Oestrogen regulates mitochondrial respiratory chain enzyme transcription in the mouse spinal cord

Journal of Neuroendocrinology

Volumn 22, Issue 8, 2010, Pages 926-935

  Johann, S ^a   Dahm, M ^a   Kipp, M ^a   Beyer, Cordian ^a   Arnold, S ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Astrocyte; ATP; Mitochondria; Motoneurone; Oestrogen; Respiratory chain; Spinal cord

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESTROGEN RECEPTOR BETA; MITOCHONDRIAL ENZYME; MITOCHONDRIAL RESPIRATORY CHAIN ENZYME; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NUCLEAR RESPIRATORY FACTOR 1; UNCLASSIFIED DRUG; ANTIESTROGEN; DNA BINDING PROTEIN; ESTROGEN; ESTROGEN RECEPTOR; MITOCHONDRIAL PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; C57BL 6 MOUSE; CONTROLLED STUDY; HORMONAL REGULATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; MALE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL GENE; MOTONEURON; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ELECTRON TRANSPORT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CELLS, CULTURED; DNA-BINDING PROTEINS; ELECTRON TRANSPORT; ESTROGEN ANTAGONISTS; ESTROGENS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; NUCLEAR RESPIRATORY FACTOR 1; RECEPTORS, ESTROGEN; SPINAL CORD; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 77954697219     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02006.x     Document Type: Article

References (67)

1. Arnold AP, Breelove SM. Organizational and activational effects of sex steroids on brain and behaviour: a reanalysis. Horm Behav 1985, 19:469-498.
2. Evrard HC. Estrogen synthesis in the spinal dorsal horn: a new central mechanism for the hormonal regulation of pain. Am J Physiol Regul Integr Comp Physiol 2006, 291:R291-R299.
3. Bethea CL, Lu NZ, Gundlah C, Streicher JM. Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 2002, 23:41-100.
4. Wilson MA. GABA physiology: modulation by benzodiazepines and hormones. Crit Rev Neurobiol 1996, 10:1-37.
5. Viña J, Borrás C, Gambini J, Sastre J, Pallardó FV. Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett 2005, 579:2541-2545.
6. Członkowska A, Ciesielska A, Gromadzka G, Kurkowska-Jastrzebska I. Gender differences in neurological disease: role of estrogens and cytokines. Endocrine 2006, 29:243-256.
7. Shulman LM. Gender differences in Parkinson's disease. Gend Med 2007, 4:8-18.
8. Pasinelli P, Brown RH. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Neurosci 2006, 7:710-723.
9. Haverkamp L, Appel V, Appel SH. Natural history of amyotrophic lateral sclerosis in a data-base population. Validation of scoring system and a model for survival prediction. Brain 1995, 118:707-719.
10. Veldink JH, Baer PR, Joosten EA, Otten M, Wokke JH, van den Berg LH. Sexual differences in onset of disease and response to exercise in a transgenic model of ALS. Neuromusc Dis 2003, 13:737-743.
11. Kachadroka S, Hall AM, Niedzielko TL, Chongthammakun S, Floyd CL. Effect of endogenous androgens on 17ß-estradiol-mediated protection after spinal cord injury in male rats. J Neurotrauma 2010, 27:611-626.
12. Yune TY, Park HG, Lee JY, Oh TH. Estrogen-induced Bcl-2 expression after spinal cord injury is mediated through phosphoinositide-3-kinase/Akt-dependent CREB activation. J Neurotrauma 2008, 25:1121-1131.
13. Baron M, Kudin AP, Kunz WS. Mitochondrial dysfunction in neurodegenerative disorders. Biochem Soc Trans 2007, 35:1228-1231.
14. Arnold S, Beyer C. Neuroprotection by estrogen in the brain: the mitochondrial compartment as presumed therapeutic target. J Neurochem 2009, 110:1-11.
15. Celsi F, Pizzo P, Brini M, Leo S, Fotino C, Pinton P, Rizzuto R. Mitochondria, calcium and cell death: a deadly triad in neurodegeneration. Biochim Biophys Acta 2009, 1787:335-344.
16. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003, 552:335-344.
17. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
18. Calabrese V, Scapagnini G, Giuffrida Stella AM, Bates TE, Clark JB. Mitochondrial involvement in brain function and dysfunction: relevance to aging, neurodegenerative disorders and longevity. Neurochem Res 2001, 26:739-764.
19. Misiak M, Beyer C, Arnold S. Gender-specific role of mitochondria in the vulnerability of 6-hydroxydopamine-treated mesencephalic neurons. Biochim Biophys Acta 2010, http://dx.doi.org/10.1016/j.bbabio.2010.04.009, doi:
20. Beal MF. Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 2005, 58:495-505.
21. Simola N, Morelli M, Carta AR. The 6-hydroxydopamine model of Parkinson's disease. Neurotox Res 2007, 11:151-167.
22. Ayala A, Venero JL, Cano J, Machado A. Mitochondrial toxins and neurodegenerative diseases. Front Biosci 2007, 12:986-1007.
23. Singh S, Misiak M, Beyer C, Arnold S. Cytochrome c oxidase isoform IV-2 is involved in 3-nitropropionic acid-induced toxicity in striatal astrocytes. Glia 2009, 57:1480-1491.
24. Pozzi S, Benedusi V, Maggi A, Vegeto E. Estrogen action in neuroprotection and brain inflammation. Ann NY Acad Sci 2006, 1089:302-323.
25. Simpkins JW, Singh M. More than a decade of estrogen neuroprotection. Alzheimers Dement 2008, 4(Suppl 1):S131-S136.
26. Kipp M, Beyer C. Impact of sex steroids on neuroinflammatory processes and experimental multiple sclerosis. Front Neuroendocrinol 2009, 30:188-200.
27. Garcia-Segura LM, Cardona-Gómez GP, Chowen JA, Azcoitia I. Insulin-like growth factor-I receptors and estrogen receptors interact in the promotion of neuronal survival and neuroprotection. J Neurocytol 2000, 29:425-437.
28. Kipp M, Karakaya S, Pawlak J, Araujo-Wright G, Arnold S, Beyer C. Estrogen and the development and protection of nigrostriatal dopaminergic neurons: concerted action of a multitude of signals, protective molecules, and growth factors. Front Neuroendocrinol 2006, 27:376-390.
29. Kipp M, Karakaya S, Johann S, Kampmann E, Mey J, Beyer C. Oestrogen and progesterone reduce lipopolysaccharide-induced expression of tumour necrosis factor-alpha and interleukin-18 in midbrain astrocytes. J Neuroendocrinol 2007, 19:819-822.
30. Gold SM, Voskuhl RR. Estrogen treatment in multiple sclerosis. J Neurol Sci 2009, 286:99-103.
31. Simpkins JW, Yang SH, Sarkar SN, Pearce V. Estrogen actions on mitochondria-physiological and pathological implications. Mol Cell Endocrinol 2008, 290:51-59.
32. Chen JQ, Delannoy M, Cooke C, Yager JD. Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am J Physiol Endocrinol Metab 2004, 286:E1011-E1022.
33. Klinge CM. Estrogenic control of mitochondrial function and biogenesis. J Cell Biochem 2008, 105:1342-1351.
34. Chen JQ, Cammarata PR, Baines CP, Yager JD. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta 2009, 1793:1540-1570.
35. Kajta M, Trotter A, Lasoń W, Beyer C. Effect of NMDA on staurosporine-induced activation of caspase-3 and LDH release in mouse neocortical and hippocampal cells. Brain Res Dev Brain Res 2005, 160:40-52.
36. Johann S, Kampmann E, Denecke B, Arnold S, Kipp M, Mey J, Beyer C. Expression of enzymes involved in the prostanoid metabolism by cortical astrocytes after LPS-induced inflammation. J Mol Neurosci 2008, 34:177-185.
37. Kampmann E, Johann S, van Neerven S, Beyer C, Mey J. Anti-inflammatory effect of retinoic acid on prostaglandin synthesis in cultured cortical astrocytes. J Neurochem 2008, 106:320-332.
38. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 2001, 44:4230-4251.
39. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 2000, 43:4934-4947.
40. Prange-Kiel J, Rune GM. Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 2006, 138:765-772.
41. Morissette M, Le Saux M, D'Astous M, Jourdain S, Al Sweidi S, Morin N, Estrada-Camarena E, Mendez P, Garcia-Segura LM, Di Paolo T. Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 2008, 108:327-338.
42. Mermelstein PG. Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors. J Neuroendocrinol 2009, 21:257-262.
43. Wang X, Simpkins JW, Dykens JA, Cammarata PR. Oxidative damage to human lens epithelial cells in culture: estrogen protection of mitochondrial potential, ATP, and cell viability. Invest Ophthalmol Vis Sci 2003, 44:2067-2075.
44. Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 2005, 68:959-965.
45. Yao M, Nguyen TV, Pike CJ. Estrogen regulates Bcl-w and Bim expression: role in protection against beta-amyloid peptide-induced neuronal death. J Neurosci 2007, 27:1422-1433.
46. Solakidi S, Psarra AM, Nikolaropoulos S, Sekeris CE. Estrogen receptors alpha and beta (ERalpha and ERbeta) and androgen receptor (AR) in human sperm: localization of ERbeta and AR in mitochondria of the midpiece. Hum Reprod 2005, 20:3481-3487.
47. Solakidi S, Psarra AM, Sekeris CE. Differential distribution of glucocorticoid and estrogen receptor isoforms: localization of GRbeta and ERalpha in nucleoli and GRalpha and ERbeta in the mitochondria of human osteosarcoma SaOS-2 and hepatocarcinoma HepG2 cell lines. J Musculoskelet Neuronal Interact 2007, 7:240-245.
48. O'Lone R, Knorr K, Jaffe IZ, Schaffer ME, Martini PG, Karas RH, Bienkowska J, Mendelsohn ME, Hansen U. Estrogen receptors alpha and beta mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species. Mol Endocrinol 2007, 21:1281-1296.
49. Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ, Klinge CM. Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol 2008, 22:609-622.
50. Virbasius JV, Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA 1994, 91:1309-1313.
51. Scarpulla RC. Nuclear activators and co activators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 2002, 1576:1-14.
52. Demonacos CV, Karayanni N, Hatzoglou E, Tsiriyiotis C, Spandidos DA, Sekeris CE. Mitochondrial genes as sites of primary action of steroid hormones. Steroids 1996, 61:226-232.
53. Chen JQ, Eshete M, Alworth WL, Yager JD. Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors alpha and beta to human mitochondrial DNA estrogen response elements. J Cell Biochem 2004, 93:358-373.
54. Brinton RD. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 2008, 31:529-537.
55. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW. Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci USA 2004, 101:4130-4135.
56. Psarra AM, Sekeris CE. Nuclear receptors and other nuclear transcription factors in mitochondria: regulatory molecules in a new environment. Biochim Biophys Acta 2008, 1783:1-11.
57. Chen JQ, Russo PA, Cooke C, Russo IH, Russo J. ERbeta shifts from mitochondria to nucleus during estrogen-induced neoplastic transformation of human breast epithelial cells and is involved in estrogen-induced synthesis of mitochondrial respiratory chain proteins. Biochim Biophys Acta 2007, 1773:1732-1746.
58. Araújo GW, Beyer C, Arnold S. Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J Neuroendocrinol 2008, 20:930-941.
59. Arnold S, de Araújo GW, Beyer C. Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J Mol Endocrinol 2008, 41:289-300.
60. Arevalo MA, Santos-Galindo M, Bellini MJ, Azcoitia I, Garcia-Segura LM. Actions of estrogens on glial cells: implications for neuroprotection. Biochim Biophys Acta 2009, http://dx.doi.org/10.1016/j.bbagen.2009.10.002, doi:
61. Braun A, Dang J, Johann S, Beyer C, Kipp M. Selective regulation of growth factor expression in cultured cortical astrocytes by neuro-pathological toxins. Neurochem Int 2009, 55:610-618.
62. Garcia-Segura LM, Balthazart J. Steroids and neuroprotection: new advances. Front Neuroendocrinol 2009, 30:v-ix.
63. Santagati S, Melcangi RC, Celotti F, Martini L, Maggi A. Estrogen receptor is expressed in different types of glial cells in culture. J Neurochem 1994, 63:2058-2064.
64. Azcoitia I, Sierra A, Garcia-Segura LM. Localization of estrogen receptor beta-immunoreactivity in astrocytes of the adult rat brain. Glia 1999, 26:260-267.
65. Sortino MA, Chisari M, Merlo S, Vancheri C, Caruso M, Nicoletti F, Canonico PL, Copani A. Glia mediates the neuroprotective action of estradiol on beta-amyloid-induced neuronal death. Endocrinology 2004, 145:5080-5086.
66. Dhandapani KM, Brann DW. Role of astrocytes in estrogen-mediated neuroprotection. Exp Gerontol 2007, 42:70-75.
67. Kruman II, Pedersen WA, Springer JE, Mattson MP. ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp Neurol 1999, 160:28-39.