Skip to main content
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
. 1985 Aug;82(15):5175–5179. doi: 10.1073/pnas.82.15.5175

Carbonic anhydrase is aberrantly and constitutively expressed in both human and murine erythroleukemia cells.

S R Frankel, J Walloch, R K Hirata, M C Bondurant, R Villanueva, S C Weil
PMCID: PMC390522  PMID: 3927299

Abstract

The levels of the erythrocyte proteins carbonic anhydrase (CA) and hemoglobin (Hb) change coordinately during human ontogeny. To further probe the coordinate gene expression of these two proteins in vitro, we used an immunoblotting technique to measure their levels during erythroid differentiation in normal human and murine erythroid progenitors, in human and murine erythroleukemia cells, and in normal murine erythroid progenitors infected with Friend virus. Levels of CA and Hb seem to gradually increase in normal differentiating stem cells. In contrast, both human and murine erythroleukemia cells show high levels of CA, but not of Hb, prior to induction of differentiation. Friend virus infection of normal murine progenitors appears to stimulate CA synthesis as an initial and integral step in transformation. In addition, both the erythroleukemia cells and the erythroid progenitors transformed with Friend virus seem to contain much higher levels of CA than Hb during the early stages of differentiation. This relationship is in marked contrast to normal erythroid differentiation, in which Hb levels are always higher than CA levels. Thus, neoplastic transformation seems to be associated with aberrant production of CA that does not correspond to a maturation arrest of the normal differentiation sequence.

Full text

PDF
5175

Images in this article

Selected References

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

  1. Boyer S. H., Siegel S., Noyes A. N. Developmental changes in human erythrocyte carbonic anhydrase levels: coordinate expression with adult hemoglobin. Dev Biol. 1983 May;97(1):250–253. doi: 10.1016/0012-1606(83)90083-0. [DOI] [PubMed] [Google Scholar]
  2. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  3. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  4. Carter N. D., Heath R., Welty R. J., Hewett-Emmett D., Jeffery S., Shiels A., Tashian R. E. Red cells genetically deficient in carbonic anhydrase II have elevated levels of a carbonic anhydrase indistinguishable from muscle CA III. Ann N Y Acad Sci. 1984;429:284–286. doi: 10.1111/j.1749-6632.1984.tb12351.x. [DOI] [PubMed] [Google Scholar]
  5. Clarke B. J., Brickenden A. M., Ives R. A., Chui D. H. Effect of modulators of erythropoiesis on the hemoglobinization of human erythroid cell cultures. Blood. 1982 Aug;60(2):346–351. [PubMed] [Google Scholar]
  6. Classification of acute leukemia. Ann Intern Med. 1977 Dec;87(6):740–753. doi: 10.7326/0003-4819-87-6-740. [DOI] [PubMed] [Google Scholar]
  7. Conscience J. F., Meier W. Coordinate expression of erythroid marker enzymes during dimethylsulfoxide-induced differentiation of Friend erythroleukemia cells. Exp Cell Res. 1980 Jan;125(1):111–119. doi: 10.1016/0014-4827(80)90195-0. [DOI] [PubMed] [Google Scholar]
  8. Conscience J. F., Miller R. A., Henry J., Ruddle F. H. Acetylcholinesterase, carbonic anhydrase and catalase activity in Friend erythroleukemic cells, non-erythroid mouse cell lines and their somatic hybrids. Exp Cell Res. 1977 Mar 15;105(2):401–412. doi: 10.1016/0014-4827(77)90137-9. [DOI] [PubMed] [Google Scholar]
  9. Curtis P. J. Cloning of mouse carbonic anhydrase mRNA and its induction in mouse erythroleukemic cells. J Biol Chem. 1983 Apr 10;258(7):4459–4463. [PubMed] [Google Scholar]
  10. Debuire B., Henry C., Bernissa M., Biserte G., Claverie J. M., Saule S., Martin P., Stehelin D. Sequencing the erbA gene of avian erythroblastosis virus reveals a new type of oncogene. Science. 1984 Jun 29;224(4656):1456–1459. doi: 10.1126/science.6328658. [DOI] [PubMed] [Google Scholar]
  11. Denton M. J., Spencer N., Arnstein H. R. Biochemical and enzymic changes during erythrocyte differentiation. The significance of the final cell division. Biochem J. 1975 Jan;146(1):205–211. doi: 10.1042/bj1460205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dreyfuss G., Adam S. A., Choi Y. D. Physical change in cytoplasmic messenger ribonucleoproteins in cells treated with inhibitors of mRNA transcription. Mol Cell Biol. 1984 Mar;4(3):415–423. doi: 10.1128/mcb.4.3.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hewett-Emmett D., Hopkins P. J., Tashian R. E., Czelusniak J. Origins and molecular evolution of the carbonic anhydrase isozymes. Ann N Y Acad Sci. 1984;429:338–358. doi: 10.1111/j.1749-6632.1984.tb12359.x. [DOI] [PubMed] [Google Scholar]
  14. Iscove N. N., Sieber F. Erythroid progenitors in mouse bone marrow detected by macroscopic colony formation in culture. Exp Hematol. 1975 Jan;3(1):32–43. [PubMed] [Google Scholar]
  15. Kabat D., Sherton C. C., Evans L. H., Bigley R., Koler R. D. Synthesis of erythrocyte-specific proteins in cultured friend leukemia cells. Cell. 1975 Jul;5(3):331–338. doi: 10.1016/0092-8674(75)90109-9. [DOI] [PubMed] [Google Scholar]
  16. Koury M. J., Bondurant M. C., Duncan D. T., Krantz S. B., Hankins W. D. Specific differentiation events induced by erythropoietin in cells infected in vitro with the anemia strain of Friend virus. Proc Natl Acad Sci U S A. 1982 Jan;79(2):635–639. doi: 10.1073/pnas.79.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Martin P., Papayannopoulou T. HEL cells: a new human erythroleukemia cell line with spontaneous and induced globin expression. Science. 1982 Jun 11;216(4551):1233–1235. doi: 10.1126/science.6177045. [DOI] [PubMed] [Google Scholar]
  19. McLeod D. L., Shreeve M. M., Axelrad A. A. Improved plasma culture system for production of erythrocytic colonies in vitro: quantitative assay method for CFU-E. Blood. 1974 Oct;44(4):517–534. [PubMed] [Google Scholar]
  20. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  21. Omine M., Iwata N., Maekawa T., Ohba Y. A case of juvenile erythroleukemia with uncoordinated expression of fetal red cell markers. Acta Haematol. 1983;69(4):275–277. doi: 10.1159/000206904. [DOI] [PubMed] [Google Scholar]
  22. Scher W., Parkes J., Friend C. Increased carbonic anhydrase activity in Friend erythroleukemia cells during DMSO-stimulated erythroid differentiation and its inhibition by BrdU. Cell Differ. 1977 Dec;6(5-6):285–296. doi: 10.1016/0045-6039(77)90003-3. [DOI] [PubMed] [Google Scholar]
  23. Stern R. H., Boyer S. H., Conscience J. F., Friend C., Margolet L., Tashian R. E., Ruddle F. H. Carbonic anhydrase isozymes in cultured Friend leukemic cells (39873). Proc Soc Exp Biol Med. 1977 Oct;156(1):52–55. doi: 10.3181/00379727-156-39873. [DOI] [PubMed] [Google Scholar]
  24. Stern R. H., Tashian R. E. Thyroid status and carbonic anhydrase levels in mouse erythroyctes. Proc Soc Exp Biol Med. 1976 Oct;153(1):143–146. doi: 10.3181/00379727-153-39497. [DOI] [PubMed] [Google Scholar]
  25. Taub R., Kirsch I., Morton C., Lenoir G., Swan D., Tronick S., Aaronson S., Leder P. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7837–7841. doi: 10.1073/pnas.79.24.7837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Volloch V., Housman D. Terminal differentiation of murine erythroleukemia cells: physical stabilization of end-stage cells. J Cell Biol. 1982 May;93(2):390–394. doi: 10.1083/jcb.93.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Weil S. C., Walloch J., Frankel S. R., Hirata R. K. Expression of carbonic anhydrase and globin during erythropoiesis in vitro. Ann N Y Acad Sci. 1984;429:335–337. doi: 10.1111/j.1749-6632.1984.tb12358.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES