The tethering of chromatin to the nuclear envelope supports nuclear mechanics

Nature Communications

Volumn 6, Issue , 2015, Pages

  Schreiner, Sarah M ^a   Koo, Peter K ^b   Zhao, Yao ^b   Mochrie, Simon G J ^b   King, Megan C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; MEMBRANE; PROTEIN; REACTION KINETICS;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL NUCLEUS MEMBRANE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEPOLYMERIZATION; IN VIVO STUDY; MICROTUBULE; NONHUMAN; NUCLEAR LAMINA; NUCLEAR SHAPE; OPTICAL TWEEZERS; SCANNING ELECTRON MICROSCOPY; WILD TYPE; YEAST CELL; CELL NUCLEUS; CHROMATIN; METABOLISM; SCHIZOSACCHAROMYCES; ULTRASTRUCTURE;

CHROMATIN;

CELL NUCLEUS; CHROMATIN; MICROSCOPY, ELECTRON, SCANNING; NUCLEAR ENVELOPE; NUCLEAR LAMINA; OPTICAL TWEEZERS; SCHIZOSACCHAROMYCES;

EID: 84935835905     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8159     Document Type: Article

References (70)

1. 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 94, 849-854 (1997).
2. Graumann, K., Irons, S. L., Runions, J. & Evans, D. E. Retention and mobility of the mammalian lamin B receptor in the plant nuclear envelope. Biol. Cell 99, 553-562 (2007).
3. Rowat, A. C. et al. Nuclear envelope composition determines the ability of neutrophil-type cells to passage through micron-scale constrictions. J. Biol. Chem. 288, 8610-8618 (2013).
4. Harada, T. et al. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J. Cell Biol. 204, 669-682 (2014).
5. Isermann, P. & Lammerding, J. Nuclear mechanics and mechanotransduction in health and disease. Curr. Biol. 23, R1113-R1121 (2013).
6. Dahl, K., Discher, D. & Wilson, K. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a "molecular shock absorber". Mol. Biol. Cell 15, 119A-120A (2004).
7. Broers, J. L. et al. Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: Implications for the development of laminopathies. Hum. Mol. Genet. 13, 2567-2580 (2004).
8. Lammerding, J. et al. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281, 25768-25780 (2006).
9. Scha?pe, J., Prau-e, S., Radmacher, M. & Stick, R. Influence of lamin A on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys. J. 96, 4319-4325 (2009).
10. Kim, Y. et al. Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334, 1706-1710 (2011).
11. Dahl, K. et al. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 103, 10271-10276 (2006).
12. Verstraeten, V. L., Ji, J. Y., Cummings, K. S., Lee, R. T. & Lammerding, J. Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: Effects of farnesyltransferase inhibitors. Aging Cell 7, 383-393 (2008).
13. Sullivan, T. et al. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147, 913-920 (1999).
14. Swift, J. et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
15. Banerjee, A. et al. Viscoelastic behavior of human lamin A proteins in the context of dilated cardiomyopathy. PLoS ONE 8, e83410 (2013).
16. Swift, J. & Discher, D. E. The nuclear lamina is mechano-responsive to ECM elasticity in mature tissue. J. Cell Sci. 127, 3005-3015 (2014).
17. Lammerding, J. et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378 (2004).
18. Guelen, L. et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951 (2008).
19. Pickersgill, H. et al. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38, 1005-1014 (2006).
20. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. & Wilson, K. L. The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31 (2005).
21. Dauer, W. T. & Worman, H. J. The nuclear envelope as a signaling node in development and disease. Dev. Cell 17, 626-638 (2009).
22. Zuleger, N. et al. Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol. 14, R14 (2013).
23. Malik, P. et al. Cell-specific and lamin-dependent targeting of novel transmembrane proteins in the nuclear envelope. Cell Mol. Life Sci. 67, 1353-1369 (2010).
24. Guo, Y., Kim, Y., Shimi, T., Goldman, R. D. & Zheng, Y. Concentrationdependent lamin assembly and its roles in the localization of other nuclear proteins. Mol. Biol. Cell 25, 1287-1297 (2014).
25. Mans, B. J., Anantharaman, V., Aravind, L. & Koonin, E. V. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3, 1612-1637 (2004).
26. King, M. C., Lusk, C. P. & Blobel, G. Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003-1007 (2006).
27. Yewdell, W. T., Colombi, P., Makhnevych, T. & Lusk, C. P. Lumenal interactions in nuclear pore complex assembly and stability. Mol. Biol. Cell 22, 1375-1388 (2011).
28. Gonzalez, Y., Saito, A. & Sazer, S. Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina. Nucleus 3, 60-76 (2012).
29. King, M., Drivas, T., Blobel, G. & Blobel, G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134, 427-438 (2008).
30. Buch, C. et al. An integral protein of the inner nuclear membrane localizes to the mitotic spindle in mammalian cells. J. Cell Sci. 122, 2100-2107 (2009).
31. Hiraoka, Y. et al. Inner nuclear membrane protein Ima1 is dispensable for intranuclear positioning of centromeres. Genes Cells 16, 1000-1011 (2011).
32. Ding, R. et al. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol. Biol. Cell 8, 1461-1479 (1997).
33. Shimanuki, M. et al. A novel fission yeast gene, kms1, is required for the formation of meiotic prophase-specific nuclear architecture. Mol. Gen. Genet. 254, 238-249 (1997).
34. Wa?lde, S. & King, M. C. The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body. J Cell Sci. 127, 3625 (2014).
35. Sawin, K. & Tran, P. T. Cytoplasmic microtubule organization in fission yeast. Yeast 23, 1001-1014 (2006).
36. Tran, P. T. et al. A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J. Cell Biol. 153, 397-411 (2001).
37. Goto, B., Okazaki, K. & Niwa, O. Cytoplasmic microtubular system implicated in De novo formation of a Rabl-like orientation of chromosomes in fission yeast. J. Cell Sci. 114, 2427-2435 (2001).
38. Funabiki, H., Hagan, I., Uzawa, S. & Yanagida, M. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121, 961-976 (1993).
39. West, R. R., Vaisberg, E. V., Ding, R., Nurse, P. & McIntosh, J. R. cut11(?): A gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. Mol. Biol. Cell 9, 2839-2855 (1998).
40. Rupes, I., Webb, B. A., Mak, A. & Young, P. G. G2/M arrest caused by actin disruption is a manifestation of the cell size checkpoint in fission yeast. Mol. Biol. Cell 12, 3892-3903 (2001).
41. Neumann, F. & Nurse, P. Nuclear size control in fission yeast. J. Cell Biol. 179, 593-600 (2007).
42. Grund, S. E. et al. The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J. Cell Biol. 182, 897-910 (2008).
43. Mekhail, K., Seebacher, J., Gygi, S. P. & Moazed, D. Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456, 667-670 (2008).
44. Steglich, B., Filion, G. J., Van Steensel, B. & Ekwall, K. The inner nuclear membrane proteins Man1 and Ima1 link to two different types of chromatin at the nuclear periphery in S. pombe. Nucleus 3, 77-87 (2012).
45. Marguerat, S. et al. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151, 671-683 (2012).
46. Ishida, M. et al. Intrinsic nucleic acid-binding activity of Chp1 chromodomain is required for heterochromatic gene silencing. Mol. Cell 47, 228-241 (2012).
47. Sadaie, M., Iida, T., Urano, T. & Nakayama, J. A chromodomain protein, Chp1, is required for the establishment of heterochromatin in fission yeast. EMBO J. 23, 3825-3835 (2004).
48. Russell, P. & Nurse, P. Cdc25? functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153 (1986).
49. Rout, M. P. & Kilmartin, J. V. Components of the yeast spindle and spindle pole body. J. Cell Biol. 111, 1913-1927 (1990).
50. Koo, P. K., Setru, S. U. & Mochrie, S. G. Active drift stabilization in three dimensions via image cross-correlation. Rev. Sci. Instrum. 84, 103705 (2013).
51. Guo, M. et al. Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy. Cell 158, 822-832 (2014).
52. Guilluy, C. et al. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16, 376-381 (2014).
53. Dahl, K. et al. Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys. J. 89, 2855-2864 (2005).
54. Rowat, A. C., Foster, L. J., Nielsen, M. M., Weiss, M. & Ipsen, J. H. Characterization of the elastic properties of the nuclear envelope. J. R. Soc. Interface 2, 63-69 (2005).
55. Pajerowski, J. D., Dahl, K., Zhong, F., Sammak, P. & Discher, D. Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl Acad. Sci. USA 104, 15619-15624 (2007).
56. Fujita, I. et al. Telomere-nuclear envelope dissociation promoted by Rap1 phosphorylation ensures faithful chromosome segregation. Curr. Biol. 22, 1932-1937 (2012).
57. Poirier, M. G. & Marko, J. F. Micromechanical studies of mitotic chromosomes. Curr. Top. Dev. Biol. 55, 75-141 (2003).
58. Cui, Y. & Bustamante, C. Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl Acad. Sci. USA 97, 127-132 (2000).
59. Rowat, A. C., Lammerding, J. & Ipsen, J. H. Mechanical properties of the cell nucleus and the effect of emerin deficiency. Biophys. J. 91, 4649-4664 (2006).
60. Broers, J. L. et al. A- and B-type lamins are differentially expressed in normal human tissues. Histochem. Cell Biol. 107, 505-517 (1997).
61. Dogterom, M. & Yurke, B. Measurement of the force-velocity relation for growing microtubules. Science 278, 856-860 (1997).
62. Batzenschlager, M. et al. The GIP gamma-tubulin complex-associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Front. Plant Sci. 4, 480 (2013).
63. Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823 (1991).
64. Bahler, J. et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951 (1998).
65. Hentges, P., Van Driessche, B., Tafforeau, L., Vandenhaute, J. & Carr, A. M. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 22, 1013-1019 (2005).
66. Snaith, H. A., Samejima, I. & Sawin, K. E. Multistep and multimode cortical anchoring of tea1p at cell tips in fission yeast. EMBO J. 24, 3690-3699 (2005).
67. Crocker, J. & Grier, D. Methods of digital video microscopy for colloidal studies. J. Colloid Interface Sci. 179, 298-310 (1996).
68. Kiseleva, E. et al. A protocol for isolation and visualization of yeast nuclei by scanning electron microscopy (SEM). Nat. Protoc. 2, 1943-1953 (2007).
69. Jotwani, A., Richerson, D. N., Motta, I., Julca-Zevallos, O. & Melia, T. J. Approaches to the study of Atg8-mediated membrane dynamics in vitro. Methods Cell Biol. 108, 93-116 (2012).
70. Mack, A. H. Practical axial optical trapping. Rev. Sci. Instrum. 83, 103106 (2012).