Mechanisms of PDL1-mediated regulation of autoimmune diabetes

Clinical Immunology

Volumn 125, Issue 1, 2007, Pages 16-25

  Guleria, Indira ^a   Gubbels Bupp, Melanie ^b   Dada, Shirine ^a   Fife, Brian ^b   Tang, Qizhi ^b   Ansari, Mohammed Javeed ^a   Trikudanathan, Subbulaxmi ^a   Vadivel, Nidyanandh ^a   Fiorina, Paolo ^a   Yagita, Hideo ^c   Azuma, Miyuki ^d   Atkinson, Mark ^e   Bluestone, Jeffrey A ^b   Sayegh, Mohamed H ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e UNIVERSITY OF FLORIDA   (United States)

Author keywords

Negative costimulatory pathways; NOD; Programmed death ligand; Type 1 diabetes

Indexed keywords

ANTIBODY; CD4 ANTIGEN; CD8 ANTIGEN; CELL PROTEIN; PROTEIN PD 1; PROTEIN PDL1; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS; PRIORITY JOURNAL; REGULATORY MECHANISM; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD80; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FEMALE; FLOW CYTOMETRY; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PEPTIDES;

EID: 34548513981     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2007.05.013     Document Type: Article

References (47)

1. Van Parijs L., and Abbas A.K. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280 (1998) 243-248
2. Rothstein D.M., and Sayegh M.H. T-cell costimulatory pathways in allograft rejection and tolerance. Immunol. Rev. 196 (2003) 85-108
3. Khoury S.J., and Sayegh M.H. The roles of the new negative T cell costimulatory pathways in regulating autoimmunity. Immunity 20 (2004) 529-538
4. Ansari M.J., and Sayegh M.H. Costimulation couture: a designer approach to regulating autoimmunity. J. Clin. Invest. 116 (2006) 2080-2083
5. Greenwald R.J., Freeman G.J., and Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol. 23 (2005) 515-548
6. Collins M., Ling V., and Carreno B.M. The B7 family of immune-regulatory ligands. Genome Biol. 6 (2005) 223
7. Tseng S.Y., Otsuji M., Gorski K., Huang X., Slansky J.E., Pai S.I., Shalabi A., Shin T., Pardoll D.M., and Tsuchiya H. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J. Exp. Med. 193 (2001) 839-846
8. Latchman Y., Wood C., Chernova T., Chaudhary D., Borde M., Chernova I., Iwai Y., Long A., Brown J., Nunes R., Greenfield E., Bourque K., Boussiotis V., Carter L., Carreno B., Malenkovich N., Nishimura H., Honjo T., Freeman G., and Sharpe A. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2 (2001) 261-268
9. Liang S.C., Latchman Y.E., Buhlmann J.E., Tomczak M.F., Horwitz B.H., Freeman G.J., and Sharpe A.H. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur. J. Immunol. 33 (2003) 2706-2716
10. Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., Azuma M., and Yagita H. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169 (2002) 5538-5545
11. Eppihimer M.J., Gunn J., Freeman G.J., Greenfield E.A., Chernova T., Erickson J., and Leonard J.P. Expression and regulation of the PD-L1 immunoinhibitory molecule on microvascular endothelial cells. Microcirculation 9 (2002) 133-145
12. Schoop R., Wahl P., Le Hir M., Heemann U., Wang M., and Wuthrich R.P. Suppressed T-cell activation by IFN-gamma-induced expression of PD-L1 on renal tubular epithelial cells. Nephrol. Dial. Transplant. 19 (2004) 2713-2720
13. Nakazawa A., Dotan I., Brimnes J., Allez M., Shao L., Tsushima F., Azuma M., and Mayer L. The expression and function of costimulatory molecules B7H and B7-H1 on colonic epithelial cells. Gastroenterology 126 (2004) 1347-1357
14. Ansari M.J., Chitnis T., Smith R.N., Yagita H., Akiba H., Azuma M., Iwai H., Auchincloss Jr. H., Khoury S., and Sayegh M.H. The programmed death-1 pathway regulates autoimmune diabetes in NOD mice. J. Exp. Med. 198 (2003) 63-69
15. Nishimura H., Minato N., Nakano T., and Honjo T. Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int. Immunol. 10 (1998) 1563-1572
16. Nishimura H., Nose M., Hiai H., Minato N., and Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11 (1999) 141-151
17. Salama A.D., Chitnis T., Imitola J., Ansari M.J., Akiba H., Tushima F., Azuma M., Yagita H., Sayegh M.H., and Khoury S.J. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J. Exp. Med. 198 (2003) 71-78
18. Latchman Y.E., Liang S.C., Wu Y., Chernova T., Sobel R.A., Klemm M., Kuchroo V.K., Freeman G.J., and Sharpe A.H. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 10691-10696
19. Wang J., Yoshida T., Nakaki F., Hiai H., Okazaki T., and Honjo T. Establishment of NOD-Pdcd1-/- mice as an efficient animal model of type I diabetes. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11823-11828
20. Keir M.E., Liang S.C., Guleria I., Latchman Y.E., Qipo A., Albacker L.A., Koulmanda M., Freeman G.J., Sayegh M.H., and Sharpe A.H. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203 (2006) 883-895
21. Gagnerault M.C., Luan J.J., Lotton C., and Lepault F. Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J. Exp. Med. 196 (2002) 369-377
22. Luhder F., Hoglund P., Allison J.P., Benoist C., and Mathis D. Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes. J. Exp. Med. 187 (1998) 427-432
23. Verdaguer J., Schmidt D., Amrani A., Anderson B., Averill N., and Santamaria P. Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J. Exp. Med. 186 (1997) 1663-1676
24. Agata Y., Kawasaki H., Nishimura H., Ishida Y., Tsubata T., Yagita H., and Honjo T. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 8 (1996) 765-772
25. Okazaki T., Iwai Y., and Honjo T. New regulatory co-receptors: inducible co-stimulator and PD-1. Curr. Opin. Immunol. 14 (2002) 779-782
26. Mora C., Wong F.S., Chang C.H., and Flavell R.A. Pancreatic infiltration but not diabetes occurs in the relative absence of MHC class II-restricted CD4 T cells: studies using NOD/CIITA-deficient mice. J. Immunol. 162 (1999) 4576-4588
27. Wicker L.S., Leiter E.H., Todd J.A., Renjilian R.J., Peterson E., Fischer P.A., Podolin P.L., Zijlstra M., Jaenisch R., and Peterson L.B. Beta 2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes 43 (1994) 500-504
28. Serreze D.V., Chapman H.D., Varnum D.S., Hanson M.S., Reifsnyder P.C., Richard S.D., Fleming S.A., Leiter E.H., and Shultz L.D. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J. Exp. Med. 184 (1996) 2049-2053
29. Serreze D.V., Fleming S.A., Chapman H.D., Richard S.D., Leiter E.H., and Tisch R.M. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 161 (1998) 3912-3918
30. Katz J.D., Wang B., Haskins K., Benoist C., and Mathis D. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74 (1993) 1089-1100
31. Gonzalez A., Katz J.D., Mattei M.G., Kikutani H., Benoist C., and Mathis D. Genetic control of diabetes progression. Immunity 7 (1997) 873-883
32. Luhder F., Chambers C., Allison J.P., Benoist C., and Mathis D. Pinpointing when T cell costimulatory receptor CTLA-4 must be engaged to dampen diabetogenic T cells. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12204-12209
33. Sandner S.E., Clarkson M.R., Salama A.D., Sanchez-Fueyo A., Domenig C., Habicht A., Najafian N., Yagita H., Azuma M., Turka L.A., and Sayegh M.H. Role of the programmed death-1 pathway in regulation of alloimmune responses in vivo. J. Immunol. 174 (2005) 3408-3415
34. Krupnick A.S., Gelman A.E., Barchet W., Richardson S., Kreisel F.H., Turka L.A., Colonna M., Patterson G.A., and Kreisel D. Murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J. Immunol. 175 (2005) 6265-6270
35. Forsgren S., Andersson A., Hillorn V., Soderstrom A., and Holmberg D. Immunoglobulin-mediated prevention of autoimmune diabetes in the non-obese diabetic (NOD) mouse. Scand. J. Immunol. 34 (1991) 445-451
36. Noorchashm H., Noorchashm N., Kern J., Rostami S.Y., Barker C.F., and Naji A. B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes 46 (1997) 941-946
37. Nagata M., Santamaria P., Kawamura T., Utsugi T., and Yoon J.W. Evidence for the role of CD8+ cytotoxic T cells in the destruction of pancreatic beta-cells in nonobese diabetic mice. J. Immunol. 152 (1994) 2042-2050
38. Wang B., Gonzalez A., Benoist C., and Mathis D. The role of CD8+ T cells in the initiation of insulin-dependent diabetes mellitus. Eur. J. Immunol. 26 (1996) 1762-1769
39. Serreze D.V., Chapman H.D., Varnum D.S., Gerling I., Leiter E.H., and Shultz L.D. Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J. Immunol. 158 (1997) 3978-3986
40. Carter L., Fouser L.A., Jussif J., Fitz L., Deng B., Wood C.R., Collins M., Honjo T., Freeman G.J., and Carreno B.M. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur. J. Immunol. 32 (2002) 634-643
41. Gao W., Demirci G., Strom T.B., and Li X.C. Stimulating PD-1-negative signals concurrent with blocking CD154 co-stimulation induces long-term islet allograft survival. Transplantation 76 (2003) 994-999
42. Ishida Y., Agata Y., Shibahara K., and Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11 (1992) 3887-3895
43. Lechner O., Lauber J., Franzke A., Sarukhan A., von Boehmer H., and Buer J. Fingerprints of anergic T cells. Curr. Biol. 11 (2001) 587-595
44. Gavin M.A., Clarke S.R., Negrou E., Gallegos A., and Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 3 (2002) 33-41
45. Raimondi G., Shufesky W.J., Tokita D., Morelli A.E., and Thomson A.W. Regulated compartmentalization of programmed cell death-1 discriminates CD4+CD25+ resting regulatory T cells from activated T cells. J. Immunol. 176 (2006) 2808-2816
46. Schreiner B., Mitsdoerffer M., Kieseier B.C., Chen L., Hartung H.P., Weller M., and Wiendl H. Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis. J. Neuroimmunol. 155 (2004) 172-182
47. Fife B., Guleria I., Gubbels-Bupp M., Tang Q., Bour-Jordan H., Yagita H., Azuma M., Sayegh M.H., and Bluestone J.A. Insulin-induced remission in new onset NOD mice is maintained by the PD-1/PD-L1 pathway. J. Exp. Med. 203 (2006) 2737-2747