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. 1989 Oct;9(10):4545–4549. doi: 10.1128/mcb.9.10.4545

Expression of the yes proto-oncogene in cerebellar Purkinje cells.

M Sudol 1, C F Kuo 1, L Shigemitsu 1, A Alvarez-Buylla 1
PMCID: PMC362541  PMID: 2685556

Abstract

To identify the kinds of cells in the brain that express the yes proto-oncogene, we examined chicken brains by using immunofluorescent staining and in situ hybridization. Both approaches showed that the highest level of the yes gene product was in cerebellar Purkinje cells. In addition, we analyzed Purkinje cell degeneration (pcd) mutant mice. The level of yes mRNA in cerebella of pcd mutants was four times lower than that found in cerebella of normal littermates. Our studies point to Purkinje cells as an attractive model for functional studies of the yes protein.

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Selected References

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  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barkley D. S., Rakic L. L., Chaffee J. K., Wong D. L. Cell separation by velocity sedimentation of postnatal mouse cerebellum. J Cell Physiol. 1973 Apr;81(2):271–279. doi: 10.1002/jcp.1040810215. [DOI] [PubMed] [Google Scholar]
  3. Brugge J. S., Erikson R. L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature. 1977 Sep 22;269(5626):346–348. doi: 10.1038/269346a0. [DOI] [PubMed] [Google Scholar]
  4. Brugge J. S., Lustig A., Messer A. Changes in the pattern of expression of pp60c-src in cerebellar mutants of mice. J Neurosci Res. 1987;18(4):532–538. doi: 10.1002/jnr.490180405. [DOI] [PubMed] [Google Scholar]
  5. Chan-Palay V., Nilaver G., Palay S. L., Beinfeld M. C., Zimmerman E. A., Wu J. Y., O'Donohue T. L. Chemical heterogeneity in cerebellar Purkinje cells: existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7787–7791. doi: 10.1073/pnas.78.12.7787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Fults D. W., Towle A. C., Lauder J. M., Maness P. F. pp60c-src in the developing cerebellum. Mol Cell Biol. 1985 Jan;5(1):27–32. doi: 10.1128/mcb.5.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gessler M., Barnekow A. Differential expression of the cellular oncogenes c-src and c-yes in embryonal and adult chicken tissues. Biosci Rep. 1984 Sep;4(9):757–770. doi: 10.1007/BF01128817. [DOI] [PubMed] [Google Scholar]
  9. Ghysdael J., Neil J. C., Wallbank A. M., Vogt P. K. Esh avian sarcoma virus codes for a gag-linked transformation-specific protein with an associated protein kinase activity. Virology. 1981 Jun;111(2):386–400. doi: 10.1016/0042-6822(81)90342-1. [DOI] [PubMed] [Google Scholar]
  10. Goodman R. R., Synder S. H. Autoradiographic localization of adenosine receptors in rat brain using [3H]cyclohexyladenosine. J Neurosci. 1982 Sep;2(9):1230–1241. doi: 10.1523/JNEUROSCI.02-09-01230.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grandori C., Hanafusa H. p60c-src is complexed with a cellular protein in subcellular compartments involved in exocytosis. J Cell Biol. 1988 Dec;107(6 Pt 1):2125–2135. doi: 10.1083/jcb.107.6.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanley M. R. Proto-oncogenes in the nervous system. Neuron. 1988 May;1(3):175–182. doi: 10.1016/0896-6273(88)90137-7. [DOI] [PubMed] [Google Scholar]
  13. Hatten M. E. Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol. 1985 Feb;100(2):384–396. doi: 10.1083/jcb.100.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hopfield J. F., Tank D. W., Greengard P., Huganir R. L. Functional modulation of the nicotinic acetylcholine receptor by tyrosine phosphorylation. Nature. 1988 Dec 15;336(6200):677–680. doi: 10.1038/336677a0. [DOI] [PubMed] [Google Scholar]
  15. Ingram V. M., Ogren M. P., Chatot C. L., Gossels J. M., Owens B. B. Diversity among Purkinje cells in the monkey cerebellum. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7131–7135. doi: 10.1073/pnas.82.20.7131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kafatos F. C., Jones C. W., Efstratiadis A. Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 1979 Nov 24;7(6):1541–1552. doi: 10.1093/nar/7.6.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Karess R. E., Hanafusa H. Viral and cellular src genes contribute to the structure of recovered avian sarcoma virus transforming protein. Cell. 1981 Apr;24(1):155–164. doi: 10.1016/0092-8674(81)90511-0. [DOI] [PubMed] [Google Scholar]
  18. Kato K., Suzuki F., Semba R. Determination of brain enolase isozymes with an enzyme immunoassay at the level of single neurons. J Neurochem. 1981 Oct;37(4):998–1005. doi: 10.1111/j.1471-4159.1981.tb04487.x. [DOI] [PubMed] [Google Scholar]
  19. Kitamura N., Kitamura A., Toyoshima K., Hirayama Y., Yoshida M. Avian sarcoma virus Y73 genome sequence and structural similarity of its transforming gene product to that of Rous sarcoma virus. Nature. 1982 May 20;297(5863):205–208. doi: 10.1038/297205a0. [DOI] [PubMed] [Google Scholar]
  20. Kuo C. F., Paulson K. E., Darnell J. E., Jr Positional and developmental regulation of glutamine synthetase expression in mouse liver. Mol Cell Biol. 1988 Nov;8(11):4966–4971. doi: 10.1128/mcb.8.11.4966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. Landis D. M., Reese T. S. Cytoplasmic organization in cerebellar dendritic spines. J Cell Biol. 1983 Oct;97(4):1169–1178. doi: 10.1083/jcb.97.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Le Beau J. M., Wiestler O. D., Walter G. An altered form of pp60c-src is expressed primarily in the central nervous system. Mol Cell Biol. 1987 Nov;7(11):4115–4117. doi: 10.1128/mcb.7.11.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Levy J. B., Dorai T., Wang L. H., Brugge J. S. The structurally distinct form of pp60c-src detected in neuronal cells is encoded by a unique c-src mRNA. Mol Cell Biol. 1987 Nov;7(11):4142–4145. doi: 10.1128/mcb.7.11.4142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lizardi P. M., Engelberg A. Rapid isolation of RNA using proteinase K and sodium perchlorate. Anal Biochem. 1979 Sep 15;98(1):116–122. doi: 10.1016/0003-2697(79)90714-0. [DOI] [PubMed] [Google Scholar]
  26. Lohmann S. M., Walter U., Miller P. E., Greengard P., De Camilli P. Immunohistochemical localization of cyclic GMP-dependent protein kinase in mammalian brain. Proc Natl Acad Sci U S A. 1981 Jan;78(1):653–657. doi: 10.1073/pnas.78.1.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martinez R., Mathey-Prevot B., Bernards A., Baltimore D. Neuronal pp60c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science. 1987 Jul 24;237(4813):411–415. doi: 10.1126/science.2440106. [DOI] [PubMed] [Google Scholar]
  28. McLean I. W., Nakane P. K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 1974 Dec;22(12):1077–1083. doi: 10.1177/22.12.1077. [DOI] [PubMed] [Google Scholar]
  29. Messer A., Snodgrass G. L., Maskin P. Enhanced survival of cultured cerebellar Purkinje cells by plating on antibody to Thy-1. Cell Mol Neurobiol. 1984 Sep;4(3):285–290. doi: 10.1007/BF00733591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Milner R. J., Bloom F. E., Sutcliffe J. G. Brain-specific genes: strategies and issues. Curr Top Dev Biol. 1987;21:117–150. doi: 10.1016/s0070-2153(08)60135-0. [DOI] [PubMed] [Google Scholar]
  31. Mullen R. J., Eicher E. M., Sidman R. L. Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci U S A. 1976 Jan;73(1):208–212. doi: 10.1073/pnas.73.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  33. Palacios J. M., Wamsley J. K., Kuhar M. J. GABA benzodiazepine and histamine-H1 receptors in the guinea pig cerebellum: effects of kainic acid injections studied by autoradiographic methods. Brain Res. 1981 Jun 9;214(1):155–162. doi: 10.1016/0006-8993(81)90447-9. [DOI] [PubMed] [Google Scholar]
  34. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  35. Ross C. A., Wright G. E., Resh M. D., Pearson R. C., Snyder S. H. Brain-specific src oncogene mRNA mapped in rat brain by in situ hybridization. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9831–9835. doi: 10.1073/pnas.85.24.9831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rotter A., Frostholm A. Cerebellar histamine-H1 receptor distribution: an autoradiographic study of Purkinje cell degeneration, staggerer, weaver and reeler mutant mouse strains. Brain Res Bull. 1986 Feb;16(2):205–214. doi: 10.1016/0361-9230(86)90034-1. [DOI] [PubMed] [Google Scholar]
  37. Rudd C. E., Trevillyan J. M., Dasgupta J. D., Wong L. L., Schlossman S. F. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5190–5194. doi: 10.1073/pnas.85.14.5190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shibuya M., Hanafusa H., Balduzzi P. C. Cellular sequences related to three new onc genes of avian sarcoma virus (fps, yes, and ros) and their expression in normal and transformed cells. J Virol. 1982 Apr;42(1):143–152. doi: 10.1128/jvi.42.1.143-152.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Slemmon J. R., Danho W., Hempstead J. L., Morgan J. I. Cerebellin: a quantifiable marker for Purkinje cell maturation. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7145–7148. doi: 10.1073/pnas.82.20.7145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sudol M., Alvarez-Buylla A., Hanafusa H. Differential developmental expression of cellular yes and cellular src proteins in cerebellum. Oncogene Res. 1988 May;2(4):345–355. [PubMed] [Google Scholar]
  41. Sudol M. Expression of proto-oncogenes in neural tissues. Brain Res. 1988 Dec;472(4):391–403. doi: 10.1016/0006-8993(88)91228-0. [DOI] [PubMed] [Google Scholar]
  42. Sudol M., Hanafusa H. Cellular proteins homologous to the viral yes gene product. Mol Cell Biol. 1986 Aug;6(8):2839–2846. doi: 10.1128/mcb.6.8.2839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sudol M. Hormonal regulation of protein synthesis in cultured kidney cells. Mol Cell Endocrinol. 1985 May;40(2-3):245–255. doi: 10.1016/0303-7207(85)90180-7. [DOI] [PubMed] [Google Scholar]
  44. Sudol M., Kieswetter C., Zhao Y. H., Dorai T., Wang L. H., Hanafusa H. Nucleotide sequence of a cDNA for the chick yes proto-oncogene: comparison with the viral yes gene. Nucleic Acids Res. 1988 Oct 25;16(20):9876–9876. doi: 10.1093/nar/16.20.9876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sudol M., Reich E. Purification and characterization of a plasminogen activator secreted by a pig kidney cell line. Biochem J. 1984 May 1;219(3):971–978. doi: 10.1042/bj2190971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sukegawa J., Semba K., Yamanashi Y., Nishizawa M., Miyajima N., Yamamoto T., Toyoshima K. Characterization of cDNA clones for the human c-yes gene. Mol Cell Biol. 1987 Jan;7(1):41–47. doi: 10.1128/mcb.7.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Swank R. T., Munkres K. D. Molecular weight analysis of oligopeptides by electrophoresis in polyacrylamide gel with sodium dodecyl sulfate. Anal Biochem. 1971 Feb;39(2):462–477. doi: 10.1016/0003-2697(71)90436-2. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. Veillette A., Bookman M. A., Horak E. M., Bolen J. B. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell. 1988 Oct 21;55(2):301–308. doi: 10.1016/0092-8674(88)90053-0. [DOI] [PubMed] [Google Scholar]
  50. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  51. Williams M. Purine receptors in mammalian tissues: pharmacology and functional significance. Annu Rev Pharmacol Toxicol. 1987;27:315–345. doi: 10.1146/annurev.pa.27.040187.001531. [DOI] [PubMed] [Google Scholar]
  52. Yamakuni T., Usui H., Iwanaga T., Kondo H., Odani S., Takahashi Y. Isolation and immunohistochemical localization of a cerebellar protein. Neurosci Lett. 1984 Apr 6;45(3):235–240. doi: 10.1016/0304-3940(84)90232-5. [DOI] [PubMed] [Google Scholar]

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