Leukemia Research
Volume 24, Issue 12 , Pages 1023-1031 , December 2000

The homeodomain protein PRH influences the differentiation of haematopoietic cells

  • Padma-Sheela Jayaraman

      Affiliations

    • These authors contributed equally to the work.
    • Department of Biochemistry, University of Bristol, University Walk, Bristol BS8 1TD, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44-117-9287439; fax: +44-117-9288274
  • ,
  • Jonathan Frampton

      Affiliations

    • These authors contributed equally to the work.
    • Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
  • ,
  • Graham Goodwin

      Affiliations

    • Institute of Cancer Research, 15 Cotswold Road, Sutton Surrey SM2 5NG, UK

Received 23 February 2000 ,Accepted 10 June 2000.

References 

  1. Gehring WJ, Affolter M, Burglin T. Homeodomain proteins. Annu. Rev. Biochem. 1994;63:487–526
  2. McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984;37(2):403–408
  3. Laughon A. DNA binding specificity of homeodomains. Biochemistry. 1991;30(48):11357–11367
  4. Dubnau J, Struhl G. RNA recognition and translational regulation by a homeodomain protein [published erratum appears in Nature 1997;388(6643):697]. Nature 1996;379(6567):694–699.
  5. Rivera-Pomar R, Niessing D, Schmidt-Ott U, Gehring WJ, Jackle H. RNA binding and translational suppression by bicoid. Nature. 1996;79(6567):746–749
  6. Lawrence HJ, Largman C. Homeobox genes in normal hematopoiesis and leukemia. Blood. 1992;80(10):2445–2453
  7. Lawrence HJ, Sauvageau G, Humphries RK, Largman C. The role of HOX homeobox genes in normal and leukemic hematopoiesis. Stem Cells. 1996;14(3):281–291
  8. Schreiber E, Matthias P, Muller MM, Schaffner W. Identification of a novel lymphoid specific octamer binding protein (OTF-2B) by proteolytic clipping bandshift assay (PCBA). EMBO J. 1988;7(13):4221–4229
  9. Staudt LM, Clerc RG, Singh H, LeBowitz JH, Sharp PA, Baltimore D. Cloning of a lymphoid-specific cDNA encoding a protein binding the regulatory octamer DNA motif. Science. 1988;241(4865):577–580
  10. Lawrence HJ, Helgason CD, Sauvageau G, Fong S, Izon DJ, Humphries RK, et al.  Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood. 1997;89(6):1922–1930
  11. Thorsteinsdottir U, Sauvageau G, Hough MR, Dragowska W, Lansdorp PM, Lawrence HJ, et al.  Overexpression of HOXA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemia. Mol. Cell. Biol. 1997;17(1):495–505
  12. Look AT. Oncogenic transcription factors in the human acute leukemias. Science. 1997;278(5340):1059–1064
  13. Crompton MR, Bartlett TJ, MacGregor AD, Manfioletti G, Buratti E, Giancotti V, et al.  Identification of a novel vertebrate homeobox gene expressed in haematopoietic cells. Nucleic Acids Res. 1992;20(21):5661–5667
  14. Bedford FK, Ashworth A, Enver T, Wiedemann LM. HEX: a novel homeobox gene expressed during haematopoiesis and conserved between mouse and human. Nucleic Acids Res. 1993;21(5):1245–1249
  15. Patterson KD, Cleaver O, Gerber WV, Grow MW, Newman CS, Krieg PA. Homeobox genes in cardiovascular development. Curr. Top. Dev. Biol. 1998;40:1–44
  16. Newman CS, Chia F, Krieg PA. The XHex homeobox gene is expressed during development of the vascular endothelium: overexpression leads to an increase in vascular endothelial cell number. Mech. Dev. 1997;66(1–2):83–93
  17. Thomas PQ, Brown A, Beddington RS. Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development. 1998;125(1):85–94
  18. Tanaka T, Inazu T, Yamada K, Myint Z, Keng VW, Inoue Y, et al.  cDNA cloning and expression of rat homeobox gene, Hex, and functional characterization of the protein. Biochem. J. 1999;339:111–117
  19. Guiral M, Bess K,Goodwin G, Jayaraman P-S. PRH represses transcription in haematopoietic cells by at least two independent mechanisms. (submitted)
  20. Hatano M, Roberts CW, Minden M, Crist WM, Korsmeyer SJ. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T cell leukemia. Science. 1991;253(5015):79–82
  21. Lu M, Gong ZY, Shen WF, Ho AD. The tcl-3 proto-oncogene altered by chromosomal translocation in T-cell leukemia codes for a homeobox protein. EMBO J. 1991;10(10):2905–2910
  22. Hawley RG, Fong AZC, Lu M, Hawley TS. The HOX11 homeobox-containing gene of human leukemia immortalizes murine hematopoietic precursors. Oncogene. 1994;9(1):1–12
  23. Allen JD, Lints T, Jenkins NA, Copeland NG, Strasser A, Harvey RP, et al.  Novel murine homeo box gene on chromosome 1 expressed in specific hematopoietic lineages and during embryogenesis. Genes Dev. 1991;5(4):509–520
  24. Deguchi Y, Moroney JF, Wilson GL, Fox CH, Winter HS, Kehrl JH. Cloning of a human homeobox gene that resembles a diverged Drosophila homeobox gene and is expressed in activated lymphocytes. New Biol. 1991;3(4):353–363
  25. Allen JD, Adams JM. Enforced expression of Hlx homeobox gene prompts myeloid cell maturation and altered adherence properties of T cells. Blood. 1993;81(12):3242–3251
  26. Manfioletti G, Gattei V, Buratti E, Rustighi A, De Iuliis A, Aldinucci D, et al.  Differential expression of a novel proline-rich homeobox gene (Prh) in human hematolymphopoietic cells. Blood. 1995;85(5):1237–1245
  27. Topcu Z, Mack DL, Hromas RA, Borden KL. The promyelocytic leukemia protein PML interacts with the proline-rich homeodomain protein PRH: a RING may link hematopoiesis and growth control. Oncogene. 1999;18(50):7091–7100
  28. Hansen GM, Justice MJ. Activation of Hex and mEg5 by retroviral insertion may contribute to mouse B-cell leukemia. Oncogene. 1999;18(47):6531–6539
  29. Frampton J, McNagny K, Sieweke M, Philip A, Smith G, Graf T. v-Myb DNA binding is required to block thrombocytic differentiation of Myb-Ets-transformed multipotent haematopoietic progenitors. EMBO J. 1995;14(12):2866–2875
  30. Kraut N, Frampton J, McNagny KM, Graf T. A functional Ets DNA-binding domain is required to maintain multipotency of hematopoietic progenitors transformed by Myb-Ets. Genes Dev. 1994;8(1):33–44
  31. Graf T, McNagny K, Brady G, Frampton J. Chicken ‘erythroid’ cells transformed by the Gag-Myb-Ets- encoding E26 leukemia virus are multipotent. Cell. 1992;70(2):201–213
  32. Beug H, Blundell PA, Graf T. Reversibility of differentiation and proliferative capacity in avian myelomonocytic cells transformed by tsE26 leukemia virus. Genes Dev. 1987;1(3):277–286
  33. Kulessa H, Frampton J, Graf T. GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev. 1995;9(10):1250–1262
  34. Metz T, Graf T. Fusion of the nuclear oncoproteins v-Myb and v-Ets is required for the leukemogenicity of E26 virus. Cell. 1991;66(1):95–105
  35. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal. Biochem. 1987;162(1):156–159
  36. Evan GI, Lewis GK, Ramsay G, Bishop JM. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 1985;5(12):3610–3616
  37. Golay J, Introna M, Graf T. A single point mutation in the v-ets oncogene affects both erythroid and myelomonocytic cell differentiation. Cell. 1988;55(6):1147–1158
  38. Moscovici MG, Jurdic P, Samarut J, Gazzolo L, Mura CV, Moscovici C. Characterization of the hemopoietic target cells for the avian leukemia virus E26. Virology. 1983;129(1):65–78
  39. Kornfeld S, Beug H, Doederlein G, Graf T. Detection of avian hematopoietic cell surface antigens with monoclonal antibodies to myeloid cells. Their distribution on normal and leukemic cells of various lineages. Exp. Cell Res. 1983;143(2):383–394
  40. McNagny KM, Lim F, Grieser S, Graf T. Cell surface proteins of chicken hematopoietic progenitors, thrombocytes and eosinophils detected by novel monoclonal antibodies. Leukemia. 1992;6(10):975–984
  41. Schmidt JA, Marshall J, Hayman MJ, Doderlein G, Beug H. Monoclonal antibodies to novel erythroid differentiation antigens reveal specific effects of oncogenes on the leukaemic cell phenotype. Leuk. Res. 1986;10(3):257–272
  42. Kaplow LS. Simplified myeloperoxidase stain using benzidine hydrochloride. Blood. 1965;26:215–219
  43. Moscovici C, Zeller N, Moscovici MG. In:  Revoltella RF,  Pontieri GM,  Basilico C,  Rovera G,  Gallo RC,  Subak-Sharpe JH editor. Expression of Differentiated Function in Cancer Cells. New York: Raven Press; 1982;p. 435–449
  44. Koeffler HP, Golde DW. Human myeloid leukemia cell lines: a review. Blood. 1980;56(3):344–350
  45. McNagny KM, Sieweke MH, Doderlein G, Graf T, Nerlov C. Regulation of eosinophil-specific gene expression by a C/EBP-Ets complex and GATA-1. EMBO J. 1998;17(13):3669–3680
  46. Nerlov C, Graf T. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 1998;12(15):2403–2412
  47. Nerlov C, McNagny KM, Doderlein G, Kowenz-Leutz E, Graf T. Distinct C/EBP functions are required for eosinophil lineage commitment and maturation. Genes Dev. 1998;12(15):2413–2423

PII: S0145-2126(00)00072-2

doi: 10.1016/S0145-2126(00)00072-2

Leukemia Research
Volume 24, Issue 12 , Pages 1023-1031 , December 2000