health Sciences › Medicine › Clinical Neurology › Spinal Cord Injury Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Keywords: progesterone, spinal cord injury, neuroprotection, brain-derived neurotrophic factor, TrkB receptor, myelination, remyelination, oligodendrocyte progenitors, motor neurons, chromatolysis, myelin basic protein, nuclear receptors, paracrine signaling
MeSH terms: Animals, Myelin Basic Protein, Myelin Sheath, Neurons, Oligodendroglia, Progesterone, Receptors, Progesterone, Spinal Cord, Spinal Cord Injuries, Stem Cells, Cyclic AMP Response Element-Binding Protein, Neuroprotective Agents, Brain-Derived Neurotrophic Factor

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Progesterone Treatment of Spinal Cord Injury: Effects on Receptors, Neurotrophins, and Myelination

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