1,943
Views
15
CrossRef citations to date
0
Altmetric
Report

Mutant lamin A links prophase to a p53 independent senescence program

, , , , &
Pages 2408-2421 | Received 08 Apr 2015, Accepted 16 May 2015, Published online: 30 Jun 2015

References

  • Tchkonia T, Zhu Y, van Deursen J, Campisi J, Kirkland JL. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J Clin Invest 2013; 123:966-72; PMID:23454759
  • Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, Kumar R, Jenkins RB, de Groen PC, Roche P, et al. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 2004; 36:744-9; PMID:15208629
  • Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011; 479:232-6; PMID:22048312; http://dx.doi.org/10.1038/nature10600
  • De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, et al. Lamin a truncation in Hutchinson-Gilford progeria. Science 2003; 300:2055; PMID:12702809; http://dx.doi.org/10.1126/science.1084125
  • Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, et al. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003; 423:293-8; PMID:12714972; http://dx.doi.org/10.1038/nature01629
  • Hennekam RC. Hutchinson-Gilford progeria syndrome: review of the phenotype. Am J Med Genet A 2006; 140:2603-24; PMID:16838330; http://dx.doi.org/10.1002/ajmg.a.31346
  • Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, Huang JD, Li KM, Chau PY, Chen DJ, et al. Genomic instability in laminopathy-based premature aging. Nat Med 2005; 11:780-5; PMID:15980864
  • Benson EK, Lee SW, Aaronson SA. Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J Cell Sci 2010; 123:2605-12; PMID:20605919
  • Krishnan V, Chow MZ, Wang Z, Zhang L, Liu B, Liu X, Zhou Z. Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc Natl Acad Sci U S A 2011; 108:12325-30; PMID:21746928
  • Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, Eriksson M, Goldman AE, Khuon S, Collins FS, et al. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci U S A 2006; 103:8703-8; PMID:16738054
  • Cao K, Capell BC, Erdos MR, Djabali K, Collins FS. A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc Natl Acad Sci U S A 2007; 104:4949-54; PMID:17360355
  • Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, et al. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 2004; 101:8963-8; PMID:15184648
  • 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
  • Glynn MW, Glover TW. Incomplete processing of mutant lamin A in Hutchinson-Gilford progeria leads to nuclear abnormalities, which are reversed by farnesyltransferase inhibition. Hum Mol Genet 2005; 14:2959-69; PMID:16126733
  • Shalev SA, De Sandre-Giovannoli A, Shani AA, Levy N. An association of Hutchinson-Gilford progeria and malignancy. Am J Med Genet A 2007; 143A:1821-6; PMID:17618517
  • Broers JL, Machiels BM, van Eys GJ, Kuijpers HJ, Manders EM, van Driel R, Ramaekers FC. Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J Cell Sci 1999; 112 ( Pt 20):3463-75; PMID:10504295
  • Peter M, Nakagawa J, Doree M, Labbe JC, Nigg EA. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 1990; 61:591-602; PMID:2188731; http://dx.doi.org/10.1016/0092-8674(90)90471-P
  • Peter M, Heitlinger E, Haner M, Aebi U, Nigg EA. Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. EMBO J 1991; 10:1535-44; PMID:1851086
  • 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
  • Hennekes H, Nigg EA. The role of isoprenylation in membrane attachment of nuclear lamins. A single point mutation prevents proteolytic cleavage of the lamin A precursor and confers membrane binding properties. J Cell Sci 1994; 107 ( Pt 4):1019-29; PMID:8056827
  • Mallampalli MP, Huyer G, Bendale P, Gelb MH, Michaelis S. Inhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 2005; 102:14416-21; PMID:16186497; http://dx.doi.org/10.1073/pnas.0503712102
  • Yang SH, Chang SY, Ren S, Wang Y, Andres DA, Spielmann HP, Fong LG, Young SG. Absence of progeria-like disease phenotypes in knock-in mice expressing a non-farnesylated version of progerin. Hum Mol Genet 2011; 20:436-44; PMID:21088111; http://dx.doi.org/10.1093/hmg/ddq490
  • Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K, et al. Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 2002; 31:94-9.; PMID:11923874
  • Barrowman J, Hamblet C, George CM, Michaelis S. Analysis of prelamin A biogenesis reveals the nucleus to be a CaaX processing compartment. Mol Biol Cell 2008; 19:5398-408; PMID:18923140; http://dx.doi.org/10.1091/mbc.E08-07-0704
  • Gruber J, Lampe T, Osborn M, Weber K. RNAi of FACE1 protease results in growth inhibition of human cells expressing lamin A: implications for Hutchinson-Gilford progeria syndrome. J Cell Sci 2005; 118:689-96; PMID:15671064; http://dx.doi.org/10.1242/jcs.01652
  • Akakura S, Nochajski P, Gao L, Sotomayor P, Matsui S, Gelman IH. Rb-dependent cellular senescence, multinucleation and susceptibility to oncogenic transformation through PKC scaffolding by SSeCKS/AKAP12. Cell Cycle 2010; 9:4656-65; PMID:21099353; http://dx.doi.org/10.4161/cc.9.23.13974
  • Spano A, Monaco G, Barni S, Sciola L. Cisplatin treatment of NIH/3T3 cultures induces a form of autophagic death in polyploid cells. Histol Histopathol 2008; 23:717-30; PMID:18366010
  • Joe AK, Liu H, Suzui M, Vural ME, Xiao D, Weinstein IB. Resveratrol induces growth inhibition, S-phase arrest, apoptosis, and changes in biomarker expression in several human cancer cell lines. Clin Cancer Res 2002; 8:893-903; PMID:11895924
  • Sudo T, Nitta M, Saya H, Ueno NT. Dependence of paclitaxel sensitivity on a functional spindle assembly checkpoint. Cancer Res 2004; 64:2502-8; PMID:15059905; http://dx.doi.org/10.1158/0008-5472.CAN-03-2013
  • Medina I, Carbonell J, Pulido L, Madeira SC, Goetz S, Conesa A, Tarraga J, Pascual-Montano A, Nogales-Cadenas R, Santoyo J, et al. Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res 2010; 38:W210-3; PMID:20478823; http://dx.doi.org/10.1093/nar/gkq388
  • Coppe JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 2010; 5:99-118; PMID:20078217
  • Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, Nabel EG, Collins FS. Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest 2011; 121:2833-44; PMID:21670498
  • Gosselin K, Martien S, Pourtier A, Vercamer C, Ostoich P, Morat L, Sabatier L, Duprez L, T'Kint de Roodenbeke C, Gilson E, et al. Senescence-associated oxidative DNA damage promotes the generation of neoplastic cells. Cancer Res 2009; 69:7917-25; PMID:19826058
  • Gerace L, Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 1980; 19:277-87; PMID:7357605; http://dx.doi.org/10.1016/0092-8674(80)90409-2
  • Vitale I, Galluzzi L, Castedo M, Kroemer G. Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 2011; 12:385-92; PMID:21527953; http://dx.doi.org/10.1038/nrm3115
  • Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol Biol Cell 2001; 12:1315-28; PMID:11359924; http://dx.doi.org/10.1091/mbc.12.5.1315
  • Panopoulos A, Pacios-Bras C, Choi J, Yenjerla M, Sussman MA, Fotedar R, Margolis RL. Failure of cell cleavage induces senescence in tetraploid primary cells. Mol Biol Cell 2014; 25:3105-18; PMID:25143403; http://dx.doi.org/10.1091/mbc.E14-03-0844
  • Uetake Y, Sluder G. Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr Biol 2010; 20:1666-71; PMID:20832310
  • Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, Graham JA, Demur C, Hercend T, Diu-Hercend A, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 2004; 10:262-7; PMID:14981513; http://dx.doi.org/10.1038/nm1003
  • Chuprin A, Gal H, Biron-Shental T, Biran A, Amiel A, Rozenblatt S, Krizhanovsky V. Cell fusion induced by ERVWE1 or measles virus causes cellular senescence. Genes Dev 2013; 27:2356-66; PMID:24186980
  • Demidenko ZN, Korotchkina LG, Gudkov AV, Blagosklonny MV. Paradoxical suppression of cellular senescence by p53. Proc Natl Acad Sci U S A 2010; 107:9660-4; PMID:20457898
  • Luderus ME, den Blaauwen JL, de Smit OJ, Compton DA, van Driel R. Binding of matrix attachment regions to lamin polymers involves single-stranded regions and the minor groove. Mol Cell Biol 1994; 14:6297-305; PMID:8065361
  • Lohka MJ, Maller JL. Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J Cell Biol 1985; 101:518-23; PMID:3926780
  • Gehrig K, Cornell RB, Ridgway ND. Expansion of the nucleoplasmic reticulum requires the coordinated activity of lamins and CTP:phosphocholine cytidylyltransferase α. Mol Biol Cell 2008; 19:237-47; PMID:17959832
  • Malhas A, Goulbourne C, Vaux DJ. The nucleoplasmic reticulum: form and function. Trends Cell Biol 2011; 21:362-73; PMID:21514163
  • McClintock D, Gordon LB, Djabali K. Hutchinson-Gilford progeria mutant lamin A primarily targets human vascular cells as detected by an anti-Lamin A G608G antibody. Proc Natl Acad Sci U S A 2006; 103:2154-9; PMID:16461887; http://dx.doi.org/10.1073/pnas.0511133103
  • Scaffidi P, Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006; 312:1059-63; PMID:16645051; http://dx.doi.org/10.1126/science.1127168
  • Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, Su L, Sharpless NE. Ink4a/Arf expression is a biomarker of aging. J Clin Invest 2004; 114:1299-307; PMID:15520862; http://dx.doi.org/10.1172/JCI22475
  • Kung AL, Sherwood SW, Schimke RT. Cell line-specific differences in the control of cell cycle progression in the absence of mitosis. Proc Natl Acad Sci U S A 1990; 87:9553-7; PMID:2263610; http://dx.doi.org/10.1073/pnas.87.24.9553
  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997; 88:593-602; PMID:9054499; http://dx.doi.org/10.1016/S0092-8674(00)81902-9
  • Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 2000; 14:2015-27; PMID:10950866
  • Chan HM, Narita M, Lowe SW, Livingston DM. The p400 E1A-associated protein is a novel component of the p53 –>p21 senescence pathway. Genes Dev 2005; 19:196-201; PMID:15655109; http://dx.doi.org/10.1101/gad.1280205
  • Moiseeva O, Bourdeau V, Vernier M, Dabauvalle MC, Ferbeyre G. Retinoblastoma-independent regulation of cell proliferation and senescence by the p53-p21 axis in lamin A /C-depleted cells. Aging Cell 2011; 10:789-97; PMID:21535365; http://dx.doi.org/10.1111/j.1474-9726.2011.00719.x
  • Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011; 479:547-51; PMID:22080947; http://dx.doi.org/10.1038/nature10599
  • Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-60; PMID:17251933; http://dx.doi.org/10.1038/nature05529
  • Voorhoeve PM, Agami R. The tumor-suppressive functions of the human INK4A locus. Cancer Cell 2003; 4:311-9; PMID:14585358; http://dx.doi.org/10.1016/S1535-6108(03)00223-X
  • Moiseeva O, Mallette FA, Mukhopadhyay UK, Moores A, Ferbeyre G. DNA Damage Signaling and p53-dependent Senescence after Prolonged β-Interferon Stimulation. Mol Biol Cell 2006; 17:1583-92; PMID:16436515; http://dx.doi.org/10.1091/mbc.E05-09-0858
  • Moiseeva O, Deschenes-Simard X, St-Germain E, Igelmann S, Huot G, Cadar AE, Bourdeau V, Pollak MN, Ferbeyre G. Metformin inhibits the senescence-associated secretory phenotype by interfering with IKK/NF-kappaB activation. Aging Cell 2013; 12:489-98; PMID:23521863; http://dx.doi.org/10.1111/acel.12075
  • Bhaumik D, Scott GK, Schokrpur S, Patil CK, Orjalo AV, Rodier F, Lithgow GJ, Campisi J. MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 2009; 1:402-11; PMID:20148189

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.