Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Oct;15(10):5563–5575. doi: 10.1128/mcb.15.10.5563

Transcriptional stimulation of the retina-specific QR1 gene upon growth arrest involves a Maf-related protein.

C Pouponnot 1, M Nishizawa 1, G Calothy 1, A Pierani 1
PMCID: PMC230807  PMID: 7565708

Abstract

The avian neural retina (NR) is derived from proliferating neuroectodermal precursors which differentiate after terminal mitosis and become organized in cell strata. Proliferation of postmitotic NR cells can be induced by infection with Rous sarcoma virus (RSV) and requires the expression of a functional v-Src protein. QR1 is a retina-specific gene expressed exclusively at the stage of growth arrest and differentiation during retinal development. In NR cells infected with tsPA101, an RSV mutant conditionally defective in pp60v-src mitogenic capacity, QR1 expression is downregulated in proliferating cells at 37 degrees C and is fully restored when the cells become quiescent as a result of pp60v-src inactivation at 41 degrees C. We were able to arrest proliferation of tsPA101-infected quail NR cells expressing an active v-Src protein by serum starvation at 37 degrees C. This allowed us to investigate the role of cell growth in regulating QR1 transcription. We report that QR1 transcription is stimulated in growth-arrested cells at 37 degrees C compared with that in proliferating cells maintained at the same temperature. Growth arrest-dependent stimulation of QR1 transcription requires the integrity of the A box, a previously characterized cis-acting element responsible for QR1 transcriptional stimulation upon v-Src inactivation and during retinal differentiation. We also show that formation of the C1 complex on the A box is increased upon growth arrest by serum starvation in the presence of an active v-Src oncoprotein. Thus, the C1 complex represents an important link between cell cycle and developmental control of QR1 gene transcription during NR differentiation and RSV infection. By using antibodies directed against different Maf proteins of the leucine zipper family and competition with Maf consensus site-containing oligonucleotides in a gel shift assay, we show that the C1 complex is likely to contain a Maf-related protein. We also show that a purified bacterially expressed v-Maf protein is able to bind the A box and that the level of a 43-kDa Maf-related protein is increased upon growth arrest in infected retinal cells. Moreover, ectopic expression of c-mafI, c-mafII, and mafB cDNAs in quiescent tsPA101-infected quail NR cells is able to stimulate transcription of a QR1 reporter gene through the A box. Therefore, QR1 appears to be the first target gene for a Maf-related protein(s) in the NR.

Full Text

The Full Text of this article is available as a PDF (526.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alber T. Structure of the leucine zipper. Curr Opin Genet Dev. 1992 Apr;2(2):205–210. doi: 10.1016/s0959-437x(05)80275-8. [DOI] [PubMed] [Google Scholar]
  2. Alema S., Tato F., Boettiger D. myc and src oncogenes have complementary effects on cell proliferation and expression of specific extracellular matrix components in definitive chondroblasts. Mol Cell Biol. 1985 Mar;5(3):538–544. doi: 10.1128/mcb.5.3.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. An G., Hidaka K., Siminovitch L. Expression of bacterial beta-galactosidase in animal cells. Mol Cell Biol. 1982 Dec;2(12):1628–1632. doi: 10.1128/mcb.2.12.1628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Andrews N. C., Kotkow K. J., Ney P. A., Erdjument-Bromage H., Tempst P., Orkin S. H. The ubiquitous subunit of erythroid transcription factor NF-E2 is a small basic-leucine zipper protein related to the v-maf oncogene. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11488–11492. doi: 10.1073/pnas.90.24.11488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Apel I., Yu C. L., Wang T., Dobry C., Van Antwerp M. E., Jove R., Prochownik E. V. Regulation of the junB gene by v-src. Mol Cell Biol. 1992 Aug;12(8):3356–3364. doi: 10.1128/mcb.12.8.3356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barnstable C. J. A molecular view of vertebrate retinal development. Mol Neurobiol. 1987 Spring-Summer;1(1-2):9–46. doi: 10.1007/BF02935263. [DOI] [PubMed] [Google Scholar]
  7. Bedard P. A., Yannoni Y., Simmons D. L., Erikson R. L. Rapid repression of quiescence-specific gene expression by epidermal growth factor, insulin, and pp60v-src. Mol Cell Biol. 1989 Mar;9(3):1371–1375. doi: 10.1128/mcb.9.3.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Beddington R. S., Morgernstern J., Land H., Hogan A. An in situ transgenic enzyme marker for the midgestation mouse embryo and the visualization of inner cell mass clones during early organogenesis. Development. 1989 May;106(1):37–46. doi: 10.1242/dev.106.1.37. [DOI] [PubMed] [Google Scholar]
  9. Birchenall-Roberts M. C., Ruscetti F. W., Kasper J., Lee H. D., Friedman R., Geiser A., Sporn M. B., Roberts A. B., Kim S. J. Transcriptional regulation of the transforming growth factor beta 1 promoter by v-src gene products is mediated through the AP-1 complex. Mol Cell Biol. 1990 Sep;10(9):4978–4983. doi: 10.1128/mcb.10.9.4978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brancolini C., Bottega S., Schneider C. Gas2, a growth arrest-specific protein, is a component of the microfilament network system. J Cell Biol. 1992 Jun;117(6):1251–1261. doi: 10.1083/jcb.117.6.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Calothy G., Poirier F., Dambrine G., Mignatti P., Combes P., Pessac B. Expression of viral oncogenes in differentiating chick embryo neuroretinal cells infected with avian tumor viruses. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):983–990. doi: 10.1101/sqb.1980.044.01.106. [DOI] [PubMed] [Google Scholar]
  12. Calothy G., Poirier F., Dambrine G., Pessac B. A transformation defective mutant of Rous sarcoma virus inducing chick embryo neuroretinal cell proliferation. Virology. 1978 Aug;89(1):75–84. doi: 10.1016/0042-6822(78)90041-7. [DOI] [PubMed] [Google Scholar]
  13. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  14. Ciccarelli C., Philipson L., Sorrentino V. Regulation of expression of growth arrest-specific genes in mouse fibroblasts. Mol Cell Biol. 1990 Apr;10(4):1525–1529. doi: 10.1128/mcb.10.4.1525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Coccia E. M., Cicala C., Charlesworth A., Ciccarelli C., Rossi G. B., Philipson L., Sorrentino V. Regulation and expression of a growth arrest-specific gene (gas5) during growth, differentiation, and development. Mol Cell Biol. 1992 Aug;12(8):3514–3521. doi: 10.1128/mcb.12.8.3514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Combes P. C., Privat A., Pessac B., Calothy G. Differentiation of chick embryo neuroretina cells in monolayer cultures. An ultrastructural study. I. Seven-day retina. Cell Tissue Res. 1977 Dec 13;185(2):159–173. doi: 10.1007/BF00220661. [DOI] [PubMed] [Google Scholar]
  17. Coppock D. L., Kopman C., Scandalis S., Gilleran S. Preferential gene expression in quiescent human lung fibroblasts. Cell Growth Differ. 1993 Jun;4(6):483–493. [PubMed] [Google Scholar]
  18. Cordes S. P., Barsh G. S. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell. 1994 Dec 16;79(6):1025–1034. doi: 10.1016/0092-8674(94)90033-7. [DOI] [PubMed] [Google Scholar]
  19. Dehbi M., Mbiguino A., Beauchemin M., Chatelain G., Bédard P. A. Transcriptional activation of the CEF-4/9E3 cytokine gene by pp60v-src. Mol Cell Biol. 1992 Apr;12(4):1490–1499. doi: 10.1128/mcb.12.4.1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Del Sal G., Ruaro M. E., Philipson L., Schneider C. The growth arrest-specific gene, gas1, is involved in growth suppression. Cell. 1992 Aug 21;70(4):595–607. doi: 10.1016/0092-8674(92)90429-g. [DOI] [PubMed] [Google Scholar]
  21. Dutta A., Stoeckle M. Y., Hanafusa H. Serum and v-src increase the level of a CCAAT-binding factor required for transcription from a retroviral long terminal repeat. Genes Dev. 1990 Feb;4(2):243–254. doi: 10.1101/gad.4.2.243. [DOI] [PubMed] [Google Scholar]
  22. Falcone G., Alemà S., Tatò F. Transcription of muscle-specific genes is repressed by reactivation of pp60v-src in postmitotic quail myotubes. Mol Cell Biol. 1991 Jun;11(6):3331–3338. doi: 10.1128/mcb.11.6.3331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Falcone G., Tatò F., Alemà S. Distinctive effects of the viral oncogenes myc, erb, fps, and src on the differentiation program of quail myogenic cells. Proc Natl Acad Sci U S A. 1985 Jan;82(2):426–430. doi: 10.1073/pnas.82.2.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Farjo Q., Jackson A. U., Xu J., Gryzenia M., Skolnick C., Agarwal N., Swaroop A. Molecular characterization of the murine neural retina leucine zipper gene, Nrl. Genomics. 1993 Nov;18(2):216–222. doi: 10.1006/geno.1993.1458. [DOI] [PubMed] [Google Scholar]
  25. Fornace A. J., Jr, Nebert D. W., Hollander M. C., Luethy J. D., Papathanasiou M., Fargnoli J., Holbrook N. J. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol Cell Biol. 1989 Oct;9(10):4196–4203. doi: 10.1128/mcb.9.10.4196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fujii M., Shalloway D., Verma I. M. Gene regulation by tyrosine kinases: src protein activates various promoters, including c-fos. Mol Cell Biol. 1989 Jun;9(6):2493–2499. doi: 10.1128/mcb.9.6.2493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Fujiwara K. T., Kataoka K., Nishizawa M. Two new members of the maf oncogene family, mafK and mafF, encode nuclear b-Zip proteins lacking putative trans-activator domain. Oncogene. 1993 Sep;8(9):2371–2380. [PubMed] [Google Scholar]
  28. Gillet G., Michel D., Crisanti P., Guérin M., Herault Y., Pessac B., Calothy G., Brun G., Volovitch M. Serum factors and v-src control two complementary mitogenic pathways in quail neuroretinal cells in culture. Oncogene. 1993 Mar;8(3):565–574. [PubMed] [Google Scholar]
  29. Gu W., Schneider J. W., Condorelli G., Kaushal S., Mahdavi V., Nadal-Ginard B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 1993 Feb 12;72(3):309–324. doi: 10.1016/0092-8674(93)90110-c. [DOI] [PubMed] [Google Scholar]
  30. Guermah M., Crisanti P., Laugier D., Dezelee P., Bidou L., Pessac B., Calothy G. Transcription of a quail gene expressed in embryonic retinal cells is shut off sharply at hatching. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4503–4507. doi: 10.1073/pnas.88.10.4503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Guermah M., Gillet G., Michel D., Laugier D., Brun G., Calothy G. Down regulation by p60v-src of genes specifically expressed and developmentally regulated in postmitotic quail neuroretina cells. Mol Cell Biol. 1990 Jul;10(7):3584–3590. doi: 10.1128/mcb.10.7.3584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Gustincich S., Schneider C. Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell Growth Differ. 1993 Sep;4(9):753–760. [PubMed] [Google Scholar]
  33. Gutman A., Wasylyk B. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J. 1990 Jul;9(7):2241–2246. doi: 10.1002/j.1460-2075.1990.tb07394.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hendricks M., Weintraub H. Multiple tropomyosin polypeptides in chicken embryo fibroblasts: differential repression of transcription by Rous sarcoma virus transformation. Mol Cell Biol. 1984 Sep;4(9):1823–1833. doi: 10.1128/mcb.4.9.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Herault Y., Chatelain G., Brun G., Michel D. V-src-induced-transcription of the avian clusterin gene. Nucleic Acids Res. 1992 Dec 11;20(23):6377–6383. doi: 10.1093/nar/20.23.6377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Hollingsworth R. E., Jr, Chen P. L., Lee W. H. Integration of cell cycle control with transcriptional regulation by the retinoblastoma protein. Curr Opin Cell Biol. 1993 Apr;5(2):194–200. doi: 10.1016/0955-0674(93)90102-v. [DOI] [PubMed] [Google Scholar]
  37. Hollingsworth R. E., Jr, Hensey C. E., Lee W. H. Retinoblastoma protein and the cell cycle. Curr Opin Genet Dev. 1993 Feb;3(1):55–62. doi: 10.1016/s0959-437x(05)80341-7. [DOI] [PubMed] [Google Scholar]
  38. Igarashi K., Kataoka K., Itoh K., Hayashi N., Nishizawa M., Yamamoto M. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature. 1994 Feb 10;367(6463):568–572. doi: 10.1038/367568a0. [DOI] [PubMed] [Google Scholar]
  39. Jähner D., Hunter T. The stimulation of quiescent rat fibroblasts by v-src and v-fps oncogenic protein-tyrosine kinases leads to the induction of a subset of immediate early genes. Oncogene. 1991 Jul;6(7):1259–1268. [PubMed] [Google Scholar]
  40. Kahn A. J. An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev Biol. 1974 May;38(1):30–40. doi: 10.1016/0012-1606(74)90256-5. [DOI] [PubMed] [Google Scholar]
  41. Kahn P., Adkins B., Beug H., Graf T. src- and fps-containing avian sarcoma viruses transform chicken erythroid cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7122–7126. doi: 10.1073/pnas.81.22.7122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kataoka K., Fujiwara K. T., Noda M., Nishizawa M. MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol Cell Biol. 1994 Nov;14(11):7581–7591. doi: 10.1128/mcb.14.11.7581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kataoka K., Igarashi K., Itoh K., Fujiwara K. T., Noda M., Yamamoto M., Nishizawa M. Small Maf proteins heterodimerize with Fos and may act as competitive repressors of the NF-E2 transcription factor. Mol Cell Biol. 1995 Apr;15(4):2180–2190. doi: 10.1128/mcb.15.4.2180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kataoka K., Nishizawa M., Kawai S. Structure-function analysis of the maf oncogene product, a member of the b-Zip protein family. J Virol. 1993 Apr;67(4):2133–2141. doi: 10.1128/jvi.67.4.2133-2141.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kataoka K., Noda M., Nishizawa M. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol Cell Biol. 1994 Jan;14(1):700–712. doi: 10.1128/mcb.14.1.700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Kawai S., Hanafusa H. The effects of reciprocal changes in temperature on the transformed state of cells infected with a rous sarcoma virus mutant. Virology. 1971 Nov;46(2):470–479. doi: 10.1016/0042-6822(71)90047-x. [DOI] [PubMed] [Google Scholar]
  47. Kerppola T. K., Curran T. A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins. Oncogene. 1994 Nov;9(11):3149–3158. [PubMed] [Google Scholar]
  48. Kerppola T. K., Curran T. Maf and Nrl can bind to AP-1 sites and form heterodimers with Fos and Jun. Oncogene. 1994 Mar;9(3):675–684. [PubMed] [Google Scholar]
  49. Kurschner C., Morgan J. I. The maf proto-oncogene stimulates transcription from multiple sites in a promoter that directs Purkinje neuron-specific gene expression. Mol Cell Biol. 1995 Jan;15(1):246–254. doi: 10.1128/mcb.15.1.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Langer-Safer P. R., Lehrman S. R., Skalka A. M. v-src inhibits differentiation via an extracellular intermediate(s). Mol Cell Biol. 1985 Oct;5(10):2847–2850. doi: 10.1128/mcb.5.10.2847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Lankat-Buttgereit B., Mann K., Deutzmann R., Timpl R., Krieg T. Cloning and complete amino acid sequences of human and murine basement membrane protein BM-40 (SPARC, osteonectin). FEBS Lett. 1988 Aug 29;236(2):352–356. doi: 10.1016/0014-5793(88)80054-1. [DOI] [PubMed] [Google Scholar]
  52. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  53. Manfioletti G., Ruaro M. E., Del Sal G., Philipson L., Schneider C. A growth arrest-specific (gas) gene codes for a membrane protein. Mol Cell Biol. 1990 Jun;10(6):2924–2930. doi: 10.1128/mcb.10.6.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Mao P. L., Beauchemin M., Bédard P. A. Quiescence-dependent activation of the p20K promoter in growth-arrested chicken embryo fibroblasts. J Biol Chem. 1993 Apr 15;268(11):8131–8139. [PubMed] [Google Scholar]
  55. Mizushima S., Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 1990 Sep 11;18(17):5322–5322. doi: 10.1093/nar/18.17.5322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nishizawa M., Kataoka K., Goto N., Fujiwara K. T., Kawai S. v-maf, a viral oncogene that encodes a "leucine zipper" motif. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7711–7715. doi: 10.1073/pnas.86.20.7711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pessac B., Calothy G. Transformation of chick embryo neuroretinal cells by Rous sarcoma virus in vitro: induction of cell proliferation. Science. 1974 Aug;185(4152):709–710. doi: 10.1126/science.185.4152.709. [DOI] [PubMed] [Google Scholar]
  58. Pessac B., Girard A., Romey G., Crisanti P., Lorinet A. M., Calothy G. A neuronal clone derived from a Rous sarcoma virus-transformed quail embryo neuroretina established culture. Nature. 1983 Apr 14;302(5909):616–618. doi: 10.1038/302616a0. [DOI] [PubMed] [Google Scholar]
  59. Pfarr C. M., Mechta F., Spyrou G., Lallemand D., Carillo S., Yaniv M. Mouse JunD negatively regulates fibroblast growth and antagonizes transformation by ras. Cell. 1994 Feb 25;76(4):747–760. doi: 10.1016/0092-8674(94)90513-4. [DOI] [PubMed] [Google Scholar]
  60. Pierani A., Pouponnot C., Calothy G. Developmental control of transcription of a retina-specific gene, QR1, during differentiation: involvement of factors from the POU family. Mol Cell Biol. 1995 Feb;15(2):642–652. doi: 10.1128/mcb.15.2.642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Pierani A., Pouponnot C., Calothy G. Transcriptional downregulation of the retina-specific QR1 gene by pp60v-src and identification of a novel v-src-responsive unit. Mol Cell Biol. 1993 Jun;13(6):3401–3414. doi: 10.1128/mcb.13.6.3401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Poirier F., Calothy G., Karess R. E., Erikson E., Hanafusa H. Role of p60src kinase activity in the induction of neuroretinal cell proliferation by rous sarcoma virus. J Virol. 1982 Jun;42(3):780–789. doi: 10.1128/jvi.42.3.780-789.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Qureshi S. A., Cao X. M., Sukhatme V. P., Foster D. A. v-Src activates mitogen-responsive transcription factor Egr-1 via serum response elements. J Biol Chem. 1991 Jun 15;266(17):10802–10806. [PubMed] [Google Scholar]
  64. Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
  65. Sage E. H., Bornstein P. Extracellular proteins that modulate cell-matrix interactions. SPARC, tenascin, and thrombospondin. J Biol Chem. 1991 Aug 15;266(23):14831–14834. [PubMed] [Google Scholar]
  66. Sato H., Kita M., Seiki M. v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements. A mechanism regulating gene expression independent of that by inflammatory cytokines. J Biol Chem. 1993 Nov 5;268(31):23460–23468. [PubMed] [Google Scholar]
  67. Schneider C., King R. M., Philipson L. Genes specifically expressed at growth arrest of mammalian cells. Cell. 1988 Sep 9;54(6):787–793. doi: 10.1016/s0092-8674(88)91065-3. [DOI] [PubMed] [Google Scholar]
  68. Simmons D. L., Levy D. B., Yannoni Y., Erikson R. L. Identification of a phorbol ester-repressible v-src-inducible gene. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1178–1182. doi: 10.1073/pnas.86.4.1178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Simonneau L., Crisanti P., Lorinet A. M., Alliot F., Courtois Y., Calothy G., Pessac B. Crystallin gene expression and lentoid body formation in quail embryo neuroretina cultures transformed by the oncogenic retrovirus Mill Hill 2 or Rous sarcoma virus. Mol Cell Biol. 1986 Nov;6(11):3704–3710. doi: 10.1128/mcb.6.11.3704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Sorge L. K., Levy B. T., Maness P. F. pp60c-src is developmentally regulated in the neural retina. Cell. 1984 Feb;36(2):249–257. doi: 10.1016/0092-8674(84)90218-6. [DOI] [PubMed] [Google Scholar]
  71. Swaroop A., Xu J. Z., Pawar H., Jackson A., Skolnick C., Agarwal N. A conserved retina-specific gene encodes a basic motif/leucine zipper domain. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):266–270. doi: 10.1073/pnas.89.1.266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Thierry F., Dostatni N., Arnos F., Yaniv M. Cooperative activation of transcription by bovine papillomavirus type 1 E2 can occur over a large distance. Mol Cell Biol. 1990 Aug;10(8):4431–4437. doi: 10.1128/mcb.10.8.4431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Trotter J., Boulter C. A., Sontheimer H., Schachner M., Wagner E. F. Expression of v-src arrests murine glial cell differentiation. Oncogene. 1989 Apr;4(4):457–464. [PubMed] [Google Scholar]
  75. Vardimon L., Fox L. E., Cohen-Kupiec R., Degenstein L., Moscona A. A. Expression of v-src in embryonic neural retina alters cell adhesion, inhibits histogenesis, and prevents induction of glutamine synthetase. Mol Cell Biol. 1991 Oct;11(10):5275–5284. doi: 10.1128/mcb.11.10.5275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Vardimon L., Fox L. E., Moscona A. A. Accumulation of c-src mRNA is developmentally regulated in embryonic neural retina. Mol Cell Biol. 1986 Nov;6(11):4109–4111. doi: 10.1128/mcb.6.11.4109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Welham M. J., Wyke J. A., Lang A., Wyke A. W. Mitogenesis induced by pp60v-src is not accompanied by increased expression of immediate early response genes. Oncogene. 1990 Feb;5(2):161–169. [PubMed] [Google Scholar]
  78. Xie W., Fletcher B. S., Andersen R. D., Herschman H. R. v-src induction of the TIS10/PGS2 prostaglandin synthase gene is mediated by an ATF/CRE transcription response element. Mol Cell Biol. 1994 Oct;14(10):6531–6539. doi: 10.1128/mcb.14.10.6531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. de Martin R., Cowled P. A., Smith S. E., Papavassiliou A. G., Sorrentino V., Philipson L., Bohmann D. Structure and regulation of the growth arrest-specific (gas-1) promoter. J Biol Chem. 1993 Oct 25;268(30):22788–22793. [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES