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On the mechanism of long-range orientational order of fibroblasts

Xuefei Li, Rajesh Balagam, Ting-Fang He, Peter P. Lee, Oleg A. Igoshin, Herbert Levine
doi: https://doi.org/10.1101/119669
Xuefei Li
aCenter for Theoretical Biological Physics, Rice University, 6500 Main Street, Houston Texas 77030, USA
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Rajesh Balagam
bDepartment of Bioengineering, Rice University, 6500 Main Street, Houston Texas 77030, USA
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Ting-Fang He
cImmuno-Oncology, City of Hope Comprehensive Cancer Center, 1500 East Duarte Road, Duarte, CA 91010, USA
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Peter P. Lee
cImmuno-Oncology, City of Hope Comprehensive Cancer Center, 1500 East Duarte Road, Duarte, CA 91010, USA
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Oleg A. Igoshin
aCenter for Theoretical Biological Physics, Rice University, 6500 Main Street, Houston Texas 77030, USA
bDepartment of Bioengineering, Rice University, 6500 Main Street, Houston Texas 77030, USA
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  • For correspondence: igoshin@rice.edu herbert.levine@rice.edu
Herbert Levine
aCenter for Theoretical Biological Physics, Rice University, 6500 Main Street, Houston Texas 77030, USA
bDepartment of Bioengineering, Rice University, 6500 Main Street, Houston Texas 77030, USA
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  • For correspondence: igoshin@rice.edu herbert.levine@rice.edu
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Abstract

Long-range alignment ordering of fibroblasts have been observed in the vicinity of cancerous tumors and can be recapitulated with in vitro experiments. However, the mechanisms driving their ordering are not understood. Here we show that local collision-driven nematic alignment interactions among fibroblasts are insufficient to explain observed long-range alignment. One possibility is that there exists another orientation field co-evolving with the cells and reinforcing their alignment. We propose that this field reflects the mechanical cross-talk between the fibroblasts and the underlying fibrous material on which they move. We demonstrate that this new long-range interaction can give rise to high nematic order and to the observed patterning of the cancer microenvironment.

Significance Statement Long-range alignment patterns of fibroblasts have been observed both in vivo and in vitro. However, there has not been much understanding of the underlying mechanism. In this work, we demonstrate that these patterns cannot be simply explained by their steric interaction with one another during collisions. Instead, we propose that fibroblasts may collectively align through non-local interactions arising from their modification of an underlying extracellular matrix. The proposed mechanism explains the observed co-alignment between fibroblasts and collagen fibers around tumors and can be be tested in future experiments that can image the dynamics of this pattern formation in vivo or in vitro

Footnotes

  • X.L., R.B., O.A.I., and H.L. designed research; X.L., R.B. and T.H. performed research; and all authors wrote the paper.

  • We declare no conflict of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted July 10, 2017.
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On the mechanism of long-range orientational order of fibroblasts
Xuefei Li, Rajesh Balagam, Ting-Fang He, Peter P. Lee, Oleg A. Igoshin, Herbert Levine
bioRxiv 119669; doi: https://doi.org/10.1101/119669
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On the mechanism of long-range orientational order of fibroblasts
Xuefei Li, Rajesh Balagam, Ting-Fang He, Peter P. Lee, Oleg A. Igoshin, Herbert Levine
bioRxiv 119669; doi: https://doi.org/10.1101/119669

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