Home LiteratureArticle Details
PMID: 11572993 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Increased levels of forkhead box M1B transcription factor in transgenic mouse hepatocytes prevent age-related proliferation defects in regenerating liver.

Wang X, Quail E, Hung NJ, Tan Y, Ye H, Costa RH

Abstract

The forkhead box (Fox) family of transcription factors share homology in the winged helix/forkhead DNA-binding domain and play important roles in regulating cellular proliferation, differentiation, longevity, and cellular transformation. Forkhead box M1B (FoxM1B) is a ubiquitously expressed member of the Fox transcription factor family whose expression is restricted to proliferating cells and that mediates hepatocyte entry into DNA synthesis and mitosis during liver regeneration. Recent cDNA microarray studies indicated that age-related defects in cellular proliferation are associated with diminished expression of the FoxM1B transcription factor. Here, we show that increased levels of FoxM1B in regenerating liver of old transgenic mice restore the sharp peaks in hepatocyte DNA replication and mitosis that are the hallmarks of young regenerating mouse liver. Restoration of the young regenerating liver phenotype is associated with increased expression of numerous cell cycle regulatory genes that include cyclin D1, cyclin A2, cyclin F, cyclin B1, cyclin B2, Cdc25B, and p55cdc. Cotransfection assays in the human hepatoma HepG2 cell line demonstrated that FoxM1B protein stimulated expression of both the cyclin B1 and cyclin D1 promoters, suggesting that these cyclin genes are a direct FoxM1B transcriptional target. These results suggest that FoxM1B controls the transcriptional network of genes that are essential for cell division and exit from mitosis. Our results indicate that reduced expression of the FoxM1B transcription factor contributes to the decline in cellular proliferation observed in the aging process.

MeSH Terms
Aging/genetics,physiology Animals Cell Division Cyclin-Dependent Kinases/metabolism Cyclophilins/genetics DNA Replication DNA-Binding Proteins/genetics Forkhead Box Protein M1 Forkhead Transcription Factors Hepatocytes/cytology,physiology Liver/physiology Liver Regeneration/physiology Mice Mice, Transgenic Phosphorylation RNA Probes RNA, Antisense Retinoblastoma Protein/metabolism Ribonucleases S Phase Transcription Factors/genetics Transfection
Chemicals
DNA-Binding Proteins FOXH1 protein, human Forkhead Box Protein M1 Forkhead Transcription Factors Foxh1 protein, mouse Foxm1 protein, mouse RNA Probes RNA, Antisense Retinoblastoma Protein Transcription Factors Cyclin-Dependent Kinases Ribonucleases Cyclophilins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wang X
Department of Molecular Genetics, University of Illinois, College of Medicine, 900 South Ashland Avenue, Chicago, IL 60607-7170, USA.
Quail E
Hung N J
Tan Y
Ye H
Costa R H
References (36)
36 references, click to expand
  1. Oncogenic transformation by the FOX protein Qin requires DNA binding.
    Oncogene. 2000 Oct 5;19(42):4815-21 PMID: 11039897
  2. Elevated levels of hepatocyte nuclear factor 3beta in mouse hepatocytes influence expression of genes involved in bile acid and glucose homeostasis.
    Mol Cell Biol. 2000 Nov;20(21):8264-82 PMID: 11027295
  3. Transcription factors in mouse lung development and function.
    Am J Physiol Lung Cell Mol Physiol. 2001 May;280(5):L823-38 PMID: 11290504
  4. Earlier expression of the transcription factor HFH-11B diminishes induction of p21(CIP1/WAF1) levels and accelerates mouse hepatocyte entry into S-phase following carbon tetrachloride liver injury.
    Hepatology. 2001 Jun;33(6):1404-14 PMID: 11391529
  5. Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head.
    Genes Dev. 1991 Mar;5(3):416-27 PMID: 1672118
  6. Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3521-4 PMID: 8475101
  7. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5.
    Nature. 1993 Jul 29;364(6436):412-20 PMID: 8332212
  8. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter.
    Mol Cell Biol. 1995 May;15(5):2782-90 PMID: 7739559
  9. Decreases in growth hormone receptor signal transduction contribute to the decline in insulin-like growth factor I gene expression with age.
    Endocrinology. 1995 Oct;136(10):4551-7 PMID: 7664676
  10. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions.
    J Biol Chem. 1995 Oct 6;270(40):23589-97 PMID: 7559524
  11. Liver regeneration. 2. Role of growth factors and cytokines in hepatic regeneration.
    FASEB J. 1995 Dec;9(15):1527-36 PMID: 8529831
  12. Liver regeneration 4: transcriptional control of liver regeneration.
    FASEB J. 1996 Mar;10(4):413-27 PMID: 8647340
  13. The hybrid PAX3-FKHR fusion protein of alveolar rhabdomyosarcoma transforms fibroblasts in culture.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9805-9 PMID: 8790412
  14. Differential regulation of cyclin B1 RNA and protein expression during hepatocyte growth in vivo.
    Cell Growth Differ. 1996 Jul;7(7):903-16 PMID: 8809408
  15. Five years on the wings of fork head.
    Mech Dev. 1996 Jun;57(1):3-20 PMID: 8817449
  16. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice.
    Science. 1996 Nov 22;274(5291):1379-83 PMID: 8910279
  17. Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues.
    Mol Cell Biol. 1997 Mar;17(3):1626-41 PMID: 9032290
  18. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1441-6 PMID: 9037072
  19. Liver regeneration.
    Science. 1997 Apr 4;276(5309):60-6 PMID: 9082986
  20. The winged-helix transcription factor Trident is expressed in cycling cells.
    Nucleic Acids Res. 1997 May 1;25(9):1715-9 PMID: 9108152
  21. Molecular analysis of a novel winged helix protein, WIN. Expression pattern, DNA binding property, and alternative splicing within the DNA binding domain.
    J Biol Chem. 1997 Aug 8;272(32):19827-36 PMID: 9242644
  22. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans.
    Nature. 1997 Oct 30;389(6654):994-9 PMID: 9353126
  23. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans.
    Science. 1997 Nov 14;278(5341):1319-22 PMID: 9360933
  24. Coexpression of C-myc and transforming growth factor alfa in the liver promotes early replicative senescence and diminishes regenerative capacity after partial hepatectomy in transgenic mice.
    Hepatology. 1997 Dec;26(6):1434-43 PMID: 9397983
  25. Uncoupling of S phase and mitosis in cardiomyocytes and hepatocytes lacking the winged-helix transcription factor Trident.
    Curr Biol. 1998 Dec 3;8(24):1327-30 PMID: 9843684
  26. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins.
    Dev Biol. 1999 May 1;209(1):1-10 PMID: 10208738
  27. Molecular mechanisms controlling lung morphogenesis.
    Clin Genet. 1999 Jul;56(1):14-27 PMID: 10466413
  28. Whose end is destruction: cell division and the anaphase-promoting complex.
    Genes Dev. 1999 Aug 15;13(16):2039-58 PMID: 10465783
  29. Premature expression of the winged helix transcription factor HFH-11B in regenerating mouse liver accelerates hepatocyte entry into S phase.
    Mol Cell Biol. 1999 Dec;19(12):8570-80 PMID: 10567581
  30. Unified nomenclature for the winged helix/forkhead transcription factors.
    Genes Dev. 2000 Jan 15;14(2):142-6 PMID: 10702024
  31. Cyclin F regulates the nuclear localization of cyclin B1 through a cyclin-cyclin interaction.
    EMBO J. 2000 Mar 15;19(6):1378-88 PMID: 10716937
  32. Cell cycle regulation by the Cdc25 phosphatase family.
    Prog Cell Cycle Res. 2000;4:107-14 PMID: 10740819
  33. Mitotic misregulation and human aging.
    Science. 2000 Mar 31;287(5462):2486-92 PMID: 10741968
  34. Transcriptional regulation of liver development.
    Dev Dyn. 2000 Oct;219(2):131-42 PMID: 11002334
  35. The Rb/E2F pathway: expanding roles and emerging paradigms.
    Genes Dev. 2000 Oct 1;14(19):2393-409 PMID: 11018009
  36. The hepatocyte nuclear factor 3 (HNF3 or FOXA) family in metabolism.
    Trends Endocrinol Metab. 2000 Sep;11(7):281-5 PMID: 10920385
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-09-25
Pages
11468-73
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC58753
Subset
IM
Grants
NIDDK NIH HHS · R01 DK054687 · United States
NIDDK NIH HHS · R01 DK54687 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]