Repression of Ccr9 transcription in mouse T lymphocyte progenitors by the Notch signaling pathway

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3191-3200

  Krishnamoorthy, Veena ^a   Carr, Tiffany ^a   De Pooter, Renee F ^a   Akinola, Emanuelle Olumide ^a   Gounari, Fotini ^a,b   Kee, Barbara L ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR9; E1A ASSOCIATED P300 PROTEIN; HISTONE H3; NOTCH1 RECEPTOR; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR HEB; UNCLASSIFIED DRUG; CC CHEMOKINE RECEPTOR 9; CHEMOKINE RECEPTOR CCR; HISTONE ACETYLTRANSFERASE PCAF; MEMBRANE ANTIGEN; MESSENGER RNA; NOTCH RECEPTOR; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CCR9 GENE; CELL MATURATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE REPRESSION; HISTONE ACETYLATION; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIMARY CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T-CELL LYMPHOMA CELL LINE; THYMOCYTE; ANIMAL; BINDING SITE; CELL LINE; CELL MOTION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOID PROGENITOR CELL; LYMPHOMA; METABOLISM; T LYMPHOCYTE SUBPOPULATION; THYMUS; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, SURFACE; BINDING SITES; CELL LINE; CELL MOVEMENT; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPHENOTYPING; LYMPHOID PROGENITOR CELLS; LYMPHOMA; MICE; MICE, TRANSGENIC; P300-CBP TRANSCRIPTION FACTORS; PROTEIN BINDING; RECEPTORS, CCR; RECEPTORS, NOTCH; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; THYMOCYTES; THYMUS GLAND; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84925881265     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402443     Document Type: Article

References (66)

1. Love, P. E., and A. Bhandoola. 2011. Signal integration and crosstalk during thymocyte migration and emigration. Nat. Rev. Immunol. 11: 469-477.
2. Allman, D., A. Sambandam, S. Kim, J. P. Miller, A. Pagan, D. Well, A. Meraz, and A. Bhandoola. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4: 168-174.
3. Petrie, H. T., and J. C. Zúñiga-Pflücker. 2007. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu. Rev. Immunol. 25: 649-679.
4. Uehara, S., A. Grinberg, J. M. Farber, and P. E. Love. 2002. A role for CCR9 in T lymphocyte development and migration. J. Immunol. 168: 2811-2819.
5. Schwarz, B. A., A. Sambandam, I. Maillard, B. C. Harman, P. E. Love, and A. Bhandoola. 2007. Selective thymus settling regulated by cytokine and chemokine receptors. J. Immunol. 178: 2008-2017.
6. Zlotoff, D. A., A. Sambandam, T. D. Logan, J. J. Bell, B. A. Schwarz, and A. Bhandoola. 2010. CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood 115: 1897-1905.
7. Krueger, A., S. Willenzon, M. Lyszkiewicz, E. Kremmer, and R. Förster. 2010. CC chemokine receptor 7 and 9 double-deficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood 115: 1906-1912.
8. Liu, C., F. Saito, Z. Liu, Y. Lei, S. Uehara, P. Love, M. Lipp, S. Kondo, N. Manley, and Y. Takahama. 2006. Coordination between CCR7- and CCR9- mediated chemokine signals in prevascular fetal thymus colonization. Blood 108: 2531-2539.
9. Robertson, P., T. K. Means, A. D. Luster, and D. T. Scadden. 2006. CXCR4 and CCR5 mediate homing of primitive bone marrow-derived hematopoietic cells to the postnatal thymus. Exp. Hematol. 34: 308-319.
10. Calderón, L., and T. Boehm. 2011. Three chemokine receptors cooperatively regulate homing of hematopoietic progenitors to the embryonic mouse thymus. Proc. Natl. Acad. Sci. USA 108: 7517-7522.
11. Misslitz, A., O. Pabst, G. Hintzen, L. Ohl, E. Kremmer, H. T. Petrie, and R. Förster. 2004. Thymic T cell development and progenitor localization depend on CCR7. J. Exp. Med. 200: 481-491.
12. Benz, C., K. Heinzel, and C. C. Bleul. 2004. Homing of immature thymocytes to the subcapsular microenvironment within the thymus is not an absolute requirement for T cell development. Eur. J. Immunol. 34: 3652-3663.
13. Uehara, S., S. M. Hayes, L. Li, D. El-Khoury, M. Canelles, B. J. Fowlkes, and P. E. Love. 2006. Premature expression of chemokine receptor CCR9 impairs T cell development. J. Immunol. 176: 75-84.
14. Radtke, F., A. Wilson, G. Stark, M. Bauer, J. van Meerwijk, H. R. MacDonald, and M. Aguet. 1999. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10: 547-558.
15. Koch, U., E. Fiorini, R. Benedito, V. Besseyrias, K. Schuster-Gossler, M. Pierres, N. R. Manley, A. Duarte, H. R. Macdonald, and F. Radtke. 2008. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205: 2515-2523.
16. Pear, W. S., and F. Radtke. 2003. Notch signaling in lymphopoiesis. Semin. Immunol. 15: 69-79.
17. Nam, Y., A. P. Weng, J. C. Aster, and S. C. Blacklow. 2003. Structural requirements for assembly of the CSL.intracellular Notch1.Mastermind-like 1 transcriptional activation complex. J. Biol. Chem. 278: 21232-21239.
18. Koch, U., and F. Radtke. 2011. Mechanisms of T cell development and transformation. Annu. Rev. Cell Dev. Biol. 27: 539-562.
19. Gounari, F., I. Aifantis, C. Martin, H. J. Fehling, S. Hoeflinger, P. Leder, H. von Boehmer, and B. Reizis. 2002. Tracing lymphopoiesis with the aid of a pTalpha-controlled reporter gene. Nat. Immunol. 3: 489-496.
20. Tomita, K., M. Hattori, E. Nakamura, S. Nakanishi, N. Minato, and R. Kageyama. 1999. The bHLH gene Hes1 is essential for expansion of early T cell precursors. Genes Dev. 13: 1203-1210.
21. De Obaldia, M. E., J. J. Bell, X. Wang, C. Harly, Y. Yashiro-Ohtani, J. H. DeLong, D. A. Zlotoff, D. A. Sultana, W. S. Pear, and A. Bhandoola. 2013. T cell development requires constraint of the myeloid regulator C/EBP-α by the Notch target and transcriptional repressor Hes1. Nat. Immunol. 14: 1277-1284.
22. Weber, B. N., A. W. Chi, A. Chavez, Y. Yashiro-Ohtani, Q. Yang, O. Shestova, and A. Bhandoola. 2011. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476: 63-68.
23. Germar, K., M. Dose, T. Konstantinou, J. Zhang, H. Wang, C. Lobry, K. L. Arnett, S. C. Blacklow, I. Aifantis, J. C. Aster, and F. Gounari. 2011. T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc. Natl. Acad. Sci. USA 108: 20060-20065.
24. Weng, A. P., A. A. Ferrando, W. Lee, J. P. Morris, IV, L. B. Silverman, C. Sanchez-Irizarry, S. C. Blacklow, A. T. Look, and J. C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
25. O'Neil, J., J. Calvo, K. McKenna, V. Krishnamoorthy, J. C. Aster, C. H. Bassing, F. W. Alt, M. Kelliher, and A. T. Look. 2006. Activating Notch1 mutations in mouse models of T-ALL. Blood 107: 781-785.
26. Reschly, E. J., C. Spaulding, T. Vilimas, W. V. Graham, R. L. Brumbaugh, I. Aifantis, W. S. Pear, and B. L. Kee. 2006. Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and -independent mechanisms. Blood 107: 4115-4121.
27. Gómez-del Arco, P., M. Kashiwagi, A. F. Jackson, T. Naito, J. Zhang, F. Liu, B. Kee, M. Vooijs, F. Radtke, J. M. Redondo, and K. Georgopoulos. 2010. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity 33: 685-698.
28. Lin, Y. W., R. A. Nichols, J. J. Letterio, and P. D. Aplan. 2006. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107: 2540-2543.
29. Thompson, B. J., S. Buonamici, M. L. Sulis, T. Palomero, T. Vilimas, G. Basso, A. Ferrando, and I. Aifantis. 2007. The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J. Exp. Med. 204: 1825-1835.
30. O'Neil, J., J. Grim, P. Strack, S. Rao, D. Tibbitts, C. Winter, J. Hardwick, M. Welcker, J. P. Meijerink, R. Pieters, et al. 2007. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 204: 1813-1824.
31. Crusio, K. M., B. King, L. B. Reavie, and I. Aifantis. 2010. The ubiquitous nature of cancer: the role of the SCF(Fbw7) complex in development and transformation. Oncogene 29: 4865-4873.
32. Talora, C., A. F. Campese, D. Bellavia, M. Pascucci, S. Checquolo, M. Groppioni, L. Frati, H. von Boehmer, A. Gulino, and I. Screpanti. 2003. Pre- TCR-triggered ERK signalling-dependent downregulation of E2A activity in Notch3-induced T-cell lymphoma. EMBO Rep. 4: 1067-1072.
33. Pui, J. C., D. Allman, L. Xu, S. DeRocco, F. G. Karnell, S. Bakkour, J. Y. Lee, T. Kadesch, R. R. Hardy, J. C. Aster, and W. S. Pear. 1999. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11: 299-308.
34. Nie, L., M. Xu, A. Vladimirova, and X. H. Sun. 2003. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22: 5780-5792.
35. Kee, B. L. 2009. E and ID proteins branch out. Nat. Rev. Immunol. 9: 175-184.
36. Engel, I., and C. Murre. 2001. The function of E- and Id proteins in lymphocyte development. Nat. Rev. Immunol. 1: 193-199.
37. Miyazaki, K., M. Miyazaki, and C. Murre. 2014. The establishment of B versus T cell identity. Trends Immunol. 35: 205-210.
38. Dias, S., R. Månsson, S. Gurbuxani, M. Sigvardsson, and B. L. Kee. 2008. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 29: 217-227.
39. Ikawa, T., H. Kawamoto, A. W. Goldrath, and C. Murre. 2006. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J. Exp. Med. 203: 1329-1342.
40. Yang, Q., L. Kardava, A. St Leger, K. Martincic, B. Varnum-Finney, I. D. Bernstein, C. Milcarek, and L. Borghesi. 2008. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J. Immunol. 181: 5885-5894.
41. Semerad, C. L., E. M. Mercer, M. A. Inlay, I. L. Weissman, and C. Murre. 2009. E2A proteins maintain the hematopoietic stem cell pool and promote the maturation of myelolymphoid and myeloerythroid progenitors. Proc. Natl. Acad. Sci. USA 106: 1930-1935.
42. Wang, D., C. L. Claus, G. Vaccarelli, M. Braunstein, T. M. Schmitt, J. C. Zúñiga-Pflücker, E. V. Rothenberg, and M. K. Anderson. 2006. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J. Immunol. 177: 109-119.
43. Jones, M. E., and Y. Zhuang. 2007. Acquisition of a functional T cell receptor during T lymphocyte development is enforced by HEB and E2A transcription factors. Immunity 27: 860-870.
44. Bain, G., I. Engel, E. C. Robanus Maandag, H. P. te Riele, J. R. Voland, L. L. Sharp, J. Chun, B. Huey, D. Pinkel, and C. Murre. 1997. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17: 4782-4791.
45. Wojciechowski, J., A. Lai, M. Kondo, and Y. Zhuang. 2007. E2A and HEB are required to block thymocyte proliferation prior to pre-TCR expression. J. Immunol. 178: 5717-5726.
46. Spaulding, C., E. J. Reschly, D. E. Zagort, Y. Yashiro-Ohtani, L. J. Beverly, A. Capobianco, W. S. Pear, and B. L. Kee. 2007. Notch1 co-opts lymphoid enhancer factor 1 for survival of murine T-cell lymphomas. Blood 110: 2650-2658.
47. Maillard, I., L. Tu, A. Sambandam, Y. Yashiro-Ohtani, J. Millholland, K. Keeshan, O. Shestova, L. Xu, A. Bhandoola, and W. S. Pear. 2006. The requirement for Notch signaling at the beta-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J. Exp. Med. 203: 2239-2245.
48. Zhang, J., A. F. Jackson, T. Naito, M. Dose, J. Seavitt, F. Liu, E. J. Heller, M. Kashiwagi, T. Yoshida, F. Gounari, et al. 2012. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13: 86-94.
49. Schmitt, T. M., and J. C. Zúñiga-Pflücker. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17: 749-756.
50. Jeffries, S., D. J. Robbins, and A. J. Capobianco. 2002. Characterization of a high-molecular-weight Notch complex in the nucleus of Notch(ic)-transformed RKE cells and in a human T-cell leukemia cell line. Mol. Cell. Biol. 22: 3927-3941.
51. Wu, L., T. Sun, K. Kobayashi, P. Gao, and J. D. Griffin. 2002. Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol. Cell. Biol. 22: 7688-7700.
52. Maillard, I., A. P. Weng, A. C. Carpenter, C. G. Rodriguez, H. Sai, L. Xu, D. Allman, J. C. Aster, and W. S. Pear. 2004. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 104: 1696-1702.
53. Kim, H. K., and G. Siu. 1998. The notch pathway intermediate HES-1 silences CD4 gene expression. Mol. Cell. Biol. 18: 7166-7175.
54. Morillon, A., N. Karabetsou, A. Nair, and J. Mellor. 2005. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol. Cell 18: 723-734.
55. Bannister, A. J., R. Schneider, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2005. Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280: 17732-17736.
56. Rada-Iglesias, A., R. Bajpai, T. Swigut, S. A. Brugmann, R. A. Flynn, and J. Wysocka. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
57. Visel, A., M. J. Blow, Z. Li, T. Zhang, J. A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, F. Chen, et al. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858.
58. Uehara, S., K. Song, J. M. Farber, and P. E. Love. 2002. Characterization of CCR9 expression and CCL25/thymus-expressed chemokine responsiveness during T cell development: CD3(high)CD69+ thymocytes and gammadeltaTCR+ thymocytes preferentially respond to CCL25. J. Immunol. 168: 134-142.
59. Svensson, M., J. Marsal, H. Uronen-Hansson, M. Cheng, W. Jenkinson, C. Cilio, S. E. Jacobsen, E. Sitnicka, G. Anderson, and W. W. Agace. 2008. Involvement of CCR9 at multiple stages of adult T lymphopoiesis. J. Leukoc. Biol. 83: 156-164.
60. Wang, H., C. Zang, L. Taing, K. L. Arnett, Y. J. Wong, W. S. Pear, S. C. Blacklow, X. S. Liu, and J. C. Aster. 2014. NOTCH1-RBPJ complexes drive target gene expression through dynamic interactions with superenhancers. Proc. Natl. Acad. Sci. USA 111: 705-710.
61. Wang, H., J. Zou, B. Zhao, E. Johannsen, T. Ashworth, H. Wong, W. S. Pear, J. Schug, S. C. Blacklow, K. L. Arnett, et al. 2011. Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc. Natl. Acad. Sci. USA 108: 14908-14913.
62. Mirandola, L., M. Chiriva-Internati, D. Montagna, F. Locatelli, M. Zecca, M. Ranzani, A. Basile, M. Locati, E. Cobos, W. M. Kast, et al. 2012. Notch1 regulates chemotaxis and proliferation by controlling the CC-chemokine receptors 5 and 9 in T cell acute lymphoblastic leukaemia. J. Pathol. 226: 713-722.
63. Chiang, M. Y., O. Shestova, L. Xu, J. C. Aster, and W. S. Pear. 2013. Divergent effects of supraphysiologic Notch signals on leukemia stem cells and hematopoietic stem cells. Blood 121: 905-917.
64. Yashiro-Ohtani, Y., Y. He, T. Ohtani, M. E. Jones, O. Shestova, L. Xu, T. C. Fang, M. Y. Chiang, A. M. Intlekofer, S. C. Blacklow, et al. 2009. Pre-TCR signaling inactivates Notch1 transcription by antagonizing E2A. Genes Dev. 23: 1665-1676.
65. Bayly, R., L. Chuen, R. A. Currie, B. D. Hyndman, R. Casselman, G. A. Blobel, and D. P. LeBrun. 2004. E2A-PBX1 interacts directly with the KIX domain of CBP/p300 in the induction of proliferation in primary hematopoietic cells. J. Biol. Chem. 279: 55362-55371.
66. Hyndman, B. D., P. Thompson, R. Bayly, G. P. Côté, and D. P. LeBrun. 2012. E2A proteins enhance the histone acetyltransferase activity of the transcriptional co-activators CBP and p300. Biochim. Biophys. Acta 1819: 446-453.