Design of a novel integration-deficient lentivector technology that incorporates genetic and posttranslational elements to target human dendritic cells

Molecular Therapy

Volumn 22, Issue 3, 2014, Pages 575-587

  Tareen, Semih U ^a   Kelley Clarke, Brenna ^a   Nicolai, Christopher J ^a   Cassiano, Linda A ^a   Nelson, Lisa T ^b   Slough, Megan M ^a   Vin, Chintan D ^a   Odegard, Jared M ^a   Sloan, Derek D ^a   Van Hoeven, Neal ^a   Allen, James M ^a   Dubensky, Thomas W ^a   Robbins, Scott H ^a,b  

^a Immune Design   (United States)

^b TRIA Bioscience Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; INTEGRATION DEFICIENT LENTIVIRUS VECTOR; LENTIVIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CD8+ T LYMPHOCYTE; DENDRITIC CELL; GENE DOSAGE; IMMUNOGENICITY; LYMPHOCYTE SUBPOPULATION; MOLECULAR WEIGHT; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; SAFETY; SIGNAL TRANSDUCTION; SINDBIS VIRUS; TARGET CELL; VIRAL GENE DELIVERY SYSTEM; VIRUS ENVELOPE;

SINDBIS VIRUS;

ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; GENETIC VECTORS; HEK293 CELLS; HUMANS; IMMUNITY, CELLULAR; LENTIVIRUS; SINDBIS VIRUS; TISSUE DISTRIBUTION; VIRAL ENVELOPE PROTEINS;

EID: 84895464998     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.278     Document Type: Article

References (67)

1. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480: 480-9.
2. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001;106: 255-8.
3. Hsu FJ, Benike C, Fagnoni F, et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med 1996;2: 52-8.
4. Bonifaz LC, Bonnyay DP, Charalambous A, et al. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 2004;199: 815-24.
5. Klimstra WB, Nangle EM, Smith MS, Yurochko AD, Ryman KD. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J Virol 2003;77: 12022-32.
6. Yang L, Yang H, Rideout K, et al. Engineered lentivector targeting of dendritic cells for in vivo immunization. Nat Biotechnol 2008;26:326.
7. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998;72: 8463-71.
8. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998;72: 9873-80.
9. Kantor B, Bayer M, Ma H, et al. Notable reduction in illegitimate integration mediated by a PPT-deleted, nonintegrating lentiviral vector. Mol Ther 2011;19: 547-56.
10. Brussel A, Delelis O, Sonigo P. Alu-LTR real-time nested PCR assay for quantifying integrated HIV-1 DNA. Methods Mol Biol 2005;304: 139-54.
11. Nightingale SJ, Hollis RP, Pepper KA, et al. Transient gene expression by nonintegrating lentiviral vectors. Mol Ther 2006;13: 1121-32.
12. Cronin J, Zhang XY, Reiser J. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 2005;5:387.
13. Byrnes AP, Griffin DE. Binding of Sindbis virus to cell surface heparan sulfate. J Virol 1998;72: 7349-56.
14. Klimstra WB, Ryman KD, Johnston RE. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 1998;72: 7357-66.
15. Klenk HD, Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol 1994;2: 39-43.
16. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. Structural changes of envelope proteins during alphavirus fusion. Nature 2010;468: 705-8.
17. Klimstra WB, Heidner HW, Johnston RE. The furin protease cleavage recognition sequence of Sindbis virus PE2 can mediate virion attachment to cell surface heparan sulfate. J. Virol. 1999;73:6299.
18. Gardner JP, Frolov I, Perri S, et al. Infection of human dendritic cells by a sindbis virus replicon vector is determined by a single amino acid substitution in the E2 glycoprotein. J Virol 2000;74: 11849-57.
19. Bear JS, Byrnes AP, Griffin DE. Heparin-binding and patterns of virulence for two recombinant strains of Sindbis virus. Virology 2006;347: 183-90.
20. Hsieh P, Robbins PW. Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells. J Biol Chem 1984;259: 2375-82.
21. Dairaku K, Spiro RG. Phylogenetic survey of endomannosidase indicates late evolutionary appearance of this N-linked oligosaccharide processing enzyme. Glycobiology 1997;7: 579-86.
22. Knight RL, Schultz KL, Kent RJ, Venkatesan M, Griffin DE. Role of N-linked glycosylation for sindbis virus infection and replication in vertebrate and invertebrate systems. J Virol 2009;83: 5640-7.
23. Morizono K, Ku A, Xie Y, et al. Redirecting lentiviral vectors pseudotyped with Sindbis virus-derived envelope proteins to DC-SIGN by modification of N-linked glycans of envelope proteins. J Virol 2010;84: 6923-34.
24. Hrecka K, Hao C, Gierszewska M, et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011;474: 658-61.
25. Laguette N, Sobhian B, Casartelli N, et al. SAMHD1 is the dendritic- and myeloid-cellspecific HIV-1 restriction factor counteracted by Vpx. Nature 2011;474: 654-7.
26. Mangeot PE, Duperrier K, Nègre D, et al. High levels of transduction of human dendritic cells with optimized SIV vectors. Mol Ther 2002;5: 283-90.
27. Goujon C, Jarrosson-Wuillème L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther 2006;13: 991-4.
28. Berger G, Goujon C, Darlix JL, Cimarelli A. SIVMAC Vpx improves the transduction of dendritic cells with nonintegrative HIV-1-derived vectors. Gene Ther 2009;16: 159-63.
29. Pertel T, Reinhard C, Luban J. Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 2011;8:49.
30. Sharova N, Wu Y, Zhu X, et al. Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog 2008;4:e1000057.
31. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 2010;467: 214-7.
32. Sunseri N, O'Brien M, Bhardwaj N, Landau NR. Human immunodeficiency virus type 1 modified to package Simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J Virol 2011;85: 6263-74.
33. Dragin L, Nguyen LA, Lahouassa H, et al. Interferon block to HIV-1 transduction in macrophages despite SAMHD1 degradation and high deoxynucleoside triphosphates supply. Retrovirology 2013;10:30.
34. Goujon C, Schaller T, Galão RP, et al. Evidence for IFNα-induced, SAMHD1- independent inhibitors of early HIV-1 infection. Retrovirology 2013;10:23.
35. Li N, Zhang W, Cao X. Identification of human homologue of mouse IFN-gamma induced protein from human dendritic cells. Immunol Lett 2000;74: 221-4.
36. St Gelais C, de Silva S, Amie SM, et al. SAMHD1 restricts HIV-1 infection in dendritic cells (DCs) by dNTP depletion, but its expression in DCs and primary CD4+ T-lymphocytes cannot be upregulated by interferons. Retrovirology 2012;9:105.
37. Apolonia L, Waddington SN, Fernandes C, et al. Stable gene transfer to muscle using non-integrating lentiviral vectors. Mol Ther 2007;15: 1947-54.
38. Leavitt AD, Robles G, Alesandro N, Varmus HE. Human immunodeficiency virus type 1 integrase mutants retain in vitro integrase activity yet fail to integrate viral DNA efficiently during infection. J Virol 1996;70: 721-8.
39. Yáñez-Muñoz RJ, Balaggan KS, MacNeil A, et al. Effective gene therapy with nonintegrating lentiviral vectors. Nat Med 2006;12: 348-53.
40. Gaur M, Leavitt AD. Mutations in the human immunodeficiency virus type 1 integrase D,D(35)E motif do not eliminate provirus formation. J Virol 1998;72: 4678-85.
41. Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 2008;118: 3132-42.
42. Hacein-Bey-Abina S, von Kalle C, Schmidt M, et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003;348: 255-6.
43. Philippe S, Sarkis C, Barkats M, et al. Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2006;103:17684.
44. Elbein AD, Tropea JE, Mitchell M, Kaushal GP. Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J Biol Chem 1990;265: 15599-605.
45. Kawar Z, Romero PA, Herscovics A, Jarvis DL. N-Glycan processing by a lepidopteran insect alpha1,2-mannosidase. Glycobiology 2000;10: 347-55.
46. Backovic M, Rey FA. Virus entry: old viruses, new receptors. Curr Opin Virol 2012;2: 4-13.
47. Geijtenbeek TB, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell-specific HIV-1- binding protein that enhances trans-infection of T cells. Cell 2000;100: 587-97.
48. Johnson TR, McLellan JS, Graham BS. Respiratory syncytial virus glycoprotein G interacts with DC-SIGN and L-SIGN to activate ERK1 and ERK2. J Virol 2012;86: 1339-47.
49. Avota E, Gulbins E, Schneider-Schaulies S. DC-SIGN mediated sphingomyelinaseactivation and ceramide generation is essential for enhancement of viral uptake in dendritic cells. PLoS Pathog 2011;7:e1001290.
50. de Witte L, Abt M, Schneider-Schaulies S, van Kooyk Y, Geijtenbeek TB. Measles virus targets DC-SIGN to enhance dendritic cell infection. J. Virol. 2006;80:3477.
51. Blanco-Melo D, Venkatesh S, Bieniasz PD. Intrinsic cellular defenses against human immunodeficiency viruses. Immunity 2012;37: 399-411.
52. Stremlau M, Perron M, Lee M, et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci U S A 2006;103: 5514-9.
53. Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002;418: 646-50.
54. Lahouassa H, Daddacha W, Hofmann H, et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 2012;13: 223-8.
55. Ohkura S, Goldstone DC, Yap MW, Holden-Dye K, Taylor IA, Stoye JP. Novel escape mutants suggest an extensive TRIM5α binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog 2011;7:e1002011.
56. Zufferey R, Donello JE, Trono D, Hope TJ. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 1999;73: 2886-92.
57. Zanta-Boussif MA, Charrier S, Brice-Ouzet A, et al. Validation of a mutated PRE sequence allowing high and sustained transgene expression while abrogating WHV-X protein synthesis: application to the gene therapy of WAS. Gene Ther 2009;16: 605-19.
58. Emerman M, Vazeux R, Peden K. The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell 1989;57: 1155-65.
59. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989;338: 254-7.
60. Leung JY, Ng MM, Chu JJ. Replication of alphaviruses: a review on the entry process of alphaviruses into cells. Adv. Virol. 2011;2011:249640.
61. Bayer M, Kantor B, Cockrell A, et al. A large U3 deletion causes increased in vivo expression from a nonintegrating lentiviral vector. Mol Ther 2008;16: 1968-76.
62. Wiskerchen M and Muesing MA. Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J. Virol. 1995;69:376.
63. Kotsopoulou E, Kim VN, Kingsman AJ, Kingsman SM, Mitrophanous KA. A Revindependent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gag-pol gene. J Virol 2000;74: 4839-52.
64. Sastry L, Xu Y, Johnson T, et al. Certification assays for HIV-1-based vectors: frequent passage of gag sequences without evidence of replication-competent viruses. Mol Ther 2003;8: 830-9.
65. Wagner R, Graf M, Bieler K, et al. Rev-independent expression of synthetic gag-pol genes of human immunodeficiency virus type 1 and simian immunodeficiency virus: implications for the safety of lentiviral vectors. Hum Gene Ther 2000;11: 2403-13.
66. Butler SL, Hansen MS, Bushman FD. A quantitative assay for HIV DNA integration in vivo. Nat Med 2001;7: 631-4.
67. Canque B, Rosenzwajg M, Gluckman JC. In vitro generation of dendritic cells from cord blood CD34+ hematopoietic progenitors cells. Methods Mol Biol 2003;215: 311-25.