Activation of CD4+ T Lymphocytes Form Interleukin 2-deficient Mice by Costimulatory B7 Molecules

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1996 Apr 2

PMID 8610140

Citations 5

Authors

G A Hollander

H Reiser

Affiliations

Soon will be listed here.

Abstract

Interleukin 2 (IL-2)-deficient (IL-2-/-) mice develop hemolytic anemia and chronic inflammatory bowel disease. Importantly, the induction of disease in IL-2-deficient mice is critically dependent on CD4+ T cells. We have studied the requirements of T cells from IL-2-deficient mice for costimulation with B7 antigens. Stable B7-1 or B7-2 chinese hamster ovary (CHO) cell transfectants could synergize with anti-CD3 monoclonal antibody (mAb) to induce the proliferation of CD4+ T cells from IL-2-/- mutant mice. Further mechanistic studies established that B7-induced activation resulted in surface expression of the alpha chain of the IL-2 receptor. B7-induced proliferation occurred independently of IL-4 and was largely independent of the common gamma chain of the IL-2, IL-4, IL-7, IL-9, and IL-15 receptors. Finally, anti-B7-2 but not anti-B7-1 mAb was able to inhibit the activation of IL-2-/- T cells induced by anti-CD3 mAb in the presence of syngeneic antigen-presenting cells. The results of our experiments indicate that IL-2-/- CD4+ T cells remain responsive to B7 stimulation and raise the possibility that B7 antagonists have a role in the prevention/treatment of inflammatory bowel disease.

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References

Blazar B, Taylor P, Linsley P, Vallera D . In vivo blockade of CD28/CTLA4: B7/BB1 interaction with CTLA4-Ig reduces lethal murine graft-versus-host disease across the major histocompatibility complex barrier in mice. Blood. 1994; 83(12):3815-25. View

Croft M, Bradley L, Swain S . Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J Immunol. 1994; 152(6):2675-85. View

Wallace P, Johnson J, MacMaster J, Kennedy K, Gladstone P, Linsley P . CTLA4Ig treatment ameliorates the lethality of murine graft-versus-host disease across major histocompatibility complex barriers. Transplantation. 1994; 58(5):602-10. DOI: 10.1097/00007890-199409150-00013. View

Guinan E, Gribben J, Boussiotis V, Freeman G, Nadler L . Pivotal role of the B7:CD28 pathway in transplantation tolerance and tumor immunity. Blood. 1994; 84(10):3261-82. View

Linsley P, Greene J, Brady W, Bajorath J, Ledbetter J, Peach R . Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4 receptors. Immunity. 1994; 1(9):793-801. DOI: 10.1016/s1074-7613(94)80021-9. View

Cao X, Shores E, Hu-Li J, Anver M, Kelsall B, Russell S . Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity. 1995; 2(3):223-38. DOI: 10.1016/1074-7613(95)90047-0. View

Freeman G, Boussiotis V, Anumanthan A, Bernstein G, Ke X, Rennert P . B7-1 and B7-2 do not deliver identical costimulatory signals, since B7-2 but not B7-1 preferentially costimulates the initial production of IL-4. Immunity. 1995; 2(5):523-32. DOI: 10.1016/1074-7613(95)90032-2. View

Boise L, Minn A, Noel P, June C, Accavitti M, LINDSTEN T . CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity. 1995; 3(1):87-98. DOI: 10.1016/1074-7613(95)90161-2. View

Powrie F . T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity. 1995; 3(2):171-4. DOI: 10.1016/1074-7613(95)90086-1. View

10.

Simpson S, Mizoguchi E, Allen D, Bhan A, Terhorst C . Evidence that CD4+, but not CD8+ T cells are responsible for murine interleukin-2-deficient colitis. Eur J Immunol. 1995; 25(9):2618-25. DOI: 10.1002/eji.1830250932. View

11.

Ma A, Datta M, Margosian E, Chen J, Horak I . T cells, but not B cells, are required for bowel inflammation in interleukin 2-deficient mice. J Exp Med. 1995; 182(5):1567-72. PMC: 2192197. DOI: 10.1084/jem.182.5.1567. View

12.

Julius M, Simpson E, Herzenberg L . A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973; 3(10):645-9. DOI: 10.1002/eji.1830031011. View

13.

Bhattacharya A, Dorf M, Springer T . A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J Immunol. 1981; 127(6):2488-95. View

14.

Malek T, Robb R, Shevach E . Identification and initial characterization of a rat monoclonal antibody reactive with the murine interleukin 2 receptor-ligand complex. Proc Natl Acad Sci U S A. 1983; 80(18):5694-8. PMC: 384325. DOI: 10.1073/pnas.80.18.5694. View

15.

OHara J, Paul W . Production of a monoclonal antibody to and molecular characterization of B-cell stimulatory factor-1. Nature. 1985; 315(6017):333-6. DOI: 10.1038/315333a0. View

16.

Leo O, Foo M, Sachs D, Samelson L, Bluestone J . Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc Natl Acad Sci U S A. 1987; 84(5):1374-8. PMC: 304432. DOI: 10.1073/pnas.84.5.1374. View

17.

Freedman A, Freeman G, Horowitz J, Daley J, Nadler L . B7, a B-cell-restricted antigen that identifies preactivated B cells. J Immunol. 1987; 139(10):3260-7. View

18.

Linsley P, Clark E, Ledbetter J . T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc Natl Acad Sci U S A. 1990; 87(13):5031-5. PMC: 54255. DOI: 10.1073/pnas.87.13.5031. View

19.

Reiser H . sgp-60, a signal-transducing glycoprotein concerned with T cell activation through the T cell receptor/CD3 complex. J Immunol. 1990; 145(7):2077-86. View

20.

Linsley P, Brady W, Grosmaire L, Aruffo A, Damle N, Ledbetter J . Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J Exp Med. 1991; 173(3):721-30. PMC: 2118836. DOI: 10.1084/jem.173.3.721. View