Primary cilium-dependent and -independent hedgehog signaling inhibits p16INK4A

Molecular Cell

Volumn 40, Issue 4, 2010, Pages 533-547

  Bishop, Cleo L ^a   Bergin, Ann Marie H ^a   Fessart, Delphine ^a   Borgdorff, Viola ^a   Hatzimasoura, Elizabeth ^a   Garbe, James C ^b   Stampfer, Martha R ^b   Koh, Jim ^c   Beach, David H ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P16; SMALL INTERFERING RNA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2;

AGING; ARTICLE; CARCINOGENESIS; CELL AGING; CELL DIVISION; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; MITOGENESIS; PROTEIN BINDING; PROTEIN EXPRESSION;

CILIA; CYCLIN-DEPENDENT KINASE INHIBITOR P16; FEMALE; GENOME, HUMAN; HEDGEHOG PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; YOUNG ADULT;

ERINACEIDAE;

EID: 78649238299     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.10.027     Document Type: Article

References (51)

1. Agren M., Kogerman P., Kleman M.I., Wessling M., Toftgård R. Expression of the PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 2004, 330:101-114.
2. Anderson C.T., Stearns T. Centriole Age Underlies Asynchronous Primary Cilium Growth in Mammalian Cells. Curr. Biol. 2009, 19:1498-1502.
3. Aza-Blanc P., Lin H.Y., Ruiz i Altaba A., Kornberg T.B. Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 2000, 127:4293-4301.
4. Brenner A.J., Stampfer M.R., Aldaz C.M. Increased p16 expression with first senescence arrest in human mammary epithelial cells and extended growth capacity with p16 inactivation. Oncogene 1998, 17:199-205.
5. Chen J.K., Taipale J., Cooper M.K., Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 2002, 16:2743-2748.
6. Chen X., Barton L.F., Chi Y., Clurman B.E., Roberts J.M. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol. Cell 2007, 26:843-852.
7. Chen M.H., Wilson C.W., Li Y.J., Law K.K., Lu C.S., Gacayan R., Zhang X., Hui C.C., Chuang P.T. Cilium-independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved. Genes Dev. 2009, 23:1910-1928.
8. Cheng J., Türkel N., Hemati N., Fuller M.T., Hunt A.J., Yamashita Y.M. Centrosome misorientation reduces stem cell division during ageing. Nature 2008, 456:599-604.
9. Chenn A., McConnell S.K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 1995, 82:631-641.
10. Chkhotua A.B., Gabusi E., Altimari A., D'Errico A., Yakubovich M., Vienken J., Stefoni S., Chieco P., Yussim A., Grigioni W.F. Increased expression of p16(INK4a) and p27(Kip1) cyclin-dependent kinase inhibitor genes in aging human kidney and chronic allograft nephropathy. Am. J. Kidney Dis. 2003, 41:1303-1313.
11. Delmas V., Beermann F., Martinozzi S., Carreira S., Ackermann J., Kumasaka M., Denat L., Goodall J., Luciani F., Viros A., et al. Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev. 2007, 21:2923-2935.
12. Eggenschwiler J.T., Anderson K.V. Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 2007, 23:345-373.
13. Garbe J.C., Bhattacharya S., Merchant B., Bassett E., Swisshelm K., Feiler H.S., Wyrobek A.J., Stampfer M.R. Molecular distinctions between stasis and telomere attrition senescence barriers shown by long-term culture of normal human mammary epithelial cells. Cancer Res. 2009, 69:7557-7568.
14. Gil J., Peters G. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat. Rev. Mol. Cell Biol. 2006, 7:667-677.
15. Gil J., Bernard D., Martínez D., Beach D. Polycomb CBX7 has a unifying role in cellular lifespan. Nat. Cell Biol. 2004, 6:67-72.
16. Hayflick L. The Limited in Vitro Lifetime of Human Diploid Cell Strains. Exp. Cell Res. 1965, 37:614-636.
17. Irelan J.T., Gutierrez Del Arroyo A., Gutierrez A., Peters G., Quon K.C., Miraglia L., Chanda S.K. A functional screen for regulators of CKDN2A reveals MEOX2 as a transcriptional activator of INK4a. PLoS ONE 2009, 4:e5067.
18. Jackson A.L., Bartz S.R., Schelter J., Kobayashi S.V., Burchard J., Mao M., Li B., Cavet G., Linsley P.S. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 2003, 21:635-637.
19. Janzen V., Forkert R., Fleming H.E., Saito Y., Waring M.T., Dombkowski D.M., Cheng T., DePinho R.A., Sharpless N.E., Scadden D.T. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
20. Jia J., Tong C., Wang B., Luo L., Jiang J. Hedgehog signalling activity of Smoothened requires phosphorylation by protein kinase A and casein kinase I. Nature 2004, 432:1045-1050.
21. Jiang J. Regulation of Hh/Gli signaling by dual ubiquitin pathways. Cell Cycle 2006, 5:2457-2463.
22. Jiang J., Hui C.C. Hedgehog signaling in development and cancer. Dev. Cell 2008, 15:801-812.
23. Kasper M., Jaks V., Fiaschi M., Toftgård R. Hedgehog signalling in breast cancer. Carcinogenesis 2009, 30:903-911.
24. Kim W.Y., Sharpless N.E. The regulation of INK4/ARF in cancer and aging. Cell 2006, 127:265-275.
25. Kiprilov E.N., Awan A., Desprat R., Velho M., Clement C.A., Byskov A.G., Andersen C.Y., Satir P., Bouhassira E.E., Christensen S.T., Hirsch R.E. Human embryonic stem cells in culture possess primary cilia with hedgehog signaling machinery. J. Cell Biol. 2008, 180:897-904.
26. Krishnamurthy J., Ramsey M.R., Ligon K.L., Torrice C., Koh A., Bonner-Weir S., Sharpless N.E. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006, 443:453-457.
27. Li H., Collado M., Villasante A., Strati K., Ortega S., Cañamero M., Blasco M.A., Serrano M. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 460:1136-1139.
28. Liu S., Fang X., Hall H., Yu S., Smith D., Lu Z., Fang D., Liu J., Stephens L.C., Woodgett J.R., Mills G.B. Homozygous deletion of glycogen synthase kinase 3beta bypasses senescence allowing Ras transformation of primary murine fibroblasts. Proc. Natl. Acad. Sci. USA 2008, 105:5248-5253.
29. Liu H., Remedi M.S., Pappan K.L., Kwon G., Rohatgi N., Marshall C.A., McDaniel M.L. Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets. Diabetes 2009, 58:663-672.
30. Matheu A., Maraver A., Collado M., Garcia-Cao I., Cañamero M., Borras C., Flores J.M., Klatt P., Viña J., Serrano M. Anti-aging activity of the Ink4/Arf locus. Aging Cell 2009, 8:152-161.
31. Meng X., Poon R., Zhang X., Cheah A., Ding Q., Hui C.C., Alman B. Suppressor of fused negatively regulates beta-catenin signaling. J. Biol. Chem. 2001, 276:40113-40119.
32. Narita M., Nũnez S., Heard E., Narita M., Lin A.W., Hearn S.A., Spector D.L., Hannon G.J., Lowe S.W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 113:703-716.
33. Nickerson S.C. Cilia on bovine mammary epithelium: ultrastructural observations. Cell Tissue Res. 1989, 255:675-677.
34. Noctor S.C., Martínez-Cerdeño V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
35. Pan J., Snell W. The primary cilium: keeper of the key to cell division. Cell 2007, 129:1255-1257.
36. Pan Y., Bai C.B., Joyner A.L., Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol. 2006, 26:3365-3377.
37. Ruiz i Altaba A., Mas C., Stecca B. The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol. 2007, 17:438-447.
38. Seeley E.S., Carrière C., Goetze T., Longnecker D.S., Korc M. Pancreatic cancer and precursor pancreatic intraepithelial neoplasia lesions are devoid of primary cilia. Cancer Res. 2009, 69:422-430.
39. 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.
40. Serrano M., Lin A.W., McCurrach M.E., Beach D., Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997, 88:593-602.
41. Smelkinson M.G., Zhou Q., Kalderon D. Regulation of Ci-SCFSlimb binding, Ci proteolysis, and hedgehog pathway activity by Ci phosphorylation. Dev. Cell 2007, 13:481-495.
42. Takahashi-Yanaga F., Sasaguri T. GSK-3beta regulates cyclin D1 expression: a new target for chemotherapy. Cell. Signal. 2008, 20:581-589.
43. Tempé D., Casas M., Karaz S., Blanchet-Tournier M.F., Concordet J.P. Multisite protein kinase A and glycogen synthase kinase 3beta phosphorylation leads to Gli3 ubiquitination by SCFbetaTrCP. Mol. Cell. Biol. 2006, 26:4316-4326.
44. Tsygankov D., Liu Y., Sanoff H.K., Sharpless N.E., Elston T.C. A quantitative model for age-dependent expression of the p16INK4a tumor suppressor. Proc. Natl. Acad. Sci. USA 2009, 106:16562-16567.
45. Wang W., Martindale J.L., Yang X., Chrest F.J., Gorospe M. Increased stability of the p16 mRNA with replicative senescence. EMBO Rep. 2005, 6:158-164.
46. Wang X., Tsai J.W., Imai J.H., Lian W.N., Vallee R.B., Shi S.H. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 2009, 461:947-955.
47. Wassermann S., Scheel S.K., Hiendlmeyer E., Palmqvist R., Horst D., Hlubek F., Haynl A., Kriegl L., Reu S., Merkel S., et al. p16INK4a is a beta-catenin target gene and indicates low survival in human colorectal tumors. Gastroenterology 2009, 136:196-205. e2.
48. Wilson C.W., Nguyen C.T., Chen M.H., Yang J.H., Gacayan R., Huang J., Chen J.N., Chuang P.T. Fused has evolved divergent roles in vertebrate Hedgehog signalling and motile ciliogenesis. Nature 2009, 459:98-102.
49. Ye X., Zerlanko B., Kennedy A., Banumathy G., Zhang R., Adams P.D. Downregulation of Wnt signaling is a trigger for formation of facultative heterochromatin and onset of cell senescence in primary human cells. Mol. Cell 2007, 27:183-196.
50. Zhong W., Chia W. Neurogenesis and asymmetric cell division. Curr. Opin. Neurobiol. 2008, 18:4-11.
51. Zmijewski J.W., Jope R.S. Nuclear accumulation of glycogen synthase kinase-3 during replicative senescence of human fibroblasts. Aging Cell 2004, 3:309-317.