Substrate stiffness regulates PDGF-induced circular dorsal ruffle formation through MLCK

Cellular and Molecular Bioengineering

Volumn 6, Issue 2, 2013, Pages 138-147

  Huynh, John ^a   Bordeleau, Francois ^a   Kraning Rush, Casey M ^a   Reinhart King, Cynthia A ^a  

^a Cornell University   (United States)

Author keywords

Actin; Cell contractility; Cell migration; Traction force; Vascular smooth muscle cells

Indexed keywords

MYOSIN LIGHT CHAIN KINASE; PLATELET DERIVED GROWTH FACTOR;

ANIMAL CELL; ARTERIAL STIFFNESS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BIOMECHANICS; CELLULAR STRESS RESPONSE; CIRCULAR DORSAL RUFFLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; EXTRACELLULAR MATRIX; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE CONTRACTILITY; UPREGULATION; VASCULAR SMOOTH MUSCLE;

EID: 84879486664     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-013-0278-7     Document Type: Article

References (56)

1. Alexander, N. R., K. M. Branch, A. Parekh, E. S. Clark, I. C. Iwueke, S. A. Guelcher, and A. M. Weaver. Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18(17):1295-1299, 2008.
2. Amano, M., M. Nakayama, and K. Kaibuchi. Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 67(9):545-554, 2010.
3. Assoian, R. K., and E. A. Klein. Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 18(7):347-352, 2008.
4. Azimifar, S. B., R. T. Bottcher, S. Zanivan, C. Grashoff, M. Kruger, K. R. Legate, M. Mann, and R. Fassler. Induction of membrane circular dorsal ruffles requires co-signalling of integrin-ILK-complex and EGF receptor. J. Cell Sci. 125(Pt 2):435-448, 2012.
5. Ballestrem, C., B. Wehrle-Haller, and B. A. Imhof. Actin dynamics in living mammalian cells. J. Cell Sci. 111(Pt 12):1649-1658, 1998.
6. Barfod, E. T., A. L. Moore, B. G. Van de Graaf, and S. D. Lidofsky. Myosin light chain kinase and Src control membrane dynamics in volume recovery from cell swelling. Mol. Biol. Cell 22(5):634-650, 2011.
7. Beamish, J. A., P. He, K. Kottke-Marchant, and R. E. Marchant. Molecular regulation of contractile smooth muscle cell phenotype: implications for vascular tissue engineering. Tissue Eng. B 16(5):467-491, 2010.
8. Bordeleau, F., M.-E. Myrand Lapierre, Y. Sheng, and N. Marceau. Keratin 8/18 regulation of cell stiffness-extracellular matrix interplay through modulation of rho-mediated actin cytoskeleton dynamics. PLoS ONE 7(6):e38780, 2012.
9. Brown, X. Q., E. Bartolak-Suki, C. Williams, M. L. Walker, V. M. Weaver, and J. Y. Wong. Effect of substrate stiffness and PDGF on the behavior of vascular smooth muscle cells: implications for atherosclerosis. J. Cell. Physiol. 225(1):115-122, 2010.
10. Clark, K., M. Langeslag, C. G. Figdor, and F. N. van Leeuwen. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 17(4):178-186, 2007.
11. Daley, W. P., E. M. Gervais, S. W. Centanni, K. M. Gulfo, D. A. Nelson, and M. Larsen. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development 139(2):411-422, 2012.
12. Davis-Dusenbery, B. N., C. Wu, and A. Hata. Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler. Thromb. Vasc. Biol. 31(11):2370-2377, 2011.
13. Discher, D. E., P. Janmey, and Y. L. Wang. Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751):1139-1143, 2005.
14. Evanko, S. P., E. W. Raines, R. Ross, L. I. Gold, and T. N. Wight. Proteoglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-beta. Am. J. Pathol. 152(2):533-546, 1998.
15. Galbraith, C. G., K. M. Yamada, and M. P. Sheetz. The relationship between force and focal complex development. J. Cell Biol. 159(4):695-705, 2002.
16. Greenwald, S. E. Ageing of the conduit arteries. J. Pathol. 211(2):157-172, 2007.
17. Gu, Z., E. H. Noss, V. W. Hsu, and M. B. Brenner. Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J. Cell Biol. 193(1):61-70, 2011.
18. Huang, S., and D. E. Ingber. Cell tension, matrix mechanics, and cancer development. Cancer Cell 8(3):175-176, 2005.
19. Huang, M., L. Satchell, J. B. Duhadaway, G. C. Prendergast, and L. D. Laury-Kleintop. RhoB links PDGF signaling to cell migration by coordinating activation and localization of Cdc42 and Rac. J. Cell. Biochem. 112(6):1572-1584, 2011.
20. Huveneers, S., and E. H. Danen. Adhesion signaling - crosstalk between integrins, Src and Rho. J. Cell Sci. 122(Pt 8):1059-1069, 2009.
21. Huynh, J., N. Nishimura, K. Rana, J. M. Peloquin, J. P. Califano, C. R. Montague, M. R. King, C. B. Schaffer, and C. A. Reinhart-King. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci. Transl. Med. 3(112):112ra122, 2011.
22. Isenberg, B. C., P. A. Dimilla, M. Walker, S. Kim, and J. Y. Wong. Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97(5):1313-1322, 2009.
23. King, S. J., D. C. Worth, T. M. Scales, J. Monypenny, G. E. Jones, and M. Parsons. Beta1 integrins regulate fibroblast chemotaxis through control of N-WASP stability. EMBO J. 30(9):1705-1718, 2011.
24. Krishnan, R., D. D. Klumpers, C. Y. Park, K. Rajendran, X. Trepat, J. van Bezu, V. W. van Hinsbergh, C. V. Carman, J. D. Brain, J. J. Fredberg, J. P. Butler, and G. P. van Nieuw Amerongen. Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am. J. Physiol. Cell Physiol. 300(1):C146-C154, 2011.
25. Krueger, E. W., J. D. Orth, H. Cao, and M. A. McNiven. A dynamin-cortactin-Arp2/3 complex mediates actin reorganization in growth factor-stimulated cells. Mol. Biol. Cell 14(3):1085-1096, 2003.
26. Kumar, S., and V. M. Weaver. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28(1-2):113-127, 2009.
27. Linder, S., C. Wiesner, and M. Himmel. Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27:185-211, 2011.
28. Lusis, A. J. Atherosclerosis. Nature 407(6801):233-241, 2000.
29. Matsumoto, T., H. Abe, T. Ohashi, Y. Kato, and M. Sato. Local elastic modulus of atherosclerotic lesions of rabbit thoracic aortas measured by pipette aspiration method. Physiol. Meas. 23(4):635-648, 2002.
30. Mattace-Raso, F. U., T. J. van der Cammen, A. Hofman, N. M. van Popele, M. L. Bos, M. A. Schalekamp, R. Asmar, R. S. Reneman, A. P. Hoeks, M. M. Breteler, and J. C. Witteman. Arterial stiffness and risk of coronary heart disease and stroke: the Rotterdam Study. Circulation 113(5):657-663, 2006.
31. McDaniel, D. P., G. A. Shaw, J. T. Elliott, K. Bhadriraju, C. Meuse, K. H. Chung, and A. L. Plant. The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype. Biophys. J. 92(5):1759-1769, 2007.
32. Murphy, D. A., and S. A. Courtneidge. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12(7):413-426, 2011.
33. Na, S., O. Collin, F. Chowdhury, B. Tay, M. Ouyang, Y. Wang, and N. Wang. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl. Acad. Sci. U.S.A. 105(18):6626-6631, 2008.
34. Owens, G. K., M. S. Kumar, and B. R. Wamhoff. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84(3):767-801, 2004.
35. Paszek, M. J., N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, and V. M. Weaver. Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241-254, 2005.
36. Peloquin, J., J. Huynh, R. M. Williams, and C. A. Reinhart-King. Indentation measurements of the subendothelial matrix in bovine carotid arteries. J. Biomech. 44(5):815-821, 2011.
37. Peyton, S. R., and A. J. Putnam. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell. Physiol. 204(1):198-209, 2005.
38. Poch, G., and S. N. Pancheva. Calculating slope and ED50 of additive dose-response curves, and application of these tabulated parameter values. J. Pharmacol. Toxicol. Methods 33(3):137-145, 1995.
39. Poincloux, R., F. Lizarraga, and P. Chavrier. Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122(Pt 17):3015-3024, 2009.
40. Raines, E. W. PDGF and cardiovascular disease. Cytokine Growth Factor Rev. 15(4):237-254, 2004.
41. Raines, E. W., H. Koyama, and N. O. Carragher. The extracellular matrix dynamically regulates smooth muscle cell responsiveness to PDGF. Ann. N. Y. Acad. Sci. 902:39-51, 2000; discussion 51-32.
42. Ridley, A. J. Life at the leading edge. Cell 145(7):1012-1022, 2011.
43. Ross, R. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340(2):115-126, 1999.
44. Ross, R., J. Masuda, E. W. Raines, A. M. Gown, S. Katsuda, M. Sasahara, L. T. Malden, H. Masuko, and H. Sato. Localization of PDGF-B protein in macrophages in all phases of atherogenesis. Science 248(4958):1009-1012, 1990.
45. Sero, J. E., C. K. Thodeti, A. Mammoto, C. Bakal, S. Thomas, and D. E. Ingber. Paxillin mediates sensing of physical cues and regulates directional cell motility by controlling lamellipodia positioning. PLoS ONE 6(12):e28303, 2011.
46. Stroka, K. M., and H. Aranda-Espinoza. Endothelial cell substrate stiffness influences neutrophil transmigration via myosin light chain kinase-dependent cell contraction. Blood 118(6):1632-1640, 2011.
47. Sun, C., M. H. Wu, and S. Y. Yuan. Nonmuscle myosin light-chain kinase deficiency attenuates atherosclerosis in apolipoprotein E-deficient mice via reduced endothelial barrier dysfunction and monocyte migration. Circulation 124(1):48-57, 2011.
48. Sutton-Tyrrell, K., S. S. Najjar, R. M. Boudreau, L. Venkitachalam, V. Kupelian, E. M. Simonsick, R. Havlik, E. G. Lakatta, H. Spurgeon, S. Kritchevsky, M. Pahor, D. Bauer, and A. Newman. Elevated aortic pulse wave velocity, a marker of arterial stiffness, predicts cardiovascular events in well-functioning older adults. Circulation 111(25):3384-3390, 2005.
49. Totsukawa, G., Y. Yamakita, S. Yamashiro, D. J. Hartshorne, Y. Sasaki, and F. Matsumura. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150(4):797-806, 2000.
50. Wang, Y., E. L. Botvinick, Y. Zhao, M. W. Berns, S. Usami, R. Y. Tsien, and S. Chien. Visualizing the mechanical activation of Src. Nature 434(7036):1040-1045, 2005.
51. Wang, Y., X. R. Zheng, N. Riddick, M. Bryden, W. Baur, X. Zhang, and H. K. Surks. ROCK isoform regulation of myosin phosphatase and contractility in vascular smooth muscle cells. Circ. Res. 104(4):531-540, 2009.
52. Webb, D. J., K. Donais, L. A. Whitmore, S. M. Thomas, C. E. Turner, J. T. Parsons, and A. F. Horwitz. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6(2):154-161, 2004.
53. Wei, W. C., H. H. Lin, M. R. Shen, and M. J. Tang. Mechanosensing machinery for cells under low substratum rigidity. Am. J. Physiol. Cell Physiol. 295(6):C1579-C1589, 2008.
54. Wolf, K., and P. Friedl. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21(12):736-744, 2011.
55. Zeng, Y., T. Lai, C. G. Koh, P. R. LeDuc, and K. H. Chiam. Investigating circular dorsal ruffles through varying substrate stiffness and mathematical modeling. Biophys. J. 101(9):2122-2130, 2011.
56. Zieman, S. J., V. Melenovsky, L. Clattenburg, M. C. Corretti, A. Capriotti, G. Gerstenblith, and D. A. Kass. Advanced glycation endproduct crosslink breaker (alagebrium) improves endothelial function in patients with isolated systolic hypertension. J. Hypertens. 25(3):577-583, 2007.