Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice

Journal of Immunological Methods

Volumn 408, Issue , 2014, Pages 89-100

  Abram, Clare L ^a   Roberge, Gray L ^a   Hu, Yongmei ^a   Lowell, Clifford A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cre recombinase; Dendritic cell; Floxed; Macrophage; Neutrophil

Indexed keywords

CRE RECOMBINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; GENE EXPRESSION; GENOTYPE; LEUKOCYTE; LOXP SITE; MOUSE; MOUSE STRAIN; MYELOID DENDRITIC CELL; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEADY STATE;

MUS;

CRE-RECOMBINASE; DENDRITIC CELL; FLOXED; MACROPHAGE; NEUTROPHIL;

ANIMALS; BACTERIAL PROTEINS; FLOW CYTOMETRY; GENE DELETION; GENE TARGETING; GENES, REPORTER; GENOTYPE; INTEGRASES; LUMINESCENT PROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; PHENOTYPE; RNA, UNTRANSLATED;

EID: 84903516068     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2014.05.009     Document Type: Article

References (59)

1. Abram C.L., Roberge G.L., Pao L.I., Neel B.G., Lowell C.A. Distinct roles for neutrophils and dendritic cells in inflammation and autoimmunity in motheaten mice. Immunity 2013, 38:489.
2. Brockschnieder D., Pechmann Y., Sonnenberg-Riethmacher E., Riethmacher D. An improved mouse line for Cre-induced cell ablation due to diphtheria toxin A, expressed from the Rosa26 locus. Genesis 2006, 44:322.
3. Calaminus S.D., Guitart A.V., Sinclair A., Schachtner H., Watson S.P., Holyoake T.L., Kranc K.R., Machesky L.M. Lineage tracing of Pf4-Cre marks hematopoietic stem cells and their progeny. PLoS One 2012, 7:e51361.
4. Caton M.L., Smith-Raska M.R., Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J. Exp. Med. 2007, 204:1653.
5. Chisaka H., Morita E., Murata K., Ishii N., Yaegashi N., Okamura K., Sugamura K. A transgenic mouse model for non-immune hydrops fetalis induced by the NS1 gene of human parvovirus B19. J. Gen. Virol. 2002, 83:273.
6. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265.
7. de Boer J., Williams A., Skavdis G., Harker N., Coles M., Tolaini M., Norton T., Williams K., Roderick K., Potocnik A.J., Kioussis D. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 2003, 33:314.
8. Deng L., Zhou J.F., Sellers R.S., Li J.F., Nguyen A.V., Wang Y., Orlofsky A., Liu Q., Hume D.A., Pollard J.W., Augenlicht L., Lin E.Y. A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis. Am. J. Pathol. 2010, 176:952.
9. Doyle A.D., Jacobsen E.A., Ochkur S.I., Willetts L., Shim K., Neely J., Kloeber J., Lesuer W.E., Pero R.S., Lacy P., Moqbel R., Lee N.A., Lee J.J. Homologous recombination into the eosinophil peroxidase locus generates a strain of mice expressing Cre recombinase exclusively in eosinophils. J. Leukoc. Biol. 2013, 94:17.
10. Eckelhart E., Warsch W., Zebedin E., Simma O., Stoiber D., Kolbe T., Rulicke T., Mueller M., Casanova E., Sexl V. A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood 2011, 117:1565.
11. Ferron M., Vacher J. Targeted expression of Cre recombinase in macrophages and osteoclasts in transgenic mice. Genesis 2005, 41:138.
12. Feyerabend T.B., Terszowski G., Tietz A., Blum C., Luche H., Gossler A., Gale N.W., Radtke F., Fehling H.J., Rodewald H.R. Deletion of Notch1 converts pro-T cells to dendritic cells and promotes thymic B cells by cell-extrinsic and cell-intrinsic mechanisms. Immunity 2009, 30:67.
13. Franke K., Kalucka J., Mamlouk S., Singh R.P., Muschter A., Weidemann A., Iyengar V., Jahn S., Wieczorek K., Geiger K., Muders M., Sykes A.M., Poitz D.M., Ripich T., Otto T., Bergmann S., Breier G., Baretton G., Fong G.H., Greaves D.R., Bornstein S., Chavakis T., Fandrey J., Gassmann M., Wielockx B. HIF-1alpha is a protective factor in conditional PHD2-deficient mice suffering from severe HIF-2alpha-induced excessive erythropoiesis. Blood 2013, 121:1436.
14. Gautier E.L., Shay T., Miller J., Greter M., Jakubzick C., Ivanov S., Helft J., Chow A., Elpek K.G., Gordonov S., Mazloom A.R., Ma'ayan A., Chua W.J., Hansen T.H., Turley S.J., Merad M., Randolph G.J., Immunological Genome C. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 2012, 13:1118.
15. Gu H., Marth J.D., Orban P.C., Mossmann H., Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 1994, 265:103.
16. Hebert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 2000, 222:296.
17. Heffner C.S., Herbert Pratt C., Babiuk R.P., Sharma Y., Rockwood S.F., Donahue L.R., Eppig J.T., Murray S.A. Supporting conditional mouse mutagenesis with a comprehensive cre characterization resource. Nat. Commun. 2012, 3:1218.
18. Higashi A.Y., Ikawa T., Muramatsu M., Economides A.N., Niwa A., Okuda T., Murphy A.J., Rojas J., Heike T., Nakahata T., Kawamoto H., Kita T., Yanagita M. Direct hematological toxicity and illegitimate chromosomal recombination caused by the systemic activation of CreERT2. J. Immunol. 2009, 182:5633.
19. Huh W.J., Mysorekar I.U., Mills J.C. Inducible activation of Cre recombinase in adult mice causes gastric epithelial atrophy, metaplasia, and regenerative changes in the absence of "floxed" alleles. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G368.
20. Hume D.A. Applications of myeloid-specific promoters in transgenic mice support in vivo imaging and functional genomics but do not support the concept of distinct macrophage and dendritic cell lineages or roles in immunity. J. Leukoc. Biol. 2011, 89:525.
21. Jasinski M., Keller P., Fujiwara Y., Orkin S.H., Bessler M. GATA1-Cre mediates Piga gene inactivation in the erythroid/megakaryocytic lineage and leads to circulating red cells with a partial deficiency in glycosyl phosphatidylinositol-linked proteins (paroxysmal nocturnal hemoglobinuria type II cells). Blood 2001, 98:2248.
22. Kaplan D.H., Li M.O., Jenison M.C., Shlomchik W.D., Flavell R.A., Shlomchik M.J. Autocrine/paracrine TGFbeta1 is required for the development of epidermal Langerhans cells. J. Exp. Med. 2007, 204:2545.
23. Lakso M., Sauer B., Mosinger B., Lee E.J., Manning R.W., Yu S.H., Mulder K.L., Westphal H. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:6232.
24. Lee J.Y., Ristow M., Lin X., White M.F., Magnuson M.A., Hennighausen L. RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J. Biol. Chem. 2006, 281:2649.
25. Lilla J.N., Chen C.C., Mukai K., BenBarak M.J., Franco C.B., Kalesnikoff J., Yu M., Tsai M., Piliponsky A.M., Galli S.J. Reduced mast cell and basophil numbers and function in Cpa3-Cre; Mcl-1fl/fl mice. Blood 2011, 118:6930.
26. Long M.A., Rossi F.M. Silencing inhibits Cre-mediated recombination of the Z/AP and Z/EG reporters in adult cells. PLoS One 2009, 4:e5435.
27. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., Lein E.S., Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133.
28. Mao X., Fujiwara Y., Orkin S.H. Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5037.
29. Miller J.C., Brown B.D., Shay T., Gautier E.L., Jojic V., Cohain A., Pandey G., Leboeuf M., Elpek K.G., Helft J., Hashimoto D., Chow A., Price J., Greter M., Bogunovic M., Bellemare-Pelletier A., Frenette P.S., Randolph G.J., Turley S.J., Merad M. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 2012, 13:888.
30. Moran A.E., Holzapfel K.L., Xing Y., Cunningham N.R., Maltzman J.S., Punt J., Hogquist K.A. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 2011, 208:1279.
31. Murray S.A., Eppig J.T., Smedley D., Simpson E.M., Rosenthal N. Beyond knockouts: cre resources for conditional mutagenesis. Mamm. Genome 2012, 23:587.
32. Musch W., Wege A.K., Mannel D.N., Hehlgans T. Generation and characterization of alpha-chymase-Cre transgenic mice. Genesis 2008, 46:163.
33. Nagy A. Cre recombinase: the universal reagent for genome tailoring. Genesis 2000, 26:99.
34. Nakamura T., Imai Y., Matsumoto T., Sato S., Takeuchi K., Igarashi K., Harada Y., Azuma Y., Krust A., Yamamoto Y., Nishina H., Takeda S., Takayanagi H., Metzger D., Kanno J., Takaoka K., Martin T.J., Chambon P., Kato S. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell 2007, 130:811.
35. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y.M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., Walzer T., Vivier E. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18324.
36. Ohnmacht C., Schwartz C., Panzer M., Schiedewitz I., Naumann R., Voehringer D. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 2010, 33:364.
37. Orban P.C., Chui D., Marth J.D. Tissue- and site-specific DNA recombination in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:6861.
38. Passegue E., Wagner E.F., Weissman I.L. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 2004, 119:431.
39. Satpathy A.T., Kc W., Albring J.C., Edelson B.T., Kretzer N.M., Bhattacharya D., Murphy T.L., Murphy K.M. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 2012, 209:1135.
40. Sauer B., Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:5166.
41. Schaller E., Macfarlane A.J., Rupec R.A., Gordon S., McKnight A.J., Pfeffer K. Inactivation of the F4/80 glycoprotein in the mouse germ line. Mol. Cell. Biol. 2002, 22:8035.
42. Schmidt E.E., Taylor D.S., Prigge J.R., Barnett S., Capecchi M.R. Illegitimate Cre-dependent chromosome rearrangements in transgenic mouse spermatids. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13702.
43. Schmidt-Supprian M., Rajewsky K. Vagaries of conditional gene targeting. Nat. Immunol. 2007, 8:665.
44. Scholten J., Hartmann K., Gerbaulet A., Krieg T., Muller W., Testa G., Roers A. Mast cell-specific Cre/loxP-mediated recombination in vivo. Transgenic Res. 2008, 17:307.
45. Schraml B.U., van Blijswijk J., Zelenay S., Whitney P.G., Filby A., Acton S.E., Rogers N.C., Moncaut N., Carvajal J.J., Reis e Sousa C. Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 2013, 154:843.
46. Schulz T.J., Glaubitz M., Kuhlow D., Thierbach R., Birringer M., Steinberg P., Pfeiffer A.F., Ristow M. Variable expression of Cre recombinase transgenes precludes reliable prediction of tissue-specific gene disruption by tail-biopsy genotyping. PLoS One 2007, 2:e1013.
47. Semprini S., Troup T.J., Kotelevtseva N., King K., Davis J.R., Mullins L.J., Chapman K.E., Dunbar D.R., Mullins J.J. Cryptic loxP sites in mammalian genomes: genome-wide distribution and relevance for the efficiency of BAC/PAC recombineering techniques. Nucleic Acids Res. 2007, 35:1402.
48. Smedley D., Salimova E., Rosenthal N. Cre recombinase resources for conditional mouse mutagenesis. Methods 2011, 53:411.
49. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
50. Stranges P.B., Watson J., Cooper C.J., Choisy-Rossi C.M., Stonebraker A.C., Beighton R.A., Hartig H., Sundberg J.P., Servick S., Kaufmann G., Fink P.J., Chervonsky A.V. Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 2007, 26:629.
51. Sullivan B.M., Liang H.E., Bando J.K., Wu D., Cheng L.E., McKerrow J.K., Allen C.D., Locksley R.M. Genetic analysis of basophil function in vivo. Nat. Immunol. 2011, 12:527.
52. Thyagarajan B., Guimaraes M.J., Groth A.C., Calos M.P. Mammalian genomes contain active recombinase recognition sites. Gene 2000, 244:47.
53. Tiedt R., Schomber T., Hao-Shen H., Skoda R.C. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood 2007, 109:1503.
54. Tkalcevic J., Novelli M., Phylactides M., Iredale J.P., Segal A.W., Roes J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 2000, 12:201.
55. Wolfler A., Danen-van Oorschot A.A., Haanstra J.R., Valkhof M., Bodner C., Vroegindeweij E., van Strien P., Novak A., Cupedo T., Touw I.P. Lineage-instructive function of C/EBPalpha in multipotent hematopoietic cells and early thymic progenitors. Blood 2010, 116:4116.
56. Wumesh K.C., Satpathy A.T., Rapaport A.S., Briseno C.G., Wu X., Albring J.C., Russler-Germain E.V., Kretzer N.M., Durai V., Persaud S.P., Edelson B.T., Loschko J., Cella M., Allen P.M., Nussenzweig M.C., Colonna M., Sleckman B.P., Murphy T.L., Murphy K.M. L-Myc expression by dendritic cells is required for optimal T-cell priming. Nature 2014, 507:243.
57. Yona S., Kim K.W., Wolf Y., Mildner A., Varol D., Breker M., Strauss-Ayali D., Viukov S., Guilliams M., Misharin A., Hume D.A., Perlman H., Malissen B., Zelzer E., Jung S. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013, 38:79.
58. Zahner S.P., Kel J.M., Martina C.A., Brouwers-Haspels I., van Roon M.A., Clausen B.E. Conditional deletion of TGF-betaR1 using Langerin-Cre mice results in Langerhans cell deficiency and reduced contact hypersensitivity. J. Immunol. 2011, 187:5069.
59. Zarbock A., Polanowska-Grabowska R.K., Ley K. Platelet-neutrophil-interactions: linking hemostasis and inflammation. Blood Rev. 2007, 21:99.