TY - JOUR
T1 - Shannon entropy for time-varying persistence of cell migration
AU - Liu, Yanping
AU - Jiao, Yang
AU - Fan, Qihui
AU - Zheng, Yu
AU - Li, Guoqiang
AU - Yao, Jingru
AU - Wang, Gao
AU - Lou, Silong
AU - Chen, Guo
AU - Shuai, Jianwei
AU - Liu, Liyu
N1 - Funding Information:
This research was supported by the National Natural Science Foundation of China (grant nos. 11974066 , 11674043 , 11675134 , and 11874310 ), the Fundamental Research Funds for the Central Universities (grant no. 2019CDYGYB007 ), and the Natural Science Foundation of Chongqing, China (grant nos. cstc2019jcyj-msxmX0477 and cstc2018jcyjA3679 ).
Funding Information:
We thank Ben Fabry, Christoph Mark, Claus Metzner, and Lena Lautscham for providing experimental data concerning channel arrays and David B. Br?ckner, Alexandra Fink, Chase Broedersz, and Joachim R?dler for providing experimental data concerning two-state micropatterns. Y.J. thanks Arizona State University for support during his sabbatical leave. This research was supported by the National Natural Science Foundation of China (grant nos. 11974066, 11674043, 11675134, and 11874310), the Fundamental Research Funds for the Central Universities (grant no. 2019CDYGYB007), and the Natural Science Foundation of Chongqing, China (grant nos. cstc2019jcyj-msxmX0477 and cstc2018jcyjA3679).
Publisher Copyright:
© 2021 Biophysical Society
PY - 2021/6/15
Y1 - 2021/6/15
N2 - Cell migration, which can be significantly affected by intracellular signaling pathways and extracellular matrix, plays a crucial role in many physiological and pathological processes. Cell migration is typically modeled as a persistent random walk, which depends on two critical motility parameters, i.e., migration speed and persistence time. It is generally very challenging to efficiently and accurately quantify the migration dynamics from noisy experimental data. Here, we introduce the normalized Shannon entropy (SE) based on the FPS of cellular velocity autocovariance function to quantify migration dynamics. The SE introduced here possesses a similar physical interpretation as the Gibbs entropy for thermal systems in that SE naturally reflects the degree of order or randomness of cellular migration, attaining the maximal value of unity for purely diffusive migration (i.e., SE = 1 for the most “random” dynamics) and the minimal value of 0 for purely ballistic dynamics (i.e., SE = 0 for the most “ordered” dynamics). We also find that SE is strongly correlated with the migration persistence but is less sensitive to the migration speed. Moreover, we introduce the time-varying SE based on the WPS of cellular dynamics and demonstrate its superior utility to characterize the time-dependent persistence of cell migration, which typically results from complex and time-varying intra- or extracellular mechanisms. We employ our approach to analyze experimental data of in vitro cell migration regulated by distinct intracellular and extracellular mechanisms, exhibiting a rich spectrum of dynamic characteristics. Our analysis indicates that the SE and wavelet transform (i.e., SE-based approach) offers a simple and efficient tool to quantify cell migration dynamics in complex microenvironment.
AB - Cell migration, which can be significantly affected by intracellular signaling pathways and extracellular matrix, plays a crucial role in many physiological and pathological processes. Cell migration is typically modeled as a persistent random walk, which depends on two critical motility parameters, i.e., migration speed and persistence time. It is generally very challenging to efficiently and accurately quantify the migration dynamics from noisy experimental data. Here, we introduce the normalized Shannon entropy (SE) based on the FPS of cellular velocity autocovariance function to quantify migration dynamics. The SE introduced here possesses a similar physical interpretation as the Gibbs entropy for thermal systems in that SE naturally reflects the degree of order or randomness of cellular migration, attaining the maximal value of unity for purely diffusive migration (i.e., SE = 1 for the most “random” dynamics) and the minimal value of 0 for purely ballistic dynamics (i.e., SE = 0 for the most “ordered” dynamics). We also find that SE is strongly correlated with the migration persistence but is less sensitive to the migration speed. Moreover, we introduce the time-varying SE based on the WPS of cellular dynamics and demonstrate its superior utility to characterize the time-dependent persistence of cell migration, which typically results from complex and time-varying intra- or extracellular mechanisms. We employ our approach to analyze experimental data of in vitro cell migration regulated by distinct intracellular and extracellular mechanisms, exhibiting a rich spectrum of dynamic characteristics. Our analysis indicates that the SE and wavelet transform (i.e., SE-based approach) offers a simple and efficient tool to quantify cell migration dynamics in complex microenvironment.
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U2 - 10.1016/j.bpj.2021.04.026
DO - 10.1016/j.bpj.2021.04.026
M3 - Article
C2 - 33940024
AN - SCOPUS:85106377381
SN - 0006-3495
VL - 120
SP - 2552
EP - 2565
JO - Biophysical journal
JF - Biophysical journal
IS - 12
ER -