RUNX genes find a niche in stem cell biology

Journal of Cellular Biochemistry

Volumn 108, Issue 1, 2009, Pages 14-21

  Appleford, Peter J ^a   Woollard, Alison ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

C. elegans; Hair follicle; Hematopoiesis; RUNX; Stem cells

Indexed keywords

TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR RUNX1;

ACUTE GRANULOCYTIC LEUKEMIA; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE; GENE FUNCTION; HAIR FOLLICLE; HEMATOPOIESIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RUNX GENE; STEM CELL;

ANIMALS; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA SUBUNITS; HEMATOPOIETIC STEM CELLS; HUMANS;

ANIMALIA; CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 69249142281     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22249     Document Type: Review

References (53)

1. Ahn MY, Huang G, Bae SC, Wee HJ, Kim WY, Ito Y. 1998. Negative regulation of granulocytic differentiation in the myeloid precursor cell line 32Dcl3 by ear-2, a mammalian homolog of Drosophila seven-up, and a chimeric leukemogenic gene, AML1/ETO. Proc Natl Acad Sci USA 95:1812-1817.
2. Aronson BD, Fisher AL, Blechman K, Caudy M, Gergen JP. 1997. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol Cell Biol 17:5581-5587.
3. Bernardin-Fried F, Kummalue T, Leijen S, Collector MI, Ravid K, Friedman AD. 2004. AML1/RUNX1 increases during G1 to S cell cycle progression independent of cytokine-dependent phosphorylation and induces cyclin D3 gene expression. J Biol Chem 279:15678-15687.
4. Cameron ER, Neil JC. 2004. The Runx genes: Lineage-specific oncogenes and tumor suppressors. Oncogene 23:4308-4314.
5. Camilleri S, McDonald F. 2006. Runx2 and dental development. Eur J Oral Sci 114:361-373.
6. Chen CL, Broom DC, Liu Y, de Nooij JC, Li Z, Cen C, Samad OA, Jessell TM, Woolf CJ, Ma Q. 2006. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365-377.
7. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. 2009. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457:887-891.
8. Coffman JA. 2003. Runx transcription factors and the developmental balance between cell proliferation and differentiation. Cell Biol Int 27:315-324.
9. Coffman JA, Kirchhamer CV, Harrington MG, Davidson EH. 1996. SpRunt-1, a new member of the runt domain family of transcription factors, is a positive regulator of the aboral ectoderm-specific CyIIIA gene in sea urchin embryos. Dev Biol 174:43-54.
10. Erickson P, Gao J, Chang KS, Look T, Whisenant E, Raimondi S, Lasher R, Trujillo J, Rowley J, Drabkin H. 1992. Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood 80:1825-1831.
11. Fuchs E, Tumbar T, Guasch G. 2004. Socializing with the neighbors: Stem cells and their niche. Cell 116:769-778.
12. Fukuyama M, Gendreau SB, Derry WB, Rothman JH. 2003. Essential embryonic roles of the CKI-1 cyclin-dependent kinase inhibitor in cell-cycle exit and morphogenesis in C. elegans. Dev Biol 260:273-286.
13. Galindo M, Pratap J, Young DW, Hovhannisyan H, Im HJ, Choi JY, Lian JB, Stein JL, Stein GS, van Wijnen AJ. 2005. The bone-specific expression of Runx2 oscillates during the cell cycle to support a G1-related antiproliferative function in osteoblasts. J Biol Chem 280:20274-20285.
14. Gergen JP, Butler BA. 1988. Isolation of the Drosophila segmentation gene runt and analysis of its expression during embryogenesis. Genes Dev 2:1179-1193.
15. Growney JD, Shigematsu H, Li Z, Lee BH, Adelsperger J, Rowan R, Curley DP, Kutok JL, Akashi K, Williams IR, Speck NA, Gilliland DG. 2005. Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood 106:494-504.
16. Hodgkin J. 1983. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103:43-64.
17. Huang G, Shigesada K, Ito K, Wee HJ, Yokomizo T, Ito Y. 2001. Dimerization with PEBP2beta protects RUNX1/AML1 from ubiquitin-proteasome- mediated degradation. EMBO J 20:723-733.
18. Ichikawa M, Goyama S, Asai T, Kawazu M, Nakagawa M, Takeshita M, Chiba S, Ogawa S, Kurokawa M. 2008. AML1/Runx1 negatively regulates quiescent hematopoietic stem cells in adult hematopoiesis. J Immunol 180:4402-4408.
19. Inoue K, Ozaki S, Shiga T, Ito K, Masuda T, Okado N, Iseda T, Kawaguchi S, Ogawa M, Bae SC, Yamashita N, Itohara S, Kudo N, Ito Y. 2002. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat Neurosci 5:946-954.
20. Inoue K, Ito K, Osato M, Lee B, Bae SC, Ito Y. 2007. The transcription factor Runx3 represses the neurotrophin receptor TrkB during lineage commitment of dorsal root ganglion neurons. J Biol Chem 282:24175-24184.
21. Ito K, Inoue KI, Bae SC, Ito Y. 2009. Runx3 expression in gastrointestinal tract epithelium: Resolving the controversy. Oncogene 28:1379-1384.
22. Kagoshima H, Shigesada K, Satake M, Ito Y, Miyoshi H, Ohki M, Pepling M, Gergen P. 1993. The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet 9:338-341.
23. Kagoshima H, Akamatsu Y, Ito Y, Shigesada K. 1996. Functional dissection of the alpha and beta subunits of transcription factor PEBP2 and the redox susceptibility of its DNA binding activity. J Biol Chem 271:33074-33082.
24. Kagoshima H, Sawa H, Mitani S, Burglin TR, Shigesada K, Kohara Y. 2005. The C. elegans RUNX transcription factor RNT-1/MAB-2 is required for asymmetrical cell division of the T blast cell. Dev Biol 287:262-273.
25. Kagoshima H, Nimmo R, Saad N, Tanaka J, Miwa Y, Mitani S, Kohara Y, Woollard A. 2007. The C. elegans CBFbeta homologue BRO-1 interacts with the Runx factor, RNT-1, to promote stem cell proliferation and self-renewal. Development 134:3905-3915.
26. Kamachi Y, Ogawa E, Asano M, Ishida S, Murakami Y, Satake M, Ito Y, Shigesada K. 1990. Purification of a mouse nuclear factor that binds to both the A and B cores of the polyomavirus enhancer. J Virol 64:4808-4819.
27. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
28. Lebestky T, Chang T, Hartenstein V, Banerjee U. 2000. Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288:146-149.
29. Lee B, Thirunavukkarasu K, Zhou L, Pastore L, Baldini A, Hecht J, Geoffroy V, Ducy P, Karsenty G. 1997. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat Genet 16:307-310.
30. Lee J, Ahnn J, Bae SC. 2004. Homologs of RUNX and CBF beta/PEBP2 beta in C. elegans. Oncogene 23:4346-4352.
31. Levanon D, Brenner O, Otto F, Groner Y. 2003. Runx3 knockouts and stomach cancer. EMBO Rep 4:560-564.
32. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, Lee KY, Nomura S, Lee CW, Han SB, Kim HM, Kim WJ, Yamamoto H, Yamashita N, Yano T, Ikeda T, Itohara S, Inazawa J, Abe T, Hagiwara A, Yamagishi H, Ooe A, Kaneda A, Sugimura T, Ushijima T, Bae SC, Ito Y. 2002. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109:113-124.
33. Licht JD. 2001. AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML. Oncogene 20:5660-5679.
34. Liu P, Tarle SA, Hajra A, Claxton DF, Marlton P, Freedman M, Siciliano MJ, Collins FS. 1993. Fusion between transcription factor CBF beta/PEBP2 beta and a myosin heavy chain in acute myeloid leukemia. Science 261:1041-1044.
35. Lou J, Cao W, Bernardin F, Ayyanathan K, Rauscher IF, Friedman AD. 2000. Exogenous cdk4 overcomes reduced cdk4 RNA and inhibition of G1 progression in hematopoietic cells expressing a dominant-negative CBF - A model for overcoming inhibition of proliferation by CBF oncoproteins. Oncogene 19:2695-2703.
36. Miyoshi H, Shimizu K, Kozu T, Maseki N, Kaneko Y, Ohki M. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci USA 88:10431-10434.
37. Niebuhr B, Fischer M, Tager M, Cammenga J, Stocking C. 2008. Gatekeeper function of the RUNX1 transcription factor in acute leukemia. Blood Cells Mol Dis 40:211-218.
38. Nimmo R, Woollard A. 2008. Worming out the biology of Runx. Dev Biol 313:492-500.
39. Nimmo R, Antebi A, Woollard A. 2005. mab-2 encodes RNT-1, a C. elegans Runx homologue essential for controlling cell proliferation in a stem cell-like developmental lineage. Development 132:5043-5054.
40. North TE, Stacy T, Matheny CJ, Speck NA, de Bruijn MF. 2004. Runx1 is expressed in adult mouse hematopoietic stem cells and differentiating myeloid and lymphoid cells, but not in maturing erythroid cells. Stem Cells 22:158-168.
41. Ogawa E, Maruyama M, Kagoshima H, Inuzuka M, Lu J, Satake M, Shigesada K, Ito Y. 1993. PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc Natl Acad Sci USA 90:6859-6863.
42. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321-330.
43. Okuda T, Cai Z, Yang S, Lenny N, Lyu CJ, van Deursen JM, Harada H, Downing JR. 1998. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood 91:3134-3143.
44. Osorio KM, Lee SE, McDermitt DJ, Waghmare SK, Zhang YV, Woo HN, Tumbar T. 2008. Runx1 modulates developmental, but not injury-driven, hair follicle stem cell activation. Development 135:1059-1068.
45. Raveh E, Cohen S, Levanon D, Negreanu V, Groner Y, Gat U. 2006. Dynamic expression of Runx1 in skin affects hair structure. Mech Dev 123:842-850.
46. Rennert J, Coffman JA, Mushegian AR, Robertson AJ. 2003. The evolution of Runx genes I. A comparative study of sequences from phylogenetically diverse model organisms. BMC Evol Biol 3:4.
47. Strom DK, Nip J, Westendorf JJ, Linggi B, Lutterbach B, Downing JR, Lenny N, Hiebert SW. 2000. Expression of the AML-1 oncogene shortens the G(1) phase of the cell cycle. J Biol Chem 275:3438-3845.
48. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110-156.
49. van Wijnen AJ, Stein GS, Gergen JP, Groner Y, Hiebert SW, Ito Y, Liu P, Neil JC, Ohki M, Speck N. 2004. Nomenclature for Runt-related (RUNX) proteins. Oncogene 23:4209-4210.
50. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci USA 93:3444-3449.
51. Wheeler JC, Shigesada K, Gergen JP, Ito Y. 2000. Mechanisms of transcriptional regulation by Runt domain proteins. Semin Cell Dev Biol 11:369-375.
52. Wunderlich M, Krejci O, Wei J, Mulloy JC. 2006. Human CD34+ cells expressing the inv(16) fusion protein exhibit a myelomonocytic phenotype with greatly enhanced proliferative ability. Blood 108:1690-1697.
53. Yamagata T, Maki K, Mitani K. 2005. Runx1/AML1 in normal and abnormal hematopoiesis. Int J Hematol 82:1-8.