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Components of Endocannabinoid Signaling System Are Expressed in the Perinatal Mouse Cerebellum and Required for Its Normal Development

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Components of Endocannabinoid Signaling System Are Expressed in the Perinatal Mouse Cerebellum and Required for Its Normal Development Research Article: New Research Development Components of Endocannabinoid Signaling System Are Expressed in the Perinatal Mouse Cerebellum and Required for Its Normal Development Luis Ricardo Martinez,1 Kylie Caroline Black,1 Brynna Tellas Webb,1 Alexandria Bell,1 Shawyon Kevin Baygani,1 Tristen Jay Mier,1 Luis Dominguez,1 Ken Mackie,1 and Anna Kalinovsky1 https://doi.org/10.1523/ENEURO.0471-19.2020 1The Gill Center for Biomolecular Science, Program in Neuroscience, Department of Psychological and Brain Sciences, Indiana University, Bloomington, 47405 IN Visual Abstract March/April 2020, 7(2) ENEURO.0471-19.2020 1–24 Research Article: New Research 2 of 24 Significance Statement In this study, we show that components of the endocannabinoid (eCB) signaling system (ECS) are prominently expressed in the perinatal [embryonic day (E)17.5 to postnatal day (P)14] mouse hindbrain. Our comprehensive characterization highlights developmentally dynamic and spatially restricted expression of cannabinoid receptor 1 (CB1), prominent at birth in pontocerebellar axons, and later in migrating and differentiating anterior vermis granule cells (GCs). We identify the role of Purkinje cells (PCs) in the regulation of eCB 2-arachidonoylglycerol (2-AG) availability, since they express both catabolic and anabolic enzymes diacylglycerol lipase a (DAGLa)and monoacylglycerol lipase (MAGL). Furthermore, we demonstrate a requirement for eCB signaling in the regulation of pontocerebellar axon distribution and of postnatal cerebellar growth. CB1 knock-outs (KOs) exhibit impair- ments in cerebellar-influenced fine-motor, but not gross-motor behaviors. Together, these results illuminate a previously unrecognized role of eCB signaling in the regulation of cerebellar development and function. Endocannabinoid (eCB) signaling system (ECS), encompassing cannabinoid receptors and enzymes involved in the synthesis and degradation of the endogenous cannabinoid signaling lipids, is highly expressed in the cerebellar cortex of adult humans and rodents. In addition to their well-established role in neuromodulation, eCBs have been shown to play key roles in aspects of neurodevelopment in the fore- and mid-brain, including neurogenesis, cell migration, and synapse specification. However, little is known about the role of ECS in cerebellar development. In this study, we conducted immunohistochemical characterization of ECS components through key stages of cere- bellar development in mice using antibodies for 2-arachidonoylglycerol (2-AG) synthetizing and degrading enzymes and the major brain cannabinoid receptor, cannabinoid receptor 1 (CB1), in combination with cerebellar cell markers. Our results reveal a temporally, spatially, and cytologically dynamic pattern of expression. Production, re- ceptor binding, and degradation of eCBs are tightly controlled, thus localization of eCB receptors and the comple- mentary cannabinoid signaling machinery determines the direction, duration, and ultimately the outcome of eCB signaling. To gain insights into the role of eCB signaling in cerebellar development, we characterized gross anat- omy of cerebellar midvermis in CB1 knock-out (CB1 KO) mice, as well as their performance in cerebellar-influ- enced motor tasks. Our results show persistent and selective anatomic and behavioral alterations in CB1 KOs. Consequently, the insights gained from this study lay down the foundation for investigating specific cellular and molecular mechanisms regulated by eCB signaling during cerebellar development. Key words: ataxia; cannabinoid; CB1; cerebellum; coordination; development Introduction Previous studies have shown robust and dynamic ex- pression of the endocannabinoid (eCB) signaling system Received November 13, 2019; accepted February 28, 2020; First published (ECS) during forebrain development, and its requirement March 11, 2020. The authors declare no competing financial interests. in regulation of multiple neurodevelopmental aspects Author contributions: A.K. designed research; K.M. provided critical feedback (Berghuis et al., 2007; Mulder et al., 2008; Vitalis et al., and contributed reagents; L.R.M., K.C.B., B.T.W., A.B., S.K.B., T.J.M., L.D., and 2008; Wu et al., 2010; Oudin et al., 2011; Díaz-Alonso et A.K. performed research; K.C.B., B.T.W., S.K.B., T.J.M., and A.K. analyzed data; al., 2012). However, very little is known about the dynam- L.R.M. and A.K. wrote the paper. This work was supported by the National Institute on Drug Abuse R21 Grant ics of ECS expression, or the role that eCB signaling DA044000 and by a research fund from the Indiana University Department of plays, in the developing hindbrain. Thus, the ubiquity of Psychological and Brain Sciences. the regulatory roles of eCB signaling in neurodevelopment Acknowledgements: We thank the dedicated undergraduate assistants who remains an open question. Furthermore, despite clear evi- contributed to the execution and the discussion of the experiments: Athanasios Liodos, Jacob LaMar, John Justin Hainline, Matthew Awad, Tin Duong, Maxime dence of the key role that eCB signaling plays in the regu- Brunet, Thomas Metcalf, Wesley Cha, Taylor Burke, and Tyler Margetts. This lation of cerebellar synaptic plasticity (Carey et al., 2011), study was initiated following inspiring discussions with our colleagues Dr. Alex the role of eCB signaling in cerebellar development has Straiker and Dr. Natalia Murataeva. We also thank Dr. Carol Mason and Dr. not yet been investigated. In this study, we undertook Alexander Gragerov for their comments on this manuscript, Indiana University Imaging Facility (LMIC) for facilitating access to confocal and slide scanning detailed immunohistochemical characterization of ECS microscopy, and Jim Powers for his invaluable assistance. localization in the perinatal hindbrain followed by charac- Correspondence should be addressed to Anna Kalinovsky at terization of anatomic and behavioral consequences of [email protected] genetic cannabinoid receptor 1 (CB1) ablation. https://doi.org/10.1523/ENEURO.0471-19.2020 Copyright © 2020 Martinez et al. This is an open-access article distributed under the terms of the Creative Cerebellar development Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is The intricate cerebellar cytoarchitecture emerges dur- properly attributed. ing a protracted developmental period (for review, see March/April 2020, 7(2) ENEURO.0471-19.2020 eNeuro.org Research Article: New Research 3 of 24 Sathyanesan et al., 2019). Shortly after the initiation of the development: embryonic day 17.5 (E17.5), P0, P3, P5, P8, cerebellar primordium, granule cell (GC) precursors popu- P10, P12. To elucidate requirements for eCB signaling in late the outer-most layer of the developing cerebellum cerebellar development, we characterized gross anatomic forming the external GC layer (EGL), a secondary prolifer- parameters throughout a developmental time course re- ative zone dedicated to GC production, which persists vealing a persistent reduction in midvermal cerebellar until postnatal day 21 (P21) in mice. Under the EGL, differ- area, accompanied by selective impairments in cerebel- entiating Purkinje cells (PCs) are located in the PC layer lar-controlled motor behaviors in young-adult mice. (PCL). Over the first four postnatal weeks, postmitotic GCs migrate inwards and settle underneath the PCL to seed the inner GC layer (IGL), while their axons form paral- Materials and Methods lel fibers (PFs) and begin to form synapses with dendrites Mice of PCs in the developing molecular layer (ML) above PCL. All mice used in this study were maintained on an out- As the IGL expands, PCs rearrange to form a monolayer bred CD1 genetic background. (around P7). Over the following two postnatal weeks the The CD1 IGS stock was initially acquired from Charles EGL is gradually depleted and disappears, and by P28 River (https://www.criver.com/products-services/find- cerebellar cytoarchitecture and synaptic connectivity model/cd-1r-igs-mouse?region=3611) and a breeding mostly achieves its mature configuration. On the gross colony was maintained in the vivarium with 12/12 h light/ anatomic level, proliferation and maturation of the cere- dark cycle under conditions stipulated by the Institutional bellar cell types is accompanied by cerebellar expansion Animal Care and Use Committee. cb1 À/À mice [CB1 and increasing complexity and refinement of cerebellar knock-out (KO)] used in this study were generated by anatomic and functional subdivisions. (Ledent et al., 1999), acquired from Charles River France and maintained in our facility by HET x HET crosses. Neurodevelopmental disorders associated with Genetic diversity was maintained by replenishing CD1 cerebellar lesions founders from Charles River annually. Mice of both sexes Lesions in the developing cerebella are linked to syn- were used for all experiments. Since we observed no sig- dromes encompassing motor, cognitive, and emotional nificant differences between sexes in expression, anat- deregulation (Koziol et al., 2014). The specific nature of omy or behavior, data are shown for the two sexes the deficits depends on their location within the cerebel- combined for all experiments. lum. Hence, traumatic and malignant lesions in the ante- rior cerebellar vermis and paravermis lead to deficits in Tissue preparation fluid and accurate execution of complex movements in- For embryonic tissue collection pregnant dams were volving
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