A synthetic synaptic organizer protein restores glutamatergic neuronal circuits
Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also perturb the excitatory-inhibitory neurotransmission balance and trigger neuropsychiatric and neurological disorders. Molecular tools to rest...
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| Published in | Science (American Association for the Advancement of Science) Vol. 369; no. 6507 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
28.08.2020
American Association for the Advancement of Science (AAAS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also perturb the excitatory-inhibitory neurotransmission balance and trigger neuropsychiatric and neurological disorders. Molecular tools to restore this balance are highly desirable. Here, we designed and characterized CPTX, a synthetic synaptic organizer combining structural elements from cerebellin-1 and neuronal pentraxin-1. CPTX can interact with presynaptic neurexins and postsynaptic AMPA-type ionotropic glutamate receptors and induced the formation of excitatory synapses both in vitro and in vivo. CPTX restored synaptic functions, motor coordination, spatial and contextual memories, and locomotion in mouse models for cerebellar ataxia, Alzheimer's disease, and spinal cord injury, respectively. Thus, CPTX represents a prototype for structure-guided biologics that can efficiently repair or remodel neuronal circuits. |
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| AbstractList | Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also perturb the excitatory/inhibitory neurotransmission balance and trigger neuropsychiatric and neurological disorders. Molecular tools to restore this balance are highly desirable. Here, we designed and characterized CPTX, a synthetic synaptic organizer combining structural elements from cerebellin-1 and neuronal pentraxin-1. CPTX can interact with presynaptic neurexins and postsynaptic AMPA-type ionotropic glutamate receptors and induced the formation of excitatory synapses both in vitro and in vivo. CPTX restored synaptic functions, motor coordination, spatial and contextual memories, and locomotion in mouse models for cerebellar ataxia, Alzheimer’s disease and spinal cord injury, respectively. Thus, CPTX represents a prototype for structure-guided biologics that can efficiently repair or remodel neuronal circuits. The human brain contains trillions of synapses within a vast network of neurons. Synapse remodeling is essential to ensure the efficient reception and integration of external stimuli and to store and retrieve information. Building and remodeling of synapses occurs throughout life under the control of synaptic organizer proteins. Errors in this process can lead to neuropsychiatric or neurological disorders. Suzuki et al. combined structural elements of natural synaptic organizers to develop an artificial version called CPTX, which has different binding properties (see the Perspective by Salinas). CPTX could act as a molecular bridge to reconnect neurons and restore excitatory synaptic function in animal models of cerebellar ataxia, familial Alzheimer's disease, and spinal cord injury. The findings illustrate how structure-guided approaches can help to repair neuronal circuits. Science , this issue p. eabb4853 ; see also p. 1052 A synthetic protein can induce functional synapses and restore normal behaviors in mouse models of neurological disease. Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also perturb the excitatory–inhibitory neurotransmission balance and trigger neuropsychiatric and neurological disorders. Molecular tools to restore this balance are highly desirable. Here, we designed and characterized CPTX, a synthetic synaptic organizer combining structural elements from cerebellin-1 and neuronal pentraxin-1. CPTX can interact with presynaptic neurexins and postsynaptic AMPA-type ionotropic glutamate receptors and induced the formation of excitatory synapses both in vitro and in vivo. CPTX restored synaptic functions, motor coordination, spatial and contextual memories, and locomotion in mouse models for cerebellar ataxia, Alzheimer’s disease, and spinal cord injury, respectively. Thus, CPTX represents a prototype for structure-guided biologics that can efficiently repair or remodel neuronal circuits. Synthetic excitatory synaptic organizerThe human brain contains trillions of synapses within a vast network of neurons. Synapse remodeling is essential to ensure the efficient reception and integration of external stimuli and to store and retrieve information. Building and remodeling of synapses occurs throughout life under the control of synaptic organizer proteins. Errors in this process can lead to neuropsychiatric or neurological disorders. Suzuki et al. combined structural elements of natural synaptic organizers to develop an artificial version called CPTX, which has different binding properties (see the Perspective by Salinas). CPTX could act as a molecular bridge to reconnect neurons and restore excitatory synaptic function in animal models of cerebellar ataxia, familial Alzheimer's disease, and spinal cord injury. The findings illustrate how structure-guided approaches can help to repair neuronal circuits.Science, this issue p. eabb4853; see also p. 1052INTRODUCTIONSynapses are fundamental structural and functional units within neural circuits, where they define the connectivity between neurons and provide avenues for communication. At a molecular level, synapses are highly dynamic and their remodeling is essential for all aspects of brain physiology. However, errors in this process can happen and often lead to an imbalance of excitatory and inhibitory signaling. This is thought to be a major cause of neuropsychiatric or neurological disorders, including autism spectrum disorders, epilepsy, schizophrenia, and Alzheimer’s disease. Thus, molecular tools to control the number and/or function of synapses would be highly desirable. Physiologically, synapse formation is driven by synaptic organizer proteins. Among these, extracellular scaffolding proteins (ESPs) such as cerebellin-1 (Cbln1) and neuronal pentraxin-1 (NP1) are distinctive in that they could rapidly induce synapse differentiation by binding pre- and/or postsynaptic cell surface proteins at the synaptic cleft. We hypothesized that synthetic molecules that would combine structural features of Cbln1 and NP1 could be used to efficiently reverse the loss of excitatory synapses and promote the structural and functional recovery of damaged neuronal circuits in animal models of neurological disease.RATIONALENP1 recruits postsynaptic AMPA-subtype ionotropic glutamate receptors (AMPARs), responsible for excitatory neurotransmission, through its pentraxin domain. However, NP1 does not seem to induce presynaptic specializations in vivo. By contrast, Cbln1 promotes presynaptic differentiation by interacting with the cell adhesion molecule neurexin (Nrx) through its N-terminal multimerization domain, but cannot bind AMPARs. Guided by structural information, we developed a hexameric synthetic soluble ESP, termed CPTX, which includes the multimerization domain of Cbln1 and the pentraxin domain of NP1. We hypothesized that CPTX should induce Nrx–CPTX–AMPAR transsynaptic molecular bridges, and thus accumulate and align presynaptic vesicle release machinery and postsynaptic neurotransmitter receptors.RESULTSRecombinant CPTX selectively bound presynaptic Nrx containing the spliced sequence 4 [Nrx(+4)] with nanomolar affinity and most AMPAR subtypes with micromolar affinity. When administered to cerebellar granule cells and hippocampal neurons in vitro, CPTX acted as a bidirectional synapse organizer and induced excitatory pre- and postsynaptic sites. In vivo, CPTX increased the number of functional excitatory synapses and improved gait performance upon injection into the cerebellum of the ataxic Cbln1-null and GluD2-null mice. Furthermore, when injected into the hippocampus of 5xFAD mice, a model of familial Alzheimer’s disease, CPTX restored dendritic spine numbers, excitatory synaptic transmission, and long-term potentiation and improved hippocampus-dependent learning. Finally, in mouse models of spinal cord injury, single injections of CPTX into the damaged tissue were sufficient to reorganize excitatory circuits and restore locomotion for more than 7 to 8 weeks.CONCLUSIONWe developed a synthetic, structure-guided, synaptic organizer termed CPTX, which induced functional and structural excitatory synapses in the cerebellar, hippocampal, and spinal cord neuronal circuits in vivo. Molecular components involved in excitatory synapses are considerably different among neuronal circuits. Rationally designed ESPs targeting distinct pre- and postsynaptic molecules may be useful to modulate neural circuit connectivity. This approach may inspire the development of a variety of innovative molecular tools for basic neuroscience as well as the treatment of neurological disorders.Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also perturb the excitatory–inhibitory neurotransmission balance and trigger neuropsychiatric and neurological disorders. Molecular tools to restore this balance are highly desirable. Here, we designed and characterized CPTX, a synthetic synaptic organizer combining structural elements from cerebellin-1 and neuronal pentraxin-1. CPTX can interact with presynaptic neurexins and postsynaptic AMPA-type ionotropic glutamate receptors and induced the formation of excitatory synapses both in vitro and in vivo. CPTX restored synaptic functions, motor coordination, spatial and contextual memories, and locomotion in mouse models for cerebellar ataxia, Alzheimer’s disease, and spinal cord injury, respectively. Thus, CPTX represents a prototype for structure-guided biologics that can efficiently repair or remodel neuronal circuits. |
| Author | Miura, Eriko Shimada, Tatsuya Takeuchi, Yuka Ferrer-Ferrer, Maura Chang, Veronica T Watanabe, Masahiko Aricescu, A Radu Stoyanov, Stoyan Takeuchi, Kosei Yuzaki, Michisuke Senkov, Oleg Matsuda, Keiko Song, Inseon Morioka, Yuki Elegheert, Jonathan Kakegawa, Wataru Kaushik, Rahul Otsuka, Shintaro Sasakura, Hiroyuki Clayton, Amber J Ikeno, Masashi Dityatev, Alexander Suzuki, Kunimichi |
| AuthorAffiliation | 3 Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany 7 Center for Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany 1 Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan 6 Medical Faculty, Otto-von-Guericke-University, 39120 Magdeburg, Germany 8 Department of Anatomy, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan 5 Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK 4 Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan 2 Division of Structural Biology, University of Oxford, Oxford OX3 7BN, UK |
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| Author_xml | – sequence: 1 givenname: Kunimichi orcidid: 0000-0001-7699-2163 surname: Suzuki fullname: Suzuki, Kunimichi organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 2 givenname: Jonathan surname: Elegheert fullname: Elegheert, Jonathan organization: Division of Structural Biology, University of Oxford, Oxford OX3 7BN, UK – sequence: 3 givenname: Inseon orcidid: 0000-0003-1739-5566 surname: Song fullname: Song, Inseon organization: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany – sequence: 4 givenname: Hiroyuki orcidid: 0000-0001-5368-7705 surname: Sasakura fullname: Sasakura, Hiroyuki organization: Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan – sequence: 5 givenname: Oleg orcidid: 0000-0003-4396-8719 surname: Senkov fullname: Senkov, Oleg organization: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany – sequence: 6 givenname: Keiko orcidid: 0000-0003-3985-5471 surname: Matsuda fullname: Matsuda, Keiko organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 7 givenname: Wataru orcidid: 0000-0003-2092-5775 surname: Kakegawa fullname: Kakegawa, Wataru organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 8 givenname: Amber J orcidid: 0000-0002-2124-3015 surname: Clayton fullname: Clayton, Amber J organization: Division of Structural Biology, University of Oxford, Oxford OX3 7BN, UK – sequence: 9 givenname: Veronica T orcidid: 0000-0001-7047-9019 surname: Chang fullname: Chang, Veronica T organization: Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK – sequence: 10 givenname: Maura surname: Ferrer-Ferrer fullname: Ferrer-Ferrer, Maura organization: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany – sequence: 11 givenname: Eriko surname: Miura fullname: Miura, Eriko organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 12 givenname: Rahul orcidid: 0000-0002-4944-8549 surname: Kaushik fullname: Kaushik, Rahul organization: Center for Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany – sequence: 13 givenname: Masashi orcidid: 0000-0001-8647-4917 surname: Ikeno fullname: Ikeno, Masashi organization: Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan – sequence: 14 givenname: Yuki surname: Morioka fullname: Morioka, Yuki organization: Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan – sequence: 15 givenname: Yuka orcidid: 0000-0002-2432-0370 surname: Takeuchi fullname: Takeuchi, Yuka organization: Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan – sequence: 16 givenname: Tatsuya orcidid: 0000-0001-6757-7590 surname: Shimada fullname: Shimada, Tatsuya organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 17 givenname: Shintaro surname: Otsuka fullname: Otsuka, Shintaro organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan – sequence: 18 givenname: Stoyan orcidid: 0000-0002-2872-7709 surname: Stoyanov fullname: Stoyanov, Stoyan organization: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany – sequence: 19 givenname: Masahiko orcidid: 0000-0001-5037-7138 surname: Watanabe fullname: Watanabe, Masahiko organization: Department of Anatomy, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan – sequence: 20 givenname: Kosei orcidid: 0000-0001-6397-2243 surname: Takeuchi fullname: Takeuchi, Kosei organization: Department of Medical Cell Biology, School of Medicine, Aichi Medical University, Aichi, Japan – sequence: 21 givenname: Alexander orcidid: 0000-0002-0472-0553 surname: Dityatev fullname: Dityatev, Alexander email: alexander.dityatev@dzne.de, radu@mrc-lmb.cam.ac.uk, myuzaki@keio.jp organization: Medical Faculty, Otto von Guericke University, 39120 Magdeburg, Germany – sequence: 22 givenname: A Radu orcidid: 0000-0003-3783-1388 surname: Aricescu fullname: Aricescu, A Radu email: alexander.dityatev@dzne.de, radu@mrc-lmb.cam.ac.uk, myuzaki@keio.jp organization: Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK – sequence: 23 givenname: Michisuke orcidid: 0000-0002-5750-3544 surname: Yuzaki fullname: Yuzaki, Michisuke email: alexander.dityatev@dzne.de, radu@mrc-lmb.cam.ac.uk, myuzaki@keio.jp organization: Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan. alexander.dityatev@dzne.de radu@mrc-lmb.cam.ac.uk myuzaki@keio.jp |
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| DOI | 10.1126/science.abb4853 |
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| Language | English |
| License | Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: Interdisciplinary Institute for Neuroscience (IINS), UMR5297 CNRS/UB, 33076 Bordeaux, France. Present address: Adaptimmune, 60 Jubilee Avenue, Milton Park, Abingdon OX14 4RX, UK. Present address: Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK Co-first authors. |
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| Snippet | Neuronal synapses undergo structural and functional changes throughout life, which are essential for nervous system physiology. However, these changes may also... The human brain contains trillions of synapses within a vast network of neurons. Synapse remodeling is essential to ensure the efficient reception and... Synthetic excitatory synaptic organizerThe human brain contains trillions of synapses within a vast network of neurons. Synapse remodeling is essential to... |
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| SubjectTerms | Affinity Alzheimer Disease - therapy Alzheimer's disease Anatomy Animal diseases Animal models Animals Ataxia Autism Autism Spectrum Disorders Balance Binding Biochemistry, Molecular Biology Brain C-Reactive Protein - chemistry C-Reactive Protein - pharmacology C-Reactive Protein - therapeutic use Cell adhesion Cell adhesion & migration Cell adhesion molecules Cell differentiation Cell surface Cerebellar ataxia Cerebellar Ataxia - therapy Cerebellum Circuit design Circuits Differentiation Disease Models, Animal Domains Epilepsy Gait Granule cells HEK293 Cells Hippocampus Humans Individualized Instruction Information retrieval Injuries Life Sciences Locomotion Long-term potentiation Mental disorders Mice Mice, Inbred C57BL Mice, Mutant Strains Nerve Tissue Proteins - chemistry Nerve Tissue Proteins - pharmacology Nerve Tissue Proteins - therapeutic use Nervous system Neural networks Neural Pathways - drug effects Neurodegenerative diseases Neurological disorders Neurons Neurotransmitters Physiology Protein Domains Protein Precursors - chemistry Protein Precursors - pharmacology Protein Precursors - therapeutic use Proteins Receptors, AMPA - metabolism Receptors, Glutamate - genetics Recombinant Proteins - chemistry Recombinant Proteins - pharmacology Recombinant Proteins - therapeutic use Recovery of function Schizophrenia Spinal cord Spinal cord injuries Spine Spine - drug effects Spine - physiology Structural Elements (Construction) Structural members Synapses Synapses - drug effects Synaptogenesis α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors |
| Title | A synthetic synaptic organizer protein restores glutamatergic neuronal circuits |
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