Protein Kinase C-Mediated Phosphorylation of the Leukemia-Associated HOXA9 Protein Impairs Its DNA Binding Ability and Induces Myeloid Differentiation

REFERENCES

• Ausubel, F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., and Struhl K. (ed.). 1987. Current protocols in molecular biology, p. 12.1.1–12.1.8. John Wiley & Sons, Hoboken, N.J.
   Google Scholar
• Berry, M., and Gehring W.. 2000. Phosphorylation status of the SCR homeodomain determines its functional activity: essential role for protein phosphatase 2A,B′. EMBO J. 19:2946–2957.
   PubMedGoogle Scholar
• Borrow, J., Shearman A. M., Stanton V. P. J., Becher R., Collins T., Williams A. J., Dube I., Katz F., Kwong Y. L., Morris C., Ohyashiki K., Toyama K., Rowley J., and Housman D. E.. 1996. The t(7;11)(p15;p15) translocation in acute myeloid leukemia fuses the genes for nucleoporin NU98 and class I homeoprotein HOXA9. Nat. Genet. 12:159–167.
   PubMed Web of Science ®Google Scholar
• Bourbon, H. M., Martin-Blanco E., Rosen D., and Kornberg T. B.. 1995. Phosphorylation of the Drosophila engrailed protein at a site outside its homeodomain enhances DNA binding. J. Biol. Chem. 270:11130–11139.
   PubMedGoogle Scholar
• Boyle, W. J., van der Geer P., and Hunter T.. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110–143.
   PubMed Web of Science ®Google Scholar
• Calvo, K. R., Knoepfler P. S., Sykes D. B., Pasillas M. P., and Kamps M. P.. 2001. Meis1a suppresses differentiation by G-CSF and promotes proliferation by SCF: potential mechanisms of cooperativity with Hoxa9 in myeloid leukemia. Proc. Natl. Acad. Sci. USA 98:13120–13125.
   PubMedGoogle Scholar
• Calvo, K. R., Sykes D. B., Pasillas M., and Kamps M. P.. 2000. Hoxa9 immortalizes a granulocyte-macrophage colony-stimulating factor-dependent promyelocyte capable of biphenotypic differentiation to neutrophils or macrophages, independent of enforced Meis expression. Mol. Cell. Biol. 20:3274–3285.
   PubMed Web of Science ®Google Scholar
• Calvo, K. R., Sykes D. B., Pasillas M. P., and Kamps M. P.. 2002. Nup98-HoxA9 immortalizes myeloid progenitors, enforces expression of Hoxa9, Hoxa7 and Meis1, and alters cytokine-specific responses in a manner similar to that induced by retroviral co-expression of Hoxa9 and Meis1. Oncogene 21:4247–4256.
   PubMed Web of Science ®Google Scholar
• Coqueret, O., Berube G., and Nepveu A.. 1998. The mammalian Cut homeodomain protein functions as a cell-cycle-dependent transcriptional repressor which downmodulates p21WAF1/CIP1/SDI1 in S phase. EMBO J. 17:4680–4694.
   PubMedGoogle Scholar
• Coqueret, O., Martin N., Berube G., Rabbat M., Litchfield D. W., and Nepveu A.. 1998. DNA binding by cut homeodomain proteins is down-modulated by casein kinase II. J. Biol. Chem. 273:2561–2566.
   PubMedGoogle Scholar
• Davies, S. P., Reddy H., Caivano M., and Cohen P.. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95–105.
   PubMed Web of Science ®Google Scholar
• Dong, J., Hung L. H., Strome R., and Krause H. M.. 1998. A phosphorylation site in the ftz homeodomain is required for activity. EMBO J. 17:2308–2318.
   PubMedGoogle Scholar
• Dorsam, T. S., Ferrell M. C., Dorsam P. G., Vijapurkar U., Khodabakhsh D., Pau B., Bernstein H., Haqq M. C., Largman C., and Lawrence H. J.. 2004. The transcriptome of the leukemogenic homeoprotein HOXA9 in human hematopoietic cells. Blood 103:1676–1684.
   PubMed Web of Science ®Google Scholar
• Eklund, E. A., Jalava A., and Kakar R.. 2000. Tyrosine phosphorylation of HoxA10 decreases DNA binding and transcriptional repression during interferon gamma-induced differentiation of myeloid leukemia cell lines. J. Biol. Chem. 275:20117–20126.
   PubMedGoogle Scholar
• Gehring, W. J. 1987. Homeo boxes in the study of development. Science 236:1245–1252.
   PubMed Web of Science ®Google Scholar
• Gehring, W. J., Qian Y. Q., Billeter M., Furukubo-Tokunaga K., Affolter M., Otting G., and Wuthrich K.. 1994. Homeodomain-DNA recognition. Cell 69:211–223.
   Google Scholar
• Ghaffari, M., Zeng X., Whitsett J. A., and Yan C.. 1997. Nuclear localization domain of thyroid transcription factor-1 in respiratory epithelial cells. Biochem. J. 328:757–761.
   PubMedGoogle Scholar
• Golub, T. R., Slonim D. K., Tamayo P., Huard C., Gaasenbeek M., Mesirov J. P., Coller H., Loh M. L., Downing J. R., Caligiuri M. A., Bloomfield C. D., and Lander E. S.. 1999. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286:531–537.
   PubMed Web of Science ®Google Scholar
• Hall, M. N., Craik C., and Hiraoka Y.. 1990. Homeodomain of yeast repressor alpha 2 contains a nuclear localization signal. Proc. Natl. Acad. Sci. USA 87:6954–6958.
   PubMedGoogle Scholar
• Izon, D. J., Komuves L. G., Rozenfeld S., Fong S., Largman C., and Lawrence H. J.. 1998. Loss of function of the homeobox gene HoxA-9 retards T-cell development and induces apoptosis. Blood 92:382–389.
   Google Scholar
• Jaffe, L., Ryoo H.-D., and Mann R. S.. 1997. A role for phosphorylation by casein kinase II in modulating Antennapedia activity in Drosophila. Genes Dev. 11:1327–1340.
   PubMedGoogle Scholar
• Kasahara, H., and Izumo S.. 1999. Identification of the in vivo casein kinase II phosphorylation site within the homeodomain of the cardiac tissue-specifying homeobox gene product Csx/Nkx2.5. Mol. Cell. Biol. 19:526–536.
   PubMedGoogle Scholar
• Kissinger, C. R., Liu B., Martin-Blanco E., Kornberg T. B., and Pabo C. O.. 1990. Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution. A framework for understanding homeodomain-DNA interactions. Cell 63:579–590.
   PubMed Web of Science ®Google Scholar
• Kmita, M., and Duboule D.. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331–333.
   PubMed Web of Science ®Google Scholar
• Koeffler, H. P., Bar-Eli M., and Territo M. C.. 1981. Phorbol ester effect on differentiation of human myeloid leukemia cell lines blocked at different stages of maturation. Cancer Res. 41:919–926.
   PubMedGoogle Scholar
• Kroon, E., Krosl J., Thorsteinsdottir U., Baban S., Buchberg A. M., and Sauvageau G.. 1998. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 17:3714–3725.
   PubMed Web of Science ®Google Scholar
• Kroon, E., Thorsteinsdottir U., Mayotte N., Nakamura T., and Sauvageau G.. 2001. NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 20:350–361.
   PubMed Web of Science ®Google Scholar
• LaRonde-LeBlanc, N. A., and C. Wolberger. 2003. Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev. 17:2060–2072.
   PubMed Web of Science ®Google Scholar
• Lawrence, H. J., Helgason C. D., Sauvageau G., Fong S., Izon D. J., Humphries R. K., and Largman C.. 1997. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 89:1922–1930.
   PubMed Web of Science ®Google Scholar
• Lawrence, H. J., Rozenfeld S., Cruz C., Matsukuma K., Kwong A., Komuves L., Buchberg A. M., and Largman C.. 1999. Frequent co-expression of the HOXA9 and MEIS1 homeobox genes in human myeloid leukemias. Leukemia 13:1993–1999.
   PubMed Web of Science ®Google Scholar
• Lawrence, H. J., Sauvageau G., Humphries R. K., and Largman C.. 1996. The role of HOX genes in normal and leukemic hematopoiesis. Stem Cells 14:281–290.
   PubMed Web of Science ®Google Scholar
• Look, T. A. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278:1059–1064.
   PubMed Web of Science ®Google Scholar
• Lotem, J., and Sachs L.. 1979. Regulation of normal differentiation in mouse and human myeloid leukemic cells by phorbol esters and the mechanism of tumor promotion. Proc. Natl. Acad. Sci. USA 76:5158–5162.
   PubMed Web of Science ®Google Scholar
• Macfarlane, D. E., and Manzel L.. 1994. Activation of beta-isozyme of protein kinase C (PKC beta) is necessary and sufficient for phorbol ester-induced differentiation of HL-60 promyelocytes. Studies with PKC beta-defective PET mutant. J. Biol. Chem. 269:4327–4331.
   PubMed Web of Science ®Google Scholar
• Magli, M. C., Largman C., and Lawrence H. J.. 1997. Effects of HOX homeobox genes in blood cell differentiation. J. Cell Physiol. 173:168–177.
   PubMed Web of Science ®Google Scholar
• McGinnis, W., and Krumlauf R.. 1992. Homeobox genes and axial patterning. Cell 68:283–302.
   PubMed Web of Science ®Google Scholar
• Meisner, H., and Czech M. P.. 1991. Phosphorylation of transcriptional factors and cell-cycle-dependent proteins by casein kinase II. Curr. Opin. Cell Biol. 3:474–483.
   PubMedGoogle Scholar
• Mischak, H., Pierce J. H., Goodnight J., Kazanietz M. G., Blumberg P. M., and Mushinski J. F.. 1993. Phorbol ester-induced myeloid differentiation is mediated by protein kinase C-alpha and -delta and not by protein kinase C-beta II, -epsilon, -zeta, and -eta. J. Biol. Chem. 268:20110–20115.
   PubMed Web of Science ®Google Scholar
• Moskow, J. J., Bullrich F., Huebner K., Daar I. O., and Buchberg A. M.. 1995. Meis, a PBX1-related homeobox gene involved in myeloid leukemias in BXH-2 mice. Mol. Cell. Biol. 15:5434–5443.
   PubMed Web of Science ®Google Scholar
• Muller, M., Affolter M., Leupin W., Otting G., Wuthrich K., and Gehring W. J.. 1988. Isolation and sequence-specific DNA binding of the Antennapedia homeodomain. EMBO J. 7:4299–4304.
   PubMedGoogle Scholar
• Nakamura, T., Largaespada D. A., Lee M. P., Johnson L. A., Ohyashiki K., Toyama K., Chen S. J., Willman C. L., Chen I.-M., Feinberg A. P., Jenkins N. A., Copeland N. G., and Shaughnessy J. D. J.. 1996. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;15) in human myeloid leukemia. Nat. Genet. 12:154–158.
   PubMed Web of Science ®Google Scholar
• Naviaux, R. K., Costanzi E., Haas M., and Verma I. M.. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701–5705.
   PubMed Web of Science ®Google Scholar
• Niedel, J. E., Kuhn L. J., and Vandenbark G. R.. 1983. Phorbol diester receptor copurifies with protein kinase C. Proc. Natl. Acad. Sci. USA 80:36–40.
   PubMed Web of Science ®Google Scholar
• Oshevski, S., Le Bousse-Kerdiles M. C., Clay D., Levashova Z., Debili N., Vitral N., Jasmin C., and Castagna M.. 1999. Differential expression of protein kinase C isoform transcripts in human hematopoietic progenitors undergoing differentiation. Biochem. Biophys. Res. Commun. 263:603–609.
   PubMed Web of Science ®Google Scholar
• Pinna, L. A. 1990. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim. Biophys. Acta 1054:267–284.
   PubMed Web of Science ®Google Scholar
• Rovera, G., Ferrero D., Pagliardi G. L., Vartikar J., Pessano S., Bottero L., Abraham S., and Lebman D.. 1982. Induction of differentiation of human myeloid leukemias by phorbol diesters: phenotypic changes and mode of action. Ann. N. Y. Acad. Sci. 397:211–220.
   PubMed Web of Science ®Google Scholar
• Schnabel, C. A., Jacobs Y., and Cleary M. L.. 2000. HoxA9-mediated immortalization of myeloid progenitors requires functional interactions with TALE cofactors Pbx and Meis. Oncogene 19:608–616.
   PubMed Web of Science ®Google Scholar
• Senderowicz, L., Wang J. X., Wang L. Y., Yoshizawa S., Kavanaugh W. M., and Turck C. W.. 1997. 3-Phosphohistidine cannot replace phosphotyrosine in high-affinity binding to phosphotyrosine binding or Src homology 2 domains. Biochemistry 36:10538–10544.
   PubMedGoogle Scholar
• Shen, W.-F., Montgomery J. C., Rozenfeld S., Lawrence H. J., Buchberg A., and Largman C.. 1997. The Abd-B-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol. Cell. Biol. 17:6448–6458.
   PubMed Web of Science ®Google Scholar
• Shen, W.-F., Rozenfeld S., Lawrence H. J., and Largman C.. 1997. The Abd-B-like Hox homeodomain proteins can be subdivided by the ability to form complexes with Pbx1a on a novel DNA target. J. Biol. Chem. 272:8198–8206.
   PubMedGoogle Scholar
• Shen, W. F., Rozenfeld S., Kwong A., Komuves L., Lawrence H. J., and Largman C.. 1999. HOXA9 forms triple complexes with PBX2 and MEIS1 in myeloid cells. Mol. Cell. Biol. 19:3051–3061.
   PubMed Web of Science ®Google Scholar
• Sock, E., Enderich J., Rosenfeld M. G., and Wegner M.. 1996. Identification of the nuclear localization signal of the POU domain protein Tst-1/Oct6. J. Biol. Chem. 271:17512–17518.
   PubMedGoogle Scholar
• Steube, K. G., and Drexler H. G.. 1993. Differentiation and growth modulation of myeloid leukemia cells by the protein kinase C activating agent bryostatin-1. Leuk Lymphoma 9:141–148.
   PubMed Web of Science ®Google Scholar
• Thorsteinsdottir, U., Kroon E., Jerome L., Blasi F., and Sauvageau G.. 2001. Defining roles for HOX and MEIS1 genes in induction of acute myeloid leukemia. Mol. Cell. Biol. 21:224–234.
   PubMed Web of Science ®Google Scholar
• Thorsteinsdottir, U., Krosl J., Kroon E., Haman A., Hoang T., and Sauvageau G.. 1999. The oncoprotein E2A-Pbx1a collaborates with Hoxa9 to acutely transform primary bone marrow cells. Mol. Cell. Biol. 19:6355–6366.
   PubMedGoogle Scholar
• Thorsteinsdottir, U., Mamo A., Kroon E., Jerome L., Bijl J., Lawrence H. J., Humphries K., and Sauvageau G.. 2002. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 99:121–129.
   PubMed Web of Science ®Google Scholar
• Tuazon, P. T., and Traugh J. A.. 1991. Casein kinase I and II—multipotential serine protein kinases: structure, function, and regulation. Adv. Second Messenger Phosphoprotein Res. 23:123–164.
   PubMedGoogle Scholar
• Tucker, K. A., Lilly M. B., Heck L., Jr., and Rado T. A.. 1987. Characterization of a new human diploid myeloid leukemia cell line (PLB-985) with granulocytic and monocytic differentiating capacity. Blood 70:372–378.
   PubMed Web of Science ®Google Scholar
• Vandenbark, G. R., Kuhn L. J., and Niedel J. E.. 1984. Possible mechanism of phorbol diester-induced maturation of human promyelocytic leukemia cells. J. Clin. Investig. 73:448–457.
   PubMedGoogle Scholar
• Ways, D. K., Messer B. R., Garris T. O., Qin W., Cook P. P., and Parker P. J.. 1992. Modulation of protein kinase C-epsilon by phorbol esters in the monoblastoid U937 cell. Cancer Res. 52:5604–5609.
   PubMedGoogle Scholar
• Wolberger, C., Vershon A. K., Liu B., Johnson A. D., and Pabo C. O.. 1991. Crystal structure of a MATα2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67:517–528.
   PubMed Web of Science ®Google Scholar
• Yaron, Y., McAdara J. K., Lynch M., Hughes E., and Gasson J. C.. 2001. Identification of novel functional regions important for the activity of HOXB7 in mammalian cells. J. Immunol. 166:5058–5067.
   PubMedGoogle Scholar