Nuclear Mechanotransduction in Skeletal Muscle
Abstract
:1. Introduction
2. Cytoskeletal Components Relevant for Force Transmission to the Nucleus
2.1. The Perinuclear Actin Network and Muscle Differentiation
2.2. The MTs
2.3. Cytoplasmic IFs
3. Mechanical Linkages between the Cytoskeleton and the Nucleoskeleton
4. The Nuclear Lamina
5. Chromatin-Mediated Mechanoresponse
6. Nuclear Positioning and Mechanotransduction
7. Conclusions and Future Directions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Abmayr, S.M.; Pavlath, G.K. Myoblast fusion: Lessons from flies and mice. Development 2012, 139, 641–656. [Google Scholar] [CrossRef] [Green Version]
- Kirby, T.J.; Lammerding, J. Emerging views of the nucleus as a cellular mechanosensor. Nat. Cell Biol. 2018, 20, 373–381. [Google Scholar] [CrossRef]
- Ato, S.; Kido, K.; Sase, K.; Fujita, S. Response of resistance exercise-induced muscle protein synthesis and skeletal muscle hypertrophy are not enhanced after disuse muscle atrophy in rat. Front. Physiol. 2020, 11, 469. [Google Scholar] [CrossRef] [PubMed]
- Burkholder, T.J. Mechanotransduction in skeletal muscle. Front. Biosci. A J. Virtual Libr. 2007, 12, 174–191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masschelein, E.; D’Hulst, G.; Zvick, J.; Hinte, L.; Soro-Arnaiz, I.; Gorski, T.; von Meyenn, F.; Bar-Nur, O.; De Bock, K. Exercise promotes satellite cell contribution to myofibers in a load-dependent manner. Skelet. Muscle 2020, 10, 21. [Google Scholar] [CrossRef] [PubMed]
- Aureille, J.; Buffière-Ribot, V.; Harvey, B.E.; Boyault, C.; Pernet, L.; Andersen, T.; Bacola, G.; Balland, M.; Fraboulet, S.; Van Landeghem, L.; et al. Nuclear envelope deformation controls cell cycle progression in response to mechanical force. EMBO Rep. 2019, 20. [Google Scholar] [CrossRef]
- Uroz, M.; Wistorf, S.; Serra-Picamal, X.; Conte, V.; Sales-Pardo, M.; Roca-Cusachs, P.; Guimerà, R.; Trepat, X. Regulation of cell cycle progression by cell-cell and cell-matrix forces. Nat. Cell Biol. 2018, 20, 646–654. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, S.; Kaneshige, A.; Kaji, T.; Noguchi, Y.-T.; Takemoto, Y.; Zhang, L.; Tsujikawa, K.; Kokubo, H.; Uezumi, A.; Maehara, K.; et al. Sustained expression of HeyL is critical for the proliferation of muscle stem cells in overloaded muscle. eLife 2019, 8, e48284. [Google Scholar] [CrossRef] [PubMed]
- Dupont, S.; Morsut, L.; Aragona, M.; Enzo, E.; Giulitti, S.; Cordenonsi, M.; Zanconato, F.; Le Digabel, J.; Forcato, M.; Bicciato, S.; et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474, 179–183. [Google Scholar] [CrossRef]
- Elosegui-Artola, A.; Andreu, I.; Beedle, A.E.M.; Lezamiz, A.; Uroz, M.; Kosmalska, A.J.; Oria, R.; Kechagia, J.Z.; Rico-Lastres, P.; Le Roux, A.-L.; et al. Force triggers YAP Nuclear entry by regulating transport across nuclear pores. Cell 2017, 171, 1397–1410.e14. [Google Scholar] [CrossRef] [PubMed]
- Kumar, A.; Mazzanti, M.; Mistrik, M.; Kosar, M.; Beznoussenko, G.V.; Mironov, A.A.; Garrè, M.; Parazzoli, D.; Shivashankar, G.V.; Mironov, A.A.; et al. ATR Mediates a checkpoint at the nuclear envelope in response to mechanical stress. Cell 2014, 158, 633–646. [Google Scholar] [CrossRef] [Green Version]
- Kidiyoor, G.R.; Li, Q.; Bastianello, G.; Bruhn, C.; Giovannetti, I.; Mohamood, A.; Beznoussenko, G.V.; Mironov, A.; Raab, M.; Piel, M.; et al. ATR is essential for preservation of cell mechanics and nuclear integrity during interstitial migration. Nat. Commun. 2020, 11, 4828. [Google Scholar] [CrossRef]
- Itano, N.; Okamoto, S.-I.; Zhang, D.; Lipton, S.A.; Ruoslahti, E. Cell spreading controls endoplasmic and nuclear calcium: A physical gene regulation pathway from the cell surface to the nucleus. Proc. Natl. Acad. Sci. USA 2003, 100, 5181–5186. [Google Scholar] [CrossRef] [Green Version]
- Enyedi, B.; Jelcic, M.; Niethammer, P. The Cell nucleus serves as a mechanotransducer of tissue damage-induced inflammation. Cell 2016, 165, 1160–1170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raab, M.; Gentili, M.; de Belly, H.; Thiam, H.-R.; Vargas, P.; Jimenez, A.J.; Lautenschlaeger, F.; Voituriez, R.; Lennon-Dumenil, A.-M.; Manel, N.; et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 2016, 352, 359–362. [Google Scholar] [CrossRef]
- Chen, N.Y.; Kim, P.H.; Fong, L.G.; Young, S.G. Nuclear membrane ruptures, cell death, and tissue damage in the setting of nuclear lamin deficiencies. Nucleus 2020, 11, 237–249. [Google Scholar] [CrossRef] [PubMed]
- Dahl, K.N.; Ribeiro, A.J.S.; Lammerding, J. Nuclear Shape, mechanics, and mechanotransduction. Circ. Res. 2008, 102, 1307–1318. [Google Scholar] [CrossRef] [Green Version]
- Janota, C.S.; Calero-Cuenca, F.J.; Gomes, E.R. The role of the cell nucleus in mechanotransduction. Curr. Opin. Cell Biol. 2020, 63, 204–211. [Google Scholar] [CrossRef]
- Enyedi, B.; Niethammer, P. Nuclear membrane stretch and its role in mechanotransduction. Nucleus 2017, 8, 156–161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stephens, A.D.; Banigan, E.J.; Adam, S.A.; Goldman, R.D.; Marko, J.F. Chromatin and lamin A determine two different mechanical response regimes of the cell nucleus. Mol. Biol. Cell 2017, 28, 1984–1996. [Google Scholar] [CrossRef]
- Stephens, A.D.; Banigan, E.J.; Marko, J.F. Separate roles for chromatin and lamins in nuclear mechanics. Nucleus 2018, 9, 119–124. [Google Scholar] [CrossRef] [Green Version]
- Nava, M.M.; Miroshnikova, Y.A.; Biggs, L.C.; Whitefield, D.B.; Metge, F.; Boucas, J.; Vihinen, H.; Jokitalo, E.; Li, X.; García Arcos, J.M.; et al. Heterochromatin-Driven nuclear softening protects the genome against mechanical stress-induced damage. Cell 2020, 181, 800–817.e22. [Google Scholar] [CrossRef] [PubMed]
- Stephens, A.D.; Banigan, E.J.; Marko, J.F. Chromatin’s physical properties shape the nucleus and its functions. Curr. Opin. Cell Biol. 2019, 58, 76–84. [Google Scholar] [CrossRef]
- Flück, M.; Hoppeler, H. Molecular basis of skeletal muscle plasticity—From gene to form and function. Rev. Physiol. Biochem. Pharmacol. 2003, 146, 159–216. [Google Scholar] [PubMed]
- Martino, F.; Perestrelo, A.R.; Vinarský, V.; Pagliari, S.; Forte, G. Cellular mechanotransduction: From tension to function. Front. Physiol. 2018, 9, 824. [Google Scholar] [CrossRef]
- Essawy, N.; Samson, C.; Petitalot, A.; Moog, S.; Bigot, A.; Herrada, I.; Marcelot, A.; Arteni, A.-A.; Coirault, C.; Zinn-Justin, S. An emerin LEM-domain mutation Impairs cell response to mechanical stress. Cells 2019, 8, 570. [Google Scholar] [CrossRef] [Green Version]
- Roman, W.; Martins, J.P.; Carvalho, F.A.; Voituriez, R.; Abella, J.V.G.; Santos, N.C.; Cadot, B.; Way, M.; Gomes, E.R. Myofibril contraction and crosslinking drive nuclear movement to the periphery of skeletal muscle. Nat. Cell Biol. 2017, 19, 1189–1201. [Google Scholar] [CrossRef]
- Fischer, M.; Rikeit, P.; Knaus, P.; Coirault, C. YAP-mediated mechanotransduction in skeletal muscle. Front. Physiol. 2016, 7. [Google Scholar] [CrossRef]
- Owens, D.J.; Fischer, M.; Jabre, S.; Moog, S.; Mamchaoui, K.; Butler-Browne, G.; Coirault, C. Lamin Mutations cause increased YAP Nuclear entry in muscle stem cells. Cells 2020, 9, 816. [Google Scholar] [CrossRef] [Green Version]
- Jorgenson, K.W.; Phillips, S.M.; Hornberger, T.A. Identifying the Structural adaptations that drive the mechanical load-induced growth of skeletal muscle: A Scoping review. Cells 2020, 9, 1658. [Google Scholar] [CrossRef]
- Owens, D.J.; Messeant, J.; Moog, S.; Viggars, M.; Ferry, A.; Mamchaoui, K.; Lacene, E.; Romero, N.; Brull, A.; Bonne, G.; et al. Lamin-Related congenital muscular dystrophy alters mechanical signaling and skeletal muscle growth. Int. J. Mol. Sci. 2020, 22, 306. [Google Scholar] [CrossRef]
- D’Alessandro, M.; Hnia, K.; Gache, V.; Koch, C.; Gavriilidis, C.; Rodriguez, D.; Nicot, A.-S.; Romero, N.B.; Schwab, Y.; Gomes, E.; et al. Amphiphysin 2 Orchestrates nucleus positioning and shape by linking the nuclear envelope to the actin and microtubule cytoskeleton. Dev. Cell 2015, 35, 186–198. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.-K.; Louhghalam, A.; Lee, G.; Schafer, B.W.; Wirtz, D.; Kim, D.-H. Nuclear lamin A/C harnesses the perinuclear apical actin cables to protect nuclear morphology. Nat. Commun. 2017, 8, 2123. [Google Scholar] [CrossRef]
- Heo, S.-J.; Driscoll, T.P.; Thorpe, S.D.; Nerurkar, N.L.; Baker, B.M.; Yang, M.T.; Chen, C.S.; Lee, D.A.; Mauck, R.L. Differentiation alters stem cell nuclear architecture, mechanics, and mechano-sensitivity. eLife 2016, 5, e18207. [Google Scholar] [CrossRef]
- Onuh, J.O.; Qiu, H. Serum response factor-cofactor interactions and their implications in disease. FEBS J. 2020. [Google Scholar] [CrossRef] [PubMed]
- Watt, K.I.; Goodman, C.A.; Hornberger, T.A.; Gregorevic, P. The Hippo signaling pathway in the regulation of skeletal muscle mass and function. Exerc. Sport Sci. Rev. 2018, 46, 92–96. [Google Scholar] [CrossRef] [PubMed]
- Gnimassou, O.; Francaux, M.; Deldicque, L. Hippo pathway and skeletal muscle mass regulation in mammals: A controversial relationship. Front. Physiol. 2017, 8, 190. [Google Scholar] [CrossRef] [PubMed]
- Gabriel, B.M.; Hamilton, D.L.; Tremblay, A.M.; Wackerhage, H. The Hippo signal transduction network for exercise physiologists. J. Appl. Physiol. 2016, 120, 1105–1117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maniotis, A.J.; Chen, C.S.; Ingber, D.E. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA 1997, 94, 849–854. [Google Scholar] [CrossRef] [Green Version]
- Wang, N.; Tytell, J.D.; Ingber, D.E. Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 2009, 10, 75–82. [Google Scholar] [CrossRef]
- Zhang, J.; Alisafaei, F.; Nikolić, M.; Nou, X.A.; Kim, H.; Shenoy, V.B.; Scarcelli, G. Nuclear mechanics within intact cells Is regulated by cytoskeletal network and internal nanostructures. Small 2020, 16, 1907688. [Google Scholar] [CrossRef]
- Ramdas, N.M.; Shivashankar, G.V. Cytoskeletal Control of nuclear morphology and chromatin organization. J. Mol. Biol. 2015, 427, 695–706. [Google Scholar] [CrossRef]
- Haque, F.; Mazzeo, D.; Patel, J.T.; Smallwood, D.T.; Ellis, J.A.; Shanahan, C.M.; Shackleton, S. Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J. Biol. Chem. 2010, 285, 3487–3498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crisp, M.; Burke, B. The nuclear envelope as an integrator of nuclear and cytoplasmic architecture. FEBS Lett. 2008, 582, 2023–2032. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crisp, M.; Liu, Q.; Roux, K.; Rattner, J.B.; Shanahan, C.; Burke, B.; Stahl, P.D.; Hodzic, D. Coupling of the nucleus and cytoplasm: Role of the LINC complex. J. Cell Biol. 2006, 172, 41–53. [Google Scholar] [CrossRef] [Green Version]
- Ingber, D.E. Cellular mechanotransduction: Putting all the pieces together again. FASEB J. 2006, 20, 811–827. [Google Scholar] [CrossRef] [PubMed]
- Khatau, S.B.; Hale, C.M.; Stewart-Hutchinson, P.J.; Patel, M.S.; Stewart, C.L.; Searson, P.C.; Hodzic, D.; Wirtz, D. A perinuclear actin cap regulates nuclear shape. Proc. Natl. Acad. Sci. USA 2009, 106, 19017–19022. [Google Scholar] [CrossRef] [Green Version]
- Luxton, G.W.G.; Gomes, E.R.; Folker, E.S.; Vintinner, E.; Gundersen, G.G. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 2010, 329, 956–959. [Google Scholar] [CrossRef] [Green Version]
- Kim, D.-H.; Chambliss, A.B.; Wirtz, D. The multi-faceted role of the actin cap in cellular mechanosensation and mechanotransduction. Soft Matter 2013, 9, 5516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chambliss, A.B.; Khatau, S.B.; Erdenberger, N.; Robinson, D.K.; Hodzic, D.; Longmore, G.D.; Wirtz, D. The LINC-anchored actin cap connects the extracellular milieu to the nucleus for ultrafast mechanotransduction. Sci. Rep. 2013, 3, 1087. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Neelam, S.; Chancellor, T.J.; Li, Y.; Nickerson, J.A.; Roux, K.J.; Dickinson, R.B.; Lele, T.P. Direct force probe reveals the mechanics of nuclear homeostasis in the mammalian cell. Proc. Natl. Acad. Sci. USA 2015, 112, 5720–5725. [Google Scholar] [CrossRef] [Green Version]
- Shiu, J.-Y.; Aires, L.; Lin, Z.; Vogel, V. Nanopillar force measurements reveal actin-cap-mediated YAP mechanotransduction. Nat. Cell Biol. 2018, 20, 262–271. [Google Scholar] [CrossRef]
- Khatau, S.B.; Kusuma, S.; Hanjaya-Putra, D.; Mali, P.; Cheng, L.; Lee, J.S.H.; Gerecht, S.; Wirtz, D. The differential formation of the LINC-Mediated perinuclear actin cap in pluripotent and somatic cells. PLoS ONE 2012, 7, e36689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cadot, B.; Gache, V.; Gomes, E.R. Moving and positioning the nucleus in skeletal muscle—One step at a time. Nucleus 2015, 6, 373–381. [Google Scholar] [CrossRef] [Green Version]
- Falcone, S.; Roman, W.; Hnia, K.; Gache, V.; Didier, N.; Lainé, J.; Auradé, F.; Marty, I.; Nishino, I.; Charlet-Berguerand, N.; et al. N-WASP is required for Amphiphysin-2/BIN 1-dependent nuclear positioning and triad organization in skeletal muscle and is involved in the pathophysiology of centronuclear myopathy. EMBO Mol. Med. 2014, 6, 1455–1475. [Google Scholar] [CrossRef]
- Lloyd, C.M.; Berendse, M.; Lloyd, D.G.; Schevzov, G.; Grounds, M.D. A novel role for non-muscle γ-actin in skeletal muscle sarcomere assembly. Exp. Cell Res. 2004, 297, 82–96. [Google Scholar] [CrossRef] [PubMed]
- Sanger, J.W.; Kang, S.; Siebrands, C.C.; Freeman, N.; Du, A.; Wang, J.; Stout, A.L.; Sanger, J.M. How to build a myofibril. J. Muscle Res. Cell Motil. 2006, 26, 343–354. [Google Scholar] [CrossRef]
- Hotulainen, P.; Lappalainen, P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 2006, 173, 383–394. [Google Scholar] [CrossRef] [Green Version]
- Bains, W.; Ponte, P.; Blau, H.; Kedes, L. Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol. Cell. Biol. 1984, 4, 1449–1453. [Google Scholar] [CrossRef] [Green Version]
- Lin, J.J.; Lin, J.L. Assembly of different isoforms of actin and tropomyosin into the skeletal tropomyosin-enriched microfilaments during differentiation of muscle cells in vitro. J. Cell Biol. 1986, 103, 2173–2183. [Google Scholar] [CrossRef] [Green Version]
- Otey, C.A.; Kalnoski, M.H.; Bulinski, J.C. Immunolocalization of muscle and nonmuscle isoforms of actin in myogenic cells and adult skeletal muscle. Cell Motil. Cytoskelet. 1988, 9, 337–348. [Google Scholar] [CrossRef]
- Craig, S.W.; Pardo, J.V. Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil. 1983, 3, 449–462. [Google Scholar] [CrossRef]
- Rybakova, I.N.; Patel, J.R.; Ervasti, J.M. The Dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell Biol. 2000, 150, 1209–1214. [Google Scholar] [CrossRef]
- Ervasti, J.M. Costameres: The Achilles’ heel of Herculean muscle. J. Biol. Chem. 2003, 278, 13591–13594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pegoraro, A.F.; Janmey, P.; Weitz, D.A. Mechanical properties of the cytoskeleton and cells. Cold Spring Harb. Perspect. Biol. 2017, 9, a022038. [Google Scholar] [CrossRef] [PubMed]
- Musa, H.; Orton, C.; Morrison, E.E.; Peckham, M. Microtubule assembly in cultured myoblasts and myotubes following nocodazole induced microtubule depolymerisation. J. Muscle Res. Cell Motil. 2003, 24, 301–308. [Google Scholar] [CrossRef]
- Becker, R.; Leone, M.; Engel, F. Microtubule Organization in striated muscle cells. Cells 2020, 9, 1395. [Google Scholar] [CrossRef]
- Chang, W.; Worman, H.J.; Gundersen, G.G. Accessorizing and anchoring the LINC complex for multifunctionality. J. Cell Biol. 2015, 208, 11–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Webster, M.; Witkin, K.L.; Cohen-Fix, O. Sizing up the nucleus: Nuclear shape, size and nuclear-envelope assembly. J. Cell Sci. 2009, 122, 1477–1486. [Google Scholar] [CrossRef] [Green Version]
- Starr, D.A. Muscle development: Nucleating Microtubules at the nuclear envelope. Curr. Biol. 2017, 27, R1071–R1073. [Google Scholar] [CrossRef]
- Srsen, V.; Fant, X.; Heald, R.; Rabouille, C.; Merdes, A. Centrosome proteins form an insoluble perinuclear matrix during muscle cell differentiation. BMC Cell Biol. 2009, 10, 28. [Google Scholar] [CrossRef] [Green Version]
- Warren, R.H. Microtubular organization in elongating myogenic cells. J. Cell Biol. 1974, 63, 550–566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pizon, V.; Gerbal, F.; Diaz, C.C.; Karsenti, E. Microtubule-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J. 2005, 24, 3781–3792. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Reuveny, A.; Volk, T. Nesprin provides elastic properties to muscle nuclei by cooperating with spectraplakin and EB1. J. Cell Biol. 2015, 209, 529–538. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mian, I.; Pierre-Louis, W.S.; Dole, N.; Gilberti, R.M.; Dodge-Kafka, K.; Tirnauer, J.S. LKB1 Destabilizes microtubules in myoblasts and Contributes to myoblast differentiation. PLoS ONE 2012, 7, e31583. [Google Scholar] [CrossRef] [Green Version]
- Gundersen, G.G.; Khawaja, S.; Bulinski, J.C. Generation of a stable, posttranslationally modified microtubule array is an early event in myogenic differentiation. J. Cell Biol. 1989, 109, 2275–2288. [Google Scholar] [CrossRef]
- Gimpel, P.; Lee, Y.L.; Sobota, R.M.; Calvi, A.; Koullourou, V.; Patel, R.; Mamchaoui, K.; Nédélec, F.; Shackleton, S.; Schmoranzer, J.; et al. Nesprin-1α-dependent microtubule nucleation from the nuclear envelope via Akap450 is necessary for nuclear positioning in muscle cells. Curr. Biol. 2017, 27, 2999–3009.e9. [Google Scholar] [CrossRef] [Green Version]
- Block, J.; Schroeder, V.; Pawelzyk, P.; Willenbacher, N.; Köster, S. Physical properties of cytoplasmic intermediate filaments. Biochimica et Biophysica Acta (BBA) Mol. Cell Res. 2015, 1853, 3053–3064. [Google Scholar] [CrossRef] [Green Version]
- Fudge, D.S.; Gardner, K.H.; Forsyth, V.T.; Riekel, C.; Gosline, J.M. The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads. Biophys. J. 2003, 85, 2015–2027. [Google Scholar] [CrossRef] [Green Version]
- Kreplak, L.; Bär, H.; Leterrier, J.F.; Herrmann, H.; Aebi, U. Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 2005, 354, 569–577. [Google Scholar] [CrossRef]
- Wagner, O.I.; Rammensee, S.; Korde, N.; Wen, Q.; Leterrier, J.-F.; Janmey, P.A. Softness, strength and self-repair in intermediate filament networks. Exp. Cell Res. 2007, 313, 2228–2235. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.; Coulombe, P.A. Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 2007, 21, 1581–1597. [Google Scholar] [CrossRef] [Green Version]
- Block, J.; Witt, H.; Candelli, A.; Peterman, E.J.G.; Wuite, G.J.L.; Janshoff, A.; Köster, S. Nonlinear loading-rate-dependent force response of individual vimentin intermediate filaments to applied strain. Phys. Rev. Lett. 2017, 118, 048101. [Google Scholar] [CrossRef]
- Lorenz, C.; Forsting, J.; Schepers, A.V.; Kraxner, J.; Bauch, S.; Witt, H.; Klumpp, S.; Köster, S. Lateral Subunit coupling determines intermediate filament mechanics. Phys. Rev. Lett. 2019, 123, 188102. [Google Scholar] [CrossRef] [PubMed]
- Smoler, M.; Coceano, G.; Testa, I.; Bruno, L.; Levi, V. Apparent stiffness of vimentin intermediate filaments in living cells and its relation with other cytoskeletal polymers. Biochimica et Biophysica Acta (BBA) Mol. Cell Res. 2020, 1867, 118726. [Google Scholar] [CrossRef]
- Lammerding, J.; Fong, L.G.; Ji, J.Y.; Reue, K.; Stewart, C.L.; Young, S.G.; Lee, R.T. Lamins A and C but Not Lamin B1 Regulate Nuclear Mechanics. J. Biol. Chem. 2006, 281, 25768–25780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patteson, A.E.; Vahabikashi, A.; Pogoda, K.; Adam, S.A.; Mandal, K.; Kittisopikul, M.; Sivagurunathan, S.; Goldman, A.; Goldman, R.D.; Janmey, P.A. Vimentin protects cells against nuclear rupture and DNA damage during migration. J. Cell Biol. 2019, 218, 4079–4092. [Google Scholar] [CrossRef]
- Hu, J.; Li, Y.; Hao, Y.; Zheng, T.; Gupta, S.K.; Parada, G.A.; Wu, H.; Lin, S.; Wang, S.; Zhao, X.; et al. High stretchability, strength, and toughness of living cells enabled by hyperelastic vimentin intermediate filaments. Proc. Natl. Acad. Sci. USA 2019, 116, 17175–17180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kreplak, L.; Herrmann, H.; Aebi, U. Tensile properties of single desmin intermediate filaments. Biophys. J. 2008, 94, 2790–2799. [Google Scholar] [CrossRef] [Green Version]
- Banwell, B.L. Intermediate filament-related myopathies. Pediatric Neurol. 2001, 24, 257–263. [Google Scholar] [CrossRef]
- Paulin, D.; Huet, A.; Khanamyrian, L.; Xue, Z. Desminopathies in muscle disease. J. Pathol. 2004, 204, 418–427. [Google Scholar] [CrossRef]
- Paulin, D.; Hovhannisyan, Y.; Kasakyan, S.; Agbulut, O.; Li, Z.; Xue, Z. Synemin-related skeletal and cardiac myopathies: An overview of pathogenic variants. Am. J. Physiol. Cell Physiol. 2020, 318, C709–C718. [Google Scholar] [CrossRef] [PubMed]
- Capetanaki, Y.; Bloch, R.J.; Kouloumenta, A.; Mavroidis, M.; Psarras, S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp. Cell Res. 2007, 313, 2063–2076. [Google Scholar] [CrossRef] [PubMed]
- Sejersen, T.; Lendahl, U. Transient expression of the intermediate filament nestin during skeletal muscle development. J. Cell Sci. 1993, 106, 1291–1300. [Google Scholar]
- Lazarides, E.; Hubbard, B.D. Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proc. Natl. Acad. Sci. USA 1976, 73, 4344–4348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mermelstein, C.S.; Andrade, L.R.; Portilho, D.M.; Costa, M.L. Desmin filaments are stably associated with the outer nuclear surface in chick myoblasts. Cell Tissue Res. 2006, 323, 351–357. [Google Scholar] [CrossRef] [PubMed]
- Wilhelmsen, K.; Litjens, S.H.; Kuikman, I.; Tshimbalanga, N.; Janssen, H.; van den Bout, I.; Raymond, K.; Sonnenberg, A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 2005, 171, 799–810. [Google Scholar] [CrossRef]
- Lazarides, E. Intermediate filaments as mechanical integrators of cellular space. Nature 1980, 283, 249–256. [Google Scholar] [CrossRef]
- Capetanaki, Y. Desmin cytoskeleton A Potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc. Med. 2002, 12, 339–348. [Google Scholar] [CrossRef]
- Reipert, S. Association of mitochondria with plectin and desmin intermediate filaments in striated muscle. Exp. Cell Res. 1999, 252, 479–491. [Google Scholar] [CrossRef] [PubMed]
- Winter, D.L.; Paulin, D.; Mericskay, M.; Li, Z. Posttranslational modifications of desmin and their implication in biological processes and pathologies. Histochem. Cell Biol. 2014, 141, 1–16. [Google Scholar] [CrossRef]
- Snider, N.T.; Omary, M.B. Post-translational modifications of intermediate filament proteins: Mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2014, 15, 163–177. [Google Scholar] [CrossRef] [Green Version]
- Gao, Q.Q.; McNally, E.M. The Dystrophin Complex: Structure, Function, and Implications for Therapy. In Comprehensive Physiology; Terjung, R., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2015; pp. 1223–1239. [Google Scholar]
- Boudriau, S.; Vincent, M.; Côté, C.H.; Rogers, P.A. Cytoskeletal structure of skeletal muscle: Identification of an intricate exosarcomeric microtubule lattice in slow- and fast-twitch muscle fibers. J. Histochem. Cytochem. 1993, 41, 1013–1021. [Google Scholar] [CrossRef]
- Wang, K.; Ramirez-Mitchell, R. A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J. Cell Biol. 1983, 96, 562–570. [Google Scholar] [CrossRef]
- Li, Z.; Colucci-Guyon, E.; Pinçon-Raymond, M.; Mericskay, M.; Pournin, S.; Paulin, D.; Babinet, C. Cardiovascular lesions and Skeletal myopathy in mice lacking desmin. Dev. Biol. 1996, 175, 362–366. [Google Scholar] [CrossRef] [Green Version]
- Price, M.G. Molecular analysis of intermediate filament cytoskeleton—A putative load-bearing structure. Am. J. Physiol. 1984, 246, H566–H572. [Google Scholar] [CrossRef] [PubMed]
- Galou, M.; Gao, J.; Humbert, J.; Mericskay, M.; Li, Z.; Paulin, D.; Vicart, P. The importance of intermediate filaments in the adaptation of tissues to mechanical stress: Evidence from gene knockout studies. Biol. Cell 1997, 89, 85–97. [Google Scholar] [CrossRef]
- Tolstonog, G.V.; Sabasch, M.; Traub, P. Cytoplasmic Intermediate filaments are stably associated with nuclear matrices and potentially modulate their DNA-binding function. DNA Cell Biol. 2002, 21, 213–239. [Google Scholar] [CrossRef] [PubMed]
- Boriek, A.M.; Capetanaki, Y.; Hwang, W.; Officer, T.; Badshah, M.; Rodarte, J.; Tidball, J.G. Desmin integrates the three-dimensional mechanical properties of muscles. Am. J. Physiol. Cell Physiol. 2001, 280, C46–C52. [Google Scholar] [CrossRef] [PubMed]
- Heffler, J.; Shah, P.P.; Robison, P.; Phyo, S.; Veliz, K.; Uchida, K.; Bogush, A.; Rhoades, J.; Jain, R.; Prosser, B.L. A Balance between intermediate filaments and microtubules maintains nuclear architecture in the cardiomyocyte. Circ. Res. 2020, 126, e10–e26. [Google Scholar] [CrossRef] [PubMed]
- Langer, H.T.; Mossakowski, A.A.; Willis, B.J.; Grimsrud, K.N.; Wood, J.A.; Lloyd, K.C.K.; Zbinden-Foncea, H.; Baar, K. Generation of desminopathy in rats using CRISPR-Cas9. J. Cachexiasarcopenia Muscle 2020. [Google Scholar] [CrossRef]
- Starr, D.A.; Fridolfsson, H.N. Interactions Between nuclei and the cytoskeleton are mediated by SUN-KASH Nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 2010, 26, 421–444. [Google Scholar] [CrossRef] [Green Version]
- Lombardi, M.L.; Lammerding, J. Keeping the LINC: The importance of nucleocytoskeletal coupling in intracellular force transmission and cellular function. Biochem. Soc. Trans. 2011, 39, 1729–1734. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Torbati, M.; Lele, T.P.; Agrawal, A. An unresolved LINC in the nuclear envelope. Cell. Mol. Bioeng. 2016, 9, 252–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Q.; Skepper, J.N.; Yang, F.; Davies, J.D.; Hegyi, L.; Roberts, R.G.; Weissberg, P.L.; Ellis, J.A.; Shanahan, C.M. Nesprins: A novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 2001, 114, 4485–4498. [Google Scholar] [PubMed]
- Roux, K.J.; Crisp, M.L.; Liu, Q.; Kim, D.; Kozlov, S.; Stewart, C.L.; Burke, B. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc. Natl. Acad. Sci. USA 2009, 106, 2194–2199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Randles, K.N.; Lam, L.T.; Sewry, C.A.; Puckelwartz, M.; Furling, D.; Wehnert, M.; McNally, E.M.; Morris, G.E. Nesprins, but not sun proteins, switch isoforms at the nuclear envelope during muscle development. Dev. Dyn. 2010, 239, 998–1009. [Google Scholar] [CrossRef] [Green Version]
- Holt, I.; Fuller, H.R.; Lam, L.T.; Sewry, C.A.; Shirran, S.L.; Zhang, Q.; Shanahan, C.M.; Morris, G.E. Nesprin-1-alpha2 associates with kinesin at myotube outer nuclear membranes, but is restricted to neuromuscular junction nuclei in adult muscle. Sci. Rep. 2019, 9, 14202. [Google Scholar] [CrossRef] [Green Version]
- Wilson, M.H.; Holzbaur, E.L.F. Nesprins anchor kinesin-1 motors to the nucleus to drive nuclear distribution in muscle cells. Development 2015, 142, 218–228. [Google Scholar] [CrossRef] [Green Version]
- Chapman, M.A.; Zhang, J.; Banerjee, I.; Guo, L.T.; Zhang, Z.; Shelton, G.D.; Ouyang, K.; Lieber, R.L.; Chen, J. Disruption of both nesprin 1 and desmin results in nuclear anchorage defects and fibrosis in skeletal muscle. Hum. Mol. Genet. 2014, 23, 5879–5892. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q. Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J. Cell Sci. 2005, 118, 673–687. [Google Scholar] [CrossRef] [Green Version]
- Tapley, E.C.; Starr, D.A. Connecting the nucleus to the cytoskeleton by SUN–KASH bridges across the nuclear envelope. Curr. Opin. Cell Biol. 2013, 25, 57–62. [Google Scholar] [CrossRef] [Green Version]
- Rajgor, D.; Mellad, J.A.; Autore, F.; Zhang, Q.; Shanahan, C.M. Multiple novel nesprin-1 and nesprin-2 Variants act as versatile tissue-specific intracellular scaffolds. PLoS ONE 2012, 7, e40098. [Google Scholar] [CrossRef] [Green Version]
- Puckelwartz, M.J.; Kessler, E.; Zhang, Y.; Hodzic, D.; Randles, K.N.; Morris, G.; Earley, J.U.; Hadhazy, M.; Holaska, J.M.; Mewborn, S.K.; et al. Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice. Hum. Mol. Genet. 2009, 18, 607–620. [Google Scholar] [CrossRef] [Green Version]
- 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, 901–908. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.; Felder, A.; Liu, Y.; Guo, L.T.; Lange, S.; Dalton, N.D.; Gu, Y.; Peterson, K.L.; Mizisin, A.P.; Shelton, G.D.; et al. Nesprin 1 is critical for nuclear positioning and anchorage. Hum. Mol. Genet. 2010, 19, 329–341. [Google Scholar] [CrossRef] [Green Version]
- Duong, N.T.; Morris, G.E.; Lam, L.T.; Zhang, Q.; Sewry, C.A.; Shanahan, C.M.; Holt, I. Nesprins: Tissue-specific expression of epsilon and other short isoforms. PLoS ONE 2014, 9, e94380. [Google Scholar] [CrossRef] [Green Version]
- Mislow, J.M.K.; Holaska, J.M.; Kim, M.S.; Lee, K.K.; Segura-Totten, M.; Wilson, K.L.; McNally, E.M. Nesprin-1α self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 2002, 525, 135–140. [Google Scholar] [CrossRef] [Green Version]
- Wheeler, M.A.; Davies, J.D.; Zhang, Q.; Emerson, L.J.; Hunt, J.; Shanahan, C.M.; Ellis, J.A. Distinct functional domains in nesprin-1α and nesprin-2β bind directly to emerin and both interactions are disrupted in X-linked Emery–Dreifuss muscular dystrophy. Exp. Cell Res. 2007, 313, 2845–2857. [Google Scholar] [CrossRef]
- Holt, I.; Duong, N.T.; Zhang, Q.; Lam, L.T.; Sewry, C.A.; Mamchaoui, K.; Shanahan, C.M.; Morris, G.E. Specific localization of nesprin-1-α2, the short isoform of nesprin-1 with a KASH domain, in developing, fetal and regenerating muscle, using a new monoclonal antibody. BMC Cell Biol. 2016, 17, 26. [Google Scholar] [CrossRef] [Green Version]
- Roman, W.; Gomes, E.R. Nuclear positioning in skeletal muscle. Semin. Cell Dev. Biol. 2018, 82, 51–56. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Rao, L.; Shanahan, C.M.; Zhang, Q. Nesprin-1/2: Roles in nuclear envelope organisation, myogenesis and muscle disease. Biochem. Soc. Trans. 2018, 46, 311–320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, L.; Qu, R.; Ouang, J.; Dai, J. A glance at the nuclear envelope spectrin repeat protein 3. Biomed Res. Int. 2019, 2019, 1651805. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ketema, M.; Wilhelmsen, K.; Kuikman, I.; Janssen, H.; Hodzic, D.; Sonnenberg, A. Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J. Cell Sci. 2007, 120, 3384–3394. [Google Scholar] [CrossRef] [Green Version]
- Wiche, G. Role of plectin in cytoskeleton organization and dynamics. J. Cell Sci. 1998, 111, 2477–2486. [Google Scholar]
- Staszewska, I.; Fischer, I.; Wiche, G. Plectin isoform 1-dependent nuclear docking of desmin networks affects myonuclear architecture and expression of mechanotransducers. Hum. Mol. Genet. 2015, 24, 7373–7389. [Google Scholar] [CrossRef] [Green Version]
- Folker, E.S.; Östlund, C.; Luxton, G.W.G.; Worman, H.J.; Gundersen, G.G. Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc. Natl. Acad. Sci. USA 2011, 108, 131–136. [Google Scholar] [CrossRef] [Green Version]
- Ho, C.Y.; Lammerding, J. Lamins at a glance. J. Cell Sci. 2012, 125, 2087–2093. [Google Scholar] [CrossRef] [Green Version]
- Hieda, M. Signal Transduction across the Nuclear envelope: Role of the LINC complex in bidirectional signaling. Cells 2019, 8, 124. [Google Scholar] [CrossRef] [Green Version]
- Burke, B.; Roux, K.J. Nuclei Take a position: Managing nuclear location. Dev. Cell 2009, 17, 587–597. [Google Scholar] [CrossRef] [Green Version]
- Fridolfsson, H.N.; Ly, N.; Meyerzon, M.; Starr, D.A. UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev. Biol. 2010, 338, 237–250. [Google Scholar] [CrossRef] [Green Version]
- Jain, N.; Iyer, K.V.; Kumar, A.; Shivashankar, G.V. Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. Proc. Natl. Acad. Sci. USA 2013, 110, 11349–11354. [Google Scholar] [CrossRef] [Green Version]
- 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. USA 2009, 106, 10207–10212. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.K.; Umeshima, H.; Kurisu, J.; Kengaku, M. Nesprins and opposing microtubule motors generate a point force that drives directional nuclear motion in migrating neurons. Development 2018, 145, dev158782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kengaku, M. Cytoskeletal control of nuclear migration in neurons and non-neuronal cells. Proc. Jpn. Acad. Ser. B 2018, 94, 337–349. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q.; Bethmann, C.; Worth, N.F.; Davies, J.D.; Wasner, C.; Feuer, A.; Ragnauth, C.D.; Yi, Q.; Mellad, J.A.; Warren, D.T.; 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, 2816–2833. [Google Scholar] [CrossRef] [PubMed]
- Stroud, M.J.; Feng, W.; Zhang, J.; Veevers, J.; Fang, X.; Gerace, L.; Chen, J. Nesprin 1α2 is essential for mouse postnatal viability and nuclear positioning in skeletal muscle. J. Cell Biol. 2017, 216, 1915–1924. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Li, C.; Zhou, B.; Sun, H.; Koullourou, V.; Holt, I.; Puckelwartz, M.J.; Warren, D.T.; Hayward, R.; Lin, Z.; et al. Novel nesprin-1 mutations associated with dilated cardiomyopathy cause nuclear envelope disruption and defects in myogenesis. Hum. Mol. Genet. 2017, 26, 2258–2276. [Google Scholar] [CrossRef]
- Schwartz, C.; Fischer, M.; Mamchaoui, K.; Bigot, A.; Lok, T.; Verdier, C.; Duperray, A.; Michel, R.; Holt, I.; Voit, T.; et al. Lamins and nesprin-1 mediate inside-out mechanical coupling in muscle cell precursors through FHOD1. Sci. Rep. 2017, 7, 1253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jahed, Z.; Mofrad, M.R. The nucleus feels the force, LINCed in or not! Curr. Opin. Cell Biol. 2019, 58, 114–119. [Google Scholar] [CrossRef]
- Li, Y.; Lovett, D.; Zhang, Q.; Neelam, S.; Kuchibhotla, R.A.; Zhu, R.; Gundersen, G.G.; Lele, T.P.; Dickinson, R.B. Moving Cell boundaries drive nuclear shaping during cell spreading. Biophys. J. 2015, 109, 670–686. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szczesny, S.E.; Mauck, R.L. The Nuclear option: Evidence Implicating the cell nucleus in mechanotransduction. J. Biomech. Eng. 2017, 139, 021006. [Google Scholar] [CrossRef] [PubMed]
- Aebi, U.; Cohn, J.; Buhle, L.; Gerace, L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 1986, 323, 560–564. [Google Scholar] [CrossRef]
- Turgay, Y.; Eibauer, M.; Goldman, A.E.; Shimi, T.; Khayat, M.; Ben-Harush, K.; Dubrovsky-Gaupp, A.; Sapra, K.T.; Goldman, R.D.; Medalia, O. The molecular architecture of lamins in somatic cells. Nature 2017, 543, 261–264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burke, B.; Stewart, C.L. The nuclear lamins: Flexibility in function. Nat. Rev. Mol. Cell Biol. 2013, 14, 13–24. [Google Scholar] [CrossRef]
- Simon, D.N.; Wilson, K.L. The nucleoskeleton as a genome-associated dynamic ‘network of networks’. Nat. Rev. Mol. Cell Biol. 2011, 12, 695–708. [Google Scholar] [CrossRef]
- Korfali, N.; Wilkie, G.S.; Swanson, S.K.; Srsen, V.; de las Heras, J.; Batrakou, D.G.; Malik, P.; Zuleger, N.; Kerr, A.R.W.; Florens, L.; et al. The nuclear envelope proteome differs notably between tissues. Nucleus 2012, 3, 552–564. [Google Scholar] [CrossRef] [Green Version]
- Hieda, M. Implications for diverse functions of the LINC Complexes based on the structure. Cells 2017, 6, 3. [Google Scholar] [CrossRef] [Green Version]
- Kalinowski, A.; Qin, Z.; Coffey, K.; Kodali, R.; Buehler, M.J.; Lösche, M.; Dahl, K.N. Calcium causes a Conformational change in lamin A Tail domain that promotes farnesyl-mediated membrane association. Biophys. J. 2013, 104, 2246–2253. [Google Scholar] [CrossRef] [Green Version]
- Osmanagic-Myers, S.; Dechat, T.; Foisner, R. Lamins at the crossroads of mechanosignaling. Genes Dev. 2015, 29, 225–237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bianchi, A.; Manti, P.G.; Lucini, F.; Lanzuolo, C. Mechanotransduction, nuclear architecture and epigenetics in Emery Dreifuss Muscular dystrophy: Tous pour un, un pour tous. Nucleus 2018, 9, 321–335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coffinier, C.; Jung, H.J.; Nobumori, C.; Chang, S.; Tu, Y.; Barnes, R.H., 2nd; Yoshinaga, Y.; de Jong, P.J.; Vergnes, L.; Reue, K.; et al. Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons. Mol. Biol. Cell 2011, 22, 4683–4693. [Google Scholar] [CrossRef] [PubMed]
- Dahl, K.N. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 2004, 117, 4779–4786. [Google Scholar] [CrossRef] [Green Version]
- Shimi, T.; Kittisopikul, M.; Tran, J.; Goldman, A.E.; Adam, S.A.; Zheng, Y.; Jaqaman, K.; Goldman, R.D. Structural organization of nuclear lamins A, C, B1, and B2 revealed by superresolution microscopy. Mol. Biol. Cell 2015, 26, 4075–4086. [Google Scholar] [CrossRef] [PubMed]
- Swift, J.; Ivanovska, I.L.; Buxboim, A.; Harada, T.; Dingal, P.C.D.P.; Pinter, J.; Pajerowski, J.D.; Spinler, K.R.; Shin, J.-W.; Tewari, M.; et al. Nuclear lamin-A Scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341, 1240104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buxboim, A.; Irianto, J.; Swift, J.; Athirasala, A.; Shin, J.-W.; Rehfeldt, F.; Discher, D.E. Coordinated increase of nuclear tension and lamin-A with matrix stiffness outcompetes lamin-B receptor that favors soft tissue phenotypes. Mol. Biol. Cell 2017, 28, 3333–3348. [Google Scholar] [CrossRef]
- Guilluy, C.; Burridge, K. Nuclear mechanotransduction: Forcing the nucleus to respond. Nucleus 2015, 6, 19–22. [Google Scholar] [CrossRef] [Green Version]
- Guilluy, C.; Osborne, L.D.; Van Landeghem, L.; Sharek, L.; Superfine, R.; Garcia-Mata, R.; Burridge, K. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 2014, 16, 376–381. [Google Scholar] [CrossRef]
- Bera, M.; Kotamarthi, H.C.; Dutta, S.; Ray, A.; Ghosh, S.; Bhattacharyya, D.; Ainavarapu, S.R.K.; Sengupta, K. Characterization of Unfolding mechanism of human lamin A Ig Fold by single-molecule force spectroscopy—Implications in EDMD. Biochemistry 2014, 53, 7247–7258. [Google Scholar] [CrossRef]
- Buxboim, A.; Swift, J.; Irianto, J.; Spinler, K.R.; Dingal, P.C.D.P.; Athirasala, A.; Kao, Y.-R.C.; Cho, S.; Harada, T.; Shin, J.-W.; et al. Matrix Elasticity regulates lamin-A,C Phosphorylation and turnover with feedback to actomyosin. Curr. Biol. 2014, 24, 1909–1917. [Google Scholar] [CrossRef]
- Xia, Y.; Pfeifer, C.R.; Cho, S.; Discher, D.E.; Irianto, J. Nuclear mechanosensing. Emerg. Top. Life Sci. 2018, 2, 713–725. [Google Scholar]
- Makarov, A.A.; Zou, J.; Houston, D.R.; Spanos, C.; Solovyova, A.S.; Cardenal-Peralta, C.; Rappsilber, J.; Schirmer, E.C. Lamin A molecular compression and sliding as mechanisms behind nucleoskeleton elasticity. Nat. Commun. 2019, 10, 3056. [Google Scholar] [CrossRef] [PubMed]
- Pajerowski, J.D.; Dahl, K.N.; Zhong, F.L.; Sammak, P.J.; Discher, D.E. Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. USA 2007, 104, 15619–15624. [Google Scholar] [CrossRef] [PubMed]
- Guelen, L.; Pagie, L.; Brasset, E.; Meuleman, W.; Faza, M.B.; Talhout, W.; Eussen, B.H.; de Klein, A.; Wessels, L.; de Laat, W.; et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453, 948–951. [Google Scholar] [CrossRef] [PubMed]
- Miroshnikova, Y.A.; Nava, M.M.; Wickström, S.A. Emerging roles of mechanical forces in chromatin regulation. J. Cell Sci. 2017, 130, 2243–2250. [Google Scholar] [CrossRef] [Green Version]
- Le, H.Q.; Ghatak, S.; Yeung, C.-Y.C.; Tellkamp, F.; Günschmann, C.; Dieterich, C.; Yeroslaviz, A.; Habermann, B.; Pombo, A.; Niessen, C.M.; et al. Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment. Nat. Cell Biol. 2016, 18, 864–875. [Google Scholar] [CrossRef]
- Robson, M.I.; de las Heras, J.I.; Czapiewski, R.; Lê Thành, P.; Booth, D.G.; Kelly, D.A.; Webb, S.; Kerr, A.R.W.; Schirmer, E.C. Tissue-specific Gene repositioning by muscle nuclear membrane proteins enhances repression of critical developmental genes during myogenesis. Mol. Cell 2016, 62, 834–847. [Google Scholar] [CrossRef] [Green Version]
- Donnaloja, F.; Carnevali, F.; Jacchetti, E.; Raimondi, M.T. Lamin A/C Mechanotransduction in laminopathies. Cells 2020, 9, 1306. [Google Scholar] [CrossRef]
- Gruenbaum, Y.; Foisner, R. Lamins: Nuclear Intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu. Rev. Biochem. 2015, 84, 131–164. [Google Scholar] [CrossRef]
- Janin, A.; Gache, V. Nesprins and Lamins in health and diseases of cardiac and skeletal muscles. Front. Physiol. 2018, 9, 1277. [Google Scholar] [CrossRef]
- Brull, A.; Morales Rodriguez, B.; Bonne, G.; Muchir, A.; Bertrand, A.T. The Pathogenesis and therapies of striated muscle laminopathies. Front. Physiol. 2018, 9, 1533. [Google Scholar] [CrossRef] [Green Version]
- Quijano-Roy, S.; Mbieleu, B.; Bönnemann, C.G.; Jeannet, P.-Y.; Colomer, J.; Clarke, N.F.; Cuisset, J.-M.; Roper, H.; De Meirleir, L.; D’Amico, A.; et al. De novo LMNA mutations cause a new form of congenital muscular dystrophy. Ann. Neurol. 2008, 64, 177–186. [Google Scholar] [CrossRef] [PubMed]
- Lammerding, J.; Schulze, P.C.; Takahashi, T.; Kozlov, S.; Sullivan, T.; Kamm, R.D.; Stewart, C.L.; Lee, R.T. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Investig. 2004, 113, 370–378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lammerding, J.; Hsiao, J.; Schulze, P.C.; Kozlov, S.; Stewart, C.L.; Lee, R.T. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 2005, 170, 781–791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hale, C.M.; Shrestha, A.L.; Khatau, S.B.; Stewart-Hutchinson, P.J.; Hernandez, L.; Stewart, C.L.; Hodzic, D.; Wirtz, D. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys. J. 2008, 95, 5462–5475. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q.; Tamashunas, A.C.; Agrawal, A.; Torbati, M.; Katiyar, A.; Dickinson, R.B.; Lammerding, J.; Lele, T.P. Local, transient tensile stress on the nuclear membrane causes membrane rupture. Mol. Biol. Cell 2019, 30, 899–906. [Google Scholar] [CrossRef]
- Earle, A.J.; Kirby, T.J.; Fedorchak, G.R.; Isermann, P.; Patel, J.; Iruvanti, S.; Moore, S.A.; Bonne, G.; Wallrath, L.L.; Lammerding, J. Mutant lamins cause nuclear envelope rupture and DNA damage in skeletal muscle cells. Nat. Mater. 2020, 19, 464–473. [Google Scholar] [CrossRef]
- Solovei, I.; Wang, A.S.; Thanisch, K.; Schmidt, C.S.; Krebs, S.; Zwerger, M.; Cohen, T.V.; Devys, D.; Foisner, R.; Peichl, L.; et al. LBR and Lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 2013, 152, 584–598. [Google Scholar] [CrossRef] [Green Version]
- Mattout, A.; Pike, B.L.; Towbin, B.D.; Bank, E.M.; Gonzalez-Sandoval, A.; Stadler, M.B.; Meister, P.; Gruenbaum, Y.; Gasser, S.M. An EDMD mutation in C. elegans Lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr. Biol. 2011, 21, 1603–1614. [Google Scholar] [CrossRef] [Green Version]
- Emerson, L.J.; Holt, M.R.; Wheeler, M.A.; Wehnert, M.; Parsons, M.; Ellis, J.A. Defects in cell spreading and ERK1/2 activation in fibroblasts with lamin A/C mutations. Biochimica et Biophysica Acta (BBA) Mol. Basis Dis. 2009, 1792, 810–821. [Google Scholar] [CrossRef] [Green Version]
- Bertrand, A.T.; Ziaei, S.; Ehret, C.; Duchemin, H.; Mamchaoui, K.; Bigot, A.; Mayer, M.; Quijano-Roy, S.; Desguerre, I.; Lainé, J.; et al. Cellular microenvironments reveal defective mechanosensing responses and elevated YAP signaling in LMNA-mutated muscle precursors. J. Cell Sci. 2014, 127, 2873–2884. [Google Scholar] [CrossRef] [Green Version]
- Furusawa, T.; Rochman, M.; Taher, L.; Dimitriadis, E.K.; Nagashima, K.; Anderson, S.; Bustin, M. Chromatin decompaction by the nucleosomal binding protein HMGN5 impairs nuclear sturdiness. Nat. Commun. 2015, 6, 6138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krause, M.; Te Riet, J.; Wolf, K. Probing the compressibility of tumor cell nuclei by combined atomic force-confocal microscopy. Phys. Biol. 2013, 10, 065002. [Google Scholar] [CrossRef]
- Lherbette, M.; Dos Santos, Á.; Hari-Gupta, Y.; Fili, N.; Toseland, C.P.; Schaap, I.A.T. Atomic force microscopy micro-rheology reveals large structural inhomogeneities in single cell-nuclei. Sci. Rep. 2017, 7, 8116. [Google Scholar] [CrossRef] [PubMed]
- Schäpe, J.; Prausse, S.; Radmacher, M.; Stick, R. Influence of lamin A on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys. J. 2009, 96, 4319–4325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hubner, M.R.; Spector, D.L. Chromatin dynamics. Annu Rev. Biophys. 2010, 39, 471–489. [Google Scholar] [CrossRef]
- Sexton, T.; Schober, H.; Fraser, P.; Gasser, S.M. Gene regulation through nuclear organization. Nat. Struct. Mol. Biol. 2007, 14, 1049–1055. [Google Scholar] [CrossRef]
- Jost, K.L.; Rottach, A.; Milden, M.; Bertulat, B.; Becker, A.; Wolf, P.; Sandoval, J.; Petazzi, P.; Huertas, D.; Esteller, M.; et al. Generation and characterization of rat and mouse monoclonal antibodies specific for MeCP2 and their use in X-inactivation studies. PLoS ONE 2011, 6, e26499. [Google Scholar] [CrossRef] [Green Version]
- Peric-Hupkes, D.; van Steensel, B. Role of the Nuclear lamina in genome organization and gene expression. Cold Spring Harb. Symp. Quant. Biol. 2010, 75, 517–524. [Google Scholar] [CrossRef] [Green Version]
- Schubeler, D.; Francastel, C.; Cimbora, D.M.; Reik, A.; Martin, D.I.; Groudine, M. Nuclear localization and histone acetylation: A pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev. 2000, 14, 940–950. [Google Scholar] [PubMed]
- Thomas, C.H.; Collier, J.H.; Sfeir, C.S.; Healy, K.E. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc. Natl. Acad. Sci. USA 2002, 99, 1972–1977. [Google Scholar] [CrossRef] [Green Version]
- Heo, S.J.; Nerurkar, N.L.; Baker, B.M.; Shin, J.W.; Elliott, D.M.; Mauck, R.L. Fiber stretch and reorientation modulates mesenchymal stem cell morphology and fibrous gene expression on oriented nanofibrous microenvironments. Ann. Biomed. Eng. 2011, 39, 2780–2790. [Google Scholar] [CrossRef] [Green Version]
- Driscoll, T.P.; Cosgrove, B.D.; Heo, S.J.; Shurden, Z.E.; Mauck, R.L. Cytoskeletal to Nuclear strain transfer regulates YAP Signaling in mesenchymal stem cells. Biophys. J. 2015, 108, 2783–2793. [Google Scholar] [CrossRef] [Green Version]
- Banerjee, I.; Zhang, J.; Moore-Morris, T.; Pfeiffer, E.; Buchholz, K.S.; Liu, A.; Ouyang, K.; Stroud, M.J.; Gerace, L.; Evans, S.M.; et al. Targeted ablation of nesprin 1 and nesprin 2 from murine myocardium results in cardiomyopathy, altered nuclear morphology and inhibition of the biomechanical gene response. PLoS Genet. 2014, 10, e1004114. [Google Scholar] [CrossRef] [Green Version]
- Martins, R.P.; Finan, J.D.; Guilak, F.; Lee, D.A. Mechanical regulation of nuclear structure and function. Annu. Rev. Biomed. Eng. 2012, 14, 431–455. [Google Scholar] [CrossRef] [Green Version]
- Jakkaraju, S.; Zhe, X.; Pan, D.; Choudhury, R.; Schuger, L. TIPs are tension-responsive proteins involved in myogenic versus adipogenic differentiation. Dev. Cell 2005, 9, 39–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tajik, A.; Zhang, Y.; Wei, F.; Sun, J.; Jia, Q.; Zhou, W.; Singh, R.; Khanna, N.; Belmont, A.S.; Wang, N. Transcription upregulation via force-induced direct stretching of chromatin. Nat. Mater. 2016, 15, 1287–1296. [Google Scholar] [CrossRef] [Green Version]
- Folker, E.S.; Baylies, M.K. Nuclear positioning in muscle development and disease. Front. Physiol. 2013, 4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Metzger, T.; Gache, V.; Xu, M.; Cadot, B.; Folker, E.S.; Richardson, B.E.; Gomes, E.R.; Baylies, M.K. MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 2012, 484, 120–124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Azevedo, M.; Baylies, M.K. Getting into position: Nuclear Movement in muscle cells. Trends Cell Biol. 2020, 30, 303–316. [Google Scholar] [CrossRef]
- Romero, N.B. Centronuclear myopathies: A widening concept. Neuromuscul. Disord. 2010, 20, 223–228. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Jabre, S.; Hleihel, W.; Coirault, C. Nuclear Mechanotransduction in Skeletal Muscle. Cells 2021, 10, 318. https://doi.org/10.3390/cells10020318
Jabre S, Hleihel W, Coirault C. Nuclear Mechanotransduction in Skeletal Muscle. Cells. 2021; 10(2):318. https://doi.org/10.3390/cells10020318
Chicago/Turabian StyleJabre, Saline, Walid Hleihel, and Catherine Coirault. 2021. "Nuclear Mechanotransduction in Skeletal Muscle" Cells 10, no. 2: 318. https://doi.org/10.3390/cells10020318