HSV-sr39TK positron emission tomography and suicide gene elimination of human hematopoietic stem cells and their progeny in humanized mice

Cancer Research

Volumn 74, Issue 18, 2014, Pages 5173-5183

  Gschweng, Eric H ^a   McCracken, Melissa N ^a   Kaufman, Michael L ^a   Ho, Michelle ^a   Hollis, Roger P ^a   Wang, Xiaoyan ^b   Saini, Navdeep ^a   Koya, Richard C ^c   Chodon, Thinle ^c   Ribas, Antoni ^a,d,e   Witte, Owen N ^a,d,e   Kohn, Donald B ^a,d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Los Angeles   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CTAG1B PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; TUMOR ANTIGEN;

ANIMAL; BLOOD; DISEASE MODEL; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HEMATOPOIETIC STEM CELL; HERPES SIMPLEX VIRUS 1; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; MOUSE; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PROCEDURES; SCINTISCANNING; SUICIDE TRANSGENE; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD34; ANTIGENS, NEOPLASM; DISEASE MODELS, ANIMAL; GENES, TRANSGENIC, SUICIDE; GENETIC THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOTHERAPY; MEMBRANE PROTEINS; MICE; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSDUCTION, GENETIC;

EID: 84907486881     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0376     Document Type: Article

References (52)

1. Bordignon C, Notarangelo LD, Nobili N, Ferrari G, Casorati G, Panina P, et al. Gene therapy in peripheral blood lymphocytes and bone marrow for ADA-immunodeficient patients. Science 1995;270:470-5.
2. Kohn DB, Weinberg KI, Nolta JA, Heiss LN, Lenarsky C, Crooks GM, et al. Engraftment of gene-modified umbilical cord blood cells in neonates with adenosine deaminase deficiency. Nat Med 1995;1:1017-23.
3. Aiuti A, Slavin S, Aker M, Ficara F, Deola S, Mortellaro A, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 2002;296:2410-3.
4. Wirth T, Parker N, Yla-Herttuala S. History of gene therapy. Gene 2013;525:162-9.
5. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006;314:126-9.
6. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. New Engl J Med 2013;368:1509-18.
7. 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.
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. J Clin Oncol 2011;29:917-24.
9. + T cells. J Clin Invest 2005;115:1616-26.
10. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol 2005;175:7046-52.
11. Ma C, Cheung AF, Chodon T, Koya RC, Wu Z, Ng C, et al. Multifunctional T-cell analyses to study response and progression in adoptive cell transfer immunotherapy. Cancer Discov 2013;3:418-29.
12. Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer 2012;12:671-84.
13. Gattinoni L, Restifo NP. Moving T memory stem cells to the clinic. Blood 2013;121:567-8.
14. Cieri N, Camisa B, Cocchiarella F, Forcato M, Oliveira G, Provasi E, et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood 2013;121:573-84.
15. Terakura S, Yamamoto TN, Gardner RA, Turtle CJ, Jensen MC, Riddell SR. Generation of CD19-chimeric antigen receptor modified CD8+ T cells derived from virus-specific central memory T cells. Blood 2012;119:72-82.
16. Wang X, Berger C, Wong CW, Forman SJ, Riddell SR, Jensen MC. Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood 2011;117:1888-98.
17. Yang L, Baltimore D. Long-term in vivo provision of antigen-specific T cell immunity by programming hematopoietic stem cells. Proc Natl Acad Sci USA 2005;102:4518-23.
18. Giannoni F, Hardee CL, Wherley J, Gschweng E, Senadheera S, Kaufman ML, et al. Allelic exclusion and peripheral reconstitution by TCR transgenic T cells arising from transduced human hematopoietic stem/progenitor cells. Mol Ther 2013;21:1044-54.
19. Vatakis DN, Koya RC, Nixon CC, Wei L, Kim SG, Avancena P, et al. Antitumor activity from antigen-specific CD8 T cells generated in vivo from genetically engineered human hematopoietic stem cells. Proc Natl Acad Sci U S A 2011;108:E1408-16.
20. Vatakis DN, Arumugam B, Kim SG, Bristol G, Yang O, Zack JA. Introduction of exogenous T-cell receptors into human hematopoietic progenitors results in exclusion of endogenous T-cell receptor expression. Mol Ther 2013;21:1055-63.
21. De Oliveira SN, Ryan C, Giannoni F, Hardee CL, Tremcinska I, Katebian B, et al. Modification of hematopoietic stem/progenitor cells with CD19-specific chimeric antigen receptors as a novel approach for cancer immunotherapy. Hum Gene Ther 2013;24:824-39.
22. Gaspar HB, Cooray S, Gilmour KC, Parsley KL, Adams S, Howe SJ, et al. Long-term persistence of a polyclonal T cell repertoire after gene therapy for X-linked severe combined immunodeficiency. Sci Trans Med 2011;3:97ra79.
23. Candotti F, Shaw KL, Muul L, Carbonaro D, Sokolic R, Choi C, et al. Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 2012;120:3635-46.
24. Hacein-Bey-Abina S, von Kalle C, Schmidt M, Le Deist F, Wulffraat N, McIntyre E, et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003;348:255-6.
25. Emery DW. The use of chromatin insulators to improve the expression and safety of integrating gene transfer vectors. Hum Gen Ther 2011;22:761-74.
26. Yu SF, von Ruden T, Kantoff PW, Garber C, Seiberg M, Rüther U, et al. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc Natl Acad Sci U S A 1986;83:3194-8.
27. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998;72:9873-80.
28. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J Virol 1998;72:8150-7.
29. 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 2010;18:843-51.
30. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Eng J Med 2011;365:725-33.
31. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009;114:535-46.
32. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013;122:863-71.
33. Blumenthal M, Skelton D, Pepper KA, Jahn T, Methangkool E, Kohn DB. Effective suicide gene therapy for leukemia in a model of insertional oncogenesis in mice. Mol Ther 2007;15:183-92.
34. Bonini C, Ferrari G, Verzeletti S, Servida P, Zappone E, Ruggieri L, et al. HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science 1997;276:1719-24.
35. Black ME, Newcomb TG, Wilson HM, Loeb LA. Creation of drugspecific herpes simplex virus type 1 thymidine kinase mutants for gene therapy. Proc Natl Acad Sci U S A 1996;93:3525-9.
36. Straathof KC, Pule MA, Yotnda P, Dotti G, Vanin EF, Brenner MK, et al. An inducible caspase 9 safety switch for T-cell therapy. Blood 2005;105:4247-54.
37. Di Stasi A, Tey SK, Dotti G, Fujita Y, Kennedy-Nasser A, Martinez C, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Eng J Med 2011;365:1673-83.
38. Wang X, Chang WC, Wong CW, Colcher D, Sherman M, Ostberg JR, et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood 2011;118:1255-63.
39. Qasim W, Thrasher AJ, Buddle J, Kinnon C, Black ME, Gaspar HB. T cell transduction and suicide with an enhanced mutant thymidine kinase. Gene Ther 2002;9:824-7.
40. Gambhir SS, Bauer E, Black ME, Liang Q, Kokoris MS, Barrio JR, et al. A mutant herpes simplex virus type 1 thymidine kinase reporter gene shows improved sensitivity for imaging reporter gene expression with positron emission tomography. Proc Natl Acad Sci U S A 2000;97:2785-90.
41. Ribas A, Butterfield LH, Hu B, Dissette VB, Chen AY, Koh A, et al. Generation of T-cell immunity to a murine melanoma using MART-1-engineered dendritic cells. J Immunother 2000;23:59-66.
42. Alauddin MM, Conti PS. Synthesis and preliminary evaluation of 9-(4-[18F]-fluoro-3-hydroxymethylbutyl) guanine ([18F]FHBG): a new potential imaging agent for viral infection and gene therapy using PET. Nucl Med Biol 1998;25:175-80.
43. Laird NM, Ware JH. Random-effects models for longitudinal data. Biometrics 1982;38:963-74.
44. Black ME, Kokoris MS, Sabo P. Herpes simplex virus-1 thymidine kinase mutants created by semi-random sequence mutagenesis improve prodrug-mediated tumor cell killing. Cancer Res 2001;61:3022-6.
45. Yaghoubi S, Barrio JR, Dahlbom M, Iyer M, Namavari M, Satyamurthy N, et al. Human pharmacokinetic and dosimetry studies of [(18) F]FHBG: a reporter probe for imaging herpes simplex virus type-1 thymidine kinase reporter gene expression. J Nucl Med 2001;42:1225-34.
46. Wang X, Rosol M, Ge S, Peterson D, McNamara G, Pollack H, et al. Dynamic tracking of human hematopoietic stem cell engraftment using in vivo bioluminescence imaging. Blood 2003;102:3478-82.
47. Su H, Forbes A, Gambhir SS, Braun J. Quantitation of cell number by a positron emission tomography reporter gene strategy. Mol Imaging Biol 2004;6:139-48.
48. Riddell SR, Elliott M, Lewinsohn DA, Gilbert MJ, Wilson L, Manley SA, et al. T-cell mediated rejection of gene-modified HIV-specific cytotoxic T lymphocytes in HIV-infected patients. Nat Med 1996;2:216-23.
49. Berger C, Flowers ME, Warren EH, Riddell SR. Analysis of transgenespecific immune responses that limit the in vivo persistence of adoptively transferred HSV-TK-modified donor T cells after allogeneic hematopoietic cell transplantation. Blood 2006;107:2294-302.
50. Fehr T, Sykes M. Tolerance induction in clinical transplantation. Transpl Immunol 2004;13:117-30.
51. McCracken MN, Gschweng EH, Nair-Gill E, McLaughlin J, Cooper AR, Riedinger M, et al. Long-term in vivo monitoring of mouse and human hematopoietic stem cell engraftment with a human positron emission tomography reporter gene. Proc Natl Acad Sci U S A 2013;110:1857-62.
52. Barese CN, Krouse AE, Metzger ME, King CA, Traversari C, Marini FC, et al. Thymidine kinase suicide gene-mediated ganciclovir ablation of autologous gene-modified rhesus hematopoiesis. Mol Ther 2012;20:1932-43.