E proteins in lymphocyte development and lymphoid diseases

Current Topics in Developmental Biology

Volumn 110, Issue , 2014, Pages 153-187

  Belle, Ian ^a   Zhuang, Yuan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

B cell; Burkitt Lymphoma; Development; E2A; HEB; Id2; Id3; Sjogren's Syndrome; T cell

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR; TCF12 PROTEIN, HUMAN; TCF3 PROTEIN, HUMAN;

ANIMAL; AUTOIMMUNE DISEASE; CELL DIFFERENTIATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; GENETICS; HUMAN; LYMPHATIC SYSTEM DISEASE; LYMPHOCYTE; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL SURVIVAL; HUMANS; LYMPHATIC DISEASES; LYMPHOCYTES; NEOPLASMS; RECEPTORS, ANTIGEN;

EID: 84907705376     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-405943-6.00004-X     Document Type: Chapter

References (133)

1. Alexander E.L., Arnett F.C., Provost T.T., Stevens M.B. Sjögren's syndrome: Association of anti-Ro (SS-A) antibodies with vasculitis, hematologic abnormalities, and serologic hyperreactivity. Annals of Internal Medicine 1983, 98(2):155-159.
2. Alexander E., Hirsch T., Arnett F., Provost T., Stevens M. Ro (SSA) and La (SSB) antibodies in the clinical spectrum of Sjogren's syndrome. The Journal of Rheumatology 1981, 9(2):239-246.
3. Anderson G., Jenkinson E.J., Moore N.C., Owen J.J. MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 1993, 362:70-73.
4. Aronheim A., Shiran R., Rosen A., Walker M.D. The E2A gene product contains two separable and functionally distinct transcription activation domains. Proceedings of the National Academy of Sciences 1993, 90(17):8063-8067.
5. Austin T.W., Solar G.P., Ziegler F.C., Liem L., Matthews W. A role for the Wnt gene family in hematopoiesis: Expansion of multilineage progenitor cells. Blood 1997, 89(10):3624-3635.
6. Azuara V., Grigoriadou K., Lembezat M.P., Nagler Anderson C., Pereira P. Strain-specific TCR repertoire selection of IL-4-producing Thy-1dull γ δ thymocytes. European Journal of Immunology 2001, 31(1):205-214.
7. Bain G., Cravatt C.B., Loomans C., Alberola-Ila J., Hedrick S.M., Murre C. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nature Immunology 2001, 2(2):165-171.
8. Bain G., Engel I., Maandag E.R., Te Riele H., Voland J.R., Sharp L.L., et al. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Molecular and Cellular Biology 1997, 17(8):4782-4791.
9. Bain G., Maandag E.C.R., Izon D.J., Amsen D., Kruisbeek A.M., Weintraub B.C., et al. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 1994, 79(5):885-892.
10. Barker N., Clevers H. Mining the Wnt pathway for cancer therapeutics. Nature Reviews Drug Discovery 2006, 5(12):997-1014.
11. Barndt R.J., Dai M., Zhuang Y. Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Molecular and Cellular Biology 2000, 20(18):6677-6685.
12. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. The protein Id: A negative regulator of helix-loop-helix DNA binding proteins. Cell 1990, 61(1):49-59.
13. Bishop P.C., Rao V.K., Wilson W.H. Burkitt's lymphoma: Molecular pathogenesis and treatment. Cancer Investigation 2000, 18(6):574-583.
14. Bloch K., Buchanan W., Wohl M., Bunim J. Sjogren's syndrome: A clinical, pathological, and serological study of sixty-two cases. Medicine 1965, 44(3):187-231.
15. Blom B., Heemskerk M.H., Verschuren M.C., Van Dongen J.J., Stegmann A.P., Bakker A.Q., et al. Disruption of αβ but not of γδ T cell development by overexpression of the helix-loop-helix protein Id3 in committed T cell progenitors. The EMBO Journal 1999, 18(10):2793-2802.
16. Boisson B., Wang Y.-D., Bosompem A., Ma C.S., Lim A., Kochetkov T., et al. A recurrent dominant negative E47 mutation causes agammaglobulinemia and BCR-B cells. The Journal of Clinical Investigation 2013, 123(11):4781.
17. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. The Journal of Experimental Medicine 2007, 204(5):1119-1130.
18. Buch T., Rieux-Laucat F., Förster I., Rajewsky K. Failure of HY-specific thymocytes to escape negative selection by receptor editing. Immunity 2002, 16(5):707-718.
19. Butler R.D., Hainsworth J.D. Optimal therapy for small noncleaved cell lymphoma. Malignant lymphomas, including Hodgkin's disease: diagnosis, management, and special problems 1993, 65-67. Springer, Boston, MA. W.D. Dana (Ed.).
20. Caricasole A., Copani A., Caruso A., Caraci F., Iacovelli L., Sortino M.A., et al. The Wnt pathway, cell-cycle activation and β-amyloid: Novel therapeutic strategies in Alzheimer's disease?. Trends in Pharmacological Sciences 2003, 24(5):233-238.
21. Chan E.A., Teng G., Corbett E., Choudhury K.R., Bassing C.H., Schatz D.G., et al. Peripheral subnuclear positioning suppresses Tcrb recombination and segregates Tcrb alleles from RAG2. Proceedings of the National Academy of Sciences 2013, 110(48):E4628-E4637.
22. Choi J.K., Shen C.-P., Radomska H., Eckhardt L., Kadesch T. E47 activates the Ig-heavy chain and TdT loci in non-B cells. The EMBO Journal 1996, 15(18):5014.
23. Dalavanga Y., Drosos A., Moutsopoulos H. Labial salivary gland immunopathology in Sjogren's syndrome. Scandinavian Journal of Rheumatology. Supplement 1985, 61:67-70.
24. De Vries J.E. The role of IL-13 and its receptor in allergy and inflammatory responses. Journal of Allergy and Clinical Immunology 1998, 102(2):165-169.
25. Deed R.W., Hara E., Atherton G.T., Peters G., Norton J.D. Regulation of Id3 cell cycle function by Cdk-2-dependent phosphorylation. Molecular and Cellular Biology 1997, 17(12):6815-6821.
26. Dias S., Månsson R., Gurbuxani S., Sigvardsson M., Kee B.L. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008, 29(2):217-227.
27. Eckner R., Yao T.-P., Oldread E., Livingston D.M. Interaction and functional collaboration of p300/CBP and bHLH proteins in muscle and B-cell differentiation. Genes & Development 1996, 10(19):2478-2490.
28. Engel I., Johns C., Bain G., Rivera R.R., Murre C. Early thymocyte development is regulated by modulation of E2A protein activity. The Journal of Experimental Medicine 2001, 194(6):733-746.
29. Engel I., Murre C. Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proceedings of the National Academy of Sciences 1999, 96(3):996-1001.
30. Ephrussi A., Church G.M., Tonegawa S., Gilbert W. B lineage-specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science 1985, 227(4683):134-140.
31. Fu X., Roberts W.G., Nobile V., Shapiro R., Kamps M.P. mAngiogenin-3, a target gene of oncoprotein E2a-Pbx1, encodes a new angiogenic member of the angiogenin family. Growth Factors 1999, 17(2):125-137.
32. Fuxa M., Skok J., Souabni A., Salvagiotto G., Roldan E., Busslinger M. Pax5 induces V-to-DJ rearrangements and locus contraction of the immunoglobulin heavy-chain gene. Genes & Development 2004, 18(4):411-422.
33. Ghosh J.K., Romanow W.J., Murre C. Induction of a diverse T cell receptor γ/δ repertoire by the helix-loop-helix proteins E2A and HEB in nonlymphoid cells. The Journal of Experimental Medicine 2001, 193(6):769-776.
34. Goebel P., Janney N., Valenzuela J.R., Romanow W.J., Murre C., Feeney A.J. Localized gene-specific induction of accessibility to V (D) J recombination induced by E2A and early B cell factor in nonlymphoid cells. The Journal of Experimental Medicine 2001, 194(5):645-656.
35. Goldfarb A.N., Flores J.P., Lewandowska K. Involvement of the E2A basic helix-loop-helix protein in immunoglobulin heavy chain class switching. Molecular Immunology 1996, 33(11):947-956.
36. Greenbaum S., Lazorchak A.S., Zhuang Y. Differential functions for the transcription factor E2A in positive and negative gene regulation in pre-B lymphocytes. Journal of Biological Chemistry 2004, 279(43):45028-45035.
37. Greenspan J., Daniels T., Talal N., Sylvester R. The histopathology of Sjögren's syndrome in labial salivary gland biopsies. Oral Surgery, Oral Medicine, Oral Pathology 1974, 37(2):217-229.
38. Grünig G., Warnock M., Wakil A.E., Venkayya R., Brombacher F., Rennick D.M., et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998, 282(5397):2261-2263.
39. Guo Z., Li H., Han M., Xu T., Wu X., Zhuang Y. Modeling Sjögren's syndrome with Id3 conditional knockout mice. Immunology Letters 2011, 135(1):34-42.
40. Hardy R.R., Hayakawa K. B cell development pathways. Annual Review of Immunology 2001, 19(1):595-621.
41. Hayakawa I., Tedder T.F., Zhuang Y. B-lymphocyte depletion ameliorates Sjögren's syndrome in Id3 knockout mice. Immunology 2007, 122(1):73-79.
42. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science 1990, 247(4941):467-470.
43. Herblot S., Steff A.-M., Hugo P., Aplan P.D., Hoang T. SCL and LMO1 alter thymocyte differentiation: Inhibition of E2A-HEB function and pre-Tα chain expression. Nature Immunology 2000, 1(2):138-144.
44. Hogquist K.A., Jameson S.C., Heath W.R., Howard J.L., Bevan M.J., Carbone F.R. T cell receptor antagonist peptides induce positive selection. Cell 1994, 76(1):17-27.
45. Hsu H.-L., Huang L., Tsan J.T., Funk W., Wright W.E., Hu J.-S., et al. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Molecular and Cellular Biology 1994, 14(2):1256-1265.
46. Hsu L.-Y., Lauring J., Liang H.-E., Greenbaum S., Cado D., Zhuang Y., et al. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 2003, 19(1):105-117.
47. Hu J.-S., Olson E., Kingston R. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Molecular and Cellular Biology 1992, 12(3):1031-1042.
48. Hu T., Wang H., Simmons A., Bajaña S., Zhao Y., Kovats S., et al. Increased level of e protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets. The Journal of Immunology 2013, 191(10):5065-5073.
49. Ji Y., Pos Z., Rao M., Klebanoff C.A., Yu Z., Sukumar M., et al. Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ T cells. Nature Immunology 2011, 12(12):1230-1237.
50. Jia J., Dai M., Zhuang Y. E proteins are required to activate germline transcription of the TCR Vβ8. 2 gene. European Journal of Immunology 2008, 38(10):2806-2820.
51. Jones M.E., Zhuang Y. Acquisition of a functional T cell receptor during T lymphocyte development is enforced by HEB and E2A transcription factors. Immunity 2007, 27(6):860-870.
52. Jones-Mason M.E., Zhao X., Kappes D., Lasorella A., Iavarone A., Zhuang Y. E protein transcription factors are required for the development of CD4+ lineage T cells. Immunity 2012, 36(3):348-361.
53. Knoepfler P.S., Calvo K.R., Chen H., Antonarakis S.E., Kamps M.P. Meis1 and pKnox1 bind DNA cooperatively with Pbx1 utilizing an interaction surface disrupted in oncoprotein E2a-Pbx1. Proceedings of the National Academy of Sciences 1997, 94(26):14553-14558.
54. Krangel M.S. Gene segment selection in V (D) J recombination: Accessibility and beyond. Nature Immunology 2003, 4(7):624-630.
55. Kruisbeek A.M., Haks M.C., Carleton M., Wiest D.L., Michie A.M., Zúñiga-Pflücker J.C. Branching out to gain control: How the pre-TCR is linked to multiple functions. Immunology Today 2000, 21(12):637-644.
56. Kusunoki T., Sugai M., Katakai T., Omatsu Y., Iyoda T., Inaba K., et al. TH2 dominance and defective development of a CD8+ dendritic cell subset in Id2-deficient mice. Journal of Allergy and Clinical Immunology 2003, 111(1):136-142.
57. Kwon K., Hutter C., Sun Q., Bilic I., Cobaleda C., Malin S., et al. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 2008, 28(6):751-762.
58. Langerak A.W., Wolvers-Tettero I.L., Van Gastel-Mol E.J., Oud M.E., Van Dongen J.J. Basic helix-loop-helix proteins E2A and HEB induce immature T-cell receptor rearrangements in nonlymphoid cells. Blood 2001, 98(8):2456-2465.
59. Lazorchak A.S., Schlissel M.S., Zhuang Y. E2A and IRF-4/Pip promote chromatin modification and transcription of the immunoglobulin κ locus in pre-B cells. Molecular and Cellular Biology 2006, 26(3):810-821.
60. Lazorchak A.S., Wojciechowski J., Dai M., Zhuang Y. E2A promotes the survival of precursor and mature B lymphocytes. The Journal of Immunology 2006, 177(4):2495-2504.
61. Lee B.H., Gauna A.E., Pauley K.M., Park Y.-J., Cha S. Animal models in autoimmune diseases: Lessons learned from mouse models for Sjögren's syndrome. Clinical Reviews in Allergy & Immunology 2012, 42(1):35-44.
62. Li H., Dai M., Zhuang Y. AT cell intrinsic role of Id3 in a mouse model for primary Sjögren's syndrome. Immunity 2004, 21(4):551-560.
63. Li J., Wu D., Jiang N., Zhuang Y. Combined deletion of Id2 and Id3 genes reveals multiple roles for E proteins in invariant NKT cell development and expansion. The Journal of Immunology 2013, 191(10):5052-5064.
64. Lin Y.C., Benner C., Mansson R., Heinz S., Miyazaki K., Miyazaki M., et al. Global changes in the nuclear positioning of genes and intra-and interdomain genomic interactions that orchestrate B cell fate. Nature Immunology 2012, 13(12):1196-1204.
65. Lin H., Grosschedl R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 1995, 376(6537):263-267.
66. Lin Y.C., Jhunjhunwala S., Benner C., Heinz S., Welinder E., Mansson R., et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nature Immunology 2010, 11(7):635-643. http://www.nature.com/ni/journal/v11/n7/suppinfo/ni.1891_S1.html.
67. Lin Y.-Y., Jones-Mason M.E., Inoue M., Lasorella A., Iavarone A., Li Q.-J., et al. Transcriptional regulator Id2 is required for the CD4 T cell immune response in the development of experimental autoimmune encephalomyelitis. The Journal of Immunology 2012, 189(3):1400-1405.
68. Loffert D., Schaal S., Ehlich A., Hardy R.R., Zou Y.R., Müller W., et al. Early B cell development in the mouse: Insights from mutations introduced by gene targeting. Immunological Reviews 1994, 137(1):135-153.
69. Love C., Sun Z., Jima D., Li G., Zhang J., Miles R., et al. The genetic landscape of mutations in Burkitt lymphoma. Nature Genetics 2012, 44(12):1321-1325.
70. Lu Q., Kamps M.P. Structural determinants within Pbx1 that mediate cooperative DNA binding with pentapeptide-containing Hox proteins: Proposal for a model of a Pbx1-Hox-DNA complex. Molecular and Cellular Biology 1996, 16(4):1632-1640.
71. Lund R.J., Löytömäki M., Naumanen T., Dixon C., Chen Z., Ahlfors H., et al. Genome-wide identification of novel genes involved in early Th1 and Th2 cell differentiation. The Journal of Immunology 2007, 178(6):3648-3660.
72. Mahlios J., Zhuang Y. Contribution of IL-13 to early exocrinopathy in Id3-/- mice. Molecular Immunology 2011, 49(1):227-233.
73. Maraskovsky E., O'Reilly L.A., Teepe M., Corcoran L.M., Peschon J.J., Strasser A. Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- Mice. Cell 1997, 89(7):1011-1019.
74. Massari M.E., Grant P.A., Pray-Grant M.G., Berger S.L., Workman J.L., Murre C. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Molecular Cell 1999, 4(1):63-73.
75. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V., et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004, 427(6972):355-360.
76. McKenzie A., Culpepper J., De Waal Malefyt R., Briere F., Punnonen J., Aversa G., et al. Interleukin 13, a T-cell-derived cytokine that regulates human monocyte and B-cell function. Proceedings of the National Academy of Sciences 1993, 90(8):3735-3739.
77. McWhirter J.R., Neuteboom S.T.C., Wancewicz E.V., Monia B.P., Downing J.R., Murre C. Proceedings of the National Academy of Sciences 1999, 96(20):11464-11469.
78. Mendoza M.C., Er E.E., Blenis J. The Ras-ERK and PI3K-mTOR pathways: Cross-talk and compensation. Trends in Biochemical Sciences 2011, 36(6):320-328.
79. Mitsias D., Tzioufas A., Veiopoulou C., Zintzaras E., Tassios I., Kogopoulou O., et al. The Th1/Th2 cytokine balance changes with the progress of the immunopathological lesion of Sjogren's syndrome. Clinical & Experimental Immunology 2002, 128(3):562-568.
80. Miyazaki M., Rivera R.R., Miyazaki K., Lin Y.C., Agata Y., Murre C. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nature Immunology 2011, 12(10):992-1001.
81. Monica K., LeBrun D.P., Dedera D.A., Brown R., Cleary M.L. Transformation properties of the E2a-Pbx1 chimeric oncoprotein: Fusion with E2a is essential, but the Pbx1 homeodomain is dispensable. Molecular and Cellular Biology 1994, 14(12):8304-8314.
82. Murre C., Baltimore D. The helix-loop-helix motif: Structure and function. Cold Spring Harbor Monograph Series 1993, 22:861.
83. Murre C., McCaw P.S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD and myc proteins. Cell 1989, 56(5):777-783.
84. Nossal G. Cellular mechanisms of immunologic tolerance. Annual Review of Immunology 1983, 1(1):33-62.
85. Nutt S.L., Heavey B., Rolink A.G., Busslinger M. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 1999, 401(6753):556-562.
86. Okada T., Maeda A., Iwamatsu A., Gotoh K., Kurosaki T. BCAP: The tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 2000, 13(6):817-827.
87. Okkenhaug K., Vanhaesebroeck B. PI3K in lymphocyte development, differentiation and activation. Nature Reviews Immunology 2003, 3(4):317-330.
88. Osborne C.S., Chakalova L., Mitchell J.A., Horton A., Wood A.L., Bolland D.J., et al. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biology 2007, 5(8):e192.
89. Pan L., Sato S., Frederick J.P., Sun X.-H., Zhuang Y. Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Molecular and Cellular Biology 1999, 19(9):5969-5980.
90. Park S.T., Nolan G.P., Sun X.-H. Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. The Journal of Experimental Medicine 1999, 189(3):501-508.
91. Plotkin J., Prockop S.E., Lepique A., Petrie H.T. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. The Journal of Immunology 2003, 171(9):4521-4527.
92. Polakis P. Wnt signaling and cancer. Genes and Development 2000, 14(15):1837-1851.
93. Quong M.W., Harris D.P., Swain S.L., Murre C. E2A activity is induced during B-cell activation to promote immunoglobulin class switch recombination. The EMBO Journal 1999, 18(22):6307-6318.
94. Reya T., O'Riordan M., Okamura R., Devaney E., Willert K., Nusse R., et al. Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 2000, 13(1):15-24.
95. Richter J., Schlesner M., Hoffmann S., Kreuz M., Leich E., Burkhardt B., et al. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nature Genetics 2012, 44(12):1316-1320.
96. Rivera R.R., Johns C.P., Quan J., Johnson R.S., Murre C. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 2000, 12(1):17-26.
97. Robey E., Fowlkes B. Selective events in T cell development. Annual Review of Immunology 1994, 12(1):675-705.
98. Romanow W.J., Langerak A.W., Goebel P., Wolvers-Tettero I.L., Van Dongen J.J., Feeney A.J., et al. E2A and EBF act in synergy with the V (D) J recombinase to generate a diverse immunoglobulin repertoire in nonlymphoid cells. Molecular Cell 2000, 5(2):343-353.
99. Sakamoto S., Wakae K., Anzai Y., Murai K., Tamaki N., Miyazaki M., et al. E2A and CBP/p300 act in synergy to promote chromatin accessibility of the immunoglobulin κ locus. The Journal of Immunology 2012, 188(11):5547-5560.
100. Sathish J.G., Johnson K.G., Leroy F.G., Fuller K.J., Hallett M.B., Brennan P., et al. Requirement for CD28 costimulation is lower in SHP 1 deficient T cells. European Journal of Immunology 2001, 31(12):3649-3658.
101. Sawada S., Littman D. A heterodimer of HEB and an E12-related protein interacts with the CD4 enhancer and regulates its activity in T-cell lines. Molecular and Cellular Biology 1993, 13(9):5620-5628.
102. Sayegh C., Jhunjhunwala S., Riblet R., Murre C. Visualization of looping involving the immunoglobulin heavy-chain locus in developing B cells. Genes & Development 2005, 19(3):322-327.
103. Sayegh C.E., Quong M.W., Agata Y., Murre C. E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nature Immunology 2003, 4(6):586-593.
104. Schlimgen R.J., Reddy K.L., Singh H., Krangel M.S. Initiation of allelic exclusion by stochastic interaction of Tcrb alleles with repressive nuclear compartments. Nature Immunology 2008, 9(7):802-809.
105. Schlissel M., Voronova A., Baltimore D. Helix-loop-helix transcription factor E47 activates germ-line immunoglobulin heavy-chain gene transcription and rearrangement in a pre-T-cell line. Genes & Development 1991, 5(8):1367-1376.
106. Schmitz R., Young R.M., Ceribelli M., Jhavar S., Xiao W., Zhang M., et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 2012, 490(7418):116-120.
107. Slattery C., Mcmorrow T., Ryan M.P. Overexpression of E2A proteins induces epithelial-mesenchymal transition in human renal proximal tubular epithelial cells suggesting a potential role in renal fibrosis. FEBS Letters 2006, 580(17):4021-4030.
108. Steininger A., Möbs M., Ullmann R., Köchert K., Kreher S., Lamprecht B., et al. Genomic loss of the putative tumor suppressor gene E2A in human lymphoma. The Journal of Experimental Medicine 2011, 208(8):1585-1593.
109. Stocker H., Andjelkovic M., Oldham S., Laffargue M., Wymann M.P., Hemmings B.A., et al. Living with lethal PIP3 levels: Viability of flies lacking PTEN restored by a PH domain mutation in Akt/PKB. Science 2002, 295(5562):2088-2091.
110. Sun X.-H., Baltimore D. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 1991, 64(2):459-470.
111. Sun X.-H., Copeland N.G., Jenkins N.A., Baltimore D. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Molecular and Cellular Biology 1991, 11(11):5603-5611.
112. Szodoray P., Alex P., Brun J., Centola M., Jonsson R. Circulating cytokines in primary Sjögren's syndrome determined by a multiplex cytokine array system. Scandinavian Journal of Immunology 2004, 59(6):592-599.
113. Tarpley T.M., Anderson L.G., White C.L. Minor salivary gland involvement in Sjögren's syndrome. Oral Surgery, Oral Medicine, Oral Pathology 1974, 37(1):64-74.
114. Thal M.A., Carvalho T.L., He T., Kim H.-G., Gao H., Hagman J., et al. Ebf1-mediated down-regulation of Id2 and Id3 is essential for specification of the B cell lineage. Proceedings of the National Academy of Sciences 2009, 106(2):552-557.
115. Treiber T., Mandel E.M., Pott S., Györy I., Firner S., Liu E.T., et al. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription-independent poising of chromatin. Immunity 2010, 32(5):714-725.
116. Tuveson D.A., Carter R.H., Soltoff S.P., Fearon D.T. CD19 of B cells as a surrogate kinase insert region to bind phosphatidylinositol 3-kinase. Science 1993, 260(5110):986-989.
117. Ueda-Hayakawa I., Mahlios J., Zhuang Y. Id3 restricts the developmental potential of γδ lineage during thymopoiesis. The Journal of Immunology 2009, 182(9):5306-5316.
118. Urbánek P., Wang Z.-Q., Fetka I., Wagner E.F., Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5BSAP. Cell 1994, 79(5):901-912.
119. Van Den Berg D.J., Sharma A.K., Bruno E., Hoffman R. Role of members of the Wnt gene family in human hematopoiesis. Blood 1998, 92(9):3189-3202.
120. Vanhaesebroeck B., Alessi D. The PI3K-PDK1 connection: More than just a road to PKB. Biochemical Journal 2000, 346:561-576.
121. Verykokakis M., Boos M.D., Bendelac A., Adams E.J., Pereira P., Kee B.L. Inhibitor of DNA binding 3 limits development of murine Slam-associated adaptor protein-dependent "innate" γδ T cells. PLoS ONE 2010, 5(2):e9303.
122. Verykokakis M., Krishnamoorthy V., Iavarone A., Lasorella A., Sigvardsson M., Kee B.L. Essential functions for ID proteins at multiple checkpoints in invariant NKT cell development. The Journal of Immunology 2013, 191(12):5973-5983. 10.4049/jimmunol.1301521.
123. Von Boehmer H. Positive selection of lymphocytes. Cell 1994, 76(2):219-228.
124. Wang D., Claus C.L., Vaccarelli G., Braunstein M., Schmitt T.M., Zúñiga-Pflücker J.C., et al. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. The Journal of Immunology 2006, 177(1):109-119.
125. Yan W., Young A.Z., Soares V.C., Kelley R., Benezra R., Zhuang Y. Molecular and Cellular Biology 1997, 17(12):7317-7327.
126. Yang C.Y., Best J.A., Knell J., Yang E., Sheridan A.D., Jesionek A.K., et al. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Nature Immunology 2011, 12(12):1221-1229.
127. Yankee T., Clark E. Signaling through the B cell antigen receptor in developing B cells. Reviews in Immunogenetics 1999, 2(2):185-203.
128. Yu W., Misulovin Z., Suh H., Hardy R.R., Jankovic M., Yannoutsos N., et al. Coordinate regulation of RAG1 and RAG2 by cell type-specific DNA elements 5' of RAG2. Science 1999, 285(5430):1080-1084.
129. Zhang B., Dai M., Li Q.-J., Zhuang Y. Tracking proliferative history in lymphocyte development with Cre-mediated sister chromatid recombination. PLoS Genetics 2013, 9(10):e1003887.
130. Zhang B., Lin Y.-Y., Dai M., Zhuang Y. Id3 and Id2 act as a dual safety mechanism in regulating the development and population size of innate-like γδ T cells. The Journal of Immunology 2014, 192:1055-1063. 1302694.
131. Zhao F., Vilardi A., Neely R.J., Choi J.K. Promotion of cell cycle progression by basic helix-loop-helix E2A. Molecular and Cellular Biology 2001, 21(18):6346-6357.
132. Zhuang Y., Cheng P., Weintraub H. B-lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2-2, and HEB. Molecular and Cellular Biology 1996, 16(6):2898-2905.
133. Zhuang Y., Soriano P., Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell 1994, 79(5):875-884.