TCR-engineered T cells to treat tumors: Seeing but not touching?

Seminars in Immunology

Volumn 28, Issue 1, 2016, Pages 10-21

  Debets, Reno ^a   Donnadieu, Emmanuel ^b,c,d   Chouaib, Salem ^e   Coukos, George ^f  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b INSTITUT COCHIN   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Equipe Labellisée Par la Ligue Nationale Contre le Cancer 20112013   (France)

^e INSERM   (France)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Antigen recognition; Immune evasion; T cell; T cell receptor; T cell trafficking; Tumor micro environment

Indexed keywords

T LYMPHOCYTE RECEPTOR; CANCER VACCINE; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ADOPTIVE TRANSFER; BIOACCUMULATION; CANCER GENE THERAPY; CANCER TISSUE; CELL MIGRATION; FEASIBILITY STUDY; GENETIC ENGINEERING; GENETIC ENHANCEMENT; HUMAN; IMMUNE RESPONSE; INTRACELLULAR TRANSPORT; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; REVIEW; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; ADOPTIVE IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL MOTION; GENE THERAPY; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; PROCEDURES; TRANSPLANTATION;

ANTIGENS, NEOPLASM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; GENETIC THERAPY; HUMANS; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; TUMOR MICROENVIRONMENT;

EID: 84961219467     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2016.03.002     Document Type: Review

References (152)

1. van der Bruggen P., Traversari C., Chomez P., Lurquin C., De Plaen E., Van den Eynde B., et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991, 254:1643-1647.
2. Straetemans T., Berrevoets C., Coccoris M., Treffers-Westerlaken E., Wijers R., Cole D.K., et al. Recurrence of melanoma following T cell treatment: continued antigen expression in a tumor that evades T cell recruitment. Mol. Ther. 2015, 23:396-406.
3. Rahir G., Moser M. Tumor microenvironment and lymphocyte infiltration. Cancer Immunol. Immunother.: CII 2012, 61:751-759.
4. Joyce J.A., Fearon D.T. T cell exclusion, immune privilege, and the tumor microenvironment. Science 2015, 348:74-80.
5. van Rooij N., van Buuren M.M., Philips D., Velds A., Toebes M., Heemskerk B., et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. 2013, 31:e439-442.
6. Robbins P.F., Lu Y.C., El-Gamil M., Li Y.F., Gross C., Gartner J., et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 2013, 19:747-752.
7. Brown S.D., Warren R.L., Gibb E.A., Martin S.D., Spinelli J.J., Nelson B.H., et al. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014, 24:743-750.
8. Cherkasova E., Weisman Q., Childs R.W. Endogenous retroviruses as targets for antitumor immunity in renal cell cancer and other tumors. Front. Oncol. 2013, 3:243.
9. Hong J.A., Kang Y., Abdullaev Z., Flanagan P.T., Pack S.D., Fischette M.R., et al. Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells. Cancer Res. 2005, 65:7763-7774.
10. Klenova E.M., Morse H.C., Ohlsson R., Lobanenkov V.V. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol. 2002, 12:399-414.
11. Loukinov D.I., Pugacheva E., Vatolin S., Pack S.D., Moon H., Chernukhin I., et al. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6806-6811.
12. Lurquin C., Lethe B., De Plaen E., Corbiere V., Theate I., van Baren N., et al. Contrasting frequencies of antitumor and anti-vaccine T cells in metastases of a melanoma patient vaccinated with a MAGE tumor antigen. J. Exp. Med. 2005, 201:249-257.
13. Lu Y.C., Yao X., Crystal J.S., Li Y.F., El-Gamil M., Gross C., et al. Efficient identification of mutated cancer antigens recognized by T cells associated with durable tumor regressions. Clin. Cancer Res. 2014, 20:3401-3410.
14. Tran E., Turcotte S., Gros A., Robbins P.F., Lu Y.C., Dudley M.E., et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 2014, 344:641-645.
15. Heemskerk B., Kvistborg P., Schumacher T.N. The cancer antigenome. EMBO J. 2013, 32:194-203.
16. Angelova M., Charoentong P., Hackl H., Fischer M.L., Snajder R., Krogsdam A.M., et al. Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy. Genome Biol. 2015, 16:64.
17. Mesri E.A., Feitelson M.A., Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe 2014, 15:266-282.
18. Caballero O.L., Chen Y.T. Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci. 2009, 100:2014-2021.
19. Yang B., O'Herrin S.M., Wu J., Reagan-Shaw S., Ma Y., Bhat K.M., et al. MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res. 2007, 67:9954-9962.
20. Doyle J.M., Gao J., Wang J., Yang M., Potts P.R. MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 2010, 39:963-974.
21. Nardiello T., Jungbluth A.A., Mei A., Diliberto M., Huang X., Dabrowski A., et al. MAGE-A inhibits apoptosis in proliferating myeloma cells through repression of Bax and maintenance of survivin. Clin. Cancer Res. 2011, 17:4309-4319.
22. Liu W., Cheng S., Asa S.L., Ezzat S. The melanoma-associated antigen A3 mediates fibronectin-controlled cancer progression and metastasis. Cancer Res. 2008, 68:8104-8112.
23. Yang F., Zhou X., Miao X., Zhang T., Hang X., Tie R., et al. MAGEC2, an epithelial-mesenchymal transition inducer, is associated with breast cancer metastasis. Breast Cancer Res. Treat. 2014, 145:23-32.
24. Snyder A., Makarov V., Merghoub T., Yuan J., Zaretsky J.M., Desrichard A., et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 2014, 371:2189-2199.
25. Rizvi N.A., Hellmann M.D., Snyder A., Kvistborg P., Makarov V., Havel J.J., et al. Cancer immunology: mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015, 348:124-128.
26. Maby P., Tougeron D., Hamieh M., Mlecnik B., Kora H., Bindea G., et al. Correlation between density of CD8+ T-cell infiltrate in microsatellite unstable colorectal cancers and frameshift mutations: a rationale for personalized immunotherapy. Cancer Res. 2015, 75:3446-3455.
27. Leisegang M., Kammertoens T., Uckert W., Blankenstein T. Targeting human melanoma neoantigens by T cell receptor gene therapy. J. Clin. Invest. 2016.
28. Feig C., Jones J.O., Kraman M., Wells R.J., Deonarine A., Chan D.S., et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:20212-20217.
29. Draper L.M., Kwong M.L., Gros A., Stevanovic S., Tran E., Kerkar S., et al. Targeting of HPV-16+ epithelial cancer cells by TCR gene engineered t cells directed against E6. Clin. Cancer Res. 2015, 21:4431-4439.
30. Covre A., Coral S., Di Giacomo A.M., Taverna P., Azab M., Maio M. Epigenetics meets immune checkpoints. Semin. Oncol. 2015, 42:506-513.
31. Weintraub K. Take two: combining immunotherapy with epigenetic drugs to tackle cancer. Nat. Med. 2016, 22:8-10.
32. Chou J., Voong L.N., Mortales C.L., Towlerton A.M., Pollack S.M., Chen X., et al. Epigenetic modulation to enable antigen-specific T-cell therapy of colorectal cancer. J. Immunother. 2012, 35:131-141.
33. Pollack S.M., Li Y., Blaisdell M.J., Farrar E.A., Chou J., Hoch B.L., et al. NYESO-1/LAGE-1s and PRAME are targets for antigen specific T cells in chondrosarcoma following treatment with 5-Aza-2-deoxycitabine. PLoS One 2012, 7:e32165.
34. Chiappinelli K.B., Strissel P.L., Desrichard A., Li H., Henke C., Akman B., et al.Inhibiting D.N.A. Methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell 2015, 162:974-986.
35. Coral S., Covre A., Nicolay H.J., Parisi G., Rizzo A., Colizzi F., et al. Epigenetic remodelling of gene expression profiles of neoplastic and normal tissues: immunotherapeutic implications. Br. J. Cancer 2012, 107:1116-1124.
36. Goodyear O., Agathanggelou A., Novitzky-Basso I., Siddique S., McSkeane T., Ryan G., et al. Induction of a CD8+ T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood 2010, 116:1908-1918.
37. Issa J.P., Roboz G., Rizzieri D., Jabbour E., Stock W., O'Connell C., et al. Safety and tolerability of guadecitabine (SGI-110) in patients with myelodysplastic syndrome and acute myeloid leukaemia: a multicentre, randomised, Dose-escalation phase 1 study. Lancet Oncol. 2015, 16:1099-1110.
38. Kunert AvS-L S., van Brakel M., da Silva M., Coulie P., Lamers C., Sleijfer S., Debets R. MAGE-C2 specific TCRs, in combination with epigenetic drug treatment of taget cells, yield tumor-selective therapeutic T cells. J. Immunol. 2016, (in press).
39. Engels B., Engelhard V.H., Sidney J., Sette A., Binder D.C., Liu R.B., et al. Relapse or eradication of cancer is predicted by peptide-major histocompatibility complex affinity. Cancer Cell 2013, 23:516-526.
40. Schietinger A., Philip M., Liu R.B., Schreiber K., Schreiber H. Bystander killing of cancer requires the cooperation of CD4(+) and CD8(+) T cells during the effector phase. J. Exp. Med. 2010, 207:2469-2477.
41. Pulido J., Kottke T., Thompson J., Galivo F., Wongthida P., Diaz R.M., et al. Using virally expressed melanoma cDNA libraries to identify tumor-associated antigens that cure melanoma. Nat. Biotechnol. 2012, 30:337-343.
42. Gure A.O., Chua R., Williamson B., Gonen M., Ferrera C.A., Gnjatic S., et al. Cancer-testis genes are coordinately expressed and are markers of poor outcome in non-small cell lung cancer. Clin. Cancer Res. 2005, 11:8055-8062.
43. Sadovnikova E., Jopling L.A., Soo K.S., Stauss H.J. Generation of human tumor-reactive cytotoxic T cells against peptides presented by non-self HLA class I molecules. Eur. J. Immunol. 1998, 28:193-200.
44. Butler M.O., Friedlander P., Milstein M.I., Mooney M.M., Metzler G., Murray A.P., et al. Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Sci. Transl. Med. 2011, 3:80ra34.
45. Li L.P., Lampert J.C., Chen X., Leitao C., Popovic J., Muller W., et al. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat. Med. 2010, 16:1029-1034.
46. Obenaus M., Leitao C., Leisegang M., Chen X., Gavvovidis I., van der Bruggen P., et al. Identification of human T-cell receptors with optimal affinity to cancer antigens using antigen-negative humanized mice. Nat. Biotechnol. 2015, 33:402-407.
47. Straetemans T., van Brakel M., van Steenbergen S., Broertjes M., Drexhage J., Hegmans J., et al. TCR gene transfer: mAGE-C2/HLA-A2 and MAGE-A3/HLA-DP4 epitopes as melanoma-specific immune targets. Clin. Dev. Immunol. 2012, 2012:586314.
48. Turchaninova M.A., Britanova O.V., Bolotin D.A., Shugay M., Putintseva E.V., Staroverov D.B., et al. Pairing of T-cell receptor chains via emulsion PCR. Eur. J. Immunol. 2013, 43:2507-2515.
49. Linnemann C., Heemskerk B., Kvistborg P., Kluin R.J., Bolotin D.A., Chen X., et al. High-throughput identification of antigen-specific TCRs by TCR gene capture. Nat. Med. 2013, 19:1534-1541.
50. Howie B., Sherwood A.M., Berkebile A.D., Berka J., Emerson R.O., Williamson D.W., et al. High-throughput pairing of T cell receptor alpha and beta sequences. Sci. Transl. Med. 2015, 7:301ra131.
51. Coccoris M., Straetemans T., Govers C., Lamers C., Sleijfer S., Debets R. T cell receptor (TCR) gene therapy to treat melanoma: lessons from clinical and preclinical studies. Expert Opin. Biol. Ther. 2010, 10:547-562.
52. Gilham D.E., Debets R., Pule M., Hawkins R.E., Abken H. CAR-T cells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol. Med. 2012, 18:377-384.
53. Kunert A., Straetemans T., Govers C., Lamers C., Mathijssen R., Sleijfer S., et al.T.C.R-Engineered T. Cells meet new challenges to treat solid tumors: choice of antigen, t cell fitness, and sensitization of tumor milieu. Front. Immunol. 2013, 4:363.
54. Govers C., Sebestyen Z., Coccoris M., Willemsen R.A., Debets R. T cell receptor gene therapy: strategies for optimizing transgenic TCR pairing. Trends Mol. Med. 2010, 16:77-87.
55. Robbins P.F., Li Y.F., El-Gamil M., Zhao Y., Wargo J.A., Zheng Z., et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J. Immunol. 2008, 180:6116-6131.
56. Li Y., Moysey R., Molloy P.E., Vuidepot A.L., Mahon T., Baston E., et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat. Biotechnol. 2005, 23:349-354.
57. Holler P.D., Chlewicki L.K., Kranz D.M. TCRs with high affinity for foreign pMHC show self-reactivity. Nat. Immunol. 2003, 4:55-62.
58. Raman M.C., Rizkallah P.J., Simmons R., Donnellan Z., Dukes J., Bossi G., et al. Direct molecular mimicry enables off-target cardiovascular toxicity by an enhanced affinity TCR designed for cancer immunotherapy. Sci. Rep. 2016, 6:18851.
59. Schmid D.A., Irving M.B., Posevitz V., Hebeisen M., Posevitz-Fejfar A., Sarria J.C., et al. Evidence for a TCR affinity threshold delimiting maximal CD8 T cell function. J. Immunol. 2010, 184:4936-4946.
60. Thomas S., Xue S.A., Bangham C.R., Jakobsen B.K., Morris E.C., Stauss H.J., Human T. cells expressing affinity-matured TCR display accelerated responses but fail to recognize low density of MHC-peptide antigen. Blood 2011, 118:319-329.
61. Hebeisen M., Baitsch L., Presotto D., Baumgaertner P., Romero P., Michielin O., et al. SHP-1 phosphatase activity counteracts increased T cell receptor affinity. J. Clin. Invest. 2013, 123:1044-1056.
62. Porter D.L., Levine B.L., Kalos M., Bagg A., June C.H. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 2011, 365:725-733.
63. Brentjens R.J., Riviere I., Park J.H., Davila M.L., Wang X., Stefanski J., et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 2011, 118:4817-4828.
64. Kochenderfer J.N., Dudley M.E., Feldman S.A., Wilson W.H., Spaner D.E., Maric I., et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 2012, 119:2709-2720.
65. Schaft N., Lankiewicz B., Drexhage J., Berrevoets C., Moss D.J., Levitsky V., et al. T cell re-targeting to EBV antigens following TCR gene transfer: cD28-containing receptors mediate enhanced antigen-specific IFNgamma production. Int. Immunol. 2006, 18:591-601.
66. Govers C., Sebestyen Z., Roszik J., van Brakel M., Berrevoets C., Szoor A., et al. TCRs genetically linked to CD28 and CD3epsilon do not mispair with endogenous TCR chains and mediate enhanced T cell persistence and anti-melanoma activity. J. Immunol. 2014, 193:5315-5326.
67. Straetemans T., Coccoris M., Berrevoets C., Treffers-Westerlaken E., Scholten C.E., Schipper D., et al. T-cell receptor gene therapy in human melanoma-bearing immune-deficient mice: human but not mouse T cells recapitulate outcome of clinical studies. Hum. Gene Ther. 2012, 23:187-201.
68. Cameron B.J., Gerry A.B., Dukes J., Harper J.V., Kannan V., Bianchi F.C., et al. Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci. Transl. Med. 2013, 5:197ra103.
69. Morgan R.A., Chinnasamy N., Abate-Daga D., Gros A., Robbins P.F., Zheng Z., et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J. Immunother. 2013, 36:133-151.
70. Bindea G., Mlecnik B., Tosolini M., Kirilovsky A., Waldner M., Obenauf A.C., et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013, 39:782-795.
71. Zhang L., Conejo-Garcia J.R., Katsaros D., Gimotty P.A., Massobrio M., Regnani G., et al.Intratumoral T. cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 2003, 348:203-213.
72. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pages C., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-1964.
73. Liu N.Q., Stingl C., Look M.P., Smid M., Braakman R.B., De Marchi T., et al. Comparative proteome analysis revealing an 11-protein signature for aggressive triple-negative breast cancer. J. Natl. Cancer Inst. 2014, 106:djt376.
74. Spivey T.L., Uccellini L., Ascierto M.L., Zoppoli G., De Giorgi V., Delogu L.G., et al. Gene expression profiling in acute allograft rejection: challenging the immunologic constant of rejection hypothesis. J. Transl. Med. 2011, 9:174.
75. Harlin H., Meng Y., Peterson A.C., Zha Y., Tretiakova M., Slingluff C., et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009, 69:3077-3085.
76. Herbst R.S., Soria J.C., Kowanetz M., Fine G.D., Hamid O., Gordon M.S., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014, 515:563-567.
77. Tumeh P.C., Harview C.L., Yearley J.H., Shintaku I.P., Taylor E.J., Robert L., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014, 515:568-571.
78. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314.
79. Mikucki M.E., Fisher D.T., Matsuzaki J., Skitzki J.J., Gaulin N.B., Muhitch J.B., et al. Non-redundant requirement for CXCR3 signalling during tumoricidal T-cell trafficking across tumour vascular checkpoints. Nat. Commun. 2015, 6:7458.
80. Charo J., Perez C., Buschow C., Jukica A., Czeh M., Blankenstein T. Visualizing the dynamic of adoptively transferred T cells during the rejection of large established tumors. Eur. J. Immunol. 2011, 41:3187-3197.
81. David R., Ma L., Ivetic A., Takesono A., Ridley A.J., Chai J.G., et al. T-cell receptor- and CD28-induced Vav1 activity is required for the accumulation of primed T cells into antigenic tissue. Blood 2009, 113:3696-3705.
82. Peng D., Kryczek I., Nagarsheth N., Zhao L., Wei S., Wang W., et al. Epigenetic silencing of TH1-type chemokines shapes tumour immunity and immunotherapy. Nature 2015, 527:249-253.
83. Molon B., Ugel S., Del Pozzo F., Soldani C., Zilio S., Avella D., et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J. Exp. Med. 2011, 208:1949-1962.
84. Barreira da Silva R., Laird M.E., Yatim N., Fiette L., Ingersoll M.A., Albert M.L. Dipeptidylpeptidase 4 inhibition enhances lymphocyte trafficking, improving both naturally occurring tumor immunity and immunotherapy. Nat. Immunol. 2015, 16:850-858.
85. Nakahara S., Raz A. Biological modulation by lectins and their ligands in tumor progression and metastasis. Anticancer Agents Med. Chem. 2008, 8:22-36.
86. Romanska H.M., Berditchevski F. Tetraspanins in human epithelial malignancies. J. Pathol. 2011, 223:4-14.
87. Buckanovich R.J., Facciabene A., Kim S., Benencia F., Sasaroli D., Balint K., et al. B Endothelin receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat. Med. 2008, 14:28-36.
88. Motz G.T., Coukos G. Deciphering and reversing tumor immune suppression. Immunity 2013, 39:61-73.
89. Zang X., Sullivan P.S., Soslow R.A., Waitz R., Reuter V.E., Wilton A., et al. Tumor associated endothelial expression of B7-H3 predicts survival in ovarian carcinomas. Mod. Pathol. 2010, 23:1104-1112.
90. Motz G.T., Santoro S.P., Wang L.P., Garrabrant T., Lastra R.R., Hagemann I.S., et al. Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors. Nat. Med. 2014, 20:607-615.
91. Sato E., Olson S.H., Ahn J., Bundy B., Nishikawa H., Qian F., et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18538-18543.
92. Salmon H., Franciszkiewicz K., Damotte D., Dieu-Nosjean M.C., Validire P., Trautmann A., et al. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J. Clin. Invest. 2012, 122:899-910.
93. Fearon D.T. The carcinoma-associated fibroblast expressing fibroblast activation protein and escape from immune surveillance. Cancer Immunol. Res. 2014, 2:187-193.
94. Turley S.J., Cremasco V., Astarita J.L. Immunological hallmarks of stromal cells in the tumour microenvironment. Nat. Rev. Immunol. 2015, 15:669-682.
95. Kraman M., Bambrough P.J., Arnold J.N., Roberts E.W., Magiera L., Jones J.O., et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010, 330:827-830.
96. Lu P., Weaver V.M., Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 2012, 196:395-406.
97. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
98. Bougherara H., Mansuet-Lupo A., Alifano M., Ngo C., Damotte D., Le Frere-Belda M.A., et al. Real-Time imaging of resident t cells in human lung and ovarian carcinomas reveals how different tumor microenvironments control t lymphocyte migration. Front. Immunol. 2015, 6:500.
99. Ene-Obong A., Clear A.J., Watt J., Wang J., Fatah R., Riches J.C., et al. Activated pancreatic stellate cells sequester CD8+ T cells to reduce their infiltration of the juxtatumoral compartment of pancreatic ductal adenocarcinoma. Gastroenterology 2013, 145:1121-1132.
100. Hartmann N., Giese N.A., Giese T., Poschke I., Offringa R., Werner J., et al. Prevailing role of contact guidance in intrastromal T-cell trapping in human pancreatic cancer. Clin. Cancer Res. 2014, 20:3422-3433.
101. Tan K.W., Evrard M., Tham M., Hong M., Huang C., Kato M., et al. Tumor stroma and chemokines control T-cell migration into melanoma following Temozolomide treatment. Oncoimmunology 2015, 4:e978709.
102. Zambirinis C.P., Levie E., Nguy S., Avanzi A., Barilla R., Xu Y., et al. TLR9 ligation in pancreatic stellate cells promotes tumorigenesis. J Exp. Med. 2015, 212:2077-2094.
103. Li X., Kostareli E., Suffner J., Garbi N., Hammerling G.J. Efficient Treg depletion induces T-cell infiltration and rejection of large tumors. Eur. J. Immunol. 2010, 40:3325-3335.
104. Lesokhin A.M., Hohl T.M., Kitano S., Cortez C., Hirschhorn-Cymerman D., Avogadri F., et al. Monocytic CCR2(+) myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell infiltration into the tumor microenvironment. Cancer Res. 2012, 72:876-886.
105. Boissonnas A., Licata F., Poupel L., Jacquelin S., Fetler L., Krumeich S., et al. CD8+ tumor-infiltrating T cells are trapped in the tumor-dendritic cell network. Neoplasia 2013, 15:85-94.
106. Engelhardt J.J., Boldajipour B., Beemiller P., Pandurangi P., Sorensen C., Werb Z., et al. Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells. Cancer Cell 2012, 21:402-417.
107. Noman M.Z., Hasmim M., Messai Y., Terry S., Kieda C., Janji B., et al. Hypoxia: a key player in antitumor immune response: a review in the theme: cellular responses to hypoxia. Am. J. Physiol. Cell Physiol. 2015, 309:C569-579.
108. Collet G., Lamerant-Fayel N., Tertil M., El Hafny-Rahbi B., Stepniewski J., Guichard A., et al. Hypoxia-regulated overexpression of soluble VEGFR2 controls angiogenesis and inhibits tumor growth. Mol. Cancer Ther. 2014, 13:165-178.
109. Hasmim M., Noman M.Z., Messai Y., Bordereaux D., Gros G., Baud V., et al. Cutting edge: hypoxia-induced Nanog favors the intratumoral infiltration of regulatory T cells and macrophages via direct regulation of TGF-beta1. J. Immunol. 2013, 191:5802-5806.
110. Gabrilovich D.I., Chen H.L., Girgis K.R., Cunningham H.T., Meny G.M., Nadaf S., et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 1996, 2:1096-1103.
111. Facciabene A., Peng X., Hagemann I.S., Balint K., Barchetti A., Wang L.P., et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 2011, 475:226-230.
112. Clambey E.T., McNamee E.N., Westrich J.A., Glover L.E., Campbell E.L., Jedlicka P., et al. Hypoxia-inducible factor-1 alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2784-2793.
113. Corzo C.A., Condamine T., Lu L., Cotter M.J., Youn J.I., Cheng P., et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 2010, 207:2439-2453.
114. Noman M.Z., Desantis G., Janji B., Hasmim M., Karray S., Dessen P., et al. PD-L1 is a novel direct target of HIF-1alpha, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J. Exp. Med. 2014, 211:781-790.
115. Grohmann U., Bronte V. Control of immune response by amino acid metabolism. Immunol. Rev. 2010, 236:243-264.
116. Uyttenhove C., Pilotte L., Theate I., Stroobant V., Colau D., Parmentier N., et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 2003, 9:1269-1274.
117. Rodriguez P.C., Hernandez C.P., Quiceno D., Dubinett S.M., Zabaleta J., Ochoa J.B., et al.Arginase I. in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med. 2005, 202:931-939.
118. Spranger S., Bao R., Gajewski T.F. Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity. Nature 2015, 523:231-235.
119. Peng W., Chen J.Q., Liu C., Malu S., Creasy C., Tetzlaff M.T., et al. Loss of PTEN promotes resistance to t cell-mediated immunotherapy. Cancer Discovery 2016, 6:202-216.
120. Hopewell E.L., Zhao W., Fulp W.J., Bronk C.C., Lopez A.S., Massengill M., et al. Lung tumor NF-kappaB signaling promotes T cell-mediated immune surveillance. J. Clin. Invest. 2013, 123:2509-2522.
121. Hong M., Puaux A.L., Huang C., Loumagne L., Tow C., Mackay C., et al. Chemotherapy induces intratumoral expression of chemokines in cutaneous melanoma, favoring T-cell infiltration and tumor control. Cancer Res. 2011, 71:6997-7009.
122. Kershaw M.H., Wang G., Westwood J.A., Pachynski R.K., Tiffany H.L., Marincola F.M., et al. Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2. Hum. Gene Ther. 2002, 13:1971-1980.
123. Craddock J.A., Lu A., Bear A., Pule M., Brenner M.K., Rooney C.M., et al. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J. Immunother. 2010, 33:780-788.
124. Moon E.K., Carpenito C., Sun J., Wang L.C., Kapoor V., Predina J., et al. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin. Cancer Res. 2011, 17:4719-4730.
125. Peranzoni E., Rivas-Caicedo A., Bougherara H., Salmon H., Donnadieu E. Positive and negative influence of the matrix architecture on antitumor immune surveillance. Cell. Mol. Life Sci: CMLS 2013, 70:4431-4448.
126. Schaefer C.J., Ruhrmund D.W., Pan L., Seiwert S.D., Kossen K. Antifibrotic activities of pirfenidone in animal models. Eur. Respir. Rev. 2011, 20:85-97.
127. Caruana I., Savoldo B., Hoyos V., Weber G., Liu H., Kim E.S., et al. Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes. Nat. Med. 2015, 21:524-529.
128. Roberts E.W., Deonarine A., Jones J.O., Denton A.E., Feig C., Lyons S.K., et al. Depletion of stromal cells expressing fibroblast activation protein-alpha from skeletal muscle and bone marrow results in cachexia and anemia. J Exp. Med. 2013, 210:1137-1151.
129. Tran E., Chinnasamy D., Yu Z., Morgan R.A., Lee C.C., Restifo N.P., et al. Immune targeting of fibroblast activation protein triggers recognition of multipotent bone marrow stromal cells and cachexia. J. Exp. Med. 2013, 210:1125-1135.
130. Makkouk A., Abdelnoor A.M. The potential use of Toll-like receptor (TLR) agonists and antagonists as prophylactic and/or therapeutic agents. Immunopharmacol. Immunotoxicol. 2009, 31:331-338.
131. Stromnes I.M., Schmitt T.M., Hulbert A., Brockenbrough J.S., Nguyen H.N., Cuevas C., et al. T cells engineered against a native antigen can surmount immunologic and physical barriers to treat pancreatic ductal adenocarcinoma. Cancer Cell 2015, 28:638-652.
132. Kieda C., El Hafny-Rahbi B., Collet G., Lamerant-Fayel N., Grillon C., Guichard A., et al. Stable tumor vessel normalization with pO(2) increase and endothelial PTEN activation by inositol trispyrophosphate brings novel tumor treatment. J. Mol. Med. 2013, 91:883-899.
133. Shrimali R.K., Yu Z., Theoret M.R., Chinnasamy D., Restifo N.P., Rosenberg S.A. Antiangiogenic agents can increase lymphocyte infiltration into tumor and enhance the effectiveness of adoptive immunotherapy of cancer. Cancer Res. 2010, 70:6171-6180.
134. Johansson A., Hamzah J., Payne C.J., Ganss R. Tumor-targeted TNFalpha stabilizes tumor vessels and enhances active immunotherapy. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7841-7846.
135. Chinnasamy D., Yu Z., Theoret M.R., Zhao Y., Shrimali R.K., Morgan R.A., et al. Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J. Clin. Invest. 2010, 120:3953-3968.
136. Chmielewski M., Kopecky C., Hombach A.A., Abken H. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively Muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res. 2011, 71:5697-5706.
137. Marabelle A., Kohrt H., Sagiv-Barfi I., Ajami B., Axtell R.C., Zhou G., et al. Depleting tumor-specific Tregs at a single site eradicates disseminated tumors. J. Clin. Invest. 2013, 123:2447-2463.
138. Sharma M.D., Hou D.Y., Liu Y., Koni P.A., Metz R., Chandler P., et al. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 2009, 113:6102-6111.
139. Kodumudi K.N., Weber A., Sarnaik A.A., Pilon-Thomas S. Blockade of myeloid-derived suppressor cells after induction of lymphopenia improves adoptive T cell therapy in a murine model of melanoma. J. Immunol. 2012, 189:5147-5154.
140. Zhang Q., Yang X., Pins M., Javonovic B., Kuzel T., Kim S.J., et al. Adoptive transfer of tumor-reactive transforming growth factor-beta-insensitive CD8+ T cells: eradication of autologous mouse prostate cancer. Cancer Res. 2005, 65:1761-1769.
141. Akhurst R.J., Hata A. Targeting the TGFbeta signalling pathway in disease. Nat. Rev. Drug Discovery 2012, 11:790-811.
142. Woo S.R., Corrales L., Gajewski T.F. The STING pathway and the T cell-inflamed tumor microenvironment. Trends Immunol. 2015, 36:250-256.
143. Morgan R.A., Dudley M.E., Wunderlich J.R., Hughes M.S., Yang J.C., Sherry R.M., et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006, 314:126-129.
144. Johnson L.A., Morgan R.A., Dudley M.E., Cassard L., Yang J.C., Hughes M.S., et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009, 114:535-546.
145. van den Berg J.H., Gomez-Eerland R., van de Wiel B., Hulshoff L., van den Broek D., Bins A., et al. Case report of a fatal serious adverse event upon administration of t cells transduced with a MART-1-specific T-cell receptor. Mol. Ther. 2015, 23:1541-1550.
146. Parkhurst M.R., Yang J.C., Langan R.C., Dudley M.E., Nathan D.A., Feldman S.A., et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 2011, 19:620-626.
147. Robbins P.F., Morgan R.A., Feldman S.A., Yang J.C., Sherry R.M., Dudley M.E., et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 2011, 29:917-924.
148. Robbins P.F., Kassim S.H., Tran T.L., Crystal J.S., Morgan R.A., Feldman S.A., et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin. Cancer Res. 2015, 21:1019-1027.
149. Rapoport A.P., Stadtmauer E.A., Binder-Scholl G.K., Goloubeva O., Vogl D.T., Lacey S.F., et al. NY-ESO-1-specific TCR-engineered T. cells mediate sustained antigen-specific antitumor effects in myeloma. Nat. Med. 2015, 21:914-921.
150. Linette G.P., Stadtmauer E.A., Maus M.V., Rapoport A.P., Levine B.L., Emery L., et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013, 122:863-871.
151. Chen L., Flies D.B. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 2013, 13:227-242.
152. Curnis F., Sacchi A., Borgna L., Magni F., Gasparri A., Corti A. Enhancement of tumor necrosis factor alpha antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat. Biotechnol. 2000, 18:1185-1190.