Toward a Rapid Production of Multivirus-Specific T Cells Targeting BKV, Adenovirus, CMV, and EBV from Umbilical Cord Blood

Molecular Therapy Methods and Clinical Development

Volumn 5, Issue , 2017, Pages 13-21

  Dave, Hema ^a   Luo, Min ^a   Blaney, J W ^d   Patel, Shabnum ^a,c   Barese, Cecilia ^a   Cruz, Conrad Russell ^a,b   Shpall, Elizabeth J ^e   Bollard, Catherine M ^a,b,c   Hanley, Patrick J ^a,b  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d HOUSTON METHODIST HOSPITAL   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

adoptive immunotherapy; antiviral T cells; cellular therapy; cord blood; cord blood transplantation; T cells; virus

Indexed keywords

VIRUS VECTOR;

ADENOVIRIDAE; ARTICLE; BK VIRUS; CELL EXPANSION; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; EPSTEIN BARR VIRUS; GOOD MANUFACTURING PRACTICE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; TRANSPLANTATION; UMBILICAL CORD BLOOD; VIRAL GENE DELIVERY SYSTEM;

EID: 85020540659     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1016/j.omtm.2017.02.001     Document Type: Article

References (42)

1. 1 Eapen, M., Rubinstein, P., Zhang, M.J., Stevens, C., Kurtzberg, J., Scaradavou, A., Loberiza, F.R., Champlin, R.E., Klein, J.P., Horowitz, M.M., Wagner, J.E., Outcomes of transplantation of unrelated donor umbilical cord blood and bone marrow in children with acute leukaemia: a comparison study. Lancet 369 (2007), 1947–1954.
2. 2 Kurtzberg, J., Laughlin, M., Graham, M.L., Smith, C., Olson, J.F., Halperin, E.C., Ciocci, G., Carrier, C., Stevens, C.E., Rubinstein, P., Placental blood as a source of hematopoietic stem cells for transplantation into unrelated recipients. N. Engl. J. Med. 335 (1996), 157–166.
3. 3 Rocha, V., Cornish, J., Sievers, E.L., Filipovich, A., Locatelli, F., Peters, C., Remberger, M., Michel, G., Arcese, W., Dallorso, S., et al. Comparison of outcomes of unrelated bone marrow and umbilical cord blood transplants in children with acute leukemia. Blood 97 (2001), 2962–2971.
4. 4 Hanley, P.J., Cruz, C.R., Shpall, E.J., Bollard, C.M., Improving clinical outcomes using adoptively transferred immune cells from umbilical cord blood. Cytotherapy 12 (2010), 713–720.
5. 5 Gluckman, E., Rocha, V., Boyer-Chammard, A., Locatelli, F., Arcese, W., Pasquini, R., Ortega, J., Souillet, G., Ferreira, E., Laporte, J.P., et al. Outcome of cord-blood transplantation from related and unrelated donors. Eurocord Transplant Group and the European Blood and Marrow Transplantation Group. N. Engl. J. Med. 337 (1997), 373–381.
6. 6 Komanduri, K.V., St John, L.S., de Lima, M., McMannis, J., Rosinski, S., McNiece, I., Bryan, S.G., Kaur, I., Martin, S., Wieder, E.D., et al. Delayed immune reconstitution after cord blood transplantation is characterized by impaired thymopoiesis and late memory T-cell skewing. Blood 110 (2007), 4543–4551.
7. 7 Ballen, K., Woo Ahn, K., Chen, M., Abdel-Azim, H., Ahmed, I., Aljurf, M., Antin, J., Bhatt, A.S., Boeckh, M., Chen, G., et al. Infection rates among acute leukemia patients receiving alternative donor hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 22 (2016), 1636–1645.
8. 8 Lucchini, G., Perales, M.A., Veys, P., Immune reconstitution after cord blood transplantation: peculiarities, clinical implications and management strategies. Cytotherapy 17 (2015), 711–722.
9. 9 Ruggeri, A., Peffault de Latour, R., Carmagnat, M., Clave, E., Douay, C., Larghero, J., Cayuela, J.M., Traineau, R., Robin, M., Madureira, A., et al. Outcomes, infections, and immune reconstitution after double cord blood transplantation in patients with high-risk hematological diseases. Transpl. Infect. Dis. 13 (2011), 456–465.
10. 10 Saliba, R.M., Rezvani, K., Leen, A., Jorgensen, J., Shah, N., Hosing, C., Parmar, S., Oran, B., Olson, A., Rondon, G., et al. General and virus-specific immune cell reconstitution after double cord blood transplantation. Biol. Blood Marrow Transplant. 21 (2015), 1284–1290.
11. 11 Escalón, M.P., Komanduri, K.V., Cord blood transplantation: evolving strategies to improve engraftment and immune reconstitution. Curr. Opin. Oncol. 22 (2010), 122–129.
12. 12 Geyer, M.B., Jacobson, J.S., Freedman, J., George, D., Moore, V., van de Ven, C., Satwani, P., Bhatia, M., Garvin, J.H., Bradley, M.B., et al. A comparison of immune reconstitution and graft-versus-host disease following myeloablative conditioning versus reduced toxicity conditioning and umbilical cord blood transplantation in paediatric recipients. Br. J. Haematol. 155 (2011), 218–234.
13. 13 Giraud, G., Priftakis, P., Bogdanovic, G., Remberger, M., Dubrulle, M., Hau, A., Gutmark, R., Mattson, J., Svahn, B.M., Ringden, O., et al. BK-viruria and haemorrhagic cystitis are more frequent in allogeneic haematopoietic stem cell transplant patients receiving full conditioning and unrelated-HLA-mismatched grafts. Bone Marrow Transplant. 41 (2008), 737–742.
14. 14 El-Zimaity, M., Saliba, R., Chan, K., Shahjahan, M., Carrasco, A., Khorshid, O., Caldera, H., Couriel, D., Giralt, S., Khouri, I., et al. Hemorrhagic cystitis after allogeneic hematopoietic stem cell transplantation: donor type matters. Blood 103 (2004), 4674–4680.
15. 15 Silva, Lde.P., Patah, P.A., Saliba, R.M., Szewczyk, N.A., Gilman, L., Neumann, J., Han, X.Y., Tarrand, J., Ribeiro, R., Gulbis, A., et al. Hemorrhagic cystitis after allogeneic hematopoietic stem cell transplants is the complex result of BK virus infection, preparative regimen intensity and donor type. Haematologica 95 (2010), 1183–1190.
16. 16 Megged, O., Stein, J., Ben-Meir, D., Shulman, L.M., Yaniv, I., Shalit, I., Levy, I., BK-virus-associated hemorrhagic cystitis in children after hematopoietic stem cell transplantation. J. Pediatr. Hematol. Oncol. 33 (2011), 190–193.
17. 17 Gilis, L., Morisset, S., Billaud, G., Ducastelle-Leprêtre, S., Labussière-Wallet, H., Nicolini, F.E., Barraco, F., Detrait, M., Thomas, X., Tedone, N., et al. High burden of BK virus-associated hemorrhagic cystitis in patients undergoing allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 49 (2014), 664–670.
18. 18 Haines, H.L., Laskin, B.L., Goebel, J., Davies, S.M., Yin, H.J., Lawrence, J., Mehta, P.A., Bleesing, J.J., Filipovich, A.H., Marsh, R.A., Jodele, S., Blood, and not urine, BK viral load predicts renal outcome in children with hemorrhagic cystitis following hematopoietic stem cell transplantation. Biol. Blood Marrow Transplant. 17 (2011), 1512–1519.
19. 19 Milano, F., Gooley, T., Wood, B., Woolfrey, A., Flowers, M.E., Doney, K., Witherspoon, R., Mielcarek, M., Deeg, J.H., Sorror, M., et al. Cord-Blood Transplantation in Patients with Minimal Residual Disease. N. Engl. J. Med. 375 (2016), 944–953.
20. 20 Rooney, C.M., Smith, C.A., Ng, C.Y., Loftin, S., Li, C., Krance, R.A., Brenner, M.K., Heslop, H.E., Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345 (1995), 9–13.
21. 21 Doubrovina, E., Oflaz-Sozmen, B., Prockop, S.E., Kernan, N.A., Abramson, S., Teruya-Feldstein, J., Hedvat, C., Chou, J.F., Heller, G., Barker, J.N., et al. Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood 119 (2012), 2644–2656.
22. 22 Peggs, K.S., Verfuerth, S., Pizzey, A., Khan, N., Guiver, M., Moss, P.A., Mackinnon, S., Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362 (2003), 1375–1377.
23. 23 Hanley, P.J., Bollard, C.M., Brunstein, C.G., Adoptive immunotherapy with the use of regulatory T cells and virus-specific T cells derived from cord blood. Cytotherapy 17 (2015), 749–755.
24. 24 Gerdemann, U., Keirnan, J.M., Katari, U.L., Yanagisawa, R., Christin, A.S., Huye, L.E., Perna, S.K., Ennamuri, S., Gottschalk, S., Brenner, M.K., et al. Rapidly generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol. Ther. 20 (2012), 1622–1632.
25. 25 Papadopoulou, A., Gerdemann, U., Katari, U.L., Tzannou, I., Liu, H., Martinez, C., Leung, K., Carrum, G., Gee, A.P., Vera, J.F., et al. Activity of broad-spectrum T cells as treatment for AdV, EBV, CMV, BKV, and HHV6 infections after HSCT. Sci. Transl. Med., 6, 2014, 242ra83.
26. 26 Naik, S., Nicholas, S.K., Martinez, C.A., Leen, A.M., Hanley, P.J., Gottschalk, S.M., Rooney, C.M., Hanson, I.C., Krance, R.A., Shpall, E.J., et al. Adoptive immunotherapy for primary immunodeficiency disorders with virus-specific T lymphocytes. J. Allergy Clin. Immunol. 137 (2016), 1498–1505.e1.
27. 27 Hanley, P.J., Cruz, C.R., Savoldo, B., Leen, A.M., Stanojevic, M., Khalil, M., Decker, W., Molldrem, J.J., Liu, H., Gee, A.P., et al. Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood 114 (2009), 1958–1967.
28. 28 Hanley, P.J., Melenhorst, J.J., Nikiforow, S., Scheinberg, P., Blaney, J.W., Demmler-Harrison, G., Cruz, C.R., Lam, S., Krance, R.A., Leung, K.S., et al. CMV-specific T cells generated from naïve T cells recognize atypical epitopes and may be protective in vivo. Sci. Transl. Med., 7, 2015, 285ra63.
29. 29 Sun, Q., Burton, R.L., Pollok, K.E., Emanuel, D.J., Lucas, K.G., CD4(+) Epstein-Barr virus-specific cytotoxic T-lymphocytes from human umbilical cord blood. Cell. Immunol. 195 (1999), 81–88.
30. 30 Szabolcs, P., Niedzwiecki, D., Immune reconstitution after unrelated cord blood transplantation. Cytotherapy 9 (2007), 111–122.
31. 31 Savoldo, B., Cubbage, M.L., Durett, A.G., Goss, J., Huls, M.H., Liu, Z., Teresita, L., Gee, A.P., Ling, P.D., Brenner, M.K., et al. Generation of EBV-specific CD4+ cytotoxic T cells from virus naive individuals. J. Immunol. 168 (2002), 909–918.
32. 32 Hanley, P.J., Shaffer, D.R., Cruz, C.R., Ku, S., Tzou, B., Liu, H., Demmler-Harrison, G., Heslop, H.E., Rooney, C.M., Gottschalk, S., Bollard, C.M., Expansion of T cells targeting multiple antigens of cytomegalovirus, Epstein-Barr virus and adenovirus to provide broad antiviral specificity after stem cell transplantation. Cytotherapy 13 (2011), 976–986.
33. 33 Ngo, M.C., Ando, J., Leen, A.M., Ennamuri, S., Lapteva, N., Vera, J.F., Min-Venditti, A., Mims, M.P., Heslop, H.E., Bollard, C.M., et al. Complementation of antigen-presenting cells to generate T lymphocytes with broad target specificity. J. Immunother. 37 (2014), 193–203.
34. 34 Serrano, L.M., Pfeiffer, T., Olivares, S., Numbenjapon, T., Bennitt, J., Kim, D., Smith, D., McNamara, G., Al-Kadhimi, Z., Rosenthal, J., et al. Differentiation of naive cord-blood T cells into CD19-specific cytolytic effectors for posttransplantation adoptive immunotherapy. Blood 107 (2006), 2643–2652.
35. 35 Merindol, N., Grenier, A.J., Caty, M., Charrier, E., Duval, A., Duval, M., Champagne, M.A., Soudeyns, H., Umbilical cord blood T cells respond against the Melan-A/MART-1 tumor antigen and exhibit reduced alloreactivity as compared with adult blood-derived T cells. J. Immunol. 185 (2010), 856–866.
36. 36 Vera, J.F., Brenner, L.J., Gerdemann, U., Ngo, M.C., Sili, U., Liu, H., Wilson, J., Dotti, G., Heslop, H.E., Leen, A.M., Rooney, C.M., Accelerated production of antigen-specific T cells for preclinical and clinical applications using gas-permeable rapid expansion cultureware (G-Rex). J. Immunother. 33 (2010), 305–315.
37. 37 Leen, A.M., Bollard, C.M., Mendizabal, A.M., Shpall, E.J., Szabolcs, P., Antin, J.H., Kapoor, N., Pai, S.Y., Rowley, S.D., Kebriaei, P., et al. Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 121 (2013), 5113–5123.
38. 38 Haque, T., McAulay, K.A., Kelly, D., Crawford, D.H., Allogeneic T-cell therapy for Epstein-Barr virus-positive posttransplant lymphoproliferative disease: long-term follow-up. Transplantation 90 (2010), 93–94.
39. 39 Barker, J.N., Doubrovina, E., Sauter, C., Jaroscak, J.J., Perales, M.A., Doubrovin, M., Prockop, S.E., Koehne, G., O'Reilly, R.J., Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood 116 (2010), 5045–5049.
40. 40 Uhlin, M., Gertow, J., Uzunel, M., Okas, M., Berglund, S., Watz, E., Brune, M., Ljungman, P., Maeurer, M., Mattsson, J., Rapid salvage treatment with virus-specific T cells for therapy-resistant disease. Clin. Infect. Dis. 55 (2012), 1064–1073.
41. 41 O'Reilly, R.J., Prockop, S., Hasan, A.N., Koehne, G., Doubrovina, E., Virus-specific T-cell banks for ‘off the shelf’ adoptive therapy of refractory infections. Bone Marrow Transplant. 51 (2016), 1163–1172.
42. 42 Hanley, P.J., Lam, S., Shpall, E.J., Bollard, C.M., Expanding cytotoxic T lymphocytes from umbilical cord blood that target cytomegalovirus, Epstein-Barr virus, and adenovirus. J. Vis. Exp., 3627, 2012, e3627.