Combinatorial anti-HIV gene therapy: Using a multipronged approach to reach beyond HAART

Gene Therapy

Volumn 20, Issue 7, 2013, Pages 695-702

  Peterson, C W ^a   Younan, P ^a   Jerome, K R ^a,b   Kiem, H P ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Berlin Patient; CCR5; Gene disruption; HIV; Restriction factors; Stem cells

Indexed keywords

ANTIRETROVIRUS AGENT; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ERADICATION THERAPY; GENE THERAPY; HEMATOPOIETIC CELL; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; REVIEW; VIRAL GENE DELIVERY SYSTEM; VIRUS REPLICATION; VIRUS UNCOATING;

ANTIGENS, CD34; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CD4-POSITIVE T-LYMPHOCYTES; GENETIC THERAPY; HEMATOPOIETIC STEM CELLS; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR TARGETED THERAPY; RECEPTORS, CCR5; RECEPTORS, CXCR4; VIRUS REPLICATION;

PRIMATES;

EID: 84880245757     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2012.98     Document Type: Review

References (120)

1. Camacho R, Teofilo E. Antiretroviral therapy in treatment-naive patients with HIV infection [review]. Curr Opin HIV AIDS 2011; 6(Suppl 1): S3-S11.
2. May MT, Ingle SM. Life expectancy of HIV-positive adults: a review [review]. Sex Health 2011; 8: 526-533.
3. Shen L, Siliciano RF. Viral reservoirs, residual viremia, and the potential of highly active antiretroviral therapy to eradicate HIV infection [review]. J Allergy Clin Immunol 2008; 122: 22-28.
4. Williams BG, Lima V, Gouws E. Modelling the impact of antiretroviral therapy on the epidemic of HIV [review]. Curr HIV Res 2011; 9: 367-382.
5. Blas-Garcia A, Apostolova N, Esplugues JV. Oxidative stress and mitochondrial impairment after treatment with anti-HIV drugs: clinical implications [review]. Curr Pharm Des 2011; 17: 4076-4086.
6. Fisher SD, Kanda BS, Miller TL, Lipshultz SE. Cardiovascular disease and therapeutic drug-related cardiovascular consequences in HIV-infected patients [review]. Am J Cardiovasc Drugs 2011; 11: 383-394.
7. Mothobi NZ, Brew BJ. Neurocognitive dysfunction in the highly active antiretroviral therapy era [review]. Curr Opin Inf Dis 2012; 25: 4-9.
8. Palios J, Kadoglou NP, Lampropoulos S. The pathophysiology of HIV-/ HAART-related metabolic syndrome leading to cardiovascular disorders: the emerging role of adipokines [review]. Exp Diabetes Res 2012; 2012: 103063.
9. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, Allers K et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 2009; 360: 692-698.
10. Allers K, Hutter G, Hofmann J, Loddenkemper C, Rieger K, Thiel E et al. Evidence for the cure of HIV infection by CCR5D32/D32 stem cell transplantation. Blood 2011; 117: 2791-2799.
11. Hutter G, Thiel E. Allogeneic transplantation of CCR5-deficient progenitor cells in a patient with HIV infection: an update after years and the search for patient no. 2. AIDS 2011; 25: 273-274.
12. Hutter G, Ganepola S. Eradication of HIV by transplantation of CCR5-deficient hematopoietic stem cells. Scientific World J 2011; 11: 1068-1076.
13. Kamp C, Wolf T, Bravo IG, Kraus B, Krause B, Neumann B et al. Decreased HIV diversity after allogeneic stem cell transplantation of an HIV-1 infected patient: a case report. Virol J 2010; 7: 55.
14. Hutter G, Zaia JA. Allogeneic haematopoietic stem cell transplantation in patients with human immunodeficiency virus: the experiences of more than years [review]. Clin Exp Immunol 2011; 163: 284-295.
15. Durand C, Ambinder R, Blankson J, Forman S. HIV-1 and hematopoietic stem cell transplantation [review]. Biol Blood Marrow Transplant 2012; 18: S172-S176.
16. Kiem H-P, Jerome KR, Deeks SG, McCune JM. Hematopoietic-stem-cell-based gene therapy for HIV disease [Review]. Cell Stem Cell 2012; 10: 137-147.
17. Lai Y. CCR5-targeted hematopoietic stem cell gene approaches for HIV disease: current progress and future prospects. Curr Stem Cell Res Ther 2012; 7: 310-317.
18. Scherer LJ, Rossi JJ. Ex vivo gene therapy for HIV-1 treatment [review]. Hum Mol Genet 2011; 20: R100-R107.
19. Arrildt KT, Joseph SB, Swanstrom R. The HIV-1 env protein: a coat of many colors [review]. Curr HIV/AIDS Rep 2012; 9: 52-63.
20. Wilen CB, Tilton JC, Doms RW. Molecular mechanisms of HIV entry [review]. Adv Exp Med Biol 2012; 726: 223-242.
21. Durand CM, Ghiaur G, Siliciano JD, Rabi SA, Eisele EE, Salgado M et al. HIV-1 DNA is detected in bone marrow populations containing CD4 T cells but is not found in purified CD34 hematopoietic progenitor cells in most patients on antiretroviral therapy. J Infect Dis 2012; 205: 1014-1018.
22. Josefsson L, Eriksson S, Sinclair E, Ho T, Killian M, Epling L et al. Hematopoietic precursor cells isolated from patients on long-term suppressive HIV therapy did not contain HIV-1 DNA. J Infect Dis 2012; 206: 28-34.
23. McNamara LA, Collins KL. Hematopoietic stem/precursor cells as HIV reservoirs [review]. Curr Opin HIV AIDS 2011; 6: 43-48.
24. McNamara LA, Ganesh JA, Collins KL. Latent HIV-1 infection occurs in multiple subsets of hematopoietic progenitor cells and is reversed by NF-kappa beta activation. J Virol 2012; 86: 9337-9350.
25. Friedrich BM, Dziuba N, Li G, Endsley MA, Murray JL, Ferguson MR. Host factors mediating HIV-1 replication [review]. Virus Res 2011; 161: 101-114.
26. Loftin LM, Kienzle M, Yi Y, Collman RG. R5-4 HIV-1 coreceptor use in primary target cells: implications for coreceptor entry blocking strategies [review]. J Transl Med 2011; 9(Suppl 1): S3.
27. Didigu CA, Doms RW. Novel approaches to inhibit HIV entry [review]. Viruses 2012; 4: 309-324.
28. Zeier MD, Nachega JB. Targeting HIV: past, present and future [review]. Infect Disord Drug Targets 2011; 11: 98-114.
29. Melum E, Karlsen TH, Broome U, Thorsby E, Schrumpf E, Boberg KM et al. The 32- base pair deletion of the chemokine receptor gene (CCR5-Delta32) is not associated with primary sclerosing cholangitis in 363 Scandinavian patients [Erratum appears in Tissue Antigens 2006; 68(2): 192]. Tissue Antigen 2006; 68: 78-81.
30. Muntinghe FL, Carrero JJ, Navis G, Stenvinkel P. TNF-alpha levels are not increased in inflamed patients carrying the CCR5 deletion 32. Cytokine 2011; 53: 16-18.
31. Kamkamidze G, Capoulade-Metay C, Butsashvili M, Dudoit Y, Chubinishvili O, Debre P et al. 32-Nucleotide deletion, associated with defence against HIV/AIDS, is a predominant mutation of CCR5 gene in the population of Georgia. Georgian Med News 2005 74-79.
32. Novembre J, Galvani AP, Slatkin M. The geographic spread of the CCR5 Delta32 HIV-resistance allele. PLoS Biol 2005; 3: e339.
33. Poljak M, Maver PJ, Seme K. Prevalence of CCR5 gene 32-basepair deletion in populations of Slavic origin. Croat Med J 2006; 47: 348-349.
34. Cannon P, June C. Chemokine receptor knockout strategies [review]. Curr Opin HIV AIDS 2011; 6: 74-79.
35. Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, Liu O et al. Establishment of HIV-1 resistance in CD4 T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 2008; 26: 808-816.
36. Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 2010; 28: 839-847.
37. Walker JE, Chen RX, McGee J, Nacey C, Pollard RB, Abedi M et al. Generation of an HIV-1-resistant immune system with CD34() hematopoietic stem cells transduced with a triple-combination anti-HIV lentiviral vector. J Virol 2012; 86: 5719-5729.
38. Anderson JS, Javien J, Nolta JA, Bauer G. Preintegration HIV-1 inhibition by a combination lentiviral vector containing a chimeric TRIM5 alpha protein, a CCR5 shRNA, and a TAR decoy. Mol Ther 2009; 17: 2103-2114.
39. Carroll D. Genome engineering with zinc-finger nucleases [review]. Genetics 2011; 188: 773-782.
40. Scholze H, Boch J. TAL effectors are remote controls for gene activation [review]. Curr Opin Microbiol 2011; 14: 47-53.
41. Stoddard BL. Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification [review]. Structure 2011; 19: 7-15.
42. Grabarz A, Barascu A, Guirouilh-Barbat J, Lopez BS. Initiation of DNA double strand break repair: signaling and single-stranded resection dictate the choice between homologous recombination, non-homologous end-joining and alternative end-joining. Am J Cancer Res 2012; 2: 249-268.
43. Munoz IG, Prieto J, Subramanian S, Coloma J, Redondo P, Villate M et al. Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res 2011; 39: 729-743.
44. Overlack N, Goldmann T, Wolfrum U, Nagel-Wolfrum K. Gene repair of an usher syndrome causing mutation by zinc-finger nuclease mediated homologous recombination. Invest Ophthalmol Vis Sci 2012; 53: 4140-4146.
45. Ghardi M, Moreels M, Chatelain B, Chatelain C, Baatout S. Radiation-induced double strand breaks and subsequent apoptotic DNA fragmentation in human peripheral blood mononuclear cells. Int J Mol Med 2012; 29: 769-780.
46. Mittelman D, Moye C, Morton J, Sykoudis K, Lin Y, Carroll D et al. Zinc-finger directed double-strand breaks within CAG repeat tracts promote repeat instability in human cells. Proc Natl Acad Sci USA 2009; 106: 9607-9612.
47. Herrmann F, Garriga-Canut M, Baumstark R, Fajardo-Sanchez E, Cotterell J, Minoche A et al. P53 gene repair with zinc finger nucleases optimised by yeast 1-hybrid and validated by Solexa sequencing. PLoS One 2011; 6: e20913.
48. Reyon D, Kirkpatrick JR, Sander JD, Zhang F, Voytas DF, Joung JK et al. ZFNGenome: a comprehensive resource for locating zinc finger nuclease target sites in model organisms. BMC Genom 2011; 12: 83.
49. Cassidy LD, Venkitaraman AR. Genome instability mechanisms and the structure of cancer genomes [review]. Curr Opin Genet Dev 2012; 22: 10-13.
50. Cunderlikova? B. Issues to be considered when studying cancer in vitro. Crit Rev Oncol Hematol 2012 (E-pub ahead of print July 2012).
51. Qiu S, Yi H, Hu J, Cao Z, Wu Y, Li W. The binding mode of fusion inhibitor T20 onto HIV-1 gp41 and relevant T20-resistant mechanisms explored by computational study. Curr HIV Res 2012; 10: 182-194.
52. Trobridge GD, Wu RA, Beard BC, Chiu SY, Muñ oz NM, von Laer D et al. Protection of stem cell-derived lymphocytes in a primate AIDS gene therapy model after in vivo selection. PLoS One 2009; 4: e7693.
53. Zahn RC, Hermann FG, Kim EY, Rett MD, Wolinsky SM, Johnson RP et al. Efficient entry inhibition of human and nonhuman primate immunodeficiency virus by cell surface-expressed gp41-derived peptides. Gene Therapy 2008; 15: 1210-1222.
54. Cossarini F, Galli A, Galli L, Bigoloni A, Salpietro S, Vinci C et al. Immune recovery and T cell subset analysis during effective treatment with maraviroc. J Antimicrob Chemother 2012; 67: 2474-2478.
55. LaBrecque J, Metz M, Lau G, Darkes MC, Wong RS, Bogucki D et al. HIV-1 entry inhibition by small-molecule CCR5 antagonists: a combined molecular modeling and mutant study using a high-throughput assay. Virology 2011; 413: 231-243.
56. Shin N, Solomon K, Zhou N, Wang KH, Garlapati V, Thomas B et al. Identification and characterization of INCB9471, an allosteric noncompetitive small-molecule antagonist of C-C chemokine receptor with potent inhibitory activity against monocyte migration and HIV-1 infection. J Pharmacol Exp Ther 2011; 338: 228-239.
57. Fessel WJ, Anderson B, Follansbee SE, Winters MA, Lewis ST, Weinheimer SP et al. The efficacy of an anti-CD4 monoclonal antibody for HIV-1 treatment. Antiviral Res 2011; 92: 484-487.
58. Jacobson JM, Thompson MA, Lalezari JP, Saag MS, Zingman BS, D'Ambrosio P et al. Anti-HIV-1 activity of weekly or biweekly treatment with subcutaneous PRO 140, a CCR5 monoclonal antibody. J Infect Dis 2010; 201: 1481-1487.
59. Duenas-Decamp MJ, O'Connell OJ, Corti D, Zolla-Pazner S, Clapham PR. The W100 pocket on HIV-1 gp120 penetrated by b12 is not a target for other CD4bs monoclonal antibodies. Retrovirology 2012; 9: 9.
60. Da LT, Quan JM, Wu YD. Understanding the binding mode and function of BMS-488043 against HIV-1 viral entry. Proteins 2011; 79: 1810-1819.
61. Duong YT, Meadows DC, Srivastava IK, Gervay-Hague J, North TW. Direct inactivation of human immunodeficiency virus type by a novel small-molecule entry inhibitor, DCM205. Antimicrob Agents Chemother 2007; 51: 1780-1786.
62. Kawai K, Tsuno NH, Kitayama J, Okaji Y, Yazawa K, Asakage M et al. Epigallocatechin gallate, the main component of tea polyphenol, binds to CD4 and interferes with gp120 binding. J Allergy Clin Immunol 2003; 112: 951-957.
63. Xue J, Gao Y, Hoorelbeke B, Kagiampakis I, Zhao B, Demeler B et al. The role of individual carbohydrate-binding sites in the function of the potent anti-HIV lectin Griffithsin. Mol Pharm 2012; 9: 2613-2625E-pub ahead of print July 2012
64. Fink RC, Roschek Jr. B, Alberte RS. HIV type-1 entry inhibitors with a new mode of action. Antivir Chem Chemother 2009; 19: 243-255.
65. Gascoigne NR, Palmer E. Signaling in thymic selection [review]. Curr Opin Immunol 2011; 23: 207-212.
66. Nepom GT. MHC class II tetramers [review]. J Immunol 2012; 188: 2477-2482.
67. Edling AE, Choksi S, Huang Z, Korngold R. An organic CD4 inhibitor reduces the clinical and pathological symptoms of acute experimental allergic encephalomyelitis. J Autoimmun 2002; 18: 169-179.
68. Xiao H, Zhang H, Yu ZY, Zhang L, Yu M, Huang YF et al. J2 prolongs the corneal allograft survival through inhibition of the CD4 T cell-mediated response in vivo. Transpl Immunol 2007; 18: 130-137.
69. Wilen CB, Wang J, Tilton JC, Miller JC, Kim KA, Rebar EJ et al. Engineering HIV-resistant human CD4 T cells with CXCR4-specific zinc-finger nucleases. PLoS Pathogen 2011; 7: e1002020.
70. Yuan J, Wang J, Crain K, Fearns C, Kim KA, Hua KL et al. Zinc-finger nuclease editing of human cxcr4 promotes HIV-1 CD4() T cell resistance and enrichment. Mol Ther 2012; 20: 849-859.
71. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 1998; 393: 591-594.
72. Chung SH, Seki K, Choi BI, Kimura KB, Ito A, Fujikado N et al. CXC chemokine receptor expressed in T cells plays an important role in the development of collagen-induced arthritis. Arthritis Res Ther 2010; 12: R188.
73. Laguette N, Benkirane M. How SAMHD1 changes our view of viral restriction [review]. Trends Immunol 2012; 33: 26-33.
74. Yan N, Chen ZJ. Intrinsic antiviral immunity [review]. Nat Immunol 2012; 13: 214-222.
75. Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008; 451: 425-430.
76. Hosseini I, Gabhann FM. Multi-scale modeling of HIV infection in vitro and APOBEC3G-based anti-retroviral therapy. PLoS Comput Biol 2012; 8: e1002371.
77. Pham QT, Bouchard A, Grutter MG, Berthoux L. Generation of human TRIM5alpha mutants with high HIV-1 restriction activity. Gene Therapy 2010; 17: 859-871.
78. Martin KL, Johnson M, D'Aquila RT. APOBEC3G complexes decrease human immunodeficiency virus type production. J Virol 2011; 85: 9314-9326.
79. Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: basic to translational [review]. Biochem J 2012; 443: 603-618.
80. Li X, Sodroski J. The TRIM5alpha B-box domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J Virol 2008; 82: 11495-11502.
81. Ganser-Pornillos BK, Chandrasekaran V, Pornillos O, Sodroski JG, Sundquist WI, Yeager M. Hexagonal assembly of a restricting TRIM5alpha protein. Proc Natl Acad Sci USA 2011; 108: 534-539.
82. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, Dekelver RC et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 2009; 27: 851-857.
83. Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 2007; 25: 1298-1306.
84. Rosenberg BR, Hamilton CE, Mwangi MM, Dewell S, Papavasiliou FN. Transcriptome- wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript UTRs [Erratum appears in Nat Struct Mol Biol 2012 Mar; 19(3): 364]. Nat Struct Mol Biol 2011; 18: 230-236.
85. Paz-Yaacov N, Levanon EY, Nevo E, Kinar Y, Harmelin A, Jacob-Hirsch J et al. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proc Natl Acad Sci USA 2010; 107: 12174-12179.
86. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011; 472: 361-365.
87. Tareen SU, Emerman M. Human Trim5alpha has additional activities that are uncoupled from retroviral capsid recognition. Virology 2011; 409: 113-120.
88. Anderson J, Akkina R. TRIM5alpharh expression restricts HIV-1 infection in lentiviral vector-transduced CD34-cell-derived macrophages. Mol Ther 2005; 12: 687-696.
89. Tyagi M, Bukrinsky M. HIV latency: the major hurdle in HIV eradication. Mol Med 2012; 18: 1096-1108.
90. Chun TW, Justement JS, Murray D, Hallahan CW, Maenza J, Collier AC et al. Rebound of plasma viremia following cessation of antiretroviral therapy despite profoundly low levels of HIV reservoir: implications for eradication. AIDS 2010; 24: 2803-2808.
91. Luo R, Piovoso MJ, Martinez-Picado J, Zurakowski R. HIV model parameter estimates from interruption trial data including drug efficacy and reservoir dynamics. PLoS One 2012; 7: e40198.
92. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 2012; 487: 482-485.
93. Gallastegui E, Marshall B, Vidal D, Sanchez-Duffhues G, Collado JA, Alvarez-Fernandez C et al. Combination of biological screening in a cellular model of viral latency and virtual screening identifies novel compounds that reactivate HIV-1. J Virol 2012; 86: 3795-3808.
94. Xing S, Bullen CK, Shroff NS, Shan L, Yang HC, Manucci JL et al. Disulfiram reactivates latent HIV-1 in a Bcl-2-transduced primary CD4 T cell model without inducing global T cell activation. J Virol 2011; 85: 6060-6064.
95. Shan L, Deng K, Shroff NS, Durand CM, Rabi SA, Yang HC et al. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 2012; 36: 491-501.
96. Lafeuillade A. Eliminating the HIV reservoir [review]. Curr HIV/AIDS Rep 2012; 9: 121-131.
97. Forde J, Volpe JM, Ciupe SM. Latently infected cell activation: a way to reduce the size of the HIV reservoir? Bull Math Biol 2012; 74: 1651-1672.
98. Aubert M, Ryu BY, Banks L, Rawlings DJ, Scharenberg AM, Jerome KR. Successful targeting and disruption of an integrated reporter lentivirus using the engineered homing endonuclease Y2 I-AniI. PLoS One 2011; 6: e16825 (Electronic Resource).
99. Schiffer JT, Aubert M, Weber N, Mintzer E, Stone D, Jerome KR. Targeted DNA mutagenesis for the cure of chronic viral infections. J Virol 2012; 86: 8920-8936.
100. Mbonye U, Karn J. Control of HIV latency by epigenetic and non-epigenetic mechanisms. Curr HIV Res 2011; 9: 554-567.
101. Hu B, Dai B, Wang P. Vaccines delivered by integration-deficient lentiviral vectors targeting dendritic cells induces strong antigen-specific immunity. Vaccine 2010; 28: 6675-6683.
102. Ebina H, Kanemura Y, Suzuki Y, Urata K, Misawa N, Koyanagi Y. Integraseindependent HIV-1 infection is augmented under conditions of DNA damage and produces a viral reservoir. Virology 2012; 427: 44-50.
103. Gaur M, Leavitt AD. Mutations in the human immunodeficiency virus type integrase D,D(35)E motif do not eliminate provirus formation. J Virol 1998; 72: 4678-4685.
104. Harui A, Suzuki S, Kochanek S, Mitani K. Frequency and stability of chromosomal integration of adenovirus vectors. J Virol 1999; 73: 6141-6146.
105. Mitani K, Kubo S. Adenovirus as an integrating vector [review]. Curr Gene Ther 2002; 2: 135-144.
106. Dormond E, Kamen AA. Manufacturing of adenovirus vectors: production and purification of helper dependent adenovirus [review]. Methods Mol Biol 2011; 737: 139-156.
107. Silva AC, Peixoto C, Lucas T, Kuppers C, Cruz PE, Alves PM et al. Adenovirus vector production and purification [review]. Curr Gene Ther 2010; 10: 437-455.
108. Duerr A, Huang Y, Buchbinder S, Coombs RW, Sanchez J, Del Rio C et al. Extended follow-up confirms early vaccine-enhanced risk of HIV acquisition and demonstrates waning effect over time among participants in a randomized trial of recombinant adenovirus HIV vaccine (Step Study). J Infect Dis 2012; 206: 258-266.
109. Qureshi H, Ma ZM, Huang Y, Hodge G, Thomas MA, DiPasquale J et al. Low-dose penile SIVmac251 exposure of rhesus macaques infected with adenovirus type 5 (Ad5) and then immunized with a replication-defective Ad5-based SIV gag/pol/ nef vaccine recapitulates the results of the phase IIb step trial of a similar HIV-1 vaccine. J Virol 2012; 86: 2239-2250.
110. Hawkins CJ. TRAIL and malignant glioma [review]. Vitamins Hormones 2004; 67: 427-452.
111. Schuhmann NK, Pozzoli O, Sallach J, Huber A, Avitabile D, Perabo L et al. Gene transfer into human cord blood-derived CD34() cells by adeno-associated viral vectors. Exp Hematol 2010; 38: 707-717.
112. Srivastava A. Gene delivery to human and murine primitive hematopoietic stem and progenitor cells by AAV vectors. Methods Mol Biol 2004; 246: 245-254.
113. Veldwijk MR, Sellner L, Stiefelhagen M, Kleinschmidt JA, Laufs S, Topaly J et al. Pseudotyped recombinant adeno-associated viral vectors mediate efficient gene transfer into primary human CD34() peripheral blood progenitor cells. Cytotherapy 2010; 12: 107-112.
114. Handel EM, Gellhaus K, Khan K, Bednarski C, Cornu TI, Muller-Lerch F et al. Versatile and efficient genome editing in human cells by combining zincfinger nucleases with adeno-associated viral vectors. Hum Gene Ther 2012; 23: 321-329.
115. Li H, Lasaro MO, Jia B, Lin SW, Haut LH, High KA et al. Capsid-specific T-cell responses to natural infections with adeno-associated viruses in humans differ from those of nonhuman primates. Mol Ther 2011; 19: 2021-2030.
116. Zhou J, Li H, Zhang J, Piotr S, Rossi J. Development of cell-type specific anti-HIV gp120 aptamers for siRNA delivery. J Vis Exp 2011; 52: 2954.
117. Zhou J, Neff CP, Liu X, Zhang J, Li H, Smith DD et al. Systemic administration of combinatorial dsiRNAs via nanoparticles efficiently suppresses HIV-1 infection in humanized mice. Mol Ther 2011; 19: 2228-2238.
118. Burnett JC, Rossi JJ. RNA-based therapeutics: current progress and future prospects [review]. Chem Biol 2012; 19: 60-71.
119. Barber GN. Cytoplasmic DNA innate immune pathways [review]. Immunol Rev 2011; 243: 99-108.
120. Kariko K, Muramatsu H, Welsh FA, Ludwig J, Kato H, Akira S et al. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol Ther 2008; 16: 1833-1840.