Dynamic force-induced direct dissociation of protein complexes in a nuclear body in living cells

Nature Communications

Volumn 3, Issue , 2012, Pages

  Poh, Yeh Chuin ^a   Shevtsov, Sergey P ^b   Chowdhury, Farhan ^a   Wu, Douglas C ^a   Na, Sungsoo ^c   Dundr, Miroslav ^b   Wang, Ning ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^c Indiana University Purdue University Indianapolis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; CELL SURFACE PROTEIN COILIN; F ACTIN; INTEGRIN; LAMIN A; LAMIN C; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG; ACTIN; LMNA PROTEIN, HUMAN; NUCLEAR PROTEIN; P80 COILIN; P80-COILIN; PLECTIN;

ARTICLE; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; CELL SURFACE; COILED BODY; CONTROLLED STUDY; CYTOMETRY; CYTOSKELETON; DYNAMICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FORCE; HUMAN; HUMAN CELL; PROTEIN PROTEIN INTERACTION; RIGIDITY; SURFACE PROPERTY; TENSION; ANIMAL; GENETICS; HELA CELL; METABOLISM; MOUSE; MOUSE MUTANT;

ACTINS; ANIMALS; COILED BODIES; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; LAMIN TYPE A; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PLECTIN;

EID: 84866424053     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1873     Document Type: Article

References (54)

1. Geiger, B., Spatz, J. P. & Bershadsky, A. D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33 (2009).
2. Wozniak, M. A. & Chen, C. S. Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10, 34-43 (2009).
3. 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. 10, 75-82 (2009).
4. Johnson, C. P., Tang, H., Carag, C., Speicher, D. W. & Discher, D. E. Forced unfolding of proteins within cells. Science 317, 663-666 (2007). (Pubitemid 47229965)
5. Del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
6. Hoffman, B. D., Grashoff, C. & Schwartz, M. A. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475, 316-323 (2011).
7. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7, 265-275 (2006).
8. 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). (Pubitemid 27074410)
9. Hu, S., Chen, J., Butler, J. P. & Wang, N. Prestress mediates force propagation into the nucleus. Biochem. Biophys. Res. Comm. 329, 423-428 (2005). (Pubitemid 40311763)
10. Lammerding, J. et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378 (2004). (Pubitemid 38544181)
11. Lammerding, J. et al. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281, 25768-25780 (2006). (Pubitemid 44401965)
12. Hale, C. M. et al. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys. J. 95, 5462-5475 (2008).
13. 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. 104, 15619-15624 (2007). (Pubitemid 350035348)
14. Gall, J. G. Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 16, 273-300 (2000). (Pubitemid 32037508)
15. Sleeman, J. & Lamond, A. Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr. Biol. 9, 1065-1074 (1999). (Pubitemid 29504476)
16. Dundr, M. et al. In vivo kinetics of Cajal body components. J. Cell Biol. 164, 831-842 (2004). (Pubitemid 38366895)
17. Kaiser, T. E., Intine, R. V. & Dundr, M. De novo formation of a subnuclear body. Science 322, 1713-1717 (2008).
18. Walker, M. P., Tian, L. & Matera, A. G. Reduced viability, fertility and fecundity in mice lacking the Cajal body marker protein, coilin. PLoS One 4, e6171 (2009).
19. Burghes, A. H. M. & Beattie, C. E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat. Rev. Neurosci. 10, 597-609 (2009).
20. Platani, M., Goldberg, I., Lamond, A. I. & Swedlow, J. R. Cajal body dynamics and association with chromatin are ATP-dependent. Nat. Cell Biol. 4, 502-508 (2002). (Pubitemid 34752435)
21. Matera, A. G. et al. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev. Cell 17, 639-647 (2009).
22. Shevtsov, P. S. & Dundr, M. Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 13, 167-173 (2011).
23. Hu, S. et al. Mechanical anisotropy of adherent cells probed by a three-dimensional magnetic twisting device. Am. J. Physiol. Cell Physiol. 56, C1184-C1191 (2004). (Pubitemid 39382876)
24. Hu, S. et al. Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Physiol. Cell Physiol. 285, C1082-C1090 (2003). (Pubitemid 37296284)
25. Hebert, M., Szymczyk, P., Shpargel, K. & Matera, A. Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev. 15, 2720-2729 (2001). (Pubitemid 32988881)
26. Discher, D. E., Janmey, P. & Wang, Y. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143 (2005). (Pubitemid 41681732)
27. Mahmoudi, S. et al. WRAP53 is essential for Cajal body formation and for targeting the survival of motor neuron complex to Cajal bodies. PLoS Biol. 8, e1000521 (2010).
28. Toyota, C. G., Davis, M. D., Cosman, A. M. & Hebert, M. D. Coilin phosphorylation mediates interaction with SMN and SmB. Chromosoma 119, 205-215 (2010).
29. Isaac, C., Yang, Y. & Meier, U. T. Nopp140 functions as a molecular link between the nucleolus and the coiled bodies. J. Cell Biol. 142, 319-329 (1998). (Pubitemid 28361541)
30. Novotný, I., Blažíková, M., Staněk, D., Herman, P. & Malinsky, J. In vivo kinetics of U4/U6 U5 tri-snRNP formation in Cajal bodies. Mol. Biol. Cell 22, 513-523 (2011).
31. Pellizzoni, L., Baccon, J., Charroux, B. & Dreyfuss, G. The survival of motor neurons (SMN) protein interacts with the snoRNP proteins fibrillarin and GAR1. Curr. Biol. 11, 1079-1088 (2001). (Pubitemid 32675759)
32. Kiseleva, E. Cell of the month: nuclear pore complexes and Cajal bodies in Xenopus laevis oocytes. Nat. Cell Biol. 5, 193 (2003).
33. Na, S. et al. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl Acad. Sci. USA. 105, 6626-6631 (2008). (Pubitemid 351754557)
34. Poh, Y. et al. Rapid activation of Rac GTPase in living cells by force is independent of Src. PLoS One 4, e7886 (2009).
35. Dahl, K. N. & Kalinowski, A. Nucleoskeleton mechanics at a glance. J. Cell. Sci. 124, 675-678 (2011).
36. 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. 42, 1717-1728 (2010).
37. Chancellor, T. J., Lee, J., Thodeti, C. K. & Lele, T. Actomyosin tension exerted on the nucleus through Nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys. J. 99, 115-123 (2010).
38. Grashoff, C. et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
39. Hearst, S. M. et al. Cajal-body formation correlates with differential coilin phosphorylation in primary and transformed cell lines. J. Cell Sci. 122, 1872-1881 (2009).
40. Hayakawa, K., Tatsumi, H. & Sokabe, M. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J. Cell Sci. 121, 496-503 (2008). (Pubitemid 351405058)
41. Platani, M. & Goldberg, I. In vivo analysis of Cajal body movement, separation, and joining in live human cells. J. Cell Biol. 151, 1561-1574 (2000). (Pubitemid 32047603)
42. Hernandez, L. et al. Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev. Cell 19, 413-425 (2010).(1)(1)
43. Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005). (Pubitemid 41317594)
44. Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009).
45. Samuel, M. S. et al. Actomyosin-mediated cellular tension drives increased tissue stiffness and β-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 19, 776-791 (2011).
46. Sleeman, J., Ajuh, P. & Lamond, A. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J. Cell Sci. 114, 4407-4419 (2001). (Pubitemid 34082861)
47. Hebert, M. & Matera, A. Self-association of coilin reveals a common theme in nuclear body localization. Mol. Biol. Cell 11, 4159-4171 (2000).
48. Dundr, M. & Misteli, T. The dynamics of postmitotic reassembly of the nucleolus. J. Cell Biol. 150, 433-446 (2000). (Pubitemid 30641391)
49. Wang, N., Butler, J. P. & Ingber, D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127 (1993). (Pubitemid 23186787)
50. Fabry, B. et al. Signal transduction in smooth muscle - selected contribution: time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells. J. Appl. Physiol. 91, 986-994 (2001). (Pubitemid 32681134)
51. Mijailovich, S. M., Kojic, M., Zivkovic, M., Fabry, B. & Fredberg, J. J. A finite element model of cell deformation during magnetic bead twisting. J. Appl. Physiol. 93, 1429-1436 (2002).
52. Chowdhury, F. et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nature Mater. 9, 82-88 (2010).
53. Rasnik, I., McKinney, S. A. & Ha, T. Nonblinking and long-lasting single-molecule fluorescence imaging. Nat. Methods 3, 891-893 (2006). (Pubitemid 44614723)
54. Na, S. & Wang, N. Application of fluorescence resonance energy transfer and magnetic twisting cytometry to quantify mechanochemical signaling activities in a living cell. Sci. Signal. 1, pl1 (2008).