SUN1 splice variants, SUN1_888, SUN1_785, and predominant SUN1_916, variably function in directional cell migration

References

• Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 2006; 172:41-53; PMID:16380439; http://dx.doi.org/10.1083/jcb.200606020
   PubMed Web of Science ®Google Scholar
• Chi YH, Haller K, Peloponese JM Jr, Jeang KT. Histone acetyltransferase hALP and nuclear membrane protein hsSUN1 function in de-condensation of mitotic chromosomes. J Biol Chem 2007; 282:27447-58; PMID:17631499; http://dx.doi.org/10.1074/jbc.M703098200
   PubMed Web of Science ®Google Scholar
• Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD. Sun2 is a novel mammalian inner nuclear membrane protein.J Biol Chem 2004; 279:25805-12; PMID:15082709; http://dx.doi.org/10.1074/jbc.M313157200
   PubMed Web of Science ®Google Scholar
• Rajgor D, Shanahan CM. Nesprins: from the nuclear envelope and beyond. Expert Rev Mol Med 2013; 15:e5; PMID:23830188; http://dx.doi.org/10.1017/erm.2013.6
   PubMed Web of Science ®Google Scholar
• Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton.Mol Cell Biol 2006; 26:3738-51; PMID:16648470; http://dx.doi.org/10.1128/MCB.26.10.3738-3751.2006
   PubMed Web of Science ®Google Scholar
• Göb E, Schmitt J, Benavente R, Alsheimer M. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One 2010; 5:e12072; PMID:20711465; http://dx.doi.org/10.1371/journal.pone.0012072
   PubMed Web of Science ®Google Scholar
• Shao X, Tarnasky HA, Lee JP, Oko R, van der Hoorn FA. Spag4, a novel sperm protein, binds outer dense-fiber protein Odf1 and localizes to microtubules of manchette and axoneme. Dev Biol 1999; 211:109-23; PMID:10373309; http://dx.doi.org/10.1006/dbio.1999.9297
   PubMed Web of Science ®Google Scholar
• Frohnert C, Schweizer S, Hoyer-Fender S. SPAG4L/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome.Mol Hum Reprod 2011; 17:207-18; PMID:21159740; http://dx.doi.org/10.1093/molehr/gaq099
   PubMed Web of Science ®Google Scholar
• Jiang XZ, Yang MG, Huang LH, Li CQ, Xing XW SPAG4L, a novel nuclear envelope protein involved in the meiotic stage of spermatogenesis. DNA Cell Biol 2011; 30:875-82; PMID:21711156; http://dx.doi.org/10.1089/dna.2010.1161
   PubMed Web of Science ®Google Scholar
• Bone CR, Starr DA. Nuclear migration events throughout development. J Cell Sci 2016; 129:1951-61; PMID:27182060; http://dx.doi.org/10.1242/jcs.179788
   PubMed Web of Science ®Google Scholar
• Gundersen GG, Worman HJ. Nuclear positioning. Cell 2013; 152:1376-89; PMID:23498944; http://dx.doi.org/10.1016/j.cell.2013.02.031
   PubMed Web of Science ®Google Scholar
• Wilhelmsen K, Ketema M, Truong H, Sonnenberg A. KASH-domain proteins in nuclear migration, anchorage and other processes. J Cell Sci 2006; 119(Pt 24):5021-9; PMID:17158909; http://dx.doi.org/10.1242/jcs.03295
   PubMed Web of Science ®Google Scholar
• Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009; 64:173-87; PMID:19874786; http://dx.doi.org/10.1016/j.neuron.2009.08.018
   PubMed Web of Science ®Google Scholar
• Chang W, Antoku S, Östlund C, Worman HJ, Gundersen GG. Linker of nucleoskeleton and cytoskeleton (LINC) complex-mediated actin-dependent nuclear positioning orients centrosomes in migrating myoblasts. Nucleus 2015; 6:77-88; PMID:25587885; http://dx.doi.org/10.1080/19491034.2015.1004947
   PubMed Web of Science ®Google Scholar
• Chambliss AB, Khatau SB, Erdenberger N, Robinson DK, Hodzic D, Longmore GD, Wirtz D. The LINC-anchored actin cap connects the extracellular milieu to the nucleus for ultrafast mechanotransduction. Sci Rep 2013; 3:1087; PMID:23336069; http://dx.doi.org/10.1038/srep01087
   PubMed Web of Science ®Google Scholar
• Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10:75-82; PMID:19197334; http://dx.doi.org/10.1038/nrm2594
   PubMed Web of Science ®Google Scholar
• Lei K, Zhu X, Xu R, Shao C, Xu T, Zhuang Y, Han M. Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in theDNA damage response.Curr Biol 2012; 22:1609-15; PMID:22863315; http://dx.doi.org/10.1016/j.cub.2012.06.043
   PubMed Web of Science ®Google Scholar
• Lottersberger F, Karssemeijer RA, Dimitrova N, de Lange. T53BP1 and the LINC Complex Promote Microtubule-Dependent DSB Mobility and DNA Repair. Cell 2015; 163:880-93; PMID:26544937; http://dx.doi.org/10.1016/j.cell.2015.09.057
   PubMed Web of Science ®Google Scholar
• Cain NE, Starr DA. SUN proteins and nuclear envelope spacing. Nucleus 2015; 6:2-7; PMID:25425085; http://dx.doi.org/10.4161/19491034.2014.990857
   PubMed Web of Science ®Google Scholar
• Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 2010; 329:956-9; PMID:20724637; http://dx.doi.org/10.1126/science.1189072
   PubMed Web of Science ®Google Scholar
• Chancellor TJ, Lee J, Thodeti CK, Lele T. Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 2010; 99:115-23; PMID:20655839; http://dx.doi.org/10.1016/j.bpj.2010.04.011
   PubMed Web of Science ®Google Scholar
• Maninová M, Klímová Z, Parsons JT, Weber MJ, Iwanicki MP, Vomastek T. The reorientation of cell nucleus promotes the establishment of front-rear polarity in migrating fibroblasts. J Mol Biol 2013; 425:2039-55; PMID:23524135; http://dx.doi.org/10.1016/j.jmb.2013.02.034
   PubMed Web of Science ®Google Scholar
• King SJ, Nowak K, Suryavanshi N, Holt I, Shanahan CM, Ridley AJ. Nesprin-1 and nesprin-2 regulate endothelial cell shape and migration. Cytoskeleton 2014; 71:423-34; PMID:24931616; http://dx.doi.org/10.1002/cm.21182
   PubMed Web of Science ®Google Scholar
• Hiraoka Y, Dernburg AF The SUN rises on meiotic chromosome dynamics. Dev Cell 2009; 17:598-605; PMID:19922865; http://dx.doi.org/10.1016/j.devcel.2009.10.014
   PubMed Web of Science ®Google Scholar
• Burke B, Stewart CL. Functional architecture of the cell's nucleus in development, aging, and disease. Curr Top Dev Biol 2014; 109:1-52; PMID:24947235; http://dx.doi.org/10.1016/B978-0-12-397920-9.00006-8
   PubMed Web of Science ®Google Scholar
• Meinke P, Nguyen TD, Wehnert MS. The LINC complex and human disease. Biochem Soc Trans 2011; 39:1693-7; http://dx.doi.org/10.1042/BST20110658
   PubMed Web of Science ®Google Scholar
• Méndez-López I, Worman HJ. Inner nuclear membrane proteins: impact on human disease. Chromosoma 2012; 121:153-67; http://dx.doi.org/10.1007/s00412-012-0360-2
   PubMed Web of Science ®Google Scholar
• Wang W, Shi Z, Jiao S, Chen C, Wang H, Liu G, Wang Q, Zhao Y, Greene MI, Zhou Z. Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res 2012; 22:1440-52; PMID:22945352; http://dx.doi.org/10.1038/cr.2012.126
   PubMed Web of Science ®Google Scholar
• Sosa BA, Rothballer A, Kutay U, Schwartz TU. LINC Complexes Form by Binding of Three KASH Peptides to the Interfaces of Trimeric SUN proteins Cell 2012; 149:1035-1047.
   Google Scholar
• Patel JT, Bottrill A, Prosser SL, Jayaraman S, Straatman K, Fry AM, Shackleton S. Mitotic phosphorylation of SUN1 loosens its connection with the nuclear lamina while the LINC complex remains intact. Nucleus 2014; 5:462-73; PMID:25482198; http://dx.doi.org/10.4161/nucl.36232
   PubMed Web of Science ®Google Scholar
• Woglar A, Daryabeigi A, Adamo A, Habacher C, Machacek T, La Volpe A, Jantsch V. Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet 2013; 9:e1003335; PMID:23505384; http://dx.doi.org/10.1371/journal.pgen.1003335
   PubMed Web of Science ®Google Scholar
• Ghosh S, Gardner JM, Smoyer CJ, Friederichs JM, Unruh JR, Slaughter BD, Alexander R, Chisholm RD, Lee KK, Workman JL, Jaspersen SL. Acetylation of the SUN protein Mps3 by Eco1 regulates its function in nuclear organization. Mol Biol Cell 2012; 23:2546-59; PMID:22593213; http://dx.doi.org/10.1091/mbc.E11-07-0600
   PubMed Web of Science ®Google Scholar
• Liu Q, Pante N, Misteli T, Elsagga M, Crisp M, Hodzic D, Burke B, Roux KJFunctional association of Sun1 with nuclear pore complexes. J Cell Biol 2007; 178:785-98; PMID:17724119; http://dx.doi.org/10.1083/jcb.200704108
   PubMed Web of Science ®Google Scholar
• Göb E, Meyer-Natus E, Benavente R, Alsheimer M. Expression of individual mammalian Sun1 isoforms depends on the cell type. Commun Integr Biol 2011; 4:440-2; PMID:21966565; http://dx.doi.org/10.4161/cib.15369
   PubMedGoogle Scholar
• Hasan S, Güttinger S, Mühlhäusser P, Anderegg F, Bürgler S, Kutay U. Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett 2006; 580:1263-8; PMID:16445915; http://dx.doi.org/10.1016/j.febslet.2006.01.039
   PubMed Web of Science ®Google Scholar
• Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 2011; 286:26743-53; PMID:21652697; http://dx.doi.org/10.1074/jbc.M111.233700
   PubMed Web of Science ®Google Scholar
• Lv XB, Liu L, Cheng C, Yu B, Xiong L, Hu K, Tang J, Zeng L, Sang Y. SUN2 exerts tumor suppressor functions by suppressing the Warburg effect in lung cancer. Sci Rep 2015; 5:17940; PMID:26658802; http://dx.doi.org/10.1038/srep17940
   PubMed Web of Science ®Google Scholar
• Matsumoto A, Hieda M, Yokoyama Y, Nishioka Y, Yoshidome K, Tsujimoto M, Matsuura N. Global loss of a nuclear lamina component, lamin A/C, and LINC complex components SUN1, SUN2, and nesprin-2 in breast cancer. Cancer Med 2015; 4:1547-57; PMID:26175118; http://dx.doi.org/10.1002/cam4.495
   PubMed Web of Science ®Google Scholar
• Meinke P, Mattioli E, Haque F, Antoku S, Columbaro M, Straatman KR, Worman HJ, Gundersen GG, Lattanzi G, Wehnert M, Shackleton S. Muscular dystrophy-associated SUN1 and SUN2 variants disrupt nuclear-cytoskeletal connections and myonuclear organization. PLoS Genet 2014; 10:e1004605; PMID:25210889; http://dx.doi.org/10.1371/journal.pgen.1004605
   PubMed Web of Science ®Google Scholar
• Chen CY, Chi YH, Mutalif RA, Starost MF, Myers TG, Anderson SA, Stewart CL, Jeang KT. Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies. Cell 2012; 149:565-77; PMID:22541428; http://dx.doi.org/10.1016/j.cell.2012.01.059
   PubMed Web of Science ®Google Scholar
• Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, Fong LG, Young SG. Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 2010; 107:5076-81; PMID:20145110; http://dx.doi.org/10.1073/pnas.0908790107
   PubMed Web of Science ®Google Scholar
• Coffinier C, Jung HJ, Nobumori C, Chang S, Tu Y, Barnes RH 2nd, Yoshinaga Y, de Jong PJ, Vergnes L, Reue K, Fong LG, Young SG. Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons. Mol Biol Cell 2011; 22:4683-93; PMID:21976703; http://dx.doi.org/10.1091/mbc.E11-06-0504
   PubMed Web of Science ®Google Scholar
• Coffinier C, Fong LG, Young SG. LINCing lamin B2 to neuronal migration: growing evidence for cell-specific roles of B-type lamins. Nucleus 2010; 1:407-11; PMID:21278813; http://dx.doi.org/10.4161/nucl.1.5.12830
   PubMed Web of Science ®Google Scholar
• Wang JY, Yu IS, Huang CC, Chen CY, Wang WP, Lin SW, Jeang KT, Chi YH. Sun1 deficiency leads to cerebellar ataxia in mice. Dis Model Mech 2015; 8:957-67; PMID:26035387; http://dx.doi.org/10.1242/dmm.019240
   PubMed Web of Science ®Google Scholar
• Takamori Y, Tamura Y, Kataoka Y, Cui Y, Seo S, Kanazawa T, Kurokawa K, Yamada H. Differential expression of nuclear lamin, the major component of nuclear lamina, during neurogenesis in two germinal regions of adult rat brain. Eur J Neurosci 2007; 25:1653-62; PMID:17432957; http://dx.doi.org/10.1111/j.1460-9568.2007.05450.x
   PubMed Web of Science ®Google Scholar
• Yokoyama Y, Hieda M, Nishioka Y, Matsumoto A, Higashi S, Kimura H, Yamamoto H, Mori M, Matsuura S, Matsuura N. Cancer associated up-regulation of H3K9 methylation promotes cell motility in vitro and drives tumor formation in vivo. Cancer Science 2013; 104:889-8; PMID:23557258; http://dx.doi.org/10.1111/cas.12166
   PubMed Web of Science ®Google Scholar
• Tokuhiro K, Ikawa M, Benham AM, Okabe M. Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein ADAM3 and male fertility [corrected]. Proc Natl Acad Sci USA 2012; 109:3850-55; PMID:22357757; http://dx.doi.org/10.1073/pnas.1117963109
   PubMed Web of Science ®Google Scholar
• Hieda M, Matsuura N, Kimura H. Histone modifications associated with cancer cell migration and invasion. Methods Mol Biol 2015; 1238:301-17; PMID:25421667; http://dx.doi.org/10.1007/978-1-4939-1804-1_16
   PubMedGoogle Scholar