Müller glia: Stem cells for generation and regeneration of retinal neurons in teleost fish

Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical dest...

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Bibliographic Details
Published inProgress in retinal and eye research Vol. 40; pp. 94 - 123
Main Authors Lenkowski, Jenny R., Raymond, Pamela A.
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 01.05.2014
Subjects
Adult neurogenesis
Animals
Cell Differentiation
Ependymoglial Cells - physiology
Müller glia
Radial glia
Retina - embryology
Retina - growth & development
Retina - injuries
Retinal Neurons - physiology
Retinal regeneration
Retinal stem cells
Stem Cells - physiology
Visual Perception - physiology
Zebrafish
CNTF
HSP60
HB-EGF
BLBP
Ngn1/2
NRL
PVR
TNF
Oct4
OLM
Cdh2
Rx1/2
Retinal regeneration
Müller glia
Mib
Dkk1
IL-6
RA
CMZ
Alcama
Acsl1a
Mdka/b
Insm1a
ERG
DHA
Olig2
ERK
IKNM
Adult neurogenesis
Tuba1
CNS
YAP
FACS
ONL
GFP
Stat
Apobec2a/2b
ESC
Epb41l5
Radial glia
ApoE
PI3/AKT
Wnt
CA
CRALBP
DAPT
hpf
dpl
Drgal1-l2
BMP
hpl
Neurod
ECM
GFAP
EdU
NICD
IdU
Sox
Vsx2
Atoh7
Nnc
NCAM
TAZ
Shh
TUNEL
Six3
group E
PSA
FGF
cMyca/b
iPSC
EM
Pax6
MAPK
EMT
MMP
Crb
Tgfβi
Ptc
NO
Nr2e3
PCNA
Retinal stem cells
INL
RPE
Crx
Moe
EGF
IGF
GS
Fzd
GCL
tgif1
Her
Jak
PDGF
Par3
TGFβ
BrdU
Online AccessGet full text
ISSN1350-9462
1873-1635
1873-1635
DOI10.1016/j.preteyeres.2013.12.007

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Abstract Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine. •Müller glia generate rod photoreceptors in growing adult fish retinas.•Injury-induced Müller glia transiently dedifferentiate but retain a glial identity.•Retinal injury induces Müller glia to generate a multipotent retinal progenitor.•Regeneration of retinal neurons in fish restores visual function.
AbstractList Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine.
Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine.
Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine. •Müller glia generate rod photoreceptors in growing adult fish retinas.•Injury-induced Müller glia transiently dedifferentiate but retain a glial identity.•Retinal injury induces Müller glia to generate a multipotent retinal progenitor.•Regeneration of retinal neurons in fish restores visual function.
Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine.Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage, and fish can regenerate retinal neurons, including photoreceptors, and restore functional vision following photic, chemical, or mechanical destruction of the retina. Müller glial cells in fish function as radial-glial-like neural stem cells. During adult growth, Müller glial nuclei undergo sporadic, asymmetric, self-renewing mitotic divisions in the inner nuclear layer to generate a rod progenitor that migrates along the radial fiber of the Müller glia into the outer nuclear layer, proliferates, and differentiates exclusively into rod photoreceptors. When retinal neurons are destroyed, Müller glia in the immediate vicinity of the damage partially and transiently dedifferentiate, re-express retinal progenitor and stem cell markers, re-enter the cell cycle, undergo interkinetic nuclear migration (characteristic of neuroepithelial cells), and divide once in an asymmetric, self-renewing division to generate a retinal progenitor. This daughter cell proliferates rapidly to form a compact neurogenic cluster surrounding the Müller glia; these multipotent retinal progenitors then migrate along the radial fiber to the appropriate lamina to replace missing retinal neurons. Some aspects of the injury-response in fish Müller glia resemble gliosis as observed in mammals, and mammalian Müller glia exhibit some neurogenic properties, indicative of a latent ability to regenerate retinal neurons. Understanding the specific properties of fish Müller glia that facilitate their robust capacity to generate retinal neurons will inform and inspire new clinical approaches for treating blindness and visual loss with regenerative medicine.
Author Lenkowski, Jenny R.
Raymond, Pamela A.
Author_xml – sequence: 1
  givenname: Jenny R.
  surname: Lenkowski
  fullname: Lenkowski, Jenny R.
  email: jenny.lenkowski@goucher.edu
– sequence: 2
  givenname: Pamela A.
  surname: Raymond
  fullname: Raymond, Pamela A.
  email: praymond@umich.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24412518$$D View this record in MEDLINE/PubMed
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Keywords CNTF
HSP60
HB-EGF
BLBP
Ngn1/2
NRL
PVR
TNF
Oct4
OLM
Cdh2
Rx1/2
Retinal regeneration
Müller glia
Mib
Dkk1
IL-6
RA
CMZ
Alcama
Acsl1a
Mdka/b
Insm1a
ERG
DHA
Olig2
ERK
IKNM
Adult neurogenesis
Tuba1
CNS
YAP
FACS
ONL
GFP
Stat
Apobec2a/2b
ESC
Epb41l5
Radial glia
ApoE
PI3/AKT
Wnt
CA
CRALBP
DAPT
hpf
dpl
Drgal1-l2
BMP
hpl
Neurod
ECM
GFAP
EdU
NICD
IdU
Sox
Vsx2
Atoh7
Nnc
NCAM
TAZ
Shh
TUNEL
Six3
group E
PSA
FGF
cMyca/b
iPSC
EM
Pax6
MAPK
EMT
MMP
Crb
Tgfβi
Ptc
NO
Nr2e3
PCNA
Retinal stem cells
INL
RPE
Crx
Moe
EGF
IGF
GS
Fzd
GCL
tgif1
Her
Jak
PDGF
Par3
TGFβ
BrdU
Language English
License Copyright © 2014. Published by Elsevier Ltd.
This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Percentage of work contributed by each author in the production of the manuscript is as follows: Jenny R. Lenkowski: 50%; Pamela A. Raymond: 50%.
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PublicationTitle Progress in retinal and eye research
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Snippet Adult zebrafish generate new neurons in the brain and retina throughout life. Growth-related neurogenesis allows a vigorous regenerative response to damage,...
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SubjectTerms Adult neurogenesis
Animals
Cell Differentiation
Ependymoglial Cells - physiology
Müller glia
Radial glia
Retina - embryology
Retina - growth & development
Retina - injuries
Retinal Neurons - physiology
Retinal regeneration
Retinal stem cells
Stem Cells - physiology
Visual Perception - physiology
Zebrafish
Title Müller glia: Stem cells for generation and regeneration of retinal neurons in teleost fish
URI https://dx.doi.org/10.1016/j.preteyeres.2013.12.007
https://www.ncbi.nlm.nih.gov/pubmed/24412518
https://www.proquest.com/docview/1530319309
https://pubmed.ncbi.nlm.nih.gov/PMC3999222
Volume 40
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