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Muller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development
C. Neophytou, A.B. Vernallis, A. Smith, M.C. Raff
Development 1997 124: 2345-2354;

Summary

In the present study, we examine rod photoreceptor development in dissociated-cell cultures of neonatal mouse retina. We show that, although very few rhodopsin+ rods develop in the presence of 10% foetal calf serum (FCS), large numbers develop in the absence of serum, but only if the cell density in the cultures is high. The rods all develop from nondividing rhodopsin- cells, and new rods continue to develop from rhodopsin- cells for at least 6–8 days, indicating that there can be a long delay between when a precursor cell withdraws from the cell cycle and when it becomes a rhodopsin+ rod. We show that FCS arrests rod development in these cultures at a postmitotic, rhodopsin-, pre-rod stage. We present evidence that FCS acts indirectly by stimulating the proliferation of Muller cells, which arrest rod differentiation by releasing leukaemia inhibitory factor (LIF). These findings identify an inhibitory cell-cell interaction, which may help to explain the long delay that can occur both in vitro and in vivo between cell-cycle withdrawal and rhodopsin expression during rod development.

REFERENCES

    1. Adamus G.,
    2. Zam Z. S.,
    3. Arendt A.,
    4. Palczewski K.,
    5. McDowell J. H.,
    6. Hargrave P. A.
    (1991) Anti-rhodopsin monoclonal antibodies of defined specificity: characterisation and application. Vis. Res 31, 17–31
    OpenUrlCrossRefPubMedWeb of Science
    1. Altshuler D.,
    2. Cepko C.
    (1992) A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. Development 114, 947–957
    OpenUrlAbstract
    1. Altshuler D.,
    2. Turco L. J. J.,
    3. Rush J.,
    4. Cepko C.
    (1993) Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119, 1317–1328
    OpenUrlAbstract
    1. Anchan R. M.,
    2. Reh T. A.,
    3. Angello J.,
    4. Balliet A.,
    5. Walker M.
    (1991) EGF and TGF-stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6, 923–936
    OpenUrlCrossRefPubMedWeb of Science
    1. Austin C. P.,
    2. Feldman D. E.,
    3. Ida J. A.,
    4. Cepko C. L.
    (1995) Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637–3650
    OpenUrlAbstract
    1. Barnstable C. J.
    (1980) Monoclonal antibodies which recognise different cell types in the rat retina. Nature 286, 231–235
    OpenUrlCrossRefPubMed
    1. Barnstable,
    2. Drager
    (1984) Thy-1 antigen: a ganglion cell specific marker in rodent retina. Neurosci 11, 847–855
    OpenUrlCrossRefPubMedWeb of Science
    1. Barnstable C. J.,
    2. Hofstein R.,
    3. Akagawa K.
    (1985) A marker for early amacrine cell development in rat retina. Dev. Brain Res 20, 286–290
    OpenUrlCrossRef
    1. Cepko C. L.
    (1996) The patterning and onset of opsin expression in vertebrate retinae. Curr. Op. Neurobiol 6, 542–546
    OpenUrlCrossRefPubMedWeb of Science
    1. Cepko C. L.,
    2. Austin C. P.,
    3. Yang X.,
    4. Alexiades M.,
    5. Ezzeddine D.
    (1996) Cell fate determination in the vertebrate retina. Proc. Nat. Acad. Sci. USA 93, 589–595
    OpenUrlAbstract/FREE Full Text
    1. De Leeuw A. M.,
    2. Gaur V. P.,
    3. Saari J. C.,
    4. Milam A. H.
    (1990) Immunolocalisation of cellular retinol-, retinaldehyde-and retinoic acid-binding proteins in rat retina during pre-and postnatal development. J. Neurocyt 19, 253–264
    OpenUrlCrossRefPubMedWeb of Science
    1. Dizhoor A.,
    2. Stryer L.
    (1991) Recoverin: A calcium sensitive activator of retinal rod guanylate cyclase. Science 251, 915–918
    OpenUrlAbstract/FREE Full Text
    1. Dorsky R.,
    2. Chang W.,
    3. Rapaport D.,
    4. Harris W.
    (1997) Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature 385, 67–70
    OpenUrlCrossRefPubMed
    1. Dorsky R.,
    2. Rapaport D.,
    3. Harris W.
    (1995) Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14, 487–496
    OpenUrlCrossRefPubMedWeb of Science
    1. Drager U. C.,
    2. Olsen J. F.
    (1981) Ganglion cell distribution in the retina of the mouse. Invest. Ophthalmol. Vis. Sci 20, 285–293
    OpenUrlAbstract/FREE Full Text
    1. Ezzeddine D. Z.,
    2. Yang X.,
    3. DeChiara T.,
    4. Yancopoulos G.,
    5. Cepko C. L.
    (1997) Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina. Development 124, 1055–1067
    OpenUrlAbstract
    1. Fekete M. D.,
    2. Barnstable C. J.
    (1983) The subcellular localisation of rat photoreceptor-specific antigens. J. Neurocyt 12, 785–803
    OpenUrlCrossRefPubMedWeb of Science
    1. Fuhrmann S.,
    2. Kirsch M.,
    3. Hofmann H.-D.
    (1995) Ciliary neurotrophic factor promotes chick photoreceptor development in vitro. Development 121, 2695–2706
    OpenUrlAbstract
    1. Guillemot F.,
    2. Cepko C. L.
    (1992) Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an vitro assay of early retinal development. Development 114, 743–754
    OpenUrlAbstract
    1. Harris W. A.,
    2. Hartenstein V.
    (1991) Neuronal determination without cell division in Xenopus embryos. Neuron 6, 499–515
    OpenUrlCrossRefPubMedWeb of Science
    1. Harris W. A.,
    2. Messersmith S. L.
    (1992) Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron 9, 357–372
    OpenUrlCrossRefPubMedWeb of Science
    1. Hicks D.,
    2. Courtois Y.
    (1992) Fibroblast growth factor stimulates photoreceptor differentiation in vitro. J. Neurosci 12, 2022–2033
    OpenUrlAbstract
    1. Holt C. E.,
    2. Bertsch T. W.,
    3. Ellis H. M.,
    4. Harris W. A.
    (1988) Cellular determination in the xenopus retina is independent of lineage and birth date. Neuron 1, 15–26
    OpenUrlCrossRefPubMedWeb of Science
    1. Hudson K.,
    2. Vernallis A.,
    3. Heath J.
    (1996) Characterisation of the receptor binding sites of human leukemia inhibitory factor and creation of antagonists. J. Biol. Chem 271, 11971–11978
    OpenUrlAbstract/FREE Full Text
    1. Hunter D.,
    2. Murphy M.,
    3. Olsson C.,
    4. Brunken W.
    (1992) S-laminin expression in adult and developing retinae: a potential cue for photoreceptor morphogenesis. Neuron 8, 399–413
    OpenUrlCrossRefPubMedWeb of Science
    1. Ip N.,
    2. McClain J.,
    3. Barrezueta N.,
    4. Aldrich T.,
    5. Pan L.,
    6. Yanping L.,
    7. Wiegand S.,
    8. Friedman B.,
    9. Davis S.,
    10. Yancopoulos G.
    (1993) The a component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron 10, 89–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Ip N.,
    2. Yancopoulos G.
    (1996) The neurotrophins and CNTF: two families of colloborative neurotrophic factors. Annu. Rev. Neurosci 19, 491–515
    OpenUrlCrossRefPubMedWeb of Science
    1. Kelley M. W.,
    2. Turner J. K.,
    3. Reh T. A.
    (1994) Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120, 2091–2102
    OpenUrlAbstract
    1. Kelley M. W.,
    2. Turner J. K.,
    3. Reh T. A.
    (1995) Ligands of steroid/thyroid receptors induce cone photoreceptors in vertebrate retina. Development 121, 3777–3785
    OpenUrlAbstract
    1. Kirsch M.,
    2. Fuhrmann S.,
    3. Wiese A.,
    4. Hofmann H.
    (1996) CNTF exerts opposite effects on in vitro development of rat and chick photoreceptors. Neuroreport 7, 697–700
    OpenUrlPubMedWeb of Science
    1. Knight J.,
    2. Raymond P.
    (1990) Time course of opsin expression in developing rod photoreceptors. Development 110, 1115–1120
    OpenUrlAbstract/FREE Full Text
    1. La Vail M. M.,
    2. Rapaport D. H.,
    3. Rakic P.
    (1991) Cytogenesis in the monkey retina. J. Comp. Neurol 309, 86–114
    OpenUrlCrossRefPubMedWeb of Science
    1. Li M.,
    2. Sendtner M.,
    3. Smith A.
    (1995) Essential function of LIF receptor in motor neurons. Nature 378, 724–727
    OpenUrlCrossRefPubMed
    1. Lillien L.
    (1995) Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 377, 158–162
    OpenUrlCrossRefPubMed
    1. Lillien L.,
    2. Cepko C.
    (1992) Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF. Development 115, 253–266
    OpenUrlAbstract
    1. Magaud J. P.,
    2. Sargent I.,
    3. Clarke P. J.,
    4. Ffrench M.,
    5. Rimokh R.,
    6. Mason D. Y.
    (1989) Double immunocytochemical labeling of cell and tissue samples with monoclonal anti-bromodeoxyuridine. J. Histochem. Cytochem 37, 1517–1527
    OpenUrlAbstract/FREE Full Text
    1. McGinnis F. J.,
    2. Whelan P. J.,
    3. Donoso A. L.
    (1992) Transient cyclic changes in mouse visual cell gene products during light-dark cycle. Journal of Neuroscience Research 31, 584–590
    OpenUrlCrossRefPubMedWeb of Science
    1. Nichols J.,
    2. Evans E.,
    3. Smith A.
    (1990) Establishment of germ line competent embryonic stem (ES) cells using differentiation inhibiting activity. Development 110, 1341–1348
    OpenUrlAbstract/FREE Full Text
    1. Onoda N.,
    2. Fujita S. C.
    (1987) A monoclonal antibody specific for a subpopulation of retinal bipolar cells in the frog and other vertebrates. Brain Res 416, 359–363
    OpenUrlCrossRefPubMedWeb of Science
    1. Rabie A.,
    2. Thomasset M.,
    3. Parkes C. O.,
    4. Clavel M. C.
    (1985) Immunocytochemical detection of 28 000-MW calcium-binding protein in horizontal cells of the rat retina. Cell Tissue Res 240, 493–496
    OpenUrlPubMed
    1. Reh T.
    (1992) Cellular interactions determine neuronal phenotypes in rodent retinal cultures. J. Neurobiol 23, 1067–1083
    OpenUrlCrossRefPubMedWeb of Science
    1. Richards L.,
    2. Kilpatrick T.,
    3. Dutton R.,
    4. Tan S.,
    5. Gearing D.,
    6. Bartlett P.
    (1996) Leukaemia inhibitory factor or related factors promote the differentiation of neuronal and astrocytic precursors within the developing murine spinal cord. Eur. J. Neurosci 8, 291–299
    OpenUrlCrossRefPubMedWeb of Science
    1. Sparrow J. R.,
    2. Hicks D.,
    3. Barnstable C. J.
    (1990) Cell commitment and differentiation in explants of embryonic rat neural retina. Comparison with the developmental potential. Dev. Brain Res 51, 69–84
    OpenUrlCrossRefPubMedWeb of Science
    1. Stockli K.,
    2. Lottspeich F.,
    3. Sendtner M.,
    4. Masiakowski P.,
    5. Carroll P.,
    6. Gotz R.,
    7. Lindholm D.,
    8. Thoenen H.
    (1989) Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342, 920–923
    OpenUrlCrossRefPubMedWeb of Science
    1. Stockli K. A.,
    2. Lillien L. E.,
    3. Naher-Noe M.,
    4. Breitfeld G.,
    5. Hughes R. A.,
    6. Raff M. C.,
    7. Thoenen H.,
    8. Sendtner M.
    (1991) Regional distribution, developmental changes and cellular localisation of CNTF-mRNA and protein in the rat brain. J. Cell Biol 115, 447–459
    OpenUrlAbstract/FREE Full Text
    1. Tomita K.,
    2. Ishibashi M.,
    3. Nakahara K.,
    4. Ang S.-L.,
    5. Nakanishi S.,
    6. Guillemot F.,
    7. 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
    OpenUrlCrossRefPubMedWeb of Science
    1. Turner D.,
    2. Cepko C.
    (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131–136
    OpenUrlCrossRefPubMedWeb of Science
    1. Turner D.,
    2. Synder E.,
    3. Cepko C.
    (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833–845
    OpenUrlCrossRefPubMedWeb of Science
    1. Ware C.,
    2. Horowitz M.,
    3. Renshaw B.,
    4. Hunt J.,
    5. Liggitt D.,
    6. Koblar S.,
    7. Gliniak B.,
    8. McKenna H.,
    9. Papayannopoullou T.,
    10. Thoma B.,
    11. Cheng L.,
    12. Donovan P.,
    13. Peschon J.,
    14. Bartlett P.,
    15. Willis C.,
    16. Wright B.,
    17. Carpenter M.,
    18. Davidson B.,
    19. Gearing D.
    (1995) Targeted disruption of the low-affinity leukemia inhibitory factor receptor genes causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121, 1283–1299
    OpenUrlAbstract
    1. Watanabe T.,
    2. Raff M.
    (1988) Retinal astrocytes are immigrants from the optic nerve. Nature 332, 834–837
    OpenUrlCrossRefPubMed
    1. Watanabe T.,
    2. Raff M.
    (1990) Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 2, 461–467
    1. Watanabe T.,
    2. Raff M.
    (1992) Diffusible rod-promoting signals in the developing rat retina. Development 114, 899–906
    OpenUrlAbstract
    1. Wetts R.,
    2. Fraser S.
    (1988) Multipotent precursors can give rise to almost all major cell types of the frog retina. Science 239, 1142–1145
    OpenUrlAbstract/FREE Full Text
    1. Young R. W.
    (1985) Cell differentiation in the retina of the mouse. Anat. Rec 212, 199–205
    OpenUrlCrossRefPubMedWeb of Science
    1. Zhang D.,
    2. Yeh H. H.
    (1991) Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: a developmental study. Vis. Neurosc 6, 429–437
    OpenUrlPubMedWeb of Science
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JOURNAL ARTICLES
Muller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development
C. Neophytou, A.B. Vernallis, A. Smith, M.C. Raff
Development 1997 124: 2345-2354;
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