A Transgenic Mouse Marking Live Replicating Cells Reveals In Vivo Transcriptional Program of Proliferation

Developmental Cell

Volumn 23, Issue 4, 2012, Pages 681-690

  Klochendler, Agnes ^a   Weinberg Corem, Noa ^b   Moran, Maya ^a   Swisa, Avital ^b   Pochet, Nathalie ^c   Savova, Virginia ^c   Vikeså, Jonas ^d   Van de Peer, Yves ^e   Brandeis, Michael ^a   Regev, Aviv ^c   Nielsen, Finn Cilius ^d   Dor, Yuval ^b   Eden, Amir ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY   (Israel)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN B1; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IN VIVO STUDY; LIVER CANCER; LIVER CELL; LIVER FUNCTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL MARKERS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN B1; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; MICE; MICE, TRANSGENIC; NIH 3T3 CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

MAMMALIA; MUS MUSCULUS;

EID: 84867676282     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.08.009     Document Type: Article

References (42)

1. Acevedo L.G., Bieda M., Green R., Farnham P.J. Analysis of the mechanisms mediating tumor-specific changes in gene expression in human liver tumors. Cancer Res. 2008, 68:2641-2651.
2. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. The cell cycle and programmed cell death. Molecular Biology of the Cell 2002, 1019-1025. Garland Science, New York. Fourth Edition.
3. Bralet M.P., Branchereau S., Brechot C., Ferry N. Cell lineage study in the liver using retroviral mediated gene transfer. Evidence against the streaming of hepatocytes in normal liver. Am. J. Pathol. 1994, 144:896-905.
4. Brandeis M., Hunt T. The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. EMBO J. 1996, 15:5280-5289.
5. Cairo S., Armengol C., De Reyniès A., Wei Y., Thomas E., Renard C.A., Goga A., Balakrishnan A., Semeraro M., Gresh L., et al. Hepatic stem-like phenotype and interplay of Wnt/beta-catenin and Myc signaling in aggressive childhood liver cancer. Cancer Cell 2008, 14:471-484.
6. Clute P., Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1999, 1:82-87.
7. Conlon I., Raff M. Size control in animal development. Cell 1999, 96:235-244.
8. Desai B.M., Oliver-Krasinski J., De Leon D.D., Farzad C., Hong N., Leach S.D., Stoffers D.A. Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J. Clin. Invest. 2007, 117:971-977.
9. Dor Y., Brown J., Martinez O.I., Melton D.A. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004, 429:41-46.
10. Dorrell C., Erker L., Schug J., Kopp J.L., Canaday P.S., Fox A.J., Smirnova O., Duncan A.W., Finegold M.J., Sander M., et al. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev. 2011, 25:1193-1203.
11. Gould J., Getz G., Monti S., Reich M., Mesirov J.P. Comparative gene marker selection suite. Bioinformatics 2006, 22:1924-1925.
12. Hagting A., Karlsson C., Clute P., Jackman M., Pines J. MPF localization is controlled by nuclear export. EMBO J. 1998, 17:4127-4138.
13. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
14. Jungermann K., Kietzmann T. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu. Rev. Nutr. 1996, 16:179-203.
15. King R.W., Deshaies R.J., Peters J.M., Kirschner M.W. How proteolysis drives the cell cycle. Science 1996, 274:1652-1659.
16. Leblond C.P. Classification of cell populations on the basis of their proliferative behavior. Natl. Cancer Inst. Monogr. 1964, 14:119-150.
17. Leblond C.P. The life history of cells in renewing systems. Am. J. Anat. 1981, 160:114-158.
18. Lee J.S., Heo J., Libbrecht L., Chu I.S., Kaposi-Novak P., Calvisi D.F., Mikaelyan A., Roberts L.R., Demetris A.J., Sun Z., et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat. Med. 2006, 12:410-416.
19. Libbrecht L., Desmet V., Van Damme B., Roskams T. The immunohistochemical phenotype of dysplastic foci in human liver: correlation with putative progenitor cells. J. Hepatol. 2000, 33:76-84.
20. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295:868-872.
21. Malato Y., Naqvi S., Schürmann N., Ng R., Wang B., Zape J., Kay M.A., Grimm D., Willenbring H. Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration. J. Clin. Invest. 2011, 121:4850-4860.
22. Moorman A.F., Vermeulen J.L., Charles R., Lamers W.H. Localization of ammonia-metabolizing enzymes in human liver: ontogenesis of heterogeneity. Hepatology 1989, 9:367-372.
23. Moreno M., Chaves J.F., Sancho-Bru P., Ramalho F., Ramalho L.N., Mansego M.L., Ivorra C., Dominguez M., Conde L., Millán C., et al. Ghrelin attenuates hepatocellular injury and liver fibrogenesis in rodents and influences fibrosis progression in humans. Hepatology 2010, 51:974-985.
24. Nasmyth K. A prize for proliferation. Cell 2001, 107:689-701.
25. Nir T., Melton D.A., Dor Y. Recovery from diabetes in mice by beta cell regeneration. J. Clin. Invest. 2007, 117:2553-2561.
26. Otu H.H., Naxerova K., Ho K., Can H., Nesbitt N., Libermann T.A., Karp S.J. Restoration of liver mass after injury requires proliferative and not embryonic transcriptional patterns. J. Biol. Chem. 2007, 282:11197-11204.
27. Reich M., Liefeld T., Gould J., Lerner J., Tamayo P., Mesirov J.P. GenePattern 2.0. Nat. Genet. 2006, 38:500-501.
28. Roskams T.A., Libbrecht L., Desmet V.J. Progenitor cells in diseased human liver. Semin. Liver Dis. 2003, 23:385-396.
29. 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.
30. Salic A., Mitchison T.J. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 2008, 105:2415-2420.
31. Salpeter S.J., Klein A.M., Huangfu D., Grimsby J., Dor Y. Glucose and aging control the quiescence period that follows pancreatic beta cell replication. Development 2010, 137:3205-3213.
32. Shin S., Walton G., Aoki R., Brondell K., Schug J., Fox A., Smirnova O., Dorrell C., Erker L., Chu A.S., et al. Foxl1-Cre-marked adult hepatic progenitors have clonogenic and bilineage differentiation potential. Genes Dev. 2011, 25:1185-1192.
33. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
34. Sudakin V., Ganoth D., Dahan A., Heller H., Hershko J., Luca F.C., Ruderman J.V., Hershko A. The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 1995, 6:185-197.
35. Sugiyama M., Sakaue-Sawano A., Iimura T., Fukami K., Kitaguchi T., Kawakami K., Okamoto H., Higashijima S.I., Miyawaki A. Illuminating cell-cycle progression in the developing zebrafish embryo. Proc. Natl. Acad. Sci. USA 2009, 106:20812-20817.
36. Suzuki A., Sekiya S., Büscher D., Izpisúa Belmonte J.C., Taniguchi H. Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing p19ARF expression. Development 2008, 135:1589-1595.
37. Teta M., Rankin M.M., Long S.Y., Stein G.M., Kushner J.A. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev. Cell 2007, 12:817-826.
38. White P., Brestelli J.E., Kaestner K.H., Greenbaum L.E. Identification of transcriptional networks during liver regeneration. J. Biol. Chem. 2005, 280:3715-3722.
39. Xu X.R., Huang J., Xu Z.G., Qian B.Z., Zhu Z.D., Yan Q., Cai T., Zhang X., Xiao H.S., Qu J., et al. Insight into hepatocellular carcinogenesis at transcriptome level by comparing gene expression profiles of hepatocellular carcinoma with those of corresponding noncancerous liver. Proc. Natl. Acad. Sci. USA 2001, 98:15089-15094.
40. Zajicek G., Oren R., Weinreb M. The streaming liver. Liver 1985, 5:293-300.
41. Zaret K.S., Grompe M. Generation and regeneration of cells of the liver and pancreas. Science 2008, 322:1490-1494.
42. Zur A., Brandeis M. Timing of APC/C substrate degradation is determined by fzy/fzr specificity of destruction boxes. EMBO J. 2002, 21:4500-4510.