Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Jul 15;25(14):2930–2937. doi: 10.1093/nar/25.14.2930

Proto-oncogene Sno expression, alternative isoforms and immediate early serum response.

S Pearson-White 1, R Crittenden 1
PMCID: PMC146803  PMID: 9207045

Abstract

The mouse Sno gene, a Ski proto-oncogene homolog, expresses two isoforms, SnoN and SnoN2 (also called sno -dE3), which differ from each other in a location downstream from the site of alternative splicing previously described in the human SNO gene. SnoN2 is missing a 138 nt coding segment present in mouse SnoN and human SNON . We have cloned and sequenced the human ortholog of mouse SnoN2 , the existence of which was predicted from conservation of the alternative splice donor site that produces the SnoN2 isoform. Mouse SnoN2 and SnoN are expressed throughout embryonic development, in neonatal muscle and in many adult tissues. SnoN2 is the major species in most tissues, but SnoN and SnoN2 are expressed at approximately equal levels in brain. In human tissues, SNON2 is the less abundantly expressed isoform. Expression of mouse SnoN and SnoN2 mRNAs is induced with immediate early kinetics upon serum stimulation of quiescent fibroblasts, even in the presence of the protein synthesis inhibitor cycloheximide, while Ski is not. Interestingly, although both isoforms of Sno are induced, SnoN2 induction is much higher than SnoN . These data are consistent with a role for Sno in the response to proliferation stimuli.

Full Text

The Full Text of this article is available as a PDF (412.4 KB).

Selected References

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

  1. Avanzi G. C., Lista P., Giovinazzo B., Miniero R., Saglio G., Benetton G., Coda R., Cattoretti G., Pegoraro L. Selective growth response to IL-3 of a human leukaemic cell line with megakaryoblastic features. Br J Haematol. 1988 Jul;69(3):359–366. doi: 10.1111/j.1365-2141.1988.tb02374.x. [DOI] [PubMed] [Google Scholar]
  2. Bernlohr D. A., Bolanowski M. A., Kelly T. J., Jr, Lane M. D. Evidence for an increase in transcription of specific mRNAs during differentiation of 3T3-L1 preadipocytes. J Biol Chem. 1985 May 10;260(9):5563–5567. [PubMed] [Google Scholar]
  3. Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blau H. M., Pavlath G. K., Hardeman E. C., Chiu C. P., Silberstein L., Webster S. G., Miller S. C., Webster C. Plasticity of the differentiated state. Science. 1985 Nov 15;230(4727):758–766. doi: 10.1126/science.2414846. [DOI] [PubMed] [Google Scholar]
  5. Boyer P. L., Colmenares C., Stavnezer E., Hughes S. H. Sequence and biological activity of chicken snoN cDNA clones. Oncogene. 1993 Feb;8(2):457–466. [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. Colmenares C., Stavnezer E. The ski oncogene induces muscle differentiation in quail embryo cells. Cell. 1989 Oct 20;59(2):293–303. doi: 10.1016/0092-8674(89)90291-2. [DOI] [PubMed] [Google Scholar]
  8. Colmenares C., Teumer J. K., Stavnezer E. Transformation-defective v-ski induces MyoD and myogenin expression but not myotube formation. Mol Cell Biol. 1991 Feb;11(2):1167–1170. doi: 10.1128/mcb.11.2.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dean M., Cleveland J. L., Rapp U. R., Ihle J. N. Role of myc in the abrogation of IL3 dependence of myeloid FDC-P1 cells. Oncogene Res. 1987 Aug;1(3):279–296. [PubMed] [Google Scholar]
  10. Dexter T. M., Garland J., Scott D., Scolnick E., Metcalf D. Growth of factor-dependent hemopoietic precursor cell lines. J Exp Med. 1980 Oct 1;152(4):1036–1047. doi: 10.1084/jem.152.4.1036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Givol I., Boyer P. L., Hughes S. H. Isolation and characterization of the chicken c-sno gene. Gene. 1995 Apr 24;156(2):271–276. doi: 10.1016/0378-1119(95)00066-f. [DOI] [PubMed] [Google Scholar]
  12. Grimes H. L., Ambrose M. R., Goodenow M. M. C-ski transcripts with and without exon 2 are expressed in skeletal muscle and throughout chick embryogenesis. Oncogene. 1993 Oct;8(10):2863–2868. [PubMed] [Google Scholar]
  13. Grimes H. L., Szente B. E., Goodenow M. M. C-ski cDNAs are encoded by eight exons, six of which are closely linked within the chicken genome. Nucleic Acids Res. 1992 Apr 11;20(7):1511–1516. doi: 10.1093/nar/20.7.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  15. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  16. Heyman H. C., Stavnezer E. A carboxyl-terminal region of the ski oncoprotein mediates homodimerization as well as heterodimerization with the related protein SnoN. J Biol Chem. 1994 Oct 28;269(43):26996–27003. [PubMed] [Google Scholar]
  17. Hofbauer R., Denhardt D. T. Cell cycle-regulated and proliferation stimulus-responsive genes. Crit Rev Eukaryot Gene Expr. 1991;1(4):247–300. [PubMed] [Google Scholar]
  18. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  19. Konieczny S. F., Emerson C. P., Jr 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regulatory genes controlling determination. Cell. 1984 Oct;38(3):791–800. doi: 10.1016/0092-8674(84)90274-5. [DOI] [PubMed] [Google Scholar]
  20. Larsen J., Beug H., Hayman M. J. The v-ski oncogene cooperates with the v-sea oncogene in erythroid transformation by blocking erythroid differentiation. Oncogene. 1992 Oct;7(10):1903–1911. [PubMed] [Google Scholar]
  21. Leferovich J. M., Lana D. P., Sutrave P., Hughes S. H., Kelly A. M. Regulation of c-ski transgene expression in developing and mature mice. J Neurosci. 1995 Jan;15(1 Pt 2):596–603. doi: 10.1523/JNEUROSCI.15-01-00596.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Linzer D. I., Nathans D. Growth-related changes in specific mRNAs of cultured mouse cells. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4271–4275. doi: 10.1073/pnas.80.14.4271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lipman D. J., Altschul S. F., Kececioglu J. D. A tool for multiple sequence alignment. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4412–4415. doi: 10.1073/pnas.86.12.4412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ludolph D. C., Neff A. W., Parker M. A., Mescher A. L., Smith R. C., Malacinski G. M. Cloning and expression of the axolotl proto-oncogene ski. Biochim Biophys Acta. 1995 Jan 2;1260(1):102–104. doi: 10.1016/0167-4781(94)00194-8. [DOI] [PubMed] [Google Scholar]
  25. Lyons G. E., Micales B. K., Herr M. J., Horrigan S. K., Namciu S., Shardy D., Stavnezer E. Protooncogene c-ski is expressed in both proliferating and postmitotic neuronal populations. Dev Dyn. 1994 Dec;201(4):354–365. doi: 10.1002/aja.1002010407. [DOI] [PubMed] [Google Scholar]
  26. Müller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature. 1984 Dec 20;312(5996):716–720. doi: 10.1038/312716a0. [DOI] [PubMed] [Google Scholar]
  27. Nagase T., Nomura N., Ishii S. Complex formation between proteins encoded by the ski gene family. J Biol Chem. 1993 Jun 25;268(18):13710–13716. [PubMed] [Google Scholar]
  28. Namciu S., Lieberman M. A., Stavnezer E. Induction of the c-ski proto-oncogene by phorbol ester correlates with induction of megakaryocyte differentiation. Oncogene. 1994 May;9(5):1407–1416. [PubMed] [Google Scholar]
  29. Namciu S., Lyons G. E., Micales B. K., Heyman H. C., Colmenares C., Stavnezer E. Enhanced expression of mouse c-ski accompanies terminal skeletal muscle differentiation in vivo and in vitro. Dev Dyn. 1995 Nov;204(3):291–300. doi: 10.1002/aja.1002040307. [DOI] [PubMed] [Google Scholar]
  30. Nomura N., Sasamoto S., Ishii S., Date T., Matsui M., Ishizaki R. Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acids Res. 1989 Jul 25;17(14):5489–5500. doi: 10.1093/nar/17.14.5489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pearson-White S., Deacon D., Crittenden R., Brady G., Iscove N., Quesenberry P. J. The ski/sno protooncogene family in hematopoietic development. Blood. 1995 Sep 15;86(6):2146–2155. [PubMed] [Google Scholar]
  32. Pearson-White S. SnoI, a novel alternatively spliced isoform of the ski protooncogene homolog, sno. Nucleic Acids Res. 1993 Sep 25;21(19):4632–4638. doi: 10.1093/nar/21.19.4632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pearson W. R. Effective protein sequence comparison. Methods Enzymol. 1996;266:227–258. doi: 10.1016/s0076-6879(96)66017-0. [DOI] [PubMed] [Google Scholar]
  34. Peden K., Mounts P., Hayward G. S. Homology between mammalian cell DNA sequences and human herpesvirus genomes detected by a hybridization procedure with high-complexity probe. Cell. 1982 Nov;31(1):71–80. doi: 10.1016/0092-8674(82)90406-8. [DOI] [PubMed] [Google Scholar]
  35. Pelzer T., Lyons G. E., Kim S., Moreadith R. W. Cloning and characterization of the murine homolog of the sno proto-oncogene reveals a novel splice variant. Dev Dyn. 1996 Feb;205(2):114–125. doi: 10.1002/(SICI)1097-0177(199602)205:2<114::AID-AJA3>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  36. Rawls A., Morris J. H., Rudnicki M., Braun T., Arnold H. H., Klein W. H., Olson E. N. Myogenin's functions do not overlap with those of MyoD or Myf-5 during mouse embryogenesis. Dev Biol. 1995 Nov;172(1):37–50. doi: 10.1006/dbio.1995.0004. [DOI] [PubMed] [Google Scholar]
  37. Ryseck R. P., Hirai S. I., Yaniv M., Bravo R. Transcriptional activation of c-jun during the G0/G1 transition in mouse fibroblasts. Nature. 1988 Aug 11;334(6182):535–537. doi: 10.1038/334535a0. [DOI] [PubMed] [Google Scholar]
  38. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sleeman J. P., Laskey R. A. Xenopus c-ski contains a novel coiled-coil protein domain, and is maternally expressed during development. Oncogene. 1993 Jan;8(1):67–77. [PubMed] [Google Scholar]
  40. Stavnezer E., Barkas A. E., Brennan L. A., Brodeur D., Li Y. Transforming Sloan-Kettering viruses generated from the cloned v-ski oncogene by in vitro and in vivo recombinations. J Virol. 1986 Mar;57(3):1073–1083. doi: 10.1128/jvi.57.3.1073-1083.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stavnezer E., Gerhard D. S., Binari R. C., Balazs I. Generation of transforming viruses in cultures of chicken fibroblasts infected with an avian leukosis virus. J Virol. 1981 Sep;39(3):920–934. doi: 10.1128/jvi.39.3.920-934.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sutrave P., Kelly A. M., Hughes S. H. ski can cause selective growth of skeletal muscle in transgenic mice. Genes Dev. 1990 Sep;4(9):1462–1472. doi: 10.1101/gad.4.9.1462. [DOI] [PubMed] [Google Scholar]
  43. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. doi: 10.1038/270725a0. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES