Morpholino antisense oligonucleotide-mediated gene knockdown during thymocyte development reveals role for Runx3 transcription factor in CD4 silencing during development of CD4-/CD8+ thymocytes

Journal of Immunology

Volumn 171, Issue 7, 2003, Pages 3594-3604

  Ehlers, Marc ^a,b   Laule Kilian, Kirsten ^a   Petter, Michaela ^a   Aldrian, Christine J ^a   Grueter, Baerbel ^b   Würch, Andreas ^a   Yoshida, Naomi ^c   Watanabe, Toshio ^c   Satake, Masanobu ^c   Steimle, Viktor ^a,d  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^c TOHOKU UNIVERSITY   (Japan)

^d UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CD4 ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE FUNCTION; GENE SILENCING; GENETIC TRANSFECTION; HELPER CELL; LYMPHOCYTE DIFFERENTIATION; MOUSE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REPORTER GENE; RNA TRANSCRIPTION; SILENCER GENE; T LYMPHOCYTE; THYMOCYTE;

EID: 0141920621     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.7.3594     Document Type: Article

References (49)

1. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative T cell selection. Annu. Rev. Immunol. 21:139.
2. Germain, R. N. 2002. T-cell development and the CD4-CD8 lineage decision. Nat. Rev. Immunol. 2:309.
3. Bendelac, A., P. Matzinger, R. A. Seder, W. E. Paul, and R. H. Schwartz. 1992. Activation events during thymic selection. J. Exp. Med. 175:731.
4. + thymocyte differentiation. Immunity 5:461.
5. Barthlott, T., H. Kohler, and K. Eichmann. 1997. Asynchronous coreceptor downregulation after positive thymic selection: prolonged maintance of the double positive state in CD8 linage differentiation due to sustained biosynthesis of the CD4 coreceptor. J. Exp. Med. 185:357.
6. Hedrick, S. M. 2002. T cell development: bottoms-up. Immunity 16:619.
7. Lutterbach, B., and S. W. Hiebert. 2000. Role of the transcription factor AML-1 in acute leukemia and hematopoietic differentiation. Gene 245:223.
8. Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R. T. Bronson, Y. H. Gao, M. Inada, et al. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755.
9. Levanon, D., V. Negreanu, Y. Bernstein, I. Bar-Am, L. Avivi, and Y. Groner. 1994. AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localisation. Genomics 23:425.
10. Levanon, D., Y. Bernstein, V. Negreanu, M. C. Ghozi, I. Bar-Am, R. Aloya, D. Goldenberg, J. Lotem, and Y. Groner. 1996. A large variety of alternatively spliced and differentially expressed mRNAs are encoded by the human acute myeloid leukemia gene AML1. DNA Cell Biol. 15:175.
11. Le, X.-F., Y. Groner, S. M. Kornblau, Y. Gu, W. N. Hittelman, D. Levanon, K. Mehta, R. B. Arlinghaus, and K.-S. Chang. 1999. Regulation of AML2/ CBFA3 in hematopoietic cells through the retinoic acid receptor α-dependent signaling pathway. J. Biol. Chem. 274:21651.
12. Shi, M. J., and J. Stavnezer. 1998. CBFα3 (AML2) is induced by TGF-β1 to bind and activate the mouse germline Ig α promoter. J. Immunol. 161:6751.
13. Li, Q. L., K. Ito, C. Sakakura, H. Fukamachi, K. Inoue, X. Z. Chi, K. Y. Lee, S. Nomura, C. W. Lee, S. B. Han, et al. 2002. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109:113.
14. Levanon, D., D. Bettoun, C. Harris-Cerruti, E. Woolf, V. Negreanu, R. Eilam, Y. Bernstein, D. Goldenberg, C. Xiao, M. Fliegauf, et al. 2002. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 21:3454.
15. Ito, Y. 1999. Molecular basis of tissue-specific gene expression mediated by the runt domain transcription factor PEBP2/CBF. Genes Cells 4:685.
16. Hayashi, K., N. Abe, T. Watanabe, M. Obinata, M. Ito, T. Sato, S. Habu, and M. Satake. 2001. Overexpression of AML1 transcription factor drives thymocytes into the CD8 single-positive lineage. J. Immunol. 167:4957.
17. Vaillant, F., K. Blyth, L. Andrew, J. C. Neil, and E. R. Cameron. 2002. Enforced expression of Runx2 perturbs T cell development at a stage coincident with β-selection. J. Immunol. 169:2866.
18. Hayashi, K., W. Natsume, T. Watanabe, N. Abe, N. Iwai, H. Okada, Y. Ito, M. Asano, Y. Iwakura, S. Habu, et al. 2000. Diminution of the AML1 transcription factor function causes differential effects on the fates of CD4 and CD8 single-positive T cells. J. Immunol. 165:6816.
19. 7) mediated binding of lymphoma cells to high endothelial venules of mucosa-associated lymph nodes. Eur. J. Cell Biol. 61:290.
20. Landry, D. B., J. D. Engel, and R. Sen. 1993. Functional GATA-3 binding sites within murine CD8α upstream regulatory sequences. J. Exp. Med. 178:941.
21. Bangsow, C., N. Rubins, G. Glusman, Y. Bernstein, V. Negreanu, D. Goldenberg, J. Lotem, E. Ben-Asher, D. Lancet, D. Levanon, et al. 2001. The RUNX3 gene: sequence, structure and regulated expression. Gene 279:221.
22. Hake, S. B., K. Masternak, C. Kammerbauer, C. Janzen, W. Reith, and V. Steimle. 2000. CIITA leucine-rich repeats control nuclear localization, in vivo recruitment to the major histocompatibility complex (MHC) class II enhanceosome, and MHC class II gene transactivation. Mol. Cell. Biol. 20:7716.
23. Kanto, S., N. Chiba, Y. Tanaka, S. Fujita, M. Endo, N. Kamada, K. Yoshikawa, A. Fukuzaki, S. Orikasa, T. Watanabe, et al. 2000. The PEBP2β/CBFβ-SMMHC chimeric protein is localized both in the cell membrane and nuclear subfractions of leukemic cells carrying chromosomal inversion 16. Leukemia 14:1253.
24. Tanaka, Y., T. Watanabe, N. Chiba, M. Niki, Y. Kuroiwa, T. Nishihira, S. Satomi, Y. Ito, and M. Satake. 1997. The protooncogene product, PEBP2β/CBFβ, is mainly located in the cytoplasm and has an affinity with cytoskeletal structures. Oncogene 15:677.
25. Sawada, S., J. D. Scarborough, N. Killeen, and D. R. Littman. 1994. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell 77:917.
26. Chung, J. H., M. Whiteley, and G. Felsenfeld. 1993. A 5′ element of the chicken β-globin domain serves as an insulator in human erythroid cells and protects against position effects in drosophila. Cell 74:505.
27. + T cells. Immunity 13:59.
28. Heasman, J. 2002. Morpholino oligos: making sense of antisense? Dev. Biol. 243:209.
29. Zhang, Y. W., S. C. Bae, G. Huang, Y. X. Fu, J. Lu, M. Y. Ahn, Y. Kanno, T. Kanno, and Y. Ito. 1997. A novel transcript encoding an N-terminally truncated AML1/PEBP2 αB protein interferes with transactivation and blocks granulocytic differentiation of 32Dc13 myeloid cells. Mol. Cell. Biol. 17:4133.
30. Xiao, Z. S., R. Thomas, T. K. Hinson, and L. D. Quarles. 1998. Genomic structure and isoform expression of the mouse, rat and human Cbfa1/Osf2 transcription factor. Gene 214:187.
31. Levanon, D., G. Glusman, T. Bangsow, E. Ben-Asher, D. A. Male, N. Avidan, C. Bangsow, M. Hattori, T. D. Taylor, S. Taudien, et al. 2001. Architecture and anatomy of the genomic locus encoding the human leukemia-associated transcription factor RUNX1/AML1. Gene 262:23.
32. Jung, T. M., W. M. Gallatin, I. L. Weissman, and M. O. Dailey. 1988. Downregulation of homing receptors after T cell activation. J. Immunol. 141:4110.
33. + thymocytes in normal mouse thymus. Int. Immunol. 13:313.
34. Siu, G., A. L. Wurster, D. D. Duncan, T. M. Soliman, and S. M. Hedrick. 1994. A transcriptional silencer controls the developmental expression of the CD4 gene. EMBO J. 13:3570.
35. Leung, R. K., K. Thomson, A. Gallimore, E. Jones, M. Van den Broek, S. Sierro, A. R. Alsheikhly, A. McMichael, and A. Rahemtulla. 2001. Deletion of the CD4 silencer element supports a stochastic mechanism of thymocyte lineage commitment. Nat. Immunol. 2:1167.
36. Zou, Y.-R., M.-J. Sunshine, I. Taniuchi, F. Hatam, N. Killeen, and D. R. Littman. 2001. Epigenetic silencing of CD4 in T cells committed to the cytotoxic lineage. Nat. Genet. 29:357.
37. Summerton, J., and D. Weller. 1997. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7:187.
38. Shortman, K., M. Egerton, G. J. Spangrude, and R. Scollay. 1990. The generation and fate of thymocytes. Semin. Immunol. 2:3.
39. McManus, M. T., B. B. Haines, C. P. Dillon, C. E. Whitehurst, L. van Parijs, J. Chen, and P. A. Sharp. 2002. Small interfering RNA-mediated gene silencing in T lymphocytes. J. Immunol. 169:5754.
40. Taniuchi, I., M. J. Sunshine, R. Festenstein, and D. R. Littman. 2002. Evidence for distinct CD4 silencer functions at different stages of thymocyte differentiation. Mol. Cell. 10:1083.
41. Taniuchi, I., M. Osato, T. Egawa, M. J. Sunshine, S. C. Bae, T. Komori, Y. Ito, and D. R. Littman. 2002. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111:621.
42. Huang, G., K. Shigesada, K. Ito, H. J. Wee, T. Yokomizo, and Y. Ito. 2001. Dimerization with PEBP2β protects RUNX1/AML1 from ubiquitin-proteasome-mediated degradation. EMBO J. 20:723.
43. Ellmeier, W., S. Sawada, and D. R. Littman. 1999. The regulation of CD4 and CD8 coreceptor gene expression during T cell development. Annu. Rev. Immunol. 17:523.
44. Duncan, D. D., M. Adlam, and G. Siu. 1996. Asymmetric redundancy in CD4 silencer function. Immunity 4:301.
45. Kim, H. K., and G. Siu. 1998. The Notch pathway intermediate HES-1 silences CD4 gene expression. Mol. Cell. Biol. 18:7166.
46. Kim, W. W. S., and G. Siu. 1999. Subclass-specific nuclear localization of a novel CD4 silencer binding factor. J. Exp. Med. 190:281.
47. Allen, R. D., III, K. Kim, S. D. Sarafova, and G. Siu. 2001. Negative regulation of CD4 gene expression by a hes-1-c-myb complex. Mol. Cell. Biol. 21:3071.
48. Javed, A., B. Guo, S. Hiebert, J. Y. Choi, J. Green, S. C. Zhao, M. A. Osborne, S. Stifani, J. L. Stein, J. B. Lian, et al. 2000. Groucho/TLE/R-esp proteins associate with the nuclear matrix and repress RUNX (CBF(α )/AML/PEBP2(α) dependent activation of tissue-specific gene transcription. J. Cell Sci. 113:2221.
49. Schmitt, T. M., and J. C. Zuniga-Pflucker. 2002. Induction of T cell development from hematopoietic progenitor cells by δ-like-1 in vitro. Immunity 17:749.