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The Journal of Neuroscience, June 24, 2009, 29(25):7966-7977; doi:10.1523/JNEUROSCI.1054-09.2009

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Development/Plasticity/Repair
GABA-cAMP Response Element-Binding Protein Signaling Regulates Maturation and Survival of Newly Generated Neurons in the Adult Hippocampus

Ravi Jagasia,¹ Kathrin Steib,¹ Elisabeth Englberger,¹ Sabine Herold,¹ Theresa Faus-Kessler,¹ Michael Saxe,² Fred H. Gage,² Hongjun Song,³ and D. Chichung Lie¹

¹Research Group/Adult Neural Stem Cells and Neurogenesis, Institute of Developmental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich-Neuherberg, Germany, ²Laboratory of Genetics, The Salk Institute for Biological Studies, La Jolla, California 92037, and ³Institute for Cell Engineering, Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Correspondence should be addressed to D. Chichung Lie, Research Group/Adult Neural Stem Cells and Neurogenesis, Institute of Developmental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, Ingolstaedter Landstrasse 1, 85764 Munich-Neuherberg, Germany. Email: chichung.lie{at}helmholtz-muenchen.de

Survival and integration of new neurons in the hippocampal circuit are rate-limiting steps in adult hippocampal neurogenesis. Neuronal network activity is a major regulator of these processes, yet little is known about the respective downstream signaling pathways. Here, we investigate the role of cAMP response element-binding protein (CREB) signaling in adult hippocampal neurogenesis. CREB is activated in new granule neurons during a distinct developmental period. Loss of CREB function in a cell-autonomous manner impairs dendritic development, decreases the expression of the neurogenic transcription factor NeuroD and of the neuronal microtubule-associated protein, doublecortin (DCX), and compromises the survival of newborn neurons. In addition, GABA-mediated excitation regulates CREB activation at early developmental stages. Importantly, developmental defects after loss of GABA-mediated excitation can be compensated by enhanced CREB signaling. These results indicate that CREB signaling is a central pathway in adult hippocampal neurogenesis, regulating the development and survival of new hippocampal neurons downstream of GABA-mediated excitation.

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Received March 4, 2009; revised April 30, 2009; accepted May 7, 2009.

Correspondence should be addressed to D. Chichung Lie, Research Group/Adult Neural Stem Cells and Neurogenesis, Institute of Developmental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, Ingolstaedter Landstrasse 1, 85764 Munich-Neuherberg, Germany. Email: chichung.lie{at}helmholtz-muenchen.de

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