Mechanosensitive mechanisms in transcriptional regulation

Journal of Cell Science

Volumn 125, Issue 13, 2012, Pages 3061-3073

  Mammoto, Akiko ^a   Mammoto, Tadanori ^a   Ingber, Donald E ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Cell shape; Cytoskeleton; Embryos; Growth; Mechanical force; Nucleus; Pattern formation; Prestress; Stem cells; Transcription

Indexed keywords

FILAMIN A; FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 4; LAMININ; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOCYTE ENHANCER FACTOR 2; MYOSIN II; OCTAMER TRANSCRIPTION FACTOR 4; RHO FACTOR; STAT5 PROTEIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR SOX2; VANILLOID RECEPTOR 4; VASCULOTROPIN C;

ACTIN FILAMENT; ANGIOGENESIS; BONE DEVELOPMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL FATE; CELL GROWTH; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRESS; CONGESTIVE CARDIOMYOPATHY; CYTOSKELETON; DISEASE COURSE; DOWN REGULATION; DROSOPHILA; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMERY DREIFUSS MUSCULAR DYSTROPHY; EXTRACELLULAR MATRIX; FAMILIAL PARTIAL LIPODYSTROPHY; FIBROBLAST; GASTROINTESTINAL SYMPTOM; GASTRULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART DEVELOPMENT; HEART VENTRICLE HYPERTROPHY; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HOMEOSTASIS; HUMAN; INNER CELL MASS; LIPID RAFT; LIPODYSTROPHY; LUNG DEVELOPMENT; MALIGNANT LENTIGO; MECHANOTRANSDUCTION; MORPHOGENESIS; MUSCLE DEVELOPMENT; MUSCULOSKELETAL SYSTEM; NONHUMAN; NOTE; NUCLEAR REPROGRAMMING; ORGANOGENESIS; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGENERATIVE MEDICINE; STRETCHING; TISSUE ENGINEERING; TRANSCRIPTION REGULATION;

ANIMALS; BIOMECHANICS; BODY PATTERNING; CELL ADHESION MOLECULES; CELL SHAPE; EMBRYONIC DEVELOPMENT; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MECHANOTRANSDUCTION, CELLULAR; ORGANOGENESIS; STRESS, MECHANICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84868111953     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.093005     Document Type: Note

References (189)

1. Aarnes, G. T., Steen, H., Ludvigsen, P., Kristiansen, L. P. and Reikerås, O. (2002). High frequency distraction improves tissue adaptation during leg lengthening in humans. J. Orthop. Res. 20, 789-792.
2. Adamo, L., Naveiras, O., Wenzel, P. L., McKinney-Freeman, S., Mack, P. J., Gracia-Sancho, J., Suchy-Dicey, A., Yoshimoto, M., Lensch, M. W., Yoder, M. C. et al. (2009). Biomechanical forces promote embryonic haematopoiesis. Nature 459, 1131-1135.
3. Agarwal, S., Deschner, J., Long, P., Verma, A., Hofman, C., Evans, C. H. and Piesco, N. (2004). Role of NF-kappaB transcription factors in antiinflammatory and proinflammatory actions of mechanical signals. Arthritis Rheum. 50, 3541-3548.
4. Ahmad, M., Theofanidis, P. and Medford, R. M. (1998). Role of activating protein-1 in the regulation of the vascular cell adhesion molecule-1 gene expression by tumor necrosis factor-alpha. J. Biol. Chem. 273, 4616-4621.
5. Alenghat, F. J., Tytell, J. D., Thodeti, C. K., Derrien, A. and Ingber, D. E. (2009). Mechanical control of cAMP signaling through integrins is mediated by the heterotrimeric Galphas protein. J. Cell. Biochem. 106, 529-538.
6. Allport, V. C., Slater, D. M., Newton, R. and Bennett, P. R. (2000). NF-kappaB and AP-1 are required for cyclo-oxygenase 2 gene expression in amnion epithelial cell line (WISH). Mol. Hum. Reprod. 6, 561-565.
7. Almendro, N., Bellón, T., Rius, C., Lastres, P., Langa, C., Corbí, A. and Bernabéu, C. (1996). Cloning of the human platelet endothelial cell adhesion molecule-1 promoter and its tissue-specific expression. Structural and functional characterization. J. Immunol. 157, 5411-5421.
8. Assoian, R. K. and Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 18, 347-352.
9. Badri, K. R., Zhou, Y. and Schuger, L. (2008). Embryological origin of airway smooth muscle. Proc. Am. Thorac. Soc. 5, 4-10.
10. Balligand, J. L., Feron, O. and Dessy, C. (2009). eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol. Rev. 89, 481-534.
11. Bartman, T., Walsh, E. C., Wen, K. K., McKane, M., Ren, J., Alexander, J., Rubenstein, P. A. and Stainier, D. Y. (2004). Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol. 2, E129.
12. Bergmann, P., Body, J. J., Boonen, S., Boutsen, Y., Devogelaer, J. P., Goemaere, S., Kaufman, J., Reginster, J. Y. and Rozenberg, S. (2010). Loading and skeletal development and maintenance. J. Osteoporos. 2011, 786752.
13. Bishop, J. E. and Lindahl, G. (1999). Regulation of cardiovascular collagen synthesis by mechanical load. Cardiovasc. Res. 42, 27-44.
14. Boutahar, N., Guignandon, A., Vico, L. and Lafage-Proust, M. H. (2004). Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J. Biol. Chem. 279, 30588-30599.
15. Bruneau, B. G. (2002). Transcriptional regulation of vertebrate cardiac morphogenesis. Circ. Res. 90, 509-519.
16. Buxboim, A., Ivanovska, I. L. and Discher, D. E. (2010). Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? J. Cell Sci. 123, 297-308.
17. Cattaruzza, M., Eberhardt, I. and Hecker, M. (2001). Mechanosensitive transcription factors involved in endothelin B receptor expression. J. Biol. Chem. 276, 36999-37003.
18. Chan, M. W., Arora, P. D., Bozavikov, P. and McCulloch, C. A. (2009). FAK, PIP5KIgamma and gelsolin cooperatively mediate force-induced expression of alpha-smooth muscle actin. J. Cell Sci. 122, 2769-2781.
19. Chaqour, B. and Goppelt-Struebe, M. (2006). Mechanical regulation of the Cyr61/ CCN1 and CTGF/CCN2 proteins. FEBS J. 273, 3639-3649.
20. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1997). Geometric control of cell life and death. Science 276, 1425-1428.
21. Chowdhury, F., Na, S., Li, D., Poh, Y. C., Tanaka, T. S., Wang, F. and Wang, N. (2010). Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 9, 82-88.
22. Costa, R. H., Kalinichenko, V. V. and Lim, L. (2001). Transcription factors in mouse lung development and function. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L823-L838.
23. Culver, J. C. and Dickinson, M. E. (2010). The effects of hemodynamic force on embryonic development. Microcirculation 17, 164-178.
24. D'Addario, M., Arora, P. D., Ellen, R. P. and McCulloch, C. A. (2002). Interaction of p38 and Sp1 in a mechanical force-induced, beta 1 integrin-mediated transcriptional circuit that regulates the actin-binding protein filamin-A. J. Biol. Chem. 277, 47541-47550.
25. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
26. Davis, M. E., Grumbach, I. M., Fukai, T., Cutchins, A. and Harrison, D. G. (2004). Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor kappaB binding. J. Biol. Chem. 279, 163-168.
27. Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H., Wieschaus, E. F. (2005). Folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178.
28. Descot, A., Rex-Haffner, M., Courtois, G., Bluteau, D., Menssen, A., Mercher, T., Bernard, O. A., Treisman, R. and Posern, G. (2008). OTT-MAL is a deregulated activator of serum response factor-dependent gene expression. Mol. Cell. Biol. 28, 6171-6181.
29. Desprat, N., Supatto, W., Pouille, P. A., Beaurepaire, E. and Farge, E. (2008). Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev. Cell 15, 470-477.
30. Dick, F. A. and Mymryk, J. S. (2011). Sweet DREAMs for Hippo. Genes Dev. 25, 889-894.
31. Dike, L. E., Chen, C. S., Mrksich, M., Tien, J., Whitesides, G. M. and Ingber, D. E. (1999). Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell. Dev. Biol. Anim. 35, 441-448.
32. Dolmetsch, R. E., Pajvani, U., Fife, K., Spotts, J. M. and Greenberg, M. E. (2001). Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294, 333-339.
33. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S. A., Gayyed, M. F., Anders, R. A., Maitra, A. and Pan, D. (2007). Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133.
34. Dreuillet, C., Tillit, J., Kress, M. and Ernoult-Lange, M. (2002). In vivo and in vitro interaction between human transcription factor MOK2 and nuclear lamin A/C. Nucleic Acids Res. 30, 4634-4642.
35. Engler, A. J., Griffin, M. A., Sen, S., Bönnemann, C. G., Sweeney, H. L. and Discher, D. E. (2004). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887.
36. Engler, A. J., Sen, S., Sweeney, H. L. and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
37. Ezzell, R. M., Goldmann, W. H., Wang, N., Parashurama, N. and Ingber, D. E. (1997). Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231, 14-26.
38. Farge, E. (2003). Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr. Biol. 13, 1365-1377.
39. Farge, E. (2011). Mechanotransduction in development. Curr. Top. Dev. Biol. 95, 243-265.
40. Fernandez-Gonzalez, R., Simoes, S. M., Röper, J. C., Eaton, S. and Zallen, J. A. (2009). Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736-743.
41. Foker, J. E., Linden, B. C., Boyle, E. M., Jr and Marquardt, C. (1997). Development of a true primary repair for the full spectrum of esophageal atresia. Ann. Surg. 226, 533-541.
42. Friday, B. B., Horsley, V. and Pavlath, G. K. (2000). Calcineurin activity is required for the initiation of skeletal muscle differentiation. J. Cell Biol. 149, 657-666.
43. Friday, B. B., Mitchell, P. O., Kegley, K. M. and Pavlath, G. K. (2003). Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD. Differentiation 71, 217-227.
44. Gayer, C. P. and Basson, M. D. (2009). The effects of mechanical forces on intestinal physiology and pathology. Cell. Signal. 21, 1237-1244.
45. Gimbrone, M. A., Jr, Topper, J. N., Nagel, T., Anderson, K. R. and Garcia-Cardeña, G. (2000). Endothelial dysfunction, hemodynamic forces, and atherogen-esis. Ann. N. Y. Acad. Sci. 902, 230-240.
46. Groenendijk, B. C., Van der Heiden, K., Hierck, B. P. and Poelmann, R. E. (2007). The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model. Physiology (Bethesda) 22, 380-389.
47. Grummt, I. (2006). Actin and myosin as transcription factors. Curr. Opin. Genet. Dev. 16, 191-196.
48. Gutierrez, J. A., Ertsey, R., Scavo, L. M., Collins, E. and Dobbs, L. G. (1999). Mechanical distention modulates alveolar epithelial cell phenotypic expression by transcriptional regulation. Am. J. Respir. Cell Mol. Biol. 21, 223-229.
49. Haraguchi, T., Holaska, J. M., Yamane, M., Koujin, T., Hashiguchi, N., Mori, C., Wilson, K. L. and Hiraoka, Y. (2004). Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 271, 1035-1045.
50. Harding, R. and Hooper, S. B. (1996). Regulation of lung expansion and lung growth before birth. J. Appl. Physiol. 81, 209-224.
51. Harding, R., Bocking, A. D. and Sigger, J. N. (1986). Influence of upper respiratory tract on liquid flow to and from fetal lungs. J. Appl. Physiol. 61, 68-74.
52. Hautala, N., Tokola, H., Luodonpää, M., Puhakka, J., Romppanen, H., Vuolteenaho, O. and Ruskoaho, H. (2001). Pressure overload increases GATA4 binding activity via endothelin-1. Circulation 103, 730-735.
53. Hautala, N., Tenhunen, O., Szokodi, I. and Ruskoaho, H. (2002). Direct left ventricular wall stretch activates GATA4 binding in perfused rat heart: involvement of autocrine/paracrine pathways. Pflugers Arch. 443, 362-369.
54. Hemsley, A. L., Hernandez, D., Mason, C., Pelling, A. E. and Veraitch, F. S. (2011). Precisely delivered nanomechanical force induce blebbing in undifferentiated mouse embryonic stem cells. Cell Health and Cytoskeleton 3, 23-34.
55. Hirokawa, M., Miura, S., Kishikawa, H., Yoshida, H., Nakamizo, H., Higuchi, H., Nakatsumi, R. C., Suzuki, H., Saito, H. and Ishii, H. (2001). Loading of mechanical pressure activates mitogen-activated protein kinase and early immediate gene in intestinal epithelial cells. Dig. Dis. Sci. 46, 1993-2003.
56. Hong, S. Y., Jeon, Y. M., Lee, H. J., Kim, J. G., Baek, J. A. and Lee, J. C. (2010). Activation of RhoA and FAK induces ERK-mediated osteopontin expression in mechanical force-subjected periodontal ligament fibroblasts. Mol. Cell. Biochem. 335, 263-272.
57. Hooper, S. B. and Wallace, M. J. (2006). Role of the physicochemical environment in lung development. Clin. Exp. Pharmacol. Physiol. 33, 273-279.
58. Hove, J. R., Köster, R. W., Forouhar, A. S., Acevedo-Bolton, G., Fraser, S. E. and Gharib, M. (2003). Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421, 172-177.
59. Huang, C. and Ogawa, R. (2010). Mechanotransduction in bone repair and regeneration. FASEB J. 24, 3625-3632.
60. Huang, S. and Ingber, D. E. (2002). A discrete cell cycle checkpoint in late G(1) that is cytoskeleton-dependent and MAP kinase (Erk)-independent. Exp. Cell Res. 275, 255-264.
61. Huang, Y., Jia, X., Bai, K., Gong, X. and Fan, Y. (2010). Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch. Med. Res. 41, 497-505.
62. Hufnagel, L., Teleman, A. A., Rouault, H., Cohen, S. M. and Shraiman, B. I. (2007). On the mechanism of wing size determination in fly development. Proc. Natl. Acad. Sci. USA 104, 3835-3840.
63. Ilizarov, G. A. (1989a). The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin. Orthop. Relat. Res. (239), 263-285.
64. Ilizarov, G. A. (1989b). The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin. Orthop. Relat. Res. (238), 249-281.
65. Inanlou, M. R., Baguma-Nibasheka, M. and Kablar, B. (2005). The role of fetal breathing-like movements in lung organogenesis. Histol. Histopathol. 20, 1261-1266.
66. Ingber, D. E. (1993). Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104, 613-627.
67. Ingber, D. E. (2003). Mechanosensation through integrins: cells act locally but think globally. Proc. Natl. Acad. Sci. USA 100, 1472-1474.
68. Ingber, D. E. (2006). Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811-827.
69. Ishida, T., Peterson, T. E., Kovach, N. L. and Berk, B. C. (1996). MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ. Res. 79, 310-316.
70. Itano, N., Okamoto, S., Zhang, D., Lipton, S. A. and Ruoslahti, E. (2003). Cell spreading controls endoplasmic and nuclear calcium: a physical gene regulation pathway from the cell surface to the nucleus. Proc. Natl. Acad. Sci. USA 100, 5181-5186.
71. Jeon, Y. M., Kook, S. H., Son, Y. O., Kim, E. M., Park, S. S., Kim, J. G. and Lee, J. C. (2009). Role of MAPK in mechanical force-induced up-regulation of type I collagen and osteopontin in human gingival fibroblasts. Mol. Cell. Biochem. 320, 45-52.
72. Kahn, J., Shwartz, Y., Blitz, E., Krief, S., Sharir, A., Breitel, D. A., Rattenbach, R., Relaix, F., Maire, P., Rountree, R. B. et al. (2009). Muscle contraction is necessary to maintain joint progenitor cell fate. Dev. Cell 16, 734-743.
73. Kanno, T., Takahashi, T., Tsujisawa, T., Ariyoshi, W. and Nishihara, T. (2007). Mechanical stress-mediated Runx2 activation is dependent on Ras/ERK1/2 MAPK signaling in osteoblasts. J. Cell. Biochem. 101, 1266-1277.
74. Khachigian, L. M., Resnick, N., Gimbrone, M. A., Jr and Collins, T. (1995). Nuclear factor-kappa B interacts functionally with the platelet-derived growth factor B-chain shear-stress response element in vascular endothelial cells exposed to fluid shear stress. J. Clin. Invest. 96, 1169-1175.
75. Khatau, S. B., Kim, D. H., Hale, C. M., Bloom, R. J. and Wirtz, D. (2010). The perinuclear actin cap in health and disease. Nucleus 1, 337-342.
76. Kihara, T., Haghparast, S. M., Shimizu, Y., Yuba, S. and Miyake, J. (2011). Physical properties of mesenchymal stem cells are coordinated by the perinuclear actin cap. Biochem. Biophys. Res. Commun. 409, 1-6.
77. Kim, J. B., Sebastiano, V., Wu, G., Araúzo-Bravo, M. J., Sasse, P., Gentile, L., Ko, K., Ruau, D., Ehrich, M., van den Boom, D. et al. (2009). Oct4-induced pluripotency in adult neural stem cells. Cell 136, 411-419.
78. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M. J., Ji, H., Ehrlich, L. I. et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
79. Kishikawa, H., Miura, S., Yoshida, H., Hirokawa, M., Nakamizo, H., Higuchi, H., Adachi, M., Nakatsumi, R. C., Suzuki, H., Saito, H. et al. (2002). Transmural pressure induces IL-6 secretion by intestinal epithelial cells. Clin. Exp. Immunol. 129, 86-91.
80. Klein, E. A., Yung, Y., Castagnino, P., Kothapalli, D. and Assoian, R. K. (2007). Cell adhesion, cellular tension, and cell cycle control. Methods Enzymol. 426, 155-175.
81. Kölsch, V., Seher, T., Fernandez-Ballester, G. J., Serrano, L. and Leptin, M. (2007). Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315, 384-386.
82. Komuro, I., Katoh, Y., Kaida, T., Shibazaki, Y., Kurabayashi, M., Hoh, E., Takaku, F. and Yazaki, Y. (1991). Mechanical loading stimulates cell hypertrophy and specific gene expression in cultured rat cardiac myocytes. Possible role of protein kinase C activation. J. Biol. Chem. 266, 1265-1268.
83. Kook, S. H., Hwang, J. M., Park, J. S., Kim, E. M., Heo, J. S., Jeon, Y. M. and Lee, J. C. (2009). Mechanical force induces type I collagen expression in human periodontal ligament fibroblasts through activation of ERK/JNK and AP-1. J. Cell. Biochem. 106, 1060-1067.
84. Kumar, A., Lnu, S., Malya, R., Barron, D., Moore, J., Corry, D. B. and Boriek, A. M. (2003). Mechanical stretch activates nuclear factor-kappaB, activator protein-1, and mitogen-activated protein kinases in lung parenchyma: implications in asthma. FASEB J. 17, 1800-1811.
85. Landsberg, K. P., Farhadifar, R., Ranft, J., Umetsu, D., Widmann, T. J., Bittig, T., Said, A., Jülicher, F. and Dahmann, C. (2009). Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 19, 1950-1955.
86. Lanyon, L. E. (1992). Control of bone architecture by functional load bearing. J. Bone Miner. Res. 7 Suppl. 2, S369-S375.
87. Lee, J. S., Yu, Q., Shin, J. T., Sebzda, E., Bertozzi, C., Chen, M., Mericko, P., Stadtfeld, M., Zhou, D., Cheng, L. et al. (2006). Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev. Cell 11, 845-857.
88. Lele, T. P., Pendse, J., Kumar, S., Salanga, M., Karavitis, J. and Ingber, D. E. (2006). Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J. Cell. Physiol. 207, 187-194.
89. Li, D., Zhou, J., Wang, L., Shin, M. E., Su, P., Lei, X., Kuang, H., Guo, W., Yang, H., Cheng, L. et al. (2010). Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. J. Cell Biol. 191, 631-644.
90. Li, J., Chen, G., Zheng, L., Luo, S. and Zhao, Z. (2007). Osteoblast cytoskeletal modulation in response to compressive stress at physiological levels. Mol. Cell. Biochem. 304, 45-52.
91. Lichtinger, M., Hoogenkamp, M., Krysinska, H., Ingram, R. and Bonifer, C. (2010). Chromatin regulation by RUNX1. Blood Cells Mol. Dis. 44, 287-290.
92. Londhe, V. A., Nguyen, H. T., Jeng, J. M., Li, X., Li, C., Tiozzo, C., Zhu, N. and Minoo, P. (2008). NF-kB induces lung maturation during mouse lung morphogenesis. Dev. Dyn. 237, 328-338.
93. Mack, C. P. and Owens, G. K. (1999). Regulation of smooth muscle alpha-actin expression in vivo is dependent on CArG elements within the 59 and first intron promoter regions. Circ. Res. 84, 852-861.
94. Mammoto, A. and Ingber, D. E. (2009). Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 21, 864-870.
95. Mammoto, A., Huang, S., Moore, K., Oh, P. and Ingber, D. E. (2004). Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J. Biol. Chem. 279, 26323-26330.
96. Mammoto, A., Huang, S. and Ingber, D. E. (2007). Filamin links cell shape and cytoskeletal structure to Rho regulation by controlling accumulation of p190RhoGAP in lipid rafts. J. Cell Sci. 120, 456-467.
97. Mammoto, A., Mammoto, T. and Ingber, D. E. (2008). Rho signaling and mechanical control of vascular development. Curr. Opin. Hematol. 15, 228-234.
98. Mammoto, A., Connor, K. M., Mammoto, T., Yung, C. W., Huh, D., Aderman, C. M., Mostoslavsky, G., Smith, L. E. and Ingber, D. E. (2009). A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457, 1103-1108.
99. Mammoto, T. and Ingber, D. E. (2010). Mechanical control of tissue and organ development. Development 137, 1407-1420.
100. Mammoto, T., Mammoto, A., Torisawa, Y. S., Tat, T., Gibbs, A., Derda, R., Mannix, R., de Bruijn, M., Yung, C. W., Huh, D. et al. (2011). Mechanochemical control of mesenchymal condensation and embryonic tooth organ formation. Dev. Cell 21, 758-769.
101. Maniotis, A. J., Bojanowski, K. and Ingber, D. E. (1997a). Mechanical continuity and reversible chromosome disassembly within intact genomes removed from living cells. J. Cell. Biochem. 65, 114-130.
102. Maniotis, A. J., Chen, C. S. and Ingber, D. E. (1997b). Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA 94, 849-854.
103. Martin, A. C., Kaschube, M. and Wieschaus, E. F. (2009). Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499.
104. Martin, T., Cardarelli, P. M., Parry, G. C., Felts, K. A. and Cobb, R. R. (1997). Cytokine induction of monocyte chemoattractant protein-1 gene expression in human endothelial cells depends on the cooperative action of NF-kappa B and AP-1. Eur. J. Immunol. 27, 1091-1097.
105. Martinac, B. (2004). Mechanosensitive ion channels: molecules of mechanotransduc-tion. J. Cell Sci. 117, 2449-2460.
106. Marttila, M., Hautala, N., Paradis, P., Toth, M., Vuolteenaho, O., Nemer, M. and Ruskoaho, H. (2001). GATA4 mediates activation of the B-type natriuretic peptide gene expression in response to hemodynamic stress. Endocrinology 142, 4693-4700.
107. Matthews, B. D., Thodeti, C. K., Tytell, J. D., Mammoto, A., Overby, D. R. and Ingber, D. E. (2010). Ultra-rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface beta1 integrins. Integr. Biol. (Camb) 2, 435-442.
108. Mazumder, A. and Shivashankar, G. V. (2007). Gold-nanoparticle-assisted laser perturbation of chromatin assembly reveals unusual aspects of nuclear architecture within living cells. Biophys. J. 93, 2209-2216.
109. Mazumder, A. and Shivashankar, G. V. (2010). Emergence of a prestressed eukaryotic nucleus during cellular differentiation and development. J. R. Soc. Interface 7 Suppl. 3, S321-S330.
110. Mazumder, A., Roopa, T., Basu, A., Mahadevan, L. and Shivashankar, G. V. (2008). Dynamics of chromatin decondensation reveals the structural integrity of a mechanically prestressed nucleus. Biophys. J. 95, 3028-3035.
111. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495.
112. McCain, M. L. and Parker, K. K. (2011). Mechanotransduction: the role of mechanical stress, myocyte shape, and cytoskeletal architecture on cardiac function. Pflugers Arch. 462, 89-104.
113. McGee, K. M., Vartiainen, M. K., Khaw, P. T., Treisman, R. and Bailly, M. (2011). Nuclear transport of the serum response factor coactivator MRTF-A is downregulated at tensional homeostasis. EMBO Rep. 12, 963-970.
114. Medvinsky, A. and Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906.
115. Meiler, S. E., Hung, R. R., Gerszten, R. E., Gianetti, J., Li, L., Matsui, T., Gimbrone, M. A., Jr, and Rosenzweig, A. (2002). Endothelial IKK beta signaling is required for monocyte adhesion under laminar flow conditions. J. Mol. Cell. Cardiol. 34, 349-359.
116. Méjat, A. and Misteli, T. (2010). LINC complexes in health and disease. Nucleus 1, 40-52.
117. Mendelson, C. R. (2000). Role of transcription factors in fetal lung development and surfactant protein gene expression. Annu. Rev. Physiol. 62, 875-915.
118. Minoo, P. (2000). Transcriptional regulation of lung development: emergence of specificity. Respir. Res. 1, 109-115.
119. Miyamoto, K., Pasque, V., Jullien, J. and Gurdon, J. B. (2011). Nuclear actin polymerization is required for transcriptional reprogramming of Oct4 by oocytes. Genes Dev. 25, 946-958.
120. Monier, B., Pelissier-Monier, A., Brand, A. H. and Sanson, B. (2010). An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nat. Cell Biol. 12, 60-65; Suppl. 1-9.
121. Moore, K. A., Huang, S., Kong, Y., Sunday, M. E. and Ingber, D. E. (2002). Control of embryonic lung branching morphogenesis by the Rho activator, cytotoxic necrotizing factor 1. J. Surg. Res. 104, 95-100.
122. Moore, K. A., Polte, T., Huang, S., Shi, B., Alsberg, E., Sunday, M. E. and Ingber, D. E. (2005). Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev. Dyn. 232, 268-281.
123. Morawietz, H., Ma, Y. H., Vives, F., Wilson, E., Sukhatme, V. P., Holtz, J. and Ives, H. E. (1999). Rapid induction and translocation of Egr-1 in response to mechanical strain in vascular smooth muscle cells. Circ. Res. 84, 678-687.
124. Morita, T., Mayanagi, T. and Sobue, K. (2007). Reorganization of the actin cytoskeleton via transcriptional regulation of cytoskeletal/focal adhesion genes by myocardin-related transcription factors (MRTFs/MAL/MKLs). Exp. Cell Res. 313, 3432-3445.
125. Moskowitz, I. P., Wang, J., Peterson, M. A., Pu, W. T., Mackinnon, A. C., Oxburgh, L., Chu, G. C., Sarkar, M., Berul, C., Smoot, L. et al. (2011). Transcription factor genes Smad4 and Gata4 cooperatively regulate cardiac valve development. [corrected]. Proc. Natl. Acad. Sci. USA 108, 4006-4011.
126. Muraoka, R. S., Bushdid, P. B., Brantley, D. M., Yull, F. E. and Kerr, L. D. (2000). Mesenchymal expression of nuclear factor-kappaB inhibits epithelial growth and branching in the embryonic chick lung. Dev. Biol. 225, 322-338.
127. Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A. and Chen, C. S. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. USA 102, 11594-11599.
128. Ning, Q. M. and Wang, X. R. (2007). Activations of mitogen-activated protein kinase and nuclear factor-kappaB by mechanical stretch result in ventilation-induced lung injury. Med. Hypotheses 68, 356-360.
129. North, T. E., Goessling, W., Peeters, M., Li, P., Ceol, C., Lord, A. M., Weber, G. J., Harris, J., Cutting, C. C., Huang, P. et al. (2009). Hematopoietic stem cell development is dependent on blood flow. Cell 137, 736-748.
130. Oh, H. and Irvine, K. D. (2008). In vivo regulation of Yorkie phosphorylation and localization. Development 135, 1081-1088.
131. Oh, H. and Irvine, K. D. (2009). In vivo analysis of Yorkie phosphorylation sites. Oncogene 28, 1916-1927.
132. Orr, A. W., Sanders, J. M., Bevard, M., Coleman, E., Sarembock, I. J. and Schwartz, M. A. (2005). The subendothelial extracellular matrix modulates NF-kappaB activation by flow: a potential role in atherosclerosis. J. Cell Biol. 169, 191-202.
133. Orr, A. W., Helmke, B. P., Blackman, B. R. and Schwartz, M. A. (2006). Mechanisms of mechanotransduction. Dev. Cell 10, 11-20.
134. Ozawa, N., Shichiri, M., Iwashina, M., Fukai, N., Yoshimoto, T. and Hirata, Y. (2004). Laminar shear stress up-regulates inducible nitric oxide synthase in the endothelium. Hypertens. Res. 27, 93-99.
135. Pajerowski, J. D., Dahl, K. N., Zhong, F. L., Sammak, P. J. and Discher, D. E. (2007). Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. USA 104, 15619-15624.
136. Papachristou, D. J., Papachroni, K. K., Basdra, E. K. and Papavassiliou, A. G. (2009). Signaling networks and transcription factors regulating mechanotransduction in bone. Bioessays 31, 794-804.
137. Park, J., Puapong, D. P., Wu, B. M., Atkinson, J. B. and Dunn, J. C. (2004). Enterogenesis by mechanical lengthening: morphology and function of the lengthened small intestine. J. Pediatr. Surg. 39, 1823-1827.
138. Parsons, S. A., Millay, D. P., Wilkins, B. J., Bueno, O. F., Tsika, G. L., Neilson, J. R., Liberatore, C. M., Yutzey, K. E., Crabtree, G. R., Tsika, R. W. et al. (2004). Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. J. Biol. Chem. 279, 26192-26200.
139. Pasque, V., Miyamoto, K. and Gurdon, J. B. (2010). Efficiencies and mechanisms of nuclear reprogramming. Cold Spring Harb. Symp. Quant. Biol. 75, 189-200.
140. Peerani, R., Rao, B. M., Bauwens, C., Yin, T., Wood, G. A., Nagy, A., Kumacheva, E. and Zandstra, P. W. (2007). Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J. 26, 4744-4755.
141. Polte, T. R., Eichler, G. S., Wang, N. and Ingber, D. E. (2004). Extracellular matrix controls myosin light chain phosphorylation and cell contractility through modulation of cell shape and cytoskeletal prestress. Am. J. Physiol. Cell Physiol. 286, C518-C528.
142. Pouille, P. A., Ahmadi, P., Brunet, A. C. and Farge, E. (2009). Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal. 2, ra16.
143. Prat, A. G. and Cantiello, H. F. (1996). Nuclear ion channel activity is regulated by actin filaments. Am. J. Physiol. 270, C1532-C1543.
144. Raab-Cullen, D. M., Thiede, M. A., Petersen, D. N., Kimmel, D. B. and Recker, R. R. (1994). Mechanical loading stimulates rapid changes in periosteal gene expression. Calcif. Tissue Int. 55, 473-478.
145. Rauch, C., Brunet, A. C., Deleule, J. and Farge, E. (2002). C2C12 myoblast/osteoblast transdifferentiation steps enhanced by epigenetic inhibition of BMP2 endocytosis. Am. J. Physiol. Cell Physiol. 283, C235-C243.
146. Ray, A., Shakya, A. and Ray, B. K. (2005). Inflammation-responsive transcription factors SAF-1 and c-Jun/c-Fos promote canine MMP-1 gene expression. Biochim. Biophys. Acta 1732, 53-61.
147. Ren, F., Zhang, L. and Jiang, J. (2010). Hippo signaling regulates Yorkie nuclear localization and activity through 14-3-3 dependent and independent mechanisms. Dev. Biol. 337, 303-312.
148. Ren, Y., Effler, J. C., Norstrom, M., Luo, T., Firtel, R. A., Iglesias, P. A., Rock, R. S. and Robinson, D. N. (2009). Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I. Curr. Biol. 19, 1421-1428.
149. Resnick, N., Collins, T., Atkinson, W., Bonthron, D. T., Dewey, C. F., Jr and Gimbrone, M. A., Jr (1993). Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc. Natl. Acad. Sci. USA 90, 4591-4595.
150. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. D. (2001). Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186.
151. Robling, A. G., Castillo, A. B. and Turner, C. H. (2006). Biomechanical and molecular regulation of bone remodeling. Annu. Rev. Biomed. Eng. 8, 455-498.
152. Rossant, J. and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
153. Rubin, C. T. and Lanyon, L. E. (1985). Regulation of bone mass by mechanical strain magnitude. Calcif. Tissue Int. 37, 411-417.
154. Ruiz, S. A. and Chen, C. S. (2008). Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells 26, 2921-2927.
155. Sadoshima, J. and Izumo, S. (1993). Mechanotransduction in stretch-induced hypertrophy of cardiac myocytes. J. Recept. Res. 13, 777-794.
156. Sandri, M. (2008). Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23, 160-170.
157. Sansores-Garcia, L., Bossuyt, W., Wada, K., Yonemura, S., Tao, C., Sasaki, H. and Halder, G. (2011). Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 30, 2325-2335.
158. Schwank, G. and Basler, K. (2010). Regulation of organ growth by morphogen gradients. Cold Spring Harb. Perspect. Biol. 2, a001669.
159. Seher, T. C., Narasimha, M., Vogelsang, E. and Leptin, M. (2007). Analysis and reconstitution of the genetic cascade controlling early mesoderm morphogenesis in the Drosophila embryo. Mech. Dev. 124, 167-179.
160. Shiu, Y. T., Weiss, J. A., Hoying, J. B., Iwamoto, M. N., Joung, I. S. and Quam, C. T. (2005). The role of mechanical stresses in angiogenesis. Crit. Rev. Biomed. Eng. 33, 431-510.
161. Shraiman, B. I. (2005). Mechanical feedback as a possible regulator of tissue growth. Proc. Natl. Acad. Sci. USA 102, 3318-3323.
162. Sims, J. R., Karp, S. and Ingber, D. E. (1992). Altering the cellular mechanical force balance results in integrated changes in cell, cytoskeletal and nuclear shape. J. Cell Sci. 103, 1215-1222.
163. Small, S., Blair, A. and Levine, M. (1992). Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. 11, 4047-4057.
164. Sotiropoulos, A., Gineitis, D., Copeland, J. and Treisman, R. (1999). Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169.
165. Stadtfeld, M., Maherali, N., Breault, D. T. and Hochedlinger, K. (2008). Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2, 230-240.
166. Thodeti, C. K., Matthews, B., Ravi, A., Mammoto, A., Ghosh, K., Bracha, A. L. and Ingber, D. E. (2009). TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ. Res. 104, 1123-1130.
167. Tidball, J. G. (2005). Mechanical signal transduction in skeletal muscle growth and adaptation. J. Appl. Physiol. 98, 1900-1908.
168. Tseng, C. P., Kim, Y. J., Kumar, R. and Verma, A. K. (1994). Involvement of protein kinase C in the transcriptional regulation of 12-O-tetradecanoylphorbol-13-acetate-inducible genes modulated by AP-1 or non-AP-1 transacting factors. Carcinogenesis 15, 707-711.
169. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H. and Schwartz, M. A. (2005). A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431.
170. Urbich, C., Stein, M., Reisinger, K., Kaufmann, R., Dimmeler, S. and Gille, J. (2003). Fluid shear stress-induced transcriptional activation of the vascular endothelial growth factor receptor-2 gene requires Sp1-dependent DNA binding. FEBS Lett. 535, 87-93.
171. Vermot, J., Forouhar, A. S., Liebling, M., Wu, D., Plummer, D., Gharib, M. and Fraser, S. E. (2009). Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol. 7, e1000246.
172. Vilos, G. A. and Liggins, G. C. (1982). Intrathoracic pressures in fetal sheep. J. Dev. Physiol. 4, 247-256.
173. Wang, N., Butler, J. P. and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127.
174. Wang, N., Tytell, J. D. and Ingber, D. E. (2009). Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82.
175. Wang, Y. and Gilmore, T. D. (2003). Zyxin and paxillin proteins: focal adhesion plaque LIM domain proteins go nuclear. Biochim. Biophys. Acta 1593, 115-120.
176. Wang, Y. and Riechmann, V. (2007). The role of the actomyosin cytoskeleton in coordination of tissue growth during Drosophila oogenesis. Curr. Biol. 17, 1349-1355.
177. Wang, Y., Maciejewski, B. S., Lee, N., Silbert, O., McKnight, N. L., Frangos, J. A. and Sanchez-Esteban, J. (2006). Strain-induced fetal type II epithelial cell differentiation is mediated via cAMP-PKA-dependent signaling pathway. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L820-L827.
178. Wheeler, D. G., Barrett, C. F., Groth, R. D., Safa, P. and Tsien, R. W. (2008). CaMKII locally encodes L-type channel activity to signal to nuclear CREB in excitation-transcription coupling. J. Cell Biol. 183, 849-863.
179. Wigglesworth, J. S., Desai, R. and Hislop, A. A. (1987). Fetal lung growth in congenital laryngeal atresia. Pediatr. Pathol. 7, 515-525.
180. Wirrig, E. E. and Yutzey, K. E. (2011). Transcriptional regulation of heart valve development and disease. Cardiovasc. Pathol. 20, 162-167.
181. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47.
182. Worman, H. J., Fong, L. G., Muchir, A. and Young, S. G. (2009). Laminopathies and the long strange trip from basic cell biology to therapy. J. Clin. Invest. 119, 1825-1836.
183. Wozniak, M. A. and Chen, C. S. (2009). Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10, 34-43.
184. Xu, R., Nelson, C. M., Muschler, J. L., Veiseh, M., Vonderhaar, B. K. and Bissell, M. J. (2009). Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol. 184, 57-66.
185. Yang, G., Im, H. J. and Wang, J. H. (2005). Repetitive mechanical stretching modulates IL-1beta induced COX-2, MMP-1 expression, and PGE2 production in human patellar tendon fibroblasts. Gene 363, 166-172.
186. Yang, Y., Beqaj, S., Kemp, P., Ariel, I. and Schuger, L. (2000). Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia. J. Clin. Invest. 106, 1321-1330.
187. Zhao, B., Li, L., Lei, Q. and Guan, K. L. (2010). The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874.
188. Zhao, X. H., Laschinger, C., Arora, P., Szászi, K., Kapus, A. and McCulloch, C. A. (2007). Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J. Cell Sci. 120, 1801-1809.
189. Ziros, P. G., Basdra, E. K. and Papavassiliou, A. G. (2008). Runx2: of bone and stretch. Int. J. Biochem. Cell Biol. 40, 1659-1663.