Tensegrity-based mechanosensing from macro to micro

被引:306
作者
Ingber, Donald E. [1 ,2 ,3 ]
机构
[1] Childrens Hosp, Dept Surg, Vasc Biol Program, Boston, MA 02115 USA
[2] Childrens Hosp, Dept Pathol, Vasc Biol Program, Boston, MA 02115 USA
[3] Harvard Univ, Sch Med, Boston, MA 02115 USA
基金
美国国家航空航天局; 美国国家卫生研究院; 美国国家科学基金会;
关键词
mechanotransduction; tensegrity; cytoskeleton; cell mechanics; integrin; tension;
D O I
10.1016/j.pbiomolbio.2008.02.005
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
This article is a Summary of a lecture on cellular rnechanotransduction that was presented at a symposium on "Cardiac Mechano-Electric Feedback and Arrhythmias" that convened at Oxford, England in April 2007. Although critical mechanosensitive molecules and cellular components, such as integrins, stretch-activated ion channels, and cytoskeletal filaments, have been shown to contribute to the response by which cells convert mechanical signals into a biochemical response, little is known about how they function in the structural context of living cells, tissues and organs to produce orchestrated changes in cell behavior in response to stress. Here, studies are reviewed that suggest our bodies use structural hierarchies (systems within systems) composed of interconnected extracellular matrix and cytoskeletal networks that span from the macroscale to the nanoscale to focus stresses on specific mechanotransducer molecules. A key feature of these networks is that they are in a state of isometric tension (i.e., experience a tensile prestress), which ensures that various molecular-scale mechanochemical transduction mechanisms proceed simultaneously and produce a concerted response. These features of living architecture are the same principles that govern tensegrity (tensional integrity) architecture, and mathematical models based on tensegrity are beginning to provide new and useful descriptions of living materials, including mammalian cells. This article reviews how the use of tensegrity at multiple size scales in our bodies guides mechanical force transfer from the macro to the micro, as well as how it facilitates conversion of mechanical signals into changes in ion flux, molecular binding kinetics, signal transduction, gene transcription, cell fate switching and developmental patterning. (c) 2008 Elsevier Ltd. All rights reserved.
引用
收藏
页码:163 / 179
页数:17
相关论文
共 97 条
[51]   Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz [J].
Maksym, GN ;
Fabry, B ;
Butler, JP ;
Navajas, D ;
Tschumperlin, DJ ;
Laporte, JD ;
Fredberg, JJ .
JOURNAL OF APPLIED PHYSIOLOGY, 2000, 89 (04) :1619-1632
[52]   Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition [J].
Mammoto, A ;
Huang, S ;
Moore, K ;
Oh, P ;
Ingber, DE .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2004, 279 (25) :26323-26330
[53]  
MAMMOTO A, 2007, CELL SPREADING CONTR
[54]  
Maniotis AJ, 1997, J CELL BIOCHEM, V65, P114
[55]   Demonstration of mechanical connections between integrins cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure [J].
Maniotis, AJ ;
Chen, CS ;
Ingber, DE .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1997, 94 (03) :849-854
[56]   Nanomagnetic actuation of receptor-mediated signal transduction [J].
Mannix, Robert J. ;
Kumar, Sanjay ;
Cassiola, Flavia ;
Montoya-Zavala, Martin ;
Feinstein, Efraim ;
Prentiss, Mara ;
Ingber, Donald E. .
NATURE NANOTECHNOLOGY, 2008, 3 (01) :36-40
[57]   Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels [J].
Matthews, BD ;
Overby, DR ;
Mannix, R ;
Ingber, DE .
JOURNAL OF CELL SCIENCE, 2006, 119 (03) :508-518
[58]   Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment [J].
McBeath, R ;
Pirone, DM ;
Nelson, CM ;
Bhadriraju, K ;
Chen, CS .
DEVELOPMENTAL CELL, 2004, 6 (04) :483-495
[59]   Mechanical control of cyclic AMP signalling and gene transcription through integrins [J].
Meyer, CJ ;
Alenghat, FJ ;
Rim, P ;
Fong, JHJ ;
Fabry, B ;
Ingber, DE .
NATURE CELL BIOLOGY, 2000, 2 (09) :666-668
[60]   INTEGRIN FUNCTION - MOLECULAR HIERARCHIES OF CYTOSKELETAL AND SIGNALING MOLECULES [J].
MIYAMOTO, S ;
TERAMOTO, H ;
COSO, OA ;
GUTKIND, JS ;
BURBELO, PD ;
AKIYAMA, SK ;
YAMADA, KM .
JOURNAL OF CELL BIOLOGY, 1995, 131 (03) :791-805