Deimmunization for gene therapy: Host matching of synthetic zinc finger constructs enables long-term mutant Huntingtin repression in mice

Molecular Neurodegeneration

Volumn 11, Issue 1, 2016, Pages

  Agustín Pavón, Carmen ^a,d   Mielcarek, Michal ^a   Garriga Canut, Mireia ^b,c   Isalan, Mark ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d UNIVERSITAT JAUME I   (Spain)

Author keywords

Gene therapy; Host optimization; Huntington's disease; Immune response; Monogenetic disease; Neurodegenerative disorder; rAAV; Synthetic transcription factors

Indexed keywords

ADENOVIRUS VECTOR; BETA ACTIN; GREEN FLUORESCENT PROTEIN; HUNTINGTIN; NEURON SPECIFIC ENOLASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN KOX1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENHANCER REGION; FEMALE; GENE EXPRESSION; GENE REPRESSION; HTT GENE; HUNTINGTON CHOREA; INFLAMMATION; MALE; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; SINGLE DRUG DOSE; TRANSGENE; VIRAL GENE THERAPY; ANIMAL; BRAIN; DISEASE MODEL; GENE THERAPY; GENE VECTOR; GENETICS; HUNTINGTON DISEASE; METABOLISM; PROCEDURES;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; GENETIC THERAPY; GENETIC VECTORS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; MICE; NEURONS; PROMOTER REGIONS, GENETIC; ZINC FINGERS;

EID: 84986261669     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/s13024-016-0128-x     Document Type: Article

References (39)

1. Basner-Tschakarjan E, Bijjiga E, Martino AT. Pre-clinical assessment of immune responses to adeno-associated virus (AAV) vectors. Front. Immunol. 2014;5:28.
2. Papayannakos C, Daniel R. Understanding lentiviral vector chromatin targeting: working to reduce insertional mutagenic potential for gene therapy. Gene Ther [Internet]. 2013;20:581-8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23171920.
3. Sillay K, Hinchman A, Kumbier L, Schomberg D, Ross C, Kubota K, et al. Strategies for the delivery of multiple collinear infusion clouds in convection-enhanced delivery in the treatment of Parkinson's disease. Stereotact Funct Neurosurg. 2013;91:153-61.
4. Yin D, Zhai Y, Gruber HE, Ibanez CE, Robbins JM, Kells a P, et al. Convection-enhanced delivery improves distribution and efficacy of tumor-selective retroviral replicating vectors in a rodent brain tumor model. Cancer Gene Ther [Internet]. 2013;20:336-41. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3733370/.
5. Biffi A, Montini E, Lorioli L, Cesani M, Fumagalli F, Plati T, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science [Internet]. 2013;341:1233158. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23845948.
6. Tebas P, Stein D, Tang WW, Frank I, Wang SQ, Lee G, et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med [Internet]. 2014;370:901-10. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24597865.
7. Isalan M. Zinc-finger nucleases: how to play two good hands. Nat Methods. 2011;9:32-4.
8. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott D a, Mikkelsen TS, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science [Internet]. 2014;343:84-7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24336571.
9. Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol. 2001;21:289-97.
10. Agustín-Pavón C, Isalan M. Synthetic biology and therapeutic strategies for the degenerating brain: Synthetic biology approaches can transform classical cell and gene therapies, to provide new cures for neurodegenerative diseases. BioEssays. 2014;36:979-90.
11. Ciesielska A, Hadaczek P, Mittermeyer G, Zhou S, Wright JF, Bankiewicz KS, et al. Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cell-mediated immune responses. Mol Ther. 2013;21:158-66.
12. Hadaczek P, Forsayeth J, Mirek H, Munson K, Bringas J, Pivirotto P, et al. Transduction of nonhuman primate brain with adeno-associated virus serotype 1: vector trafficking and immune response. Hum Gene Ther. 2009;20:225-37.
13. Samaranch L, San Sebastian W, Kells AP, Salegio E a, Heller G, Bringas JR, et al. AAV9-mediated expression of a non-self protein in nonhuman primate central nervous system triggers widespread neuroinflammation driven by antigen-presenting cell transduction. Mol Ther [Internet]. 2014;22:329-37. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24419081.
14. Garriga-Canut M, Agustin-Pavon C, Herrmann F, Sanchez A, Dierssen M, Fillat C, et al. PNAS Plus: Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice. Proc Natl Acad Sci. 2012;109:E3136-45.
15. Zuccato C, Valenza M, Cattaneo E. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol Rev. 2010;90:905-81.
16. Zielonka D, Mielcarek M, Landwehrmeyer GB. Update on Huntington's disease: Advances in care and emerging therapeutic options. Park. Relat. Disord. 2015;21:169-78.
17. Kordasiewicz HB, Stanek LM, Wancewicz EV, Mazur C, McAlonis MM, Pytel KA, et al. Sustained therapeutic reversal of huntington's disease by transient repression of huntingtin synthesis. Neuron. 2012;74:1031-44.
18. Yu D, Pendergraff H, Liu J, Kordasiewicz HB, Cleveland DW, Swayze EE, et al. Single-stranded RNAs use RNAi to potently and allele-selectively inhibit mutant huntingtin expression. Cell. 2012;150:895-908.
19. Thiesen HJ. Multiple genes encoding zinc finger domains are expressed in human T cells. New Biol. 1990;2:363-74.
20. Herchenröder O, Hahne JC, Meyer WKH, Thiesen HJ, Schneider J. Repression of the human immunodeficiency virus type 1 promoter by the human KRAB domain results in inhibition of virus production. Biochim Biophys Acta - Gene Struct Expr. 1999;1445:216-23.
21. Groner AC, Meylan S, Ciuffi A, Zangger N, Ambrosini G, Dénervaud N, et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet. 2010;6:e1000869.
22. Pavletich NP, Pabo CO. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science. 1991;252:809-17.
23. Abrink M, Ortiz JA, Mark C, Sanchez C, Looman C, Hellman L, et al. Conserved interaction between distinct Krüppel-associated box domains and the transcriptional intermediary factor 1 beta. Proc Natl Acad Sci USA. 2001;98:1422-6.
24. Isalan M, Klug A, Choo Y. A rapid, generally applicable method to engineer zinc fingers illustrated by targeting the HIV-1 promoter. Nat Biotechnol. 2001;19:656-60.
25. Moore M, Klug A, Choo Y. Improved DNA binding specificity from polyzinc finger peptides by using strings of two-finger units. Proc Natl Acad Sci USA. 2001;98:1437-41.
26. Benn CL, Butler R, Mariner L, Nixon J, Moffitt H, Mielcarek M, et al. Genetic knock-down of HDAC7 does not ameliorate disease pathogenesis in the R6/2 mouse model of Huntington's disease. PLoS One. 2009;4:e5747.
27. Mielcarek M, Landles C, Weiss A, Bradaia A, Seredenina T, Inuabasi L, et al. HDAC4 reduction: a novel therapeutic strategy to target cytoplasmic huntingtin and ameliorate neurodegeneration. PLoS Biol. 2013;11:e1001717.
28. Garg S, Oran AE, Hon H, Jacob J. The hybrid cytomegalovirus enhancer/chicken beta-actin promoter along with woodchuck hepatitis virus posttranscriptional regulatory element enhances the protective efficacy of DNA vaccines. J Immunol. 2004;173:550-8.
29. Kim J-Y, Grunke SD, Levites Y, Golde TE, Jankowsky JL. Intracerebroventricular viral injection of the neonatal mouse brain for persistent and widespread neuronal transduction. J Vis Exp [Internet]. 2014;19:51863. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25286085 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199253/.
30. Oorschot DE. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: A stereological study using the cavalieri and optical disector methods. J Comp Neurol. 1996;366:580-99.
31. Zhou Y, Zhang T, Zhang QK, Jiang Y, Xu DG, Zhang M, et al. Unstable expression of transgene is associated with the methylation of CAG promoter in the offspring from the same litter of homozygous transgenic mice. Mol Biol Rep. 2014;41:5177-86.
32. Peel AL, Zolotukhin S, Schrimsher GW, Muzyczka N, Reier PJ. Efficient transduction of green fluorescent protein in spinal cord neurons using adeno-associated virus vectors containing cell type-specific promoters. Gene Ther. 1997;4:16-24.
33. Forss-Petter S, Danielson PE, Catsicas S, Battenberg E, Price J, Nerenberg M, et al. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron. 1990;5:187-97.
34. Xu R, Janson CG, Mastakov M, Lawlor P, Young D, Mouravlev A, et al. Quantitative comparison of expression with adeno-associated virus (AAV-2) brain-specific gene cassettes. Gene Ther. 2001;8:1323-32.
35. Carter P, Presta L, Gorman CM, Ridgway JB, Henner D, Wong WL, et al. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc Natl Acad Sci USA. 1992;89:4285-9.
36. Presta LG, Chen H, O'Connor SJ, Chisholm V, Meng YG, Krummen L, et al. Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res. 1997;57:4593-9.
37. Parker AS, Zheng W, Griswold KE, Bailey-Kellogg C. Optimization algorithms for functional deimmunization of therapeutic proteins. BMC Bioinformatics. 2010;11:180.
38. Papadakis ED, Nicklin SA, Baker AH, White SJ. Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther [Internet]. 2004;4:89-113. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15032617.
39. George Paxinos KF. Paxinos and Franklin's the Mouse Brain in Stereotaxic Coordinates [Internet]. São Paulo: Acad Press; 2012. p. 360. Available from: https://www.elsevier.com/books/paxinos-and-franklins-the-mouse-brain-in-stereotaxic-coordinates/paxinos/978-0-12-391057-8.