Hoxa9 Transduction Induces Hematopoietic Stem and Progenitor Cell Activity through Direct Down-Regulation of Geminin Protein

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Ohno, Yoshinori ^a   Yasunaga, Shin'ichiro ^a   Janmohamed, Salima ^b   Ohtsubo, Motoaki ^a,c   Saeki, Keita ^a   Kurogi, Toshiaki ^a   Mihara, Keichiro ^a   Iscove, Norman N ^b   Takihara, Yoshihiro ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b UNIVERSITY OF TORONTO   (Canada)

^c BEPPU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GEMININ; NUCLEOPORIN 98; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HOXA9; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HOX GENE; HOXA9 GENE; HOXB4 GENE; HOXC13 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; NUP98 GENE; PROTEIN EXPRESSION; UBIQUITINATION; UPREGULATION;

ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; COLONY-FORMING UNITS ASSAY; CULLIN PROTEINS; DNA-BINDING PROTEINS; DOWN-REGULATION; HEK293 CELLS; HEMATOPOIETIC STEM CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOBLOTTING; MICE; MICE, INBRED C57BL; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN BINDING; RETROVIRIDAE; RNA INTERFERENCE; SF9 CELLS; TRANSDUCTION, GENETIC; UBIQUITINATION;

EID: 84872260401     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053161     Document Type: Article

References (52)

1. McGinnis W, Krumlauf R, (1992) Homeobox genes and axial patterning. Cell 68: 283-302.
2. McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ, (1984) A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308: 428-433.
3. Levine M, Hoey T, (1988) Homeobox proteins as sequence-specific transcription factors. Cell 55: 537-540.
4. Sauvageau G, Thorsteinsdottir U, Eaves CJ, Lawrence HJ, Largman C, et al. (1995) Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev 9: 1753-1765.
5. Thorsteinsdottir U, Mamo A, Kroon E, Jerome L, Bijl J, et al. (2002) Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 99: 121-129.
6. Armstrong SA, Staunton JE, Silverman LB, Pieters R, den Boer ML, et al. (2002) MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 30: 41-47.
7. Milne TA, Martin ME, Brock HW, Slany RK, Hess J, (2005) Leukemogenic MLL fusion proteins bind across a broad region of the Hox a9 locus, promoting transcription and multiple histone modifications. Cancer Res 65: 11367-11374.
8. Faber J, Krivtsov AV, Stubbs MC, Wright R, Davis TN, et al. (2009) HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood 113: 2375-2385.
9. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, et al. (1999) Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286: 531-537.
10. Ito T, Kwon HY, Zimdahl B, Congdon KL, Blum J, et al. (2010) Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 466: 765-768.
11. Moore MA, (2005) Converging pathways in leukemogenesis and stem cell self-renewal. Exp Hematol 33: 719-737.
12. Kroon E, Thorsteinsdottir U, Mayotte N, Nakamura T, Sauvageau G, (2001) NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J 20: 350-361.
13. Pineault N, Buske C, Feuring-Buske M, Abramovich C, Rosten P, et al. (2003) Induction of acute myeloid leukemia in mice by the human leukemia-specific fusion gene NUP98-HOXD13 in concert with Meis1. Blood 101: 4529-4538.
14. Lin YW, Slape C, Zhang Z, Aplan PD, (2005) NUP98-HOXD13 transgenic mice develop a highly penetrant, severe myelodysplastic syndrome that progresses to acute leukemia. Blood 106: 287-295.
15. Iwasaki M, Kuwata T, Yamazaki Y, Jenkins NA, Copeland NG, (2005) Identification of cooperative genes for NUP98-HOXA9 in myeloid leukemogenesis using a mouse model. Blood 105: 784-793.
16. Lei H, Wang H, Juan AH, Ruddle FH, (2005) The identification of Hoxc8 target genes. Proc Natl Acad Sci U S A 102: 2420-2424.
17. Chen H, Rubin E, Zhang H, Chung S, Jie CC, et al. (2005) Identification of transcriptional targets of HOXA5. J Biol Chem 280: 19373-19380.
18. Schiedlmeier B, Santos AC, Ribeiro A, Moncaut N, Lesinski D, et al. (2007) HOXB4's road map to stem cell expansion. Proc Natl Acad Sci U S A 104: 16952-16957.
19. Oshima M, Endoh M, Endo TA, Toyoda T, Nakajima-Takagi Y, et al. (2011) Genome-wide analysis of target genes regulated by HoxB4 in hematopoietic stem and progenitor cells developing from embryonic stem cells. Blood 117: 142-150.
20. Takihara Y, Hara J, (2000) Polycomb-group genes and hematopoiesis. Int J Hematol 72: 165-172.
21. Ohtsubo M, Yasunaga S, Ohno Y, Tsumura M, Okada S, et al. (2008) Polycomb-group complex 1 acts as an E3 ubiquitin ligase for Geminin to sustain hematopoietic stem cell activity. Proc Natl Acad Sci U S A 105: 10396-10401.
22. Takihara Y, (2008) Role of Polycomb-group genes in normal and malignant stem cells. Int J Hematol 87: 25-34.
23. Ohno Y, Yasunaga S, Ohtsubo M, Mori S, Tsumura M, et al. (2010) Hoxb4 transduction down-regulates Geminin protein, providing hematopoietic stem and progenitor cells with proliferation potential. Proc Natl Acad Sci U S A 107: 21529-21534.
24. Blow JJ, Hodgson B, (2002) Replication licensing-defining the proliferative state? Trends in Cell Biol 12: 72-78.
25. Lutzmann M, Maiorano D, Méchali M, (2006) A Cdt1-geminin complex licenses chromatin for DNA replication and prevents rereplication during S phase in Xenopus. EMBO J 25: 5764-5774.
26. Wohlschlege JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, et al. (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290: 2309-2312.
27. Kroll KL, Salic AN, Evans LM, Kirschner MW, (1998) Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 125: 3247-3258.
28. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, et al. (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19: 1723-1734.
29. Luo LYX, Takihara Y, Knoetgen H, Kessel M, (2004) The cell-cycle regulator geminin inhibits Hox function through direct and polycomb-mediated interactions. Nature 427: 749-753.
30. Del Bene F, Tessmar-Raible K, Wittbrodt J, (2004) Direct interaction of geminin and Six3 in eye development. Nature 427: 745-749.
31. Kim MY, Jeong BC, Lee JH, Kee HJ, Kook H, et al. (2006) A repressor complex, AP4 transcription factor and geminin, negatively regulates expression of target genes in nonneuronal cells. Proc Natl Acad Sci U S A 103: 13074-13079.
32. Gonzalez MA, Tachibana KE, Adams DJ, van der Weyden L, Hemberger M, et al. (2006) Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev 20: 1880-1884.
33. Shinnick KM, Eklund EA, McGarry TJ, (2010) Geminin deletion from hematopoietic cells causes anemia and thrombocytosis in mice. J Clin Invest 120: 4303-4315.
34. McGarry TJ, Kirschner MW, (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93: 1043-1053.
35. Yang VS, Carter SA, Hyland SJ, Tachibana-Konwalski K, Laskey RA, et al. (2011) Geminin escapes degradation in G1 of mouse pluripotent cells and mediates the expression of Oct4, Sox2, and Nanog. Curr Biol 21: 692-699.
36. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, et al. (2008) Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135: 1118-1129.
37. Ohtsubo M, Okazaki H, Nishimoto T, (1989) The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J Cell Biol 109: 1389-1397.
38. Morita S, Kojima T, Kitamura T, (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063-1066.
39. Ohta H, Sawada A, Kim JY, Tokimasa S, Nishiguchi S, et al. (2002) Polycomb group gene rae28 is required for sustaining activity of hematopoietic stem cells. J Exp Med 195: 759-770.
40. Vaughn JL, Goodwin RH, Tompkins GJ, McCawley P, (1977) The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro 13: 213-217.
41. Zhang Y, Morrone G, Zhang J, Chen X, Lu X, et al. (2003) CUL-4A stimulates ubiquitylation and degradation of the HOXA9 homeodomain protein. EMBO J 22: 6057-6067.
42. Osawa M, Hanada K, Hamada H, Nakauchi H, (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245.
43. Chung KY, Morrone G, Schuringa JJ, Plasilova M, Shieh JH, et al. (2006) Enforced expression of NUP98-HOXA9 in human CD34(+) cells enhances stem cell proliferation. Cancer Res 66: 11781-11191.
44. Brun AC, Björnsson JM, Magnusson M, Larsson N, Leveén P, et al. (2004) Hoxb4-deficient mice undergo normal hematopoietic development but exhibit a mild proliferation defect in hematopoietic stem cells. Blood 103: 4126-4133.
45. Lawrence HJ, Helgason CD, Sauvageau G, Fong S, Izon DJ, et al. (1997) Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 89: 1922-1930.
46. Lawrence HJ, Christensen J, Fong S, Hu YL, Weissman I, et al. (2005) Loss of expression of the Hoxa-9 homeobox gene impairs the proliferation and repopulating ability of hematopoietic stem cells. Blood 106: 3988-3994.
47. Lebert-Ghali CE, Fournier M, Dickson GJ, Thompson ASG, Bijl JJ, (2010) HoxA cluster is haploinsufficient for activity of hematopoietic stem and progenitor cells. Exp Hematol 38: 1074-1086.
48. Di-Poï N, Koch U, Radtke F, Duboule D, (2010) Additive and global functions of HoxA cluster genes in mesoderm derivatives. Dev Biol 341: 488-498.
49. Bijl J, Thompson A, Ramirez-Solis R, Krosl J, Grier DG, et al. (2006) Analysis of HSC activity and compensatory Hox gene expression profile in Hoxb cluster mutant fetal liver cells. Blood 108: 116-122.
50. Kasper LH, Brindle PK, Schnabel CA, Pritchard CE, Cleary ML, et al. (1999) CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol Cell Biol 19: 764-776.
51. Yamada T, Shimizu T, Suzuki M, Kihara-Negishi F, Nanashima N, et al. (2008) Interaction between the homeodomain protein HOXC13 and ETS family transcription factor PU.1 and its implication in the differentiation of murine erythroleukemia cells. Exp Cell Res 314: 847-858.
52. Comelli L, Marchetti L, Arosio D, Riva S, Abdurashidova G, et al. (2009) The homeotic protein HOXC13 is a member of human DNA replication complexes. Cell Cycle 8: 454-459.