Measuring forces and stresses in situ in living tissues

Development, homeostasis and regeneration of tissues result from a complex combination of genetics and mechanics, and progresses in the former have been quicker than in the latter. Measurements of in situ forces and stresses appear to be increasingly important to delineate the role of mechanics in development. We review here several emerging techniques: contact manipulation, manipulation using light, visual sensors, and non-mechanical observation techniques. We compare their fields of applications, their advantages and limitations, and their validations. These techniques complement measurements of deformations and of mechanical properties. We argue that such approaches could have a significant impact on our understanding of the development of living tissues in the near future. Summary: This Primer summarizes the current range of invasive and non-invasive techniques to measure forces in cells and tissues, and discusses their applications in developmental contexts.

[1]  N. Borghi,et al.  FRET-based Molecular Tension Microscopy. , 2016, Methods.

[2]  Sophia Mã ¶ ller,et al.  Biomechanics — Mechanical properties of living tissue , 1982 .

[3]  Aude Michel,et al.  Mechanical induction of the tumorigenic β-catenin pathway by tumour growth pressure , 2015, Nature.

[4]  François Nédélec,et al.  Pulsatile cell-autonomous contractility drives compaction in the mouse embryo , 2015, Nature Cell Biology.

[5]  Corinna Blasse,et al.  Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing , 2015, eLife.

[6]  Arezki Boudaoud,et al.  Quantifying Hydrostatic Pressure in Plant Cells by Using Indentation with an Atomic Force Microscope , 2015, Biophysical journal.

[7]  J. Bacri,et al.  Magnetic flattening of stem-cell spheroids indicates a size-dependent elastocapillary transition. , 2015, Physical review letters.

[8]  Spandan Maiti,et al.  Force production and mechanical accommodation during convergent extension , 2015, Development.

[9]  Araxi O. Urrutia,et al.  YAP is essential for tissue tension to ensure vertebrate 3D body shape , 2015, Nature.

[10]  Pierre-François Lenne,et al.  Direct laser manipulation reveals the mechanics of cell contacts in vivo , 2015, Proceedings of the National Academy of Sciences.

[11]  Philippe Marcq,et al.  Colloquium: Mechanical formalisms for tissue dynamics , 2013, The European physical journal. E, Soft matter.

[12]  E. Paluch.  Biophysical methods in cell biology , 2015 .

[13]  Vaishnavi Ananthanarayanan,et al.  Single-molecule imaging of cytoplasmic dynein in vivo. , 2015, Methods in cell biology.

[14]  Arezki Boudaoud,et al.  Flowers under pressure: ins and outs of turgor regulation in development , 2014, Annals of botany.

[15]  Orion D. Weiner,et al.  Illuminating cell signalling with optogenetic tools , 2014, Nature Reviews Molecular Cell Biology.

[16]  M. Davidson,et al.  The cancer glycocalyx mechanically primes integrin-mediated growth and survival , 2014, Nature.

[17]  G. Wayne Brodland,et al.  CellFIT: A Cellular Force-Inference Toolkit Using Curvilinear Cell Boundaries , 2014, PloS one.

[18]  Gaudenz Danuser,et al.  Mechanical Feedback through E-Cadherin Promotes Direction Sensing during Collective Cell Migration , 2014, Cell.

[19]  E. Meyerowitz,et al.  Physical Forces Regulate Plant Development and Morphogenesis , 2014, Current Biology.

[20]  Michael Krieg,et al.  Mechanical Control of the Sense of Touch by β Spectrin , 2014, Nature Cell Biology.

[21]  Donald E Ingber,et al.  Quantifying cell-generated mechanical forces within living embryonic tissues , 2013, Nature Methods.

[22]  C. Heisenberg,et al.  Tension-oriented cell divisions limit anisotropic tissue tension in epithelial spreading during zebrafish epiboly , 2013, Nature Cell Biology.

[23]  Frédéric Dumas-Bouchiat,et al.  Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria , 2013, Nature Communications.

[24]  Kaoru Sugimura,et al.  The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing , 2013, Development.

[25]  P. Saramito,et al.  Mechanical formalism for tissue dynamics , 2013 .

[26]  Katsumi Imada,et al.  Glycine Insertion Makes Yellow Fluorescent Protein Sensitive to Hydrostatic Pressure , 2013, PloS one.

[27]  R. Gómez-Martínez,et al.  Silicon chips detect intracellular pressure changes in living cells. , 2013, Nature nanotechnology.

[28]  Thomas Lecuit,et al.  Mechanics of Epithelial Tissue Homeostasis and Morphogenesis , 2013, Science.

[29]  Enrico Gratton,et al.  Fluid Shear Stress on Endothelial Cells Modulates Mechanical Tension across VE-Cadherin and PECAM-1 , 2013, Current Biology.

[30]  C. Heisenberg,et al.  Forces in Tissue Morphogenesis and Patterning , 2013, Cell.

[31]  J. Turner,et al.  In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling. , 2013, The Plant journal : for cell and molecular biology.

[32]  M. Trejo,et al.  Elasticity and wrinkled morphology of Bacillus subtilis pellicles , 2013, Proceedings of the National Academy of Sciences.

[33]  F Graner,et al.  Comparative study of non-invasive force and stress inference methods in tissue , 2013, The European physical journal. E, Soft matter.

[34]  Kaoru Sugimura,et al.  Bayesian inference of force dynamics during morphogenesis. , 2012, Journal of theoretical biology.

[35]  L. Oddershede,et al.  Force probing of individual molecules inside the living cell is now a reality. , 2012, Nature chemical biology.

[36]  Jean-Léon Maître,et al.  Adhesion Functions in Cell Sorting by Mechanically Coupling the Cortices of Adhering Cells , 2012, Science.

[37]  Felix Oswald,et al.  Forces Driving Epithelial Spreading in Zebrafish Gastrulation , 2012, Science.

[38]  Beth L. Pruitt,et al.  E-cadherin is under constitutive actomyosin-generated tension that is increased at cell–cell contacts upon externally applied stretch , 2012, Proceedings of the National Academy of Sciences.

[39]  Donald E. Ingber,et al.  Mechanosensitive mechanisms in transcriptional regulation , 2012, Journal of Cell Science.

[40]  Philippe Marcq,et al.  Mechanical state, material properties and continuous description of an epithelial tissue , 2012, Journal of The Royal Society Interface.

[41]  E. Kolb,et al.  Radial force development during root growth measured by photoelasticity , 2012, Plant and Soil.

[42]  Lars Hufnagel,et al.  Supplementary Information for Mechanical Stress Inference for Two Dimensional Cell Arrays , 2012 .

[43]  Pierre-François Lenne,et al.  Force generation, transmission, and integration during cell and tissue morphogenesis. , 2011, Annual review of cell and developmental biology.

[44]  L. Mahadevan,et al.  On the growth and form of the gut , 2011, Nature.

[45]  Ben Fabry,et al.  Linear and Nonlinear Rheology of Living Cells , 2011 .

[46]  Atsushi Miyawaki,et al.  Development of probes for cellular functions using fluorescent proteins and fluorescence resonance energy transfer. , 2011, Annual review of biochemistry.

[47]  Michel Labouesse,et al.  Forces and tension in development , 2011 .

[48]  Sriram Narasimhan,et al.  Video force microscopy reveals the mechanics of ventral furrow invagination in Drosophila , 2010, Proceedings of the National Academy of Sciences.

[49]  S. Grill,et al.  Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows , 2010, Nature.

[50]  D. Robinson,et al.  Cortical Mechanics and Meiosis II Completion in Mammalian Oocytes Are Mediated by Myosin-II and Ezrin-Radixin-Moesin (ERM) Proteins , 2010, Molecular biology of the cell.

[51]  Taekjip Ha,et al.  Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics , 2010, Nature.

[52]  T. Schluck,et al.  Photo-elastic properties of the wing imaginal disc of Drosophila , 2010, The European physical journal. E, Soft matter.

[53]  Françoise Brochard-Wyart,et al.  Aspiration , 2019, Differential Diagnosis of Cardiopulmonary Disease.

[54]  C. Aegerter,et al.  Determination of mechanical stress distribution in Drosophila wing discs using photoelasticity , 2009, Mechanisms of Development.

[55]  Frank Jülicher,et al.  Increased Cell Bond Tension Governs Cell Sorting at the Drosophila Anteroposterior Compartment Boundary , 2009, Current Biology.

[56]  J. Tinevez,et al.  Role of cortical tension in bleb growth , 2009, Proceedings of the National Academy of Sciences.

[57]  L. Davidson,et al.  Multi-scale mechanics from molecules to morphogenesis. , 2009, The international journal of biochemistry & cell biology.

[58]  François Graner,et al.  The role of fluctuations and stress on the effective viscosity of cell aggregates , 2009, Proceedings of the National Academy of Sciences.

[59]  Carl-Philipp Heisenberg,et al.  Biology and Physics of Cell Shape Changes in Development , 2009, Current Biology.

[60]  Andrew C. Oates,et al.  Quantitative approaches in developmental biology , 2009, Nature Reviews Genetics.

[61]  D. Kingsley,et al.  Muscle contraction is necessary to maintain joint progenitor cell fate. , 2009, Developmental cell.

[62]  Abbas Mgharbel,et al.  Measuring accurately liquid and tissue surface tension with a compression plate tensiometer , 2009, HFSP journal.

[63]  Xiaoyan Ma,et al.  Probing embryonic tissue mechanics with laser hole drilling , 2008, Physical biology.

[64]  Pierre-François Lenne,et al.  Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis , 2008, Nature Cell Biology.

[65]  Emmanuel Farge,et al.  Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. , 2008, Developmental cell.

[66]  John P Wikswo,et al.  Measurement Techniques for Cellular Biomechanics In Vitro , 2008, Experimental biology and medicine.

[67]  Frederick Sachs,et al.  A fluorescence energy transfer‐based mechanical stress sensor for specific proteins in situ , 2008, The FEBS journal.

[68]  M. Krieg,et al.  Tensile forces govern germ-layer organization in zebrafish , 2008, Nature Cell Biology.

[69]  Adrian Neagu,et al.  Experimental evaluation of apparent tissue surface tension based on the exact solution of the Laplace equation , 2007, 0706.3678.

[70]  Frank Jülicher,et al.  The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing , 2007, Current Biology.

[71]  Konrad Basler,et al.  Model for the regulation of size in the wing imaginal disc of Drosophila , 2007, Mechanisms of Development.

[72]  A. Curtis,et al.  Measuring cell forces by a photoelastic method. , 2007, Biophysical journal.

[73]  Lars Hufnagel,et al.  On the mechanism of wing size determination in fly development , 2007, Proceedings of the National Academy of Sciences.

[74]  Alexander R. A. Anderson,et al.  Single-Cell-Based Models in Biology and Medicine , 2007 .

[75]  L. Davidson,et al.  Measuring mechanical properties of embryos and embryonic tissues. , 2007, Methods in cell biology.

[76]  Michael Sheetz,et al.  Magnetic tweezers in cell biology. , 2007, Methods in cell biology.

[77]  R. Waugh,et al.  Rheological analysis and measurement of neutrophil indentation. , 2004, Biophysical journal.

[78]  Robert D. Goldman,et al.  Live Cell Imaging: A Laboratory Manual , 2004 .

[79]  L. Sulak,et al.  Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation , 2004, Nature.

[80]  M. Cobb.  Making sense of life: explaining biological development with models, metaphors and machines , 2004, Heredity.

[81]  G. Wayne Brodland,et al.  Computational modeling of cell sorting, tissue engulfment, and related phenomena: A review , 2004 .

[82]  Rudolf Oldenbourg,et al.  Polarization microscopy with the LC-PolScope , 2003 .

[83]  E. Farge.  Mechanical Induction of Twist in the Drosophila Foregut/Stomodeal Primordium , 2003, Current Biology.

[84]  Michael Shribak,et al.  Techniques for fast and sensitive measurements of two-dimensional birefringence distributions. , 2003, Applied optics.

[85]  A. Vogel,et al.  Mechanisms of pulsed laser ablation of biological tissues. , 2003, Chemical reviews.

[86]  G. Edwards,et al.  Forces for Morphogenesis Investigated with Laser Microsurgery and Quantitative Modeling , 2003, Science.

[87]  W. Kraus,et al.  Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. , 2001, Journal of biomechanics.

[88]  Wayne L. Rickoll,et al.  Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila , 2000, The Journal of cell biology.

[89]  G. Forgacs,et al.  Surface tensions of embryonic tissues predict their mutual envelopment behavior. , 1996, Development.

[90]  Steinberg,et al.  Liquid properties of embryonic tissues: Measurement of interfacial tensions. , 1994, Physical review letters.

[91]  K. Svoboda,et al.  Biological applications of optical forces. , 1994, Annual review of biophysics and biomolecular structure.

[92]  J Cairns,et al.  Cold spring harbor. , 1991, Science.

[93]  D. Kiehart,et al.  Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. , 1991, Development.

[94]  E. Evans,et al.  Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. , 1989, Biophysical journal.

[95]  G. S. Davis.  Migration-Directing Liquid Properties of Embryonic Amphibian Tissues , 1984 .

[96]  M. Stein,et al.  Epithelia as bubble rafts: a new method for analysis of cell shape and intercellular adhesion in embryonic and other epithelia. , 1982, Journal of theoretical biology.

[97]  L V Beloussov,et al.  Mechanical stresses and morphological patterns in amphibian embryos. , 1975, Journal of embryology and experimental morphology.

[98]  J. Mitchison,et al.  The Mechanical Properties of the Cell Surface , 1955 .

[99]  J. Mitchison,et al.  The Mechanical Properties of the Cell Surface I. The Cell Elastimeter , 1954 .