Downregulation of Wnt Signaling Is a Trigger for Formation of Facultative Heterochromatin and Onset of Cell Senescence in Primary Human Cells

Molecular Cell

Volumn 27, Issue 2, 2007, Pages 183-196

  Ye, Xiaofen ^a   Zerlanko, Brad ^a   Kennedy, Alyssa ^a   Banumathy, Gowrishankar ^a   Zhang, Rugang ^a   Adams, Peter D ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

BETA ACTIN; BETA CATENIN; CHAPERONE; HISTONE; HISTONE H3; TUMOR SUPPRESSOR PROTEIN; WNT PROTEIN; WNT2 PROTEIN;

AGING; ARTICLE; CANCER; CANCER GROWTH; CELL DIVISION; CELL PROLIFERATION; CELL STRESS; CELLULAR STRESS RESPONSE; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION REGULATION; HETEROCHROMATIN; HOMEOSTASIS; HUMAN; SENESCENCE; SIGNAL TRANSDUCTION;

CELL AGING; CELL CYCLE PROTEINS; CELLS, CULTURED; DOWN-REGULATION; GLYCOGEN SYNTHASE KINASE 3; HETEROCHROMATIN; HUMANS; LIGANDS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT2 PROTEIN;

EID: 34447343780     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.05.034     Document Type: Article

References (65)

1. Adams P.D. Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene (2007) 10.1016/j.gene.2007.04.020 Published online May 1, 2007
2. Ahuja D., Saenz-Robles M.T., and Pipas J.M. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24 (2005) 7729-7745
3. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.V., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444 (2006) 633-637
4. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., and MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl. Acad. Sci. USA 102 (2005) 3324-3329
5. Braig M., Lee S., Loddenkemper C., Rudolph C., Peters A.H., Schlegelberger B., Stein H., Dorken B., Jenuwein T., and Schmitt C.A. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436 (2005) 660-665
6. Campisi J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120 (2005) 513-522
7. Chan H.M., Narita M., Lowe S.W., and Livingston D.M. The p400 E1A-associated protein is a novel component of the p53→p21 senescence pathway. Genes Dev. 19 (2005) 196-201
8. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., Koutcher J.A., Scher H.I., Ludwig T., Gerald W., et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436 (2005) 725-730
9. Chenn A., and Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297 (2002) 365-369
10. Clement G., Braunschweig R., Pasquier N., Bosman F.T., and Benhattar J. Alterations of the Wnt signaling pathway during the neoplastic progression of Barrett's esophagus. Oncogene 25 (2006) 3084-3092
11. Cohen P., and Goedert M. GSK3 inhibitors: development and therapeutic potential. Nat. Rev. Drug Discov. 3 (2004) 479-487
12. Collado M., Gil J., Efeyan A., Guerra C., Schuhmacher A.J., Barradas M., Benguria A., Zaballos A., Flores J.M., Barbacid M., et al. Tumour biology: senescence in premalignant tumours. Nature 436 (2005) 642
13. Courtois-Cox S., Genther Williams S.M., Reczek E.E., Johnson B.W., McGillicuddy L.T., Johannessen C.M., Hollstein P.E., MacCollin M., and Cichowski K. A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 10 (2006) 459-472
14. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., and Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
15. Daganzo S.M., Erzberger J.P., Lam W.M., Skordalakes E., Zhang R., Franco A.A., Brill S.J., Adams P.D., Berger J.M., and Kaufman P.D. Structure and function of the conserved core of histone deposition protein Asf1. Curr. Biol. 13 (2003) 2148-2158
16. Dale T.C., Weber-Hall S.J., Smith K., Huguet E.L., Jayatilake H., Gusterson B.A., Shuttleworth G., O'Hare M., and Harris A.L. Compartment switching of WNT-2 expression in human breast tumors. Cancer Res. 56 (1996) 4320-4323
17. Damalas A., Kahan S., Shtutman M., Ben-Ze'ev A., and Oren M. Deregulated beta-catenin induces a p53- and ARF-dependent growth arrest and cooperates with Ras in transformation. EMBO J. 20 (2001) 4912-4922
18. Denoyelle C., Abou-Rjaily G., Bezrookove V., Verhaegen M., Johnson T.M., Fullen D.R., Pointer J.N., Gruber S.B., Su L.D., Nikiforov M.A., et al. Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat. Cell Biol. 8 (2006) 1053-1063
19. Di Micco R., Fumagalli M., Cicalese A., Piccinin S., Gasparini P., Luise C., Schurra C., Garre M., Nuciforo P.G., Bensimon A., et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444 (2006) 638-642
20. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92 (1995) 9363-9367
21. Fiol C.J., Mahrenholz A.M., Wang Y., Roeske R.W., and Roach P.J. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J. Biol. Chem. 262 (1987) 14042-14048
22. Funayama R., Saito M., Tanobe H., and Ishikawa F. Loss of linker histone H1 in cellular senescence. J. Cell Biol. 175 (2006) 869-880
23. Gazit A., Yaniv A., Bafico A., Pramila T., Igarashi M., Kitajewski J., and Aaronson S.A. Human frizzled 1 interacts with transforming Wnts to transduce a TCF dependent transcriptional response. Oncogene 18 (1999) 5959-5966
24. Geiger H., and Van Zant G. The aging of lympho-hematopoietic stem cells. Nat. Immunol. 3 (2002) 329-333
25. Guney I., Wu S., and Sedivy J.M. Reduced c-Myc signaling triggers telomere-independent senescence by regulating Bmi-1 and p16(INK4a). Proc. Natl. Acad. Sci. USA 103 (2006) 3645-3650
26. Hedgepeth C.M., Deardorff M.A., Rankin K., and Klein P.S. Regulation of glycogen synthase kinase 3beta and downstream Wnt signaling by axin. Mol. Cell. Biol. 19 (1999) 7147-7157
27. Herbig U., Jobling W.A., Chen B.P., Chen D.J., and Sedivy J.M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14 (2004) 501-513
28. Herbig U., Ferreira M., Condel L., Carey D., and Sedivy J.M. Cellular senescence in aging primates. Science 311 (2006) 1257
29. Janzen V., Forkert R., Fleming H.E., Saito Y., Waring M.T., Dombkowski D.M., Cheng T., Depinho R.A., Sharpless N.E., and Scadden D.T. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16(INK4a). Nature 443 (2006) 421-426
30. Jeyapalan J.C., Ferreira M., Sedivy J.M., and Herbig U. Accumulation of senescent cells in mitotic tissue of aging primates. Mech. Ageing Dev. 128 (2007) 36-44
31. Karasawa T., Yokokura H., Kitajewski J., and Lombroso P.J. Frizzled-9 is activated by Wnt-2 and functions in Wnt/beta -catenin signaling. J. Biol. Chem. 277 (2002) 37479-37486
32. Kortlever R.M., Higgins P.J., and Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat. Cell Biol. 8 (2006) 877-884
33. Krishnamurthy J., Ramsey M.R., Ligon K.L., Torrice C., Koh A., Bonner-Weir S., and Sharpless N.E. p16(INK4a) induces an age-dependent decline in islet regenerative potential. Nature 443 (2006) 453-457
34. Loppin B., Bonnefoy E., Anselme C., Laurencon A., Karr T.L., and Couble P. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437 (2005) 1386-1390
35. Mallette F.A., Gaumont-Leclerc M.F., and Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev. 21 (2007) 43-48
36. Michaloglou C., Vredeveld L.C., Soengas M.S., Denoyelle C., Kuilman T., van der Horst C.M., Majoor D.M., Shay J.W., Mooi W.J., and Peeper D.S. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436 (2005) 720-724
37. Molofsky A.V., Slutsky S.G., Joseph N.M., He S., Pardal R., Krishnamurthy J., Sharpless N.E., and Morrison S.J. Increasing p16(INK4a) expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443 (2006) 448-452
38. Moshkin Y.M., Armstrong J.A., Maeda R.K., Tamkun J.W., Verrijzer P., Kennison J.A., and Karch F. Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev. 16 (2002) 2621-2626
39. Narita M., Nunez S., Heard E., Lin A.W., Hearn S.A., Spector D.L., Hannon G.J., and Lowe S.W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113 (2003) 703-716
40. Narita M., Narita M., Krizhanovsky V., Nunez S., Chicas A., Hearn S.A., Myers M.P., and Lowe S.W. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 126 (2006) 503-514
41. Palmer T.D., Schwartz P.H., Taupin P., Kaspar B., Stein S.A., and Gage F.H. Cell culture. Progenitor cells from human brain after death. Nature 411 (2001) 42-43
42. Phelps-Durr T.L., Thomas J., Vahab P., and Timmermans M.C. Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17 (2005) 2886-2898
43. Polesskaya A., Seale P., and Rudnicki M.A. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113 (2003) 841-852
44. Ramirez R.D., Morales C.P., Herbert B.S., Rohde J.M., Passons C., Shay J.W., and Wright W.E. Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev. 15 (2001) 398-403
45. Reya T., and Clevers H. Wnt signalling in stem cells and cancer. Nature 434 (2005) 843-850
46. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., Hintz L., Nusse R., and Weissman I.L. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423 (2003) 409-414
47. Salomoni P., and Pandolfi P.P. The role of PML in tumor suppression. Cell 108 (2002) 165-170
48. Serrano M., Lin A.W., McCurrach M.E., Beach D., and Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88 (1997) 593-602
49. Sharp J.A., Fouts E.T., Krawitz D.C., and Kaufman P.D. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11 (2001) 463-473
50. Sherwood P.W., Tsang S.V., and Osley M.A. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13 (1993) 28-38
51. Singer M.S., Kahana A., Wolf A.J., Meisinger L.L., Peterson S.E., Goggin C., Mahowald M., and Gottschling D.E. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150 (1998) 613-632
52. Suzuki H., Watkins D.N., Jair K.W., Schuebel K.E., Markowitz S.D., Chen W.D., Pretlow T.P., Yang B., Akiyama Y., Van Engeland M., et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat. Genet. 36 (2004) 417-422
53. Tagami H., Ray-Gallet D., Almouzni G., and Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116 (2004) 51-61
54. Tang Y., Poustovoitov M.V., Zhao K., Garfinkel M., Canutescu A., Dunbrack R., Adams P.D., and Marmorstein R. Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat. Struct. Mol. Biol. 13 (2006) 921-929
55. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., and Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 (1999) 555-560
56. van der Heijden G.W., Derijck A.A., Posfai E., Giele M., Pelczar P., Ramos L., Wansink D.G., van der Vlag J., Peters A.H., and de Boer P. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat. Genet. 39 (2007) 251-258
57. Vider B.Z., Zimber A., Chastre E., Prevot S., Gespach C., Estlein D., Wolloch Y., Tronick S.R., Gazit A., and Yaniv A. Evidence for the involvement of the Wnt 2 gene in human colorectal cancer. Oncogene 12 (1996) 153-158
58. Willert K., Brown J.D., Danenberg E., Duncan A.W., Weissman I.L., Reya T., Yates III J.R., and Nusse R. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423 (2003) 448-452
59. Ye X., Zerlanko B., Zhang R., Somaiah N., Lipinski M., and Adams P.D. Definition of pRB- and p53-dependent and independent steps in HIRA/ASF1a-mediated formation of senecence-associated heterochromatin foci. Mol. Cell. Biol. 27 (2007) 2452-2465
60. Yoshida O., Habuchi T., and Ogawa O. Recent advances in the molecular genetics of urogenital tumors. Int. J. Urol. 1 (1994) 1-16
61. Young C.S., Kitamura M., Hardy S., and Kitajewski J. Wnt-1 induces growth, cytosolic beta-catenin, and Tcf/Lef transcriptional activation in Rat-1 fibroblasts. Mol. Cell. Biol. 18 (1998) 2474-2485
62. Zhang R., Poustovoitov M.V., Ye X., Santos H.A., Chen W., Daganzo S.M., Erzberger J.P., Serebriiskii I.G., Canutescu A.A., Dunbrack R.L., et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 8 (2005) 19-30
63. Zhang R., Chen W., and Adams P.D. Molecular dissection of formation of senescent associated heterochromatin foci. Mol. Cell. Biol. 27 (2007) 2343-2358
64. Zhang R., Liu S.-T., Chen W., Bonner B., Pehrson J., Yen T.J., and Adams P.D. HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol. Cell. Biol. 27 (2007) 949-962
65. Zmijewski J.W., and Jope R.S. Nuclear accumulation of glycogen synthase kinase-3 during replicative senescence of human fibroblasts. Aging Cell 3 (2004) 309-317