Trithorax, Hox, and TALE-class homeodomain proteins ensure cell survival through repression of the BH3-only gene egl-1

Developmental Biology

Volumn 329, Issue 2, 2009, Pages 374-385

  Potts, Malia B ^a   Wang, David P ^a   Cameron, Scott ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Apoptosis; egl 1; Hox; Leukemia; Meis; MLL; Trithorax

Indexed keywords

BH3 PROTEIN; HOMEODOMAIN PROTEIN; HOX PROTEIN; TALE CLASS PROTEIN; TRITHORAX PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; EGL 1 GENE; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; LEUKEMIA; MOTONEURON; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; REGULATORY MECHANISM;

CAENORHABDITIS ELEGANS;

EID: 67349124418     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.02.022     Document Type: Article

References (73)

1. Aboobaker A., and Blaxter M. Hox gene evolution in nematodes: novelty conserved. Curr. Opin. Genet. Dev. 13 (2003) 593-598
2. Afonja O., Smith Jr. J.E., Cheng D.M., Goldenberg A.S., Amorosi E., Shimamoto T., Nakamura S., Ohyashiki K., Ohyashiki J., Toyama K., and Takeshita K. MEIS1 and HOXA7 genes in human acute myeloid leukemia. Leuk. Res. 24 (2000) 849-855
3. Argiropoulos B., Yung E., and Humphries R.K. Unraveling the crucial roles of Meis1 in leukemogenesis and normal hematopoiesis. Genes Dev. 21 (2007) 2845-2849
4. Armstrong S.A., Staunton J.E., Silverman L.B., Pieters R., den Boer M.L., Minden M.D., Sallan S.E., Lander E.S., Golub T.R., and Korsmeyer S.J. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat. Genet. 30 (2002) 41-47
5. Ayton P.M., and Cleary M.L. Transformation of myeloid progenitors by MLL oncoproteins dependent on Hoxa7 and Hoxa9. Genes Dev. 17 (2003) 2298-2307
6. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
7. Cameron S., Clark S.G., McDermott J.B., Aamodt E., and Horvitz H.R. PAG-3, a Zn-finger transcription factor, determines neuroblast fate in C. elegans. Development 129 (2002) 1763-1774
8. Chamberlin H.M., and Thomas J.H. The bromodomain protein LIN-49 and trithorax-related protein LIN-59 affect development and gene expression in Caenorhabditis elegans. Development 127 (2000) 713-723
9. Chang C.P., Shen W.F., Rozenfeld S., Lawrence H.J., Largman C., and Cleary M.L. Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev. 9 (1995) 663-674
10. Clark S.G., Chisholm A.D., and Horvitz H.R. Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39. Cell 74 (1993) 43-55
11. Conradt B., and Horvitz H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93 (1998) 519-529
12. Conradt B., and Horvitz H.R. The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98 (1999) 317-327
13. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
14. Drabkin H.A., Parsy C., Ferguson K., Guilhot F., Lacotte L., Roy L., Zeng C., Baron A., Hunger S.P., Varella-Garcia M., Gemmill R., Brizard F., Brizard A., and Roche J. Quantitative HOX expression in chromosomally defined subsets of acute myelogenous leukemia. Leukemia 16 (2002) 186-195
15. Egle A., Harris A.W., Bouillet P., and Cory S. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 6164-6169
16. Ellis H.M., and Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell 44 (1986) 817-829
17. Faber, J., Krivtsov, A.V., Stubbs, M.C., Wright, R., Davis, T.N., van den Heuvel-Eibrink, M., Zwaan, C.M., Kung, A.L., Armstrong, S.A., in press. HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood. doi:10.1182/blood-2007-09-113597.
18. Ferrando A.A., Armstrong S.A., Neuberg D.S., Sallan S.E., Silverman L.B., Korsmeyer S.J., and Look A.T. Gene expression signatures in MLL-rearranged T-lineage and B-precursor acute leukemias: dominance of HOX dysregulation. Blood 102 (2003) 262-268
19. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., and Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408 (2000) 325-330
20. 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. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286 (1999) 531-537
21. Grimwade D., Walker H., Oliver F., Wheatley K., Harrison C., Harrison G., Rees J., Hann I., Stevens R., Burnett A., and Goldstone A. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood 92 (1998) 2322-2333
22. Hengartner M.O., and Horvitz H.R. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76 (1994) 665-676
23. Hengartner M.O., Ellis R.E., and Horvitz H.R. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356 (1992) 494-499
24. Inaba T., Roberts W.M., Shapiro L.H., Jolly K.W., Raimondi S.C., Smith S.D., and Look A.T. Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science 257 (1992) 531-534
25. Inaba T., Inukai T., Yoshihara T., Seyschab H., Ashmun R.A., Canman C.E., Laken S.J., Kastan M.B., and Look A.T. Reversal of apoptosis by the leukaemia-associated E2A-HLF chimaeric transcription factor. Nature 382 (1996) 541-544
26. Inukai T., Inoue A., Kurosawa H., Goi K., Shinjyo T., Ozawa K., Mao M., Inaba T., and Look A.T. SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol. Cell 4 (1999) 343-352
27. Jaynes J.B., and O'Farrell P.H. Active repression of transcription by the engrailed homeodomain protein. EMBO J. 10 (1991) 1427-1433
28. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
29. Knoepfler P.S., and Kamps M.P. The pentapeptide motif of Hox proteins is required for cooperative DNA binding with Pbx1, physically contacts Pbx1, and enhances DNA binding by Pbx1. Mol. Cell. Biol. 15 (1995) 5811-5819
30. Krivtsov A.V., Twomey D., Feng Z., Stubbs M.C., Wang Y., Faber J., Levine J.E., Wang J., Hahn W.C., Gilliland D.G., Golub T.R., and Armstrong S.A. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 (2006) 818-822
31. Kroon E., Krosl J., Thorsteinsdottir U., Baban S., Buchberg A.M., and Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 17 (1998) 3714-3725
32. Kumar A.R., Hudson W.A., Chen W., Nishiuchi R., Yao Q., and Kersey J.H. Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia. Blood 103 (2004) 1823-1828
33. Liu J., and Fire A. Overlapping roles of two Hox genes and the exd ortholog ceh-20 in diversification of the C. elegans postembryonic mesoderm. Development 127 (2000) 5179-5190
34. Liu H., Strauss T.J., Potts M.B., and Cameron S. Direct regulation of egl-1 and of programmed cell death by the Hox protein MAB-5 and by CEH-20, a C. elegans homolog of Pbx1. Development 133 (2006) 641-650
35. Lohmann I., McGinnis N., Bodmer M., and McGinnis W. The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110 (2002) 457-466
36. Maloof J.N., and Kenyon C. The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 125 (1998) 181-190
37. Maurer C.W., Chiorazzi M., and Shaham S. Timing of the onset of a developmental cell death is controlled by transcriptional induction of the C. elegans ced-3 caspase-encoding gene. Development 134 (2007) 1357-1368
38. Metzstein M.M., Hengartner M.O., Tsung N., Ellis R.E., and Horvitz H.R. Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382 (1996) 545-547
39. Metzstein M.M., and Horvitz H.R. The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell. 4 (1999) 309-319
40. Metzstein M.M., Stanfield G.M., and Horvitz H.R. Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet (1998)
41. Milne T.A., Briggs S.D., Brock H.W., Martin M.E., Gibbs D., Allis C.D., and Hess J.L. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell. 10 (2002) 1107-1117
42. Moens C.B., and Selleri L. Hox cofactors in vertebrate development. Dev. Biol. 291 (2006) 193-206
43. Nakamura T., Mori T., Tada S., Krajewski W., Rozovskaia T., Wassell R., Dubois G., Mazo A., Croce C.M., and Canaani E. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell. 10 (2002) 1119-1128
44. Neuteboom S.T., Peltenburg L.T., van Dijk M.A., and Murre C. The hexapeptide LFPWMR in Hoxb-8 is required for cooperative DNA binding with Pbx1 and Pbx2 proteins. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9166-9170
45. Park D., Jia H., Rajakumar V., and Chamberlin H.M. Pax2/5/8 proteins promote cell survival in C. elegans. Development 133 (2006) 4193-4202
46. Phelan M.L., and Featherstone M.S. Distinct HOX N-terminal arm residues are responsible for specificity of DNA recognition by HOX monomers and HOX.PBX heterodimers. J. Biol. Chem. 272 (1997) 8635-8643
47. Phelan M.L., Rambaldi I., and Featherstone M.S. Cooperative interactions between HOX and PBX proteins mediated by a conserved peptide motif. Mol. Cell. Biol. 15 (1995) 3989-3997
48. Pui C.H., Relling M.V., and Downing J.R. Acute lymphoblastic leukemia. N. Engl. J. Med. 350 (2004) 1535-1548
49. Ranger A.M., Zha J., Harada H., Datta S.R., Danial N.N., Gilmore A.P., Kutok J.L., Le Beau M.M., Greenberg M.E., and Korsmeyer S.J. Bad-deficient mice develop diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9324-9329
50. Rozovskaia T., Ravid-Amir O., Tillib S., Getz G., Feinstein E., Agrawal H., Nagler A., Rappaport E.F., Issaeva I., Matsuo Y., Kees U.R., Lapidot T., Lo Coco F., Foa R., Mazo A., Nakamura T., Croce C.M., Cimino G., Domany E., and Canaani E. Expression profiles of acute lymphoblastic and myeloblastic leukemias with ALL-1 rearrangements. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7853-7858
51. Salser S.J., Loer C.M., and Kenyon C. Multiple HOM-C gene interactions specify cell fates in the nematode central nervous system. Genes Dev. 7 (1993) 1714-1724
52. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., and Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 128 (2007) 735-745
53. Serrano E., Lasa A., Perea G., Carnicer M.J., Brunet S., Aventin A., Sierra J., and Nomdedeu J.F. Acute myeloid leukemia subgroups identified by pathway-restricted gene expression signatures. Acta Haematol. 116 (2006) 77-89
54. Shaham S., and Horvitz H.R. Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev. 10 (1996) 578-591
55. Simmer F., Tijsterman M., Parrish S., Koushika S.P., Nonet M.L., Fire A., Ahringer J., and Plasterk R.H. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12 (2002) 1317-1319
56. Sitwala K.V., Dandekar M.N., and Hess J.L. HOX Proteins and Leukemia. Int. J. Clin. Exp. Pathol. 1 (2008) 461-474
57. So C.W., Karsunky H., Wong P., Weissman I.L., and Cleary M.L. Leukemic transformation of hematopoietic progenitors by MLL-GAS7 in the absence of Hoxa7 or Hoxa9. Blood 103 (2004) 3192-3199
58. Somervaille T.C., and Cleary M.L. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 10 (2006) 257-268
59. Spector M.S., Desnoyers S., Hoeppner D.J., and Hengartner M.O. Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature 385 (1997) 653-656
60. Stevens K.E., and Mann R.S. A balance between two nuclear localization sequences and a nuclear export sequence governs extradenticle subcellular localization. Genetics 175 (2007) 1625-1636
61. Sulston J.E. Post-embryonic development in the ventral cord of Caenorhabditis elegans. Philos Trans. R Soc. Lond. B Biol. Sci. 275 (1976) 287-297
62. Sulston J.E., and Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56 (1977) 110-156
63. Sulston J.E., Schierenberg E., White J.G., and Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100 (1983) 64-119
64. Sze J.Y., Liu Y., and Ruvkun G. VP16-activation of the C. elegans neural specification transcription factor UNC-86 suppresses mutations in downstream genes and causes defects in neural migration and axon outgrowth. Development 124 (1997) 1159-1168
65. Thellmann M., Hatzold J., and Conradt B. The Snail-like CES-1 protein of C. elegans can block the expression of the BH3-only cell-death activator gene egl-1 by antagonizing the function of bHLH proteins. Development 130 (2003) 4057-4071
66. Van Auken K., Weaver D., Robertson B., Sundaram M., Saldi T., Edgar L., Elling U., Lee M., Boese Q., and Wood W.B. Roles of the Homothorax/Meis/Prep homolog UNC-62 and the Exd/Pbx homologs CEH-20 and CEH-40 in C. elegans embryogenesis. Development 129 (2002) 5255-5268
67. Wagmaister J.A., Gleason J.E., and Eisenmann D.M. Transcriptional upregulation of the C. elegans Hox gene lin-39 during vulval cell fate specification. Mech. Dev. 123 (2006) 135-150
68. Wang B.B., Muller-Immergluck M.M., Austin J., Robinson N.T., Chisholm A., and Kenyon C. A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74 (1993) 29-42
69. Wong P., Iwasaki M., Somervaille T.C., So C.W., and Cleary M.L. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev. 21 (2007) 2762-2774
70. Wu D., Wallen H.D., Inohara N., and Nunez G. Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J. Biol. Chem. 272 (1997) 21449-21454
71. Yang L., Sym M., and Kenyon C. The roles of two C. elegans HOX co-factor orthologs in cell migration and vulva development. Development 132 (2005) 1413-1428
72. Yeoh E.J., Ross M.E., Shurtleff S.A., Williams W.K., Patel D., Mahfouz R., Behm F.G., Raimondi S.C., Relling M.V., Patel A., Cheng C., Campana D., Wilkins D., Zhou X., Li J., Liu H., Pui C.H., Evans W.E., Naeve C., Wong L., and Downing J.R. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell. 1 (2002) 133-143
73. Zinkel S.S., Ong C.C., Ferguson D.O., Iwasaki H., Akashi K., Bronson R.T., Kutok J.L., Alt F.W., and Korsmeyer S.J. Proapoptotic BID is required for myeloid homeostasis and tumor suppression. Genes Dev. 17 (2003) 229-239