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Otx2 Binding to Perineuronal Nets Persistently Regulates Plasticity in the Mature Visual Cortex
Open accessAbstract
Specific transfer of (orthodenticle homeobox 2) Otx2 homeoprotein into GABAergic interneurons expressing parvalbumin (PV) is necessary and sufficient to open, then close, a critical period (CP) of plasticity in the developing mouse visual cortex. The accumulation of endogenous Otx2 in PV cells suggests the presence of specific Otx2 binding sites. Here, we find that perineuronal nets (PNNs) on the surfaces of PV cells permit the specific, constitutive capture of Otx2. We identify a 15 aa domain containing an arginine-lysine doublet (RK peptide) within Otx2, bearing prototypic traits of a glycosaminoglycan (GAG) binding sequence that mediates Otx2 binding to PNNs, and specifically to chondroitin sulfate D and E, with high affinity. Accordingly, PNN hydrolysis by chondroitinase ABC reduces the amount of endogenous Otx2 in PV cells. Direct infusion of RK peptide similarly disrupts endogenous Otx2 localization to PV cells, reduces PV and PNN expression, and reopens plasticity in adult mice. The closure of one eye during this transient window reduces cortical acuity and is specific to the RK motif, as an Alanine-Alanine variant or a scrambled peptide fails to reactivate plasticity. Conversely, this transient reopening of plasticity in the adult restores binocular vision in amblyopic mice. Thus, one function of PNNs is to facilitate the persistent internalization of Otx2 by PV cells to maintain CP closure. The pharmacological use of the Otx2 GAG binding domain offers a novel, potent therapeutic tool with which to restore cortical plasticity in the mature brain.
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In the citing paper
“Interestingly, PNNs have been proposed as indispensable mediators of the modulation of synaptic plasticity by the transcription factor Otx259–61.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [59]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Across multiple neuropsychiatric disorders, including autism, schizophrenia, and bipolar disorder, the developmental gene expression program in PV cells is instead immature (54).”
From Perineuronal nets protect fast-spiking interneurons against oxidative stress (2013) · cites this paper as [54]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“While OTX2 and Sema3A bind to 4,6 disulphated GAGs in the PNNs [23, 28], Nptx2 binds to both 4,6 sulphated GAGs and HA [29].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [23]
The cited source says what the claim attributes to it.
In the citing paper
“The soluble transcription factor OTX2 binds to PNNs and is internalised, leading to maturation of PV neurons and maintenance of PNNs in adulthood [23, 26].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [23]
The cited source says what the claim attributes to it.
In the citing paper
“Otx--2, which maintains PNNs (Beurdeley et al., 2012;Bernard and Prochiantz, 2016)”
From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Compromised PNNs prevent the persistent uptake of Otx2 homeoprotein into the enwrapped PV-cells needed for their maturation (including PNN maintenance itself) (27, 40, 41).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [41]
In the citing paper
“Subsequent inability to engage downstream molecular pathways by Otx2 within the PV-cell would retain a juvenile plastic state (41).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [41]
In the citing paper
“Second, PNN disruption prevents the persistent uptake of Otx2 homeoprotein into the enwrapped PV-cells required for their maintenance (27, 40, 41) (Fig. S3).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [41]
In the citing paper
“This may offer novel strategies or drug targets, in addition to antioxidants (18, 25) or Otx2 up-regulation (41, 51), for correcting aberrant brain plasticity in mental illness.”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [41]
In the citing paper
“Importantly, the second threshold is ‘reversible’ as decreasing Otx2 concentration engages the plastic regime (this study; (Beurdeley et al., 2012)).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Beurdeley et al., 2012
In the citing paper
“The model also stipulates that early sensory experience (sensory input) initiates expression of Otx2 binding sites on nascent PNNs (Beurdeley et al., 2012; Miyata et al., 2012), facilitating Otx2 import and opening a period of plasticity.”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Beurdeley et al., 2012
In the citing paper
“The same scheme also explain show a general source, thanks to mature, fully assembled PNNs, participates in maintaining a non-plastic state, allowing for the possibility to reopen plasticity in adulthood (Beurdeley et al., 2012; Pizzorusso et al., 2002).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Beurdeley et al., 2012
In the citing paper
“and that the permanent transfer of Otx2 through PNN recognition is necessary to repress plasticity in the adult (Beurdeley et al., 2012).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Once formed, and throughout adulthood, PNNs control neuronal access to growth and transcription factors, stabilize synaptic connectivity and compartmentalize the neuronal surface, regulating the availability of glutamatergic receptors to postsynaptic specializations and, thus, neuronal firing properties.23, 25, 38”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [38]
In the citing paper
“In fact, PV and PNN colocalization is correlated with critical period closure and reduced synaptic plasticity, particularly in sensory cortices (Nowicka et al., 2009; Beurdeley et al., 2012).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Beurdeley et al., 2012
In the citing paper
“PNNs are necessary for the uptake of Otx2 by PV cells, which promotes PV cell maturation (Beurdeley et al., 2012).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Studies of rodent visual cortex development indicate that Otx2 is localized to GABAergic cells, and is more likely found in PV cells that are enwrapped with PNNs, which contain a specific Otx2 binding site (Beurdeley et al., 2012).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Long believed to be responsible primarily for structural support, PNNs have in recent years come to the forefront of neuroscience research as critical elements regulating synaptic functions and plasticity during development and adulthood (Beurdeley et al., 2012; Dityatev et al., 2010; Gogolla et al., 2009; Gundelfinger et al., 2010; Pizzorusso et al., 2002; Xue et al., 2014; Yamada and Jinno, 2013”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Beurdeley et al., 2012
In the citing paper
“this homeoprotein signals the maturation of the parvalbumin-containing GABAergic interneurons, which contributes to the opening and possibly also the closure of the critical period”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Beurdeley et al., 2012
In the citing paper
“the PNN to play a role in the “capture” of the homeodeomain transcription factor orthodenticle homeobox 2 (Otx2) from thalamic inputs to visual cortex (Beurdeley et al., 2012)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Namely, PNNs permit Otx2 capture and transfer into GABAergic interneurons expressing parvalbumin.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Beurdeley et al., 2012
In the citing paper
“Indeed, the maturation and phenotypic maintenance of PVI require incorporation of a non-cell autonomous homeobox protein, Otx2, through its affinity with PNN (Beurdeley et al., 2012; Miyata et al., 2012).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Beurdeley et al., 2012
In the citing paper
“PNNs also facilitate the capture and uptake of the transcription factor Otx2, which in turn promotes PVBC maturation as well as further PNN development (100, 173, 912, 1063).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [100]
In the citing paper
“PNNs also facilitate the capture and uptake of the transcription factor Otx2, which in turn promotes PVBC maturation as well as further PNN development (100, 173, 912, 1063).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [100]
In the citing paper
“Similarly, blocking the ability of Otx2 to bind to PNNs results in their degradation and reopens the critical period in adults (100).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [100]
In the citing paper
“In contrast, removing PNNs or reducing Otx2 uptake reopens plasticity in adulthood (Beurdeley et al., 2012; Pizzorusso et al., 2002; Spatazza et al., 2013).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Beurdeley et al., 2012
In the citing paper
“which in turn contributes to closure of critical period plasticity (Beurdeley et al., 2012; Carulli et al., 2010; Pizzorusso et al., 2002).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Beurdeley et al., 2012
In the citing paper
“With PV-cell maturation, perineuronal nets (PNNs) of extracellular matrix molecules condense around their somata”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Beurdeley et al., 2012
In the citing paper
“The maturation of PNNs in the developing cortex coincides with the closure of the critical periods of synaptogenesis and circuit refinement (Beurdeley et al., 2012; Ye and Miao, 2013).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Beurdeley et al., 2012
In the citing paper
“PNNs are thought to limit plasticity and are responsible for the closure of the critical period for ocular dominance in the visual cortex (28).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [28]
In the citing paper
“OTX2 produced in the choroid plexus binds to PNNs in the visual cortex where it facilitates the expression of PNNs (28).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [28]
In the citing paper
“Continual binding of OTX2 to PNNs has been shown to be necessary for synaptic stability in the adult visual cortex and blocking OTX2 uptake into PV+ cells in adults has been demonstrated to reduce PNN expression and reinstate juvenile levels of plasticity (28).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [28]
In the citing paper
“Continual binding of OTX2 to PNNs has been shown to be necessary for synaptic stability in the adult visual cortex and blocking OTX2 uptake into PV+ cells in adults has been demonstrated to reduce PNN expression and reinstate juvenile levels of plasticity (28).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [28]
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Metadata
- Authors
- Beurdeley, M., Spatazza, J., Lee, H. H. C., Sugiyama, S., Bernard, C., Di Nardo, A. A., Hensch, T. K., & Prochiantz, A.
- Affiliations
- Collège de France (FR)
- Centre National de la Recherche Scientifique (FR)
- Boston Children's Hospital (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-07-04
- Volume
- 32
- Issue
- 27
- Pages
- 9429-9437
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3419577
- OpenAlex
- W2040502575
- Cited by
- 398
- References
- 50
- Citations by year
- 2026: 17 · 2025: 25 · 2024: 21 · 2023: 28 · 2022: 22 · 2021: 38 · 2020: 37 · 2019: 38 · 2018: 26 · 2017: 34 · 2016: 22 · 2015: 32 · 2014: 29 · 2013: 26 · 2012: 3
- FWCI
- 9.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- Journal of Neuroscience (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Agence Nationale de la Recherche
- Croucher Foundation
- Ministry of Education, Science and Technology
- Centre National de la Recherche Scientifique
- National Institutes of Health (DP1OD003699)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- Otx2, perineuronal nets, critical period, visual cortex plasticity, parvalbumin interneurons, glycosaminoglycan binding, chondroitin sulfate, chondroitinase ABC, amblyopia, binocular vision, homeodomain transcription factor
- MeSH terms
- Age Factors, Animals, Extracellular Matrix, Interneurons, Male, Mice, Inbred C57BL, Neuronal Plasticity, Protein Binding, Visual Cortex, Mice, Otx Transcription Factors, GABAergic Neurons
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