Artículo

González, S.L.; López-Costa, J.J.; Labombarda, F.; Deniselle, M.C.G.; Guennoun, R.; Schumacher, M.; De Nicola, A.F. "Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury" (2009) Cellular and Molecular Neurobiology. 29(1):27-39
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Abstract:

(1) Following acute spinal cord injury, progesterone modulates several molecules essential for motoneuron function, although the morphological substrates for these effects are unknown. (2) The present study analyzed morphological changes in motoneurons distal to the lesion site from rats with or without progesterone treatment. We employed electron microscopy to study changes in nucleus and cytoplasm and immunohistochemistry for the microtubule-associated protein 2 (MAP2) for changes in cytoskeleton. (3) After spinal cord injury, the nucleoplasm appeared more finely dispersed resulting in reduced electron opacity and the nucleus adopted an eccentric position. Changes of perikarya included dissolution of Nissl bodies and dissociation of polyribosomes (chromatolysis). After progesterone treatment for 3 days, the deafferented motoneurons now presented a clumped nucleoplasm, a better-preserved rough endoplasmic reticulum and absence of chromatolysis. Progesterone partially prevented development of nuclear eccentricity. Whereas 50% of injured motoneurons showed nuclear eccentricity, only 16% presented this phenotype after receiving progesterone. Additionally, injured rats showed reduced immunostaining for MAP2 in dendrites, pointing to cytoskeleton abnormalities, whereas progesterone treatment attenuated the injury-induced loss of MAP2. (4) Our data indicated that progesterone maintained in part neuronal ultrastructure, attenuated chromatolysis, and preclude the loss of MAP2, suggesting a protective effect during the early phases of spinal cord injury. © 2008 Springer Science+Business Media, LLC.

Registro:

Documento: Artículo
Título:Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury
Autor:González, S.L.; López-Costa, J.J.; Labombarda, F.; Deniselle, M.C.G.; Guennoun, R.; Schumacher, M.; De Nicola, A.F.
Filiación:Laboratory of Neuroendocrine Biochemistry, Instituto de Biología y Medicina Experimental, Obligado 2490, Buenos Aires 1428, Argentina
Department of Human Biochemistry, Faculty of Medicine, University of Buenos Aires, Buenos Aires, Argentina
Instituto de Biología Celular y Neurociencias Prof. Eduardo de Robertis, Faculty of Medicine, University of Buenos Aires, Buenos Aires, Argentina
UMR 788 INSERM, University Paris 11: (Steroids Neuroprotection and Neuroregeneration), Kremlin-Bicêtre 94276, France
Instituto de Biologia y Medicina Experimental, Obligado 2490, Buenos Aires 1428, Argentina
Palabras clave:Chromatolysis; Electron microscopy; MAP2; Motoneuron; Neuroprotection; Progesterone; Spinal cord injury; microtubule associated protein 2; microtubule protein; progesterone; animal cell; animal experiment; animal model; article; cell ultrastructure; controlled study; cytoplasm; cytoskeleton; dendritic spine; electron microscopy; immunohistochemistry; male; motoneuron; neuromodulation; neuroprotection; Nissl substance; nonhuman; nucleus accumbens; perikaryon; polysome; priority journal; rat; rough endoplasmic reticulum; spinal cord injury; therapy effect; treatment duration; treatment outcome; treatment response; Acute Disease; Animals; Cell Nucleolus; Immunohistochemistry; Male; Microtubule-Associated Proteins; Motor Neurons; Neurons; Progesterone; Rats; Rats, Sprague-Dawley; Spinal Cord Injuries; Rattus
Año:2009
Volumen:29
Número:1
Página de inicio:27
Página de fin:39
DOI: http://dx.doi.org/10.1007/s10571-008-9291-0
Título revista:Cellular and Molecular Neurobiology
Título revista abreviado:Cell. Mol. Neurobiol.
ISSN:02724340
CODEN:CMNED
CAS:progesterone, 57-83-0; Microtubule-Associated Proteins; Mtap2 protein, rat; Progesterone, 57-83-0
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02724340_v29_n1_p27_Gonzalez

Referencias:

  • Acheson, A., Linsday, R.M., Non target-derived roles of the neurotrophins (1996) Philos Trans R Soc Lond B Biol Sci, 351, pp. 417-422
  • Azbill, R.D., Mu, X., Bruce-Keller, A.J., Mattson, M.P., Springer, J.E., Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury (1997) Brain Res, 765, pp. 283-290. , 10.1016/S0006-8993(97)00573-8
  • Azcoitia, J., Leonelli, E., Magnaghi, V., Veiga, S., García-Segura, L.M., Melcangi, R.C., Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats (2003) Neurobiol Aging, 24, pp. 853-860. , 10.1016/S0197-4580(02)00234-8
  • Bareyre, F.M., Schwab, M.E., Inflammation, degeneration and regeneration in the injured spinal cord: Insights from DNA microarrays (2003) Trends Neurosci, 26, pp. 555-563. , 10.1016/j.tins.2003.08.004
  • Barr, M., Hamilton, J.D., A quantitative study of certain morphological changes in spinal motor neurons during axon reaction (1948) J Comp Neurol, 89, pp. 93-121. , 10.1002/cne.900890203
  • Bernhardt, R., Matus, A., Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: A difference between dendritic and axonal cytoskeletons (1984) J Comp Neurol, 226, pp. 203-221. , 10.1002/cne.902260205
  • Bjugn, R., Nyengaard, J.R., Rosland, J.H., Spinal cord transection-no loss of distal ventral horn neurons. Modern stereological techniques reveal no transneuronal changes in the ventral horns of the mouse lumbar spinal cord after thoracic cord transection (1997) Exp Neurol, 148, pp. 179-186. , 10.1006/exnr.1997.6610
  • Caceres, A., Busciglio, J., Ferreira, A., Steward, O., An immunocytochemical and biochemical study of the microtubule-associated protein MAP-2 during post-lesion dendritic remodeling in the central nervous system of adult rats (1988) Brain Res, 427, pp. 233-246
  • Cragg, B.G., What is the signal for chromatolysis? (1970) Brain Res, 23, pp. 1-21. , 10.1016/0006-8993(70)90345-8
  • Cutler, S.M., Cekic, M., Miller, D.M., Wali, B., Van Landingham, J.W., Stein, D.G., Progesterone improves acute recovery after traumatic brain injury in the aged rat (2007) J Neurotrauma, 24, pp. 1475-1486. , 10.1089/neu.2007.0294
  • Davies, A.M., Paracrine and autocrine actions of neurotrophic factors (1996) Neurochem Res, 2, pp. 749-753. , 10.1007/BF02532296
  • De Nicola, A.F., Gonzalez, S.L., Labombarda, F., Gonzalez Deniselle, M.C., Garay, L., Guennoun, R., Progesterone treatment of spinal cord injury: Effects on receptors, neurotrophins, and myelination (2006) J Mol Neurosci, 28, pp. 3-15. , 10.1385/JMN:28:1:3
  • Desarnaud, F., Do Thai, A.N., Brown, A.M., Lemke, G., Suter, U., Baulieu, E.E., Progesterone stimulates the activity of the promoters of peripheral myelin protein-22 and protein zero genes in Schwann cells (1998) J Neurochem, 71, pp. 1765-1768
  • Di Michele, F., Lekieffre, D., Pasini, A., Bernardi, G., Benavides, J., Romeo, E., Increased neurosteroids synthesis after brain and spinal cord injury in rats (2000) Neurosci Lett, 284, pp. 65-68. , 10.1016/S0304-3940(00)00965-4
  • Di Stefano, G., Casoli, T., Fattoretti, P., Balietti, M., Grossi, Y., Giorgetti, B., Level and distribution of microtubule-associated protein-2 (MAP2) as an index of dendritic structural dynamics (2006) Rejuvenation Res, 9, pp. 94-98. , 10.1089/rej.2006.9.94
  • Eidelberg, E., Nguyen, L.H., Polich, R., Walden, J.G., Transsynaptic degeneration of motoneurones caudal to spinal cord lesions (1989) Brain Res Bull, 22, pp. 39-45. , 10.1016/0361-9230(89)90125-1
  • Farah, C.A., Liazoghli, D., Perreault, S., Desjardins, M., Guimont, A., Anton, A., Interaction of microtubule-associated protein-2 and p63: A new link between microtubules and rough endoplasmic reticulum membranes in neurons (2005) J Biol Chem, 280, pp. 9439-9449. , 10.1074/jbc.M412304200
  • Fee, D.B., Swartz, K.R., Joy, K.M., Roberts, K.N., Scheff, N.N., Scheff, S.W., Effects of progesterone on experimental spinal cord injury (2007) Brain Res, 1137, pp. 146-152. , 10.1016/j.brainres.2006.12.024
  • Fontaine-Lenoir, V., Chambraud, B., Fellous, A., David, S., Duchossoy, Y., Baulieu, E.E., Microtubule-associated protein 2 (MAP2) is a neurosteroid receptor (2006) Proc Natl Acad Sci USA, 103, pp. 4711-4716. , 10.1073/pnas.0600113103
  • Fukumitsu, H., Ohashi, A., Nitta, A., Nomoto, H., Furukawa, S., BDNF and NT-3 modulate expression and threonine phosphorylation of microtubule-associated protein 2 analogues, and alter their distribution in the developing rat cerebral cortex (1997) Neurosci Lett, 238, pp. 107-110. , 10.1016/S0304-3940(97)00852-5
  • Garay, L., Gonzalez Deniselle, M.C., Lima, A., Roig, P., De Nicola, A.F., Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis (2007) J Steroid Biochem Mol Biol, 107, pp. 228-237. , 10.1016/j.jsbmb.2007.03.040
  • Ghoumari, A.M., Ibanez, C., El-Etr, M., Leclerc, P., Eychenne, B., O'Malley, B.W., Progesterone and its metabolites increase myelin basic protein expression in organotypic slices cultures of rat cerebellum (2003) J Neurochem, 86, pp. 848-859. , 10.1046/j.1471-4159.2003.01881.x
  • Gold, B.G., Mobley, W.C., Matheson, S.F., Regulation of axonal caliber, neurofilament content, and nuclear localization in mature sensory neurons by nerve growth factor (1991) J Neurosci, 11, pp. 943-955
  • González, S.L., Labombarda, F., Deniselle González, M.C., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone up-regulates neuronal brain-derived neurotrophic factor expression in the injured spinal cord (2004) Neuroscience, 125, pp. 605-614. , 10.1016/j.neuroscience.2004.02.024
  • Gonzalez, S.L., Labombarda, F., Gonzalez Deniselle, M.C., Mougel, A., Guennoun, R., Schumacher, M., Progesterone neuroprotection in spinal cord trauma involves up-regulation of brain-derived neurotrophic factor in motoneurons (2005) J Steroid Biochem Mol Biol, 94, pp. 143-149. , 10.1016/j.jsbmb.2005.01.016
  • Gonzalez Deniselle, M.C., Garay, L., Gonzalez, S.L., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone restores retrograde labelling of cervical motoneurons in Wobbler mouse motoneuron disease (2005) Exp Neurol, 195, pp. 518-523. , 10.1016/j.expneurol.2005.06.015
  • Gonzalez Deniselle, M.C., Garay, L., Gonzalez, S.L., Saravia, F., Labombarda, F., Guennoun, R., Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons (2007) Exp Neurol, 203, pp. 406-414. , 10.1016/j.expneurol.2006.08.019
  • Deniselle González, M.C., López-Costa, J.J., González, S.L., Labombarda, F., Garay, L., Guennoun, R., Basis of progesterone neuroprotection in spinal cord neurodegeneration (2003) J Steroid Biochem Mol Biol, 83, pp. 199-209. , 10.1016/S0960-0760(02)00262-5
  • Grossman, K.J., Goss, C.W., Stein, D.G., Effects of progesterone on the inflammatory response to brain injury in the rat (2004) Brain Res, 1008, pp. 29-39. , 10.1016/j.brainres.2004.02.022
  • Hayashi, T., Sakurai, M., Abe, K., Sadahiro, M., Tabayashi, K., Itoyama, Y., Apoptosis of motor neurons with induction of caspases in the spinal cord after ischemia (1998) Stroke, 29, pp. 1007-1012
  • Hayes, R.L., Yang, K., Whitson, J.S., Postmantur, R., Cytoskeletal derangements following central nervous system injury: Modulation of neurotrophic gene transfection (1995) J Neurotrauma, 2, pp. 933-941
  • Ibanez, C., Shields, S.A., El-Etr, M., Leonelli, E., Magnaghi, V., Li, W.W., Steroids and the reversal of age-associated changes in myelination and remyelination (2003) Prog Neurobiol, 71, pp. 49-56. , 10.1016/j.pneurobio.2003.09.002
  • Jamieson, S.M.F., Liu, J.J., Connor, B., Dragunow, M., McKeage, M.J., Nucleolar enlargement, nuclear eccentricity and altered cell body immunostaining characteristics of large-sized sensory neurons following treatment of rats with paclitaxel (2007) Neurotoxicology, 28, pp. 1092-1098. , 10.1016/j.neuro.2007.04.009
  • Kaur, P., Jodhka, P.K., Underwood, W.A., Bowles, C.A., De Fiebre, N.C., De Fiebre, C.M., Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants (2007) J Neurosci Res, 85, pp. 2441-2449. , 10.1002/jnr.21370
  • Kikuchi, H., Doh-Ura, K., Kawashima, T., Kira, J., Iwaki, T., Immunohistochemical analysis of spinal cord lesions in amyotrophic lateral sclerosis using microtubule-associated protein 2 (MAP2) antibodies (1999) Acta Neuropathol, 97, pp. 13-21. , 10.1007/s004010050950
  • Koenig, H.L., Schumacher, M., Ferzaz, B., Progesterone synthesis and myelin formation by Schwann cells (1995) Science, 268, pp. 1500-1502. , 10.1126/science.7770777
  • Kupina, N.C., Detloff, M.R., Bobrowski, W.F., Snyder, B.J., Hall, E.D., Cytoskeletal protein degradation and neurodegeneration evolves differently in males and females following experimental head injury (2003) Exp Neurol, 180, pp. 55-73. , doi: 10.1016/S0014-4886(02)00048-1
  • Labombarda, F., González, S.L., Gonzalez Deniselle, M.C., Guennoun, R., Schumacher, M., De Nicola, A.F., Cellular basis for progesterone neuroprotection in the injured spinal cord (2002) J Neurotrauma, 19, pp. 343-355. , 10.1089/089771502753594918
  • Labombarda, F., Gonzalez, S., Gonzalez Deniselle, M.C., Vinson, G.P., Schumacher, M., De Nicola, A.F., Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25 Dx in the rat spinal cord (2003) J Neurochem, 87, pp. 902-913. , 10.1046/j.1471-4159.2003.02055.x
  • Labombarda, F., Gonzalez, S., Gonzalez Deniselle, M.C., Garay, L., Guennoun, R., Schumacher, M., Progesterone increases the expression of myelin basic protein and the number of cells showing NG2 immunostaining in the lesioned spinal cord (2006) J Neurotrauma, 23, pp. 181-192. , 10.1089/neu.2006.23.181
  • Labombarda, F., Pianos, A., Liere, P., Eychenne, B., Gonzalez, S., Cambourg, A., Injury elicited increase in spinal cord neurosteroid content analyzed by gas chromatography mass spectrometry (2006) Endocrinology, 147, pp. 1847-1859. , 10.1210/en.2005-0955
  • Leist, M., Jaattela, M., Four deaths and a funeral: From caspases to alternative mechanisms (2001) Nat Rev Mol Cell Biol, 2, pp. 589-598. , 10.1038/35085008
  • Magnaghi, V., Cavarretta, I., Galbiati, M., Martini, L., Melcangi, R.C., Neuroactive steroids and peripheral myelin proteins (2001) Brain Res Brain Res Rev, 37, pp. 360-371. , 10.1016/S0165-0173(01)00140-0
  • Marsh, H.N., Scholz, W.K., Lamballe, F., Klein, R., Nanduri, V., Barbacid, M., Signal transduction events mediated by the BDNF receptor gp 145trkB in primary hippocampal pyramidal cell culture (1993) J Neurosci, 13, pp. 4281-4292
  • McIlwain, D.L., Hoke, V.B., The role of the cytoskeleton in cell body enlargement, increased nuclear eccentricity and chromatolysis in axotomized spinal motor neurons (2005) BMC Neurosci, 6, pp. 1-13. , 10.1186/1471-2202-6-19
  • Melcangi, R.C., Mensah-Nyagan, A.G., Neuroprotective effects of neuroactive steroids in the spinal cord and peripheral nerves (2006) J Mol Neurosci, 28, pp. 1-2. , 10.1385/JMN:28:1:1
  • Miranda, R.C., Sohrabji, F., Toran-Allerand, C.D., Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions (1993) Proc Natl Acad Sci USA, 90, pp. 6439-6443. , 10.1073/pnas.90.14.6439
  • Nacimiento, W., Sappok, T., Brook, G.A., Tóth, L., Schoen, S.W., Noth, J., Structural changes of anterior horn neurons and their synaptic input caudal to low thoracic spinal cord hemisection in the adult rat: A light and electron microscopic study (1995) Acta Neuropathol, 90, pp. 552-564. , 10.1007/BF00318567
  • Patte-Mensah, C., Penning, T.M., Mensah-Nyagan, A.G., Anatomical and cellular localization of neuroactive 5 alpha/3 alpha-reduced steroid-synthesizing enzymes in the spinal cord (2004) J Comp Neurol, 477, pp. 286-299. , 10.1002/cne.20251
  • Price, D.L., Porter, K.R., The response of ventral horn neurons to axonal transection (1972) J Cell Biol, 53, pp. 24-37. , 10.1083/jcb.53.1.24
  • Reyna-Neyra, A., Camacho-Arroyo, I., Ferrera, P., Arias, C., Estradiol and progesterone modify microtubule associated protein 2 content in the rat hippocampus (2002) Brain Res Bull, 58, pp. 607-612. , 10.1016/S0361-9230(02)00829-8
  • Roof, R., Hoffman, S., Stein, D., Progesterone protects against lipid peroxidation following traumatic brain injury in rats (1997) Mol Chem Neuropathol, 31, pp. 1-11. , 10.1007/BF02815156
  • Siegel, S., Castellan, N., (1989) Nonparametric Statistics for Behavioral Sciences, , 2 Singapore McGraw-Hill
  • Sperandio, S., De Belle, I., Bredesen, D.E., An alternative, nonapoptotic form of programmed cell death (2000) Proc Natl Acad Sci USA, 97, pp. 14376-14381. , 10.1073/pnas.97.26.14376
  • Springer, J.E., Azbill, R.D., Kennedy, S.E., George, J., Geddes, J.W., Rapid calpain i activation and cytoskeletal protein degradation following traumatic spinal cord injury: Attenuation with riluzole pretreatment (1997) J Neurochem, 69, pp. 1592-1600
  • Stein, D.G., The case for progesterone (2005) Ann N y Acad Sci, 1052, pp. 152-169. , 10.1196/annals.1347.011
  • Thomas, A., Nockels, R., Pan, H., Shaffrey, C.I., Chopp, M., Progesterone is neuroprotective after acute experimental spinal cord trauma in rats (1999) Spine, 24, pp. 2134-2138. , 10.1097/00007632-199910150-00013
  • Wakayama, I., Morphometry of spinal motor neurons in amyotrophic lateral sclerosis with special reference to chromatolysis and intracytoplasmic inclusion bodies (1992) Brain Res, 586, pp. 12-18. , 10.1016/0006-8993(92)91365-L
  • Wright, D.W., Kellermann, A.L., Hertzberg, V.S., Clark, P.L., Frankel, M., Goldstein, F.C., ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury (2007) Ann Emerg Med, 49, pp. 391-402. , 10.1016/j.annemergmed.2006.07.932
  • Yu, W.R., Westergren, H., Farooque, M., Holtz, A., Olsson, Y., Systemic hypothermia following spinal cord compression injury in the rat: An immunohistochemical study on MAP 2 with special reference to dendrite changes (2000) Acta Neuropathol, 100, pp. 546-552. , 10.1007/s004010000206
  • Zeman, R.J., Peng, H., Etingler, J.D., Clenbuterol retards loss of motor function in motor neuron degeneration mice (2004) Exp Neurol, 187, pp. 460-467. , 10.1016/j.expneurol.2004.03.006
  • Zhang, S.X., Underwood, M., Landfield, A., Huang, F.F., Gison, S., Geddes, J.W., Cytoskeletal disruption following contusion injury to the rat spinal cord (2000) J Neuropathol Exp Neurol, 59, pp. 287-296

Citas:

---------- APA ----------
González, S.L., López-Costa, J.J., Labombarda, F., Deniselle, M.C.G., Guennoun, R., Schumacher, M. & De Nicola, A.F. (2009) . Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury. Cellular and Molecular Neurobiology, 29(1), 27-39.
http://dx.doi.org/10.1007/s10571-008-9291-0
---------- CHICAGO ----------
González, S.L., López-Costa, J.J., Labombarda, F., Deniselle, M.C.G., Guennoun, R., Schumacher, M., et al. "Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury" . Cellular and Molecular Neurobiology 29, no. 1 (2009) : 27-39.
http://dx.doi.org/10.1007/s10571-008-9291-0
---------- MLA ----------
González, S.L., López-Costa, J.J., Labombarda, F., Deniselle, M.C.G., Guennoun, R., Schumacher, M., et al. "Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury" . Cellular and Molecular Neurobiology, vol. 29, no. 1, 2009, pp. 27-39.
http://dx.doi.org/10.1007/s10571-008-9291-0
---------- VANCOUVER ----------
González, S.L., López-Costa, J.J., Labombarda, F., Deniselle, M.C.G., Guennoun, R., Schumacher, M., et al. Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury. Cell. Mol. Neurobiol. 2009;29(1):27-39.
http://dx.doi.org/10.1007/s10571-008-9291-0