Cellular control lies in the balance of forces

Current Opinion in Cell Biology

Volumn 10, Issue 2, 1998, Pages 232-239

  Chicurel, Marina E ^a   Chen, Christopher S ^a   Ingber, Donald E ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; APOPTOSIS; BRAIN DEVELOPMENT; CELL SHAPE; CHROMOSOME; CYTOSKELETON; FORCE; INTERMEDIATE FILAMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TENSION;

EID: 0032053788     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80145-2     Document Type: Article

References (71)

1. Van Essen DC. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385:1997;313-318.
2. Chada S, Lamoreux P, Buxbaum RE, Heideman SR. Cytomechanics of neurite outgrowth from chick brain neurons. J Cell Sci. 110:1997;1179-1186.
3. Condron BG, Zinn K. Regulated neurite tension as a mechanism for determination of neuronal arbor geometries in vivo. Curr Biol. 7:1997;813-816.
4. Wang NJ, Butler P, Ingber DE. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1993;1124-1127.
5. Potard US, Butler JP, Wang N. Cytoskeletal mechanics in confluent epithelial cells probed through integrins and E-cadherins. Am J Physiol. 272:1997;C1654-C1663.
6. Yoshida M, Westlin WF, Wang N, Ingber DE, Rosenzweig A, Resnick N, Gimbrone MA. Leukocyte adhesion to vascular endothelium induces E-selectin linkage to the actin cytoskeleton. J Cell Biol. 133:1996;445-455.
7. Choquet D, Felsenfeld DP, Sheetz MP. Extracellular matrix rigidity causes strengthening of integrin - cytoskeleton linkages. of outstanding interest Cell. 88:1997;39-48 Optical tweezers were used to physically restrain ECM-coated microbeads bound to cell-surface integrin receptors. The strength of integrin - cytoskeleton linkages was shown to increase proportionally as the restraining force was raised.
8. Felsenfeld DP, Choquet D, Sheetz MP. Ligand binding regulates the directed movement of β1 integrins on fibroblasts. Nature. 383:1996;438-440.
9. Plopper G, McNamee HP, Dike LE, Bojanowski K, Ingber D. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol Biol Cell. 6:1995;1349-1365.
10. Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, Akiyama SK, Yamada KM. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol. 131:1995;791-805.
11. Ezzell RM, Goldmann WH, Wang N, Parasharama N, Ingber DE. Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. of outstanding interest Exp Cell Res. 231:1997;14-26 By replacing lost vinculin protein in F9 embryonic carcinoma cells through transfection, this focal adhesion protein was found to play a critical role in transmembrane mechanical coupling, stress fiber formation and cell shape control.
12. Smith PG, Garcia R, Kogerman L. Strain reorganizes focal adhesions and cytoskeleton in cultured airway smooth muscle cells. Exp Cell Res. 232:1997;127-136.
13. Thoumine O, Nerem RM, Girard PR. Oscillatory shear stress and hydrostatic pressure modulates cell-matrix attachment proteins in cultured endothelial cells. In Vitro Cell Dev Biol Anim. 31:1995;45-54.
14. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem. 271:1996;20246-20249.
15. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). of special interest Science. 273:1996;245-248 This paper describes the identification of Rho-kinase which mediates the effects of Rho on myosin light chain phosphorylation.
16. Chrzanowska-Wodnicka M, Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. of outstanding interest J Cell Biol. 133:1996;1403-1415 This paper clearly defines the critical role of mechanical tension in terms of mediating the effects of Rho on focal adhesion formation and stress fiber assembly.
17. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y, Kaibuchi K. Formation of actin stress fibers and focal adhesions enhanced by rho-kinase. of special interest Science. 275:1997;1308-1311 Another paper that definitively demonstrates the key roles of rho-kinase and cell tension in control of cytoskeletal structure.
18. Ingber DE, Dike L, Hansen L, Karp S, Liley H, Maniotis A, McNamee H, Mooney D, Plopper G, Sims J, et al. Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration, and tissue pattern during morphogenesis. Int Rev Cytol. 150:1994;173-224.
19. Kaech S, Ludin B, Matus A. Cytoskeletal plasticity in cells expressing neuronal microtubule-associated proteins. of outstanding interest Neuron. 17:1996;1189-1199 Time-lapse video microscopy demonstrated individual microtubules buckling under compression in living cells that expressed microtubule-associated proteins labelled with green fluorescent protein. These time-lapse video images can be downloaded from the investigator's Web site.
20. Waterman-Storer CM, Salmon ED. Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol. 139:1997;417-434.
21. Maniotis AJ, Chen JS, Ingber DE. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. of outstanding interest Proc Natl Acad Sci USA. 94:1997;849-854 This study uses a micromanipulation approach to directly demonstrate the existence of hard-wiring in living cells. By pulling on cell-surface integrin receptors, immediate structural alterations were induced in the cytoskeleton and in the center of the nucleus in both interphase and metaphase cells.
22. Goldman RD, Khuon S, Chou YH, Opal P, Steinert PM. The function of intermediate filaments in cell shape and cytoskeletal integrity. J Cell Biol. 134:1996;971-983.
23. Wan X, Harris JA, Morris CE. Responses of neurons to extreme osmomechanical stress. J Membr Biol. 145:1995;21-31.
24. Kolodney MS, Elson EL. Contraction due to microtubule disruption is associated with increased phosphorylation of myosin regulatory light chain. Proc Natl Acad Sci USA. 92:1995;10252-10256.
25. Bershadsky A, Chausovsky A, Becker E, Lyubimova A, Geiger B. Involvement of microtubules in the control of adhesion-dependent signal transduction. of special interest Curr Biol. 6:1996;1279-1289 This study shows that shifting the cellular force balance by disrupting microtubule struts can feedback to regulate signal transduction in the focal adhesion.
26. Tagawa H, Wang N, Narishige T, Ingber DE, Zile MR, Cooper GT. Cytoskeletal mechanics in pressure-overload cardiac hypertrophy. Circ Res. 80:1997;281-289.
27. Davies PF, Barbee KA, Volin MV, Robotewskyi A, Chen J, Joseph L, Griem ML, Wernick MN, Jacobs E, Polacek DC, et al. Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. of special interest Annu Rev Physiol. 59:1997;527-549 A review of mechanotransduction in endothelial cells exposed to hemodynamic forces. Data are also included which demonstrate that fluid shear stress applied to the cell apex can induce biochemical changes in the focal adhesions at the cell base.
28. Ingber DE. Tensegrity: the architectural basis of cellular mechanotransduction. of outstanding interest Annu Rev Physiol. 59:1997;575-599 A detailed discussion of how cells use tensegrity architecture to balance mechanical forces and to mediate mechanochemical transduction in living cells.
29. Maniotis AJ, Bojanowski K, Ingber DE. Mechanical continuity and reversible chromosome disassembly within intact genomes removed from living cells. of special interest J Cell Biochem. 65:1997;114-130 When a single chromosome is removed from living endothelial cells with a micropipette, all of the remaining chromosomes follow like beads on a continous elastic string. Use of various enzymes and dyes revealed that DNA provides mechanical coupling throughout the entire genome.
30. Hubmayr RD, Shore SA, Fredberg JJ, Planus E, Panettieri RAJ, Moller W, Heyder J, Wang N. Pharmacological activation changes stiffness of cultured human airway smooth muscle cells. of special interest Am J Physiol. 271:1996;C1660-C1668 Soluble vasoagonists are used in combination with magnetic twisting cytometry to directly demonstrate that cellular stiffness is controlled by pre-stress in the cytoskeleton of cultured smooth muscle cells.
31. Lee K-M, Tsai KY, Wang N, Ingber DE. Extracellular matrix and pulmonary hypertension: control of vascular smooth muscle cell contractility. Am J Physiol. 274:1998;H76-H82. (Heart Circ Physiol 43).
32. Pickett-Heaps JD, Forer A, Spurck T. Traction fibre: toward a 'tensegral' model of the spindle. of outstanding interest Cell Motil Cytoskeleton. 37:1997;1-6 A detailed discussion of the limitations of current models of chromosome movement and of the possibility that the mitotic spindle is organized as a prestressed tensegrity structure. Implications for control of chromosome movements are discussed.
33. Spurck TP, Forer A, Pickett-Heaps JD. Ultraviolet microbeam irradiations of epithelial and spermatocyte spindles suggest that forces act on the kinetochore fibre, and are not generated by its disassembly. of special interest Cell Motil Cytoskeleton. 36:1997;136-148 When a single microtubule in the mitotic spindle is ablated using an ultrafine laser beam, pre-stress in the spindle can be visualized by both movement of the spindle pole and buckling of the remaining microtubules.
34. Nickerson JA, Penman S. Localization of nuclear matrix core filament proteins at interphase and mitosis. Cell Biol Int Rep. 16:1992;811-826.
35. DeBiasio RL, LaRocca GM, Post PL, Taylor DL. Mysoin II transport, organization and phosphorylation: evidence for cortical flow/solation-contraction coupling during cytokinesis and cell locomotion. Mol Biol Cell. 7:1996;1259-1282.
36. Czaban BB, Forer A. Rhodamine-labelled phalloidin stains components in the chromosomal spindle fibres of crane-fly spermatocytes and Haemanthus endosperm cells. Biochem Cell Biol. 70:1992;664-676.
37. Stamenovic D, Fredberg JJ, Wang N, Butler JP, Ingber DE. A microstructural approach to cytoskeletal mechanics based on tensegrity. J Theor Biol. 181:1996;125-136.
38. Coughlin MF, Stamenovic D. A tensegrity structure with buckling compression elements. J Appl Mech. 64:1997;480-486.
39. Pommerenke H, Schreiber E, Durr F, Nebe B, Hahnel C, Moller W, Rychly J. Stimulation of integrin receptors using a magnetic drag force device induces an intracellular free calcium response. of outstanding interest Eur J Cell Biol. 70:1996;157-164 Pulling on integrins, but not on other receptors, is shown to induce release of intracellular calcium.
40. Muller JM, Chilian WM, Davis MJ. Integrin signaling transduces shear stress-dependent vasodilation of coronary arterioles. Circ Res. 80:1997;32-326.
41. Wilson E, Sudhir K, Ives HE. Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. J Clin Invest. 96:1995;2364-2372.
42. Salter DM, Robb JE, Wright MO. Electrophysiological responses of human bone cells to mechanical stimulation: evidence for specific integrin function in mechanotransduction. J Bone Miner Res. 12:1997;1133-1141.
43. 2+ dependence and biophysical properties of integrin-mediated mechanical modulation of transmitter release from frog motor nerve terminals. of special interest J Neurosci. 17:1997;904-916 Stress transfer across integrins is shown to produce a chemical response within a few milliseconds after stress application.
44. Liu J, Schrank B, Waterston RH. Interaction between a putative mechanosensory membrane channel and a collagen. Science. 273:1996;361-364.
45. Chicurel ME, Singer RH, Meyer CM, Ingber DE. Recruitment of mRNA and ribosomes to focal adhesions triggered by integrin binding and mechanical tension. of outstanding interest Nature. 1998; Altering the balance of mechanical forces across integrins induces recruitment of mRNA and ribosomes to the focal adhesion and hence, formation of a microcompartment specialized for protein translation.
46. Wada H, Ivester CT, Carabello BA, Cooper G IV, McDermott PJ. Translational initiation factor elF-4E. A link between cardiac load and protein synthesis. J Biol Chem. 271:1996;8359-8364.
47. Zhang Q, Magnusson MK, Mosher DF. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through rho-dependent actin stress fiber formation and cell contraction. of special interest Mol Biol Cell. 8:1997;1415-1425 This study shows how the cellular force balance and associated ECM remodelling may be altered by either increasing cytoskeletal tension generation or disrupting internal microtubule struts.
48. Tomasek JJ, Halliday NL, Updike DL, Ahern-Moore JS, Vu T-KH, Liu RW, Howard EW. Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J Biol Chem. 272:1997;7482-7487.
49. Doong H, Dissanayake S, Gowrishankar TR, LaBarbera MC, Lee RC. Calcium antagonists alter cell shape and induce procollagenase synthesis in keloid and normal human dermal fibroblasts. J Burn Care Rehabil. 17:1996;497-514.
50. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. of special interest Nature. 385:1997;537-540 This study demonstrates the dramatic effects that altering the strength of integrin-ECM adhesions can have on cell motility.
51. Wei Y, Lukashev M, Simon DI, Bodary SC, Rosenberg S, Doyle MV, Chapman HA. Regulation of integrin function by the urokinase receptor. Science. 273:1996;1551-1555.
52. Stefansson S, Lawrence DA. The serpin PAI-1 inhibits cell migration by blocking integrin αVβ3 binding to vitronectin. Nature. 383:1996;441-443.
53. Planus E, Barlovatz-Meimon G, Rogers R, Bonavaud S, Ingber D, Wang N. Binding of urokinase to plasminogen activator inhibitor type-1 mediates cell adhesion and spreading. J Cell Sci. 110:1997;1091-1098.
54. Galbraith CG, Sheetz MP. A micromachined device provides a new bend on fibroblast traction forces. of special interest Proc Natl Acad Sci USA. 94:1997;9114-9118 A new technique for measuring cell tractional forces beneath localized regions of the cell membrane.
55. Lamoreux P, Altun-Gultekin Z, Lin C, Wagner J, Heidemann S. Rac is required for growth cone function but not neurite assembly. J Cell Sci. 110:1997;635-641.
56. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. Geometric control of cell life and death. of outstanding interest Science. 276:1997;1425-1428 This paper clearly separates changes in cell shape from alterations in cell - ECM binding using a novel micropatterning technique. Using this approach, cell shape is shown to govern whether individual capillary cells will grow or die.
57. Roskelley CD, Desprez PY, Bissell MJ. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc Natl Acad Sci USA. 91:1994;12378-12382.
58. Singhvi R, Kumar A, Lopez GP, Stephanopoulos GN, Wang DIC, Whitesides GM, Ingber DE. Engineering cell shape and function. Science. 264:1994;696-698.
59. Bohmer R-M, Scharf E, Assoian RK. Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates the anchorage-dependent expression of cyclin D1. of special interest Mol Biol Cell. 7:1996;101-111 Changes in the cytoskeleton associated with cell adhesion and spreading are shown to play a key role in cell cycle progression.
60. Li M, Choo B, Wong ZM, Filmus J, Buick RN. Expression of OCI-5/glypican 3 during intestinal morphogenesis: regulation by cell shape in intestinal epithelial cells. Exp Cell Res. 235:1997;3-12.
61. Close M, Howelett A, Roskelley C, Desprez P, Bailey N, Rowning B, Teng C, Stampfer M, Yaswen P. Lactoferrin expression in mammary epithelial cells is mediated by changes in cell shape and actin cytoskeleton. J Cell Sci. 110:1997;2861-2871.
62. Schischmanoff PO, Yaswen P, Parra MK, Lee G, Chasis JA, Mohandas N, Conboy JG. Cell shape-dependent regulation of protein 4.1 alternative pre-mRNA splicing in mammary epithelial cells. J Biol Chem. 272:1997;10254-10259.
63. Manfruelli P, Arquier N, Hanratty WP, Semeriva M. The tumor suppressor gene, lethal(2)giant larvae (I(2)gl), is required for cell shape change of epithelial cells during Drosophila development. Development. 122:1996;2283-2294.
64. Gimona M, Kazzaz JA, Helfman DM. Forced expression of tropomyosin 2 or 3 in v-Ki-ras-transformed fibroblasts results in distinct phenotypic effects. Proc Natl Acad Sci USA. 93:1996;9618-9623.
65. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. of special interest J Cell Biol. 137:1997;231-245 The transformed phenotype is reversed in vitro and in vivo by adding integrin-blocking antibodies to mammary epithelial tumor cells. Integrin binding results in coordinated changes in intracellular structure, cell - cell contacts and associated restoration of normal growth patterns.
66. Nicklas RB, Ward SC, Gorbsky GJ. Kinetochore chemistry is sensitive to tension and may link mitolic forces to a cell cycle checkpoint. J Cell Biol. 130:1995;929-939.
67. Li X, Nicklas RB. Tension-sensitive kinetochore phosphorylation and the chromosome distribution checkpoint in praying mantid spermatocytes. of outstanding interest J Cell Sci. 110:1997;537-545 Mechanical tension applied directly to chromosomes using micropipettes is shown to regulate kinetochore phosphorylation. This local mechanochemical event in turn controls the movement of all the remaining chromosomes.
68. Khan S, Sheetz MP. Force effects on biochemical kinetics. Annu Rev Biochem. 66:1997;785-805.
69. Hamill OP, McBride DWJ. Rapid adaptation of single mechanosensitive channels in Xenopus oocytes. Proc Natl Acad Sci USA. 89:1992;7462-7466.
70. Sukharev SI, Martinac B, Arshavsky VY, Kung C. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J. 65:1993;177-183.
71. Gudi SR, Clark CB, Frangos JA. Fluid flow rapidly activates G proteins in human endothelial cells. Involvement of G proteins in mechanochemical signal transduction. Circ Res. 79:1996;834-839.