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. 1983 Dec 10;11(23):8317–8332. doi: 10.1093/nar/11.23.8317

Vimentin gene expression during myogenesis: two functional transcripts from a single copy gene.

Z E Zehner, B M Paterson
PMCID: PMC326584  PMID: 6672766

Abstract

We have previously reported that a single vimentin gene is present in the chicken genome (22). In vivo transcription of this gene yields two distinct classes of mRNA's (approximatley 2200 and-2500 nts) generated through the possible differential utilization of polyadenylylation sites. In this report we demonstrate that 1) both transcripts are functional in vitro and direct the cell-free synthesis of the vimentin polypeptide, as judged by two dimensional gel analysis; 2) three of the four possible adenylylation signals indicated in the sequence of the gene are utilized in vivo as determined by S1 analysis; 3) furthermore, these adenylylation sites are utilized identically in all tissues of the chicken examined; 4) the adenylylation site closest to the body of the message is apparently not used as judged by the S1 conditions employed in the assay. Levels of vimentin mRNA decrease in different tissues of the chicken during the embryonic to adult transition. There is no evidence for a tissue specific or developmentally regulated pattern of expression for either of the two vimentin transcripts. The same pattern of vimentin mRNA expression is seen in all tissues examined, only the level of expression is altered.

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Selected References

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

  1. Bailey J. M., Davidson N. Methylmercury as a reversible denaturing agent for agarose gel electrophoresis. Anal Biochem. 1976 Jan;70(1):75–85. doi: 10.1016/s0003-2697(76)80049-8. [DOI] [PubMed] [Google Scholar]
  2. Bennett G. S., Fellini S. A., Toyama Y., Holtzer H. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol. 1979 Aug;82(2):577–584. doi: 10.1083/jcb.82.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benoist C., O'Hare K., Breathnach R., Chambon P. The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res. 1980 Jan 11;8(1):127–142. doi: 10.1093/nar/8.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Spliced early mRNAs of simian virus 40. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1274–1278. doi: 10.1073/pnas.75.3.1274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  6. Cervera M., Dreyfuss G., Penman S. Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells. Cell. 1981 Jan;23(1):113–120. doi: 10.1016/0092-8674(81)90276-2. [DOI] [PubMed] [Google Scholar]
  7. Cooke P. A filamentous cytoskeleton in vertebrate smooth muscle fibers. J Cell Biol. 1976 Mar;68(3):539–556. doi: 10.1083/jcb.68.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fagan J. B., Sobel M. E., Yamada K. M., de Crombrugghe B., Pastan I. Effects of transformation on fibronectin gene expression using cloned fibronectin cDNA. J Biol Chem. 1981 Jan 10;256(1):520–525. [PubMed] [Google Scholar]
  9. Fitzgerald M., Shenk T. The sequence 5'-AAUAAA-3'forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell. 1981 Apr;24(1):251–260. doi: 10.1016/0092-8674(81)90521-3. [DOI] [PubMed] [Google Scholar]
  10. Frank E. D., Warren L. Aortic smooth muscle cells contain vimentin instead of desmin. Proc Natl Acad Sci U S A. 1981 May;78(5):3020–3024. doi: 10.1073/pnas.78.5.3020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fuchs E., Green H. Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell. 1980 Apr;19(4):1033–1042. doi: 10.1016/0092-8674(80)90094-x. [DOI] [PubMed] [Google Scholar]
  12. Fuchs E., Green H. Regulation of terminal differentiation of cultured human keratinocytes by vitamin A. Cell. 1981 Sep;25(3):617–625. doi: 10.1016/0092-8674(81)90169-0. [DOI] [PubMed] [Google Scholar]
  13. Gabbiani G., Schmid E., Winter S., Chaponnier C., de Ckhastonay C., Vandekerckhove J., Weber K., Franke W. W. Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific alpha-type actin. Proc Natl Acad Sci U S A. 1981 Jan;78(1):298–302. doi: 10.1073/pnas.78.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gard D. L., Bell P. B., Lazarides E. Coexistence of desmin and the fibroblastic intermediate filament subunit in muscle and nonmuscle cells: identification and comparative peptide analysis. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3894–3898. doi: 10.1073/pnas.76.8.3894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gard D. L., Lazarides E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell. 1980 Jan;19(1):263–275. doi: 10.1016/0092-8674(80)90408-0. [DOI] [PubMed] [Google Scholar]
  16. Granger B. L., Lazarides E. Desmin and vimentin coexist at the periphery of the myofibril Z disc. Cell. 1979 Dec;18(4):1053–1063. doi: 10.1016/0092-8674(79)90218-6. [DOI] [PubMed] [Google Scholar]
  17. Groudine M., Weintraub H. Rous sarcoma virus activates embryonic globin genes in chicken fibroblasts. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4464–4468. doi: 10.1073/pnas.72.11.4464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hendricks M., Weintraub H. Tropomyosin is decreased in transformed cells. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5633–5637. doi: 10.1073/pnas.78.9.5633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Holtzer H., Bennett G. S., Tapscott S. J., Croop J. M., Toyama Y. Intermediate-size filaments: changes in synthesis and distribution in cells of the myogenic and neurogenic lineages. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):317–329. doi: 10.1101/sqb.1982.046.01.033. [DOI] [PubMed] [Google Scholar]
  20. Hubbard B. D., Lazarides E. Copurification of actin and desmin from chicken smooth muscle and their copolymerization in vitro to intermediate filaments. J Cell Biol. 1979 Jan;80(1):166–182. doi: 10.1083/jcb.80.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hunter T., Garrels J. I. Characterization of the mRNAs for alpha-, beta- and gamma-actin. Cell. 1977 Nov;12(3):767–781. doi: 10.1016/0092-8674(77)90276-8. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Lagacé L., Chandra T., Woo S. L., Means A. R. Identification of multiple species of calmodulin messenger RNA using a full length complementary DNA. J Biol Chem. 1983 Feb 10;258(3):1684–1688. [PubMed] [Google Scholar]
  24. Lazarides E., Granger B. L., Gard D. L., O'Connor C. M., Breckler J., Price M., Danto S. I. Desmin- and vimentin-containing filaments and their role inthe assembly of the Z disk in muscle cells. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):351–378. doi: 10.1101/sqb.1982.046.01.036. [DOI] [PubMed] [Google Scholar]
  25. Lazarides E. Intermediate filaments as mechanical integrators of cellular space. Nature. 1980 Jan 17;283(5744):249–256. doi: 10.1038/283249a0. [DOI] [PubMed] [Google Scholar]
  26. Lazarides E. Intermediate filaments--chemical heterogeneity in differentiation. Cell. 1981 Mar;23(3):649–650. doi: 10.1016/0092-8674(81)90427-x. [DOI] [PubMed] [Google Scholar]
  27. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  28. O'Connor C. M., Balzer D. R., Jr, Lazarides E. Phosphorylation of subunit proteins of intermediate filaments from chicken muscle and nonmuscle cells. Proc Natl Acad Sci U S A. 1979 Feb;76(2):819–823. doi: 10.1073/pnas.76.2.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Osborn M., Weber K. Intermediate filaments: cell-type-specific markers in differentiation and pathology. Cell. 1982 Dec;31(2 Pt 1):303–306. doi: 10.1016/0092-8674(82)90122-2. [DOI] [PubMed] [Google Scholar]
  31. Parnes J. R., Robinson R. R., Seidman J. G. Multiple mRNA species with distinct 3' termini are transcribed from the beta 2-microglobulin gene. 1983 Mar 31-Apr 6Nature. 302(5907):449–452. doi: 10.1038/302449a0. [DOI] [PubMed] [Google Scholar]
  32. Paterson B. M., Bishop J. O. Changes in the mRNA population of chick myoblasts during myogenesis in vitro. Cell. 1977 Nov;12(3):751–765. doi: 10.1016/0092-8674(77)90275-6. [DOI] [PubMed] [Google Scholar]
  33. Pelham H. R., Jackson R. J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem. 1976 Aug 1;67(1):247–256. doi: 10.1111/j.1432-1033.1976.tb10656.x. [DOI] [PubMed] [Google Scholar]
  34. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  35. Quax-Jeuken Y. E., Quax W. J., Bloemendal H. Primary and secondary structure of hamster vimentin predicted from the nucleotide sequence. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3548–3552. doi: 10.1073/pnas.80.12.3548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Rowe D. W., Moen R. C., Davidson J. M., Byers P. H., Bornstein P., Palmiter R. D. Correlation of procollagen mRNA levels in normal and transformed chick embryo fibroblasts with different rates of procollagen synthesis. Biochemistry. 1978 May 2;17(9):1581–1590. doi: 10.1021/bi00602a001. [DOI] [PubMed] [Google Scholar]
  38. Sasavage N. L., Smith M., Gillam S., Woychik R. P., Rottman F. M. Variation in the polyadenylylation site of bovine prolactin mRNA. Proc Natl Acad Sci U S A. 1982 Jan;79(2):223–227. doi: 10.1073/pnas.79.2.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sefton B. M., Hunter T., Ball E. H., Singer S. J. Vinculin: a cytoskeletal target of the transforming protein of Rous sarcoma virus. Cell. 1981 Apr;24(1):165–174. doi: 10.1016/0092-8674(81)90512-2. [DOI] [PubMed] [Google Scholar]
  40. Strohman R. C., Moss P. S., Micou-Eastwood J., Spector D., Przybyla A., Paterson B. Messenger RNA for myosin polypeptides: isolation from single myogenic cell cultures. Cell. 1977 Feb;10(2):265–273. doi: 10.1016/0092-8674(77)90220-3. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Zehner Z. E., Paterson B. M. Characterization of the chicken vimentin gene: single copy gene producing multiple mRNAs. Proc Natl Acad Sci U S A. 1983 Feb;80(4):911–915. doi: 10.1073/pnas.80.4.911. [DOI] [PMC free article] [PubMed] [Google Scholar]

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