Hierarchical differentiation of myeloid progenitors is encoded in the transcription factor network

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Krumsiek, Jan ^a   Marr, Carsten ^a   Schroeder, Timm ^a   Theis, Fabian J ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; ERYTHROID KRUPPEL LIKE FACTOR; PROTEIN C JUN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EGRNAB; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR FOG 1; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GFI 1; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG; MESSENGER RNA;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; COMPUTER MODEL; CONTROLLED STUDY; ERYTHROCYTE; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GRANULOCYTE; HEMATOPOIETIC STEM CELL; KNOCKOUT GENE; MEGAKARYOCYTE; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; MONOCYTE; PHENOTYPE; STEADY STATE; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CYTOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; MOUSE; MYELOID PROGENITOR CELL; SYSTEMS BIOLOGY;

ANIMALS; CELL DIFFERENTIATION; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; MICE; MODELS, GENETIC; MYELOID PROGENITOR CELLS; RNA, MESSENGER; SYSTEMS BIOLOGY; TRANSCRIPTION FACTORS;

EID: 80051505603     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022649     Document Type: Article

References (95)

1. Orkin SH, Zon LI, (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631-644.
2. Cantor AB, Orkin SH, (2001) Hematopoietic development: a balancing act. Curr Opin Genet Dev 11: 513-519.
3. Akashi K, Traver D, Miyamoto T, Weissman IL, (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404: 193-197.
4. Iwasaki H, Akashi K, (2007) Myeloid lineage commitment from the hematopoietic stem cell. Immunity 26: 726-740.
5. Mackey MC, (1997) pp. 149-178 The Art of Mathematical Modelling: Case Studies in Ecology, Physiology and Biouids, Prentice Hall, chapter Mathematical models of hematopoietic cell replication and control.
6. Roeder I, Glauche I, (2006) Towards an understanding of lineage specification in hematopoietic stem cells: a mathematical model for the interaction of transcription factors gata-1 and pu.1. J Theor Biol 241: 852-865.
7. Huang S, Guo YP, May G, Enver T, (2007) Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev Biol 305: 695-713.
8. Narula J, Smith AM, Gottgens B, Igoshin OA, (2010) Modeling reveals bistability and low-pass filtering in the network module determining blood stem cell fate. PLoS Comput Biol 6: e1000771.
9. Kauffman SA, (1969) Metabolic stability and epigenesis in randomly constructed genetic nets. J Theor Biol 22: 437-467.
10. Mendoza L, Thieffry D, Alvarez-Buylla ER, (1999) Genetic control of ower morphogenesis in arabidopsis thaliana: a logical analysis. Bioinformatics 15: 593-606.
11. Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER, (2004) A gene regulatory network model for cell-fate determination during arabidopsis thaliana ower development that is robust and recovers experimental gene expression profiles. Plant Cell 16: 2923-2939.
12. Li F, Long T, Lu Y, Ouyang Q, Tang C, (2004) The yeast cell-cycle network is robustly designed. Proc Natl Acad Sci U S A 101: 4781-4786.
13. Davidich MI, Bornholdt S, (2008) Boolean network model predicts cell cycle sequence of fission yeast. PLoS ONE 3: e1672.
14. Albert R, Othmer HG, (2003) The topology of the regulatory interactions predicts the expression pattern of the segment polarity genes in drosophila melanogaster. J Theor Biol 223: 1-18.
15. Wittmann DM, Blöchl F, Trümbach D, Wurst W, Prakash N, et al. (2009) Spatial analysis of expression patterns predicts genetic interactions at the mid-hindbrain boundary. PLoS Comput Biol 5: e1000569.
16. Bornholdt S, (2005) Less is more in modeling large genetic networks. Science 310: 449-451.
17. Fauré A, Naldi A, Chaouiya C, Thieffry D, (2006) Dynamical analysis of a generic boolean model for the control of the mammalian cell cycle. Bioinformatics 22: e124-e131.
18. Laiosa CV, Stadtfeld M, Graf T, (2006) Determinants of lymphoid-myeloid lineage diversification. Annu Rev Immunol 24: 705-738.
19. Laslo P, Pongubala JMR, Lancki DW, Singh H, (2008) Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin Immunol 20: 228-235.
20. Laslo P, Spooner CJ, Warmash A, Lancki DW, Lee HJ, et al. (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126: 755-766.
21. Tenen DG, Hromas R, Licht JD, Zhang DE, (1997) Transcription factors, normal myeloid development, and leukemia. Blood 90: 489-519.
22. Rosenbauer F, Wagner K, Kutok JL, Iwasaki H, Beau MML, et al. (2004) Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, pu.1. Nat Genet 36: 624-630.
23. Moroni E, Mastrangelo T, Razzini R, Cairns L, Moi P, et al. (2000) Regulation of mouse p45 nf-e2 transcription by an erythroid-specific gata-dependent intronic alternative promoter. J Biol Chem 275: 10567-10576.
24. McCormack MP, Hall MA, Schoenwaelder SM, Zhao Q, Ellis S, et al. (2006) A critical role for the transcription factor scl in platelet production during stress thrombopoiesis. Blood 108: 2248-2256.
25. Takayama M, Fujita R, Suzuki M, Okuyama R, Aiba S, et al. (2010) Genetic analysis of hierarchical regulation for gata1 and nf-e2 p45 gene expression in megakaryopoiesis. Mol Cell Biol 30: 2668-2680.
26. Tsujimura H, Nagamura-Inoue T, Tamura T, Ozato K, (2002) Ifn consensus sequence binding protein/ifn regulatory factor-8 guides bone marrow progenitor cells toward the macrophage lineage. J Immunol 169: 1261-1269.
27. Wang H, Lee CH, Qi C, Tailor P, Feng J, et al. (2008) Irf8 regulates b-cell lineage specification, commitment, and differentiation. Blood 112: 4028-4038.
28. Jones LC, Lin ML, Chen SS, Krug U, Hofmann WK, et al. (2002) Expression of c/ebpbeta from the c/ebpalpha gene locus is sufficient for normal hematopoiesis in vivo. Blood 99: 2032-2036.
29. Huang DY, Kuo YY, Lai JS, Suzuki Y, Sugano S, et al. (2004) Gata-1 and nf-y cooperate to mediate erythroid-specific transcription of gfi-1b gene. Nucleic Acids Res 32: 3935-3946.
30. Orkin SH, Zon LI, (2008) Snapshot: hematopoiesis. Cell 132: 712.
31. Taoudi S, Bee T, Hilton A, Knezevic K, Scott J, et al. (2011) Erg dependence distinguishes developmental control of hematopoietic stem cell maintenance from hematopoietic specification. Genes Dev.
32. Elagib KE, Goldfarb AN, (2007) Regulation of runx1 transcriptional function by gata-1. Crit Rev Eukaryot Gene Expr 17: 271-280.
33. Scherf M, Epple A, Werner T, (2005) The next generation of literature analysis: integration of genomic analysis into text mining. Brief Bioinform 6: 287-297.
34. Göttgens B, Nastos A, Kinston S, Piltz S, Delabesse ECM, et al. (2002) Establishing the transcriptional programme for blood: the scl stem cell enhancer is regulated by a multiprotein complex containing ets and gata factors. EMBO J 21: 3039-3050.
35. Duan Z, Horwitz M, (2005) Gfi-1 takes center stage in hematopoietic stem cells. Trends Mol Med 11: 49-52.
36. Pimanda JE, Ottersbach K, Knezevic K, Kinston S, Chan WYI, et al. (2007) Gata2, i1, and scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci U S A 104: 17692-17697.
37. Du J, Stankiewicz MJ, Liu Y, Xi Q, Schmitz JE, et al. (2002) Novel combinatorial interactions of gata-1, pu.1, and c/ebpepsilon isoforms regulate transcription of the gene encoding eosinophil granule major basic protein. J Biol Chem 277: 43481-43494.
38. Walsh JC, DeKoter RP, Lee HJ, Smith ED, Lancki DW, et al. (2002) Cooperative and antagonistic interplay between pu.1 and gata-2 in the specification of myeloid cell fates. Immunity 17: 665-676.
39. Alon U, (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
40. Gardner TS, Cantor CR, Collins JJ, (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342.
41. Thomas R, Kaufman M, (2001) Multistationarity, the basis of cell differentiation and memory. ii. logical analysis of regulatory networks in terms of feedback circuits. Chaos 11: 180-195.
42. Radde N, Bar N, Banaji M, (2009) Graphical methods for analysing feedback in biological networks- a survey-. Int J Syst Sci.
43. Mangan S, Alon U, (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci U S A 100: 11980-11985.
44. Minegishi N, Suzuki N, Yokomizo T, Pan X, Fujimoto T, et al. (2003) Expression and domainspecific function of gata-2 during differentiation of the hematopoietic precursor cells in midgestation mouse embryos. Blood 102: 896-905.
45. Friedman AD, (2007) C/ebpalpha induces pu.1 and interacts with ap-1 and nf-kappab to regulate myeloid development. Blood Cells Mol Dis 39: 340-343.
46. Yeamans C, Wang D, Paz-Priel I, Torbett BE, Tenen DG, et al. (2007) C/ebpalpha binds and activates the pu.1 distal enhancer to induce monocyte lineage commitment. Blood 110: 3136-3142.
47. Dahl R, Iyer SR, Owens KS, Cuylear DD, Simon MC, (2007) The transcriptional repressor gfi-1 antagonizes pu.1 activity through protein-protein interaction. J Biol Chem 282: 6473-6483.
48. Arinobu Y, Mizuno S, Chong Y, Shigematsu H, Iino T, et al. (2007) Reciprocal activation of gata-1 and pu.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 1: 416-427.
49. Chou ST, Khandros E, Bailey LC, Nichols KE, Vakoc CR, et al. (2009) Graded repression of pu.1/sfpi1 gene transcription by gata factors regulates hematopoietic cell fate. Blood 114: 983-994.
50. Chambers SM, Boles NC, Lin KYK, Tierney MP, Bowman TV, et al. (2007) Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell 1: 578-591.
51. Pronk CJH, Rossi DJ, Månsson R, Attema JL, Norddahl GL, et al. (2007) Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 1: 428-442.
52. Zhang Y, Payne KJ, Zhu Y, Price MA, Parrish YK, et al. (2005) Scl expression at critical points in human hematopoietic lineage commitment. Stem Cells 23: 852-860.
53. Pevny L, Simon MC, Robertson E, Klein WH, Tsai SF, et al. (1991) Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor gata-1. Nature 349: 257-260.
54. Fujiwara Y, Browne CP, Cunniff K, Goff SC, Orkin SH, (1996) Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor gata-1. Proc Natl Acad Sci U S A 93: 12355-12358.
55. Scott EW, Simon MC, Anastasi J, Singh H, (1994) Requirement of transcription factor pu.1 in the development of multiple hematopoietic lineages. Science 265: 1573-1577.
56. McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, et al. (1996) Targeted disruption of the pu.1 gene results in multiple hematopoietic abnormalities. EMBO J 15: 5647-5658.
57. Tsai FY, Orkin SH, (1997) Transcription factor gata-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 89: 3636-3643.
58. Yamaguchi Y, Zon LI, Ackerman SJ, Yamamoto M, Suda T, (1998) Forced gata-1 expression in the murine myeloid cell line m1: induction of c-mpl expression and megakaryocytic/erythroid differentiation. Blood 91: 450-457.
59. Iwasaki H, Mizuno S, Wells RA, Cantor AB, Watanabe S, et al. (2003) Gata-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/erythrocyte lineages. Immunity 19: 451-462.
60. Nerlov C, Graf T, (1998) Pu.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev 12: 2403-2412.
61. Kulessa H, Frampton J, Graf T, (1995) Gata-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev 9: 1250-1262.
62. Heyworth C, Pearson S, May G, Enver T, (2002) Transcription factor-mediated lineage switching reveals plasticity in primary committed progenitor cells. EMBO J 21: 3770-3781.
63. Landry JR, Kinston S, Knezevic K, de Bruijn MFTR, Wilson N, et al. (2008) Runx genes are direct targets of scl/tal1 in the yolk sac and fetal liver. Blood 111: 3005-3014.
64. Tokita K, Maki K, Mitani K, (2007) Runx1/evi1, which blocks myeloid differentiation, inhibits ccaat-enhancer binding protein alpha function. Cancer Sci 98: 1752-1757.
65. Graf T, (2002) Differentiation plasticity of hematopoietic cells. Blood 99: 3089-3101.
66. Graf T, Enver T, (2009) Forcing cells to change lineages. Nature 462: 587-594.
67. Rieger MA, Schroeder T, (2009) Analyzing cell fate control by cytokines through continuous single cell biochemistry. J Cell Biochem 108: 343-352.
68. Kirouac DC, Ito C, Csaszar E, Roch A, Yu M, et al. (2010) Dynamic interaction networks in a hierarchically organized tissue. Mol Syst Biol 6: 417.
69. Gangaraju VK, Lin H, (2009) Micrornas: key regulators of stem cells. Nat Rev Mol Cell Biol 10: 116-125.
70. Tsang AP, Visvader JE, Turner CA, Fujiwara Y, Yu C, et al. (1997) Fog, a multitype zinc finger protein, acts as a cofactor for transcription factor gata-1 in erythroid and megakaryocytic differentiation. Cell 90: 109-119.
71. Tsang AP, Fujiwara Y, Hom DB, Orkin SH, (1998) Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the gata-1 transcriptional cofactor fog. Genes Dev 12: 1176-1188.
72. Nuez B, Michalovich D, Bygrave A, Ploemacher R, Grosveld F, (1995) Defective haematopoiesis in fetal liver resulting from inactivation of the eklf gene. Nature 375: 316-318.
73. Perkins AC, Sharpe AH, Orkin SH, (1995) Lethal beta-thalassaemia in mice lacking the erythroid caccc-transcription factor eklf. Nature 375: 318-322.
74. Lim SK, Bieker JJ, Lin CS, Costantini F, (1997) A shortened life span of eklf-/- adult erythrocytes, due to a deficiency of beta-globin chains, is ameliorated by human gamma-globin chains. Blood 90: 1291-1299.
75. Kawada H, Ito T, Pharr PN, Spyropoulos DD, Watson DK, et al. (2001) Defective megakaryopoiesis and abnormal erythroid development in i-1 gene-targeted mice. Int J Hematol 73: 463-468.
76. Moussa O, Larue AC, Abangan RS, Williams CR, Zhang XK, et al. (2010) Thrombocytopenia in mice lacking the carboxy-terminal regulatory domain of the ets transcription factor i1. Mol Cell Biol.
77. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, et al. (1997) Absence of granulocyte colony-stimulating factor signaling and neutrophil development in ccaat enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci U S A 94: 569-574.
78. Zhang P, Iwasaki-Arai J, Iwasaki H, Fenyus ML, Dayaram T, et al. (2004) Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor c/ebp alpha. Immunity 21: 853-863.
79. Karsunky H, Zeng H, Schmidt T, Zevnik B, Kluge R, et al. (2002) Inammatory reactions and severe neutropenia in mice lacking the transcriptional repressor gfi1. Nat Genet 30: 295-300.
80. Hock H, Hamblen MJ, Rooke HM, Traver D, Bronson RT, et al. (2003) Intrinsic requirement for zinc finger transcription factor gfi-1 in neutrophil differentiation. Immunity 18: 109-120.
81. Ohneda K, Yamamoto M, (2002) Roles of hematopoietic transcription factors gata-1 and gata-2 in the development of red blood cell lineage. Acta Haematol 108: 237-245.
82. Grass JA, Boyer ME, Pal S, Wu J, Weiss MJ, et al. (2003) Gata-1-dependent transcriptional repression of gata-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc Natl Acad Sci U S A 100: 8811-8816.
83. Rekhtman N, Radparvar F, Evans T, Skoultchi AI, (1999) Direct interaction of hematopoietic transcription factors pu.1 and gata-1: functional antagonism in erythroid cells. Genes Dev 13: 1398-1411.
84. Tsai SF, Strauss E, Orkin SH, (1991) Functional analysis and in vivo footprinting implicate the erythroid transcription factor gata-1 as a positive regulator of its own promoter. Genes Dev 5: 919-931.
85. Orkin SH, (1992) Gata-binding transcription factors in hematopoietic cells. Blood 80: 575-581.
86. Trainor CD, Omichinski JG, Vandergon TL, Gronenborn AM, Clore GM, et al. (1996) A palindromic regulatory site within vertebrate gata-1 promoters requires both zinc fingers of the gata-1 dna-binding domain for high-affinity interaction. Mol Cell Biol 16: 2238-2247.
87. Starck J, Cohet N, Gonnet C, Sarrazin S, Doubeikovskaia Z, et al. (2003) Functional crossantagonism between transcription factors i-1 and eklf. Mol Cell Biol 23: 1390-1402.
88. Crossley M, Tsang AP, Bieker JJ, Orkin SH, (1994) Regulation of the erythroid kruppel-like factor(eklf) gene promoter by the erythroid transcription factor gata-1. J Biol Chem 269: 15440-15444.
89. Barbeau B, Barat C, Bergeron D, Rassart E, (1999) The gata-1 and spi-1 transcriptional factors bind to a gata/ebs dual element in the i-1 exon 1. Oncogene 18: 5535-5545.
90. Bockamp EO, McLaughlin F, Murrell AM, Göttgens B, Robb L, et al. (1995) Lineage-restricted regulation of the murine scl/tal-1 promoter. Blood 86: 1502-1514.
91. Clech ML, Chalhoub E, Dohet C, Roure V, Fichelson S, et al. (2006) Pu.1/spi-1 binds to the human tal-1 silencer to mediate its activity. J Mol Biol 355: 9-19.
92. Chickarmane V, Enver T, Peterson C, (2009) Computational modeling of the hematopoietic erythroid-myeloid switch reveals insights into cooperativity, priming, and irreversibility. PLoS Comput Biol 5: e1000268.
93. Okuno Y, Huang G, Rosenbauer F, Evans EK, Radomska HS, et al. (2005) Potential autoregulation of transcription factor pu.1 by an upstream regulatory element. Mol Cell Biol 25: 2832-2845.
94. Leddin M, Perrod C, Hoogenkamp M, Ghani S, Assi S, et al. (2011) Two distinct auto-regulatory loops operate at the pu.1 locus in b cells and myeloid cells. Blood 117: 2827-2838.
95. Steidl U, Rosenbauer F, Verhaak RGW, Gu X, Ebralidze A, et al. (2006) Essential role of jun family transcription factors in pu.1 knockdown-induced leukemic stem cells. Nat Genet 38: 1269-1277.