Allopregnanolone increases mature excitatory synapses along dendrites via protein kinase A signaling

Neuroscience

Volumn 305, Issue , 2015, Pages 139-145

  Shimizu, H ^a   Ishizuka, Y ^a   Yamazaki, H ^a   Shirao, T ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Allopregnanolone; Dendritic spine; Drebrin; Excitatory synapse; Protein kinase A; Synaptogenesis

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; AMPA RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DREBRIN; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMINO ACID RECEPTOR BLOCKING AGENT; ELTANOLONE; ENZYME INHIBITOR; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DRUG EFFECT; EMBRYO; ENZYME ACTIVATION; EXCITATORY SYNAPSE; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETIC TRANSFECTION; MALE; MAMMALIAN EMBRYO; METABOLISM; NERVE CELL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEURONS; PREGNANOLONE; SIGNAL TRANSDUCTION; TRANSFECTION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84944520173     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.07.079     Document Type: Article

References (40)

1. Aoki C, Sekino Y, Hanamura K, Fujisawa S, Mahadomrongkul V, Ren Y, Shirao T (2005) Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 483:383-402.
2. Counts SE, Nadeem M, Lad SP, Wuu J, Mufson EJ (2006) Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J Neuropathol Exp Neurol 65:592-601.
3. Counts SE, He B, Nadeem M, Wuu J, ScheffSW, Mufson EJ (2012) Hippocampal drebrin loss in mild cognitive impairment. Neurodegener Dis 10:216-219.
4. Delghandi MP, Johannessen M, Moens U (2005) The cAMP signalling pathway activates CREB through PKA, p38 and MSK1 in NIH 3T3 cells. Cell Signal 17:1343-1351.
5. Duman RS, Aghajanian GK (2012) Synaptic dysfunction in depression: potential therapeutic targets. Science 338:68-72.
6. Duric V, Banasr M, Stockmeier CA, Simen AA, Newton SS, Overholser JC, Jurjus GJ, Dieter L, Duman RS (2013) Altered expression of synapse and glutamate related genes in postmortem hippocampus of depressed subjects. Int J Neuropsychopharmacol 16:69-82.
7. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
8. Feyissa AM, Chandran A, Stockmeier CA, Karolewicz B (2009) Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuropsychopharmacol Biol Psychiatry 33:70-75.
9. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
10. Harigaya Y, Shoji M, Shirao T, Hirai S (1996) Disappearance of actinbinding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J Neurosci Res 43:87-92.
11. Irwin RW, Wang JM, Chen S, Brinton RD (2011) Neuroregenerative mechanisms of allopregnanolone in Alzheimer's disease. Front Endocrinol (Lausanne) 2:117.
12. Ishizuka Y, Shimizu H, Takagi E, Kato M, Yamagata H, Mikuni M, Shirao T (2014) Histone deacetylase mediates the decrease in drebrin cluster density induced by amyloid beta oligomers. Neurochem Int 76:114-121.
13. Kang HJ, Voleti B, Hajszan T, Rajkowska G, Stockmeier CA, Licznerski P, Lepack A, Majik MS, Jeong LS, Banasr M, Son H, Duman RS (2012) Decreased expression of synapse-related genes and loss of synapses in major depressive disorder. Nat Med 18:1413-1417.
14. Kwon HB, Sabatini BL (2011) Glutamate induces de novo growth of functional spines in developing cortex. Nature 474:100-104.
15. Lu CC, Tsai SC (2007) The cyclic AMP-dependent protein kinase A pathway is involved in progesterone effects on calcitonin secretion from TT cells. Life Sci 81:1411-1420.
16. Man HY, Sekine-Aizawa Y, Huganir RL (2007) Regulation of α- amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci U S A 104:3579-3584.
17. Marx CE, Trost WT, Shampine LJ, Stevens RD, Hulette CM, Steffens DC, Ervin JF, Butterfield MI, Blazer DG, Massing MW, Lieberman JA (2006) The neurosteroid allopregnanolone is reduced in prefrontal cortex in Alzheimer's disease. Biol Psychiatry 60:1287-1294.
18. Middei S, Spalloni A, Longone P, Pittenger C, O'Mara SM, Marie H, Ammassari-Teule M (2012) CREB selectively controls learninginduced structural remodeling of neurons. Learn Mem 19:330-336.
19. A receptors during postnatal development. Neuroscience 118:655-666.
20. Mukai H, Hatanaka Y, Mitsuhashi K, Hojo Y, Komatsuzaki Y, Sato R, Murakami G, Kimoto T, Kawato S (2011) Automated analysis of spines from confocal laser microscopy images: application to the discrimination of androgen and estrogen effects on spinogenesis. Cereb Cortex 21:2704-2711.
21. Naylor JC, Kilts JD, Hulette CM, Steffens DC, Blazer DG, Ervin JF, Strauss JL, Allen TB, Massing MW, Payne VM, Youssef NA, Shampine LJ, Marx CE (2010) Allopregnanolone levels are reduced in temporal cortex in patients with Alzheimer's disease compared to cognitively intact control subjects. Biochim Biophys Acta 1801:951-959.
22. Nothdurfter C, Rammes G, Baghai TC, Schüle C, Schumacher M, Papadopoulos V, Rupprecht R (2012) Translocator protein (18 kDa) as a target for novel anxiolytics with a favourable sideeffect profile. J Neuroendocrinol 24:82-92.
23. Pang Y, Dong J, Thomas P (2013) Characterization, neurosteroid binding and brain distribution of human membrane progesterone receptors δ and epsilon (mPRδ and mPRε) and mPRd involvement in neurosteroid inhibition of apoptosis. Endocrinology 154:283-295.
24. 2+ channels are essential for glutamate-mediated CREB phosphorylation and c-fos gene expression in striatal neurons. J Neurosci 19:6348-6359.
25. Rapkin AJ, Morgan M, Goldman L, Brann DW, Simone D, Mahesh VB (1997) Progesterone metabolite allopregnanolone in women with premenstrual syndrome. Obstet Gynecol 90:709-714.
26. Romeo E, Ströhle A, Spalletta G, di Michele F, Hermann B, Holsboer F, Pasini A, Rupprecht R (1998) Effects of antidepressant treatment on neuroactive steroids in major depression. Am J Psychiatry 155:910-913.
27. Sargin D, Mercaldo V, Yiu AP, Higgs G, Han JH, Frankland PW, Josselyn SA (2013) CREB regulates spine density of lateral amygdala neurons: implications for memory allocation. Front Behav Neurosci 7:209.
28. Schüle C, Nothdurfter C, Rupprecht R (2014) The role of allopregnanolone in depression and anxiety. Prog Neurobiol 113:79-87.
29. Schüle C, Romeo E, Uzunov DP, Eser D, di Michele F, Baghai TC, Pasini A, Schwarz M, Kempter H, Rupprecht R (2006) Influence of mirtazapine on plasma concentrations of neuroactive steroids in major depression and on 3alpha-hydroxysteroid dehydrogenase activity. Mol Psychiatry 11:261-272.
30. Sekino Y, Kojima N, Shirao T (2007) Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int 51:92-104.
31. Shingo AS, Kito S (2005) Estradiol induces PKA activation through the putative membrane receptor in the living hippocampal neuron. J Neural Transm 112:1469-1473.
32. Shirao T, Obata K (1986) Immunochemical homology of 3 developmentally regulated brain proteins and their developmental change in neuronal distribution. Brain Res 394:233-244.
33. Singh C, Liu L, Wang JM, Irwin RW, Yao J, Chen S, Henry S, Thompson RF, Brinton RD (2012) Allopregnanolone restores hippocampal-dependent learning and memory and neural progenitor survival in aging 3xTgAD and nonTg mice. Neurobiol Aging 33:1493-1506.
34. Ströhle A, Romeo E, di Michele F, Pasini A, Yassouridis A, Holsboer F, Rupprecht R (2002) GABA(A) receptor-modulating neuroactive steroid composition in patients with panic disorder before and during paroxetine treatment. Am J Psychiatry 159:145-147.
35. Takahashi H, Mizui T, Shirao T (2006) Down-regulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones. J Neurochem 97(Suppl. 1):110-115.
36. Takahashi H, Yamazaki H, Hanamura K, Sekino Y, Shirao T (2009) Activity of the AMPA receptor regulates drebrin stabilization in dendritic spine morphogenesis. J Cell Sci 122:1211-1219.
37. Takahashi H, Sekino Y, Tanaka S, Mizui T, Kishi S, Shirao T (2003) Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J Neurosci 23:6586-6595.
38. Wang JM, Johnston PB, Ball BG, Brinton RD (2005) The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J Neurosci 25:4706-4718.
39. Wang JM, Singh C, Liu L, Irwin RW, Chen S, Chung EJ, Thompson RF, Brinton RD (2010) Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 107:6498-6503.
40. Yamazaki H, Kojima N, Kato K, Hirose E, Iwasaki T, Mizui T, Takahashi H, Hanamura K, Roppongi RT, Koibuchi N, Sekino Y, Mori N, Shirao T (2014) Spikar, a novel drebrin-binding protein, regulates the formation and stabilization of dendritic spines. J Neurochem 128:507-522.