CAR T Cell Therapy for Solid Tumors

Annual Review of Medicine

Volumn 68, Issue , 2017, Pages 139-152

  Newick, Kheng ^a   O'Brien, Shaun ^a   Moon, Edmund ^a   Albelda, Steven M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Adoptive T cell transfer; Chimeric antigen receptor T cells; Immunotherapy; Tumor microenvironment

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; CYTOKINE; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL THERAPY; CLINICAL TRIAL; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SOLID TUMOR; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; ADOPTIVE IMMUNOTHERAPY; CELLULAR IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; NEOPLASM; PROCEDURES; TUMOR ASSOCIATED LEUKOCYTE;

ANTIGENS, NEOPLASM; HUMANS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 85009945297     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-062315-120245     Document Type: Article

References (77)

1. Topalian SL, Drake CG, Pardoll DM. 2015. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 27:450-61
2. Willemsen RA, Debets R, Hart E, et al. 2001. A phage display selected fab fragment with MHC class I-restricted specificity for MAGE-A1 allows for retargeting of primary human T lymphocytes. Gene Ther. 8:1601-8
3. Gill S, Maus MV, Porter DL. 2015. Chimeric antigen receptor T cell therapy: 25 years in the making. Blood Rev. 30:157-67
4. Fousek K, Ahmed N. 2015. The evolution of T-cell therapies for solid malignancies. Clin. Cancer Res. 21:3384-92
5. Louis CU, Savoldo B, Dotti G, et al. 2011. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118:6050-56
6. AhmedN, Brawley VS, Hegde M, et al. 2015. Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J. Clin. Oncol. 33:1688-96
7. Feng K, Guo Y, Dai H, et al. 2016. Chimeric antigen receptor-modified T cells for the immunotherapy of patients with EGFR-expressing advanced relapsed/refractory non-small cell lung cancer. Sci. China Life Sci. 59:468-7
8. Restifo NP, Dudley ME, Rosenberg SA. 2012. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12:269-81
9. Kenter GG, Welters MJ, Valentijn AR, et al. 2009. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361:1838-47
10. Johnson LA, Scholler J, Ohkuri T, et al. 2015. Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma. Sci. Transl. Med. 7:275-22
11. Morgan RA, Johnson LA, Davis JL, et al. 2012. Recognition of glioma stem cells by genetically modifiedT cells targeting EGFRvIII and development of adoptive cell therapy for glioma. Hum. Gene Ther. 23:1043-53
12. Wilkie S, Picco G, Foster J, et al. 2008. Retargeting of human T cells to tumor-associated MUC1: the evolution of a chimeric antigen receptor. J. Immunol. 180:4901-9
13. Chekmasova AA, RaoTD, Nikhamin Y, et al. 2010. Successful eradication of established peritoneal ovarian tumors in SCID-Beige mice following adoptive transfer of T cells genetically targeted to the MUC16 antigen. Clin. Cancer Res. 16:3594-606
14. Morello A, Sadelain M, Adusumilli PS. 2015. Mesothelin-targeted CARs: driving T cells to solid tumors. Cancer Discov. 6:133-46
15. Pastan I, Hassan R. 2014. Discovery ofmesothelin and exploiting it as a target for immunotherapy. Cancer Res. 74:2907-12
16. Chowdhury PS, Viner JL, Beers R, Pastan I. 1998. Isolation of a high-affinity stable single-chain Fv specific for mesothelin from DNA-immunized mice by phage display and construction of a recombinant immunotoxin with anti-tumor activity. PNAS 95:669-74
17. Lanitis E, Poussin M, Hagemann IS, et al. 2012. Redirected antitumor activity of primary human lymphocytes transduced with a fully human anti-mesothelin chimeric receptor. Mol. Ther. 20:633-43
18. Adusumilli PS, Cherkassky L, Villena-Vargas J, et al. 2014. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci. Transl. Med. 6:261-151
19. Morgan RA, Yang JC, KitanoM, et al. 2010. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol. Ther. 18:843-51
20. Lanitis E, Poussin M, Klattenhoff AW, et al. 2013. Chimeric antigen receptor T cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo. Cancer Immunol. Res. 1:43-53
21. Kloss CC, Condomines M, Cartellieri M, et al. 2013.combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat. Biotechnol. 31:71-75
22. Sampson JH, Choi BD, Sanchez-Perez L, et al. 2014. EGFRvIII mCAR-modified T-cell therapy cures mice with established intracerebral glioma and generates host immunity against tumor-antigen loss. Clin. Cancer Res. 20:972-84
23. Beatty GL, Haas AR, Maus MV, et al. 2014. Mesothelin-specific chimeric antigen receptor mRNA-engineeredTcells induce anti-tumor activity in solid malignancies. Cancer Immunol. Res. 2:112-20
24. Wilkie S, van Schalkwyk MC, Hobbs S, et al. 2012. Dual targeting of ErbB2 and MUC1 in breast cancer using chimeric antigen receptors engineered to provide complementary signaling. J. Clin. Immunol. 32:1059-70
25. Grada Z, Hegde M, Byrd T, et al. 2013. TanCAR: a novel bispecific chimeric antigen receptor for cancer immunotherapy. Mol. Ther. Nucleic Acids 2:e105
26. Wang LC, Lo A, Scholler J, et al. 2014. Targeting fibroblast activation protein in tumor stroma with chimeric antigen receptor T cells can inhibit tumor growth and augment host immunity without severe toxicity. Cancer Immunol. Res. 2:154-66
27. Chinnasamy D, Tran E, Yu Z, et al. 2013. Simultaneous targeting of tumor antigens and the tumor vasculature using T lymphocyte transfer synergize to induce regression of established tumors in mice. Cancer Res. 73:3371-80
28. ChmielewskiM, Hombach AA, AbkenH. 2014. Of CARs andTRUCKs: chimeric antigen receptor (CAR) T cells engineered with an inducible cytokine to modulate the tumor stroma. Immunol. Rev. 257:83-90
29. Zhang L, Morgan RA, Beane JD, et al. 2015. Tumor-infiltrating lymphocytes genetically engineered with an inducible gene encoding interleukin-12 for the immunotherapy of metastatic melanoma. Clin. Cancer Res. 21:2278-88
30. Pegram HJ, Lee JC, Hayman EG, et al. 2012. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 119:4133-41
31. Iwahori K, Kakarla S, Velasquez MP, et al. 2015. Engager T cells: a new class of antigen-specific T cells that redirect bystander T cells. Mol. Ther. 23:171-78
32. Compte M, Blanco B, Serrano F, et al. 2007. Inhibition of tumor growth in vivo by in situ secretion of bispecific anti-CEA × anti-CD3 diabodies from lentivirally transduced human lymphocytes. Cancer Gene Ther. 14:380-88
33. Curran KJ, Seinstra BA, Nikhamin Y, et al. 2015. Enhancing antitumor efficacy of chimeric antigen receptor T cells through constitutive CD40L expression. Mol. Ther. 23:769-78
34. Harlin H, Meng Y, Peterson AC, et al. 2009. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 69:3077-85
35. Craddock JA, Lu A, Bear A, et al. 2010. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J. Immunother. 33:780-88
36. Moon EK, Carpenito C, Sun J, et al. 2011. 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. 17:4719-30
37. Newick K, O'Brien S, Sun J, et al. 2016. Augmentation of CAR T cell trafficking and antitumor efficacy by blocking protein kinase A (PKA) localization. Cancer Immunol. Res. 4:541-51
38. Nishio N, Diaconu I, Liu H, et al. 2014. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res. 74:5195-205
39. VanSeggelen H, Hammill JA, Dvorkin-Gheva A, et al. 2015. T cells engineered with chimeric antigen receptors targeting NKG2D ligands display lethal toxicity in mice. Mol. Ther. 23:1600-10
40. Caruana I, Savoldo B, Hoyos V, et al. 2015. Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes. Nat. Med. 21:524-29
41. Zhang Y, Ertl HC. 2016. Starved and asphyxiated: How can CD8+ T cells within a tumor microenvironment prevent tumor progression Front. Immunol. 7:32
42. Hatfield SM, Kjaergaard J, Lukashev D, et al. 2015. Immunological mechanisms of the antitumor effects of supplemental oxygenation. Sci. Transl. Med. 7:277ra30
43. Fischer K, Hoffmann P, Voelkl S, et al. 2007. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 109:3812-19
44. Jacobs SR, Herman CE, Maciver NJ, et al. 2008. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 180:4476-86
45. HowieD, Waldmann H, Cobbold S. 2014. Nutrient sensing via mTOR in T cells maintains a tolerogenic microenvironment. Front. Immunol. 5:409
46. Ninomiya S, Narala N, Huye L, et al. 2015. Tumor indoleamine 2, 3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs. Blood 125:3905-16
47. Velica P, Zech M, Henson S, et al. 2015. Genetic regulation of fate decisions in therapeutic T cells to enhance tumor protection and memory formation. Cancer Res. 75:2641-52
48. SukumarM, Liu J, Ji Y, et al. 2013. Inhibiting glycolytic metabolism enhances CD8+ T cell memory and antitumor function. J. Clin. Investig. 123:4479-88
49. Goodwin JS, Bankhurst AD, Messner RP. 1977. Suppression of human T-cell mitogenesis by prostaglandin. Existence of a prostaglandin-producing suppressor cell. J. Exp. Med. 146:1719-34
50. Su Y, Huang X, Raskovalova T, et al. 2008. Cooperation of adenosine and prostaglandin E2 (PGE2) in amplification of cAMP-PKA signaling and immunosuppression. Cancer Immunol. Immunother. 57:1611-23
51. Oh SA, Li MO. 2013. TGF-beta: guardian of T cell function. J. Immunol. 191:3973-79
52. Massague J. 2008. TGFin cancer. Cell 134:215-30
53. Wallace A, Kapoor V, Sun J, et al. 2008. Transforming growth factor-beta receptor blockade augments the effectiveness of adoptive T-cell therapy of established solid cancers. Clin. Cancer Res. 14:3966-74
54. BollardCM, RossigC, CalongeMJ, et al. 2002. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 99:3179-87
55. Gabrilovich DI, Nagaraj S. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9:162-74
56. Mussai F, Egan S, Hunter S, et al. 2015. Neuroblastoma arginase activity creates an immunosuppressive microenvironment that impairs autologous and engineered immunity. Cancer Res. 75:3043-53
57. Burga RA, Thorn M, Point GR, et al. 2015. Liver myeloid-derived suppressor cells expand in response to liver metastases in mice and inhibit the anti-tumor efficacy of anti-CEA CAR-T. Cancer Immunol. Immunother. 64:817-29
58. Spear P, Barber A, Rynda-Apple A, Sentman CL. 2012. Chimeric antigen receptor T cells shape myeloid cell function within the tumor microenvironment through IFN-gamma and GM-CSF. J. Immunol. 188:6389-98
59. Sakaguchi S, Miyara M, Costantino CM, Hafler DA. 2010. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10:490-500
60. Zhou Q, Munger ME, Highfill SL, et al. 2010. Program death-1 signaling and regulatory T cells collaborate to resist the function of adoptively transferred cytotoxic T lymphocytes in advanced acute myeloid leukemia. Blood 116:2484-93
61. Liu Y, Wang L, Predina J, et al. 2013. Inhibition of p300 impairs Foxp3+ T regulatory cell function and promotes antitumor immunity. Nat. Med. 19:1173-77
62. Perna SK, Pagliara D, Mahendravada A, et al. 2014. Interleukin-7 mediates selective expansion of tumorredirected cytotoxic T lymphocytes (CTLs) without enhancement of regulatory T-cell inhibition. Clin. Cancer Res. 20:131-39
63. Yao X, Ahmadzadeh M, Lu YC, et al. 2012. Levels of peripheral CD4+FoxP3+ regulatory T cells are negatively associated with clinical response to adoptive immunotherapy of human cancer. Blood 119:5688-96
64. KoflerDM, ChmielewskiM, Rappl G, et al. 2011. CD28 costimulation impairs the efficacy of a redirected T-cell antitumor attack in the presence of regulatory T cells which can be overcome by preventing Lck activation. Mol. Ther. 19:760-67
65. Markley JC, Sadelain M. 2010. IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human T cell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood 115:3508-19
66. Finney HM, Akbar AN, Lawson AD. 2004. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCR zeta chain. J. Immunol. 172:104-13
67. Moon EK, Wang LC, Dolfi DV, et al. 2014. Multifactorial T-cell hypofunction that is reversible can limit the efficacy of chimeric antigen receptor-transduced human T cells in solid tumors. Clin. Cancer Res. 20:4262-73
68. John LB, Devaud C, DuongCP, et al. 2013. Anti-PD-1 antibody therapy potently enhances the eradication of established tumors by gene-modified T cells. Clin. Cancer Res. 19:5636-46
69. Moon EK, Ranganathan R, Eruslanov E, et al. 2016. Blockade of programmed death 1 augments the ability of human T cells engineered to target NY-ESO-1 to control tumor growth after adoptive transfer. Clin. Cancer Res. 22:436-47
70. Kobold S, Grassmann S, Chaloupka M, et al. 2015. Impact of a new fusion receptor on PD-1-mediated immunosuppression in adoptive T cell therapy. J. Natl. Cancer Inst. 107:djv146
71. Mahvi DA, Meyers JV, Tatar AJ, et al. 2015. CTLA-4 blockade plus adoptive T-cell transfer promotes optimal melanoma immunity in mice. J. Immunother. 38:54-61
72. Wang LC, Riese MJ, Moon EK, Albelda SM. 2013. Overcoming intrinsic inhibitory pathways to augment the antineoplastic activity of adoptively transferred T cells: re-tuning your CAR before hitting a rocky road. Oncoimmunology 2:e26492
73. Riese MJ, Wang LC, Moon EK, et al. 2013. Enhanced effector responses in activated CD8+ T cells deficient in diacylglycerol kinases. Cancer Res. 73:3566-77
74. Charo J, Finkelstein SE, Grewal N, et al. 2005. Bcl-2 overexpression enhances tumor-specific T-cell survival. Cancer Res. 65:2001-8
75. Guedan S, Chen X, Madar A, et al. 2014. ICOS-based chimeric antigen receptors program bipolar TH17/TH1 cells. Blood 124:1070-80
76. Song DG, Ye Q, PoussinM, et al. 2012. CD27 costimulation augments the survival and antitumor activity of redirected human T cells in vivo. Blood 119:696-706
77. Wang E, Wang LC, Tsai CY, et al. 2015. Generation of potent T-cell immunotherapy for cancer using DAP12-based, multichain, chimeric immunoreceptors. Cancer Immunol. Res. 3:815-26