Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni

In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens....

Full description

Saved in:
Bibliographic Details
Published inJournal of comparative neurology (1911) Vol. 529; no. 10; pp. 2813 - 2823
Main Authors Mack, Andreas F., DeOliveira‐Mello, Laura, Mattheus, Ulrich, Neckel, Peter H.
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.07.2021
Wiley Subscription Services, Inc
Subjects
Online AccessGet full text

Cover

Loading…
Abstract In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens. These animals grow to a standard length of 10–12 cm in this fish species, corresponding to a more than 100‐fold increase in brain volume. Focusing on the telencephalon where glial cells are arranged radially in the everted (dorsal) pallium, immunocytochemistry for glial markers revealed an aberrant pattern of radial glial fibers in the central division of the dorsal pallium (DC, i.e., DC4 and DC5). The main glial processes curved around these nuclei, especially in the posterior part of the telencephalon. This was verified in tissue‐cleared brains stained for glial markers. We further analyzed the growth of radial glia by immunocytochemically applied stem cell (proliferating cell nuclear antigen [PCNA], Sox2) and differentiation marker (doublecortin) and found that these markers were expressed at the ventricular surface consistent with a stacking growth pattern. In addition, we detected doublecortin and Sox2 positive cells in deeper nuclei of DC areas. Our data suggest that radial glial cells give rise to migrating cells providing new neurons and glia to deeper pallial regions. This results in expansion of the central pallial areas and displacement of existing radial glial. In summary, we show that radial glial cells can adapt to morphological growth processes in the adult fish brain and contribute to this growth. The orientation of radial glia in the dorsal telencephalon of teleost fish follows a morphogenetic process called eversion. We studied the radial glia in the cichlid fish Astatotilapia burtoni and found that glial processes get increasingly displaced by central pallial areas during growth. New cells are added to the growing brain subventricularly consistent with a stacking growth pattern (Cell Addition I). In addition, our data suggest that radial glial cells give rise to migrating astroglial cells providing new neurons and glia to deeper pallial regions (Cell Addition II).
AbstractList In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens. These animals grow to a standard length of 10–12 cm in this fish species, corresponding to a more than 100‐fold increase in brain volume. Focusing on the telencephalon where glial cells are arranged radially in the everted (dorsal) pallium, immunocytochemistry for glial markers revealed an aberrant pattern of radial glial fibers in the central division of the dorsal pallium (DC, i.e., DC4 and DC5). The main glial processes curved around these nuclei, especially in the posterior part of the telencephalon. This was verified in tissue‐cleared brains stained for glial markers. We further analyzed the growth of radial glia by immunocytochemically applied stem cell (proliferating cell nuclear antigen [PCNA], Sox2) and differentiation marker (doublecortin) and found that these markers were expressed at the ventricular surface consistent with a stacking growth pattern. In addition, we detected doublecortin and Sox2 positive cells in deeper nuclei of DC areas. Our data suggest that radial glial cells give rise to migrating cells providing new neurons and glia to deeper pallial regions. This results in expansion of the central pallial areas and displacement of existing radial glial. In summary, we show that radial glial cells can adapt to morphological growth processes in the adult fish brain and contribute to this growth. The orientation of radial glia in the dorsal telencephalon of teleost fish follows a morphogenetic process called eversion. We studied the radial glia in the cichlid fish Astatotilapia burtoni and found that glial processes get increasingly displaced by central pallial areas during growth. New cells are added to the growing brain subventricularly consistent with a stacking growth pattern (Cell Addition I). In addition, our data suggest that radial glial cells give rise to migrating astroglial cells providing new neurons and glia to deeper pallial regions (Cell Addition II).
In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens. These animals grow to a standard length of 10–12 cm in this fish species, corresponding to a more than 100‐fold increase in brain volume. Focusing on the telencephalon where glial cells are arranged radially in the everted (dorsal) pallium, immunocytochemistry for glial markers revealed an aberrant pattern of radial glial fibers in the central division of the dorsal pallium (DC, i.e., DC4 and DC5). The main glial processes curved around these nuclei, especially in the posterior part of the telencephalon. This was verified in tissue‐cleared brains stained for glial markers. We further analyzed the growth of radial glia by immunocytochemically applied stem cell (proliferating cell nuclear antigen [PCNA], Sox2) and differentiation marker (doublecortin) and found that these markers were expressed at the ventricular surface consistent with a stacking growth pattern. In addition, we detected doublecortin and Sox2 positive cells in deeper nuclei of DC areas. Our data suggest that radial glial cells give rise to migrating cells providing new neurons and glia to deeper pallial regions. This results in expansion of the central pallial areas and displacement of existing radial glial. In summary, we show that radial glial cells can adapt to morphological growth processes in the adult fish brain and contribute to this growth.
ArticleNumber cne.25126
Author Mack, Andreas F.
DeOliveira‐Mello, Laura
Mattheus, Ulrich
Neckel, Peter H.
Author_xml – sequence: 1
  givenname: Andreas F.
  orcidid: 0000-0001-7591-4374
  surname: Mack
  fullname: Mack, Andreas F.
  email: an.mack@uni-tuebingen.de
  organization: University of Tübingen
– sequence: 2
  givenname: Laura
  orcidid: 0000-0001-8154-3354
  surname: DeOliveira‐Mello
  fullname: DeOliveira‐Mello, Laura
  organization: University of Salamanca
– sequence: 3
  givenname: Ulrich
  surname: Mattheus
  fullname: Mattheus, Ulrich
  organization: University of Tübingen
– sequence: 4
  givenname: Peter H.
  orcidid: 0000-0003-1976-0512
  surname: Neckel
  fullname: Neckel, Peter H.
  organization: University of Tübingen
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33580516$$D View this record in MEDLINE/PubMed
BookMark eNp1kcFO3DAQhq1qUXeBHvoClaVe2kPAdhKvfVytgFZCcIGz5ZjJxiuvndoOiD49LqE9VOI0h_nm06_5j9HCBw8IfabkjBLCzo2HM9ZSxj-gFSWSV1JwukCrsqOVlHy9RMcp7QkhUtbiI1rWdStIS_kKxdu4097-1tkGj0OPo36w2uGdsxpHeATtEt7F8JQHPOqcIXpsPc4D4AwOvIFx0G4-1XiEaMIhxHHAvU0D3qSsc8jW6bHouinm4O0pOuqLFT69zRN0f3lxt_1RXd9e_dxuritTC8ErQUrEbg3cMEmEYawTLQXZdLTvWmJE3XPRyVZoQxmjayM1YaJutOFN03ED9Qn6NnvHGH5NkLI62GTAOe0hTEmxRsjytYaQgn79D92HKfqSTrGWNQ1tiZCF-j5TJoaUIvRqjPag47OiRP0pQpUi1GsRhf3yZpy6Azz8I_9-vgDnM_BkHTy_b1Lbm4tZ-QIyPJPq
CitedBy_id crossref_primary_10_3389_fnmol_2022_855786
crossref_primary_10_3390_ijms23031188
crossref_primary_10_3390_ijms23031334
crossref_primary_10_3390_biology11020248
Cites_doi 10.1016/j.cell.2008.01.033
10.1002/cne.24374
10.1016/j.neuroscience.2012.09.022
10.1002/cne.20824
10.1016/j.abb.2007.03.036
10.1159/000351994
10.1016/j.brainres.2010.12.089
10.1021/acschemneuro.7b00496
10.1038/s41598-019-41521-6
10.1098/rstb.2006.2015
10.1101/cshperspect.a019018
10.1016/j.exer.2017.05.012
10.1002/glia.22990
10.1002/cne.23733
10.1002/cne.22481
10.1016/j.cub.2017.09.052
10.1126/science.aat0473
10.1016/j.physbeh.2010.04.003
10.1002/neu.480210804
10.1007/s00429-020-02038-1
10.1016/S0166-2236(02)02156-2
10.1002/cne.24092
10.1038/293141a0
10.1111/ede.12308
10.1016/B978-0-12-418669-9.00002-7
10.1242/dev.185595
10.1002/cne.23065
10.1111/j.1749-6632.1969.tb20432.x
10.1002/0471733849
10.1159/000235613
10.1007/s00429-010-0285-6
10.1523/JNEUROSCI.3222-16.2017
10.1073/pnas.1010442107
10.1016/j.cell.2019.05.050
10.1038/srep34331
10.1002/cne.22757
10.1242/dev.071878
10.1016/j.neuron.2016.09.005
10.1126/science.183.4123.425
10.1016/j.cub.2019.05.026
10.1016/j.brainres.2019.146350
10.1002/glia.22856
10.1002/glia.23849
10.1002/dvdy.22455
10.1038/nature25975
10.1016/j.brainresbull.2007.10.058
10.1002/cne.21604
10.1111/j.1460-9568.2004.03813.x
10.1002/bies.20615
10.1002/cne.20571
10.1002/glia.20971
10.1159/000229013
10.1002/cne.23100
ContentType Journal Article
Copyright 2021 The Authors. published by Wiley Periodicals LLC.
2021 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.
2021. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2021 The Authors. published by Wiley Periodicals LLC.
– notice: 2021 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.
– notice: 2021. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
DBID 24P
WIN
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7QR
7TK
8FD
FR3
K9.
P64
7X8
DOI 10.1002/cne.25126
DatabaseName Wiley Online Library Open Access
Wiley Online Library Free Content
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
Chemoreception Abstracts
Neurosciences Abstracts
Technology Research Database
Engineering Research Database
ProQuest Health & Medical Complete (Alumni)
Biotechnology and BioEngineering Abstracts
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
ProQuest Health & Medical Complete (Alumni)
Chemoreception Abstracts
Engineering Research Database
Technology Research Database
Neurosciences Abstracts
Biotechnology and BioEngineering Abstracts
MEDLINE - Academic
DatabaseTitleList
ProQuest Health & Medical Complete (Alumni)
MEDLINE
Database_xml – sequence: 1
  dbid: 24P
  name: Wiley-Blackwell Titles (Open access)
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Zoology
EISSN 1096-9861
EndPage 2823
ExternalDocumentID 10_1002_cne_25126
33580516
CNE25126
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: Banco de Santander. Spain
GroupedDBID ---
-DZ
-~X
.3N
.GA
05W
0R~
10A
123
1L6
1OB
1OC
1ZS
24P
33P
3SF
3WU
4.4
4ZD
50Y
50Z
51W
51X
52M
52N
52O
52P
52S
52T
52U
52W
52X
5RE
5VS
66C
702
79B
7PT
8-0
8-1
8-3
8-4
8-5
8UM
930
A03
AAESR
AAEVG
AAHHS
AANLZ
AAONW
AAXRX
AAZKR
ABCQN
ABCUV
ABIJN
ABIVO
ABJNI
ABOCM
ACAHQ
ACCFJ
ACCZN
ACGFS
ACIWK
ACPOU
ACPRK
ACXBN
ACXQS
ADBBV
ADEOM
ADIZJ
ADKYN
ADMGS
ADOZA
ADXAS
ADZMN
AEEZP
AEIGN
AEIMD
AELAQ
AENEX
AEQDE
AEUQT
AEUYR
AFBPY
AFFNX
AFFPM
AFGKR
AFPWT
AFZJQ
AHBTC
AHMBA
AITYG
AIURR
AIWBW
AJBDE
AJXKR
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AMBMR
AMYDB
ATUGU
AUFTA
AZBYB
AZVAB
BAFTC
BDRZF
BFHJK
BHBCM
BMNLL
BMXJE
BNHUX
BROTX
BRXPI
BY8
C45
CS3
D-E
D-F
DCZOG
DPXWK
DR1
DR2
DRFUL
DRSTM
DU5
EBS
EMOBN
F00
F01
F04
F5P
G-S
G.N
GNP
GODZA
H.T
H.X
HBH
HGLYW
HHY
HHZ
HZ~
IX1
J0M
JPC
KQQ
L7B
LATKE
LAW
LC2
LC3
LEEKS
LH4
LITHE
LOXES
LP6
LP7
LUTES
LW6
LYRES
MEWTI
MK4
MRFUL
MRSTM
MSFUL
MSSTM
MXFUL
MXSTM
N04
N05
N9A
NF~
NNB
O66
O9-
OVD
P2P
P2W
P2X
P4D
PALCI
PQQKQ
Q.N
Q11
QB0
QRW
R.K
ROL
RWD
RWI
RX1
RYL
SUPJJ
SV3
TEORI
UB1
V2E
W8V
W99
WBKPD
WIB
WIH
WIK
WIN
WJL
WNSPC
WOHZO
WQJ
WRC
WUP
WXSBR
WYISQ
XG1
XV2
YQT
ZZTAW
~IA
~WT
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7QR
7TK
8FD
FR3
K9.
P64
7X8
ID FETCH-LOGICAL-c3886-80805b7e6c2908c22b851e94b1fb50c83f68b958ac12217c9a02834ac644b6ce3
IEDL.DBID DR2
ISSN 0021-9967
IngestDate Fri Aug 16 10:02:15 EDT 2024
Thu Oct 10 19:33:26 EDT 2024
Fri Aug 23 00:35:34 EDT 2024
Sat Sep 28 08:25:59 EDT 2024
Sat Aug 24 01:03:23 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 10
Keywords Sox2
doublecortin
radial glia
cell proliferation
pallium
tissue clearing
telencephalon
astrocyte
Language English
License Attribution-NonCommercial
2021 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c3886-80805b7e6c2908c22b851e94b1fb50c83f68b958ac12217c9a02834ac644b6ce3
Notes Funding information
Banco de Santander. Spain
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0001-7591-4374
0000-0001-8154-3354
0000-0003-1976-0512
OpenAccessLink https://proxy.k.utb.cz/login?url=https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fcne.25126
PMID 33580516
PQID 2524415089
PQPubID 1006438
PageCount 11
ParticipantIDs proquest_miscellaneous_2489251400
proquest_journals_2524415089
crossref_primary_10_1002_cne_25126
pubmed_primary_33580516
wiley_primary_10_1002_cne_25126_CNE25126
PublicationCentury 2000
PublicationDate July 1, 2021
PublicationDateYYYYMMDD 2021-07-01
PublicationDate_xml – month: 07
  year: 2021
  text: July 1, 2021
  day: 01
PublicationDecade 2020
PublicationPlace Hoboken, USA
PublicationPlace_xml – name: Hoboken, USA
– name: United States
– name: New York
PublicationTitle Journal of comparative neurology (1911)
PublicationTitleAlternate J Comp Neurol
PublicationYear 2021
Publisher John Wiley & Sons, Inc
Wiley Subscription Services, Inc
Publisher_xml – name: John Wiley & Sons, Inc
– name: Wiley Subscription Services, Inc
References 2018; 362
2019; 1722
2010; 58
2012; 520
2010; 107
2018; 526
2019; 13
2007; 463
2008; 507
2010; 101
2005; 21
2006; 494
2008; 75
1969; 167
1974; 183
2007; 29
2018; 9
2010; 518
2017; 37
2010; 239
2019; 21
2019; 29
2017; 161
1968; 10
2017; 525
2011; 215
2019; 9
2015; 523
2017; 27
2020; 225
2005
2013; 140
2020; 147
2016; 91
2012; 226
2008; 363
2011; 1381
2002; 25
2016; 6
1990; 21
1981; 293
2009; 74
2017; 11
2005; 488
2015; 63
2018; 555
2016; 64
2013; 82
2020; 68
2016
2018; 11
2008; 132
2016; 8
2019; 178
e_1_2_9_31_1
e_1_2_9_52_1
e_1_2_9_50_1
e_1_2_9_10_1
e_1_2_9_35_1
e_1_2_9_56_1
e_1_2_9_12_1
e_1_2_9_33_1
e_1_2_9_54_1
e_1_2_9_14_1
e_1_2_9_39_1
e_1_2_9_16_1
e_1_2_9_37_1
e_1_2_9_58_1
e_1_2_9_18_1
Olivera‐Pasilio V. (e_1_2_9_48_1) 2017; 11
e_1_2_9_41_1
e_1_2_9_20_1
Garcia‐Pradas L. (e_1_2_9_23_1) 2018; 11
e_1_2_9_22_1
e_1_2_9_45_1
e_1_2_9_24_1
e_1_2_9_43_1
e_1_2_9_8_1
e_1_2_9_4_1
e_1_2_9_2_1
Rahmann H. (e_1_2_9_49_1) 1968; 10
e_1_2_9_26_1
e_1_2_9_28_1
e_1_2_9_47_1
e_1_2_9_30_1
e_1_2_9_53_1
e_1_2_9_51_1
e_1_2_9_11_1
e_1_2_9_34_1
e_1_2_9_57_1
e_1_2_9_13_1
e_1_2_9_32_1
e_1_2_9_55_1
e_1_2_9_15_1
e_1_2_9_38_1
e_1_2_9_17_1
e_1_2_9_36_1
e_1_2_9_19_1
e_1_2_9_42_1
e_1_2_9_40_1
e_1_2_9_21_1
e_1_2_9_46_1
Baeuml S. W. (e_1_2_9_6_1) 2019; 13
e_1_2_9_44_1
e_1_2_9_7_1
e_1_2_9_5_1
e_1_2_9_3_1
e_1_2_9_9_1
e_1_2_9_25_1
e_1_2_9_27_1
e_1_2_9_29_1
References_xml – volume: 526
  start-page: 899
  issue: 5
  year: 2018
  end-page: 919
  article-title: Comparative expression patterns of Sox2 and Sox19 genes in the forebrain of developing and adult turbot ( )
  publication-title: Journal of Comparative Neurology
– start-page: 27
  year: 2016
  end-page: 157
– volume: 63
  start-page: 1406
  issue: 8
  year: 2015
  end-page: 1428
  article-title: Radial glia and neural progenitors in the adult zebrafish central nervous system
  publication-title: Glia
– year: 2005
– volume: 225
  start-page: 817
  year: 2020
  end-page: 839
  article-title: Characterization of neurogenic niches in the telencephalon of juvenile and adult sharks
  publication-title: Brain Structure & Function.
– volume: 494
  start-page: 620
  issue: 4
  year: 2006
  end-page: 634
  article-title: A phylotypic stage in vertebrate brain development: GABA cell patterns in zebrafish compared with mouse
  publication-title: Journal of Comparative Neurology
– volume: 525
  start-page: 610
  issue: 3
  year: 2017
  end-page: 638
  article-title: Localization of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish,
  publication-title: Journal of Comparative Neurology
– volume: 29
  start-page: 745
  issue: 8
  year: 2007
  end-page: 757
  article-title: Adult neurogenesis in non‐mammalian vertebrates
  publication-title: Bioessays
– volume: 161
  start-page: 174
  year: 2017
  end-page: 192
  article-title: Sox2 regulates Muller glia reprogramming and proliferation in the regenerating zebrafish retina via Lin28 and Ascl1a
  publication-title: Experimental Eye Research
– volume: 183
  start-page: 425
  year: 1974
  end-page: 427
  article-title: Neurons in rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition
  publication-title: Science
– volume: 215
  start-page: 141
  issue: 3–4
  year: 2011
  end-page: 157
  article-title: The development and general morphology of the telencephalon of actinopterygian fishes: Synopsis, documentation and commentary
  publication-title: Brain Structure & Function
– volume: 74
  start-page: 110
  issue: 2
  year: 2009
  end-page: 120
  article-title: Cytoarchitecture of a cichlid fish telencephalon
  publication-title: Brain Behavior and Evolution
– volume: 518
  start-page: 4277
  issue: 21
  year: 2010
  end-page: 4287
  article-title: Astroglial structures in the zebrafish brain
  publication-title: Journal of Comparative Neurology
– volume: 64
  start-page: 1170
  issue: 7
  year: 2016
  end-page: 1189
  article-title: Gfap‐positive radial glial cells are an essential progenitor population for later‐born neurons and glia in the zebrafish spinal cord
  publication-title: Glia
– volume: 1722
  year: 2019
  article-title: Sox2 expression in the visual system of two teleost species
  publication-title: Brain Research
– volume: 11
  start-page: 1
  issue: 437
  year: 2017
  end-page: 23
  article-title: Cell proliferation, migration, and neurogenesis in the adult brain of the pulse type weakly electric fish, Gymnotus omarorum
  publication-title: Frontiers in Neuroscience
– volume: 362
  start-page: 181
  issue: 6411
  year: 2018
  end-page: 185
  article-title: Glia as architects of central nervous system formation and function
  publication-title: Science
– volume: 1381
  start-page: 95
  year: 2011
  end-page: 105
  article-title: The dorsal pallium in zebrafish, (Cyprinidae, Teleostei)
  publication-title: Brain Research
– volume: 132
  start-page: 645
  issue: 4
  year: 2008
  end-page: 660
  article-title: Mechanisms and functional implications of adult neurogenesis
  publication-title: Cell
– volume: 13
  start-page: 1
  issue: 19
  year: 2019
  end-page: 29
  article-title: Adult islet1 expression outlines ventralized derivatives along Zebrafish Neuraxis
  publication-title: Frontiers in Neuroanatomy
– volume: 523
  start-page: 1202
  issue: 8
  year: 2015
  end-page: 1221
  article-title: Comprehensive expression map of transcription regulators in the adult zebrafish telencephalon reveals distinct neurogenic niches
  publication-title: Journal of Comparative Neurology
– volume: 463
  start-page: 218
  issue: 2
  year: 2007
  end-page: 230
  article-title: Expression, characterization, and gene knockdown of zebrafish doublecortin‐like protein kinase
  publication-title: Archives of Biochemistry and Biophysics
– volume: 167
  start-page: 31
  year: 1969
  end-page: 64
  article-title: A survey of the structure of the forebrain in higher bony fishes (Osteichthyes)
  publication-title: Annals of the New York Academy of Sciences
– volume: 74
  start-page: 56
  issue: 1
  year: 2009
  end-page: 76
  article-title: Stalking the everted telencephalon: Comparisons of forebrain organization in basal ray‐finned fishes and teleosts
  publication-title: Brain, Behavior and Evolution
– volume: 27
  start-page: 3288
  issue: 21
  year: 2017
  end-page: 3301.e3283
  article-title: Life‐long neurogenic activity of individual neural stem cells and continuous growth establish an outside‐in architecture in the teleost pallium
  publication-title: Current Biology
– volume: 520
  start-page: 3471
  year: 2012
  end-page: 3491
  article-title: Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status
  publication-title: The Journal of Comparative Neurology
– volume: 147
  issue: 1
  year: 2020
  article-title: Single cell sequencing of radial glia progeny reveals the diversity of newborn neurons in the adult zebrafish brain
  publication-title: Development
– volume: 555
  start-page: 377
  year: 2018
  end-page: 381
  article-title: Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults
  publication-title: Nature
– volume: 10
  start-page: 279
  year: 1968
  end-page: 284
  article-title: Autoradiographische Untersuchungen zum DNA‐Stoffwechsel Mitose‐Häufigkeit im ZNS von Brachydanio rerio HAM. BUCH. Cyprinidae, Pisces
  publication-title: Journal für Hirnforschung
– volume: 178
  start-page: 27
  issue: 1
  year: 2019
  end-page: 43.e19
  article-title: Glia accumulate evidence that actions are futile and suppress unsuccessful behavior
  publication-title: Cell
– volume: 58
  start-page: 870
  issue: 7
  year: 2010
  end-page: 888
  article-title: Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon
  publication-title: Glia
– volume: 91
  start-page: 1219
  issue: 6
  year: 2016
  end-page: 1227
  article-title: Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development
  publication-title: Neuron
– volume: 21
  start-page: 1180
  year: 1990
  end-page: 1188
  article-title: Social control of neuronal soma size
  publication-title: Journal of Neurobiology
– volume: 11
  start-page: 1
  issue: 367
  year: 2018
  end-page: 12
  article-title: Glial cells in the fish retinal nerve fiber layer form tight junctions, separating and surrounding axons
  publication-title: Frontiers in Molecular Neuroscience
– volume: 239
  start-page: 3336
  issue: 12
  year: 2010
  end-page: 3349
  article-title: Expression of the transcription factor Olig2 in proliferating cells in the adult Zebrafish telencephalon
  publication-title: Developmental Dynamics
– volume: 9
  start-page: 1951
  issue: 8
  year: 2018
  end-page: 1962
  article-title: : A model system for analyzing the neurobiology of behavior
  publication-title: ACS Chemical Neuroscience
– volume: 520
  start-page: 2275
  issue: 10
  year: 2012
  end-page: 2316
  article-title: The cellular composition of neurogenic periventricular zones in the adult zebrafish forebrain
  publication-title: Journal of Comparative Neurology
– volume: 226
  start-page: 367
  year: 2012
  end-page: 381
  article-title: Cell proliferation pattern in adult zebrafish forebrain is sexually dimorphic
  publication-title: Neuroscience
– volume: 6
  start-page: 34331
  year: 2016
  article-title: Large‐scale tissue clearing (PACT): Technical evaluation and new perspectives in immunofluorescence, histology, and ultrastructure
  publication-title: Scientific Reports
– volume: 140
  start-page: 1445
  issue: 7
  year: 2013
  end-page: 1456
  article-title: SOX2 maintains the quiescent progenitor cell state of postnatal retinal Müller glia
  publication-title: Development
– volume: 21
  start-page: 330
  issue: 6
  year: 2019
  end-page: 341
  article-title: Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes
  publication-title: Evolution & Development
– volume: 101
  start-page: 32
  issue: 1
  year: 2010
  end-page: 39
  article-title: Forebrain cell proliferation, behavior, and physiology of zebrafish, , kept in enriched or barren environments
  publication-title: Physiology and Behavior
– volume: 8
  start-page: 1
  issue: 7
  year: 2016
  end-page: 21
  article-title: Adult neurogenesis in fish
  publication-title: Cold Spring Harbor Perspectives in Biology
– volume: 107
  start-page: 21176
  issue: 49
  year: 2010
  end-page: 21180
  article-title: Female genomic response to mate information
  publication-title: Proceedings of the National Academy of Sciences
– volume: 520
  start-page: 633
  issue: 3
  year: 2012
  end-page: 655
  article-title: Subdivisions of the adult zebrafish subpallium by molecular marker analysis
  publication-title: Journal of Comparative Neurology
– volume: 21
  start-page: 1
  issue: 1
  year: 2005
  end-page: 14
  article-title: Doublecortin expression levels in adult brain reflect neurogenesis
  publication-title: European Journal of Neuroscience
– volume: 507
  start-page: 1245
  issue: 2
  year: 2008
  end-page: 1257
  article-title: Early teleostean basal ganglia development visualized by Zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression
  publication-title: Journal of Comparative Neurology
– volume: 488
  start-page: 290
  issue: 3
  year: 2005
  end-page: 319
  article-title: Proliferation, migration, neuronal differentiation, and long‐term survival of new cells in the adult zebrafish brain
  publication-title: Journal of Comparative Neurology
– volume: 75
  start-page: 191
  issue: 2–4
  year: 2008
  end-page: 205
  article-title: Forebrain evolution in bony fishes
  publication-title: Brain Research Bulletin
– volume: 363
  start-page: 101
  issue: 1489
  year: 2008
  end-page: 122
  article-title: Proliferation, neurogenesis and regeneration in the non‐mammalian vertebrate brain
  publication-title: Philosophical Transactions of the Royal Society B‐Biological Sciences
– volume: 9
  start-page: 5083
  issue: 1
  year: 2019
  article-title: Male dominance status regulates odor‐evoked processing in the forebrain of a cichlid fish
  publication-title: Scientific Reports
– volume: 293
  start-page: 141
  year: 1981
  end-page: 142
  article-title: Genesis of rods in teleost fish retina
  publication-title: Nature
– volume: 25
  start-page: 235
  issue: 5
  year: 2002
  end-page: 238
  article-title: Radial glia: Multi‐purpose cells for vertebrate brain development
  publication-title: Trends in Neurosciences
– volume: 82
  start-page: 31
  issue: 1
  year: 2013
  end-page: 44
  article-title: The Pallium and mind/behavior relationships in teleost fishes
  publication-title: Brain, Behavior and Evolution
– volume: 29
  start-page: R647
  issue: 13
  year: 2019
  end-page: R662
  article-title: Evolution of the chordate telencephalon
  publication-title: Current Biology
– volume: 68
  start-page: 2451
  issue: 12
  year: 2020
  end-page: 2470
  article-title: Radial glia in the zebrafish brain: Functional, structural, and physiological comparison with the mammalian glia
  publication-title: Glia
– volume: 37
  start-page: 1900
  issue: 7
  year: 2017
  end-page: 1909
  article-title: Circadian kinetics of cell cycle progression in adult neurogenic niches of a diurnal vertebrate
  publication-title: The Journal of Neuroscience
– ident: e_1_2_9_57_1
  doi: 10.1016/j.cell.2008.01.033
– ident: e_1_2_9_54_1
  doi: 10.1002/cne.24374
– ident: e_1_2_9_5_1
  doi: 10.1016/j.neuroscience.2012.09.022
– ident: e_1_2_9_39_1
  doi: 10.1002/cne.20824
– ident: e_1_2_9_51_1
  doi: 10.1016/j.abb.2007.03.036
– ident: e_1_2_9_15_1
  doi: 10.1159/000351994
– ident: e_1_2_9_38_1
  doi: 10.1016/j.brainres.2010.12.089
– volume: 13
  start-page: 1
  issue: 19
  year: 2019
  ident: e_1_2_9_6_1
  article-title: Adult islet1 expression outlines ventralized derivatives along Zebrafish Neuraxis
  publication-title: Frontiers in Neuroanatomy
  contributor:
    fullname: Baeuml S. W.
– ident: e_1_2_9_34_1
  doi: 10.1021/acschemneuro.7b00496
– ident: e_1_2_9_45_1
  doi: 10.1038/s41598-019-41521-6
– ident: e_1_2_9_29_1
  doi: 10.1098/rstb.2006.2015
– ident: e_1_2_9_21_1
  doi: 10.1101/cshperspect.a019018
– ident: e_1_2_9_24_1
  doi: 10.1016/j.exer.2017.05.012
– ident: e_1_2_9_27_1
  doi: 10.1002/glia.22990
– ident: e_1_2_9_18_1
  doi: 10.1002/cne.23733
– ident: e_1_2_9_25_1
  doi: 10.1002/cne.22481
– ident: e_1_2_9_20_1
  doi: 10.1016/j.cub.2017.09.052
– ident: e_1_2_9_4_1
  doi: 10.1126/science.aat0473
– ident: e_1_2_9_56_1
  doi: 10.1016/j.physbeh.2010.04.003
– ident: e_1_2_9_14_1
  doi: 10.1002/neu.480210804
– ident: e_1_2_9_19_1
  doi: 10.1007/s00429-020-02038-1
– ident: e_1_2_9_11_1
  doi: 10.1016/S0166-2236(02)02156-2
– ident: e_1_2_9_32_1
  doi: 10.1002/cne.24092
– ident: e_1_2_9_26_1
  doi: 10.1038/293141a0
– ident: e_1_2_9_2_1
  doi: 10.1111/ede.12308
– ident: e_1_2_9_40_1
  doi: 10.1016/B978-0-12-418669-9.00002-7
– ident: e_1_2_9_30_1
  doi: 10.1242/dev.185595
– ident: e_1_2_9_31_1
  doi: 10.1002/cne.23065
– ident: e_1_2_9_43_1
  doi: 10.1111/j.1749-6632.1969.tb20432.x
– ident: e_1_2_9_10_1
  doi: 10.1002/0471733849
– ident: e_1_2_9_9_1
  doi: 10.1159/000235613
– ident: e_1_2_9_44_1
  doi: 10.1007/s00429-010-0285-6
– ident: e_1_2_9_3_1
  doi: 10.1523/JNEUROSCI.3222-16.2017
– ident: e_1_2_9_17_1
  doi: 10.1073/pnas.1010442107
– ident: e_1_2_9_37_1
  doi: 10.1016/j.cell.2019.05.050
– ident: e_1_2_9_42_1
  doi: 10.1038/srep34331
– ident: e_1_2_9_22_1
  doi: 10.1002/cne.22757
– ident: e_1_2_9_53_1
  doi: 10.1242/dev.071878
– ident: e_1_2_9_47_1
  doi: 10.1016/j.neuron.2016.09.005
– ident: e_1_2_9_50_1
  doi: 10.1126/science.183.4123.425
– volume: 11
  start-page: 1
  issue: 437
  year: 2017
  ident: e_1_2_9_48_1
  article-title: Cell proliferation, migration, and neurogenesis in the adult brain of the pulse type weakly electric fish, Gymnotus omarorum
  publication-title: Frontiers in Neuroscience
  contributor:
    fullname: Olivera‐Pasilio V.
– ident: e_1_2_9_8_1
  doi: 10.1016/j.cub.2019.05.026
– ident: e_1_2_9_16_1
  doi: 10.1016/j.brainres.2019.146350
– ident: e_1_2_9_55_1
  doi: 10.1002/glia.22856
– ident: e_1_2_9_28_1
  doi: 10.1002/glia.23849
– ident: e_1_2_9_36_1
  doi: 10.1002/dvdy.22455
– ident: e_1_2_9_52_1
  doi: 10.1038/nature25975
– volume: 10
  start-page: 279
  year: 1968
  ident: e_1_2_9_49_1
  article-title: Autoradiographische Untersuchungen zum DNA‐Stoffwechsel Mitose‐Häufigkeit im ZNS von Brachydanio rerio HAM. BUCH. Cyprinidae, Pisces
  publication-title: Journal für Hirnforschung
  contributor:
    fullname: Rahmann H.
– ident: e_1_2_9_46_1
  doi: 10.1016/j.brainresbull.2007.10.058
– ident: e_1_2_9_41_1
  doi: 10.1002/cne.21604
– ident: e_1_2_9_13_1
  doi: 10.1111/j.1460-9568.2004.03813.x
– ident: e_1_2_9_12_1
  doi: 10.1002/bies.20615
– volume: 11
  start-page: 1
  issue: 367
  year: 2018
  ident: e_1_2_9_23_1
  article-title: Glial cells in the fish retinal nerve fiber layer form tight junctions, separating and surrounding axons
  publication-title: Frontiers in Molecular Neuroscience
  contributor:
    fullname: Garcia‐Pradas L.
– ident: e_1_2_9_58_1
  doi: 10.1002/cne.20571
– ident: e_1_2_9_35_1
  doi: 10.1002/glia.20971
– ident: e_1_2_9_7_1
  doi: 10.1159/000229013
– ident: e_1_2_9_33_1
  doi: 10.1002/cne.23100
SSID ssj0009938
Score 2.4384973
Snippet In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth...
SourceID proquest
crossref
pubmed
wiley
SourceType Aggregation Database
Index Database
Publisher
StartPage 2813
SubjectTerms Animals
Astatotilapia burtoni
astrocyte
Astrocytes
Brain
Cell differentiation
cell proliferation
Cichlids - growth & development
doublecortin
Doublecortin protein
Ependymoglial Cells - physiology
Female
Glial cells
Growth patterns
Immunocytochemistry
Male
Neurogenesis - physiology
Neuronal-glial interactions
Pallium
Proliferating cell nuclear antigen
radial glia
Radial glial cells
Sox2
Stem cells
Telencephalon
Telencephalon - growth & development
tissue clearing
Ventricle
Title Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fcne.25126
https://www.ncbi.nlm.nih.gov/pubmed/33580516
https://www.proquest.com/docview/2524415089
https://search.proquest.com/docview/2489251400
Volume 529
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1La9wwEB7SQKGXJm362CQNauihF29s2ZIlcgp5EAoNITQQSsFIWjlrutjLrveSX58Zeb1JGgqlN4OshzUz0jfSzGeAL5RbKQXXkXDGRpkXZaQzM4pyK7VEMZempETh7xfy_Dr7diNu1uCwz4Xp-CFWB25kGWG9JgM3dn7wQBrqaj-kzZnotpM0p3Cuk6sH6ijcd7tVmEIQtMx7VqGYH6xqPt2LngHMp3g1bDhnG_CrH2oXZ_J7uGjt0N39weL4n9-yCa-XQJQddZrzBtZ8_RZe_mzCMfsWzB4nabKmZDMiMZiw20llGNE-odqyW_Th2zGbBo7OmlU1QzjJWh8SmaZjM-mqGjb1MxxSgzJlZTUfsyPKY2railLpDEO5IgKt3sH12emP4_No-X-GyKVKEY-xioXNvXRcx8pxbhG-eZ3ZpLQidiotpbJaKOMSjp6P04bATGYcYjArnU_fw3rd1P4jMGX4iAvjHKW28sRanmsfvD2JmjMqB7DfS6qYdjQcRUe4zAucvCJM3gB2exkWS0ucYwknlzFWegCfV8VoQ3QxYmrfLPCdTGlsAZezAXzoZL_qJaV7YpFg41-DBP_efXF8cRoetv_91R14xUlDQ_zvLqy3s4X_hCintXvwgmeXe0Gp7wEOxvjS
link.rule.ids 315,783,787,1378,11574,27936,27937,46064,46306,46488,46730
linkProvider Wiley-Blackwell
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB6VIgQXyqOFbQsY1AOXbLNO7LWlXqo-tEC7B9RKFVIV2V6nG7FKVtvshV_fGWezfQkJcYvkZzwz9je25zPADsVWSsF1JJyxUepFHunUjKK-lVqimHOTU6Dw6VAOztPvF-JiBfbaWJiGH2K54UaWEeZrMnDakN69ZQ11pe_S6iyfwFM094Qebjj8eUsehStvMw_TJQQt-y2vUMx3l0Xvr0aPIOZ9xBqWnOM1uGw729w0-d2d17br_jzgcfzfv3kFLxdYlO03yvMaVnz5Bp79qsJO-1uY3Y3TZFXOZsRjMGFXk8IwYn5CzWVX6MbXYzYNNJ0lK0qGiJLVPsQyTcdm0hQ1bOpn2KcKxcry4nrM9imUqaoLiqYzDEWLILRYh_Pjo7ODQbR4oiFyiVJEZaxiYfteOq5j5Ti3iOC8Tm0vtyJ2Ksmlsloo43ocnR-nDeGZ1DiEYVY6n2zAalmV_j0wZfiIC-McRbfynrW8r31w-CQqzyjvwJdWVNm0YeLIGs5lnuHgZWHwOrDdCjFbGOM1pnDyGmOlO_B5mYxmRGcjpvTVHPOkSmMNOKN14F0j_GUrCR0Vix5W_jWI8O_NZwfDo_Cx-e9ZP8HzwdnpSXbybfhjC15wUtdwHXgbVuvZ3H9A0FPbj0G3bwCuE_wT
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3Pb9MwFH4qQ0NcJmAMOgZ4iAOXbKkTu7Y4TWPVgFH1QKVpl8h27TVSlURd9v_zntN2VBMSt0j-Jb33bH_P9vcF4DNxK6XgOhHO2CT3IiQ6N7NkaKWW6OZgAhGFf43l5TT_cS2ue_B1zYXp9CE2B240M-J6TRO8mYXTB9FQV_kT2pzlE3iaIwwn4XyeTx4Ud3XWLcP0BkHL4VpWKOWnm6bbm9EjhLkNWOOOM3oBeyuoyM46376Enq9ewe5NHQ_C92H5N42S1YEtSWZgwW4XpWEkzISBxW4xy27nrIkqmhUrK4aAj7U-Uo2auVl0TQ1r_BINUKPVWSjv5uyMmEZ1WxLZzTC0PGLE8jVMRxe_zy-T1R8UEpcpRUrDKhV26KXjOlWOc4sAy-vcDoIVqVNZkMpqoYwbcMxNnDYEN3LjECVZ6Xx2ADtVXfm3wJThMy6Mc0Q-5QNr-VD7mI9J9O0s9OHT2pRF0wllFJ0kMi_Q3kW0dx-O1kYuVnPlDks4JXWp0n043hRjlNPVhal8fY91cqWxB1xw-vCmc85mlIxucsUAO_8SvfXv4Yvz8UX8OPz_qh_h2eTbqLj6Pv75Dp5ziqYoq3kEO-3y3r9HSNLaDzH0_gAwZdqZ
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Organization+of+radial+glia+reveals+growth+pattern+in+the+telencephalon+of+a+percomorph+fish+Astatotilapia+burtoni&rft.jtitle=Journal+of+comparative+neurology+%281911%29&rft.au=Mack%2C+Andreas+F.&rft.au=DeOliveira%E2%80%90Mello%2C+Laura&rft.au=Mattheus%2C+Ulrich&rft.au=Neckel%2C+Peter+H.&rft.date=2021-07-01&rft.issn=0021-9967&rft.eissn=1096-9861&rft_id=info:doi/10.1002%2Fcne.25126&rft.externalDBID=n%2Fa&rft.externalDocID=10_1002_cne_25126
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0021-9967&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0021-9967&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0021-9967&client=summon