|
|
|
|
|
|
|
|
|||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
doi: 10.1242/10.1242/jcs.00360
Commentary |
Departments of Surgery and Pathology, Children's Hospital and Harvard Medical School, Enders 1007, 300 Longwood Avenue, Boston, MA 02115, USA
e-mail: donald.ingber{at}tch.harvard.edu
The major challenge in biology today is biocomplexity: the need to explain how cell and tissue behaviors emerge from collective interactions within complex molecular networks. Part I of this two-part article, described a mechanical model of cell structure based on tensegrity architecture that explains how the mechanical behavior of the cell emerges from physical interactions among the different molecular filament systems that form the cytoskeleton. Recent work shows that the cytoskeleton also orients much of the cell's metabolic and signal transduction machinery and that mechanical distortion of cells and the cytoskeleton through cell surface integrin receptors can profoundly affect cell behavior. In particular, gradual variations in this single physical control parameter (cell shape distortion) can switch cells between distinct gene programs (e.g. growth, differentiation and apoptosis), and this process can be viewed as a biological phase transition. Part II of this article covers how combined use of tensegrity and solid-state mechanochemistry by cells may mediate mechanotransduction and facilitate integration of chemical and physical signals that are responsible for control of cell behavior. In addition, it examines how cell structural networks affect gene and protein signaling networks to produce characteristic phenotypes and cell fate transitions during tissue development.
Key words: Mechanobiology, Mechanotransduction, Biocomplexity, Bioinformatics, Integrins
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JCS:
This article has been cited by other articles:
|
|
 |
|
  A. Qian, S. Di, X. Gao, W. Zhang, Z. Tian, J. Li, L. Hu, P. Yang, D. Yin, and P. Shang cDNA microarray reveals the alterations of cytoskeleton-related genes in osteoblast under high magneto-gravitational environment Acta Biochim Biophys Sin, July 1, 2009; 41(7): 561 - 577. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Alessandri-Haber, O. A. Dina, X. Chen, and J. D. Levine TRPC1 and TRPC6 Channels Cooperate with TRPV4 to Mediate Mechanical Hyperalgesia and Nociceptor Sensitization J. Neurosci., May 13, 2009; 29(19): 6217 - 6228. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. A. Martinez-Lemus, M. A. Hill, and G. A. Meininger The Plastic Nature of the Vascular Wall: A Continuum of Remodeling Events Contributing to Control of Arteriolar Diameter and Structure Physiology, February 1, 2009; 24(1): 45 - 57. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Senju and H. Miyata The Role of Actomyosin Contractility in the Formation and Dynamics of Actin Bundles During Fibroblast Spreading J. Biochem., February 1, 2009; 145(2): 137 - 150. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Yu, P. Khandelwal, and G. Apodaca Distinct Apical and Basolateral Membrane Requirements for Stretch-induced Membrane Traffic at the Apical Surface of Bladder Umbrella Cells Mol. Biol. Cell, January 1, 2009; 20(1): 282 - 295. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. M. Goeckeler, P. C. Bridgman, and R. B. Wysolmerski Nonmuscle myosin II is responsible for maintaining endothelial cell basal tone and stress fiber integrity Am J Physiol Cell Physiol, October 1, 2008; 295(4): C994 - C1006. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Ghosh, C. K. Thodeti, A. C. Dudley, A. Mammoto, M. Klagsbrun, and D. E. Ingber Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro PNAS, August 12, 2008; 105(32): 11305 - 11310. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. A. Whipple, E. M. Balzer, E. H. Cho, M. A. Matrone, J. R. Yoon, and S. S. Martin Vimentin Filaments Support Extension of Tubulin-Based Microtentacles in Detached Breast Tumor Cells Cancer Res., July 15, 2008; 68(14): 5678 - 5688. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Wang, F.-X. Liang, and X.-P. Kong Characteristics of the Phagocytic Cup Induced by Uropathogenic Escherichia coli J. Histochem. Cytochem., June 1, 2008; 56(6): 597 - 604. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. M. Stiening, J. B. Hoying, M. B. Abdallah, A. M. Hoying, R. Pandey, K. Greer, and R. J. Collier The Effects of Endocrine and Mechanical Stimulation on Stage I Lactogenesis in Bovine Mammary Epithelial Cells J Dairy Sci, March 1, 2008; 91(3): 1053 - 1066. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Shiva Kumar, M. H. H. Stevens, and J. Z. Kiss Plastid movement in statocytes of the arg1 (altered response to gravity) mutant Am. J. Botany, February 1, 2008; 95(2): 177 - 184. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. P. Daley, S. B. Peters, and M. Larsen Extracellular matrix dynamics in development and regenerative medicine J. Cell Sci., February 1, 2008; 121(3): 255 - 264. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Alessandri-Haber, O. A. Dina, E. K. Joseph, D. B. Reichling, and J. D. Levine Interaction of Transient Receptor Potential Vanilloid 4, Integrin, and Src Tyrosine Kinase in Mechanical Hyperalgesia J. Neurosci., January 30, 2008; 28(5): 1046 - 1057. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Sun, P. McMinn, S. Coakley, M. Holcombe, R. Smallwood, and S. MacNeil An integrated systems biology approach to understanding the rules of keratinocyte colony formation J R Soc Interface, December 22, 2007; 4(17): 1077 - 1092. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Hayashida, M.-H. Wu, A. Pierce, A.-C. Poncelet, J. Varga, and H. W. Schnaper MAP-kinase activity necessary for TGFbeta1-stimulated mesangial cell type I collagen expression requires adhesion-dependent phosphorylation of FAK tyrosine 397 J. Cell Sci., December 1, 2007; 120(23): 4230 - 4240. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. H. Craig, B. Haimovich, and M. D. Basson {alpha}-Actinin-1 phosphorylation modulates pressure-induced colon cancer cell adhesion through regulation of focal adhesion kinase-Src interaction Am J Physiol Cell Physiol, December 1, 2007; 293(6): C1862 - C1874. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. J. Sniadecki, A. Anguelouch, M. T. Yang, C. M. Lamb, Z. Liu, S. B. Kirschner, Y. Liu, D. H. Reich, and C. S. Chen From the Cover: Magnetic microposts as an approach to apply forces to living cells PNAS, September 11, 2007; 104(37): 14553 - 14558. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. K Parker and D. E Ingber Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering Phil Trans R Soc B, August 29, 2007; 362(1484): 1267 - 1279. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J.G. Horrevoets Profilin-1: An Unexpected Molecule Linking Vascular Inflammation to the Actin Cytoskeleton Circ. Res., August 17, 2007; 101(4): 328 - 330. [Full Text] [PDF]
|
|
|
|
 |
|
 P. E. Thomas, M. Peters-Golden, E. S. White, V. J. Thannickal, and B. B. Moore PGE2 inhibition of TGF-beta1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signaling Am J Physiol Lung Cell Mol Physiol, August 1, 2007; 293(2): L417 - L428. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Lamalice, F. Le Boeuf, and J. Huot Endothelial Cell Migration During Angiogenesis Circ. Res., March 30, 2007; 100(6): 782 - 794. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Uetake, J. Loncarek, J. J. Nordberg, C. N. English, S. La Terra, A. Khodjakov, and G. Sluder Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells J. Cell Biol., January 16, 2007; 176(2): 173 - 182. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Wilhelmsen, M. Ketema, H. Truong, and A. Sonnenberg KASH-domain proteins in nuclear migration, anchorage and other processes J. Cell Sci., December 15, 2006; 119(24): 5021 - 5029. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Feng, X. Lu, J. C. Resendiz, and M. H. Kroll Pathological shear stress directly regulates platelet {alpha}IIbbeta3 signaling Am J Physiol Cell Physiol, December 1, 2006; 291(6): C1346 - C1354. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. W. Telewski A unified hypothesis of mechanoperception in plants Am. J. Botany, October 1, 2006; 93(10): 1466 - 1476. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Martin-Ventura, V. Nicolas, X. Houard, L. M. Blanco-Colio, A. Leclercq, J. Egido, R. Vranckx, J.-B. Michel, and O. Meilhac Biological Significance of Decreased HSP27 in Human Atherosclerosis Arterioscler. Thromb. Vasc. Biol., June 1, 2006; 26(6): 1337 - 1343. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. von Wnuck Lipinski, P. Keul, S. Lucke, G. Heusch, J. Wohlschlaeger, H. A. Baba, and B. Levkau Degraded collagen induces calpain-mediated apoptosis and destruction of the X-chromosome-linked inhibitor of apoptosis (xIAP) in human vascular smooth muscle cells Cardiovasc Res, February 15, 2006; 69(3): 697 - 705. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Wilhelmsen, S. H.M. Litjens, I. Kuikman, N. Tshimbalanga, H. Janssen, I. van den Bout, K. Raymond, and A. Sonnenberg Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin J. Cell Biol., December 5, 2005; 171(5): 799 - 810. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. M. Harold Molecules into Cells: Specifying Spatial Architecture Microbiol. Mol. Biol. Rev., December 1, 2005; 69(4): 544 - 564. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Fortemaison, S. Blancquaert, J. E. Dumont, C. Maenhaut, K. Aktories, P. P. Roger, and S. Dremier Differential Involvement of the Actin Cytoskeleton in Differentiation and Mitogenesis of Thyroid Cells: Inactivation of Rho Proteins Contributes to Cyclic Adenosine Monophosphate-Dependent Gene Expression but Prevents Mitogenesis Endocrinology, December 1, 2005; 146(12): 5485 - 5495. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Yoshigi, L. M. Hoffman, C. C. Jensen, H. J. Yost, and M. C. Beckerle Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement J. Cell Biol., October 24, 2005; 171(2): 209 - 215. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Ning, R. Zeineldin, Y. Liu, M. Rosenberg, M. S. Stack, and L. G. Hudson Down-regulation of Integrin {alpha}2 Surface Expression by Mutant Epidermal Growth Factor Receptor (EGFRvIII) Induces Aberrant Cell Spreading and Focal Adhesion Formation Cancer Res., October 15, 2005; 65(20): 9280 - 9286. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. C. R. Jones, K. Lane, S. B. Hopkinson, E. Lecuona, R. C. Geiger, D. A. Dean, E. Correa-Meyer, M. Gonzales, K. Campbell, J. I. Sznajder, et al. Laminin-6 assembles into multimolecular fibrillar complexes with perlecan and participates in mechanical-signal transduction via a dystroglycan-dependent, integrin-independent mechanism J. Cell Sci., June 15, 2005; 118(12): 2557 - 2566. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. S. Stein Mechanogenomic Control of DNA Exposure and Sequestration Am. J. Pathol., April 1, 2005; 166(4): 959 - 962. [Full Text] [PDF]
|
|
|
|
|
|
J.-r. Kim-Kaneyama, W. Suzuki, K. Ichikawa, T. Ohki, Y. Kohno, M. Sata, K. Nose, and M. Shibanuma Uni-axial stretching regulates intracellular localization of Hic-5 expressed in smooth-muscle cells in vivo J. Cell Sci., March 1, 2005; 118(5): 937 - 949. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. M. Langevin, N. A. Bouffard, G. J. Badger, J. C. Iatridis, and A. K. Howe Dynamic fibroblast cytoskeletal response to subcutaneous tissue stretch ex vivo and in vivo Am J Physiol Cell Physiol, March 1, 2005; 288(3): C747 - C756. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Meder, A. Shevchenko, K. Simons, and J. Fullekrug Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells J. Cell Biol., January 17, 2005; 168(2): 303 - 313. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Parre and A. Geitmann More Than a Leak Sealant. The Mechanical Properties of Callose in Pollen Tubes Plant Physiology, January 1, 2005; 137(1): 274 - 286. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. M. Adam, S. H. Eaton, C. Estrada, A. Nimgaonkar, S.-C. Shih, L. E. H. Smith, I. S. Kohane, D. Bagli, and M. R. Freeman Mechanical stretch is a highly selective regulator of gene expression in human bladder smooth muscle cells Physiol Genomics, December 15, 2004; 20(1): 36 - 44. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L.V. Broers, E. A.G. Peeters, H. J.H. Kuijpers, J. Endert, C. V.C. Bouten, C. W.J. Oomens, F. P.T. Baaijens, and F. C.S. Ramaekers Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies Hum. Mol. Genet., November 1, 2004; 13(21): 2567 - 2580. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Daffara, L. Botto, E. Beretta, E. Conforti, A. Faini, P. Palestini, and G. Miserocchi Endothelial cells as early sensors of pulmonary interstitial edema J Appl Physiol, October 1, 2004; 97(4): 1575 - 1583. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. J. Mack, M. R. Kaazempur-Mofrad, H. Karcher, R. T. Lee, and R. D. Kamm Force-induced focal adhesion translocation: effects of force amplitude and frequency Am J Physiol Cell Physiol, October 1, 2004; 287(4): C954 - C962. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. J. Zwartz, A. Chigaev, D. C. Dwyer, T. D. Foutz, B. S. Edwards, and L. A. Sklar Real-time Analysis of Very Late Antigen-4 Affinity Modulation by Shear J. Biol. Chem., September 10, 2004; 279(37): 38277 - 38286. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Heil and W. Schaper Influence of Mechanical, Cellular, and Molecular Factors on Collateral Artery Growth (Arteriogenesis) Circ. Res., September 3, 2004; 95(5): 449 - 458. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Deng, N. J. Fairbank, B. Fabry, P. G. Smith, and G. N. Maksym Localized mechanical stress induces time-dependent actin cytoskeletal remodeling and stiffening in cultured airway smooth muscle cells Am J Physiol Cell Physiol, August 1, 2004; 287(2): C440 - C448. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Zhao, H. Xiao, W. Long, W. J. Pearce, and L. D. Longo Expression of several cytoskeletal proteins in ovine cerebral arteries: developmental and functional considerations J. Physiol., July 15, 2004; 558(2): 623 - 632. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. L. Wu, S. Khan, S. Lakhe-Reddy, G. Jarad, A. Mukherjee, C. A. Obejero-Paz, M. Konieczkowski, J. R. Sedor, and J. R. Schelling The NHE1 Na+/H+ Exchanger Recruits Ezrin/Radixin/Moesin Proteins to Regulate Akt-dependent Cell Survival J. Biol. Chem., June 18, 2004; 279(25): 26280 - 26286. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. M. Norvell, S. M. Ponik, D. K. Bowen, R. Gerard, and F. M. Pavalko Fluid shear stress induction of COX-2 protein and prostaglandin release in cultured MC3T3-E1 osteoblasts does not require intact microfilaments or microtubules J Appl Physiol, March 1, 2004; 96(3): 957 - 966. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-B. Michel Anoikis in the Cardiovascular System: Known and Unknown Extracellular Mediators Arterioscler. Thromb. Vasc. Biol., December 1, 2003; 23(12): 2146 - 2154. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. B. Blancaflor and P. H. Masson Plant Gravitropism. Unraveling the Ups and Downs of a Complex Process Plant Physiology, December 1, 2003; 133(4): 1677 - 1690. [Full Text] [PDF]
|
|
|
|
|
|
F. Baluska, J. Samaj, P. Wojtaszek, D. Volkmann, and D. Menzel Cytoskeleton-Plasma Membrane-Cell Wall Continuum in Plants. Emerging Links Revisited Plant Physiology, October 1, 2003; 133(2): 482 - 491. [Full Text] [PDF]
|
|
|
|
|
|
J. Eggermont Rho's role in cell volume: sensing, strutting, or signaling? Focus on "Hyperosmotic stress activates Rho: differential involvement in Rho kinase-dependent MLC phosphorylation and NKCC activation" Am J Physiol Cell Physiol, September 1, 2003; 285(3): C509 - C511. [Full Text] [PDF]
|
|
|
|
|
|
D. E. Ingber Tensegrity I. Cell structure and hierarchical systems biology J. Cell Sci., April 1, 2003; 116(7): 1157 - 1173. [Abstract] [Full Text] [PDF]
|
|
