CRISPR-Cas9 genome editing of a single regulatory element nearly abolishes target gene expression in mice - Brief report

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 2, 2015, Pages 312-315

  Han, Yu ^a   Slivano, Orazio J ^a   Christie, Christine K ^a   Cheng, Albert W ^b   Miano, Joseph M ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

CArG box; CRISPR; mice; muscle, smooth; serum response factor; transgenic

Indexed keywords

KI 67 ANTIGEN; MESSENGER RNA; MUTANT PROTEIN; PROTEIN CNN1; REGULATOR PROTEIN; SERUM RESPONSE FACTOR; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CALCIUM BINDING PROTEIN; CALPONIN;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CNN1 GENE; CRISPR CAS SYSTEM; CRISPR CAS9 GENE; DNA SYNTHESIS; FOUNDER EFFECT; GENE; GENE EXPRESSION REGULATION; GENOME; IMMUNOFLUORESCENCE MICROSCOPY; IN VIVO STUDY; INTRON; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; DOWN REGULATION; GENETICS; HOMOZYGOTE; METABOLISM; PATHOLOGY; PHENOTYPE; REGULATORY SEQUENCE; TRANSGENIC MOUSE;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL PROLIFERATION; CRISPR-CAS SYSTEMS; DOWN-REGULATION; HOMOZYGOTE; INTRONS; KI-67 ANTIGEN; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; POINT MUTATION; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA, MESSENGER;

EID: 84922061336     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.305017     Document Type: Article

References (25)

1. Palmiter RD, Brinster RL. Germ-line transformation of mice. Annu Rev Genet. 1986;20:465-499. doi: 10.1146/annurev.ge.20.120186.002341.
2. Giraldo P, Montoliu L. Size matters: use of YACs, BACs and PACs in transgenic animals. Transgenic Res. 2001;10:83-103.
3. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315:1709-1712. doi: 10.1126/ science.1138140.
4. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol. 2013;31:227-229. doi: 10.1038/ nbt.2501.
5. Hai T, Teng F, Guo R, Li W, Zhou Q. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res. 2014;24:372-375. doi: 10.1038/cr.2014.11.
6. Li W, Teng F, Li T, Zhou Q. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol. 2013;31:684-686. doi: 10.1038/nbt.2652.
7. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell. 2013;153:910-918. doi: 10.1016/j.cell.2013.04.025.
8. Yang D, Xu J, Zhu T, Fan J, Lai L, Zhang J, Chen YE. Effective gene targeting in rabbits using RNA-guided Cas9 nucleases. J Mol Cell Biol. 2014;6:97-99. doi: 10.1093/jmcb/mjt047.
9. Niu Y, Shen B, Cui Y, et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell. 2014;156:836-843. doi: 10.1016/j.cell.2014.01.027.
10. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/ Cas systems. Science. 2013;339:819-823. doi: 10.1126/science.1231143.
11. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/ Cas-mediated genome engineering. Cell. 2013;154:1370-1379. doi: 10.1016/j.cell.2013.08.022.
12. Sander JD, Joung JK. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol. 2014;32:347-355. doi: 10.1038/ nbt.2842.
13. Maurano MT, Humbert R, Rynes E, et al. Systematic localization of common disease-associated variation in regulatory DNA. Science. 2012;337:1190-1195. doi: 10.1126/science.1222794.
14. Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol. 2003;35:577-593.
15. Miano JM, Carlson MJ, Spencer JA, Misra RP. Serum response factordependent regulation of the smooth muscle calponin gene. J Biol Chem. 2000;275:9814-9822.
16. Long X, Slivano OJ, Cowan SL, Georger MA, Lee TH, Miano JM. Smooth muscle calponin: an unconventional CArG-dependent gene that antagonizes neointimal formation. Arterioscler Thromb Vasc Biol. 2011;31:2172-2180. doi: 10.1161/ATVBAHA.111.232785.
17. Taniguchi S. Suppression of cancer phenotypes through a multifunctional actin-binding protein, calponin, that attacks cancer cells and simultaneously protects the host from invasion. Cancer Sci. 2005;96:738-746. doi: 10.1111/j.1349-7006.2005.00118.x.
18. Khromov AS, Wang H, Choudhury N, McDuffie M, Herring BP, Nakamoto R, Owens GK, Somlyo AP, Somlyo AV. Smooth muscle of telokin-deficient mice exhibits increased sensitivity to Ca2+ and decreased cGMPinduced relaxation. Proc Natl Acad Sci U S A. 2006;103:2440-2445. doi: 10.1073/pnas.0508566103.
19. Capecchi MR. Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century. Nat Rev Genet. 2005;6:507-512. doi: 10.1038/nrg1619.
20. Davis J, Maillet M, Miano JM, Molkentin JD. Lost in transgenesis: a user's guide for genetically manipulating the mouse in cardiac research. Circ Res. 2012;111:761-777. doi: 10.1161/CIRCRESAHA.111.262717.
21. Sur IK, Hallikas O, Vähärautio A, Yan J, Turunen M, Enge M, Taipale M, Karhu A, Aaltonen LA, Taipale J. Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science. 2012;338:1360-1363. doi: 10.1126/science.1228606.
22. Attanasio C, Nord AS, Zhu Y, et al. Fine tuning of craniofacial morphology by distant-acting enhancers. Science. 2013;342:1241006. doi: 10.1126/science.1241006.
23. Chen M, Zhang W, Lu X, Hoggatt AM, Gunst SJ, Kassab GS, Tune JD, Herring BP. Regulation of 130-kDa smooth muscle myosin light chain kinase expression by an intronic CArG element. J Biol Chem. 2013;288:34647-34657. doi: 10.1074/jbc.M113.510362.
24. Meier ID, Bernreuther C, Tilling T, Neidhardt J, Wong YW, Schulze C, Streichert T, Schachner M. Short DNA sequences inserted for gene targeting can accidentally interfere with off-target gene expression. FASEB J. 2010;24:1714-1724. doi: 10.1096/fj.09-140749.
25. Benson CC, Zhou Q, Long X, Miano JM. Identifying functional single nucleotide polymorphisms in the human CArGome. Physiol Genomics. 2011;43:1038-1048. doi: 10.1152/physiolgenomics.00098.2011.