Tumor PD-L1 co-stimulates primary human CD8+ cytotoxic T cells modified to express a PD1: CD28 chimeric receptor

Molecular Immunology

Volumn 51, Issue 3-4, 2012, Pages 263-272

  Prosser, Megan E ^a   Brown, Christine E ^a   Shami, Andrew F ^a   Forman, Stephen J ^a   Jensen, Michael C ^a,b,c  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

Adoptive T cell therapy; Costimulation; Programmed death 1 (PD 1) receptor

Indexed keywords

CD28 ANTIGEN; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON ANTIBODY; GRANZYME B; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ARTICLE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL SURFACE; CHIMERA; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ADOPTIVE TRANSFER; ANTIGENS, CD274; ANTIGENS, CD28; CD8-POSITIVE T-LYMPHOCYTES; CELL GROWTH PROCESSES; CELL LINE; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GRANZYMES; HUMANS; IMMUNOSUPPRESSION; LEUKOCYTES, MONONUCLEAR; LIGANDS; LYMPHOCYTE ACTIVATION; MUROMONAB-CD3; PHOSPHORYLATION; PROGRAMMED CELL DEATH 1 RECEPTOR; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84861224393     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.03.023     Document Type: Article

References (44)

1. Ahmadzadeh M., Johnson L.A., Heemskerk B., Wunderlich J.R., Dudley M.E., White D.E., Rosenberg S.A. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009, 114:1537-1544.
2. Anderson R.C., Anderson D.E., Elder J.B., Brown M.D., Mandigo C.E., Parsa A.T., Goodman R.R., McKhann G.M., Sisti M.B., Bruce J.N. Lack of B7 expression, not human leukocyte antigen expression, facilitates immune evasion by human malignant gliomas. Neurosurgery 2007, 60:1129-1136. (Discussion 1136).
3. Brown R.D., Pope B., Yuen E., Gibson J., Joshua D.E. The expression of T cell related costimulatory molecules in multiple myeloma. Leuk Lymphoma 1998, 31:379-384.
4. Carter L., Fouser L.A., Jussif J., Fitz L., Deng B., Wood C.R., Collins M., Honjo T., Freeman G.J., 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. 2002, 32:634-643.
5. Chinnasamy D., Chinnasamy N., Enriquez M.J., Otsu M., Morgan R.A., Candotti F. Lentiviral-mediated gene transfer into human lymphocytes: role of HIV-1 accessory proteins. Blood 2000, 96:1309-1316.
6. Denfeld R.W., Dietrich A., Wuttig C., Tanczos E., Weiss J.M., Vanscheidt W., Schopf E., Simon J.C. In situ expression of B7 and CD28 receptor families in human malignant melanoma: relevance for T-cell-mediated anti-tumor immunity. Int. J. Cancer 1995, 62:259-265.
7. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., Roche P.C., Lu J., Zhu G., Tamada K., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 2002, 8:793-800.
8. Dong H., Zhu G., Tamada K., Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat. Med. 1999, 5:1365-1369.
9. Freeman G.J., Long A.J., Iwai Y., Bourque K., Chernova T., Nishimura H., Fitz L.J., Malenkovich N., Okazaki T., Byrne M.C., et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 2000, 192:1027-1034.
10. Freeman G.J., Wherry E.J., Ahmed R., Sharpe A.H. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J. Exp. Med. 2006, 203:2223-2227.
11. Gajewski T.F., Meng Y., Blank C., Brown I., Kacha A., Kline J., Harlin H. Immune resistance orchestrated by the tumor microenvironment. Immunol. Rev. 2006, 213:131-145.
12. Gajewski T.F., Meng Y., Harlin H. Immune suppression in the tumor microenvironment. J. Immunother. 2006, 29:233-240.
13. Geppert T.D., Lipsky P.E. Accessory cell independent proliferation of human T4 cells stimulated by immobilized monoclonal antibodies to CD3. J. Immunol. 1987, 138:1660-1666.
14. Geppert T.D., Lipsky P.E. Activation of T lymphocytes by immobilized monoclonal antibodies to CD3. Regulatory influences of monoclonal antibodies to additional T cell surface determinants. J. Clin. Invest. 1988, 81:1497-1505.
15. Ghebeh H., Mohammed S., Al-Omair A., Qattan A., Lehe C., Al-Qudaihi G., Elkum N., Alshabanah M., Bin Amer S., Tulbah A., et al. The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors. Neoplasia 2006, 8:190-198.
16. Groh V., Wu J., Yee C., Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002, 419:734-738.
17. Hamanishi J., Mandai M., Iwasaki M., Okazaki T., Tanaka Y., Yamaguchi K., Higuchi T., Yagi H., Takakura K., Minato N., et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3360-3365.
18. Harding F.A., McArthur J.G., Gross J.A., Raulet D.H., Allison J.P. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 1992, 356:607-609.
19. Hino R., Kabashima K., Kato Y., Yagi H., Nakamura M., Honjo T., Okazaki T., Tokura Y. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 2010, 116:1757-1766.
20. Hirano F., Kaneko K., Tamura H., Dong H., Wang S., Ichikawa M., Rietz C., Flies D.B., Lau J.S., Zhu G., et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 2005, 65:1089-1096.
21. Ito T., Ueno T., Clarkson M.R., Yuan X., Jurewicz M.M., Yagita H., Azuma M., Sharpe A.H., Auchincloss H., Sayegh M.H., et al. Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8 T cell-mediated alloimmune responses in vivo. J. Immunol. 2005, 174:6648-6656.
22. Iwai Y., Ishida M., Tanaka Y., Okazaki T., Honjo T., Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:12293-12297.
23. Jensen M.C., Clarke P., Tan G., Wright C., Chung-Chang W., Clark T.N., Zhang F., Slovak M.L., Wu A.M., Forman S.J., et al. Human T lymphocyte genetic modification with naked DNA. J. Mol. Ther. 2000, 1:49-55.
24. Kowolik C.M., Topp M.S., Gonzalez S., Pfeiffer T., Olivares S., Gonzalez N., Smith D.D., Forman S.J., Jensen M.C., Cooper L.J. CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res. 2006, 66:10995-11004.
25. Levine B.L., Bernstein W.B., Connors M., Craighead N., Lindsten T., Thompson C.B., June C.H. Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells. J. Immunol. 1997, 159:5921-5930.
26. Luxembourg A.T., Brunmark A., Kong Y., Jackson M.R., Peterson P.A., Sprent J., Cai Z. Requirements for stimulating naive CD8+ T cells via signal 1 alone. J. Immunol. 1998, 161:5226-5235.
27. Menke J., Lucas J.A., Zeller G.C., Keir M.E., Huang X.R., Tsuboi N., Mayadas T.N., Lan H.Y., Sharpe A.H., Kelley V.R. Programmed death 1 ligand (PD-L) 1 and PD-L2 limit autoimmune kidney disease: distinct roles. J. Immunol. 2007, 179:7466-7477.
28. Milone M.C., Fish J.D., Carpenito C., Carroll R.G., Binder G.K., Teachey D., Samanta M., Lakhal M., Gloss B., Danet-Desnoyers G., et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 2009, 17:1453-1464.
29. Nomi T., Sho M., Akahori T., Hamada K., Kubo A., Kanehiro H., Nakamura S., Enomoto K., Yagita H., Azuma M., et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin. Cancer Res. 2007, 13:2151-2157.
30. Parry R.V., Chemnitz J.M., Frauwirth K.A., Lanfranco A.R., Braunstein I., Kobayashi S.V., Linsley P.S., Thompson C.B., Riley J.L. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell Biol. 2005, 25:9543-9553.
31. Rajasekaran K., Xiong V., Fong L., Gorski J., Malarkannan S. Functional dichotomy between NKG2D and CD28-mediated co-stimulation in human CD8+ T cells. PLoS One 2010, 5.
32. Sheppard K.A., Fitz L.J., Lee J.M., Benander C., George J.A., Wooters J., Qiu Y., Jussif J.M., Carter L.L., Wood C.R., et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett. 2004, 574:37-41.
33. Stastny M.J., Brown C.E., Ruel C., Jensen M.C. Medulloblastomas expressing IL13Ralpha2 are targets for IL13-zetakine+ cytolytic T cells. J. Pediatr. Hematol. Oncol. 2007, 29:669-677.
34. Strome S.E., Dong H., Tamura H., Voss S.G., Flies D.B., Tamada K., Salomao D., Cheville J., Hirano F., Lin W., et al. B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 2003, 63:6501-6505.
35. Tatsumi T., Takehara T., Katayama K., Mochizuki K., Yamamoto M., Kanto T., Sasaki Y., Kasahara A., Hayashi N. Expression of costimulatory molecules B7-1 (CD80) and B7-2 (CD86) on human hepatocellular carcinoma. Hepatology (Baltimore, Md) 1997, 25:1108-1114.
36. Thompson R.H., Kuntz S.M., Leibovich B.C., Dong H., Lohse C.M., Webster W.S., Sengupta S., Frank I., Parker A.S., Zincke H., et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006, 66:3381-3385.
37. Topp M.S., Riddell S.R., Akatsuka Y., Jensen M.C., Blattman J.N., Greenberg P.D. Restoration of CD28 expression in CD28- CD8+ memory effector T cells reconstitutes antigen-induced IL-2 production. J. Exp. Med. 2003, 198:947-955.
38. Townsend S.E., Allison J.P. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science 1993, 259:368-370.
39. Wang J., Yoshida T., Nakaki F., Hiai H., Okazaki T., Honjo T. Establishment of NOD-Pdcd1-/- mice as an efficient animal model of type I diabetes. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:11823-11828.
40. Ward S.G. CD28: a signalling perspective. Biochem. J. 1996, 318(Pt 2):361-377.
41. Wintterle S., Schreiner B., Mitsdoerffer M., Schneider D., Chen L., Meyermann R., Weller M., Wiendl H. Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis. Cancer Res. 2003, 63:7462-7467.
42. Yam P.Y., Li S., Wu J., Hu J., Zaia J.A., Yee J.K. Design of HIV vectors for efficient gene delivery into human hematopoietic cells. Mol. Ther. 2002, 5:479-484.
43. Young J.R., Davison T.F., Tregaskes C.A., Rennie M.C., Vainio O. Monomeric homologue of mammalian CD28 is expressed on chicken T cells. J. Immunol. 1994, 152:3848-3851.
44. Zhong X.S., Matsushita M., Plotkin J., Riviere I., Sadelain M. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol. Ther. 2010, 18:413-420.