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Ras and Rap Signal Bidirectional Synaptic Plasticity via Distinct Subcellular Microdomains

How signaling molecules achieve signal diversity and specificity is a long-standing cell biology question. Here we report the development of a targeted delivery method that permits specific expression of homologous Ras-family small GTPases (i.e., Ras, Rap2, and Rap1) in different subcellular microdo... Full description

Journal Title: Neuron (Cambridge Mass.), 2018-05-16, Vol.98 (4), p.783-800.e4
Main Author: Zhang, Lei
Other Authors: Zhang, Peng , Wang, Guangfu , Zhang, Huaye , Zhang, Yajun , Yu, Yilin , Zhang, Mingxu , Xiao, Jian , Crespo, Piero , Hell, Johannes W , Lin, Li , Huganir, Richard L , Zhu, J. Julius
Format: Electronic Article Electronic Article
Language: English
Subjects:
Quelle: Alma/SFX Local Collection
Publisher: United States: Elsevier Inc
ID: ISSN: 0896-6273
Link: https://www.ncbi.nlm.nih.gov/pubmed/29706584
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6192044
title: Ras and Rap Signal Bidirectional Synaptic Plasticity via Distinct Subcellular Microdomains
format: Article
creator:
  • Zhang, Lei
  • Zhang, Peng
  • Wang, Guangfu
  • Zhang, Huaye
  • Zhang, Yajun
  • Yu, Yilin
  • Zhang, Mingxu
  • Xiao, Jian
  • Crespo, Piero
  • Hell, Johannes W
  • Lin, Li
  • Huganir, Richard L
  • Zhu, J. Julius
subjects:
  • 1-Phosphatidylinositol 3-kinase
  • AMPA-R phorphorylation
  • AMPA-R trafficking
  • Analysis
  • Animals
  • Article
  • CA1 Region, Hippocampal - cytology
  • CA1 Region, Hippocampal - metabolism
  • Cells
  • endocrine system
  • Endoplasmic reticulum
  • Endoplasmic Reticulum - metabolism
  • Excitatory Postsynaptic Potentials
  • Experiments
  • Extracellular signal-regulated kinase
  • G proteins
  • GluA1
  • GluA2
  • GluA2L
  • GluA4
  • Golgi apparatus
  • Golgi Apparatus - metabolism
  • Grants
  • Hippocampus
  • In Vitro Techniques
  • Kinases
  • Lipid rafts
  • Lipids
  • Long-term depression
  • Long-Term Potentiation
  • Long-Term Synaptic Depression
  • Lysosomes
  • Lysosomes - metabolism
  • MAP Kinase Signaling System
  • Medical colleges
  • Membrane Microdomains - metabolism
  • Mice
  • nanocluster
  • Neuronal Plasticity
  • Neurons
  • Neurons - metabolism
  • Neurosciences
  • organelle fractionation
  • p38 Mitogen-Activated Protein Kinases - metabolism
  • Patch-Clamp Techniques
  • Phosphatidylinositol 3-Kinases - metabolism
  • Physiology
  • Potentiation
  • Proteins
  • rap GTP-Binding Proteins - metabolism
  • rap1 GTP-Binding Proteins - metabolism
  • Rap1 protein
  • Ras protein
  • ras Proteins - metabolism
  • Rats
  • Receptors, AMPA - metabolism
  • Signal Transduction
  • subcellular signaling
  • Synaptic plasticity
  • Synaptic Transmission
ispartof: Neuron (Cambridge, Mass.), 2018-05-16, Vol.98 (4), p.783-800.e4
description: How signaling molecules achieve signal diversity and specificity is a long-standing cell biology question. Here we report the development of a targeted delivery method that permits specific expression of homologous Ras-family small GTPases (i.e., Ras, Rap2, and Rap1) in different subcellular microdomains, including the endoplasmic reticulum, lipid rafts, bulk membrane, lysosomes, and Golgi complex, in rodent hippocampal CA1 neurons. The microdomain-targeted delivery, combined with multicolor fluorescence protein tagging and high-resolution dual-quintuple simultaneous patch-clamp recordings, allows systematic analysis of microdomain-specific signaling. The analysis shows that Ras signals long-term potentiation via endoplasmic reticulum PI3K and lipid raft ERK, whereas Rap2 and Rap1 signal depotentiation and long-term depression via bulk membrane JNK and lysosome p38MAPK, respectively. These results establish an effective subcellular microdomain-specific targeted delivery method and unveil subcellular microdomain-specific signaling as the mechanism for homologous Ras and Rap to achieve signal diversity and specificity to control multiple forms of synaptic plasticity. •Microdomain-targeted delivery method reveals signal diversity and specificity•Endoplasmic reticulum Ras-PI3K and lipid rafts Ras-ERK signal long-term potentiation•Bulk membrane Rap2-JNK signals depotentiation•Lysosome Rap1-p38MAPK signals long-term depression Zhang et al. develop an effective subcellular microdomain-specific targeted delivery method and demonstrate that homologous proteins (e.g., Ras and Rap) confine their signaling within distinct subcellular microdomains to achieve signal transduction diversity and specificity.
language: eng
source: Alma/SFX Local Collection
identifier: ISSN: 0896-6273
fulltext: fulltext
issn:
  • 0896-6273
  • 1097-4199
url: Link


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titleRas and Rap Signal Bidirectional Synaptic Plasticity via Distinct Subcellular Microdomains
sourceAlma/SFX Local Collection
creatorZhang, Lei ; Zhang, Peng ; Wang, Guangfu ; Zhang, Huaye ; Zhang, Yajun ; Yu, Yilin ; Zhang, Mingxu ; Xiao, Jian ; Crespo, Piero ; Hell, Johannes W ; Lin, Li ; Huganir, Richard L ; Zhu, J. Julius
creatorcontribZhang, Lei ; Zhang, Peng ; Wang, Guangfu ; Zhang, Huaye ; Zhang, Yajun ; Yu, Yilin ; Zhang, Mingxu ; Xiao, Jian ; Crespo, Piero ; Hell, Johannes W ; Lin, Li ; Huganir, Richard L ; Zhu, J. Julius
descriptionHow signaling molecules achieve signal diversity and specificity is a long-standing cell biology question. Here we report the development of a targeted delivery method that permits specific expression of homologous Ras-family small GTPases (i.e., Ras, Rap2, and Rap1) in different subcellular microdomains, including the endoplasmic reticulum, lipid rafts, bulk membrane, lysosomes, and Golgi complex, in rodent hippocampal CA1 neurons. The microdomain-targeted delivery, combined with multicolor fluorescence protein tagging and high-resolution dual-quintuple simultaneous patch-clamp recordings, allows systematic analysis of microdomain-specific signaling. The analysis shows that Ras signals long-term potentiation via endoplasmic reticulum PI3K and lipid raft ERK, whereas Rap2 and Rap1 signal depotentiation and long-term depression via bulk membrane JNK and lysosome p38MAPK, respectively. These results establish an effective subcellular microdomain-specific targeted delivery method and unveil subcellular microdomain-specific signaling as the mechanism for homologous Ras and Rap to achieve signal diversity and specificity to control multiple forms of synaptic plasticity. •Microdomain-targeted delivery method reveals signal diversity and specificity•Endoplasmic reticulum Ras-PI3K and lipid rafts Ras-ERK signal long-term potentiation•Bulk membrane Rap2-JNK signals depotentiation•Lysosome Rap1-p38MAPK signals long-term depression Zhang et al. develop an effective subcellular microdomain-specific targeted delivery method and demonstrate that homologous proteins (e.g., Ras and Rap) confine their signaling within distinct subcellular microdomains to achieve signal transduction diversity and specificity.
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0ISSN: 0896-6273
1EISSN: 1097-4199
2DOI: 10.1016/j.neuron.2018.03.049
3PMID: 29706584
languageeng
publisherUnited States: Elsevier Inc
subject1-Phosphatidylinositol 3-kinase ; AMPA-R phorphorylation ; AMPA-R trafficking ; Analysis ; Animals ; Article ; CA1 Region, Hippocampal - cytology ; CA1 Region, Hippocampal - metabolism ; Cells ; endocrine system ; Endoplasmic reticulum ; Endoplasmic Reticulum - metabolism ; Excitatory Postsynaptic Potentials ; Experiments ; Extracellular signal-regulated kinase ; G proteins ; GluA1 ; GluA2 ; GluA2L ; GluA4 ; Golgi apparatus ; Golgi Apparatus - metabolism ; Grants ; Hippocampus ; In Vitro Techniques ; Kinases ; Lipid rafts ; Lipids ; Long-term depression ; Long-Term Potentiation ; Long-Term Synaptic Depression ; Lysosomes ; Lysosomes - metabolism ; MAP Kinase Signaling System ; Medical colleges ; Membrane Microdomains - metabolism ; Mice ; nanocluster ; Neuronal Plasticity ; Neurons ; Neurons - metabolism ; Neurosciences ; organelle fractionation ; p38 Mitogen-Activated Protein Kinases - metabolism ; Patch-Clamp Techniques ; Phosphatidylinositol 3-Kinases - metabolism ; Physiology ; Potentiation ; Proteins ; rap GTP-Binding Proteins - metabolism ; rap1 GTP-Binding Proteins - metabolism ; Rap1 protein ; Ras protein ; ras Proteins - metabolism ; Rats ; Receptors, AMPA - metabolism ; Signal Transduction ; subcellular signaling ; Synaptic plasticity ; Synaptic Transmission
ispartofNeuron (Cambridge, Mass.), 2018-05-16, Vol.98 (4), p.783-800.e4
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1Zhang, Peng
2Wang, Guangfu
3Zhang, Huaye
4Zhang, Yajun
5Yu, Yilin
6Zhang, Mingxu
7Xiao, Jian
8Crespo, Piero
9Hell, Johannes W
10Lin, Li
11Huganir, Richard L
12Zhu, J. Julius
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0Ras and Rap Signal Bidirectional Synaptic Plasticity via Distinct Subcellular Microdomains
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descriptionHow signaling molecules achieve signal diversity and specificity is a long-standing cell biology question. Here we report the development of a targeted delivery method that permits specific expression of homologous Ras-family small GTPases (i.e., Ras, Rap2, and Rap1) in different subcellular microdomains, including the endoplasmic reticulum, lipid rafts, bulk membrane, lysosomes, and Golgi complex, in rodent hippocampal CA1 neurons. The microdomain-targeted delivery, combined with multicolor fluorescence protein tagging and high-resolution dual-quintuple simultaneous patch-clamp recordings, allows systematic analysis of microdomain-specific signaling. The analysis shows that Ras signals long-term potentiation via endoplasmic reticulum PI3K and lipid raft ERK, whereas Rap2 and Rap1 signal depotentiation and long-term depression via bulk membrane JNK and lysosome p38MAPK, respectively. These results establish an effective subcellular microdomain-specific targeted delivery method and unveil subcellular microdomain-specific signaling as the mechanism for homologous Ras and Rap to achieve signal diversity and specificity to control multiple forms of synaptic plasticity. •Microdomain-targeted delivery method reveals signal diversity and specificity•Endoplasmic reticulum Ras-PI3K and lipid rafts Ras-ERK signal long-term potentiation•Bulk membrane Rap2-JNK signals depotentiation•Lysosome Rap1-p38MAPK signals long-term depression Zhang et al. develop an effective subcellular microdomain-specific targeted delivery method and demonstrate that homologous proteins (e.g., Ras and Rap) confine their signaling within distinct subcellular microdomains to achieve signal transduction diversity and specificity.
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01-Phosphatidylinositol 3-kinase
1AMPA-R phorphorylation
2AMPA-R trafficking
3Analysis
4Animals
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6CA1 Region, Hippocampal - cytology
7CA1 Region, Hippocampal - metabolism
8Cells
9endocrine system
10Endoplasmic reticulum
11Endoplasmic Reticulum - metabolism
12Excitatory Postsynaptic Potentials
13Experiments
14Extracellular signal-regulated kinase
15G proteins
16GluA1
17GluA2
18GluA2L
19GluA4
20Golgi apparatus
21Golgi Apparatus - metabolism
22Grants
23Hippocampus
24In Vitro Techniques
25Kinases
26Lipid rafts
27Lipids
28Long-term depression
29Long-Term Potentiation
30Long-Term Synaptic Depression
31Lysosomes
32Lysosomes - metabolism
33MAP Kinase Signaling System
34Medical colleges
35Membrane Microdomains - metabolism
36Mice
37nanocluster
38Neuronal Plasticity
39Neurons
40Neurons - metabolism
41Neurosciences
42organelle fractionation
43p38 Mitogen-Activated Protein Kinases - metabolism
44Patch-Clamp Techniques
45Phosphatidylinositol 3-Kinases - metabolism
46Physiology
47Potentiation
48Proteins
49rap GTP-Binding Proteins - metabolism
50rap1 GTP-Binding Proteins - metabolism
51Rap1 protein
52Ras protein
53ras Proteins - metabolism
54Rats
55Receptors, AMPA - metabolism
56Signal Transduction
57subcellular signaling
58Synaptic plasticity
59Synaptic Transmission
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titleRas and Rap Signal Bidirectional Synaptic Plasticity via Distinct Subcellular Microdomains
authorZhang, Lei ; Zhang, Peng ; Wang, Guangfu ; Zhang, Huaye ; Zhang, Yajun ; Yu, Yilin ; Zhang, Mingxu ; Xiao, Jian ; Crespo, Piero ; Hell, Johannes W ; Lin, Li ; Huganir, Richard L ; Zhu, J. Julius
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01-Phosphatidylinositol 3-kinase
1AMPA-R phorphorylation
2AMPA-R trafficking
3Analysis
4Animals
5Article
6CA1 Region, Hippocampal - cytology
7CA1 Region, Hippocampal - metabolism
8Cells
9endocrine system
10Endoplasmic reticulum
11Endoplasmic Reticulum - metabolism
12Excitatory Postsynaptic Potentials
13Experiments
14Extracellular signal-regulated kinase
15G proteins
16GluA1
17GluA2
18GluA2L
19GluA4
20Golgi apparatus
21Golgi Apparatus - metabolism
22Grants
23Hippocampus
24In Vitro Techniques
25Kinases
26Lipid rafts
27Lipids
28Long-term depression
29Long-Term Potentiation
30Long-Term Synaptic Depression
31Lysosomes
32Lysosomes - metabolism
33MAP Kinase Signaling System
34Medical colleges
35Membrane Microdomains - metabolism
36Mice
37nanocluster
38Neuronal Plasticity
39Neurons
40Neurons - metabolism
41Neurosciences
42organelle fractionation
43p38 Mitogen-Activated Protein Kinases - metabolism
44Patch-Clamp Techniques
45Phosphatidylinositol 3-Kinases - metabolism
46Physiology
47Potentiation
48Proteins
49rap GTP-Binding Proteins - metabolism
50rap1 GTP-Binding Proteins - metabolism
51Rap1 protein
52Ras protein
53ras Proteins - metabolism
54Rats
55Receptors, AMPA - metabolism
56Signal Transduction
57subcellular signaling
58Synaptic plasticity
59Synaptic Transmission
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8Crespo, Piero
9Hell, Johannes W
10Lin, Li
11Huganir, Richard L
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1Zhang, Peng
2Wang, Guangfu
3Zhang, Huaye
4Zhang, Yajun
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7Xiao, Jian
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9Hell, Johannes W
10Lin, Li
11Huganir, Richard L
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notesContribute equally
abstractHow signaling molecules achieve signal diversity and specificity is a long-standing cell biology question. Here we report the development of a targeted delivery method that permits specific expression of homologous Ras-family small GTPases (i.e., Ras, Rap2, and Rap1) in different subcellular microdomains, including the endoplasmic reticulum, lipid rafts, bulk membrane, lysosomes, and Golgi complex, in rodent hippocampal CA1 neurons. The microdomain-targeted delivery, combined with multicolor fluorescence protein tagging and high-resolution dual-quintuple simultaneous patch-clamp recordings, allows systematic analysis of microdomain-specific signaling. The analysis shows that Ras signals long-term potentiation via endoplasmic reticulum PI3K and lipid raft ERK, whereas Rap2 and Rap1 signal depotentiation and long-term depression via bulk membrane JNK and lysosome p38MAPK, respectively. These results establish an effective subcellular microdomain-specific targeted delivery method and unveil subcellular microdomain-specific signaling as the mechanism for homologous Ras and Rap to achieve signal diversity and specificity to control multiple forms of synaptic plasticity. •Microdomain-targeted delivery method reveals signal diversity and specificity•Endoplasmic reticulum Ras-PI3K and lipid rafts Ras-ERK signal long-term potentiation•Bulk membrane Rap2-JNK signals depotentiation•Lysosome Rap1-p38MAPK signals long-term depression Zhang et al. develop an effective subcellular microdomain-specific targeted delivery method and demonstrate that homologous proteins (e.g., Ras and Rap) confine their signaling within distinct subcellular microdomains to achieve signal transduction diversity and specificity.
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pmid29706584
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