Scaffold, mechanics and functions of nuclear lamins.
intermediate filaments
lamins
mechanobiology
nuclear lamina
progeria
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
05
09
2023
received:
16
06
2023
accepted:
26
09
2023
medline:
29
11
2023
pubmed:
10
10
2023
entrez:
9
10
2023
Statut:
ppublish
Résumé
Nuclear lamins are type-V intermediate filaments that are involved in many nuclear processes. In mammals, A- and B-type lamins assemble into separate physical meshwork underneath the inner nuclear membrane, the nuclear lamina, with some residual fraction localized within the nucleoplasm. Lamins are the major part of the nucleoskeleton, providing mechanical strength and flexibility to protect the genome and allow nuclear deformability, while also contributing to gene regulation via interactions with chromatin. While lamins are the evolutionary ancestors of all intermediate filament family proteins, their ultimate filamentous assembly is markedly different from their cytoplasmic counterparts. Interestingly, hundreds of genetic mutations in the lamina proteins have been causally linked with a broad range of human pathologies, termed laminopathies. These include muscular, neurological and metabolic disorders, as well as premature aging diseases. Recent technological advances have contributed to resolving the filamentous structure of lamins and the corresponding lamina organization. In this review, we revisit the multiscale lamin organization and discuss its implications on nuclear mechanics and chromatin organization within lamina-associated domains.
Identifiants
pubmed: 37813648
doi: 10.1002/1873-3468.14750
doi:
Substances chimiques
Lamins
0
Chromatin
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2791-2805Subventions
Organisme : BIRAX Regenerative Medicine Initiative
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 310030_207453
Informations de copyright
© 2023 Federation of European Biochemical Societies.
Références
Franke WW, Scheer U, Krohne G and Jarasch ED (1981) The nuclear envelope and the architecture of the nuclear periphery. J Cell Biol 91, 39s-50s.
Watson ML (1954) Pores in the mammalian nuclear membrane. Biochim Biophys Acta 15, 475-479.
Romanauska A and Kohler A (2018) The inner nuclear membrane is a metabolically active territory that generates nuclear lipid droplets. Cell 174, 700-715.e18.
Gorlich D and Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15, 607-660.
Grossman E, Medalia O and Zwerger M (2012) Functional architecture of the nuclear pore complex. Annu Rev Biophys 41, 557-584.
Fawcett DW (1966) On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. Am J Anat 119, 129-145.
Burke B and Stewart CL (2013) The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14, 13-24.
Schuller AP, Wojtynek M, Mankus D, Tatli M, Kronenberg-Tenga R, Regmi SG, Dip PV, Lytton-Jean AKR, Brignole EJ, Dasso M et al. (2021) The cellular environment shapes the nuclear pore complex architecture. Nature 598, 667-671.
Koreny L and Field MC (2016) Ancient eukaryotic origin and evolutionary plasticity of nuclear lamina. Genome Biol Evol 8, 2663-2671.
Stick R and Peter A (2020) Evolution of the Lamin protein family at the base of the vertebrate lineage. Cell Tissue Res 379, 37-44.
Dechat T, Adam SA, Taimen P, Shimi T and Goldman RD (2010) Nuclear lamins. Cold Spring Harb Perspect Biol 2, a000547.
Ho CY and Lammerding J (2012) Lamins at a glance. J Cell Sci 125, 2087-2093.
Dittmer TA and Misteli T (2011) The Lamin protein family. Genome Biol 12, 222.
Lehner CF, Stick R, Eppenberger HM and Nigg EA (1987) Differential expression of nuclear Lamin proteins during chicken development. J Cell Biol 105, 577-587.
Zuela N, Bar DZ and Gruenbaum Y (2012) Lamins in development, tissue maintenance and stress. EMBO Rep 13, 1070-1078.
Constantinescu D, Gray HL, Sammak PJ, Schatten GP and Csoka AB (2006) Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185.
Stuurman N, Heins S and Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122, 42-66.
Turgay Y and Medalia O (2017) The structure of Lamin filaments in somatic cells as revealed by cryo-electron tomography. Nucleus 8, 475-481.
Fisher DZ, Chaudhary N and Blobel G (1986) cDNA sequencing of nuclear lamins a and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 83, 6450-6454.
Steinert PM and Roop DR (1988) Molecular and cellular biology of intermediate filaments. Annu Rev Biochem 57, 593-625.
Lin Y, Mori E, Kato M, Xiang S, Wu L, Kwon I and McKnight SL (2016) Toxic PR poly-dipeptides encoded by the C9orf72 repeat expansion target LC domain polymers. Cell 167, 789-802.e12.
Zhou X, Lin Y, Kato M, Mori E, Liszczak G, Sutherland L, Sysoev VO, Murray DT, Tycko R and McKnight SL (2021) Transiently structured head domains control intermediate filament assembly. Proc Natl Acad Sci USA 118, e2022121118.
Torvaldson E, Kochin V and Eriksson JE (2015) Phosphorylation of lamins determine their structural properties and signaling functions. Nucleus 6, 166-171.
Sept D and McCammon JA (2001) Thermodynamics and kinetics of Actin filament nucleation. Biophys J 81, 667-674.
Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A and Dalton M (1994) The processing pathway of prelamin a. J Cell Sci 107 (Pt 1), 61-67.
Young SG, Meta M, Yang SH and Fong LG (2006) Prelamin a farnesylation and progeroid syndromes. J Biol Chem 281, 39741-39745.
Zheng M, Jin G and Zhou Z (2022) Post-translational modification of Lamins: mechanisms and functions. Front Cell Dev Biol 10, 864191.
Michaelis S and Hrycyna CA (2013) Biochemistry. A protease for the ages. Science 339, 1529-1530.
Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K et al. (2002) Defective prelamin a processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 31, 94-99.
Worman HJ and Michaelis S (2018) Permanently Farnesylated Prelamin a, progeria, and atherosclerosis. Circulation 138, 283-286.
Parry DA and Steinert PM (1999) Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Q Rev Biophys 32, 99-187.
Makarov AA, Zou J, Houston DR, Spanos C, Solovyova AS, Cardenal-Peralta C, Rappsilber J and Schirmer EC (2019) Lamin a molecular compression and sliding as mechanisms behind nucleoskeleton elasticity. Nat Commun 10, 3056.
Ahn J, Jo I, Kang SM, Hong S, Kim S, Jeong S, Kim YH, Park BJ and Ha NC (2019) Structural basis for Lamin assembly at the molecular level. Nat Commun 10, 3757.
Lilina AV, Chernyatina AA, Guzenko D and Strelkov SV (2019) Lateral A11 type tetramerization in lamins. J Struct Biol 209, 107404.
Zwerger M and Medalia O (2013) From lamins to lamina: a structural perspective. Histochem Cell Biol 140, 3-12.
Eibauer M, Weber MS, Kronenberg-Tenga R, Beales CT, Boujemaa-Paterski R, Turgay Y, Sivagurunathan S, Kraxner J, Koester S, Goldman RD et al. (2023) Vimentin filaments integrate low complexity domains in a highly complex helical structure. bioRxiv. doi: 10.1101/2023.05.22.541714 [PREPRINT].
Kittisopikul M, Shimi T, Tatli M, Tran JR, Zheng Y, Medalia O, Jaqaman K, Adam SA and Goldman RD (2021) Computational analyses reveal spatial relationships between nuclear pore complexes and specific lamins. J Cell Biol 220, e202007082.
Harapin J, Bormel M, Sapra KT, Brunner D, Kaech A and Medalia O (2015) Structural analysis of multicellular organisms with cryo-electron tomography. Nat Methods 12, 634-636.
Weber MS, Wojtynek M and Medalia O (2019) Cellular and structural studies of eukaryotic cells by Cryo-electron tomography. Cells 8, 57.
Tenga R and Medalia O (2020) Structure and unique mechanical aspects of nuclear Lamin filaments. Curr Opin Struct Biol 64, 152-159.
Lucic V, Forster F and Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74, 833-865.
Fridman K, Mader A, Zwerger M, Elia N and Medalia O (2012) Advances in tomography: probing the molecular architecture of cells. Nat Rev Mol Cell Biol 13, 736-742.
Irobalieva RN, Martins B and Medalia O (2016) Cellular structural biology as revealed by cryo-electron tomography. J Cell Sci 129, 469-476.
Wang C, Wojtynek M and Medalia O (2023) Structural investigation of eukaryotic cells: from the periphery to the interior by cryo-electron tomography. Adv Biol Regul 87, 100923.
Medalia O, Weber I, Frangakis AS, Nicastro D, Gerisch G and Baumeister W (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298, 1209-1213.
Medeiros JM, Bock D and Pilhofer M (2018) Imaging bacteria inside their host by cryo-focused ion beam milling and electron cryotomography. Curr Opin Microbiol 43, 62-68.
Ghosal D, Kim KW, Zheng H, Kaplan M, Truchan HK, Lopez AE, McIntire IE, Vogel JP, Cianciotto NP and Jensen GJ (2019) In vivo structure of the legionella type II secretion system by electron cryotomography. Nat Microbiol 4, 2101-2108.
Chung WL, Eibauer M, Li W, Boujemaa-Paterski R, Geiger B and Medalia O (2022) A network of mixed Actin polarity in the leading edge of spreading cells. Commun Biol 5, 1338.
Turgay Y, Eibauer M, Goldman AE, Shimi T, Khayat M, Ben-Harush K, Dubrovsky-Gaupp A, Sapra KT, Goldman RD and Medalia O (2017) The molecular architecture of lamins in somatic cells. Nature 543, 261-264.
Stick R and Peter A (2017) Evolutionary changes in Lamin expression in the vertebrate lineage. Nucleus 8, 392-403.
Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, Tewari M et al. (2013) Nuclear Lamin-a scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104.
Wesley CC and Levy DL (2023) Differentiation-dependent changes in Lamin B1 dynamics and Lamin B receptor localization. Mol Biol Cell 34, ar10.
Malashicheva A and Perepelina K (2021) Diversity of nuclear Lamin a/C action as a key to tissue-specific regulation of cellular identity in health and disease. Front Cell Dev Biol 9, 761469.
Wagner T, Merino F, Stabrin M, Moriya T, Antoni C, Apelbaum A, Hagel P, Sitsel O, Raisch T, Prumbaum D et al. (2019) SPHIRE-crYOLO is a fast and accurate fully automated particle picker for cryo-EM. Commun Biol 2, 218.
Evangelisti C, Rusciano I, Mongiorgi S, Ramazzotti G, Lattanzi G, Manzoli L, Cocco L and Ratti S (2022) The wide and growing range of Lamin B-related diseases: from laminopathies to cancer. Cell Mol Life Sci 79, 126.
Rankin J and Ellard S (2006) The laminopathies: a clinical review. Clin Genet 70, 261-274.
Atalaia A, Ben Yaou R, Wahbi K, De Sandre-Giovannoli A, Vigouroux C and Bonne G (2021) Laminopathies' treatments systematic review: a contribution towards a ‘Treatabolome’. J Neuromuscul Dis 8, 419-439.
Tatli M and Medalia O (2018) Insight into the functional organization of nuclear lamins in health and disease. Curr Opin Cell Biol 54, 72-79.
Shin JY and Worman HJ (2022) Molecular pathology of Laminopathies. Annu Rev Pathol 17, 159-180.
Bertrand AT, Brull A, Azibani F, Benarroch L, Chikhaoui K, Stewart CL, Medalia O, Ben Yaou R and Bonne G (2020) Lamin a/C assembly defects in LMNA-congenital muscular dystrophy is responsible for the increased severity of the disease compared with Emery-Dreifuss muscular dystrophy. Cells 9, 844.
Heller SA, Shih R, Kalra R and Kang PB (2020) Emery-Dreifuss muscular dystrophy. Muscle Nerve 61, 436-448.
Captur G, Arbustini E, Bonne G, Syrris P, Mills K, Wahbi K, Mohiddin SA, McKenna WJ, Pettit S, Ho CY et al. (2018) Lamin and the heart. Heart 104, 468-479.
Chaouch M, Allal Y, De Sandre-Giovannoli A, Vallat JM, Amer-el-Khedoud A, Kassouri N, Chaouch A, Sindou P, Hammadouche T, Tazir M et al. (2003) The phenotypic manifestations of autosomal recessive axonal Charcot-Marie-tooth due to a mutation in Lamin A/C gene. Neuromuscul Disord 13, 60-67.
Piekarowicz K, Machowska M, Dzianisava V and Rzepecki R (2019) Hutchinson-Gilford progeria syndrome-current status and prospects for gene therapy treatment. Cells 8, 88.
Kreienkamp R and Gonzalo S (2019) Hutchinson-Gilford progeria syndrome: challenges at bench and bedside. Subcell Biochem 91, 435-451.
Gotzmann J and Foisner R (2006) A-type Lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? Histochem Cell Biol 125, 33-41.
Briand N and Collas P (2018) Laminopathy-causing Lamin a mutations reconfigure lamina-associated domains and local spatial chromatin conformation. Nucleus 9, 216-226.
Osmanagic-Myers S, Dechat T and Foisner R (2015) Lamins at the crossroads of mechanosignaling. Genes Dev 29, 225-237.
Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, Lacene E, Fromes Y, Toussaint M, Mura AM, Keller DI et al. (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet 14, 155-169.
Bank EM, Ben-Harush K, Feinstein N, Medalia O and Gruenbaum Y (2012) Structural and physiological phenotypes of disease-linked Lamin mutations in C. elegans. J Struct Biol 177, 106-112.
Camozzi D, Capanni C, Cenni V, Mattioli E, Columbaro M, Squarzoni S and Lattanzi G (2014) Diverse Lamin-dependent mechanisms interact to control chromatin dynamics. Focus on laminopathies. Nucleus 5, 427-440.
Hennekam RC (2006) Hutchinson-Gilford progeria syndrome: review of the phenotype. Am J Med Genet A 140, 2603-2624.
Maynard S, Keijzers G, Akbari M, Ezra MB, Hall A, Morevati M, Scheibye-Knudsen M, Gonzalo S, Bartek J and Bohr VA (2019) Lamin A/C promotes DNA base excision repair. Nucleic Acids Res 47, 11709-11728.
Taimen P, Pfleghaar K, Shimi T, Moller D, Ben-Harush K, Erdos MR, Adam SA, Herrmann H, Medalia O, Collins FS et al. (2009) A progeria mutation reveals functions for Lamin a in nuclear assembly, architecture, and chromosome organization. Proc Natl Acad Sci USA 106, 20788-20793.
Batista NJ, Desai SG, Perez AM, Finkelstein A, Radigan R, Singh M, Landman A, Drittel B, Abramov D, Ahsan M et al. (2023) The molecular and cellular basis of Hutchinson-Gilford progeria syndrome and potential treatments. Genes (Basel) 14, 602.
Misteli T (2011) HGPS-derived iPSCs for the ages. Cell Stem Cell 8, 4-6.
Dahl KN, Scaffidi P, Islam MF, Yodh AG, Wilson KL and Misteli T (2006) Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 103, 10271-10276.
Zhang J, Lian Q, Zhu G, Zhou F, Sui L, Tan C, Mutalif RA, Navasankari R, Zhang Y, Tse HF et al. (2011) A human iPSC model of Hutchinson Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8, 31-45.
Stierle V, Couprie J, Ostlund C, Krimm I, Zinn-Justin S, Hossenlopp P, Worman HJ, Courvalin JC and Duband-Goulet I (2003) The carboxyl-terminal region common to lamins a and C contains a DNA binding domain. Biochemistry 42, 4819-4828.
Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, Lee CW, Ye C, Ping JL, Mulawadi F et al. (2011) CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 43, 630-638.
Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M and van Steensel B (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 38, 1005-1014.
van Steensel B and Belmont AS (2017) Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169, 780-791.
Harr JC, Luperchio TR, Wong X, Cohen E, Wheelan SJ and Reddy KL (2015) Directed targeting of chromatin to the nuclear lamina is mediated by chromatin state and A-type lamins. J Cell Biol 208, 33-52.
Padeken J, Methot SP and Gasser SM (2022) Establishment of H3K9-methylated heterochromatin and its functions in tissue differentiation and maintenance. Nat Rev Mol Cell Biol 23, 623-640.
Cai Y, Zhang Y, Loh YP, Tng JQ, Lim MC, Cao Z, Raju A, Lieberman Aiden E, Li S, Manikandan L et al. (2021) H3K27me3-rich genomic regions can function as silencers to repress gene expression via chromatin interactions. Nat Commun 12, 719.
Wu F and Yao J (2017) Identifying novel transcriptional and epigenetic features of nuclear lamina-associated genes. Sci Rep 7, 100.
Meuleman W, Peric-Hupkes D, Kind J, Beaudry JB, Pagie L, Kellis M, Reinders M, Wessels L and van Steensel B (2013) Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence. Genome Res 23, 270-280.
Ye Q and Worman HJ (1996) Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to drosophila HP1. J Biol Chem 271, 14653-14656.
Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L et al. (2013) LBR and Lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584-598.
Buxboim A, Irianto J, Swift J, Athirasala A, Shin JW, Rehfeldt F and Discher DE (2017) Coordinated increase of nuclear tension and Lamin-A with matrix stiffness outcompetes Lamin-B receptor that favors soft tissue phenotypes. Mol Biol Cell 28, 3333-3348.
Zullo JM, Demarco IA, Pique-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio TR, Bernstein BE, Pritchard JK, Reddy KL et al. (2012) DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149, 1474-1487.
Foisner R and Gerace L (1993) Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267-1279.
Furukawa K (1999) LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J Cell Sci 112 (Pt 15), 2485-2492.
Wong X, Cutler JA, Hoskins VE, Gordon M, Madugundu AK, Pandey A and Reddy KL (2021) Mapping the micro-proteome of the nuclear lamina and lamina-associated domains. Life Sci Alliance 4, e202000774.
Amendola M and van Steensel B (2015) Nuclear lamins are not required for lamina-associated domain organization in mouse embryonic stem cells. EMBO Rep 16, 610-617.
Harada T, Swift J, Irianto J, Shin JW, Spinler KR, Athirasala A, Diegmiller R, Dingal PC, Ivanovska IL and Discher DE (2014) Nuclear Lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 204, 669-682.
Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K and Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352, 353-358.
Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Dumenil AM, Manel N et al. (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352, 359-362.
Cho S, Vashisth M, Abbas A, Majkut S, Vogel K, Xia Y, Ivanovska IL, Irianto J, Tewari M, Zhu K et al. (2019) Mechanosensing by the lamina protects against nuclear rupture, DNA damage, and cell-cycle arrest. Dev Cell 49, 920-935.e5.
Athirasala A, Hirsch N and Buxboim A (2017) Nuclear mechanotransduction: sensing the force from within. Curr Opin Cell Biol 46, 119-127.
Buxboim A, Swift J, Irianto J, Spinler KR, Dingal PC, Athirasala A, Kao YR, Cho S, Harada T, Shin JW et al. (2014) Matrix elasticity regulates Lamin-a,C phosphorylation and turnover with feedback to actomyosin. Curr Biol 24, 1909-1917.
Sapra KT, Qin Z, Dubrovsky-Gaupp A, Aebi U, Muller DJ, Buehler MJ and Medalia O (2020) Nonlinear mechanics of Lamin filaments and the meshwork topology build an emergent nuclear lamina. Nat Commun 11, 6205.
Qin Z and Buehler MJ (2011) Flaw tolerance of nuclear intermediate filament lamina under extreme mechanical deformation. ACS Nano 5, 3034-3042.
Fudge DS, Gardner KH, Forsyth VT, Riekel C and Gosline JM (2003) The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. Biophys J 85, 2015-2027.
Kreplak L, Herrmann H and Aebi U (2008) Tensile properties of single desmin intermediate filaments. Biophys J 94, 2790-2799.
Qin Z, Kreplak L and Buehler MJ (2009) Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLoS ONE 4, e7294.
Kreplak L, Bar H, Leterrier JF, Herrmann H and Aebi U (2005) Exploring the mechanical behavior of single intermediate filaments. J Mol Biol 354, 569-577.
Litvinov RI, Faizullin DA, Zuev YF and Weisel JW (2012) The alpha-helix to beta-sheet transition in stretched and compressed hydrated fibrin clots. Biophys J 103, 1020-1027.
Zhmurov A, Kononova O, Litvinov RI, Dima RI, Barsegov V and Weisel JW (2012) Mechanical transition from alpha-helical coiled coils to beta-sheets in fibrin(ogen). J Am Chem Soc 134, 20396-20402.
Brown AE, Litvinov RI, Discher DE, Purohit PK and Weisel JW (2009) Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325, 741-744.
Gachon E and Mesquida P (2020) Stretching single collagen fibrils reveals nonlinear mechanical behavior. Biophys J 118, 1401-1408.
Kreplak L, Doucet J, Dumas P and Briki F (2004) New aspects of the alpha-helix to beta-sheet transition in stretched hard alpha-keratin fibers. Biophys J 87, 640-647.
Qin Z and Buehler MJ (2010) Molecular dynamics simulation of the alpha-helix to beta-sheet transition in coiled protein filaments: evidence for a critical filament length scale. Phys Rev Lett 104, 198304.
Albert R, Jeong H and Barabasi AL (2000) Error and attack tolerance of complex networks. Nature 406, 378-382.
Cohen R, Erez K, ben-Avraham D and Havlin S (2000) Resilience of the internet to random breakdowns. Phys Rev Lett 85, 4626-4628.
Callaway DS, Newman ME, Strogatz SH and Watts DJ (2000) Network robustness and fragility: percolation on random graphs. Phys Rev Lett 85, 5468-5471.
Miroshnikova YA and Wickstrom SA (2022) Mechanical forces in nuclear organization. Cold Spring Harb Perspect Biol 14, a039685.
Samwer M, Schneider MWG, Hoefler R, Schmalhorst PS, Jude JG, Zuber J and Gerlich DW (2017) DNA cross-bridging shapes a single nucleus from a set of mitotic chromosomes. Cell 170, 956-972.e23.
Schreiner SM, Koo PK, Zhao Y, Mochrie SG and King MC (2015) The tethering of chromatin to the nuclear envelope supports nuclear mechanics. Nat Commun 6, 7159.
Guilak F, Tedrow JR and Burgkart R (2000) Viscoelastic properties of the cell nucleus. Biochem Biophys Res Commun 269, 781-786.
Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL, Young SG and Lee RT (2006) Lamins a and C but not Lamin B1 regulate nuclear mechanics. J Biol Chem 281, 25768-25780.
Caille N, Thoumine O, Tardy Y and Meister JJ (2002) Contribution of the nucleus to the mechanical properties of endothelial cells. J Biomech 35, 177-187.
Dahl KN, Engler AJ, Pajerowski JD and Discher DE (2005) Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys J 89, 2855-2864.
Dahl KN, Kahn SM, Wilson KL and Discher DE (2004) The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J Cell Sci 117, 4779-4786.
Neelam S, Chancellor TJ, Li Y, Nickerson JA, Roux KJ, Dickinson RB and Lele TP (2015) Direct force probe reveals the mechanics of nuclear homeostasis in the mammalian cell. Proc Natl Acad Sci USA 112, 5720-5725.
Hobson CM, Falvo MR and Superfine R (2021) A survey of physical methods for studying nuclear mechanics and mechanobiology. APL Bioeng 5, 041508.
Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ and Discher DE (2007) Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA 104, 15619-15624.
Bronshtein I, Kepten E, Kanter I, Berezin S, Lindner M, Redwood AB, Mai S, Gonzalo S, Foisner R, Shav-Tal Y et al. (2015) Loss of Lamin a function increases chromatin dynamics in the nuclear interior. Nat Commun 6, 8044.
Naetar N, Korbei B, Kozlov S, Kerenyi MA, Dorner D, Kral R, Gotic I, Fuchs P, Cohen TV, Bittner R et al. (2008) Loss of nucleoplasmic LAP2alpha-Lamin a complexes causes erythroid and epidermal progenitor hyperproliferation. Nat Cell Biol 10, 1341-1348.
Versaevel M, Riaz M, Corne T, Grevesse T, Lantoine J, Mohammed D, Bruyere C, Alaimo L, De Vos WH and Gabriele S (2017) Probing cytoskeletal pre-stress and nuclear mechanics in endothelial cells with spatiotemporally controlled (de-)adhesion kinetics on micropatterned substrates. Cell Adh Migr 11, 98-109.
Stephens AD, Banigan EJ, Adam SA, Goldman RD and Marko JF (2017) Chromatin and Lamin a determine two different mechanical response regimes of the cell nucleus. Mol Biol Cell 28, 1984-1996.
Wintner O, Hirsch-Attas N, Schlossberg M, Brofman F, Friedman R, Kupervaser M, Kitsberg D and Buxboim A (2020) A unified linear viscoelastic model of the cell nucleus defines the mechanical contributions of Lamins and chromatin. Adv Sci (Weinh) 7, 1901222.
Krause M, Te Riet J and Wolf K (2013) Probing the compressibility of tumor cell nuclei by combined atomic force-confocal microscopy. Phys Biol 10, 065002.
Shimamoto Y, Tamura S, Masumoto H and Maeshima K (2017) Nucleosome-nucleosome interactions via histone tails and linker DNA regulate nuclear rigidity. Mol Biol Cell 28, 1580-1589.
Haase K, Macadangdang JK, Edrington CH, Cuerrier CM, Hadjiantoniou S, Harden JL, Skerjanc IS and Pelling AE (2016) Extracellular forces cause the nucleus to deform in a highly controlled anisotropic manner. Sci Rep 6, 21300.
Nakazawa N and Kengaku M (2020) Mechanical regulation of nuclear translocation in migratory neurons. Front Cell Dev Biol 8, 150.
Naetar N, Georgiou K, Knapp C, Bronshtein I, Zier E, Fichtinger P, Dechat T, Garini Y and Foisner R (2021) LAP2alpha maintains a mobile and low assembly state of A-type lamins in the nuclear interior. Elife 10, e63476.
Davidson PM, Denais C, Bakshi MC and Lammerding J (2014) Nuclear deformability constitutes a rate-limiting step during cell migration in 3-D environments. Cell Mol Bioeng 7, 293-306.
Lee H, Adams WJ, Alford PW, McCain ML, Feinberg AW, Sheehy SP, Goss JA and Parker KK (2015) Cytoskeletal prestress regulates nuclear shape and stiffness in cardiac myocytes. Exp Biol Med (Maywood) 240, 1543-1554.
Nitsan I, Drori S, Lewis YE, Cohen S and Tzlil S (2016) Mechanical communication in cardiac cell synchronized beating. Nat Phys 12, 472-477.
Alisafaei F, Jokhun DS, Shivashankar GV and Shenoy VB (2019) Regulation of nuclear architecture, mechanics, and nucleocytoplasmic shuttling of epigenetic factors by cell geometric constraints. Proc Natl Acad Sci USA 116, 13200-13209.
Hobson CM and Stephens AD (2020) Modeling of cell nuclear mechanics: classes, components, and applications. Cells 9, 1623.
Hochmuth RM (2000) Micropipette aspiration of living cells. J Biomech 33, 15-22.
Houchmandzadeh B, Marko JF, Chatenay D and Libchaber A (1997) Elasticity and structure of eukaryote chromosomes studied by micromanipulation and micropipette aspiration. J Cell Biol 139, 1-12.
Stephens AD, Banigan EJ and Marko JF (2018) Separate roles for chromatin and lamins in nuclear mechanics. Nucleus 9, 119-124.
Liu H, Wen J, Xiao Y, Liu J, Hopyan S, Radisic M, Simmons CA and Sun Y (2014) In situ mechanical characterization of the cell nucleus by atomic force microscopy. ACS Nano 8, 3821-3828.
Bustamante CJ, Chemla YR, Liu S and Wang MD (2021) Optical tweezers in single-molecule biophysics. Nat Rev Methods Primers 1, 25.
Aermes C, Hayn A, Fischer T and Mierke CT (2020) Environmentally controlled magnetic nano-tweezer for living cells and extracellular matrices. Sci Rep 10, 13453.
Gosse C and Croquette V (2002) Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys J 82, 3314-3329.
Guck J, Ananthakrishnan R, Mahmood H, Moon TJ, Cunningham CC and Kas J (2001) The optical stretcher: a novel laser tool to micromanipulate cells. Biophys J 81, 767-784.
Chalut KJ, Hopfler M, Lautenschlager F, Boyde L, Chan CJ, Ekpenyong A, Martinez-Arias A and Guck J (2012) Chromatin decondensation and nuclear softening accompany Nanog downregulation in embryonic stem cells. Biophys J 103, 2060-2070.
Gilbert HTJ, Mallikarjun V, Dobre O, Jackson MR, Pedley R, Gilmore AP, Richardson SM and Swift J (2019) Nuclear decoupling is part of a rapid protein-level cellular response to high-intensity mechanical loading. Nat Commun 10, 4149.
Hung CT and Williams JL (1994) A method for inducing equi-biaxial and uniform strains in elastomeric membranes used as cell substrates. J Biomech 27, 227-232.
Schaffer JL, Rizen M, L'Italien GJ, Benbrahim A, Megerman J, Gerstenfeld LC and Gray ML (1994) Device for the application of a dynamic biaxially uniform and isotropic strain to a flexible cell culture membrane. J Orthop Res 12, 709-719.
Seelbinder B, Scott AK, Nelson I, Schneider SE, Calahan K and Neu CP (2020) TENSCell: imaging of stretch-activated cells reveals divergent nuclear behavior and tension. Biophys J 118, 2627-2640.
Zuela-Sopilniak N, Bar-Sela D, Charar C, Wintner O, Gruenbaum Y and Buxboim A (2020) Measuring nucleus mechanics within a living multicellular organism: physical decoupling and attenuated recovery rate are physiological protective mechanisms of the cell nucleus under high mechanical load. Mol Biol Cell 31, 1943-1950.
Lomakin AJ, Cattin CJ, Cuvelier D, Alraies Z, Molina M, Nader GPF, Srivastava N, Saez PJ, Garcia-Arcos JM, Zhitnyak IY et al. (2020) The nucleus acts as a ruler tailoring cell responses to spatial constraints. Science 370, eaba2894.
Cattin CJ, Duggelin M, Martinez-Martin D, Gerber C, Muller DJ and Stewart MP (2015) Mechanical control of mitotic progression in single animal cells. Proc Natl Acad Sci USA 112, 11258-11263.
Lherbette M, Dos Santos A, Hari-Gupta Y, Fili N, Toseland CP and Schaap IAT (2017) Atomic force microscopy micro-rheology reveals large structural inhomogeneities in single cell-nuclei. Sci Rep 7, 8116.
Schape J, Prausse S, Radmacher M and Stick R (2009) Influence of Lamin a on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys J 96, 4319-4325.
Nava MM, Miroshnikova YA, Biggs LC, Whitefield DB, Metge F, Boucas J, Vihinen H, Jokitalo E, Li X, Garcia Arcos JM et al. (2020) Heterochromatin-driven nuclear softening protects the genome against mechanical stress-induced damage. Cell 181, 800-817.e22.
Guilluy C, Osborne LD, Van Landeghem L, Sharek L, Superfine R, Garcia-Mata R and Burridge K (2014) Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat Cell Biol 16, 376-381.
Tajik A, Zhang Y, Wei F, Sun J, Jia Q, Zhou W, Singh R, Khanna N, Belmont AS and Wang N (2016) Transcription upregulation via force-induced direct stretching of chromatin. Nat Mater 15, 1287-1296.
Hu S, Chen J, Butler JP and Wang N (2005) Prestress mediates force propagation into the nucleus. Biochem Biophys Res Commun 329, 423-428.
Stephens AD, Liu PZ, Kandula V, Chen H, Almassalha LM, Herman C, Backman V, O'Halloran T, Adam SA, Goldman RD et al. (2019) Physicochemical mechanotransduction alters nuclear shape and mechanics via heterochromatin formation. Mol Biol Cell mbcE19050286T. doi: 10.1091/mbc.E19-05-0286-T
Stephens AD, Liu PZ, Banigan EJ, Almassalha LM, Backman V, Adam SA, Goldman RD and Marko JF (2018) Chromatin histone modifications and rigidity affect nuclear morphology independent of lamins. Mol Biol Cell 29, 220-233.
Lincoln B, Schinkinger S, Travis K, Wottawah F, Ebert S, Sauer F and Guck J (2007) Reconfigurable microfluidic integration of a dual-beam laser trap with biomedical applications. Biomed Microdevices 9, 703-710.
Guck J, Ananthakrishnan R, Moon TJ, Cunningham CC and Kas J (2000) Optical deformability of soft biological dielectrics. Phys Rev Lett 84, 5451-5454.
Zwerger M, Roschitzki-Voser H, Zbinden R, Denais C, Herrmann H, Lammerding J, Grutter MG and Medalia O (2015) Altering lamina assembly reveals lamina-dependent and -independent functions for A-type lamins. J Cell Sci 128, 3607-3620.
Ben-Harush K, Wiesel N, Frenkiel-Krispin D, Moeller D, Soreq E, Aebi U, Herrmann H, Gruenbaum Y and Medalia O (2009) The supramolecular organization of the C. elegans nuclear Lamin filament. J Mol Biol 386, 1392-1402.
Grossman E, Dahan I, Stick R, Goldberg MW, Gruenbaum Y and Medalia O (2012) Filaments assembly of ectopically expressed Caenorhabditis elegans Lamin within Xenopus oocytes. J Struct Biol 177, 113-118.