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Research Paper

Linker of nucleoskeleton and cytoskeleton (LINC) complex-mediated actin-dependent nuclear positioning orients centrosomes in migrating myoblasts

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Pages 77-88 | Received 19 Nov 2014, Accepted 22 Dec 2014, Published online: 04 Mar 2015

References

  • Gundersen GG, Worman HJ. Nuclear positioning. Cell 2013; 152:1376-89; PMID:23498944; http://dx.doi.org/10.1016/j.cell.2013.02.031
  • Gomes ER, Jani S, Gundersen GG. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 2005; 121:451-63; PMID:15882626; http://dx.doi.org/10.1016/j.cell.2005.02.022
  • Chang W, Folker ES, Worman HJ, Gundersen GG. Emerin organizes actin flow for nuclear movement and centrosome orientation in migrating fibroblasts. Mol Biol Cell 2013; 24:3869-80; PMID:24152738; http://dx.doi.org/10.1091/mbc.E13-06-0307
  • 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
  • Luxton GW, Gomes ER, Folker ES, Worman HJ, Gundersen GG. TAN lines: a novel nuclear envelope structure involved in nuclear positioning. Nucleus 2011; 2:173-81; PMID:21818410; http://dx.doi.org/10.4161/nucl.2.3.16243
  • Kutscheidt S, Zhu R, Antoku S, Luxton GW, Stagljar I, Fackler OT, Gundersen GG. FHOD1 interaction with nesprin-2G mediates TAN line formation and nuclear movement. Nat Cell Biol 2014; 16:708-15; PMID:24880667; http://dx.doi.org/10.1038/ncb2981
  • 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 U S A 2011; 108:131-6; PMID:21173262; http://dx.doi.org/10.1073/pnas.1000824108
  • Borrego-Pinto J, Jegou T, Osorio DS, Aurade F, Gorjanacz M, Koch B, Mattaj IW, Gomes ER. Samp1 is a component of TAN lines and is required for nuclear movement. J Cell Sci 2012; 125:1099-105; PMID:22349700; http://dx.doi.org/10.1242/jcs.087049
  • Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD, Kennedy BK. Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 2006; 20:486-500; PMID:16481476; http://dx.doi.org/10.1101/gad.1364906
  • Bonne G, Di Barletta MR, Varnous S, Becane HM, Hammouda EH, Merlini L, Muntoni F, Greenberg CR, Gary F, Urtizberea JA, et al. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 1999; 21:285-8; PMID:10080180; http://dx.doi.org/10.1038/6799
  • Fatkin D, MacRae C, Sasaki T, Wolff MR, Porcu M, Frenneaux M, Atherton J, Vidaillet HJ, Jr., Spudich S, De Girolami U, et al. Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. New Engl J Med 1999; 341:1715-24; PMID:10580070; http://dx.doi.org/10.1056/NEJM199912023412302
  • Muchir A, Bonne G, van der Kooi AJ, van Meegen M, Baas F, Bolhuis PA, de Visser M, Schwartz K. Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Human Mol Genetics 2000; 9:1453-9; PMID:10814726; http://dx.doi.org/10.1093/hmg/9.9.1453
  • Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 1994; 8:323-7; PMID:7894480; http://dx.doi.org/10.1038/ng1294-323
  • Brosig M, Ferralli J, Gelman L, Chiquet M, Chiquet-Ehrismann R. Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int J Biochem Cell Biol 2010; 42:1717-28; PMID:20621196; http://dx.doi.org/10.1016/j.biocel.2010.07.001
  • Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, Ragnauth CD, Yi Q, Mellad JA, Warren DT, et al. Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet 2007; 16:2816-33; PMID:17761684; http://dx.doi.org/10.1093/hmg/ddm238
  • Puckelwartz MJ, Kessler E, Zhang Y, Hodzic D, Randles KN, Morris G, Earley JU, Hadhazy M, Holaska JM, Mewborn SK, et al. Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice. Hum Mol Genet 2009; 18:607-20; PMID:19008300; http://dx.doi.org/10.1093/hmg/ddn386
  • Meinke P, Mattioli E, Haque F, Antoku S, Columbaro M, Straatman KR, Worman HJ, Gundersen GG, Lattanzi G, Wehnert M, et al. Muscular Dystrophy-Associated SUN1 and SUN2 Variants Disrupt Nuclear-Cytoskeletal Connections and Myonuclear Organization. PLoS Genet 2014; 10:e1004605; PMID:25210889
  • Lei K, Zhang X, Ding X, Guo X, Chen M, Zhu B, Xu T, Zhuang Y, Xu R, Han M. SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci U S A 2009; 106:10207-12; PMID:19509342; http://dx.doi.org/10.1073/pnas.0812037106
  • Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M. Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 2007; 134:901-8; PMID:17267447; http://dx.doi.org/10.1242/dev.02783
  • Bruusgaard JC, Liestol K, Ekmark M, Kollstad K, Gundersen K. Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J Physiol 2003; 551:467-78; PMID:12813146; http://dx.doi.org/10.1113/jphysiol.2003.045328
  • Folker ES, Baylies MK. Nuclear positioning in muscle development and disease. Front Physiol 2013; 4:363; PMID:24376424; http://dx.doi.org/10.3389/fphys.2013.00363
  • Cadot B, Gache V, Vasyutina E, Falcone S, Birchmeier C, Gomes ER. Nuclear movement during myotube formation is microtubule and dynein dependent and is regulated by Cdc42, Par6 and Par3. EMBO Rep 2012; 13:741-9; PMID:22732842; http://dx.doi.org/10.1038/embor.2012.89
  • Metzger T, Gache V, Xu M, Cadot B, Folker ES, Richardson BE, Gomes ER, Baylies MK. MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 2012; 484:120-4; PMID:22425998; http://dx.doi.org/10.1038/nature10914
  • Wilson MH, Holzbaur EL. Opposing microtubule motors drive robust nuclear dynamics in developing muscle cells. J Cell Sci 2012; 125:4158-69; PMID:22623723; http://dx.doi.org/10.1242/jcs.108688
  • Folker ES, Schulman VK, Baylies MK. Muscle length and myonuclear position are independently regulated by distinct Dynein pathways. Development 2012; 139:3827-37; PMID:22951643; http://dx.doi.org/10.1242/dev.079178
  • Capers CR. Multinucleation of skeletal muscle in vitro. J Biophys Biochem Cytol 1960; 7:559-66; PMID:13807523; http://dx.doi.org/10.1083/jcb.7.3.559
  • Hughes SM, Blau HM. Migration of myoblasts across basal lamina during skeletal muscle development. Nature 1990; 345:350-3; PMID:2111464; http://dx.doi.org/10.1038/345350a0
  • Abmayr SM, Pavlath GK. Myoblast fusion: lessons from flies and mice. Development 2012; 139:641-56; PMID:22274696; http://dx.doi.org/10.1242/dev.068353
  • Hill E, Boontheekul T, Mooney DJ. Designing scaffolds to enhance transplanted myoblast survival and migration. Tissue Eng 2006; 12:1295-304; PMID:16771642; http://dx.doi.org/10.1089/ten.2006.12.1295
  • Skuk D, Goulet M, Tremblay JP. Transplanted myoblasts can migrate several millimeters to fuse with damaged myofibers in nonhuman primate skeletal muscle. J Neuropathol Exp Neurol 2011; 70:770-8; PMID:21865885; http://dx.doi.org/10.1097/NEN.0b013e31822a6baa
  • Li R, Gundersen GG. Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat Rev Mol Cell Biol 2008; 9:860-73; PMID:18946475; http://dx.doi.org/10.1038/nrm2522
  • Luxton GW, Gundersen GG. Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 2011; 23:579-88; PMID:21885270; http://dx.doi.org/10.1016/j.ceb.2011.08.001
  • Vaz R, Martins GG, Thorsteinsdottir S, Rodrigues G. Fibronectin promotes migration, alignment and fusion in an in vitro myoblast cell model. Cell Tissue Res 2012; 348:569-78; PMID:22427060; http://dx.doi.org/10.1007/s00441-012-1364-1
  • Schmoranzer J, Fawcett JP, Segura M, Tan S, Vallee RB, Pawson T, Gundersen GG. Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr Biol 2009; 19:1065-74; PMID:19540120; http://dx.doi.org/10.1016/j.cub.2009.05.065
  • Cencetti F, Bruno G, Blescia S, Bernacchioni C, Bruni P, Donati C. Lysophosphatidic acid stimulates cell migration of satellite cells. A role for the sphingosine kinase/sphingosine 1-phosphate axis. FEBS J 2014; 281:4467-78; PMID:25131845; http://dx.doi.org/10.1111/febs.12955
  • Palazzo AF, Joseph HL, Chen YJ, Dujardin DL, Alberts AS, Pfister KK, Vallee RB, Gundersen GG. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol 2001; 11:1536-41; PMID:11591323; http://dx.doi.org/10.1016/S0960-9822(01)00475-4
  • 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
  • Schultz E, Jaryszak DL, Valliere CR. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 1985; 8:217-22; PMID:4058466; http://dx.doi.org/10.1002/mus.880080307
  • Elric J, Etienne-Manneville S. Centrosome positioning in polarized cells: Common themes and variations. Exp Cell Res 2014; PMID:25218948
  • Jansen KM, Pavlath GK. Molecular control of mammalian myoblast fusion. Methods Mol Biol 2008; 475:115-33; PMID:18979241; http://dx.doi.org/10.1007/978-1-59745-250-2_7
  • Goetsch KP, Myburgh KH, Niesler CU. In vitro myoblast motility models: investigating migration dynamics for the study of skeletal muscle repair. J Muscle Res Cell Motil 2013; 34:333-47; PMID:24150600; http://dx.doi.org/10.1007/s10974-013-9364-7
  • Bondesen BA, Jones KA, Glasgow WC, Pavlath GK. Inhibition of myoblast migration by prostacyclin is associated with enhanced cell fusion. FASEB J 2007; 21:3338-45; PMID:17488951; http://dx.doi.org/10.1096/fj.06-7070com
  • Bentzinger CF, von Maltzahn J, Dumont NA, Stark DA, Wang YX, Nhan K, Frenette J, Cornelison DD, Rudnicki MA. Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. J Cell Biol 2014; 205:97-111; PMID:24711502; http://dx.doi.org/10.1083/jcb.201310035
  • Gomes ER, Gundersen GG. Real-time centrosome reorientation during fibroblast migration. Methods Enzymol 2006; 406:579-92; PMID:16472689; http://dx.doi.org/10.1016/S0076-6879(06)06045-9

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