Progesterone attenuates several hippocampal abnormalities of the wobbler mouse

Journal of Neuroendocrinology

Volumn 25, Issue 3, 2013, Pages 235-243

  Meyer, M ^a   Gonzalez Deniselle, M C ^a,b   Gargiulo Monachelli, G ^a   Lima, A ^a   Roig, P ^a   Guennoun, R ^c   Schumacher, M ^c   De Nicola, A F ^a,b  

^a CONICET ^*  (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSERM   (France)

Author keywords

Hippocampus; Neuroprotection; Progesterone; Wobbler mouse

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; PROGESTERONE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL DENSITY; CONTROLLED STUDY; DENTATE GYRUS; DRUG PELLET; FEMALE; GENE EXPRESSION REGULATION; GRANULE CELL; HIPPOCAMPAL STRATUM LUCIDUM; HIPPOCAMPUS; HISTOPATHOLOGY; HORMONE ACTION; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; MOUSE STRAIN; NERVE DEGENERATION; NEUROBLAST; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; STRATUM LACUNOSUM MOLECULARE; STRATUM RADIATUM; WOBBLER MOUSE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICE; PROGESTERONE; RNA, MESSENGER;

EID: 84874213437     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12004     Document Type: Article

References (58)

1. Zago S, Poletti B, Morelli C, Doretti A, Silani V. Amyotrophic lateral sclerosis and frontotemporal dementia (ALS-FTD). Arch Ital Biol 2011; 149: 39-56.
2. Geser F, Stein B, Partain M, Elman LB, McCluskey LF, Xie SX, Van Deerlin VM, Kwong LK, Lee VM, Trojanowski JQ. Motor neuron disease clinically limited to the lower motor neuron is a diffuse TDP-43 proteinopathy. Acta Neuropathol 2011; 121: 509-517.
3. Dave KR, Bradley WG, Perez-Pinzon MA. Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the Wobbler mouse. Exp Neurol 2003; 182: 412-420.
4. Xu GP, Dave KR, Moraes CT, Busto R, Sick TJ, Bradley WG, Perez-Pinzon MA. Dysfunctional mitochondrial respiration in the wobbler mouse brain. Neurosci Lett 2001; 300: 141-144.
5. Nieto-Gonzalez JL, Moser J, Lauritzen M, Schmitt-John T, Jensen K. Reduced GABAergic inhibition explains cortical hyperexcitability in the wobbler mouse model of ALS. Cereb Cortex 2011; 21: 625-635.
6. Bonanno G, Fumagalli E, Milanese M, Zappettini S, Mennini T. Release of [3H]D-aspartate induced by K + -stimulation is increased in the cervical spinal cord of the wobbler mouse: a model of motor neuron disease. Neurochem Int 2009; 55: 302-306.
7. Yang WW, Sidman RL, Taksir TV, Treleaven CM, Fidler JA, Cheng SH, Dodge JC, Shihabuddin LS. Relationship between neuropathology and disease progression in the SOD1(G93A) ALS mouse. Exp Neurol 2011; 227: 287-295.
8. Takeda T, Uchihara T, Arai N, Mizutani T, Iwata M. Progression of hippocampal degeneration in amyotrophic lateral sclerosis with or without memory impairment: distinction from Alzheimer disease. Acta Neuropathol 2009; 117: 35-44.
9. Patacchioli FR, Monnazzi P, Scontrini A, Tremante E, Caridi I, Brunetti E, Buttarelli FR, Pontieri FE. Adrenal dysregulation in amyotrophic lateral sclerosis. J Endocrinol Invest 2003; 26: RC23-RC25.
10. González Deniselle MC, Gonzalez S, Piroli G, Ferrini M, Lima AE, De Nicola AF. Glucocorticoid receptors and actions in the spinal cord of the Wobbler mouse, a model for neurodegenerative diseases. J Steroid Biochem Mol Biol 1997; 60: 205-213.
11. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22: 105-122.
12. Reul JM, Sutanto W, van Eekelen JA, Rothuizen J, de Kloet ER. Central action of adrenal steroids during stress and adaptation. Adv Exp Med Biol 1990; 274: 243-256.
13. De Nicola AF, Labombarda F, Deniselle MC, Gonzalez SL, Garay L, Meyer M, Gargiulo G, Guennoun R, Schumacher M. Progesterone neuroprotection in traumatic CNS injury and motoneuron degeneration. Front Neuroendocrinol 2009; 30: 173-187.
14. Koenig HL, Schumacher M, Ferzaz B, Thi AN, Ressouches A, Guennoun R, Jung-Testas I, Robel P, Akwa Y, Baulieu EE. Progesterone synthesis and myelin formation by Schwann cells. Science 1995; 268: 1500-1503.
15. Melcangi RC, Panzica G. Neuroactive steroids: an update of their roles in central and peripheral nervous system. Psychoneuroendocrinology 2009; 34(Suppl 1): S1-S8.
16. Sayeed I, Stein DG. Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog Brain Res 2009; 175: 219-237.
17. Schumacher M, Guennoun R, Stein DG, De Nicola AF. Progesterone: therapeutic opportunities for neuroprotection and myelin repair. Pharmacol Ther 2007; 116: 77-106.
18. Stein DG. Is progesterone a worthy candidate as a novel therapy for traumatic brain injury? Dialogues Clin Neurosci 2011; 13: 352-359.
19. Wang JM, Singh C, Liu L, Irwin RW, Chen S, Chung EJ, Thompson RF, Brinton RD. Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2010; 107: 6498-6503.
20. González Deniselle MC, Lopez-Costa JJ, Saavedra JP, Pietranera L, Gonzalez SL, Garay L, Guennoun R, Schumacher M, De Nicola AF. Progesterone neuroprotection in the Wobbler mouse, a genetic model of spinal cord motor neuron disease. Neurobiol Dis 2002; 11: 457-468.
21. González Deniselle MC, Garay L, Lopez-Costa JJ, Gonzalez S, Mougel A, Guennoun R, Schumacher M, De Nicola AF. Progesterone treatment reduces NADPH-diaphorase/nitric oxide synthase in Wobbler mouse motoneuron disease. Brain Res 2004; 1014: 71-79.
22. González Deniselle MC, Garay L, Gonzalez S, Saravia F, Labombarda F, Guennoun R, Schumacher M, De Nicola AF. Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons. Exp Neurol 2007; 203: 406-414.
23. Meyer M, Gonzalez Deniselle MC, Gargiulo-Monachelli G, Garay LI, Schumacher M, Guennoun R, De Nicola AF. Progesterone effects on neuronal brain-derived neurotrophic factor and glial cells during progression of Wobbler mouse neurodegeneration. Neuroscience 2012; 201: 267-279.
24. Thind KK, Goldsmith PC. Expression of estrogen and progesterone receptors in glutamate and GABA neurons of the pubertal female monkey hypothalamus. Neuroendocrinology 1997; 65: 314-324.
25. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986; 232: 1004-1007.
26. Ge S, Pradhan DA, Ming GL, Song H. GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 2007; 30: 1-8.
27. Rathke-Hartlieb S, Schmidt VC, Jockusch H, Schmitt-John T, Bartsch JW. Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse. NeuroReport 1999; 10: 3411-3416.
28. González Deniselle MC, Garay L, Gonzalez S, Guennoun R, Schumacher M, De Nicola AF. Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease. Exp Neurol 2005; 195: 518-523.
29. Keith BJF, George P. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1997.
30. Liu QR, Lu L, Zhu XG, Gong JP, Shaham Y, Uhl GR. Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res 2006; 1067: 1-12.
31. Wong JY, Liberatore GT, Donnan GA, Howells DW. Expression of brain-derived neurotrophic factor and TrkB neurotrophin receptors after striatal injury in the mouse. Exp Neurol 1997; 148: 83-91.
32. He J, Nixon K, Shetty AK, Crews FT. Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 2005; 21: 2711-2720.
33. Meyer M, Gonzalez Deniselle MC, Garay LI, Monachelli GG, Lima A, Roig P, Guennoun R, Schumacher M, De Nicola AF. Stage dependent effects of progesterone on motoneurons and glial cells of wobbler mouse spinal cord degeneration. Cell Mol Neurobiol 2010; 30: 123-135.
34. de Groot DM, Coenen AJ, Verhofstad A, van Herp F, Martens GJ. In vivo induction of glial cell proliferation and axonal outgrowth and myelination by brain-derived neurotrophic factor. Mol Endocrinol 2006; 20: 2987-2998.
35. Murray PS, Holmes PV. An overview of brain-derived neurotrophic factor and implications for excitotoxic vulnerability in the hippocampus. Int J Pept 2011; 2011: 654085.
36. Sayer FT, Oudega M, Hagg T. Neurotrophins reduce degeneration of injured ascending sensory and corticospinal motor axons in adult rat spinal cord. Exp Neurol 2002; 175: 282-296.
37. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995; 270: 593-598.
38. Schaaf MJ, de Jong J, de Kloet ER, Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 1998; 813: 112-120.
39. Jodhka PK, Kaur P, Underwood W, Lydon JP, Singh M. The differences in neuroprotective efficacy of progesterone and medroxyprogesterone acetate correlate with their effects on brain-derived neurotrophic factor expression. Endocrinology 2009; 150: 3162-3168.
40. Kaur P, Jodhka PK, Underwood WA, Bowles CA, de Fiebre NC, de Fiebre CM, Singh 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. J Neurosci Res 2007; 85: 2441-2449.
41. Morita K, Her S. Progesterone pretreatment enhances serotonin-stimulated BDNF gene expression in rat c6 glioma cells through production of 5alpha-reduced neurosteroids. J Mol Neurosci 2008; 34: 193-200.
42. Ankeny DP, McTigue DM, Guan Z, Yan Q, Kinstler O, Stokes BT, Jakeman LB. Pegylated brain-derived neurotrophic factor shows improved distribution into the spinal cord and stimulates locomotor activity and morphological changes after injury. Exp Neurol 2001; 170: 85-100.
43. Jakeman LB, Wei P, Guan Z, Stokes BT. Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp Neurol 1998; 154: 170-184.
44. Yan Q, Matheson C, Lopez OT, Miller JA. The biological responses of axotomized adult motoneurons to brain-derived neurotrophic factor. J Neurosci 1994; 14: 5281-5291.
45. Laage S, Zobel G, Jockusch H. Astrocyte overgrowth in the brain stem and spinal cord of mice affected by spinal atrophy, wobbler. Dev Neurosci 1988; 10: 190-198.
46. Hantaz-Ambroise D, Jacque C, Ait IA, Parmentier C, Leclerc P, Cambier D, Zadigue G, Rieger F. Specific features of chronic astrocyte gliosis after experimental central nervous system (CNS) xenografting and in Wobbler neurological mutant CNS. Differentiation 2001; 69: 100-107.
47. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, Viera L, Estevez AG, Beckman JS. A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 2004; 47: 263-274.
48. Blondet B, Hantaz-Ambroise D, Ait-Ikhlef A, Cambier D, Murawsky M, Rieger F. Astrocytosis in wobbler mouse spinal cord involves a population of astrocytes which is glutamine synthetase-negative. Neurosci Lett 1995; 183: 179-182.
49. González Deniselle MC, Lavista-Llanos S, Ferrini MG, Lima AE, Roldan AG, De Nicola AF. In vitro differences between astrocytes of control and wobbler mice spinal cord. Neurochem Res 1999; 24: 1535-1541.
50. Julien JP. ALS: astrocytes move in as deadly neighbors. Nat Neurosci 2007; 10: 535-537.
51. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005; 47: 803-815.
52. Liu L, Wang J, Zhao L, Nilsen J, McClure K, Wong K, Brinton RD. Progesterone increases rat neural progenitor cell cycle gene expression and proliferation via extracellularly regulated kinase and progesterone receptor membrane components 1 and 2. Endocrinology 2009; 150: 3186-3196.
53. Pawluski JL, Brummelte S, Barha CK, Crozier TM, Galea LA. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front Neuroendocrinol 2009; 30: 343-357.
54. Tanapat P, Hastings NB, Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 2005; 481: 252-265.
55. Galea LA, Spritzer MD, Barker JM, Pawluski JL. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006; 16: 225-232.
56. Barha CK, Ishrat T, Epp JR, Galea LA, Stein DG. Progesterone treatment normalizes the levels of cell proliferation and cell death in the dentate gyrus of the hippocampus after traumatic brain injury. Exp Neurol 2011; 231: 72-81.
57. Zhang Z, Yang R, Cai W, Bai Y, Sokabe M, Chen L. Treatment with progesterone after focal cerebral ischemia suppresses proliferation of progenitor cells but enhances survival of newborn neurons in adult male mice. Neuropharmacology 2010; 58: 930-939.
58. Schoenfeld TJ, Gould E. Stress, stress hormones, and adult neurogenesis. Exp Neurol 2012; 233: 12-21.