Comparing lamin proteins post-translational relative stability using a 2A peptide-based system reveals elevated resistance of progerin to cellular degradation

References

• Fawcett DW. On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. Am J Anat (1966); 119:129-45; PMID:6007824; http://dx.doi.org/10.1002/aja.1001190108
   PubMedGoogle Scholar
• Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. Nuclear lamins: building blocks of nuclear architecture. Genes Dev (2002); 16:533-47; PMID:11877373; http://dx.doi.org/10.1101/gad.960502
   PubMed Web of Science ®Google Scholar
• Krohne G, Benavente R, Scheer U, Dabauvalle MC. The nuclear lamina in Heidelberg and W??rzburg: A personal view. Eur J Cell Biol (2005); 84:163-179; PMID:15819398; http://dx.doi.org/10.1016/j.ejcb.2004.12.005
   PubMed Web of Science ®Google Scholar
• McKeon FD, Kirschner MW, Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature (1986); 319:463-8; PMID:3453101; http://dx.doi.org/10.1038/319463a0
   PubMed Web of Science ®Google Scholar
• Furukawa K, Inagaki H, Hotta Y. Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp Cell Res (1994); 212:426-30; PMID:8187835; http://dx.doi.org/10.1006/excr.1994.1164
   PubMed Web of Science ®Google Scholar
• Machiels BM, Zorenc AH, Endert JM, Kuijpers HJ, van Eys GJ, Ramaekers FC, Broers JL. An alternative splicing product of the lamin A/C gene lacks exon 10. J Biol Chem (1996); 271:9249-53; PMID:8621584; http://dx.doi.org/10.1074/jbc.271.16.9249
   PubMed Web of Science ®Google Scholar
• Pollard KM, Chan EK, Grant BJ, Sullivan KF, Tan EM, Glass CA. In vitro posttranslational modification of lamin B cloned from a human T-cell line. Mol Cell Biol (1990); 10:2164-75; PMID:2325650; http://dx.doi.org/10.1128/MCB.10.5.2164
   PubMed Web of Science ®Google Scholar
• Furukawa K, Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J (1993); 12:97-106; PMID:8094052
   PubMed Web of Science ®Google Scholar
• Spann TP, Goldman AE, Wang C, Huang S, Goldman RD. Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J Cell Biol (2002); 156:603-8; PMID:11854306; http://dx.doi.org/10.1083/jcb.200112047
   PubMed Web of Science ®Google Scholar
• Bridger JM, Foeger N, Kill IR, Herrmann H. The nuclear lamina. Both a structural framework and a platform for genome organization. FEBS J (2007); 274:1354-61
   PubMed Web of Science ®Google Scholar
• Gruenbaum Y, Foisner R. Lamins: Nuclear Intermediate Filament Proteins with Fundamental Functions in Nuclear Mechanics and Genome Regulation. Annu Rev Biochem (2014); 84:150306093657004
   Web of Science ®Google Scholar
• Capell BC, Collins FS. Human laminopathies: nuclei gone genetically awry. Nat Rev Genet (2006); 7:940-52; PMID:17139325; http://dx.doi.org/10.1038/nrg1906
   PubMed Web of Science ®Google Scholar
• Cao K, Park C. Cellular Basis of Laminopathies (2012); 1-7
   Google Scholar
• Sarkar PK, Shinton RA. Hutchinson-Guilford progeria syndrome. Postgrad Med J (2001); 77:312-7; PMID:11320273; http://dx.doi.org/10.1136/pmj.77.907.312
   PubMed Web of Science ®Google Scholar
• Hutchinson J. Congenital absence of hair and mammary glands with atrophic condition of the skin and its appendages, in a boy whose mother had been almost wholly bald from alopecia areata from the age of Six. Med Chir Trans (1886); 69:473-7; PMID:20896687; http://dx.doi.org/10.1177/095952878606900127
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A, Dalton M. The processing pathway of prelamin A. J Cell Sci (1994); 107:( Pt 1, 61-7; PMID:8175923
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• D'Apice MR, Tenconi R, Mammi I, van den Ende J, Novelli G. Paternal origin of LMNA mutations in Hutchinson-Gilford progeria. Clin Genet (2004); 65:52-4; http://dx.doi.org/10.1111/j..2004.00181.x
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1073/pnas.0611640104
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1073/pnas.0402943101
   PubMed Web of Science ®Google Scholar
• McCord RP, Nazario-Toole A, Zhang H, Chines PS, Zhan Y, Erdos MR, Collins FS, Dekker J, Cao K. Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res (2013); 23:260-9; PMID:23152449; http://dx.doi.org/10.1101/gr.138032.112
   PubMed Web of Science ®Google Scholar
• DeBusk FL. The Hutchinson-Gilford progeria syndrome. Report of 4 cases and review of the literature. J Pediatr (1972); 80:697-724; PMID:4552697; http://dx.doi.org/10.1016/S0022-3476(72)80229-4
   PubMed Web of Science ®Google Scholar
• Baker PB, Baba N, Boesel CP. Cardiovascular abnormalities in progeria. Case report and review of the literature. Arch Pathol Lab Med (1981); 105:384-6; PMID:6894691
   PubMed Web of Science ®Google Scholar
• Gordon LB, Massaro J, D'Agostino RB Sr, Campbell SE, Brazier J, Brown WT, Kleinman ME, Kieran MW; Progeria Clinical Trials Collaborative. Impact of farnesylation inhibitors on survival in Hutchinson-Gilford progeria syndrome. Circulation (2014); 130:27-34; PMID:24795390; http://dx.doi.org/10.1161/CIRCULATIONAHA.113.008285
   PubMed Web of Science ®Google Scholar
• Ullrich NJ, Gordon LB. Hutchinson-Gilford progeria syndrome. Handb Clin Neurol (2015); 132:249-64; PMID:26564085; http://dx.doi.org/10.1016/B978-0-444-62702-5.00018-4
   PubMedGoogle Scholar
• Zhou P. Determining protein half-lives. Methods Mol Biol (2004); 284:67-77; PMID:15173609
   PubMedGoogle Scholar
• Fritzsche S, Springer S. Pulse-chase analysis for studying protein synthesis and maturation. Curr Protoc Protein Sci (2014); 78:30.3.1-23
   Google Scholar
• Bertacchini J, Beretti F, Cenni V, Guida M, Gibellini F, Mediani L, Marin O, Maraldi NM, de Pol A, Lattanzi G, et al. The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FASEB J (2013); 27:2145-55; PMID:23430973; http://dx.doi.org/10.1096/fj.12-218214
   PubMed Web of Science ®Google Scholar
• Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol (2010); 2:a000547; PMID:20826548; http://dx.doi.org/10.1101/cshperspect.a000547
   PubMed Web of Science ®Google Scholar
• Rodriguez-Contreras D, Aslan H, Feng X, Tran K, Yates PA, Kamhawi S, Landfear SM. Regulation and biological function of a flagellar glucose transporter in Leishmania mexicana: a potential glucose sensor. FASEB J (2015); 29:11-24; PMID:25300620; http://dx.doi.org/10.1096/fj.14-251991
   PubMed Web of Science ®Google Scholar
• De Felipe P, Luke GA, Hughes LE, Gani D, Halpin C, Ryan MD. E unum pluribus: Multiple proteins from a self-processing polyprotein. Trends Biotechnol (2006); 24:68-75; PMID:16380176; http://dx.doi.org/10.1016/j.tibtech.2005.12.006
   PubMed Web of Science ®Google Scholar
• Ryan MD, King AM, Thomas GP. Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. J Gen Virol (1991); 72:( Pt 11, 2727-32; PMID:1658199; http://dx.doi.org/10.1099/0022-1317-72-11-2727
   PubMed Web of Science ®Google Scholar
• Donnelly ML, Luke G, Mehrotra A, Li X, Hughes LE, Gani D, Ryan MD. Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal ‘skip’. J Gen Virol (2001); 82:1013-25; PMID:11297676; http://dx.doi.org/10.1099/0022-1317-82-5-1013
   PubMed Web of Science ®Google Scholar
• de Felipe P, Luke GA, Brown JD, Ryan MD. Inhibition of 2A-mediated ‘cleavage’ of certain artificial polyproteins bearing N-terminal signal sequences. Biotechnol J (2010); 5:213-23; PMID:19946875; http://dx.doi.org/10.1002/biot.200900134
   PubMed Web of Science ®Google Scholar
• Kim JH, Lee SR, Li LH, Park HJ, Park JH, Lee KY, Kim MK, Shin BA, Choi SY. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One (2011); 6:1-8
   Web of Science ®Google Scholar
• Xiong Z-M, Choi JY, Wang K, Zhang H, Tariq Z, Wu D, Ko E, LaDana C, Sesaki H, Cao K. Methylene blue alleviates nuclear and mitochondrial abnormalities in progeria. Aging Cell (2015); 15:279-90; PMID:26663466; http://dx.doi.org/10.1111/acel.12434
   PubMed Web of Science ®Google Scholar
• Toth JI, Yang SH, Qiao X, Beigneux AP, Gelb MH, Moulson CL, Miner JH, Young SG, Fong LG. Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc Natl Acad Sci U S A (2005); 102:12873-8; PMID:16129834; http://dx.doi.org/10.1073/pnas.0505767102
   PubMed Web of Science ®Google Scholar
• Yang SH, Meta M, Qiao X, Frost D, Bauch J, Coffinier C, Majumdar S, Bergo MO, Young SG, Fong LG. A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest (2006); 116:2115-21; PMID:16862216; http://dx.doi.org/10.1172/JCI28968
   PubMed Web of Science ®Google Scholar
• Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, Conneely KN, Gordon LB, Der CJ, Cox AD, Collins FS. Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A (2005); 102:12879-84; PMID:16129833; http://dx.doi.org/10.1073/pnas.0506001102
   PubMed Web of Science ®Google Scholar
• Gordon LB, Kleinman ME, Miller DT, Neuberg DS, Giobbie-Hurder A, Gerhard-Herman M, Smoot LB, Gordon CM, Cleveland R, Snyder BD, et al. Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson – Gilford progeria syndrome 2012); 2-7
   Google Scholar
• Adam SA, Butin-Israeli V, Cleland MM, Shimi T, Goldman RD. Disruption of lamin B1 and lamin B2 processing and localization by farnesyltransferase inhibitors. Nucleus (2013); 4:142-50; PMID:23475125; http://dx.doi.org/10.4161/nucl.24089
   PubMed Web of Science ®Google Scholar
• Adam SA, Butin-Israeli V, Cleland MM, Shimi T, Goldman RD. Disruption of lamin B1 and lamin B2 processing and localization by farnesyltransferase inhibitors. Nucleus (2013); 4:142-50; PMID:23475125; http://dx.doi.org/10.4161/nucl.24089
   PubMed Web of Science ®Google Scholar
• 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 (2011); 121
   Google Scholar
• Capell BC, Olive M, Erdos MR, Cao K, Faddah DA, Tavarez UL, Conneely KN, Qu X, San H, Ganesh SK, et al. A farnesyltransferase inhibitor prevents both the onset and late progression of cardiovascular disease in a progeria mouse model. Proc Natl Acad Sci U S A (2008); 105:15902-7; PMID:18838683; http://dx.doi.org/10.1073/pnas.0807840105
   PubMed Web of Science ®Google Scholar
• Verstraeten VL, Peckham LA, Olive M, Capell BC, Collins FS, Nabel EG, Young SG, Fong LG, Lammerding J. Protein farnesylation inhibitors cause donut-shaped cell nuclei attributable to a centrosome separation defect. Proc Natl Acad Sci (2011); 108:4997-5002; PMID:21383178; http://dx.doi.org/10.1073/pnas.1019532108
   PubMed Web of Science ®Google Scholar
• Maske CP, Hollinshead MS, Higbee NC, Bergo MO, Young SG, Vaux DJ. A carboxyl-terminal interaction of lamin B1 is dependent on the CAAX endoprotease Rce1 and carboxymethylation. J Cell Biol (2003); 162:1223-32; PMID:14504265; http://dx.doi.org/10.1083/jcb.200303113
   PubMed Web of Science ®Google Scholar
• Jung H-J, Nobumori C, Goulbourne CN, Tu Y, Lee JM, Tatar A, Wu D, Yoshinaga Y, de Jong PJ, Coffinier C, et al. Farnesylation of lamin B1 is important for retention of nuclear chromatin during neuronal migration. Proc Natl Acad Sci U S A (2013); 110, E1923-32; PMID:23650370; http://dx.doi.org/10.1073/pnas.1303916110
   PubMed Web of Science ®Google Scholar
• Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, Ivanov A, Capell BC, Drake AM, Shah PP, et al. Autophagy mediates degradation of nuclear lamina. Nature (2015); 527:1-17; ; http://dx.doi.org/10.1038/nature15548
   Web of Science ®Google Scholar
• GREENBERG JR. High Stability of Messenger RNA in Growing Cultured Cells. Nature (1972); 240:102-4; PMID:4564814; http://dx.doi.org/10.1038/240102a0
   PubMed Web of Science ®Google Scholar
• Wu D, Flannery AR, Cai H, Ko E, Cao K. Nuclear localization signal deletion mutants of lamin A and progerin reveal insights into lamin A processing and emerin targeting. Nucleus (2014); 5:66-74; PMID:24637396; http://dx.doi.org/10.4161/nucl.28068
   PubMed Web of Science ®Google Scholar