Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

The carbonic anhydrase I locus contains a c-Myb target promoter and modulates differentiation of murine erythroleukemia cells

Oncogene volume 25, pages 2758–2772 (2006)Cite this article

Abstract

The Myb proto-oncogene encodes a transcription factor (c-Myb) that is essential for normal hematopoiesis and is thought to regulate hematopoietic cell proliferation and differentiation by regulating expression of specific target genes. We identify the mouse erythroid-specific carbonic anhydrase I promoter (CAIe) as a target of c-Myb activity and demonstrate that Myb activity is critical for carbonic anhydrase I (CAI) expression in C19 MEL cells. CAI expression is downregulated when MEL cells differentiate in response to MEnT or treatment with N, N-hexamethylene bisacetamide (HMBA). Coexpression of GATA-1 with c-Myb results in synergistic activation of transcription from the CAIe promoter and both transcription factors interact with the CAIe promoter in vivo. We identify a novel 20 bp sequence in the CAIe promoter that is sufficient to mediate synergistic activation of the CAIe promoter by c-Myb and GATA-1. c-Myb and GATA-1 interact with this DNA sequence suggesting that c-Myb and GATA-1 may be contained in a complex that interacts with this region of the CAIe promoter. Forced expression of CAI delayed HMBA-induced differentiation of MEL cells and maintained them in a proliferating state. These data strongly suggest that CAI is a c-Myb target and is involved in regulating MEL cell proliferation and differentiation.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  • Allen RD, Bender TP, Siu G . (1999). Genes Dev 13: 1073–1078.

  • Aziz N, Miglarese MR, Hendrickson RC, Shabanowitz J, Sturgill T, Hunt D et al. (1995). Proc Natl Acad Sci USA 92: 6429–6433.

  • Badiani P, Corbella P, Kioussis D, Marvel J, Weston K . (1994). Genes Dev 8: 770–782.

  • Bender TP, Kremer CS, Kraus M, Buch T, Rajewsky K . (2004). Nat Immunol 5: 721–729.

  • Bender TP, Kuehl WM . (1986). Proc Natl Acad Sci USA 83: 3204–3208.

  • Beug H, Bauer A, Dolznig H, von Lindern M, Lobmayer L, Mellitzer G et al. (1996). Biochim Biophys Acta 1288: M35–M47.

  • Brady HJ, Lowe N, Sowden JC, Edwards M, Butterworth PH . (1991). Biochem J 277: 903–905.

  • Brady HJ, Sowden JC, Edwards M, Lowe N, Butterworth PH . (1989). FEBS Lett 257: 451–456.

  • Burk O, Worpenberg S, Haenig B, Klempnauer KH . (1997). EMBO J 16: 1371–1380.

  • Busfield SJ, Spadaccini A, Riches KJ, Tilbrook PA, Klinken SP . (1995). Eur J Biochem 230: 475–480.

  • Cardone RA, Casavola V, Reshkin SJ . (2005). Nat Rev Cancer 5: 786–795.

  • Chen J, Kremer CS, Bender TP . (2002). Oncogene 21: 1859–1869.

  • Ciana P, Braliou GG, Demay FG, von Lindern M, Barettino D, Beug H et al. (1998). EMBO J 17: 7382–7394.

  • Clarke MF, Kukowska-Latallo JF, Westin E, Smith M, Prochownik EV . (1988). Mol Cell Biol 8: 884–892.

  • Cuddihy AE, Brents LA, Aziz N, Bender TP, Kuehl WM . (1993). Mol Cell Biol 13: 3505–3513.

  • Disela C, Glineur C, Bugge T, Sap J, Stengl G, Dodgson J et al. (1991). Genes Dev 5: 2033–2047.

  • Emambokus N, Vegiopoulos A, Harman B, Jenkinson E, Anderson G, Frampton J . (2003). EMBO J 22: 4478–4488.

  • Endo T, Ishibashi Y, Okana H, Fukumaki Y . (1994). Leuk Res 18: 49–54.

  • Evans JL, Moore TL, Kuehl WM, Bender TP, Ting JP . (1990). Mol Cell Biol 10: 5747–5752.

  • Fraser P, Cummings P, Curtis P . (1989). Mol Cell Biol 9: 3308–3313.

  • Fraser PJ, Curtis PJ . (1986). J Mol Evol 23: 294–299.

  • Fraser PJ, Curtis PJ . (1987). Genes Dev 1: 855–861.

  • Friend C, Scher W, Holland JG, Sato T . (1971). Proc Natl Acad Sci USA 68: 378–382.

  • Fuerstenberg S, Leitner I, Schroeder C, Schwarz H, Vennstrom B, Beug H . (1992). EMBO J 11: 3355–3365.

  • Ganter B, Lipsick JS . (1997). Oncogene 15: 193–202.

  • Golay J, Capucci A, Arsura M, Castellano M, Rizzo V, Introna M . (1991). Blood 77: 149–158.

  • Golay J, Luppi M, Songia S, Palvarini C, Lombardi L, Aiello A et al. (1996). Blood 87: 1900–1911.

  • Gonda TJ, Metcalf D . (1984). Nature 310: 249–251.

  • Graf T . (1992). Curr Opin Genet Dev 2: 249–255.

  • Henry R . (1996). Annu Rev Physiol 58: 523–538.

  • Inoue T, Kimura T, Azuma C, Inazawa J, Takemura M, Kikuchi T et al. (1994). J Biol Chem 269: 32451–32456.

  • Kanei-Ishii C, Tanikawa J, Nakai A, Morimoto RI, Ishii S . (1997). Science 277: 246–248.

  • Kirsch IR, Bertness V, Silver J, Hollis GF . (1986). J Cell Biochem 32: 11–21.

  • Lang G, White JR, Argent-Katwala MJ, Allinson CG, Weston K . (2005). Oncogene 24: 1375–1384.

  • Latchman DS . (1993). Transcription Factors: a Practical Approach. IRL Press: New York.

    Google Scholar 

  • Leverson JD, Koskinen PJ, Orrico FC, Rainio EM, Jalkanen KJ, Dash AB et al. (1998). Mol Cell 2: 417–425.

  • Liao SY, Aurelio ON, Jan K, Zavada J, Stanbridge EJ . (1997). Cancer Res 57: 2827–2831.

  • Lipsick JS . (1996). Oncogene 13: 223–235.

  • Lowe N, Brady HJ, Barlow JH, Sowden JC, Edwards M, Butterworth PH . (1990). Gene 93: 277–283.

  • Marks PA, Ramsay R, Sheffery M, Rifkind RA . (1987). Prog Clin Biol Res 251: 253–268.

  • Marks PA, Rifkind RA . (1978). Annu Rev Biochem 47: 419–448.

  • Martinez-Zaguilan R, Seftor EA, Seftor RE, Chu YW, Gillies RJ, Hendrix MJ . (1996). Clin Exp Metast 14: 176–186.

  • McAdams TA, Miller WM, Papoutsakis ET . (1998). Br J Haematol 103: 317–325.

  • McClinton D, Stafford J, Brents L, Bender TP, Kuehl WM . (1990). Mol Cell Biol 10: 705–710.

  • Melotti P, Calabretta B . (1994). J Biol Chem 269: 25303–25309.

  • Melotti P, Ku DH, Calabretta B . (1994). J Exp Med 179: 1023–1028.

  • Miglarese MR, Richardson AF, Aziz N, Bender TP . (1996). J Biol Chem 271: 22697–22705.

  • Mucenski ML, McLain K, Kier AB, Swerdlow SH, Schreiner CM, Miller TA et al. (1991). Cell 65: 677–689.

  • Ness SA . (1999). Oncogene 18: 3039–3046.

  • Ness SA, Kowenz-Leutz E, Casini T, Graf T, Leutz A . (1993). Genes Dev 7: 749–759.

  • Ness SA, Marknell A, Graf T . (1989). Cell 59: 1115–1125.

  • Nomura N, Takahashi M, Matsui M, Ishii S, Date T, Sasamoto S et al. (1988). Nucleic Acids Res 16: 11075–11089.

  • Nuchprayoon I, Simkevich CP, Luo M, Friedman AD, Rosmarin AG . (1997). Blood 89: 4546–4554.

  • Oelgeschlager M, Nuchprayoon I, Luscher B, Friedman AD . (1996). Mol Cell Biol 16: 4717–4725.

  • Oh IH, Reddy EP . (1999). Oncogene 18: 3017–3033.

  • Parkkila S, Rajaniemi H, Parkkila AK, Kivela J, Waheed A, Pastorekova S et al. (2000). Proc Natl Acad Sci USA 97: 2220–2224.

  • Pastorekova S, Parkkila S, Pastorek J, Supuran CT . (2004). J Enzyme Inhib Med Chem 19: 199–229.

  • Radke K, Beug H, Kornfeld S, Graf T . (1982). Cell 31: 643–653.

  • Ratajczak MZ, Perrotti D, Melotti P, Powzaniuk M, Calabretta B, Onodera K et al. (1998). Blood 91: 1934–1946.

  • Reiss K, Travali S, Calabretta B, Baserga R . (1991). J Cell Physiol 148: 338–343.

  • Rushton JJ, Davis LM, Lei W, Mo X, Leutz A, Ness SA . (2003). Oncogene 22: 308–313.

  • Scher W, Parkes J, Friend C . (1977). Cell Differ 6: 285–296.

  • Schmidt M, Nazarov V, Stevens L, Watson R, Wolff L . (2000). Mol Cell Biol 20: 1970–1981.

  • Shapiro LH . (1995). J Biol Chem 270: 8763–8771.

  • Siu G, Wurster AL, Lipsick JS, Hedrick SM . (1992). Mol Cell Biol 12: 1592–1604.

  • Sowden J, Leigh S, Talbot I, Delhanty J, Edwards Y . (1993). Differentiation 53: 67–74.

  • Takahashi T, Suwabe N, Dai P, Yamamoto M, Ishii S, Nakano T . (2000). Oncogene 19: 134–140.

  • Tashian RE . (1989). BioEssays 10: 186–192.

  • Tureci O, Sahin U, Vollmar E, Siemer S, Gottert E, Seitz G et al. (1998). Proc Natl Acad Sci USA 95: 7608–7613.

  • Webb SD, Sherratt JA, Fish RG . (1999). J Theor Biol 196: 237–250.

  • Westin EH, Gallo RC, Arya SK, Eva A, Souza LM, Baluda MA et al. (1982). Proc Natl Acad Sci USA 79: 2194–2198.

  • Zenke M, Kahn P, Disela C, Vennstrom B, Leutz A, Keegan K et al. (1988). Cell 52: 107–119.

Download references

Acknowledgements

We are indebted to Dr M Yamamoto for the gift of mouse GATA-1 and GATA-2 expression vectors, Dr R Watson for the mouse B-Myb expression vector and Dr E Weston for the 5E monoclonal antibody. We thank Drs A Bouton and A Goldfarb for discussions and critical review of the manuscript. This work was supported by Grants CA85842 and GM55985 to TPB from the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Molecular Physiology and Biological Physics, University of Virginia Health System, Charlottesville, VA, USA

    J Chen

  2. Department of Microbiology, University of Virginia Health System, Charlottesville, VA, USA

    C S Kremer & T P Bender

Authors
  1. J Chen
    View author publications

    Search author on:PubMed Google Scholar

  2. C S Kremer
    View author publications

    Search author on:PubMed Google Scholar

  3. T P Bender
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to T P Bender.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, J., Kremer, C. & Bender, T. The carbonic anhydrase I locus contains a c-Myb target promoter and modulates differentiation of murine erythroleukemia cells. Oncogene 25, 2758–2772 (2006). https://doi.org/10.1038/sj.onc.1209295

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/sj.onc.1209295

Keywords

This article is cited by

Search

Advanced search

Quick links