---
_id: '9756'
abstract:
- lang: eng
text: High-resolution visualization and quantification of membrane proteins contribute
to the understanding of their functions and the roles they play in physiological
and pathological conditions. Sodium dodecyl sulfate-digested freeze-fracture replica
labeling (SDS-FRL) is a powerful electron microscopy method to study quantitatively
the two-dimensional distribution of transmembrane proteins and their tightly associated
proteins. During treatment with SDS, intracellular organelles and proteins not
anchored to the replica are dissolved, whereas integral membrane proteins captured
and stabilized by carbon/platinum deposition remain on the replica. Their intra-
and extracellular domains become exposed on the surface of the replica, facilitating
the accessibility of antibodies and, therefore, providing higher labeling efficiency
than those obtained with other immunoelectron microscopy techniques. In this chapter,
we describe the protocols of SDS-FRL adapted for mammalian brain samples, and
optimization of the SDS treatment to increase the labeling efficiency for quantification
of Cav2.1, the alpha subunit of P/Q-type voltage-dependent calcium channels utilizing
deep learning algorithms.
acknowledgement: This work was supported by the European Union (European Research
Council Advanced grant no. 694539 and Human Brain Project Ref. 720270 to R. S.)
and the Austrian Academy of Sciences (DOC fellowship to D.K.).
alternative_title:
- Neuromethods
article_processing_charge: No
author:
- first_name: Walter
full_name: Kaufmann, Walter
id: 3F99E422-F248-11E8-B48F-1D18A9856A87
last_name: Kaufmann
orcid: 0000-0001-9735-5315
- first_name: David
full_name: Kleindienst, David
id: 42E121A4-F248-11E8-B48F-1D18A9856A87
last_name: Kleindienst
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: 'Kaufmann W, Kleindienst D, Harada H, Shigemoto R. High-Resolution localization
and quantitation of membrane proteins by SDS-digested freeze-fracture replica
labeling (SDS-FRL). In: Receptor and Ion Channel Detection in the Brain.
Vol 169. Neuromethods. New York: Humana; 2021:267-283. doi:10.1007/978-1-0716-1522-5_19'
apa: 'Kaufmann, W., Kleindienst, D., Harada, H., & Shigemoto, R. (2021). High-Resolution
localization and quantitation of membrane proteins by SDS-digested freeze-fracture
replica labeling (SDS-FRL). In Receptor and Ion Channel Detection in the Brain
(Vol. 169, pp. 267–283). New York: Humana. https://doi.org/10.1007/978-1-0716-1522-5_19'
chicago: 'Kaufmann, Walter, David Kleindienst, Harumi Harada, and Ryuichi Shigemoto.
“High-Resolution Localization and Quantitation of Membrane Proteins by SDS-Digested
Freeze-Fracture Replica Labeling (SDS-FRL).” In Receptor and Ion Channel Detection
in the Brain, 169:267–83. Neuromethods. New York: Humana, 2021. https://doi.org/10.1007/978-1-0716-1522-5_19.'
ieee: 'W. Kaufmann, D. Kleindienst, H. Harada, and R. Shigemoto, “High-Resolution
localization and quantitation of membrane proteins by SDS-digested freeze-fracture
replica labeling (SDS-FRL),” in Receptor and Ion Channel Detection in the
Brain, vol. 169, New York: Humana, 2021, pp. 267–283.'
ista: 'Kaufmann W, Kleindienst D, Harada H, Shigemoto R. 2021.High-Resolution localization
and quantitation of membrane proteins by SDS-digested freeze-fracture replica
labeling (SDS-FRL). In: Receptor and Ion Channel Detection in the Brain. Neuromethods,
vol. 169, 267–283.'
mla: Kaufmann, Walter, et al. “High-Resolution Localization and Quantitation of
Membrane Proteins by SDS-Digested Freeze-Fracture Replica Labeling (SDS-FRL).”
Receptor and Ion Channel Detection in the Brain, vol. 169, Humana, 2021,
pp. 267–83, doi:10.1007/978-1-0716-1522-5_19.
short: W. Kaufmann, D. Kleindienst, H. Harada, R. Shigemoto, in:, Receptor and
Ion Channel Detection in the Brain, Humana, New York, 2021, pp. 267–283.
date_created: 2021-07-30T09:34:56Z
date_published: 2021-07-27T00:00:00Z
date_updated: 2024-03-28T23:30:31Z
day: '27'
ddc:
- '573'
department:
- _id: RySh
- _id: EM-Fac
doi: 10.1007/978-1-0716-1522-5_19
ec_funded: 1
has_accepted_license: '1'
intvolume: ' 169'
keyword:
- 'Freeze-fracture replica: Deep learning'
- Immunogold labeling
- Integral membrane protein
- Electron microscopy
language:
- iso: eng
month: '07'
oa_version: None
page: 267-283
place: New York
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
- _id: 25CBA828-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '720270'
name: Human Brain Project Specific Grant Agreement 1 (HBP SGA 1)
publication: ' Receptor and Ion Channel Detection in the Brain'
publication_identifier:
eisbn:
- '9781071615225'
isbn:
- '9781071615218'
publication_status: published
publisher: Humana
quality_controlled: '1'
related_material:
record:
- id: '9562'
relation: dissertation_contains
status: public
series_title: Neuromethods
status: public
title: High-Resolution localization and quantitation of membrane proteins by SDS-digested
freeze-fracture replica labeling (SDS-FRL)
type: book_chapter
user_id: D865714E-FA4E-11E9-B85B-F5C5E5697425
volume: 169
year: '2021'
...
---
_id: '7391'
abstract:
- lang: eng
text: Electron microscopy (EM) is a technology that enables visualization of single
proteins at a nanometer resolution. However, current protein analysis by EM mainly
relies on immunolabeling with gold-particle-conjugated antibodies, which is compromised
by large size of antibody, precluding precise detection of protein location in
biological samples. Here, we develop a specific chemical labeling method for EM
detection of proteins at single-molecular level. Rational design of α-helical
peptide tag and probe structure provided a complementary reaction pair that enabled
specific cysteine conjugation of the tag. The developed chemical labeling with
gold-nanoparticle-conjugated probe showed significantly higher labeling efficiency
and detectability of high-density clusters of tag-fused G protein-coupled receptors
in freeze-fracture replicas compared with immunogold labeling. Furthermore, in
ultrathin sections, the spatial resolution of the chemical labeling was significantly
higher than that of antibody-mediated labeling. These results demonstrate substantial
advantages of the chemical labeling approach for single protein visualization
by EM.
article_processing_charge: No
article_type: original
author:
- first_name: Shigekazu
full_name: Tabata, Shigekazu
id: 4427179E-F248-11E8-B48F-1D18A9856A87
last_name: Tabata
- first_name: Marijo
full_name: Jevtic, Marijo
id: 4BE3BC94-F248-11E8-B48F-1D18A9856A87
last_name: Jevtic
- first_name: Nobutaka
full_name: Kurashige, Nobutaka
last_name: Kurashige
- first_name: Hirokazu
full_name: Fuchida, Hirokazu
last_name: Fuchida
- first_name: Munetsugu
full_name: Kido, Munetsugu
last_name: Kido
- first_name: Kazushi
full_name: Tani, Kazushi
last_name: Tani
- first_name: Naoki
full_name: Zenmyo, Naoki
last_name: Zenmyo
- first_name: Shohei
full_name: Uchinomiya, Shohei
last_name: Uchinomiya
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Makoto
full_name: Itakura, Makoto
last_name: Itakura
- first_name: Itaru
full_name: Hamachi, Itaru
last_name: Hamachi
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Akio
full_name: Ojida, Akio
last_name: Ojida
citation:
ama: Tabata S, Jevtic M, Kurashige N, et al. Electron microscopic detection of single
membrane proteins by a specific chemical labeling. iScience. 2019;22(12):256-268.
doi:10.1016/j.isci.2019.11.025
apa: Tabata, S., Jevtic, M., Kurashige, N., Fuchida, H., Kido, M., Tani, K., … Ojida,
A. (2019). Electron microscopic detection of single membrane proteins by a specific
chemical labeling. IScience. Elsevier. https://doi.org/10.1016/j.isci.2019.11.025
chicago: Tabata, Shigekazu, Marijo Jevtic, Nobutaka Kurashige, Hirokazu Fuchida,
Munetsugu Kido, Kazushi Tani, Naoki Zenmyo, et al. “Electron Microscopic Detection
of Single Membrane Proteins by a Specific Chemical Labeling.” IScience.
Elsevier, 2019. https://doi.org/10.1016/j.isci.2019.11.025.
ieee: S. Tabata et al., “Electron microscopic detection of single membrane
proteins by a specific chemical labeling,” iScience, vol. 22, no. 12. Elsevier,
pp. 256–268, 2019.
ista: Tabata S, Jevtic M, Kurashige N, Fuchida H, Kido M, Tani K, Zenmyo N, Uchinomiya
S, Harada H, Itakura M, Hamachi I, Shigemoto R, Ojida A. 2019. Electron microscopic
detection of single membrane proteins by a specific chemical labeling. iScience.
22(12), 256–268.
mla: Tabata, Shigekazu, et al. “Electron Microscopic Detection of Single Membrane
Proteins by a Specific Chemical Labeling.” IScience, vol. 22, no. 12, Elsevier,
2019, pp. 256–68, doi:10.1016/j.isci.2019.11.025.
short: S. Tabata, M. Jevtic, N. Kurashige, H. Fuchida, M. Kido, K. Tani, N. Zenmyo,
S. Uchinomiya, H. Harada, M. Itakura, I. Hamachi, R. Shigemoto, A. Ojida, IScience
22 (2019) 256–268.
date_created: 2020-01-29T15:56:56Z
date_published: 2019-12-20T00:00:00Z
date_updated: 2024-03-28T23:30:12Z
day: '20'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1016/j.isci.2019.11.025
ec_funded: 1
external_id:
isi:
- :000504652000020
pmid:
- '31786521'
file:
- access_level: open_access
checksum: f3e90056a49f09b205b1c4f8c739ffd1
content_type: application/pdf
creator: dernst
date_created: 2020-02-04T10:48:36Z
date_updated: 2020-07-14T12:47:57Z
file_id: '7448'
file_name: 2019_iScience_Tabata.pdf
file_size: 7197776
relation: main_file
file_date_updated: 2020-07-14T12:47:57Z
has_accepted_license: '1'
intvolume: ' 22'
issue: '12'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '12'
oa: 1
oa_version: Published Version
page: 256-268
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
- _id: 25CBA828-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '720270'
name: Human Brain Project Specific Grant Agreement 1 (HBP SGA 1)
publication: iScience
publication_identifier:
issn:
- 2589-0042
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
record:
- id: '11393'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: Electron microscopic detection of single membrane proteins by a specific chemical
labeling
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 22
year: '2019'
...
---
_id: '736'
abstract:
- lang: eng
text: The neurotransmitter receptor subtype, number, density, and distribution relative
to the location of transmitter release sites are key determinants of signal transmission.
AMPA-type ionotropic glutamate receptors (AMPARs) containing GluA3 and GluA4 subunits
are prominently expressed in subsets of neurons capable of firing action potentials
at high frequencies, such as auditory relay neurons. The auditory nerve (AN) forms
glutamatergic synapses on two types of relay neurons, bushy cells (BCs) and fusiform
cells (FCs) of the cochlear nucleus. AN-BC and AN-FC synapses have distinct kinetics;
thus, we investigated whether the number, density, and localization of GluA3 and
GluA4 subunits in these synapses are differentially organized using quantitative
freeze-fracture replica immunogold labeling. We identify a positive correlation
between the number of AMPARs and the size of AN-BC and AN-FC synapses. Both types
of AN synapses have similar numbers of AMPARs; however, the AN-BC have a higher
density of AMPARs than AN-FC synapses, because the AN-BC synapses are smaller.
A higher number and density of GluA3 subunits are observed at AN-BC synapses,
whereas a higher number and density of GluA4 subunits are observed at AN-FC synapses.
The intrasynaptic distribution of immunogold labeling revealed that AMPAR subunits,
particularly GluA3, are concentrated at the center of the AN-BC synapses. The
central distribution of AMPARs is absent in GluA3-knockout mice, and gold particles
are evenly distributed along the postsynaptic density. GluA4 gold labeling was
homogenously distributed along both synapse types. Thus, GluA3 and GluA4 subunits
are distributed at AN synapses in a target-cell-dependent manner.
article_processing_charge: No
author:
- first_name: María
full_name: Rubio, María
last_name: Rubio
- first_name: Ko
full_name: Matsui, Ko
last_name: Matsui
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Naomi
full_name: Kamasawa, Naomi
last_name: Kamasawa
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Makoto
full_name: Itakura, Makoto
last_name: Itakura
- first_name: Elek
full_name: Molnár, Elek
last_name: Molnár
- first_name: Manabu
full_name: Abe, Manabu
last_name: Abe
- first_name: Kenji
full_name: Sakimura, Kenji
last_name: Sakimura
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Rubio M, Matsui K, Fukazawa Y, et al. The number and distribution of AMPA receptor
channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses
depend on the target cells. Brain Structure and Function. 2017;222(8):3375-3393.
doi:10.1007/s00429-017-1408-0
apa: Rubio, M., Matsui, K., Fukazawa, Y., Kamasawa, N., Harada, H., Itakura, M.,
… Shigemoto, R. (2017). The number and distribution of AMPA receptor channels
containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend
on the target cells. Brain Structure and Function. Springer. https://doi.org/10.1007/s00429-017-1408-0
chicago: Rubio, María, Ko Matsui, Yugo Fukazawa, Naomi Kamasawa, Harumi Harada,
Makoto Itakura, Elek Molnár, Manabu Abe, Kenji Sakimura, and Ryuichi Shigemoto.
“The Number and Distribution of AMPA Receptor Channels Containing Fast Kinetic
GluA3 and GluA4 Subunits at Auditory Nerve Synapses Depend on the Target Cells.”
Brain Structure and Function. Springer, 2017. https://doi.org/10.1007/s00429-017-1408-0.
ieee: M. Rubio et al., “The number and distribution of AMPA receptor channels
containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend
on the target cells,” Brain Structure and Function, vol. 222, no. 8. Springer,
pp. 3375–3393, 2017.
ista: Rubio M, Matsui K, Fukazawa Y, Kamasawa N, Harada H, Itakura M, Molnár E,
Abe M, Sakimura K, Shigemoto R. 2017. The number and distribution of AMPA receptor
channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses
depend on the target cells. Brain Structure and Function. 222(8), 3375–3393.
mla: Rubio, María, et al. “The Number and Distribution of AMPA Receptor Channels
Containing Fast Kinetic GluA3 and GluA4 Subunits at Auditory Nerve Synapses Depend
on the Target Cells.” Brain Structure and Function, vol. 222, no. 8, Springer,
2017, pp. 3375–93, doi:10.1007/s00429-017-1408-0.
short: M. Rubio, K. Matsui, Y. Fukazawa, N. Kamasawa, H. Harada, M. Itakura, E.
Molnár, M. Abe, K. Sakimura, R. Shigemoto, Brain Structure and Function 222 (2017)
3375–3393.
date_created: 2018-12-11T11:48:14Z
date_published: 2017-11-01T00:00:00Z
date_updated: 2023-09-27T14:14:51Z
day: '01'
ddc:
- '571'
department:
- _id: RySh
doi: 10.1007/s00429-017-1408-0
external_id:
isi:
- '000414761700002'
file:
- access_level: open_access
checksum: 73787a22507de8fb585bb598e1418ca7
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:10:20Z
date_updated: 2020-07-14T12:47:56Z
file_id: '4806'
file_name: IST-2017-881-v1+1_s00429-017-1408-0.pdf
file_size: 4011126
relation: main_file
file_date_updated: 2020-07-14T12:47:56Z
has_accepted_license: '1'
intvolume: ' 222'
isi: 1
issue: '8'
language:
- iso: eng
month: '11'
oa: 1
oa_version: Published Version
page: 3375 - 3393
publication: Brain Structure and Function
publication_identifier:
issn:
- '18632653'
publication_status: published
publisher: Springer
publist_id: '6932'
pubrep_id: '881'
quality_controlled: '1'
scopus_import: '1'
status: public
title: The number and distribution of AMPA receptor channels containing fast kinetic
GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 222
year: '2017'
...
---
_id: '1094'
abstract:
- lang: eng
text: Immunogold labeling of freeze-fracture replicas has recently been used for
high-resolution visualization of protein localization in electron microscopy.
This method has higher labeling efficiency than conventional immunogold methods
for membrane molecules allowing precise quantitative measurements. However, one
of the limitations of freeze-fracture replica immunolabeling is difficulty in
keeping structural orientation and identifying labeled profiles in complex tissues
like brain. The difficulty is partly due to fragmentation of freeze-fracture replica
preparations during labeling procedures and limited morphological clues on the
replica surface. To overcome these issues, we introduce here a grid-glued replica
method combined with SEM observation. This method allows histological staining
before dissolving the tissue and easy handling of replicas during immunogold labeling,
and keeps the whole replica surface intact without fragmentation. The procedure
described here is also useful for matched double-replica analysis allowing further
identification of labeled profiles in corresponding P-face and E-face.
acknowledged_ssus:
- _id: EM-Fac
acknowledgement: 'We thank Prof. Elek Molnár for providing us a pan-AMPAR anti-body
used in Fig.2 and Dr. Ludek Lovicar for technical assistance in scanning electron
microscope imaging. This work was supported by the European Union (HBP—Project Ref.
604102). '
alternative_title:
- Methods in Molecular Biology
article_processing_charge: No
author:
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: 'Harada H, Shigemoto R. Immunogold protein localization on grid-glued freeze-fracture
replicas. In: High-Resolution Imaging of Cellular Proteins. Vol 1474. Springer;
2016:203-216. doi:10.1007/978-1-4939-6352-2_12'
apa: Harada, H., & Shigemoto, R. (2016). Immunogold protein localization on
grid-glued freeze-fracture replicas. In High-Resolution Imaging of Cellular
Proteins (Vol. 1474, pp. 203–216). Springer. https://doi.org/10.1007/978-1-4939-6352-2_12
chicago: Harada, Harumi, and Ryuichi Shigemoto. “Immunogold Protein Localization
on Grid-Glued Freeze-Fracture Replicas.” In High-Resolution Imaging of Cellular
Proteins, 1474:203–16. Springer, 2016. https://doi.org/10.1007/978-1-4939-6352-2_12.
ieee: H. Harada and R. Shigemoto, “Immunogold protein localization on grid-glued
freeze-fracture replicas,” in High-Resolution Imaging of Cellular Proteins,
vol. 1474, Springer, 2016, pp. 203–216.
ista: 'Harada H, Shigemoto R. 2016.Immunogold protein localization on grid-glued
freeze-fracture replicas. In: High-Resolution Imaging of Cellular Proteins. Methods
in Molecular Biology, vol. 1474, 203–216.'
mla: Harada, Harumi, and Ryuichi Shigemoto. “Immunogold Protein Localization on
Grid-Glued Freeze-Fracture Replicas.” High-Resolution Imaging of Cellular Proteins,
vol. 1474, Springer, 2016, pp. 203–16, doi:10.1007/978-1-4939-6352-2_12.
short: H. Harada, R. Shigemoto, in:, High-Resolution Imaging of Cellular Proteins,
Springer, 2016, pp. 203–216.
date_created: 2018-12-11T11:50:06Z
date_published: 2016-08-12T00:00:00Z
date_updated: 2023-09-05T14:09:01Z
day: '12'
department:
- _id: RySh
doi: 10.1007/978-1-4939-6352-2_12
ec_funded: 1
intvolume: ' 1474'
language:
- iso: eng
month: '08'
oa_version: None
page: 203 - 216
project:
- _id: 25CD3DD2-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '604102'
name: Localization of ion channels and receptors by two and three-dimensional immunoelectron
microscopic approaches
publication: High-Resolution Imaging of Cellular Proteins
publication_identifier:
eissn:
- 1611-3349
issn:
- 0302-9743
publication_status: published
publisher: Springer
publist_id: '6281'
quality_controlled: '1'
status: public
title: Immunogold protein localization on grid-glued freeze-fracture replicas
type: book_chapter
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 1474
year: '2016'
...
---
_id: '1546'
abstract:
- lang: eng
text: Synaptic efficacy and precision are influenced by the coupling of voltage-gated
Ca2+ channels (VGCCs) to vesicles. But because the topography of VGCCs and their
proximity to vesicles is unknown, a quantitative understanding of the determinants
of vesicular release at nanometer scale is lacking. To investigate this, we combined
freeze-fracture replica immunogold labeling of Cav2.1 channels, local [Ca2+] imaging,
and patch pipette perfusion of EGTA at the calyx of Held. Between postnatal day
7 and 21, VGCCs formed variable sized clusters and vesicular release became less
sensitive to EGTA, whereas fixed Ca2+ buffer properties remained constant. Experimentally
constrained reaction-diffusion simulations suggest that Ca2+ sensors for vesicular
release are located at the perimeter of VGCC clusters (<30nm) and predict that
VGCC number per cluster determines vesicular release probability without altering
release time course. This "perimeter release model" provides a unifying
framework accounting for developmental changes in both synaptic efficacy and time
course.
acknowledgement: This work was supported by the Core Research for Evolutional Science
and Technology (CREST) of Japan Science and Technology Agency to T.T. and R.S.;
by the funding provided by Okinawa Institute of Science and Technology (OIST) to
T.T. and Y.N.; by JSPS Core-to-Core Program, A. Advanced Networks to T.T.; by the
Grant-in-Aid for Young Scientists from the Japanese Ministry of Education, Culture,
Sports, Science and Technology (#23700474) to Y.N.; by the Centre National de la
Recherche Scientifique through the Actions Thematiques et Initatives sur Programme,
Fondation Fyssen, Fondation pour la Recherche Medicale, Federation pour la Recherche
sur le Cerveau, Agence Nationale de la Recherche (ANR-2007-Neuro-008-01 and ANR-2010-BLAN-1411-01)
to D.D. and Y.N.; and by the European Commission Coordination Action ENINET (LSHM-CT-2005-19063)
to D.D. and R.A.S. R.A.S. and J.S.R. were funded by Wellcome Trust Senior (064413)
and Principal (095667) Research Fellowship and an ERC advance grant (294667) to
RAS.
author:
- first_name: Yukihiro
full_name: Nakamura, Yukihiro
last_name: Nakamura
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Naomi
full_name: Kamasawa, Naomi
last_name: Kamasawa
- first_name: Ko
full_name: Matsui, Ko
last_name: Matsui
- first_name: Jason
full_name: Rothman, Jason
last_name: Rothman
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: R Angus
full_name: Silver, R Angus
last_name: Silver
- first_name: David
full_name: Digregorio, David
last_name: Digregorio
- first_name: Tomoyuki
full_name: Takahashi, Tomoyuki
last_name: Takahashi
citation:
ama: Nakamura Y, Harada H, Kamasawa N, et al. Nanoscale distribution of presynaptic
Ca2+ channels and its impact on vesicular release during development. Neuron.
2015;85(1):145-158. doi:10.1016/j.neuron.2014.11.019
apa: Nakamura, Y., Harada, H., Kamasawa, N., Matsui, K., Rothman, J., Shigemoto,
R., … Takahashi, T. (2015). Nanoscale distribution of presynaptic Ca2+ channels
and its impact on vesicular release during development. Neuron. Elsevier.
https://doi.org/10.1016/j.neuron.2014.11.019
chicago: Nakamura, Yukihiro, Harumi Harada, Naomi Kamasawa, Ko Matsui, Jason Rothman,
Ryuichi Shigemoto, R Angus Silver, David Digregorio, and Tomoyuki Takahashi. “Nanoscale
Distribution of Presynaptic Ca2+ Channels and Its Impact on Vesicular Release
during Development.” Neuron. Elsevier, 2015. https://doi.org/10.1016/j.neuron.2014.11.019.
ieee: Y. Nakamura et al., “Nanoscale distribution of presynaptic Ca2+ channels
and its impact on vesicular release during development,” Neuron, vol. 85,
no. 1. Elsevier, pp. 145–158, 2015.
ista: Nakamura Y, Harada H, Kamasawa N, Matsui K, Rothman J, Shigemoto R, Silver
RA, Digregorio D, Takahashi T. 2015. Nanoscale distribution of presynaptic Ca2+
channels and its impact on vesicular release during development. Neuron. 85(1),
145–158.
mla: Nakamura, Yukihiro, et al. “Nanoscale Distribution of Presynaptic Ca2+ Channels
and Its Impact on Vesicular Release during Development.” Neuron, vol. 85,
no. 1, Elsevier, 2015, pp. 145–58, doi:10.1016/j.neuron.2014.11.019.
short: Y. Nakamura, H. Harada, N. Kamasawa, K. Matsui, J. Rothman, R. Shigemoto,
R.A. Silver, D. Digregorio, T. Takahashi, Neuron 85 (2015) 145–158.
date_created: 2018-12-11T11:52:39Z
date_published: 2015-01-07T00:00:00Z
date_updated: 2021-01-12T06:51:31Z
day: '07'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1016/j.neuron.2014.11.019
file:
- access_level: open_access
checksum: 725f4d5be2dbb44b283ce722645ef37d
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:15:47Z
date_updated: 2020-07-14T12:45:01Z
file_id: '5170'
file_name: IST-2016-482-v1+1_1-s2.0-S0896627314010472-main.pdf
file_size: 3080111
relation: main_file
file_date_updated: 2020-07-14T12:45:01Z
has_accepted_license: '1'
intvolume: ' 85'
issue: '1'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
page: 145 - 158
publication: Neuron
publication_status: published
publisher: Elsevier
publist_id: '5625'
pubrep_id: '482'
quality_controlled: '1'
scopus_import: 1
status: public
title: Nanoscale distribution of presynaptic Ca2+ channels and its impact on vesicular
release during development
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 85
year: '2015'
...
---
_id: '1898'
abstract:
- lang: eng
text: Fast synaptic transmission is important for rapid information processing.
To explore the maximal rate of neuronal signaling and to analyze the presynaptic
mechanisms, we focused on the input layer of the cerebellar cortex, where exceptionally
high action potential (AP) frequencies have been reported invivo. With paired
recordings between presynaptic cerebellar mossy fiber boutons and postsynaptic
granule cells, we demonstrate reliable neurotransmission upto ~1 kHz. Presynaptic
APs are ultrafast, with ~100μs half-duration. Both Kv1 and Kv3 potassium channels
mediate the fast repolarization, rapidly inactivating sodium channels ensure metabolic
efficiency, and little AP broadening occurs during bursts of up to 1.5 kHz. Presynaptic
Cav2.1 (P/Q-type) calcium channels open efficiently during ultrafast APs. Furthermore,
a subset of synaptic vesicles is tightly coupled to Ca2+ channels, and vesicles
are rapidly recruited to the release site. These data reveal mechanisms of presynaptic
AP generation and transmitter release underlying neuronal kHz signaling.
author:
- first_name: Andreas
full_name: Ritzau Jost, Andreas
last_name: Ritzau Jost
- first_name: Igor
full_name: Delvendahl, Igor
last_name: Delvendahl
- first_name: Annika
full_name: Rings, Annika
last_name: Rings
- first_name: Niklas
full_name: Byczkowicz, Niklas
last_name: Byczkowicz
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Johannes
full_name: Hirrlinger, Johannes
last_name: Hirrlinger
- first_name: Jens
full_name: Eilers, Jens
last_name: Eilers
- first_name: Stefan
full_name: Hallermann, Stefan
last_name: Hallermann
citation:
ama: Ritzau Jost A, Delvendahl I, Rings A, et al. Ultrafast action potentials mediate
kilohertz signaling at a central synapse. Neuron. 2014;84(1):152-163. doi:10.1016/j.neuron.2014.08.036
apa: Ritzau Jost, A., Delvendahl, I., Rings, A., Byczkowicz, N., Harada, H., Shigemoto,
R., … Hallermann, S. (2014). Ultrafast action potentials mediate kilohertz signaling
at a central synapse. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2014.08.036
chicago: Ritzau Jost, Andreas, Igor Delvendahl, Annika Rings, Niklas Byczkowicz,
Harumi Harada, Ryuichi Shigemoto, Johannes Hirrlinger, Jens Eilers, and Stefan
Hallermann. “Ultrafast Action Potentials Mediate Kilohertz Signaling at a Central
Synapse.” Neuron. Elsevier, 2014. https://doi.org/10.1016/j.neuron.2014.08.036.
ieee: A. Ritzau Jost et al., “Ultrafast action potentials mediate kilohertz
signaling at a central synapse,” Neuron, vol. 84, no. 1. Elsevier, pp.
152–163, 2014.
ista: Ritzau Jost A, Delvendahl I, Rings A, Byczkowicz N, Harada H, Shigemoto R,
Hirrlinger J, Eilers J, Hallermann S. 2014. Ultrafast action potentials mediate
kilohertz signaling at a central synapse. Neuron. 84(1), 152–163.
mla: Ritzau Jost, Andreas, et al. “Ultrafast Action Potentials Mediate Kilohertz
Signaling at a Central Synapse.” Neuron, vol. 84, no. 1, Elsevier, 2014,
pp. 152–63, doi:10.1016/j.neuron.2014.08.036.
short: A. Ritzau Jost, I. Delvendahl, A. Rings, N. Byczkowicz, H. Harada, R. Shigemoto,
J. Hirrlinger, J. Eilers, S. Hallermann, Neuron 84 (2014) 152–163.
date_created: 2018-12-11T11:54:36Z
date_published: 2014-10-01T00:00:00Z
date_updated: 2021-01-12T06:53:55Z
day: '01'
department:
- _id: RySh
doi: 10.1016/j.neuron.2014.08.036
intvolume: ' 84'
issue: '1'
language:
- iso: eng
month: '10'
oa_version: None
page: 152 - 163
publication: Neuron
publication_status: published
publisher: Elsevier
publist_id: '5197'
quality_controlled: '1'
scopus_import: 1
status: public
title: Ultrafast action potentials mediate kilohertz signaling at a central synapse
type: journal_article
user_id: 4435EBFC-F248-11E8-B48F-1D18A9856A87
volume: 84
year: '2014'
...
---
_id: '2478'
abstract:
- lang: eng
text: Despite the pivotal functions of the NMDA receptor (NMDAR) for neural circuit
development and synaptic plasticity, the molecular mechanisms underlying the dynamics
of NMDAR trafficking are poorly understood. The cell adhesion molecule neuroligin-1
(NL1) modifies NMDAR-dependent synaptic transmission and synaptic plasticity,
but it is unclear whether NL1 controls synaptic accumulation or function of the
receptors. Here, we provide evidence that NL1 regulates the abundance of NMDARs
at postsynaptic sites. This function relies on extracellular, NL1 isoform-specific
sequences that facilitate biochemical interactions between NL1 and the NMDAR GluN1
subunit. Our work uncovers NL1 isoform-specific cisinteractions with ionotropic
glutamate receptors as a key mechanism for controlling synaptic properties.
author:
- first_name: Elaine
full_name: Budreck, Elaine C
last_name: Budreck
- first_name: Oh
full_name: Kwon, Oh-Bin
last_name: Kwon
- first_name: Jung
full_name: Jung, Jung-Hoon
last_name: Jung
- first_name: Stéphane
full_name: Baudouin, Stéphane J
last_name: Baudouin
- first_name: Albert
full_name: Thommen, Albert
last_name: Thommen
- first_name: Hye
full_name: Kim, Hye-Sun
last_name: Kim
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Harumi
full_name: Harumi Harada
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Katsuhiko
full_name: Tabuchi, Katsuhiko
last_name: Tabuchi
- first_name: Ryuichi
full_name: Ryuichi Shigemoto
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Peter
full_name: Scheiffele, Peter
last_name: Scheiffele
- first_name: Joung
full_name: Kim, Joung-Hun
last_name: Kim
citation:
ama: Budreck E, Kwon O, Jung J, et al. Neuroligin-1 controls synaptic abundance
of NMDA-type glutamate receptors through extracellular coupling. PNAS.
2013;110(2):725-730. doi:10.1073/pnas.1214718110
apa: Budreck, E., Kwon, O., Jung, J., Baudouin, S., Thommen, A., Kim, H., … Kim,
J. (2013). Neuroligin-1 controls synaptic abundance of NMDA-type glutamate receptors
through extracellular coupling. PNAS. National Academy of Sciences. https://doi.org/10.1073/pnas.1214718110
chicago: Budreck, Elaine, Oh Kwon, Jung Jung, Stéphane Baudouin, Albert Thommen,
Hye Kim, Yugo Fukazawa, et al. “Neuroligin-1 Controls Synaptic Abundance of NMDA-Type
Glutamate Receptors through Extracellular Coupling.” PNAS. National Academy
of Sciences, 2013. https://doi.org/10.1073/pnas.1214718110.
ieee: E. Budreck et al., “Neuroligin-1 controls synaptic abundance of NMDA-type
glutamate receptors through extracellular coupling,” PNAS, vol. 110, no.
2. National Academy of Sciences, pp. 725–730, 2013.
ista: Budreck E, Kwon O, Jung J, Baudouin S, Thommen A, Kim H, Fukazawa Y, Harada
H, Tabuchi K, Shigemoto R, Scheiffele P, Kim J. 2013. Neuroligin-1 controls synaptic
abundance of NMDA-type glutamate receptors through extracellular coupling. PNAS.
110(2), 725–730.
mla: Budreck, Elaine, et al. “Neuroligin-1 Controls Synaptic Abundance of NMDA-Type
Glutamate Receptors through Extracellular Coupling.” PNAS, vol. 110, no.
2, National Academy of Sciences, 2013, pp. 725–30, doi:10.1073/pnas.1214718110.
short: E. Budreck, O. Kwon, J. Jung, S. Baudouin, A. Thommen, H. Kim, Y. Fukazawa,
H. Harada, K. Tabuchi, R. Shigemoto, P. Scheiffele, J. Kim, PNAS 110 (2013) 725–730.
date_created: 2018-12-11T11:57:54Z
date_published: 2013-01-08T00:00:00Z
date_updated: 2021-01-12T06:57:43Z
day: '08'
doi: 10.1073/pnas.1214718110
extern: 1
intvolume: ' 110'
issue: '2'
month: '01'
page: 725 - 730
publication: PNAS
publication_status: published
publisher: National Academy of Sciences
publist_id: '4423'
quality_controlled: 0
status: public
title: Neuroligin-1 controls synaptic abundance of NMDA-type glutamate receptors through
extracellular coupling
type: journal_article
volume: 110
year: '2013'
...
---
_id: '2690'
abstract:
- lang: eng
text: Establishing the spatiotemporal concentration profile of neurotransmitter
following synaptic vesicular release is essential for our understanding of inter-neuronal
communication. Such profile is a determinant of synaptic strength, short-term
plasticity and inter-synaptic crosstalk. Synaptically released glutamate has been
suggested to reach a few millimolar in concentration and last for <1 ms. The
synaptic cleft is often conceived as a single concentration compartment, whereas
a huge gradient likely exists. Modelling studies have attempted to describe this
gradient, but two key parameters, the number of glutamate in a vesicle (NGlu)
and its diffusion coefficient (DGlu) in the extracellular space, remained unresolved.
To determine this profile, the rat calyx of Held synapse at postnatal day 12-16
was studied where diffusion of glutamate occurs two-dimensionally and where quantification
of AMPA receptor distribution on individual postsynaptic specialization on medial
nucleus of the trapezoid body principal cells is possible using SDS-digested freeze-fracture
replica labelling. To assess the performance of these receptors as glutamate sensors,
a kinetic model of the receptors was constructed from outside-out patch recordings.
From here, we simulated synaptic responses and compared them with the EPSC recordings.
Combinations of NGlu and DGlu with an optimum of 7000 and 0.3 μm2 ms-1 reproduced
the data, suggesting slow diffusion. Further simulations showed that a single
vesicle does not saturate the synaptic receptors, and that glutamate spillover
does not affect the conductance amplitude at this synapse. Using the estimated
profile, we also evaluated how the number of multiple vesicle releases at individual
active zones affects the amplitude of postsynaptic signals.
author:
- first_name: Timotheus
full_name: Budisantoso, Timotheus
last_name: Budisantoso
- first_name: Harumi
full_name: Harumi Harada
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Naomi
full_name: Kamasawa, Naomi
last_name: Kamasawa
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Ryuichi
full_name: Ryuichi Shigemoto
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Ko
full_name: Matsui, Ko
last_name: Matsui
citation:
ama: Budisantoso T, Harada H, Kamasawa N, Fukazawa Y, Shigemoto R, Matsui K. Evaluation
of glutamate concentration transient in the synaptic cleft of the rat calyx of
Held. Journal of Physiology. 2013;591(1):219-239. doi:10.1113/jphysiol.2012.241398
apa: Budisantoso, T., Harada, H., Kamasawa, N., Fukazawa, Y., Shigemoto, R., &
Matsui, K. (2013). Evaluation of glutamate concentration transient in the synaptic
cleft of the rat calyx of Held. Journal of Physiology. Wiley-Blackwell.
https://doi.org/10.1113/jphysiol.2012.241398
chicago: Budisantoso, Timotheus, Harumi Harada, Naomi Kamasawa, Yugo Fukazawa, Ryuichi
Shigemoto, and Ko Matsui. “Evaluation of Glutamate Concentration Transient in
the Synaptic Cleft of the Rat Calyx of Held.” Journal of Physiology. Wiley-Blackwell,
2013. https://doi.org/10.1113/jphysiol.2012.241398.
ieee: T. Budisantoso, H. Harada, N. Kamasawa, Y. Fukazawa, R. Shigemoto, and K.
Matsui, “Evaluation of glutamate concentration transient in the synaptic cleft
of the rat calyx of Held,” Journal of Physiology, vol. 591, no. 1. Wiley-Blackwell,
pp. 219–239, 2013.
ista: Budisantoso T, Harada H, Kamasawa N, Fukazawa Y, Shigemoto R, Matsui K. 2013.
Evaluation of glutamate concentration transient in the synaptic cleft of the rat
calyx of Held. Journal of Physiology. 591(1), 219–239.
mla: Budisantoso, Timotheus, et al. “Evaluation of Glutamate Concentration Transient
in the Synaptic Cleft of the Rat Calyx of Held.” Journal of Physiology,
vol. 591, no. 1, Wiley-Blackwell, 2013, pp. 219–39, doi:10.1113/jphysiol.2012.241398.
short: T. Budisantoso, H. Harada, N. Kamasawa, Y. Fukazawa, R. Shigemoto, K. Matsui,
Journal of Physiology 591 (2013) 219–239.
date_created: 2018-12-11T11:59:05Z
date_published: 2013-01-01T00:00:00Z
date_updated: 2021-01-12T06:59:04Z
day: '01'
doi: 10.1113/jphysiol.2012.241398
extern: 1
intvolume: ' 591'
issue: '1'
month: '01'
page: 219 - 239
publication: Journal of Physiology
publication_status: published
publisher: Wiley-Blackwell
publist_id: '4207'
quality_controlled: 0
status: public
title: Evaluation of glutamate concentration transient in the synaptic cleft of the
rat calyx of Held
type: journal_article
volume: 591
year: '2013'
...
---
_id: '2615'
abstract:
- lang: eng
text: Taste-mGluR4, cloned from taste tissues, is a truncated variant of brain-expressed
mGluR4a (brain-mGluR4), and is known to be a candidate for the receptor involved
in the umami taste sense. Although the expression patterns of taste- and brain-mGluR4
mRNAs have been demonstrated, no mention has so far been made of the expression
of these two mGluR4 proteins in taste tissues. The present study examined the
expression of taste-mGluR4 and brain-mGluR4 proteins in rat taste tissues by using
a specific antibody for mGluR4a which shared a C-terminus of both taste- and brain-mGluR4,
for immunoblot analysis and immunohistochemistry. Immunoblot analysis showed that
both brain-mGluR4 and taste-mGluR4 were expressed in the taste tissues. Taste-mGluR4
was not detected in the cerebellum. The immunoreactive band for brain-mGluR4 protein
was much stronger than that for taste-mGluR4 protein. In the cryosections of fungiform,
foliate and circumvallate papillae, the antibody against taste-mGluR4 exhibited
intense labeling of the taste pores and taste hairs in all the taste buds of gustatory
papillae examined; the immunoreaction to the antibody against brain-mGluR4 was
more intense at the same sites of the taste buds. The portions of the taste bud
cells below the taste pore and surrounding keratinocytes did not show any immunoreactivities.
The results of the present study strongly suggest that, in addition to taste-mGluR4,
brain-mGluR4 may function even more importantly than the former as a receptor
for glutamate, i.e. the umami taste sensation.
article_processing_charge: No
article_type: original
author:
- first_name: Takashi
full_name: Toyono, Takashi
last_name: Toyono
- first_name: Yuji
full_name: Seta, Yuji
last_name: Seta
- first_name: Shinji
full_name: Sataoka, Shinji
last_name: Sataoka
- first_name: Harumi
full_name: Harada, Harumi
id: 2E55CDF2-F248-11E8-B48F-1D18A9856A87
last_name: Harada
orcid: 0000-0001-7429-7896
- first_name: Takahiko
full_name: Morotomi, Takahiko
last_name: Morotomi
- first_name: Shintaro
full_name: Kawano, Shintaro
last_name: Kawano
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Kuniaki
full_name: Toyoshima, Kuniaki
last_name: Toyoshima
citation:
ama: Toyono T, Seta Y, Sataoka S, et al. Expression of the metabotropic glutamate
receptor, mGluR4a, in the taste hairs of taste buds in rat gustatory papillae.
Archives of Histology and Cytology. 2002;65(1):91-96. doi:10.1679/aohc.65.91
apa: Toyono, T., Seta, Y., Sataoka, S., Harada, H., Morotomi, T., Kawano, S., …
Toyoshima, K. (2002). Expression of the metabotropic glutamate receptor, mGluR4a,
in the taste hairs of taste buds in rat gustatory papillae. Archives of Histology
and Cytology. Japan Society of Histological Documentation. https://doi.org/10.1679/aohc.65.91
chicago: Toyono, Takashi, Yuji Seta, Shinji Sataoka, Harumi Harada, Takahiko Morotomi,
Shintaro Kawano, Ryuichi Shigemoto, and Kuniaki Toyoshima. “Expression of the
Metabotropic Glutamate Receptor, MGluR4a, in the Taste Hairs of Taste Buds in
Rat Gustatory Papillae.” Archives of Histology and Cytology. Japan Society
of Histological Documentation, 2002. https://doi.org/10.1679/aohc.65.91.
ieee: T. Toyono et al., “Expression of the metabotropic glutamate receptor,
mGluR4a, in the taste hairs of taste buds in rat gustatory papillae,” Archives
of Histology and Cytology, vol. 65, no. 1. Japan Society of Histological Documentation,
pp. 91–96, 2002.
ista: Toyono T, Seta Y, Sataoka S, Harada H, Morotomi T, Kawano S, Shigemoto R,
Toyoshima K. 2002. Expression of the metabotropic glutamate receptor, mGluR4a,
in the taste hairs of taste buds in rat gustatory papillae. Archives of Histology
and Cytology. 65(1), 91–96.
mla: Toyono, Takashi, et al. “Expression of the Metabotropic Glutamate Receptor,
MGluR4a, in the Taste Hairs of Taste Buds in Rat Gustatory Papillae.” Archives
of Histology and Cytology, vol. 65, no. 1, Japan Society of Histological Documentation,
2002, pp. 91–96, doi:10.1679/aohc.65.91.
short: T. Toyono, Y. Seta, S. Sataoka, H. Harada, T. Morotomi, S. Kawano, R. Shigemoto,
K. Toyoshima, Archives of Histology and Cytology 65 (2002) 91–96.
date_created: 2018-12-11T11:58:41Z
date_published: 2002-01-01T00:00:00Z
date_updated: 2023-07-25T10:00:15Z
day: '01'
doi: 10.1679/aohc.65.91
extern: '1'
external_id:
pmid:
- '12002614'
intvolume: ' 65'
issue: '1'
language:
- iso: eng
month: '01'
oa_version: None
page: 91 - 96
pmid: 1
publication: Archives of Histology and Cytology
publication_identifier:
issn:
- 0914-9465
publication_status: published
publisher: Japan Society of Histological Documentation
publist_id: '4283'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Expression of the metabotropic glutamate receptor, mGluR4a, in the taste hairs
of taste buds in rat gustatory papillae
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 65
year: '2002'
...