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The Journal of Neuroscience, February 1, 2006, 26(5):1551-1561; doi:10.1523/JNEUROSCI.3101-05.2006

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Cellular/Molecular
The Endocannabinoid System Promotes Astroglial Differentiation by Acting on Neural Progenitor Cells

Tania Aguado,¹ Javier Palazuelos,¹ Krisztina Monory,² Nephi Stella,³ Benjamin Cravatt,⁴ Beat Lutz,² Giovanni Marsicano,² Zaal Kokaia,⁵ Manuel Guzmán,¹ and Ismael Galve-Roperh¹

¹Department of Biochemistry and Molecular Biology I, School of Biology, Complutense University, 28040 Madrid, Spain, ²Max-Planck Institute of Psychiatry, 80804 Munich, Germany, ³Department of Pharmacology, Washington University, Seattle, Washington 98195, ⁴The Skaggs Institute for Chemical Biology and Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037, and ⁵Laboratory of Neural Stem Cell Biology, Lund Strategic Research Center for Stem Cell Biology and Cell Therapy, University Hospital, SE-221 84 Lund, Sweden

Correspondence should be addressed to Ismael Galve-Roperh, Biochemistry and Molecular Biology I, School of Biology, Complutense University, Calle Jose Antonio Novais, 28040 Madrid, Spain. Email: igr{at}quim.ucm.es

Endocannabinoids exert an important neuromodulatory role via presynaptic cannabinoid CB₁ receptors and may also participate in the control of neural cell death and survival. The function of the endocannabinoid system has been extensively studied in differentiated neurons, but its potential role in neural progenitor cells remains to be elucidated. Here we show that the CB₁ receptor and the endocannabinoid-inactivating enzyme fatty acid amide hydrolase are expressed, both in vitro and in vivo, in postnatal radial glia (RC2⁺ cells) and in adult nestin type I (nestin⁺GFAP⁺) neural progenitor cells. Cell culture experiments show that CB₁ receptor activation increases progenitor proliferation and differentiation into astroglial cells in vitro. In vivo analysis evidences that, in postnatal CB₁^–/– mouse brain, progenitor proliferation and astrogliogenesis are impaired. Likewise, in adult CB₁-deficient mice, neural progenitor proliferation is decreased but is increased in fatty acid amide hydrolase-deficient mice. In addition, endocannabinoid signaling controls neural progenitor differentiation in the adult brain by promoting astroglial differentiation of newly born cells. These results show a novel physiological role of endocannabinoids, which constitute a new family of signaling cues involved in the regulation of neural progenitor cell function.

Key words: cannabinoid; neural progenitor; proliferation; astrogliogenesis; radial glia; CB₁ receptor

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Received March 4, 2005; revised Nov. 16, 2005; accepted Dec. 21, 2005.

Correspondence should be addressed to Ismael Galve-Roperh, Biochemistry and Molecular Biology I, School of Biology, Complutense University, Calle Jose Antonio Novais, 28040 Madrid, Spain. Email: igr{at}quim.ucm.es

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