IGF1R- and ROR1-Specific CAR T cells as a potential therapy for high risk sarcomas

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Huang, Xin ^a   Park, Haein ^a   Greene, Joseph ^b   Pao, James ^a   Mulvey, Erin ^a   Zhou, Sophia X ^c   Albert, Catherine M ^d   Moy, Fred ^a   Sachdev, Deepali ^c   Yee, Douglas ^c   Rader, Christoph ^e   Hamby, Carl V ^a   Loeb, David M ^d   Cairo, Mitchell S ^a   Zhou, Xianzheng ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 13; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; SOMATOMEDIN C RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TYROSINE KINASE LIKE ORPHAN RECEPTOR 1; UNCLASSIFIED DRUG; ALPHA INTERFERON; IGF1R PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; ROR1 PROTEIN, HUMAN; SOMATOMEDIN RECEPTOR; TRANSPOSON;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYONAL RHABDOMYOSARCOMA; EWING SARCOMA; FEMALE; FIBROSARCOMA; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; OSTEOSARCOMA; RHABDOMYOSARCOMA; SARCOMA; SARCOMA CELL LINE; T LYMPHOCYTE; TUMOR REGRESSION; ANIMAL; BONE NEOPLASMS; GENETICS; IMMUNOLOGY; K-562 CELL LINE; MCF-7 CELL LINE; METABOLISM; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; TRANSPOSON; TUMOR CELL LINE;

ADOPTIVE TRANSFER; ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; DNA TRANSPOSABLE ELEMENTS; HUMANS; INTERFERON-ALPHA; INTERFERON-GAMMA; INTERLEUKIN-13; K562 CELLS; MCF-7 CELLS; MICE; MICE, INBRED NOD; MICE, SCID; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, SOMATOMEDIN; SARCOMA; T-LYMPHOCYTES;

EID: 84940676094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133152     Document Type: Article

References (53)

1. June CH, Riddell SR, Schumacher TN. Adoptive cellular therapy: A race to the finish line. Science translational medicine. 2015; 7(280):280ps7. doi: 10.1126/scitranslmed.aaa3643 PMID: 25810311.
2. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Current opinion in immunology. 2009; 21(2):233-40. doi: 10.1016/j.coi.2009.03.002 PMID: 19304471; PubMed Central PMCID: PMC3459355.
3. Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. The New England journal of medicine. 2014; 371(16):1507-17. doi: 10.1056/NEJMoa1407222 PMID: 25317870; PubMed Central PMCID: PMC4267531.
4. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. The New England journal of medicine. 2011; 365(8):725-33. doi: 10.1056/NEJMoa1103849 PMID: 21830940; PubMed Central PMCID: PMC3387277.
5. 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. Science translational medicine. 2013; 5(177):177ra38. doi: 10.1126/scitranslmed.3005930 PMID: 23515080; PubMed Central PMCID: PMC3742551.
6. Maus MV, Grupp SA, Porter DL, June CH. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood. 2014; 123(17):2625-35. doi: 10.1182/blood-2013-11-492231 PMID: 24578504; PubMed Central PMCID: PMC3999751.
7. Kakarla S, Gottschalk S. CAR T cells for solid tumors: armed and ready to go? Cancer journal. 2014; 20(2):151-5. doi: 10.1097/PPO.0000000000000032 PMID: 24667962; PubMed Central PMCID: PMC4050065.
8. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2011; 29(7):917-24. doi: 10.1200/JCO.2010.32.2537 PMID: 21282551; PubMed Central PMCID: PMC3068063.
9. Kailayangiri S, Altvater B, Meltzer J, Pscherer S, Luecke A, Dierkes C, et al. The ganglioside antigen G (D2) is surface-expressed in Ewing sarcoma and allows for MHC-independent immune targeting. British journal of cancer. 2012; 106(6):1123-33. doi: 10.1038/bjc.2012.57 PMID: 22374462; PubMed Central PMCID: PMC3304425.
10. Huang G, Yu L, Cooper LJ, Hollomon M, Huls H, Kleinerman ES. Genetically modified T cells targeting interleukin-11 receptor alpha-chain kill human osteosarcoma cells and induce the regression of established osteosarcoma lung metastases. Cancer research. 2012; 72(1):271-81. doi: 10.1158/0008-5472.CAN-11-2778 PMID: 22075555; PubMed Central PMCID: PMC3833671.
11. Ahmed N, Salsman VS, Yvon E, Louis CU, Perlaky L, Wels WS, et al. Immunotherapy for osteosarcoma: genetic modification of T cells overcomes low levels of tumor antigen expression. Molecular therapy: the journal of the American Society of Gene Therapy. 2009; 17(10):1779-87. doi: 10.1038/mt.2009.133 PMID: 19532139; PubMed Central PMCID: PMC2835000.
12. Gattenlohner S, Marx A, Markfort B, Pscherer S, Landmeier S, Juergens H, et al. Rhabdomyosarcoma lysis by T cells expressing a human autoantibody-based chimeric receptor targeting the fetal acetylcholine receptor. Cancer research. 2006; 66(1):24-8. doi: 10.1158/0008-5472.CAN-05-0542 PMID: 16397210.
13. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nature medicine. 2008; 14(11):1264-70. doi: 10.1038/nm.1882 PMID: 18978797; PubMed Central PMCID: PMC2749734.
14. Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C, et al. Human Epidermal Growth Factor Receptor 2 (HER2)-Specific Chimeric Antigen Receptor-Modified T Cells for the Immunotherapy of HER2-Positive Sarcoma. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2015; 33(15):1688-96. doi: 10.1200/JCO.2014.58.0225 PMID: 25800760; PubMed Central PMCID: PMC4429176.
15. Yee D, Favoni RE, Lebovic GS, Lombana F, Powell DR, Reynolds CP, et al. Insulin-like growth factor I expression by tumors of neuroectodermal origin with the t(11;22) chromosomal translocation. A potential autocrine growth factor. The Journal of clinical investigation. 1990; 86(6):1806-14. doi: 10.1172/JCI114910 PMID: 2174908; PubMed Central PMCID: PMC329812.
16. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Akiyama M, et al. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors. Cancer cell. 2004; 5(3):221-30. PMID: 15050914.
17. Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nature reviews Cancer. 2012; 12(3):159-69. doi: 10.1038/nrc3215 PMID: 22337149.
18. Juergens H, Daw NC, Geoerger B, Ferrari S, Villarroel M, Aerts I, et al. Preliminary efficacy of the antiinsulin-like growth factor type 1 receptor antibody figitumumab in patients with refractory Ewing sarcoma. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2011; 29(34):4534-40. doi: 10.1200/JCO.2010.33.0670 PMID: 22025154; PubMed Central PMCID: PMC3236653.
19. Pappo AS, Patel SR, Crowley J, Reinke DK, Kuenkele KP, Chawla SP, et al. R1507, a monoclonal antibody to the insulin-like growth factor 1 receptor, in patients with recurrent or refractory Ewing sarcoma family of tumors: results of a phase II Sarcoma Alliance for Research through Collaboration study. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2011; 29(34):4541-7. doi: 10.1200/JCO.2010.34.0000 PMID: 22025149; PubMed Central PMCID: PMC3236654.
20. Malempati S, Weigel B, Ingle AM, Ahern CH, Carroll JM, Roberts CT, et al. Phase I/II trial and pharmacokinetic study of cixutumumab in pediatric patients with refractory solid tumors and Ewing sarcoma: a report from the Children's Oncology Group. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2012; 30(3):256-62. doi: 10.1200/JCO.2011.37.4355 PMID: 22184397; PubMed Central PMCID: PMC3269952.
21. Baskar S, Kwong KY, Hofer T, Levy JM, Kennedy MG, Lee E, et al. Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14(2):396-404. doi: 10.1158/1078-0432.CCR-07-1823 PMID: 18223214.
22. Fukuda T, Chen L, Endo T, Tang L, Lu D, Castro JE, et al. Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(8):3047-52. doi: 10.1073/pnas.0712148105 PMID: 18287027; PubMed Central PMCID: PMC2268582.
23. Yang J, Baskar S, Kwong KY, Kennedy MG, Wiestner A, Rader C. Therapeutic potential and challenges of targeting receptor tyrosine kinase ROR1 with monoclonal antibodies in B-cell malignancies. PloS one. 2011; 6(6):e21018. doi: 10.1371/journal.pone.0021018 PMID: 21698301; PubMed Central PMCID: PMC3115963.
24. Baskar S, Wiestner A, Wilson WH, Pastan I, Rader C. Targeting malignant B cells with an immunotoxin against ROR1. mAbs. 2012; 4(3):349-61. doi: 10.4161/mabs.19870 PMID: 22531447; PubMed Central PMCID: PMC3355487.
25. Zhang S, Chen L, Cui B, Chuang HY, Yu J, Wang-Rodriguez J, et al. ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PloS one. 2012; 7(3):e31127. doi: 10.1371/journal.pone.0031127 PMID: 22403610; PubMed Central PMCID: PMC3293865.
26. Dave H, Anver MR, Butcher DO, Brown P, Khan J, Wayne AS, et al. Restricted cell surface expression of receptor tyrosine kinase ROR1 in pediatric B-lineage acute lymphoblastic leukemia suggests targetability with therapeutic monoclonal antibodies. PloS one. 2012; 7(12):e52655. doi: 10.1371/journal.pone.0052655 PMID: 23285131; PubMed Central PMCID: PMC3527582.
27. Broome HE, Rassenti LZ, Wang HY, Meyer LM, Kipps TJ. ROR1 is expressed on hematogones (non-neoplastic human B-lymphocyte precursors) and a minority of precursor-B acute lymphoblastic leukemia. Leukemia research. 2011; 35(10):1390-4. doi: 10.1016/j.leukres.2011.06.021 PMID: 21813176; PubMed Central PMCID: PMC3163753.
28. Bicocca VT, Chang BH, Masouleh BK, Muschen M, Loriaux MM, Druker BJ, et al. Crosstalk between ROR1 and the Pre-B cell receptor promotes survival of t(1;19) acute lymphoblastic leukemia. Cancer cell. 2012; 22(5):656-67. doi: 10.1016/j.ccr.2012.08.027 PMID: 23153538; PubMed Central PMCID: PMC3500515.
29. Yamaguchi T, Yanagisawa K, Sugiyama R, Hosono Y, Shimada Y, Arima C, et al. NKX2-1/TITF1/TTF-1-Induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer cell. 2012; 21(3):348-61. doi: 10.1016/j.ccr.2012.02.008 PMID: 22439932.
30. Zhang S, Cui B, Lai H, Liu G, Ghia EM, Widhopf GF 2nd, et al. Ovarian cancer stem cells express ROR1, which can be targeted for anti-cancer-stem-cell therapy. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111(48):17266-71. doi: 10.1073/pnas.1419599111 PMID: 25411317; PubMed Central PMCID: PMC4260559.
31. Cui B, Zhang S, Chen L, Yu J, Widhopf GF 2nd, Fecteau JF, et al. Targeting ROR1 inhibits epithelial-mesenchymal transition and metastasis. Cancer research. 2013; 73(12):3649-60. doi: 10.1158/0008-5472.CAN-12-3832 PMID: 23771907; PubMed Central PMCID: PMC3832210.
32. Hudecek M, Schmitt TM, Baskar S, Lupo-Stanghellini MT, Nishida T, Yamamoto TN, et al. The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood. 2010; 116(22):4532-41. doi: 10.1182/blood-2010-05-283309 PMID: 20702778; PubMed Central PMCID: PMC2996114.
33. Sachdev D, Singh R, Fujita-Yamaguchi Y, Yee D. Down-regulation of insulin receptor by antibodies against the type I insulin-like growth factor receptor: implications for anti-insulin-like growth factor therapy in breast cancer. Cancer research. 2006; 66(4):2391-402. doi: 10.1158/0008-5472.CAN-05-3126 PMID: 16489046
34. Sachdev D, Li SL, Hartell JS, Fujita-Yamaguchi Y, Miller JS, Yee D. A chimeric humanized single-chain antibody against the type I insulin-like growth factor (IGF) receptor renders breast cancer cells refractory to the mitogenic effects of IGF-I. Cancer research. 2003; 63(3):627-35. PMID: 12566306.
35. Zhou X, Jun DY, Thomas AM, Huang X, Huang LQ, Mautner J, et al. Diverse CD8+ T-cell responses to renal cell carcinoma antigens in patients treated with an autologous granulocyte-macrophage colony-stimulating factor gene-transduced renal tumor cell vaccine. Cancer research. 2005; 65(3):1079-88. PMID: 15705910.
36. Luo W, Gangwal K, Sankar S, Boucher KM, Thomas D, Lessnick SL. GSTM4 is a microsatellite-containing EWS/FLI target involved in Ewing's sarcoma oncogenesis and therapeutic resistance. Oncogene. 2009; 28(46):4126-32. doi: 10.1038/onc.2009.262 PMID: 19718047.
37. Owen LA, Kowalewski AA, Lessnick SL. EWS/FLI mediates transcriptional repression via NKX2.2 during oncogenic transformation in Ewing's sarcoma. PloS one. 2008; 3(4):e1965. doi: 10.1371/journal.pone.0001965 PMID: 18414662; PubMed Central PMCID: PMC2291578.
38. Huang X, Guo H, Kang J, Choi S, Zhou TC, Tammana S, et al. Sleeping Beauty transposon-mediated engineering of human primary T cells for therapy of CD19+ lymphoid malignancies. Molecular therapy: the journal of the American Society of Gene Therapy. 2008; 16(3):580-9. doi: 10.1038/sj.mt.6300404 PMID: 18227839.
39. Kusada Y, Morizono T, Matsumoto-Takasaki A, Sakai K, Sato S, Asanuma H, et al. Construction and characterization of single-chain antibodies against human insulin-like growth factor-I receptor from hybridomas producing 1H7 or 3B7 monoclonal antibody. Journal of biochemistry. 2008; 143(1):9-19. doi: 10.1093/jb/mvm192 PMID: 17956902.
40. Xue X, Huang X, Nodland SE, Mates L, Ma L, Izsvak Z, et al. Stable gene transfer and expression in cord blood-derived CD34+ hematopoietic stem and progenitor cells by a hyperactive Sleeping Beauty transposon system. Blood. 2009; 114(7):1319-30. doi: 10.1182/blood-2009-03-210005 PMID: 19414858.
41. Tammana S, Huang X, Wong M, Milone MC, Ma L, Levine BL, et al. 4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies. Human gene therapy. 2010; 21(1):75-86. doi: 10.1089/hum.2009.122 PMID: 19719389; PubMed Central PMCID: PMC2861957.
42. Chitnis MM, Yuen JS, Protheroe AS, Pollak M, Macaulay VM. The type 1 insulin-like growth factor receptor pathway. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14(20):6364-70. doi: 10.1158/1078-0432.CCR-07-4879 PMID: 18927274.
43. Wagner MJ, Maki RG. Type 1 insulin-like growth factor receptor targeted therapies in pediatric cancer. Frontiers in oncology. 2013; 3:9. doi: 10.3389/fonc.2013.00009 PMID: 23383402; PubMed Central PMCID: PMC3563098.
44. Cecil DL, Park KH, Gad E, Childs JS, Higgins DM, Plymate SR, et al. T-helper I immunity, specific for the breast cancer antigen insulin-like growth factor-I receptor (IGF-IR), is associated with increased adiposity. Breast cancer research and treatment. 2013; 139(3):657-65. doi: 10.1007/s10549-013-2577-z PMID: 23749321.
45. Disis ML, Gad E, Herendeen DR, Lai VP, Park KH, Cecil DL, et al. A multiantigen vaccine targeting neu, IGFBP-2, and IGF-IR prevents tumor progression in mice with preinvasive breast disease. Cancer prevention research. 2013; 6(12):1273-82. doi: 10.1158/1940-6207.CAPR-13-0182 PMID: 24154719; PubMed Central PMCID: PMC3864759.
46. Langer CJ, Novello S, Park K, Krzakowski M, Karp DD, Mok T, et al. Randomized, phase III trial of first-line figitumumab in combination with paclitaxel and carboplatin versus paclitaxel and carboplatin alone in patients with advanced non-small-cell lung cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2014; 32(19):2059-66. doi: 10.1200/JCO.2013.54.4932 PMID: 24888810; PubMed Central PMCID: PMC4067944.
47. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? Journal of the National Cancer Institute. 2012; 104(13):975-81. doi: 10.1093/jnci/djs258 PMID: 22761272; PubMed Central PMCID: PMC3634550.
48. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity. 1996; 4(6):565-71. PMID: 8673703.
49. Anders K, Blankenstein T. Molecular pathways: comparing the effects of drugs and T cells to effectively target oncogenes. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19(2):320-6. doi: 10.1158/1078-0432.CCR-12-3017 PMID: 23197254.
50. Fedorov VD, Themeli M, Sadelain M. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Science translational medicine. 2013; 5(215):215ra172. doi: 10.1126/scitranslmed.3006597 PMID: 24337479; PubMed Central PMCID: PMC4238416.
51. Hojjat-Farsangi M, Moshfegh A, Daneshmanesh AH, Khan AS, Mikaelsson E, Osterborg A, et al. The receptor tyrosine kinase ROR1-an oncofetal antigen for targeted cancer therapy. Seminars in cancer biology. 2014; 29:21-31. doi: 10.1016/j.semcancer.2014.07.005 PMID: 25068995.
52. Hudecek M, Lupo-Stanghellini MT, Kosasih PL, Sommermeyer D, Jensen MC, Rader C, et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19(12):3153-64. doi: 10.1158/1078-0432.CCR-13-0330 PMID: 23620405; PubMed Central PMCID: PMC3804130.
53. Berger C, Sommermeyer D, Hudecek M, Berger M, Balakrishnan A, Paszkiewicz PJ, et al. Safety of Targeting ROR1 in Primates with Chimeric Antigen Receptor-Modified T Cells. Cancer immunology research. 2014. doi: 10.1158/2326-6066.CIR-14-0163 PMID: 25355068.