Pregnenolone sulfate increases glutamate release at neonatal climbing fiber-to-Purkinje cell synapses

Neuroscience

Volumn 175, Issue , 2011, Pages 24-36

  Zamudio Bulcock, P A ^a   Valenzuela, C F ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

Cerebellar cortex; Climbing fiber; Development; Neurosteroid; Purkinje cell; Synaptic transmission

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BUNGAROTOXIN RECEPTOR; CALCIUM ION; GLUTAMIC ACID; GLYCINE; N METHYL DEXTRO ASPARTIC ACID; PREGNENOLONE SULFATE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM CORTEX; CEREBELLUM VERMIS; CHELATION; CLIMBING FIBER; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME RELEASE; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, NEWBORN; CEREBELLAR CORTEX; GLUTAMIC ACID; ORGAN CULTURE TECHNIQUES; PREGNENOLONE; PRESYNAPTIC TERMINALS; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; TIME FACTORS; UP-REGULATION;

EID: 78951484033     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.11.063     Document Type: Article

References (56)

1. Akk G., Bracamontes J., Steinbach J.H. Pregnenolone sulfate block of GABA(A) receptors: mechanism and involvement of a residue in the M2 region of the alpha subunit. J Physiol 2001, 532:673-684.
2. Albert A.P., Pucovsky V., Prestwich S.A., Large W.A. TRPC3 properties of a native constitutively active Ca2+-permeable cation channel in rabbit ear artery myocytes. J Physiol 2006, 571:361-369.
3. Ango F., di Cristo G., Higashiyama H., Bennett V., Wu P., Huang Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment. Cell 2004, 119:257-272.
4. Bidoret C., Ayon A., Barbour B., Casado M. Presynaptic NR2A-containing NMDA receptors implement a high-pass filter synaptic plasticity rule. Proc Natl Acad Sci U S A 2009, 106:14126-14131.
5. Bosman L.W., Konnerth A. Activity-dependent plasticity of developing climbing fiber-Purkinje cell synapses. Neuroscience 2009, 162:612-623.
6. Bosman L.W., Takechi H., Hartmann J., Eilers J., Konnerth A. Homosynaptic long-term synaptic potentiation of the "winner" climbing fiber synapse in developing Purkinje cells. J Neurosci 2008, 28:798-807.
7. Caldeira J.C., Wu Y., Mameli M., Purdy R.H., Li P.K., Akwa Y., Savage D.D., Engen J.R., Valenzuela C.F. Fetal alcohol exposure alters neurosteroid levels in the developing rat brain. J Neurochem 2004, 90:1530-1539.
8. Cesa R., Strata P. Axonal competition in the synaptic wiring of the cerebellar cortex during development and in the mature cerebellum. Neuroscience 2009, 162:624-632.
9. Chen L., Sokabe M. Presynaptic modulation of synaptic transmission by pregnenolone sulfate as studied by optical recordings. J Neurophysiol 2005, 94:4131-4144.
10. Cline H., Haas K. The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol 2008, 586:1509-1517.
11. Dong Y., Fu Y.M., Sun J.L., Zhu Y.H., Sun F.Y., Zheng P. Neurosteroid enhances glutamate release in rat prelimbic cortex via activation of alpha1-adrenergic and sigma1 receptors. Cell Mol Life Sci 2005, 62:1003-1014.
12. Eilers J., Plant T.D., Marandi N., Konnerth A. GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones. J Physiol 2001, 536:429-437.
13. Gibbs T.T., Russek S.J., Farb D.H. Sulfated steroids as endogenous neuromodulators. Pharmacol Biochem Behav 2006, 84:555.
14. Goel M., Sinkins W.G., Schilling W.P. Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 2002, 277:48303-48310.
15. Grimm C., Kraft R., Sauerbruch S., Schultz G., Harteneck C. Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem 2003, 278:21493-21501.
16. Hartmann J., Dragicevic E., Adelsberger H., Henning H.A., Sumser M., Abramowitz J., Blum R., Dietrich A., Freichel M., Flockerzi V., Birnbaumer L., Konnerth A. TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 2008, 59:392-398.
17. Hige T., Fujiyoshi Y., Takahashi T. Neurosteroid pregnenolone sulfate enhances glutamatergic synaptic transmission by facilitating presynaptic calcium currents at the calyx of Held of immature rats. Eur J Neurosci 2006, 24:1955-1966.
18. Hoffmann A., Grimm C., Kraft R., Goldbaum O., Wrede A., Nolte C., Hanisch U.K., Richter-Landsberg C., Bruck W., Kettenmann H., Harteneck C. TRPM3 is expressed in sphingosine-responsive myelinating oligodendrocytes. J Neurochem 2010, 114:654-665.
19. Huang W.C., Young J.S., Glitsch M.D. Changes in TRPC channel expression during postnatal development of cerebellar neurons. Cell Calcium 2007, 42:1-10.
20. Huang Z.J., Di Cristo G., Ango F. Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci 2007, 8:673-686.
21. Ito-Ishida A., Miura E., Emi K., Matsuda K., Iijima T., Kondo T., Kohda K., Watanabe M., Yuzaki M. Cbln1 regulates rapid formation and maintenance of excitatory synapses in mature cerebellar Purkinje cells in vitro and in vivo. J Neurosci 2008, 28:5920-5930.
22. Ito M. Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann N Y Acad Sci 2002, 978:273-288.
23. Kano M., Hashimoto K. Synapse elimination in the central nervous system. Curr Opin Neurobiol 2009, 19:154-161.
24. Kawa K. Acute synaptic modulation by nicotinic agonists in developing cerebellar Purkinje cells of the rat. J Physiol 2002, 538:87-102.
25. Kawa K. Glycine facilitates transmitter release at developing synapses: a patch clamp study from Purkinje neurons of the newborn rat. Brain Res Dev Brain Res 2003, 144:57-71.
26. Kim S.J., Kim Y.S., Yuan J.P., Petralia R.S., Worley P.F., Linden D.J. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 2003, 426:285-291.
27. Konnerth A., Llano I., Armstrong C.M. Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci U S A 1990, 87:2662-2665.
28. Kraft R., Harteneck C. The mammalian melastatin-related transient receptor potential cation channels: an overview. Pflügers Arch 2005, 451:204-211.
29. Kurihara H., Hashimoto K., Kano M., Takayama C., Sakimura K., Mishina M., Inoue Y., Watanabe M. Impaired parallel fiber->Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor delta2 subunit. J Neurosci 1997, 17:9613-9623.
30. Lee K.H., Cho J.H., Choi I.S., Park H.M., Lee M.G., Choi B.J., Jang I.S. Pregnenolone sulfate enhances spontaneous glutamate release by inducing presynaptic Ca(2+)-induced Ca(2+) release. Neuroscience 2010, 171:106-116.
31. Mameli M., Botta P., Zamudio P.A., Zucca S., Valenzuela C.F. Ethanol decreases Purkinje neuron excitability by increasing GABA release in rat cerebellar slices. J Pharmacol Exp Ther 2008, 327:910-917.
32. Mameli M., Carta M., Partridge L.D., Valenzuela C.F. Neurosteroid-induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors. J Neurosci 2005, 25:2285-2294.
33. Mameli M., Valenzuela C.F. Alcohol increases efficacy of immature synapses in a neurosteroid-dependent manner. Eur J Neurosci 2006, 23:835-839.
34. Mellon S.H. Neurosteroid regulation of central nervous system development. Pharmacol Ther 2007, 116:107-124.
35. Meyer D.A., Carta M., Partridge L.D., Covey D.F., Valenzuela C.F. Neurosteroids enhance spontaneous glutamate release in hippocampal neurons. Possible role of metabotropic sigma1-like receptors. J Biol Chem 2002, 277:28725-28732.
36. Morara S., van der Want J.J., de Weerd H., Provini L., Rosina A. Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience 2001, 108:655-671.
37. Mtchedlishvili Z., Kapur J. A presynaptic action of the neurosteroid pregnenolone sulfate on GABAergic synaptic transmission. Mol Pharmacol 2003, 64:857-864.
38. Naylor J., Li J., Milligan C.J., Zeng F., Sukumar P., Hou B., Sedo A., Yuldasheva N., Majeed Y., Beri D., Jiang S., Seymour V.A., McKeown L., Kumar B., Harteneck C., O'Regan D., Wheatcroft S.B., Kearney M.T., Jones C., Porter K.E., Beech D.J. Pregnenolone sulphate- and cholesterol-regulated TRPM3 channels coupled to vascular smooth muscle secretion and contraction. Circ Res 2010, 106:1507-1515.
39. Nichols R.A., Dengler A.F., Nakagawa E.M., Bashkin M., Paul B.T., Wu J., Khan G.M. A constitutive, transient receptor potential-like Ca2+ influx pathway in presynaptic nerve endings independent of voltage-gated Ca2+ channels and Na+/Ca2+ exchange. J Biol Chem 2007, 282:36102-36111.
40. Ohtsuki G., Hirano T. Bidirectional plasticity at developing climbing fiber-Purkinje neuron synapses. Eur J Neurosci 2008, 28:2393-2400.
41. Perez-Velazquez J.L., Valiante T.A., Carlen P.L. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J Neurosci 1994, 14:4308-4317.
42. Piochon C., Irinopoulou T., Brusciano D., Bailly Y., Mariani J., Levenes C. NMDA receptor contribution to the climbing fiber response in the adult mouse Purkinje cell. J Neurosci 2007, 27:10797-10809.
43. Sasahara K., Shikimi H., Haraguchi S., Sakamoto H., Honda S., Harada N., Tsutsui K. Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J Neurosci 2007, 27:7408-7417.
44. Scelfo B., Strata P. Correlation between multiple climbing fibre regression and parallel fibre response development in the postnatal mouse cerebellum. Eur J Neurosci 2005, 21:971-978.
45. Schiess A.R., Partridge L.D. Pregnenolone sulfate acts through a G-protein-coupled sigma1-like receptor to enhance short term facilitation in adult hippocampal neurons. Eur J Pharmacol 2005, 518:22-29.
46. Schmahmann J.D. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 2004, 16:367-378.
47. Schumacher M., Liere P., Akwa Y., Rajkowski K., Griffiths W., Bodin K., Sjovall J., Baulieu E.E. Pregnenolone sulfate in the brain: a controversial neurosteroid. Neurochem Int 2008, 52:522-540.
48. Selvaraj S., Sun Y., Singh B.B. TRPC channels and their implication in neurological diseases. CNS Neurol Disord Drug Targets 2010, 9:94-104.
49. Servais L., Hourez R., Bearzatto B., Gall D., Schiffmann S.N., Cheron G. Purkinje cell dysfunction and alteration of long-term synaptic plasticity in fetal alcohol syndrome. Proc Natl Acad Sci U S A 2007, 104:9858-9863.
50. Shi L., Smith S.E., Malkova N., Tse D., Su Y., Patterson P.H. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun 2009, 23:116-123.
51. Teschemacher A., Kasparov S., Kravitz E.A., Rahamimoff R. Presynaptic action of the neurosteroid pregnenolone sulfate on inhibitory transmitter release in cultured hippocampal neurons. Brain Res 1997, 772:226-232.
52. Tsutsui K., Sakamoto H., Ukena K. Biosynthesis and action of neurosteroids in the cerebellar Purkinje neuron. J Steroid Biochem Mol Biol 2003, 85:311-321.
53. Tsutsui K., Ukena K. Neurosteroids in the cerebellar Purkinje neuron and their actions (review). Int J Mol Med 1999, 4:49-56.
54. Valenzuela C.F., Partridge L.D., Mameli M., Meyer D.A. Modulation of glutamatergic transmission by sulfated steroids: role in fetal alcohol spectrum disorder. Brain Res Rev 2008, 57:506-519.
55. Wagner T.F., Loch S., Lambert S., Straub I., Mannebach S., Mathar I., Dufer M., Lis A., Flockerzi V., Philipp S.E., Oberwinkler J. Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic beta cells. Nat Cell Biol 2008, 10:1421-1430.
56. Watt A.J., Cuntz H., Mori M., Nusser Z., Sjostrom P.J., Hausser M. Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat Neurosci 2009, 12:463-473.