Emergent Patterns of Growth Controlled by Multicellular Form and Mechanics

Spatial patterns of cellular growth generate mechanical stresses that help to push, fold, expand, and deform tissues into their specific forms. Genetic factors are thought to specify patterns of growth and other behaviors to drive morphogenesis. Here, we show that tissue form itself can feed back to...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 102; no. 33; pp. 11594 - 11599
Main Authors Nelson, Celeste M., Jean, Ronald P., Tan, John L., Liu, Wendy F., Sniadecki, Nathan J., Spector, Alexander A., Chen, Christopher S., Langer, Robert
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 16.08.2005
National Acad Sciences
SeriesFrom the Cover
Subjects
Animals
Biological Sciences
Cattle
Cell growth
Cell Proliferation
Cells
Cells, Cultured
Cellular biology
Cultured cells
Cytoskeleton - metabolism
Endothelial cells
Endothelial Cells - cytology
Endothelial Cells - physiology
Epithelial cells
Epithelial Cells - cytology
Finite element analysis
Fracture mechanics
Geometry
Image contrast
Mechanical properties
Mechanical stress
Morphogenesis
Physical Sciences
Rats
Space life sciences
Stress, Mechanical
Tissues
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Summary:Spatial patterns of cellular growth generate mechanical stresses that help to push, fold, expand, and deform tissues into their specific forms. Genetic factors are thought to specify patterns of growth and other behaviors to drive morphogenesis. Here, we show that tissue form itself can feed back to regulate patterns of proliferation. Using microfabrication to control the organization of sheets of cells, we demonstrated the emergence of stable patterns of proliferative foci. Regions of concentrated growth corresponded to regions of high tractional stress generated within the sheet, as predicted by a finite-element model of multicellular mechanics and measured directly by using a micromechanical force sensor array. Inhibiting actomyosin-based tension or cadherin-mediated connections between cells disrupted the spatial pattern of proliferation. These findings demonstrate the existence of patterns of mechanical forces that originate from the contraction of cells, emerge from their multicellular organization, and result in patterns of growth. Thus, tissue form is not only a consequence but also an active regulator of tissue growth.
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Abbreviations: VE, vascular endothelial; FEM, finite-element method.
This paper was submitted directly (Track II) to the PNAS office.
Edited by Robert Langer, Massachusetts Institute of Technology, Cambridge, MA, and approved June 17, 2005
To whom correspondence may be addressed. E-mail: cmnelson@lbl.gov or chrischen@seas.upenn.edu.
Author contributions: C.M.N. and C.S.C. designed research; C.M.N., R.P.J., J.L.T., W.F.L., N.J.S., and A.A.S. performed research; C.M.N. and C.S.C. analyzed data; and C.M.N. and C.S.C. wrote the paper.
See Commentary on page 11571.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0502575102