Estradiol modulates translocator protein (tspo) and steroid acute regulatory protein (StAR) via Protein Kinase A (PKA) signaling in hypothalamic astrocytes

Endocrinology

Volumn 155, Issue 8, 2014, Pages 2976-2985

  Chen, Claire ^a   Kuo, John ^a   Wong, Angela ^a,b   Micevych, Paul ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ASTROCYTES; CARRIER PROTEINS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ESTRADIOL; FEMALE; HYPOTHALAMUS; PHOSPHOPROTEINS; PROGESTERONE; RATS; RATS, LONG-EVANS; RECEPTORS, GABA-A; SIGNAL TRANSDUCTION;

EID: 84905040926     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1844     Document Type: Article

References (75)

1. Herbison A. Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill J, ed. Physiology of Reproduction, 3rd Ed. Burlington, MA: Elsevier; 2006:1415-1482.
2. Micevych P, Sinchak K, Mills RH, Tao L, LaPolt P., Lu JK. The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adre-nalectomized rats. Neuroendocrinology. 2003; 78(1):29-35.
3. Micevych P, Bondar G, Kuo J. Estrogen actions on neuroendocrine glia. Neuroendocrinology. 2010; 91(3):211-222.
4. Paaske LK, Micevych PE, Sinchak K. Kisspeptin mediates neuro-progesterone induction of the luteinizing hormone surge. Paper presented at: 95th Annual Meeting of The Endocrine Society; June 15-18, 2013; San Francisco, CA.
5. Micevych P, Sinchak K. Estradiol regulation of progesterone synthesis in the brain. Mol Cell Endocrinol. 2008; 290(1-2):44-50.
6. Micevych P, Sinchak K. Synthesis and function of hypothalamic neuroprogesterone in reproduction. Endocrinology. 2008; 149(6): 2739-2742.
7. Zwain IH, Yen SS. Neurosteroidogenesis in astrocytes, oligoden-drocytes, and neurons of cerebral cortex of rat brain. Endocrinology. 1999; 140(8):3843-3852.
8. Zwain IH, Arroyo A, Amato P, Yen SS. A role for hypothalamic astrocytes in dehydroepiandrosterone and estradiol regulation of gonadotropin-releasing hormone (GnRH) release by GnRH neurons. Neuroendocrinology. 2002; 75(6):375-383.
9. Sinchak K, Mills RH, Tao L, LaPolt P, Lu J.K., Micevych P. Estrogen induces de novo progesterone synthesis in astrocytes. Dev Neurosci. 2003; 25(5):343-348.
10. Chaban VV, Lakhter AJ, Micevych P. A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology. 2004; 145(8):3788-3795.
11. Micevych P, Soma KK, Sinchak K. Neuroprogesterone: key to estrogen positive feedback? Brain Res Rev. 2008; 57(2):470-480.
12. Kuo J, Hariri OR, Bondar G, Ogi J., Micevych P. Membraneestrogen receptor-alpha interacts with metabotropic glutamate receptor type 1a to mobilize intracellular calcium in hypothalamic astrocytes. Endocrinology. 2009; 150(3):1369-1376.
13. Kuo J, Hamid N, Bondar G, Prossnitz E.R., Micevych P. Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes. J Neurosci. 2010; 30(39):12950-12957.
14. Itzhak Y, Baker L, Norenberg MD. Characterization of the peripheral-type benzodiazepine receptors in cultured astrocytes: evidence for multiplicity. Glia. 1993; 9(3):211-218.
15. Papadopoulos V, Baraldi M, Guilarte TR, et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiaz-epine receptor basedon its structure and molecular function. Trends Pharmacol Sci. 2006; 27(8):402-409.
16. Morohaku K, Pelton SH, Daugherty DJ, Butler W.R., Deng W., Selvaraj V. Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology. 2014; 155(1):89-97.
17. Dewing P, Christensen A, Bondar G, Micevych P. Protein kinase C signaling in the hypothalamic arcuate nucleus regulates sexual receptivity in female rats. Endocrinology. 2008; 149(12):5934-5942.
18. Li H, Degenhardt B, Tobin D., Yao ZX, Tasken K, Papadopoulos V. Identification, localization, and function in stero idogenesis of PAP7: a peripheral-type benzodiazepine receptor- and PKA (RIalpha)-as-sociated protein. Mol Endocrinol. 2001; 15(12):2211-2228.
19. Papadopoulos V, Miller WL. Role of mitochondria in steroidogen-esis. Best Pract Res Clin Endocrinol Metab. 2012; 26(6):771-790.
20. Manna PR, Soh JW, Stocco DM. The involvement of specific PKC isoenzymes in phorbol ester-mediated regulation of steroidogenic acute regulatory protein expression and steroid synthesis in mouse Leydig cells. Endocrinology. 2011; 152(1):313-325.
21. Liu J, Rone MB, Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem. 2006; 281(50):38879-38893.
22. Dyson MT, Kowalewski MP, Manna PR, Stocco DM. The differential regulation ofsteroidogenic acute regulatory protein-mediated steroidogenesis by type I and type II PKA in MA-10 cells. Mol Cell Endocrinol. 2009; 300(1-2):94-103.
23. Rone MB, Fan J, Papadopoulos V. Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim Biophys Acta. 2009; 1791(7):646-658.
24. Krsmanovic LZ, Mores N, Navarro CE, Tomi M, Catt KJ. Regulation of Ca2 + -sensitive adenylyl cyclase in gonadotropin-releasing hormone neurons. Mol Endocrinol. 2001; 15(3):429-440.
25. Filardo EJ, Quinn JA, Frackelton AR Jr, Bland KI. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol. 2002; 16(1):70-84.
26. Dominguez R, Dewing P, Kuo J, Micevych P. Membrane-initiated estradiol signaling in immortalized hypothalamic N-38 neurons. Steroids. 2013; 78(6):607-613.
27. Cordey M, Gundimeda U, Gopalakrishna R, Pike CJ. Estrogen activates protein kinase C in neurons: role in neuroprotection. J Neu-rochem. 2003; 84(6):1340-1348.
28. Chen C, Micevych P, Kuo J. Estradiol membrane signaling modulates the translocator protein (TSPO) via protein kinase A (PKA) pathway in hypothalamic astrocytes. Paper presented at: Society for Neuroscience 2013; November 9-13, 2013; San Diego, CA.
29. Bondar G, Kuo J, Hamid N, Micevych P. Estradiol-induced estrogen receptor-alpha trafficking. J Neurosci. 2009; 29(48):15323-15330.
30. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980; 85(3):890-902.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25(4):402-408.
32. Micevych PE, Chaban V, Ogi J, Dewing P., Lu JK, Sinchak K. Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology. 2007; 148(2):782-789.
33. Kallen CB, Arakane F, Christenson LK, Watari H, Devoto L., Strauss JF 3rd. Unveiling the mechanism of action and regulation of the steroidogenic acute regulatory protein. Mol Cell Endocrinol. 1998; 145(1-2):39-45.
34. Whalin ME, Boujrad N, Papadopoulos V, Krueger KE. Studies on the phosphorylation of the 18 kDa mitochondrial benzodiazepine receptor protein. J Recept Res. 1994; 14(3-4):217-228.
35. Papadopoulos V, Brown AS. Role of the peripheral-type benzodiazepine receptor and the polypeptide diazepam binding inhibitor in steroidogenesis. J Steroid Biochem Mol Biol. 1995; 53(1-6):103-110.
36. Micevych P, Sinchak K. Temporal and concentration-dependent oestradiol effects on neural pathways mediating sexual receptivity. J Neuroendocrinol. 2013; 25(11):1012-1023.
37. Gemzell-Danielsson K, Marions L. Mechanisms of action of mifepristone and levonorgestrel when used for emergency contraception. Hum Reprod Update. 2004; 10(4):341-348.
38. Kuo J, Hamid N, Bondar G, Dewing P., Clarkson J, Micevych P. Sex differences in hypothalamic astrocyte response to estradiol stimulation. Biol Sex Differ. 2010; 1(1):7.
39. Fares F, Bar-Ami S, Brandes JM, Gavish M. Changes in the density of peripheral benzodiazepine binding sites in genital organs of the female rat during the oestrous cycle. J Reprod Fertil. 1988; 83(2): 619-625.
40. Bar-Ami S, Amiri Z, Fares F, Gavish M. Modulation of peripheral benzodiazepine receptors in female rat genital organs by various gonadal steroids. Life Sci. 1994; 54(25):1965-1975.
41. Mazurika C, Veenman L, Weizman R, et al. Estradiol modulates uterine 18 kDa translocator protein gene expression in uterus and kidney of rats. Mol Cell Endocrinol. 2009; 307(1-2):43-49.
42. Batarseh A, Papadopoulos V. Regulation of translocator protein 18 kDa (TSPO) expression in health and disease states. Mol Cell Endocrinol. 2010; 327(1-2):1-12.
43. Sprengel R, Werner P, Seeburg PH, et al. Molecular cloning and expression of cDNA encoding a peripheral-type benzodiazepine receptor. J Biol Chem. 1989; 264(34):20415-20421.
44. Soma KK, Alday NA, Hau M, Schlinger BA. Dehydroepiandros-terone metabolism by 3beta-hydroxysteroid dehydrogenase/Del-ta5-Delta4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology. 2004; 145(4):1668-1677.
45. Miller WL. Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol. 2013; 379(1-2):62-73.
46. Arakane F, King SR, Du Y, et al. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J Biol Chem. 1997; 272(51):32656-32662.
47. Arakane F, Sugawara T, Nishino H, et al. Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mito-chondrial import sequence: implications for the mechanism of StAR action. Proc Natl Acad Sci U S. A. 1996; 93(24):13731-13736.
48. West LA, Horvat RD, Roess D.A., Barisas BG, Juengel JL, Niswender GD. Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology. 2001; 142(1):502-505.
49. Hauet T, Yao ZX, Bose HS, et al. Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into leydig cell mitochondria. Mol Endocrinol. 2005; 19(2):540-554.
50. Clark BJ, Wells J, King SR, Stocco DM. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochon-drial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J Biol Chem. 1994; 269(45):28314-28322.
51. Epstein LF, Orme-Johnson NR. Regulation of steroid hormone biosynthesis. Identification of precursors of a phosphoprotein targeted to the mitochondrion in stimulated rat adrenal cortex cells. J Biol Chem. 1991; 266(29):19739-19745.
52. Stocco DM, Sodeman TC. The 30-kDa mitochondrial proteins induced by hormone stimulation in MA-10 mouse Leydig tumor cells are processed from larger precursors. J Biol Chem. 1991; 266(29): 19731-19738.
53. Artemenko IP, Zhao D, Hales DB, Hales K.H., Jefcoate CR. Mito-chondrial processing of newly synthesized steroidogenic acute regulatory protein (StAR), but not total St AR, mediates cholesterol transfer to cytochrome P450 side chain cleavage enzyme in adrenal cells. J Biol Chem. 2001; 276(49):46583-46596.
54. Stocco DM, Clark BJ. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem Pharmacol. 1996; 51(3): 197-205.
55. Furukawa A, Miyatake A, Ohnishi T, Ichikawa Y. Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of St AR, cy-tochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehy-drogenase in the rat brain. J Neurochem. 1998; 71(6):2231-2238.
56. King SR, Manna PR, Ishii T, et al. An essential component insteroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain. J Neurosci. 2002; 22(24):10613-10620.
57. Kim HJ, Park CH, Roh GS, Kang S.S., Cho GJ, Choi WS. Changes of steroidogenic acute regulatory protein mRNA expression in postnatal rat development. Brain Res Dev Brain Res. 2002; 139(2):247-254.
58. Karri S, Dertien JS, Stocco DM, Syapin PJ. Steroidogenic acute regulatory protein expression and pregnenolone synthesis in rat astro-cyte cultures. J Neuroendocrinol. 2007; 19(11):860-869.
59. Braestrup C, Squires RF. Specific benzodiazepine receptors in rat brain characterized by high-affinity (3H)diazepam binding. Proc Natl Acad Sci U S A. 1977; 74(9):3805-3809.
60. Papadopoulos V. Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr Rev. 1993; 14(2):222-240.
61. Jamin N, Neumann JM, Ostuni MA, et al. Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor. Mol Endocrinol. 2005; 19(3):588-594.
62. Li H, Yao Z, Degenhardt B., Teper G, Papadopoulos V. Cholesterol binding at the cholesterol recognition/ interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc Natl Acad Sci U S A. 2001; 98(3):1267-1272.
63. Papadopoulos V, Amri H, Li H, Boujrad N., Vidic B, Garnier M. Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J Biol Chem. 1997; 272(51):32129-32135.
64. Rupprecht R, Papadopoulos V, Rammes G, et al. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nature reviews Drug discovery. 2010; 9(12): 971-988.
65. Rone MB, Midzak AS, Issop L, et al. Identification of a dynamic mitochondrial protein complex driving cholesterol import, trafficking, and metabolism to steroid hormones. Mol Endocrinol. 2012; 26(11):1868-1882.
66. Miller WL, Strauss JF 3rd. Molecular pathology and mechanism of action of the steroidogenic acute regulatory protein, St AR. J Steroid Biochem Mol Biol. 1999; 69(1-6):131-141.
67. Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev. 2011; 32(1):81-151.
68. Daugherty DJ, Selvaraj V, Chechneva OV, Liu X.B., Pleasure DE, Deng W. A TSPO ligand is protective in a mouse model of multiple sclerosis. EMBO Mol Med. 2013; 5(6):891-903.
69. Ferzaz B, Brault E, Bourliaud G, et al. SSR180575(7-chloro-N, N,5-trimethyl-4-oxo-3-phenyl-3, 5-dihydro-4H-pyridazino[4, 5-b]in-dole-1- acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J Pharmacol Exp Ther. 2002; 301(3):1067-1078.
70. Barron AM, Garcia-Segura LM, Caruso D, et al. Ligand for trans-locator protein reverses pathology in a mouse model of Alzheimer's disease. J Neurosci. 2013; 33(20):8891-8897.
71. Costa B, DaPozzo E, Martini C. Translocator proteinasapromising target for novel anxiolytics. Curr Top Med Chem. 2012; 12(4):270-285.
72. Nothdurfter C, Baghai TC, Schüle C, Rupprecht R. Translocator protein (18 kDa) (TSPO) as a therapeutic target for anxiety and neurologic disorders. Eur Arch Psychiatry Clin Neurosci. 2012; 262(SUPPL. 2):S107-S112.
73. Dell'Osso L, Da Pozzo E, Carmassi C, Trincavelli ML, Ciapparelli A, Martini C. Lifetime manic-hypomanic symptoms in post-traumatic stress disorder: relationship with the 18 kDa mitochondrial translocator protein density. Psychiatry Res. 2010; 177(1-2):139-143.
74. Gavish M, Laor N, Bidder M, et al. Altered platelet peripheral-type benzodiazepine receptor in posttraumatic stress disorder. Neuro- psychopharmacology. 1996; 14(3):181-186.
75. Qiu ZK, Zhang LM, Zhao N, et al. Repeated administration of AC-5216, a ligand for the 18 kDa translocator protein, improves behavioral deficits in a mouse model of post-traumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2013; 45:40-46.