Rac1 Modulates Excitatory Synaptic Transmission in Mouse Retinal Ganglion Cells
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摘要
Ras-related C3 botulinum toxin substrate 1(Racl),a member of the Rho GTPase family which plays important roles in dendritic spine morphology and plasticity,is a key regulator of cytoskeletal reorganization in dendrites and spines.Here,we investigated whether and how Racl modulates synaptic transmission in mouse retinal ganglion cells(RGCs)using selective conditional knockout of Racl(Racl-cKO).Racl-cKO significantly reduced the frequency of AMPA receptor-mediated miniature excitatory postsynaptic currents,while glycine/GABA_A receptor-mediated miniature inhibitory postsynaptic currents were not affected.Although the total GluA1 protein level was increased in Racl-cKO mice,its expression in the membrane component was unchanged.RaclcKO did not affect spine-like branch density in single dendrites,but significantly reduced the dendritic complexity,which resulted in a decrease in the total number of dendritic spine-like branches.These results suggest that Racl selectively affects excitatory synaptic transmission in RGCs by modulating dendritic complexity.
Ras-related C3 botulinum toxin substrate 1(Racl),a member of the Rho GTPase family which plays important roles in dendritic spine morphology and plasticity,is a key regulator of cytoskeletal reorganization in dendrites and spines.Here,we investigated whether and how Racl modulates synaptic transmission in mouse retinal ganglion cells(RGCs)using selective conditional knockout of Racl(Racl-cKO).Racl-cKO significantly reduced the frequency of AMPA receptor-mediated miniature excitatory postsynaptic currents,while glycine/GABA_A receptor-mediated miniature inhibitory postsynaptic currents were not affected.Although the total GluA1 protein level was increased in Racl-cKO mice,its expression in the membrane component was unchanged.RaclcKO did not affect spine-like branch density in single dendrites,but significantly reduced the dendritic complexity,which resulted in a decrease in the total number of dendritic spine-like branches.These results suggest that Racl selectively affects excitatory synaptic transmission in RGCs by modulating dendritic complexity.
Ras-related C3 botulinum toxin substrate 1(Racl),a member of the Rho GTPase family which plays important roles in dendritic spine morphology and plasticity,is a key regulator of cytoskeletal reorganization in dendrites and spines.Here,we investigated whether and how Racl modulates synaptic transmission in mouse retinal ganglion cells(RGCs)using selective conditional knockout of Racl(Racl-cKO).Racl-cKO significantly reduced the frequency of AMPA receptor-mediated miniature excitatory postsynaptic currents,while glycine/GABA_A receptor-mediated miniature inhibitory postsynaptic currents were not affected.Although the total GluA1 protein level was increased in Racl-cKO mice,its expression in the membrane component was unchanged.RaclcKO did not affect spine-like branch density in single dendrites,but significantly reduced the dendritic complexity,which resulted in a decrease in the total number of dendritic spine-like branches.These results suggest that Racl selectively affects excitatory synaptic transmission in RGCs by modulating dendritic complexity.
引文
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2.Tolias KF,Duman JG,Um K.Control of synapse development and plasticity by Rho GTPase regulatory proteins.Prog Neurobiol2011,94:133-148.
3.Linseman DA,Loucks FA.Diverse roles of Rho family GTPases in neuronal development,survival,and death.Front Biosci 2008,13:657-676.
4.Ridley AJ.Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking Trends.Cell Biol 2006,16:522-529.
5.Hoffman GR,Nassar N,Cerione RA.Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI.Cell 2000,100:345-356.
6.Zalcman G,Dorseuil O,Garcia-Ranea JA,Gacon G,Camonis J.RhoGAPs and RhoGDIs,(His)stories of two families.Prog Mol Subcell Biol 1999,22:85-113.
7.Bustelo XR,Sauzeau V,Berenjeno IM.GTP-binding proteins of the Rho/Rac family:regulation,effectors and functions in vivo.Bioessays 2007,29:356-370.
8.Cingolani LA,Goda Y.Actin in action:the interplay between the actin cytoskeleton and synaptic efficacy.Nat Rev Neurosci 2008,9:344-356.
9.Davis RL.Rac in the act of forgetting.Cell 2010,140:456-458.
10.Etienne-Manneville S,Hall A.Rho GTPases in cell biology.Nature 2012,420:629-635.
11.Hall A,Lalli G.Rho and Ras GTPases in axon growth,guidance,and branching.Cold Spring Harb Perspect Biol 2010,2:a001818.
12.Shuai Y,Zhong Y.Forgetting and small G protein Rac Protein.Protein Cell 2010,1:503-506.
13.Mitchell DC,Bryan BA,Liu JP,Liu WB,Zhang L,Qu J,et al.Developmental expression of three small GTPases in the mouse eye.Mol Vis 2007,13:1144-1153.
14.Namekata K,Kimura A,Kawamura K,Guo X,Harada C,Tanaka K,et al.Dock3 attenuates neural cell death due to NMDAneurotoxicity and oxidative stress in a mouse model of normal tension glaucoma.Cell Death Differ 2013,20:1250-1256.
15.Lorenzetto E,Ettorre M,Pontelli V,Bolomini-Vittori M,Bolognin S,Zorzan S,et al.Rac1 selective activation improves retina ganglion cell survival and regeneration.PLoS One 2013,8:e64350.
16.Dong N,Xu B,Shi H,Lu Y.miR-124 Regulates AmadoriGlycated Albumin-Induced Retinal Microglial Activation and Inflammation by Targeting Rac1.Invest Ophthalmol Vis Sci2016,57:2522-2532.
17.Li YJ,Zhang J,Han J,Du ZJ,Wang P,Guo Y.Ras-related C3botulinum toxin substrate 1 activation is involved in the pathogenesis of diabetic retinopathy.Exp Ther Med 2015,9:89-97.
18.Marc RE,Liu W.Fundamental GABAergic amacrine cell circuitries in the retina:nested feedback,concatenated inhibition,and axosomatic synapses.J Comp Neurol 2000,425:560-582.
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20.Wassle H.Parallel processing in the mammalian retina.Nat Rev Neurosci 2004,5:747-757.
21.Wassle H,Boycott BB.Functional architecture of the mammalian retina.Physiol Rev 1991,71:447-480.
22.Dong LD,Gao F,Wang XH,Miao Y,Wang SY,Wu Y,et al.GluA2 trafficking is involved in apoptosis of retinal ganglion cells induced by activation of EphB/EphrinB reverse signaling in a rat chronic ocular hypertension model.J Neurosci 2015,35:5409-5421.
23.Gao F,Li F,Miao Y,Xu LJ,Zhao Y,Li Q,et al.Involvement of the MEK-ERK/p38-CREB/c-fos signaling pathway in Kir channel inhibition-induced rat retinal Muller cell gliosis.Sci Rep2017,7:1480.
24.Li C,Chen T.A novel hematoxylin and eosin stain assay for detection of the parasitic dinoflagellate amoebophrya.Harmful Algae 2017,62:30-36.
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26.Cui P,Li XY,Zhao Y,Li Q,Gao F,Li LZ,et al.Activation of dopamine D1 receptors enhances the temporal summation and excitability of rat retinal ganglion cells.Neuroscience 2017,355:71-83.
27.Wang XH,Wu Y,Yang XF,Miao Y,Zhang CQ,Dong LD,et al.Cannabinoid CB1 receptor signaling dichotomously modulates inhibitory and excitatory synaptic transmission in rat inner retina.Brain Struct Funct 2016b,221:301-316.
28.Li Q,Cui P,Miao Y,Gao F,Li XY,Qian WJ,et al.Activation of group I metabotropic glutamate receptors regulates the excitability of rat retinal ganglion cells by suppressing Kir and I h.Brain Struct Funct 2017,222:813-830.
29.Qian WJ,Yin N,Gao F,Miao Y,Li Q,Li F,et al.Cannabinoid CB1 and CB2 receptors differentially modulate L-and T-type Ca2?channels in rat retinal ganglion cells.Neuropharmacology2017,124:143-156.
30.Ramoa AS,Campbell G,Shatz CJ.Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development.J Neurosci 1988,8:4239-4261.
31.Liu HM,Sang SM,Lu Y,Wang ZF,Yu X,Zhong CJ.Thiamine metabolism is critical for regulating correlated growth of dendrite arbors and neuronal somata.Sci Rep 2017,7:5342.
32.Williams PA,Thirgood RA,Oliphant H,Frizzati A,Littlewood E,Votruba M,et al.Retinal ganglion cell dendritic degeneration in a mouse model of Alzheimer’s disease.Neurobiol Aging 2013,34:1799-1806.
33.Zhao Y,Li Q,Li XY,Cui P,Gao F,Zhu K,et al.Involvement of mGluR I in EphB/ephrinB reverse signaling activation induced retinal ganglion cell apoptosis in a rat chronic hypertension model.Brain Res 2018,1683:27-35.
34.Erickson CS,Lee SJ,Barlow-Anacker AJ,Druckenbrod NR,Epstein ML,Gosain A.Appearance of cholinergic myenteric neurons during enteric nervous system development:comparison of different ChAT fluorescent mouse reporter lines.Neurogastroenterol Motil 2014,26:874-884.
35.Ivanova E,Hwang GS,Pan ZH.Characterization of transgenic mouse lines expressing Cre recombinase in the retina.Neuroscience 2010,165:233-243.
36.Bongmba OY,Martinez LA,Elhardt ME,Butler K,TejadaSimon MV.Modulation of dendritic spines and synaptic function by Rac1:a possible link to Fragile X syndrome pathology.Brain Res 2011,1399:79-95.
37.Lee T,Winter C,Marticke SS,Lee A,Luo L.Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis.Neuron 2000,25:307-316.
38.Luo L,Hensch TK,Ackerman L,Barbel S,Jan LY,Jan YN.Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines.Nature 1996,379:837-840.
39.Nakayama AY,Harms MB,Luo L.Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons.J Neurosci 2000,20:5329-5338.
40.Ruchhoeft ML,Ohnuma S,McNeill L,Holt CE,Harris WA.The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo.J Neurosci 1999,19:8454-8463.
41.Tashiro A,Minden A,Yuste R.Regulation of dendritic spine morphology by the Rho family of small GTPases:Antagonistic roles of Rac and Rho.Cereb Cortex 2000,10:927-938.
42.Threadgill R,Bobb K,Ghosh A.Regulation of dendritic growth and remodeling by Rho,Rac,and Cdc42.Neuron 1997,19:625-634.
43.Sun W,Li N,He S.Large-scale morphological survey of mouse retinal ganglion cells.J Comp Neurol 2002,451:115-126.
44.Caserta F,Eldred WD,Fernandez E,Hausman RE,Stanford LR,Bulderev SV,et al..Determination of fractal dimension of physiologically characterized neurons in two and three dimensions.J Neurosci Methods 1995,56:133-144.
45.Duan H,Wearne SL,Rocher AB,Macedo A,Morrison JH,Hof PR.Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys.Cereb Cortex 2003,13:950-961.
46.Gutierrez H,Davies AM.A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology.J Neurosci Methods 2007,163:24-30.
47.Haas K,Li J,Cline HT.AMPA receptors regulate experiencedependent dendritic arbor growth in vivo.Proc Natl Acad Sci U SA 2006,103:12127-12131.
48.Lowndes M,Stanford D,Stewart MG.A system for the reconstruction and analysis of dendritic fields.J Neurosci Methods 1990,31:235-245.
49.Robinson TE,Kolb B.Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine.J Neurosci 1997,17:8491-8497.
50.Zagrebelsky M,Holz A,Dechant G,Barde YA,Bonhoeffer T,Korte M.The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons.J Neurosci 2005,25:9989-9999.
51.Sholl DA.Dendritic organization in the neurons of the visual and motor cortices of the cat.J Anat 1953,87:387-406.
52.Branda CS,Dymecki SM.Talking about a revolution:The impact of site-specific recombinases on genetic analyses in mice.Dev Cell 2004,6:7-28.
53.Nagy A.Cre recombinase:the universal reagent for genome tailoring.Genesis 2000,26:99-109.
54.Larsen AK,Osborne NN.Involvement of adenosine in retinal ischemia.Studies on the rat.Invest Ophthalmol Vis Sci 1996,37:2603-2611.
55.Rom S,Fan S,Reichenbach N,Dykstra H,Ramirez SH,Persidsky Y.Glycogen synthase kinase 3beta inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation.Am J Pathol 2012,181:1414-1425.
56.Rom S,Zuluaga-Ramirez V,Dykstra H,Reichenbach NL,Pacher P,Persidsky Y.Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier.Am J Pathol 2013,183:1548-1558.
57.Dyka FM,May CA,Enz R.Metabotropic glutamate receptors are differentially regulated under elevated intraocular pressure.J Neurochem 2004,90:190-202.
58.Koulen,P,Kuhn R,Wassle H,Brandstatter JH.Group Imetabotropic glutamate receptors mGluR1alpha and mGluR5a:localization in both synaptic layers of the rat retina.J Neurosci1997,17:2200-2211.
59.Tehrani A,Wheeler-Schilling TH,Guenther E.Coexpression patterns of mGLuR mRNAs in rat retinal ganglion cells:a singlecell RT-PCR study.Invest Ophthalmol Vis Sci 2000,41:314-319.
60.Ji M,Miao Y,Dong LD,Chen J,Mo XF,Jiang,SX,et al.Group ImGluR-mediated inhibition of Kir channels contributes to retinal Muller cell gliosis in a rat chronic ocular hypertension model.J Neurosci 2012,32:12744-12755.
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2.Tolias KF,Duman JG,Um K.Control of synapse development and plasticity by Rho GTPase regulatory proteins.Prog Neurobiol2011,94:133-148.
3.Linseman DA,Loucks FA.Diverse roles of Rho family GTPases in neuronal development,survival,and death.Front Biosci 2008,13:657-676.
4.Ridley AJ.Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking Trends.Cell Biol 2006,16:522-529.
5.Hoffman GR,Nassar N,Cerione RA.Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI.Cell 2000,100:345-356.
6.Zalcman G,Dorseuil O,Garcia-Ranea JA,Gacon G,Camonis J.RhoGAPs and RhoGDIs,(His)stories of two families.Prog Mol Subcell Biol 1999,22:85-113.
7.Bustelo XR,Sauzeau V,Berenjeno IM.GTP-binding proteins of the Rho/Rac family:regulation,effectors and functions in vivo.Bioessays 2007,29:356-370.
8.Cingolani LA,Goda Y.Actin in action:the interplay between the actin cytoskeleton and synaptic efficacy.Nat Rev Neurosci 2008,9:344-356.
9.Davis RL.Rac in the act of forgetting.Cell 2010,140:456-458.
10.Etienne-Manneville S,Hall A.Rho GTPases in cell biology.Nature 2012,420:629-635.
11.Hall A,Lalli G.Rho and Ras GTPases in axon growth,guidance,and branching.Cold Spring Harb Perspect Biol 2010,2:a001818.
12.Shuai Y,Zhong Y.Forgetting and small G protein Rac Protein.Protein Cell 2010,1:503-506.
13.Mitchell DC,Bryan BA,Liu JP,Liu WB,Zhang L,Qu J,et al.Developmental expression of three small GTPases in the mouse eye.Mol Vis 2007,13:1144-1153.
14.Namekata K,Kimura A,Kawamura K,Guo X,Harada C,Tanaka K,et al.Dock3 attenuates neural cell death due to NMDAneurotoxicity and oxidative stress in a mouse model of normal tension glaucoma.Cell Death Differ 2013,20:1250-1256.
15.Lorenzetto E,Ettorre M,Pontelli V,Bolomini-Vittori M,Bolognin S,Zorzan S,et al.Rac1 selective activation improves retina ganglion cell survival and regeneration.PLoS One 2013,8:e64350.
16.Dong N,Xu B,Shi H,Lu Y.miR-124 Regulates AmadoriGlycated Albumin-Induced Retinal Microglial Activation and Inflammation by Targeting Rac1.Invest Ophthalmol Vis Sci2016,57:2522-2532.
17.Li YJ,Zhang J,Han J,Du ZJ,Wang P,Guo Y.Ras-related C3botulinum toxin substrate 1 activation is involved in the pathogenesis of diabetic retinopathy.Exp Ther Med 2015,9:89-97.
18.Marc RE,Liu W.Fundamental GABAergic amacrine cell circuitries in the retina:nested feedback,concatenated inhibition,and axosomatic synapses.J Comp Neurol 2000,425:560-582.
19.Protti DA,Gerschenfeld HM,Llano I.GABAergic and glycinergic IPSCs in ganglion cells of rat retinal slices.J Neurosci1997,17:6075-6085.
20.Wassle H.Parallel processing in the mammalian retina.Nat Rev Neurosci 2004,5:747-757.
21.Wassle H,Boycott BB.Functional architecture of the mammalian retina.Physiol Rev 1991,71:447-480.
22.Dong LD,Gao F,Wang XH,Miao Y,Wang SY,Wu Y,et al.GluA2 trafficking is involved in apoptosis of retinal ganglion cells induced by activation of EphB/EphrinB reverse signaling in a rat chronic ocular hypertension model.J Neurosci 2015,35:5409-5421.
23.Gao F,Li F,Miao Y,Xu LJ,Zhao Y,Li Q,et al.Involvement of the MEK-ERK/p38-CREB/c-fos signaling pathway in Kir channel inhibition-induced rat retinal Muller cell gliosis.Sci Rep2017,7:1480.
24.Li C,Chen T.A novel hematoxylin and eosin stain assay for detection of the parasitic dinoflagellate amoebophrya.Harmful Algae 2017,62:30-36.
25.Miao Y,Dong LD,Chen J,Hu XC,Yang XL,Wang Z.Involvement of calpain/p35-p25/Cdk5/NMDAR signaling pathway in glutamate-induced neurotoxicity in cultured rat retinal neurons.PLoS One 2012,7:e42318.
26.Cui P,Li XY,Zhao Y,Li Q,Gao F,Li LZ,et al.Activation of dopamine D1 receptors enhances the temporal summation and excitability of rat retinal ganglion cells.Neuroscience 2017,355:71-83.
27.Wang XH,Wu Y,Yang XF,Miao Y,Zhang CQ,Dong LD,et al.Cannabinoid CB1 receptor signaling dichotomously modulates inhibitory and excitatory synaptic transmission in rat inner retina.Brain Struct Funct 2016b,221:301-316.
28.Li Q,Cui P,Miao Y,Gao F,Li XY,Qian WJ,et al.Activation of group I metabotropic glutamate receptors regulates the excitability of rat retinal ganglion cells by suppressing Kir and I h.Brain Struct Funct 2017,222:813-830.
29.Qian WJ,Yin N,Gao F,Miao Y,Li Q,Li F,et al.Cannabinoid CB1 and CB2 receptors differentially modulate L-and T-type Ca2?channels in rat retinal ganglion cells.Neuropharmacology2017,124:143-156.
30.Ramoa AS,Campbell G,Shatz CJ.Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development.J Neurosci 1988,8:4239-4261.
31.Liu HM,Sang SM,Lu Y,Wang ZF,Yu X,Zhong CJ.Thiamine metabolism is critical for regulating correlated growth of dendrite arbors and neuronal somata.Sci Rep 2017,7:5342.
32.Williams PA,Thirgood RA,Oliphant H,Frizzati A,Littlewood E,Votruba M,et al.Retinal ganglion cell dendritic degeneration in a mouse model of Alzheimer’s disease.Neurobiol Aging 2013,34:1799-1806.
33.Zhao Y,Li Q,Li XY,Cui P,Gao F,Zhu K,et al.Involvement of mGluR I in EphB/ephrinB reverse signaling activation induced retinal ganglion cell apoptosis in a rat chronic hypertension model.Brain Res 2018,1683:27-35.
34.Erickson CS,Lee SJ,Barlow-Anacker AJ,Druckenbrod NR,Epstein ML,Gosain A.Appearance of cholinergic myenteric neurons during enteric nervous system development:comparison of different ChAT fluorescent mouse reporter lines.Neurogastroenterol Motil 2014,26:874-884.
35.Ivanova E,Hwang GS,Pan ZH.Characterization of transgenic mouse lines expressing Cre recombinase in the retina.Neuroscience 2010,165:233-243.
36.Bongmba OY,Martinez LA,Elhardt ME,Butler K,TejadaSimon MV.Modulation of dendritic spines and synaptic function by Rac1:a possible link to Fragile X syndrome pathology.Brain Res 2011,1399:79-95.
37.Lee T,Winter C,Marticke SS,Lee A,Luo L.Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis.Neuron 2000,25:307-316.
38.Luo L,Hensch TK,Ackerman L,Barbel S,Jan LY,Jan YN.Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines.Nature 1996,379:837-840.
39.Nakayama AY,Harms MB,Luo L.Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons.J Neurosci 2000,20:5329-5338.
40.Ruchhoeft ML,Ohnuma S,McNeill L,Holt CE,Harris WA.The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo.J Neurosci 1999,19:8454-8463.
41.Tashiro A,Minden A,Yuste R.Regulation of dendritic spine morphology by the Rho family of small GTPases:Antagonistic roles of Rac and Rho.Cereb Cortex 2000,10:927-938.
42.Threadgill R,Bobb K,Ghosh A.Regulation of dendritic growth and remodeling by Rho,Rac,and Cdc42.Neuron 1997,19:625-634.
43.Sun W,Li N,He S.Large-scale morphological survey of mouse retinal ganglion cells.J Comp Neurol 2002,451:115-126.
44.Caserta F,Eldred WD,Fernandez E,Hausman RE,Stanford LR,Bulderev SV,et al..Determination of fractal dimension of physiologically characterized neurons in two and three dimensions.J Neurosci Methods 1995,56:133-144.
45.Duan H,Wearne SL,Rocher AB,Macedo A,Morrison JH,Hof PR.Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys.Cereb Cortex 2003,13:950-961.
46.Gutierrez H,Davies AM.A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology.J Neurosci Methods 2007,163:24-30.
47.Haas K,Li J,Cline HT.AMPA receptors regulate experiencedependent dendritic arbor growth in vivo.Proc Natl Acad Sci U SA 2006,103:12127-12131.
48.Lowndes M,Stanford D,Stewart MG.A system for the reconstruction and analysis of dendritic fields.J Neurosci Methods 1990,31:235-245.
49.Robinson TE,Kolb B.Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine.J Neurosci 1997,17:8491-8497.
50.Zagrebelsky M,Holz A,Dechant G,Barde YA,Bonhoeffer T,Korte M.The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons.J Neurosci 2005,25:9989-9999.
51.Sholl DA.Dendritic organization in the neurons of the visual and motor cortices of the cat.J Anat 1953,87:387-406.
52.Branda CS,Dymecki SM.Talking about a revolution:The impact of site-specific recombinases on genetic analyses in mice.Dev Cell 2004,6:7-28.
53.Nagy A.Cre recombinase:the universal reagent for genome tailoring.Genesis 2000,26:99-109.
54.Larsen AK,Osborne NN.Involvement of adenosine in retinal ischemia.Studies on the rat.Invest Ophthalmol Vis Sci 1996,37:2603-2611.
55.Rom S,Fan S,Reichenbach N,Dykstra H,Ramirez SH,Persidsky Y.Glycogen synthase kinase 3beta inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation.Am J Pathol 2012,181:1414-1425.
56.Rom S,Zuluaga-Ramirez V,Dykstra H,Reichenbach NL,Pacher P,Persidsky Y.Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier.Am J Pathol 2013,183:1548-1558.
57.Dyka FM,May CA,Enz R.Metabotropic glutamate receptors are differentially regulated under elevated intraocular pressure.J Neurochem 2004,90:190-202.
58.Koulen,P,Kuhn R,Wassle H,Brandstatter JH.Group Imetabotropic glutamate receptors mGluR1alpha and mGluR5a:localization in both synaptic layers of the rat retina.J Neurosci1997,17:2200-2211.
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