Plasticity-related Gene 5 Promotes Spine Formation in Murine Hippocampal Neurons

Coiro, Pierluca; Stoenica, Luminita; Strauß, Ulf; Bräuer, Anja U.

doi:10.1074/jbc.m114.597880

Cited by 18 publications

(73 citation statements)

References 52 publications

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“…Overexpression of either LPPR1 or LPPR5 induces membrane protrusions in neuronal and non-neuronal cell lines (Broggini et al, 2010;Savaskan et al, 2004;Sigal et al, 2007). LPPR1 has been reported to promote neurite shaft protrusion in primary neurons (Velmans et al, 2013), whereas LPPR5 has been shown to induce neurite outgrowth (Broggini et al, 2010) and, more recently, to promote dendritic spine formation in hippocampal neurons (Coiro et al, 2014). The current findings suggest that LPPRs play putative roles in axonal outgrowth, regeneration and synaptic plasticity.…”

Section: Introductionmentioning

confidence: 67%

Cooperative interactions of LPPR/PRG family members in membrane localization and alteration of cellular morphology

Agbaegbu

Malide²,

et al. 2015

Journal of Cell Science

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The lipid phosphate phosphatase-related proteins (LPPRs), also known as plasticity-related genes (PRGs), are classified as a new brain-enriched subclass of the lipid phosphate phosphatase (LPP) superfamily. They induce membrane protrusions, neurite outgrowth or dendritic spine formation in cell lines and primary neurons. However, the exact roles of LPPRs and the mechanisms underlying their effects are not certain. Here, we present the results of a large-scale proteome analysis to determine LPPR1-interacting proteins using coimmunoprecipitation coupled to mass spectrometry. We identified putative LPPR1-binding proteins involved in various biological processes. Most interestingly, we identified the interaction of LPPR1 with its family member LPPR3, LPPR4 and LPPR5. Their interactions were characterized by co-immunoprecipitation and colocalization analysis using confocal and super-resolution microscopy. Moreover, co-expressing two LPPR members mutually elevated their protein levels, facilitated their plasma membrane localization and resulted in an increased induction of membrane protrusions as well as the phosphorylation of S6 ribosomal protein. Taken together, we revealed a new functional cooperation between LPPR family members and discovered for the first time that LPPRs likely exert their function through forming complex with its family members.

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Section: Introductionmentioning

confidence: 67%

Cooperative interactions of LPPR/PRG family members in membrane localization and alteration of cellular morphology

Agbaegbu

Malide²,

et al. 2015

Journal of Cell Science

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“…-Neuropathic pain (Choi et al, 2010); -Ischemic stroke (Savitz et al, 2006;Kimura et al, 2008); -Schizophrenia (Cunningham et al, 2006;Musazzi et al, 2011); -Behavioral dysfunctions (Santin et al, 2009); -Seizure (Elmes et al, 2004). (Suckau et al, 2019); -Neuronal differentiation (Spohr et al, 2008;E Spohr et al, 2011); -Survival and differentiation of neural progenitor cells (NPCs; Chun et al, 2002); -Neuronal hyperexcitability and neuro-plasticity (Broggini et al, 2010;Coiro et al, 2014);…”

Section: Receptors G Proteins Signaling Pathways Biological Functionsmentioning

confidence: 99%

“…Second, the accumulated LPA promotes the release of autotaxin (ATX) from astrocytes, further enhancing the glutamate concentration in the synaptic cleft (Thalman et al, 2018). Other evidence is also available showing that PRG-1 modulates LPA release in a non-cell-autonomous pattern, thus leading to an elevation of pre-synaptical glutamate vesicle release, as well as a series of alterations in structural plasticity such as filopodia formation, neurite extension, and brain reorganization after lesion (Broggini et al, 2010;Coiro et al, 2014).…”

Section: Lpa and Neuroplasticitymentioning

confidence: 99%

Lysophospholipids and Their G-Coupled Protein Signaling in Alzheimer’s Disease: From Physiological Performance to Pathological Impairment

Hao

Guo

Feng

et al. 2020

Front. Mol. Neurosci.

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Lysophospholipids (LPLs) are bioactive signaling lipids that are generated from phospholipase-mediated hydrolyzation of membrane phospholipids (PLs) and sphingolipids (SLs). Lysophosphatidic acid (LPA) and sphingosine-1-phosphate (S1P) are two of the best-characterized LPLs which mediate a variety of cellular physiological responses via specific G-protein coupled receptor (GPCR) mediated signaling pathways. Considerable evidence now demonstrates the crucial role of LPA and S1P in neurodegenerative diseases, especially in Alzheimer's disease (AD). Dysfunction of LPA and S1P metabolism can lead to aberrant accumulation of amyloid-β (Aβ) peptides, the formation of neurofibrillary tangles (NFTs), neuroinflammation and ultimately neuronal death. Summarizing LPA and S1P signaling profile may aid in profound health and pathological processes. In the current review, we will introduce the metabolism as well as the physiological roles of LPA and S1P in maintaining the normal functions of the nervous system. Given these pivotal functions, we will further discuss the role of dysregulation of LPA and S1P in promoting AD pathogenesis.

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“…PRG-1 is expressed at postsynaptic sites of principal neurons and acts in a non-cell-autonomous fashion by controlling LPA in the synaptic cleft, which in turn stimulates presynaptic LPA receptors resulting in an increased release probability of glutamate vesicles at excitatory synapses (Tokumitsu et al, 2010;Trimbuch et al, 2009;Vogt et al, 2016). Previous studies have shown that various members of the PRG family play a role in regulating structural plasticity, including filopodia formation, neurite extension, and brain reorganization after lesion (Brauer et al, 2003;Broggini et al, 2010;Coiro et al, 2014;Peeva et al, 2006;Savaskan et al, 2004;Sigal et al, 2007;Velmans et al, 2013). However, using ionmobility enhanced data-independent label-free liquid chromatography (LC)-tandem mass spectrometry (MS), we have detected PRG-1 as a characteristic postsynaptic density (PSD) protein, while the other members of the PRG family were not found in a high-confidence PSD preparation (Distler et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

PRG-1 Regulates Synaptic Plasticity via Intracellular PP2A/β1-Integrin Signaling

et al. 2016

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Alterations in dendritic spine numbers are linked to deficits in learning and memory. While we previously revealed that postsynaptic plasticity-related gene 1 (PRG-1) controls lysophosphatidic acid (LPA) signaling at glutamatergic synapses via presynaptic LPA receptors, we now show that PRG-1 also affects spine density and synaptic plasticity in a cell-autonomous fashion via protein phosphatase 2A (PP2A)/β1-integrin activation. PRG-1 deficiency reduces spine numbers and β1-integrin activation, alters long-term potentiation (LTP), and impairs spatial memory. The intracellular PRG-1 C terminus interacts in an LPA-dependent fashion with PP2A, thus modulating its phosphatase activity at the postsynaptic density. This results in recruitment of adhesome components src, paxillin, and talin to lipid rafts and ultimately in activation of β1-integrins. Consistent with these findings, activation of PP2A with FTY720 rescues defects in spine density and LTP of PRG-1-deficient animals. These results disclose a mechanism by which bioactive lipid signaling via PRG-1 could affect synaptic plasticity and memory formation.

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Plasticity-related Gene 5 Promotes Spine Formation in Murine Hippocampal Neurons

Cited by 18 publications

References 52 publications

Cooperative interactions of LPPR/PRG family members in membrane localization and alteration of cellular morphology

Cooperative interactions of LPPR/PRG family members in membrane localization and alteration of cellular morphology

Lysophospholipids and Their G-Coupled Protein Signaling in Alzheimer’s Disease: From Physiological Performance to Pathological Impairment

PRG-1 Regulates Synaptic Plasticity via Intracellular PP2A/β1-Integrin Signaling

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