Differential basal-to-apical accessibility of lamin A/C epitopes in the nuclear lamina regulated by changes in cytoskeletal tension

Nature Materials

Volumn 14, Issue 12, 2015, Pages 1252-1261

  Ihalainen, Teemu O ^a,b   Aires, Lina ^a   Herzog, Florian A ^a   Schwartlander, Ruth ^a   Moeller, Jens ^a   Vogel, Viola ^a  

^a ETH ZURICH   (Switzerland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CELL CULTURE; PROTEINS; STEM CELLS;

COMPRESSIVE FORCES; CONFORMATIONAL EPITOPES; ENVIRONMENTAL CONDITIONS; HUMAN MESENCHYMAL STEM CELLS; MICROENVIRONMENTS; NUCLEAR ENVELOPE; POLYACRYLAMIDE HYDROGELS; STRUCTURAL POLARIZATION;

EPITOPES;

BIOPOLYMER; LAMIN A; LMNA PROTEIN, HUMAN;

CHEMISTRY; CYTOSKELETON; HUMAN; METABOLISM; NUCLEAR LAMINA; PROTEIN CONFORMATION;

BIOPOLYMERS; CYTOSKELETON; HUMANS; LAMIN TYPE A; NUCLEAR LAMINA; PROTEIN CONFORMATION;

EID: 84947870719     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat4389     Document Type: Article

References (50)

1. Swift, J. et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
2. Jaalouk, D. E. & Lammerding, J. Mechanotransduction gone awry. Nature Rev. Mol. Cell Biol. 10, 63-73 (2009).
3. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nature Rev. Mol. Cell Biol. 7, 265-275 (2006).
4. Trappmann, B. et al. Extracellular-matrix tethering regulates stem-cell fate. Nature Mater. 11, 642-649 (2012).
5. Wang, N., Tytell, J. D. & Ingber, D. E. Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nature Rev. Mol. Cell Biol. 10, 75-82 (2009).
6. Sosa, B. A., Rothballer, A., Kutay, U. & Schwartz, T. U. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 149, 1035-1047 (2012).
7. Crisp, M. et al. Coupling of the nucleus and cytoplasm: Role of the LINC complex. J. Cell Biol. 172, 41-53 (2006).
8. Isermann, P. & Lammerding, J. Nuclear mechanics and mechanotransduction in health and disease. Curr. Biol. 23, R1113-R1121 (2013).
9. Aebi, U., Cohn, J., Buhle, L. & Gerace, L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323, 560-564 (1986).
10. Gerace, L. & Huber, M. D. Nuclear lamina at the crossroads of the cytoplasm and nucleus. J. Struct. Biol. 177, 24-31 (2012).
11. Senda, T., Iizuka-Kogo, A. & Shimomura, A. Visualization of the nuclear lamina in mouse anterior pituitary cells and immunocytochemical detection of lamin A/C by quick-freeze freeze-substitution electron microscopy. J. Histochem. Cytochem. 53, 497-507 (2005).
12. Dechat, T., Adam, S. A., Taimen, P., Shimi, T. & Goldman, R. D. Nuclear lamins. Cold Spring Harb. Perspect. Biol. 2, a000547 (2010).
13. Lammerding, J. et al. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281, 25768-25780 (2006).
14. Solovei, I. et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584-598 (2013).
15. Guilluy, C. et al. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nature Cell Biol. 16, 376-381 (2014).
16. Stuurman, N., Sasse, B. & Fisher, P. A. Intermediate filament protein polymerization: Molecular analysis of Drosophila nuclear lamin head-to-tail binding. J. Struct. Biol. 117, 1-15 (1996).
17. Heitlinger, E. et al. The role of the head and tail domain in lamin structure and assembly: Analysis of bacterially expressed chicken lamin A and truncated B2 lamins. J. Struct. Biol. 108, 74-89 (1992).
18. Strelkov, S. V., Schumacher, J., Burkhard, P., Aebi, U. & Herrmann, H. Crystal structure of the human lamin A coil 2B dimer: Implications for the head-to-tail association of nuclear lamins. J. Mol. Biol. 343, 1067-1080 (2004).
19. Kapinos, L. E. et al. Characterization of the head-to-tail overlap complexes formed by human lamin A, B1 and B2 "half-minilamin" dimers.J. Mol. Biol. 396, 719-731 (2010).
20. Khatau, S. B. et al. A perinuclear actin cap regulates nuclear shape. Proc. Natl Acad. Sci. USA 106, 19017-19022 (2009).
21. Kim, D. H. & Wirtz, D. Cytoskeletal tension induces the polarized architecture of the nucleus. Biomaterials 48, 161-172 (2015).
22. Shimi, T. et al. The A- and B-type nuclear lamin networks: Microdomains involved in chromatin organization and transcription. Genes Dev. 22, 3409-3421 (2008).
23. Manilal, S., Randles, K. N., Aunac, C., Nguyen, M. & Morris, G. E. A lamin A/C β-strand containing the site of lipodystrophy mutations is a major surface epitope for a new panel of monoclonal antibodies. Biochim. Biophys. Acta 1671, 87-92 (2004).
24. Isobe, K., Gohara, R., Ueda, T., Takasaki, Y. & Ando, S. The last twenty residues in the head domain of mouse lamin A contain important structural elements for formation of head-to-tail polymers in vitro. Biosci. Biotechnol. Biochem. 71, 1252-1259 (2007).
25. Amendola, M. & van Steensel, B. Mechanisms and dynamics of nuclear lamina-genome interactions. Curr. Opin. Cell Biol. 28, 61-68 (2014).
26. Stierle, V. et al. The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochemistry 42, 4819-4828 (2003).
27. Simon, D. N., Domaradzki, T., Hofmann, W. A. & Wilson, K. L. Lamin A tail modification by SUMO1 is disrupted by familial partial lipodystrophy-causing mutations. Mol. Biol. Cell 24, 342-350 (2013).
28. Collard, J. F., Senecal, J. L. & Raymond, Y. Differential accessibility of the tail domain of nuclear lamin A in interphase and mitotic cells. Biochem. Biophys. Res. Commun. 173, 363-369 (1990).
29. Pelham, R. J. Jr & Wang, Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13661-13665 (1997).
30. Yeung, T. et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005).
31. Kihara, T., Haghparast, S. M., Shimizu, Y., Yuba, S. & Miyake, J. Physical properties of mesenchymal stem cells are coordinated by the perinuclear actin cap. Biochem. Biophys. Res. Commun. 409, 1-6 (2011).
32. Tee, S. Y., Fu, J., Chen, C. S. & Janmey, P. A. Cell shape and substrate rigidity both regulate cell stiffness. Biophys. J. 100, L25-L27 (2011).
33. 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 110, 11349-11354 (2013).
34. Thery, M., Pepin, A., Dressaire, E., Chen, Y. & Bornens, M. Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil. Cytoskeleton 63, 341-355 (2006).
35. Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
36. Li, Q., Kumar, A., Makhija, E. & Shivashankar, G. V. The regulation of dynamic mechanical coupling between actin cytoskeleton and nucleus by matrix geometry. Biomaterials 35, 961-969 (2014).
37. Luxton, G. W., 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 329, 956-959 (2010).
38. Stewart-Hutchinson, P. J., Hale, C. M., Wirtz, D. & Hodzic, D. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell Res. 314, 1892-1905 (2008).
39. Constantinescu, D., Gray, H. L., Sammak, P. J., Schatten, G. P. & Csoka, A. B. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185 (2006).
40. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004).
41. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
42. Ramdas, N. M. & Shivashankar, G. V. Cytoskeletal control of nuclear morphology and chromatin organization. J. Mol. Biol. 427, 695-706 (2015).
43. Taniura, H., Glass, C. & Gerace, L. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol. 131, 33-44 (1995).
44. 0 binds histones H2A and H2B. Proc. Natl Acad. Sci. USA 96, 2852-2857 (1999).
45. Guelen, L. et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951 (2008).
46. Towbin, B. D. et al. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150, 934-947 (2012).
47. Talwar, S., Jain, N. & Shivashankar, G. V. The regulation of gene expression during onset of differentiation by nuclear mechanical heterogeneity. Biomaterials 35, 2411-2419 (2014).
48. Dittmer, T. A. & Misteli, T. The lamin protein family. Genome Biol. 12, 222 (2011).
49. Tse, J. R. & Engler, A. J. Preparation of hydrogel substrates with tunable mechanical properties. Curr. Protoc. Cell Biol. 10, 1-10 (2010).
50. Möller, J., Emge, P., Avalos Vizcarra, I., Kollmannsberger, P. & Vogel, V. Bacterial filamentation accelerates colonization of adhesive spots embedded in biopassive surfaces. New J. Phys. 15, 125016 (2013).