RFX1 and RFX3 Transcription Factors Interact with the D Sequence of Adeno-Associated Virus Inverted Terminal Repeat and Regulate AAV Transduction

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Julien, Laura ^a   Chassagne, Julie ^a   Peccate, Cécile ^a   Lorain, Stéphanie ^a   Piétri Rouxel, France ^a   Danos, Olivier ^b   Benkhelifa Ziyyat, Sofia ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b REGENXBIO INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BINDING; REGULATORY FACTOR X TRANSCRIPTION FACTOR; REGULATORY FACTOR X1; RFX1 PROTEIN, HUMAN; RFX3 PROTEIN, HUMAN;

DEPENDOPARVOVIRUS; GENETIC TRANSDUCTION; GENETICS; HEK293 CELL LINE; HUMAN; LONG TERMINAL REPEAT; METABOLISM;

DEPENDOVIRUS; HEK293 CELLS; HUMANS; PROTEIN BINDING; REGULATORY FACTOR X TRANSCRIPTION FACTORS; REGULATORY FACTOR X1; TERMINAL REPEAT SEQUENCES; TRANSDUCTION, GENETIC;

EID: 85040531200     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-18604-3     Document Type: Article

References (54)

1. Sanlioglu, S., Monick, M. M., Luleci, G., Hunninghake, G. W. & Engelhardt, J. F. Rate limiting steps of AAV transduction and implications for human gene therapy. Curr Gene Ther 1, 137-147 (2001).
2. Weitzman, M. D., Carson, C. T., Schwartz, R. A. & Lilley, C. E. Interactions of viruses with the cellular DNA repair machinery. DNA Repair (Amst) 3, 1165-1173, https://doi.org/10.1016/j.dnarep.2004.03.018 (2004).
3. Davidoff, A. M., Ng, C. Y., Zhou, J., Spence, Y. & Nathwani, A. C. Sex significantly influences transduction of murine liver by recombinant adeno-Associated viral vectors through an androgen-dependent pathway. Blood 102, 480-488, https://doi.org/10.1182/blood-2002-09-2889 (2003).
4. Haberman, R. P., McCown, T. J. & Samulski, R. J. Novel transcriptional regulatory signals in the adeno-Associated virus terminal repeat A/D junction element. J Virol 74, 8732-8739 (2000).
5. Flotte, T. R. et al. Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-Associated virus promoter. J Biol Chem 268, 3781-3790 (1993).
6. Ellis, B. L. et al. A survey of ex vivo/in vitro transduction efficiency of mammalian primary cells and cell lines with Nine natural adeno-Associated virus (AAV1-9) and one engineered adeno-Associated virus serotype. Virol J 10, 74, https://doi.org/10.1186/1743-422X-10-74 (2013).
7. Srivastava, A. In vivo tissue-Tropism of adeno-Associated viral vectors. Curr Opin Virol 21, 75-80, https://doi.org/10.1016/j.coviro.2016.08.003 (2016).
8. Balakrishnan, B. & Jayandharan, G. R. Basic biology of adeno-Associated virus (AAV) vectors used in gene therapy. Curr Gene Ther 14, 86-100 (2014).
9. Ferrari, F. K., Samulski, T., Shenk, T. & Samulski, R. J. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-Associated virus vectors. J Virol 70, 3227-3234 (1996).
10. Zentilin, L., Marcello, A. & Giacca, M. Involvement of cellular double-stranded DNA break binding proteins in processing of the recombinant adeno-Associated virus genome. J Virol 75, 12279-12287, https://doi.org/10.1128/JVI.75.24.12279-12287.2001 (2001).
11. Inagaki, K., Ma, C., Storm, T. A., Kay, M. A. & Nakai, H. The role of DNA-PKcs and artemis in opening viral DNA hairpin termini in various tissues in mice. J Virol 81, 11304-11321, https://doi.org/10.1128/JVI.01225-07 (2007).
12. Choi, V. W., McCarty, D. M. & Samulski, R. J. Host cell DNA repair pathways in adeno-Associated viral genome processing. J Virol 80, 10346-10356, https://doi.org/10.1128/JVI.00841-06 (2006).
13. Duan, D., Yue, Y. & Engelhardt, J. F. Consequences of DNA-dependent protein kinase catalytic subunit deficiency on recombinant adeno-Associated virus genome circularization and heterodimerization in muscle tissue. J Virol 77, 4751-4759 (2003).
14. Song, S., Laipis, P. J., Berns, K. I. & Flotte, T. R. Effect of DNA-dependent protein kinase on the molecular fate of the rAAV2 genome in skeletal muscle. Proc Natl Acad Sci USA 98, 4084-4088, https://doi.org/10.1073/pnas.061014598 (2001).
15. Cataldi, M. P. & McCarty, D. M. Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-Associated virus vector genomes. J Virol 84, 8673-8682, https://doi.org/10.1128/JVI.00641-10 (2010).
16. Qing, K. et al. Adeno-Associated virus type 2-mediated gene transfer: role of cellular FKBP52 protein in transgene expression. J Virol 75, 8968-8976, https://doi.org/10.1128/JVI.75.19.8968-8976.2001 (2001).
17. Qing, K. et al. Adeno-Associated virus type 2-mediated gene transfer: role of cellular T-cell protein tyrosine phosphatase in transgene expression in established cell lines in vitro and transgenic mice in vivo. J Virol 77, 2741-2746 (2003).
18. Jayandharan, G. R. et al. Optimized adeno-Associated virus (AAV)-protein phosphatase-5 helper viruses for efficient liver transduction by single-stranded AAV vectors: Therapeutic expression of factor IX at reduced vector doses. Hum Gene Ther 21, 271-283, https://doi.org/10.1089/hum.2009.100 (2010).
19. Ling, C. et al. Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-Associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo. J Virol 89, 952-961, https://doi.org/10.1128/JVI.02581-14 (2015).
20. Jayandharan, G. R. et al. Activation of the NF-kappaB pathway by adeno-Associated virus (AAV) vectors and its implications in immune response and gene therapy. Proc Natl Acad Sci USA 108, 3743-3748, https://doi.org/10.1073/pnas.1012753108 (2011).
21. Dean, J., Plante, J., Huggins, G. S., Snyder, R. O. & Aikawa, R. Role of cyclic AMP-dependent kinase response element-binding protein in recombinant adeno-Associated virus-mediated transduction of heart muscle cells. Hum Gene Ther 20, 1005-1012, https://doi.org/10.1089/hum.2009.054 (2009).
22. Gajiwala, K. S. et al. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 403, 916-921, https://doi.org/10.1038/35002634 (2000).
23. Emery, P. et al. A consensus motif in the RFX DNA binding domain and binding domain mutants with altered specificity. Mol Cell Biol 16, 4486-4494 (1996).
24. Morotomi-Yano, K. et al. Human regulatory factor X 4 (RFX4) is a testis-specific dimeric DNA-binding protein that cooperates with other human RFX members. J Biol Chem 277, 836-842, https://doi.org/10.1074/jbc.M108638200 (2002).
25. Choksi, S. P., Lauter, G., Swoboda, P. & Roy, S. Switching on cilia: Transcriptional networks regulating ciliogenesis. Development 141, 1427-1441, https://doi.org/10.1242/dev.074666 (2014).
26. Iwama, A. et al. Dimeric RFX proteins contribute to the activity and lineage specificity of the interleukin-5 receptor alpha promoter through activation and repression domains. Mol Cell Biol 19, 3940-3950 (1999).
27. Nakayama, A. et al. Role for RFX transcription factors in non-neuronal cell-specific inactivation of the microtubule-Associated protein MAP1A promoter. J Biol Chem 278, 233-240, https://doi.org/10.1074/jbc.M209574200 (2003).
28. Reith, W. et al. RFX1, a transactivator of hepatitis B virus enhancer I, belongs to a novel family of homodimeric and heterodimeric DNA-binding proteins. Mol Cell Biol 14, 1230-1244 (1994).
29. Siegrist, C. A. & Mach, B. Antisense oligonucleotides specific for regulatory factor RFX-1 inhibit inducible but not constitutive expression of all major histocompatibility complex class II genes. Eur J Immunol 23, 2903-2908, https://doi.org/10.1002/eji.1830231126 (1993).
30. Reinhold, W. et al. The myc intron-binding polypeptide associates with RFX1 in vivo and binds to the major histocompatibility complex class II promoter region, to the hepatitis B virus enhancer, and to regulatory regions of several distinct viral genes. Mol Cell Biol 15, 3041-3048 (1995).
31. Sáfrány, G. & Perry, R. P. Transcription factor RFX1 helps control the promoter of the mouse ribosomal protein-encoding gene rpL30 by binding to its alpha element. Gene 132, 279-283 (1993).
32. Liu, M., Lee, B. H. & Mathews, M. B. Involvement of RFX1 protein in the regulation of the human proliferating cell nuclear antigen promoter. J Biol Chem 274, 15433-15439 (1999).
33. David, E., Garcia, A. D. & Hearing, P. Interaction of EF-C/RFX-1 with the inverted repeat of viral enhancer regions is required for transactivation. J Biol Chem 270, 8353-8360 (1995).
34. Kobr, M., Reith, W., Herrero-Sanchez, C. & Mach, B. Two DNA-binding proteins discriminate between the promoters of different members of the major histocompatibility complex class II multigene family. Mol Cell Biol 10, 965-971 (1990).
35. Masternak, K., Muhlethaler-Mottet, A., Villard, J., Peretti, M. & Reith, W. Molecular genetics of the Bare lymphocyte syndrome. Rev Immunogenet 2, 267-282 (2000).
36. Tammimies, K. et al. Ciliary dyslexia candidate genes DYX1C1 and DCDC2 are regulated by Regulatory Factor X (RFX) transcription factors through X-box promoter motifs. FASEB J 30, 3578-3587, https://doi.org/10.1096/fj.201500124RR (2016).
37. Lubelsky, Y., Reuven, N. & Shaul, Y. Autorepression of rfx1 gene expression: functional conservation from yeast to humans in response to DNA replication arrest. Mol Cell Biol 25, 10665-10673, https://doi.org/10.1128/MCB.25.23.10665-10673.2005 (2005).
38. Cathomen, T., Stracker, T. H., Gilbert, L. B. & Weitzman, M. D. A genetic screen identifies a cellular regulator of adeno-Associated virus. Proc Natl Acad Sci USA 98, 14991-14996, https://doi.org/10.1073/pnas.261567198 (2001).
39. Yan, Z. et al. Optimization of Recombinant Adeno-Associated Virus-Mediated Expression for Large Transgenes, Using a Synthetic Promoter and Tandem Array Enhancers. Hum Gene Ther 26, 334-346, https://doi.org/10.1089/hum.2015.001 (2015).
40. Wang, X. S., Ponnazhagan, S. & Srivastava, A. Rescue and replication of adeno-Associated virus type 2 as well as vector DNA sequences from recombinant plasmids containing deletions in the viral inverted terminal repeats: selective encapsidation of viral genomes in progeny virions. J Virol 70, 1668-1677 (1996).
41. Gao, G. P. et al. Novel adeno-Associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99, 11854-11859, https://doi.org/10.1073/pnas.182412299 (2002).
42. Nonnenmacher, M. & Weber, T. Intracellular transport of recombinant adeno-Associated virus vectors. Gene Ther 19, 649-658, https://doi.org/10.1038/gt.2012.6 (2012).
43. Siegrist, C. A. et al. RFX1 is identical to enhancer factor C and functions as a transactivator of the hepatitis B virus enhancer. Mol Cell Biol 13, 6375-6384 (1993).
44. Moreno, C. S., Beresford, G. W., Louis-Plence, P., Morris, A. C. & Boss, J. M. CREB regulates MHC class II expression in a CIITA-dependent manner. Immunity 10, 143-151 (1999).
45. Zhu, X. S. et al. Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter. Mol Cell Biol 20, 6051-6061 (2000).
46. Buckwold, V. E., Chen, M. & Ou, J. H. Interaction of transcription factors RFX1 and MIBP1 with the gamma motif of the negative regulatory element of the hepatitis B virus core promoter. Virology 227, 515-518, https://doi.org/10.1006/viro.1996.8360 (1997).
47. Seguín-Estévez, Q. et al. The transcription factor RFX protects MHC class II genes against epigenetic silencing by DNA methylation. J Immunol 183, 2545-2553, https://doi.org/10.4049/jimmunol.0900376 (2009).
48. Léger, A. et al. Adeno-Associated viral vector-mediated transgene expression is independent of DNA methylation in primate liver and skeletal muscle. PLoS One 6, e20881, https://doi.org/10.1371/journal.pone.0020881 (2011).
49. Cornille, F. et al. DNA binding properties of a chemically synthesized DNA binding domain of hRFX1. Nucleic Acids Res 26, 2143-2149 (1998).
50. Agami, R. & Shaul, Y. The kinase activity of c-Abl but not v-Abl is potentiated by direct interaction with RFXI, a protein that binds the enhancers of several viruses and cell-cycle regulated genes. Oncogene 16, 1779-1788, https://doi.org/10.1038/sj.onc.1201708 (1998).
51. Smeenk, G. & Mailand, N. Writers, Readers, and Erasers of Histone Ubiquitylation in DNA Double-Strand Break Repair. Front Genet 7, 122, https://doi.org/10.3389/fgene.2016.00122 (2016).
52. Chen, L. et al. Activation of protein kinase C induces nuclear translocation of RFX1 and down-regulates c-myc via an intron 1 X box in undifferentiated leukemia HL-60 cells. J Biol Chem 275, 32227-32233, https://doi.org/10.1074/jbc.M002645200 (2000).
53. Dignam, J. D., Lebovitz, R. M. & Roeder, R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11, 1475-1489 (1983).
54. Grieger, J. C., Choi, V. W. & Samulski, R. J. Production and characterization of adeno-Associated viral vectors. Nat Protoc 1, 1412-1428, https://doi.org/10.1038/nprot.2006.207 (2006).