Cancer cell migration in 3d tissue: Negotiating space by proteolysis and nuclear deformability

Cell Adhesion and Migration

Volumn 9, Issue 5, 2015, Pages 357-366

  Krause, Marina ^a   Wolf, Katarina ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Actomyosin contractility; Cancer cell migration; Chromatin; Confined ECM space; Integrin mediated mechanocoupling; Lamin; Nuclear deformation

Indexed keywords

CANCER CELL; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CELL ORGANELLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOSKELETON; EXTRACELLULAR MATRIX; GEOMETRY; INTERPERSONAL COMMUNICATION; MECHANICS; NUCLEAR LAMINA; PROTEIN DEGRADATION; STROMA; TUMOR INVASION; AIR AND AIR RELATED PHENOMENA; ANIMAL; CELL MOTION; CHROMATIN; HUMAN; METABOLISM; NEOPLASM; NUCLEAR SHAPE; PATHOLOGY;

CHROMATIN;

ANIMALS; CELL MOVEMENT; CELL NUCLEUS SHAPE; CHROMATIN; CONFINED SPACES; EXTRACELLULAR MATRIX; HUMANS; NEOPLASMS; PROTEOLYSIS;

EID: 84953881471     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.1080/19336918.2015.1061173     Document Type: Article

References (100)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell. 2011.02.013.
2. Fidler IJ. The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 2003; 3:453-8; PMID:12778135; http://dx.doi.org/10.1038/nrc1098.
3. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clinical Invest 2009; 119:1420-8; PMID:19487818; http://dx.doi.org/10.1172/JCI39104.
4. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell Migration: Integrating Signals from Front to Back 2003; 302:1704-9.
5. Friedl P, Wolf K, Lammerding J. Nuclear mechanics during cell migration. Cur Opin Cell Biol 2011; 23:55-64; PMID:21109415; http://dx.doi.org/10.1016/j.ceb.2010.10.015.
6. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010; 11:366-78; PMID:20414258; http://dx.doi.org/10.1038/nrm2889.
7. Wolf K, Te Lindert M, Krause M, Alexander S, Te Riet J, Willis AL, Hoffman RM, Figdor CG, Weiss SJ, Friedl P. Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol 2013; 201:1069-84; PMID:23798731; http://dx.doi.org/10.1083/jcb.201210152.
8. Friedl P, Wolf K. Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem Soc Symposium 2003:277-85; PMID:14587300.
9. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, Keller M, Forster R, Critchley DR, Fassler R, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008; 453:51-5; PMID:18451854; http://dx.doi.org/10.1038/nature06887.
10. Voisin MB, Woodfin A, Nourshargh S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler Thromb Vasc Biol 2009; 29:1193-9; PMID:19498176; http://dx.doi.org/10.1161/ATVBAHA.109.187450.
11. Wolf K, Muller R, Borgmann S, Brocker EB, Friedl P. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 2003; 102:3262-9; PMID:12855577; http://dx.doi.org/10.1182/blood-2002-12-3791.
12. Charras G, Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol 2014; 15:813-24; PMID:25355506; http://dx.doi.org/10.1038/nrm3897.
13. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011; 147:992-1009; PMID:22118458; http://dx.doi.org/10.1016/j.cell.2011.11.016.
14. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, van Rheenen J, Deryugina E, Friedl P. Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 2009; 20:931-41; PMID:19682592; http://dx.doi.org/10.1016/j.semcdb. 2009.08.005.
15. Weigelin B, Bakker G-J, Friedl P. Intravital third harmonic generation microscopy of collective melanoma cell invasion. IntraVital 2014; 1:32-43; http://dx.doi.org/10.4161/intv.21223.
16. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6:392-401; PMID:16572188; http://dx.doi.org/10.1038/nrc1877.
17. Khamis ZI, Sahab ZJ, Sang QX. Active roles of tumor stroma in breast cancer metastasis. Intl J Breast Cancer 2012; 2012:574025; PMID:22482059; http://dx.doi.org/10.1155/2012/574025.
18. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG, Keely PJ. Collagen density promotes mammary tumor initiation and progression. BMC Med 2008; 6:11; PMID:18442412; http://dx.doi.org/10.1186/1741-7015-6-11.
19. Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol 2006; 16:1515-23; PMID:16890527; http://dx.doi.org/10.1016/j.cub. 2006.05.065.
20. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007; 9:893-904; PMID:17618273; http://dx.doi.org/10.1038/ncb1616.
21. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 2006; 6:764-75; PMID:16990854; http://dx.doi.org/10.1038/nrc1949.
22. Wolf K, Friedl P. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol 2011; 21:736-44; PMID:22036198; http://dx.doi.org/10.1016/j.tcb.2011.09.006.
23. Lu P, Takai K, Weaver VM, Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harbor Perspect Biol 2011; 3:pii: a005058; PMID:21917992; http://dx.doi.org/10.1101/cshperspect.a005058.
24. Wagenaar-Miller RA, Engelholm LH, Gavard J, Yamada SS, Gutkind JS, Behrendt N, Bugge TH, Holmbeck K. Complementary roles of intracellular and pericellular collagen degradation pathways in vivo. Mol Cell Biol 2007; 27:6309-22; PMID:17620416; http://dx.doi.org/10.1128/MCB. 00291-07.
25. Ranjan A, Kalraiya RD. Invasive potential of melanoma cells correlates with the expression of MT1- MMP and regulated by modulating its association with motility receptors via N-glycosylation on the receptors. BioMed Res Internat 2014; 2014:804680; PMID:25180193; http://dx.doi.org/10.1155/2014/ 804680.
26. Fisher KE, Sacharidou A, Stratman AN, Mayo AM, Fisher SB, Mahan RD, Davis MJ, Davis GE. MT1- MMP- and Cdc42-dependent signaling co-regulate cell invasion and tunnel formation in 3D collagen matrices. J Cell Sci. 2009 Dec 15; 122(Pt 24):4558-69; PMID:19934222; http://dx.doi.org/10.1242/ jcs.050724.
27. Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M, Lopez-Otin C, Shapiro S, Inada M, Krane S, et al. Tumor cell traffic through the extracellular matrix is controlled by the membraneanchored collagenase MT1-MMP. The J Cell Biol 2004; 167:769-81; PMID:15557125; http://dx.doi.org/10.1083/jcb.200408028.
28. Haage A, Nam DH, Ge X, Schneider IC. Matrix metalloproteinase- 14 is a mechanically regulated activator of secreted MMPs and invasion. Biochem Biophys Res Commun 2014; 450:213-8; PMID:24878529; http://dx.doi.org/10.1016/j.bbrc.2014.05.086.
29. Arnoszky SP, Lavagnino M, Whallon JH, Hoonjan A. In situ cell nucleus deformation in tendons under tensile load; a morphological analysis using confocal laser microscopy. J Orthop Res 2002; 20:29-35; PMID:11853087; http://dx.doi.org/10.1016/S0736- 0266(01)00080-8.
30. Beadle C, Assanah MC, Monzo P, Vallee R, Rosenfeld SS, Canoll P. The role of myosin II in glioma invasion of the brain. Mol Biol Cell 2008; 19:3357-68; PMID:18495866; http://dx.doi.org/10.1091/ mbc.E08-03-0319.
31. Caille N, Thoumine O, Tardy Y, Meister JJ. Contribution of the nucleus to the mechanical properties of endothelial cells. J Biomech 2002; 35:177-87; PMID:11784536; http://dx.doi.org/10.1016/S0021- 9290(01)00201-9.
32. Guilak F, Tedrow JR, Burgkart R. Viscoelastic properties of the cell nucleus. Biochem Biophys Res Commun 2000; 269:781-6; PMID:10720492; http://dx.doi.org/10.1006/bbrc.2000.2360.
33. Belin BJ, Cimini BA, Blackburn EH, Mullins RD. Visualization of actin filaments and monomers in somatic cell nuclei. Mol Biol Cell 2013; 24:982-94; PMID:23447706; http://dx.doi.org/10.1091/mbc. E12-09-0685.
34. Fedorchak GR, Kaminski A, Lammerding J. Cellular mechanosensing: getting to the nucleus of it all. Prog Biophys Mol Biol 2014; 115:76-92; PMID:25008017; http://dx.doi.org/10.1016/j.pbiomolbio.2014.06.009.
35. Piccolo S. Embracing mechanical forces in cell biology. Differentiation 2013; 86:75-6; PMID:24054842; http://dx.doi.org/10.1016/j.diff.2013.08.001.
36. Swift J, Discher DE. The nuclear lamina is mechanoresponsive to ECM elasticity in mature tissue. J Cell Sci 2014; 127:3005-15; PMID:24963133; http://dx.doi.org/10.1242/jcs.149203.
37. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE. Physical plasticity of the nucleus in stem cell differentiation. Proceedings of the Natl Acad Sci U S A 2007; 104:15619-24; PMID:17893336; http://dx.doi.org/10.1073/pnas.0702576104.
38. Swaminathan V, Mythreye K, O’Brien ET, Berchuck A, Blobe GC, Superfine R. Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines. Cancer Res 2011; 71:5075-80; PMID:21642375; http://dx.doi.org/10.1158/0008- 5472.CAN-11-0247.
39. Scianna M, Preziosi L, Wolf K. A Cellular Potts Model simulating cell migration on and in matrix environments. Math Biosci Eng 2013; 10:235-61; PMID:23311371; http://dx.doi.org/10.3934/mbe. 2013.10.235.
40. Lammermann T, Sixt M. Mechanical modes of ‘amoeboid’ cell migration. Curr Opin Cell Biol 2009; 21:636-44; PMID:19523798; http://dx.doi.org/10.1016/j.ceb.2009.05.003.
41. Sosa BA, Rothballer A, Kutay U, Schwartz TU. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 2012; 149:1035-47; PMID:22632968; http://dx.doi.org/10.1016/j.cell.2012.03.046.
42. Dupin I, Etienne-Manneville S. Nuclear positioning: mechanisms and functions. Intl J Biochem Cell iol 2011; 43:1698-707; PMID:21959251; http://dx.doi.org/10.1016/j.biocel.2011.09.004.
43. Gomes ER, Jani S, Gundersen GG. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 2005; 121:451-63; PMID:15882626; http://dx.doi.org/10.1016/j.cell.2005.02.022.
44. Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 2010; 329:956-9; PMID:20724637; http://dx.doi.org/10.1126/science.1189072.
45. Houben F, Willems CH, Declercq IL, Hochstenbach K, Kamps MA, Snoeckx LH, Ramaekers FC, Broers JL. Disturbed nuclear orientation and cellular migration in A-type lamin deficient cells. Bioch Biophys Acta 2009; 1793:312-24; PMID:19013199; http://dx.doi.org/10.1016/j.bbamcr.2008.10.003.
46. Kim DH, Cho S, Wirtz D. Tight coupling between nucleus and cell migration through the perinuclear actin cap. J Cell Sci 2014; 127:2528-41; PMID:24639463; http://dx.doi.org/10.1242/ jcs.144345.
47. Wu J, Kent IA, Shekhar N, Chancellor TJ, Mendonca A, Dickinson RB, Lele TP. Actomyosin pulls to advance the nucleus in a migrating tissue cell. Biophys J 2014; 106:7-15; PMID:24411232; http://dx.doi.org/10.1016/j.bpj.2013.11.4489.
48. Alam SG, Lovett D, Kim DI, Roux KJ, Dickinson RB, Lele TP. The nucleus is an intracellular propagator of tensile forces in NIH 3T3 fibroblasts. J Cell Sci 2015; 128:1901-11; PMID:25908852; http://dx.doi.org/10.1242/jcs.161703.
49. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL, Searson PC, Hodzic D, Wirtz D. A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci USA 2009; 106:19017-22; PMID:19850871; http://dx.doi.org/10.1073/pnas. 0908686106.
50. Razafsky D, Wirtz D, Hodzic D. Nuclear envelope in nuclear positioning and cell migration. Adv Exp Med Biol 2014; 773:471-90; PMID:24563361; http://dx.doi.org/10.1007/978-1-4899-8032-8_21.
51. Neelam S, Chancellor TJ, Li Y, Nickerson JA, Roux KJ, Dickinson RB, Lele TP. Direct force probe reveals the mechanics of nuclear homeostasis in the mammalian cell. Proc Natl Acad Sci U S A 2015; 112:5720-5; PMID:25901323; http://dx.doi.org/10.1073/pnas. 1502111112.
52. Khatau SB, Bloom RJ, Bajpai S, Razafsky D, Zang S, Giri A, Wu PH, Marchand J, Celedon A, Hale CM, et al. The distinct roles of the nucleus and nucleuscytoskeleton connections in three-dimensional cell migration. Sci Rep 2012; 2:488; PMID:22761994; http://dx.doi.org/10.1038/srep00488.
53. Chalut KJ, Hopfler M, Lautenschlager F, Boyde L, Chan CJ, Ekpenyong A, Martinez-Arias A, Guck J. Chromatin decondensation and nuclear softening accompany Nanog downregulation in embryonic stem cells. Biophys J 2012; 103:2060-70; PMID:23200040; http://dx.doi.org/10.1016/j.bpj. 2012.10.015.
54. Dey P. Cancer nucleus: morphology and beyond. Diagn Cytopathol 2010; 38:382-90; PMID:19894267.
55. Jevtic P, Levy DL. Mechanisms of nuclear size regulation in model systems and cancer. Adv Exp Medi Biol 2014; 773:537-69; PMID:24563365; http://dx.doi.org/10.1007/978-1-4899-8032-8_25.
56. Contrepois K, Thuret J-Y, Courbeyrette R, Fenaille F, Mann C. Deacetylation of H4-K16Ac and heterochromatin assembly in senescence. Epigenetics Chromatin 2015; 5:15; http://dx.doi.org/10.1186/ 1756-8935-5-15.
57. Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature 2007; 447:433-40; PMID:17522677; http://dx.doi.org/10.1038/ nature05919.
58. Verdone L, Agricola E, Caserta M, Di Mauro E. Histone acetylation in gene regulation. Brief Funct Genom Prot 2006; 5:209-21; PMID:16877467; http://dx.doi.org/10.1093/bfgp/ell028.
59. Kurdistani SK, Grunstein M. Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 2003; 4:276-84; PMID:12671650; http://dx.doi.org/10.1038/nrm1075.
60. Zentner GE, Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 2013; 20:259-66; PMID:23463310; http://dx.doi.org/10.1038/nsmb.2470.
61. Krause M, Te Riet J, Wolf K. Probing the compressibility of tumor cell nuclei by combined atomic forceconfocal microscopy. Phys Biol 2013; 10:065002; PMID:24304807; http://dx.doi.org/10.1088/1478- 3975/10/6/065002.
62. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008; 22:832-53; PMID:18381888; http://dx.doi.org/10.1101/gad.1652708.
63. Gerlitz G, Bustin M. Efficient cell migration requires global chromatin condensation. J Cell Sci 2010; 123:2207-17; PMID:20530575; http://dx.doi.org/10.1242/jcs.058271.
64. Gerlitz G, Bustin M. The role of chromatin structure in cell migration. Trends Cell Biol 2011; 21:6-11; PMID:20951589; http://dx.doi.org/10.1016/j.tcb. 2010.09.002.
65. Kaufmann A, Heinemann F, Radmacher M, Stick R. Amphibian oocyte nuclei expressing lamin A with the progeria mutation E145K exhibit an increased elastic modulus. Nucleus 2011; 2:310-9; PMID:21941106; http://dx.doi.org/10.4161/nucl.2.4.16119.
66. Lombardi ML, Lammerding J. Keeping the LINC: the importance of nucleocytoskeletal coupling in intracellular force transmission and cellular function. Biochem Soc Trans 2011; 39:1729-34; PMID:22103516; http://dx.doi.org/10.1042/ BST20110686.
67. Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL, Young SG, Lee RT. Lamins A and C but not lamin B1 regulate nuclear mechanics. J Biol Chem 2006; 281:25768-80; PMID:16825190; http://dx.doi.org/10.1074/jbc.M513511200.
68. Dechat T, Korbei B, Vaughan OA, Vlcek S, Hutchison CJ, Foisner R. Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. J Cell Sci 2000; 113 Pt 19:3473-84; PMID:10984438.
69. Gruenbaum Y, Goldman RD, Meyuhas R, Mills E, Margalit A, Fridkin A, Dayani Y, Prokocimer M, Enosh A. The nuclear lamina and its functions in the nucleus. Int Rev Cytol 2003; 226:1-62; PMID:12921235; http://dx.doi.org/10.1016/S0074- 7696(03)01001-5.
70. Camozzi D, Capanni C, Cenni V, Mattioli E, Columbaro M, Squarzoni S, Lattanzi G. Diverse lamindependent mechanisms interact to control chromatin dynamics. Focus on laminopathies. Nucleus 2014; 5:427-40; PMID:25482195; http://dx.doi.org/10.4161/nucl.36289.
71. de Las Heras JI, Batrakou DG, Schirmer EC. Cancer biology and the nuclear envelope: a convoluted relationship. Semin cancer Biol 2013; 23:125-37; PMID:22311402; http://dx.doi.org/10.1016/j. semcancer.2012.01.008.
72. Gruenbaum Y, Wilson KL, Harel A, Goldberg M, Cohen M. Review: nuclear lamins–structural proteins with fundamental functions. J Struct Biol 2000; 129:313-23; PMID:10806082; http://dx.doi.org/10.1006/jsbi.2000.4216.
73. Bridger JM, Foeger N, Kill IR, Herrmann H. The nuclear lamina. FEBS J 2007; 274:1354-61; PMID:17489093; http://dx.doi.org/10.1111/j.1742- 4658.2007.05694.x
74. Kubben N, Voncken JW, Misteli T. Mapping of protein- and chromatin-interactions at the nuclear lamina. Nucleus 2010; 1:460-71; PMID:21327087; http://dx.doi.org/10.4161/nucl.1.6.13513.
75. Mattout A, Goldberg M, Tzur Y, Margalit A, Gruenbaum Y. Specific and conserved sequences in D. melanogaster and C. elegans lamins and histone H2A mediate the attachment of lamins to chromosomes. J Cell Sci 2007; 120:77-85; PMID:17148572; http://dx.doi.org/10.1242/jcs.03325.
76. Andres V, Gonzalez JM. Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol 2009; 187:945-57; PMID:20038676; http://dx.doi.org/10.1083/jcb.200904124.
77. Boban M, Braun J, Foisner R. Lamins: ‘structure goes cycling’. Bioch Soc Trans 2009; 38:301-6; http://dx.doi.org/10.1042/BST0380301.
78. Broers JL, Ramaekers FC. The role of the nuclear lamina in cancer and apoptosis. Adv Exp Med Biol 2014; 773:27-48; PMID:24563342; http://dx.doi.org/10.1007/978-1-4899-8032-8_2.
79. Shin JW, Swift J, Ivanovska I, Spinler KR, Buxboim A, Discher DE. Mechanobiology of bone marrow stem cells: from myosin-II forces to compliance of matrix and nucleus in cell forms and fates. Differentiation 2013; 86:77-86; PMID:23790394; http://dx.doi.org/10.1016/j.diff.2013.05.001.
80. Olins AL, Ernst A, Zwerger M, Herrmann H, Olins DE. An in vitro model for Pelger-Hu€et anomaly. Nucleus 2010; 1:506-12; http://dx.doi.org/10.4161/ nucl.1.6.13271.
81. Hoffmann K, Dreger CK, Olins AL, Olins DE, Shultz LD, Lucke B, Karl H, Kaps R, Muller D, Vaya A, et al. Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nat Genet 2002; 31:410-4; PMID:12118250.
82. Rowat AC, Jaalouk DE, Zwerger M, Ung WL, Eydelnant IA, Olins DE, Olins AL, Herrmann H, Weitz DA, Lammerding J. Nuclear envelope composition determines the ability of neutrophil-type cells to passage through micron-scale constrictions. J Biol Chem 2013; 288:8610-8; PMID:23355469; http://dx.doi.org/10.1074/jbc.M112.441535.
83. Hass R, Giese G, Meyer G, Hartmann A, Dork T, Kohler L, Resch K, Traub P, Goppelt-Strube M. Differentiation and retrodifferentiation of U937 cells: reversible induction and suppression of intermediate filament protein synthesis. Eur J Cell Biol 1990; 51:265-71; PMID:2351153.
84. Chow KH, Factor RE, Ullman KS. The nuclear envelope environment and its cancer connections. Nat Rev Cancer 2012; 12:196-209; PMID:22337151.
85. Belt EJ, Fijneman RJ, van den Berg EG, Bril H, Delisvan Diemen PM, Tijssen M, van Essen HF, de Langede Klerk ES, Belien JA, Stockmann HB, et al. Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence. Eur J Cancer 2011; 47:1837-45; PMID:21621406; http://dx.doi.org/10.1016/j.ejca.2011.04.025.
86. Moss SF, Krivosheyev V, de Souza A, Chin K, Gaetz HP, Chaudhary N, Worman HJ, Holt PR. Decreased and aberrant nuclear lamin expression in gastrointestinal tract neoplasms. Gut 1999; 45:723-9; PMID:10517909; http://dx.doi.org/10.1136/gut.45.5.723.
87. Schape J, Prausse S, Radmacher M, Stick R. Influence of lamin A on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys J 2009; 96:4319-25; PMID:19450502; http://dx.doi.org/10.1016/j.bpj.2009.02.048.
88. Broers JL, Peeters EA, Kuijpers HJ, Endert J, Bouten CV, Oomens CW, Baaijens FP, Ramaekers FC. Decreased mechanical stiffness in LMNA-/-cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum Mol Genet 2004; 13:2567-80; PMID:15367494; http://dx.doi.org/10.1093/hmg/ddh295.
89. Harada T, Swift J, Irianto J, Shin JW, Spinler KR, Athirasala A, Diegmiller R, Dingal PC, Ivanovska IL, Discher DE. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 2014; 204:669-82; PMID:24567359; http://dx.doi.org/10.1083/jcb.201308029.
90. Ferrera D, Canale C, Marotta R, Mazzaro N, Gritti M, Mazzanti M, Capellari S, Cortelli P, Gasparini L. Lamin B1 overexpression increases nuclear rigidity in autosomal dominant leukodystrophy fibroblasts. FASEB J 2014; PMID:24858279.
91. Buxboim A, Swift J, Irianto J, Spinler KR, Dingal PC, Athirasala A, Kao YR, Cho S, Harada T, Shin JW, et al. Matrix elasticity regulates lamin-A,C phosphorylation and turnover with feedback to actomyosin. Curr Biol 2014; 24:1909-17; PMID:25127216; http://dx.doi.org/10.1016/j. cub.2014.07.001.
92. Humphrey JD, Dufresne ER, Schwartz MA. Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 2014; 15:802-12; PMID:25355505; http://dx.doi.org/10.1038/nrm3896.
93. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, Tewari M, et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013; 341:1240104; PMID:23990565; http://dx.doi.org/10.1126/science.1240104.
94. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Muller S, Eils R, Cremer C, Speicher MR, et al. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 2005; 3:e157; PMID:15839726; http://dx.doi.org/10.1371/journal.pbio.0030157.
95. Kong L, et al. Lamin A/C protein is overexpressed in tissue-invading prostate cancer and promotes prostate cancer cell growth, migration and invasion through the PI3K/AKT/PTEN pathway. Carcinogenesis, 2012; 33(4):751-9.
96. Willis ND, Cox TR, Rahman-Casans SF, Smits K, Przyborski SA, van den Brandt P, van Engeland M, Weijenberg M, Wilson RG, de Bruine A, et al. Lamin A/C is a risk biomarker in colorectal cancer. PloS One 2008; 3:e2988; http://dx.doi.org/10.1371/journal. pone.0002988.
97. Davidson PM, Denais C, Bakshi MC, Lammerding J. Nuclear deformability constitutes a rate-limiting step during cell migration in 3-D environments. Cell Mol Bioeng 2014; 7: 293-306; PMID:25436017; http://dx.doi.org/10.1007/s12195-014-0342-y
98. Greiner AM, Jackel M, Scheiwe AC, Stamow DR, Autenrieth TJ, Lahann J, Franz CM, Bastmeyer M. Multifunctional polymer scaffolds with adjustable pore size and chemoattractant gradients for studying cell matrix invasion. Biomaterials 2014; 35:611-9; PMID:24140047; http://dx.doi.org/10.1016/j. biomaterials.2013.09.095.
99. Davidson PM, Lammerding J. Broken nuclei–lamins, nuclear mechanics, and disease. Trends Cell Biol 2014; 24:247-56; PMID:24309562; http://dx.doi.org/10.1016/j.tcb.2013.11.004.
100. Navarro-Lerida I, Pellinen T, Sanchez SA, Guadamillas MC, Wang Y, Mirtti T, Calvo E, Del Pozo MA. Rac1 nucleocytoplasmic shuttling drives nuclear shape changes and tumor invasion. Dev Cell 2015; 32:318-34; PMID:25640224; http://dx.doi.org/10.1016/j. devcel.2014.12.019