Genome editing in cardiovascular diseases

Nature Reviews Cardiology

Volumn 14, Issue 1, 2016, Pages 11-20

  Strong, Alanna ^a,b   Musunuru, Kiran ^b  

^a ST CHRISTOPHER'S HOSPITAL FOR CHILDREN   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

AMINO TERMINAL SEQUENCE; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CELL LABELING; DISEASE MODEL; DNA CLEAVAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENE EDITING; GENE MUTATION; GENE TECHNOLOGY; HERITABILITY; HUMAN; LIPID METABOLISM; MUTAGENESIS; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; TRANSGENE; GENETICS;

CARDIOVASCULAR DISEASES; GENE EDITING; HUMANS;

EID: 84986634232     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2016.139     Document Type: Review

References (110)

1. Urnov, F. D., et al. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646 (2010).
2. Bogdanove, A. J., & Voytas, D. F. TAL effectors: customizable proteins for DNA targeting. Science 333, 1843-1846 (2011).
3. Hsu, P. D., Lander, E. S., & Zhang, F. Development and applications of CRISPR Cas9 for genome engineering. Cell 157, 1262-1278 (2014).
4. Gupta, R. M., & Musunuru, K. Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR Cas9. J. Clin. Invest. 124, 4154-4161 (2014).
5. Wright, A. V., Nuñez, J. K., & Doudna, J. A. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164, 29-44 (2016).
6. Kim, Y. G., Cha, J., & Chandrasegaran, S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl Acad. Sci. USA 93, 1156-1160 (1996).
7. Bitinaite, J., Wah, D. A., Aggarwal, A. K., & Schildkraut, I. FokI dimerization is required for DNA cleavage. Proc. Natl Acad. Sci. USA 95, 10570-10575 (1998).
8. Moscou, M. J., & Bogdanove, A. J. A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501 (2009).
9. Boch, J., et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512 (2009).
10. Christian, M., et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761 (2010).
11. Jinek, M., et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
12. Cong, L., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
13. Mali, P., et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
14. Hwang, W. Y., et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31, 227-229 (2013).
15. Cho, S. W., Kim, S., Kim, J. M., & Kim, J. S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232 (2013).
16. Hou, Z., et al. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl Acad. Sci. USA 110, 15644-15649 (2013).
17. Esvelt, K. M., et al. Orthogonal Cas9 proteins for RNA guided gene regulation and editing. Nat. Methods 10, 1116-1121 (2013).
18. Ran, F. A., et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520, 186-191 (2015).
19. Kleinstiver, B. P., et al. Engineered CRISPR Cas9 nucleases with altered PAM specificities. Nature 523, 481-485 (2015).
20. Hirano, H., et al. Structure and engineering of Francisella novicida Cas9. Cell 164, 950-961 (2016).
21. Zetsche, B., et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163, 759-771 (2015).
22. West, S. C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4, 435-445 (2003).
23. Bibikova, M., Golic, M., Golic, K. G., & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169-1175 (2002).
24. Branzei, D., & Foiani, M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9, 297-308 (2008).
25. Bibikova, M., et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol. 21, 289-297 (2001).
26. Kleinstiver, B. P., et al. Broadening the targeting range of Staphylococcus aureus CRISPR Cas9 by modifying PAM recognition. Nat. Biotechnol. 33, 1293-1298 (2015).
27. Wang, G., et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart on chip technologies. Nat. Med. 20, 616-623 (2014).
28. Hinson, J. T., et al. Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science 349, 982-986 (2015).
29. Karakikes, I., et al. Correction of human phospholamban R14del mutation associated with cardiomyopathy using targeted nucleases and combination therapy. Nat. Commun. 6, 6955 (2015).
30. Wang, Y., et al. Genome editing of isogenic human induced pluripotent stem cells recapitulates long QT phenotype for drug testing. J. Am. Coll. Cardiol. 64, 451-459 (2014).
31. Zhang, M., et al. Recessive cardiac phenotypes in induced pluripotent stem cell models of Jervell and Lange-Nielsen syndrome: disease mechanisms and pharmacological rescue. Proc. Natl Acad. Sci. USA 111, E5383-E5392 (2014).
32. Theodoris, C. V., et al. Human disease modeling reveals integrated transcriptional and epigenetic mechanisms of NOTCH1 haploinsufficiency. Cell 160, 1072-1086 (2015).
33. Ding, Q., et al. A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12, 238-251 (2013).
34. Maetzel, D., et al. Genetic and chemical correction of cholesterol accumulation and impaired autophagy in hepatic and neural cells derived from Niemann-Pick type C patient-specific iPS cells. Stem Cell Rep. 2, 866-880 (2014).
35. Gupta, R. M., Meissner, T. B., Cowan, C. A., & Musunuru, K. Genome-edited human pluripotent stem cell-derived macrophages as a model of reverse cholesterol transport-brief report. Arterioscler. Thromb. Vasc. Biol. 36, 15-18 (2016).
36. Rossi, A., et al. Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524, 230-233 (2015).
37. Novodvorsky, P., et al. klf2ash317 mutant zebrafish do not recapitulate morpholino-induced vascular and haematopoietic phenotypes. PLoS ONE 10, e0141611 (2015).
38. Ota, S., Hisano, Y., Ikawa, Y., & Kawahara, A. Multiple genome modifications by the CRISPR/Cas9 system in zebrafish. Genes Cells 19, 555-564 (2014).
39. Kotani, H., Taimatsu, K., Ohga, R., Ota, S., & Kawahara, A. Efficient multiple genome modifications induced by the crRNAs, tracrRNA and Cas9 protein complex in zebrafish. PLoS ONE 10, e0128319 (2015).
40. Cao, J., et al. Single epicardial cell transcriptome sequencing identifies Caveolin 1 as an essential factor in zebrafish heart regeneration. Development 143, 232-243 (2016).
41. Zou, J., et al. An internal promoter underlies the difference in disease severity between N- and C terminal truncation mutations of Titin in zebrafish. eLife 4, e09406 (2015).
42. Wang, H., et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
43. Yang, H., et al. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379 (2013).
44. Liu, H., et al. TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14, 323-328 (2014).
45. Niu, Y., et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156, 836-843 (2014).
46. Jacob, H. J., Lazar, J., & Dwinell, M. R., Moreno, C., & Geurts, A. M. Gene targeting in the rat: advances and opportunities. Trends Genet. 26, 510-518 (2010
47. Moreno, C., et al. Creation and characterization of a renin knockout rat. Hypertension 57, 614-619 (2011).
48. Endres, B. T., et al. Mutation of Plekha7 attenuates salt-sensitive hypertension in the rat. Proc. Natl Acad. Sci. USA 111, 12817-12822 (2014).
49. Larcher, T., et al. Characterization of dystrophin deficient rats: a new model for Duchenne muscular dystrophy. PLoS ONE 9, e110371 (2014).
50. Li, J., et al. Cold-inducible RNA-binding protein regulates cardiac repolarization by targeting transient outward potassium channels. Circ. Res. 116, 1655-1659 (2015).
51. Zhu, X., et al. Exacerbating pressure overload-induced cardiac hypertrophy: novel role of adaptor molecule Src homology 2 B3. Hypertension 66, 571-581 (2015).
52. Yang, D., et al. Effective gene targeting in rabbits using RNA-guided Cas9 nucleases. J. Mol. Cell. Biol. 6, 97-99 (2014).
53. Ji, D., Zhao, G., Songstad, A., Cui, X., & Weinstein, E. J. Efficient creation of an APOE knockout rabbit. Transgenic Res. 24, 227-235 (2015).
54. Niimi, M., et al. ApoE knockout rabbits: a novel model for the study of human hyperlipidemia. Atherosclerosis 245, 187-193 (2016).
55. Wang, T., et al. Efficient generation of gene-modified pigs via injection of zygote with Cas9/sgRNA. Sci. Rep. 5, 8256 (2015).
56. Umeyama, K., et al. Generation of heterozygous fibrillin 1 mutant cloned pigs from genome-edited foetal fibroblasts. Sci. Rep. 6, 24413 (2016).
57. Ding, Q., et al. Permanent alteration of PCSK9 with in vivo CRISPR Cas9 genome editing. Circ. Res. 115, 488-492 (2014).
58. Yin, H., et al. Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat. Biotechnol. 34, 328-333 (2016).
59. Platt, R. J., et al. CRISPR Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440-455 (2014).
60. Carroll, K. J., et al. A mouse model for adult cardiac-specific gene deletion with CRISPR/Cas9. Proc. Natl Acad. Sci. USA 113, 338-343 (2016).
61. Gantz, J. A., et al. Targeted genomic integration of a selectable floxed dual fluorescence reporter in human embryonic stem cells. PLoS ONE 7, e46971 (2012).
62. Wang, Y., et al. Genome editing of human embryonic stem cells and induced pluripotent stem cells with zinc finger nucleases for cellular imaging. Circ. Res. 111, 1494-1503 (2012).
63. Lepperhof, V., et al. Bioluminescent imaging of genetically selected induced pluripotent stem cell-derived cardiomyocytes after transplantation into infarcted heart of syngeneic recipients. PLoS ONE 9, e107363 (2014).
64. Luo, Y., et al. Stable enhanced green fluorescent protein expression after differentiation and transplantation of reporter human induced pluripotent stem cells generated by AAVS1 transcription activator-like effector nucleases. Stem Cells Transl. Med. 3, 821-835 (2014).
65. Shiba, Y., et al. Human ES cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489, 322-325 (2012).
66. Han, Y., Slivano, O. J., Christie, C. K., Cheng, A. W., & Miano, J. M. CRISPR Cas9 genome editing of a single regulatory element nearly abolishes target gene expression in mice-brief report. Arterioscler. Thromb. Vasc. Biol. 35, 312-315 (2015).
67. Beaudoin, M., et al. Myocardial infarction-Associated SNP at 6p24 interferes with MEF2 binding and associates with PHACTR1 expression levels in human coronary arteries. Arterioscler. Thromb. Vasc. Biol. 35, 1472-1479 (2015).
68. Gilbert, L. A., et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661 (2014).
69. Mandegar, M. A., et al. CRISPR interference efficiently induces specific and reversible gene silencing in human iPSCs. Cell Stem Cell 18, 541-553 (2016).
70. Sakurai, T., et al. Creation of apolipoprotein C II (apoC II) mutant mice and correction of their hypertriglyceridemia with an apoC II mimetic peptide. J. Pharmacol. Exp. Ther. 356, 341-353 (2016).
71. Nagiec, M. M., et al. Modulators of hepatic lipoprotein metabolism identified in a search for small-molecule inducers of tribbles pseudokinase 1 expression. PLoS ONE 10, e0120295 (2015).
72. Zhang, H. S., et al. A designed zinc-finger transcriptional repressor of phospholamban improves function of the failing heart. Mol. Ther. 20, 1508-1515 (2012).
73. Cohen, J. C., Boerwinkle, E., Mosley, T. H. Jr & Hobbs, H. H. Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N. Engl. J. Med. 354, 1264-1272 (2006).
74. Wang, X., et al. CRISPR-Cas9 targeting of PCSK9 in human hepatocytes in vivo-brief report. Arterioscler. Thromb. Vasc. Biol. 36, 783-786 (2016).
75. Long, C., et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351, 400-403 (2016).
76. Nelson, C. E., et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351, 403-407 (2016).
77. Tabebordbar, M., et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351, 407-411 (2016).
78. Yang, Y., et al. A dual AAV system enables the Cas9 mediated correction of a metabolic liver disease in newborn mice. Nat. Biotechnol. 34, 334-338 (2016).
79. Jiang, J., Wakimoto, H., Seidman, J. G., & Seidman, C. E. Allele-specific silencing of mutant Myh6 transcripts in mice suppresses hypertrophic cardiomyopathy. Science 342, 111-114 (2013).
80. Coelho, T., et al. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N. Engl. J. Med. 369, 819-829 (2013).
81. Chong, J. J., et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 12, 273-277 (2014).
82. Tebas, P., et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med. 370, 901-910 (2014).
83. Hsu, P. D., et al. DNA targeting specificity of RNA guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
84. Hinz, J. M., Laughery, M. F., & Wyrick, J. J. Nucleosomes inhibit Cas9 endonuclease activity in vitro. Biochemistry 54, 7063-7066 (2015).
85. Knight, S. C., et al. Dynamics of CRISPR Cas9 genome interrogation in living cells. Science 350, 823-826 (2015).
86. Maruyama, T., et al. Increasing the efficiency of precise genome editing with CRISPR Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33, 538-542 (2015).
87. Chu, V. T., et al. Increasing the efficiency of homology-directed repair for CRISPR Cas9 induced precise gene editing in mammalian cells. Nat. Biotechnol. 33, 543-548 (2015).
88. Yu, C., et al. Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16, 142-147 (2015).
89. Orthwein, A., et al. A mechanism for the suppression of homologous recombination in G1 cells. Nature 528, 422-426 (2015).
90. Lin, S., Staahl, B. T., Alla, R. K., & Doudna, J. A. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. eLife 3, e04766 (2014).
91. Howden, S. E., et al. A Cas9 variant for efficient generation of indel-free knockin or gene-corrected human pluripotent stem cells. Stem Cell Rep. http:// dx.doi.org/10.1016/j.stemcr.2016.07.001 (2016).
92. Sternberg, S. H., LaFrance, B., Kaplan, M., & Doudna, J. A. Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 527, 110-113 (2015).
93. Fu, Y., et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
94. Mali, P., et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013).
95. Pattanayak, V., et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
96. Smith, C., et al. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 15, 12-13 (2014).
97. Veres, A., et al. Low incidence of off-target mutations in individual CRISPR Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15, 27-30 (2014).
98. Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M., & Joung, J. K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32, 279-284 (2014).
99. Ran, F. A., et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
100. Shen, B., et al. Efficient genome modification by CRISPR Cas9 nickase with minimal off-target effects. Nat. Methods 11, 399-402 (2014).
101. Tsai, S. Q., et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569-576 (2014).
102. Guilinger, J. P., Thompson, D. B., & Liu, D. R. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat. Biotechnol. 32, 577-582 (2014).
103. Slaymaker, I. M., et al. Rationally engineered Cas9 nucleases with improved specificity. Science 351, 84-88 (2016).
104. Kleinstiver, B. P., et al. High-fidelity CRISPR Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529, 490-495 (2016).
105. Tsai, S. Q., et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 33, 187-197 (2015).
106. Kim, D., et al. Digenome-seq: genome-wide profiling of CRISPR Cas9 off-target effects in human cells. Nat. Methods 12, 237-243 (2015).
107. Long, C., et al. Prevention of muscular dystrophy in mice by CRISPR/Cas9 mediated editing of germline DNA. Science 345, 1184-1188 (2014).
108. Wu, Y., et al. Correction of a genetic disease by CRISPR Cas9 mediated gene editing in mouse spermatogonial stem cells. Cell Res. 25, 67-79 (2015).
109. Liang, P., et al. CRISPR/Cas9 mediated gene editing in human tripronuclear zygotes. Protein Cell 6, 363-372 (2015).
110. Kang, X., et al. Introducing precise genetic modifications into human 3PN embryos by CRISPR/ Cas-mediated genome editing. J. Assist. Reprod. Genet. 33, 581-588 (2016