Modeling reveals bistability and low-pass filtering in the network module determining blood stem cell fate

PLoS Computational Biology

Volumn 6, Issue 5, 2010, Pages 1-16

  Narula, Jatin ^a   Smith, Aileen M ^b   Gottgens, Berthold ^b   Igoshin, Oleg A ^a  

^a Rice University   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; LOW PASS FILTERS; PHYSIOLOGICAL MODELS; STEM CELLS;

BI-STABILITY; CELL-FATE; CONTROL ELEMENTS; DYNAMICS PROPERTIES; GENES EXPRESSION; HAEMATOPOIETIC STEM CELLS; LOW-PASS FILTERING; MULTIPLE INPUTS; REGULATORY CONTROL; STEM-CELL;

PROTEINS;

BONE MORPHOGENETIC PROTEIN 4; NOTCH RECEPTOR; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR TAL1;

ARTICLE; BINDING SITE; CELL FATE; CELL SPECIFICITY; CONTROLLED STUDY; FILTRATION; GENE REGULATORY NETWORK; HEMATOPOIETIC STEM CELL; MATHEMATICAL MODEL; MUTATIONAL ANALYSIS; PREDICTION; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STEADY STATE; THERMODYNAMICS;

EID: 77955502318     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000771     Document Type: Article

References (53)

1. Davidson EH (2006) The regulatory genome: gene regulatory networks in development and evolution. Amsterdam; Boston: Academic Press. xi, 289 p.
2. Chaves M, Albert R, Sontag ED (2005) Robustness and fragility of Boolean models for genetic regulatory networks. J Theor Biol 235(3): 431-49.
3. Kauffman S, Peterson C, Samuelsson B, Troein C (2003) Random Boolean network models and the yeast transcriptional network. Proc Natl Acad Sci U S A 100(25): 14796-9.
4. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, et al. (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126(4): 755-66.
5. Bintu L, Buchler NE, Garcia HG, Gerland U, Hwa T, et al. (2005) Transcriptional regulation by the numbers: models. Curr Opin Genet Dev 15(2): 116-24.
6. Buchler NE, Gerland U, Hwa T (2003) On schemes of combinatorial transcription logic. Proc Natl Acad Sci U S A 100(9): 5136-41.
7. Shea MA, Ackers GK (1985) The OR control system of bacteriophage lambda. A physical-chemical model for gene regulation. J Mol Biol 181(2): 211-30.
8. Bintu L, Buchler NE, Garcia HG, Gerland U, Hwa T, et al. (2005) Transcriptional regulation by the numbers: applications. Curr Opin Genet Dev 15(2): 125-35.
9. Raveh-Sadka T, Levo M, Segal E (2009) Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res 19(8): 1480-96.
10. Orkin SH, Zon LI (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132(4): 631-44.
11. Miranda-Saavedra D, Gottgens B (2008) Transcriptional regulatory networks in haematopoiesis. Curr Opin Genet Dev 18(6): 530-5.
12. Gottgens B, Nastos A, Kinston S, Piltz S, Delabesse EC, 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(12): 3039-50.
13. Landry JR, Bonadies N, Kinston S, Knezevic K, Wilson NK, et al. (2009) Expression of the leukemia oncogene Lmo2 is controlled by an array of tissuespecific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 113(23): 5783-92.
14. Landry JR, Kinston S, Knezevic K, de Bruijn MF, Wilson N, et al. (2008) Runx genes are direct targets of Scl/Tal1 in the yolk sac and fetal liver. Blood 111(6): 3005-14.
15. Wilson NK, Miranda-Saavedra D, Kinston S, Bonadies N, Foster SD, et al. (2009) The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood 113(22): 5456-65.
16. Donaldson IJ, Chapman M, Kinston S, Landry JR, Knezevic K, et al. (2005) Genome-wide identification of cis-regulatory sequences controlling blood and endothelial development. Hum Mol Genet 14(5): 595-601.
17. Pimanda JE, Chan WY, Wilson NK, Smith AM, Kinston S, et al. (2008) Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code. Blood 112(12): 4512-22.
18. Pimanda JE, Donaldson IJ, de Bruijn MF, Kinston S, Knezevic K, et al. (2007) The SCL transcriptional network and BMP signaling pathway interact to regulate RUNX1 activity. Proc Natl Acad Sci U S A 104(3): 840-5.
19. Foster SD, Oram SH, Wilson NK, Gottgens B (2009) From genes to cells to tissues-modelling the haematopoietic system. Mol Biosyst.
20. Pimanda JE, Ottersbach K, Knezevic K, Kinston S, Chan WY, et al. (2007) Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci U S A 104(45): 17692-7.
21. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298(5594): 824-7.
22. Chickarmane V, Troein C, Nuber UA, Sauro HM, Peterson C (2006) Transcriptional dynamics of the embryonic stem cell switch. PLoS Comput Biol 2(9): e123.
23. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6): 947-56.
24. Smith AM, Sanchez MJ, Follows GA, Kinston S, Donaldson IJ, et al. (2008) A novel mode of enhancer evolution: the Tal1 stem cell enhancer recruited a MIR element to specifically boost its activity. Genome Res 18(9): 1422-32.
25. Oren T, Torregroza I, Evans T (2005) An Oct-1 binding site mediates activation of the gata2 promoter by BMP signaling. Nucleic Acids Res 33(13): 4357-67.
26. Robert-Moreno A, Espinosa L, de la Pompa JL, Bigas A (2005) RBPjkappadependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells. Development 132(5): 1117-26.
27. Lugus JJ, Chung YS, Mills JC, Kim SI, Grass J, et al. (2007) GATA2 functions at multiple steps in hemangioblast development and differentiation. Development 134(2): 393-405.
28. Robb L, Elwood NJ, Elefanty AG, Kontgen F, Li R, et al. (1996) The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. Embo J 15(16): 4123-9.
29. Shivdasani RA, Mayer EL, Orkin SH (1995) Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373(6513): 432-4.
30. Spyropoulos DD, Pharr PN, Lavenburg KR, Jackers P, Papas TS, et al. (2000) Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol Cell Biol 20(15): 5643-52.
31. Tsai FY, Keller G, Kuo FC, Weiss M, Chen J, et al. (1994) An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371(6494): 221-6.
32. Curtis DJ, Hall MA, Van Stekelenburg LJ, Robb L, Jane SM, et al. (2004) SCL is required for normal function of short-term repopulating hematopoietic stem cells. Blood 103(9): 3342-8.
33. Rodrigues NP, Janzen V, Forkert R, Dombkowski DM, Boyd AS, et al. (2005) Haploinsufficiency of GATA-2 perturbs adult hematopoietic stem-cell homeostasis. Blood 106(2): 477-84.
34. Roberts MJ (2008) Fundamentals of signals and systems. Boston: McGraw-Hill Higher Education. xix, 759 p.
35. Savageau MA (1976) Biochemical systems analysis: a study of function and design in molecular biology. ReadingMass.: Addison-Wesley Pub. Co. xvii, 379 p.
36. Saiz L, Vilar JM (2008) Ab initio thermodynamic modeling of distal multisite transcription regulation. Nucleic Acids Res 36(3): 726-31.
37. Walters MC, Fiering S, Eidemiller J, Magis W, Groudine M, et al. (1995) Enhancers increase the probability but not the level of gene expression. Proc Natl Acad Sci U S A 92(15): 7125-9.
38. Polach KJ, Widom J (1995) Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J Mol Biol 254(2): 130-49.
39. Milot E, Strouboulis J, Trimborn T, Wijgerde M, de Boer E, et al. (1996) Heterochromatin effects on the frequency and duration of LCR-mediated gene transcription. Cell 87(1): 105-14.
40. Sutherland HG, Martin DI, Whitelaw E (1997) A globin enhancer acts by increasing the proportion of erythrocytes expressing a linked transgene. Mol Cell Biol 17(3): 1607-14.
41. Kumano K, Chiba S, Kunisato A, Sata M, Saito T, et al. (2003) Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 18(5): 699-711.
42. Durand C, Robin C, Bollerot K, Baron MH, Ottersbach K, et al. (2007) Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Proc Natl Acad Sci U S A 104(52): 20838-43.
43. Tang T, Arbiser JL, Brandt SJ (2002) Phosphorylation by mitogen-activated protein kinase mediates the hypoxia-induced turnover of the TAL1/SCL transcription factor in endothelial cells. J Biol Chem 277(21): 18365-72.
44. Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ (2008) Global protein stability profiling in mammalian cells. Science 322(5903): 918-23.
45. Maeda YT, Sano M (2006) Regulatory dynamics of synthetic gene networks with positive feedback. J Mol Biol 359(4): 1107-24.
46. 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(15): 8811-6.
47. Ramos CA, Bowman TA, Boles NC, Merchant AA, Zheng Y, et al. (2006) Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet 2(9): e159.
48. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453(7194): 544-7.
49. Kitajima K, Masuhara M, Era T, Enver T, Nakano T (2002) GATA-2 and GATA-2/ER display opposing activities in the development and differentiation of blood progenitors. Embo J 21(12): 3060-9.
50. Lam FH, Steger DJ, O'Shea EK (2008) Chromatin decouples promoter threshold from dynamic range. Nature 453(7192): 246-50.
51. Duncan AW, Rattis FM, DiMascio LN, Congdon KL, Pazianos G, et al. (2005) Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 6(3): 314-22.
52. Li G, Levitus M, Bustamante C, Widom J (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat Struct Mol Biol 12(1): 46-53.
53. Ermentrout (2002) Simulating, Analyzing, and Animating Dynamical Systems. Philadelphia PA: SIAM.