Prep1 and Meis1 competition for Pbx1 binding regulates protein stability and tumorigenesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 10, 2014, Pages

  Dardaei, Leila ^a   Longobardi, Elena ^a   Blasi, Francesco ^a  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; DEAD BOX PROTEIN; DEAD BOX PROTEIN 3; DEAD BOX PROTEIN P68; MESSENGER RNA; MYELOID ECOTROPIC VIRAL INTEGRATION SITE 1; ONCOPROTEIN; PBX REGULATING PROTEIN 1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR PBX1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BRAIN TUMOR; CARCINOGENESIS; CARCINOGENIC ACTIVITY; CARCINOGENICITY; CELL COUNT; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; COLONY FORMATION; CONTROLLED STUDY; DELETION MUTANT; DNA BINDING; DOWN REGULATION; FIBROBLAST; GENE ONTOLOGY; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC REGULATION; GENOTYPE; GROWTH RATE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; IN VITRO STUDY; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; BINDING, COMPETITIVE; CARCINOGENESIS; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DEAD-BOX RNA HELICASES; DNA PRIMERS; HOMEODOMAIN PROTEINS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MICE; MICE, NUDE; NEOPLASM PROTEINS; PROTEIN STABILITY; REAL-TIME POLYMERASE CHAIN REACTION; RNA HELICASES; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84896287615     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321200111     Document Type: Article

References (44)

1. Moens CB, Selleri L (2006) Hox cofactors in vertebrate development. Dev Biol 291(2): 193-206.
2. Longobardi E, et al. (2014) Biochemistry of the tale transcription factors PREP, MEIS, and PBX in vertebrates. Dev Dyn 243(1):59-75.
3. Knoepfler PS, Calvo KR, Chen H, Antonarakis SE, Kamps MP (1997) Meis1 and pKnox1 bind DNA cooperatively with Pbx1 utilizing an interaction surface disrupted in oncoprotein E2a-Pbx1. Proc Natl Acad Sci USA 94(26):14553-14558.
4. Berthelsen J, Kilstrup-Nielsen C, Blasi F, Mavilio F, Zappavigna V (1999) The subcellular localization of PBX1 and EXD proteins depends on nuclear import and export signals and is modulated by association with PREP1 and HTH. Genes Dev 13(8):946-953.
5. Longobardi E, Blasi F (2003) Overexpression of PREP-1 in F9 teratocarcinoma cells leads to a functionally relevant increase of PBX-2 by preventing its degradation. J Biol Chem 278(40):39235-39241.
6. Ferretti E, et al. (2000) Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 127(1):155-166.
7. Ferretti E, Schulz H, Talarico D, Blasi F, Berthelsen J (1999) The PBX-regulating protein PREP1 is present in different PBX-complexed forms in mouse. Mech Dev 83(1-2):53-64.
8. Jacobs Y, Schnabel CA, Cleary ML (1999) Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol Cell Biol 19(7): 5134-5142.
9. Kroon E, et al. (1998) Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J 17(13):3714-3725.
10. Lawrence HJ, et al. (1999) Frequent co-expression of the HOXA9 and MEIS1 homeobox genes in human myeloid leukemias. Leukemia 13(12):1993-1999.
11. Imamura T, et al. (2002) Frequent co-expression of HoxA9 and Meis1 genes in infant acute lymphoblastic leukaemia with MLL rearrangement. Br J Haematol 119(1): 119-121.
12. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML (2007) Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev 21(21): 2762-2774.
13. Baird K, et al. (2005) Gene expression profiling of human sarcomas: Insights into sarcoma biology. Cancer Res 65(20):9226-9235.
14. Crijns AP, et al. (2007) MEIS and PBX homeobox proteins in ovarian cancer. Eur J Cancer 43(17):2495-2505.
15. Spieker N, et al. (2001) The MEIS1 oncogene is highly expressed in neuroblastoma and amplified in cell line IMR32. Genomics 71(2):214-221.
16. Ferretti E, et al. (2006) Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol Cell Biol 26(15):5650-5662.
17. Longobardi E, et al. (2010) Prep1 (pKnox1)-deficiency leads to spontaneous tumor development in mice and accelerates EmuMyc lymphomagenesis: A tumor suppressor role for Prep1. Mol Oncol 4(2):126-134.
18. Thorsteinsdottir U, Kroon E, Jerome L, Blasi F, Sauvageau G (2001) Defining roles for HOX and MEIS1 genes in induction of acute myeloid leukemia. Mol Cell Biol 21(1): 224-234.
19. Iotti G, et al. (2011) Homeodomain transcription factor and tumor suppressor Prep1 is required to maintain genomic stability. Proc Natl Acad Sci USA 108(29):E314-E322.
20. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88(5):593-602.
21. MacPherson I, Montagnier L (1964) Agar suspension culture for the selective assay of cells transformed by polyoma virus. Virology 23:291-294.
22. Freedman VH, Shin SI (1974) Cellular tumorigenicity in nude mice: Correlation with cell growth in semi-solid medium. Cell 3(4):355-359.
23. Jalal C, Uhlmann-Schiffler H, Stahl H (2007) Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res 35(11):3590-3601.
24. Penkov D, et al. (2013) Analysis of the DNA-binding profile and function of TALE homeoproteins reveals their specialization and specific interactions with Hox genes/ proteins. Cell Rep 3(4):1321-1333.
25. Micali N, Ferrai C, Fernandez-Diaz LC, Blasi F, Crippa MP (2009) Prep1 directly regulates the intrinsic apoptotic pathway by controlling Bcl-XL levels. Mol Cell Biol 29(5): 1143-1151.
26. Micali N, et al. (2010) Down syndrome fibroblasts and mouse Prep1-overexpressing cells display increased sensitivity to genotoxic stress. Nucleic Acids Res 38(11):3595-3604.
27. Díaz VM, et al. (2007) p160 Myb-binding protein interacts with Prep1 and inhibits its transcriptional activity. Mol Cell Biol 27(22):7981-7990.
28. Díaz VM, Bachi A, Blasi F (2007) Purification of the Prep1 interactome identifies novel pathways regulated by Prep1. Proteomics 7(15):2617-2623.
29. Botlagunta M, et al. (2008) Oncogenic role of DDX3 in breast cancer biogenesis. Oncogene 27(28):3912-3922.
30. Causevic M, et al. (2001) Overexpression and poly-ubiquitylation of the DEAD-box RNA helicase p68 in colorectal tumours. Oncogene 20(53):7734-7743.
31. Lai MC, Chang WC, Shieh SY, Tarn WY (2010) DDX3 regulates cell growth through translational control of cyclin E1. Mol Cell Biol 30(22):5444-5453.
32. Jones TA, Flomen RH, Senger G, Nizeti-C D, Sheer D (2000) The homeobox gene MEIS1 is amplified in IMR-32 and highly expressed in other neuroblastoma cell lines. Eur J Cancer 36(18):2368-2374.
33. Grandori C, Cowley SM, James LP, Eisenman RN (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 16:653-699.
34. Wang GG, Pasillas MP, Kamps MP (2005) Meis1 programs transcription of FLT3 and cancer stem cell character, using a mechanism that requires interaction with Pbx and a novel function of the Meis1 C-terminus. Blood 106(1):254-264.
35. Mamo A, et al. (2006) Molecular dissection of Meis1 reveals 2 domains required for leukemia induction and a key role for Hoxa gene activation. Blood 108(2):622-629.
36. Bisaillon R, Wilhelm BT, Krosl J, Sauvageau G (2011) C-terminal domain of MEIS1 converts PKNOX1 (PREP1) into a HOXA9-collaborating oncoprotein. Blood 118(17): 4682-4689.
37. Land H, Parada LF, Weinberg RA (1983) Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304(5927):596-602.
38. Schröder M (2010) Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem Pharmacol 79(3):297-306.
39. Fuller-Pace FV (2006) DExD/H box RNA helicases: Multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res 34(15):4206-4215.
40. Shin S, Rossow KL, Grande JP, Janknecht R (2007) Involvement of RNA helicases p68 and p72 in colon cancer. Cancer Res 67(16):7572-7578.
41. Rossow KL, Janknecht R (2003) Synergism between p68 RNA helicase and the transcriptional coactivators CBP and p300. Oncogene 22(1):151-156.
42. Wortham NC, et al. (2009) The DEAD-box protein p72 regulates ERalpha-/oestrogendependent transcription and cell growth, and is associated with improved survival in ERalpha-positive breast cancer. Oncogene 28(46):4053-4064.
43. Ji T, Lee M, Pruitt SC, Hangauer DG (2004) Privileged scaffolds for blocking proteinprotein interactions: 1, 4-disubstituted naphthalene antagonists of transcription factor complex HOX-PBX/DNA. Bioorg Med Chem Lett 14(15):3875-3879.
44. Hulsen T, de Vlieg J, Alkema W (2008) BioVenn- A web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488.