We have identified Math5, a mouse basic helix-loop-helix (bHLH) gene that is closely related to Drosophila atonal and Xenopus Xath5 and is largely restricted to the developing eye. Math5 retinal expression precedes differentiation of the first neurons and persists within progenitor cells until after birth. To position Math5 in a hierarchy of retinal development, we compared Math5 and Hes1 expression in wild-type and Pax6-deficient (Sey) embryos. Math5 expression is downregulated in Sey/+ eyes and abolished in Sey/Sey eye rudiments, whereas the bHLH gene Hes1 is upregulated in a similar dose-dependent manner. These results link Pax6 to the process of retinal neurogenesis and provide the first molecular correlate for the dosage-sensitivity of the Pax6 phenotype. During retinogenesis, Math5 is expressed significantly before NeuroD, Ngn2 or Mash1. To test whether these bHLH genes influence the fates of distinct classes of retinal neurons, we ectopically expressed Math5 and Mash1 in Xenopus retinal progenitors. Unexpectedly, lipofection of either mouse gene into the frog retina caused an increase in differentiated bipolar cells. Directed expression of Math5, but not Xath5, in Xenopus blastomeres produced an expanded retinal phenotype. We propose that Math5 acts as a proneural gene, but has properties different from its most closely related vertebrate family member, Xath5.

REFERENCES

Acharya
H. R.
,
Dooley
C. M.
,
Thoreson
W. B.
,
Ahmad
I.
(
1997
)
cDNA cloning and expression analysis of NeuroD mRNA in human retina.
Biochem. Biophys. Res. Commun
233
,
459
463
Akazawa
C.
,
Ishibashi
M.
,
Shimizu
C.
,
Nakanishi
S.
,
Kageyama
R.
(
1995
)
A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system.
J. Biol. Chem
270
,
8730
8738
Alexiades
M. R.
,
Cepko
C. L.
(
1997
)
Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny.
Development
124
,
1119
1131
Belecky-Adams
T.
,
Tomarev
S.
,
Li
H.-S.
,
Ploder
L.
,
McInnes
R. R.
,
Sundin
O.
,
Adler
R.
(
1997
)
Pax-6, Prox1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells.
Invest. Ophth. Vis. Sci
38
,
1293
1303
Ben-Arie
N.
,
McCall
A. E.
,
Berkman
S.
,
Eichele
G.
,
Bellen
H. J.
,
Zoghbi
H.
(
1996
)
Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis.
Hum. Mol. Genet
5
,
1207
1216
Brown
N. L.
,
Paddock
S. W.
,
Sattler
C. A.
,
Cronmiller
C.
,
Thomas
B. J.
,
Carroll
S. B.
(
1996
)
daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression.
Dev. Biol
179
,
65
78
Brown
N. L.
,
Sattler
C. A.
,
Paddock
S. W.
,
Carroll
S. B.
(
1995
)
Hairy and Emc negatively regulate morphogenetic furrow progression in the Drosophila eye.
Cell
80
,
879
887
Campuzano
S.
,
Modolell
J.
(
1992
)
Patterning of the Drosophila nervous system: the achaete-scute gene complex.
Trends Genet
8
,
202
208
Carter-Dawson
L. D.
,
LaVail
M. M.
(
1979
)
Rods and cones in the mouse retina 1. Autoradiographic analysis of cell generation using tritiated thymidine.
J. Comp. Neurol
188
,
263
272
Cau
E.
,
Gradwohl
G.
,
Fode
C.
,
Guillemot
F.
(
1997
)
Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors.
Development
124
,
1611
1621
Caudy
M.
,
Grell
E. H.
,
Dambly-Chaudiere
C.
,
Ghysen
A.
,
Jan
L. Y.
,
Jan
Y. N.
(
1988
)
The maternal sex determination gene daughterless has zygotic activity necessary for the formation of peripheral neurons in Drosophila.
Genes Dev
2
,
843
852
Cepko
C. L.
,
Austin
C. P.
,
Yang
X.
,
Alexiades
M.
,
Ezzeddine
D.
(
1996
)
Cell fate determination in the vertebrate retina.
Proc. Nat. Acad. Sci. USA
93
,
589
595
Chien
C.-T.
,
Hsiao
C.-D.
,
Jan
L. Y.
,
Jan
Y. N.
(
1996
)
Neuronal typeinformation encoded in the basic helix-loop-helix domain of proneural genes.
Proc. Nat. Acad. Sci.USA
93
,
13239
13244
Chisolm
A.D.
,
Horvitz
H.R.
(
1995
)
Patterning of the Caenorhabditis elegans head region by the Pax-6 family member, vab-3.
Nature
377
,
52
55
Cronmiller
C.
,
Schedl
P.
,
Cline
T. W.
(
1988
)
Molecular characterization of daughterless, a Drosophila sex determination gene with multiple roles in development.
Genes Dev
2
,
1666
1676
Cvekl
A.
,
Piatigorsky
J.
(
1996
)
Lens development and crystallin gene expression: many roles for Pax-6.
BioEssays
18
,
621
630
Davis
J. A.
,
Reed
R. L.
(
1996
)
Role of Olf-1 and Pax-6 transcription factors in neurodevelopment.
J. Neurosci
16
,
5082
5094
del Rio
J. A.
,
Soriano
E.
(
1989
)
Immunocytochemical detection of 5-bromodeoxyuridine incorporation in the central nervous system of the mouse.
Brain Res. Dev. Brain Res
49
,
311
317
Desplan
C.
(
1997
)
Eye development: governed by dictator or junta?.
Cell
91
,
861
864
Dokucu
M. E.
,
Zipursky
S. L.
,
Cagan
R. L.
(
1996
)
Atonal, Rough, and the resolution of proneural clusters in the developing Drosophila retina.
Development
122
,
4139
4147
Dorsky
R. I.
,
Rapaport
D. H.
,
Harris
W. A.
(
1995
)
Xotch inhibits cell differentiation in the Xenopus retina.
Neuron
14
,
487
496
Dorsky
R. I.
,
Chang
W. S.
,
Rapaport
D. H.
,
Harris
W. A.
(
1997
)
Regulation of neuronal diversity in the Xenopus retina by Delta signalling.
Nature
385
,
67
70
Erkman
L.
,
McEvilly
R. J.
,
Luo
L.
,
Ryan
A. K.
,
Hooshmand
F.
,
O'Connell
S. M.
,
Keithley
E. M.
,
Rapaport
D. H.
,
Ryan
A. F.
,
Rosenfeld
M. G.
(
1996
).
Role of transcription factors Brn-3.1 and Brn-3.2 in auditory and visual system development.
Nature
381
,
603
606
Ferreiro
B.
,
Skoglund
P.
,
Bailey
A.
,
Dorsky
R.
,
Harris
W. A.
(
1992
)
XASH1, a Xenopus homolog of achaete-scute: A proneural gene in anterior regions of the vertebrate CNS.
Mech. Dev
40
,
25
36
Fujiwara
M.
,
Uchida
T.
,
Osumi-Yamashita
N.
,
Eto
K.
(
1994
)
Uchida rat (rSey): a new mutant rat with craniofacial abnormalities resembling those of the mouse Sey mutant.
Differentiation
57
,
31
38
Furukawa
T.
,
Kozak
C. A.
,
Cepko
C. L.
(
1997
)
rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina.
Proc. Nat. Acad. Sci.USA
94
,
3088
3093
Furukawa
T.
,
Morrow
E. M.
,
Cepko
C. L.
(
1997
)
Crx, a novel otx-like homeobox gene, shows photoreceptor specific expression and regulates photoreceptor differentiation.
Cell
91
,
531
541
Ghysen
A.
,
Dambly-Chaudiere
C.
,
Jan
L. Y.
,
Jan
Y. N.
(
1993
)
Cell interactions and gene interactions in peripheral neurogenesis.
Genes Dev
7
,
723
733
Glaser
T.
,
Lane
J.
,
Housman
D.
(
1990
)
A mouse model of the Aniridia-Wilms tumor deletion syndrome.
Science
250
,
823
827
Glaser
T.
,
Walton
D. S.
,
Maas
R. L.
(
1992
)
Genomic structure, evolutionary conservation and aniridia mutations in the human Pax6 gene.
Nat. Genet
2
,
232
239
Glaser
T.
,
Jepeal
L.
,
Edwards
J. G.
,
Young
S. R.
,
Favor
J.
,
Maas
R. L.
(
1994
)
PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects.
Nat. Genet
7
,
463
471
Gradwohl
G.
,
Fode
C.
,
Guillemot
F.
(
1996
)
Restricted expression of a novel murine atonal -related bHLH protein in undifferentiated neural precursors.
Dev. Biol
180
,
227
241
Grindley
J. C.
,
Davidson
D. R.
,
Hill
R. E.
(
1995
)
The role of Pax-6 in eye and nasal development.
Development
121
,
1433
1442
Guillemot
F.
,
Cepko
C.
(
1992
)
Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an in vitro assay of early retinal development.
Development
114
,
743
754
Guillemot
F.
,
Joyner
A. L.
(
1993
)
Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system.
Mech. Dev
42
,
171
185
Guillemot
F.
,
Lo
L.-C.
,
Johnson
J.
,
Auerbach
A.
,
Anderson
D. J.
,
Joyner
A. L.
(
1993
)
Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons.
Cell
75
,
463
476
Halder
G.
,
Callaerts
P.
,
Flister
S.
,
Walldorf
U.
,
Gehring
W. J.
(
1998
)
eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development.
Development
125
,
2181
2191
Halder
G.
,
Callaerts
P.
,
Gehring
W. J.
(
1995
)
New perspective on eye evolution.
Curr. Biol
5
,
602
609
Hanson
I.
,
van Heyningen
V.
(
1995
)
Pax6: more than meets the eye.
Trends. Genet
11
,
268
272
Harland
R.
(
1991
)
In situ hybridization: an improved whole-mount method for Xenopus embryos.
Methods Cell Biol
36
,
685
695
Henrique
D.
,
Hirsinger
E.
,
Adam
J.
,
Le Roux
I.
,
Pourquie
O.
,
Ish-Horowicz
D.
,
Lewis
J.
(
1997
)
Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina.
Current Biol
7
,
661
670
Hill
R. E.
,
Favor
J.
,
Hogan
B. L.
,
Ton
C. C.
,
Saunders
G. F.
,
Hanson
I. M.
,
Prosser
J.
,
Jordan
T.
,
Hastie
N. D.
,
van Heyningen
V.
(
1991
)
Mouse Small eye results from mutations in a paired-like homeobox-containing gene.
Nature
354
,
522
525
Hinds
J. W.
,
Hinds
P. L.
(
1974
)
Early ganglion cell differentiation in the mouse retina: An electron microscopic analysis utilizing serial sections.
Dev. Biol
37
,
381
416
Hogan
B. L. M.
,
Horsburgh
G.
,
Cohen
J.
,
Hetherington
C. M.
,
Fisher
G.
,
Lyon
M. F.
(
1986
)
Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse.
J. Embry. Exp. Morph
97
,
95
110
Holt
C. E.
,
Bertsch
T. W.
,
Ellis
H. M.
,
Harris
W. A.
(
1988
)
Cell determination in the Xenopus retina is independent of lineage and birth date.
Neuron
1
,
15
26
Huang
S.
,
Moody
S. A.
(
1993
)
The retinal fate of Xenopus cleavage stage progenitors is dependent upon blastomere position and competence: studies of normal and regulated clones.
J. Neurosci
13
,
3193
3210
Isaka
F.
,
Shimizu
C.
,
Shigetada
N.
,
Kageyama
R.
(
1996
)
Genetic mapping of four mouse bHLH genes related to Drosophila proneural gene atonal.
Genomics
37
,
400
402
Ishibashi
M.
,
Ang
S.-L.
,
Shiota
K.
,
Nakanishi
S.
,
Kageyama
R.
,
Guillemot
F.
(
1995
)
Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-lop-helix factors, premature neurogenesis, and severe neural tube defects.
Genes Dev
9
,
9136
9148
Jan
Y. N.
,
Jan
L. Y.
(
1993
)
HLH proteins, fly neurogenesis, and vertebrate neurogenesis.
Cell
75
,
827
830
Jarman
A. P.
,
Grau
Y.
,
Jan
L. Y.
,
Jan
Y. N.
(
1993
)
atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system.
Cell
73
,
1307
1321
Jarman
A. P.
,
Grell
E. H.
,
Ackerman
L.
,
Jan
L. Y.
,
Jan
Y. N.
(
1994
)
atonal is the proneural gene for Drosophila photoreceptors.
Nature
369
,
398
400
Jarman
A. P.
,
Sun
Y.
,
Jan
L. Y.
,
Jan
Y. N.
(
1995
)
Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors.
Development
121
,
2019
2030
Jasoni
C.
,
Reh
T.
(
1996
)
Temporal and spatial pattern of MASH-1 expression in the developing rat retina demonstrates progenitor cell heterogeneity.
J. Comp. Neurol
369
,
319
327
Johnson
J. E.
,
Birren
S. J.
,
Anderson
D. J.
(
1990
)
Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors.
Nature
346
,
858
861
Kageyama
R.
,
Sasai
Y.
,
Akazawa
C.
,
Makoto
I.
,
Takebayashi
K.
,
Shimizu
C.
,
Tomita
K.
,
Nakanishi
S.
(
1995
)
Regulation of mammalian neural development by helix-loop-helix transcription factors.
Crit. Rev. Neurobiol
9
,
177
188
Kanekar
S.
,
Perron
M.
,
Dorsky
R.
,
Harris
W. A.
,
Jan
L. Y.
,
Jan
Y. N.
,
Vetter
M. L.
(
1997
)
Xath5 participates in a network of bHLH genes in the developing Xenopus retina.
Neuron
19
,
981
994
Koroma
B. M.
,
Yang
J.-M.
,
Sundin
O. H.
(
1997
)
The Pax-6 homeobox gene is expressed throughout the corneal and conjunctival epithelia.
Invest. Ophth. Vis. Sci
38
,
108
120
Kozak
M.
(
1989
)
The Scanning Model for Translation: An Update.
J. Cell Biol
108
,
229
241
Laird
P. W.
,
Zijderveld
A.
,
Linders
K.
,
Rudnicki
M. A.
,
Jaenisch
R.
,
Berns
A.
(
1991
)
Simplified mammalian DNA isolation procedure.
Nucl. Acids Res
19
,
4293
–.
Lalley
P. A.
,
Francke
U.
,
Minna
J. D.
(
1978
)
Homologous genes for enolase, phosphogluconate dehydrogenase, phophoglucomutase, and adenylate kinase are syntenic on mouse chromosome 4 and human chromosome 1p.
Proc. Nat. Acad. Sci.USA
75
,
2382
2386
Lee
J.
(
1997
)
Basic helix-loop-helix genes in neural development.
Curr. Op. Neuro
7
,
13
20
Lee
J. E.
,
Hollenberg
S. M.
,
Snider
L.
,
Turner
D. L.
,
Lipnick
N.
,
Weintraub
H.
(
1995
)
Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein.
Science
268
,
836
844
Loster
J.
,
Immervoll
T.
,
Schmitt-John
T.
,
Graw
J.
(
1997
)
Cat3vl and Catvao cataract mutations on mouse chromosome 10: phenotypic characterization, linkage studies and analysis of candidate genes.
Mol. Gen. Genet
275
,
95
102
Ma
Q.
,
Chen
Z.
,
Barrantes
I.
,
de la Pompa
J. L.
,
Anderson
D. J.
(
1998
)
neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia.
Neuron
20
,
469
482
Ma
Q.
,
Kintner
C.
,
Anderson
D. J.
(
1996
)
Identification of neurogenin, a vertebrate determination gene.
Cell
87
,
43
52
Mastick
G. M.
,
Davis
N. M.
,
Andrews
G. L.
,
Easter
S. S.
(
1997
)
Pax6 functions in boundary formation and axon guidance in the embryonic mouse forebrain.
Development
124
,
1985
1997
Mathers
P. H.
,
Grinbery
A.
,
Mahon
K. A.
,
Jamrich
M.
(
1997
)
The Rx homeobox gene is essential for vertebrate eye development.
Nature
387
,
603
607
Moody
S. A.
(
1987
)
Fates of the blastomeres of the 16-cell stage Xenopus embryo.
Dev. Biol
119
,
560
578
Ohsako
S.
,
Hyer
J.
,
Panganiban
G.
,
Oliver
I.
,
Caudy
M.
(
1994
)
hairy function as a DNA-binding HLH repressor of Drosophila sensory organ formation.
Genes Dev
8
,
2743
2755
Park
C. M.
,
Hollenberg
M. J.
(
1989
)
Basic fibroblast growth factor induces retinal regeneration in vivo.
Dev. Biol
134
,
201
205
Perron
M.
,
Kanekar
S.
,
Vetter
M. L.
,
Harris
W. A.
(
1998
)
The genetic sequence of retinal development in the ciliary margin of the Xenopus eye.
Dev. Biol
199
,
185
200
Pittack
C.
,
Jones
M.
,
Reh
T. A.
(
1991
)
Basic fibroblast growth factor induces retinal pigment epithelium to generate neural retina in vitro.
Development
113
,
577
588
Porter
F. D.
,
Drago
J.
,
Xu
Y.
,
Cheema
S. S.
,
Wassif
C.
,
Huang
S. P.
,
Lee
E.
,
Grinberg
A.
,
Massalas
J. S.
,
Bodine
D.
,
Alt
F.
,
Westphal
H.
(
1997
)
Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development.
Development
124
,
2935
2944
Reddy
G. V.
,
Gupta
B.
,
Ray
K.
,
Rodrigues
V.
(
1997
)
Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage.
Development
124
,
703
712
Richter
K.
,
Grunz
H.
,
Dawid
I. B.
(
1988
)
Gene expression in the embryonic nervous system of Xenopus laevis.
Proc. Nat. Acad. Sci.USA
85
,
8086
8090
Roztocil
T.
,
Matter-Sadzinski
L.
,
Alliod
C.
,
Ballivet
M.
,
Matter
J.-M.
(
1997
)
NeuroM, a neural helix-loop-helix transcription factor, defines a new transition state in neurogenesis.
Development
124
,
3263
3272
Rupp
R. A. W.
,
Snider
L.
,
Weintraub
H.
(
1994
)
Xenopus embryos regulate the nuclear localization of XMyoD.
Genes Dev
8
,
1311
1323
Sakaguchi
D. S.
,
Moeller
J. F.
,
Coffman
C. R.
,
Gallenson
N.
,
Harris
W. A.
(
1989
)
Growth cone interactions with a glial cell line from embryonic Xenopus retina.
Dev. Biol
134
,
158
174
Sasai
Y.
,
Kageyama
R.
,
Tagawa
Y.
,
Shigemoto
R.
,
Nakanishi
S.
(
1992
)
Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split.
Genes Dev
6
,
2620
2634
Satakato
I.
,
Maas
R.
(
1994
)
Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development.
Nat. Genet
6
,
348
356
Schaeren-Weimers
N.
,
Gerfin-Moser
A.
(
1993
)
A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes.
Histochemistry
100
,
431
440
Schedl
A.
,
Ross
A.
,
Lee
M.
,
Engelkamp
D.
,
Rashbass
P.
,
van Heynigen
V.
,
Hastie
N. D.
(
1996
)
Influence of PAX gene dosage on development: overexpression causes severe eye abnormalities.
Cell
86
,
71
82
Shimizu
C.
,
Akazawa
C.
,
Nakanishi
N.
,
Kageyama
R.
(
1995
)
Math-2, a mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal, is specifically expressed in the nervous system.
Eur. J. Biol
229
,
239
248
Sommer
L.
,
Ma
Q.
,
Anderson
D. J.
(
1996
)
neurogenins, a novel family of atonal -related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS.
Mol. Cell. Neuro
8
,
221
241
Takebayashi
K.
,
Takahashi
S.
,
Yokota
C.
,
Tsuda
H.
,
Nakanishi
S.
,
Asashima
M.
,
Kageyama
R.
(
1997
)
Conversion of ectoderm into a neural fate by ATH-3, a vertebrate basic helix-loop-helix gene homologous to Drosophila proneural gene atonal.
EMBO J
16
,
384
395
Theiler
K.
,
Varnum
D. S.
,
Stevens
L. C.
(
1978
)
Development of Dickie's small eye, a mutation in the house mouse.
Anat. Embryol
155
,
81
86
Tomita
K.
,
Ishibashi
M.
,
Nakahara
K.
,
Ang
S.-L.
,
Nakanishi
S.
,
Guillemot
F.
,
Kageyama
R.
(
1996
)
Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis.
Neuron
16
,
723
734
Ton
C. C.
,
Hirvonen
H.
,
Miwa
H.
,
Weil
M. M.
,
Monaghan
P.
,
Jordan
T.
,
van Heyningen
V.
,
Hastie
N. D.
,
Meijers-Heijboer
H.
,
Dreschler
M.
, et al. 
(
1991
)
Positional cloning and characterization of a paired box-and homeobox-containing gene from the Aniridia region.
Cell
67
,
1059
1074
Turner
D. L.
,
Snyder
E. Y.
,
Cepko
C. L.
(
1987
)
A common progenitor for neurons and glia persists in rat retina late in development.
Neuron
4
,
833
845
Turner
D. L.
,
Weintraub
H.
(
1994
)
Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate.
Genes Dev
8
,
1434
1447
Van Doren
M.
,
Bailey
A. M.
,
Esnayra
J.
,
Ede
K.
,
Posakony
J. W.
(
1994
)
Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete.
Genes Dev
8
,
2729
2742
Van Doren
M.
,
Ellis
H.
,
Posakony
J. W.
(
1991
)
The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes.
Development
113
,
245
255
Walther
C.
,
Gruss
P.
(
1991
)
Pax-6 a murine paired box gene, is expressed in the developing CNS.
Development
113
,
1435
1449
Wantanabe
T.
,
Raff
M. C.
(
1990
)
Rod photoreceptor development in vitro: Intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina.
Neuron
2
,
461
467
Wetts
R.
,
Fraser
S. E.
(
1988
)
Multipotent precursors can give rise to all major cell types of the frog retina.
Science
239
,
1142
1145
Wetts
R.
,
Kook
J. H.
,
Fraser
S. E.
(
1993
)
Proportion of proliferative cells in the tadpole retina is increased after embryonic lesion.
Dev. Dynam
198
,
54
64
Williams
R. W.
,
Goldowitz
D.
(
1992
)
Lineage versus environment in embryonic retina: a revisionist perspective.
Trends. Genet
15
,
368
373
Wrischnik
L. A.
,
Kenyon
C. J.
(
1997
)
The role of lin22, a hairy/Enhancer of split homolog, in patterning the peripheral nervous system of C. elegans.
Development
124
,
2875
2888
Xu
P.-X.
,
Woo
I.
,
Her
H.
,
Beier
D. R.
,
Maas
R. L.
(
1997
)
Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode.
Development
124
,
219
231
Young
R. W.
(
1983
)
The life history of retinal cells.
Trans. Am. Ophthalmol. Soc
81
,
193
228
Young
R. W.
(
1985
)
Cell proliferation during postnatal development of the retina in the mouse.
Brain Research
353
,
229
239
Zhang
Y.
,
Emmons
S. W.
(
1995
)
Specification of sense-organ identity by a Caenorhabditis elegans Pax-6 homologue.
Nature
377
,
55
59
Zhao
C.
,
Emmons
S. W.
(
1995
)
A transcription factor controlling development of peripheral sense organs in C. elegans.
Nature
373
,
74
78
This content is only available via PDF.