Cyclosporin A and rapamycin relieve distinct lentiviral restriction blocks in hematopoietic stem and progenitor cells

Molecular Therapy

Volumn 23, Issue 2, 2015, Pages 352-362

  Petrillo, Carolina ^a,b   Cesana, Daniela ^a   Piras, Francesco ^a   Bartolaccini, Sara ^a   Naldini, Luigi ^a,b   Montini, Eugenio ^a   Kajaste Rudnitski, Anna ^a  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CYCLOPHILIN A; CYCLOSPORIN A; LENTIVIRUS VECTOR; RAPAMYCIN; CYCLOSPORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; CYCLOPHILIN A GENE; GENE TRANSFER; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CAPSID; VIRUS GENOME; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; FETUS BLOOD; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOPHENOTYPING; LENTIVIRINAE; METABOLISM; PHENOTYPE; TRANSGENE;

MIRIDAE; MURINAE;

ANIMALS; CELL DIFFERENTIATION; CYCLOSPORINE; FETAL BLOOD; GENE EXPRESSION; GENETIC VECTORS; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOPHENOTYPING; LENTIVIRUS; MICE; PHENOTYPE; SIROLIMUS; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84930486755     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.193     Document Type: Article

References (50)

1. Aiuti A, Cattaneo F, Galimberti S, Benninghoff U, Cassani B, Callegaro L., et al. (2009). Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 360: 447-458
2. Boztug K, Schmidt M, Schwarzer A, Banerjee PP, Díez IA, Dewey RA., et al. (2010). Stem-cell gene therapy for the Wiskott-Aldrich syndrome. N Engl J Med 363: 1918-1927
3. Hacein-Bey-Abina S, Hauer J, Lim A, Picard C, Wang GP, Berry CC., et al. (2010). Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 363: 355-364
4. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, Veres G, Schmidt M, Kutschera I., et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326: 818-823
5. Aiuti A, Biasco L, Scaramuzza S, Ferrua F, Cicalese MP, Baricordi C., et al. (2013). Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 341: 1233151
6. Biffi A, Montini E, Lorioli L, Cesani M, Fumagalli F, Plati T., et al. (2013). Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 341: 1233158
7. Yan N and Chen ZJ. (2012). Intrinsic antiviral immunity. Nat Immunol 13: 214-222
8. Agudo J, Ruzo A, Kitur K, Sachidanandam R, Blander JM and Brown BD. (2012). A TLR and non-TLR mediated innate response to lentiviruses restricts hepatocyte entry and can be ameliorated by pharmacological blockade. Mol Ther 20: 2257-2267
9. Brown BD, Sitia G, Annoni A, Hauben E, Sergi LS, Zingale A., et al. (2007). In vivo administration of lentiviral vectors triggers a type I interferon response that restricts hepatocyte gene transfer and promotes vector clearance. Blood 109: 2797-2805
10. Schreiber SL and Crabtree GR. (1992). The mechanism of action of cyclosporin A and FK506. Immunol Today 13: 136-142
11. Harding MW, Galat A, Uehling DE and Schreiber SL. (1989). A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341: 758-760
12. Sokolskaja E and Luban J. (2006). Cyclophilin TRIM5, and innate immunity to HIV-1. Curr Opin Microbiol 9: 404-408
13. Hilditch L and Towers GJ. (2014). A model for cofactor use during HIV-1 reverse transcription and nuclear entry. Curr Opin Virol 4: 32-36
14. Kahl CA, Cannon PM, Oldenburg J, Tarantal AF and Kohn DB. (2008). Tissuespecific restriction of cyclophilin A-independent HIV-1- and SIV-derived lentiviral vectors. Gene Ther 15: 1079-1089
15. Santoni de Sio FR, Gritti A, Cascio P, Neri M, Sampaolesi M, Galli C., et al. (2008). Lentiviral vector gene transfer is limited by the proteasome at postentry steps in various types of stem cells. Stem Cells 26: 2142-2152
16. Uchida N, Hsieh MM, Washington KN and Tisdale JF. (2013). Efficient transduction of human hematopoietic repopulating cells with a chimeric HIV1-based vector including SIV capsid. Exp Hematol 41: 779-788.e1
17. Rohrabaugh SL, Campbell TB, Hangoc G and Broxmeyer HE. (2011). Ex vivo rapamycin treatment of human cord blood CD34+ cells enhances their engraftment of NSG mice. Blood Cells Mol Dis 46: 318-320
18. Huang J, Nguyen-McCarty M, Hexner EO, Danet-Desnoyers G and Klein PS. (2012). Maintenance of hematopoietic stem cells through regulation of Wnt and mTOR pathways. Nat Med 18: 1778-1785
19. Kondo Y, Kanzawa T, Sawaya R and Kondo S. (2005). The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5: 726-734
20. Richetta C and Faure M. (2013). Autophagy in antiviral innate immunity. Cell Microbiol 15: 368-376
21. Amirache F, Lévy C, Costa C, Mangeot PE, Torbett BE, Wang CX., et al. (2014). Mystery solved: VSV-G-LVs do not allow efficient gene transfer into unstimulated T cells B cells and HSCs because they lack the LDL receptor. Blood 123: 1422-1424
22. De Iaco A and Luban J. (2014). Cyclophilin A promotes HIV-1 reverse transcription but its effect on transduction correlates best with its effect on nuclear entry of viral cDNA. Retrovirology 11: 11
23. Doulatov S, Notta F, Laurenti E and Dick JE. (2012). Hematopoiesis: a human perspective. Cell Stem Cell 10: 120-136
24. Naldini L. (2011). Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet 12: 301-315
25. Merten OW, Charrier S, Laroudie N, Fauchille S, Dugué C, Jenny C., et al. (2011). Large-scale manufacture and characterization of a lentiviral vector produced for clinical ex vivo gene therapy application. Hum Gene Ther 22: 343-356
26. Zhu K, Dunner K Jr and McConkey DJ. (2010). Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 29: 451-462
27. Campbell GR and Spector SA. (2011). Hormonally active vitamin D3 (1alpha,25- dihydroxycholecalciferol) triggers autophagy in human macrophages that inhibits HIV-1 infection. J Biol Chem 286: 18890-18902
28. Wang CX, Sather BD, Wang X, Adair J, Khan I, Singh S., et al. (2014). Rapamycin relieves lentiviral vector transduction resistance in human and mouse hematopoietic stem cells. Blood 124: 913-923
29. Noser JA, Towers GJ, Sakuma R, Dumont JM, Collins MK and Ikeda Y. (2006). Cyclosporine increases human immunodeficiency virus type 1 vector transduction of primary mouse cells. J Virol 80: 7769-7774
30. Luban J, Bossolt KL, Franke EK, Kalpana GV and Goff SP. (1993). Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73: 1067-1078
31. Colgan J, Asmal M, Yu, B and Luban J. (2005). Cyclophilin A-deficient mice are resistant to immunosuppression by cyclosporine. J Immunol 174: 6030-6038
32. Evans ME, Kumkhaek C, Hsieh MM, Donahue RE, Tisdale JF and Uchida N. (2014). TRIM5a variations influence transduction efficiency with lentiviral vectors in both human and rhesus CD34(+) cells in vitro and in vivo. Mol Ther 22: 348-358
33. Liu Z, Pan Q, Ding S, Qian J, Xu, F, Zhou J., et al. (2013). The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14: 398-410
34. Busnadiego I, Kane M, Rihn SJ, Preugschas HF, Hughes J, Blanco-Melo D., et al. (2014). Host and viral determinants of Mx2 antiretroviral activity. J Virol 88: 7738-7752
35. Goujon C, Moncorgé O, Bauby H, Doyle T, Ward CC, Schaller T., et al. (2013). Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502: 559-562
36. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL., et al. (2011). HIV-1 capsid-cyclophilin interactions determine nuclear import pathway integration targeting and replication efficiency. PLoS Pathog 7: e1002439
37. Allouch A, Di Primio C, Alpi E, Lusic M, Arosio D, Giacca M., et al. (2011). The TRIM family protein KAP1 inhibits HIV-1 integration. Cell Host Microbe 9: 484-495
38. Zhang J, Scadden DT and Crumpacker CS. (2007). Primitive hematopoietic cells resist HIV-1 infection via p21. J Clin Invest 117: 473-481
39. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, Hilditch L., et al. (2013). HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature 503: 402-405
40. Sokolskaja E, Sayah DM and Luban J. (2004). Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J Virol 78: 12800-12808
41. Montini E, Cesana D, Schmidt M, Sanvito F, Ponzoni M, Bartholomae C., et al. (2006). Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat Biotechnol 24: 687-696
42. Gentner B, Visigalli I, Hiramatsu H, Lechman E, Ungari S, Giustacchini A., et al. (2010). Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med 2: 58ra84
43. Cassetta L, Kajaste-Rudnitski A, Coradin T, Saba E, Della Chiara G, Barbagallo M., et al. (2013). M1 polarization of human monocyte-derived macrophages restricts pre and postintegration steps of HIV-1 replication. AIDS 27: 1847-1856
44. Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA., et al. (2007). Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25: 1298-1306
45. Kajaste-Rudnitski A, Mashimo T, Frenkiel MP, Guénet JL, Lucas M and Desprès P. (2006). The 2',5'-oligoadenylate synthetase 1b is a potent inhibitor of West Nile virus replication inside infected cells. J Biol Chem 281: 4624-4637
46. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG., et al. (2010). Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7: 221-233
47. Price AJ, Fletcher AJ, Schaller T, Elliott T, Lee K, KewalRamani VN., et al. (2012). CPSF6 defines a conserved capsid interface that modulates HIV-1 replication. PLoS Pathog 8: e1002896
48. Veillette M, Bichel K, Pawlica P, Freund SM, Plourde MB, Pham QT., et al. (2013). The V86M mutation in HIV-1 capsid confers resistance to TRIM5a by abrogation of cyclophilin A-dependent restriction and enhancement of viral nuclear import. Retrovirology 10: 25
49. Qi, M, Yang R and Aiken C. (2008). Cyclophilin A-dependent restriction of human immunodeficiency virus type 1 capsid mutants for infection of nondividing cells. J Virol 82: 12001-12008
50. Ylinen LM, Schaller T, Price A, Fletcher AJ, Noursadeghi M, James LC., et al. (2009). Cyclophilin A levels dictate infection efficiency of human immunodeficiency virus type 1 capsid escape mutants A92E and G94D. J Virol 83: 2044-2047