A novel, non-apoptotic role for Scythe/BAT3: A functional switch between the pro- and anti-proliferative roles of p21 during the cell cycle

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Yong, Sheila T ^a,b   Wang, Xiao Fan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIN A; CYCLIN DEPENDENT KINASE 2; NOCODAZOLE; PROTEIN BAT3; PROTEIN P21; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL CYCLE CHECKPOINT; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; DOWN REGULATION; HUMAN; HUMAN CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

APOPTOSIS; BLOTTING, WESTERN; BONE NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA REPLICATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MOLECULAR CHAPERONES; OSTEOSARCOMA; PHOSPHORYLATION; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84862983395     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038085     Document Type: Article

References (67)

1. Kabbage M, Dickman MB, (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65: 1390-1402.
2. Takayama S, Reed JC, (2001) Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 3: E237-241.
3. Minami R, Hayakawa A, Kagawa H, Yanagi Y, Yokosawa H, et al. (2010) BAG-6 is essential for selective elimination of defective proteasomal substrates. J Cell Biol 190: 637-650.
4. Sasaki T, Gan EC, Wakeham A, Kornbluth S, Mak TW, et al. (2007) HLA-B-associated transcript 3 (Bat3)/Scythe is essential for p300-mediated acetylation of p53. Genes Dev 21: 848-861.
5. Desmots F, Russell HR, Michel D, McKinnon PJ, (2008) Scythe regulates apoptosis-inducing factor stability during endoplasmic reticulum stress-induced apoptosis. J Biol Chem 283: 3264-3271.
6. Corduan A, Lecomte S, Martin C, Michel D, Desmots F, (2009) Sequential interplay between BAG6 and HSP70 upon heat shock. Cell Mol Life Sci 66: 1998-2004.
7. Sasaki T, Marcon E, McQuire T, Arai Y, Moens PB, et al. (2008) Bat3 deficiency accelerates the degradation of Hsp70-2/HspA2 during spermatogenesis. J Cell Biol 182: 449-458.
8. Desmots F, Russell HR, Lee Y, Boyd K, McKinnon PJ, (2005) The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol Cell Biol 25: 10329-10337.
9. Vermeulen K, Van Bockstaele DR, Berneman ZN, (2003) The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 36: 131-149.
10. Israels ED, Israels LG, (2001) The cell cycle. Stem Cells 19: 88-91.
11. Blundell R, Harrison DJ, O'Dea S, (2004) p21(Waf1/Cip1) regulates proliferation and apoptosis in airway epithelial cells and alternative forms have altered binding activities. Exp Lung Res 30: 447-464.
12. Child ES, Mann DJ, (2006) The intricacies of p21 phosphorylation: protein/protein interactions, subcellular localization and stability. Cell Cycle 5: 1313-1319.
13. Han Z, Wei W, Dunaway S, Darnowski JW, Calabresi P, et al. (2002) Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin. J Biol Chem 277: 17154-17160.
14. Van Nguyen T, Puebla-Osorio N, Pang H, Dujka ME, Zhu C, (2007) DNA damage-induced cellular senescence is sufficient to suppress tumorigenesis: a mouse model. J Exp Med 204: 1453-1461.
15. Di Leonardo A, Linke SP, Clarkin K, Wahl GM, (1994) DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev 8: 2540-2551.
16. te Poele RH, Okorokov AL, Jardine L, Cummings J, Joel SP, (2002) DNA damage is able to induce senescence in tumor cells in vitro and in vivo. Cancer Res 62: 1876-1883.
17. Amador V, Ge S, Santamaria PG, Guardavaccaro D, Pagano M, (2007) APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol Cell 27: 462-473.
18. Abbas T, Sivaprasad U, Terai K, Amador V, Pagano M, et al. (2008) PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev 22: 2496-2506.
19. Kim Y, Starostina NG, Kipreos ET, (2008) The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev 22: 2507-2519.
20. Bornstein G, Bloom J, Sitry-Shevah D, Nakayama K, Pagano M, et al. (2003) Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J Biol Chem 278: 25752-25757.
21. Bloom J, Amador V, Bartolini F, DeMartino G, Pagano M, (2003) Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115: 71-82.
22. LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, et al. (1997) New functional activities for the p21 family of CDK inhibitors. Genes Dev 11: 847-862.
23. Dash BC, El-Deiry WS, (2005) Phosphorylation of p21 in G2/M promotes cyclin B-Cdc2 kinase activity. Mol Cell Biol 25: 3364-3387.
24. Wakeman TP, Wang Q, Feng J, Wang XF, (2012) Bat3 facilitates H3K79 dimethylation by DOT1L and promotes DNA damage-induced 53BP1 foci at G1/G2 cell-cycle phases. Embo J 31: 2169-2181.
25. Dulic V, Stein GH, Far DF, Reed SI, (1998) Nuclear accumulation of p21Cip1 at the onset of mitosis: a role at the G2/M-phase transition. Mol Cell Biol 18: 546-557.
26. Hengst L, Gopfert U, Lashuel HA, Reed SI, (1998) Complete inhibition of Cdk/cyclin by one molecule of p21(Cip1). Genes Dev 12: 3882-3888.
27. Thress K, Henzel W, Shillinglaw W, Kornbluth S, (1998) Scythe: a novel reaper-binding apoptotic regulator. EMBO J 17: 6135-6143.
28. Thress K, Evans EK, Kornbluth S, (1999) Reaper-induced dissociation of a Scythe-sequestered cytochrome c-releasing activity. Embo J 18: 5486-5493.
29. Wu YH, Shih SF, Lin JY, (2004) Ricin triggers apoptotic morphological changes through caspase-3 cleavage of BAT3. J Biol Chem 279: 19264-19275.
30. Preta G, Fadeel B, (2012) Scythe cleavage during Fas (APO-1)-and staurosporine-mediated apoptosis. FEBS Lett.
31. Funk JO, Waga S, Harry JB, Espling E, Stillman B, et al. (1997) Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev 11: 2090-2100.
32. Li R, Hannon GJ, Beach D, Stillman B, (1996) Subcellular distribution of p21 and PCNA in normal and repair-deficient cells following DNA damage. Curr Biol 6: 189-199.
33. Waga S, Hannon GJ, Beach D, Stillman B, (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369: 574-578.
34. Wang W, Nacusi L, Sheaff RJ, Liu X, (2005) Ubiquitination of p21Cip1/WAF1 by SCFSkp2: substrate requirement and ubiquitination site selection. Biochemistry 44: 14553-14564.
35. Jin Y, Lee H, Zeng SX, Dai MS, Lu H, (2003) MDM2 promotes p21waf1/cip1 proteasomal turnover independently of ubiquitylation. Embo J 22: 6365-6377.
36. Wang B, Liu K, Lin HY, Bellam N, Ling S, et al. (2010) 14-3-3Tau regulates ubiquitin-independent proteasomal degradation of p21, a novel mechanism of p21 downregulation in breast cancer. Mol Cell Biol 30: 1508-1527.
37. Blundell R, Kaminski N, Harrison D, (2004) Increase in p21 expression independent of the p53 pathway in bleomycin-induced lung fibrosis. Exp Mol Pathol 77: 231-237.
38. Dumaz N, Meek DW, (1999) Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J 18: 7002-7010.
39. Shieh SY, Ikeda M, Taya Y, Prives C, (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
40. Sheaff RJ, Singer JD, Swanger J, Smitherman M, Roberts JM, et al. (2000) Proteasomal turnover of p21Cip1 does not require p21Cip1 ubiquitination. Mol Cell 5: 403-410.
41. Touitou R, Richardson J, Bose S, Nakanishi M, Rivett J, et al. (2001) A degradation signal located in the C-terminus of p21WAF1/CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. Embo J 20: 2367-2375.
42. Vinayagam A, Stelzl U, Foulle R, Plassmann S, Zenkner M, et al. (2011) A directed protein interaction network for investigating intracellular signal transduction. Sci Signal 4: rs8.
43. Alt JR, Gladden AB, Diehl JA, (2002) p21(Cip1) Promotes cyclin D1 nuclear accumulation via direct inhibition of nuclear export. J Biol Chem 277: 8517-8523.
44. Hwang CY, Lee C, Kwon KS, (2009) Extracellular signal-regulated kinase 2-dependent phosphorylation induces cytoplasmic localization and degradation of p21Cip1. Mol Cell Biol 29: 3379-3389.
45. Rossig L, Badorff C, Holzmann Y, Zeiher AM, Dimmeler S, (2002) Glycogen synthase kinase-3 couples AKT-dependent signaling to the regulation of p21Cip1 degradation. J Biol Chem 277: 9684-9689.
46. Yamada K, Tamamori-Adachi M, Goto I, Iizuka M, Yasukawa T, et al. (2011) Degradation of p21Cip1 through anaphase-promoting complex/cyclosome and its activator Cdc20 (APC/CCdc20) ubiquitin ligase complex-mediated ubiquitylation is inhibited by cyclin-dependent kinase 2 in cardiomyocytes. J Biol Chem 286: 44057-44066.
47. Zhou BP, Liao Y, Xia W, Spohn B, Lee MH, et al. (2001) Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat Cell Biol 3: 245-252.
48. Dong Y, Chi SL, Borowsky AD, Fan Y, Weiss RH, (2004) Cytosolic p21Waf1/Cip1 increases cell cycle transit in vascular smooth muscle cells. Cell Signal 16: 263-269.
49. Coqueret O, (2003) New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol 13: 65-70.
50. Manchen ST, (2002) Characterization and subcellular localization of the human BAT3 protein. Ottawa: National Library of Canada = Bibliothèque nationale du Canada.
51. Kaye FJ, Modi S, Ivanovska I, Koonin EV, Thress K, et al. (2000) A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. FEBS Lett 467: 348-355.
52. Biggins S, Ivanovska I, Rose MD, (1996) Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. J Cell Biol 133: 1331-1346.
53. Winnefeld M, Grewenig A, Schnolzer M, Spring H, Knoch TA, et al. (2006) Human SGT interacts with Bag-6/Bat-3/Scythe and cells with reduced levels of either protein display persistence of few misaligned chromosomes and mitotic arrest. Exp Cell Res 312: 2500-2514.
54. Townsend PA, Cutress RI, Sharp A, Brimmell M, Packham G, (2003) BAG-1 prevents stress-induced long-term growth inhibition in breast cancer cells via a chaperone-dependent pathway. Cancer Res 63: 4150-4157.
55. Yamauchi H, Adachi M, Sakata K, Hareyama M, Satoh M, et al. (2001) Nuclear BAG-1 localization and the risk of recurrence after radiation therapy in laryngeal carcinomas. Cancer Lett 165: 103-110.
56. Zheng HC, Xu XY, Xing YN, Wei ZL, Takahashi H, et al. (2010) Nuclear or cytoplasmic localization of Bag-1 distinctly correlates with pathologic behavior and outcome of gastric carcinomas. Hum Pathol 41: 724-736.
57. Zeiner M, Niyaz Y, Gehring U, (1999) The hsp70-associating protein Hap46 binds to DNA and stimulates transcription. Proc Natl Acad Sci U S A 96: 10194-10199.
58. Gamerdinger M, Kaya AM, Wolfrum U, Clement AM, Behl C, (2010) BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep 12: 149-156.
59. Kyratsous CA, Silverstein SJ, (2008) The co-chaperone BAG3 regulates Herpes Simplex Virus replication. Proc Natl Acad Sci U S A 105: 20912-20917.
60. Carrettiero DC, Hernandez I, Neveu P, Papagiannakopoulos T, Kosik KS, (2009) The cochaperone BAG2 sweeps paired helical filament- insoluble tau from the microtubule. J Neurosci 29: 2151-2161.
61. Tsukahara T, Kimura S, Ichimiya S, Torigoe T, Kawaguchi S, et al. (2009) Scythe/BAT3 regulates apoptotic cell death induced by papillomavirus binding factor in human osteosarcoma. Cancer Sci 100: 47-53.
62. Manchen ST, Hubberstey AV, (2001) Human Scythe contains a functional nuclear localization sequence and remains in the nucleus during staurosporine-induced apoptosis. Biochem Biophys Res Commun 287: 1075-1082.
63. Wang Y, Broderick P, Webb E, Wu X, Vijayakrishnan J, et al. (2008) Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat Genet 40: 1407-1409.
64. Rudd MF, Webb EL, Matakidou A, Sellick GS, Williams RD, et al. (2006) Variants in the GH-IGF axis confer susceptibility to lung cancer. Genome Res 16: 693-701.
65. Ter-Minassian M, Zhai R, Asomaning K, Su L, Zhou W, et al. (2008) Apoptosis gene polymorphisms, age, smoking and the risk of non-small cell lung cancer. Carcinogenesis 29: 2147-2152.
66. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, et al. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
67. Waddell DS, Liberati NT, Guo X, Frederick JP, Wang XF, (2004) Casein kinase Iepsilon plays a functional role in the transforming growth factor-beta signaling pathway. J Biol Chem 279: 29236-29246.