Loss of c-Met disrupts gene expression program required for G2/M progression during liver regeneration in mice

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-10

  Factor, Valentina M ^a   Seo, Daekwan ^a   Ishikawa, Tsuyoshi ^a   Kaposi Novak, Pal ^a   Marquardt, Jens U ^a   Andersen, Jesper B ^a   Conner, Elizabeth A ^a   Thorgeirsson, Snorri S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; AURORA B KINASE; CYCLIN DEPENDENT KINASE 1; DUAL SPECIFICITY PHOSPHATASE 6; EPIDERMAL GROWTH FACTOR; HEAT SHOCK PROTEIN; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; MYC PROTEIN; POLO LIKE KINASE 1; PROTEIN C FOS; PROTEIN C JUN; PROTEIN IKBZ; PROTEIN MAD2; SCATTER FACTOR RECEPTOR; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR MAFK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA MICROARRAY; DNA REPLICATION; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE LOSS; LIVER CELL; LIVER REGENERATION; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL DIVISION; CYTOLOGY; ENZYMOLOGY; FEMALE; GENETICS; LIVER; MALE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS;

ANIMALS; CELL DIVISION; FEMALE; G2 PHASE; GENE EXPRESSION REGULATION; HEPATOCYTES; LIVER; LIVER REGENERATION; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-MET; UP-REGULATION;

EID: 77958544269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012739     Document Type: Article

References (46)

1. Taub R (2004) Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 5: 836-847.
2. Fausto N, Campbell JS, Riehle KJ (2006) Liver regeneration. Hepatology 43: S45-53.
3. Michalopoulos GK (2010) Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 176: 2-13.
4. Matsumoto K, Nakamura T (1991) Hepatocyte growth factor: molecular structure and implications for a central role in liver regeneration. J Gastroenterol Hepatol 6: 509-519.
5. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, et al. (1991) Identification of the hepatocyte growth factor receptor as the c-met protooncogene product. Science 251: 802-804.
6. Vande Woude GF, Jeffers M, Cortner J, Alvord G, Tsarfaty I, et al. (1997) Met- HGF/SF: tumorigenesis, invasion and metastasis. Ciba Found Symp 212: 119-130; discussion 130-112, 148-154.
7. Borowiak M, Garratt AN, Wustefeld T, Strehle M, Trautwein C, et al. (2004) Met provides essential signals for liver regeneration. Proc Natl Acad Sci U S A 101: 10608-10613.
8. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, et al. (2004) Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A 101: 4477-4482.
9. Paranjpe S, Bowen WC, Bell AW, Nejak-Bowen K, Luo JH, et al. (2007) Cell cycle effects resulting from inhibition of hepatocyte growth factor and its receptor c-Met in regenerating rat livers by RNA interference. Hepatology 45: 1471-1477.
10. Shiota G, Kawasaki H (1998) Hepatocyte growth factor in transgenic mice. Int J Exp Pathol 79: 267-277.
11. Boccaccio C, Ando M, Tamagnone L, Bardelli A, Michieli P, et al. (1998) Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391: 285-288.
12. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF (2003) Met, metastasis, motility and more. Nat Rev Mol Cell Biol 4: 915-925.
13. Ito T (2007) Role of histone modification in chromatin dynamics. J Biochem 141: 609-614.
14. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, et al. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
15. Li J, Campbell JS, Mitchell C, McMahan RS, Yu X, et al. (2009) Relationships between deficits in tissue mass and transcriptional programs after partial hepatectomy in mice. Am J Pathol 175: 947-957.
16. Thrower DA, Jordan MA, Schaar BT, Yen TJ, Wilson L (1995) Mitotic HeLa cells contain a CENP-E-associated minus end-directed microtubule motor. EMBO J 14: 918-926.
17. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, et al. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 13: 1977-2000.
18. Goto H, Yasui Y, Nigg EA, Inagaki M (2002) Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 7: 11-17.
19. Fang G, Yu H, Kirschner MW (1998) The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev 12: 1871-1883.
20. Murphy LO, MacKeigan JP, Blenis J (2004) A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol Cell Biol 24: 144-153.
21. Liao Y, Shikapwashya ON, Shteyer E, Dieckgraefe BK, Hruz PW, et al. (2004) Delayed hepatocellular mitotic progression and impaired liver regeneration in early growth response-1-deficient mice. J Biol Chem 279: 43107-43116.
22. Scheving LA, Stevenson MC, Taylormoore JM, Traxler P, Russell WE (2002) Integral role of the EGF receptor in HGF-mediated hepatocyte proliferation. Biochem Biophys Res Commun 290: 197-203.
23. Natarajan A, Wagner B, Sibilia M (2007) The EGF receptor is required for efficient liver regeneration. Proc Natl Acad Sci U S A 104: 17081-17086.
24. Fremin C, Bessard A, Ezan F, Gailhouste L, Regeard M, et al. (2009) Multiple division cycles and long-term survival of hepatocytes are distinctly regulated by extracellular signal-regulated kinases ERK1 and ERK2. Hepatology 49: 930-939.
25. Meloche S, Pouyssegur J (2007) The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene 26: 3227-3239.
26. Talarmin H, Rescan C, Cariou S, Glaise D, Zanninelli G, et al. (1999) The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G(1) phase progression in proliferating hepatocytes. Mol Cell Biol 19: 6003-6011.
27. Chambard JC, Lefloch R, Pouyssegur J, Lenormand P (2007) ERK implication in cell cycle regulation. Biochim Biophys Acta 1773: 1299-1310.
28. Dumesic PA, Scholl FA, Barragan DI, Khavari PA (2009) Erk1/2 MAP kinases are required for epidermal G2/M progression. J Cell Biol 185: 409-422.
29. Murphy LO, Blenis J (2006) MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31: 268-275.
30. Yamamoto T, Ebisuya M, Ashida F, Okamoto K, Yonehara S, et al. (2006) Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr Biol 16: 1171-1182.
31. Liu X, Yan S, Zhou T, Terada Y, Erikson RL (2004) The MAP kinase pathway is required for entry into mitosis and cell survival. Oncogene 23: 763-776.
32. Roberts EC, Shapiro PS, Nahreini TS, Pages G, Pouyssegur J, et al. (2002) Distinct cell cycle timing requirements for extracellular signal-regulated kinase and phosphoinositide 3-kinase signaling pathways in somatic cell mitosis. Mol Cell Biol 22: 7226-7241.
33. Wright JH, Munar E, Jameson DR, Andreassen PR, Margolis RL, et al. (1999) Mitogen-activated protein kinase kinase activity is required for the G(2)/M transition of the cell cycle in mammalian fibroblasts. Proc Natl Acad Sci U S A 96: 11335-11340.
34. Bollen M, Gerlich DW, Lesage B (2009) Mitotic phosphatases: from entry guards to exit guides. Trends Cell Biol 19: 531-541.
35. Fu Z, Malureanu L, Huang J, Wang W, Li H, et al. (2008) Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat Cell Biol 10: 1076-1082.
36. Lindqvist A, Rodriguez-Bravo V, Medema RH (2009) The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 185: 193-202.
37. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
38. Larsson N, Melander H, Marklund U, Osterman O, Gullberg M (1995) G2/M transition requires multisite phosphorylation of oncoprotein 18 by two distinct protein kinase systems. J Biol Chem 270: 14175-14183.
39. Suryadinata R, Sadowski M, Sarcevic B (2010) Control of cell cycle progression by phosphorylation of cyclin-dependent kinase (CDK) substrates. Biosci Rep 30: 243-255.
40. Laoukili J, Alvarez M, Meijer LA, Stahl M, Mohammed S, et al. (2008) Activation of FoxM1 during G2 requires cyclin A/Cdk-dependent relief of autorepression by the FoxM1 N-terminal domain. Mol Cell Biol 28: 3076-3087.
41. Postic C, Magnuson MA (2000) DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis 26: 149-150.
42. Lee JS, Chu IS, Heo J, Calvisi DF, Sun Z, et al. (2004) Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40: 667-676.
43. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
44. Quackenbush J (2002) Microarray data normalization and transformation. Nat Genet 32 suppl: 496-501.
45. Neuhauser M, Jockel KH (2006) A bootstrap test for the analysis of microarray experiments with a very small number of replications. Appl Bioinformatics 5: 173-179.
46. Strimmer K (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24: 1461-1462.