Bmi1 directly represses p21Waf1/Cip1 in Shh-induced proliferation of cerebellar granule cell progenitors

Molecular and Cellular Neuroscience

Volumn 45, Issue 2, 2010, Pages 151-162

  Subkhankulova, T ^a   Zhang, X ^a   Leung, C ^b   Marino, S ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Bmi1; Cerebellum; Granule cells; Medulloblastoma; P21waf1 cip1; Shh

Indexed keywords

BMI1 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; PROTEIN P19ARF; SONIC HEDGEHOG PROTEIN; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL ADHESION; CELL CYCLE REGULATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GRANULE CELL; MOUSE; NEURAL STEM CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CEREBELLUM; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HEDGEHOG PROTEINS; MICE; NEURAL STEM CELLS; NEUROGENESIS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77955772813     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.06.006     Document Type: Article

References (47)

1. Behesti H., Marino S. Cerebellar granule cells: insights into proliferation, differentiation, and role in medulloblastoma pathogenesis. Int. J. Biochem. Cell Biol. 2009, 41:435-445.
2. Bracken A.P., Dietrich N., Pasini D., Hansen K.H., Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006, 20:1123-1136.
3. Bracken A.P., Kleine-Kohlbrecher D., Dietrich N., Pasini D., Gargiulo G., Beekman C., Theilgaard-Monch K., Minucci S., Porse B.T., Marine J.C., Hansen K.H., Helin K. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 2007, 21:525-530.
4. Browd S.R., Kenney A.M., Gottfried O.N., Yoon J.W., Walterhouse D., Pedone C.A., Fults D.W. N-myc can substitute for insulin-like growth factor signaling in a mouse model of sonic hedgehog-induced medulloblastoma. Cancer Res. 2006, 66:2666-2672.
5. Bruggeman S.W., Valk-Lingbeek M.E., van der Stoop P.P., Jacobs J.J., Kieboom K., Tanger E., Hulsman D., Leung C., Arsenijevic Y., Marino S., van Lohuizen M. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev. 2005, 19:1438-1443.
6. Bruggeman S.W., Hulsman D., van Lohuizen M. Bmi1 deficient neural stem cells have increased Integrin dependent adhesion to self-secreted matrix. Biochim. Biophys. Acta 2009.
7. Buchwald G., van der Stoop P., Weichenrieder O., Perrakis A., van Lohuizen M., Sixma T.K. Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 2006, 25:2465-2474.
8. Dahmane N., Ruiz-i-Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development (Cambridge, England) 1999, 126:3089-3100.
9. DeCamp D.L., Thompson T.M., de Sauvage F.J., Lerner M.R. Smoothened activates Galphai-mediated signaling in frog melanophores. J. Biol. Chem. 2000, 275:26322-26327.
10. Fasano C.A., Dimos J.T., Ivanova N.B., Lowry N., Lemischka I.R., Temple S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 2007, 1:87-99.
11. Feng Y.Z., Shiozawa T., Miyamoto T., Kashima H., Kurai M., Suzuki A., Ying-Song J., Konishi I. Overexpression of hedgehog signaling molecules and its involvement in the proliferation of endometrial carcinoma cells. Clin. Cancer Res. 2007, 13:1389-1398.
12. Ferguson K.L., Vanderluit J.L., Hebert J.M., McIntosh W.C., Tibbo E., MacLaurin J.G., Park D.S., Wallace V.A., Vooijs M., McConnell S.K., Slack R.S. Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J. 2002, 21:3337-3346.
13. Hatten M.E., Alder J., Zimmerman K., Heintz N. Genes involved in cerebellar cell specification and differentiation. Curr. Opin. Neurobiol. 1997, 7:40-47.
14. Hatton B.A., Knoepfler P.S., Kenney A.M., Rowitch D.H., de Alboran I.M., Olson J.M., Eisenman R.N. N-myc is an essential downstream effector of Shh signaling during both normal and neoplastic cerebellar growth. Cancer Res. 2006, 66:8655-8661.
15. Hernandez-Munoz I., Taghavi P., Kuijl C., Neefjes J., van Lohuizen M. Association of BMI1 with polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1. Mol. Cell. Biol. 2005, 25:11047-11058.
16. Hubbell E., Liu W.M., Mei R. Robust estimators for expression analysis. Bioinformatics (Oxford, England) 2002, 18:1585-1592.
17. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 2001, 15:3059-3087.
18. Iscove N.N., Barbara M., Gu M., Gibson M., Modi C., Winegarden N. Representation is faithfully preserved in global cDNA amplified exponentially from sub-picogram quantities of mRNA. Nat. Biotechnol. 2002, 20:940-943.
19. Jacobs J.J., Kieboom K., Marino S., DePinho R.A., van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999, 397:164-168.
20. Kenney A.M., Rowitch D.H. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 2000, 20:9055-9067.
21. Kenney A.M., Cole M.D., Rowitch D.H. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development (Cambridge, England) 2003, 130:15-28.
22. Leung C., Lingbeek M., Shakhova O., Liu J., Tanger E., Saremaslani P., Van Lohuizen M., Marino S. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004, 428:337-341.
23. Liu W.M., Mei R., Di X., Ryder T.B., Hubbell E., Dee S., Webster T.A., Harrington C.A., Ho M.H., Baid J., Smeekens S.P. Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics (Oxford, England) 2002, 18:1593-1599.
24. Lowe S.W., Sherr C.J. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr. Opin. Genet. Dev. 2003, 13:77-83.
25. Marino S., Vooijs M., van Der Gulden H., Jonkers J., Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 2000, 14:994-1004.
26. Marino S., Hoogervoorst D., Brandner S., Berns A. are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development (Cambridge, England) 2003, 130:3359-3368. Rb.
27. Messer A. Factors influencing monolayer cell culture morphology and survival of cerebellar granule cells from wild-type and mutant mice. Prog. Clin. Biol. Res. 1977, 15:251-257.
28. Michael L.E., Westerman B.A., Ermilov A.N., Wang A., Ferris J., Liu J., Blom M., Ellison D.W., van Lohuizen M., Dlugosz A.A. Bmi1 is required for Hedgehog pathway-driven medulloblastoma expansion. Neoplasia (New York, N.Y) 2008, 10:1343-1349. 1345p following 1349.
29. Miyazawa K., Himi T., Garcia V., Yamagishi H., Sato S., Ishizaki Y. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J. Neurosci. 2000, 20:5756-5763.
30. Molofsky A.V., He S., Bydon M., Morrison S.J., Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 2005, 19:1432-1437.
31. Ohta M., Tateishi K., Kanai F., Watabe H., Kondo S., Guleng B., Tanaka Y., Asaoka Y., Jazag A., Imamura J., Ijichi H., Ikenoue T., Sata M., Miyagishi M., Taira K., Tada M., Kawabe T., Omata M. p53-Independent negative regulation of p21/cyclin-dependent kinase-interacting protein 1 by the sonic hedgehog-glioma-associated oncogene 1 pathway in gastric carcinoma cells. Cancer Res. 2005, 65:10822-10829.
32. Ono K., Yasui Y., Ikenaka K. Lower rhombic lip-derived cells undergo transmedian tangential migration followed by radial migration in the chick embryo brainstem. Eur. J. Neurosci. 2004, 20:914-922.
33. Park I.K., Morrison S.J., Clarke M.F. Bmi1, stem cells, and senescence regulation. J. Clin. Invest. 2004, 113:175-179.
34. Pogoriler J., Millen K., Utset M., Du W. Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation. Development (Cambridge, England) 2006, 133:3929-3937.
35. Puskas L.G., Zvara A., Hackler L., Van Hummelen P. RNA amplification results in reproducible microarray data with slight ratio bias. Biotechniques 2002, 32:1330-1334. 1336, 1338, 1340.
36. Quelle D.E., Zindy F., Ashmun R.A., Sherr C.J. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 1995, 83:993-1000.
37. Serrano M., Hannon G.J., Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993, 366:704-707.
38. Shapiro G.I., Edwards C.D., Rollins B.J. The physiology of p16(INK4A)-mediated G1 proliferative arrest. Cell Biochem. Biophys. 2000, 33:189-197.
39. Sharpless N.E., DePinho R.A. The INK4A/ARF locus and its two gene products. Curr. Opin. Genet. Dev. 1999, 9:22-30.
40. Shinwari Z., Manogaran P.S., Alrokayan S.A., Al-Hussein K.A., Aboussekhra A. Vincristine and lomustine induce apoptosis and p21(WAF1) up-regulation in medulloblastoma and normal human epithelial and fibroblast cells. Journal of neuro-oncology 2008, 87:123-132.
41. Sillitoe R.V., Joyner A.L. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu. Rev. Cell Dev. Biol. 2007, 23:549-577.
42. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J., Davidson E.H., Wong W.H., McMahon A.P. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development (Cambridge, England) 2007, 134:1977-1989.
43. Wechsler-Reya R.J., Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999, 22:103-114.
44. Yuasa S. [Developmental mechanisms of neural network in the cerebellar system]. Nihon shinkei seishin yakurigaku zasshi = Japanese journal of psychopharmacology 1995, 15:177-183.
45. Yun J.S., Rust J.M., Ishimaru T., Diaz E. A novel role of the Mad family member Mad3 in cerebellar granule neuron precursor proliferation. Mol. Cell. Biol. 2007, 27:8178-8189.
46. Zencak D., Lingbeek M., Kostic C., Tekaya M., Tanger E., Hornfeld D., Jaquet M., Munier F.L., Schorderet D.F., van Lohuizen M., Arsenijevic Y. Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation. J. Neurosci. 2005, 25:5774-5783.
47. Zhao Q., Kho A., Kenney A.M., Yuk Di D.I., Kohane I., Rowitch D.H. Identification of genes expressed with temporal-spatial restriction to developing cerebellar neuron precursors by a functional genomic approach. Proc. Natl Acad. Sci. USA 2002, 99:5704-5709.