Alternative splice forms of CTLA-4 induced by antisense mediated splice-switching influences autoimmune diabetes susceptibility in NOD mice

Nucleic Acid Therapeutics

Volumn 24, Issue 2, 2014, Pages 114-126

  Mourich, Dan V ^a   Oda, Shannon K ^b   Schnell, Frederick J ^a   Crumley, Stacy L ^a   Hauck, Laura L ^c   Moentenich, Carla A ^d   Marshall, Nikki B ^e   Hinrichs, Dave J ^f   Iversen, Patrick L ^a  

^a AVI BIOPHARMA INC   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d PORTLAND COMMUNITY COLLEGE   (United States)

^e NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^f PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERCELLULAR ADHESION MOLECULE 1;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTISENSE THERAPY; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE PREDISPOSITION; EXON; FEMALE; GLUCOSE BLOOD LEVEL; INSULITIS; LYMPHOCYTE PROLIFERATION; MOUSE; MOUSE STRAIN; NONHUMAN; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TRANSGENE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; AUTOIMMUNITY; BASE SEQUENCE; CELL ADHESION; CELL PROLIFERATION; CTLA-4 ANTIGEN; DIABETES MELLITUS, TYPE 1; DISEASE SUSCEPTIBILITY; EXONS; GENE EXPRESSION REGULATION; IMMUNOCONJUGATES; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN ISOFORMS; SEVERITY OF ILLNESS INDEX; T-LYMPHOCYTES, REGULATORY;

EID: 84896929436     PISSN: 21593337     EISSN: None     Source Type: Journal    
DOI: 10.1089/nat.2013.0449     Document Type: Article

References (52)

1. ALTER, J., LOU, F., RABINOWITZ, A., YIN, H., ROSENFELD, J., WILTON, S. D., PARTRIDGE, T. A., and LU, Q. L. (2006). Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat. Med. 12, 175-177.
2. ARAKI, M., CHUNG, D., LIU, S., RAINBOW, D. B., CHAMBERLAIN, G., GARNER, V., HUNTER, K. M., VIJAYAKRISHNAN, L., PETERSON, L. B., OUKKA, M., SHARPE, et al. (2009). Genetic evidence that the differential expression of the ligand-independent isoform of CTLA-4 is the molecular basis of the Idd5. 1 type 1 diabetes region in nonobese diabetic mice. J. Immunol. 183, 5146-5157.
3. BLACK, D. L. (2003). Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72, 291-336.
4. BLOMHOFF, A., LIE, B. A., MYHRE, A. G., KEMP, E. H., WEETMAN, A. P., AKSELSEN, H. E., HUSEBY, E. S., and UNDLIEN, D. E. (2004). Polymorphisms in the cytotoxic T lymphocyte antigen-4 gene region confer susceptibility to Addison's disease. J. Clin. Endocrinol. Metab. 89, 3474-3476.
5. CHIKUMA, S., ABBAS, A. K., and BLUESTONE, J. A. (2005). B7-independent inhibition of T cells by CTLA-4. J. Immunol. 175, 177-181.
6. CROOKE, S. T. (1999). Molecular mechanisms of action of antisense drugs. Biochim. Biophys. Acta 1489, 31-44.
7. ELLENHORN, J. D., HIRSCH, R., SCHREIBER, H., and BLUESTONE, J. A. (1988). In vivo administration of anti-CD3 prevents malignant progressor tumor growth. Science 242, 569-571.
8. FAUSTINO, N. A., and COOPER, T. A. (2003). Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437.
9. FIFE, B. T., GRIFFIN, M. D., ABBAS, A. K., LOCKSLEY, R. M., and BLUESTONE, J. A. (2006). Inhibition of T cell activation and autoimmune diabetes using a B cell surfacelinked CTLA-4 agonist. J. Clin. Invest. 116, 2252-2261.
10. FLETCHER, S., HONEYMAN, K., FALL, A. M., HARDING, P. L., JOHNSEN, R. D., STEINHAUS, J. P., MOULTON, H. M., IVERSEN, P. L., and WILTON, S. D. (2007). Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol Ther. 15, 1587-1592.
11. GOUGH, S. C., WALKER, L. S., and SANSOM, D. M. (2005). CTLA4 gene polymorphism and autoimmunity. Immunol. Rev. 204, 102-115.
12. GREVE, B., VIJAYAKRISHNAN, L., KUBAL, A., SOBEL, R. A., PETERSON, L. B., WICKER, L. S., and KUCHROO, V. K. (2004). The diabetes susceptibility locus Idd5. 1 on mouse chromosome 1 regulates ICOS expression and modulates murine experimental autoimmune encephalomyelitis. J. Immunol. 173, 157-163.
13. GUNTERMANN, C., and ALEXANDER, D. R. (2002). CTLA-4 suppresses proximal TCR signaling in resting human CD4(+) T cells by inhibiting ZAP-70 Tyr(319) phosphorylation: a potential role for tyrosine phosphatases. J. Immunol. 168, 4420-4429.
14. ICHINOSE, K., ZHANG, Z., KOGA, T., JUANG, Y. T., KISTOTH, K., SHARPE, A. H., KUCHROO, V., CRISPIN, J. C., and TSOKOS, G. C. (2013). Increased expression of a short splice variant of CTLA-4 exacerbates lupus in MRL/lpr mice. Arthritis Rheum. 65, 764-769.
15. JOHNSON, J. M., CASTLE, J., GARRETT-ENGELE, P., KAN, Z., LOERCH, P. M., ARMOUR, C. D., SANTOS, R., SCHADT, E. E., STOUGHTON, R., and SHOEMAKER, D. D. (2003). Genome-wide survey of human alternative premRNA splicing with exon junction microarrays. Science 302, 2141-2144.
16. KAKOULIDOU, M., WANG, X., ZHAO, X., PIRSKANEN, R., and LEFVERT, A. K. (2007). Soluble costimulatory factors sCD28, sCD80, sCD86 and sCD152 in relation to other markers of immune activation in patients with myasthenia gravis. J. Neuroimmunol. 185, 150-161.
17. KING, A. L., MOODIE, S. J., FRASER, J. S., CURTIS, D., REID, E., DEARLOVE, A. M., and CICLITIRA, P. J. (2003). Coeliac disease: investigation of proposed causal variants in the CTLA4 gene region. Eur. J. Immunogenet. 30, 427-432.
18. KISSLER, S., FISHER, K., and AL., E. (2009). The soluble CTLA-4 splice variant affects the function of CD4+ CD25+ regulatory T cells. The American Association of Immunologists, Inc. 2009 Meeting 182. Seattle, WA, May 8-12, 2009.
19. J. Immunol. 182, 49. 10.
20. KOUKI, T., GARDINE, C. A., YANAGAWA, T., and DEGROOT, L. J. (2002). Relation of three polymorphisms of the CTLA-4 gene in patients with Graves' disease. J. Endocrinol. Invest. 25, 208-213.
21. KRUMMEL, M. F., and ALLISON, J. P. (1995). CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 182, 459-465.
22. KRUMMEL, M. F., and ALLISON, J. P. (1996). CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 183, 2533-2540.
23. KUHNS, M. S., EPSHTEYN, V., SOBEL, R. A., and ALLISON, J. P. (2000). Cytotoxic T lymphocyte antigen-4 (CTLA-4) regulates the size, reactivity, and function of a primed pool of CD4+ T cells. Proc. Natl. Acad. Sci. U. S. A. 97, 12711-12716.
24. LIU, M. F., WANG, C. R., CHEN, P. C., and FUNG, L. L. (2003). Increased expression of soluble cytotoxic T-lymphocyte-associated antigen-4 molecule in patients with systemic lupus erythematosus. Scand. J. Immunol. 57, 568-572.
25. LIU, S. M., SUTHERLAND, A. P., ZHANG, Z., RAINBOW, D. B., QUINTANA, F. J., PATERSON, A. M., SHARPE, A. H., OUKKA, M., WICKER, L. S., and KUCHROO, V. K. (2012). Overexpression of the Ctla-4 isoform lacking exons 2 and 3 causes autoimmunity. J. Immunol. 188, 155-162.
26. LUHDER, F., HOGLUND, P., ALLISON, J. P., BENOIST, C., and MATHIS, D. (1998). Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes. J. Exp. Med. 187, 427-432.
27. MARSHALL, N. B., ODA, S. K., LONDON, C. A., MOULTON, H. M., IVERSEN, P. L., KERKVLIET, N. I., and MOURICH, D. V. (2007). Arginine-rich cell-penetrating peptides facilitate delivery of antisense oligomers into murine leukocytes and alter pre-mRNA splicing. J. Immunol. Methods 325, 114-126.
28. NELSON, M. H., STEIN, D. A., KROEKER, A. D., HATLEVIG, S. A., IVERSEN, P. L., and MOULTON, H. M. (2005). Arginine-rich peptide conjugation to morpholino oligomers: effects on antisense activity and specificity. Bioconjug. Chem. 16, 959-966.
29. NIELSEN, C., BARINGTON, T., HANSEN, S., and LILLEVANG, S. T. (2007). Comment on Aberrant regulation of synovial T cell activation by soluble costimulatory molecules in rheumatoid arthritis. J. Immunol. 178, 4708; author reply 4709.
30. OAKS, M. K., HALLETT, K. M., PENWELL, R. T., STAUBER, E. C., WARREN, S. J., and TECTOR, A. J. (2000). A native soluble form of CTLA-4. Cell Immunol. 201, 144-153.
31. PENTCHEVA-HOANG, T., EGEN, J. G., WOJNOONSKI, K., and ALLISON, J. P. (2004). B7-1 and B7-2 selectively recruit CTLA-4 and CD28 to the immunological synapse. Immunity 21, 401-413.
32. PEREZ, V. L., VAN PARIJS, L., BIUCKIANS, A., ZHENG, X. X., STROM, T. B., and ABBAS, A. K. (1997). Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 6, 411-417.
33. READ, S., GREENWALD, R., IZCUE, A., ROBINSON, N., MANDELBROT, D., FRANCISCO, L., SHARPE, A. H., and POWRIE, F. (2006). Blockade of CTLA-4 on CD4+ CD25+ regulatory T cells abrogates their function in vivo. J. Immunol. 177, 4376-4383.
34. SAITO, T., YOKOSUKA, T., and HASHIMOTO-TANE, A. (2010). Dynamic regulation of T cell activation and costimulation through TCR-microclusters. FEBS Lett. 584, 4865-4871.
35. SALOMON, B., and BLUESTONE, J. A. (2001). Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu. Rev. Immunol. 19, 225-252.
36. SAZANI, P., GEMIGNANI, F., KANG, S. H., MAIER, M. A., MANOHARAN, M., PERSMARK, M., BORTNER, D., and KOLE, R. (2002). Systemically delivered antisense oligomers upregulate gene expression in mouse tissues. Nat. Biotechnol. 20, 1228-1233.
37. SCHNEIDER, H., MANDELBROT, D. A., GREENWALD, R. J., NG, F., LECHLER, R., SHARPE, A. H., and RUDD, C. E. (2002). Cutting edge: CTLA-4 (CD152) differentially regulates mitogen-activated protein kinases (extracellular signal-regulated kinase and c-Jun N-terminal kinase) in CD4+ T cells from receptor/ligand-deficient mice. J. Immunol. 169, 3475-3479.
38. SCHNEIDER, H., VALK, E., DA ROCHA DIAS, S., WEI, B., and RUDD, C. E. (2005). CTLA-4 up-regulation of lymphocyte function-associated antigen 1 adhesion and clustering as an alternate basis for coreceptor function. Proc. Natl. Acad. Sci. U. S. A. 102, 12861-12366.
39. SIMONE, R., and SAVERINO, D. (2009). The soluble CTLA-4 receptor and its emerging role in autoimmune diseases. Curr. Immunol. Rev. 5, 54-68.
40. STEIN, D., FOSTER, E., HUANG, S. B., WELLER, D., and SUMMERTON, J. (1997). A specificity comparison of four antisense types: morpholino, 2'-O-methyl RNA, DNA, and phosphorothioate DNA. Antisense Nucleic Acid Drug Dev. 7, 151-157.
41. STUMPF, M., ZHOU, X., and BLUESTONE, J. A. (2013). The b7-independent isoform of ctla-4 functions to regulate autoimmune diabetes. J. Immunol. 190, 961-969.
42. SUMMERTON, J., and WELLER, D. (1997). Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7, 187-195.
43. TANG, Q., BODEN, E. K., HENRIKSEN, K. J., BOURJORDAN, H., BI, M., and BLUESTONE, J. A. (2004). Distinct roles of CTLA-4 and TGF-beta in CD4+ CD25+ regulatory T cell function. Eur. J. Immunol. 34, 2996-3005.
44. TIVOL, E. A., BORRIELLO, F., SCHWEITZER, A. N., LYNCH, W. P., BLUESTONE, J. A., and SHARPE, A. H. (1995). Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3, 541-547.
45. UEDA, H., HOWSON, J. M., ESPOSITO, L., HEWARD, J., SNOOK, H., CHAMBERLAIN, G., RAINBOW, D. B., HUNTER, K. M., SMITH, A. N., DI GENOVA, G., HERR, M. H., et al. (2003). Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 423, 506-511.
46. VACEK, M., SAZANI, P., and KOLE, R. (2003). Antisensemediated redirection of mRNA splicing. Cell Mol. Life Sci. 60, 825-833.
47. VANDERLUGT, C. L., KARANDIKAR, N. J., LENSCHOW, D. J., DAL CANTO, M. C., BLUESTONE, J. A., and MILLER, S. D. (1997). Treatment with intact anti-B7-1 mAb during disease remission enhances epitope spreading and exacerbates relapses in R-EAE. J. Neuroimmunol. 79, 113-118.
48. VASU, C., PRABHAKAR, B. S., and HOLTERMAN, M. J. (2004). Targeted CTLA-4 engagement induces CD4+ CD25+ CTLA-4high T regulatory cells with target (allo)antigen specificity. J. Immunol. 173, 2866-2876.
49. VIJAYAKRISHNAN, L., SLAVIK, J. M., ILLES, Z., GREENWALD, R. J., RAINBOW, D., GREVE, B., PETERSON, L. B., HAFLER, D. A., FREEMAN, G. J., SHARPE, A. H., WICKER, L. S., and KUCHROO, V. K. (2004). An autoimmune disease-associated CTLA-4 splice variant lacking the B7 binding domain signals negatively in T cells. Immunity 20, 563-575.
50. WAN, B., NIE, H., LIU, A., FENG, G., HE, D., XU, R., ZHANG, Q., DONG, C., and ZHANG, J. Z. (2006). Aberrant regulation of synovial T cell activation by soluble costimulatory molecules in rheumatoid arthritis. J. Immunol. 177, 8844-8850.
51. WILTON, S. D., LLOYD, F., CARVILLE, K., FLETCHER, S., HONEYMAN, K., AGRAWAL, S., and KOLE, R. (1999). Specific removal of the nonsense mutation from the mdx dystrophin mRNA using antisense oligonucleotides. Neuromuscul. Disord. 9, 330-338.
52. YOKOSUKA, T., KOBAYASHI, W., TAKAMATSU, M., SAKATA-SOGAWA, K., ZENG, H., HASHIMOTO-TANE, A., YAGITA, H., TOKUNAGA, M., and SAITO, T. (2010). Spatiotemporal basis of CTLA-4 costimulatory moleculemediated negative regulation of T cell activation. Immunity 33, 326-339.