Linking morphodynamics and directional persistence of T lymphocyte migration

Xiaji Liu, Erik S. Welf, Jason M. Haugh

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

T cells play a central role in the adaptive immune response, and their directed migration is essential for homing to sites of antigen presentation. Like neutrophils, T lymphocytes are rapidly moving cells that exhibit amoeboid movement, characterized by a definitive polarity with F-actin concentrated at the front and myosin II elsewhere. In this study, we used total internal reflection fluorescence (TIRF) microscopy to monitor the cells' areas of contact with a surface presenting adhesive ICAM-1 and the chemokine, CXCL12/ SDF-1. Our analysis reveals that T-cell migration and reorientation are achieved by bifurcation and lateral separation of protrusions along the leading membrane edge, followed by cessation of one of the protrusions, which acts as a pivot for cell turning. We show that the distribution of bifurcation frequencies exhibits characteristics of a random, spontaneous process; yet, the waiting time between bifurcation events depends on whether or not the pivot point remains on the same side of the migration axis. Our analysis further suggests that switching of the dominant protrusion between the two sides of the migration axis is associated with persistent migration, whereas the opposite is true of cell turning. To help explain the bifurcation phenomenon and how distinct migration behaviours might arise, a spatio-temporal, stochastic model describing F-actin dynamics is offered.

Original languageEnglish (US)
Article number20141412
JournalJournal of the Royal Society Interface
Volume12
Issue number106
DOIs
StatePublished - May 6 2015

Fingerprint

T-cells
T-Lymphocytes
Actins
Myosin Type II
Chemokine CXCL12
Fluorescence microscopy
Intercellular Adhesion Molecule-1
Stochastic models
Antigens
Adhesives
Antigen Presentation
Adaptive Immunity
Fluorescence Microscopy
Cell Movement
Membranes
Neutrophils

Keywords

  • Cell migration
  • Chemokine
  • Image analysis
  • TIRF microscopy

ASJC Scopus subject areas

  • Biotechnology
  • Bioengineering
  • Biophysics
  • Biochemistry
  • Biomaterials
  • Biomedical Engineering

Cite this

Linking morphodynamics and directional persistence of T lymphocyte migration. / Liu, Xiaji; Welf, Erik S.; Haugh, Jason M.

In: Journal of the Royal Society Interface, Vol. 12, No. 106, 20141412, 06.05.2015.

Research output: Contribution to journalArticle

@article{cd8c57b725334b36a9f65c20cc7271a8,
title = "Linking morphodynamics and directional persistence of T lymphocyte migration",
abstract = "T cells play a central role in the adaptive immune response, and their directed migration is essential for homing to sites of antigen presentation. Like neutrophils, T lymphocytes are rapidly moving cells that exhibit amoeboid movement, characterized by a definitive polarity with F-actin concentrated at the front and myosin II elsewhere. In this study, we used total internal reflection fluorescence (TIRF) microscopy to monitor the cells' areas of contact with a surface presenting adhesive ICAM-1 and the chemokine, CXCL12/ SDF-1. Our analysis reveals that T-cell migration and reorientation are achieved by bifurcation and lateral separation of protrusions along the leading membrane edge, followed by cessation of one of the protrusions, which acts as a pivot for cell turning. We show that the distribution of bifurcation frequencies exhibits characteristics of a random, spontaneous process; yet, the waiting time between bifurcation events depends on whether or not the pivot point remains on the same side of the migration axis. Our analysis further suggests that switching of the dominant protrusion between the two sides of the migration axis is associated with persistent migration, whereas the opposite is true of cell turning. To help explain the bifurcation phenomenon and how distinct migration behaviours might arise, a spatio-temporal, stochastic model describing F-actin dynamics is offered.",
keywords = "Cell migration, Chemokine, Image analysis, TIRF microscopy",
author = "Xiaji Liu and Welf, {Erik S.} and Haugh, {Jason M.}",
year = "2015",
month = "5",
day = "6",
doi = "10.1098/rsif.2014.1412",
language = "English (US)",
volume = "12",
journal = "Journal of the Royal Society Interface",
issn = "1742-5689",
publisher = "Royal Society of London",
number = "106",

}

TY - JOUR

T1 - Linking morphodynamics and directional persistence of T lymphocyte migration

AU - Liu, Xiaji

AU - Welf, Erik S.

AU - Haugh, Jason M.

PY - 2015/5/6

Y1 - 2015/5/6

N2 - T cells play a central role in the adaptive immune response, and their directed migration is essential for homing to sites of antigen presentation. Like neutrophils, T lymphocytes are rapidly moving cells that exhibit amoeboid movement, characterized by a definitive polarity with F-actin concentrated at the front and myosin II elsewhere. In this study, we used total internal reflection fluorescence (TIRF) microscopy to monitor the cells' areas of contact with a surface presenting adhesive ICAM-1 and the chemokine, CXCL12/ SDF-1. Our analysis reveals that T-cell migration and reorientation are achieved by bifurcation and lateral separation of protrusions along the leading membrane edge, followed by cessation of one of the protrusions, which acts as a pivot for cell turning. We show that the distribution of bifurcation frequencies exhibits characteristics of a random, spontaneous process; yet, the waiting time between bifurcation events depends on whether or not the pivot point remains on the same side of the migration axis. Our analysis further suggests that switching of the dominant protrusion between the two sides of the migration axis is associated with persistent migration, whereas the opposite is true of cell turning. To help explain the bifurcation phenomenon and how distinct migration behaviours might arise, a spatio-temporal, stochastic model describing F-actin dynamics is offered.

AB - T cells play a central role in the adaptive immune response, and their directed migration is essential for homing to sites of antigen presentation. Like neutrophils, T lymphocytes are rapidly moving cells that exhibit amoeboid movement, characterized by a definitive polarity with F-actin concentrated at the front and myosin II elsewhere. In this study, we used total internal reflection fluorescence (TIRF) microscopy to monitor the cells' areas of contact with a surface presenting adhesive ICAM-1 and the chemokine, CXCL12/ SDF-1. Our analysis reveals that T-cell migration and reorientation are achieved by bifurcation and lateral separation of protrusions along the leading membrane edge, followed by cessation of one of the protrusions, which acts as a pivot for cell turning. We show that the distribution of bifurcation frequencies exhibits characteristics of a random, spontaneous process; yet, the waiting time between bifurcation events depends on whether or not the pivot point remains on the same side of the migration axis. Our analysis further suggests that switching of the dominant protrusion between the two sides of the migration axis is associated with persistent migration, whereas the opposite is true of cell turning. To help explain the bifurcation phenomenon and how distinct migration behaviours might arise, a spatio-temporal, stochastic model describing F-actin dynamics is offered.

KW - Cell migration

KW - Chemokine

KW - Image analysis

KW - TIRF microscopy

UR - http://www.scopus.com/inward/record.url?scp=84929483892&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84929483892&partnerID=8YFLogxK

U2 - 10.1098/rsif.2014.1412

DO - 10.1098/rsif.2014.1412

M3 - Article

VL - 12

JO - Journal of the Royal Society Interface

JF - Journal of the Royal Society Interface

SN - 1742-5689

IS - 106

M1 - 20141412

ER -