Engineering HIV-Resistant, Anti-HIV Chimeric Antigen Receptor T Cells

Molecular Therapy

Volumn 25, Issue 3, 2017, Pages 570-579

  Hale, Malika ^a   Mesojednik, Taylor ^b   Romano Ibarra, Guillermo S ^a   Sahni, Jaya ^a   Bernard, Alison ^b   Sommer, Karen ^a   Scharenberg, Andrew M ^a,c,d   Rawlings, David J ^a,c,d   Wagner, Thor A ^b,c  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

CAR T cell; cell therapy; chimeric antigen receptor; gene editing; HIV

Indexed keywords

BROADLY NEUTRALIZING MONOCLONAL ANTIBODY; CHEMOKINE RECEPTOR CCR5; CHIMERIC ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG; EPITOPE; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; NEUTRALIZING ANTIBODY;

ANTIVIRAL ACTIVITY; ARTICLE; CD3+ T LYMPHOCYTE; CELL ACTIVATION; CELL ENGINEERING; CELL KILLING; CONTROLLED STUDY; DRUG TARGETING; FEASIBILITY STUDY; GENE CASSETTE; GENE EDITING; GENE LOCUS; GENETIC RECOMBINATION; HOMOLOGY DIRECTED RECOMBINATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOTHERAPY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS RESISTANCE; CYTOTOXICITY; GENE ORDER; GENE VECTOR; GENETIC ENGINEERING; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBPOPULATION; METABOLISM;

ANTIBODIES, NEUTRALIZING; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; GENE ORDER; GENETIC ENGINEERING; GENETIC VECTORS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBSETS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CCR5; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; VIRUS REPLICATION;

EID: 85016249693     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1016/j.ymthe.2016.12.023     Document Type: Article

References (74)

1. 1 Joint United Nations Programme on HIV/AIDS (UNAIDS) (2016). Global AIDS Response Progress Reporting. https://aidsreportingtool.unaids.org/static/docs/GARPR_Guidelines_2016_EN.pdf.
2. 2 Palella, F.J. Jr., Baker, R.K., Moorman, A.C., Chmiel, J.S., Wood, K.C., Brooks, J.T., Holmberg, S.D., HIV Outpatient Study Investigators. Mortality in the highly active antiretroviral therapy era: changing causes of death and disease in the HIV outpatient study. J. Acquir. Immune Defic. Syndr. 43 (2006), 27–34.
3. 3 Deeken, J.F., Tjen-A-Looi, A., Rudek, M.A., Okuliar, C., Young, M., Little, R.F., Dezube, B.J., The rising challenge of non-AIDS-defining cancers in HIV-infected patients. Clin. Infect. Dis. 55 (2012), 1228–1235.
4. 4 Triant, V.A., Josephson, F., Rochester, C.G., Althoff, K.N., Marcus, K., Munk, R., Cooper, C., D'Agostino, R.B., Costagliola, D., Sabin, C.A., et al. Adverse outcome analyses of observational data: assessing cardiovascular risk in HIV disease. Clin. Infect. Dis. 54 (2012), 408–413.
5. 5 Mothobi, N.Z., Brew, B.J., Neurocognitive dysfunction in the highly active antiretroviral therapy era. Curr. Opin. Infect. Dis. 25 (2012), 4–9.
6. 6 Harrison, K.M., Song, R., Zhang, X., Life expectancy after HIV diagnosis based on national HIV surveillance data from 25 states, United States. J. Acquir. Immune Defic. Syndr. 53 (2010), 124–130.
7. 7 Romeo, C., Seed, B., Cellular immunity to HIV activated by CD4 fused to T cell or Fc receptor polypeptides. Cell 64 (1991), 1037–1046.
8. 8 Yang, O.O., Tran, A.C., Kalams, S.A., Johnson, R.P., Roberts, M.R., Walker, B.D., Lysis of HIV-1-infected cells and inhibition of viral replication by universal receptor T cells. Proc. Natl. Acad. Sci. USA 94 (1997), 11478–11483.
9. 9 Masiero, S., Del Vecchio, C., Gavioli, R., Mattiuzzo, G., Cusi, M.G., Micheli, L., Gennari, F., Siccardi, A., Marasco, W.A., Palù, G., Parolin, C., T-cell engineering by a chimeric T-cell receptor with antibody-type specificity for the HIV-1 gp120. Gene Ther. 12 (2005), 299–310.
10. 10 Zhen, A., Kamata, M., Rezek, V., Rick, J., Levin, B., Kasparian, S., Chen, I.S., Yang, O.O., Zack, J.A., Kitchen, S.G., HIV-specific Immunity Derived From Chimeric Antigen Receptor-engineered Stem Cells. Mol. Ther. 23 (2015), 1358–1367.
11. 11 Wang, C.X., Cannon, P.M., The clinical applications of genome editing in HIV. Blood 127 (2016), 2546–2552.
12. 12 Furtado, M.R., Callaway, D.S., Phair, J.P., Kunstman, K.J., Stanton, J.L., Macken, C.A., Perelson, A.S., Wolinsky, S.M., Persistence of HIV-1 transcription in peripheral-blood mononuclear cells in patients receiving potent antiretroviral therapy. N. Engl. J. Med. 340 (1999), 1614–1622.
13. 13 Santosuosso, M., Righi, E., Lindstrom, V., Leblanc, P.R., Poznansky, M.C., HIV-1 envelope protein gp120 is present at high concentrations in secondary lymphoid organs of individuals with chronic HIV-1 infection. J. Infect. Dis. 200 (2009), 1050–1053.
14. 14 Palmer, S., Maldarelli, F., Wiegand, A., Bernstein, B., Hanna, G.J., Brun, S.C., Kempf, D.J., Mellors, J.W., Coffin, J.M., King, M.S., Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc. Natl. Acad. Sci. USA 105 (2008), 3879–3884.
15. 15 Pasternak, A.O., Jurriaans, S., Bakker, M., Prins, J.M., Berkhout, B., Lukashov, V.V., Cellular levels of HIV unspliced RNA from patients on combination antiretroviral therapy with undetectable plasma viremia predict the therapy outcome. PLoS ONE, 4, 2009, e8490.
16. 16 Hatano, H., Delwart, E.L., Norris, P.J., Lee, T.H., Neilands, T.B., Kelley, C.F., Hunt, P.W., Hoh, R., Linnen, J.M., Martin, J.N., et al. Evidence of persistent low-level viremia in long-term HAART-suppressed, HIV-infected individuals. AIDS 24 (2010), 2535–2539.
17. 17 Liu, Y., McNevin, J.P., Holte, S., McElrath, M.J., Mullins, J.I., Dynamics of viral evolution and CTL responses in HIV-1 infection. PLoS ONE, 6, 2011, e15639.
18. 18 Moore, C.B., John, M., James, I.R., Christiansen, F.T., Witt, C.S., Mallal, S.A., Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296 (2002), 1439–1443.
19. 19 Deng, K., Pertea, M., Rongvaux, A., Wang, L., Durand, C.M., Ghiaur, G., Lai, J., McHugh, H.L., Hao, H., Zhang, H., et al. Broad CTL response is required to clear latent HIV-1 due to dominance of escape mutations. Nature 517 (2015), 381–385.
20. 20 Schwartz, O., Maréchal, V., Le Gall, S., Lemonnier, F., Heard, J.M., Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2 (1996), 338–342.
21. 21 Collins, K.L., Chen, B.K., Kalams, S.A., Walker, B.D., Baltimore, D., HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391 (1998), 397–401.
22. 22 Mueller, Y.M., De Rosa, S.C., Hutton, J.A., Witek, J., Roederer, M., Altman, J.D., Katsikis, P.D., Increased CD95/Fas-induced apoptosis of HIV-specific CD8(+) T cells. Immunity 15 (2001), 871–882.
23. 23 Petrovas, C., Chaon, B., Ambrozak, D.R., Price, D.A., Melenhorst, J.J., Hill, B.J., Geldmacher, C., Casazza, J.P., Chattopadhyay, P.K., Roederer, M., et al. Differential association of programmed death-1 and CD57 with ex vivo survival of CD8+ T cells in HIV infection. J. Immunol. 183 (2009), 1120–1132.
24. 24 Elahi, S., Dinges, W.L., Lejarcegui, N., Laing, K.J., Collier, A.C., Koelle, D.M., McElrath, M.J., Horton, H., Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat. Med. 17 (2011), 989–995.
25. 25 Kolte, L., Gaardbo, J.C., Skogstrand, K., Ryder, L.P., Ersbøll, A.K., Nielsen, S.D., Increased levels of regulatory T cells (Tregs) in human immunodeficiency virus-infected patients after 5 years of highly active anti-retroviral therapy may be due to increased thymic production of naive Tregs. Clin. Exp. Immunol. 155 (2009), 44–52.
26. 26 Maude, S., Barrett, D.M., Current status of chimeric antigen receptor therapy for haematological malignancies. Br. J. Haematol. 172 (2016), 11–22.
27. 27 Ghorashian, S., Pule, M., Amrolia, P., CD19 chimeric antigen receptor T cell therapy for haematological malignancies. Br. J. Haematol. 169 (2015), 463–478.
28. 28 Porter, D.L., Levine, B.L., Kalos, M., Bagg, A., June, C.H., Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365 (2011), 725–733.
29. 29 Maus, M.V., Grupp, S.A., Porter, D.L., June, C.H., Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 123 (2014), 2625–2635.
30. 30 Deeks, S.G., Wagner, B., Anton, P.A., Mitsuyasu, R.T., Scadden, D.T., Huang, C., Macken, C., Richman, D.D., Christopherson, C., June, C.H., et al. A phase II randomized study of HIV-specific T-cell gene therapy in subjects with undetectable plasma viremia on combination antiretroviral therapy. Mol. Ther. 5 (2002), 788–797.
31. 31 Mitsuyasu, R.T., Anton, P.A., Deeks, S.G., Scadden, D.T., Connick, E., Downs, M.T., Bakker, A., Roberts, M.R., June, C.H., Jalali, S., et al. Prolonged survival and tissue trafficking following adoptive transfer of CD4zeta gene-modified autologous CD4(+) and CD8(+) T cells in human immunodeficiency virus-infected subjects. Blood 96 (2000), 785–793.
32. 32 Scholler, J., Brady, T.L., Binder-Scholl, G., Hwang, W.T., Plesa, G., Hege, K.M., Vogel, A.N., Kalos, M., Riley, J.L., Deeks, S.G., et al. Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci. Transl. Med., 4, 2012, 132ra53.
33. 33 Liu, L., Patel, B., Ghanem, M.H., Bundoc, V., Zheng, Z., Morgan, R.A., Rosenberg, S.A., Dey, B., Berger, E.A., Novel CD4-based bispecific chimeric antigen receptor designed for enhanced anti-HIV potency and absence of HIV Entry receptor activity. J. Virol. 89 (2015), 6685–6694.
34. 34 Corti, D., Lanzavecchia, A., Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 31 (2013), 705–742.
35. 35 Kwong, P.D., Mascola, J.R., Nabel, G.J., Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13 (2013), 693–701.
36. 36 Dragic, T., Litwin, V., Allaway, G.P., Martin, S.R., Huang, Y., Nagashima, K.A., Cayanan, C., Maddon, P.J., Koup, R.A., Moore, J.P., Paxton, W.A., HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381 (1996), 667–673.
37. 37 Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Di Marzio, P., Marmon, S., Sutton, R.E., Hill, C.M., et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381 (1996), 661–666.
38. 38 Huang, Y., Paxton, W.A., Wolinsky, S.M., Neumann, A.U., Zhang, L., He, T., Kang, S., Ceradini, D., Jin, Z., Yazdanbakhsh, K., et al. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat. Med. 2 (1996), 1240–1243.
39. 39 Allers, K., Hütter, G., Hofmann, J., Loddenkemper, C., Rieger, K., Thiel, E., Schneider, T., Evidence for the cure of HIV infection by CCR5Δ32/Δ32 stem cell transplantation. Blood 117 (2011), 2791–2799.
40. 40 Hütter, G., Nowak, D., Mossner, M., Ganepola, S., Müssig, A., Allers, K., Schneider, T., Hofmann, J., Kücherer, C., Blau, O., et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N. Engl. J. Med. 360 (2009), 692–698.
41. 41 Didigu, C.A., Wilen, C.B., Wang, J., Duong, J., Secreto, A.J., Danet-Desnoyers, G.A., Riley, J.L., Gregory, P.D., June, C.H., Holmes, M.C., Doms, R.W., Simultaneous zinc-finger nuclease editing of the HIV coreceptors ccr5 and cxcr4 protects CD4+ T cells from HIV-1 infection. Blood 123 (2014), 61–69.
42. 42 Mock, U., Machowicz, R., Hauber, I., Horn, S., Abramowski, P., Berdien, B., Hauber, J., Fehse, B., mRNA transfection of a novel TAL effector nuclease (TALEN) facilitates efficient knockout of HIV co-receptor CCR5. Nucleic Acids Res. 43 (2015), 5560–5571.
43. 43 Romano Ibarra, G.S., Paul, B., Sather, B.D., Younan, P.M., Sommer, K., Kowalski, J.P., Hale, M., Stoddard, B., Jarjour, J., Astrakhan, A., et al. Efficient modification of the CCR5 locus in primary human T cells with megaTAL nuclease establishes HIV-1 resistance. Mol. Ther. Nucleic Acids, 5, 2016, e352.
44. 44 Tebas, P., Stein, D., Tang, W.W., Frank, I., Wang, S.Q., Lee, G., Spratt, S.K., Surosky, R.T., Giedlin, M.A., Nichol, G., et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med. 370 (2014), 901–910.
45. 45 Ye, L., Wang, J., Beyer, A.I., Teque, F., Cradick, T.J., Qi, Z., Chang, J.C., Bao, G., Muench, M.O., Yu, J., et al. Seamless modification of wild-type induced pluripotent stem cells to the natural CCR5Δ32 mutation confers resistance to HIV infection. Proc. Natl. Acad. Sci. USA 111 (2014), 9591–9596.
46. 46 Bhoj, V.G., Thibodeaux, S.R., Levine, B.L., Novel gene and cellular therapy approaches for treating HIV. Discov. Med. 21 (2016), 283–292.
47. 47 Hubbard, N., Hagin, D., Sommer, K., Song, Y., Khan, I., Clough, C., Ochs, H.D., Rawlings, D.J., Scharenberg, A.M., Torgerson, T.R., Targeted gene editing restores regulated CD40L function in X-linked hyper-IgM syndrome. Blood 127 (2016), 2513–2522.
48. 48 Sather, B.D., Romano Ibarra, G.S., Sommer, K., Curinga, G., Hale, M., Khan, I.F., Singh, S., Song, Y., Gwiazda, K., Sahni, J., et al. Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template. Sci. Transl. Med., 7, 2015, 307ra156.
49. 49 Wang, J., Exline, C.M., DeClercq, J.J., Llewellyn, G.N., Hayward, S.B., Li, P.W., Shivak, D.A., Surosky, R.T., Gregory, P.D., Holmes, M.C., Cannon, P.M., Homology-driven genome editing in hematopoietic stem and progenitor cells using ZFN mRNA and AAV6 donors. Nat. Biotechnol. 33 (2015), 1256–1263.
50. 50 Porteus, M.H., Towards a new era in medicine: therapeutic genome editing. Genome Biol., 16, 2015, 286.
51. 51 Walker, L.M., Huber, M., Doores, K.J., Falkowska, E., Pejchal, R., Julien, J.P., Wang, S.K., Ramos, A., Chan-Hui, P.Y., Moyle, M., et al., Protocol G Principal Investigators. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477 (2011), 466–470.
52. 52 Huang, J., Ofek, G., Laub, L., Louder, M.K., Doria-Rose, N.A., Longo, N.S., Imamichi, H., Bailer, R.T., Chakrabarti, B., Sharma, S.K., et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491 (2012), 406–412.
53. 53 Rudicell, R.S., Kwon, Y.D., Ko, S.Y., Pegu, A., Louder, M.K., Georgiev, I.S., Wu, X., Zhu, J., Boyington, J.C., Chen, X., et al., NISC Comparative Sequencing Program. Enhanced potency of a broadly neutralizing HIV-1 antibody in vitro improves protection against lentiviral infection in vivo. J. Virol. 88 (2014), 12669–12682.
54. 54 Zhu, J., Ofek, G., Yang, Y., Zhang, B., Louder, M.K., Lu, G., McKee, K., Pancera, M., Skinner, J., Zhang, Z., et al., NISC Comparative Sequencing Program. Mining the antibodyome for HIV-1-neutralizing antibodies with next-generation sequencing and phylogenetic pairing of heavy/light chains. Proc. Natl. Acad. Sci. USA 110 (2013), 6470–6475.
55. 55 Zheng, Z., Chinnasamy, N., Morgan, R.A., Protein L: a novel reagent for the detection of chimeric antigen receptor (CAR) expression by flow cytometry. J. Transl. Med., 10, 2012, 29.
56. 56 Rooney, C.M., Smith, C.A., Ng, C.Y., Loftin, S.K., Sixbey, J.W., Gan, Y., Srivastava, D.K., Bowman, L.C., Krance, R.A., Brenner, M.K., Heslop, H.E., Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92 (1998), 1549–1555.
57. 57 Sommermeyer, D., Hudecek, M., Kosasih, P.L., Gogishvili, T., Maloney, D.G., Turtle, C.J., Riddell, S.R., Chimeric antigen receptor-modified T cells derived from defined CD8+ and CD4+ subsets confer superior antitumor reactivity in vivo. Leukemia 30 (2016), 492–500.
58. 58 Ali, A., Kitchen, S.G., Chen, I.S., Ng, H.L., Zack, J.A., Yang, O.O., HIV-1-Specific Chimeric Antigen Receptors Based on Broadly Neutralizing Antibodies. J. Virol. 90 (2016), 6999–7006.
59. 59 Chakrabarti, B.K., Walker, L.M., Guenaga, J.F., Ghobbeh, A., Poignard, P., Burton, D.R., Wyatt, R.T., Direct antibody access to the HIV-1 membrane-proximal external region positively correlates with neutralization sensitivity. J. Virol. 85 (2011), 8217–8226.
60. 60 Brudno, J.N., Kochenderfer, J.N., Toxicities of chimeric antigen receptor T cells: recognition and management. Blood 127 (2016), 3321–3330.
61. 61 Lee, D.W., Gardner, R., Porter, D.L., Louis, C.U., Ahmed, N., Jensen, M., Grupp, S.A., Mackall, C.L., Current concepts in the diagnosis and management of cytokine release syndrome. Blood 124 (2014), 188–195.
62. 62 Hill, A.L., Rosenbloom, D.I., Goldstein, E., Hanhauser, E., Kuritzkes, D.R., Siliciano, R.F., Henrich, T.J., Real-time predictions of reservoir size and rebound time during antiretroviral therapy interruption trials for HIV. PLoS Pathog., 12, 2016, e1005535.
63. 63 Laird, G.M., Bullen, C.K., Rosenbloom, D.I., Martin, A.R., Hill, A.L., Durand, C.M., Siliciano, J.D., Siliciano, R.F., Ex vivo analysis identifies effective HIV-1 latency-reversing drug combinations. J. Clin. Invest. 125 (2015), 1901–1912.
64. 64 Milone, M.C., Fish, J.D., Carpenito, C., Carroll, R.G., Binder, G.K., Teachey, D., Samanta, M., Lakhal, M., Gloss, B., Danet-Desnoyers, G., et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17 (2009), 1453–1464.
65. 65 Challita, P.M., Skelton, D., el-Khoueiry, A., Yu, X.J., Weinberg, K., Kohn, D.B., Multiple modifications in cis elements of the long terminal repeat of retroviral vectors lead to increased expression and decreased DNA methylation in embryonic carcinoma cells. J. Virol. 69 (1995), 748–755.
66. 66 Clouse, K.A., Powell, D., Washington, I., Poli, G., Strebel, K., Farrar, W., Barstad, P., Kovacs, J., Fauci, A.S., Folks, T.M., Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J. Immunol. 142 (1989), 431–438.
67. 67 Folks, T.M., Clouse, K.A., Justement, J., Rabson, A., Duh, E., Kehrl, J.H., Fauci, A.S., Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc. Natl. Acad. Sci. USA 86 (1989), 2365–2368.
68. 68 Buttke, T.M., Folks, T.M., Complete replacement of membrane cholesterol with 4,4′,14-trimethyl sterols in a human T cell line defective in lanosterol demethylation. J. Biol. Chem. 267 (1992), 8819–8826.
69. 69 Folks, T., Benn, S., Rabson, A., Theodore, T., Hoggan, M.D., Martin, M., Lightfoote, M., Sell, K., Characterization of a continuous T-cell line susceptible to the cytopathic effects of the acquired immunodeficiency syndrome (AIDS)-associated retrovirus. Proc. Natl. Acad. Sci. USA 82 (1985), 4539–4543.
70. 70 Wang, J., Press, O.W., Lindgren, C.G., Greenberg, P., Riddell, S., Qian, X., Laugen, C., Raubitschek, A., Forman, S.J., Jensen, M.C., Cellular immunotherapy for follicular lymphoma using genetically modified CD20-specific CD8+ cytotoxic T lymphocytes. Mol. Ther. 9 (2004), 577–586.
71. 71 Cann, A.J., Zack, J.A., Go, A.S., Arrigo, S.J., Koyanagi, Y., Green, P.L., Koyanagi, Y., Pang, S., Chen, I.S., Human immunodeficiency virus type 1 T-cell tropism is determined by events prior to provirus formation. J. Virol. 64 (1990), 4735–4742.
72. 72 Koyanagi, Y., Miles, S., Mitsuyasu, R.T., Merrill, J.E., Vinters, H.V., Chen, I.S., Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236 (1987), 819–822.
73. 73 McClure, J., van't Wout, A.B., Tran, T., Mittler, J.E., Granulocyte-monocyte colony-stimulating factor upregulates HIV-1 replication in monocyte-derived macrophages cultured at low density. J. Acquir. Immune Defic. Syndr. 44 (2007), 254–261.
74. 74 Sourisseau, M., Sol-Foulon, N., Porrot, F., Blanchet, F., Schwartz, O., Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81 (2007), 1000–1012.