Abstract
The multigene family which codes for the mouse major urinary proteins consists of about 35 genes. Most of these are members of two distinct groups, group 1 and group 2. The group 1 and group 2 genes are organized in head-to-head pairs within 12 to 15 remarkably uniform chromosomal units or domains about 45 kilobase pairs (kb) in size. The 45-kb units are located on chromosome 4, and many of them are adjacent to each other. We propose that the 45-kb unit is a unit both of organization and of evolutionary change. In this study the homologies within the unit were observed by examining, in an electron microscope, heteroduplex and foldback structures made from cloned major urinary protein genes. These show that the 45-kb unit is a gigantic imperfect palindrome. Each arm of the palindrome contains two regions of inverted symmetry of 9.5 and 4.5 kb separated by a 3-kb nonsymmetrical region. We argue that the nonsymmetrical regions arose by a series of deletion events in the two arms of the palindrome. The center of the 45-kb unit is an 8-kb sequence without inverted symmetry flanked by the 9.5-kb regions, which contain the 4-kb genes and their immediate 5' and 3' flanking regions. The junction between adjacent 45-kb units is a 2- to 4-kb sequence without inverted symmetry flanked by the 4.5-kb regions. Some of the 45-kb units are arranged as direct tandem repeats. Others appear to be in inverted orientation with respect to a neighboring unit. Cloned major urinary protein genes show few incidences of the repetitive elements B1, B2, R, and MIF. Two elements, a B1 and an R, may be a constant feature of the 45-kb units. If so, in those cases in which the units are in tandem array, both of these elements will occur with a 45-kb periodicity. A comparison of corresponding parts of different 45-kb units shows that they differ because of a number of deletion or insertion events, particularly in the regions 3' to the genes.
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- Bennett K. L., Hill R. E., Pietras D. F., Woodworth-Gutai M., Kane-Haas C., Houston J. M., Heath J. K., Hastie N. D. Most highly repeated dispersed DNA families in the mouse genome. Mol Cell Biol. 1984 Aug;4(8):1561–1571. doi: 10.1128/mcb.4.8.1561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bennett K. L., Lalley P. A., Barth R. K., Hastie N. D. Mapping the structural genes coding for the major urinary proteins in the mouse: combined use of recombinant inbred strains and somatic cell hybrids. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1220–1224. doi: 10.1073/pnas.79.4.1220. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bishop J. O., Clark A. J., Clissold P. M., Hainey S., Francke U. Two main groups of mouse major urinary protein genes, both largely located on chromosome 4. EMBO J. 1982;1(5):615–620. doi: 10.1002/j.1460-2075.1982.tb01217.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown S. D., Dover G. Organization and evolutionary progress of a dispersed repetitive family of sequences in widely separated rodent genomes. J Mol Biol. 1981 Aug 25;150(4):441–466. doi: 10.1016/0022-2836(81)90374-0. [DOI] [PubMed] [Google Scholar]
- Cheng S. M., Schildkraut C. L. A family of moderately repetitive sequences in mouse DNA. Nucleic Acids Res. 1980 Sep 25;8(18):4075–4090. doi: 10.1093/nar/8.18.4075. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chow L. T., Roberts J. M., Lewis J. B., Broker T. R. A map of cytoplasmic RNA transcripts from lytic adenovirus type 2, determined by electron microscopy of RNA:DNA hybrids. Cell. 1977 Aug;11(4):819–836. doi: 10.1016/0092-8674(77)90294-x. [DOI] [PubMed] [Google Scholar]
- Clark A. J., Clissold P. M., Al Shawi R., Beattie P., Bishop J. Structure of mouse major urinary protein genes: different splicing configurations in the 3'-non-coding region. EMBO J. 1984 May;3(5):1045–1052. doi: 10.1002/j.1460-2075.1984.tb01925.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. J., Clissold P. M., Bishop J. O. Variation between mouse major urinary protein genes isolated from a single inbred line. Gene. 1982 Jun;18(3):221–230. doi: 10.1016/0378-1119(82)90159-7. [DOI] [PubMed] [Google Scholar]
- Clark A. J., Hickman J., Bishop J. A 45-kb DNA domain with two divergently orientated genes is the unit of organisation of the murine major urinary protein genes. EMBO J. 1984 Sep;3(9):2055–2064. doi: 10.1002/j.1460-2075.1984.tb02091.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clissold P. M., Bishop J. O. Variation in mouse major urinary protein (MUP) genes and the MUP gene products within and between inbred lines. Gene. 1982 Jun;18(3):211–220. doi: 10.1016/0378-1119(82)90158-5. [DOI] [PubMed] [Google Scholar]
- Clissold P. M., Hainey S., Bishop J. O. Messenger RNAs coding for mouse major urinary proteins are differentially induced by testosterone. Biochem Genet. 1984 Apr;22(3-4):379–387. doi: 10.1007/BF00484236. [DOI] [PubMed] [Google Scholar]
- Finlayson J. S., Potter M., Shinnick C. S., Smithies O. Components of the major urinary protein complex of inbred mice: determination of NH2-terminal sequences and comparison with homologous components from wild mice. Biochem Genet. 1974 Apr;11(4):325–335. doi: 10.1007/BF00486000. [DOI] [PubMed] [Google Scholar]
- Harshey R. M., Bukhari A. I. A mechanism of DNA transposition. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1090–1094. doi: 10.1073/pnas.78.2.1090. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heller R., Arnheim N. Structure and organization of the highly repeated and interspersed 1.3 kb EcoRI-Bg1II sequence family in mice. Nucleic Acids Res. 1980 Nov 11;8(21):5031–5042. doi: 10.1093/nar/8.21.5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knopf J. L., Gallagher J. F., Held W. A. Differential, multihormonal regulation of the mouse major urinary protein gene family in the liver. Mol Cell Biol. 1983 Dec;3(12):2232–2240. doi: 10.1128/mcb.3.12.2232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krauter K., Leinwand L., D'Eustachio P., Ruddle F., Darnell J. E., Jr Structural genes of the mouse major urinary protein are on chromosome 4. J Cell Biol. 1982 Aug;94(2):414–417. doi: 10.1083/jcb.94.2.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krayev A. S., Kramerov D. A., Skryabin K. G., Ryskov A. P., Bayev A. A., Georgiev G. P. The nucleotide sequence of the ubiquitous repetitive DNA sequence B1 complementary to the most abundant class of mouse fold-back RNA. Nucleic Acids Res. 1980 Mar 25;8(6):1201–1215. doi: 10.1093/nar/8.6.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krayev A. S., Markusheva T. V., Kramerov D. A., Ryskov A. P., Skryabin K. G., Bayev A. A., Georgiev G. P. Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B2 sequencing. Nucleic Acids Res. 1982 Dec 11;10(23):7461–7475. doi: 10.1093/nar/10.23.7461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lueders K. K., Paterson B. M. A short interspersed repetitive element found near some mouse structural genes. Nucleic Acids Res. 1982 Dec 11;10(23):7715–7729. doi: 10.1093/nar/10.23.7715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meunier-Rotival M., Soriano P., Cuny G., Strauss F., Bernardi G. Sequence organization and genomic distribution of the major family of interspersed repeats of mouse DNA. Proc Natl Acad Sci U S A. 1982 Jan;79(2):355–359. doi: 10.1073/pnas.79.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roeder G. S., Fink G. R. DNA rearrangements associated with a transposable element in yeast. Cell. 1980 Aug;21(1):239–249. doi: 10.1016/0092-8674(80)90131-2. [DOI] [PubMed] [Google Scholar]
- Shaw P. H., Held W. A., Hastie N. D. The gene family for major urinary proteins: expression in several secretory tissues of the mouse. Cell. 1983 Mar;32(3):755–761. doi: 10.1016/0092-8674(83)90061-2. [DOI] [PubMed] [Google Scholar]
- Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]