Mechanical control of tissue and organ development

doi:10.1242/DEV.024166

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Mechanical control of tissue and organ development

Journal Article•DOI•

Mechanical control of tissue and organ development

Tadanori Mammoto¹, Donald E. Ingber², Donald E. Ingber¹•Institutions (2)

Harvard University¹, Wyss Institute for Biologically Inspired Engineering²

01 May 2010-Development (Company of Biologists)-Vol. 137, Iss: 9, pp 1407-1420

TL;DR: Work based on the convergence of physics, engineering and biology that suggests that mechanical forces generated by living cells are as crucial as genes and chemical signals for the control of embryological development, morphogenesis and tissue patterning is reviewed.

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Abstract: Many genes and molecules that drive tissue patterning during organogenesis and tissue regeneration have been discovered. Yet, we still lack a full understanding of how these chemical cues induce the formation of living tissues with their unique shapes and material properties. Here, we review work based on the convergence of physics, engineering and biology that suggests that mechanical forces generated by living cells are as crucial as genes and chemical signals for the control of embryological development, morphogenesis and tissue patterning.

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Journal Article•DOI•

Role of YAP/TAZ in mechanotransduction

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Sirio Dupont¹, Leonardo Morsut¹, Mariaceleste Aragona¹, Elena Enzo¹, Stefano Giulitti¹, Michelangelo Cordenonsi¹, Francesca Zanconato¹, Jimmy Le Digabel², Mattia Forcato³, Silvio Bicciato³, Nicola Elvassore¹, Stefano Piccolo¹ - Show less +8 more•Institutions (3)

University of Padua¹, Paris Diderot University², University of Modena and Reggio Emilia³

09 Jun 2011-Nature

TL;DR: YAP/TAZ are identified as sensors and mediators of mechanical cues instructed by the cellular microenvironment and are functionally required for differentiation of mesenchymal stem cells induced by ECM stiffness and for survival of endothelial cells regulated by cell geometry.

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Abstract: Cells perceive their microenvironment not only through soluble signals but also through physical and mechanical cues, such as extracellular matrix (ECM) stiffness or confined adhesiveness. By mechanotransduction systems, cells translate these stimuli into biochemical signals controlling multiple aspects of cell behaviour, including growth, differentiation and cancer malignant progression, but how rigidity mechanosensing is ultimately linked to activity of nuclear transcription factors remains poorly understood. Here we report the identification of the Yorkie-homologues YAP (Yes-associated protein) and TAZ (transcriptional coactivator with PDZ-binding motif, also known as WWTR1) as nuclear relays of mechanical signals exerted by ECM rigidity and cell shape. This regulation requires Rho GTPase activity and tension of the actomyosin cytoskeleton, but is independent of the Hippo/LATS cascade. Crucially, YAP/TAZ are functionally required for differentiation of mesenchymal stem cells induced by ECM stiffness and for survival of endothelial cells regulated by cell geometry; conversely, expression of activated YAP overrules physical constraints in dictating cell behaviour. These findings identify YAP/TAZ as sensors and mediators of mechanical cues instructed by the cellular microenvironment.

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4,120 citations

Cites methods from "Mechanical control of tissue and or..."

...23 for positive controls) had marginal effect on YAP/TAZ inactivation by mechanical cues, as judged by (1) YAP/TAZ nuclear exit induced by micropatterns or cytoskeletal inhibition in MEC, MSC or HMVEC (Fig....
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Journal Article•DOI•

The extracellular matrix modulates the hallmarks of cancer

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Michael W. Pickup¹, Janna K. Mouw¹, Valerie M. Weaver•Institutions (1)

University of California, San Francisco¹

01 Dec 2014-EMBO Reports

TL;DR: It is suggested that the success of cancer prevention and therapy programs requires an intimate understanding of the reciprocal feedback between the evolving extracellular matrix, the tumor cells and its cancer‐associated cellular stroma.

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Abstract: The extracellular matrix regulates tissue development and homeostasis, and its dysregulation contributes to neoplastic progression. The extracellular matrix serves not only as the scaffold upon which tissues are organized but provides critical biochemical and biomechanical cues that direct cell growth, survival, migration and differentiation and modulate vascular development and immune function. Thus, while genetic modifications in tumor cells undoubtedly initiate and drive malignancy, cancer progresses within a dynamically evolving extracellular matrix that modulates virtually every behavioral facet of the tumor cells and cancer-associated stromal cells. Hanahan and Weinberg defined the hallmarks of cancer to encompass key biological capabilities that are acquired and essential for the development, growth and dissemination of all human cancers. These capabilities include sustained proliferation, evasion of growth suppression, death resistance, replicative immortality, induced angiogenesis, initiation of invasion, dysregulation of cellular energetics, avoidance of immune destruction and chronic inflammation. Here, we argue that biophysical and biochemical cues from the tumor-associated extracellular matrix influence each of these cancer hallmarks and are therefore critical for malignancy. We suggest that the success of cancer prevention and therapy programs requires an intimate understanding of the reciprocal feedback between the evolving extracellular matrix, the tumor cells and its cancer-associated cellular stroma.

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1,301 citations

Journal Article•DOI•

Extracellular matrix: A dynamic microenvironment for stem cell niche

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Francesca Gattazzo¹, Anna Urciuolo¹, Paolo Bonaldo¹•Institutions (1)

University of Padua¹

01 Aug 2014-Biochimica et Biophysica Acta

TL;DR: Engineered biomaterials able to mimic the in vivo characteristics of stem cell niche provide suitable in vitro tools for dissecting the different roles exerted by the ECM and its molecular components on stem cell behavior.

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1,022 citations

Cites background from "Mechanical control of tissue and or..."

...tion [11,13], and that tissue elasticity is altered during aging, disease and injury [18,76]....
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...forces, which in the end leads to the fine regulation of cell behavior [11,72,73]....
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Journal Article•DOI•

Soft Robotics: A Perspective—Current Trends and Prospects for the Future

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MajidiCarmel

01 Mar 2014-Soft robotics

TL;DR: Soft robots as mentioned in this paper are composed of easily deformable matter such as fluids, gels, and elastomers that match the elastic and rheological properties of biological tissue and organs.

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Abstract: Soft robots are primarily composed of easily deformable matter such as fluids, gels, and elastomers that match the elastic and rheological properties of biological tissue and organs. Like an octopus squeezing through a narrow opening or a caterpillar rolling through uneven terrain, a soft robot must adapt its shape and locomotion strategy for a broad range of tasks, obstacles, and environmental conditions. This emerging class of elastically soft, versatile, and biologically inspired machines represents an exciting and highly interdisciplinary paradigm in engineering that could revolutionize the role of robotics in healthcare, field exploration, and cooperative human assistance.

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968 citations

Journal Article•DOI•

Harnessing nanotopography and integrin–matrix interactions to influence stem cell fate

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Matthew J. Dalby¹, Nikolaj Gadegaard¹, Richard O.C. Oreffo²•Institutions (2)

University of Glasgow¹, University of Southampton²

01 Jun 2014-Nature Materials

TL;DR: How cell adhesions interact with nanotopography is discussed, and insight is provided as to how materials scientists can exploit these interactions to direct stem cell fate and to understand how the behaviour of stem cells in their niche can be controlled.

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Abstract: Stem cells respond to nanoscale surface features, with changes in cell growth and differentiation mediated by alterations in cell adhesion. The interaction of nanotopographical features with integrin receptors in the cells' focal adhesions alters how the cells adhere to materials surfaces, and defines cell fate through changes in both cell biochemistry and cell morphology. In this Review, we discuss how cell adhesions interact with nanotopography, and we provide insight as to how materials scientists can exploit these interactions to direct stem cell fate and to understand how the behaviour of stem cells in their niche can be controlled. We expect knowledge gained from the study of cell-nanotopography interactions to accelerate the development of next-generation stem cell culture materials and implant interfaces, and to fuel discovery of stem cell therapeutics to support regenerative therapies.

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879 citations

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References

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Journal Article•DOI•

Matrix elasticity directs stem cell lineage specification.

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Adam J. Engler¹, Shamik Sen¹, H. Lee Sweeney¹, Dennis E. Discher•Institutions (1)

University of Pennsylvania¹

25 Aug 2006-Cell

TL;DR: Naive mesenchymal stem cells are shown here to specify lineage and commit to phenotypes with extreme sensitivity to tissue-level elasticity, consistent with the elasticity-insensitive commitment of differentiated cell types.

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12,204 citations

"Mechanical control of tissue and or..." refers background in this paper

...Interestingly, cells preferentially differentiate into distinct cell types (e.g. neuron versus bone or muscle) when cultured on ECMs with a mechanical stiffness that is most similar to that of the respective in vivo tissue (Engler et al., 2006)....
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...…including cell shape (Chen et al., 1997; Dike et al., 1999), the actin or microtubule cytoskeleton (Mooney et al., 1994), ECM elasticity (Engler et al., 2006), tissue patterns (Ruiz and Chen, 2008; Nelson et al., 2005) or Rho/ROCK signaling (McBeath et al., 2004; Mammoto et al., 2004;…...
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Journal Article•DOI•

Geometric control of cell life and death.

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Christopher S. Chen¹, Milan Mrksich¹, Sui Huang¹, George M. Whitesides¹, Donald E. Ingber¹ - Show less +1 more•Institutions (1)

Harvard University¹

30 May 1997-Science

TL;DR: Human and bovine capillary endothelial cells were switched from growth to apoptosis by using micropatterned substrates that contained extracellular matrix-coated adhesive islands of decreasing size to progressively restrict cell extension.

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Abstract: Human and bovine capillary endothelial cells were switched from growth to apoptosis by using micropatterned substrates that contained extracellular matrix-coated adhesive islands of decreasing size to progressively restrict cell extension. Cell spreading also was varied while maintaining the total cell-matrix contact area constant by changing the spacing between multiple focal adhesion-sized islands. Cell shape was found to govern whether individual cells grow or die, regardless of the type of matrix protein or antibody to integrin used to mediate adhesion. Local geometric control of cell growth and viability may therefore represent a fundamental mechanism for developmental regulation within the tissue microenvironment.

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4,641 citations

"Mechanical control of tissue and or..." refers background in this paper

...…that changes in cell fate between growth, differentiation and apoptosis can be controlled by altering similar parameters, including cell shape (Chen et al., 1997; Dike et al., 1999), the actin or microtubule cytoskeleton (Mooney et al., 1994), ECM elasticity (Engler et al., 2006), tissue…...
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...…Cell shape distortion can be precisely controlled by culturing cells on ECM-coated adhesive islands (the shape, size and position of which can be determined on the micrometer scale) that are engineered using microcontact printing techniques and surrounded by nonadhesive regions (Chen et al., 1997)....
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Book•

On Growth and Form

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D'Arcy Wentworth Thompson

01 Jan 1917

TL;DR: This book is an application of some of the concepts of physical science and sundry mathematical methods to the study of organic form and is like one of Darwin's books, well-considered, patiently wrought-out, learned, and cautious.

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Abstract: Introduction John Tyler Bonner VII 1. Introductory 2. On magnitude 3. The forms of cells 4. The forms of tissues, of cell-aggregates 5. On spicules and spicular skeletons 6. The equiangular spiral 7. The shapes of horns and of teeth or tusks 8. On form and mechanical efficiency 9. On the theory of transformations, or the comparison of related forms 10. Epilogue Index.

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4,470 citations

Journal Article•DOI•

Cell shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment

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Rowena McBeath¹, Dana M. Pirone¹, Celeste M. Nelson¹, Kiran Bhadriraju¹, Christopher S. Chen¹ - Show less +1 more•Institutions (1)

Johns Hopkins University School of Medicine¹

01 Apr 2004-Developmental Cell

TL;DR: It is demonstrated that cell shape regulates commitment of human mesenchymal stem cells to adipocyte or osteoblast fate and mechanical cues experienced in developmental and adult contexts, embodied by cell shape, cytoskeletal tension, and RhoA signaling, are integral to the commitment of stem cell fate.

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3,995 citations

"Mechanical control of tissue and or..." refers background in this paper

...…that are coated with ECM proteins decide their fate depending on the elasticity of their ECM substrate, even when cultured in the presence of soluble inducing factors, and this mechanical control mechanism depends on the generation of Rho-dependent cytoskeletal tension (McBeath et al., 2004)....
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...…shape (Chen et al., 1997; Dike et al., 1999), the actin or microtubule cytoskeleton (Mooney et al., 1994), ECM elasticity (Engler et al., 2006), tissue patterns (Ruiz and Chen, 2008; Nelson et al., 2005) or Rho/ROCK signaling (McBeath et al., 2004; Mammoto et al., 2004; Numaguchi et al., 2003)....
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Journal Article•DOI•

Tensional homeostasis and the malignant phenotype.

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Matthew J. Paszek¹, Nastaran Zahir¹, Kandice R. Johnson¹, Johnathon N. Lakins¹, Gabriela I. Rozenberg¹, Amit Gefen², Cynthia A. Reinhart-King¹, Susan S. Margulies¹, Micah Dembo³, David Boettiger¹, Daniel A. Hammer¹, Valerie M. Weaver¹ - Show less +8 more•Institutions (3)

University of Pennsylvania¹, Tel Aviv University², Boston University³

01 Sep 2005-Cancer Cell

TL;DR: It is found that tumors are rigid because they have a stiff stroma and elevated Rho-dependent cytoskeletal tension that drives focal adhesions, disrupts adherens junctions, perturbs tissue polarity, enhances growth, and hinders lumen formation.

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3,553 citations

"Mechanical control of tissue and or..." refers background in this paper

...Interestingly, neoplastic transformation might also involve alterations in the physical interactions between cells and the ECM that increase cell tension (Paszek et al., 2005; Butcher et al., 2009; Ingber, 2008; Bissell et al., 2005; Levental et al., 2009)....
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