The evolutionary origin of the Runx/CBFbeta transcription factors - Studies of the most basal metazoans

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Sullivan, James C ^a   Sher, Daniel ^b   Eisenstein, Miriam ^c   Shigesada, Katsuya ^d   Reitzel, Adam M ^a   Marlow, Heather ^e   Levanon, Ditsa ^c   Groner, Yoram ^c   Finnerty, John R ^a   Gat, Uri ^b  

^a Boston University   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d DOSHISHA UNIVERSITY   (Japan)

^e UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORE BINDING FACTOR BETA; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR;

ARTICLE; COELENTERATE; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; ECTODERM; IN SITU HYBRIDIZATION; METAZOON; NERVE CELL; NONHUMAN; PHYLOGENY; PROTEIN EXPRESSION; REGENERATIVE ABILITY; SPONGE (PORIFERA); STEM CELL; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; CONTIG MAPPING; EXPRESSED SEQUENCE TAG; GENETICS; MOLECULAR EVOLUTION; PROTEIN CONFORMATION;

ANIMALIA; BILATERIA; CNIDARIA; HEXAPODA; MAMMALIA; METAZOA; NEMATOSTELLA;

ANIMALS; CNIDARIA; CONTIG MAPPING; CORE BINDING FACTOR ALPHA SUBUNITS; CORE BINDING FACTOR BETA SUBUNIT; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; MODELS, MOLECULAR; PHYLOGENY; PORIFERA; PROTEIN CONFORMATION; TRANSCRIPTION FACTORS;

EID: 50449100342     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-228     Document Type: Article

References (83)

1. Blood cells and blood cell development in the animal kingdom. V Hartenstein, Annu Rev Cell Dev Biol 2006 22 677 712 10.1146/annurev.cellbio.22. 010605.093317 16824014
2. The Molecular Control of Corpus Luteum Formation, Function, and Regression. C Stocco C Telleria G Gibori, Endocr Rev 2007 28 1 117 149 10.1210/er.2006-0022 17077191
3. Controls of hair follicle cycling. KS Stenn R Paus, Physiol Rev 2001 81 1 449 494 11152763
4. Matrix metalloproteinases and the regulation of tissue remodelling. A Page-McCaw AJ Ewald Z Werb, Nat Rev Mol Cell Biol 2007 8 3 221 233 10.1038/nrm2125 17318226
5. Stem cells and their applications in skin-cell therapy. C Shi Y Zhu Y Su T Cheng, Trends in Biotechnology 2006 24 1 48 52 10.1016/j.tibtech.2005.11.003 16298447
6. Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. TC Bosch, Dev Biol 2007 303 2 421 433 10.1016/j.ydbio.2006.12.012 17234176
7. The evolution of Runx genes I. A comparative study of sequences from phylogenetically diverse model organisms. J Rennert JA Coffman AR Mushegian AJ Robertson, BMC Evol Biol 2003 3 4 12659662 10.1186/1471-2148-3-4
8. Structure and regulated expression of mammalian RUNX genes. D Levanon Y Groner, Oncogene 2004 23 24 4211 4219 10.1038/sj.onc.1207670 15156175
9. Evaluation of developmental phenotypes produced by morpholino antisense targeting of a sea urchin Runx gene. JA Coffman C Dickey-Sims JS Haug JJ McCarthy AJ Robertson, BMC Biol 2004 2 6 15132741 10.1186/1741-7007-2-6
10. Runx-dependent expression of PKC is critical for cell survival in the sea urchin embryo. C Dickey-Sims AJ Robertson DE Rupp JJ McCarthy JA Coffman, BMC Biol 2005 3 18 16076398 10.1186/1741-7007-3-18
11. CBFbeta is a facultative Runx partner in the sea urchin embryo. AJ Robertson C Dickey-Sims A Ransick DE Rupp JJ McCarthy JA Coffman, BMC Biol 2006 4 4 16469111 10.1186/1741-7007-4-4
12. Osteogenic transcription factor Runx2 is a maternal determinant of dorsoventral patterning in zebrafish. MV Flores EY Lam KE Crosier PS Crosier, Nat Cell Biol 2008 10 3 346 352 10.1038/ncb1697 18246063
13. Runx1 is expressed in adult mouse hematopoietic stem cells and differentiating myeloid and lymphoid cells, but not in maturing erythroid cells. TE North T Stacy CJ Matheny NA Speck MF de Bruijn, Stem Cells 2004 22 2 158 168 10.1634/stemcells.22-2-158 14990855
14. mab-2 encodes RNT-1, a C. elegans Runx homologue essential for controlling cell proliferation in a stem cell-like developmental lineage. R Nimmo A Antebi A Woollard, Development 2005 132 22 5043 5054 10.1242/dev.02102 16236764
15. Dynamic expression of Runx1 in skin affects hair structure. E Raveh S Cohen D Levanon V Negreanu Y Groner U Gat, Mech Dev 2006 17011173
16. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Q Wang T Stacy M Binder M Marin-Padilla AH Sharpe NA Speck, Proc Natl Acad Sci U S A 1996 93 8 3444 3449 8622955 10.1073/pnas.93.8.3444
17. AML1 and the 8;21 and 3;21 translocations in acute and chronic myeloid leukemia. G Nucifora JD Rowley, Blood 1995 86 1 1 14 7795214
18. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. MF de Bruijn NA Speck MC Peeters E Dzierzak, Embo J 2000 19 11 2465 2474 10835345 10.1093/emboj/19.11.2465
19. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. F Otto AP Thornell T Crompton A Denzel KC Gilmour IR Rosewell GW Stamp RS Beddington S Mundlos BR Olsen PB Selby MJ Owen, Cell 1997 89 5 765 771 10.1016/S0092-8674(00) 80259-7 9182764
20. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. P Ducy R Zhang V Geoffroy AL Ridall G Karsenty, Cell 1997 89 5 747 754 10.1016/S0092-8674(00)80257-3 9182762
21. Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. JB Lian A Javed SK Zaidi C Lengner M Montecino AJ van Wijnen JL Stein GS Stein, Crit Rev Eukaryot Gene Expr 2004 14 1-2 1 41 10.1615/CritRevEukaryotGeneExpr.v14.i12.10 15104525
22. Networks and hubs for the transcriptional control of osteoblastogenesis. JB Lian GS Stein A Javed AJ van Wijnen JL Stein M Montecino MQ Hassan T Gaur CJ Lengner DW Young, Rev Endocr Metab Disord 2006 17051438
23. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. T Komori H Yagi S Nomura A Yamaguchi K Sasaki K Deguchi Y Shimizu RT Bronson YH Gao M Inada M Sato R Okamoto Y Kitamura S Yoshiki T Kishimoto, Cell 1997 89 5 755 764 10.1016/S0092-8674(00)80258-5 9182763
24. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. D Levanon D Bettoun C Harris-Cerruti E Woolf V Negreanu R Eilam Y Bernstein D Goldenberg C Xiao M Fliegauf E Kremer F Otto O Brenner A Lev-Tov Y Groner, Embo J 2002 21 13 3454 3463 12093746 10.1093/emboj/cdf370
25. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. K Inoue S Ozaki T Shiga K Ito T Masuda N Okado T Iseda S Kawaguchi M Ogawa SC Bae N Yamashita S Itohara N Kudo Y Ito, Nat Neurosci 2002 5 10 946 954 10.1038/nn925 12352981
26. Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. JD Growney H Shigematsu Z Li BH Lee J Adelsperger R Rowan DP Curley JL Kutok K Akashi IR Williams NA Speck DG Gilliland, Blood 2005 106 2 494 504 15784726 10.1182/blood-2004-08-3280
27. High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. V Geoffroy M Kneissel B Fournier A Boyde P Matthias, Mol Cell Biol 2002 22 17 6222 6233 12167715 10.1128/MCB.22.17.6222-6233.2002
28. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. O Fainaru E Woolf J Lotem M Yarmus O Brenner D Goldenberg V Negreanu Y Bernstein D Levanon S Jung Y Groner, Embo J 2004 23 4 969 979 14765120 10.1038/sj.emboj.7600085
29. Upstream and downstream targets of RUNX proteins. F Otto M Lubbert M Stock, J Cell Biochem 2003 89 1 9 18 10.1002/jcb.10491 12682904
30. Runx transcription factors and the developmental balance between cell proliferation and differentiation. JA Coffman, Cell Biol Int 2003 27 4 315 324 10.1016/S1065-6995(03)00018-0 12788047
31. Mammalian runt-domain proteins and their roles in hematopoiesis, osteogenesis, and leukemia. JJ Westendorf SW Hiebert, J Cell Biochem 1999 Suppl 32-33 51 58 10.1002/(SICI)1097-4644(1999)75:32+<51::AID-JCB7>3.0.CO;2-S 10629103
32. Function of CBFbeta/Bro proteins. N Adya LH Castilla PP Liu, Semin Cell Dev Biol 2000 11 5 361 368 10.1006/scdb.2000.0189 11105900
33. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. D Levanon RE Goldstein Y Bernstein H Tang D Goldenberg S Stifani Z Paroush Y Groner, Proc Natl Acad Sci U S A 1998 95 20 11590 11595 9751710 10.1073/pnas.95.20.11590
34. Redox regulation of the DNA binding activity in transcription factor PEBP2. The roles of two conserved cysteine residues. Y Akamatsu T Ohno K Hirota H Kagoshima J Yodoi K Shigesada, J Biol Chem 1997 272 23 14497 14500 10.1074/jbc.272.23.14497 9169404
35. Functional dissection of the alpha and beta subunits of transcription factor PEBP2 and the redox susceptibility of its DNA binding activity. H Kagoshima Y Akamatsu Y Ito K Shigesada, J Biol Chem 1996 271 51 33074 33082 10.1074/jbc.271.51.33074 8955155
36. The RUNX genes: gain or loss of function in cancer. K Blyth ER Cameron JC Neil, Nat Rev Cancer 2005 5 5 376 387 10.1038/nrc1607 15864279
37. Regeneration of hydra from reaggregated cells. A Gierer S Berking H Bode CN David K Flick G Hansmann H Schaller E Trenkner, Nat New Biol 1972 239 91 98 101 4507522
38. Parameters of self-organization in Hydra aggregates. U Technau C Cramer von Laue F Rentzsch S Luft B Hobmayer HR Bode TW Holstein, Proc Natl Acad Sci U S A 2000 97 22 12127 12131 11050241 10.1073/pnas.97.22.12127
39. Elimination by Hydra interstitial and nerve cells by means of colchicine. RD Campbell, J Cell Sci 1976 21 1 1 13 932105
40. Excitability of nerve-free hydra. RD Campbell RK Josephson WE Schwab NB Rushforth, Nature 1976 262 5567 388 390 10.1038/262388a0 958390
41. Cnidarians: an evolutionarily conserved model system for regeneration? TW Holstein E Hobmayer U Technau, Dev Dyn 2003 226 2 257 267 10.1002/dvdy.10227 12557204
42. The stem cell concept in sponges (Porifera): Metazoan traits. WE Muller, Semin Cell Dev Biol 2006 17 4 481 491 10.1016/j.semcdb.2006.05.006 16807004
43. Origin of metazoan stem cell system in sponges: first approach to establish the model (Suberites domuncula). WE Muller M Korzhev G Le Pennec IM Muller HC Schroder, Biomol Eng 2003 20 4-6 369 379 10.1016/S1389-0344(03)00055-8 12919822
44. Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. FM Theriault HN Nuthall Z Dong R Lo F Barnabe-Heider FD Miller S Stifani, J Neurosci 2005 25 8 2050 2061 10.1523/JNEUROSCI.5108-04.2005 15728845
45. AML1/Runx1 is important for the development of hindbrain cholinergic branchiovisceral motor neurons and selected cranial sensory neurons. FM Theriault P Roy S Stifani, Proc Natl Acad Sci U S A 2004 101 28 10343 10348 15240886 10.1073/pnas.0400768101
46. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. CL Chen DC Broom Y Liu JC de Nooij Z Li C Cen OA Samad TM Jessell CJ Woolf Q Ma, Neuron 2006 49 3 365 377 10.1016/j.neuron.2005. 10.036 16446141
47. The transcription factor Runx3 represses the neurotrophin receptor TrkB during lineage commitment of dorsal root ganglion neurons. KI Inoue K Ito M Osato B Lee SC Bae Y Ito, J Biol Chem 2007
48. The NCBI Entrez protein database. http://www.ncbi.nlm.nih.gov/sites/ entrez?db=Protein
49. Class-level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. D Bridge CW Cunningham B Schierwater R DeSalle LW Buss, Proc Natl Acad Sci U S A 1992 89 18 8750 8753 1356268 10.1073/pnas.89.18.8750
50. Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. D Bridge CW Cunningham R DeSalle LW Buss, Mol Biol Evol 1995 12 4 679 689 7659022
51. A mutation in the S-switch region of the Runt domain alters the dynamics of an allosteric network responsible for CBFbeta regulation. Z Li SM Lukasik Y Liu J Grembecka I Bielnicka JH Bushweller NA Speck, J Mol Biol 2006 364 5 1073 1083 17059830 10.1016/j.jmb.2006.10.002
52. Partial correlation coefficient between distance matrices as a new indicator of protein-protein interactions. T Sato Y Yamanishi K Horimoto M Kanehisa H Toh, Bioinformatics 2006 22 20 2488 2492 10.1093/bioinformatics/ btl419 16882650
53. An enigmatic fourth runt domain gene in the fugu genome: ancestral gene loss versus accelerated evolution. G Glusman A Kaur L Hood L Rowen, BMC Evol Biol 2004 4 43 15527507 10.1186/1471-2148-4-43
54. cDNA cloning of Runx family genes from the pufferfish (Fugu rubripes). CE Ng M Osato BH Tay B Venkatesh Y Ito, Gene 2007 399 2 162 173 10.1016/j.gene.2007.05.014 17604919
55. Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. A Christoffels EG Koh JM Chia S Brenner S Aparicio B Venkatesh, Mol Biol Evol 2004 21 6 1146 1151 10.1093/molbev/msh114 15014147
56. Duplicate zebrafish runx2 orthologues are expressed in developing skeletal elements. MV Flores VW Tsang W Hu M Kalev-Zylinska J Postlethwait P Crosier K Crosier S Fisher, Gene Expr Patterns 2004 4 5 573 581 10.1016/j.modgep.2004.01.016 15261836
57. Rising starlet: the starlet sea anemone, Nematostella vectensis. JA Darling AR Reitzel PM Burton ME Mazza JF Ryan JC Sullivan JR Finnerty, Bioessays 2005 27 2 211 221 10.1002/bies.20181 15666346
58. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. RD Kortschak G Samuel R Saint DJ Miller, Curr Biol 2003 13 24 2190 2195 10.1016/j.cub.2003.11. 030 14680636
59. A high percentage of introns in human genes were present early in animal evolution: evidence from the basal metazoan Nematostella vectensis. JC Sullivan AM Reitzel JR Finnerty, Genome Inform 2006 17 1 219 229 17503371
60. Assessing protein co-evolution in the context of the tree of life assists in the prediction of the interactome. F Pazos JA Ranea D Juan MJ Sternberg, J Mol Biol 2005 352 4 1002 1015 10.1016/j.jmb.2005.07.005 16139301
61. Ultrastructural evidence for two-cell and three-cell neural pathways in the tentacle epidermis of the sea anemone Aiptasia pallida. JA Westfall CF Elliott RW Carlin, J Morphol 2002 251 1 83 92 10.1002/jmor.1075 11746469
62. A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. I Kramer M Sigrist JC de Nooij I Taniuchi TM Jessell S Arber, Neuron 2006 49 3 379 393 10.1016/j.neuron.2006.01.008 16446142
63. Phylogenesis and regulated expression of the RUNT domain transcription factors RUNX1 and RUNX3. D Levanon G Glusman D Bettoun E Ben-Asher V Negreanu Y Bernstein C Harris-Cerruti O Brenner R Eilam J Lotem O Fainaru D Goldenberg A Pozner E Woolf C Xiao M Yarmus Y Groner, Blood Cells Mol Dis 2003 30 2 161 163 10.1016/S1079-9796(03)00023-8 12732178
64. The culture, sexual and asexual reproduction and growth of the sea-anemone Nematostella vectensis. C Hand KR Uhlinger, Biological Bulletin 1992 182 169 176 10.2307/1542110
65. The King lab site. http://mcb.berkeley.edu/labs/king/blast/
66. Evolution of key cell signaling and adhesion protein families predates animal origins. N King CT Hittinger SB Carroll, Science 2003 301 5631 361 363 10.1126/science.1083853 12869759
67. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman, Nucleic Acids Research 1997 25 3389 3402 9254694 10.1093/nar/25.17.3389
68. The Craig Venter Institute site. https://research.venterinstitute.org/ files/hydra_magnipapillata_WGS_assembly
69. The Nematostella vectensis Genomics Database. http://stellabase.com
70. StellaBase: the Nematostella vectensis Genomics Database. JC Sullivan JF Ryan JA Watson J Webb JC Mullikin D Rokhsar JR Finnerty, Nucleic Acids Res 2006 34 Database issue D495 9 16381919 10.1093/nar/gkj020
71. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins, Nucleic Acids Res 1997 25 24 4876 4882 9396791 10.1093/nar/25.24.4876
72. RUNX regulates stem cell proliferation and differentiation: Insights from studies of C. elegans. H Kagoshima K Shigesada Y Kohara, J Cell Biochem 2007 100 5 1119 1130 10.1002/jcb.21174 17265434
73. Basic local alignment search tool. SF Altschul W Gish W Miller EW Myers DJ Lipman, J Mol Biol 1990 215 3 403 410 2231712
74. ProtTest: selection of best-fit models of protein evolution. F Abascal R Zardoya D Posada, Bioinformatics 2005 21 9 2104 2105 10.1093/bioinformatics/ bti263 15647292
75. AIC model selection using Akaike weights. EJ Wagenmakers S Farrell, Psychon Bull Rev 2004 11 1 192 196 15117008
76. rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. MW Dimmic JS Rest DP Mindell RA Goldstein, J Mol Evol 2002 55 1 65 73 10.1007/s00239-001-2304-y 12165843
77. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 5 696 704 10.1080/10635150390235520 14530136
78. The rapid generation of mutation data matrices from protein sequences. DT Jones WR Taylor JM Thornton, Computer Applications in the Biosciences 1992 8 2 275 282 1633570
79. Phylogenies from molecular sequences: inference and reliability. J Felsenstein, Annu Rev Genet 1988 22 521 565 10.1146/annurev.ge.22.120188.002513 3071258
80. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. KJ Peterson NJ Butterfield, Proc Natl Acad Sci U S A 2005 102 27 9547 9552 15983372 10.1073/pnas.0503660102
81. The leukemia-associated AML1 (Runx1) - CBF beta complex functions as a DNA-induced molecular clamp. J Bravo Z Li NA Speck AJ Warren, Nat Struct Biol 2001 8 4 371 378 10.1038/86264 11276260
82. Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra. DE Martinez ML Dirksen PM Bode M Jamrich RE Steele HR Bode, Dev Biol 1997 192 2 523 536 10.1006/dbio.1997.8715 9441686
83. PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. S Guindon F Lethiec P Duroux O Gascuel, Nucleic Acids Res 2005 33 Web Server issue W557 9 15980534 10.1093/nar/gki352