Highly Significant Antiviral Activity of HIV-1 LTR-Specific Tre-Recombinase in Humanized Mice

PLoS Pathogens

Volumn 9, Issue 9, 2013, Pages

  Hauber, Ilona ^a   Hofmann Sieber, Helga ^a   Chemnitz, Jan ^a   Dubrau, Danilo ^a   Chusainow, Janet ^b   Stucka, Rolf ^c   Hartjen, Philip ^a,d   Schambach, Axel ^e,f   Ziegler, Patrick ^g,h   Hackmann, Karl ^b   Schröck, Evelin ^b   Schumacher, Udo ^d   Lindner, Christoph ⁱ   Grundhoff, Adam ^a   Baum, Christopher ^e   Manz, Markus G ^g,j   Buchholz, Frank ^b   Hauber, Joachim ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^h RWTH AACHEN UNIVERSITY   (Germany)

ⁱ Day Kimball Healthcare Hospital   (Germany)

^j UNIVERSITY HOSPITAL ZURICH   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 4; LENTIVIRUS VECTOR; RECOMBINASE;

ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CD34 SELECTION; CD4+ T LYMPHOCYTE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; KARYOTYPING; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; VIREMIA; VIRUS LOAD; WESTERN BLOTTING;

ANIMALS; GENETIC THERAPY; GENETIC VECTORS; HIV INFECTIONS; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; INTEGRASES; MICE; MICE, KNOCKOUT; PROVIRUSES; TRANSDUCTION, GENETIC; TRANSPLANTATION CHIMERA; VIRUS INTEGRATION;

EID: 84884680571     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003587     Document Type: Article

References (77)

1. Thompson MA, Aberg JA, Cahn P, Montaner JS, Rizzardini G, et al. (2010) Antiretroviral treatment of adult HIV infection: 2010 recommendations of the International AIDS Society-USA panel. JAMA 304: 321-333.
2. Schackman BR, Gebo KA, Walensky RP, Losina E, Muccio T, et al. (2006) The lifetime cost of current human immunodeficiency virus care in the United States. Med Care 44: 990-997.
3. Chen RY, Accortt NA, Westfall AO, Mugavero MJ, Raper JL, et al. (2006) Distribution of health care expenditures for HIV-infected patients. Clin Infect Dis 42: 1003-1010.
4. Deeks SG, Phillips AN, (2009) HIV infection, antiretroviral treatment, ageing, and non-AIDS related morbidity. BMJ 338: a3172.
5. Calmy A, Hirschel B, Cooper DA, Carr A, (2009) A new era of antiretroviral drug toxicity. Antivir Ther 14: 165-179.
6. Deeks SG, (2011) HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 62: 141-155.
7. Lewin SR, Evans VA, Elliott JH, Spire B, Chomont N, (2011) Finding a cure for HIV: will it ever be achievable? J Int AIDS Soc 14: 4.
8. Schulze zur Wiesch J, van Lunzen J, (2011) Hide and seek. Can we eradicate HIV by treatment intensification? J Infect Dis 203: 894-897.
9. Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, et al. (2009) The challenge of finding a cure for HIV infection. Science 323: 1304-1307.
10. Iglesias-Ussel MD, Romerio F, (2011) HIV reservoirs: the new frontier. AIDS Rev 13: 13-29.
11. Lafeuillade A, Stevenson M, (2011) The search for a cure for persistent HIV reservoirs. AIDS Rev 13: 63-66.
12. Margolis DM, (2011) Eradication therapies for HIV Infection: time to begin again. AIDS Res Hum Retroviruses 27: 347-353.
13. Smith MZ, Wightman F, Lewin SR, (2012) HIV Reservoirs and Strategies for Eradication. Curr HIV/AIDS Rep 9: 5-15.
14. Lafeuillade A, (2012) Eliminating the HIV Reservoir. Curr HIV/AIDS Rep 9: 121-131.
15. Durand CM, Blankson JN, Siliciano RF, (2012) Developing strategies for HIV-1 eradication. Trends Immunol 33: 554-562.
16. Choudhary SK, Margolis DM, (2011) Curing HIV: Pharmacologic approaches to target HIV-1 latency. Annu Rev Pharmacol Toxicol 51: 397-418.
17. Wightman F, Ellenberg P, Churchill M, Lewin SR, (2012) HDAC inhibitors in HIV. Immunol Cell Biol 90: 47-54.
18. Sarkar I, Hauber I, Hauber J, Buchholz F, (2007) HIV-1 proviral DNA excision using an evolved recombinase. Science 316: 1912-1915.
19. Buchholz F, Hauber J, (2011) In vitro evolution and analysis of HIV-1 LTR-specific recombinases. Methods 53: 102-109.
20. Buchholz F, Hauber J, (2013) Engineered DNA modifying enzymes: components of a future strategy to cure HIV/AIDS. Antiviral Res 97: 211-217.
21. Blackard JT, Renjifo BR, Mwakagile D, Montano MA, Fawzi WW, et al. (1999) Transmission of human immunodeficiency type 1 viruses with intersubtype recombinant long terminal repeat sequences. Virology 254: 220-225.
22. van Lunzen J, Fehse B, Hauber J, (2011) Gene Therapy Strategies: Can We Eradicate HIV? Curr HIV/AIDS Rep 8: 78-84.
23. Rossi JJ, June CH, Kohn DB, (2007) Genetic therapies against HIV. Nat Biotechnol 25: 1444-1454.
24. Scherer LJ, Rossi JJ, (2011) Ex vivo gene therapy for HIV-1 treatment. Hum Mol Genet 20: R100-R107.
25. Kiem HP, Jerome KR, Deeks SG, McCune JM, (2012) Hematopoietic-stem-cell-based gene therapy for HIV disease. Cell Stem Cell 10: 137-147.
26. Baltimore D, (1988) Gene therapy. Intracellular immunization. Nature 335: 395-396.
27. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, et al. (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471.
28. Schambach A, Galla M, Maetzig T, Loew R, Baum C, (2007) Improving transcriptional termination of self-inactivating gamma-retroviral and lentiviral vectors. Mol Ther 15: 1167-1173.
29. Emerman M, Malim MH, (1998) HIV-1 regulatory/accessory genes: keys to unraveling viral and host cell biology. Science 280: 1880-1884.
30. Larochelle N, Stucka R, Rieger N, Schermelleh L, Schiedner G, et al. (2011) Genomic integration of adenoviral gene transfer vectors following transduction of fertilized mouse oocytes. Transgenic Res 20: 123-135.
31. Paruzynski A, Arens A, Gabriel R, Bartholomae CC, Scholz S, et al. (2010) Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat Protoc 5: 1379-1395.
32. Schröck E, Zschieschang P, O'Brien P, Helmrich A, Hardt T, et al. (2006) Spectral karyotyping of human, mouse, rat and ape chromosomes-applications for genetic diagnostics and research. Cytogenet Genome Res 114: 199-221.
33. Schröck E, Weaver Z, Albertson D, (2001) Comparative genomic hybridization (CGH)-detection of unbalanced genetic aberrations using conventional and micro-array techniques. Curr Protoc Cytom Chapter 8: Unit 8.12.
34. Mariyanna L, Priyadarshini P, Hofmann-Sieber H, Krepstakies M, Walz N, et al. (2012) Excision of HIV-1 Proviral DNA by Recombinant Cell Permeable Tre-Recombinase. PLoS One 7: e31576.
35. Surendranath V, Chusainow J, Hauber J, Buchholz F, Habermann BH, (2010) SeLOX-a locus of recombination site search tool for the detection and directed evolution of site-specific recombination systems. Nucleic Acids Res 38: W293-W298.
36. Mazurier F, Fontanellas A, Salesse S, Taine L, Landriau S, et al. (1999) A novel immunodeficient mouse model-RAG2 x common cytokine receptor gamma chain double mutants-requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J Interferon Cytokine Res 19: 533-541.
37. Traggiai E, Chicha L, Mazzucchelli L, Bronz L, Piffaretti JC, et al. (2004) Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 304: 104-107.
38. Baenziger S, Tussiwand R, Schlaepfer E, Mazzucchelli L, Heikenwalder M, et al. (2006) Disseminated and sustained HIV infection in CD34+ cord blood cell-transplanted Rag2-/-gamma c-/- mice. Proc Natl Acad Sci U S A 103: 15951-15956.
39. Neagu MR, Ziegler P, Pertel T, Strambio-De-Castillia C, Grutter C, et al. (2009) Potent inhibition of HIV-1 by TRIM5-cyclophilin fusion proteins engineered from human components. J Clin Invest 119: 3035-3047.
40. Berges BK, Rowan MR, (2011) The utility of the new generation of humanized mice to study HIV-1 infection: transmission, prevention, pathogenesis, and treatment. Retrovirology 8: 65.
41. Zou W, Denton PW, Watkins RL, Krisko JF, Nochi T, et al. (2012) Nef functions in BLT mice to enhance HIV-1 replication and deplete CD4+CD8+ thymocytes. Retrovirology 9: 44.
42. DiGiusto DL, Krishnan A, Li L, Li H, Li S, et al. (2010) RNA-based gene therapy for HIV with lentiviral vector-modified CD34(+) cells in patients undergoing transplantation for AIDS-related lymphoma. Sci Transl Med 2: 36ra43.
43. Neff CP, Zhou J, Remling L, Kuruvilla J, Zhang J, et al. (2011) An aptamer-siRNA chimera suppresses HIV-1 viral loads and protects from helper CD4(+) T cell decline in humanized mice. Sci Transl Med 3: 66ra6.
44. ter Brake O, Legrand N, von Eije KJ, Centlivre M, Spits H, et al. (2009) Evaluation of safety and efficacy of RNAi against HIV-1 in the human immune system (Rag-2(-/-)gammac(-/-)) mouse model. Gene Ther 16: 148-153.
45. van Lunzen J, Glaunsinger T, Stahmer I, von Baehr V, Baum C, et al. (2007) Transfer of autologous gene-modified T cells in HIV-infected patients with advanced immunodeficiency and drug-resistant virus. Mol Ther 15: 1024-1033.
46. Kimpel J, Braun SE, Qiu G, Wong FE, Conolle M, et al. (2010) Survival of the fittest: positive selection of CD4+ T cells expressing a membrane-bound fusion inhibitor following HIV-1 infection. PLoS One 5: e12357.
47. Hütter G, Nowak D, Mossner M, Ganepola S, Müßig A, et al. (2009) Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360: 692-698.
48. Allers K, Hutter G, Hofmann J, Loddenkemper C, Rieger K, et al. (2011) Evidence for the cure of HIV infection by CCR5Delta32/Delta32 stem cell transplantation. Blood 117: 2791-2799.
49. Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, et al. (2008) Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26: 808-816.
50. Holt N, Wang J, Kim K, Friedman G, Wang X, et al. (2010) Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28: 839-847.
51. Katlama C, Deeks SG, Autran B, Martinez-Picado J, van Lunzen J, et al. (2013) Barriers to a cure for HIV: new ways to target and eradicate HIV-1 reservoirs. Lancet 381: 2109-2117.
52. Barton KM, Burch BD, Soriano-Sarabia N, Margolis DM, (2013) Prospects for treatment of latent HIV. Clin Pharmacol Ther 93: 46-56.
53. Marsden MD, Zack JA, (2013) HIV/AIDS eradication. Bioorg Med Chem Lett 23: 4003-4010.
54. Shan L, Siliciano RF, (2013) From reactivation of latent HIV-1 to elimination of the latent reservoir: The presence of multiple barriers to viral eradication. Bioessays 35: 544-552.
55. Archin NM, Espeseth A, Parker D, Cheema M, Hazuda D, et al. (2009) Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res Hum Retroviruses 25: 207-212.
56. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, et al. (2012) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487: 482-485.
57. Shan L, Deng K, Shroff NS, Durand CM, Rabi SA, et al. (2012) Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 36: 491-501.
58. Deeks SG, McCune JM, (2010) Can HIV be cured with stem cell therapy? Nat Biotechnol 28: 807-810.
59. Zintzaras E, Kowald A, (2011) A mathematical model of HIV dynamics in the presence of a rescuing virus with replication deficiency. Theory Biosci 130: 127-134.
60. Lachmann N, Brennig S, Pfaff N, Schermeier H, Dahlmann J, et al. (2012) Efficient in vivo regulation of cytidine deaminase expression in the haematopoietic system using a doxycycline-inducible lentiviral vector system. Gene Ther 20: 298-307.
61. Ludwig C, Wagner R, (2007) Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol 18: 537-545.
62. Van Duyne GD, (2001) A structural view of cre-loxp site-specific recombination. Annu Rev Biophys Biomol Struct 30: 87-104.
63. Pattanayak V, Ramirez CL, Joung JK, Liu DR, (2011) Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods 8: 765-770.
64. Gabriel R, Lombardo A, Arens A, Miller JC, Genovese P, et al. (2011) An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol 29: 816-823.
65. McIntyre GJ, Groneman JL, Yu YH, Jaramillo A, Shen S, et al. (2009) 96 shRNAs designed for maximal coverage of HIV-1 variants. Retrovirology 6: 55.
66. Schambach A, Bohne J, Chandra S, Will E, Margison GP, et al. (2006) Equal potency of gammaretroviral and lentiviral SIN vectors for expression of O6-methylguanine-DNA methyltransferase in hematopoietic cells. Mol Ther 13: 391-400.
67. Egelhofer M, Brandenburg G, Martinius H, Schult-Dietrich P, Melikyan G, et al. (2004) Inhibition of human immunodeficiency virus type 1 entry in cells expressing gp41-derived peptides. J Virol 78: 568-575.
68. Schambach A, Galla M, Modlich U, Will E, Chandra S, et al. (2006) Lentiviral vectors pseudotyped with murine ecotropic envelope: increased biosafety and convenience in preclinical research. Exp Hematol 34: 588-592.
69. Weber K, Mock U, Petrowitz B, Bartsch U, Fehse B, (2010) Lentiviral gene ontology (LeGO) vectors equipped with novel drug-selectable fluorescent proteins: new building blocks for cell marking and multi-gene analysis. Gene Ther 17: 511-520.
70. Hwang SS, Boyle TJ, Lyerly HK, Cullen BR, (1991) Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253: 71-74.
71. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
72. Beyer WR, Westphal M, Ostertag W, von Laer D, (2002) Oncoretrovirus and lentivirus vectors pseudotyped with lymphocytic choriomeningitis virus glycoprotein: generation, concentration, and broad host range. J Virol 76: 1488-1495.
73. Chemnitz J, Pieper D, Grüttner C, Hauber J, (2009) Phosphorylation of the HuR ligand APRIL by casein kinase 2 regulates CD83 expression. Eur J Immunol 39: 267-279.
74. Fries B, Heukeshoven J, Hauber I, Grüttner C, Stocking C, et al. (2007) Analysis of Nucleocytoplasmic Trafficking of the HuR Ligand APRIL and Its Influence on CD83 Expression. J Biol Chem 282: 4504-4515.
75. Schulze zur Wiesch J, Thomssen A, Hartjen P, Toth I, Lehmann C, et al. (2011) Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+ T regulatory cells correlates with progressive disease. J Virol 85: 1287-1297.
76. Schulze zur Wiesch J, Pieper D, Stahmer I, Eiermann T, Buggisch P, et al. (2009) Sustained virological response after early antiviral treatment of acute hepatitis C virus and HIV coinfection. Clin Infect Dis 49: 466-472.
77. Schröck E, du MS, Veldman T, Schoell B, Wienberg J, et al. (1996) Multicolor spectral karyotyping of human chromosomes. Science 273: 494-497.