Dynamics of CDKN1A in Single Cells Defined by an Endogenous Fluorescent Tagging Toolkit

Cell Reports

Volumn 14, Issue 7, 2016, Pages 1800-1811

  Stewart Ornstein, Jacob ^a   Lahav, Galit ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DNA; BACTERIAL PROTEIN; CAS9 PROTEIN, FRANCISELLA NOVICIDA; CATALASE; ENDONUCLEASE; FLUORESCENT DYE; HYDROPEROXIDASE II; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL HETEROGENEITY; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DYNAMICS; FLUORESCENCE ANALYSIS; MAMMAL CELL; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; REPORTER GENE; SEQUENCE HOMOLOGY; SINGLE CELL ANALYSIS; TRANSCRIPTION REGULATION; ANIMAL; CELL CYCLE CHECKPOINT; CHEMISTRY; DOG; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HUMAN; LIVER CELL; MDCK CELL LINE; METABOLISM; MOUSE; NIH 3T3 CELL LINE; PATHOLOGY; PROCEDURES; STAINING; TUMOR CELL LINE;

ANIMALS; BACTERIAL PROTEINS; CATALASE; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DOGS; ENDONUCLEASES; EPITHELIAL CELLS; FLUORESCENT DYES; GENE EXPRESSION REGULATION; GENES, REPORTER; HEK293 CELLS; HEPATOCYTES; HUMANS; LUMINESCENT PROTEINS; MADIN DARBY CANINE KIDNEY CELLS; MICE; NIH 3T3 CELLS; PLASMIDS; SINGLE-CELL ANALYSIS; STAINING AND LABELING; TRANSFECTION;

EID: 84959137041     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.045     Document Type: Article

References (36)

1. Baudin A., Ozier-Kalogeropoulos O., Denouel A., Lacroute F., Cullin C. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 1993, 21:3329-3330.
2. Bornstein G., Bloom J., Sitry-Shevah D., Nakayama K., Pagano M., Hershko A. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 2003, 278:25752-25757.
3. Böttcher R., Hollmann M., Merk K., Nitschko V., Obermaier C., Philippou-Massier J., Wieland I., Gaul U., Förstemann K. Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured Drosophila cells. Nucleic Acids Res. 2014, 42:e89.
4. Calnan D.R., Brunet A. The FoxO code. Oncogene 2008, 27:2276-2288.
5. Caussinus E., Kanca O., Affolter M. Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat. Struct. Mol. Biol. 2012, 19:117-121.
6. Celis J.E., Celis A. Cell cycle-dependent variations in the distribution of the nuclear protein cyclin proliferating cell nuclear antigen in cultured cells: subdivision of S phase. Proc. Natl. Acad. Sci. USA 1985, 82:3262-3266.
7. Chen E.Y., DeRan M.T., Ignatius M.S., Grandinetti K.B., Clagg R., McCarthy K.M., Lobbardi R.M., Brockmann J., Keller C., Wu X., Langenau D.M. Glycogen synthase kinase 3 inhibitors induce the canonical WNT/β-catenin pathway to suppress growth and self-renewal in embryonal rhabdomyosarcoma. Proc. Natl. Acad. Sci. USA 2014, 111:5349-5354.
8. Cohen A.A., Geva-Zatorsky N., Eden E., Frenkel-Morgenstern M., Issaeva I., Sigal A., Milo R., Cohen-Saidon C., Liron Y., Kam Z., et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008, 322:1511-1516.
9. Cohen-Saidon C., Cohen A.A., Sigal A., Liron Y., Alon U. Dynamics and variability of ERK2 response to EGF in individual living cells. Mol. Cell 2009, 36:885-893.
10. Costa M., Marchi M., Cardarelli F., Roy A., Beltram F., Maffei L., Ratto G.M. Dynamic regulation of ERK2 nuclear translocation and mobility in living cells. J. Cell Sci. 2006, 119:4952-4963.
11. Dulić V., Kaufmann W.K., Wilson S.J., Tisty T.D., Lees E., Harper J.W., Elledge S.J., Reed S.I. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 1994, 76:1013-1023.
12. el-Deiry W.S., Harper J.W., O'Connor P.M., Velculescu V.E., Canman C.E., Jackman J., Pietenpol J.A., Burrell M., Hill D.E., Wang Y., et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 1994, 54:1169-1174.
13. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
14. Griffith T.D., Tolmach L.J. Lethal response of HeLa cells to x-irradiation in the latter part of the generation cycle. Biophys. J. 1976, 16:303-318.
15. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
16. Lahav G., Rosenfeld N., Sigal A., Geva-Zatorsky N., Levine A.J., Elowitz M.B., Alon U. Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 2004, 36:147-150.
17. Lengner C.J., Camargo F.D., Hochedlinger K., Welstead G.G., Zaidi S., Gokhale S., Scholer H.R., Tomilin A., Jaenisch R. Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 2007, 1:403-415.
18. Loewer A., Batchelor E., Gaglia G., Lahav G. Basal dynamics of p53 reveal transcriptionally attenuated pulses in cycling cells. Cell 2010, 142:89-100.
19. Longtine M.S., McKenzie A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
20. Maddocks O.D., Berkers C.R., Mason S.M., Zheng L., Blyth K., Gottlieb E., Vousden K.H. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 2013, 493:542-546.
21. Overton K.W., Spencer S.L., Noderer W.L., Meyer T., Wang C.L. Basal p21 controls population heterogeneity in cycling and quiescent cell cycle states. Proc. Natl. Acad. Sci. USA 2014, 111:E4386-E4393.
22. Park A., Won S.T., Pentecost M., Bartkowski W., Lee B. CRISPR/Cas9 allows efficient and complete knock-in of a destabilization domain-tagged essential protein in a human cell line, allowing rapid knockdown of protein function. PLoS ONE 2014, 9:e95101.
23. Purvis J.E., Karhohs K.W., Mock C., Batchelor E., Loewer A., Lahav G. p53 dynamics control cell fate. Science 2012, 336:1440-1444.
24. Raj A., van den Bogaard P., Rifkin S.A., van Oudenaarden A., Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 2008, 5:877-879.
25. Ran F.A., Hsu P.D., Wright J., Agarwala V., Scott D.A., Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 2013, 8:2281-2308.
26. Sakaue-Sawano A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., Kashiwagi S., Fukami K., Miyata T., Miyoshi H., et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132:487-498.
27. Shaltiel I.A., Aprelia M., Saurin A.T., Chowdhury D., Kops G.J., Voest E.E., Medema R.H. Distinct phosphatases antagonize the p53 response in different phases of the cell cycle. Proc. Natl. Acad. Sci. USA 2014, 111:7313-7318.
28. Sheff M.A., Thorn K.S. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 2004, 21:661-670.
29. Sigal A., Milo R., Cohen A., Geva-Zatorsky N., Klein Y., Alaluf I., Swerdlin N., Perzov N., Danon T., Liron Y., et al. Dynamic proteomics in individual human cells uncovers widespread cell-cycle dependence of nuclear proteins. Nat. Methods 2006, 3:525-531.
30. Tay S., Hughey J.J., Lee T.K., Lipniacki T., Quake S.R., Covert M.W. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 2010, 466:267-271.
31. Tkach J.M., Yimit A., Lee A.Y., Riffle M., Costanzo M., Jaschob D., Hendry J.A., Ou J., Moffat J., Boone C., et al. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat. Cell Biol. 2012, 14:966-976.
32. van Dierendonck J.H., Keijzer R., van de Velde C.J., Cornelisse C.J. Nuclear distribution of the Ki-67 antigen during the cell cycle: comparison with growth fraction in human breast cancer cells. Cancer Res. 1989, 49:2999-3006.
33. Wang J., Walsh K. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 1996, 273:359-361.
34. Wilfling F., Weber A., Potthoff S., Vögtle F.N., Meisinger C., Paschen S.A., Häcker G. BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax. Cell Death Differ. 2012, 19:1328-1336.
35. Yu C., Liu Y., Ma T., Liu K., Xu S., Zhang Y., Liu H., La Russa M., Xie M., Ding S., Qi L.S. Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 2015, 16:142-147.
36. Zhang Y., Xing D., Liu L. PUMA promotes Bax translocation by both directly interacting with Bax and by competitive binding to Bcl-X L during UV-induced apoptosis. Mol. Biol. Cell 2009, 20:3077-3087.