Keratin 8/18 regulation of cell stiffness-extracellular matrix interplay through modulation of rho-mediated actin cytoskeleton dynamics

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bordeleau, François ^a,b   Lapierre, Marie Eve ^a   Sheng, Yunlong ^b   Marceau, Normand ^a  

^a Centre de recherche en cancerologie and Centre de Recherche du Centre hospitalier de Québec   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 18; CYTOKERATIN 8; FIBRONECTIN; PROTEIN ROCK; REGULATOR PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL SHAPE; CELL STIFFNESS; CELL STRUCTURE; CELL SURFACE; CELLULAR PARAMETERS; CONTROLLED STUDY; DYNAMICS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE SILENCING; HEPATOMA CELL; INTERMEDIATE FILAMENT; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; NONHUMAN; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM;

ACRYLIC RESINS; ACTINS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBRONECTINS; FOCAL ADHESIONS; INTERMEDIATE FILAMENTS; KERATIN-18; KERATIN-8; KINETICS; MICROSCOPY, CONFOCAL; MICROSPHERES; RATS; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE;

EID: 84862023935     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038780     Document Type: Article

References (56)

1. Butcher DT, Alliston T, Weaver VM, (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9: 108-122.
2. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE, (2007) Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci U S A 104: 15619-15624.
3. Lopez JI, Mouw JK, Weaver VM, (2008) Biomechanical regulation of cell orientation and fate. Oncogene 27: 6981-6993.
4. Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, et al. (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 88: 3689-3698.
5. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
6. Matthews BD, Overby DR, Mannix R, Ingber DE, (2006) Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119: 508-518.
7. Bausch AR, Moller W, Sackmann E, (1999) Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophysical Journal 76: 573-579.
8. Matthews BD, Overby DR, Alenghat FJ, Karavitis J, Numaguchi Y, et al. (2004) Mechanical properties of individual focal adhesions probed with a magnetic microneedle. Biochemical and Biophysical Research Communications 313: 758-764.
9. Bordeleau F, Bessard J, Marceau N, Sheng Y, (2011) Measuring integrated cellular mechanical stress response at focal adhesions by optical tweezers. Journal of Biomedical Optics 16: 095005.
10. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS, (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
11. Asparuhova MB, Gelman L, Chiquet M, (2009) Role of the actin cytoskeleton in tuning cellular responses to external mechanical stress. Scand J Med Sci Sports 19: 490-499.
12. Amano M, Nakayama M, Kaibuchi K, (2010) Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 67: 545-554.
13. Schweizer J, Bowden PE, Coulombe PA, Langbein L, Lane EB, et al. (2006) New consensus nomenclature for mammalian keratins. J Cell Biol 174: 169-174.
14. Pekny M, Lane EB, (2007) Intermediate filaments and stress. Exp Cell Res 313: 2244-2254.
15. Omary MB, Ku NO, (1997) Intermediate filament proteins of the liver: emerging disease association and functions. Hepatology 25: 1043-1048.
16. Oshima RG, Baribault H, Caulin C, (1996) Oncogenic regulation and function of keratins 8 and 18. Cancer Metastasis Rev 15: 445-471.
17. Coulombe PA, Wong P, (2004) Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat Cell Biol 6: 699-706.
18. Alam H, Kundu ST, Dalal SN, Vaidya MM, (2011) Loss of keratins 8 and 18 leads to alterations in alpha6beta4-integrin-mediated signalling and decreased neoplastic progression in an oral-tumour-derived cell line. J Cell Sci 124: 2096-2106.
19. Omary MB, Ku NO, Strnad P, Hanada S, (2009) Toward unraveling the complexity of simple epithelial keratins in human disease. J Clin Invest 119: 1794-1805.
20. Jung KS, Kim SU, Ahn SH, Park YN, Kim do Y, et al. (2011) Risk assessment of hepatitis B virus-related hepatocellular carcinoma development using liver stiffness measurement (FibroScan). Hepatology 53: 885-894.
21. Kuo YH, Lu SN, Hung CH, Kee KM, Chen CH, et al. (2010) Liver stiffness measurement in the risk assessment of hepatocellular carcinoma for patients with chronic hepatitis. Hepatol Int 4: 700-706.
22. Bordeleau F, Galarneau L, Gilbert S, Loranger A, Marceau N, (2010) Keratin 8/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells. Mol Biol Cell 21: 1698-1713.
23. Oshima RG, (2002) Apoptosis and keratin intermediate filaments. Cell Death Differ 9: 486-492.
24. Galarneau L, Loranger A, Gilbert S, Marceau N, (2007) Keratins modulate hepatic cell adhesion, size and G1/S transition. Exp Cell Res 313: 179-194.
25. Wang YL, Pelham RJ Jr, (1998) Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol 298: 489-496.
26. Bordeleau F, Bessard J, Sheng Y, Marceau N, (2008) Keratin contribution to cellular mechanical stress response at focal adhesions as assayed by laser tweezers. Biochem Cell Biol 86: 352-359.
27. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, et al. (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60: 24-34.
28. Barnes SL, Lyshchik A, Washington MK, Gore JC, Miga MI, (2007) Development of a mechanical testing assay for fibrotic murine liver. Med Phys 34: 4439-4450.
29. Chen EJ, Novakofski J, Jenkins WK, O'Brien WD Jr, (1996) Young's modulus measurements of soft tissues with application to elasticity imaging. Ultrasonics, Ferroelectrics and Frequency Control, IEEE Transactions on 43: 191-194.
30. Wang Y, Ganger DR, Levitsky J, Sternick LA, McCarthy RJ, et al. (2011) Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol 196: 553-561.
31. Kocgozlu L, Lavalle P, Koenig G, Senger B, Haikel Y, et al. (2010) Selective and uncoupled role of substrate elasticity in the regulation of replication and transcription in epithelial cells. J Cell Sci 123: 29-39.
32. Fung Y, (1993) Biomechanics: mechanical properties of living tissues: Springer-Verlag.
33. Jiang G, Giannone G, Critchley DR, Fukumoto E, Sheetz MP, (2003) Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424: 334-337.
34. Roca-Cusachs P, Gauthier NC, Del Rio A, Sheetz MP, (2009) Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc Natl Acad Sci U S A 106: 16245-16250.
35. Subramanian A, Lin HY, (2005) Crosslinked chitosan: its physical properties and the effects of matrix stiffness on chondrocyte cell morphology and proliferation. J Biomed Mater Res A 75: 742-753.
36. Wei WC, Lin HH, Shen MR, Tang MJ, (2008) Mechanosensing machinery for cells under low substratum rigidity. Am J Physiol Cell Physiol 295: C1579-1589.
37. Huynh J, Nishimura N, Rana K, Peloquin JM, Califano JP, et al. (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 3: 112ra122.
38. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA, (2007) Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93: 4453-4461.
39. Tee SY, Fu J, Chen CS, Janmey PA, (2011) Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100: L25-27.
40. Fereol S, Fodil R, Laurent VM, Balland M, Louis B, et al. (2009) Prestress and adhesion site dynamics control cell sensitivity to extracellular stiffness. Biophys J 96: 2009-2022.
41. Galbraith CG, Yamada KM, Sheetz MP, (2002) The relationship between force and focal complex development. J Cell Biol 159: 695-705.
42. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
43. Wu M, Wu ZF, Rosenthal DT, Rhee EM, Merajver SD, (2010) Characterization of the roles of RHOC and RHOA GTPases in invasion, motility, and matrix adhesion in inflammatory and aggressive breast cancers. Cancer 116: 2768-2782.
44. Pertz O, (2010) Spatio-temporal Rho GTPase signaling- where are we now? J Cell Sci 123: 1841-1850.
45. Katoh K, Kano Y, Amano M, Kaibuchi K, Fujiwara K, (2001) Stress fiber organization regulated by MLCK and Rho-kinase in cultured human fibroblasts. Am J Physiol Cell Physiol 280: C1669-1679.
46. Huveneers S, Danen EH, (2009) Adhesion signaling- crosstalk between integrins, Src and Rho. J Cell Sci 122: 1059-1069.
47. Brandt D, Gimona M, Hillmann M, Haller H, Mischak H, (2002) Protein kinase C induces actin reorganization via a Src- and Rho-dependent pathway. J Biol Chem 277: 20903-20910.
48. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, et al. (2008) PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 180: 187-203.
49. Marceau N, Loranger A, Gilbert S, Daigle N, Champetier S, (2001) Keratin-mediated resistance to stress and apoptosis in simple epithelial cells in relation to health and disease. Biochem Cell Biol 79: 543-555.
50. Steinbock FA, Wiche G, (1999) Plectin: a cytolinker by design. Biol Chem 380: 151-158.
51. Mamidipudi V, Zhang J, Lee KC, Cartwright CA, (2004) RACK1 regulates G1/S progression by suppressing Src kinase activity. Mol Cell Biol 24: 6788-6798.
52. Blouin R, Blouin MJ, Royal I, Grenier A, Roop DR, et al. (1992) Cytokeratin 14 expression in rat liver cells in culture and localization in vivo. Differentiation 52: 45-54.
53. Engvall E, Ruoslahti E, (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer 20: 1-5.
54. Robert A, Smadja-Lamere N, Landry MC, Champagne C, Petrie R, et al. (2006) Adenovirus E4orf4 hijacks rho GTPase-dependent actin dynamics to kill cells: a role for endosome-associated actin assembly. Mol Biol Cell 17: 3329-3344.
55. Lamarche N, Tapon N, Stowers L, Burbelo PD, Aspenstrom P, et al. (1996) Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87: 519-529.
56. Gilbert S, Loranger A, Daigle N, Marceau N, (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 154: 763-773.