Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury

Cellular and Molecular Neurobiology

Volumn 29, Issue 1, 2009, Pages 27-39

  González, Susana L ^a,b   López Costa, Juan José ^b   Labombarda, Florencia ^a,b   Deniselle, Maria Claudia González ^a,b   Guennoun, Rachida ^c   Schumacher, Michael ^c   De Nicola, Alejandro F ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Universite Paris Sud   (France)

Author keywords

Chromatolysis; Electron microscopy; MAP2; Motoneuron; Neuroprotection; Progesterone; Spinal cord injury

Indexed keywords

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;

EID: 58849088392     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-008-9291-0     Document Type: Article

References (62)

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