Cellular stress induces Bax-regulated nuclear bubble budding and rupture followed by nuclear protein release

References

• Walde S, Kehlenbach RH. The Part and the Whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol 2010; 20:461-9; PMID:20627572; http://dx.doi.org/10.1016/j.tcb.2010.05.001.
   PubMed Web of Science ®Google Scholar
• Wente SR, Rout MP. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2010; 2:a000562; PMID:20630994; http://dx.doi.org/10.1101/cshperspect.a000562.
   PubMed Web of Science ®Google Scholar
• Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar DZ, Barkan R, Meshorer E, Gruenbaum Y. Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 2009; 13:1059-85; PMID:19210577; http://dx.doi.org/10.1111/j.1582-4934.2008.00676.x.
   PubMed Web of Science ®Google Scholar
• Bank EM, Gruenbaum Y. The nuclear lamina and heterochromatin: a complex relationship. Biochem Soc Trans 2011; 39:1705-9; PMID:22103511; http://dx.doi.org/10.1042/BST20110603.
   PubMed Web of Science ®Google Scholar
• Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006; 86:967-1008; PMID:16816143; http://dx.doi.org/10.1152/physrev.00047.2005.
   PubMed Web of Science ®Google Scholar
• Wilson KL, Foisner R. Lamin-binding Proteins. Cold Spring Harb Perspect Biol 2010; 2:a000554; PMID:20452940; http://dx.doi.org/10.1101/cshperspect.a000554.
   PubMed Web of Science ®Google Scholar
• Pop C, Salvesen GS. Human caspases: activation, specificity, and regulation. J Biol Chem 2009; 284:21777-81; PMID:19473994; http://dx.doi.org/10.1074/jbc.R800084200.
   PubMed Web of Science ®Google Scholar
• Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9:47-59; PMID:18097445; http://dx.doi.org/10.1038/nrm2308.
   PubMed Web of Science ®Google Scholar
• Ferrando-May E. Nucleocytoplasmic transport in apoptosis. Cell Death Differ 2005; 12:1263-76; PMID:15861192; http://dx.doi.org/10.1038/sj.cdd.4401626.
   PubMed Web of Science ®Google Scholar
• Lindenboim L, Borner C, Stein R. Nuclear proteins acting on mitochondria. Biochim Biophys Acta 2011; 1813:584-96; PMID:21130123; http://dx.doi.org/10.1016/j.bbamcr.2010.11.016.
   PubMedGoogle Scholar
• Ferrando-May E, Cordes V, Biller-Ckovric I, Mirkovic J, Gorlich D, Nicotera P. Caspases mediate nucleoporin cleavage, but not early redistribution of nuclear transport factors and modulation of nuclear permeability in apoptosis. Cell Death Differ 2001; 8:495-505; PMID:11423910; http://dx.doi.org/10.1038/sj.cdd.4400837.
   PubMed Web of Science ®Google Scholar
• Patre M, Tabbert A, Hermann D, Walczak H, Rackwitz HR, Cordes VC, Ferrando-May E. Caspases target only two architectural components within the core structure of the nuclear pore complex. J Biol Chem 2006; 281:1296-304; PMID:16286466; http://dx.doi.org/10.1074/jbc.M511717200.
   PubMed Web of Science ®Google Scholar
• Faleiro L, Lazebnik Y. Caspases disrupt the nuclear-cytoplasmic barrier. J Cell Biol 2000; 151:951-9; PMID:11085998; http://dx.doi.org/10.1083/jcb.151.5.951.
   PubMed Web of Science ®Google Scholar
• Kihlmark M, Imreh G, Hallberg E. Sequential degradation of proteins from the nuclear envelope during apoptosis. J Cell Sci 2001; 114:3643-53; PMID:11707516.
   PubMed Web of Science ®Google Scholar
• Buendia B, Santa-Maria A, Courvalin JC. Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis. J Cell Sci 1999; 112 1743-53; PMID:10318766.
   PubMed Web of Science ®Google Scholar
• Bano D, Dinsdale D, Cabrera-Socorro A, Maida S, Lambacher N, McColl B, Ferrando-May E, Hengartner MO, Nicotera P. Alteration of the nuclear pore complex in Ca(2+)-mediated cell death. Cell Death Differ 2010; 17:119-33; PMID:19713973; http://dx.doi.org/10.1038/cdd.2009.112.
   PubMed Web of Science ®Google Scholar
• Lindenboim L, Blacher E, Borner C, Stein R. Regulation of stress-induced nuclear protein redistribution: a new function of Bax and Bak uncoupled from Bcl-x(L). Cell Death Differ 2010; 17:346-59; PMID:19816507; http://dx.doi.org/10.1038/cdd.2009.145.
   PubMed Web of Science ®Google Scholar
• Lindenboim L, Ferrando-May E, Borner C, Stein R. Non-canonical function of Bax in stress-induced nuclear protein redistribution. Cell Mol Life Sci 2013; 70:3013-27; PMID:23475110; http://dx.doi.org/10.1007/s00018-013-1306-4.
   PubMedGoogle Scholar
• Zhou H, Hou Q, Chai Y, Hsu YT. Distinct domains of Bcl-XL are involved in Bax and Bad antagonism and in apoptosis inhibition. Exp Cell Res 2005; 309:316-28; PMID:16061221; http://dx.doi.org/10.1016/j.yexcr.2005.06.014.
   PubMedGoogle Scholar
• Borner C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003; 39:615-47; PMID:12493639; http://dx.doi.org/10.1016/S0161-5890(02)00252-3.
   PubMed Web of Science ®Google Scholar
• George NM, Evans JJD, Luo X. A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Gene Dev 2007; 21:1937-48; PMID:17671092; http://dx.doi.org/10.1101/gad.1553607.
   PubMed Web of Science ®Google Scholar
• Heimlich G, McKinnon AD, Bernardo K, Brdiczka D, Reed JC, Kain R, Kronke M, Jurgensmeier JM. Bax-induced cytochrome c release from mitochondria depends on α-helices-5 and -6. Biochem J 2004; 378:247-55; PMID:14614769; http://dx.doi.org/10.1042/BJ20031152.
   PubMed Web of Science ®Google Scholar
• Minn AJ, Kettlun CS, Liang H, Kelekar A, Vander Heiden MG, Chang BS, Fesik SW, Fill M, Thompson CB. Bcl-xL regulates apoptosis by heterodimerization-dependent and -independent mechanisms. EMBO J 1999; 18:632-43; PMID:9927423; http://dx.doi.org/10.1093/emboj/18.3.632.
   PubMed Web of Science ®Google Scholar
• Gajkowska B, Motyl T, Olszewska-Badarczuk H, Godlewski MM. Expression of BAX in cell nucleus after experimentally induced apoptosis revealed by immunogold and embedment-free electron microscopy. Cell Biol Int 2001; 25:725-33; PMID:11482896; http://dx.doi.org/10.1006/cbir.2001.0768.
   PubMedGoogle Scholar
• Gajkowska B, Wojewodzka U, Gajda J. Translocation of Bax and Bid to mitochondria, endoplasmic reticulum and nuclear envelope: possible control points in apoptosis. J Mol Histol 2004; 35:11-9; PMID:15323345; http://dx.doi.org/10.1023/B:HIJO.0000020900.86650.89.
   PubMed Web of Science ®Google Scholar
• Ostlund C, Sullivan T, Stewart CL, Worman HJ. Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 2006; 45:1374-82; PMID:16445279; http://dx.doi.org/10.1021/bi052156n.
   PubMedGoogle Scholar
• Folker ES, Ostlund C, Luxton GW, Worman HJ, Gundersen GG. Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc Natl Acad Sci USA 2011; 108:131-6; PMID:21173262; http://dx.doi.org/10.1073/pnas.1000824108.
   PubMed Web of Science ®Google Scholar
• Östlund C, Bonne G, Schwartz K, Worman HJ. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J Cell Sci 2001; 114:4435-45.
   PubMed Web of Science ®Google Scholar
• Ruchaud S, Korfali N, Villa P, Kottke TJ, Dingwall C, Kaufmann SH, Earnshaw WC. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J 2002; 21:1967-77; PMID:11953316; http://dx.doi.org/10.1093/emboj/21.8.1967.
   PubMed Web of Science ®Google Scholar
• Konishi A, Shimizu S, Hirota J, Takao T, Fan Y, Matsuoka Y, Zhang L, Yoneda Y, Fujii Y, Skoultchi AI, et al. Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 2003; 114:673-88; PMID:14505568; http://dx.doi.org/10.1016/S0092-8674(03)00719-0.
   PubMed Web of Science ®Google Scholar
• Lenz-Bohme B, Wismar J, Fuchs S, Reifegerste R, Buchner E, Betz H, Schmitt B. Insertional mutation of the Drosophila nuclear lamin Dm0 gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J Cell Biol 1997; 137:1001-16; PMID:9166402; http://dx.doi.org/10.1083/jcb.137.5.1001.
   PubMed Web of Science ®Google Scholar
• Liu J, Rolef Ben-Shahar T, Riemer D, Treinin M, Spann P, Weber K, Fire A, Gruenbaum Y. Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 2000; 11:3937-47; PMID:11071918; http://dx.doi.org/10.1091/mbc.11.11.3937.
   PubMed Web of Science ®Google Scholar
• Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 1999; 147:913-20; PMID:10579712; http://dx.doi.org/10.1083/jcb.147.5.913.
   PubMed Web of Science ®Google Scholar
• Vergnes L, Peterfy M, Bergo MO, Young SG, Reue K. Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA 2004; 101:10428-33; PMID:15232008; http://dx.doi.org/10.1073/pnas.0401424101.
   PubMed Web of Science ®Google Scholar
• De Vos WH, Houben F, Kamps M, Malhas A, Verheyen F, Cox J, Manders EM, Verstraeten VL, van Steensel MA, Marcelis CL, et al. Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum Mol Genet 2011; 20:4175-86; PMID:21831885; http://dx.doi.org/10.1093/hmg/ddr344.
   PubMed Web of Science ®Google Scholar
• Zwerger M, Kolb T, Richter K, Karakesisoglou I, Herrmann H. Induction of a massive endoplasmic reticulum and perinuclear space expansion by expression of lamin B receptor mutants and the related sterol reductases TM7SF2 and DHCR7. Mol Biol Cell 2010; 21:354-68; PMID:19940018; http://dx.doi.org/10.1091/mbc.E09-08-0739.
   PubMed Web of Science ®Google Scholar
• de Noronha CM, Sherman MP, Lin HW, Cavrois MV, Moir RD, Goldman RD, Greene WC. Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science 2001; 294:1105-8; PMID:11691994; http://dx.doi.org/10.1126/science.1063957.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang YT, Li Q, et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012; 149:832-46; PMID:22579286; http://dx.doi.org/10.1016/j.cell.2012.03.032.
   PubMed Web of Science ®Google Scholar
• Heald R, McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 1990; 61:579-89; PMID:2344612; http://dx.doi.org/10.1016/0092-8674(90)90470-Y.
   PubMed Web of Science ®Google Scholar
• Wan KF, Chan SL, Sukumaran SK, Lee MC, Yu VC. Chelerythrine induces apoptosis through a Bax/Bak-independent mitochondrial mechanism. J Biol Chem 2008; 283:8423-33; PMID:18230621; http://dx.doi.org/10.1074/jbc.M707687200.
   PubMed Web of Science ®Google Scholar
• Hoetelmans R, van Slooten HJ, Keijzer R, Erkeland S, van de Velde CJ, Dierendonck JH. Bcl-2 and Bax proteins are present in interphase nuclei of mammalian cells. Cell Death Differ 2000; 7:384-92; PMID:10773823; http://dx.doi.org/10.1038/sj.cdd.4400664.
   PubMed Web of Science ®Google Scholar
• Hoetelmans RW. Nuclear partners of Bcl-2: Bax and PML. DNA Cell Biol 2004; 23:351-4; PMID:15231068; http://dx.doi.org/10.1089/104454904323145236.
   PubMed Web of Science ®Google Scholar
• Gajkowska B, Motyl T, Olszewska-Badarczuk H, Gniadecki R, Koronkiewicz M. Structural association of Bax with nuclear matrix and cytomatrix revealed by embedment-free immunogold electron microscopy. Cell Biol Int 2000; 24:649-56; PMID:10964454; http://dx.doi.org/10.1006/cbir.2000.0530.
   PubMed Web of Science ®Google Scholar
• Mandal M, Adam L, Mendelsohn J, Kumar R. Nuclear targeting of Bax during apoptosis in human colorectal cancer cells. Oncogene 1998; 17:999-1007; PMID:9747879; http://dx.doi.org/10.1038/sj.onc.1202020.
   PubMed Web of Science ®Google Scholar
• Wang X, Olberding KE, White C, Li C. Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ 2011; 18:38-47; PMID:20539308; http://dx.doi.org/10.1038/cdd.2010.68.
   PubMed Web of Science ®Google Scholar
• Tzur YB, Margalit A, Melamed-Book N, Gruenbaum Y. Matefin/SUN-1 is a nuclear envelope receptor for CED-4 during Caenorhabditis elegans apoptosis. Proc Natl Acad Sci USA 2006; 103:13397-402.
   Google Scholar
• Kerr LE, Birse-Archbold JL, Short DM, McGregor AL, Heron I, Macdonald DC, Thompson J, Carlson GJ, Kelly JS, McCulloch J, et al. Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene 2007; 26:2554-62; PMID:17072349; http://dx.doi.org/10.1038/sj.onc.1210044.
   PubMed Web of Science ®Google Scholar
• Schinzel A, Kaufmann T, Schuler M, Martinalbo J, Grubb D, Borner C. Conformational control of Bax localization and apoptotic activity by Pro168. J Cell Biol 2004; 164:1021-32; PMID:15037603; http://dx.doi.org/10.1083/jcb.200309013.
   PubMed Web of Science ®Google Scholar
• Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C. Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 2003; 160:53-64; PMID:12515824; http://dx.doi.org/10.1083/jcb.200210084.
   PubMed Web of Science ®Google Scholar
• George NM, Targy N, Evans JJ, Zhang L, Luo X. Bax contains two functional mitochondrial targeting sequences and translocates to mitochondria in a conformational change- and homo-oligomerization-driven process. J Biol Chem 2010; 285:1384-92; PMID:19880508; http://dx.doi.org/10.1074/jbc.M109.049924.
   PubMedGoogle Scholar
• Ostlund C, Folker ES, Choi JC, Gomes ER, Gundersen GG, Worman HJ. Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci 2009; 122:4099-108; PMID:19843581; http://dx.doi.org/10.1242/jcs.057075.
   PubMed Web of Science ®Google Scholar
• Di Segni A, Farin K, Pinkas-Kramarski R. Identification of nucleolin as new ErbB receptors- interacting protein. PloS One 2008; 3:e2310; PMID:18523588; http://dx.doi.org/10.1371/journal.pone.0002310.
   PubMed Web of Science ®Google Scholar
• Farin K, Di Segni A, Mor A, Pinkas-Kramarski R. Structure-function analysis of nucleolin and ErbB receptors interactions. PloS One 2009; 4:e6128; PMID:19578540; http://dx.doi.org/10.1371/journal.pone.0006128.
   PubMed Web of Science ®Google Scholar
• Vos JC, Reits EA, Wojcik-Jacobs E, Neefjes J. Head-head/tail-tail relative orientation of the pore-forming domains of the heterodimeric ABC transporter TAP. Curr Biol 2000; 10:1-7; PMID:10660295; http://dx.doi.org/10.1016/S0960-9822(99)00257-2.
   PubMedGoogle Scholar
• Lindenboim L, Kringel S, Braun T, Borner C, Stein R. Bak but not Bax is essential for Bcl-xS-induced apoptosis. Cell Death Differ 2005; 12:713-23; PMID:15861188; http://dx.doi.org/10.1038/sj.cdd.4401638.
   PubMedGoogle Scholar