Implications for gene therapy-limiting expression of IL- 2Rγc delineate differences in signaling thresholds required for lymphocyte development and maintenance

Journal of Immunology

Volumn 185, Issue 3, 2010, Pages 1393-1403

  Orr, Selinda J ^a   Roessler, Stephen ^a   Quigley, Laura ^a   Chan, Tim ^a   Ford, Jill W ^a   O'Connor, Geraldine M ^a   McVicar, Daniel W ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 2 RECEPTOR GAMMA; INTERLEUKIN 2 RECEPTOR GAMMAC; INTERLEUKIN 7 RECEPTOR ALPHA; STAT5 PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; GENE THERAPY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; IMMUNOLOGY; METABOLISM; METHODOLOGY; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; SEVERE COMBINED IMMUNODEFICIENCY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENE THERAPY; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; INTERLEUKIN-15; INTERLEUKIN-2; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, SCID; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; SEVERE COMBINED IMMUNODEFICIENCY; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTE SUBSETS; TRANSDUCTION, GENETIC;

EID: 77956399493     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903528     Document Type: Article

References (40)

1. Kovanen, P. E., and W. J. Leonard. 2004. Cytokines and immunodeficiency diseases: critical roles of the gamma(c)-dependent cytokines interleukins 2, 4, 7, 9, 15, and 21, and their signaling pathways. Immunol. Rev. 202: 67-83.
2. Sugamura, K., H. Asao, M. Kondo, N. Tanaka, N. Ishii, K. Ohbo, M. Nakamura, and T. Takeshita. 1996. The interleukin-2 receptor gamma chain: its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu. Rev. Immunol. 14: 179-205.
3. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191: 771-780.
4. von Freeden-Jeffry, U., P. Vieira, L. A. Lucian, T. McNeil, S. E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181: 1519-1526.
5. Cao, X., E. W. Shores, J. Hu-Li, M. R. Anver, B. L. Kelsall, S. M. Russell, J. Drago, M. Noguchi, A. Grinberg, E. T. Bloom, et al. 1995. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 2: 223-238.
6. Sun, J. C., A. Ma, and L. L. Lanier. 2009. Cutting edge: IL-15-independent NK cell response to mouse cytomegalovirus infection. J. Immunol. 183: 2911-2914.
7. Noguchi, M., H. Yi, H. M. Rosenblatt, A. H. Filipovich, S. Adelstein, W. S. Modi, O. W. McBride, and W. J. Leonard. 1993. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73: 147-157.
8. Cavazzana-Calvo, M., C. Lagresle, S. Hacein-Bey-Abina, and A. Fischer. 2005. Gene therapy for severe combined immunodeficiency. Annu. Rev. Med. 56: 585-602.
9. Hacein-Bey-Abina, S., C. Von Kalle, M. Schmidt, M. P. McCormack, N. Wulffraat, P. Leboulch, A. Lim, C. S. Osborne, R. Pawliuk, E. Morillon, et al. 2003. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302: 415-419. (Pubitemid 37296260)
10. Howe, S. J., M. R. Mansour, K. Schwarzwaelder, C. Bartholomae, M. Hubank, H. Kempski, M. H. Brugman, K. Pike-Overzet, S. J. Chatters, D. de Ridder, et al. 2008. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118: 3143-3150.
11. Woods, N. B., V. Bottero, M. Schmidt, C. von Kalle, and I. M. Verma. 2006. Gene therapy: therapeutic gene causing lymphoma. Nature 440: 1123.
12. Amorosi, S., I. Russo, G. Amodio, C. Garbi, L. Vitiello, L. Palamaro, M. Adriani, I. Vigliano, and C. Pignata. 2009. The cellular amount of the common gamma-chain influences spontaneous or induced cell proliferation. J. Immunol. 182: 3304-3309.
13. Lo, M., M. L. Bloom, K. Imada, M. Berg, J. M. Bollenbacher, E. T. Bloom, B. L. Kelsall, and W. J. Leonard. 1999. Restoration of lymphoid populations in a murine model of X-linked severe combined immunodeficiency by a gene-therapy approach. Blood 94: 3027-3036.
14. Otsu, M., S. M. Anderson, D. M. Bodine, J. M. Puck, J. J. O'Shea, and F. Candotti. 2000. Lymphoid development and function in X-linked severe combined immunodeficiency mice after stem cell gene therapy. Mol. Ther. 1: 145-153.
15. Otsu, M., K. Sugamura, and F. Candotti. 2001. Lack of dominant-negative effects of a truncated gamma(c) on retroviral-mediated gene correction of immunodeficient mice. Blood 97: 1618-1624. (Pubitemid 32217226)
16. Soudais, C., T. Shiho, L. I. Sharara, D. Guy-Grand, T. Taniguchi, A. Fischer, and J. P. Di Santo. 2000. Stable and functional lymphoid reconstitution of common cytokine receptor gamma chain deficient mice by retroviral-mediated gene transfer. Blood 95: 3071-3077.
17. Hacein-Bey-Abina, S., F. Le Deist, F. Carlier, C. Bouneaud, C. Hue, J. P. De Villartay, A. J. Thrasher, N. Wulffraat, R. Sorensen, S. Dupuis-Girod, et al. 2002. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N. Engl. J. Med. 346: 1185-1193.
18. Gaspar, H. B., K. L. Parsley, S. Howe, D. King, K. C. Gilmour, J. Sinclair, G. Brouns, M. Schmidt, C. Von Kalle, T. Barington, et al. 2004. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364: 2181-2187. (Pubitemid 40018447)
19. Smyth, C. M., S. L. Ginn, C. T. Deakin, G. J. Logan, and I. E. Alexander. 2007. Limiting gammac expression differentially affects signaling via the interleukin (IL)-7 and IL-15 receptors. Blood 110: 91-98.
20. Zhang, W., C. L. Sommers, D. N. Burshtyn, C. C. Stebbins, J. B. DeJarnette, R. P. Trible, A. Grinberg, H. C. Tsay, H. M. Jacobs, C. M. Kessler, et al. 1999. Essential role of LAT in T cell development. Immunity 10: 323-332. (Pubitemid 29165287)
21. Orr, S. J., L. Quigley, and D. W. McVicar. 2009. In vivo expression of signaling proteins in reconstituted NK cells. J. Immunol. Methods 340: 158-163.
22. Van De Wiele, C. J., J. H. Marino, B. W. Murray, S. S. Vo, M. E. Whetsell, and T. K. Teague. 2004. Thymocytes between the beta-selection and positive selection checkpoints are nonresponsive to IL-7 as assessed by STAT-5 phosphorylation. J. Immunol. 172: 4235-4244.
23. Crawley, J. B., J. Willcocks, and B. M. Foxwell. 1996. Interleukin-7 induces T cell proliferation in the absence of Erk/MAP kinase activity. Eur. J. Immunol. 26: 2717-2723.
24. Lockyer, H. M., E. Tran, and B. H. Nelson. 2007. STAT5 is essential for Akt/p70S6 kinase activity during IL-2-induced lymphocyte proliferation. J. Immunol. 179: 5301-5308.
25. Huntington, N. D., N. Legrand, N. L. Alves, B. Jaron, K. Weijer, A. Plet, E. Corcuff, E. Mortier, Y. Jacques, H. Spits, and J. P. Di Santo. 2009. IL-15 transpresentation promotes human NK cell development and differentiation in vivo. J. Exp. Med. 206: 25-34.
26. Ma, A., R. Koka, and P. Burkett. 2006. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 24: 657-679.
27. Cooper, M. A., J. E. Bush, T. A. Fehniger, J. B. VanDeusen, R. E. Waite, Y. Liu, H. L. Aguila, and M. A. Caligiuri. 2002. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100: 3633-3638.
28. Koka, R., P. R. Burkett, M. Chien, S. Chai, F. Chan, J. P. Lodolce, D. L. Boone, and A. Ma. 2003. Interleukin (IL)-15R[alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J. Exp. Med. 197: 977-984.
29. Biron, C. A., K. S. Byron, and J. L. Sullivan. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320: 1731-1735.
30. Ching, C., and C. Lopez. 1979. Natural killing of herpes simplex virus type 1-infected target cells: normal human responses and influence of antiviral antibody. Infect. Immun. 26: 49-56.
31. Joncas, J., Y. Monczak, F. Ghibu, C. Alfieri, A. Bonin, G. Ahronheim, and G. Rivard. 1989. Brief report: killer cell defect and persistent immunological abnormalities in two patients with chronic active Epstein-Barr virus infection. J. Med. Virol. 28: 110-117.
32. Quinnan, G. V., Jr., N. Kirmani, A. H. Rook, J. F. Manischewitz, L. Jackson, G. Moreschi, G. W. Santos, R. Saral, and W. H. Burns. 1982. Cytotoxic t cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non-T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N. Engl. J. Med. 307: 7-13.
33. Johnston, J. A., C. M. Bacon, D. S. Finbloom, R. C. Rees, D. Kaplan, K. Shibuya, J. R. Ortaldo, S. Gupta, Y. Q. Chen, J. D. Giri, et al. 1995. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc. Natl. Acad. Sci. USA 92: 8705-8709.
34. Ravichandran, K. S., and S. J. Burakoff. 1994. The adapter protein Shc interacts with the interleukin-2 (IL-2) receptor upon IL-2 stimulation. J. Biol. Chem. 269: 1599-1602.
35. Ahmed, N. N., H. L. Grimes, A. Bellacosa, T. O. Chan, and P. N. Tsichlis. 1997. Transduction of interleukin-2 antiapoptotic and proliferative signals via Akt protein kinase. Proc. Natl. Acad. Sci. USA 94: 3627-3632.
36. Migone, T. S., S. Rodig, N. A. Cacalano, M. Berg, R. D. Schreiber, and W. J. Leonard. 1998. Functional cooperation of the interleukin-2 receptor beta chain and Jak1 in phosphatidylinositol 3-kinase recruitment and phosphorylation. Mol. Cell. Biol. 18: 6416-6422.
37. Witherden, D., N. van Oers, C. Waltzinger, A. Weiss, C. Benoist, and D. Mathis. 2000. Tetracycline-controllable selection of CD4(+) T cells: half-life and survival signals in the absence of major histocompatibility complex class II molecules. J. Exp. Med. 191: 355-364.
38. Vivien, L., C. Benoist, and D. Mathis. 2001. T lymphocytes need IL-7 but not IL-4 or IL-6 to survive in vivo. Int. Immunol. 13: 763-768.
39. Bakker, A. B., R. M. Hoek, A. Cerwenka, B. Blom, L. Lucian, T. McNeil, R. Murray, L. H. Phillips, J. D. Sedgwick, and L. L. Lanier. 2000. DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity 13: 345-353.
40. Takai, T., M. Li, D. Sylvestre, R. Clynes, and J. V. Ravetch. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76: 519-529.