Recent Advances in Gene Therapy and Modeling of Chronic Granulomatous Disease
-
Arefeh Jafarian
,
Gelareh Shokri
,
Mahdieh Shokrollahi Barough
,
Mostafa Moin
,
Zahra Pourpak
,
Masoud Soleimani
Abstract
The Chronic granulomatous disease (CGD) is a primary immunodeficiency that characterized by mutations in phagocyte nicotinamide adenine dinucleotide phosphate (NADPH) oxidase, resulting in deficient antimicrobial activity of phagocytic cells and recurrent childhood infections. Hematopoietic stem cell transplantation (HSCT) is a curative option for patients with human leukocyte antigen (HLA) matched donor, when conventional cares and therapies fail. However, in many cases when the patients have not an HLA-matched donor, they need to a method to recapitulate the function of the affected gene within the patient’s own cells. Gene therapy is a promising approach for CGD. While, the success of retroviral or lentiviral vectors in gene therapy for CGD has been hampered by random integration and insertional activation of proto-oncogenes. These serious adverse events led to improvement and generations of viral vectors with increased safety characteristics. Gene therapy continues to progress and the advent of new technologies, such as engineered endonucleases that have shown a great promise for the treatment of genetic disease. This review focuses on the application of gene therapy for the CGD, the limitations encountered in current clinical trials, advantages and disadvantages of endonucleases in gene correction and modeling with CRISPR/Cas9 approach.
1. Roos D. Chronic granulomatous disease. Br Med Bull 2016; 118(1):50-63.
2. Jones LB, McGrogan P, Flood TJ, Gennery AR, Morton L, Thrasher A, et al. Special article: chronic granulomatous disease in the United Kingdom and Ireland: a comprehensive national patient-based registry. Clin Exp Immunol 2008; 152(2):211-8.
3. Seger RA. Modern management of chronic granulomatous disease. Br J Haematol 2008; 140(3):255-66.
4. Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010; 116(9):1570-3.
5. Rezvani Z, Mohammadzadeh I, Pourpak Z, Moin M, Teimourian S. CYBB Gene Mutation Detection in an Iranian Patient with Chronic Granulomatous Disease. Iran J Allergy Asthma Immunol 2005; 4(2):103-6.
6. Roos D, Kuhns DB, Maddalena A, Bustamante J, Kannengiesser C, de Boer M, et al. Hematologically important mutations: the autosomal recessive forms of chronic granulomatous disease (second update). Blood Cells Mol Dis 2010; 44(4):291-9.
7. van den Berg JM, van Koppen E, Ahlin A, Belohradsky BH, Bernatowska E, Corbeel L, et al. Chronic granulomatous disease: the European experience. PLoS One 2009; 4(4):21.
8. Kuhns DB, Alvord WG, Heller T, Feld JJ, Pike KM, Marciano BE, et al. Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med 2010; 363(27):2600-10.
9. Hager M, Cowland JB, Borregaard N. Neutrophil granules in health and disease. J Intern Med 2010; 268(1):25-34.
10. Bagaitkar J, Barbu EA, Perez-Zapata LJ, Austin A, Huang G, Pallat S, et al. PI(3)P-p40phox binding regulates NADPH oxidase activation in mouse macrophages and magnitude of inflammatory responses in vivo. J Leukoc Biol 2016; 101(2):449-57.
11. Kaufmann KB, Chiriaco M, Siler U, Finocchi A, Reichenbach J, Stein S, et al. Gene therapy for chronic granulomatous disease: current status and future perspectives. Curr Gene Ther 2014; 14(6):447-60.
12. Fattahi F, Badalzadeh M, Sedighipour L, Movahedi M, Fazlollahi MR, Mansouri SD, et al. Inheritance pattern and clinical aspects of 93 Iranian patients with chronic granulomatous disease. J Clin Immunol 2011; 31(5):792-801.
13. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013; 8(11):2281-308.
14. Ott MG, Schmidt M, Schwarzwaelder K, Stein S, Siler U, Koehl U, et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 2006; 12(4):401-9.
15. Stein S, Ott MG, Schultze-Strasser S, Jauch A, Burwinkel B, Kinner A, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010; 16(2):198-204.
16. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114(13):2619-22.
17. Malech HL, Maples PB, Whiting-Theobald N, Linton GF, Sekhsaria S, Vowells SJ, et al. Prolonged production of NADPH oxidase-corrected granulocytes after gene therapy of chronic granulomatous disease. Proc Natl Acad Sci U S A 1997; 94(22):12133-8.
18. Goebel WS, Dinauer MC. Retroviral-mediated gene transfer and nonmyeloablative conditioning: studies in a murine X-linked chronic granulomatous disease model. J Pediatr Hematol Oncol 2002;24(9):787-90.
19. Ott MG, Seger R, Stein S, Siler U, Hoelzer D, Grez M. Advances in the treatment of Chronic Granulomatous Disease by gene therapy. Curr Gene Ther 2007; 7(3):155-61.
20. Kang EM, Choi U, Theobald N, Linton G, Long Priel DA, Kuhns D, et al. Retrovirus gene therapy for X-linked chronic granulomatous disease can achieve stable long-term correction of oxidase activity in peripheral blood neutrophils. Blood 2010; 115(4):783-91.
21. Held PK, Olivares EC, Aguilar CP, Finegold M, Calos MP, Grompe M. In vivo correction of murine hereditary tyrosinemia type I by phiC31 integrase-mediated gene delivery. Mol Ther. 2005;11(3):399-408.
22. Rivat C, Santilli G, Gaspar HB, Thrasher AJ. Gene therapy for primary immunodeficiencies. Hum Gene Ther 2012; 23(7):668-75.
23. Kohn DB, Kuo CY. New frontiers in the therapy of primary immunodeficiency: From gene addition to gene editing. J Allergy Clin Immunol 2017; 139(3):726-32.
24. Chiriaco M, Farinelli G, Capo V, Zonari E, Scaramuzza S, Di Matteo G, et al. Dual-regulated lentiviral vector for gene therapy of X-linked chronic granulomatosis. Mol Ther 2014; 22(8):1472-83.
25. Barde I, Laurenti E, Verp S, Wiznerowicz M, Offner S, Viornery A, et al. Lineage- and stage-restricted lentiviral vectors for the gene therapy of chronic granulomatous disease. Gene therapy 2011; 18(11):1087-97.
26. Sauer AV, Di Lorenzo B, Carriglio N, Aiuti A. Progress in gene therapy for primary immunodeficiencies using lentiviral vectors. Curr Opin Allergy Clin Immunol 2014; 14(6):527-34.
27. Malech HL. Use of serum-free medium with fibronectin fragment enhanced transduction in a system of gas permeable plastic containers to achieve high levels of retrovirus transduction at clinical scale. Stem cells (Dayton, Ohio) 2000; 18(2):155-6.
28. Cavazzana-Calvo M, Fischer A, Hacein-Bey-Abina S, Aiuti A. Gene therapy for primary immunodeficiencies: Part 1. Curr Opin Immunol 2012; 24(5):580-4.
29. Jafarian A, Taghikani M, Abroun S, Allahverdi A, Lamei M, Lakpour N, et al. The Generation of Insulin Producing Cells from Human Mesenchymal Stem Cells by MiR-375 and Anti-MiR-9. PLoS One 2015; 10(6):e0128650.
30. Hacein-Bey-Abina S, et al. A modified gamma-retrovirus vector for X-linked severe combined immunodeficiency. N Engl J Med 2014; 371(15):1407-17.
31. Aiuti A, Biasco L, Scaramuzza S, Ferrua F, Cicalese MP, Baricordi C, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013; 341(6148):1233151.
32. Xu W, Russ JL, Eiden MV. Evaluation of Residual Promoter Activity in [gamma]-Retroviral Self-inactivating (SIN) Vectors. Mol Ther 2012; 20(1):84-90.
33. Yu SF, von Ruden T, Kantoff PW, Garber C, Seiberg M, Ruther U, et al. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc Natl Acad Sci U S A 1986; 83(10):3194-8.
34. Kaufmann KB, Brendel C, Suerth JD, Mueller-Kuller U, Chen-Wichmann L, Schwable J, et al. Alpharetroviral vector-mediated gene therapy for X-CGD: functional correction and lack of aberrant splicing. Mol Ther 2013; 21(3):648-61.
35. Maria Chiriaco, Giada Farinelli, Valentina Capo, Erika Zonari, Samantha Scaramuzza, Gigliola Di Matteo, et al. Dual-regulated Lentiviral Vector for Gene Therapy of X-linked Chronic Granulomatosis. Mol Ther. 2014 Aug; 22(8): 1472–1483.
36. Mobarra N, Shafiee A, Rad SMAH, Tasharrofi N, Soufi-zomorod M, Hafizi M, et al. Overexpression of microRNA-16 declines cellular growth, proliferation and induces apoptosis in human breast cancer cells. In Vitro Cell Dev Biol Anim 2015; 51(6):604-11.
37. Santilli G, Almarza E, Brendel C, Choi U, Beilin C, Blundell MP, et al. Biochemical correction of X-CGD by a novel chimeric promoter regulating high levels of transgene expression in myeloid cells. Mol Ther 2011; 19(1):122-32.
38. Brendel C, Muller-Kuller U, Schultze-Strasser S, Stein S, Chen-Wichmann L, Krattenmacher A, et al. Physiological regulation of transgene expression by a lentiviral vector containing the A2UCOE linked to a myeloid promoter. Gene therapy 2012; 19(10):1018-29.
39. Chiriaco M, Farinelli G, Capo V, Zonari E, Scaramuzza S, Di Matteo G, et al. Dual-regulated Lentiviral Vector for Gene Therapy of X-linked Chronic Granulomatosis. Molecular Therapy 2014; 22(8):1472-83.
40. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 2003; 4(9):712-20.
41. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, et al. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 1998; 17(18):5497-508.
42. Naldini L. Gene therapy returns to centre stage. Nature 2015; 526(7573):351-60.
43. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, et al. Widespread siRNA “off-target” transcript silencing mediated by seed region sequence complementarity. RNA 2006; 12(7):1179-87.
44. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 2014; 24(1):132-41.
45. Carroll D. Genome engineering with zinc-finger nucleases. Genetics. 2011;188(4):773-82.
46. Porteus MH, Carroll D. Gene targeting using zinc finger nucleases. Nat Biotechnol 2005; 23(8):967-73.
47. Boch J, Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual review of phytopathology. 2010;48:419-36.
48. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Research. 2011;39(12):e82-e.
49. Xiao-Hui Zhang, Louis Y Tee, Xiao-Gang Wang, Qun-Shan Huang, Shi-Hua Yang. Off-target Effects in CRISPR/Cas9-mediated Genome Engineering. Mol Ther Nucleic Acids. 2015; 4(11): e264.
50. Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 2012; 109(39):E2579-86.
51. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, et al. RNA-Guided RNA Cleavage by a CRISPR RNA-Cas Protein Complex. Cell 2009; 139(5):945-56.
52. Eric SL. CRISPR Timeline USA: Broad institute; 2015 [cited 2016]. Available from: https://www.broadinstitute.org/what-broad/areas-focus/project-spotlight/crispr-timeline.
53. Lander Eric S. The Heroes of CRISPR. Cell 2016; 164(1–2):18-28.
54. Barrangou R, Marraffini Luciano A. CRISPR-Cas Systems: Prokaryotes Upgrade to Adaptive Immunity. Molecular Cell 2014; 54(2):234-44.
55. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, Snijders APL, et al. Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes. Science 2008; 321(5891):960-4.
56. Zou J, Sweeney CL, Chou BK, Choi U, Pan J, Wang H, et al. Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease-mediated safe harbor targeting. Blood 2011; 117(21):5561-72.
57. Merling RK, Sweeney CL, Chu J, Bodansky A, Choi U, Priel DL, et al. An AAVS1-targeted minigene platform for correction of iPSCs from all five types of chronic granulomatous disease. Mol Ther 2015; 23(1):147-57.
58. Dreyer AK, Hoffmann D, Lachmann N, Ackermann M, Steinemann D, Timm B, et al. TALEN-mediated functional correction of X-linked chronic granulomatous disease in patient-derived induced pluripotent stem cells. Biomaterials 2015; 69:191-200.
59. Sweeney CL, Zou J, Choi U, Merling RK, Liu A, Bodansky A, et al. Targeted Repair of CYBB in X-CGD iPSCs Requires Retention of Intronic Sequences for Expression and Functional Correction. Mol Ther 2017; 25(2):321-30.
60. Flynn R, Grundmann A, Renz P, Hanseler W, James WS, Cowley SA, et al. CRISPR-mediated genotypic and phenotypic correction of a chronic granulomatous disease mutation in human iPS cells. Exp Hematol 2015; 43(10):838-48.
61. De Ravin SS, Li L, Wu X, Choi U, Allen C, Koontz S, et al. CRISPR-Cas9 gene repair of hematopoietic stem cells from patients with X-linked chronic granulomatous disease. Sci Transl Med 2017; 9(372).
62. Nishiguchi M, Kikuyama H, Kanazawa T, Tsutsumi A, Kaneko T, Uenishi H, et al. Increases in iPS Transcription Factor (Oct4, Sox2, c-Myc, and Klf4) Gene Expression after Modified Electroconvulsive Therapy. Psychiatry Investig 2015; 12(4):532-7.
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2. Jones LB, McGrogan P, Flood TJ, Gennery AR, Morton L, Thrasher A, et al. Special article: chronic granulomatous disease in the United Kingdom and Ireland: a comprehensive national patient-based registry. Clin Exp Immunol 2008; 152(2):211-8.
3. Seger RA. Modern management of chronic granulomatous disease. Br J Haematol 2008; 140(3):255-66.
4. Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010; 116(9):1570-3.
5. Rezvani Z, Mohammadzadeh I, Pourpak Z, Moin M, Teimourian S. CYBB Gene Mutation Detection in an Iranian Patient with Chronic Granulomatous Disease. Iran J Allergy Asthma Immunol 2005; 4(2):103-6.
6. Roos D, Kuhns DB, Maddalena A, Bustamante J, Kannengiesser C, de Boer M, et al. Hematologically important mutations: the autosomal recessive forms of chronic granulomatous disease (second update). Blood Cells Mol Dis 2010; 44(4):291-9.
7. van den Berg JM, van Koppen E, Ahlin A, Belohradsky BH, Bernatowska E, Corbeel L, et al. Chronic granulomatous disease: the European experience. PLoS One 2009; 4(4):21.
8. Kuhns DB, Alvord WG, Heller T, Feld JJ, Pike KM, Marciano BE, et al. Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med 2010; 363(27):2600-10.
9. Hager M, Cowland JB, Borregaard N. Neutrophil granules in health and disease. J Intern Med 2010; 268(1):25-34.
10. Bagaitkar J, Barbu EA, Perez-Zapata LJ, Austin A, Huang G, Pallat S, et al. PI(3)P-p40phox binding regulates NADPH oxidase activation in mouse macrophages and magnitude of inflammatory responses in vivo. J Leukoc Biol 2016; 101(2):449-57.
11. Kaufmann KB, Chiriaco M, Siler U, Finocchi A, Reichenbach J, Stein S, et al. Gene therapy for chronic granulomatous disease: current status and future perspectives. Curr Gene Ther 2014; 14(6):447-60.
12. Fattahi F, Badalzadeh M, Sedighipour L, Movahedi M, Fazlollahi MR, Mansouri SD, et al. Inheritance pattern and clinical aspects of 93 Iranian patients with chronic granulomatous disease. J Clin Immunol 2011; 31(5):792-801.
13. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013; 8(11):2281-308.
14. Ott MG, Schmidt M, Schwarzwaelder K, Stein S, Siler U, Koehl U, et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 2006; 12(4):401-9.
15. Stein S, Ott MG, Schultze-Strasser S, Jauch A, Burwinkel B, Kinner A, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010; 16(2):198-204.
16. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114(13):2619-22.
17. Malech HL, Maples PB, Whiting-Theobald N, Linton GF, Sekhsaria S, Vowells SJ, et al. Prolonged production of NADPH oxidase-corrected granulocytes after gene therapy of chronic granulomatous disease. Proc Natl Acad Sci U S A 1997; 94(22):12133-8.
18. Goebel WS, Dinauer MC. Retroviral-mediated gene transfer and nonmyeloablative conditioning: studies in a murine X-linked chronic granulomatous disease model. J Pediatr Hematol Oncol 2002;24(9):787-90.
19. Ott MG, Seger R, Stein S, Siler U, Hoelzer D, Grez M. Advances in the treatment of Chronic Granulomatous Disease by gene therapy. Curr Gene Ther 2007; 7(3):155-61.
20. Kang EM, Choi U, Theobald N, Linton G, Long Priel DA, Kuhns D, et al. Retrovirus gene therapy for X-linked chronic granulomatous disease can achieve stable long-term correction of oxidase activity in peripheral blood neutrophils. Blood 2010; 115(4):783-91.
21. Held PK, Olivares EC, Aguilar CP, Finegold M, Calos MP, Grompe M. In vivo correction of murine hereditary tyrosinemia type I by phiC31 integrase-mediated gene delivery. Mol Ther. 2005;11(3):399-408.
22. Rivat C, Santilli G, Gaspar HB, Thrasher AJ. Gene therapy for primary immunodeficiencies. Hum Gene Ther 2012; 23(7):668-75.
23. Kohn DB, Kuo CY. New frontiers in the therapy of primary immunodeficiency: From gene addition to gene editing. J Allergy Clin Immunol 2017; 139(3):726-32.
24. Chiriaco M, Farinelli G, Capo V, Zonari E, Scaramuzza S, Di Matteo G, et al. Dual-regulated lentiviral vector for gene therapy of X-linked chronic granulomatosis. Mol Ther 2014; 22(8):1472-83.
25. Barde I, Laurenti E, Verp S, Wiznerowicz M, Offner S, Viornery A, et al. Lineage- and stage-restricted lentiviral vectors for the gene therapy of chronic granulomatous disease. Gene therapy 2011; 18(11):1087-97.
26. Sauer AV, Di Lorenzo B, Carriglio N, Aiuti A. Progress in gene therapy for primary immunodeficiencies using lentiviral vectors. Curr Opin Allergy Clin Immunol 2014; 14(6):527-34.
27. Malech HL. Use of serum-free medium with fibronectin fragment enhanced transduction in a system of gas permeable plastic containers to achieve high levels of retrovirus transduction at clinical scale. Stem cells (Dayton, Ohio) 2000; 18(2):155-6.
28. Cavazzana-Calvo M, Fischer A, Hacein-Bey-Abina S, Aiuti A. Gene therapy for primary immunodeficiencies: Part 1. Curr Opin Immunol 2012; 24(5):580-4.
29. Jafarian A, Taghikani M, Abroun S, Allahverdi A, Lamei M, Lakpour N, et al. The Generation of Insulin Producing Cells from Human Mesenchymal Stem Cells by MiR-375 and Anti-MiR-9. PLoS One 2015; 10(6):e0128650.
30. Hacein-Bey-Abina S, et al. A modified gamma-retrovirus vector for X-linked severe combined immunodeficiency. N Engl J Med 2014; 371(15):1407-17.
31. Aiuti A, Biasco L, Scaramuzza S, Ferrua F, Cicalese MP, Baricordi C, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013; 341(6148):1233151.
32. Xu W, Russ JL, Eiden MV. Evaluation of Residual Promoter Activity in [gamma]-Retroviral Self-inactivating (SIN) Vectors. Mol Ther 2012; 20(1):84-90.
33. Yu SF, von Ruden T, Kantoff PW, Garber C, Seiberg M, Ruther U, et al. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc Natl Acad Sci U S A 1986; 83(10):3194-8.
34. Kaufmann KB, Brendel C, Suerth JD, Mueller-Kuller U, Chen-Wichmann L, Schwable J, et al. Alpharetroviral vector-mediated gene therapy for X-CGD: functional correction and lack of aberrant splicing. Mol Ther 2013; 21(3):648-61.
35. Maria Chiriaco, Giada Farinelli, Valentina Capo, Erika Zonari, Samantha Scaramuzza, Gigliola Di Matteo, et al. Dual-regulated Lentiviral Vector for Gene Therapy of X-linked Chronic Granulomatosis. Mol Ther. 2014 Aug; 22(8): 1472–1483.
36. Mobarra N, Shafiee A, Rad SMAH, Tasharrofi N, Soufi-zomorod M, Hafizi M, et al. Overexpression of microRNA-16 declines cellular growth, proliferation and induces apoptosis in human breast cancer cells. In Vitro Cell Dev Biol Anim 2015; 51(6):604-11.
37. Santilli G, Almarza E, Brendel C, Choi U, Beilin C, Blundell MP, et al. Biochemical correction of X-CGD by a novel chimeric promoter regulating high levels of transgene expression in myeloid cells. Mol Ther 2011; 19(1):122-32.
38. Brendel C, Muller-Kuller U, Schultze-Strasser S, Stein S, Chen-Wichmann L, Krattenmacher A, et al. Physiological regulation of transgene expression by a lentiviral vector containing the A2UCOE linked to a myeloid promoter. Gene therapy 2012; 19(10):1018-29.
39. Chiriaco M, Farinelli G, Capo V, Zonari E, Scaramuzza S, Di Matteo G, et al. Dual-regulated Lentiviral Vector for Gene Therapy of X-linked Chronic Granulomatosis. Molecular Therapy 2014; 22(8):1472-83.
40. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 2003; 4(9):712-20.
41. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, et al. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 1998; 17(18):5497-508.
42. Naldini L. Gene therapy returns to centre stage. Nature 2015; 526(7573):351-60.
43. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, et al. Widespread siRNA “off-target” transcript silencing mediated by seed region sequence complementarity. RNA 2006; 12(7):1179-87.
44. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 2014; 24(1):132-41.
45. Carroll D. Genome engineering with zinc-finger nucleases. Genetics. 2011;188(4):773-82.
46. Porteus MH, Carroll D. Gene targeting using zinc finger nucleases. Nat Biotechnol 2005; 23(8):967-73.
47. Boch J, Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual review of phytopathology. 2010;48:419-36.
48. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Research. 2011;39(12):e82-e.
49. Xiao-Hui Zhang, Louis Y Tee, Xiao-Gang Wang, Qun-Shan Huang, Shi-Hua Yang. Off-target Effects in CRISPR/Cas9-mediated Genome Engineering. Mol Ther Nucleic Acids. 2015; 4(11): e264.
50. Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 2012; 109(39):E2579-86.
51. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, et al. RNA-Guided RNA Cleavage by a CRISPR RNA-Cas Protein Complex. Cell 2009; 139(5):945-56.
52. Eric SL. CRISPR Timeline USA: Broad institute; 2015 [cited 2016]. Available from: https://www.broadinstitute.org/what-broad/areas-focus/project-spotlight/crispr-timeline.
53. Lander Eric S. The Heroes of CRISPR. Cell 2016; 164(1–2):18-28.
54. Barrangou R, Marraffini Luciano A. CRISPR-Cas Systems: Prokaryotes Upgrade to Adaptive Immunity. Molecular Cell 2014; 54(2):234-44.
55. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, Snijders APL, et al. Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes. Science 2008; 321(5891):960-4.
56. Zou J, Sweeney CL, Chou BK, Choi U, Pan J, Wang H, et al. Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease-mediated safe harbor targeting. Blood 2011; 117(21):5561-72.
57. Merling RK, Sweeney CL, Chu J, Bodansky A, Choi U, Priel DL, et al. An AAVS1-targeted minigene platform for correction of iPSCs from all five types of chronic granulomatous disease. Mol Ther 2015; 23(1):147-57.
58. Dreyer AK, Hoffmann D, Lachmann N, Ackermann M, Steinemann D, Timm B, et al. TALEN-mediated functional correction of X-linked chronic granulomatous disease in patient-derived induced pluripotent stem cells. Biomaterials 2015; 69:191-200.
59. Sweeney CL, Zou J, Choi U, Merling RK, Liu A, Bodansky A, et al. Targeted Repair of CYBB in X-CGD iPSCs Requires Retention of Intronic Sequences for Expression and Functional Correction. Mol Ther 2017; 25(2):321-30.
60. Flynn R, Grundmann A, Renz P, Hanseler W, James WS, Cowley SA, et al. CRISPR-mediated genotypic and phenotypic correction of a chronic granulomatous disease mutation in human iPS cells. Exp Hematol 2015; 43(10):838-48.
61. De Ravin SS, Li L, Wu X, Choi U, Allen C, Koontz S, et al. CRISPR-Cas9 gene repair of hematopoietic stem cells from patients with X-linked chronic granulomatous disease. Sci Transl Med 2017; 9(372).
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| Files | ||
| Issue | Vol 18, No 2 (2019) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v18i2.916 | |
| Keywords | ||
| Chronic granulomatous disease Endonucleases Gene editing NADPH oxidases | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Jafarian A, Shokri G, Shokrollahi Barough M, Moin M, Pourpak Z, Soleimani M. Recent Advances in Gene Therapy and Modeling of Chronic Granulomatous Disease. Iran J Allergy Asthma Immunol. 2019;18(2):131-142.
