Home LiteratureArticle Details
PMID: 2427930 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

RNA-mediated gene duplication: the rat preproinsulin I gene is a functional retroposon.

Molecular and cellular biology ·Vol. 5 ·No. 8 ·1985-08-00 ·Pages 2090-103

Soares MB, Schon E, Henderson A, Karathanasis SK, Cate R, Zeitlin S, Chirgwin J, Efstratiadis A

Abstract

Rats and mice have two, equally expressed, nonallelic genes encoding preproinsulin (genes I and II). Cytological hybridization with metaphase chromosomes indicated that both genes reside on rat chromosome I but are approximately 100,000 kilobases apart. In mice the two genes reside on two different chromosomes. DNA sequence comparisons of the gene-flanking regions in rats and mice indicated that the preproinsulin gene I has lost one of the two introns present in gene II, is flanked by a long (41-base) direct repeat, and has a remnant of a polydeoxyadenylate acid tract preceding the downstream direct repeat. These structural features indicated that gene I was generated by an RNA-mediated duplication-transposition event involving a transcript of gene II which was initiated upstream from the normal capping site. Sequence divergence analysis indicated that the pair of the original gene and its retroposed, but functional, counterpart (which appeared about 35 million years ago) is maintained by strong negative selection operating primarily on the segments encoding the chains of the mature hormone, whereas the segments encoding the parts of the polypeptide that are eliminated during processing and also the introns and the flanking regions are evolving neutrally.

MeSH Terms
Animals Base Sequence Cell Line Chromosome Mapping DNA Replication DNA Restriction Enzymes Genes Globins/genetics Insulin Karyotyping Mice Nucleic Acid Hybridization Proinsulin/genetics Protein Precursors/genetics RNA/genetics Rats Transcription, Genetic
Chemicals
Insulin Protein Precursors preproinsulin RNA Globins Proinsulin DNA Restriction Enzymes
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Soares M B
Schon E
Henderson A
Karathanasis S K
Cate R
Zeitlin S
Chirgwin J
Efstratiadis A
References (65)
65 references, click to expand
  1. Characterization of a mouse somatic cytochrome c gene and three cytochrome c pseudogenes.
    Nucleic Acids Res. 1985 Jan 25;13(2):617-30 PMID: 2987801
  2. The structure and evolution of the two nonallelic rat preproinsulin genes.
    Cell. 1979 Oct;18(2):545-58 PMID: 498284
  3. Sequence of the human insulin gene.
    Nature. 1980 Mar 6;284(5751):26-32 PMID: 6243748
  4. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  5. The evolution of genes: the chicken preproinsulin gene.
    Cell. 1980 Jun;20(2):555-66 PMID: 7388949
  6. Unusual alpha-globin-like gene that has cleanly lost both globin intervening sequences.
    Proc Natl Acad Sci U S A. 1980 May;77(5):2806-9 PMID: 6930668
  7. Genetic variation in the human insulin gene.
    Science. 1980 Aug 1;209(4456):612-5 PMID: 6248962
  8. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini.
    Nucleic Acids Res. 1985 Feb 25;13(4):1347-68 PMID: 2987822
  9. Adenosine deaminase: characterization and expression of a gene with a remarkable promoter.
    EMBO J. 1985 Feb;4(2):437-43 PMID: 3839456
  10. Species variation in the amino acid sequence of insulin.
    Am J Med. 1966 May;40(5):662-6 PMID: 5949593
  11. Insulin biosynthesis in the rat: demonstration of two proinsulins.
    Proc Natl Acad Sci U S A. 1969 Jan;62(1):278-85 PMID: 4890253
  12. Fluorescence banding patterns of the rat chromosomes.
    Chromosoma. 1973;40(2):173-82 PMID: 4118111
  13. An improved banding technique exemplified in the karyotype analysis of two strains of rat.
    Chromosoma. 1973;41(3):259-63 PMID: 4120630
  14. Evolutionary relationships between rat and mouse chromosomes.
    Chromosoma. 1974 Jun 11;46(2):217-24 PMID: 4136731
  15. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  16. Cloning and amplification of alpha and beta mouse globin gene sequences synthesised in vitro.
    Gene. 1977 May;1(3-4):229-39 PMID: 338418
  17. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  18. Interactions between adenovirus, a tumor promoter, and chemical carcinogens in transformation of rat embryo cell cultures.
    Proc Natl Acad Sci U S A. 1978 May;75(5):2311-4 PMID: 276873
  19. A bacterial clone synthesizing proinsulin.
    Proc Natl Acad Sci U S A. 1978 Aug;75(8):3727-31 PMID: 358198
  20. Rat gene mapping by rat-mouse somatic cell hybridization and a comparative Q-banding analysis between rat and mouse chromosomes.
    Cytogenet Cell Genet. 1978;22(1-6):606-9 PMID: 752550
  21. A mouse alpha-globin-related pseudogene lacking intervening sequences.
    Nature. 1980 Jul 17;286(5770):222-6 PMID: 6250049
  22. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855-9 PMID: 6933441
  23. Transforming DNA integrates into the host chromosome.
    Cell. 1981 Jan;23(1):29-39 PMID: 7214526
  24. The highly polymorphic region near the human insulin gene is composed of simple tandemly repeating sequences.
    Nature. 1982 Jan 7;295(5844):31-5 PMID: 7035959
  25. Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts?
    Cell. 1981 Oct;26(2 Pt 2):141-2 PMID: 6277493
  26. Identification of DNA sequences required for transcription of the human alpha 1-globin gene in a new SV40 host-vector system.
    Cell. 1981 Dec;27(2 Pt 1):279-88 PMID: 6277501
  27. Processes of gene duplication.
    Nature. 1982 Mar 4;296(5852):9-10 PMID: 7063011
  28. Variation in the sequence and modification state of the human insulin gene flanking regions.
    Nucleic Acids Res. 1982 Apr 10;10(7):2225-40 PMID: 6283472
  29. Biosynthesis of rat insulins I and II: evidence for differential expression of the two genes.
    Proc Natl Acad Sci U S A. 1982 May;79(9):2803-7 PMID: 7045871
  30. Precise location of two promoters for the beta-lactamase gene of pBR322. S1 mapping of ribonucleic acid isolated from Escherichia coli or synthesized in vitro.
    J Biol Chem. 1982 Aug 10;257(15):9205-10 PMID: 6178738
  31. The ovalbumin gene family. The 5' end region of the X and Y genes.
    J Mol Biol. 1982 Mar 25;156(1):1-19 PMID: 6178832
  32. Repetitive sequences in eukaryotic DNA and their expression.
    Annu Rev Biochem. 1982;51:813-44 PMID: 7051966
  33. Cytological hybridization to mammalian chromosomes.
    Int Rev Cytol. 1982;76:1-46 PMID: 6181006
  34. Heterogeneous initiation regions for transcription of the chicken ovomucoid gene.
    Nucleic Acids Res. 1982 Sep 25;10(18):5553-67 PMID: 6128724
  35. DNA sequence analysis of a Drosophila foldback transposable element rearrangement.
    Mol Gen Genet. 1982;188(1):107-10 PMID: 6294476
  36. Cell-specific expression controlled by the 5'-flanking region of insulin and chymotrypsin genes.
    Nature. 1983 Dec 8-14;306(5943):557-61 PMID: 6358900
  37. Linkage and polymorphism of a gene controlling lactate dehydrogenase in the rat.
    Biochem Genet. 1983 Oct;21(9-10):933-41 PMID: 6661178
  38. Pseudogenes for human U2 small nuclear RNA do not have a fixed site of 3' truncation.
    Nucleic Acids Res. 1984 Feb 10;12(3):1463-71 PMID: 6199740
  39. Long terminal repeat-like elements flank a human immunoglobulin epsilon pseudogene that lacks introns.
    EMBO J. 1982;1(12):1539-44 PMID: 6327276
  40. Processed pseudogenes. Characteristics and evolution.
    Biochim Biophys Acta. 1984 Jul 18;782(3):231-41 PMID: 6733106
  41. The rabbit C family of short, interspersed repeats. Nucleotide sequence determination and transcriptional analysis.
    J Mol Biol. 1984 Jun 15;176(1):1-20 PMID: 6204060
  42. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers.
    Gene. 1982 Oct;19(3):259-68 PMID: 6295879
  43. Cloning and nucleotide sequence analysis of the dog insulin gene. Coded amino acid sequence of canine preproinsulin predicts an additional C-peptide fragment.
    J Biol Chem. 1983 Feb 25;258(4):2357-63 PMID: 6296142
  44. Retroposons defined.
    Nature. 1983 Feb 10;301(5900):460 PMID: 6185851
  45. Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes.
    Nature. 1983 Feb 10;301(5900):471-2 PMID: 6185852
  46. Intronless human dihydrofolate reductase genes are derived from processed RNA molecules.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7435-9 PMID: 6961421
  47. How mammalian RNA returns to its genome.
    Science. 1983 Mar 4;219(4588):1052-4 PMID: 6186029
  48. Three regions upstream from the cap site are required for efficient and accurate transcription of the rabbit beta-globin gene in mouse 3T6 cells.
    Cell. 1983 Mar;32(3):695-706 PMID: 6299573
  49. Common and interchangeable elements in the promoters of genes transcribed by RNA polymerase iii.
    Cell. 1983 Mar;32(3):725-33 PMID: 6299574
  50. A processed gene defining a gene family encoding a human non-muscle tropomyosin.
    J Mol Biol. 1983 Jul 5;167(3):523-37 PMID: 6308263
  51. The tubulins: from DNA to RNA to protein and back again.
    Cell. 1983 Sep;34(2):330-2 PMID: 6193888
  52. Tissue-specific expression of a chicken calmodulin pseudogene lacking intervening sequences.
    Proc Natl Acad Sci U S A. 1983 Nov;80(21):6485-9 PMID: 6579534
  53. Structure of two human beta-actin-related processed genes one of which is located next to a simple repetitive sequence.
    EMBO J. 1983;2(5):757-61 PMID: 6571702
  54. A straight LINE story.
    Nature. 1983 Nov 10-16;306(5939):113-4 PMID: 6196638
  55. Cell-specified expression of a selectable hybrid gene.
    Proc Natl Acad Sci U S A. 1984 Aug;81(15):4657-61 PMID: 6087339
  56. Guinea pig preproinsulin gene: an evolutionary compromise?
    Proc Natl Acad Sci U S A. 1984 Aug;81(16):5046-50 PMID: 6591179
  57. Dispersal process associated with the L1 family of interspersed repetitive DNA sequences.
    J Mol Biol. 1984 Oct 5;178(4):795-813 PMID: 6492166
  58. Genes and pseudogenes for human U2 RNA. Implications for the mechanism of pseudogene formation.
    J Mol Biol. 1984 Oct 25;179(2):157-69 PMID: 6209403
  59. Molecular cloning and characterization of mutant and wild-type human beta-actin genes.
    Mol Cell Biol. 1984 Oct;4(10):1961-9 PMID: 6095033
  60. On the origin of the Alu family of repeated sequences.
    Nature. 1984 Nov 8-14;312(5990):106 PMID: 6209576
  61. Alu sequences are processed 7SL RNA genes.
    Nature. 1984 Nov 8-14;312(5990):171-2 PMID: 6209580
  62. In vivo splicing products of the rabbit beta-globin pre-mRNA.
    Cell. 1984 Dec;39(3 Pt 2):589-602 PMID: 6096012
  63. Processed pseudogenes for rat cytochrome c are preferentially derived from one of three alternate mRNAs.
    Mol Cell Biol. 1984 Nov;4(11):2279-88 PMID: 6096691
  64. alpha-Amanitin-insensitive transcription of mouse beta major-globin 5'-flanking and structural gene sequences correlates with mRNA expression.
    Proc Natl Acad Sci U S A. 1984 Dec;81(24):7782-6 PMID: 6595660
  65. Human genes and pseudogenes for the 7SL RNA component of signal recognition particle.
    EMBO J. 1984 Dec 20;3(13):3303-10 PMID: 6084597
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.5.8.2090-2103.1985
Published
1985-08-00
Pages
2090-103
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC366927
Subset
IM
Databases
GENBANK
J00747, J00748
External Links
PubMed source DOI: 10.1128/mcb.5.8.2090-2103.1985 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2