Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1984 Nov;4(11):2279–2288. doi: 10.1128/mcb.4.11.2279

Processed pseudogenes for rat cytochrome c are preferentially derived from one of three alternate mRNAs.

R C Scarpulla
PMCID: PMC369056  PMID: 6096691

Abstract

Three cytochrome c mRNAs (1,400, 1,100 and 700 nucleotides) are colinear with RC4, a gene that has introns and correctly encodes cytochrome c. A comparison of RC4 to six nonallelic clones isolated from the rat cytochrome c multigene family demonstrates that all three mRNAs are represented in the genome as processed pseudogenes. Four of the six pseudogenes are derived from the 1,100-nucleotide mRNA, and genomic hybridizations further establish that nearly all of the 30 or so gene family members are also genomic copies of this mRNA despite the equimolar ratio of the three messages in rat tissues. Thus, the surprising multiplicity of cytochrome c sequences in the rat genome is mainly accounted for by the selective use of the 1,100-nucleotide mRNA for the formation of processed pseudogenes. In contrast to 700- and 1,400-nucleotide species which are polyadenylated downstream from AAGUAAA and AAUUAAA, respectively, the 1,100-nucleotide mRNA uses the ubiquitous AAUAAA and also displays a unique stem and loop structure (delta G = -59.4 kJ) centered 37 base pairs upstream from this sequence.

Full text

PDF

Images in this article

2282Image
on p.2282
2286Image
on p.2286

Selected References

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

  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. Bennetzen J. L., Hall B. D. The primary structure of the Saccharomyces cerevisiae gene for alcohol dehydrogenase. J Biol Chem. 1982 Mar 25;257(6):3018–3025. [PubMed] [Google Scholar]
  3. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  4. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blin N., Stafford D. W. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976 Sep;3(9):2303–2308. doi: 10.1093/nar/3.9.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  7. Chen M. J., Shimada T., Moulton A. D., Harrison M., Nienhuis A. W. Intronless human dihydrofolate reductase genes are derived from processed RNA molecules. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7435–7439. doi: 10.1073/pnas.79.23.7435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  9. Denison R. A., Van Arsdell S. W., Bernstein L. B., Weiner A. M. Abundant pseudogenes for small nuclear RNAs are dispersed in the human genome. Proc Natl Acad Sci U S A. 1981 Feb;78(2):810–814. doi: 10.1073/pnas.78.2.810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hennig B. Change of cytochrome c structure during development of the mouse. Eur J Biochem. 1975 Jun 16;55(1):167–183. doi: 10.1111/j.1432-1033.1975.tb02149.x. [DOI] [PubMed] [Google Scholar]
  11. Hollis G. F., Hieter P. A., McBride O. W., Swan D., Leder P. Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing. Nature. 1982 Mar 25;296(5855):321–325. doi: 10.1038/296321a0. [DOI] [PubMed] [Google Scholar]
  12. Karin M., Richards R. I. Human metallothionein genes--primary structure of the metallothionein-II gene and a related processed gene. Nature. 1982 Oct 28;299(5886):797–802. doi: 10.1038/299797a0. [DOI] [PubMed] [Google Scholar]
  13. Lee M. G., Lewis S. A., Wilde C. D., Cowan N. J. Evolutionary history of a multigene family: an expressed human beta-tubulin gene and three processed pseudogenes. Cell. 1983 Jun;33(2):477–487. doi: 10.1016/0092-8674(83)90429-4. [DOI] [PubMed] [Google Scholar]
  14. Lemischka I., Sharp P. A. The sequences of an expressed rat alpha-tubulin gene and a pseudogene with an inserted repetitive element. Nature. 1982 Nov 25;300(5890):330–335. doi: 10.1038/300330a0. [DOI] [PubMed] [Google Scholar]
  15. Li W. H., Gojobori T., Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981 Jul 16;292(5820):237–239. doi: 10.1038/292237a0. [DOI] [PubMed] [Google Scholar]
  16. Limbach K. J., Wu R. Isolation and characterization of two alleles of the chicken cytochrome c gene. Nucleic Acids Res. 1983 Dec 20;11(24):8931–8950. doi: 10.1093/nar/11.24.8931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Margoliash E., Schejter A. Cytochrome c. Adv Protein Chem. 1966;21:113–286. doi: 10.1016/s0065-3233(08)60128-x. [DOI] [PubMed] [Google Scholar]
  18. Masters J. N., Yang J. K., Cellini A., Attardi G. A human dihydrofolate reductase pseudogene and its relationship to the multiple forms of specific messenger RNA. J Mol Biol. 1983 Jun 15;167(1):23–36. doi: 10.1016/s0022-2836(83)80032-1. [DOI] [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Moore G. W., Goodman M., Callahan C., Holmquist R., Moise H. Stochastic versus augmented maximum parsimony method for estimating superimposed mutations in the divergent evolution of protein sequences. Methods tested on cytochrome c amino acid sequences. J Mol Biol. 1976 Jul 25;105(1):15–37. doi: 10.1016/0022-2836(76)90193-5. [DOI] [PubMed] [Google Scholar]
  22. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nishioka Y., Leder A., Leder P. Unusual alpha-globin-like gene that has cleanly lost both globin intervening sequences. Proc Natl Acad Sci U S A. 1980 May;77(5):2806–2809. doi: 10.1073/pnas.77.5.2806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oxender D. L., Zurawski G., Yanofsky C. Attenuation in the Escherichia coli tryptophan operon: role of RNA secondary structure involving the tryptophan codon region. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5524–5528. doi: 10.1073/pnas.76.11.5524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Sargent T. D., Wu J. R., Sala-Trepat J. M., Wallace R. B., Reyes A. A., Bonner J. The rat serum albumin gene: analysis of cloned sequences. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3256–3260. doi: 10.1073/pnas.76.7.3256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scarpulla R. C., Agne K. M., Wu R. Cytochrome c gene-related sequences in mammalian genomes. Proc Natl Acad Sci U S A. 1982 Feb;79(3):739–743. doi: 10.1073/pnas.79.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Scarpulla R. C., Agne K. M., Wu R. Isolation and structure of a rat cytochrome c gene. J Biol Chem. 1981 Jun 25;256(12):6480–6486. [PubMed] [Google Scholar]
  29. Scarpulla R. C., Wu R. Nonallelic members of the cytochrome c multigene family of the rat may arise through different messenger RNAs. Cell. 1983 Feb;32(2):473–482. doi: 10.1016/0092-8674(83)90467-1. [DOI] [PubMed] [Google Scholar]
  30. Seif I., Khoury G., Dhar R. BKV splice sequences based on analysis of preferred donor and acceptor sites. Nucleic Acids Res. 1979 Jul 25;6(10):3387–3398. doi: 10.1093/nar/6.10.3387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sherman F., Stewart J. W. Genetics and biosynthesis of cytochrome c. Annu Rev Genet. 1971;5:257–296. doi: 10.1146/annurev.ge.05.120171.001353. [DOI] [PubMed] [Google Scholar]
  32. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  33. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  34. Vanin E. F., Goldberg G. I., Tucker P. W., Smithies O. A mouse alpha-globin-related pseudogene lacking intervening sequences. Nature. 1980 Jul 17;286(5770):222–226. doi: 10.1038/286222a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES