Vertebrate neural cell-fate determination: Lessons from the retina (original) (raw)
Cepko, C. L., Austin, C. P., Yang, X., Alexiades, M. & Ezzeddine, D. Cell fate determination in the vertebrate retina. Proc. Natl Acad. Sci. USA93, 589– 595 (1996).The first proposal of the competence model for retinal development. ArticleCASPubMedPubMed Central Google Scholar
Edlund, T. & Jessell, T. M. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system . Cell96, 211–224 (1999). ArticleCASPubMed Google Scholar
Harris, W. A. Cellular diversification in the vertebrate retina. Curr. Opin. Genet. Dev.7, 651–658 ( 1997). ArticleCASPubMed Google Scholar
LaVail, M. M., Rapaport, D. H. & Rakic, P. Cytogenesis in the monkey retina. J. Comp. Anat.309, 86–114 ( 1991). CAS Google Scholar
Stiemke, M. M. & Hollyfield, J. G. Cell birthdays in Xenopus laevis retina. Differentiation58, 189 –193 (1995). ArticleCASPubMed Google Scholar
Young, R. W. Cell differentiation in the retina of the mouse. Anat. Rec.212, 199–205 (1985). ArticleCASPubMed Google Scholar
Carter-Dawson, L. D. & LaVail, M. M. Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol.188, 263–272 (1979).References4–7are classic studies that describe the birthdates of the main classes of retinal cells in several species. ArticleCASPubMed Google Scholar
Turner, D. L., Snyder, E. Y. & Cepko, C. L. Lineage-independent determination of cell type in the embryonic mouse retina. Neuron4, 833 –845 (1990).References8–11describe the multipotency of retinal progenitors. ArticleCASPubMed Google Scholar
Turner, D. L. & Cepko, C. L. A common progenitor for neurons and glia persists in rat retina late in development. Nature328, 131–136 (1987). ArticleCASPubMed Google Scholar
Holt, C. E., Bertsch, T. W., Ellis, H. M. & Harris, W. A. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron1, 15– 26 (1988). ArticleCASPubMed Google Scholar
Wetts, R. & Fraser, S. E. Multipotent precursors can give rise to all major cell types of the frog retina. Science239, 1142–1145 (1988). ArticleCASPubMed Google Scholar
Hu, M. & Easter, S. S. Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev. Biol.207, 309–321 (1999). Describes a hitherto unrecognized order in the genesis of some cell types in a vertebrate retina. ArticleCASPubMed Google Scholar
Austin, C. P., Feldman, D. E., Ida, J. A. & Cepko, C. L. Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development121, 3637–3650 (1995). ArticleCASPubMed Google Scholar
Belliveau, M. J. & Cepko, C. L. Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development126, 555– 556 (1999).Shows a number of key features of retinal cell-fate determination, including limitations in the competence of retinal progenitors at different times and the ability of extrinsic signals to alter the relative proportions of cell types generated within a given competence state. ArticleCASPubMed Google Scholar
Belliveau, M. J., Young, T. L. & Cepko, C. L. Late retinal progenitor cells show intrinsic limitations in the production of cell types and the kinetics of opsin synthesis. J. Neurosci.20, 2247–2254 (2000). ArticleCASPubMedPubMed Central Google Scholar
McConnell, S. K. Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J. Neurosci.8, 945– 974 (1988). ArticleCASPubMedPubMed Central Google Scholar
Briscoe, J. et al. Homeobox gene Nkx2.2 and specification of neuronal identity by graded sonic hedgehog signalling. Nature398, 622–627 (1999). ArticleCASPubMed Google Scholar
Ericson, J., Morton, S., Kawakami, A., Roelink, H. & Jessell, T. M. Two critical periods of sonic hedgehog signaling required for the specification of motor neuron identity. Cell87, 661–673 (1996). ArticleCASPubMed Google Scholar
Desai, A. R. & McConnell, S. K. Progressive restriction in fate potential by neural progenitors during cerebral cortical development . Development127, 2863– 2872 (2000). ArticleCASPubMed Google Scholar
Selleck, M. A. & Bronner-Fraser, M. The genesis of avian neural crest cells: a classic embryonic induction. Proc. Natl Acad. Sci. USA93, 9352–9357 (1996). ArticleCASPubMedPubMed Central Google Scholar
Freeman, M. Cell determination strategies in the Drosophila eye. Development124, 261–270 ( 1997). ArticleCASPubMed Google Scholar
Alexiades, M. R. & Cepko, C. L. Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny. Development124, 1119– 1131 (1997).Shows heterogeneity in retinal progenitors and an intrinsic bias in one subset of progenitors to produce distinct cell types. ArticleCASPubMed Google Scholar
Lillien, L. & Cepko, C. Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF-α. Development115, 253–266 ( 1992). ArticleCASPubMed Google Scholar
Lillien, L. Changes in retinal cell fate induced by overexpression of EGF receptor. Nature377, 158–162 ( 1995). ArticleCASPubMed Google Scholar
Dyer, M. A. & Cepko, C. L. Control of Muller glial cell proliferation and activation following retinal injury. Nature Neurosci.3, 873–880 (2000). ArticleCASPubMed Google Scholar
Dyer, M. A. & Cepko, C. L. p57Kip2 regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development127, 3593– 3605 (2000). ArticleCASPubMed Google Scholar
Ohnuma, S., Philpott, A., Wang, K., Holt, C. E. & Harris, W. A. p27Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. Cell99, 499–510 ( 1999). ArticleCASPubMed Google Scholar
Livesey, F. J., Furukawa, T., Steffen, M. A., Church, G. M. & Cepko, C. L. Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr. Biol.10, 301–310 (2000). ArticleCASPubMed Google Scholar
Alexiades, M. R. & Cepko, C. L. Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev. Dyn.205, 293– 307 (1996).Comprehensive study of the kinetics of progenitor proliferation and cell numbers in the developing mammalian retina. ArticleCASPubMed Google Scholar
Chenn, A. & McConnell, S. K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis . Cell82, 631–641 (1995).Classic study that describes the occurrence of asymmetric progenitor divisions in the mammalian nervous system. ArticleCASPubMed Google Scholar
Mione, M. C., Cavanagh, J. F. R., Harris, B. & Parnavelas, J. G. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J. Neurosci.17, 2018– 2029 (1997). ArticleCASPubMedPubMed Central Google Scholar
Zhong, W., Feder, J. N., Jiang, M. M., Jan, L. Y. & Jan, Y. N. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron17, 43–53 (1996). ArticleCASPubMed Google Scholar
Young, R. W. Cell death during differentiation of the retina in the mouse. J. Comp. Neurol.229, 362–373 (1984). ArticleCASPubMed Google Scholar
Voyvodic, J. T., Burne, J. F. & Raff, M. C. Quantification of normal cell death in the rat retina: Implications for clone composition in cell lineage analysis. Eur. J. Neurosci.7, 2469–2478 (1995). ArticleCASPubMed Google Scholar
Jensen, A. M. & Raff, M. C. Continuous observation of multipotential retinal progenitor cells in clonal density culture. Dev. Biol.188, 267–279 ( 1997). ArticleCASPubMed Google Scholar
Reh, T. A. & Tully, T. Regulation of tyrosine hydroxylase-containing amacrine cell number in larval frog retina. Dev. Biol.114, 463–469 (1986). First report of the possible role of feedback control of progenitor decision-making by postmitotic cells. ArticleCASPubMed Google Scholar
Waid, D. K. & McLoon, S. C. Ganglion cells influence the fate of dividing retinal cells in culture. Development125 , 1059–1066 (1998). Clearly shows feedback inhibition of ganglion cell genesis by postmitotic ganglion cells, and also shows that this action is distinct from the Delta-Notch signalling pathway. ArticleCASPubMed Google Scholar
Jasoni, C. L. & Reh, T. A. Temporal and spatial pattern of MASH-1 expression in the developing rat retina demonstrates progenitor cell heterogeneity. J. Comp. Neurol.369, 319–327 (1996). ArticleCASPubMed Google Scholar
Brown, N. L. et al. Math5 encodes a murine basic helix-loop-helix transcription factor expressed during early stages of retinal neurogenesis. Development125, 4821–4833 (1998). ArticleCASPubMed Google Scholar
Levine, E. M., Close, J., Fero, M., Ostrovsky, A. & Reh, T. A. p27Kip1 regulates cell cycle withdrawal of late multipotent progenitor cells in the mammalian retina. Dev. Biol.219, 299–314 (2000). CASPubMed Google Scholar
Ezzeddine, Z. D., Yang, X., DeChiara, T., Yancopoulos, G. & Cepko, C. L. Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina. Development124, 1055–1067 ( 1997). ArticleCASPubMed Google Scholar
Altshuler, D., Lo Turco, J. J., Rush, J. & Cepko, C. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development119, 1317– 1328 (1993). ArticleCASPubMed Google Scholar
Levine, E. M., Fuhrmann, S. & Reh, T. A. Soluble factors and the development of rod photoreceptors . Cell. Mol. Life Sci.57, 224– 234 (2000). ArticleCASPubMed Google Scholar
Artavanis-Tsakonas, S., Rand, M. D. & Lake, R. J. Notch signaling: cell fate control and signal integration in development. Science284, 770– 776 (1999). ArticleCASPubMed Google Scholar
Dorsky, R. I., Chang, W. S., Rapaport, D. H. & Harris, W. A. Regulation of neuronal diversity in the Xenopus retina by Delta signalling . Nature385, 67–70 (1997). ArticleCASPubMed Google Scholar
Bao, Z. Z. & Cepko, C. L. The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci.17, 1425–1434 (1997). ArticleCASPubMedPubMed Central Google Scholar
Furukawa, T., Mukherjee, S., Bao, Z. Z., Morrow, E. M. & Cepko, C. L. rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron26, 383–394 ( 2000). ArticleCASPubMed Google Scholar
Gaiano, N., Nye, J. S. & Fishell, G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron26, 395– 404 (2000). ArticleCASPubMed Google Scholar
Morrison, S. J. et al. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell101, 499–510 ( 2000). ArticleCASPubMed Google Scholar
Deftos, M. L. & Bevan, M. J. Notch signaling in T cell development . Curr. Opin. Immunol.12, 166– 172 (2000). ArticleCASPubMed Google Scholar
Baonza, A. & Garcia-Bellido, A. Notch signaling directly controls cell proliferation in the Drosophila wing disc. Proc. Natl Acad. Sci. USA97, 2609– 2614 (2000). ArticleCASPubMedPubMed Central Google Scholar
Mathers, P. H., Grinberg, A., Mahon, K. A. & Jamrich, M. The Rx homeobox gene is essential for vertebrate eye development. Nature387, 603–607 ( 1997). ArticleCASPubMed Google Scholar
Hogan, B. L. M., Hirst, E. M. A., Horsburgh, G. & Hetherington, C. M. Small eye(Sey): a mouse model for the genetic analysis of craniofacial abnormalities . Development103, 115– 119 (1988). ArticlePubMed Google Scholar
Hill, R. E. et al. Mouse small eye results from mutaions in a paired-like homeobox-containing gene. Nature354, 522–525 (1991). ArticleCASPubMed Google Scholar
Belecky-Adams, T. et al. Pax-6, Prox1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest. Ophthalmol. Vis. Sci.38, 1293– 1303 (1997). CASPubMed Google Scholar
Chen, C. M. & Cepko, C. L. Expression of Chx10 and Chx10-1 in the developing chicken retina. Mech. Dev.90, 293–297 (2000). ArticleCASPubMed Google Scholar
Liu, I. S. et al. Developmental expression of a novel murine homeobox gene ( Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron13, 377– 393 (1994). ArticleCASPubMed Google Scholar
Burmeister, M. et al. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation . Nature Genetics12, 376– 384 (1996).Shows dual functions for the transcription factor Chx10 in retinal development: a role in proliferation of progenitors and a second role in differentiation of bipolar cells. ArticleCASPubMed Google Scholar
Bennett, G. S., Hollander, B. A. & Laskowska, D. Expression and phosphorylation of the mid-sized neurofilament protein NF-M during chick spinal cord neurogenesis. J. Neurosci. Res.21, 376–390 ( 1988). ArticleCASPubMed Google Scholar
Bennett, G. S. & DiLullo, C. Expression of a neurofilament protein by the precursors of a subpopulation of ventral spinal cord neurons. Dev. Biol.107, 94– 106 (1985). ArticleCASPubMed Google Scholar
Tapscott, S. J., Bennett, G. S. & Holtzer, H. Neuronal precursor cells in the chick neural tube express neurofilament proteins. Nature292, 836– 838 (1981). ArticleCASPubMed Google Scholar
Orkin, S. Diversification of haematopoietic stem cells to specific lineages. Nature Rev. Genet.1, 57–64 (2000). ArticleCASPubMed Google Scholar
Xiang, M. et al. The Brn-3 family of POU-domain factors: Primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J. Neurosci.15, 4762– 4785 (1995). ArticleCASPubMedPubMed Central Google Scholar
Erkman, L. et al. Role of transcription factors Brn-3.1 and Brn-3.2 in auditory and visual system development. Nature381, 603–606 (1996). ArticleCASPubMed Google Scholar
Furukawa, T., Morrow, E. M. & Cepko, C. L. Crx, a novel _otx_-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation . Cell91, 531–541 (1997). ArticleCASPubMed Google Scholar
Freund, C. L. et al. Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor . Cell91, 543–553 (1997). ArticleCASPubMed Google Scholar
Chen, S. et al. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron19, 1017–1030 (1997). ArticleCASPubMed Google Scholar
Gan, L., Wang, S. W., Huang, Z. & Klein, W. H. POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev. Biol.210, 469–480 (1999). ArticleCASPubMed Google Scholar
Gan, L. et al. POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proc. Natl Acad. Sci. USA93, 3920–3925 (1996). ArticleCASPubMedPubMed Central Google Scholar
Waid, D. K. & McLoon, S. C. Immediate differentiation of ganglion cells following mitosis in the developing retina. Neuron14, 117–124 (1995). This striking study shows that differentiation of ganglion cells can occur within ∼15 minutes of the exit from M phase. This supports the proposal that there is transcription of genes required in the postmitotic cells before M phase in the progenitor. ArticleCASPubMed Google Scholar
Flores, G. V. et al. Combinatorial signaling in the specification of unique cell fates. Cell103, 75–85 (2000). ArticleCASPubMed Google Scholar
Xu, C., Kauffmann, R. C., Zhang, J., Kladny, S. & Carthew, R. W. Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell103, 87– 97 (2000). ArticleCASPubMed Google Scholar
Halfon, M. S. et al. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell103, 63–74 ( 2000). ArticleCASPubMed Google Scholar
Qian, X. et al. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron28, 69–80 ( 2000). ArticleCASPubMed Google Scholar
Leber, S., Breedlove, S. & Sanes, J. Lineage, arrangement, and death of clonally related motoneurons in the chick spinal cord. J. Neurosci.10, 2451–2462 (1990). ArticleCASPubMedPubMed Central Google Scholar
McConnell, S. K. & Kaznowski, C. E. Cell cycle dependence of laminar determination in developing neocortex. Science254, 282–285 ( 1991). ArticleCASPubMed Google Scholar
Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. & Jessell, T. M. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell84, 309–320 (1996). ArticleCASPubMed Google Scholar
Briscoe, J., Pierani, A., Jessell, T. M. & Ericson, J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell101, 435–445 (2000). ArticleCASPubMed Google Scholar
Freeman, M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell87, 651 –660 (1996). ArticleCASPubMed Google Scholar
Ikuta, K. et al. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell62, 863–874 (1990). ArticleCASPubMed Google Scholar
Weinmaster, G., Roberts, V. & Lemke, G. A homolog of Drosophila Notch expressed during mammalian development. Development113, 199–205 (1991). ArticleCASPubMed Google Scholar
Tomita, K. et al. Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis . Neuron16, 723–734 (1996). ArticleCASPubMed Google Scholar
Hitchcock, P. F., Macdonald, R. E., VanDeRyt, J. T. & Wilson, S. W. Antibodies against Pax6 Immunostain amacrine and ganglion cells and neuronal progenitors, but not rod precursors, in the normal and regenerating retina of the gold fish. J. Neurobiol.29, 399– 413 (1996). ArticleCASPubMed Google Scholar
Tomarev, S. I. et al. Chicken homeobox gene Prox1 related to Drosophila prospero is expressed in the developing lens and retina. Dev. Dyn.206, 354–367 ( 1996); erratum 207, 120 ( 1996). PubMed ArticleCASPubMed Google Scholar
Masland, R. H. & Raviola, E. Confronting complexity: strategies for understanding the microcircuitry of the retina. Annu. Rev. Neurosci.23, 249–284 (2000). ArticleCASPubMed Google Scholar
MacNeil, M. A. & Masland, R. H. Extreme diversity among amacrine cells: implications for function. Neuron20, 971–982 (1998). ArticleCASPubMed Google Scholar
Ellis, H. M., Spann, D. R. & Posakony, J. W. Extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell61, 27–38 (1990). ArticleCASPubMed Google Scholar
Bang, A. G., Bailey, A. M. & Posakony, J. W. Hairless promotes stable commitment to the sensory organ precursor cell fate by negatively regulating the activity of the Notch signaling pathway. Dev. Biol.172, 479– 494 (1995). ArticleCASPubMed Google Scholar
Leviten, M. W. & Posakony, J. W. Gain-of-function alleles of Bearded interfere with alternative cell fate decisions in Drosophila adult sensory organ development. Dev. Biol.176 , 264–283 (1996). ArticleCASPubMed Google Scholar
Takahashi, T., Nowakowski, R. S. & Caviness, V. S. Jr The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis . J. Neurosci.16, 6183– 6196 (1996). ArticleCASPubMedPubMed Central Google Scholar
Lu, B., Jan, L. & Jan, Y. N. Control of cell divisions in the nervous system: symmetry and asymmetry. Annu. Rev. Neurosci.23, 531–556 (2000). ArticleCASPubMed Google Scholar
Coffman, C., Harris, W. & Kinter, C. Xotch, the Xenopus homolog of Drosophila Notch. Science249, 1438– 1441 (1990). ArticleCASPubMed Google Scholar
Henrique, D. et al. Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol.7, 661–670 (1997). ArticleCASPubMed Google Scholar
Toy, J. & Sundin, O. H. Expression of the optx2 homeobox gene during mouse development. Mech. Dev.83, 183–186 (1999). ArticleCASPubMed Google Scholar
Toy, J., Yang, J. M., Leppert, G. S. & Sundin, O. H. The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc. Natl Acad. Sci. USA95, 10643–10648 ( 1998). ArticleCASPubMedPubMed Central Google Scholar
Morrow, E. M., Furukawa, T., Lee, J. E. & Cepko, C. L. NeuroD regulates cell fate determination in the developing neural retina. Development126, 23–36 ( 1999). ArticleCASPubMed Google Scholar
Acharya, H. R., Dooley, C. M., Thoreson, W. B. & Ahmad, I. cDNA cloning and expression analysis of NeuroD mRNA in human retina. Biochem. Biophys. Res. Commun.233, 459– 463 (1997). ArticleCASPubMed Google Scholar
Yan, R. -T. & Wang, S. -Z. NeuroD induces photoreceptor cell overproduction in vivo and de novo generation in vitro. J. Neurobiol.36, 485–496 (1998). ArticleCASPubMedPubMed Central Google Scholar
Matter, J. M., Matter-Sadzinski, L. & Ballivet, M. Activity of the β3 nicotinic receptor promoter is a marker of neuron fate determination during retina development. J. Neurosci.15, 5919–5928 (1995). ArticleCASPubMedPubMed Central Google Scholar