TY - JOUR
T1 - Computational and experimental study of the mechanics of embryonic wound healing
AU - Wyczalkowski, Matthew A.
AU - Varner, Victor D.
AU - Taber, Larry A.
N1 - Funding Information:
This work was supported by Grants F32 GM093396 (MAW) , R01 GM075200 and R01 N5070918 (LAT) from the National Institutes of Health , as well as Grant 09PRE2060795 from the American Heart Association (VDV). We thank Elliot Elson, Benjamen Filas, and Yunfei Shi for helpful discussions.
PY - 2013/12
Y1 - 2013/12
N2 - Wounds in the embryo show a remarkable ability to heal quickly without leaving a scar. Previous studies have found that an actomyosin ring (purse string) forms around the wound perimeter and contracts to close the wound over the course of several dozens of minutes. Here, we report experiments that reveal an even faster mechanism which remarkably closes wounds by more than 50% within the first 30. s. Circular and elliptical wounds (~ 100 μm in size) were made in the blastoderm of early chick embryos and allowed to heal, with wound area and shape characterized as functions of time. The closure rate displayed a biphasic behavior, with rapid constriction lasting about a minute, followed by a period of more gradual closure to complete healing. Fluorescent staining suggests that both healing phases are driven by actomyosin contraction, with relatively rapid contraction of fibers at cell borders within a relatively thick ring of tissue (several cells wide) around the wound followed by slower contraction of a thin supracellular actomyosin ring along the margin, consistent with a purse string mechanism. Finite-element modeling showed that this idea is biophysically plausible, with relatively isotropic contraction within the thick ring giving way to tangential contraction in the thin ring. In addition, consistent with experimental results, simulated elliptical wounds heal with little change in aspect ratio, and decreased membrane tension can cause these wounds to open briefly before going on to heal. These results provide new insight into the healing mechanism in embryonic epithelia.
AB - Wounds in the embryo show a remarkable ability to heal quickly without leaving a scar. Previous studies have found that an actomyosin ring (purse string) forms around the wound perimeter and contracts to close the wound over the course of several dozens of minutes. Here, we report experiments that reveal an even faster mechanism which remarkably closes wounds by more than 50% within the first 30. s. Circular and elliptical wounds (~ 100 μm in size) were made in the blastoderm of early chick embryos and allowed to heal, with wound area and shape characterized as functions of time. The closure rate displayed a biphasic behavior, with rapid constriction lasting about a minute, followed by a period of more gradual closure to complete healing. Fluorescent staining suggests that both healing phases are driven by actomyosin contraction, with relatively rapid contraction of fibers at cell borders within a relatively thick ring of tissue (several cells wide) around the wound followed by slower contraction of a thin supracellular actomyosin ring along the margin, consistent with a purse string mechanism. Finite-element modeling showed that this idea is biophysically plausible, with relatively isotropic contraction within the thick ring giving way to tangential contraction in the thin ring. In addition, consistent with experimental results, simulated elliptical wounds heal with little change in aspect ratio, and decreased membrane tension can cause these wounds to open briefly before going on to heal. These results provide new insight into the healing mechanism in embryonic epithelia.
KW - Biomechanics
KW - Chick embryo
KW - Epithelial morphogenesis
KW - Epithelium
KW - Finite elements
KW - Growth
KW - Mechanobiology
UR - http://www.scopus.com/inward/record.url?scp=84883243436&partnerID=8YFLogxK
U2 - 10.1016/j.jmbbm.2013.07.018
DO - 10.1016/j.jmbbm.2013.07.018
M3 - Article
C2 - 23973771
AN - SCOPUS:84883243436
SN - 1751-6161
VL - 28
SP - 125
EP - 146
JO - Journal of the Mechanical Behavior of Biomedical Materials
JF - Journal of the Mechanical Behavior of Biomedical Materials
ER -