Reduction of MDSCs with all-trans retinoic acid improves CAR therapy efficacy for sarcomas

Cancer Immunology Research

Volumn 4, Issue 10, 2016, Pages 869-880

  Long, Adrienne H ^a,b   Highfill, Steven L ^a   Cui, Yongzhi ^a   Smith, Jillian P ^a   Walker, Alec J ^a   Ramakrishna, Sneha ^a   El Etriby, Rana ^a   Galli, Susana ^a,d   Tsokos, Maria G ^a,e   Orentas, Rimas J ^a,f   Mackall, Crystal L ^a,c,g  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^f Lentigen Corporation   (United States)

^g STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CD28 ANTIGEN; ALPHA CD3 ANTIGEN; CD134 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD3 ZETA ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; GANGLIOSIDE GD2; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 8; RETINOIC ACID; UNCLASSIFIED DRUG; CD19-SPECIFIC CHIMERIC ANTIGEN RECEPTOR; GANGLIOSIDE; GANGLIOSIDE, GD2; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; EWING SARCOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NEUROBLASTOMA CELL LINE; NONHUMAN; OSTEOSARCOMA; PHENOTYPE; PROTEIN EXPRESSION; RHABDOMYOSARCOMA; SARCOMA CELL LINE; SUPPRESSOR CELL; TISSUE SECTION; TUMOR VOLUME; TUMOR XENOGRAFT; ADOPTIVE IMMUNOTHERAPY; ANIMAL; CHILD; DRUG EFFECTS; DRUG SCREENING; IMMUNOLOGY; METABOLISM; MULTIMODALITY CANCER THERAPY; MYELOID-DERIVED SUPPRESSOR CELL; NEUROBLASTOMA; NONOBESE DIABETIC MOUSE; PATHOLOGY; PROCEDURES; SARCOMA; T LYMPHOCYTE; TRANSPLANTATION; TREATMENT OUTCOME; TUMOR CELL CULTURE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHILD; COMBINED MODALITY THERAPY; GANGLIOSIDES; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE, INBRED NOD; MYELOID-DERIVED SUPPRESSOR CELLS; NEUROBLASTOMA; RECEPTORS, ANTIGEN, T-CELL; SARCOMA; T-LYMPHOCYTES; TREATMENT OUTCOME; TRETINOIN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84994083486     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0230     Document Type: Article

References (50)

1. Lee DW, Barrett DM, Mackall C, Orentas R, Grupp SA. The future is now: chimeric antigen receptors as new targeted therapies for childhood cancer. Clin Cancer Res 2012; 18: 2780-90.
2. Sadelain M, Brentjens R, Riviere I. The basic principles of chimeric antigen receptor design. Cancer Discov 2013; 3: 388-98.
3. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet 2015; 385: 517-28.
4. Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptorT cells for sustained remissions in leukemia. N Engl J Med 2014; 371: 1507-17.
5. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, 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: 2709-20.
6. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365: 725-33.
7. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 2013; 368: 1509-18.
8. Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest 2011; 121: 1822-6.
9. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013; 5: 177ra38.
10. Davila ML, Riviere I, Wang X, Bartido S, Park J, Curran K, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med 2014; 6: 224ra25.
11. Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006; 12: 6106-15.
12. Lamers CHJ, Sleijfer S, van Steenbergen S, van Elzakker P, van Krimpen B, Groot C, et al. Treatmentofmetastaticrenal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol Ther 2013; 21: 904-12.
13. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specific Tcells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008; 14: 1264-70.
14. Park JR, DiGiusto DL, Slovak M, Wright C, Naranjo A, Wagner J, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther 2007; 15: 825-33.
15. Long AH, Haso WM, Shern JF, Wanhainen KM, Murgai M, Ingaramo M, et al. 4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors. Nat Med 2015; 21: 581-90.
16. Gilham DE, Debets R, Pule M, Hawkins RE, Abken H. CAR-Tcells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol Med 2012; 18: 377-84.
17. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12: 253-68.
18. Arina A, Bronte V. Myeloid-derived suppressor cell impact on endogenous and adoptively transferred T cells. Curr Opin Immunol 2015; 33: 120-5.
19. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cellsas regulators of the immune system. Nat Rev Immunol 2009; 9: 162-74.
20. Ostrand-Rosenberg S. Myeloid-derived suppressor cells: moremechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 2010; 59: 1593-600.
21. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363: 1324-34.
22. Roth M, Linkowski M, Tarim J, Piperdi S, Sowers R, Geller D, et al. Ganglioside GD2 as a therapeutic target for antibody-mediated therapy in patients with osteosarcoma. Cancer 2014; 120: 548-54.
23. Kailayangiri S, Altvater B, Meltzer J, Pscherer S, Luecke A, Dierkes C, et al. The ganglioside antigen GD2 is surface-expressed in Ewing sarcoma and allows for MHC-independent immune targeting. Br J Cancer 2012; 106: 1123-33.
24. Suzuki M, Cheung N-KV. Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin Ther Targets 2015; 19: 349-62.
25. Yvon E, Del Vecchio M, Savoldo B, Hoyos V, Dutour A, Anichini A, et al. Immunotherapy of metastatic melanoma using genetically engineered GD2-specific T cells. Clin Cancer Res 2009; 15: 5852-60.
26. Gargett T, Brown MP. Different cytokine and stimulation conditions influence the expansion and immune phenotype of third-generation chimeric antigen receptor T cells specific for tumor antigen GD2. Cytotherapy 2015; 17: 487-95.
27. Gargett T, Fraser CK, Dotti G, Yvon ES, Brown MP. BRAF and MEK inhibition variably affect GD2-specific chimeric antigen receptor (CAR) T-cell function in vitro. J Immunother 2015; 38: 12-23.
28. Pule MA, Straathof KC, Dotti G, Heslop HE, Rooney CM, Brenner MK. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther 2005; 12: 933-41.
29. Martin CE, van Leeuwen EMM, Im SJ, Roopenian DC, Sung Y-C, Surh CD. IL-7/anti-IL-7 mAb complexes augment cytokine potency in mice through association with IgG-Fc and by competition with IL-7R. Blood 2013; 121: 4484-92.
30. Highfill SL, Cui Y, Giles AJ, Smith JP, Zhang H, Morse E, et al. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci Transl Med 2014; 6: 237ra67.
31. Bronte V, Apolloni E, Cabrelle A, Ronca R, Serafini P, Zamboni P, et al. Identification of a CD11b+/Gr-1+/CD31+ myeloid progenitor capable of activating or suppressing CD8+T cells. Blood 2000; 96: 3838-46.
32. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009; 182: 4499-506.
33. Talmadge JE, Gabrilovich DI. History of myeloid-derived suppressor cells. Nat Rev Cancer 2013; 13: 739-52.
34. Kusmartsev S, Cheng F, Yu B, Nefedova Y, Sotomayor E, Lush R, et al. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res 2003; 63: 4441-9.
35. Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, et al. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res 2006; 66: 9299-307.
36. Iclozan C, Antonia S, Chiappori A, Chen D-T, Gabrilovich D. Therapeutic regulation of myeloid-derived suppressor cells and immune response to cancer vaccine in patients with extensive stage small cell lung cancer. Cancer Immunol Immunother 2013; 62: 909-18.
37. Lu L, Lan Q, Li Z, Zhou X, Gu J, Li Q, et al. Critical role of all-trans retinoic acid in stabilizing human natural regulatory T cells under inflammatory conditions. Proc Natl Acad Sci 2014; 111: E3432-40.
38. Golovina TN, Mikheeva T, Brusko TM, Blazar BR, Bluestone JA, Riley JL. Retinoic acid and rapamycin differentially affect and synergistically promote the Ex Vivo expansion of natural human T regulatory cells. PLoS One 2011; 6: e15868.
39. Poon VI, Roth M, Piperdi S, Geller D, Gill J, Rudzinski ER, et al. Ganglioside GD2 expression is maintained upon recurrence in patients with osteosarcoma. Clin Sarcoma Res 2015; 5: 4.
40. Heiner JP, Miraldi F, Kallick S, Makley J, Neely J, Smith-Mensah WH, et al. Localization of GD2-specific monoclonal antibody 3F8 in human osteosarcoma. Cancer Res 1987; 47: 5377-81.
41. Chang HR, Cordon-Cardo C, Houghton AN, Cheung NK, Brennan MF. Expression of disialogangliosides GD2 and GD3 on human soft tissue sarcomas. Cancer 1992; 70: 633-8.
42. Zhang H, Maric I, DiPrima MJ, Khan J, Orentas RJ, Kaplan RN, et al. Fibrocytes represent a novel MDSC subset circulating in patients with metastatic cancer. Blood 2013; 122: 1105-13.
43. Giles AJ, Reid CM, Evans JD, Murgai M, Vicioso Y, Highfill SL, et al. Activation of hematopoietic stem/progenitor cells promotes immunosuppression within the pre-metastatic niche. Cancer Res 2016; 76: 1335-47.
44. Stroncek DF, Ren J, Lee DW, Tran M, Frodigh SE, Sabatino M, et al. Myeloid cells in peripheral blood mononuclear cell concentrates inhibit the expansion of chimeric antigen receptor T cells. Cytotherapy 2016; 18: 893-901.
45. Asgharzadeh S, Salo JA, Ji L, Oberthuer A, Fischer M, Berthold F, et al. Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol 2012; 30: 3525-32.
46. Liu D, Song L, Wei J, Courtney AN, Gao X, Marinova E, et al. IL-15 protects NKT cells from inhibition by tumor-associated macrophages and enhances antimetastatic activity. J Clin Invest 2012; 122: 2221-33.
47. Chinnasamy D, Yu Z, Kerkar SP, Zhang L, Morgan RA, Restifo NP, et al. Local delivery of lnterleukin-12 using T cells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin Cancer Res 2012; 18: 1672-83.
48. John LB, Devaud C, Duong CP, Yong CS, Beavis PA, Haynes NM, et al. Anti-PD-1 antibody therapy potently enhances the eradication of established tumors by gene-modified T cells. Clin Cancer Res 2013; 19: 5636-46.
49. Lo-Coco F, Cicconi L, Breccia M. Current standard treatment of adult acute promyelocytic leukaemia. Br J Haematol 2016; 172: 841-54.
50. Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA, Gabrilovich DI. Mechanism of all-Trans retinoic acid effect on tumor-associated myeloidderived suppressor cells. Cancer Res 2007; 67: 11021-8.