Regulatory gene network circuits underlying T cell development from multipotent progenitors

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 4, Issue 1, 2012, Pages 79-102

  Kueh, Hao Yuan ^a   Rothenberg, Ellen V ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 7; NOTCH RECEPTOR;

ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HUMAN; LYMPHOCYTE ACTIVATION; MOUSE; MULTIPOTENT STEM CELL; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; INTERLEUKIN-7; LYMPHOCYTE ACTIVATION; MICE; MODELS, BIOLOGICAL; MULTIPOTENT STEM CELLS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 83755205792     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.162     Document Type: Review

References (120)

1. Shoval O, Alon U. SnapShot: network motifs. Cell 2010, 143:326.e1-326.e2.
2. Xiong W, Ferrell JE, Jr. A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 2003, 426:460-465.
3. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 2002, 21:3368-3376.
4. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006, 126:755-766.
5. Levine M, Davidson EH. Gene regulatory networks for development. Proc Natl Acad Sci U S A 2005, 102:4936-4942.
6. Goentoro L, Shoval O, Kirschner MW, Alon U. The incoherent feedforward loop can provide fold-change detection in gene regulation. Mol Cell 2009, 36:894-899.
7. Ma W, Trusina A, El-Samad H, Lim WA, Tang C. Defining network topologies that can achieve biochemical adaptation. Cell 2009, 138:760-773.
8. Krejci A, Bernard F, Housden BE, Collins S, Bray SJ. Direct response to Notch activation: signaling crosstalk and incoherent logic. Sci Signal 2009, 2:ra1.
9. Cohen-Saidon C, Cohen AA, Sigal A, Liron Y, Alon U. Dynamics and variability of ERK2 response to EGF in individual living cells. Mol Cell 2009, 36:885-893.
10. Sambandam A, Maillard I, Zediak VP, Xu L, Gerstein RM, Aster JC, Pear WS, Bhandoola A. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 2005, 6:663-670.
11. Koch U, Fiorini E, Benedito R, Besseyrias V, Schuster-Gossler K, Pierres M, Manley NR, Duarte A, Macdonald HR, Radtke F. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med 2008, 205:2515-2523.
12. Yui MA, Feng N, Rothenberg EV. Fine-scale staging of T cell lineage commitment in adult mouse thymus. J Immunol 2010, 185:284-293.
13. Rothenberg EV, Zhang J, Li L. Multilayered specification of the T-cell lineage fate. Immunol Rev 2010, 238:150-168.
14. Schmitt TM, Ciofani M, Petrie HT, Zuniga-Pflucker JC. Maintenance of T cell specification and differentiation requires recurrent notch receptor-ligand interactions. J Exp Med 2004, 200:469-479.
15. Taghon TN, David ES, Zuniga-Pflucker JC, Rothenberg EV. Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev 2005, 19:965-978.
16. Heinzel K, Benz C, Martins VC, Haidl ID, Bleul CC. Bone marrow-derived hemopoietic precursors commit to the T cell lineage only after arrival in the thymic microenvironment. J Immunol 2007, 178:858-868.
17. Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T, Katsura Y, Kawamoto H. Adult T-cell progenitors retain myeloid potential. Nature 2008, 452:768-72.
18. Bell JJ, Bhandoola A. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 2008, 452:764-767.
19. Porritt HE, Rumfelt LL, Tabrizifard S, Schmitt TM, Zuniga-Pflucker JC, Petrie HT. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 2004, 20:735-745.
20. Carlyle JR, Michie AM, Furlonger C, Nakano T, Lenardo MJ, Paige CJ, Zuniga-Pflucker JC. Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med 1997, 186:173-182.
21. Ikawa T, Kawamoto H, Fujimoto S, Katsura Y. Commitment of common T/Natural killer (NK) progenitors to unipotent T and NK progenitors in the murine fetal thymus revealed by a single progenitor assay. J Exp Med 1999, 190:1617-1626.
22. Rodewald HR, Moingeon P, Lucich JL, Dosiou C, Lopez P, Reinherz EL. A population of early fetal thymocytes expressing Fc γ RII/III contains precursors of T lymphocytes and natural killer cells. Cell 1992, 69:139-150.
23. Rothenberg EV. T cell lineage commitment: identity and renunciation. J Immunol 2011, 186:6649-6655.
24. Mangan S, Zaslaver A, Alon U. The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J Mol Biol 2003, 334:197-204.
25. Swiers G, Patient R, Loose M. Genetic regulatory networks programming hematopoietic stem cells and erythroid lineage specification. Dev Biol 2006, 294:525-540.
26. Massa S, Balciunaite G, Ceredig R, Rolink AG. Critical role for c-kit (CD117) in T cell lineage commitment and early thymocyte development in vitro. Eur J Immunol 2006, 36:526-532.
27. Jensen CT, Boiers C, Kharazi S, Lubking A, Ryden T, Sigvardsson M, Sitnicka E, Jacobsen SE. Permissive roles of hematopoietin and cytokine tyrosine kinase receptors in early T-cell development. Blood 2008, 111:2083-2090.
28. Ikawa T, Hirose S, Masuda K, Kakugawa K, Satoh R, Shibano-Satoh A, Kominami R, Katsura Y, Kawamoto H. An essential developmental checkpoint for production of the T cell lineage. Science 2010, 329:93-96.
29. Schlenner SM, Madan V, Busch K, Tietz A, Laufle C, Costa C, Blum C, Fehling HJ, Rodewald HR. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 2010, 32:426-436.
30. Allman D, Sambandam A, Kim S, Miller JP, Pagan A, Well D, Meraz A, Bhandoola A. Thymopoiesis independent of common lymphoid progenitors. Nat Immunol 2003, 4:168-174.
31. Ceredig R, Rolink T. A positive look at double-negative thymocytes. Nat Rev Immunol 2002, 2:888-897.
32. von Freeden-Jeffry U, Solvason N, Howard M, Murray R. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 1997, 7:147-154.
33. Balciunaite G, Ceredig R, Fehling HJ, Zuniga-Pflucker JC, Rolink AG. The role of Notch and IL-7 signaling in early thymocyte proliferation and differentiation. Eur J Immunol 2005, 35:1292-1300.
34. Wojciechowski J, Lai A, Kondo M, Zhuang Y. E2A and HEB are required to block thymocyte proliferation prior to pre-TCR expression. J Immunol 2007, 178:5717-5726.
35. Braunstein M, Anderson MK. HEB-deficient T-cell precursors lose T-cell potential and adopt an alternative pathway of differentiation. Mol Cell Biol 2011, 31:971-982.
36. Mazzucchelli R, Durum SK. Interleukin-7 receptor expression: intelligent design. Nat Rev Immunol 2007, 7:144-154.
37. Peter IS, Davidson EH. Modularity and design principles in the sea urchin embryo gene regulatory network. FEBS Lett 2009, 583:3948-3958.
38. Singh H, Medina KL, Pongubala JM. Contingent gene regulatory networks and B cell fate specification. Proc Natl Acad Sci U S A 2005, 102:4949-4953.
39. Mandel EM, Grosschedl R. Transcription control of early B cell differentiation. Curr Opin Immunol 2010, 22:161-167.
40. Chickarmane V, Enver T, Peterson C. Computational modeling of the hematopoietic erythroid-myeloid switch reveals insights into cooperativity, priming, and irreversibility. PLoS Comput Biol 2009, 5:e1000268.
41. Laiosa CV, Stadtfeld M, Graf T. Determinants of lymphoid-myeloid lineage diversification. Annu Rev Immunol 2006, 24:705-738.
42. Spooner CJ, Cheng JX, Pujadas E, Laslo P, Singh H. A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 2009, 31:576-586.
43. Li L, Leid M, Rothenberg EV. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 2010, 329:89-93.
44. Li P, Burke S, Wang J, Chen X, Ortiz M, Lee SC, Lu D, Campos L, Goulding D, Ng BL, et al. Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science 2010, 329:85-89.
45. Weber BN, Chi AW, Chavez A Y-O Y, Yang Q, Shestova O, Bhandoola A. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 2011, 476:63-68.
46. Georgescu C, Longabaugh WJ, Scripture-Adams DD, David-Fung ES, Yui MA, Zarnegar MA, Bolouri H, Rothenberg EV. A gene regulatory network armature for T lymphocyte specification. Proc Natl Acad Sci U S A 2008, 105:20100-20105.
47. Schmitt TM, Zuniga-Pflucker JC. T-cell development, doing it in a dish. Immunol Rev 2006, 209:95-102.
48. Young RA. Control of the embryonic stem cell state. Cell 2011, 144:940-954.
49. Oram SH, Thoms JA, Pridans C, Janes ME, Kinston SJ, Anand S, Landry JR, Lock RB, Jayaraman PS, Huntly BJ, et al. A previously unrecognized promoter of LMO2 forms part of a transcriptional regulatory circuit mediating LMO2 expression in a subset of T-acute lymphoblastic leukaemia patients. Oncogene 2010, 29:5796-5808.
50. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010, 38:576-589.
51. Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J, et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol 2010, 11:635-643.
52. Kastner P, Chan S, Vogel WK, Zhang LJ, Topark-Ngarm A, Golonzhka O, Jost B, Le Gras S, Gross MK, Leid M. Bcl11b represses a mature T-cell gene expression program in immature CD4(+)CD8(+) thymocytes. Eur J Immunol 2010, 40:2143-2154.
53. Izon DJ, Aster JC, He Y, Weng A, Karnell FG, Patriub V, Xu L, Bakkour S, Rodriguez C, Allman D, et al. Deltex1 redirects lymphoid progenitors to the B cell lineage by antagonizing Notch1. Immunity 2002, 16:231-243.
54. Jia J, Dai M, Zhuang Y. E proteins are required to activate germline transcription of the TCR Vβ8.2 gene. Eur J Immunol 2008, 38:2806-2820.
55. Gregoire JM, Romeo PH. T-cell expression of the human GATA-3 gene is regulated by a non-lineage-specific silencer. J Biol Chem 1999, 274:6567-6578.
56. Xu W, Kee BL. Growth factor independent 1B (Gfi1b) is an E2A target gene that modulates Gata3 in T-cell lymphomas. Blood 2007, 109:4406-4414.
57. Ikawa T, Kawamoto H, Goldrath AW, Murre C. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J Exp Med 2006, 203:1329-1342.
58. Schwartz R, Engel I, Fallahi-Sichani M, Petrie HT, Murre C. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc Natl Acad Sci U S A 2006, 103:9976-9981.
59. Wang D, Claus CL, Vaccarelli G, Braunstein M, Schmitt TM, Zuniga-Pflucker JC, Rothenberg EV, Anderson MK. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J Immunol 2006, 177:109-119.
60. Dias S, Mansson R, Gurbuxani S, Sigvardsson M, Kee BL. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008, 29:217-227.
61. Yashiro-Ohtani Y, He Y, Ohtani T, Jones ME, Shestova O, Xu L, Fang TC, Chiang MY, Intlekofer AM, Blacklow SC, et al. Pre-TCR signaling inactivates Notch1 transcription by antagonizing E2A. Genes Dev 2009, 23:1665-1676.
62. San-Marina S, Han Y, Suarez Saiz F, Trus MR, Minden MD. Lyl1 interacts with CREB1 and alters expression of CREB1 target genes. Biochim Biophys Acta 2008, 1783:503-517.
63. Donaldson IJ, Chapman M, Kinston S, Landry JR, Knezevic K, Piltz S, Buckley N, Green AR, Gottgens B. Genome-wide identification of cis-regulatory sequences controlling blood and endothelial development. Hum Mol Genet 2005, 14:595-601.
64. Wilson NK, Miranda-Saavedra D, Kinston S, Bonadies N, Foster SD, Calero-Nieto F, Dawson MA, Donaldson IJ, Dumon S, Frampton J, et al. The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood 2009, 113: 5456-5465.
65. Lecuyer E, Herblot S, Saint-Denis M, Martin R, Begley CG, Porcher C, Orkin SH, Hoang T. The SCL complex regulates c-kit expression in hematopoietic cells through functional interaction with Sp1. Blood 2002, 100:2430-2440.
66. Herblot S, Steff AM, Hugo P, Aplan PD, Hoang T. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T α chain expression. Nat Immunol 2000, 1:138-144.
67. Landry JR, Kinston S, Knezevic K, de Bruijn MF, Wilson N, Nottingham WT, Peitz M, Edenhofer F, Pimanda JE, Ottersbach K, et al. Runx genes are direct targets of Scl/Tal1 in the yolk sac and fetal liver. Blood 2008, 111:3005-3014.
68. Kim WY, Sieweke M, Ogawa E, Wee HJ, Englmeier U, Graf T, Ito Y. Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains. EMBO J 1999, 18: 1609-1620.
69. Taghon T, Yui MA, Rothenberg EV. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat Immunol 2007, 8:845-855.
70. Wang HC, Perry SS, Sun XH. Id1 attenuates Notch signaling and impairs T-cell commitment by elevating Deltex1 expression. Mol Cell Biol 2009, 29:4640-4652.
71. Yang XO, Doty RT, Hicks JS, Willerford DM. Regulation of T-cell receptor D β 1 promoter by KLF5 through reiterated GC-rich motifs. Blood 2003, 101:4492-4499.
72. Wei W, Wen L, Huang P, Zhang Z, Chen Y, Xiao A, Huang H, Zhu Z, Zhang B, Lin S. Gfi1.1 regulates hematopoietic lineage differentiation during zebrafish embryogenesis. Cell Res 2008, 18:677-685.
73. Koldehoff M, Zakrzewski JL, Klein-Hitpass L, Beelen DW, Elmaagacli AH. Gene profiling of growth factor independence 1B gene (Gfi-1B) in leukemic cells. Int J Hematol 2008, 87:39-47.
74. Doan LL, Porter SD, Duan Z, Flubacher MM, Montoya D, Tsichlis PN, Horwitz M, Gilks CB, Grimes HL. Targeted transcriptional repression of Gfi1 by GFI1 and GFI1B in lymphoid cells. Nucleic Acids Res 2004, 32:2508-2519.
75. Chari S, Winandy S. Ikaros regulates Notch target gene expression in developing thymocytes. J Immunol 2008, 181:6265-6274.
76. Kikuchi K, Lai AY, Hsu CL, Kondo M. IL-7 receptor signaling is necessary for stage transition in adult B cell development through up-regulation of EBF. J Exp Med 2005, 201:1197-1203.
77. Yu Q, Erman B, Park JH, Feigenbaum L, Singer A. IL-7 receptor signals inhibit expression of transcription factors TCF-1, LEF-1, and RORγt: impact on thymocyte development. J Exp Med 2004, 200:797-803.
78. Grutz GG, Bucher K, Lavenir I, Larson T, Larson R, Rabbitts TH. The oncogenic T cell LIM-protein Lmo2 forms part of a DNA-binding complex specifically in immature T cells. EMBO J 1998, 17:4594-4605.
79. McCormack MP, Young LF, Vasudevan S, de Graaf CA, Codrington R, Rabbitts TH, Jane SM, Curtis DJ. The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte self-renewal. Science 2010, 327:879-883.
80. Maurice D, Hooper J, Lang G, Weston K. c-Myb regulates lineage choice in developing thymocytes via its target gene Gata3. EMBO J 2007, 26:3629-3640.
81. Franco CB, Scripture-Adams DD, Proekt I, Taghon T, Weiss AH, Yui MA, Adams SL, Diamond RA, Rothenberg EV. Notch/Delta signaling constrains reengineering of pro-T cells by PU.1. Proc Natl Acad Sci U S A 2006, 103:11993-11998.
82. Maillard I, Tu L, Sambandam A, Yashiro-Ohtani Y, Millholland J, Keeshan K, Shestova O, Xu L, Bhandoola A, Pear WS. The requirement for Notch signaling at the β-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J Exp Med 2006, 203:2239-2245.
83. Gonzalez-Garcia S, Garcia-Peydro M, Martin-Gayo E, Ballestar E, Esteller M, Bornstein R, de la Pompa JL, Ferrando AA, Toribio ML. CSL-MAML-dependent Notch1 signaling controls T lineage-specific IL-7R{α} gene expression in early human thymopoiesis and leukemia. J Exp Med 2009, 206:779-791.
84. Krebs LT, Deftos ML, Bevan MJ, Gridley T. The Nrarp gene encodes an ankyrin-repeat protein that is transcriptionally regulated by the notch signaling pathway. Dev Biol 2001, 238:110-119.
85. Pirot P, van Grunsven LA, Marine JC, Huylebroeck D, Bellefroid EJ. Direct regulation of the Nrarp gene promoter by the Notch signaling pathway. Biochem Biophys Res Commun 2004, 322:526-534.
86. Reizis B, Leder P. Direct induction of T lymphocyte-specific gene expression by the mammalian Notch signaling pathway. Genes Dev 2002, 16:295-300.
87. Nakagawa M, Ichikawa M, Kumano K, Goyama S, Kawazu M, Asai T, Ogawa S, Kurokawa M, Chiba S. AML1/Runx1 rescues Notch1-null mutation-induced deficiency of para-aortic splanchnopleural hematopoiesis. Blood 2006, 108:3329-3334.
88. Yun TJ, Bevan MJ. Notch-regulated ankyrin-repeat protein inhibits Notch1 signaling: multiple Notch1 signaling pathways involved in T cell development. J Immunol 2003, 170:5834-5841.
89. Chang HC, Han L, Jabeen R, Carotta S, Nutt SL, Kaplan MH. PU.1 regulates TCR expression by modulating GATA-3 activity. J Immunol 2009, 183:4887-4894.
90. DeKoter RP, Lee HJ, Singh H. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity 2002, 16:297-309.
91. Landry JR, Bonadies N, Kinston S, Knezevic K, Wilson NK, Oram SH, Janes M, Piltz S, Hammett M, Carter J, et al. Expression of the leukemia oncogene Lmo2 is controlled by an array of tissue-specific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 2009, 113:5783-5792.
92. Chan WY, Follows GA, Lacaud G, Pimanda JE, Landry JR, Kinston S, Knezevic K, Piltz S, Donaldson IJ, Gambardella L, et al. The paralogous hematopoietic regulators Lyl1 and Scl are coregulated by Ets and GATA factors, but Lyl1 cannot rescue the early Scl-/- phenotype. Blood 2007, 109:1908-1916.
93. Okuno Y, Huang G, Rosenbauer F, Evans EK, Radomska HS, Iwasaki H, Akashi K, Moreau-Gachelin F, Li Y, Zhang P, et al. Potential autoregulation of transcription factor PU.1 by an upstream regulatory element. Mol Cell Biol 2005, 25:2832-2845.
94. Zarnegar MA, Chen J, Rothenberg EV. Cell-type-specific activation and repression of PU.1 by a complex of discrete, functionally specialized cis-regulatory elements. Mol Cell Biol 2010, 30:4922-4939.
95. Yannoutsos N, Barreto V, Misulovin Z, Gazumyan A, Yu W, Rajewsky N, Peixoto BR, Eisenreich T, Nussenzweig MC. A cis element in the recombination activating gene locus regulates gene expression by counteracting a distant silencer. Nat Immunol 2004, 5:443-450.
96. Rosenbauer F, Owens BM, Yu L, Tumang JR, Steidl U, Kutok JL, Clayton LK, Wagner K, Scheller M, Iwasaki H, et al. Lymphoid cell growth and transformation are suppressed by a key regulatory element of the gene encoding PU.1. Nat Genet 2006, 38:27-37.
97. Guo L, Wei G, Zhu J, Liao W, Leonard WJ, Zhao K, Paul W. IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc Natl Acad Sci U S A 2009, 106:13463-13468.
98. Van de Walle I, De Smet G, De Smedt M, Vandekerckhove B, Leclercq G, Plum J, Taghon T. An early decrease in Notch activation is required for human TCR-αβ lineage differentiation at the expense of TCR-γδ T cells. Blood 2009, 113:2988-2998.
99. Weerkamp F, Luis TC, Naber BA, Koster EE, Jeannotte L, van Dongen JJ, Staal FJ. Identification of Notch target genes in uncommitted T-cell progenitors: no direct induction of a T-cell specific gene program. Leukemia 2006, 20:1967-1977.
100. Tydell CC, David-Fung ES, Moore JE, Rowen L, Taghon T, Rothenberg EV. Molecular dissection of prethymic progenitor entry into the T lymphocyte developmental pathway. J Immunol 2007, 179:421-438.
101. Huang G, Zhang P, Hirai H, Elf S, Yan X, Chen Z, Koschmieder S, Okuno Y, Dayaram T, Growney JD, et al. PU.1 is a major downstream target of AML1 (RUNX1) in adult mouse hematopoiesis. Nat Genet 2008, 40:51-60.
102. Li TW, Ting JH, Yokoyama NN, Bernstein A, van de Wetering M, Waterman ML. Wnt activation and alternative promoter repression of LEF1 in colon cancer. Mol Cell Biol 2006, 26:5284-5299.
103. Yu Q, Sharma A, Oh SY, Moon HG, Hossain MZ, Salay TM, Leeds KE, Du H, Wu B, Waterman ML, et al. T cell factor 1 initiates the T helper type 2 fate by inducing the transcription factor GATA-3 and repressing interferon-γ. Nat Immunol 2009, 10:992-999.
104. Longabaugh WJ, Davidson EH, Bolouri H. Computational representation of developmental genetic regulatory networks. Dev Biol 2005, 283:1-16.
105. Longabaugh WJ, Davidson EH, Bolouri H. Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. Biochim Biophys Acta 2009, 1789:363-374.
106. Jeannet G, Scheller M, Scarpellino L, Duboux S, Gardiol N, Back J, Kuttler F, Malanchi I, Birchmeier W, Leutz A, et al. Long-term, multilineage hematopoiesis occurs in the combined absence of β-catenin and γ-catenin. Blood 2008, 111:142-149.
107. Rothenberg EV, Moore JE, Yui MA. Launching the T-cell-lineage developmental programme. Nat Rev Immunol 2008, 8:9-21.
108. Alon U. An Introduction to Systems Biology: Design Principles of Biological Circuits. Chapman & Hall/CRC Mathematical and Computational Biology Series, vol xvi. Boca Raton, FL: Chapman & Hall/CRC; 2007, 301 p., 4 p. of plates.
109. Saba I, Kosan C, Vassen L, Moroy T. IL-7R-dependent survival and differentiation of early T-lineage progenitors is regulated by the BTB/POZ domain transcription factor Miz-1. Blood 2011, 117: 3370-3381.
110. Henriques CM, Rino J, Nibbs RJ, Graham GJ, Barata JT. IL-7 induces rapid clathrin-mediated internalization and JAK3-dependent degradation of IL-7Rα in T cells. Blood 2010, 115:3269-3277.
111. Alves NL, van Leeuwen EM, Derks IA, van Lier RA. Differential regulation of human IL-7 receptor α expression by IL-7 and TCR signaling. J Immunol 2008, 180:5201-5210.
112. Park JH, Yu Q, Erman B, Appelbaum JS, Montoya-Durango D, Grimes HL, Singer A. Suppression of IL7Rα transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 2004, 21:289-302.
113. Busslinger M. Transcriptional control of early B cell development. Annu Rev Immunol 2004, 22:55-79.
114. Decker T, Pasca di Magliano M, McManus S, Sun Q, Bonifer C, Tagoh H, Busslinger M. Stepwise activation of enhancer and promoter regions of the B cell commitment gene Pax5 in early lymphopoiesis. Immunity 2009, 30:508-520.
115. Nutt SL, Metcalf D, D'Amico A, Polli M, Wu L. Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J Exp Med 2005, 201:221-231.
116. Back J, Allman D, Chan S, Kastner P. Visualizing PU.1 activity during hematopoiesis. Exp Hematol 2005, 33:395-402.
117. Alon U. Network motifs: theory and experimental approaches. Nat Rev Genet 2007, 8:450-461.
118. Davidson EH. The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. San Diego, CA: Academic Press; 2006.
119. Enver T, Pera M, Peterson C, Andrews PW. Stem cell states, fates, and the rules of attraction. Cell Stem Cell 2009, 4:387-397.
120. Rothenberg EV, Anderson MK. Elements of transcription factor network design for T-lineage specification. Dev Biol 2002, 246:29-44.