Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1985 May 1;100(5):1548–1557. doi: 10.1083/jcb.100.5.1548

Anion transporter: highly cell-type-specific expression of distinct polypeptides and transcripts in erythroid and nonerythroid cells

PMCID: PMC2113867  PMID: 3838751

Abstract

Affinity-purified antibodies and cDNA probes specific for the chicken erythrocyte anion transporter (also referred to as band 3) have been used to demonstrate that this protein is expressed in a highly cell- type-specific manner in the avian kidney. Indirect immunofluorescence analysis indicates that this polypeptide is present in only a small subset of total kidney cells and is predominantly localized to the proximal convoluted tubule of this organ. Chicken erythrocytes synthesize and accumulate two structurally and serologically related band 3 polypeptides. The polypeptide that accumulates in kidney membranes has an apparent molecular weight greater than either of its erythroid counterparts. This diversity is also reflected at the RNA level, as the single band 3 mRNA species detected during various stages of erythroid development is distinct in size from that found in kidney cells. Genomic DNA blot analysis suggests that both the erythroid and kidney band 3 RNAs arise from a single gene. Furthermore, of the adult tissues we have examined that are known to express ankyrin and spectrin polypeptides, only kidney accumulates detectable levels of the band 3 mRNA and polypeptide. These observations suggest that a subset of kidney cells use an anion transport mechanism analogous to that of erythrocytes and that band 3 is expressed in a noncoordinate manner with other components of the erythroid membrane skeleton in nonerythroid cells.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Aster J. C., Welsh M. J., Brewer G. J., Maisel H. Identification of spectrin and protein 4.1-like proteins in mammalian lens. Biochem Biophys Res Commun. 1984 Mar 15;119(2):726–734. doi: 10.1016/s0006-291x(84)80311-3. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Bennett V., Davis J., Fowler W. E. Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin. Nature. 1982 Sep 9;299(5879):126–131. doi: 10.1038/299126a0. [DOI] [PubMed] [Google Scholar]
  4. Bennett V., Stenbuck P. J. The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature. 1979 Aug 9;280(5722):468–473. doi: 10.1038/280468a0. [DOI] [PubMed] [Google Scholar]
  5. Bruns G. A., Ingram V. M. The erythroid cells and haemoglobins of the chick embryo. Philos Trans R Soc Lond B Biol Sci. 1973 Oct 25;266(877):225–305. doi: 10.1098/rstb.1973.0050. [DOI] [PubMed] [Google Scholar]
  6. Burridge K., Kelly T., Mangeat P. Nonerythrocyte spectrins: actin-membrane attachment proteins occurring in many cell types. J Cell Biol. 1982 Nov;95(2 Pt 1):478–486. doi: 10.1083/jcb.95.2.478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Capetanaki Y. G., Ngai J., Flytzanis C. N., Lazarides E. Tissue-specific expression of two mRNA species transcribed from a single vimentin gene. Cell. 1983 Dec;35(2 Pt 1):411–420. doi: 10.1016/0092-8674(83)90174-5. [DOI] [PubMed] [Google Scholar]
  8. Cassoly R., Salhany J. M. Spectral and oxygen-release kinetic properties of human hemoglobin bound to the cytoplasmic fragment of band 3 protein in solution. Biochim Biophys Acta. 1983 Jun 15;745(2):134–139. doi: 10.1016/0167-4838(83)90041-9. [DOI] [PubMed] [Google Scholar]
  9. Davis J. Q., Bennett V. Brain ankyrin. A membrane-associated protein with binding sites for spectrin, tubulin, and the cytoplasmic domain of the erythrocyte anion channel. J Biol Chem. 1984 Nov 10;259(21):13550–13559. [PubMed] [Google Scholar]
  10. Drenckhahn D., Zinke K., Schauer U., Appell K. C., Low P. S. Identification of immunoreactive forms of human erythrocyte band 3 in nonerythroid cells. Eur J Cell Biol. 1984 May;34(1):144–150. [PubMed] [Google Scholar]
  11. Elder J. H., Pickett R. A., 2nd, Hampton J., Lerner R. A. Radioiodination of proteins in single polyacrylamide gel slices. Tryptic peptide analysis of all the major members of complex multicomponent systems using microgram quantities of total protein. J Biol Chem. 1977 Sep 25;252(18):6510–6515. [PubMed] [Google Scholar]
  12. Frizzell R. A., Koch M. J., Schultz S. G. Ion transport by rabbit colon. I. Active and passive components. J Membr Biol. 1976;27(3):297–316. doi: 10.1007/BF01869142. [DOI] [PubMed] [Google Scholar]
  13. Glenney J. R., Jr, Glenney P., Weber K. F-actin-binding and cross-linking properties of porcine brain fodrin, a spectrin-related molecule. J Biol Chem. 1982 Aug 25;257(16):9781–9787. [PubMed] [Google Scholar]
  14. Goodman S. R., Casoria L. A., Coleman D. B., Zagon I. S. Identification and location of brain protein 4.1. Science. 1984 Jun 29;224(4656):1433–1436. doi: 10.1126/science.6374897. [DOI] [PubMed] [Google Scholar]
  15. Goodman S. R., Zagon I. S., Kulikowski R. R. Identification of a spectrin-like protein in nonerythroid cells. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7570–7574. doi: 10.1073/pnas.78.12.7570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Granger B. L., Lazarides E. Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression. Cell. 1984 Jun;37(2):595–607. doi: 10.1016/0092-8674(84)90390-8. [DOI] [PubMed] [Google Scholar]
  17. Granger B. L., Repasky E. A., Lazarides E. Synemin and vimentin are components of intermediate filaments in avian erythrocytes. J Cell Biol. 1982 Feb;92(2):299–312. doi: 10.1083/jcb.92.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hargreaves W. R., Giedd K. N., Verkleij A., Branton D. Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles. J Biol Chem. 1980 Dec 25;255(24):11965–11972. [PubMed] [Google Scholar]
  19. 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]
  20. Jay D. G. Characterization of the chicken erythrocyte anion exchange protein. J Biol Chem. 1983 Aug 10;258(15):9431–9436. [PubMed] [Google Scholar]
  21. Kay M. M., Tracey C. M., Goodman J. R., Cone J. C., Bassel P. S. Polypeptides immunologically related to band 3 are present in nucleated somatic cells. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6882–6886. doi: 10.1073/pnas.80.22.6882. [DOI] [PMC free article] [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. Leslie B. R., Schwartz J. H., Steinmetz P. R. Coupling between Cl- absorption and HCO3- secretion in turtle urinary bladder. Am J Physiol. 1973 Sep;225(3):610–617. doi: 10.1152/ajplegacy.1973.225.3.610. [DOI] [PubMed] [Google Scholar]
  24. Moon R. T., Ngai J., Wold B. J., Lazarides E. Tissue-specific expression of distinct spectrin and ankyrin transcripts in erythroid and nonerythroid cells. J Cell Biol. 1985 Jan;100(1):152–160. doi: 10.1083/jcb.100.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mueller T. J., Morrison M. Detection of a variant of protein 3, the major transmembrane protein of the human erythrocyte. J Biol Chem. 1977 Oct 10;252(19):6573–6576. [PubMed] [Google Scholar]
  26. Nelson W. J., Lazarides E. Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3292–3296. doi: 10.1073/pnas.81.11.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nelson W. J., Lazarides E. The patterns of expression of two ankyrin isoforms demonstrate distinct steps in the assembly of the membrane skeleton in neuronal morphogenesis. Cell. 1984 Dec;39(2 Pt 1):309–320. doi: 10.1016/0092-8674(84)90009-6. [DOI] [PubMed] [Google Scholar]
  28. Pitts R. F., Ayer J. L., Schiess W. A., Miner P. THE RENAL REGULATION OF ACID-BASE BALANCE IN MAN. III. THE REABSORPTION AND EXCRETION OF BICARBONATE. J Clin Invest. 1949 Jan;28(1):35–44. doi: 10.1172/JCI102050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Repasky E. A., Granger B. L., Lazarides E. Widespread occurrence of avian spectrin in nonerythroid cells. Cell. 1982 Jul;29(3):821–833. doi: 10.1016/0092-8674(82)90444-5. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Slater D. W., Slater I., Gillespie D. Post-fertilization synthesis of polyadenylic acid in sea urchin embryos. Nature. 1972 Dec 8;240(5380):333–337. doi: 10.1038/240333a0. [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. Swanson C. H., Solomon A. K. A micropuncture investigation of the whole tissue mechanism of electrolyte secretion by the in vitro rabbit pancreas. J Gen Physiol. 1973 Oct;62(4):407–429. doi: 10.1085/jgp.62.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ullrich K. J., Capasso G., Rumrich G., Papavassiliou F., Klöss S. Coupling between proximal tubular transport processes. Studies with ouabain, SITS and HCO3-free solutions. Pflugers Arch. 1977 Apr 25;368(3):245–252. doi: 10.1007/BF00585203. [DOI] [PubMed] [Google Scholar]
  36. Weise M. J., Chan L. N. Membrane protein synthesis in embryonic chick erythroid cells. J Biol Chem. 1978 Mar 25;253(6):1892–1897. [PubMed] [Google Scholar]
  37. Young R. A., Davis R. W. Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1194–1198. doi: 10.1073/pnas.80.5.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Young R. A., Davis R. W. Yeast RNA polymerase II genes: isolation with antibody probes. Science. 1983 Nov 18;222(4625):778–782. doi: 10.1126/science.6356359. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES