An adhesion-dependent switch between mechanisms that determine motile cell shape

Erin L. Barnhart, Kun Chun Lee, Kinneret Keren, Alex Mogilner, Julie A. Theriot

Research output: Contribution to journalArticle

159 Citations (Scopus)

Abstract

Keratocytes are fast-moving cells in which adhesion dynamics are tightly coupled to the actin polymerization motor that drives migration, resulting in highly coordinated cell movement. We have found that modifying the adhesive properties of the underlying substrate has a dramatic effect on keratocyte morphology. Cells crawling at intermediate adhesion strengths resembled stereotypical keratocytes, characterized by a broad, fan-shaped lamellipodium, clearly defined leading and trailing edges, and persistent rates of protrusion and retraction. Cells at low adhesion strength were small and round with highly variable protrusion and retraction rates, and cells at high adhesion strength were large and asymmetrical and, strikingly, exhibited traveling waves of protrusion. To elucidate the mechanisms by which adhesion strength determines cell behavior, we examined the organization of adhesions, myosin II, and the actin network in keratocytes migrating on substrates with different adhesion strengths. On the whole, our results are consistent with a quantitative physical model in which keratocyte shape and migratory behavior emerge from the self-organization of actin, adhesions, and myosin, and quantitative changes in either adhesion strength or myosin contraction can switch keratocytes among qualitatively distinct migration regimes.

Original languageEnglish (US)
Article numbere1001059
JournalPLoS Biology
Volume9
Issue number5
DOIs
StatePublished - May 2011

Fingerprint

Cell Shape
Bond strength (materials)
adhesion
Adhesion
Switches
Actins
Myosins
myosin
cells
actin
Myosin Type II
Pseudopodia
Polymerization
Adhesives
Cell Movement
Substrates
pseudopodia
Fans
physical models
fans (equipment)

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Barnhart, E. L., Lee, K. C., Keren, K., Mogilner, A., & Theriot, J. A. (2011). An adhesion-dependent switch between mechanisms that determine motile cell shape. PLoS Biology, 9(5), [e1001059]. https://doi.org/10.1371/journal.pbio.1001059

An adhesion-dependent switch between mechanisms that determine motile cell shape. / Barnhart, Erin L.; Lee, Kun Chun; Keren, Kinneret; Mogilner, Alex; Theriot, Julie A.

In: PLoS Biology, Vol. 9, No. 5, e1001059, 05.2011.

Research output: Contribution to journalArticle

Barnhart, EL, Lee, KC, Keren, K, Mogilner, A & Theriot, JA 2011, 'An adhesion-dependent switch between mechanisms that determine motile cell shape', PLoS Biology, vol. 9, no. 5, e1001059. https://doi.org/10.1371/journal.pbio.1001059
Barnhart, Erin L. ; Lee, Kun Chun ; Keren, Kinneret ; Mogilner, Alex ; Theriot, Julie A. / An adhesion-dependent switch between mechanisms that determine motile cell shape. In: PLoS Biology. 2011 ; Vol. 9, No. 5.
@article{a7e78e8b92c743ea8fb7bacc3dec4416,
title = "An adhesion-dependent switch between mechanisms that determine motile cell shape",
abstract = "Keratocytes are fast-moving cells in which adhesion dynamics are tightly coupled to the actin polymerization motor that drives migration, resulting in highly coordinated cell movement. We have found that modifying the adhesive properties of the underlying substrate has a dramatic effect on keratocyte morphology. Cells crawling at intermediate adhesion strengths resembled stereotypical keratocytes, characterized by a broad, fan-shaped lamellipodium, clearly defined leading and trailing edges, and persistent rates of protrusion and retraction. Cells at low adhesion strength were small and round with highly variable protrusion and retraction rates, and cells at high adhesion strength were large and asymmetrical and, strikingly, exhibited traveling waves of protrusion. To elucidate the mechanisms by which adhesion strength determines cell behavior, we examined the organization of adhesions, myosin II, and the actin network in keratocytes migrating on substrates with different adhesion strengths. On the whole, our results are consistent with a quantitative physical model in which keratocyte shape and migratory behavior emerge from the self-organization of actin, adhesions, and myosin, and quantitative changes in either adhesion strength or myosin contraction can switch keratocytes among qualitatively distinct migration regimes.",
author = "Barnhart, {Erin L.} and Lee, {Kun Chun} and Kinneret Keren and Alex Mogilner and Theriot, {Julie A.}",
year = "2011",
month = "5",
doi = "10.1371/journal.pbio.1001059",
language = "English (US)",
volume = "9",
journal = "PLoS Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "5",

}

TY - JOUR

T1 - An adhesion-dependent switch between mechanisms that determine motile cell shape

AU - Barnhart, Erin L.

AU - Lee, Kun Chun

AU - Keren, Kinneret

AU - Mogilner, Alex

AU - Theriot, Julie A.

PY - 2011/5

Y1 - 2011/5

N2 - Keratocytes are fast-moving cells in which adhesion dynamics are tightly coupled to the actin polymerization motor that drives migration, resulting in highly coordinated cell movement. We have found that modifying the adhesive properties of the underlying substrate has a dramatic effect on keratocyte morphology. Cells crawling at intermediate adhesion strengths resembled stereotypical keratocytes, characterized by a broad, fan-shaped lamellipodium, clearly defined leading and trailing edges, and persistent rates of protrusion and retraction. Cells at low adhesion strength were small and round with highly variable protrusion and retraction rates, and cells at high adhesion strength were large and asymmetrical and, strikingly, exhibited traveling waves of protrusion. To elucidate the mechanisms by which adhesion strength determines cell behavior, we examined the organization of adhesions, myosin II, and the actin network in keratocytes migrating on substrates with different adhesion strengths. On the whole, our results are consistent with a quantitative physical model in which keratocyte shape and migratory behavior emerge from the self-organization of actin, adhesions, and myosin, and quantitative changes in either adhesion strength or myosin contraction can switch keratocytes among qualitatively distinct migration regimes.

AB - Keratocytes are fast-moving cells in which adhesion dynamics are tightly coupled to the actin polymerization motor that drives migration, resulting in highly coordinated cell movement. We have found that modifying the adhesive properties of the underlying substrate has a dramatic effect on keratocyte morphology. Cells crawling at intermediate adhesion strengths resembled stereotypical keratocytes, characterized by a broad, fan-shaped lamellipodium, clearly defined leading and trailing edges, and persistent rates of protrusion and retraction. Cells at low adhesion strength were small and round with highly variable protrusion and retraction rates, and cells at high adhesion strength were large and asymmetrical and, strikingly, exhibited traveling waves of protrusion. To elucidate the mechanisms by which adhesion strength determines cell behavior, we examined the organization of adhesions, myosin II, and the actin network in keratocytes migrating on substrates with different adhesion strengths. On the whole, our results are consistent with a quantitative physical model in which keratocyte shape and migratory behavior emerge from the self-organization of actin, adhesions, and myosin, and quantitative changes in either adhesion strength or myosin contraction can switch keratocytes among qualitatively distinct migration regimes.

UR - http://www.scopus.com/inward/record.url?scp=79958046639&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79958046639&partnerID=8YFLogxK

U2 - 10.1371/journal.pbio.1001059

DO - 10.1371/journal.pbio.1001059

M3 - Article

C2 - 21559321

AN - SCOPUS:79958046639

VL - 9

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 5

M1 - e1001059

ER -