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Macromolecular crowding effect is critical for maintaining SIRT1's nuclear localization in cancer cells

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Pages 2647-2655 | Received 04 May 2016, Accepted 01 Jul 2016, Published online: 10 Sep 2016

References

  • Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000; 403:795-800; PMID:10693811; http://dx.doi.org/10.1038/35001622
  • Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P, Reinberg D. Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol Cell 2004; 16:93-105; PMID:15469825; http://dx.doi.org/10.1016/j.molcel.2004.08.031
  • Martinez-Redondo P, Vaquero A. The diversity of histone versus nonhistone sirtuin substrates. Genes Cancer 2013; 4:148-63; PMID:24020006; http://dx.doi.org/10.1177/1947601913483767
  • Bosch-Presegue L, Vaquero A. The dual role of sirtuins in cancer. Genes Cancer 2011; 2:648-62; PMID:21941620; http://dx.doi.org/10.1177/1947601911417862
  • Liu T, Liu PY, Marshall GM. The critical role of the class III histone deacetylase SIRT1 in cancer. Cancer Res 2009; 69:1702-5; PMID:19244112; http://dx.doi.org/10.1158/0008-5472.CAN-08-3365
  • Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, Shimohama S, Sato M, Horio Y. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci U S A 2008; 105:15599-604; PMID:18829436; http://dx.doi.org/10.1073/pnas.0800612105
  • Hou J, Chong ZZ, Shang YC, Maiese K. Early apoptotic vascular signaling is determined by Sirt1 through nuclear shuttling, forkhead trafficking, bad, and mitochondrial caspase activation. Curr Neurovasc Res 2010; 7:95-112; PMID:20370652; http://dx.doi.org/10.2174/156720210791184899
  • Maloney SC, Antecka E, Odashiro AN, Fernandes BF, Doyle M, Lim LA, Katib Y, Burnier MN Jr. Expression of SIRT1 and DBC1 in developing and adult retinas. Stem Cells Int 2012; 2012:908183; PMID:22969813; http://dx.doi.org/10.1155/2012/908183
  • Tanno M, Kuno A, Yano T, Miura T, Hisahara S, Ishikawa S, Shimamoto K, Horio Y. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem 2010; 285:8375-82; PMID:20089851; http://dx.doi.org/10.1074/jbc.M109.090266
  • Tong C, Morrison A, Mattison S, Qian S, Bryniarski M, Rankin B, Wang J, Thomas DP, Li J. Impaired SIRT1 nucleocytoplasmic shuttling in the senescent heart during ischemic stress. FASEB J 2013; 27:4332-42; PMID:23024374; http://dx.doi.org/10.1096/fj.12-216473
  • Tanno M, Sakamoto J, Miura T, Shimamoto K, Horio Y. Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1. J Biol Chem 2007; 282:6823-32; PMID:17197703; http://dx.doi.org/10.1074/jbc.M609554200
  • Ohsawa S, Miura M. Caspase-mediated changes in Sir2alpha during apoptosis. FEBS Lett 2006; 580:5875-9; PMID:17027980; http://dx.doi.org/10.1016/j.febslet.2006.09.051
  • Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, Guarente L, Weinberg RA. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 2001; 107:149-59; PMID:11672523; http://dx.doi.org/10.1016/S0092-8674(01)00527-X
  • Lin Z, Fang D. The Roles of SIRT1 in Cancer. Genes Cancer 2013; 4:97-104; PMID:24020000; http://dx.doi.org/10.1177/1947601912475079
  • Song NY, Surh YJ. Janus-faced role of SIRT1 in tumorigenesis. Ann N Y Acad Sci 2012; 1271:10-9; PMID:23050959; http://dx.doi.org/10.1111/j.1749-6632.2012.06762.x
  • Chen Y, Zhao W, Yang JS, Cheng Z, Luo H, Lu Z, Tan M, Gu W, Zhao Y. Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Mol Cell Proteomics 2012; 11:1048-62; PMID:22826441; http://dx.doi.org/10.1074/mcp.M112.019547
  • Andersen JL, Thompson JW, Lindblom KR, Johnson ES, Yang CS, Lilley LR, Freel CD, Moseley MA, Kornbluth S. A biotin switch-based proteomics approach identifies 14-3-3zeta as a target of Sirt1 in the metabolic regulation of caspase-2. Mol Cell 2011; 43:834-42; PMID:21884983; http://dx.doi.org/10.1016/j.molcel.2011.07.028
  • Byles V, Chmilewski LK, Wang J, Zhu L, Forman LW, Faller DV, Dai Y. Aberrant cytoplasm localization and protein stability of SIRT1 is regulated by PI3K/IGF-1R signaling in human cancer cells. Int J Biol Sci 2010; 6:599-612; PMID:20941378; http://dx.doi.org/10.7150/ijbs.6.599
  • Ghosh HS, McBurney M, Robbins PD. SIRT1 negatively regulates the mammalian target of rapamycin. PloS One 2010; 5:e9199; PMID:20169165; http://dx.doi.org/10.1371/journal.pone.0009199
  • Nakatani Y, Ogryzko V. Immunoaffinity purification of mammalian protein complexes. Methods Enzymol 2003; 370:430-44; PMID:14712665; http://dx.doi.org/10.1016/S0076-6879(03)70037-8
  • Yamamori T, DeRicco J, Naqvi A, Hoffman TA, Mattagajasingh I, Kasuno K, Jung SB, Kim CS, Irani K. SIRT1 deacetylates APE1 and regulates cellular base excision repair. Nucleic Acids Res 2010; 38:832-45; PMID:19934257; http://dx.doi.org/10.1093/nar/gkp1039
  • Zhang J. The direct involvement of SirT1 in insulin-induced insulin receptor substrate-2 tyrosine phosphorylation. J Biol Chem 2007; 282:34356-64; PMID:17901049; http://dx.doi.org/10.1074/jbc.M706644200
  • Menssen A, Hydbring P, Kapelle K, Vervoorts J, Diebold J, Luscher B, Larsson LG, Hermeking H. The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop. Proc Natl Acad Sci U S A 2012; 109:E187-96; PMID:22190494; http://dx.doi.org/10.1073/pnas.1105304109
  • Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 2005; 16:4623-35; PMID:16079181; http://dx.doi.org/10.1091/mbc.E05-01-0033
  • Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983; 11:1475-89; PMID:6828386; http://dx.doi.org/10.1093/nar/11.5.1475
  • Schreiber E, Matthias P, Muller MM, Schaffner W. Rapid detection of octamer binding proteins with ‘mini-extracts’, prepared from a small number of cells. Nucleic Acids Res 1989; 17:6419; PMID:2771659; http://dx.doi.org/10.1093/nar/17.15.6419
  • Chang Y, Sun L, Kokura K, Horton JR, Fukuda M, Espejo A, Izumi V, Koomen JM, Bedford MT, Zhang X, et al. MPP8 mediates the interactions between DNA methyltransferase Dnmt3a and H3K9 methyltransferase GLP/G9a. Nat Commun 2011; 2:533; PMID:22086334; http://dx.doi.org/10.1038/ncomms1549
  • Kokura K, Sun L, Bedford MT, Fang J. Methyl-H3K9-binding protein MPP8 mediates E-cadherin gene silencing and promotes tumour cell motility and invasion. EMBO J 2010; 29:3673-87; PMID:20871592; http://dx.doi.org/10.1038/emboj.2010.239
  • Schnell U, Dijk F, Sjollema KA, Giepmans BN. Immunolabeling artifacts and the need for live-cell imaging. Nat Methods 2012; 9:152-8; PMID:22290187; http://dx.doi.org/10.1038/nmeth.1855
  • Jiang SW, Eberhardt NL. A micro-scale method to isolate DNA-binding proteins suitable for quantitative comparison of expression levels from transfected cells. Nucleic Acids Res 1995; 23:3607-8; PMID:7567478; http://dx.doi.org/10.1093/nar/23.17.3607
  • Shiyanov P, Hayes SA, Donepudi M, Nichols AF, Linn S, Slagle BL, Raychaudhuri P. The naturally occurring mutants of DDB are impaired in stimulating nuclear import of the p125 subunit and E2F1-activated transcription. Mol Cell Biol 1999; 19:4935-43; PMID:10373543; http://dx.doi.org/10.1128/MCB.19.7.4935
  • Holden P, Horton WA. Crude subcellular fractionation of cultured mammalian cell lines. BMC Res Notes 2009; 2:243; PMID:20003239; http://dx.doi.org/10.1186/1756-0500-2-243
  • Liu X, Fagotto F. A method to separate nuclear, cytosolic, and membrane-associated signaling molecules in cultured cells. Sci Signal 2011; 4:pl2; PMID:22169476
  • Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K. REAP: A two minute cell fractionation method. BMC Res Notes 2010; 3:294; PMID:21067583; http://dx.doi.org/10.1186/1756-0500-3-294
  • Schulz I. Permeabilizing cells: some methods and applications for the study of intracellular processes. Methods Enzymol 1990; 192:280-300; PMID:2074793; http://dx.doi.org/10.1016/0076-6879(90)92077-Q
  • Adam SA, Marr RS, Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J Cell Biol 1990; 111:807-16; PMID:2391365; http://dx.doi.org/10.1083/jcb.111.3.807
  • Jin Q, Yan T, Ge X, Sun C, Shi X, Zhai Q. Cytoplasm-localized SIRT1 enhances apoptosis. J Cell Physiol 2007; 213:88-97; PMID:17516504; http://dx.doi.org/10.1002/jcp.21091
  • Rosania GR, Swanson JA. Effects of macromolecular crowding on nuclear size. Exp Cell Res 1995; 218:114-22; PMID:7537686; http://dx.doi.org/10.1006/excr.1995.1137
  • Hancock R, Hadj-Sahraoui Y. Isolation of cell nuclei using inert macromolecules to mimic the crowded cytoplasm. PloS one 2009; 4:e7560; PMID:19851505; http://dx.doi.org/10.1371/journal.pone.0007560
  • Lue NF, Kornberg RD. Accurate initiation at RNA polymerase II promoters in extracts from Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1987; 84:8839-43; PMID:3321057; http://dx.doi.org/10.1073/pnas.84.24.8839
  • Sun L, Kokura K, Izumi V, Koomen JM, Seto E, Chen J, Fang J. MPP8 and SIRT1 crosstalk in E-cadherin gene silencing and epithelial-mesenchymal transition. EMBO Rep 2015; 16:689-99; PMID:25870236; http://dx.doi.org/10.15252/embr.201439792
  • Giepmans BN, Adams SR, Ellisman MH, Tsien RY. The fluorescent toolbox for assessing protein location and function. Science (New York, NY) 2006; 312:217-24; PMID:16614209; http://dx.doi.org/10.1126/science.1124618
  • Conner MT, Conner AC, Bland CE, Taylor LH, Brown JE, Parri HR, Bill RM. Rapid aquaporin translocation regulates cellular water flow: mechanism of hypotonicity-induced subcellular localization of aquaporin 1 water channel. J Biol Chem 2012; 287:11516-25; PMID:22334691; http://dx.doi.org/10.1074/jbc.M111.329219
  • Pedersen S, Lambert IH, Thoroed SM, Hoffmann EK. Hypotonic cell swelling induces translocation of the alpha isoform of cytosolic phospholipase A2 but not the gamma isoform in Ehrlich ascites tumor cells. Eur J Biochem 2000; 267:5531-9; PMID:10951212; http://dx.doi.org/10.1046/j.1432-1327.2000.01615.x
  • Tamma G, Procino G, Strafino A, Bononi E, Meyer G, Paulmichl M, Formoso V, Svelto M, Valenti G. Hypotonicity induces aquaporin-2 internalization and cytosol-to-membrane translocation of ICln in renal cells. Endocrinology 2007; 148:1118-30; PMID:17138647; http://dx.doi.org/10.1210/en.2006-1277
  • Tong EH, Guo JJ, Huang AL, Liu H, Hu CD, Chung SS, Ko BC. Regulation of nucleocytoplasmic trafficking of transcription factor OREBP/TonEBP/NFAT5. J Biol Chem 2006; 281:23870-9; PMID:16782704; http://dx.doi.org/10.1074/jbc.M602556200
  • Xu S, Wong CC, Tong EH, Chung SS, Yates JR, 3rd, Yin Y, Ko BC. Phosphorylation by casein kinase 1 regulates tonicity-induced osmotic response element-binding protein/tonicity enhancer-binding protein nucleocytoplasmic trafficking. J Biol Chem 2008; 283:17624-34; PMID:18411282; http://dx.doi.org/10.1074/jbc.M800281200
  • Davis SK, Bardeen CJ. The connection between chromatin motion on the 100 nm length scale and core histone dynamics in live XTC-2 cells and isolated nuclei. Biophys J 2004; 86:555-64; PMID:14695300; http://dx.doi.org/10.1016/S0006-3495(04)74134-X
  • Kornberg A. Ten commandments: lessons from the enzymology of DNA replication. J Bacteriol 2000; 182:3613-8; PMID:10850972; http://dx.doi.org/10.1128/JB.182.13.3613-3618.2000
  • Hatch E, Hetzer M. Breaching the nuclear envelope in development and disease. J Cell Biol 2014; 205:133-41; PMID:24751535; http://dx.doi.org/10.1083/jcb.201402003
  • Vargas JD, Hatch EM, Anderson DJ, Hetzer MW. Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus 2012; 3:88-100; PMID:22567193; http://dx.doi.org/10.4161/nucl.18954
  • Dickmanns A, Kehlenbach RH, Fahrenkrog B. Nuclear pore complexes and nucleocytoplasmic transport: From structure to function to disease. Int Rev Cell Mol Biol 2015; 320:171-233; PMID:26614874; http://dx.doi.org/10.1016/bs.ircmb.2015.07.010
  • Denais CM, Gilbert RM, Isermann P, McGregor AL, Te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J. Nuclear envelope rupture and repair during cancer cell migration. Science (New York, NY) 2016; 352:353-8; PMID:27013428; http://dx.doi.org/10.1126/science.aad7297
  • Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Duménil AM, Manel N, et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science (New York, NY) 2016; 352:359-62; PMID:27013426; http://dx.doi.org/10.1126/science.aad7611
  • Ling H, Peng L, Seto E, Fukasawa K. Suppression of centrosome duplication and amplification by deacetylases. Cell Cycle (Georgetown, Tex) 2012; 11:3779-91; PMID:23022877; http://dx.doi.org/10.4161/cc.21985
  • Yuan Z, Zhang X, Sengupta N, Lane WS, Seto E. SIRT1 regulates the function of the Nijmegen breakage syndrome protein. Mol Cell 2007; 27:149-62; PMID:17612497; http://dx.doi.org/10.1016/j.molcel.2007.05.029
  • Leach C, Eto M, Brautigan DL. Domains of type 1 protein phosphatase inhibitor-2 required for nuclear and cytoplasmic localization in response to cell-cell contact. J Cell Sci 2002; 115:3739-45; PMID:12235284; http://dx.doi.org/10.1242/jcs.00052

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