Mechanosensing by the nucleus: From pathways to scaling relationships

Journal of Cell Biology

Volumn 216, Issue 2, 2017, Pages 305-315

  Cho, Sangkyun ^a   Irianto, Jerome ^a   Discher, Dennis E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; LAMIN; LAMIN A; MEMBRANE PROTEIN; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR; NUCLEAR PROTEIN;

AGING; CELL MEMBRANE; CELL MIGRATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CHROMOSOME STRUCTURE; DEVELOPMENT; DISEASES; HUMAN; MECHANOTRANSDUCTION; MEMBRANE RUPTURE; NONHUMAN; NUCLEAR MECHANOSENSING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; TRANSCRIPTOMICS; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; MECHANICAL STRESS; META ANALYSIS; METABOLISM; PHOSPHORYLATION; PROCEDURES;

ANIMALS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEOMICS; STRESS, MECHANICAL;

EID: 85012188476     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201610042     Document Type: Review

References (104)

1. Alam, S.G., D. Lovett, D.I. Kim, K.J. Roux, R.B. Dickinson, and T.P. Lele. 2015. The nucleus is an intracellular propagator of tensile forces in NIH 3T3 fibroblasts. J. Cell Sci. 128:1901-1911. http://dx. doi. org/10. 1242/jcs. 161703
2. Barrett, T., S.E. Wilhite, P. Ledoux, C. Evangelista, I.F. Kim, M. Tomashevsky, K.A. Marshall, K.H. Phillippy, P.M. Sherman, M. Holko, et al. 2013. NCBI GEO: Archive for functional genomics data sets-update. Nucleic Acids Res. 41(D1):D991-D995. http://dx. doi. org/10. 1093/nar/gks1193
3. Bengtsson, L., and H. Otto. 2008. LUMA interacts with emerin and influences its distribution at the inner nuclear membrane. J. Cell Sci. 121:536-548. http://dx. doi. org/10. 1242/jcs. 019281
4. Bertacchini, J., F. Beretti, V. Cenni, M. Guida, F. Gibellini, L. Mediani, O. Marin, N.M. Maraldi, A. de Pol, G. Lattanzi, et al. 2013. The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FAS EB J. 27:2145-2155. http://dx. doi. org/10. 1096/fj. 12-218214
5. Bione, S., E. Maestrini, S. Rivella, M. Mancini, S. Regis, G. Romeo, and D. Toniolo. 1994. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8:323-327. http://dx. doi. org/10. 1038/ng1294-323
6. Bonne, G., M.R. Di Barletta, S. Varnous, H.M. Becane, E.H. Hammouda, L. Merlini, F. Muntoni, C.R. Greenberg, F. Gary, J.A. Urtizberea, et al. 1999. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21:285-288. http://dx. doi. org/10. 1038/6799
7. Brower, G.L., J.D. Gardner, M.F. Forman, D.B. Murray, T. Voloshenyuk, S.P. Levick, and J.S. Janicki. 2006. The relationship between myocardial extracellular matrix remodeling and ventricular function. Eur. J. Cardiothorac. Surg. 30:604-610. http://dx. doi. org/10. 1016/j. ejcts. 2006. 07. 006
8. Burtner, C.R., and B.K. Kennedy. 2010. Progeria syndromes and ageing: What is the connection? Nat. Rev. Mol. Cell Biol. 11:567-578. http://dx. doi. org/10. 1038/nrm2944
9. Buxboim, A., J. Swift, J. Irianto, K.R. Spinler, P.C. Dingal, A. Athirasala, Y.R. Kao, S. Cho, T. Harada, J.W. Shin, and D.E. Discher. 2014. Matrix elasticity regulates lamin-A, C phosphorylation and turnover with feedback to actomyosin. Curr. Biol. 24:1909-1917. http://dx. doi. org/10. 1016/j. cub. 2014. 07. 001
10. Chancellor, T.J., J. Lee, C.K. Thodeti, and T. Lele. 2010. 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. http://dx. doi. org/10. 1016/j. bpj. 2010. 04. 011
11. Chang, L., and R.D. Goldman. 2004. Intermediate filaments mediate cytoskeletal crosstalk. Nat. Rev. Mol. Cell Biol. 5:601-613. http://dx. doi. org/10. 1038/nrm1438
12. Chopra, A., M.E. Murray, F.J. Byfield, M.G. Mendez, R. Halleluyan, D.J. Restle, D. Raz-Ben Aroush, P.A. Galie, K. Pogoda, R. Bucki, et al. 2014. Augmentation of integrin-mediated mechanotransduction by hyaluronic acid. Biomaterials. 35:71-82. http://dx. doi. org/10. 1016/j. biomaterials. 2013. 09. 066
13. Cremer, T., and C. Cremer. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2:292-301. http://dx. doi. org/10. 1038/35066075
14. Crisp, M., Q. Liu, K. Roux, J.B. Rattner, C. Shanahan, B. Burke, P.D. Stahl, and D. Hodzic. 2006. Coupling of the nucleus and cytoplasm: Role of the LINC complex. J. Cell Biol. 172:41-53. http://dx. doi. org/10. 1083/jcb. 200509124
15. Dahl, K.N., P. Scaffidi, M.F. Islam, A.G. Yodh, K.L. Wilson, and T. Misteli. 2006. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. USA. 103:10271-10276. http://dx. doi. org/10. 1073/pnas. 0601058103
16. Dahl, K.N., A.J. Ribeiro, and J. Lammerding. 2008. Nuclear shape, mechanics, and mechanotransduction. Circ. Res. 102:1307-1318. http://dx. doi. org/10. 1161/CIR CRE SAHA. 108. 173989 de la Rosa, J., J.M. Freije, R. Cabanillas, F.G. Osorio, M.F. Fraga, M.S. Fernandez-
17. de la Rosa, J., J.M. Freije, R. Cabanillas, F.G. Osorio, M.F. Fraga, M.S. Fernandez-Garcia, R. Rad, V. Fanjul, A.P. Ugalde, Q. Liang, et al. 2013. Prelamin A causes progeria through cell-extrinsic mechanisms and prevents cancer invasion. Nat. Commun. 4:2268. http://dx. doi. org/10. 1038/ncomms3268
18. Denais, C.M., R.M. Gilbert, P. Isermann, A.L. McGregor, M. te Lindert, B. Weigelin, P.M. Davidson, P. Friedl, K. Wolf, and J. Lammerding. 2016. Nuclear envelope rupture and repair during cancer cell migration. Science. 352:353-358. http://dx. doi. org/10. 1126/science. aad7297
19. De Vos, W.H., F. Houben, M. Kamps, A. Malhas, F. Verheyen, J. Cox, E.M. Manders, V.L. Verstraeten, M.A. van Steensel, C.L. Marcelis, et al. 2011. Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum. Mol. Genet. 20:4175-4186. http://dx. doi. org/10. 1093/hmg/ddr344
20. Dingal, P.C., and D.E. Discher. 2014. Systems mechanobiology: Tensioninhibited protein turnover is sufficient to physically control gene circuits. Biophys. J. 107:2734-2743. http://dx. doi. org/10. 1016/j. bpj. 2014. 10. 042
21. Dingal, P.C., A.M. Bradshaw, S. Cho, M. Raab, A. Buxboim, J. Swift, and D.E. Discher. 2015. Fractal heterogeneity in minimal matrix models of scars modulates stiff-niche stem-cell responses via nuclear exit of a mechanorepressor. Nat. Mater. 14:951-960. http://dx. doi. org/10. 1038/nmat4350
22. Discher, D.E., P. Janmey, and Y.L. Wang. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science. 310:1139-1143. http://dx. doi. org/10. 1126/science. 1116995
23. Discher, D.E., D.J. Mooney, and P.W. Zandstra. 2009. Growth factors, matrices, and forces combine and control stem cells. Science. 324:1673-1677. http://dx. doi. org/10. 1126/science. 1171643
24. Dittmer, T.A., and T. Misteli. 2011. The lamin protein family. Genome Biol. 12:222. http://dx. doi. org/10. 1186/gb-2011-12-5-222
25. Dupont, S., L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature. 474:179-183. http://dx. doi. org/10. 1038/nature10137
26. Eckersley-Maslin, M.A., J.H. Bergmann, Z. Lazar, and D.L. Spector. 2013. Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucleus. 4:53-60. http://dx. doi. org/10. 4161/nucl. 23384
27. Enyedi, B., M. Jelcic, and P. Niethammer. 2016. The cell nucleus serves as a mechanotransducer of tissue damage-induced inflammation. Cell. 165:1160-1170. http://dx. doi. org/10. 1016/j. cell. 2016. 04. 016
28. Flynn, B.P., A.P. Bhole, N. Saeidi, M. Liles, C.A. Dimarzio, and J.W. Ruberti. 2010. Mechanical strain stabilizes reconstituted collagen fibrils against enzymatic degradation by mammalian collagenase matrix metalloproteinase 8 (MMP-8). PLoS One. 5:e12337. http://dx. doi. org/10. 1371/journal. pone. 0012337
29. Gennes, P.-G. 1979. Scaling Concepts in Polymer Physics. Cornell University Press, Ithaca, NY. 324 pp.
30. Gerace, L., and G. Blobel. 1980. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 19:277-287. http://dx. doi. org/10. 1016/0092-8674(80)90409-2
31. Goldman, R.D., Y. Gruenbaum, R.D. Moir, D.K. Shumaker, and T.P. Spann. 2002. Nuclear lamins: Building blocks of nuclear architecture. Genes Dev. 16:533-547. http://dx. doi. org/10. 1101/gad. 960502
32. Gonzalez-Suarez, I., A.B. Redwood, and S. Gonzalo. 2009. Loss of A-type lamins and genomic instability. Cell Cycle. 8:3860-3865. http://dx. doi. org/10. 4161/cc. 8. 23. 10092
33. Gonzalo, S. 2014. DNA damage and lamins. Adv. Exp. Med. Biol. 773:377-399. http://dx. doi. org/10. 1007/978-1-4899-8032-8 17
34. Gruenbaum, Y., A. Margalit, R.D. Goldman, D.K. Shumaker, and K.L. Wilson. 2005. The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6:21-31. http://dx. doi. org/10. 1038/nrm1550
35. Guilluy, C., L.D. Osborne, L. Van Landeghem, L. Sharek, R. Superfine, R. Garcia-Mata, and K. Burridge. 2014. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16:376-381. http://dx. doi. org/10. 1038/ncb2927
36. Gutierrez-Fernandez, A., C. Soria-Valles, F.G. Osorio, J. Gutierrez-Abril, C. Garabaya, A. Aguirre, A. Fueyo, M.S. Fernandez-Garcia, X.S. Puente, and C. Lopez-Otin. 2015. Loss of MT1-MMP causes cell senescence and nuclear defects which can be reversed by retinoic acid. EMBO J. 34:1875-1888. http://dx. doi. org/10. 15252/embj. 201490594
37. Halder, G., S. Dupont, and S. Piccolo. 2012. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13:591-600. http://dx. doi. org/10. 1038/nrm3416
38. Hampoelz, B., Y. Azou-Gros, R. Fabre, O. Markova, P.H. Puech, and T. Lecuit. 2011. Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos. Development. 138:3377-3386. http://dx. doi. org/10. 1242/dev. 065706
39. Harada, T., J. Swift, J. Irianto, J.W. Shin, K.R. Spinler, A. Athirasala, R. Diegmiller, P.C. Dingal, I.L. Ivanovska, and D.E. Discher. 2014. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J. Cell Biol. 204:669-682. http://dx. doi. org/10. 1083/jcb. 201308029
40. Heald, R., and F. McKeon. 1990. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell. 61:579-589. http://dx. doi. org/10. 1016/0092-8674(90)90470-Y
41. Ho, C.Y., D.E. Jaalouk, M.K. Vartiainen, and J. Lammerding. 2013. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature. 497:507-511. http://dx. doi. org/10. 1038/nature12105
42. Ihalainen, T.O., L. Aires, F.A. Herzog, R. Schwartlander, J. Moeller, and V. Vogel. 2015. Differential basal-to-apical accessibility of lamin A/C epitopes in the nuclear lamina regulated by changes in cytoskeletal tension. Nat. Mater. 14:1252-1261. http://dx. doi. org/10. 1038/nmat4389
43. Ingber, D.E. 2006. Cellular mechanotransduction: Putting all the pieces together again. FAS EB J. 20:811-827. http://dx. doi. org/10. 1096/fj. 05-5424rev
44. Irianto, J., C.R. Pfeifer, R.R. Bennett, Y. Xia, I.L. Ivanovska, A.J. Liu, R.A. Greenberg, and D.E. Discher. 2016a. Nuclear constriction segregates mobile nuclear proteins away from chromatin. Mol. Biol. Cell. 27:4011-4020. http://dx. doi. org/10. 1091/mbc. E16-06-0428
45. Irianto, J., Y. Xia, C.R. Pfeifer, A. Athirasala, J. Ji, C. Alvey, M. Tewari, R. Bennett, S. Harding, A. Liu, R.A. Greenberg, and D.E. Discher. 2016b. DNA damage follows repair factor depletion and portends genome variation in cancer cells after pore migration. Curr. Biol. http://dx. doi. org/10. 1016/j. cub. 2016. 11. 049
46. Irianto, J., Y. Xia, C.R. Pfeifer, R.A. Greenberg, and D.E. Discher. 2016c. As a nucleus enters a small pore, chromatin stretches and maintains integrity, even with DNA breaks. Biophys. J. http://dx. doi. org/10. 1016/j. bpj. 2016. 09. 047
47. Jahn, D., S. Schramm, M. Schnolzer, C.J. Heilmann, C.G. de Koster, W. Schutz, R. Benavente, and M. Alsheimer. 2012. A truncated lamin A in the Lmna-/-mouse line: Implications for the understanding of laminopathies. Nucleus. 3:463-474. http://dx. doi. org/10. 4161/nucl. 21676
48. Jung, H.J., C. Coffinier, Y. Choe, A.P. Beigneux, B.S. Davies, S.H. Yang, R.H. Barnes II, J. Hong, T. Sun, S.J. Pleasure, et al. 2012. Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA. Proc. Natl. Acad. Sci. USA. 109:E423-E431. http://dx. doi. org/10. 1073/pnas. 1111780109
49. Khatau, S.B., C.M. Hale, P.J. Stewart-Hutchinson, M.S. Patel, C.L. Stewart, P.C. Searson, D. Hodzic, and D. Wirtz. 2009. A perinuclear actin cap regulates nuclear shape. Proc. Natl. Acad. Sci. USA. 106:19017-19022. http://dx. doi. org/10. 1073/pnas. 0908686106
50. Kim, D.H., and D. Wirtz. 2015. Cytoskeletal tension induces the polarized architecture of the nucleus. Biomaterials. 48:161-172. http://dx. doi. org/10. 1016/j. biomaterials. 2015. 01. 023
51. Kim, D.H., S. Cho, and D. Wirtz. 2014a. Tight coupling between nucleus and cell migration through the perinuclear actin cap. J. Cell Sci. 127:2528-2541. http://dx. doi. org/10. 1242/jcs. 144345
52. Kim, D.H., B. Li, F. Si, J.M. Phillip, D. Wirtz, and S.X. Sun. 2015. Volume regulation and shape bifurcation in the cell nucleus. J. Cell Sci. 128:3375-3385. http://dx. doi. org/10. 1242/jcs. 166330
53. Kim, M.S., S.M. Pinto, D. Getnet, R.S. Nirujogi, S.S. Manda, R. Chaerkady, A.K. Madugundu, D.S. Kelkar, R. Isserlin, S. Jain, et al. 2014b. A draft map of the human proteome. Nature. 509:575-581. http://dx. doi. org/10. 1038/nature13302
54. Kochin, V., T. Shimi, E. Torvaldson, S.A. Adam, A. Goldman, C.G. Pack, J. Melo-Cardenas, S.Y. Imanishi, R.D. Goldman, and J.E. Eriksson. 2014. Interphase phosphorylation of lamin A. J. Cell Sci. 127:2683-2696. http://dx. doi. org/10. 1242/jcs. 141820
55. Korfali, N., G.S. Wilkie, S.K. Swanson, V. Srsen, J. de Las Heras, D.G. Batrakou, P. Malik, N. Zuleger, A.R. Kerr, L. Florens, and E.C. Schirmer. 2012. The nuclear envelope proteome differs notably between tissues. Nucleus. 3:552-564. http://dx. doi. org/10. 4161/nucl. 22257
56. Koser, D.E., A.J. Thompson, S.K. Foster, A. Dwivedy, E.K. Pillai, G.K. Sheridan, H. Svoboda, M. Viana, L.D. Costa, J. Guck, et al. 2016. Mechanosensing is critical for axon growth in the developing brain. Nat. Neurosci. 19:1592-1598. http://dx. doi. org/10. 1038/nn. 4394 Kubben, N., J.W. Voncken, G. Konings, M. van Weeghel, M.M. van den Hoogenhof, M. Gijbels, A. van Erk, K. Schoonderwoerd, B. van den
57. Kubben, N., J.W. Voncken, G. Konings, M. van Weeghel, M.M. van den Hoogenhof, M. Gijbels, A. van Erk, K. Schoonderwoerd, B. van den Bosch, V. Dahlmans, et al. 2011. Post-natal myogenic and adipogenic developmental: Defects and metabolic impairment upon loss of A-type lamins. Nucleus. 2:195-207. http://dx. doi. org/10. 4161/nucl. 2. 3. 15731
58. Lammerding, J., J. Hsiao, P.C. Schulze, S. Kozlov, C.L. Stewart, and R.T. Lee. 2005. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170:781-791. http://dx. doi. org/10. 1083/jcb. 200502148
59. Le, H.Q., S. Ghatak, C.Y. Yeung, F. Tellkamp, C. Gunschmann, C. Dieterich, A. Yeroslaviz, B. Habermann, A. Pombo, C.M. Niessen, and S.A. Wickstrom. 2016. Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment. Nat. Cell Biol. 18:864-875. http://dx. doi. org/10. 1038/ncb3387
60. Lehner, C.F., R. Stick, H.M. Eppenberger, and E.A. Nigg. 1987. Differential expression of nuclear lamin proteins during chicken development. J. Cell Biol. 105:577-587. http://dx. doi. org/10. 1083/jcb. 105. 1. 577
61. Li, Y., J.S. Chu, K. Kurpinski, X. Li, D.M. Bautista, L. Yang, K.L. Sung, and S. Li. 2011. Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys. J. 100:1902-1909. http://dx. doi. org/10. 1016/j. bpj. 2011. 03. 008
62. Liu, B., J. Wang, K.M. Chan, W.M. Tjia, W. Deng, X. Guan, J.D. Huang, K.M. Li, P.Y. Chau, D.J. Chen, et al. 2005. Genomic instability in laminopathy-based premature aging. Nat. Med. 11:780-785. http://dx. doi. org/10. 1038/nm1266
63. Liu, Y., A. Rusinol, M. Sinensky, Y. Wang, and Y. Zou. 2006. DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J. Cell Sci. 119:4644-4649. http://dx. doi. org/10. 1242/jcs. 03263
64. Lloyd, D.J., R.C. Trembath, and S. Shackleton. 2002. A novel interaction between lamin A and SRE BP1: Implications for partial lipodystrophy and other laminopathies. Hum. Mol. Genet. 11:769-777. http://dx. doi. org/10. 1093/hmg/11. 7. 769
65. Lovett, D.B., N. Shekhar, J.A. Nickerson, K.J. Roux, and T.P. Lele. 2013. Modulation of nuclear shape by substrate rigidity. Cell. Mol. Bioeng. 6:230-238. http://dx. doi. org/10. 1007/s12195-013-0270-2
66. Maharana, S., K.V. Iyer, N. Jain, M. Nagarajan, Y. Wang, and G.V. Shivashankar. 2016. Chromosome intermingling-the physical basis of chromosome organization in differentiated cells. Nucleic Acids Res. 44:5148-5160. http://dx. doi. org/10. 1093/nar/gkw131
67. Majkut, S., T. Idema, J. Swift, C. Krieger, A. Liu, and D.E. Discher. 2013. Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 23:2434-2439. http://dx. doi. org/10. 1016/j. cub. 2013. 10. 057
68. Margalit, A., M. Segura-Totten, Y. Gruenbaum, and K.L. Wilson. 2005. Barrier-to-autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc. Natl. Acad. Sci. USA. 102:3290-3295. http://dx. doi. org/10. 1073/pnas. 0408364102
69. Marganski, W.A., M. Dembo, and Y.L. Wang. 2003. Measurements of cellgenerated deformations on flexible substrata using correlation-based optical flow. Methods Enzymol. 361:197-211. http://dx. doi. org/10. 1016/S0076-6879(03)61012-8
70. Meshorer, E., D. Yellajoshula, E. George, P.J. Scambler, D.T. Brown, and T. Misteli. 2006. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell. 10:105-116. http://dx. doi. org/10. 1016/j. devcel. 2005. 10. 017
71. Moiseeva, O., S. Lopes-Paciencia, G. Huot, F. Lessard, and G. Ferbeyre. 2016. Permanent farnesylation of lamin A mutants linked to progeria impairs its phosphorylation at serine 22 during interphase. Aging. 8:366-381. http://dx. doi. org/10. 18632/aging. 100903
72. Murphy, A.J., J. Pierce, C. de Caestecker, J. Libes, D. Neblett, M. de Caestecker, A.O. Perantoni, S. Tanigawa, J.R. Anderson, J.S. Dome, et al. 2014. Aberrant activation, nuclear localization, and phosphorylation of Yesassociated protein-1 in the embryonic kidney and Wilms tumor. Pediatr. Blood Cancer. 61:198-205. http://dx. doi. org/10. 1002/pbc. 24788
73. Narula, N., V. Favalli, P. Tarantino, M. Grasso, A. Pilotto, R. Bellazzi, A. Serio, F.I. Gambarin, P. Charron, B. Meder, et al. 2012. Quantitative expression of the mutated lamin A/C gene in patients with cardiolaminopathy. J. Am. Coll. Cardiol. 60:1916-1920. http://dx. doi. org/10. 1016/j. jacc. 2012. 05. 059
74. Neelam, S., T.J. Chancellor, Y. Li, J.A. Nickerson, K.J. Roux, R.B. Dickinson, and T.P. Lele. 2015. Direct force probe reveals the mechanics of nuclear homeostasis in the mammalian cell. Proc. Natl. Acad. Sci. USA. 112:5720-5725. http://dx. doi. org/10. 1073/pnas. 1502111112
75. Osorio, F.G., C.L. Navarro, J. Cadinanos, I.C. Lopez-Mejia, P.M. Quiros, C. Bartoli, J. Rivera, J. Tazi, G. Guzman, I. Varela, et al. 2011. Splicingdirected therapy in a new mouse model of human accelerated aging. Sci. Transl. Med. 3:106ra107. http://dx. doi. org/10. 1126/scitranslmed. 3002847
76. Paddy, M.R., A.S. Belmont, H. Saumweber, D.A. Agard, and J.W. Sedat. 1990. Interphase nuclear envelope lamins form a discontinuous network that interacts with only a fraction of the chromatin in the nuclear periphery. Cell. 62:89-106. http://dx. doi. org/10. 1016/0092-8674(90)90243-8
77. Pajerowski, J.D., K.N. Dahl, F.L. Zhong, P.J. Sammak, and D.E. Discher. 2007. Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. USA. 104:15619-15624. http://dx. doi. org/10. 1073/pnas. 0702576104
78. Poh, Y.C., S.P. Shevtsov, F. Chowdhury, D.C. Wu, S. Na, M. Dundr, and N. Wang. 2012. Dynamic force-induced direct dissociation of protein complexes in a nuclear body in living cells. Nat. Commun. 3:866. http://dx. doi. org/10. 1038/ncomms1873
79. Raab, M., M. Gentili, H. de Belly, H.R. Thiam, P. Vargas, A.J. Jimenez, F. Lautenschlaeger, R. Voituriez, A.M. Lennon-Dumenil, N. Manel, and M. Piel. 2016. ESC RT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science. 352:359-362. http://dx. doi. org/10. 1126/science. aad7611
80. Rajan, S., S.S. Williams, G. Jagatheesan, R.P. Ahmed, G. Fuller-Bicer, A. Schwartz, B.J. Aronow, and D.F. Wieczorek. 2006. Microarray analysis of gene expression during early stages of mild and severe cardiac hypertrophy. Physiol. Genomics. 27:309-317. http://dx. doi. org/10. 1152/physiolgenomics. 00072. 2006
81. Rober, R.A., K. Weber, and M. Osborn. 1989. Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: A developmental study. Development. 105:365-378.
82. Rodríguez, J., F. Calvo, J.M. Gonzalez, B. Casar, V. Andres, and P. Crespo. 2010. ERK1/2 MAP kinases promote cell cycle entry by rapid, kinaseindependent disruption of retinoblastoma-lamin A complexes. J. Cell Biol. 191:967-979. (published erratum appears in J. Cell Biol. 2011. 192:201) http://dx. doi. org/10. 1083/jcb. 201004067
83. Sawada, Y., M. Tamada, B.J. Dubin-Thaler, O. Cherniavskaya, R. Sakai, S. Tanaka, and M.P. Sheetz. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell. 127:1015-1026. http://dx. doi. org/10. 1016/j. cell. 2006. 09. 044
84. Schirmer, E.C., L. Florens, T. Guan, J.R. Yates III, and L. Gerace. 2003. Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science. 301:1380-1382. http://dx. doi. org/10. 1126/science. 1088176
85. Shao, X., Q. Li, A. Mogilner, A.D. Bershadsky, and G.V. Shivashankar. 2015. Mechanical stimulation induces formin-dependent assembly of a perinuclear actin rim. Proc. Natl. Acad. Sci. USA. 112:E2595-E2601. http://dx. doi. org/10. 1073/pnas. 1504837112
86. Shoulders, M.D., and R.T. Raines. 2009. Collagen structure and stability. Annu. Rev. Biochem. 78:929-958. http://dx. doi. org/10. 1146/annurev. biochem. 77. 032207. 120833
87. Solovei, I., A.S. Wang, K. Thanisch, C.S. Schmidt, S. Krebs, M. Zwerger, T.V. Cohen, D. Devys, R. Foisner, L. Peichl, et al. 2013. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell. 152:584-598. http://dx. doi. org/10. 1016/j. cell. 2013. 01. 009
88. Sullivan, T., D. Escalante-Alcalde, H. Bhatt, M. Anver, N. Bhat, K. Nagashima, C.L. Stewart, and B. Burke. 1999. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147:913-920. http://dx. doi. org/10. 1083/jcb. 147. 5. 913
89. Sun, Y., K.M. Yong, L.G. Villa-Diaz, X. Zhang, W. Chen, R. Philson, S. Weng, H. Xu, P.H. Krebsbach, and J. Fu. 2014. Hippo/YAP-mediated rigiditydependent motor neuron differentiation of human pluripotent stem cells. Nat. Mater. 13:599-604. http://dx. doi. org/10. 1038/nmat3945
90. Swift, J., I.L. Ivanovska, A. Buxboim, T. Harada, P.C. Dingal, J. Pinter, J.D. Pajerowski, K.R. Spinler, J.W. Shin, M. Tewari, et al. 2013. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science. 341:1240104. http://dx. doi. org/10. 1126/science. 1240104
91. Tajik, A., Y. Zhang, F. Wei, J. Sun, Q. Jia, W. Zhou, R. Singh, N. Khanna, A.S. Belmont, and N. Wang. 2016. Transcription upregulation via forceinduced direct stretching of chromatin. Nat. Mater. 15:1287-1296. http://dx. doi. org/10. 1038/nmat4729
92. Tamiello, C., M.A. Kamps, A. van den Wijngaard, V.L. Verstraeten, F.P. Baaijens, J.L. Broers, and C.C. Bouten. 2013. Soft substrates normalize nuclear morphology and prevent nuclear rupture in fibroblasts from a laminopathy patient with compound heterozygous LMNA mutations. Nucleus. 4:61-73. http://dx. doi. org/10. 4161/nucl. 23388
93. Taylor, M.R., D. Slavov, A. Gajewski, S. Vlcek, L. Ku, P.R. Fain, E. Carniel, A. Di Lenarda, G. Sinagra, M.M. Boucek, et al. 2005. Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Hum. Mutat. 26:566-574. http://dx. doi. org/10. 1002/humu. 20250
94. Tunnah, D., C.A. Sewry, D. Vaux, E.C. Schirmer, and G.E. Morris. 2005. The apparent absence of lamin B1 and emerin in many tissue nuclei is due to epitope masking. J. Mol. Histol. 36:337-344. http://dx. doi. org/10. 1007/s10735-005-9004-7
95. van der Rest, M., and R. Garrone. 1991. Collagen family of proteins. FAS EB J. 5:2814-2823.
96. Vargas, J.D., E.M. Hatch, D.J. Anderson, and M.W. Hetzer. 2012. Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus. 3:88-100. http://dx. doi. org/10. 4161/nucl. 18954
97. Vartiainen, M.K., S. Guettler, B. Larijani, and R. Treisman. 2007. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science. 316:1749-1752. http://dx. doi. org/10. 1126/science. 1141084
98. Versaevel, M., T. Grevesse, and S. Gabriele. 2012. Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat. Commun. 3:671. http://dx. doi. org/10. 1038/ncomms1668
99. Vizcaino, J.A., A. Csordas, N. del-Toro, J.A. Dianes, J. Griss, I. Lavidas, G. Mayer, Y. Perez-Riverol, F. Reisinger, T. Ternent, et al. 2016. 2016 update of the PRI DE database and its related tools. Nucleic Acids Res. 44(D1):D447-D456. http://dx. doi. org/10. 1093/nar/gkv1145
100. Wilson, K.L., and R. Foisner. 2010. Lamin-binding proteins. Cold Spring Harb. Perspect. Biol. 2:a000554. http://dx. doi. org/10. 1101/cshperspect. a000554
101. Worman, H.J. 2012. Nuclear lamins and laminopathies. J. Pathol. 226:316-325. http://dx. doi. org/10. 1002/path. 2999
102. Yang, Y.L., and L.J. Kaufman. 2009. Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly. Biophys. J. 96:1566-1585. http://dx. doi. org/10. 1016/j. bpj. 2008. 10. 063
103. Yang, C., M.W. Tibbitt, L. Basta, and K.S. Anseth. 2014. Mechanical memory and dosing influence stem cell fate. Nat. Mater. 13:645-652. http://dx. doi. org/10. 1038/nmat3889
104. Zhang, Q., C. Bethmann, N.F. Worth, J.D. Davies, C. Wasner, A. Feuer, C.D. Ragnauth, Q. Yi, J.A. Mellad, D.T. Warren, et al. 2007. Nesprin-1 and-2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum. Mol. Genet. 16:2816-2833. http://dx. doi. org/10. 1093/hmg/ddm238