Abstract
Wnt signaling elicits changes in gene expression and cell physiology through β-catenin and LEF1/TCF proteins. The signal transduction pathway regulates many cellular and developmental processes, including cell proliferation, cell fate decisions and differentiation. In cells that have been stimulated by a Wnt protein, cytoplasmic β-catenin is stabilized and transferred to the nucleus, where it interacts with the nuclear mediators of Wnt signaling, the LEF1/TCF proteins, to elicit a transcriptional response. Loss-of-function and gain-of-function experiments in the mouse have provided insight into the role of this signaling pathway in lymphopoiesis. The self-renewal and maintenance of hematopoietic stem cells is regulated by Wnt signals. Differentiation of T cells and natural killer cells is blocked in the absence of LEF1/TCF proteins, and pro-B cell proliferation is regulated by Wnt signaling.
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References
Aberle H, Bauer A, Stappert J, Kispert A, Kemler R (1997) Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797–3804
Ahumada A, Slusarski DC, Liu X, Moon RT, Malbon CC, Wang HY (2002) Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298:2006–2010
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
Atcha FA, Munguia JE, Li TW, Hovanes K, Waterman ML (2003) A new beta-catenin-dependent activation domain in T cell factor. J Biol Chem 278:16169–16175
Austin TW, Solar GP, Ziegler FC, Liem L, Matthews W (1997) A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells. Blood 89:3624–3635
Balciunaite G, Keller MP, Balciunaite E, Piali L, Zuklys S, Mathieu YD, Gill J, Boyd R, Sussman DJ, Hollander GA (2002) Wnt glycoproteins regulate the expression of FoxN1, the gene defective in nude mice. Nat Immunol 3:1102–1108
Barker N, Hurstone A, Musisi H, Miles A, Bienz M, Clevers H (2001) The chromatin remodeling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J 20:4935–4943
Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H (2002) Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111:251–263
Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, Wirtz R, Kuhl M, Wedlich D, Birchmeier W (1998) Functional interaction of an axin homolog, conductin, with beta-catenin APC, and GSK3beta. Science 280:596–599
Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W (1996) Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382:638–642
Belenkaya TY, Han C, Standley HJ, Lin X, Houston DW, Heasman J, Lin X (2002) Pygopus encodes a nuclear protein essential for wingless/Wnt signaling. Development 129:4089–4101
Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R (1996) A new member of the Frizzled family from Drosophila functions as a Wingless receptor. Nature 382:225–230
Bienz M (1998) TCF: transcriptional activator or repressor? Curr Opin Cell Biol 10:366–372
Bradley RS, Brown AM (1990) The proto-oncogene int-1 encodes a secreted protein associated with the extracellular matrix. EMBO J 9:1569–1575
Brannon M, Gomperts M, Sumoy L, Moon R, Kimelman D (1997) A b-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev 11:2359–2370
Brannon M, Brown JD, Bates R, Kimelman D, Moon RT (1999) XCtBP is a XTcf-3 corepressor with roles throughout Xenopus development. Development 126:3159–3170
Brantjes H, Roose J, van de Wetering M, Clevers H (2001) All Tcf HMG box transcription factors interact with Groucho-related corepressors. Nucleic Acid Res 29:1410–1419
Brennan J, Mager D, Jefferies W, Takei F (1994) Expression of different members of the Ly-49 gene family defines distinct natural killer cell subsets and cell adhesion properties. J Exp Med 180:2287–2295
Bruhn L, Munnerlyn A, Grosschedl R (1997) ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRalpha enhancer function. Genes Dev 11:640–653
Carlsson P, Waterman ML, Jones KA (1993) The hLEF/TCF-1 alpha HMG protein contains a context-dependent transcriptional activation domain that induces the TCR alpha enhancer in T cells. Genes Dev 5:880–894
Cavallo R, Cox R, Moline M, Roose J, Polevoy G, Clevers H, Pfeifer M, Bejsovec A (1998) Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 8:181–190
Cobas M, Wilson A, Ernst B, Stéphane JC, Mancini H, MacDonald R, Kemler R, Radtke F (2004) β-Catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 199:221–229
Collins RT, Treisman JE (2000) Osa-containing Brahma chromatin remodelling complexes are required for the repression of wingless target genes. Genes Dev 14:3140–3152
Daniels DL, Weis WI (2002) ICAT inhibits beta-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol Cell 10:573–584
David RP, Tree DM, Axelrod JD (2002) A three-tiered mechanism for regulation of planar cell polarity. Semin Cell Dev Biol 13:217–224
Fisher A, Caudy M (1998) Groucho proteins: transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev 12:1931–1940
Galceran J, Farinas I, Depew MJ, Grosschedl R (1999) Wnt3a-/--like phenotype and limb deficiency in Lef1-/-Tcf1-/- mice. Genes Dev 13:709–717
Galceran J, Miyashita-Lin E, Devaney E, Rubenstein J, Grosschedl R (2000) Hippocampus development and generation of dentate gyrus cells is regulated by LEF1. Development 127:469–482
Giese K, Grosschedl R (1993) LEF-1 contains an activation domain that stimulates transcription only in a specific context of factor-binding sites. EMBO J 12:4667–4676
Giese K, Amsterdam A, Grosschedl R (1991) DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev 5:2567–2578
Giese K, Cox J, Grosschedl R (1992) The HMG domain of the lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69:185–195
Giese K, Kingsley C, Kirshner JR, Grosschedl R (1995) Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev 9:995–1008
Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A (1994) Onset of the TCR-β gene rearrangement and the role of TCR-β expression during CD3−CD4−CD8− thymocyte differentiation. J Immunology 152:4783–4792
Gounari F, Aifantis I, Khazaie K, Hoeflinger S, Harada N, Taketo MM, von Boehmer H (2001) Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat Immunol 2:863–869
Graham TA, Weaver C, Mao F, Kimelman D, Xu W (2000) Crystal structure of a beta-catenin/Tcf complex. Cell 103:885–896
Graham TA, Clements WK, Kimelman D, Xu W (2002) The crystal structure of the beta-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol Cell 10:563–571
Hardy RR, Carmack CE, Shinton SA, Kemp JD, Hayakawa K (1991) Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med 173:1213–1225
Hattori N, Kawamoto H, Fujimoto S, Kuno K, Katsura Y (1996) Involvement of transcription factors TCF-1 and GATA-3 in the initiation of the earliest step of T cell development in the thymus. J Exp Med 184:1137–1147
Hecht A, Stemmler MP (2003) Identification of a promoter-specific transcriptional activation domain at the C terminus of the Wnt effector protein T-cell factor 4. J Biol Chem 278:3776–3785
Hecht A, Litterst CM, Huber O, Kemler R (1999) Functional characterization of multiple transactivating elements in beta-catenin, some of which interact with the TATA-binding protein in vitro. J Biol Chem 274:18017–18025
Hecht A, Vleminckx K, Stemmler MP, Van Roy F, Kemler R (2000) The p300/CBP acetyltransferase function as transcriptional coactivators of b-catenin in vertebrates. EMBO J 19:1839–1850
Held W, Kunz B, Lowing-Kropf B, van de Wetering M, Clevers H (1999) Clonal acquisition of the Ly49A NK cell receptor is dependent on the trans-acting factor TCF-1. Immunity 11:433–442
Held W, Clevers H, Grosschedl R (2003) Redundant functions of TCF-1 and LEF-1 during T and NK cell development, but unique role of TCF-1 for Ly49 NK cell receptor acquisition. Eur J Immunol 33:1393–1398
Hinck L, Nathke IS, Papkoff J, Nelson WJ (1994a) Beta-catenin: a common target for the regulation of cell adhesion by Wnt-1 and Src signaling pathways. Trends Biochem Sci 19:538–542
Hinck L, Nelson WJ, Papkoff J (1994b) Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing beta-catenin binding to the cell adhesion protein cadherin. J Cell Biol 124:729–741
Houghton L, Freeman A, Morgan BA (2003) Expression and regulation of Groucho-related genes in the embryonic chicken feather bud. Dev Dyn 226:587–595
Hsu S-C, Galceran J, Grosschedl R (1998) Modulation of the transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with β-catenin. Mol Cell Biol 18:4807–4818
Hsu W, Shakya R, Costantini F (2001) Impaired mammary gland and lymphoid development caused by inducible expression of Axin in transgenic mice. J Cell Biol 155:1055–1064
Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R (1996) Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev 59:3–10
Hurlstone A, Clevers H (2002) T-cell factors: turn-ons and turn-offs. EMBO J 21:2303–2311
Ikeda S, Kishida M, Matsuura Y, Usui H, Kikuchi A (2000) GSK-3beta-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by beta-catenin and protein phosphatase 2A complexed with Axin. Oncogene 19:537–545
Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17:1371–1384
Ioannidis V, Beermann F, Clevers H, Held W (2001) The beta-catenin-TCF-1 pathway ensures CD4(+)CD8(+) thymocyte survival. Nat Immunol 2:691–697
Ishitani T, Ninomiya-Tsuji J, Matsumoto K (2003) Regulation of lymphoid enhancer factor 1/T-cell factor by mitogen-activated protein kinase-related Nemo-like kinase-dependent phosphorylation in Wnt/beta-catenin signaling. Mol Cell Biol 23:1379–1389
Itoh K, Antipova A, Ratcliffe MJ, Sokol S (2000) Interaction of dishevelled and Xeno-pus axin-related protein is required for wnt signal transduction. Mol Cell Biol 20:2228–2238
Jamora C, DasGupta R, Kocieniewski P, Fuchs E (2003) Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422:317–322
Jiang J, Struhl G (1998) Regulation of the Hedgehog and wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391:493–496
Karlhofer FM, Ribaudo RK, Yokoyama WM (1992) MHC class I alloantigen specificity of Ly-49+ IL-2 activated natural killer cells. Nature 358:66–70
Kishida S, Yamamoto H, Ikeda S, Kishida M, Sakamoto I, Koyama S, Kikuchi A (1998) Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of β-catenin. J Biol Chem 273:10823–10826
Kishida S, Yamamoto H, Hino S, Ikeda S, Kishida M, Kikuchi A (1999) DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Mol Cell Biol 19:4414–4422
Kondo M, Weissman IL, Akashi K (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:661–672
Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H (1998a) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19:379–383
Korinek V, Barker N, Willert K, Molenaar M, Roose J, Wagenaar G, Markman M, Lamers W, Destree O, Clevers H (1998b) Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol Cell Biol 18:1248–1256
Kramps T, Peter O, Brunner E, Nellen D, Froesch B, Chatterjee S, Murone M, Zullig S, Basler K (2002) Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109:47–60
Kratochwil K, Galceran J, Tontsch S, Roth W, Grosschedl R (2002) FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev 16:3173–3185
Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT (2000) The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 16:279–283
Labbe E, Letamendia A, Attisano L (2000) Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc Natl Acad Sci USA 97:8358–8363
Levanon D, Goldstein RE, Bernstein Y, Tang H, Goldenberg D, Stifani S, Paroush Z, Gromer Y (1998) Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc Natl Acad Sci USA 95:11590–11595
Li YS, Wasserman R, Hayakawa K, Hardy RR (1996) Identification of the earliest B lineage stage in mouse bone marrow. Immunity 5:527–535
Logie C, Peterson CL (1997) Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J 16:6772–6782
Mao B, Niehrs C (2003) Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene 302:179–183
Mao B, Wu W, Davidson G, Marhold J, Li M, Mechler BM, Delius H, Hoppe D, Stannek P, Walter C, Glinka A, Niehrs C (2002) Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 417:664–667
Marikawa Y, Elinson R (1998) β-TrCP is a negative regulator of Wnt/β-catenin signaling pathway and dorsal axis formatin in Xenopus embryos. Mech Dev 77:75–80
McCrea PD, Turck CW, Gumbiner B (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 154:1359–1361
McQueen KL, Freeman JD, Takei F, Mager DL (1998) Localization of five new Ly49 genes, including three closely related to Ly49c. Immunogenetics 48:174–183
McWhirter JR, Neuteboom ST, Wancewicz EV, Monia BP, Downing JR, Murre C (1999) Oncogenic homeodomain transcription factor E2A-Pbx1 activates a novel WNT gene in pre-B acute lymphoblastoid leukemia. Proc Natl Acad Sci USA 96:11464–11469
Miyagishi M, Fujii R, Hatta M, Yoshida E, Araya N, Nagafuchi A, Ishihara S, Nakajima T, Fukamizu A (2000) Regulation of Lef-mediated transcription and p53-dependent pathway by associating β-catenin with CBP/p300. J Biol Chem 275:35170–35175
Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O, Clevers H (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391–399
Mombaerts P, Clarke AR, Rudnicki MA, Iacomini J, Itohara S, Lafaille JJ, Wang L, Ichikawa Y, Jaenisch R, Hooper ML et al. (1992) Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 360:225–231
Mulroy T, McMahon JA, Burakoff SJ, McMahon AP, Sen J (2002) Wnt-1 and Wnt-4 regulate thymic cellularity. Eur J Immunol 32:967–971
Nishita M, Hashimoto MK, Ogata S, Laurent MN, Ueno N, Shibuya H, Cho KW (2000) Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann s organizer. Nature 403:781–785
Noordermeer J, Klingensmith J, Perrimon N, Nusse R (1994) dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature 367:80–83
Okamura RM, Sigvardsson M, Galceran J, Verbeek S, Clevers H, Grosschedl R (1998) Redundant regulation of T cell differentiation and TCRα gene expression by the transcription factors LEF-1 and TCF-1. Immunity 8:11–20
Oosterwegel M, van de Wetering M, Dooijes D, Klomp L, Winoto A, Georgopoulos K, Meijlink F, Clevers H (1991) Cloning of murine TCF-1, a T cell-specific transcription factor interacting with functional motifs in the CD3-epsilon and T cell receptor alpha enhancers. J Exp Med 173:1133–1142
Osawa M, Hanada K, Hamada H, Nakauchi H (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273:242–245
Papkoff J, Schryver B (1990) Secreted int-1 protein is associated with the cell surface. Mol Cell Biol 10:2723–2730
Parker DS, Jemison J, Cadigan KM (2002) Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129:2565–2576
Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC (2000) An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535–538
Reya T, O’Riordan M, Okamura R, Devaney E, Willert K, Nusse R, Grosschedl R (2000) Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 13:15–24
Reya T, Duncan AW, Ailles L, Domen J, Sherer DC, Willert K, Hintz L, Nusse R, Weismann IL (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423:409–414
Riese J, Yu X, Munnerlyn A, Eresh S, Hsu S, Grosschedl R, Bienz M (1997) LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88:777–787
Rolink A, Melchers F (1993) B lymphopoiesis in the mouse. Adv Immunol 53:123–156
Roose J, Molenaar M, Peterson J, Hurenkamp J, Brantjes H, Moerer P, van de Wetering M, Destree O, Clevers H (1998) The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395:608–612
Ross DA, Kadesch T (2001) The notch intracellular domain can function as a coactivator for LEF-1. Mol Cell Biol 21:7537–7544
Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15:3088–3103
Saint-Ruf C, Ungewiss K, Groettrup M, Bruno L, Fehling HJ, von Boehmer H (1994) Analysis and expression of a cloned pre-T cell receptor gene. Science 266:1208–1212
Schilham MW, Wilson A, Moerer P, Benaissa-Trouw BJ, Cumano A, Clevers HC (1998) Critical involvement of Tcf-1 in expansion of thymocytes. J Immunol 161:3984–3991
Slusarski DC, Corces VG, Moon RT (1997) Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390:410–413
Smalley MJ, Sara E, Paterson H, Naylor S, Cook D, Jayatilake H, Fryer LG, Hutchinson L, Fry MJ, Dale TC (1999) Interaction of axin and Dvl-2 proteins regulates Dvl-2-stimulated TCF-dependent transcription. EMBO J 18:2823–2835
Smith HRC, Karlhofer FM, Yokoyama WM (1994) Ly-49 multigene family expressed by IL-2 activated NK-cells. J Immunol 153:1068–1079
Staal FJ, Meeldijk J, Moerer P, Jay P, van de Weerdt BC, Vainio S, Nolan GP, Clevers H (2001) Wnt signaling is required for thymocyte development and activates Tcf-1 mediated transcription. Eur J Immunol 31:285–293
Staal FJ, van Noort M, Strous GJ, Clevers HC (2002) Wnt signals are transmitted through N-terminally dephosphorylated β-catenin. EMBO Reports 3:63–68
Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez-Navarro S, Rondon AG, Aguilera A, Struhl K, Reed R, Hurt E (2002) TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417:304–308
Tago K, Nakamura T, Nishita M, Hyodo J, Nagai S, Murata Y, Adachi S, Ohwada S, Morishita Y, Shibuya H, Akiyama T (2000) Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev 14:1741–1749
Takada S, Stark KL, Shea MJ, Vassileva G, McMahon JA, McMahon AP (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174–189
Takemaru KI, Moon RT (2000) The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J Biol Chem 149:249–254
Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X (2000) LDL-receptor-related proteins in Wnt signal transduction. Nature 407:530–535
Thompson B, Townsley F, Rosin-Arbesfeld R, Musisi H, Bienz M (2002) A new nuclear component of the Wnt signalling pathway. Nat Cell Biol 4:367–373
Travis A, Amsterdam A, Belanger C, Grosschedl R (1991) LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain regulates T-cell receptor α enhancer function. Genes Dev 5:880–894
Tutter AV, Fryer CJ, Jones KA (2001) Chromatin-specific regulation of LEF-1-beta-catenin transcription activation and inhibition in vitro. Genes Dev 15:3342–3354
Van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789–799
Van de Wetering M, Oosterwegel M, Dooijes D, Clevers H (1991) Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J 10:123–132
Van den Berg D, Sharma AK, Bruno E, Hoffman R (1998) Role of members of the Wnt gene family in human hematopoiesis. Blood 92:3189–3202
Van Genderen C, Okamura RM, Farinas I, Quo RG, Parslow TG, Bruhn L, Grosschedl R (1994) Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 8:2691–2703
Verbeek S, Izon D, Hofhuis F, Robanus-Maandag E, te Riele H, van de Wetering M, Oosterwegel M, Wilson A, MacDonald HR, Clevers H (1995) An HMG-box-containing T-cell factor required for thymocyte differentiation. Nature 374:70–74
Wang HY, Malbon CC (2003) Wnt signaling Ca2+, and cyclic GMP: visualizing Frizzled functions. Science 300:1529–1530
Weber U, Paricio N, Mlodzik M (2000) Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye. Development 127:3619–3629
Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168
Wheelock MJ, Knudsen KA (1991) Cadherins and associated proteins. In Vivo 5:505–513
Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR 3rd, Nusse R (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448–452
Wong S, Freeman JD, Kelleher C, Mager D, Takei F (1991) Ly-49 multigene family. New members of a superfamily of type II membrane proteins with lectin-like domains. J Immunol 147:1417–1423
Wu L, Scollay R, Egerton M, Pearse M, Spangurude GJ, Shortman K (1991) CD4 expressed on earliest T-lineage precursor cells in the adult mouse thymus. Nature 374:71–74
Xu Y, Banerjee D, Huelsken J, Birchmeier W, Sen JM (2003) Deletion of β-catenin impairs T cell development. Nat Immunol 4:1177–1182
Yamamoto H, Ihara M, Matsuura Y, Kikuchi A (2003) Sumoylation is involved in beta-catenin-dependent activation of Tcf-4. EMBO J 22:2047–2059
Zhang HS, Gavin M, Dahiya A, Postigo AA, Ma D, Luo RX, Harbour JW, Dean DC (2000) Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101:79–89
Zhou Z, Luo MJ, Straesser K, Katahira J, Hurt E, Reed R (2000) The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407:401–405
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Timm, A., Grosschedl, R. (2005). Wnt Signaling in Lymphopoiesis. In: Singh, H., Grosschedl, R. (eds) Molecular Analysis of B Lymphocyte Development and Activation. Current Topics in Microbiology and Immunology, vol 290. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-26363-2_10
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