Reduced DEAF1 function during type 1 diabetes inhibits translation in lymph node stromal cells by suppressing Eif4g3

Journal of Molecular Cell Biology

Volumn 5, Issue 2, 2013, Pages 99-110

  Yip, Linda ^a   Creusot, Remi J ^a   Pager, Cara T ^b   Sarnow, Peter ^b   Fathman, C Garrison ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

DEAF1; Eif4g3; peripheral tolerance; translational control; type 1 diabetes

Indexed keywords

CASPASE 3; DEFORMED EPIDERMAL AUTOREGULATORY FACTOR 1; INITIATION FACTOR 4G; INITIATION FACTOR 4G3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CHROMOSOME 7; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE GENE; INSULIN DEPENDENT DIABETES MELLITUS; LARGE RIBOSOMAL SUBUNIT; LYMPH NODE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RNA SPLICING; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; CASPASE 3; DIABETES MELLITUS, TYPE 1; EUKARYOTIC INITIATION FACTOR-4G; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNE TOLERANCE; LYMPH NODES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, KNOCKOUT; PANCREAS; PROTEIN BIOSYNTHESIS; STROMAL CELLS; TRANSCRIPTION FACTORS;

EUKARYOTA; MUS;

EID: 84875692817     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjs052     Document Type: Article

References (36)

1. Abbott, C.M., and Proud, C.G., (2004). Translation factors: In sickness and in health. Trends Biochem. Sci. 29, 25-31.
2. Anderson, M.S., Venanzi, E.S., Klein, L., et al., (2002). Projection of an immunological self shadow within the thymus by the aire protein. Science 298, 1395-1401.
3. Bagri, A., Marin, O., Plump, A.S., et al., (2002). Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33, 233-248.
4. Baker, C.C., and Fuller, M.T., (2007). Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog. Development 134, 2863-2869.
5. Caron, S., Charon, M., Cramer, E., et al., (2004). Selective modification of eukaryotic initiation factor 4F, (eIF4F) at the onset of cell differentiation: Recruitment of eIF4GII and long-lasting phosphorylation of eIF4E. Mol. Cell. Biol. 24, 4920-4928.
6. Castello, A., Alvarez, E., and Carrasco, L., (2006). Differential cleavage of eIF4GI and eIF4GII in mammalian cells. Effects on translation. J. Biol. Chem. 281, 33206-33216.
7. Clarkson, B.K., Gilbert, W.V., and Doudna, J.A., (2010). Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoS One 5, e9114.
8. Cohen, J.N., Guidi, C.J., Tewalt, E.F., et al., (2010). Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J. Exp. Med. 207, 681-688.
9. Coldwell, M.J., and Morley, S.J., (2006). Specific isoforms of translation initiation factor 4GI show differences in translational activity. Mol. Cell. Biol. 26, 8448-8460.
10. Ftcher, A.L., Lukacs-Kornek, V., Reynoso, E.D., et al., (2010). Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J. Exp. Med. 207, 689-697.
11. Fletcher, A.L., Malhotra, D., and Turley, S.J., (2011). Lymph node stroma broaden the peripheral tolerance paradigm. Trends Immunol. 32, 12-18.
12. Gabrilovac, J., Cupic, B., Zivkovic, E., et al., (2011). Expression, regulation and functional activities of aminopeptidase N, (EC 3.4.11.2; APN; CD13) on murine macrophage J774 cell line. Immunobiology 216, 132-144.
13. Gagnerault, M.C., Luan, J.J., Lotton, C., et al., (2002). Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J. Exp. Med. 196, 369-377.
14. Gardner, J.M., Devoss, J.J., Friedman, R.S., et al., (2008). Deletional tolerance mediated by extrathymic Aire-expressing cells. Science 321, 843-847.
15. Gingras, A.C., Raught, B., and Sonenberg, N., (1999). eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963.
16. Gradi, A., Imataka, H., Svitkin, Y.V., et al., (1998a). A novel functional human eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 18, 334-342.
17. Gradi, A., Svitkin, Y.V., Imataka, H., et al., (1998b). Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl Acad. Sci. USA 95, 11089-11094.
18. Hahm, K., Sum, E.Y., Fujiwara, Y., et al., (2004). Defective neural tube closure and anteroposterior patterning in mice lacking the LIM protein LMO4 or its interacting partner Deaf-1. Mol. Cell. Biol. 24, 2074-2082.
19. Hansen, A.S., Noren, O., Sjostrom, H., et al., (1993). A mouse aminopeptidase N is a marker for antigen-presenting cells and appears to be co-expressed with major histocompatibility complex class II molecules. Eur. J. Im munol. 23, 2358-2364.
20. Huggenvik, J.I., Michelson, R.J., Collard, M.W., et al., (1998). Characterization of a nuclear deformed epidermal autoregulatory factor-1, (DEAF-1)-related, (NUDR) transcriptional regulator protein. Mol. Endocrinol. 12, 1619-1639.
21. Katakai, T., Hara, T., Sugai, M., et al., (2004). Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J. Exp. Med. 200, 783-795.
22. Kimball, S.R., Jefferson, L.S., Fadden, P., et al., (1996). Insulin and diabetes cause reciprocal changes in the association of eIF-4E and PHAS-I in rat skeletal muscle. Am. J. Physiol. 270, C705-C709.
23. Larsen, S.L., Pedersen, L.O., Buus, S., et al., (1996). T cell responses affected by aminopeptidase N, (CD13)-mediated trimming of major histocompatibility complex class II-bound peptides. J. Exp. Med. 184, 183-189.
24. Lee, J.W., Epardaud, M., Sun, J., et al., (2007). Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat. Immunol. 8, 181-190.
25. Leenen, P.J., Melis, M., Kraal, G., et al., (1992). The monoclonal antibody ER-BMDM1 recognizes a macrophage and dendritic cell differentiation antigen with aminopeptidase activity. Eur. J. Immunol. 22, 1567-1572.
26. Liadis, N., Murakami, K., Eweida, M., et al., (2005). Caspase-3-dependent betacell apoptosis in the initiation of autoimmune diabetes mellitus. Mol. Cell. Biol. 25, 3620-3629.
27. Link, A., Vogt, T.K., Favre, S., et al., (2007). Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8, 1255-1265.
28. Lynch, S.A., (2005). Non-multifactorial neural tube defects. Am. J. Med. Genet. C Semin. Med. Genet. 135C, 69-76.
29. Marissen, W.E., Gradi, A., Sonenberg, N., et al., (2000). Cleavage of eukaryotic translation initiation factor 4GII correlates with translation inhibition during apoptosis. Cell. Death Differ. 7, 1234-1243.
30. Marissen, W.E., and Lloyd, R.E., (1998). Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18, 7565-7574.
31. Meric, F., and Hunt, K.K., (2002). Translation initiation in cancer: A novel target for therapy. Mol. Cancer Ther. 1, 971-979.
32. Michelson, R.J., Collard, M.W., Ziemba, A.J., et al., (1999). Nuclear DEAF-1-related, (NUDR) protein contains a novel DNA binding domain and represses transcription of the heterogeneous nuclear ribonucleoprotein A2/B1 promoter. J. Biol. Chem. 274, 30510-30519.
33. Nichols, L.A., Chen, Y., Colella, T.A., et al., (2007). Deletional self-Tolerance to a melanocyte/melanoma antigen derived from tyrosinase is mediated by a radio-resistant cell in peripheral and mesenteric lymph nodes. J. Immunol. 179, 993-1003.
34. Sun, F., Palmer, K., and Handel, M.A., (2010). Mutation of Eif4g3, encoding a eukaryotic translation initiation factor, causes male infertility and meiotic arrest of mouse spermatocytes. Development 137, 1699-1707.
35. Wehner, K.A., Schutz, S., and Sarnow, P., (2010). OGFOD1, a novel modulator of eukaryotic translation initiation factor 2alpha phosphorylation and the cellular response to stress. Mol. Cell. Biol. 30, 2006-2016.
36. Yip, L., Su, L., Sheng, D., et al., (2009). Deaf1 isoforms control the expression of genes encoding peripheral tissue antigens in the pancr eatic lymph nodes during type 1 diabetes. Nat. Immunol. 10, 1026-1033.