Nuclear localization signal deletion mutants of lamin A and progerin reveal insights into lamin A processing and emerin targeting

References

• Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol 2010; 2:a000547; http://dx.doi.org/10.1101/cshperspect.a000547; PMID: 20826548
   PubMed Web of Science ®Google Scholar
• Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. Nuclear lamins: building blocks of nuclear architecture. Genes Dev 2002; 16:533 - 47; http://dx.doi.org/10.1101/gad.960502; PMID: 11877373
   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; http://dx.doi.org/10.1152/physrev.00047.2005; PMID: 16816143
   PubMed Web of Science ®Google Scholar
• Gordon LB, Cao K, Collins FS. Progeria: translational insights from cell biology. J Cell Biol 2012; 199:9 - 13; http://dx.doi.org/10.1083/jcb.201207072; PMID: 23027899
   PubMed Web of Science ®Google Scholar
• Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, Jogia D, Kesteven SH, Michalicek J, Otway R, Verheyen F, et al. Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest 2004; 113:357 - 69; http://dx.doi.org/10.1172/JCI200419448; PMID: 14755333
   PubMed Web of Science ®Google Scholar
• Worman HJ, Courvalin JC. How do mutations in lamins A and C cause disease?. J Clin Invest 2004; 113:349 - 51; http://dx.doi.org/10.1172/JCI20832; PMID: 14755330
   PubMed Web of Science ®Google Scholar
• Dahl KN, Scaffidi P, Islam MF, Yodh AG, Wilson KL, Misteli T. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 2006; 103:10271 - 6; http://dx.doi.org/10.1073/pnas.0601058103; PMID: 16801550
   PubMed Web of Science ®Google Scholar
• Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 2004; 113:370 - 8; http://dx.doi.org/10.1172/JCI200419670; PMID: 14755334
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1073/pnas.0602569103; PMID: 16738054
   PubMed Web of Science ®Google Scholar
• Capell BC, Collins FS. Human laminopathies: nuclei gone genetically awry. Nat Rev Genet 2006; 7:940 - 52; http://dx.doi.org/10.1038/nrg1906; PMID: 17139325
   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; http://dx.doi.org/10.1101/gr.138032.112; PMID: 23152449
   PubMed Web of Science ®Google Scholar
• Ly DH, Lockhart DJ, Lerner RA, Schultz PG. Mitotic misregulation and human aging. Science 2000; 287:2486 - 92; http://dx.doi.org/10.1126/science.287.5462.2486; PMID: 10741968
   PubMed Web of Science ®Google Scholar
• Marji J, O’Donoghue SI, McClintock D, Satagopam VP, Schneider R, Ratner D, Worman HJ, Gordon LB, Djabali K. Defective lamin A-Rb signaling in Hutchinson-Gilford Progeria Syndrome and reversal by farnesyltransferase inhibition. PLoS One 2010; 5:e11132; http://dx.doi.org/10.1371/journal.pone.0011132; PMID: 20559568
   PubMed Web of Science ®Google Scholar
• Csoka AB, English SB, Simkevich CP, Ginzinger DG, Butte AJ, Schatten GP, Rothman FG, Sedivy JM. Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/mesenchymal defects and accelerated atherosclerosis. Aging Cell 2004; 3:235 - 43; http://dx.doi.org/10.1111/j.1474-9728.2004.00105.x; PMID: 15268757
   PubMed Web of Science ®Google Scholar
• Halaschek-Wiener J, Brooks-Wilson A. Progeria of stem cells: stem cell exhaustion in Hutchinson-Gilford progeria syndrome. J Gerontol A Biol Sci Med Sci 2007; 62:3 - 8; http://dx.doi.org/10.1093/gerona/62.1.3; PMID: 17301031
   PubMed Web of Science ®Google Scholar
• Wilson KL, Foisner R. Lamin-binding Proteins. Cold Spring Harb Perspect Biol 2010; 2:a000554; http://dx.doi.org/10.1101/cshperspect.a000554; PMID: 20452940
   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; http://dx.doi.org/10.1073/pnas.0402943101; PMID: 15184648
   PubMed Web of Science ®Google Scholar
• Kubben N, Voncken JW, Demmers J, Calis C, van Almen G, Pinto Y, Misteli T. Identification of differential protein interactors of lamin A and progerin. Nucleus 2010; 1:513 - 25; PMID: 21327095
   PubMed Web of Science ®Google Scholar
• Zhang H, Kieckhaefer JE, Cao K. Mouse models of laminopathies. Aging Cell 2013; 12:2 - 10; http://dx.doi.org/10.1111/acel.12021; PMID: 23095062
   PubMed Web of Science ®Google Scholar
• Berk JM, Maitra S, Dawdy AW, Shabanowitz J, Hunt DF, Wilson KL. O-Linked β-N-acetylglucosamine (O-GlcNAc) regulates emerin binding to barrier to autointegration factor (BAF) in a chromatin- and lamin B-enriched “niche”. J Biol Chem 2013; 288:30192 - 209; http://dx.doi.org/10.1074/jbc.M113.503060; PMID: 24014020
   PubMed Web of Science ®Google Scholar
• Gruenbaum Y, Lee KK, Liu J, Cohen M, Wilson KL. The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J Cell Sci 2002; 115:923 - 9; PMID: 11870211
   PubMed Web of Science ®Google Scholar
• Holaska JM, Wilson KL. Multiple roles for emerin: implications for Emery-Dreifuss muscular dystrophy. Anat Rec A Discov Mol Cell Evol Biol 2006; 288:676 - 80; http://dx.doi.org/10.1002/ar.a.20334; PMID: 16761279
   PubMedGoogle Scholar
• Stuurman N, Heins S, Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 1998; 122:42 - 66; http://dx.doi.org/10.1006/jsbi.1998.3987; PMID: 9724605
   PubMed Web of Science ®Google Scholar
• Vlcek S, Foisner R. Lamins and lamin-associated proteins in aging and disease. Curr Opin Cell Biol 2007; 19:298 - 304; http://dx.doi.org/10.1016/j.ceb.2007.04.001; PMID: 17466505
   PubMed Web of Science ®Google Scholar
• Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari HM, Goldman RD. Introducing intermediate filaments: from discovery to disease. J Clin Invest 2009; 119:1763 - 71; http://dx.doi.org/10.1172/JCI38339; PMID: 19587451
   PubMed Web of Science ®Google Scholar
• Holtz D, Tanaka RA, Hartwig J, McKeon F. The CaaX motif of lamin A functions in conjunction with the nuclear localization signal to target assembly to the nuclear envelope. Cell 1989; 59:969 - 77; http://dx.doi.org/10.1016/0092-8674(89)90753-8; PMID: 2557160
   PubMed Web of Science ®Google Scholar
• Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, Sandoval S, Meta M, Bendale P, Gelb MH, Young SG, et al. Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc Natl Acad Sci U S A 2005; 102:10291 - 6; http://dx.doi.org/10.1073/pnas.0504641102; PMID: 16014412
   PubMed Web of Science ®Google Scholar
• Shumaker DK, Lopez-Soler RI, Adam SA, Herrmann H, Moir RD, Spann TP, Goldman RD. Functions and dysfunctions of the nuclear lamin Ig-fold domain in nuclear assembly, growth, and Emery-Dreifuss muscular dystrophy. Proc Natl Acad Sci U S A 2005; 102:15494 - 9; http://dx.doi.org/10.1073/pnas.0507612102; PMID: 16227433
   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; http://dx.doi.org/10.1073/pnas.0506001102; PMID: 16129833
   PubMed Web of Science ®Google Scholar
• Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol 2005; 6:21 - 31; http://dx.doi.org/10.1038/nrm1550; PMID: 15688064
   PubMed Web of Science ®Google Scholar
• Gelb MH, Brunsveld L, Hrycyna CA, Michaelis S, Tamanoi F, Van Voorhis WC, Waldmann H. Therapeutic intervention based on protein prenylation and associated modifications. Nat Chem Biol 2006; 2:518 - 28; http://dx.doi.org/10.1038/nchembio818; PMID: 16983387
   PubMed Web of Science ®Google Scholar
• 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; 107:1019 - 29; PMID: 8056827
   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; 107:61 - 7; PMID: 8175923
   PubMed Web of Science ®Google Scholar
• Boyartchuk VL, Ashby MN, Rine J. Modulation of Ras and a-factor function by carboxyl-terminal proteolysis. Science 1997; 275:1796 - 800; http://dx.doi.org/10.1126/science.275.5307.1796; PMID: 9065405
   PubMed Web of Science ®Google Scholar
• Dai Q, Choy E, Chiu V, Romano J, Slivka SR, Steitz SA, Michaelis S, Philips MR. Mammalian prenylcysteine carboxyl methyltransferase is in the endoplasmic reticulum. J Biol Chem 1998; 273:15030 - 4; http://dx.doi.org/10.1074/jbc.273.24.15030; PMID: 9614111
   PubMed Web of Science ®Google Scholar
• Wright LP, Philips MR. Thematic review series: lipid posttranslational modifications. CAAX modification and membrane targeting of Ras. J Lipid Res 2006; 47:883 - 91; http://dx.doi.org/10.1194/jlr.R600004-JLR200; PMID: 16543601
   PubMed Web of Science ®Google Scholar
• Bergo MO, Gavino B, Ross J, Schmidt WK, Hong C, Kendall LV, Mohr A, Meta M, Genant H, Jiang Y, et al. Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc Natl Acad Sci U S A 2002; 99:13049 - 54; http://dx.doi.org/10.1073/pnas.192460799; PMID: 12235369
   PubMed Web of Science ®Google Scholar
• Barrowman J, Hamblet C, Kane MS, Michaelis S. Requirements for efficient proteolytic cleavage of prelamin A by ZMPSTE24. PLoS One 2012; 7:e32120; http://dx.doi.org/10.1371/journal.pone.0032120; PMID: 22355414
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1091/mbc.E08-07-0704; PMID: 18923140
   PubMed Web of Science ®Google Scholar
• Vlcek S, Foisner R. A-type lamin networks in light of laminopathic diseases. Biochim Biophys Acta 2007; 1773:661 - 74; http://dx.doi.org/10.1016/j.bbamcr.2006.07.002; PMID: 16934891
   PubMed Web of Science ®Google 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; http://dx.doi.org/10.1038/nature01629; PMID: 12714972
   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; http://dx.doi.org/10.1126/science.1084125; PMID: 12702809
   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; PMID: 15032975
   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; http://dx.doi.org/10.1073/pnas.0611640104; PMID: 17360355
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1093/hmg/ddq490; PMID: 21088111
   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; http://dx.doi.org/10.1073/pnas.0505767102; PMID: 16129834
   PubMed Web of Science ®Google Scholar
• Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA, Spielmann HP, Sinensky MS, Goldman RD. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc Natl Acad Sci U S A 2007; 104:4955 - 60; http://dx.doi.org/10.1073/pnas.0700854104; PMID: 17360326
   PubMed Web of Science ®Google Scholar
• Lee J, Lee HJ, Shin MK, Ryu WS. Versatile PCR-mediated insertion or deletion mutagenesis. Biotechniques 2004; 36:398 - 400; PMID: 15038153
   PubMed Web of Science ®Google Scholar
• Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 1995; 131:1715 - 26; http://dx.doi.org/10.1083/jcb.131.6.1715; PMID: 8557739
   PubMed Web of Science ®Google Scholar
• Munro S, Pelham HR. A C-terminal signal prevents secretion of luminal ER proteins. Cell 1987; 48:899 - 907; http://dx.doi.org/10.1016/0092-8674(87)90086-9; PMID: 3545499
   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; http://dx.doi.org/10.1172/JCI28968; PMID: 16862216
   PubMed Web of Science ®Google Scholar
• Yang SH, Andres DA, Spielmann HP, Young SG, Fong LG. Progerin elicits disease phenotypes of progeria in mice whether or not it is farnesylated. J Clin Invest 2008; 118:3291 - 300; http://dx.doi.org/10.1172/JCI35876; PMID: 18769635
   PubMed Web of Science ®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; http://dx.doi.org/10.1073/pnas.0807840105; PMID: 18838683
   PubMed Web of Science ®Google Scholar
• Vaughan A, Alvarez-Reyes M, Bridger JM, Broers JL, Ramaekers FC, Wehnert M, Morris GE, Hutchison CJ, Whitfield WGF. Both emerin and lamin C depend on lamin A for localization at the nuclear envelope. J Cell Sci 2001; 114:2577 - 90; PMID: 11683386
   PubMed Web of Science ®Google Scholar
• Astejada MN, Goto K, Nagano A, Ura S, Noguchi S, Nonaka I, Nishino I, Hayashi YK. Emerinopathy and laminopathy clinical, pathological and molecular features of muscular dystrophy with nuclear envelopathy in Japan. Acta Myol 2007; 26:159 - 64; PMID: 18646565
   PubMedGoogle Scholar
• Lee KK, Haraguchi T, Lee RS, Koujin T, Hiraoka Y, Wilson KL. Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 2001; 114:4567 - 73; PMID: 11792821
   PubMed Web of Science ®Google Scholar
• Mislow JM, Holaska JM, Kim MS, Lee KK, Segura-Totten M, Wilson KL, McNally EM. Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett 2002; 525:135 - 40; http://dx.doi.org/10.1016/S0014-5793(02)03105-8; PMID: 12163176
   PubMed Web of Science ®Google Scholar
• Ostlund C, Ellenberg J, Hallberg E, Lippincott-Schwartz J, Worman HJ. Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein. J Cell Sci 1999; 112:1709 - 19; PMID: 10318763
   PubMedGoogle Scholar
• Clements L, Manilal S, Love DR, Morris GE. Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 2000; 267:709 - 14; http://dx.doi.org/10.1006/bbrc.1999.2023; PMID: 10673356
   PubMed Web of Science ®Google Scholar
• Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 2013; 497:507 - 11; http://dx.doi.org/10.1038/nature12105; PMID: 23644458
   PubMed Web of Science ®Google Scholar