BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway

Science Signaling

Volumn 1, Issue 41, 2008, Pages

  Lund, Ingrid V ^a   Hu, Yinghui ^c   Raol, YogendraSinh H ^b   Benham, Rebecca S ^c   Faris, Ramona ^c   Russek, Shelley J ^c   Brooks Kayal, Amy R ^d,e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Children's Hospital Colorado   (United States)

^e CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CREBBP PROTEIN, HUMAN; CREBBP PROTEIN, RAT; CREM PROTEIN, HUMAN; CREM PROTEIN, RAT; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; JANUS KINASE; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN; STAT3 PROTEIN, RAT; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BIOSYNTHESIS; EPILEPSY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPTIC MEMBRANE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CREB-BINDING PROTEIN; CYCLIC AMP RESPONSE ELEMENT MODULATOR; EPILEPSY; GENE EXPRESSION REGULATION; HUMANS; JANUS KINASES; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SYNAPTIC MEMBRANES;

EID: 58149237194     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.1162396     Document Type: Article

References (81)

1. U. Rudolph, H. Mohler, GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr. Opin. Pharmacol. 6, 18-23 (2006).
2. W. Sieghart, Structure, pharmacology, and function of GABAA receptor subtypes. Adv. Pharmacol. 54, 231-263 (2006).
3. A. R. Brooks-Kayal, M. D. Shumate, H. Jin, T. Y. Rikhter, M. E. Kelly, D. A. Coulter, gamma-Aminobutyric acid(A) receptor subunit expression predicts functional changes in hippocampal dentate granule cells during postnatal development. J. Neurochem. 77, 1266-1278 (2001).
4. A. R. Brooks-Kayal, H. Jin, M. Price, M. A. Dichter, Developmental expression of GABA(A) receptor subunit mRNAs in individual hippocampal neurons in vitro and in vivo. J. Neurochem. 70, 1017-1028 (1998).
5. H. Mohler, Molecular recognition of cognitive functions and developmental plasticity: Impact of GABA(A) receptors. J. Neurochem. 102, 1-12 (2007).
6. H. B. Lauren, A. Pitkanen, J. Nissinen, S. L. Soini, E. R. Korpi, I. E. Holopainen, Selective changes in gamma-aminobutyric acid type A receptor subunits in the hippocampus in spontaneously seizing rats with chronic temporal lobe epilepsy. Neurosci. Lett. 349, 58-62 (2003).
7. G. Sperk, S. Furtinger, C. Schwarzer, S. Pirker, GABA and its receptors in epilepsy. Adv. Exp. Med. Biol. 548, 92-103 (2004).
8. H. Mohler, GABAA receptors in central nervous system disease: Anxiety, epilepsy, and insomnia. J. Recept. Signal Transduct. Res. 26, 731-740 (2006).
9. A. R. Brooks-Kayal, M. D. Shumate, H. Jin, T. Y. Rikhter, D. A. Coulter, Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat. Med. 4, 1166-1172 (1998).
10. A. C. Grobin, J. M. Fritschy, A. L. Morrow, Chronic ethanol administration alters immunoreactivity for GABA(A) receptor subunits in rat cortex in a region-specific manner. Alcohol. Clin. Exp. Res. 24, 1137-1144 (2000).
11. H. Shen, Q. H. Gong, C. Aoki, M. Yuan, Y. Ruderman, M. Dattilo, K.Williams, S. S. Smith, Reversal of neurosteroid effects at α4β2δ GABAA receptors triggers anxiety at puberty. Nat. Neurosci. 10, 469-477 (2007).
12. P. Montpied, A. Weizman, R. Weizman, K. A. Kook, A. L. Morrow, S.M. Paul, Repeated swim-stress reduces GABAA receptor alpha subunit mRNAs in the mouse hippocampus. Brain. Res. Mol. Brain. Res. 18, 267-272 (1993).
13. F. C. Hsu, G. Zhang, Y. S. Raol, R. J. Valentino, D. A. Coulter, A. R. Brooks-Kayal, Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc. Natl. Acad. Sci. U.S.A. 100, 12213-12218 (2003).
14. M. Orchinik, N. G. Weiland, B. S. McEwen, Chronic exposure to stress levels of corticosterone alters GABAA receptor subunit mRNA levels in rat hippocampus. Brain. Res. Mol. Brain. Res. 34, 29-37 (1995).
15. Z. Peng, C. S. Huang, B. M. Stell, I. Mody, C. R. Houser, Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J. Neurosci. 24, 8629-8639 (2004).
16. C. Sun, Z. Mtchedlishvili, A. Erisir, J. Kapur, Diminished neurosteroid sensitivity of synaptic inhibition and altered location of the a4 subunit of GABA(A) receptors in an animal model of epilepsy. J. Neurosci. 27, 12641-12650 (2007).
17. N. Zhang, W. Wei, I. Mody, C. R. Houser, Altered localization of GABA(A) receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J. Neurosci. 27, 7520-7531 (2007).
18. A. S. Cohen, D. D. Lin, G. L. Quirk, D. A. Coulter, Dentate granule cell GABA(A) receptors in epileptic hippocampus: Enhanced synaptic efficacy and altered pharmacology. Eur. J. Neurosci. 17, 1607-1616 (2003).
19. G. Zhang, Y. H. Raol, F. C. Hsu, D. A. Coulter, A. R. Brooks-Kayal, Effects of status epilepticus on hippocampal GABAA receptors are age-dependent. Neuroscience 125, 299-303 (2004).
20. Y. H. Raol, I.V. Lund, S. Bandyopadhyay,G. Zhang, D. S. Roberts, J. H. Wolfe, S. J. Russek, A. R. Brooks-Kayal, Enhancing GABA(A) receptor α1 subunit levels in hippocampal dentate gyrus inhibits epilepsy development in an animalmodel of temporal lobe epilepsy. J. Neurosci. 26, 11342-11346 (2006).
21. D. S. Roberts, Y. H. Raol, S. Bandyopadhyay, I. V. Lund, E. C. Budreck, M. A. Passini, J. H. Wolfe, A. R. Brooks-Kayal, S. J. Russek, Egr3 stimulation of GABRA4 promoter activity as a mechanism for seizure-induced up-regulation of GABA(A) receptor α4 subunit expression. Proc. Natl. Acad. Sci. U.S.A. 102, 11894-11899 (2005).
22. D. S. Roberts, Y. Hu, I. V. Lund, A. R. Brooks-Kayal, S. J. Russek, Brain-derived neurotrophic factor (BDNF)-induced synthesis of early growth response factor 3 (Egr3) controls the levels of type A GABA receptor α4 subunits in hippocampal neurons. J. Biol. Chem. 281, 29431-29435 (2006).
23. Y. Hu, I. V. Lund, M. C. Gravielle, D. H. Farb, A. R. Brooks-Kayal, S. J. Russek, Surface expression of GABA (A) receptors is transcriptionally controlled by the interplay of CREB and its binding partner ICER. J. Biol. Chem. 283, 9328-9340 (2008).
24. M. R. Montminy, K. A. Sevarino, J. A. Wagner, G. Mandel, R. H. Goodman, Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl. Acad. Sci. U.S.A. 83, 6682-6686 (1986).
25. B. E. Lonze, D. D. Ginty, Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623 (2002).
26. A. J. Shaywitz, M. E. Greenberg, CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861 (1999).
27. M. Sheng, M. E. Greenberg, The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4, 477-485 (1990).
28. D. A. Frank, M. E. Greenberg, CREB: A mediator of long-term memory from mollusks to mammals. Cell 79, 5-8 (1994).
29. B. Mayr, M. Montminy, Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609 (2001).
30. J. C. Chrivia, R. P. Kwok, N. Lamb, M. Hagiwara, M. R. Montminy, R. H. Goodman, Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859 (1993).
31. G. A. Gonzalez, M. R. Montminy, Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675-680 (1989).
32. C. A. Molina, N. S. Foulkes, E. Lalli, P. Sassone-Corsi, Inducibility and negative autoregulation of CREM: An alternative promoter directs the expression of ICER, an early response repressor. Cell 75, 875-886 (1993).
33. N. S. Foulkes, E. Borrelli, P. Sassone-Corsi, CREM gene: Use of alternative DNAbinding domains generates multiple antagonists of camp-induced transcription. Cell 64, 739-749 (1991).
34. J. Jaworski, B. Mioduszewska, A. Sanchez-Capelo, I. Figiel, A. Habas, A. Gozdz, T. Proszynski, M. Hetman, J. Mallet, L. Kaczmarek, Inducible camp early repressor, an endogenous antagonist of camp responsive element-binding protein, evokes neuronal apoptosis in vitro. J. Neurosci. 23, 4519-4526 (2003).
35. B. Mioduszewska, J. Jaworski, L. Kaczmarek, Inducible camp early repressor (ICER) in the nervous system - A transcriptional regulator of neuronal plasticity and programmed cell death. J. Neurochem. 87, 1313-1320 (2003).
36. L. R. Fitzgerald, V. A. Vaidya, R. Z. Terwilliger, R. S. Duman, Electroconvulsive seizure increases the expression of CREM (cyclic AMP response element modulator) and ICER (inducible cyclic AMP early repressor) in rat brain. J. Neurochem. 66, 429-432 (1996).
37. A. N. Moore, M. N. Waxham, P. K. Dash, Neuronal activity increases the phosphorylation of the transcription factor camp response element-binding protein (CREB) in rat hippocampus and cortex. J. Biol. Chem. 271, 14214-14220 (1996).
38. B. Lee, H. Dziema, K. H. Lee, Y. S. Choi, K. Obrietan, CRE-mediated transcription and COX-2 expression in the pilocarpine model of status epilepticus. Neurobiol. Dis. 25, 80-91 (2007).
39. K. Q. Tanis, R. S. Duman, S. S. Newton, CREB binding and activity in brain: Regional specificity and induction by electroconvulsive seizure. Biol. Psychiatry 63, 710-720 (2008).
40. B. E. Porter, I. V. Lund, F. P. Varodayan, R. W. Wallace, J. A. Blendy, The role of transcription factors cyclic-AMP responsive element modulator (CREM) and inducible cyclic-AMP early repressor (ICER) in epileptogenesis. Neuroscience 152, 829-836 (2008).
41. R. A. Bender, J. C. Lauterborn, C. M. Gall, W. Cariaga, T. Z. Baram, Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation. Eur. J. Neurosci. 13, 679-686 (2001).
42. A. H. Lagrange, E. J. Botzolakis, R. L. Macdonald, Enhanced macroscopic desensitization shapes the response of α4 subtype-containing GABAA receptors to synaptic and extrasynaptic GABA. J. Physiol. 578, 655-676 (2007).
43. C. Schwarzer, K. Tsunashima, C. Wanzenbock, K. Fuchs, W. Sieghart, G. Sperk, GABA(A) receptor subunits in the rat hippocampus II: Altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience 80, 1001-1017 (1997).
44. G. Sperk, C. Schwarzer, K. Tsunashima, S. Kandlhofer, Expression of GABA(A) receptor subunits in the hippocampus of the rat after kainic acid-induced seizures. Epilepsy Res. 32, 129-139 (1998).
45. S. J. Moss, T. G. Smart, Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240-250 (2001).
46. C. Essrich, M. Lorez, J. A. Benson, J. M. Fritschy, B. Luscher, Postsynaptic clustering of major GABAA receptor subtypes requires the g2 subunit and gephyrin. Nat. Neurosci. 1, 563-571 (1998).
47. D. K. Binder, M. J. Routbort, J. O. McNamara, Immunohistochemical evidence of seizureinduced activation of trk receptors in the mossy fiber pathway of adult rat hippocampus. J. Neurosci. 19, 4616-4626 (1999).
48. J. S. Rudge, P. E. Mather, E. M. Pasnikowski, N. Cai, T. Corcoran, A. Acheson, K. Anderson, R. M. Lindsay, S. J. Wiegand, Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Exp. Neurol. 149, 398-410 (1998).
49. G.Mudo, X. H. Jiang, T. Timmusk,M. Bindoni, N. Belluardo, Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine. Epilepsia 37, 198-207 (1996).
50. C. A. Altar, P. Laeng, L.W. Jurata, J. A. Brockman, A. Lemire, J. Bullard, Y. V. Bukhman, T. A. Young, V. Charles, M. G. Palfreyman, Electroconvulsive seizures regulate gene expression of distinct neurotrophic signaling pathways. J. Neurosci. 24, 2667-2677 (2004).
51. J. O. McNamara, Y. Z. Huang, A. S. Leonard, Molecular signaling mechanisms underlying epileptogenesis. Sci. STKE 2006, re12 (2006).
52. L. A. O'Neill, Targeting signal transduction as a strategy to treat inflammatory diseases. Nat. Rev. Drug Discov. 5, 549-563 (2006).
53. I. L. Campbell, Cytokine-mediated inflammation, tumorigenesis, and disease-associated JAK/STAT/SOCS signaling circuits in the CNS. Brain Res. Brain Res. Rev. 48, 166-177 (2005).
54. J. E.Thompson,R.M.Cubbon, R.T.Cummings, L.S.Wicker,R.Frankshun,B.R. Cunningham, P. M. Cameron, P. T. Meinke, N. Liverton et al., Photochemical preparation of a pyridone containing tetracycle:AJak protein kinase inhibitor. Bioorg. Med. Chem. Lett. 12, 1219-1223 (2002).
55. L. L. Devaud, J. M. Fritschy, W. Sieghart, A. L. Morrow, Bidirectional alterations of GABA(A) receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J. Neurochem. 69, 126-130 (1997).
56. P. Montpied, E. I. Ginns, B. M. Martin, D. Roca, D. H. Farb, S. M. Paul, gamma- Aminobutyric acid (GABA) induces a receptor-mediated reduction in GABAA receptor alpha subunit messenger RNAs in embryonic chick neurons in culture. J. Biol. Chem. 266, 6011-6014 (1991).
57. C. Henneberger, R. Juttner, S. A. Schmidt, J. Walter, J. C. Meier, T. Rothe, R. Grantyn, GluR- and TrkB-mediated maturation of GABA receptor function during the period of eye opening. Eur. J. Neurosci. 21, 431-440 (2005).
58. E. Sibille, C. Pavlides, D. Benke, M. Toth, Genetic inactivation of the serotonin(1A) receptor in mice results in downregulation of major GABA(A) receptor alpha subunits, reduction of GABA(A) receptor binding, and benzodiazepine-resistant anxiety. J. Neurosci. 20, 2758-2765 (2000).
59. M. J. Brown, D. R. Bristow, Molecular mechanisms of benzodiazepine- induced downregulation of GABAA receptor α1 subunit protein in rat cerebellar granule cells. Br. J. Pharmacol. 118, 1103-1110 (1996).
60. C. A. McClung, E. J. Nestler, Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci. 6, 1208-1215 (2003).
61. D. R. Kaplan, F. D. Miller, Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391 (2000).
62. R. A. Segal, M. E. Greenberg, Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463-489 (1996).
63. E. J. Huang, L. F. Reichardt, Trk receptors: Roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642 (2003).
64. R. A. Segal, Selectivity in neurotrophin signaling: Theme and variations. Annu. Rev. Neurosci. 26, 299-330 (2003).
65. J. S. Choi, S. Y. Kim,H. J. Park, J. H. Cha, Y. S. Choi, J. E. Kang, J.W.Chung, M. H. Chun, M. Y. Lee, Upregulation of gp130 and differential activation of STAT and p42/44 MAPK in the rat hippocampus following kainic acid-induced seizures. Brain Res. Mol. Brain Res. 119, 10-18 (2003).
66. S. Suzuki, K. Tanaka, S. Nogawa, T. Dembo, A. Kosakai, Y. Fukuuchi, Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Exp. Neurol. 170, 63-71 (2001).
67. A. M. Planas, M. A. Soriano, M. Berruezo, C. Justicia, A. Estrada, S. Pitarch, I. Ferrer, Induction of Stat3, a signal transducer and transcription factor, in reactive microglia following transient focal cerebral ischaemia. Eur. J. Neurosci. 8, 2612-2618 (1996).
68. J. E. Darnell Jr., I. M. Kerr, G. R. Stark, Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421 (1994).
69. Z. Zhong, Z. Wen, J. Darnell, STAT3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264, 95-98 (1994).
70. Z. Zhong, Z. Wen, J. Darnell, STAT3 and STAT4: Members of the family of signal transducers and activators of transcription. Proc. Natl. Acad. Sci. U.S.A. 91, 4806-4810 (1994).
71. C. Schindler, J. E. Darnell Jr., Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu. Rev. Biochem. 64, 621-651 (1995).
72. J. N. Ihle, STATs: Signal transducers and activators of transcription. Cell 84, 331-334 (1996).
73. D. S. Aaronson, C. M. Horvath, A road map for those who don't know JAK-STAT. Science 296, 1653-1655 (2002).
74. A. J. Bella, G. Lin, K. Tantiwongse, M. Garcia, C. S. Lin,W. Brant, T. F. Lue, Brain-derived neurotrophic factor (BDNF) acts primarily via the JAK/STAT pathway to promote neurite growth in the major pelvic ganglion of the rat: Part I. J. Sex. Med. 3, 815-820 (2006).
75. J. Kapur, Hippocampal neurons express GABAA receptor insensitive to diazepam in hyperexcitable conditions. Epilepsia 41 Suppl 6, S86-S89 (2000).
76. F. C. Hsu, R. Waldeck, D. S. Faber, S. S. Smith, Neurosteroid effects on GABAergic synaptic plasticity in hippocampus. J. Neurophysiol. 89, 1929-1940 (2003).
77. P. B. Shieh, A. Ghosh, Molecular mechanisms underlying activity-dependent regulation of BDNF expression. J. Neurobiol. 41, 127-134 (1999).
78. N. Kojima, G. Borlikova, T. Sakamoto, K. Yamada, T. Ikeda, S. Itohara, H. Niki, S. Endo, Inducible camp early repressor acts as a negative regulator for kindling epileptogenesis and long-term fear memory. J. Neurosci. 28, 6459-6472 (2008).
79. R. J. Racine, Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294 (1972).
80. Y. H. Raol, G. Zhang, I. V. Lund, B. E. Porter, M. A. Maronski, A. R. Brooks-Kayal, Increased GABA(A)-receptor alpha1-subunit expression in hippocampal dentate gyrus after early-life status epilepticus. Epilepsia 47, 1665-1673 (2006).
81. V. Drewett, H. Molina, A. Millar, S. Muller, F. von Hesler, P. E. Shaw, DNA-bound transcription factor complexes analysed by mass-spectrometry: Binding of novel proteins to the human c-fos SRE and related sequences. Nucleic Acids. Res. 29, 479-487 (2001).