Strategies to achieve conditional gene mutation in mice

Cold Spring Harbor Protocols

Volumn 2014, Issue 4, 2014, Pages 339-349

  Gierut, Jessica J ^a   Jacks, Tyler E ^b   Haigis, Kevin M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; DNA FRAGMENT; ESTROGEN RECEPTOR; FATTY ACID BINDING PROTEIN; RECOMBINASE;

ARTICLE; CHROMATIN STRUCTURE; CONDITIONAL GENE MUTATION; DNA METHYLATION; DNA RECOMBINATION; DNA SEQUENCE; ENZYME ACTIVITY; GAIN OF FUNCTION MUTATION; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENETIC ENGINEERING; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; MOUSE STRAIN; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; TRANSGENE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; GENE EXPRESSION REGULATION; MICE; MUTATION; RECOMBINATION, GENETIC;

EID: 84897375039     PISSN: 19403402     EISSN: 15596095     Source Type: Journal    
DOI: 10.1101/pdb.top069807     Document Type: Article

References (95)

1. Albert H., Dale EC, Lee E, Ow DW. 1995. Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7: 649-659.
2. Anastassiadis K., Fu J, Patsch C, Hu S, Weidlich S, Duerschke K, Buchholz F, Edenhofer F., Stewart AF. 2009. Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E. coli, mammalian cells and mice. Disease Models Mech 2: 508-515.
3. Araki K., Araki M, Yamamura K. 1997. Targeted integration of DNA using mutant lox sites in embryonic stem cells. Nucleic Acids Res 25: 868-872.
4. Awatramani R., Soriano P, Rodriguez C, Mai JJ, Dymecki SM. 2003. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet 35: 70-75.
5. Babaei-Jadidi R, Li N, Saadeddin A, Spencer-Dene B, Jandke A, Muhammad B, Ibrahim EE, Muraleedharan R, Abuzinadah M, Davis H, et al. 2011. FBXW7 influences murine intestinal homeostasis and cancer, targeting Notch, Jun, and DEK for degradation. J Exp Med 208: 295-312.
6. Barker N., van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A., Korving J, Begthel H, Peters PJ, et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
7. Barlow C., Schroeder M, Lekstrom-Himes J, Kylefjord H, Deng CX, Wynshaw-Boris A, Spiegelman BM, Xanthopoulos KG. 1997. Targeted expression of Cre recombinase to adipose tissue of transgenic mice directs adipose-specific excision of loxP-flanked gene segments. Nucleic Acids Res 25: 2543-2545.
8. Bethke B., Sauer B. 1997. Segmental genomic replacement by Cre-mediated recombination: Genotoxic stress activation of the p53 promoter in single-copy transformants. Nucleic Acids Res 25: 2828-2834.
9. Boross P., Breukel C, van Loo PF, van der Kaa J, Claassens JW, Bujard H, Schonig K., Verbeek JS. 2009. Highly B lymphocyte-specific tamoxifen inducible transgene expression of CreER T2 by using the LC-1 locus BAC vector. Genesis 47: 729-735.
10. Branda C. S, Dymecki SM. 2004. Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev Cell 6: 7-28.
11. Braun B. S, Tuveson DA, Kong N, Le DT, Kogan SC, Rozmus J, Le Beau MM, Jacks T. E, Shannon KM. 2004. Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc Natl Acad Sci 101: 597-602.
12. Buchholz F., Ringrose L, Angrand PO, Rossi F, Stewart AF. 1996. Different thermostabilities of FLP and Cre recombinases: Implications for applied site-specific recombination. Nucleic Acids Res 24: 4256-4262.
13. Buchholz F., Angrand PO, Stewart AF. 1998. Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat Biotechnol 16: 657-662.
14. Capecchi M.R. 1989. The new mouse genetics: Altering the genome by gene targeting. Trends Genet 5: 70-76.
15. Danielian P. S, Muccino D, Rowitch DH, Michael SK, McMahon AP. 1998. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8: 1323-1326.
16. Dassule H. R, Lewis P, Bei M, Maas R, McMahon AP. 2000. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127: 4775-4785.
17. DuPage M, Cheung AF, Mazumdar C, Winslow MM, Bronson R, Schmidt LM, Crowley D, Chen J, Jacks T. 2011. Endogenous T cell responses to antigens expressed in lung adenocarcinomas delay malignant tumor progression. Cancer Cell 19: 72-85.
18. el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, Louvard D, Chambon P., Metzger D, Robine S. 2004. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39: 186-193.
19. Farley F. W, Soriano P, Steffen LS, Dymecki SM. 2000. Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28: 106-110.
20. Feil R., Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P. 1996. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci 93: 10887-10890.
21. Forni P. E, Scuoppo C, Imayoshi I, Taulli R, Dastru W, Sala V, Betz UA, Muzzi P, Martinuzzi D, Vercelli AE, et al. 2006. High levels of Cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. J Neurosci 26: 9593-9602.
22. Gannon M., Herrera PL, Wright CV. 2000a. Mosaic Cre-mediated recombination in pancreas using the pdx-1 enhancer/promoter. Genesis 26: 143-144.
23. Gannon M., Shiota C, Postic C, Wright CV, Magnuson M. 2000b. Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas. Genesis 26: 139-142.
24. Gierut J. J, Jacks TE, Haigis KM. 2014a. Producing and concentrating lenti-Cre for mouse infections. Cold Spring Harb Protoc doi: 10.1101/pdb. prot073437.
25. Gierut J. J, Jacks TE, Haigis KM. 2014b. In vivo delivery of lenti-Cre or adeno-Cre using intranasal instillation. Cold Spring Harb Protoc doi: 10.1101/ pdb.prot073445.
26. Gierut J. J, Jacks TE, Haigis KM. 2014c. Whole mount X-Gal staining of mouse tissues. Cold Spring Harb Protoc doi: 10.1101/pdb.prot073452.
27. Gossen M., Bujard H. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci 89: 5547-5551.
28. Grindley N. D, Whiteson KL, Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75: 567-605.
29. Gu H., Marth JD, Orban PC, Mossmann H, Rajewsky K. 1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265: 103-106.
30. Gupta M., Zak R, Libermann TA, Gupta MP. 1998. Tissue-restricted expression of the cardiac alpha-myosin heavy chain gene is controlled by a downstream repressor element containing a palindrome of two etsbinding sites. Mol Cell Biol 18: 7243-7258.
31. Hayashi S., McMahon AP. 2002. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: A tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
32. Heldt S. A, Ressler KJ. 2009. The use of lentiviral vectors and Cre/loxP to investigate the function of genes in complex behaviors. Front Mol Neurosci 2: 22.
33. Hinoi T., Akyol A, Theisen BK, Ferguson DO, Greenson JK, Williams BO, Cho K. R, Fearon ER. 2007. Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation. Cancer Res 67: 9721-9730.
34. Hoess R. H, Wierzbicki A, Abremski K. 1986. The role of the loxP spacer region in P1 site-specific recombination. Nucleic Acids Res 14: 2287-2300.
35. Indra A. K, Warot X, Brocard J, Bornert JM, Xiao JH, Chambon P, Metzger D. 1999. Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: Comparison of the recombinase activity of the tamoxifen-inducible Cre-ERT and Cre-ERT2 recombinases. Nucleic Acids Res 27: 4324-4327.
36. Ireland H., Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ, Winton DJ. 2004. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: Effect of loss of β-catenin. Gastroenterology 126: 1236-1246.
37. Iwano M., Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. 2002. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350.
38. Jackson E. L, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA. 2001. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 15: 3243-3248.
39. Jackson E. L, Olive KP, Tuveson DA, Bronson R, Crowley D, Brown M, Jacks T. 2005. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res 65: 10280-10288.
40. Jonkers J., Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. 2001. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 29: 418-425.
41. Jullien N., Sampieri F, Enjalbert A, Herman JP. 2003. Regulation of Cre recombinase by ligand-induced complementation of inactive fragments. Nucleic Acids Res 31: e131.
42. Kennedy M. J, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL. 2010. Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods 7: 973-975.
43. Kolb A.F. 2001. Selection-marker-free modification of the murine β-casein gene using a lox2272 [correction of lox2722] site. Anal Biochem 290: 260-271.
44. Kucherlapati M. H, Yang K, Fan K, Kuraguchi M, Sonkin D, Rosulek A, Lipkin M., Bronson RT, Aronow BJ, Kucherlapati R. 2008. Loss of Rb1 in the gastrointestinal tract of Apc1638N mice promotes tumors of the cecum and proximal colon. Proc Natl Acad Sci 105: 15493-15498.
45. Kuhn R., Schwenk F, Aguet M, Rajewsky K. 1995. Inducible gene targeting in mice. Science 269: 1427-1429.
46. Lai Z., Han I, Park M, Brady RO. 2002. Design of an HIV-1 lentiviral-based gene-trap vector to detect developmentally regulated genes in mammalian cells. Proc Natl Acad Sci 99: 3651-3656.
47. Lakso M., Sauer B, Mosinger B Jr, Lee EJ, Manning RW, Yu SH, Mulder KL, Westphal H. 1992. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc Natl Acad Sci 89: 6232-6236.
48. Levin M. C, Monetti M, Watt MJ, Sajan MP, Stevens RD, Bain JR, Newgard CB, Farese RV Sr, Farese RV Jr. 2007. Increased lipid accumulation and insulin resistance in transgenic mice expressing DGAT2 in glycolytic (type II) muscle. Am J Physiol Endocrinol Metab 293: E1772-1781.
49. Levskaya A., Weiner OD, Lim WA, Voigt CA. 2009. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461: 997-1001.
50. Lewandoski M. 2001. Conditional control of gene expression in the mouse. Nat Rev Genet 2: 743-755.
51. Li Q., Haigis KM, McDaniel A, Harding-Theobald E, Kogan SC, Akagi K, Wong J. C, Braun BS, Wolff L, Jacks T, et al. 2011. Hematopoiesis and leukemogenesis in mice expressing oncogenic NrasG12D from the endogenous locus. Blood 117: 2022-2032.
52. Lobe C. G, Nagy A. 1998. Conditional genome alteration in mice. BioEssays 20: 200-208.
53. Logie C., Stewart AF. 1995. Ligand-regulated site-specific recombination. Proc Natl Acad Sci 92: 5940-5944.
54. Loonstra A., Vooijs M, Beverloo HB, Allak BA, van Drunen E, Kanaar R, Berns A, Jonkers J. 2001. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc Natl Acad Sci 98: 9209-9214.
55. Madison B. B, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. 2002. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277: 33275-33283.
56. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell B. B, Fanselow MS, Wilson MA, Tonegawa S. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317: 94-99.
57. Metzger D., Clifford J, Chiba H, Chambon P. 1995. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc Natl Acad Sci 92: 6991-6995.
58. Meuwissen R., Linn SC, Linnoila RI, Zevenhoven J, Mooi WJ, Berns A. 2003. Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 4: 181-189.
59. Nagy A. 2000. Cre recombinase: The universal reagent for genome tailoring. Genesis 26: 99-109.
60. Nagy A., Rossant J. 2001. Chimaeras and mosaics for dissecting complex mutant phenotypes. Int J Dev Biol 45: 577-582.
61. Naldini L., Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
62. Okubo T., Hogan BL. 2004. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol 3: 11.
63. Pfeifer A., Brandon EP, Kootstra N, Gage FH, Verma IM. 2001. Delivery of the Cre recombinase by a self-deleting lentiviral vector: Efficient gene targeting in vivo. Proc Natl Acad Sci 98: 11450-11455.
64. Postic C., Magnuson MA. 1999. [Role of glucokinase (GK) in the maintenance of glucose homeostasis. Specific disruption of the gene by the Cre-loxP technique]. J Annu Diabetol Hotel Dieu 1999: 115-124.
65. Raymond C. S, Soriano P. 2007. High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PloS One 2: e162.
66. Rickert R. C, Roes J, Rajewsky K. 1997. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res 25: 1317-1318.
67. Rossant J., McMahon A. 1999. "Cre"-ating mouse mutants-A meeting review on conditional mouse genetics. Genes Dev 13: 142-145.
68. Saam J. R, Gordon JI. 1999. Inducible gene knockouts in the small intestinal and colonic epithelium. J Biol Chem 274: 38071-38082.
69. Sadowski P.D. 1995. The Flp recombinase of the 2-microns plasmid of Saccharomyces cerevisiae. Progr Nucleic Acid Res Mol Biol 51: 53-91.
70. Sansom O. J, Meniel VS, Muncan V, Phesse TJ, Wilkins JA, Reed KR, Vass JK, Athineos D., Clevers H, Clarke AR. 2007. Myc deletion rescues Apc deficiency in the small intestine. Nature 446: 676-679.
71. Sauer B. 1994. Recycling selectable markers in yeast. BioTechniques 16: 1086-1088.
72. Sauer B., McDermott J. 2004. DNA recombination with a heterospecific Cre homolog identified from comparison of the pac-c1 regions of P1-related phages. Nucleic Acids Res 32: 6086-6095.
73. Schlake T., Bode J. 1994. Use of mutated FLP recognition target (FRT) sites for the exchange of expression cassettes at defined chromosomal loci. Biochemistry 33: 12746-12751.
74. Schuler M., Dierich A, Chambon P, Metzger D. 2004. Efficient temporally controlled targeted somatic mutagenesis in hepatocytes of the mouse. Genesis 39: 167-172.
75. Schwenk F., Baron U, Rajewsky K. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081.
76. Schwenk F., Kuhn R, Angrand PO, Rajewsky K, Stewart AF. 1998. Temporally and spatially regulated somatic mutagenesis in mice. Nucleic Acids Res 26: 1427-1432.
77. Senecoff J. F, Cox MM. 1986. Directionality in FLP protein-promoted sitespecific recombination is mediated by DNA-DNA pairing. J Biol Chem 261: 7380-7386.
78. Senecoff J. F, Rossmeissl PJ, Cox MM. 1988. DNA recognition by the FLP recombinase of the yeast 2 mu plasmid. A mutational analysis of the FLP binding site. J Mol Biol 201: 405-421.
79. Sgaier S. K, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL. 2005. Morphogenetic and cellular movements that shape the mouse cerebellum: Insights from genetic fate mapping. Neuron 45: 27-40.
80. Shimizu-Sato S, Huq E, Tepperman JM, Quail PH. 2002. A light-switchable gene promoter system. Nat Biotechnol 20: 1041-1044.
81. Shimshek D. R, Kim J, Hubner MR, Spergel DJ, Buchholz F, Casanova E, Stewart A. F, Seeburg PH, Sprengel R. 2002. Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32: 19-26.
82. Silver D. P, Livingston DM. 2001. Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol Cell 8: 233-243.
83. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
84. Taniguchi H., He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J., Lin Y, et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71: 995-1013.
85. Tuveson D. A, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, Mercer KL, Grochow R, Hock H, Crowley D, et al. 2004. Endogenous oncogenic K-rasG12D stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5: 375-387.
86. Vasioukhin V., Degenstein L, Wise B, Fuchs E. 1999. The magical touch: Genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci 96: 8551-8556.
87. Vooijs M., van der Valk M, te Riele H, Berns A. 1998. Flp-mediated tissuespecific inactivation of the retinoblastoma tumor suppressor gene in the mouse. Oncogene 17: 1-12.
88. Vooijs M., Jonkers J, Berns A. 2001. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep 2: 292-297.
89. Wagner K. U, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L, Li M, Furth PA, Hennighausen L. 1997. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 25: 4323-4330.
90. Wang Y., Krushel LA, Edelman GM. 1996. Targeted DNA recombination in vivo using an adenovirus carrying the cre recombinase gene. Proc Natl Acad Sci 93: 3932-3936.
91. Wang X., Chen X, Yang Y. 2012. Spatiotemporal control of gene expression by a light-switchable transgene system. Nat Meth 9: 266-269.
92. Young N. P, Crowley D, Jacks T. 2011. Uncoupling cancer mutations reveals critical timing of p53 loss in sarcomagenesis. Cancer Res 71: 4040-4047.
93. Zhang Z., Lutz B. 2002. Cre recombinase-mediated inversion using lox66 and lox71: Method to introduce conditional point mutations into the CREB-binding protein. Nucleic Acids Res 30: e90.
94. Zhu H., Acquaviva J, Ramachandran P, Boskovitz A, Woolfenden S, Pfannl R, Bronson RT, Chen JW, Weissleder R, Housman DE, Charest A. 2009. Oncogenic E. GFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci USA 106: 2712-2716.
95. Zoltowski B. D, Crane BR. 2008. Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47: 7012-7019.