Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice

Genes and Development

Volumn 19, Issue 12, 2005, Pages 1438-1443

  Bruggeman, Sophia W M ^a   Valk Lingbeek, Merel E ^a   Van Der Stoop, Petra P M ^a   Jacobs, Jacqueline J L ^a   Kieboom, Karin ^a   Tanger, Ellen ^a   Hulsman, Danielle ^a   Leung, Carly ^b   Arsenijevic, Yvan ^c   Marino, Silvia ^b   Van Lohuizen, Maarten ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Arf; Bmi1; Ink4a; Polycomb; Stem cell development

Indexed keywords

PROTEIN; PROTEIN BMI 1; PROTEIN P16INK4A; PROTEIN P19; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BMI 1 GENE; CELL CYCLE; CELL PROLIFERATION; CELL RENEWAL; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; ENZYME REPRESSION; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE TARGETING; GENETIC ANALYSIS; GENETIC PROCEDURES; IN VIVO STUDY; LYMPHOID CELL; MOUSE; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEM CELL;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; CYCLIN-DEPENDENT KINASE INHIBITOR P16; GENES, P16; HETEROZYGOTE; LYMPHOID TISSUE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPOTENT STEM CELLS; NEURONS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 20544453888     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1299305     Document Type: Article

References (38)

1. Akasaka, T., Kanno, M., Balling, R., Mieza, M.A., Taniguchi, M., and Koseki, H. 1996. A role for mel-18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development 122: 1513-1522.
2. Baptista, C.A., Hatten, M.E., Blazeski, R., and Mason, C.A. 1994. Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12: 243-260.
3. Core, N., Bel, S., Gaunt, S.J., Aurrand-Lions, M., Pearce, J., Fisher, A., and Djabali, M. 1997. Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice. Development 124: 721-729.
4. Core, N., Joly, F., Boned, A., and Djabali, M. 2004. Disruption of E2F signaling suppresses the INK4a-induced proliferative defect in M33-deficient mice. Oncogene 23: 7660-7668.
5. Dahmane, N. and Ruiz-i-Altaba, A. 1999. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126: 3089-3100.
6. De Napoles, M., Mermoud, J.E., Wakao, R., Tang, Y.A., Endoh, M., Appanah, R., Nesterova, T.B., Silva, J., Otte, A.P., Vidal, M., et al. 2004. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7: 663-676.
7. Del Mar Lorente, M., Marcos-Gutierrez, C., Perez, C., Schoorlemmer, J., Ramirez, A., Magin, T., and Vidal, M. 2000. Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice. Development 127: 5093-5100.
8. Doetsch, F. 2003. A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 13: 543-550.
9. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery Jr., C.A., Butel, J.S., and Bradley, A. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
10. Gil, J., Bernard, D., Martinez, D., and Beach, D. 2004. Polycomb CBX7 has a unifying role in cellular lifespan. Nat. Cell. Biol. 6: 67-72.
11. Haupt, Y., Alexander, W.S., Barri, G., Klinken, S.P., and Adams, J.M. 1991. Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E μ-myc transgenic mice. Cell 65: 753-763.
12. Iwama, A., Oguro, H., Negishi, M., Kato, Y., Morita, Y., Tsukui, H., Ema, H., Kamijo, T., Katoh-Fukui, Y., Koseki, H., et al. 2004. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21: 843-851.
13. Jacobs, J.J., Kieboom, K., Marino, S., DePinho, R.A., and van Lohuizen, M. 1999. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
14. Kamijo, T., Zindy, F., Roussel, M.F., Quelle, D.E., Downing, J.R., Ashmun, R.A., Grosveld, G., and Sherr, C.J. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91: 649-659.
15. Kenney, A.M., Cole, M.D., and Rowitch, D.H. 2003. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130: 15-28.
16. Kirmizis, A., Bartley, S.M., Kuzmichev, A., Margueron, R., Reinberg, D., Green, R., and Farnham, P.J. 2004. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes & Dev. 18: 1592-1605.
17. Krimpenfort, P., Quon, K.C., Mooi, W.J., Loonstra, A., and Berns, A. 2001. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413: 83-86.
18. Kuzmichev, A., Jenuwein, T., Tempst, P., and Reinberg, D. 2004. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell 14: 183-193.
19. Lessard, J. and Sauvageau, G. 2003. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260.
20. Leung, C., Lingbeek, M., Shakhova, O., Liu, J., Tanger, E., Saremaslani, P., Van Lohuizen, M., and Marino, S. 2004. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 428: 337-341.
21. Lowe, S.W. and Sherr, C.J. 2003. Tumor suppression by Ink4a-Arf: Progress and puzzles. Curr. Opin. Genet. Dev. 13: 77-83.
22. Molofsky, A.V., Pardal, R., Iwashita, T., Park, I.K., Clarke, M.F., and Morrison, S.J. 2003. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425: 962-967.
23. Arf senescence pathways. Genes & Dev. (this issue).
24. Morshead, C.M., Reynolds, B.A., Craig, C.G., McBurney, M.W., Staines, W.A., Morassutti, D., Weiss, S., and van der Kooy, D. 1994. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071-1082.
25. Park, I.K., Qian, D., Kiel, M., Becker, M.W., Pihalja, M., Weissman, I.L., Morrison, S.J., and Clarke, M.F. 2003. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305.
26. Quelle, D.E., Zindy, F., Ashmun, R.A., and Sherr, C.J. 1995. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83: 993-1000.
27. Reynolds, B.A. and Weiss, S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
28. Serrano, M., Hannon, G.J., and Beach, D. 1993. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704-707.
29. Serrano, M., Lee, H., Chin, L., Cordon-Cardo, C., Beach, D., and DePinho, R.A. 1996. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85: 27-37.
30. Sharpless, N.E. and DePinho, R.A. 1999. The INK4A/ARF locus and its two gene products. Curr. Opin. Genet. Dev. 9: 22-30.
31. Sherr, C.J. and Weber, J.D. 2000. The ARF/p53 pathway. Curr. Opin. Genet. Dev. 10: 94-99.
32. Valk-Lingbeek, M.E. Bruggeman, S.W., and van Lohuizen, M. 2004. Stem cells and cancer: The polycomb connection. Cell 118: 409-418.
33. Van der Lugt, N.M., Domen, J., Linders, K., van Roon, M., Robanus-Maandag, E., te Riele, H., van der Valk, M., Deschamps, J., Sofroniew, M., and van Lohuizen, M. 1994. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes & Dev. 8: 757-769.
34. Van Lohuizen, M., Verbeek, S., Scheijen, B., Wientjens, E., van der Gulden, H., and Berns, A. 1991. Identification of cooperating oncogenes in E μ-myc transgenic mice by provirus tagging. Cell 65: 737-752.
35. Voncken, J.W., Roelen, B.A., Roefs, M., de Vries, S., Verhoeven, E., Marino, S., Deschamps, J., and van Lohuizen, M. 2003. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl. Acad. Sci. 100: 2468-2473.
36. Wang, V.Y. and Zoghbi, H.Y. 2001. Genetic regulation of cerebellar development. Nat. Rev. Neurosci. 2: 484-491.
37. Wechsler-Reya, R.J. and Scott, M.P. 1999. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22: 103-114.
38. Zencak, D., Lingbeek, M., Kostic, C., Tekaya, M., Tanger, E., Hornfeld, D., Jaquet, M., Munier, F.L., Schorderet, D.F., van Lohuizen, M., et al. 2005. Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation. J. Neurosci. (in press).