Lrp4 in astrocytes modulates glutamatergic transmission
Open accessAbstract
Neurotransmission requires precise control of neurotransmitter release from axon terminals. This process is regulated by glial cells; however, the underlying mechanisms are not fully understood. We found that glutamate release in the brain was impaired in mice lacking low-density lipoprotein receptor-related protein 4 (Lrp4), a protein that is critical for neuromuscular junction formation. Electrophysiological studies revealed compromised release probability in astrocyte-specific Lrp4 knockout mice. Lrp4 mutant astrocytes suppressed glutamatergic transmission by enhancing the release of ATP, whose level was elevated in the hippocampus of Lrp4 mutant mice. Consequently, the mutant mice were impaired in locomotor activity and spatial memory and were resistant to seizure induction. These impairments could be ameliorated by blocking the adenosine A1 receptor. The results reveal a critical role for Lrp4, in response to agrin, in modulating astrocytic ATP release and synaptic transmission. Our findings provide insight into the interaction between neurons and astrocytes for synaptic homeostasis and/or plasticity.
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Astrocytic Lrp4, rather than neuronal Lrp4, mediates this process.
“it is not neuronally expressed Lrp4, but rather astrocytic Lrp4 that mediates this process”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [95]
The released ATP is broken down into adenosine in the extracellular space.
“which is subsequently broken down into adenosine in the extracellular milieu [95]”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [95]
In astrocytes, Agrin signaling through Lrp4 increases ATP release.
“In the astrocyte, Agrin signaling through Lrp4 leads to the increased release of ATP”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [95]
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“In the astrocyte, Agrin signaling through Lrp4 leads to the increased release of ATP, which is subsequently broken down into adenosine in the extracellular milieu [95].”
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Self-citationLin, S., Huang, L., Luo, Z.-C., Li, X., Jin, S., Du, Z., Wu, D., Xiong, W., Huang, L., Luo, Z.-Y., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.02.014 · Cited by 130 · see citing works
Self-citationPiacentini, R., Puma, D. D. L., Mainardi, M., Lazzarino, G., Tavazzi, B., Arancio, O., & Grassi, C. (2017) · Glia · doi:10.1002/glia.23163 · Cited by 116 · see citing works
“…P2X receptors (e.g. 1, 2/3, and 3) at the presynaptic membrane it promotes glutamate release; on the contrary, if it binds metabotropic P2Y receptors (e.g. 1, 2 and/or 4) it triggers an inhibitory action (Koizumi et al., 2003; Pougnet et al., 2014; Rodrigues et al., 2005; Sun et al., 2016).”
Dong, Z., Chen, W., Chen, C., Wang, H., Cui, W., Tan, Z., Robinson, H., Gao, N., Luo, B., Zhang, L., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.10.035 · Cited by 109 · see citing works
Self-citationGuan, Y., Huang, G., Xu, M.-D., Gao, F., Lin, S., Huang, J., Wang, J., Li, Y., Wu, C.-H., Yao, S., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.032 · Cited by 112 · see citing works
Self-citationFunctional Roles of the Interaction of APP and Lipoprotein Receptors
Pohlkamp, T., Wasser, C. R., & Herz, J. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00054 · Cited by 92 · see citing works
Fundamental Molecules and Mechanisms for Forming and Maintaining Neuromuscular Synapses
Burden, S. J., Huijbers, M. G. M., & Remédio, L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020490 · Cited by 100 · see citing works
Gao, F., Huang, J., Huang, G., You, Q.-L., Yao, S., Zhao, S., Liu, J., Wu, C.-H., Chen, G.-F., Liu, S., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci166356 · Cited by 75 · see citing works
“made based on previous studies (50, 51), not predetermined by a statis-”
MethodSelf-citationPresynaptic LRP4 promotes synapse number and function of excitatory CNS neurons
Mosca, T. J., Luginbuhl, D. J., Wang, I. E., & Luo, L. (2017) · eLife · doi:10.7554/elife.27347 · Cited by 65 · see citing works
“2015), through functioning in astrocytes in some cases (Sun et al., 2016).”
A discrete serotonergic circuit regulates vulnerability to social stress
Zou, W.-J., Song, Y., Wu, M., Chen, X.-T., You, Q.-L., Yang, Q., Luo, Z.-Y., Huang, L., Kong, Y., Feng, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18010-w · Cited by 57 · see citing works
Self-citationA role of low-density lipoprotein receptor-related protein 4 (LRP4) in astrocytic Aβ clearance
Zhang, H., Chen, W., Tan, Z., Zhang, L., Dong, Z., Cui, W., Zhao, K., Wang, H., Jing, H., Cao, R., et al. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0250-20.2020 · Cited by 58 · see citing works
“Lrp4f/f (Wu et al., 2012), GFAP-Cre (Zhuo et al., 2001), Ai9 (Madisen et al., 2010), GFAP-CreERT2 (Casper et al., 2007), Neurod6-Cre (Goebbels et al., 2006), Thy1GFP (Feng et al., 2000), and Slc1a2-EGFP (Gong et al., 2003) were as described previously (Sun et al., 2016).”
BackgroundMethodResultInfluentialSelf-citationLi, W., Su, X., Hu, N.-Y., Hu, J., Li, X., Yang, J., & Gao, T. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.04.019 · Cited by 61 · see citing works
Self-citationAgrin-Lrp4-Ror2 signaling regulates adult hippocampal neurogenesis in mice
Zhang, H., Sathyamurthy, A., Liu, F., Li, L., Zhang, L., Dong, Z., Cui, W., Sun, X., Zhao, K., Wang, H., et al. (2019) · eLife · doi:10.7554/elife.45303 · Cited by 58 · see citing works
“In situ X-gal assay was carried out as previously described (Sun et al., 2016).”
BackgroundMethodInfluentialSelf-citationTransient Astrocytic Gq Signaling Underlies Remote Memory Enhancement
Iwai, Y., Ozawa, K., Yahagi, K., Mishima, T., Akther, S., Vo, C. T., Lee, A. B., Tanaka, M., Itohara, S., & Hirase, H. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.658343 · Cited by 56 · see citing works
Otto, N., Marelja, Z., Schoofs, A., Kranenburg, H., Bittern, J., Yildirim, K., Berh, D., Bethke, M., Thomas, S., Rode, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05645-z · Cited by 61 · see citing works
Neogenin, a regulator of adult hippocampal neurogenesis, prevents depressive-like behavior
Sun, D., Sun, X.-D., Zhao, L., Lee, D.-H., Hu, J.-X., Tang, F., Pan, J., Mei, L., Zhu, X., & Xiong, W. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0019-2 · Cited by 56 · see citing works
Self-citationRivner, M. H., Liu, S. M., Quarles, B. M., Fleenor, B., Shen, C., Pan, J., & Mei, L. (2016) · Muscle & Nerve · doi:10.1002/mus.25438 · Cited by 55 · see citing works
Self-citationThalman, C., Horta, G., Qiao, L., Endle, H., Tegeder, I., Cheng, H., Laube, G., Sigurdsson, T., Hauser, M. J., Tenzer, S., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0053-1 · Cited by 52 · see citing works
“In sum, our data suggest that ATX is a key molecule within a stimulatory feedforward mechanism of excitatory transmission and is in line with recent reports suggesting that astrocytes are a novel regulatory element of excitatory synaptic function acting via lipid-mediated pathways [38].”
ResultGraphene oxide enhances β-amyloid clearance by inducing autophagy of microglia and neurons
Li, X., Li, K., Chu, F., Huang, J., & Yang, Z. R. (2020) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2020.109126 · Cited by 52 · see citing works
“When the cells adhered and grown well, one cover slip of BV2 cells and one cover slip of SH-SY5Y cells were placed in one 60-mm dish and co-cultured in culture medium [38].”
BackgroundMethodThyroid hormone remodels cortex to coordinate body-wide metabolism and exploration
Hochbaum, D. R., Hulshof, L., Urke, A., Wang, W., Dubinsky, A. C., Farnsworth, H. C., Hakim, R., Lin, S., Kleinberg, G., Robertson, K., et al. (2024) · Cell · doi:10.1016/j.cell.2024.07.041 · Cited by 54 · see citing works
Potential Roles of the WNT Signaling Pathway in Amyotrophic Lateral Sclerosis
Jiang, X., Guan, Y., Zhao, Z., Meng, F., Wang, X., Gao, X., Liu, J., Chen, Y., Zhou, F., Zhou, F., et al. (2021) · Cells · doi:10.3390/cells10040839 · Cited by 45 · see citing works
“Glutamatergic transmission in LRP4 mutant mice is likely suppressed by A1 receptor activation by adenosine, a product of ATP hydrolysis, offering insight into the interaction between neurons and astrocytes for synaptic homeostasis and/or plasticity [70].”
BackgroundSelf-citationAgrin and LRP4 antibodies as new biomarkers of myasthenia gravis
Yan, M., Xing, G., Xiong, W., & Mei, L. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13573 · Cited by 45 · see citing works
Self-citationLiu, Y., Du, T., Zhang, W., Lu, W., Peng, Z., Huang, S., Sun, X., Zhu, X., Chen, C., Qian, L., et al. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/8340192 · Cited by 44 · see citing works
“We conclude that these two mechanisms may be linked, since NMDA receptors can decrease adenosine kinase activity and evoke adenosine accumulation [59, 60], and adenosine can also regulate glutamatergic transmission [61].”
Self-citationBriel, N., Pratsch, K., Roeber, S., Arzberger, T., & Herms, J. W. (2020) · Brain Pathology · doi:10.1111/bpa.12914 · Cited by 41 · see citing works
“There are external factors provided by glial cells that regulate the integrity of neurons and their cellular compartments in vitro (25) and in vivo (43, 44).”
BackgroundShan, W., Nagai, T., Tanaka, M., Itoh, N., Furukawa‐Hibi, Y., Nabeshima, T., Sokabe, M., & Yamada, K. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14274 · Cited by 41 · see citing works
The synaptic receptor Lrp4 promotes peripheral nerve regeneration
Gribble, K. D., Walker, L. J., Saint‐Amant, L., Kuwada, J. Y., & Granato, M. (2018) · Nature Communications · doi:10.1038/s41467-018-04806-4 · Cited by 40 · see citing works
Li, H., Liu, Z., Wu, Y., Chen, Y., Wang, J., Wang, Z., Huang, D., Wang, M., Yu, M., Fei, J., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.165590 · Cited by 40 · see citing works
Self-citationChen, W., Luo, B., Gao, N., Li, H., Wang, H., Li, L., Cui, W., Zhang, L., Sun, D., Liu, F., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci136956 · Cited by 39 · see citing works
“On the other hand, astrocytes could modulate the neuronal activity by altering 486 extracellular concentrations of ATP, potassium, and glutamate and thus epileptogenesis 487 (99-102).”
BackgroundSelf-citationAstrocytic cell adhesion genes linked to schizophrenia correlate with synaptic programs in neurons
Pietiläinen, O. P. H., Trehan, A., Meyer, D., Mitchell, J. M., Tegtmeyer, M., Valakh, V., Gebre, H., Chen, T., Vartiainen, E., Farhi, S. L., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2022.111988 · Cited by 36 · see citing works
“…were synaptic genes, including the cell adhesion molecules LRRC4, LRRC4B, and NRXN1, as well as the astrocytic LRP4 involved in regulation of glutamate transmission, 35 and included genes in 10 genome-wide significant loci (LRP4, AP3B2, LRRC4B, KCNB1, CCDC39, PCDHB4, MSI2, B9D1, NALCN, and SNX32).”
Astrocyte-Derived Lactate Modulates the Passive Coping Response to Behavioral Challenge in Male Mice
Yin, Y., Hu, J., Wei, Y., Li, Z., Luo, Z.-C., Wang, R., Yang, K.-X., Li, S.-J., Li, X., Yang, J., et al. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00553-z · Cited by 37 · see citing works
Self-citationYe, X.-C., Hu, J.-X., Li, L., Li, Q., Tang, F., Lin, S., Sun, D., Sun, X.-D., Cui, G., Mei, L., et al. (2017) · Stroke · doi:10.1161/strokeaha.117.018115 · Cited by 36 · see citing works
“In this mutant line, LacZ expression is under the control of endogenous Lrp4 promoter.(9) In response to ischemia/stroke, the LacZ activity was selectively elevated in the penumbra region (Figure IB in the online-only Data Supplement), providing additional evidence for an increase of Lrp4’s transcription in response to”
Self-citationPassarella, D., Ciampi, S., Liberto, V. D., Zuccarini, M., Ronci, M., Medoro, A., Foderà, E., Frinchi, M., Mignogna, D., Russo, C., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168921 · Cited by 35 · see citing works
“Although it is mainly expressed in bone, where it regulates bone formation by inhibiting sclerostin in Wnt1/β-catenin signaling [62], LRP4 is also found in astrocytes of the prefrontal cortex and hippocampus, regions particularly vulnerable to AD [63].”
BackgroundPark, Y. M., Chun, H., Shin, J.-I., & Lee, C. J. (2018) · Experimental Neurobiology · doi:10.5607/en.2018.27.6.508 · Cited by 33 · see citing works
Synaptic Microenvironment in Depressive Disorder: Insights from Synaptic Plasticity
Ren, F., & Guo, R. (2021) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s268012 · Cited by 31 · see citing works
Zhang, J., Wang, Y., Zheng, Z., Sun, X., Chen, T., Li, C., Zhang, X., & Guo, J. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101112 · Cited by 32 · see citing works
Self-citationZDHHC8 critically regulates seizure susceptibility in epilepsy
Yang, Q. Z., Zheng, F., Hu, Y., Yang, Y., Li, Y., Chen, G., Wang, W., He, M., Zhou, R., Ma, Y., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0842-0 · Cited by 30 · see citing works
Handara, G., Hetsch, F., Jüttner, R., Schick, A., Haupt, C., Rathjen, F. G., & Kröger, S. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.10.017 · Cited by 30 · see citing works
mGluR5 in hippocampal CA1 pyramidal neurons mediates stress-induced anxiety-like behavior
Li, X., Du, Z., Xu, J.-N., Liang, Z.-M., Lin, S., Chen, H. H., Li, S.-J., Li, X., Yang, J., & Gao, T. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01548-w · Cited by 30 · see citing works
“Besides our results, many previous studies have showed that dorsal CA1 is implicated in regulating anxiety-like behaviors [20, 38, 39].”
BackgroundResultSelf-citationNeogenin in Amygdala for Neuronal Activity and Information Processing
Sun, X., Chen, W., Sun, D., Huang, J., Li, Y., Pan, J., Wang, Y., Zhao, K., Dong, Z., Wang, H., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0433-18.2018 · Cited by 27 · see citing works
“In GFAP-Cre mice, Cre expression is restricted in neural progenitor cells that give rise to neurons and glial cells in the brain (Zhuo et al., 2001) (Fig.”
MethodInfluentialSelf-citationNeuronal LRP4 regulates synapse formation in the developing CNS
Karakatsani, A., Marichal, N., Urban, S., Kalamakis, G., Ghanem, A., Schick, A., Zhang, Y., Conzelmann, K., Rüegg, M. A., Berninger, B., et al. (2017) · Development · doi:10.1242/dev.150110 · Cited by 25 · see citing works
“A recent study (Sun et al., 2016) reported that in adult mice βgalactosidase expression driven by the endogenous Lrp4 promoter is mostly detectable in astrocytes, which is in concordance with our data showing that LRP4 levels, detected by western blotting, are higher in astrocytes than in neurons…”
BackgroundResultInfluentialThe effect of ketogenic diet on behaviors and synaptic functions of naive mice
Huang, J., Li, Y., Wu, C., Zhang, Y., Zhao, S., Chen, Y., Deng, Y., Xuan, A., & Sun, X. (2019) · Brain and Behavior · doi:10.1002/brb3.1246 · Cited by 28 · see citing works
Self-citationAgrin to YAP in Cancer and Neuromuscular Junctions
Xiong, W., & Mei, L. (2017) · Trends in cancer · doi:10.1016/j.trecan.2017.03.005 · Cited by 25 · see citing works
“Agrin, LRP4 and MuSK are not restricted at the NMJ; rather, they are expressed in a number of tissues or organs and have been implicated in the development and function of the brain, kidney, mammary glands and bones(6, 7).”
BackgroundSelf-citationConservation and Innovation: Versatile Roles for LRP4 in Nervous System Development
DePew, A. T., & Mosca, T. J. (2021) · Journal of Developmental Biology · doi:10.3390/jdb9010009 · Cited by 23 · see citing works
“This effect is mediated by Agrin, though the requirement for MuSK is unknown [84].”
BackgroundVascular endothelial cells: a fundamental approach for brain waste clearance
Wei, H., Jiang, H., Zhou, Y., Xiao, X., Zhou, C., & Ji, X. (2022) · Brain · doi:10.1093/brain/awac495 · Cited by 20 · see citing works
Chen, J., Chen, H., Dong, X., Hui, T., Yan, M., Ren, D., Zou, S., Wang, S., Fei, E., Zhang, W., et al. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06581-1 · Cited by 22 · see citing works
Neuregulin 1/ErbB4 signaling contributes to the anti-epileptic effects of the ketogenic diet
Wang, J., Huang, J., Li, Y., Yao, S., Cui-hong, W., Wang, Y., Gao, F., Xu, M.-D., Huang, G., Zhao, C., et al. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00536-1 · Cited by 20 · see citing works
“Sample size choice was made based on previous studies [36, 37].”
MethodSelf-citationZhang, Z., Jin, P., Guo, Z., Tu, Z., Yang, H., Hu, M., Li, Q., Liu, X., Li, W., & Hou, S. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03734-9 · Cited by 20 · see citing works
“Morris water maze (MWM) test was performed as described previously with some modifications [21].”
MethodXie, W.-L., Zheng, H., Li, H., Lu, J.-J., Xue, S.-G., Luo, Y., Ma, C., Liu, J., Hu, Z., Ni, L., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.10.022 · Cited by 18 · see citing works
Increasing LRP4 diminishes neuromuscular deficits in a mouse model of Duchenne muscular dystrophy
Hui, T., Jing, H., Zhou, T. G., Chen, P., Liu, Z., Dong, X., Yan, M., Ren, D., Zou, S., Wang, S., et al. (2021) · Human Molecular Genetics · doi:10.1093/hmg/ddab135 · Cited by 18 · see citing works
“HSA-LRP4 mice were described previously (30,34,35,47).”
Jing, H., Chen, P., Hui, T., Zheng, Y., Zhou, J., Fei, E., Wang, S., Ren, D., Lai, X., & Li, B. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00619-z · Cited by 17 · see citing works
“The following mice were described previously LRP4-LacZ with genotyping primers being: 5ʹ-TTC TGC CCA GGA ATA GCC AG-3ʹ and 5ʹ-TGA GCG AGT AAC AAC CCG TC-3ʹ (KOMP, stock #VG15248) [30], LRP4-ECD with genotyping primers being: 5ʹ-CTC CAA TTT CCT GTC CCT TG-3ʹ, 5ʹ-GCC AGA GGC CAC TTG TGT AG-3ʹ and 5ʹ-CTG CAG CAG AGC TGA…”
BackgroundMethodResultInfluentialSelf-citationArzola, E. P., Xiong, W., & Mei, L. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.05.016 · Cited by 17 · see citing works
Self-citationVTA dopamine neuron plasticity – the unusual suspects
Xin, W., Edwards, N., & Bonci, A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13425 · Cited by 17 · see citing works
“from astrocytic ATP release acted on presynaptic adenosine A1 receptors to suppress glutamatergic transmission (Sun et al., 2016).”
BackgroundIntrafusal-fiber LRP4 for muscle spindle formation and maintenance in adult and aged animals
Cao, R., Chen, P., Wang, H., Jing, H., Zhang, H., Xing, G., Luo, B., Pan, J., Zheng, Y., Xiong, W., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36454-8 · Cited by 17 · see citing works
Self-citationAmygdalar Endothelin-1 Regulates Pyramidal Neuron Excitability and Affects Anxiety
Chen, M., Yan, H., Shu, S., Pei, L., Zang, L.-K., Fu, Y., Wang, Z., Wan, Q., & Bi, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-02583-6 · Cited by 17 · see citing works
Prömer, J. J., Barresi, C., & Herbst, R. (2023) · Cellular Signalling · doi:10.1016/j.cellsig.2022.110584 · Cited by 14 · see citing works
Ding, N., Song, Y., Zhang, Y., Yu, W., Li, X., Li, W., & Li, L. (2025) · Autophagy · doi:10.1080/15548627.2025.2466144 · Cited by 12 · see citing works
“TEM preparation was described as previously described [90], With some modifications, mice were perfused intracardially with 4% PFA.”
Self-citationLRP4-related signalling pathways and their regulatory role in neurological diseases
Chen, B., Lin, Z.-Y., Zeng, X.-X., Jiang, Y., & Geng, F. (2023) · Brain Research · doi:10.1016/j.brainres.2023.148705 · Cited by 12 · see citing works
Wang, K., Wu, J., Wang, J., & Jiang, K. (2021) · Brain and Behavior · doi:10.1002/brb3.2247 · Cited by 10 · see citing works
Hippocampal Endothelin-1 decreases excitability of pyramidal neurons and produces anxiolytic effects
Chen, M., Shu, S., Yan, H., Pei, L., Wang, Z.-F., Wan, Q., & Bi, L. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.014 · Cited by 10 · see citing works
“According to the previous studies (Bi et al., 2015b; Bi et al., 2013; Lu et al., 2014; Sun et al., 2016; Tian et al., 2015; Yin et al., 2013), spontaneous excitatory postsynaptic currents (sEPSCs) were recorded with a V-cl mp in the presence of the GABAAR antagonist BMI (20 µM).”
MethodSu, X., Li, W., Wang, Y.-J., Liu, J., Liu, J.-Y., Jiang, Y., & Peng, F. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01168-6 · Cited by 9 · see citing works
“Hippocampal slices were prepared as described previously [32].”
MethodLRP4 is required for the olfactory association task in the piriform cortex
Yan, M., Xiong, M., Wu, Y., Dong, L., Chen, P., Chen, J., Liu, Z., Zhang, H., Ren, D., Fei, E., et al. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00792-9 · Cited by 9 · see citing works
“Animals Lrp4LacZ/+ mice were described before; in brief words, β-galactosidase (β-gal) protein cassette, including stop code and a polyadenylation termination signal, was inserted into the downstream of Lrp4 promoter [1].”
BackgroundResultInfluentialA Panel of Synapse-Related Genes as a Biomarker for Gliomas
Ji, X., Zhang, H., & Cui, Q. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00822 · Cited by 9 · see citing works
“More genes do not belong to receptors, and they perform neuronal-specific synthesis and glycosylation [TNR (Woodworth et al., 2004)], signal transduction [MAPK8IP2 (Kennedy et al., 2007)], neurotransmission [UNC13A (Reddy-Alla et al., 2017), LRP4 (Sun et al., 2016)], synapse formation [LRP4 (Karakatsani et al., 2017)]…”
InfluentialAblation of Lrp4 in Schwann Cells Promotes Peripheral Nerve Regeneration in Mice
Hui, T., Lai, X., Dong, X., Jing, H., Liu, Z., Fei, E., Chen, W., Wang, S., Ren, D., Zou, S., et al. (2021) · Biology · doi:10.3390/biology10060452 · Cited by 9 · see citing works
“In the nervous system, Lrp4 participates in CNS development [18], cognitive function and plasticity [19], adult hippocampal neurogenesis [20], amyotrophic lateral sclerosis (ALS) [21], and Aβ clearance in Alzheimer’s disease [22].”
BackgroundMethodInfluentialSelf-citationLRP4 LDLα repeats of astrocyte enhance dendrite arborization of the neuron
Yan, M., Guo, A., Chen, P., Jing, H., Ren, D., Zhong, Y., Wu, Y., Fei, E., Lai, X., Zou, S., et al. (2020) · Molecular Brain · doi:10.1186/s13041-020-00708-z · Cited by 8 · see citing works
Lrp4 in hippocampal astrocytes serves as a negative feedback factor in seizures
Zheng, Y., Zhang, M., Luo, B., Jing, H., Yu, Y., Wang, S., & Luo, S. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00498-w · Cited by 8 · see citing works
Jin, S., Lin, C., Li, P., Wang, X., Wang, Y., Zhang, C., Wang, X., Peng, Y., Li, H., Lu, Y., et al. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.08.011 · Cited by 7 · see citing works
“Adenosine triphosphate (ATP), while mainly recognized as an intracellular energy molecule, also has extracellular functions, acting as neurotransmitters when in the form of ATP or its metabolite adenosine (ADO), affecting psychiatric conditions and drug addiction 11-14 .”
Wu, Y., Zhong, Y., Liao, X., Miao, X., Yu, J., Lai, X., Zhang, Y., Ma, C., Pan, H., & Wang, S. (2022) · Molecular Brain · doi:10.1186/s13041-022-00918-7 · Cited by 7 · see citing works
“Behavioral seizure score was according to the criteria by Racine [21]: stage 0, no seizure; stage 1, head nodding; stage 2, sporadic full-body shaking and spasms; stage 3, chronic full-body spasms; stage 4, jumping, shrieking, and falling over; stage 5, violent convulsions, falling over and dying.”
MethodBenvenga, S., Antonelli, A., Fallahi, P., Bonanno, C., Rodolico, C., & Guarneri, F. (2021) · Journal of Clinical & Translational Endocrinology · doi:10.1016/j.jcte.2021.100274 · Cited by 7 · see citing works
Sun, Q., Xu, W., Liu, Y., Zhan, S., Shao, X., Wu, Z., Weng, P., Cheng, K., & Zhang, X. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202101170 · Cited by 7 · see citing works
Neuregulin-1-dependent control of amygdala microcircuits is critical for fear extinction
Chen, M., Li, Y., Liu, Y., Xu, H., & Bi, L. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108842 · Cited by 6 · see citing works
Satb2 ablation decreases PTZ-induced seizure susceptibility and pyramidal neuronal excitability
Li, Y. Z., Huang, W. Y., Lv, C.-Y., Cong, J., Jie, W., Li, S. J., & Li, J. M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.05.006 · Cited by 6 · see citing works
Liu, Z., Li, Y., Wang, D.-L., Wang, Y., Qiu, W.-T., Qiu, Y.-Y., Zhang, H., You, Q.-L., Liu, S.-M., Liang, Q.-N., et al. (2024) · Cell & Bioscience · doi:10.1186/s13578-024-01241-5 · Cited by 5 · see citing works
“Results from a previous study have indicated that Lrp4 in astrocyte regulates ATP release, which could be degraded to adenosine quickly in the extracellular space [25].”
BackgroundMethodResultInfluentialSelf-citationTiming and localization of myasthenia gravis‐related gene expression
Vergoossen, D. L. E., Keo, A., Mahfouz, A. E., & Huijbers, M. G. M. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15382 · Cited by 5 · see citing works
Thyroid hormone rewires cortical circuits to coordinate body-wide metabolism and exploratory drivePreprint
Hochbaum, D. R., Dubinsky, A. C., Farnsworth, H. C., Hulshof, L., Kleinberg, G., Urke, A., Wang, W., Hakim, R., Robertson, K., Park, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.10.552874 · Cited by 5 · see citing works
Social Company by a Receptive Mating Partner Facilitates Fear Extinction
Gao, F., Huang, J., Guan, Y., Huang, G., Li, W., He, X.-Y., Qiu, Z., Zhang, Y., Zhao, S., Li, J., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00062 · Cited by 4 · see citing works
“The sample size choice was based on previous studies (Lu et al., 2014; Sun et al., 2016), and it was not predetermined by a statistical method.”
MethodSelf-citationNRG1-ErbB4 signaling in the medial amygdala controls mating motivation in adult male mice
Huang, J., Zhang, Y.-Y., Qiu, Y.-Y., Yao, S., Qiu, W.-T., Peng, J.-L., Li, Y., You, Q.-L., Wu, C.-H., Wu, E.-J., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113905 · Cited by 4 · see citing works
Self-citationCavieres-Lepe, J., & Stuardo, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2352-20.2021 · Cited by 4 · see citing works
Jain, K. K. (2019) · Springer protocols handbooks/Springer protocols · doi:10.1007/978-1-4939-9465-6_1 · Cited by 3 · see citing works
DePew, A. T., Bruckner, J. J., O’Connor-Giles, K. M., & Mosca, T. J. (2024) · Development · doi:10.1242/dev.202517 · Cited by 3 · see citing works
“We have now added an additional figure demonstrating that overexpression of SRPK79D in an lrp4 mutant background is also sufficient to rescue the active zone / glutamate receptor apposition defects we observe (Figure 8).”
Wang, J., Zhou, F., Wang, D., Li, J., Lu, D., Li, Q., Zhou, H., Li, W., Wang, Q., Wu, Y., et al. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.01.007 · Cited by 3 · see citing works
“Primary hippocampal astrocytes culture Culture of the primary hippocampal astrocytes was performed as described (Mamber et al., 2012; Schildge et al., 2013; Sun et al., 2016).”
Formation and synaptic control of active transient working memory representationsPreprint
Becker, S., Nold, A., & Tchumatchenko, T. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.30.273995 · Cited by 3 · see citing works
Gao, S., Lin, Q., Liu, X., Jia, M., Zhang, A.-Y., Feng, Z., Han, L., Qiu, N., Liu, X., Zhai, H., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-71922-x · Cited by 2 · see citing works
“Synaptic dysfunction is implicated in numerous neurological and psychiatricdisorders, includingASD 50 .”
Revisiting the Peripheral Nerve Injury and Regeneration
Liu, Z.-G., Zou, Y., Zhang, M.-X., Yang, F., Li, P., & Zhang, B.-Y. (2026) · NeuroMolecular Medicine · doi:10.1007/s12017-026-08914-z · Cited by 2 · see citing works
Arzola, E. P., Yu, G., Xiong, L., Lee, D., Wu, A., Paruchuri, S., Skinner, J., Wang, M., Zhang, B., Mei, L., et al. (2025) · Glia · doi:10.1002/glia.70114 · Cited by 1 · see citing works
“These results verified that Lrp4+ cells are astrocytes in the somato-sensory cortex (ssc), consistent with previous findings in the hippocampus (Sun et al. 2016; Zhang et al. 2020).”
Self-citationJiménez-Torres, A. C., Ortega, A. G., & Najimi, M. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1733612 · Cited by 1 · see citing works
Zhao, L., Qu, H. L., Zhang, Y., Wu, X., Ji, Q. X., Zhang, Z., & Li, D. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae237 · Cited by 1 · see citing works
Exploring Molecular Targets for Epilepsy Treatment from the Perspective of Neuronal Homeostasis
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LRP4 mediated synaptic plasticity in the piriform cortexPreprint
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“Lrp4LacZ/+mice were described before; in brief words, β-galactosidase (β-gal) protein cassette, including stop code and a polyadenylation termination signal, was inserted into the downstream of Lrp4 promoter[1].”
BackgroundResultInfluentialDePew, A. T., Bruckner, J. J., O’Connor-Giles, K. M., & Mosca, T. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.03.564481
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Identification of Mood Disorders Causal Genes by Integrating the Brain Proteome and Transcriptome
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“LRP4 modulates glutamatergic signaling and influences synaptic homeostasis between neurons and astrocytes, making it associated with neurological and psychiatric disorders [54].”
Gao, S., Lin, Q., Liu, X., Jia, M., Zhang, A., Feng, Z., Han, L., Qiu, N., Zhai, H., Zhang, X., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-6665030/v1
Additional file 1 of LRP4 is required for the olfactory association task in the piriform cortex
Yan, M., Xiong, M., Wu, Y., Lin, D., Chen, P., Chen, J., Liu, Z., Zhang, H., Ren, D., Fei, E., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19728580
Additional file 1 of Lrp4 in hippocampal astrocytes serves as a negative feedback factor in seizures
Yu, Z., Zhang, M., Luo, B., Jing, H., Yu, Y., Wang, S., & Luo, S. (2020) · Figshare · doi:10.6084/m9.figshare.13279460
Wu, Y., Zhong, Y., Liao, X., Miao, X., Yu, J., Lai, X., Zhang, Y., Ma, C., Pan, H., & Wang, S. (2022) · Figshare · doi:10.6084/m9.figshare.19581866
Jing, H., Chen, P., Hui, T., Yu, Z., Zhou, J., Fei, E., Wang, S., Ren, D., Lai, X., & Li, B. (2021) · Figshare · doi:10.6084/m9.figshare.14738690
Self-citation
- Authors
- Sun, X.-D., Li, L., Liu, F., Huang, Z.-H., Bean, J. C., Jiao, H.-F., Barik, A., Kim, S.-M., Wu, H., Shen, C., Tian, Y., Lin, T. W., Bates, R., Sathyamurthy, A., Chen, Y.-J., Yin, D.-M., Xiong, L., Lin, H.-P., Hu, J.-X., Li, B.-M., Gao, T.-M., Xiong, W.-C., & Mei, L.
- Affiliations
- Augusta University (US)
- Nanchang University (CN)
- Key Laboratory of Guangdong Province (CN)
- Corresponding author
- Sun, Xiang-Dong
- Mei, Lin
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2016-06-13
- Volume
- 19
- Issue
- 8
- Pages
- 1010-1018
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4961622
- OpenAlex
- W2429682989
- Cited by
- 102
- References
- 63
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 6 · 2023: 11 · 2022: 10 · 2021: 18 · 2020: 12 · 2019: 8 · 2018: 12 · 2017: 11 · 2016: 3
- FWCI
- 6.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX001020)
- National Institute of Mental Health (R01MH083317)
- National Institute of Neurological Disorders and Stroke (R01NS082007)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- LRP4, astrocytes, glutamatergic neurotransmission, ATP release, adenosine A1 receptor, agrin, neuron-glia interactions, synaptic transmission, synaptic homeostasis, synaptic plasticity, seizure resistance, spatial memory, locomotor activity, hippocampus, neuromuscular junction
- MeSH terms
- Adenosine Triphosphate, Animals, Astrocytes, Hippocampus, Synaptic Transmission, Neuromuscular Junction, Neuronal Plasticity, Receptors, Cholinergic, Receptors, LDL, Presynaptic Terminals, Agrin, Mice, Knockout, LDL-Receptor Related Proteins
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