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

Molecular and Cellular Biology

Volumn 24, Issue 9, 2004, Pages 3827-3837

  Vijapurkar, Ulka ^a   Fischbach, Neal ^a   Shen, Weifang ^a   Brandts, Christian ^b   Stokoe, David ^b   Lawrence, H Jeffrey ^a   Largman, Corey ^a,c  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; HOMEODOMAIN PROTEIN; HOX PROTEIN; HOXA9 PROTEIN; PHORBOL ESTER; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BONE MARROW CELL; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CELL LINE; CELL TRANSPLANTATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; GENE OVEREXPRESSION; LEUKEMOGENESIS; MOUSE; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; BONE MARROW CELLS; CASEIN KINASE II; CELL DIFFERENTIATION; CELL LINE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HOMEODOMAIN PROTEINS; ISOENZYMES; LEUKEMIA, MYELOID; MICE; MOLECULAR SEQUENCE DATA; MYELOID CELLS; PHORBOL ESTERS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; SERINE;

ANIMALIA; MURINAE;

EID: 1942518374     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.9.3827-3837.2004     Document Type: Article

References (62)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology, p. 12.1.1-12.1.8. John Wiley & Sons, Hoboken, N.J.
2. Berry, M., and W. Gehring. 2000. Phosphorylation status of the SCR homeodomain determines its functional activity: essential role for protein phosphatase 2A,B′. EMBO J. 19:2946-2957.
3. Borrow, J., A. M. Shearman, V. P. J. Stanton, R. Becher, T. Collins, A. J. Williams, I. Dube, F. Katz, Y. L. Kwong, C. Morris, K. Ohyashiki, K. Toyama, J. Rowley, and D. E. Housman. 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.
4. Bourbon, H. M., E. Martin-Blanco, D. Rosen, and T. B. Kornberg. 1995. Phosphorylation of the Drosophila engrailed protein at a site outside its homeodomain enhances DNA binding. J. Biol. Chem. 270:11130-11139.
5. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110-143.
6. Calvo, K. R., P. S. Knoepfler, D. B. Sykes, M. P. Pasillas, and M. P. Kamps. 2001. Meisla 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.
7. Calvo, K. R., D. B. Sykes, M. Pasillas, and M. P. Kamps. 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.
8. Calvo, K. R., D. B. Sykes, M. P. Pasillas, and M. P. Kamps. 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.
9. Coqueret, O., G. Berube, and A. Nepveu. 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.
10. Coqueret, O., N. Martin, G. Berube, M. Rabbat, D. W. Litchfield, and A. Nepveu. 1998. DNA binding by cut homeodomain proteins is down-modulated by casein kinase II. J. Biol. Chem. 273:2561-2566.
11. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95-105.
12. Dong, J., L. H. Hung, R. Strome, and H. M. Krause. 1998. A phosphorylation site in the ftz homeodomain is required for activity. EMBO J. 17:2308-2318.
13. Dorsam, T. S., M. C. Ferrell, P. G. Dorsam, U. Vijapurkar, D. Khodabakhsh, B. Pau, H. Bernstein, M. C. Haqq, C. Largman, and H. J. Lawrence. 2004. The transcriptome of the leukemogenic homeoprotein HOXA9 in human hematopoietic cells. Blood 103:1676-1684.
14. Eklund, E. A., A. Jalava, and R. Kakar. 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.
15. Gehring, W. J. 1987. Homeo boxes in the study of development. Science 236:1245-1252.
16. Gehring, W. J., Y. Q. Qian, M. Billeter, K. Furukubo-Tokunaga, M. Affolter, G. Otting, and K. Wuthrich. 1994. Homeodomain-DNA recognition. Cell 69:211-223.
17. Ghaffari, M., X. Zeng, J. A. Whitsett, and C. Yan. 1997. Nuclear localization domain of thyroid transcription factor-1 in respiratory epithelial cells. Biochem. J. 328:757-761.
18. Golub, T. R., D. K. Slonim, P. Tamayo, C. Huard, M. Gaasenbeek, J. P. Mesirov, H. Coller, M. L. Loh, J. R. Downing, M. A. Caligiuri, C. D. Bloomfield, and E. S. Lander. 1999. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286:531-537.
19. Hall, M. N., C. Craik, and Y. Hiraoka. 1990. Homeodomain of yeast repressor alpha 2 contains a nuclear localization signal. Proc. Natl. Acad. Sci. USA 87:6954-6958.
20. Izon, D. J., L. G. Komuves, S. Rozenfeld, S. Fong, C. Largman, and H. J. Lawrence. 1998. Loss of function of the homeobox gene HoxA-9 retards T-cell development and induces apoptosis. Blood 92:382-389.
21. Jaffe, L., H.-D. Ryoo, and R. S. Mann. 1997. A role for phosphorylation by casein kinase II in modulating Antennapedia activity in Drosophila. Genes Dev. 11:1327-1340.
22. Kasahara, H., and S. Izumo. 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.
23. Kissinger, C. R., B. Liu, E. Martin-Blanco, T. B. Kornberg, and C. O. Pabo. 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.
24. Kmita, M., and D. Duboule. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331-333.
25. Koeffler, H. P., M. Bar-Eli, and M. C. Territo. 1981. Phorbol ester effect on differentiation of human myeloid leukemia cell lines blocked at different stages of maturation. Cancer Res. 41:919-926.
26. Kroon, E., J. Krosl, U. Thorsteinsdottir, S. Baban, A. M. Buchberg, and G. Sauvageau. 1998. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meisla but not Pbx1b. EMBO J. 17:3714-3725.
27. Kroon, E., U. Thorsteinsdottir, N. Mayotte, T. Nakamura, and G. Sauvageau. 2001. NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 20:350-361.
28. 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.
29. Lawrence, H. J., C. D. Helgason, G. Sauvageau, S. Fong, D. J. Izon, R. K. Humphries, and C. Largman. 1997. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 89:1922-1930.
30. Lawrence, H. J., S. Rozenfeld, C. Cruz, K. Matsukuma, A. Kwong, L. Komuves, A. M. Buchberg, and C. Largman. 1999. Frequent co-expression of the HOXA9 and MEIS1 homeobox genes in human myeloid leukemias. Leukemia 13:1993-1999.
31. Lawrence, H. J., G. Sauvageau, R. K. Humphries, and C. Largman. 1996. The role of HOX genes in normal and leukemic hematopoiesis. Stem Cells 14:281-290.
32. Look, T. A. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278:1059-1064.
33. Lotem, J., and L. Sachs. 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.
34. Macfarlane, D. E., and L. Manzel. 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.
35. Magli, M. C., C. Largman, and H. J. Lawrence. 1997. Effects of HOX homeobox genes in blood cell differentiation. J. Cell Physiol. 173:168-177.
36. McGinnis, W., and R. Krumlauf. 1992. Homeobox genes and axial patterning. Cell 68:283-302.
37. Meisner, H., and M. P. Czech. 1991. Phosphorylation of transcriptional factors and cell-cycle-dependent proteins by casein kinase II. Curr. Opin. Cell Biol. 3:474-483.
38. Mischak, H., J. H. Pierce, J. Goodnight, M. G. Kazanietz, P. M. Blumberg, and J. F. Mushinski. 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.
39. Moskow, J. J., F. Bullrich, K. Huebner, I. O. Daar, and A. M. Buchberg. 1995. Meis, a PBX1-related homeobox gene involved in myeloid leukemias in BXH-2 mice. Mol. Cell. Biol. 15:5434-5443.
40. Muller, M., M. Affolter, W. Leupin, G. Otting, K. Wuthrich, and W. J. Gehring. 1988. Isolation and sequence-specific DNA binding of the Antennapedia homeodomain. EMBO J. 7:4299-4304.
41. Nakamura, T., D. A. Largaespada, M. P. Lee, L. A. Johnson, K. Ohyashiki, K. Toyama, S. J. Chen, C. L. Willman, I.-M. Chen, A. P. Feinberg, N. A. Jenkins, N. G. Copeland, and J. D. J. Shaughnessy. 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.
42. Navlaux, R. K., E. Costanzi, M. Haas, and I. M. Verma. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701-5705.
43. Niedel, J. E., L. J. Kuhn, and G. R. Vandenbark. 1983. Phorbol diester receptor copurifies with protein kinase C. Proc. Natl. Acad. Sci. USA 80:36-40.
44. Oshevski, S., M. C. Le Bousse-Kerdiles, D. Clay, Z. Levashova, N. Debili, N. Vitral, C. Jasmin, and M. Castagna. 1999. Differential expression of protein kinase C isoform transcripts in human hematopoietic progenitors undergoing differentiation. Biochem. Biophys. Res. Commun. 263:603-609.
45. Pinna, L. A. 1990. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim. Biophys. Acta 1054:267-284.
46. Rovera, G., D. Ferrero, G. L. Pagliardi, J. Vartikar, S. Pessano, L. Bottero, S. Abraham, and D. Lebman. 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.
47. Schnabel, C. A., Y. Jacobs, and M. L. Cleary. 2000. HoxA9-mediated immortalization of myeloid progenitors requires functional interactions with TALE cofactors Pbx and Meis. Oncogene 19:608-616.
48. Senderowicz, L., J. X. Wang, L. Y. Wang, S. Yoshizawa, W. M. Kavanaugh, and C. W. Turck. 1997. 3-Phosphohistidine cannot replace phosphotyrosine in high-affinity binding to phosphotyrosine binding or Src homology 2 domains. Biochemistry 36:10538-10544.
49. Shen, W.-F., J. C. Montgomery, S. Rozenfeld, H. J. Lawrence, A. Buchberg, and C. Largman. 1997. The Abd-B-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol. Cell. Biol. 17:6448-5458.
50. Shen, W.-F., S. Rozenfeld, H. J. Lawrence, and C. Largman. 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.
51. Shen, W. F., S. Rozenfeld, A. Kwong, L. Komuves, H. J. Lawrence, and C. Largman. 1999. HOXA9 forms triple complexes with PBX2 and MEIS1 in myeloid cells. Mol. Cell. Biol. 19:3051-3061.
52. Sock, E., J. Enderich, M. G. Rosenfeld, and M. Wegner. 1996. Identification of the nuclear localization signal of the POU domain protein Tst-1/Oct6. J. Biol. Chem. 271:17512-17518.
53. Steube, K. G., and H. G. Drexler. 1993. Differentiation and growth modulation of myeloid leukemia cells by the protein kinase C activating agent bryostatin-1. Leuk Lymphoma 9:141-148.
54. Thorsteinsdottir, U., E. Kroon, L. Jerome, F. Blasi, and G. Sauvageau. 2001. Defining roles for HOX and MEIS1 genes in induction of acute myeloid leukemia. Mol. Cell. Biol. 21:224-234.
55. Thorsteinsdottir, U., J. Krosl, E. Kroon, A. Haman, T. Hoang, and G. Sauvageau. 1999. The oncoprotein E2A-Pbx1a collaborates with Hoxa9 to acutely transform primary bone marrow cells. Mol. Cell. Biol. 19:6355-6366.
56. Thorsteinsdottir, U., A. Mamo, E. Kroon, L. Jerome, J. Bijl, H. J. Lawrence, K. Humphries, and G. Sauvageau. 2002. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 99:121-129.
57. Tuazon, P. T., and J. A. Traugh. 1991. Casein kinase I and II-multipotential serine protein kinases: structure, function, and regulation. Adv. Second Messenger Phosphoprotein Res. 23:123-164.
58. Tucker, K. A., M. B. Lilly, L. Heck, Jr., and T. A. Rado. 1987. Characterization of a new human diploid myeloid leukemia cell line (PLB-985) with granulocytic and monocytic differentiating capacity. Blood 70:372-378.
59. Vandenbark, G. R., L. J. Kuhn, and J. E. Niedel. 1984. Possible mechanism of phorbol diester-induced maturation of human promyelocytic leukemia cells. J. Clin. Investig. 73:448-457.
60. Ways, D. K., B. R. Messer, T. O. Garris, W. Qin, P. P. Cook, and P. J. Parker. 1992. Modulation of protein kinase C-epsilon by phorbol esters in the monoblastoid U937 cell. Cancer Res. 52:5604-5609.
61. Wolberger, C., A. K. Vershon, B. Liu, A. D. Johnson, and C. O. Pabo. 1991. Crystal structure of a MATα2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67:517-528.
62. Yaron, Y., J. K. McAdara, M. Lynch, E. Hughes, and J. C. Gasson. 2001. Identification of novel functional regions important for the activity of HOXB7 in mammalian cells. J. Immunol. 166:5058-5067.