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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Oct;84(20):7149–7153. doi: 10.1073/pnas.84.20.7149

Multiple tissue-specific sites of transcriptional initiation of the mouse anion antiport gene in erythroid and renal cells.

R R Kopito 1, M A Andersson 1, H F Lodish 1
PMCID: PMC299247  PMID: 3478687

Abstract

Primer extension and nuclease protection analysis were used to map the 5' end of mRNA transcripts of the single gene encoding the mouse erythroid anion-exchange protein, band 3. RNA from induced Friend murine erythroleukemia cells contains transcripts whose 5' ends are heterogeneous but that map to five clustered sites between 146 and 189 nucleotides upstream of the initiator AUG codon. The steady-state level of band 3 mRNA increases markedly following dimethyl sulfoxide-induced differentiation, but the pattern of transcription initiation does not vary. mRNA from anemic and normal mouse spleen exhibits the same pattern, with the addition of another transcript whose 5' end maps to position -260. In contrast, mRNA from mouse kidney has a single predominant transcript, mapping to -260. These data establish that the band 3 gene is expressed in kidney as well as in erythroid cells and suggest the presence of tissue-specific alternate promoter elements within the first exon of the band 3 gene. The nucleotide sequence of 1.7 kilobases of genomic DNA 5' to the first intron of the single-copy mouse band 3 gene, although moderately (G + C)-rich, has no "TATA" or "CAAT" boxes or other homologies with globin or other eukaryotic polymerase II promoter regions.

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Selected References

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  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. Baty D., Barrera-Saldana H. A., Everett R. D., Vigneron M., Chambon P. Mutational dissection of the 21 bp repeat region of the SV40 early promoter reveals that it contains overlapping elements of the early-early and late-early promoters. Nucleic Acids Res. 1984 Jan 25;12(2):915–932. doi: 10.1093/nar/12.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benyajati C., Spoerel N., Haymerle H., Ashburner M. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5' end in different developmental stages. Cell. 1983 May;33(1):125–133. doi: 10.1016/0092-8674(83)90341-0. [DOI] [PubMed] [Google Scholar]
  4. Braell W. A., Lodish H. F. Biosynthesis of the erythrocyte anion transport protein. J Biol Chem. 1981 Nov 10;256(21):11337–11344. [PubMed] [Google Scholar]
  5. Braell W. A., Lodish H. F. The erythrocyte anion transport protein is contranslationally inserted into microsomes. Cell. 1982 Jan;28(1):23–31. doi: 10.1016/0092-8674(82)90371-3. [DOI] [PubMed] [Google Scholar]
  6. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  7. Chang H., Langer P. J., Lodish H. F. Asynchronous synthesis of erythrocyte membrane proteins. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3206–3210. doi: 10.1073/pnas.73.9.3206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charnay P., Mellon P., Maniatis T. Linker scanning mutagenesis of the 5'-flanking region of the mouse beta-major-globin gene: sequence requirements for transcription in erythroid and nonerythroid cells. Mol Cell Biol. 1985 Jun;5(6):1498–1511. doi: 10.1128/mcb.5.6.1498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Choi O. R., Engel J. D. A 3' enhancer is required for temporal and tissue-specific transcriptional activation of the chicken adult beta-globin gene. Nature. 1986 Oct 23;323(6090):731–734. doi: 10.1038/323731a0. [DOI] [PubMed] [Google Scholar]
  11. Crouse G. F., Simonsen C. C., McEwan R. N., Schimke R. T. Structure of amplified normal and variant dihydrofolate reductase genes in mouse sarcoma S180 cells. J Biol Chem. 1982 Jul 10;257(13):7887–7897. [PubMed] [Google Scholar]
  12. Demuth D. R., Showe L. C., Ballantine M., Palumbo A., Fraser P. J., Cioe L., Rovera G., Curtis P. J. Cloning and structural characterization of a human non-erythroid band 3-like protein. EMBO J. 1986 Jun;5(6):1205–1214. doi: 10.1002/j.1460-2075.1986.tb04348.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drenckhahn D., Schlüter K., Allen D. P., Bennett V. Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney. Science. 1985 Dec 13;230(4731):1287–1289. doi: 10.1126/science.2933809. [DOI] [PubMed] [Google Scholar]
  14. Dynan W. S., Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 1983 Nov;35(1):79–87. doi: 10.1016/0092-8674(83)90210-6. [DOI] [PubMed] [Google Scholar]
  15. Everett R. D., Baty D., Chambon P. The repeated GC-rich motifs upstream from the TATA box are important elements of the SV40 early promoter. Nucleic Acids Res. 1983 Apr 25;11(8):2447–2464. doi: 10.1093/nar/11.8.2447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fischer J. A., Maniatis T. Regulatory elements involved in Drosophila Adh gene expression are conserved in divergent species and separate elements mediate expression in different tissues. EMBO J. 1986 Jun;5(6):1275–1289. doi: 10.1002/j.1460-2075.1986.tb04357.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Giguére V., Isobe K., Grosveld F. Structure of the murine Thy-1 gene. EMBO J. 1985 Aug;4(8):2017–2024. doi: 10.1002/j.1460-2075.1985.tb03886.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Green M. R., Roeder R. G. Definition of a novel promoter for the major adenovirus-associated virus mRNA. Cell. 1980 Nov;22(1 Pt 1):231–242. doi: 10.1016/0092-8674(80)90171-3. [DOI] [PubMed] [Google Scholar]
  19. Jay D., Cantley L. Structural aspects of the red cell anion exchange protein. Annu Rev Biochem. 1986;55:511–538. doi: 10.1146/annurev.bi.55.070186.002455. [DOI] [PubMed] [Google Scholar]
  20. Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
  21. Kopito R. R., Andersson M., Lodish H. F. Structure and organization of the murine band 3 gene. J Biol Chem. 1987 Jun 15;262(17):8035–8040. [PubMed] [Google Scholar]
  22. Kopito R. R., Lodish H. F. Primary structure and transmembrane orientation of the murine anion exchange protein. Nature. 1985 Jul 18;316(6025):234–238. doi: 10.1038/316234a0. [DOI] [PubMed] [Google Scholar]
  23. Kopito R. R., Lodish H. F. Structure of the murine anion exchange protein. J Cell Biochem. 1985;29(1):1–17. doi: 10.1002/jcb.240290102. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Marks P. A., Rifkind R. A. Erythroleukemic differentiation. Annu Rev Biochem. 1978;47:419–448. doi: 10.1146/annurev.bi.47.070178.002223. [DOI] [PubMed] [Google Scholar]
  26. McKnight S. L., Kingsbury R. Transcriptional control signals of a eukaryotic protein-coding gene. Science. 1982 Jul 23;217(4557):316–324. doi: 10.1126/science.6283634. [DOI] [PubMed] [Google Scholar]
  27. Melton D. W., Konecki D. S., Brennand J., Caskey C. T. Structure, expression, and mutation of the hypoxanthine phosphoribosyltransferase gene. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2147–2151. doi: 10.1073/pnas.81.7.2147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Patel V. P., Lodish H. F. Loss of adhesion of murine erythroleukemia cells to fibronectin during erythroid differentiation. Science. 1984 Jun 1;224(4652):996–998. doi: 10.1126/science.6585955. [DOI] [PubMed] [Google Scholar]
  29. Periasamy M., Strehler E. E., Garfinkel L. I., Gubits R. M., Ruiz-Opazo N., Nadal-Ginard B. Fast skeletal muscle myosin light chains 1 and 3 are produced from a single gene by a combined process of differential RNA transcription and splicing. J Biol Chem. 1984 Nov 10;259(21):13595–13604. [PubMed] [Google Scholar]
  30. Reynolds G. A., Goldstein J. L., Brown M. S. Multiple mRNAs for 3-hydroxy-3-methylglutaryl coenzyme A reductase determined by multiple transcription initiation sites and intron splicing sites in the 5'-untranslated region. J Biol Chem. 1985 Aug 25;260(18):10369–10377. [PubMed] [Google Scholar]
  31. Sabban E., Marchesi V., Adesnik M., Sabatini D. D. Erythrocyte membrane protein band 3: its biosynthesis and incorporation into membranes. J Cell Biol. 1981 Dec;91(3 Pt 1):637–646. doi: 10.1083/jcb.91.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schibler U., Hagenbüchle O., Wellauer P. K., Pittet A. C. Two promoters of different strengths control the transcription of the mouse alpha-amylase gene Amy-1a in the parotid gland and the liver. Cell. 1983 Jun;33(2):501–508. doi: 10.1016/0092-8674(83)90431-2. [DOI] [PubMed] [Google Scholar]
  33. Schuster V. L., Bonsib S. M., Jennings M. L. Two types of collecting duct mitochondria-rich (intercalated) cells: lectin and band 3 cytochemistry. Am J Physiol. 1986 Sep;251(3 Pt 1):C347–C355. doi: 10.1152/ajpcell.1986.251.3.C347. [DOI] [PubMed] [Google Scholar]
  34. Shaw P., Sordat B., Schibler U. The two promoters of the mouse alpha-amylase gene Amy-1a are differentially activated during parotid gland differentiation. Cell. 1985 Apr;40(4):907–912. doi: 10.1016/0092-8674(85)90350-2. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Tjian R. T antigen binding and the control of SV40 gene expression. Cell. 1981 Oct;26(1 Pt 1):1–2. doi: 10.1016/0092-8674(81)90026-x. [DOI] [PubMed] [Google Scholar]
  37. Valerio D., Duyvesteyn M. G., Dekker B. M., Weeda G., Berkvens T. M., van der Voorn L., van Ormondt H., van der Eb A. J. Adenosine deaminase: characterization and expression of a gene with a remarkable promoter. EMBO J. 1985 Feb;4(2):437–443. doi: 10.1002/j.1460-2075.1985.tb03648.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vigneron M., Barrera-Saldana H. A., Baty D., Everett R. E., Chambon P. Effect of the 21-bp repeat upstream element on in vitro transcription from the early and late SV40 promoters. EMBO J. 1984 Oct;3(10):2373–2382. doi: 10.1002/j.1460-2075.1984.tb02142.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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