Advances in chimeric antigen receptor immunotherapy for neuroblastoma

Discovery Medicine

Volumn 16, Issue 90, 2013, Pages 287-294

  Heczey, Andras ^a   Louis, Chrystal U ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 9; CD28 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; DISEASE SURVEILLANCE; FOLLOW UP; HUMAN; IMMUNE RESPONSE; NEUROBLASTOMA; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PROGNOSIS; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

ADOPTIVE TRANSFER; ANTIBODIES, MONOCLONAL; CHILD; CLINICAL TRIALS AS TOPIC; GENES, T-CELL RECEPTOR; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; NEUROBLASTOMA; PROGNOSIS; RECEPTORS, ANTIGEN; RISK;

EID: 84890850147     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Altvater B, Landmeier S, Pscherer S, Temme J, Schweer K, Kailayangiri S, Campana D, Juergens H, Pule M, Rossig C. 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin Cancer Res 15(15):4857-4866, 2009.
2. Alvarez-Rueda N, Desselle A, Cochonneau D, Chaumette T, Clemenceau B, Leprieur S, Bougras G, Supiot S, Mussini JM, Barbet J, Saba J, Paris F, Aubry J, Birkle S. A monoclonal antibody to O-acetyl-GD2 ganglioside and not to GD2 shows potent anti-tumor activity without peripheral nervous system cross-reactivity. PLoS One 6(9):e25220, 2011.
3. Arlt MJ, Novak-Hofer I, Gast D, Gschwend V, Moldenhauer G, Grunberg J, Honer M, Schubiger PA, Altevogt P, Kruger A. Efficient inhibition of intra-peritoneal tumor growth and dissemination of human ovarian carcinoma cells in nude mice by anti-L1-cell adhesion molecule monoclonal antibody treatment. Cancer Res 66(2):936-943, 2006.
4. Baker DL, Schmidt ML, Cohn SL, Maris JM, London WB, Buxton A, Stram D, Castleberry RP, Shimada H, Sandler A, Shamberger RC, Look AT, Reynolds CP, Seeger RC, Matthay KK. Outcome after reduced chemotherapy for intermediate-risk neuroblastoma. N Engl J Med 363(14):1313-1323, 2010.
5. Bowman L, Grossmann M, Rill D, Brown M, Zhong WY, Alexander B, Leimig T, Coustan-Smith E, Campana D, Jenkins J, Woods D, Kitchingman G, Vanin E, Brenner M. IL-2 adenovector-transduced autologous tumor cells induce antitumor immune responses in patients with neuroblastoma. Blood 92(6):1941-1949, 1998.
6. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366(26):2455-2465, 2012.
7. Brenner MK, Heslop H, Krance R, Horowitz M, Strother D, Nuchtern J, Grilley B, Martingano E, Cooper K. Phase I study of chemokine and cytokine gene-modified autologous neuroblastoma cells for treatment of relapsed/refractory neuroblastoma using an adenoviral vector. Hum Gene Ther 11(10):1477-1488, 2000.
8. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, Bartido S, Stefanski J, Taylor C, Olszewska M, Borquez-Ojeda O, Qu J, Wasielewska T, He Q, Bernal Y, Rijo IV, Hedvat C, Kobos R, Curran K, Steinherz P et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 5(177):177ra38, 2013.
9. Brentjens RJ, Santos E, Nikhamin Y, Yeh R, Matsushita M, La PK, Quintas-Cardama A, Larson SM, Sadelain M. Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res 13(18 Pt 1):5426-5435, 2007.
10. Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP, De BB, Evans AE, Favrot M, Hedborg F, . Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 11(8):1466-1477, 1993.
11. Cheung NK. Immunotherapy. Neuroblastoma as a model. Pediatr Clin North Am 38(2):425-441, 1991.
12. Cheung NK, Cheung IY, Kushner BH, Ostrovnaya I, Chamberlain E, Kramer K, Modak S. Murine anti-GD2 monoclonal antibody 3F8 combined with granulocyte-macrophage colony-stimulating factor and 13-cis-retinoic acid in high-risk patients with stage 4 neuroblastoma in first remission. J Clin Oncol 30(26):3264-3270, 2012.
13. Craddock JA, Lu A, Bear A, Pule M, Brenner MK, Rooney CM, Foster AE. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother 33(8):780-788, 2010.
14. del Campo AB, Carretero J, Aptsiauri N, Garrido F. Targeting HLA class I expression to increase tumor immunogenicity. Tissue Antigens 79(3):147-154, 2012.
15. Di SA, Tey SK, Dotti G, Fujita Y, Kennedy-Nasser A, Martinez C, Straathof K, Liu E, Durett AG, Grilley B, Liu H, Cruz CR, Savoldo B, Gee AP, Schindler J, Krance RA, Heslop HE, Spencer DM, Rooney CM, Brenner MK. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 365(18):1673-1683, 2011.
16. Esser R, Muller T, Stefes D, Kloess S, Seidel D, Gillies SD, Aperlo-Iffland C, Huston JS, Uherek C, Schonfeld K, Tonn T, Huebener N, Lode HN, Koehl U, Wels WS. NK cells engineered to express a GD2 -specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J Cell Mol Med 16(3):569-581, 2012.
17. Euer NI, Kaul S, Deissler H, Mobus VJ, Zeillinger R, Weidle UH. Identification of L1CAM, Jagged2 and Neuromedin U as ovarian cancer-associated antigens. Oncol Rep 13(3):375-387, 2005.
18. Fogel M, Gutwein P, Mechtersheimer S, Riedle S, Stoeck A, Smirnov A, Edler L, Ben-Arie A, Huszar M, Altevogt P. L1 expression as a predictor of progression and survival in patients with uterine and ovarian carcinomas. Lancet 362(9387):869-875, 2003.
19. Foster AE, Dotti G, Lu A, Khalil M, Brenner MK, Heslop HE, Rooney CM, Bollard CM. Antitumor activity of EBV-specific T lymphocytes transduced with a dominant negative TGF-beta receptor. J Immunother 31(5):500-505, 2008.
20. Gerdemann U, Katari UL, Papadopoulou A, Keirnan JM, Craddock JA, Liu H, Martinez CA, Kennedy-Nasser A, Leung KS, Gottschalk SM, Krance RA, Brenner MK, Rooney CM, Heslop HE, Leen AM. Safety and clinical efficacy of rapidly-generated trivirus-directed T cells as treatment for adenovirus, EBV, and CMV infections after allogeneic hematopoietic stem cell transplant. Mol Ther 21(11):2113-2121, 2013.
21. Hank JA, Robinson RR, Surfus J, Mueller BM, Reisfeld RA, Cheung NK, Sondel PM. Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res 50(17):5234-5239, 1990.
22. Heczey A, Liu D, Courtney A, Marinova E, Guo L, Gao X, Yvon E, Hicks J, Dotti G, Metelitsa LS. NKT Cells as a Novel Platform for Cancer Immunotherapy with Chimeric Antigen Receptors. American Society of Gell and Cell Therapy Annual Meeting, Poster #12, 2013.
23. Hoyos V, Savoldo B, Quintarelli C, Mahendravada A, Zhang M, Vera J, Heslop HE, Rooney CM, Brenner MK, Dotti G. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 24(6):1160-1170, 2010.
24. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, Rodmyre R, Jungbluth A, Gnjatic S, Thompson JA, Yee C. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358(25):2698-2703, 2008.
25. Izumoto S, Ohnishi T, Arita N, Hiraga S, Taki T, Hayakawa T. Gene expression of neural cell adhesion molecule L1 in malignant gliomas and biological significance of L1 in glioma invasion. Cancer Res 56(6):1440-1444, 1996.
26. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, June CH. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 3(95):95ra73, 2011.
27. Kennedy-Nasser AA, Bollard CM, Myers GD, Leung KS, Gottschalk S, Zhang Y, Liu H, Heslop HE, Brenner MK, Krance RA. Comparable outcome of alternative donor and matched sibling donor hematopoietic stem cell transplant for children with acute lymphoblastic leukemia in first or second remission using alemtuzumab in a myeloablative conditioning regimen. Biol Blood Marrow Transplant 14(11):1245-1252, 2008.
28. Klebanoff CA, Gattinoni L, Restifo NP. Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J Immunother 35(9):651-660, 2012.
29. Krause A, Guo HF, Latouche JB, Tan C, Cheung NK, Sadelain M. Antigen-dependent CD28 signaling selectively enhances survival and proliferation in genetically modified activated human primary T lymphocytes. J Exp Med 188(4):619-626, 1998.
30. Kronenberg M, Gapin L. The unconventional lifestyle of NKT cells. Nat Rev Immunol 2(8):557-568, 2002.
31. Ladenstein R, Potschger U, Hartman O, Pearson AD, Klingebiel T, Castel V, Yaniv I, Demirer T, Dini G. 28 years of high-dose therapy and SCT for neuroblastoma in Europe: lessons from more than 4000 procedures. Bone Marrow Transplant 41(Suppl 2):S118-S127, 2008.
32. Leen AM, Christin A, Myers GD, Liu H, Cruz CR, Hanley PJ, Kennedy-Nasser AA, Leung KS, Gee AP, Krance RA, Brenner MK, Heslop HE, Rooney CM, Bollard CM. Cytotoxic T lymphocyte therapy with donor T cells prevents and treats adenovirus and Epstein-Barr virus infections after haploidentical and matched unrelated stem cell transplantation. Blood 114(19):4283-4292, 2009.
33. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, Litzky L, Bagg A, Carreno BM, Cimino PJ, Binder-Scholl GK, Smethurst DP, Gerry AB, Pumphrey NJ, Bennett AD, Brewer JE, Dukes J, Harper J, Tayton-Martin HK, Jakobsen BK, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122(6):863-871, 2013.
34. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, Rossig C, Russell hv, Diouf O, Liu E, Liu H, Wu MF, Gee AP, Mei Z, Rooney CM, Heslop HE, Brenner MK. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118(23):6050-6056, 2011.
35. Matthay KK, Seeger RC, Reynolds CP, Stram DO, O'Leary MC, Harris RE, Selch M, Atkinson JB, Haase GM, Ramsay NK. Allogeneic versus autologous purged bone marrow transplantation for neuroblastoma: a report from the Childrens Cancer Group. J Clin Oncol 12(11):2382-2389, 1994.
36. Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, Swift P, Shimada H, Black CT, Brodeur GM, Gerbing RB, Reynolds CP. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group. N Engl J Med 341(16):1165-1173, 1999.
37. Modak S, Kramer K, Gultekin SH, Guo HF, Cheung NK. Monoclonal antibody 8H9 targets a novel cell surface antigen expressed by a wide spectrum of human solid tumors. Cancer Res 61(10):4048-4054, 2001.
38. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, Zheng Z, Nahvi A, de Vries CR, Rogers-Freezer LJ, Mavroukakis SA, Rosenberg SA. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314(5796):126-129, 2006.
39. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 18(4):843-851, 2010.
40. Muranski P, Boni A, Wrzesinski C, Citrin DE, Rosenberg SA, Childs R, Restifo NP. Increased intensity lymphodepletion and adoptive immunotherapy-how far can we go? Nat Clin Pract Oncol 3(12):668-681, 2006.
41. Nuchtern JG, London WB, Barnewolt CE, Naranjo A, McGrady PW, Geiger JD, Diller L, Schmidt ML, Maris JM, Cohn SL, Shamberger RC. A prospective study of expectant observation as primary therapy for neuroblastoma in young infants: a Children's Oncology Group study. Ann Surg 256(4):573-580, 2012.
42. Park JR, Digiusto DL, Slovak M, Wright C, Naranjo A, Wagner J, Meechoovet HB, Bautista C, Chang WC, Ostberg JR, Jensen MC. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther 15(4):825-833, 2007.
43. Perez-Martinez A, Leung W, Munoz E, Iyengar R, Ramirez M, Vicario JL, Lassaletta A, Sevilla J, Gonzalez-Vicent M, Madero L, Diaz-Perez MA. KIR-HLA receptor-ligand mismatch associated with a graft-versus-tumor effect in haploidentical stem cell transplantation for pediatric metastatic solid tumors. Pediatr Blood Cancer 53(1):120-124, 2009.
44. Perna SK, Pagliara D, Mahendravada A, Liu H, Brenner MK, Savoldo B, Dotti G. Interleukin-7 mediates selective expansion of tumor-redirected cytotoxic T lymphocytes without enhancement of regulatory T-cell inhibition. Clin Cancer Res, epub ahead of print, Nov. 26, 2013.
45. Pistoia V, Morandi F, Bianchi G, Pezzolo A, Prigione I, Raffaghello L. Immunosuppressive microenvironment in neuroblastoma. Front Oncol 3:167, 2013.
46. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365(8):725-733, 2011.
47. Pule MA, Savoldo B, Myers GD, Rossig C, Russell hv, Dotti G, Huls MH, Liu E, Gee AP, Mei Z, Yvon E, Weiss HL, Liu H, Rooney CM, Heslop HE, Brenner MK. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14(11):1264-1270, 2008.
48. 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 12(5):933-941, 2005.
49. Raffaghello L, Prigione I, Bocca P, Morandi F, Camoriano M, Gambini C, Wang X, Ferrone S, Pistoia V. Multiple defects of the antigen-processing machinery components in human neuroblastoma: immunotherapeutic implications. Oncogene 24(29):4634-4644, 2005.
50. Riddell SR, Watanabe KS, Goodrich JM, Li CR, Agha ME, Greenberg PD. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257(5067):238-241, 1992.
51. Rossig C, Bollard CM, Nuchtern JG, Merchant DA, Brenner MK. Targeting of G(D2)-positive tumor cells by human T lymphocytes engineered to express chimeric T-cell receptor genes. Int J Cancer 94(2):228-236, 2001.
52. Rossig C, Nuchtern JG, Brenner MK. Selection of human antitumor single-chain Fv antibodies from the B-cell repertoire of patients immunized against autologous neuroblastoma. Med Pediatr Oncol 35(6):692-695, 2000.
53. Savoldo B, Dotti G. Chimeric antigen receptors (CARs) from bench-to-bedside. Immunol Lett 155(1-2):40-42, 2013.
54. Schonmann SM, Iyer J, Laeng H, Gerber HA, Kaser H, Blaser K. Production and characterization of monoclonal antibodies against human neuroblastoma. Int J Cancer 37(2):255-262, 1986.
55. Smith MA, Seibel NL, Altekruse SF, Ries LA, Melbert DL, O'Leary M, Smith FO, Reaman GH. Outcomes for children and adolescents with cancer: challenges for the twenty-first century. J Clin Oncol 28(15):2625-2634, 2010.
56. Song L, Asgharzadeh S, Salo J, Engell K, Wu HW, Sposto R, Ara T, Silverman AM, DeClerck YA, Seeger RC, Metelitsa LS. Valpha24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Invest 119(6):1524-1536, 2009.
57. Sun J, Dotti G, Huye LE, Foster AE, Savoldo B, Gramatges MM, Spencer DM, Rooney CM. T cells expressing constitutively active Akt resist multiple tumor-associated inhibitory mechanisms. Mol Ther 18(11):2006-2017, 2010.
58. Thies A, Schachner M, Moll I, Berger J, Schulze HJ, Brunner G, Schumacher U. Overexpression of the cell adhesion molecule L1 is associated with metastasis in cutaneous malignant melanoma. Eur J Cancer 38(13):1708-1716, 2002.
59. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366(26):2443-2454, 2012.
60. Watarai H, Nakagawa R, Omori-Miyake M, Dashtsoodol N, Taniguchi M. Methods for detection, isolation and culture of mouse and human invariant NKT cells. Nat Protoc 3(1):70-78, 2008.
61. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, Burke MM, Caldwell A, Kronenberg SA, Agunwamba BU, Zhang X, Lowy I, Inzunza HD, Feely W, Horak CE, Hong Q, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369(2):122-133, 2013.
62. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, Shimada H, Grupp SA, Seeger R, Reynolds CP, Buxton A, Reisfeld RA, Gillies SD, Cohn SL, Maris JM, Sondel PM. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 363(14):1324-1334, 2010.
63. Zhao XJ, Cheung NK. GD2 oligosaccharide: target for cytotoxic T lymphocytes. J Exp Med 182(1):67-74, 1995.
64. Zhong XS, 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 18(2):413-420, 2010.