1932

Abstract

The cell nucleus is best known as the container of the genome. Its envelope provides a barrier for passive macromolecule diffusion, which enhances the control of gene expression. As its largest and stiffest organelle, the nucleus also defines the minimal space requirements of a cell. Internal or external pressures that deform a cell to its physical limits cause a corresponding nuclear deformation. Evidence is consolidating that the nucleus, in addition to its genetic functions, serves as a physical sensing device for critical cell body deformation. Nuclear mechanotransduction allows cells to adapt their acute behaviors, mechanical stability, paracrine signaling, and fate to their physical surroundings. This review summarizes the basic chemical and mechanical properties of nuclear components, and how these properties are thought to be utilized for mechanosensing.

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2021-10-06
2024-04-20
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Literature Cited

  1. Aebi U, Cohn J, Buhle L, Gerace L. 1986. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323:6088560–64
    [Google Scholar]
  2. Agrawal A, Lele TP. 2019. Mechanics of nuclear membranes. J. Cell Sci. 132:14jcs229245
    [Google Scholar]
  3. Akter R, Rivas D, Geneau G, Drissi H, Duque G. 2009. Effect of lamin A/C knockdown on osteoblast differentiation and function. J. Bone Miner. Res. 24:2283–93
    [Google Scholar]
  4. Amulic B, Knackstedt SL, Abu Abed U, Deigendesch N, Harbort CJ et al. 2017. Cell-cycle proteins control production of neutrophil extracellular traps. Dev. Cell 43:4449–62.e5
    [Google Scholar]
  5. Aureille J, Buffière-Ribot V, Harvey BE, Boyault C, Pernet L et al. 2019. Nuclear envelope deformation controls cell cycle progression in response to mechanical force. EMBO Rep 20:9e48084
    [Google Scholar]
  6. Bengtsson L, Wilson KL. 2004. Multiple and surprising new functions for emerin, a nuclear membrane protein. Curr. Opin. Cell Biol. 16:173–79
    [Google Scholar]
  7. Bergo MO, Gavino B, Ross J, Schmidt WK, Hong C et al. 2002. Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. PNAS 99:2013049–54
    [Google Scholar]
  8. Bigay J, Antonny B. 2012. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev. Cell 23:5886–95
    [Google Scholar]
  9. Blackwell KA, Raisz LG, Pilbeam CC. 2010. Prostaglandins in bone: bad cop, good cop?. Trends Endocrinol. Metab. 21:5294–301
    [Google Scholar]
  10. Boni A, Politi AZ, Strnad P, Xiang W, Hossain MJ, Ellenberg J. 2015. Live imaging and modeling of inner nuclear membrane targeting reveals its molecular requirements in mammalian cells. J. Cell Biol. 209:5705–20
    [Google Scholar]
  11. Bronshtein I, Kepten E, Kanter I, Berezin S, Lindner M et al. 2015. Loss of lamin A function increases chromatin dynamics in the nuclear interior. Nat. Commun. 6:8044
    [Google Scholar]
  12. Brotherus J, Renkonen O. 1977. Phospholipids of subcellular organelles isolated from cultured BHK cells. Biochim. Biophys. Acta Lipids Lipid Metab 486:2243–53
    [Google Scholar]
  13. Buchwalter A, Schulte R, Tsai H, Capitanio J, Hetzer M 2019. Selective clearance of the inner nuclear membrane protein emerin by vesicular transport during ER stress. eLife 8:e49796
    [Google Scholar]
  14. Burke JE, Dennis EA. 2009. Phospholipase A2 structure/function, mechanism, and signaling. J. Lipid Res. 50:Suppl.S237–42
    [Google Scholar]
  15. Buxboim A, Swift J, Irianto J, Spinler KR, Dingal PCDP et al. 2014. Matrix elasticity regulates lamin-A,C phosphorylation and turnover with feedback to actomyosin. Curr. Biol. 24:161909–17
    [Google Scholar]
  16. Cao K, Capell BC, Erdos MR, Djabali K, Collins FS 2007. A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. PNAS 104:124949–54
    [Google Scholar]
  17. Carmo-Fonseca M. 2002. The contribution of nuclear compartmentalization to gene regulation. Cell 108:4513–21
    [Google Scholar]
  18. Cenni V, D'Apice MR, Garagnani P, Columbaro M, Novelli G et al. 2018. Mandibuloacral dysplasia: a premature ageing disease with aspects of physiological ageing. Ageing Res. Rev 42:1–13
    [Google Scholar]
  19. Chang K-H, Multani PS, Sun K-H, Vincent F, de Pablo Y et al. 2011. Nuclear envelope dispersion triggered by deregulated Cdk5 precedes neuronal death. Mol. Biol. Cell 22:91452–62
    [Google Scholar]
  20. Chen NY, Kim P, Weston TA, Edillo L, Tu Y et al. 2018. Fibroblasts lacking nuclear lamins do not have nuclear blebs or protrusions but nevertheless have frequent nuclear membrane ruptures. PNAS 115:4010100–5
    [Google Scholar]
  21. Chizmadzhev YA, Kumenko DA, Kuzmin PI, Chernomordik LV, Zimmerberg J, Cohen FS. 1999. Lipid flow through fusion pores connecting membranes of different tensions. Biophys. J. 76:62951–65
    [Google Scholar]
  22. Cho S, Irianto J, Discher DE. 2017. Mechanosensing by the nucleus: from pathways to scaling relationships. J. Cell Biol. 216:2305–15
    [Google Scholar]
  23. Cho S, Vashisth M, Abbas A, Majkut S, Vogel K et al. 2019. Mechanosensing by the lamina protects against nuclear rupture, DNA damage, and cell-cycle arrest. Dev. Cell 49:6920–35.e5
    [Google Scholar]
  24. Codelia VA, Sun G, Irvine KD. 2014. Regulation of YAP by mechanical strain through Jnk and Hippo signaling. Curr. Biol. 24:172012–17
    [Google Scholar]
  25. Constantinescu D, Gray HL, Sammak PJ, Schatten GP, Csoka AB. 2006. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24:1177–85
    [Google Scholar]
  26. Cremer T, Cremer C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2:4292–301
    [Google Scholar]
  27. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C et al. 2006. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172:141–53
    [Google Scholar]
  28. Dahl KN, Engler AJ, Pajerowski JD, Discher DE. 2005. Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys. J. 89:42855–64
    [Google Scholar]
  29. Dahl KN, Kahn SM, Wilson KL, Discher DE. 2004. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 117:Part 204779–86
    [Google Scholar]
  30. Dai J, Sheetz MP. 1995. Axon membrane flows from the growth cone to the cell body. Cell 83:5693–701
    [Google Scholar]
  31. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J et al. 2003. Lamin A truncation in Hutchinson-Gilford progeria. Science 300:56282055
    [Google Scholar]
  32. Dechat T, Gesson K, Foisner R. 2010. Lamina-independent lamins in the nuclear interior serve important functions. Cold Spring Harb. Symp. Quant. Biol. 75:533–43
    [Google Scholar]
  33. Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA et al. 2007. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. PNAS 104:124955–60
    [Google Scholar]
  34. Delbarre E, Tramier M, Coppey-Moisan M, Gaillard C, Courvalin J-C, Buendia B. 2006. The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum. Mol. Genet. 15:71113–22
    [Google Scholar]
  35. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M et al. 2016. Nuclear envelope rupture and repair during cancer cell migration. Science 352:6283353–58
    [Google Scholar]
  36. Deshpande S, Wunnava S, Hueting D, Dekker C. 2019. Membrane tension-mediated growth of liposomes. Small 15:38e1902898
    [Google Scholar]
  37. Diz-Muñoz A, Fletcher DA, Weiner OD. 2013. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol 23:247–53
    [Google Scholar]
  38. Driscoll TP, Cosgrove BD, Heo S-J, Shurden ZE, Mauck RL. 2015. Cytoskeletal to nuclear strain transfer regulates YAP signaling in mesenchymal stem cells. Biophys. J. 108:122783–93
    [Google Scholar]
  39. Drozdz MM, Vaux DJ. 2017. Shared mechanisms in physiological and pathological nucleoplasmic reticulum formation. Nucleus 8:134–45
    [Google Scholar]
  40. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:7350179–83
    [Google Scholar]
  41. Eckersley-Maslin MA, Bergmann JH, Lazar Z, Spector DL. 2013. Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucleus 4:153–60
    [Google Scholar]
  42. Ege N, Dowbaj AM, Jiang M, Howell M, Hooper S et al. 2018. Quantitative analysis reveals that actin and Src-family kinases regulate nuclear YAP1 and its export. Cell Syst 6:6692–708.e13
    [Google Scholar]
  43. Elosegui-Artola A, Andreu I, Beedle AEM, Lezamiz A, Uroz M et al. 2017. Force triggers YAP nuclear entry by regulating transport across nuclear pores. Cell 171:61397–410.e14
    [Google Scholar]
  44. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:4677–89
    [Google Scholar]
  45. Enyedi B, Jelcic M, Niethammer P. 2016. The cell nucleus serves as a mechanotransducer of tissue damage-induced inflammation. Cell 165:51160–70
    [Google Scholar]
  46. Enyedi B, Kala S, Nikolich-Zugich T, Niethammer P. 2013. Tissue damage detection by osmotic surveillance. Nat. Cell Biol. 15:91123–30
    [Google Scholar]
  47. Enyedi B, Niethammer P. 2016. A case for the nuclear membrane as a mechanotransducer. Cell Mol. Bioeng. 9:2247–51
    [Google Scholar]
  48. Enyedi B, Niethammer P. 2017. Nuclear membrane stretch and its role in mechanotransduction. Nucleus 8:2156–61
    [Google Scholar]
  49. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J et al. 2003. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423:6937293–98
    [Google Scholar]
  50. Fidziańska A, Toniolo D, Hausmanowa-Petrusewicz I. 1998. Ultrastructural abnormality of sarcolemmal nuclei in Emery-Dreifuss muscular dystrophy (EDMD). J. Neurol. Sci. 159:188–93
    [Google Scholar]
  51. Franke WW, Deumling B, Baerbelermen Jarasch ED, Kleinig H 1970. Nuclear membranes from mammalian liver. I. Isolation procedure and general characterization. J. Cell Biol. 46:2379–95
    [Google Scholar]
  52. Fricker M, Hollinshead M, White N, Vaux D. 1997. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136:3531–44
    [Google Scholar]
  53. Funkhouser CM, Sknepnek R, Shimi T, Goldman AE, Goldman RD, Olvera de la Cruz M 2013. Mechanical model of blebbing in nuclear lamin meshworks. PNAS 110:93248–53
    [Google Scholar]
  54. Furusawa T, Rochman M, Taher L, Dimitriadis EK, Nagashima K et al. 2015. Chromatin decompaction by the nucleosomal binding protein HMGN5 impairs nuclear sturdiness. Nat. Commun. 6:6138
    [Google Scholar]
  55. García-González A, Jacchetti E, Marotta R, Tunesi M, Rodríguez Matas JF, Raimondi MT 2018. The effect of cell morphology on the permeability of the nuclear envelope to diffusive factors. Front. Physiol. 9:925
    [Google Scholar]
  56. Gargiuli C, Schena E, Mattioli E, Columbaro M, D'Apice MR et al. 2018. Lamins and bone disorders: current understanding and perspectives. Oncotarget 9:3222817–31
    [Google Scholar]
  57. Gault WJ, Enyedi B, Niethammer P. 2014. Osmotic surveillance mediates rapid wound closure through nucleotide release. J. Cell Biol. 207:6767–82
    [Google Scholar]
  58. Gauthier NC, Masters TA, Sheetz MP. 2012. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol 22:10527–35
    [Google Scholar]
  59. Gerace L, Blobel G. 1980. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19:1277–87
    [Google Scholar]
  60. Goswami R, Asnacios A, Hamant O, Chabouté M-E. 2020. Is the plant nucleus a mechanical rheostat?. Curr. Opin. Plant Biol. 57:155–63
    [Google Scholar]
  61. Graham DM, Andersen T, Sharek L, Uzer G, Rothenberg K et al. 2018. Enucleated cells reveal differential roles of the nucleus in cell migration, polarity, and mechanotransduction. J. Cell Biol. 217:3895–914
    [Google Scholar]
  62. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB et al. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:7197948–51
    [Google Scholar]
  63. Guilluy C, Osborne LD, Van Landeghem L, Sharek L, Superfine R et al. 2014. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16:4376–81
    [Google Scholar]
  64. Guo Y, Kim Y, Shimi T, Goldman RD, Zheng Y. 2014. Concentration-dependent lamin assembly and its roles in the localization of other nuclear proteins. Mol. Biol. Cell 25:81287–97
    [Google Scholar]
  65. Haider A, Wei Y-C, Lim K, Barbosa AD, Liu C-H et al. 2018. PCYT1A regulates phosphatidylcholine homeostasis from the inner nuclear membrane in response to membrane stored curvature elastic stress. Dev. Cell 45:4481–95.e8
    [Google Scholar]
  66. Hallett FR, Marsh J, Nickel BG, Wood JM. 1993. Mechanical properties of vesicles. II. A model for osmotic swelling and lysis. Biophys. J. 64:2435–42
    [Google Scholar]
  67. Hatch E, Hetzer M. 2014. Breaching the nuclear envelope in development and disease. J. Cell Biol. 205:2133–41
    [Google Scholar]
  68. Hatzakis NS, Bhatia VK, Larsen J, Madsen KL, Bolinger P-Y et al. 2009. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 5:11835–41
    [Google Scholar]
  69. Hennekes H, Nigg EA. 1994. The role of isoprenylation in membrane attachment of nuclear lamins. A single point mutation prevents proteolytic cleavage of the lamin A precursor and confers membrane binding properties. J. Cell Sci. 107:Part 41019–29
    [Google Scholar]
  70. Hetzer MW. 2010. The nuclear envelope. Cold Spring Harb. Perspect. Biol. 2:3a000539
    [Google Scholar]
  71. Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J. 2013. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497:7450507–11
    [Google Scholar]
  72. Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol. Rev. 89:1193–277
    [Google Scholar]
  73. Holaska JM, Kowalski AK, Wilson KL. 2004. Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLOS Biol 2:9E231
    [Google Scholar]
  74. Huang C, Niethammer P. 2018. Tissue damage signaling is a prerequisite for protective neutrophil recruitment to microbial infection in zebrafish. Immunity 48:51006–13.e6
    [Google Scholar]
  75. Ihalainen TO, Aires L, Herzog FA, Schwartlander R, Moeller J, Vogel V. 2015. Differential basal-to-apical accessibility of lamin A/C epitopes in the nuclear lamina regulated by changes in cytoskeletal tension. Nat. Mater. 14:121252–61
    [Google Scholar]
  76. Irianto J, Pfeifer CR, Bennett RR, Xia Y, Ivanovska IL et al. 2016. Nuclear constriction segregates mobile nuclear proteins away from chromatin. Mol. Biol. Cell 27:254011–20
    [Google Scholar]
  77. Irianto J, Xia Y, Pfeifer CR, Athirasala A, Ji J et al. 2017. DNA damage follows repair factor depletion and portends genome variation in cancer cells after pore migration. Curr. Biol. 27:2210–23
    [Google Scholar]
  78. Jaalouk DE, Lammerding J. 2009. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10:63–73
    [Google Scholar]
  79. Jacobson EC, Perry JK, Long DS, Olins AL, Olins DE et al. 2018. Migration through a small pore disrupts inactive chromatin organization in neutrophil-like cells. BMC Biol 16:142
    [Google Scholar]
  80. Janin A, Bauer D, Ratti F, Millat G, Méjat A. 2017. Nuclear envelopathies: a complex LINC between nuclear envelope and pathology. Orphanet J. Rare Dis 12:147
    [Google Scholar]
  81. Katikaneni A, Jelcic M, Gerlach GF, Ma Y, Overholtzer M, Niethammer P. 2020. Lipid peroxidation regulates long-range wound detection through 5-lipoxygenase in zebrafish. Nat. Cell Biol. 22:91049–55
    [Google Scholar]
  82. Khandwala AS, Kasper CB. 1971. The fatty acid composition of individual phospholipids from rat liver nuclear membrane and nuclei. J. Biol. Chem. 246:206242–46
    [Google Scholar]
  83. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL et al. 2009. A perinuclear actin cap regulates nuclear shape. PNAS 106:4519017–22
    [Google Scholar]
  84. Kume K, Cantwell H, Burrell A, Nurse P. 2019. Nuclear membrane protein Lem2 regulates nuclear size through membrane flow. Nat. Commun. 10:1871
    [Google Scholar]
  85. Kusumi A, Fujiwara TK, Chadda R, Xie M, Tsunoyama TA et al. 2012. Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson's fluid-mosaic model. Annu. Rev. Cell Dev. Biol. 28:215–50
    [Google Scholar]
  86. Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL et al. 2006. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281:3525768–80
    [Google Scholar]
  87. Lammerding J, Hsiao J, Schulze PC, Kozlov S, Stewart CL, Lee RT. 2005. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170:5781–91
    [Google Scholar]
  88. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T et al. 2004. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113:3370–78
    [Google Scholar]
  89. Lamparter L, Galic M. 2020. Cellular membranes, a versatile adaptive composite material. Front. Cell Dev. Biol. 8:684
    [Google Scholar]
  90. Le HQ, Ghatak S, Yeung C-YC, Tellkamp F, Günschmann C et al. 2016. Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment. Nat. Cell Biol. 18:8864–75
    [Google Scholar]
  91. Le Roux A-L, Quiroga X, Walani N, Arroyo M, Roca-Cusachs P 2019. The plasma membrane as a mechanochemical transducer. Philos. Trans. R. Soc. B 374: 1779.20180221
    [Google Scholar]
  92. Lehner CF, Stick R, Eppenberger HM, Nigg EA. 1987. Differential expression of nuclear lamin proteins during chicken development. J. Cell Biol. 105:1577–87
    [Google Scholar]
  93. Li Y, Li M, Weigel B, Mall M, Werth VP, Liu M-L. 2020. Nuclear envelope rupture and NET formation is driven by PKCα-mediated lamin B disassembly. EMBO Rep 21:8e48779
    [Google Scholar]
  94. Liu Y-J, Le Berre M, Lautenschlaeger F, Maiuri P, Callan-Jones A et al. 2015. Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 160:4659–72
    [Google Scholar]
  95. Lomakin AJ, Cattin CJ, Cuvelier D, Alraies Z, Molina M et al. 2020. The nucleus acts as a ruler tailoring cell responses to spatial constraints. Science 370:6514eaba2894
    [Google Scholar]
  96. Maciejowski J, Li Y, Bosco N, Campbell PJ, de Lange T 2015. Chromothripsis and kataegis induced by telomere crisis. Cell 163:71641–54
    [Google Scholar]
  97. Maharana S, Iyer KV, Jain N, Nagarajan M, Wang Y, Shivashankar GV. 2016. Chromosome intermingling—the physical basis of chromosome organization in differentiated cells. Nucleic Acids Res 44:115148–60
    [Google Scholar]
  98. Mall M, Walter T, Gorjánácz M, Davidson IF, Nga Ly-Hartig TB et al. 2012. Mitotic lamin disassembly is triggered by lipid-mediated signaling. J. Cell Biol. 198:6981–90
    [Google Scholar]
  99. Markiewicz E, Tilgner K, Barker N, van de Wetering M, Clevers H et al. 2006. The inner nuclear membrane protein emerin regulates β-catenin activity by restricting its accumulation in the nucleus. EMBO J 25:143275–85
    [Google Scholar]
  100. Maurer M, Lammerding J. 2019. The driving force: nuclear mechanotransduction in cellular function, fate, and disease. Annu. Rev. Biomed. Eng. 21:443–68
    [Google Scholar]
  101. Mazumder A, Roopa T, Basu A, Mahadevan L, Shivashankar GV. 2008. Dynamics of chromatin decondensation reveals the structural integrity of a mechanically prestressed nucleus. Biophys. J. 95:63028–35
    [Google Scholar]
  102. Méjat A, Misteli T. 2010. LINC complexes in health and disease. Nucleus 1:140–52
    [Google Scholar]
  103. Miralles F, Posern G, Zaromytidou A-I, Treisman R. 2003. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113:3329–42
    [Google Scholar]
  104. Miroshnikova YA, Cohen I, Ezhkova E, Wickström SA. 2019. Epigenetic gene regulation, chromatin structure, and force-induced chromatin remodelling in epidermal development and homeostasis. Curr. Opin. Genet. Dev. 55:46–51
    [Google Scholar]
  105. Morris CE, Homann U. 2001. Cell surface area regulation and membrane tension. J. Membr. Biol. 179:279–102
    [Google Scholar]
  106. Nakada C, Ritchie K, Oba Y, Nakamura M, Hotta Y et al. 2003. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5:7626–32
    [Google Scholar]
  107. Nava MM, Miroshnikova YA, Biggs LC, Whitefield DB, Metge F et al. 2020. Heterochromatin-driven nuclear softening protects the genome against mechanical stress-induced damage. Cell 181:4800–17.e22
    [Google Scholar]
  108. Navarro CL, De Sandre-Giovannoli A, Bernard R, Boccaccio I, Boyer A et al. 2004. Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 13:202493–503
    [Google Scholar]
  109. Needham D, Nunn RS. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:4997–1009
    [Google Scholar]
  110. Neubert E, Meyer D, Rocca F, Günay G, Kwaczala-Tessmann A et al. 2018. Chromatin swelling drives neutrophil extracellular trap release. Nat. Commun. 9:3767
    [Google Scholar]
  111. Niemelä PS, Miettinen MS, Monticelli L, Hammaren H, Bjelkmar P et al. 2010. Membrane proteins diffuse as dynamic complexes with lipids. J. Am. Chem. Soc. 132:227574–75
    [Google Scholar]
  112. Nmezi B, Xu J, Fu R, Armiger TJ, Rodriguez-Bey G et al. 2019. Concentric organization of A- and B-type lamins predicts their distinct roles in the spatial organization and stability of the nuclear lamina. PNAS 116:104307–15
    [Google Scholar]
  113. Noll M, Thomas JO, Kornberg RD. 1975. Preparation of native chromatin and damage caused by shearing. Science 187:41821203–6
    [Google Scholar]
  114. Olson EN, Nordheim A. 2010. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 11:5353–65
    [Google Scholar]
  115. Ostlund C, Bonne G, Schwartz K, Worman HJ. 2001. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J. Cell Sci. 114:Part 244435–45
    [Google Scholar]
  116. Ottaviano Y, Gerace L. 1985. Phosphorylation of the nuclear lamins during interphase and mitosis. J. Biol. Chem. 260:1624–32
    [Google Scholar]
  117. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. 2010. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191:3677–91
    [Google Scholar]
  118. Peter A, Stick R. 2012. Evolution of the lamin protein family: what introns can tell. Nucleus 3:144–59
    [Google Scholar]
  119. Pfeifer CR, Xia Y, Zhu K, Liu D, Irianto J et al. 2018. Constricted migration increases DNA damage and independently represses cell cycle. Mol. Biol. Cell 29:161948–62
    [Google Scholar]
  120. Pfleger RC, Anderson NG, Snyder F. 1968. Lipid class and fatty acid composition of rat liver plasma membranes isolated by zonal centrifugation. Biochemistry 7:82826–33
    [Google Scholar]
  121. Pinot M, Vanni S, Ambroggio E, Guet D, Goud B, Manneville J-B. 2018. Feedback between membrane tension, lipid shape and curvature in the formation of packing defects. bioRxiv 389627: https://doi.org/10.1101/389627
    [Crossref] [Google Scholar]
  122. Piovesan A, Pelleri MC, Antonaros F, Strippoli P, Caracausi M, Vitale L. 2019. On the length, weight and GC content of the human genome. BMC Res. Notes 12:106
    [Google Scholar]
  123. Pocaterra A, Romani P, Dupont S. 2020. YAP/TAZ functions and their regulation at a glance. J. Cell Sci. 133:2jcs230425
    [Google Scholar]
  124. Qin Z, Kreplak L, Buehler MJ. 2009. Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLOS ONE 4:10e7294
    [Google Scholar]
  125. Raab M, Gentili M, de Belly H, Thiam HR, Vargas P et al. 2016. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352:6283359–62
    [Google Scholar]
  126. Ranade SS, Syeda R, Patapoutian A. 2015. Mechanically activated ion channels. Neuron 87:61162–79
    [Google Scholar]
  127. Riegman M, Sagie L, Galed C, Levin T, Steinberg N et al. 2020. Ferroptosis occurs through an osmotic mechanism and propagates independently of cell rupture. Nat. Cell Biol. 22:1042–48
    [Google Scholar]
  128. Röber RA, Weber K, Osborn M. 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 105:2365–78
    [Google Scholar]
  129. Robertson G, Xie C, Chen D, Awad H, Schwarz EM et al. 2006. Alteration of femoral bone morphology and density in COX-2−/− mice. Bone 39:4767–72
    [Google Scholar]
  130. Romanauska A, Köhler A. 2018. The inner nuclear membrane is a metabolically active territory that generates nuclear lipid droplets. Cell 174:3700–15.e18
    [Google Scholar]
  131. Rowat AC, Lammerding J, Ipsen JH. 2006. Mechanical properties of the cell nucleus and the effect of emerin deficiency. Biophys. J. 91:124649–64
    [Google Scholar]
  132. Ruprecht V, Wieser S, Callan-Jones A, Smutny M, Morita H et al. 2015. Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell 160:4673–85
    [Google Scholar]
  133. Sadoshima J, Izumo S. 1993. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO J 12:41681–92
    [Google Scholar]
  134. Sapra KT, Qin Z, Dubrovsky-Gaupp A, Aebi U, Müller DJ et al. 2020. Nonlinear mechanics of lamin filaments and the meshwork topology build an emergent nuclear lamina. Nat. Commun. 11:6205
    [Google Scholar]
  135. Schatten G, Maul GG, Schatten H, Chaly N, Simerly C et al. 1985. Nuclear lamins and peripheral nuclear antigens during fertilization and embryogenesis in mice and sea urchins. PNAS 82:144727–31
    [Google Scholar]
  136. Schreiner SM, Koo PK, Zhao Y, Mochrie SGJ, King MC. 2015. The tethering of chromatin to the nuclear envelope supports nuclear mechanics. Nat. Commun. 6:7159
    [Google Scholar]
  137. Sciaky N, Presley J, Smith C, Zaal KJ, Cole N et al. 1997. Golgi tubule traffic and the effects of Brefeldin A visualized in living cells. J. Cell Biol. 139:51137–55
    [Google Scholar]
  138. Shachar S, Misteli T. 2017. Causes and consequences of nuclear gene positioning. J. Cell Sci. 130:91501–8
    [Google Scholar]
  139. Shah P, Hobson CM, Cheng S, Colville MJ, Paszek MJ et al. 2020. Nuclear deformation causes DNA damage by increasing replication stress. Curr. Biol. 31:4753–65.e6
    [Google Scholar]
  140. Shen Z, Niethammer P. 2020. A cellular sense of space and pressure. Science 370:6514295–96
    [Google Scholar]
  141. Shi Z, Graber ZT, Baumgart T, Stone HA, Cohen AE. 2018. Cell membranes resist flow. Cell 175:71769–79.e13
    [Google Scholar]
  142. Shimamoto Y, Tamura S, Masumoto H, Maeshima K. 2017. Nucleosome-nucleosome interactions via histone tails and linker DNA regulate nuclear rigidity. Mol. Biol. Cell 28:111580–89
    [Google Scholar]
  143. Shimi T, Butin-Israeli V, Adam SA, Hamanaka RB, Goldman AE et al. 2011. The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 25:242579–93
    [Google Scholar]
  144. Staykova M, Holmes DP, Read C, Stone HA 2011. Mechanics of surface area regulation in cells examined with confined lipid membranes. PNAS 108:229084–88
    [Google Scholar]
  145. Stephens AD, Banigan EJ, Adam SA, Goldman RD, Marko JF. 2017. Chromatin and lamin A determine two different mechanical response regimes of the cell nucleus. Mol. Biol. Cell 28:141984–96
    [Google Scholar]
  146. Stephens AD, Banigan EJ, Marko JF. 2019. Chromatin's physical properties shape the nucleus and its functions. Curr. Opin. Cell Biol. 58:76–84
    [Google Scholar]
  147. Stephens AD, Liu PZ, Banigan EJ, Almassalha LM, Backman V et al. 2018. Chromatin histone modifications and rigidity affect nuclear morphology independent of lamins. Mol. Biol. Cell 29:2220–33
    [Google Scholar]
  148. Stewart C, Burke B. 1987. Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51:3383–92
    [Google Scholar]
  149. Strick R, Strissel PL, Gavrilov K, Levi-Setti R. 2001. Cation-chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes. J. Cell Biol. 155:6899–910
    [Google Scholar]
  150. Sun Z, Guo SS, Fässler R. 2016. Integrin-mediated mechanotransduction. J. Cell Biol. 215:4445–56
    [Google Scholar]
  151. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PCDP et al. 2013. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341:61491240104
    [Google Scholar]
  152. Tajik A, Zhang Y, Wei F, Sun J, Jia Q et al. 2016. Transcription upregulation via force-induced direct stretching of chromatin. Nat. Mater. 15:121287–96
    [Google Scholar]
  153. Tapley EC, Starr DA. 2013. Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr. Opin. Cell Biol. 25:157–62
    [Google Scholar]
  154. Thiam HR, Wong SL, Qiu R, Kittisopikul M, Vahabikashi A et al. 2020. NETosis proceeds by cytoskeleton and endomembrane disassembly and PAD4-mediated chromatin decondensation and nuclear envelope rupture. PNAS 117:137326–37
    [Google Scholar]
  155. Tifft KE, Bradbury KA, Wilson KL. 2009. Tyrosine phosphorylation of nuclear-membrane protein emerin by Src, Abl and other kinases. J. Cell Sci. 122:Part 203780–90
    [Google Scholar]
  156. Torbati M, Lele TP, Agrawal A 2016. Ultradonut topology of the nuclear envelope. PNAS 113:4011094–99
    [Google Scholar]
  157. Turgay Y, Eibauer M, Goldman AE, Shimi T, Khayat M et al. 2017. The molecular architecture of lamins in somatic cells. Nature 543:7644261–64
    [Google Scholar]
  158. Uhlén M, Björling E, Agaton C, Szigyarto CA-K, Amini B et al. 2005. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell Proteom. 4:121920–32
    [Google Scholar]
  159. Ungricht R, Klann M, Horvath P, Kutay U. 2015. Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J. Cell Biol. 209:5687–703
    [Google Scholar]
  160. van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:2112–24
    [Google Scholar]
  161. van Steensel B, Belmont AS. 2017. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169:5780–91
    [Google Scholar]
  162. Vanni S, Hirose H, Barelli H, Antonny B, Gautier R. 2014. A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment. Nat. Commun. 5:4916
    [Google Scholar]
  163. Vanni S, Vamparys L, Gautier R, Drin G, Etchebest C et al. 2013. Amphipathic lipid packing sensor motifs: probing bilayer defects with hydrophobic residues. Biophys. J. 104:3575–84
    [Google Scholar]
  164. Vargas JD, Hatch EM, Anderson DJ, Hetzer MW. 2012. Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus 3:188–100
    [Google Scholar]
  165. Vartiainen MK, Guettler S, Larijani B, Treisman R. 2007. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science31658321749–52
    [Google Scholar]
  166. Vaughan A, Alvarez-Reyes M, Bridger JM, Broers JL, Ramaekers FC et al. 2001. Both emerin and lamin C depend on lamin A for localization at the nuclear envelope. J. Cell Sci. 114:Part 142577–90
    [Google Scholar]
  167. Venturini V, Pezzano F, Català Castro F, Häkkinen HM, Jiménez-Delgado S et al. 2020. The nucleus measures shape changes for cellular proprioception to control dynamic cell behavior. Science 370:6514eaba2644
    [Google Scholar]
  168. Vortmeyer-Krause M, te Lindert M, te Riet J, te Boekhorst V, Marke R et al. 2020. Lamin B2 follows lamin A/C-mediated nuclear mechanics and cancer cell invasion efficacy. bioRxiv 028969 https://doi.org/10.1101/2020.04.07.028969
    [Crossref]
  169. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B 2004. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. PNAS 101:1396–401
    [Google Scholar]
  170. Wang P, Dreger M, Madrazo E, Williams CJ, Samaniego R et al. 2018. WDR5 modulates cell motility and morphology and controls nuclear changes induced by a 3D environment. PNAS 115:348581–86
    [Google Scholar]
  171. Wang Y, Li M, Stadler S, Correll S, Li P et al. 2009. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184:2205–13
    [Google Scholar]
  172. Wilhelmsen K, Litjens SHM, Kuikman I, Tshimbalanga N, Janssen H et al. 2005. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 171:5799–810
    [Google Scholar]
  173. Xia Y, Ivanovska IL, Zhu K, Smith L, Irianto J et al. 2018. Nuclear rupture at sites of high curvature compromises retention of DNA repair factors. J. Cell Biol. 217:113796–808
    [Google Scholar]
  174. Xia Y, Pfeifer CR, Zhu K, Irianto J, Liu D et al. 2019. Rescue of DNA damage after constricted migration reveals a mechano-regulated threshold for cell cycle. J. Cell Biol. 218:82545–63
    [Google Scholar]
  175. Zhang Q, Ragnauth C, Greener MJ, Shanahan CM, Roberts RG. 2002. The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 80:5473–81
    [Google Scholar]
  176. Zhang X, Schwarz EM, Young DA, Puzas JE, Rosier RN, O'Keefe RJ. 2002. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J. Clin. Invest. 109:111405–15
    [Google Scholar]
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