Cell–matrix feedback controls stretch-induced cellular memory and fibroblast activation

Y Yuan Hong (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) X Xiangjun Peng (Department of Engineering Mechanics, Applied Mechanics Laboratory, Institute of Biomechanics and Medical Engineering) H Haomin Yu (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) M Mohammad Jafari (Department of Mechanical and Industrial Engineering, New Jersey Institute of Technology) D Delaram Shakiba (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) Y Yuxuan Huang (State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences) C Chengqing Qu (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) E Ermia E. Melika (NSF Science and Technology Center for Engineering Mechanobiology) A Andrew K. Tawadros (NSF Science and Technology Center for Engineering Mechanobiology) A Aliza Mujahid (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) Y Yin-Yuan Huang (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) J Jacob A. Sandler (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) K Kenneth M. Pryse (NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) J Justin M. Sacks (Division of Plastic and Reconstructive Surgery, Washington University in St. Louis School of Medicine) E Elliot L. Elson (National Science Foundation Science and Technology Center for Engineering Mechanobiology, Department of Mechanical Engineering and Materials Science) G Guy M. Genin (National Science Foundation Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis) F Farid Alisafaei (Department of Mechanical and Industrial Engineering, New Jersey Institute of Technology)

Abstract

Mechanical stretch can activate long-lived changes in fibroblasts, increasing their contractility and initiating phenotypic transformations. This activation, critical to wound healing and procedures such as skin grafting, increases with mechanical stimulus for cells cultured in two-dimensional but is highly variable in cells in three-dimensional (3D) tissue. Here, we show that static mechanical stretch of cells in 3D tissues can either increase or decrease fibroblast activation depending upon recursive cell–extracellular matrix (ECM) feedback and demonstrate control of this activation through integrated in vitro and mathematical models. ECM viscoelasticity, signaling dynamics, and cell mechanics combine to yield a predictable, but nonmonotonic, relationship between mechanical stretch and long-term cell activation. Results demonstrate that feedback between cells and ECM determine how cells retain memory of mechanical stretch and have direct implications for improving outcomes in skin grafting procedures.

Article Details

Volume / Issue Vol. 122, Issue 12
Published March 25, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

Y

Yuan Hong

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

X

Xiangjun Peng

Department of Engineering Mechanics, Applied Mechanics Laboratory, Institute of Biomechanics and Medical Engineering

H

Haomin Yu

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

M

Mohammad Jafari

Department of Mechanical and Industrial Engineering, New Jersey Institute of Technology

D

Delaram Shakiba

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

Y

Yuxuan Huang

State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences

C

Chengqing Qu

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

E

Ermia E. Melika

NSF Science and Technology Center for Engineering Mechanobiology

A

Andrew K. Tawadros

NSF Science and Technology Center for Engineering Mechanobiology

A

Aliza Mujahid

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

Y

Yin-Yuan Huang

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

J

Jacob A. Sandler

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

K

Kenneth M. Pryse

NSF Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

J

Justin M. Sacks

Division of Plastic and Reconstructive Surgery, Washington University in St. Louis School of Medicine

E

Elliot L. Elson

National Science Foundation Science and Technology Center for Engineering Mechanobiology, Department of Mechanical Engineering and Materials Science

G

Guy M. Genin

National Science Foundation Science and Technology Center for Engineering Mechanobiology, Washington University in St. Louis

F

Farid Alisafaei

Department of Mechanical and Industrial Engineering, New Jersey Institute of Technology