Stretch-induced stress fiber remodeling and the activations of JNK and ERK depend on mechanical strain rate, but not FAK

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Hsu, Hui Ju ^a   Lee, Chin Fu ^a   Locke, Andrea ^a   Vanderzyl, Susan Q ^a   Kaunas, Roland ^a  

^a Texas A and M University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; CYTOCHALASIN D; FOCAL ADHESION KINASE; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; MITOGEN ACTIVATED PROTEIN KINASE P38;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL RETRACTION; CELL STRESS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; CYCLIC INDUCED STRESS FIBER ALIGNMENT; EMBRYO CELL; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FIBROBLAST; MECHANICAL STRESS; NONHUMAN; NULL ALLELE; OSTEOSARCOMA CELL; PROCEDURES CONCERNING CELLS; STRESS FIBER; VASCULAR ENDOTHELIUM; ANIMAL; BIOMECHANICS; CATTLE; CELL SHAPE; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION; TUMOR CELL LINE;

BOVINAE;

ACTINS; ANIMALS; BIOMECHANICS; CATTLE; CELL LINE, TUMOR; CELL SHAPE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; STRESS FIBERS; STRESS, MECHANICAL;

EID: 77957969256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012470     Document Type: Article

References (39)

1. Gavara N, Roca-Cusachs P, Sunyer R, Farre R, Navajas D (2008) Mapping cellmatrix stresses during stretch reveals inelastic reorganization of the cytoskeleton. Biophys J 95: 464-471.
2. Brown RA, Prajapati R, McGrouther DA, Yannas IV, Eastwood M (1998) Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J Cell Physiol 175: 323-332.
3. Lu L, Feng Y, Hucker WJ, Oswald SJ, Longmore GD, et al. (2008) Actin stress fiber pre-extension in human aortic endothelial cells. Cell Motil Cytoskeleton 65: 281-294.
4. Costa KD, Hucker WJ, Yin FC (2002) Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil Cytoskeleton 52: 266-274.
5. Nekouzadeh A, Pryse KM, Elson EL, Genin GM (2008) Stretch-activated force shedding, force recovery, and cytoskeletal remodeling in contractile fibroblasts. J Biomech 41: 2964-2971.
6. Jungbauer S, Gao H, Spatz JP, Kemkemer R (2008) Two Characteristic Regimes in Frequency Dependent Dynamic Reorientation of Fibroblasts on Cyclically Stretched Substrates. Biophys J 95: 3470-3478.
7. Hsu HJ, Lee CF, Kaunas R (2009) A dynamic stochastic model of frequencydependent stress fiber alignment induced by cyclic stretch. PLoS ONE 4: e4853.
8. De R, Zemel A, Safran SA (2007) Dynamics of Cell Orientation. Nature Physics 3: 655-659.
9. Kito H, Chen EL, Wang X, Ikeda M, Azuma N, et al. (2000) Role of mitogenactivated protein kinases in pulmonary endothelial cells exposed to cyclic strain. J Appl Physiol 89: 2391-2400.
10. Hoefen RJ, Berk BC (2002) The role of MAP kinases in endothelial activation. Vascul Pharmacol 38: 271-273.
11. Nerem RM, Levesque MJ, Cornhill JF (1981) Vascular endothelial morphology as an indicator of the pattern of blood flow. J Biomech Eng 103: 172-176.
12. Pradhan S, Sumpio B (2004) Molecular and biological effects of hemodynamics on vascular cells. Front Biosci 9: 3276-3285.
13. Kaunas R, Usami S, Chien S (2006) Regulation of stretch-induced JNK activation by stress fiber orientation. Cell Signal 18: 1924-1931.
14. Martineau LC, Gardiner PF (2001) Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91: 693-702.
15. Katsumi A, Naoe T, Matsushita T, Kaibuchi K, Schwartz MA (2005) Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J Biol Chem 280: 16546-16549.
16. Tilghman RW, Parsons JT (2008) Focal adhesion kinase as a regulator of cell tension in the progression of cancer. Semin Cancer Biol 18: 45-52.
17. Wang HB, Dembo M, Hanks SK, Wang Y (2001) Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci U S A 98: 11295-11300.
18. Naruse K, Yamada T, Sai XR, Hamaguchi M, Sokabe M (1998) Pp125FAK is required for stretch dependent morphological response of endothelial cells. Oncogene 17: 455-463.
19. Sai X, Naruse K, Sokabe M (1999) Activation of pp60(src) is critical for stretchinduced orienting response in fibroblasts. J Cell Sci 112 (Pt 9): 1365-1373.
20. Nadruz W, Jr., Corat MA, Marin TM, Guimaraes Pereira GA, Franchini KG (2005) Focal adhesion kinase mediates MEF2 and c-Jun activation by stretch: role in the activation of the cardiac hypertrophic genetic program. Cardiovasc Res 68: 87-97.
21. Aikawa R, Nagai T, Kudoh S, Zou Y, Tanaka M, et al. (2002) Integrins play a critical role in mechanical stress-induced p38 MAPK activation. Hypertension 39: 233-238.
22. Wang JG, Miyazu M, Matsushita E, Sokabe M, Naruse K (2001) Uniaxial cyclic stretch induces focal adhesion kinase (FAK) tyrosine phosphorylation followed by mitogen-activated protein kinase (MAPK) activation. Biochem Biophys Res Commun 288: 356-361.
23. Petzold T, Orr AW, Hahn C, Jhaveri KA, Parsons JT, et al. (2009) Focal adhesion kinase modulates activation of NF-kappaB by flow in endothelial cells. Am J Physiol Cell Physiol 297: C814-822.
24. Humphrey JD (2002) Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York: Springer-Verlag.
25. Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP, et al. (2006) Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90: 3762-3773.
26. Owen JD, Ruest PJ, Fry DW, Hanks SK (1999) Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol Cell Biol 19: 4806-4818.
27. Hayakawa K, Sato N, Obinata T (2001) Dynamic reorientation of cultured cells and stress fibers under mechanical stress from periodic stretching. Exp Cell Res 268: 104-114.
28. Qu MJ, Liu B, Wang HQ, Yan ZQ, Shen BR, et al. (2007) Frequencydependent phenotype modulation of vascular smooth muscle cells under cyclic mechanical strain. J Vasc Res 44: 345-353.
29. Hosokawa H, Aiuchi S, Kambe T, Hagiwara Y, Kubo T (2002) Mechanical stretch-induced mitogen-activated protein kinase activation is mediated via angiotensin and endothelin systems in vascular smooth muscle cells. Biol Pharm Bull 25: 1588-1592.
30. MacKenna DA, Dolfi F, Vuori K, Ruoslahti E (1998) Extracellular signalregulated kinase and c-Jun NH2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix-specific in rat cardiac fibroblasts. J Clin Invest 101: 301-310.
31. Trepat X, Deng L, An SS, Navajas D, Tschumperlin DJ, et al. (2007) Universal physical responses to stretch in the living cell. Nature 447: 592-595.
32. Sato K, Adachi T, Matsuo M, Tomita Y (2005) Quantitative evaluation of threshold fiber strain that induces reorganization of cytoskeletal actin fiber structure in osteoblastic cells. J Biomech 38: 1895-1901.
33. Shemesh T, Geiger B, Bershadsky AD, Kozlov MM (2005) Focal adhesions as mechanosensors: a physical mechanism. Proc Natl Acad Sci U S A 102: 12383-12388.
34. Goeckeler ZM, Bridgman PC, Wysolmerski RB (2008) Nonmuscle myosin II is responsible for maintaining endothelial cell basal tone and stress fiber integrity. Am J Physiol Cell Physiol 295: C994-1006.
35. Mofrad MR, Golji J, Abdul Rahim NA, Kamm RD (2004) Force-induced unfolding of the focal adhesion targeting domain and the influence of paxillin binding. Mech Chem Biosyst 1: 253-265.
36. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, et al. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAKdeficient mice. Nature 377: 539-544.
37. Schober M, Raghavan S, Nikolova M, Polak L, Pasolli HA, et al. (2007) Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol 176: 667-680.
38. Butcher DT, Alliston T, Weaver VM (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9: 108-122.
39. Deguchi S, Ohashi T, Sato M (2006) Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells. J Biomech 39: 2603-2610.