Progesterone prevents mitochondrial dysfunction in the spinal cord of wobbler mice

Journal of Neurochemistry

Volumn 122, Issue 1, 2012, Pages 185-195

  Deniselle, Maria Claudia Gonzalez ^a,b   Carreras, Maria Cecilia ^b   Garay, Laura ^a,b   Gargiulo Monachelli, Gisella ^a   Meyer, Maria ^a   Poderoso, Juan Jose ^b   De Nicola, Alejandro F ^a,b  

^a Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

mitochondria; motoneuron degeneration; neuroprotection; progesterone; Wobbler mouse

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CYTOCHROME C OXIDASE; MANGANESE SUPEROXIDE DISMUTASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; PROGESTERONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL ORGANELLE; CERVICAL SPINAL CORD; CONTROLLED STUDY; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; INTRACELLULAR MEMBRANE; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; MOUSE STRAIN; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; SPINAL CORD; WOBBLER MOUSE;

ALBINISM, OCULOCUTANEOUS; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DISEASE MODELS, ANIMAL; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MICE; MICE, MUTANT STRAINS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MOTOR NEURONS; MULTIENZYME COMPLEXES; NADPH DEHYDROGENASE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE SYNTHASE TYPE I; PROGESTERONE; RNA, MESSENGER; RNA-BINDING PROTEINS; SPINAL CORD; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE; VESICULAR TRANSPORT PROTEINS;

EID: 84862173041     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07753.x     Document Type: Article

References (51)

1. Barbeito L. H., Pehar M., Cassina P., Vargas M. R., Peluffo H., Viera L., Estévez A.G., and, Beckman J. S., (2004) A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res. Brain Res. Rev. 47, 263-274. (Pubitemid 39574324)
2. Bastone A., Fumagalli E., Bigini P., Perini P., Bernardinello D., Cagnotto A., Mereghetti I., Curti D., Salmona M., and, Mennini T., (2009) Proteomic profiling of cervical and lumbar spinal cord reveals potential protective mechanisms in the wobbler mouse, a model of motor neuron degeneration. J. Proteome Res. 8, 5229-5240.
3. Boczkowski J., Lisdero C. L., Lanone S., Samb A., Carreras M. C., Boveris A., Aubier M., and, Poderoso J. J., (1999) Endogenous peroxynitrite mediates mitochondrial dysfunction in rat diaphragm during endotoxemia. FASEB J. 13, 1637-1646.
4. Boillée S., Peschanski M., and, Junier M-P., (2003) The Wobbler mouse: a neurodegeneration jigsaw puzzle. Mol. Neurobiol. 28, 65-106. (Pubitemid 38165332)
5. Cardoso S. M., Pereira C., and, Oliveira R., (1999) Mitochondrial function is differentially affected upon oxidative stress. Free Radic. Biol. Med. 26, 3-13.
6. Carreras M. C., Franco M. C., Peralta J. G., and, Poderoso J. J., (2004) Nitric oxide, complex I, and the modulation of mitochondrial reactive species in biology and disease. Mol. Asp. Med. 25, 125-139. (Pubitemid 38401937)
7. Clarke P. G. H., (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181, 195-213. (Pubitemid 20153523)
8. Clowry G. J., and, McHanwell S., (1996) Expression of nitric oxide synthase by motor neurones in the spinal cord of the mutant mouse wobbler. Neurosci. Lett. 215, 177-180. (Pubitemid 26323455)
9. Dave K. R., Bradley W. G., and, Pérez-Pinzõn M. A., (2003a) Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the Wobbler mouse. Exp. Neurol. 182, 412-420. (Pubitemid 36937093)
10. Dave K. R., Prado R., Busto R., Raval A. P., Bradley W. G., Torbati D., and, Pérez-Pinzõn M. A., (2003b) Hyperbaric oxygen therapy protects against mitochondrial dysfunction and delays onset of motor neuron disease in Wobbler mice. Neuroscience 120, 113-120. (Pubitemid 36782636)
11. De Nicola A. F., Labombarda F., Gonzalez Deniselle M. C., Gonzalez S. L., Garay L., Meyer M., Gargiulo G., Guennoun R., and, Schumacher M., (2009) Progesterone neuroprotection in traumatic CNS injury and motoneuron degeneration. Front. Neuroendocrinol. 30, 173-187.
12. Dennis J. S., and, Citron B. A., (2009) Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein. Neuroscience 158, 745-750.
13. Eve D. J., Dennis J. S., and, Citron B. A., (2007) Transcription factor p53 in degenerating spinal cords. Brain Res. 30, 1150: 174-181. (Pubitemid 46702113)
14. Finocchietto P., Franco M. C., Holod S., Gonzalez A. S., Converso D. P., Antico Arciuch V. G., Serra M. P., Poderoso J. J., and, Carreras M. C., (2009) Mitochondrial nitric oxide synthase: a masterpiece of metabolic adaptation, cell growth, transformation and death. Exp. Biol. Med. 234, 1020-1028.
15. Fumagalli E., Bigini P., Barbera S., De Paola M., and, Mennini T., (2006) Riluzole, unlike the AMPA antagonist RPR119990, reduces motor impairment and partially prevents motoneuron death in the wobbler mouse, a model of neurodegenerative disease. Exp. Neurol. 198, 114-128. (Pubitemid 43243750)
16. Giulivi C., Poderoso J. J., and, Boveris A., (1998) Production of nitric oxide by mitochondria. J. Biol. Chem. 273, 11038-11043. (Pubitemid 28204947)
17. Gonzalez Deniselle M. C., Gonzalez S. L., and, De Nicola A. F., (2001) Cellular basis of steroid neuroprotection in the wobbler mouse, a genetic model of motoneuron disease. Cell. Mol. Neurobiol. 21, 237-254. (Pubitemid 32852778)
18. Gonzalez Deniselle M. C., Lõpez-Costa J. J., Saavedra J. P., Pietranera L., Gonzalez S. L., Garay L., Guennoun R., Schumacher M., and, De Nicola A. F., (2002) Progesterone neuroprotection in the Wobbler mouse, a genetic model of spinal cord motor neuron disease. Neurobiol. Dis. 11, 457-468. (Pubitemid 36269130)
19. Gonzalez Deniselle M. C., Garay L., Lõpez-Costa J. J., Gonzalez S., Mougel A., Guennoun R., Schumacher M., and, De Nicola A. F., (2004) Progesterone treatment reduces NADPH-diaphorase/nitric oxide synthase in Wobbler mouse motoneuron disease. Brain Res. 1014, 71-79. (Pubitemid 38798454)
20. Gonzalez Deniselle M. C., Garay L., Gonzalez S., Guennoun R., Schumacher M., and, De Nicola A. F., (2005) Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease. Exp. Neurol. 195, 518-523. (Pubitemid 41297802)
21. Gonzalez Deniselle M. C., Garay L., Gonzalez S., Saravia F., Labombarda F., Guennoun R., Schumacher M., and, De Nicola A. F., (2007) Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons. Exp. Neurol. 203, 406-414. (Pubitemid 46164803)
22. Hantaz-Ambroise D., Blondet B., Murawsky M., and, Rieger F., (1994) Abnormal astrocyte differentiation and defective cellular interactions in wobbler mouse spinal cord. J. Neurocytol. 23, 179-192. (Pubitemid 24105844)
23. Henderson J. T., Javaheri M., Kopko S., and, Roder J. C., (1996) Reduction of lower motor neuron degeneration in wobbler mice by n-acetyl-l-cysteine. J. Neurosci. 16, 7574-7582. (Pubitemid 26389697)
24. Ikeda K., Iwasaki Y., and, Kinoshita M., (1998) Neuronal nitric oxide synthase inhibitor, 7-nitroindazole, delays motor dysfunction and spinal motoneuron degeneration in the wobbler mouse. J. Neurol. Sci. 160, 9-15. (Pubitemid 28473879)
25. Ikeda K., Iwasaki Y., Kinoshita M., Marubuchi S., and, Ono S., (2000) T-588, a novel neuroprotective agent, delays progression of neuromuscular dysfunction in wobbler mouse motoneuron disease. Brain Res. 858, 84-91. (Pubitemid 30105786)
26. Irwin R. W., Yao J., Hamilton R. T., Cadenas E., Brinton R. D., and, Nilsen J., (2008) Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 149, 3167-3175. (Pubitemid 351724522)
27. Laage S., Zobel G., and, Jockusch H., (1988) Astrocyte overgrowth in the brain stem and spinal cord of mice affected by spinal atrophy, wobbler. Dev. Neurosci. 10, 190-198.
28. Linker R. A., Sendtner M., and, Gold R., (2005) Mechanisms of axonal degeneration in EAE-lessons from CNTF and MHC I knockout mice. J. Neurol. Sci. 233, 167-172. (Pubitemid 40804832)
29. Livak K. J., and, Schmittgen T. D., (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CT) Method. Methods 25, 402-408. (Pubitemid 34164012)
30. Martin L. J., (2010) Mitochondrial and cell death mechanisms in neurodegenerative diseases. Pharmaceuticals (Basel) 3, 839-915.
31. McCombe P. A., and, Henderson R. D., (2010) Effects of gender in amyotrophic lateral sclerosis. Gend. Med. 7, 557-570.
32. Melcangi R. C., and, Panzica G., (2009) Neuroactive steroids: an update of their roles in central and peripheral nervous system. Psychoneuroendocrinology 34 (Suppl 1), S1-S8.
33. Meyer M., Gonzalez Deniselle M. C., Garay L. I., Gargiulo-Monachelli G. G., Lima A., Roig P., Guennoun R., Schumacher M., and, De Nicola A. F., (2010) Stage dependent effects of progesterone on motoneurons and glial cells of wobbler mouse spinal cord degeneration. Cell. Mol. Neurobiol. 30, 123-135.
34. Meyer M., Gonzalez Deniselle M. C., Gargiulo-Monachelli G., Garay L. I., Schumacher M., Guennoun R., and, De Nicola A. F., (2012) Progesterone effects on neuronal brain-derived neurotrophic factor and glial cells during progression of Wobbler mouse neurodegeneration. Neuroscience 201, 267-279.
35. Mitsumoto H., and, Bradley W. G., (1982) Murine motor neuron disease (the wobbler mouse): degeneration and regeneration of the lower motor neuron. Brain 105, 811-834. (Pubitemid 13241013)
36. Nieto-Gonzalez J. L., Moser J., Lauritzen M., Schmitt-John T., and, Jensen K., (2011) Reduced GABAergic inhibition explains cortical hyperexcitability in the wobbler mouse model of ALS. Cereb. Cortex 21, 625-635.
37. Pacher P., Beckman J. S., and, Liaudet L., (2007) Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315-424. (Pubitemid 46217686)
38. Palmisano R., Golfi P., Heimann P., Shaw C., Troakes C., Schmitt-John T., and, Bartsch. W., (2011) Endosomal accumulation of APP in wobbler motor neurons reflects impaired vesicle trafficking: Implications for human motor neuron disease. BMC Neurosci. 12, 24.
39. Rathke-Hartlieb S., Schmidt V. C., Jockusch H., Schmitt-John T., and, Bartsch J. W., (1999) Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse. NeuroReport 10, 3411-3416.
40. Robertson C. L., Puskar A., Hoffman G. E., Murphy A. Z., Saraswati M., and, Fiskum G., (1996) Physiologic progesterone reduces mitochondrial dysfunction and hippocampal cell loss after traumatic brain injury in female rats. Exp. Neurol. 197, 235-243.
41. Santoro B., Bigini P., Levandis G., Nobile V., Biggiogera M., Botti F., Mennini T., and, Curti D., (2004) Evidence for chronic mitochondrial impairment in the cervical spinal cord of a murine model of motor neuron disease. Neurobiol. Dis. 17, 349-357. (Pubitemid 39345790)
42. Sayeed I., and, Stein D. G., (2009) Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 175, 219-37.
43. Sayeed I., Parvez S., Wali B., Siemen D., and, Stein D. G., (2009) Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism for better neuroprotective effects of allopregnanolone over progesterone. Brain Res. 1263, 165-173.
44. Schon E. A., and, Przedborski S., (2011) Mitochondria: the next (neurode)generation. Neuron 70, 1033-1053.
45. Staunton L., Jockusch H., and, Ohlendieck K., (2011) Proteomic analysis of muscle affected by motor neuron degeneration: The wobbler mouse model of amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 406, 595-600.
46. Stein D. G., (2011) Progesterone in the treatment of acute traumatic brain injury: a clinical perspective and update. Neuroscience 191, 101-106.
47. Tsuzaka K., Ishiyama T., Pioro E. P., and, Mitsumoto H., (2001) Role of brain-derived neurotrophic factor in wobbler mouse motor neuron disease. Muscle Nerve 24, 474-480. (Pubitemid 32246782)
48. Vincent S. R., and, Kimura H., (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46, 755-784.
49. Wang J. M., Singh C., Liu L., Irwin R. W., Chen S., Chung E. J., Thompson R. F., and, Brinton R. D., (2010) Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 107, 6498-6503.
50. Wharton D. C., and, Tzagoloff A,.(1967) Cytochrome oxidase from beef heart mitochondria, in Methods in Enzymology (, Estabrook R. W., and, Pullman M. E,., eds), Vol 10, pp. 245-250. Academic Press, New York and London.
51. Xu G. P., Dave K. R., Moraes C. T., Busto R., Sick T. B., Bradley W. G., and, Perez-Pinzon M. A., (2001) Dysfunctional mitochondrial respiration in the wobbler mouse brain. Neurosci. Lett. 300, 141-144. (Pubitemid 32168207)