Consequences of increased CD45RA and RC isoforms for TCR signaling and peripheral T cell deficiency resulting from heterogeneous nuclear ribonucleoprotein L-like mutation

Journal of Immunology

Volumn 185, Issue 1, 2010, Pages 231-238

  Wu, Zuopeng ^a   Yates, Adele L ^a,b   Hoyne, Gerard F ^a,b   Goodnow, Christopher C ^a  

^a Australian National University   (Australia)

^b Food Standards Australia New Zealand   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RA ANTIGEN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L LIKE; ISOPROTEIN; MESSENGER RNA; PROTEIN KINASE LCK; PROTEIN TYROSINE PHOSPHATASE; RNA BINDING PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD45 ANTIGEN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HNRNPLL PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; PTPRA PROTEIN, MOUSE; PTPRC PROTEIN, MOUSE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CELL MUTANT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; IMMUNOREGULATION; LONGEVITY; MOUSE; MUTATION; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; RNA SPLICING; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; THYMUS; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL SURVIVAL; ENZYMOLOGY; GENETICS; IMMUNOLOGY; LYMPHOCYTOPENIA; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PEDIGREE; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD45; BASE SEQUENCE; CELL SURVIVAL; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; LYMPHOPENIA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PEDIGREE; PROTEIN ISOFORMS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 4; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 77956214250     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903625     Document Type: Article

References (45)

1. Hermiston, M. L., Z. Xu, and A. Weiss. 2003. CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21: 107-137.
2. van Vliet, S. J., S. I. Gringhuis, T. B. Geijtenbeek, and Y. van Kooyk. 2006. Regulation of effector T cells by antigen-presenting cells via interaction of the C-type lectin MGL with CD45. Nat. Immunol. 7: 1200-1208.
3. Tchilian, E. Z., and P. C. Beverly. 2006. Altered CD45 expression and disease. Trends Immunol. 27: 146-153.
4. McNeill, L., R. J. Salmond, J. C. Cooper, C. K. Carret, R. L. Cassady-Cain, M. Roche-Molina, P. Tandon, N. Holmes, and D. R. Alexander. 2007. The differential regulation of Lck kinase phosphorylation sites by CD45 is critical for T cell receptor signaling responses. Immunity 27: 425-437.
5. Wu, Z., X. Jia, L. de la Cruz, X. C. Su, B. Marzolf, P. Troisch, D. Zak, A. Hamilton, B. Whittle, D. Yu, et al. 2008. Memory T cell RNA rearrangement programmed by heterogeneous nuclear ribonucleoprotein hnRNPLL. Immunity 29: 863-875.
6. Kishihara, K., J. Penninger, V. A. Wallace, T. M. Kündig, K. Kawai, A. Wakeham, E. Timms, K. Pfeffer, P. S. Ohashi, M. L. Thomas, et al. 1993. Normal B lymphocyte development but impaired T cell maturation in CD45-exon6 protein tyrosine phosphatase-deficient mice. Cell 74: 143-156.
7. Veillette, A., L. Caron, M. Fournel, and T. Pawson. 1992. Regulation of the enzymatic function of the lymphocyte-specific tyrosine protein kinase p56lck by the non-catalytic SH2 and SH3 domains. Oncogene 7: 971-980.
8. D'Oro, U., and J. D. Ashwell. 1999. Cutting edge: the CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes. J. Immunol. 162: 1879-1883.
9. Ostergaard, H. L., D. A. Shackelford, T. R. Hurley, P. Johnson, R. Hyman, B. M. Sefton, and I. S. Trowbridge. 1989. Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc. Natl. Acad. Sci. USA 86: 8959-8963.
10. Leitenberg, D., Y. Boutin, D. D. Lu, and K. Bottomly. 1999. Biochemical association of CD45 with the T cell receptor complex: regulation by CD45 isoform and during T cell activation. Immunity 10: 701-711.
11. Farber, D. L., O. Acuto, and K. Bottomly. 1997. Differential T cell receptor-mediated signaling in naive and memory CD4 T cells. Eur. J. Immunol. 27: 2094-2101.
12. Hall, S. R., B. M. Heffernan, N. T. Thompson, and W. C. Rowan. 1999. CD4+ CD45RA+ and CD4+ CD45RO+ T cells differ in their TCR-associated signaling responses. Eur. J. Immunol. 29: 2098-2106.
13. Stone, J. D., L. A. Conroy, K. F. Byth, R. A. Hederer, S. Howlett, Y. Takemoto, N. Holmes, and D. R. Alexander. 1997. Aberrant TCR-mediated signaling in CD45-null thymocytes involves dysfunctional regulation of Lck, Fyn, TCR-zeta, and ZAP-70. J. Immunol. 158: 5773-5782.
14. Kozieradzki, I., T. Kündig, K. Kishihara, C. J. Ong, D. Chiu, V. A. Wallace, K. Kawai, E. Timms, J. Ionescu, P. Ohashi, et al. 1997. T cell development in mice expressing splice variants of the protein tyrosine phosphatase CD45. J. Immunol. 158: 3130-3139.
15. McNeill, L., R. L. Cassady, S. Sarkardei, J. C. Cooper, G. Morgan, and D. R. Alexander. 2004. CD45 isoforms in T cell signalling and development. Immunol. Lett. 92: 125-134.
16. Tchilian, E. Z., R. Dawes, L. Hyland, M. Montoya, A. Le Bon, P. Borrow, S. Hou, D. Tough, and P. C. Beverley. 2004. Altered CD45 isoform expression affects lymphocyte function in CD45 Tg mice. Int. Immunol. 16: 1323-1332.
17. Dawes, R., S. Petrova, Z. Liu, D. Wraith, P. C. Beverley, and E. Z. Tchilian. 2006. Combinations of CD45 isoforms are crucial for immune function and disease. J. Immunol. 176: 3417-3425.
18. Salmond, R. J., L. McNeill, N. Holmes, and D. R. Alexander. 2008. CD4+ T cell hyper-responsiveness in CD45 transgenic mice is independent of isoform. Int. Immunol. 20: 819-827.
19. Oberdoerffer, S., L. F. Moita, D. Neems, R. P. Freitas, N. Hacohen, and A. Rao. 2008. Regulation of CD45 alternative splicing by heterogeneous ribonucleo-protein, hnRNPLL. Science 321: 686-691.
20. Topp, J. D., J. Jackson, A. A. Melton, and K. W. Lynch. 2008. A cell-based screen for splicing regulators identifies hnRNP LL as a distinct signal-induced repressor of CD45 variable exon 4. RNA 14: 2038-2049.
21. Nelms, K. A., and C. C. Goodnow. 2001. Genome-wide ENU mutagenesis to reveal immune regulators. Immunity 15: 409-418.
22. Akkaraju, S., W. Y. Ho, D. Leong, K. Canaan, M. M. Davis, and C. C. Goodnow. 1997. A range of CD4 T cell tolerance: partial inactivation to organ-specific antigen allows nondestructive thyroiditis or insulitis. Immunity 7: 255-271.
23. Liston, A., S. Lesage, J. Wilson, L. Peltonen, and C. C. Goodnow. 2003. Aire regulates negative selection of organ-specific T cells. Nat. Immunol. 4: 350-354.
24. Gosling, K. M., L. E. Makaroff, A. Theodoratos, Y. H. Kim, B. Whittle, L. Rui, H. Wu, N. A. Hong, G. C. Kennedy, J. A. Fritz, et al. 2007. A mutation in a chromosome condensin II subunit, kleisin beta, specifically disrupts T cell development. Proc. Natl. Acad. Sci. USA 104: 12445-12450.
25. Azzam, H. S., J. B. DeJarnette, K. Huang, R. Emmons, C. S. Park, C. L. Sommers, D. El-Khoury, E. W. Shores, and P. E. Love. 2001. Fine tuning of TCR signaling by CD5. J. Immunol. 166: 5464-5472.
26. Siggs, O. M., L. A. Miosge, A. L. Yates, E. M. Kucharska, D. Sheahan, T. Brdicka, A. Weiss, A. Liston, and C. C. Goodnow. 2007. Opposing functions of the T cell receptor kinase ZAP-70 in immunity and tolerance differentially titrate in response to nucleotide substitutions. Immunity 27: 912-926.
27. Leitenberg, D., T. J. Novak, D. Farber, B. R. Smith, and K. Bottomly. 1996. The extracellular domain of CD45 controls association with the CD4-T cell receptor complex and the response to antigen-specific stimulation. J. Exp. Med. 183: 249-259.
28. Dornan, S., Z. Sebestyen, J. Gamble, P. Nagy, A. Bodnar, L. Alldridge, S. Doe, N. Holmes, L. K. Goff, P. Beverley, et al. 2002. Differential association of CD45 isoforms with CD4 and CD8 regulates the actions of specific pools of p56lck tyrosine kinase in T cell antigen receptor signal transduction. J. Biol. Chem. 277: 1912-1918.
29. Xu, Z., and A. Weiss. 2002. Negative regulation of CD45 by differential homodimerization of the alternatively spliced isoforms. Nat. Immunol. 3: 764-771.
30. Dawes, R., B. Hennig, W. Irving, S. Petrova, S. Boxall, V. Ward, D. Wallace, D. C. Macallan, M. Thursz, A. Hill, et al. 2006. Altered CD45 expression in C77G carriers influences immune function and outcome of hepatitis C infection. J. Med. Genet. 43: 678-684.
31. Do, H. T., W. Baars, K. Borns, A. Windhagen, and R. Schwinzer. 2006. The 77C-〉 G mutation in the human CD45 (PTPRC) gene leads to increased intensity of TCR signaling in T cell lines from healthy individuals and patients with multiple sclerosis. J. Immunol. 176: 931-938.
32. Jacobsen, M., D. Schweer, A. Ziegler, R. Gaber, S. Schock, R. Schwinzer, K. Wonigeit, R.-B. Lindert, O. Kantarci, J. Schaefer-Klein, et al. 2000. A point mutation in PTPRC is associated with the development of multiple sclerosis. Nat. Genet. 26: 495-499.
33. Ballerini, C., E. Rosati, M. Salvetti, G. Ristori, S. Cannoni, T. Biagioli, L. Massacesi, S. Sorbi, and M. Vergelli. 2002. Protein tyrosine phosphatase receptor-type C exon 4 gene mutation distribution in an Italian multiple sclerosis population. Neurosci. Lett. 328: 325-327.
34. Vogel, A., C. P. Strassburg, and M. P. Manns. 2003. 77C/G mutation in the tyrosine phosphatase CD45 gene and autoimmune hepatitis: evidence for a genetic link. Genes Immun. 4: 79-81.
35. Vorechovsky, I., J. Kralovicova, E. Tchilian, T. Masterman, Z. Zhang, B. Ferry, S. Misbah, H. Chapel, D. Webster, D. Hellgren, et al. 2001. Does 77C→G in PTPRC modify autoimmune disorders linked to the major histocompatibility locus? Nat. Genet. 29: 22-23.
36. Jacobsen, M., S. Hoffmann, S. Cepok, S. Stei, A. Ziegler, N. Sommer, and B. Hemmer. 2002. A novel mutation in PTPRC interferes with splicing and alters the structure of the human CD45 molecule. Immunogenetics 54: 158-163. (Pubitemid 34666941)
37. Boxall, S., T. Stanton, K. Hirai, V. Ward, T. Yasui, H. Tahara, A. Tamori, S. Nishiguchi, S. Shiomi, O. Ishiko, et al. 2004. Disease associations and altered immune function in CD45 138G variant carriers. Hum. Mol. Genet. 13: 2377-2384.
38. Majeti, R., Z. Xu, T. G. Parslow, J. L. Olson, D. I. Daikh, N. Killeen, and A. Weiss. 2000. An inactivating point mutation in the inhibitory wedge of CD45 causes lymphoproliferation and autoimmunity. Cell 103: 1059-1070.
39. Liston, A., D. H. Gray, S. Lesage, A. L. Fletcher, J. Wilson, K. E. Webster, H. S. Scott, R. L. Boyd, L. Peltonen, and C. C. Goodnow. 2004. Gene dosage-limiting role of Aire in thymic expression, clonal deletion, and organ-specific autoimmunity. J. Exp. Med. 200: 1015-1026.
40. Cocco, E., M. R. Murru, C. Melis, L. Schirru, E. Solla, M. Lai, M. Rolesu, and M. G. Marrosu. 2004. PTPRC (CD45) C77G mutation does not contribute to multiple sclerosis susceptibility in Sardinian patients. J. Neurol. 251: 1085-1088.
41. Esteghamat, F., B. Noorinayer, M. H. Sanati, A. Hekmatdoost, M. Zafarghandi, H. M. Shalmani, M. Agah, and M. R. Zali. 2005. C77G mutation in protein tyrosine phosphatase CD45 gene and autoimmune hepatitis. Hepatol. Res. 32: 154-157.
42. Kirsten, H., M. Blume, F. Emmrich, N. Hunzelmann, R. Mierau, R. Rzepka, P. Vaith, T. Witte, I. Melchers, and P. Ahnert. 2008. No association between systemic sclerosis and C77G polymorphism in the human PTPRC (CD45) gene. J. Rheumatol. 35: 1817-1819.
43. Sabouri, A. H., M. Saito, W. Matsumoto, D. Kodama, R. Farid, S. Izumo, K. Usuku, and M. Osame. 2003. A C77G point mutation in CD45 exon 4, which is associated with the development of multiple sclerosis and increased susceptibility to HIV-1 infection, is undetectable in Japanese population. Eur. J. Neurol. 10: 737-739.
44. Szvetko, A. L., A. Jones, J. Mackenzie, L. Tajouri, P. A. Csurhes, J. M. Greer, M. P. Pender, and L. R. Griffiths. 2009. An investigation of the C77G and C772T variations within the human protein tyrosine phosphatase receptor type C gene for association with multiple sclerosis in an Australian population. Brain Res. 1255: 148-152.
45. Surh, C. D., and J. Sprent. 2008. Homeostasis of naive and memory T cells. Immunity 29: 848-862.