Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions

Dynamic localization of receptors and signaling molecules at the plasma membrane and within intracellular vesicular compartments is crucial for T lymphocyte sensing environmental cues, triggering membrane receptors, recruiting signaling molecules, and fine-tuning of intracellular signals. The orches...

Full description

Bibliographic Details
Main Authors: Marta Mastrogiovanni, Marie Juzans, Andrés Alcover, Vincenzo Di Bartolo
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2020.591348/full
_version_ 1811323685300076544
author Marta Mastrogiovanni
Marta Mastrogiovanni
Marie Juzans
Andrés Alcover
Vincenzo Di Bartolo
author_facet Marta Mastrogiovanni
Marta Mastrogiovanni
Marie Juzans
Andrés Alcover
Vincenzo Di Bartolo
author_sort Marta Mastrogiovanni
collection DOAJ
description Dynamic localization of receptors and signaling molecules at the plasma membrane and within intracellular vesicular compartments is crucial for T lymphocyte sensing environmental cues, triggering membrane receptors, recruiting signaling molecules, and fine-tuning of intracellular signals. The orchestrated action of actin and microtubule cytoskeleton and intracellular vesicle traffic plays a key role in all these events that together ensure important steps in T cell physiology. These include extravasation and migration through lymphoid and peripheral tissues, T cell interactions with antigen-presenting cells, T cell receptor (TCR) triggering by cognate antigen–major histocompatibility complex (MHC) complexes, immunological synapse formation, cell activation, and effector functions. Cytoskeletal and vesicle traffic dynamics and their interplay are coordinated by a variety of regulatory molecules. Among them, polarity regulators and membrane–cytoskeleton linkers are master controllers of this interplay. Here, we review the various ways the T cell plasma membrane, receptors, and their signaling machinery interplay with the actin and microtubule cytoskeleton and with intracellular vesicular compartments. We highlight the importance of this fine-tuned crosstalk in three key stages of T cell biology involving cell polarization: T cell migration in response to chemokines, immunological synapse formation in response to antigen cues, and effector functions. Finally, we discuss two examples of perturbation of this interplay in pathological settings, such as HIV-1 infection and mutation of the polarity regulator and tumor suppressor adenomatous polyposis coli (Apc) that leads to familial polyposis and colorectal cancer.
first_indexed 2024-04-13T13:59:35Z
format Article
id doaj.art-456c92c9032348ce971e9ec4146a403e
institution Directory Open Access Journal
issn 2296-634X
language English
last_indexed 2024-04-13T13:59:35Z
publishDate 2020-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cell and Developmental Biology
spelling doaj.art-456c92c9032348ce971e9ec4146a403e2022-12-22T02:44:04ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-10-01810.3389/fcell.2020.591348591348Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector FunctionsMarta Mastrogiovanni0Marta Mastrogiovanni1Marie Juzans2Andrés Alcover3Vincenzo Di Bartolo4Ligue Nationale Contre le Cancer – Equipe Labellisée LIGUE 2018, Lymphocyte Cell Biology Unit, INSERM-U1221, Department of Immunology, Institut Pasteur, Paris, FranceCollège Doctoral, Sorbonne Université, Paris, FranceLigue Nationale Contre le Cancer – Equipe Labellisée LIGUE 2018, Lymphocyte Cell Biology Unit, INSERM-U1221, Department of Immunology, Institut Pasteur, Paris, FranceLigue Nationale Contre le Cancer – Equipe Labellisée LIGUE 2018, Lymphocyte Cell Biology Unit, INSERM-U1221, Department of Immunology, Institut Pasteur, Paris, FranceLigue Nationale Contre le Cancer – Equipe Labellisée LIGUE 2018, Lymphocyte Cell Biology Unit, INSERM-U1221, Department of Immunology, Institut Pasteur, Paris, FranceDynamic localization of receptors and signaling molecules at the plasma membrane and within intracellular vesicular compartments is crucial for T lymphocyte sensing environmental cues, triggering membrane receptors, recruiting signaling molecules, and fine-tuning of intracellular signals. The orchestrated action of actin and microtubule cytoskeleton and intracellular vesicle traffic plays a key role in all these events that together ensure important steps in T cell physiology. These include extravasation and migration through lymphoid and peripheral tissues, T cell interactions with antigen-presenting cells, T cell receptor (TCR) triggering by cognate antigen–major histocompatibility complex (MHC) complexes, immunological synapse formation, cell activation, and effector functions. Cytoskeletal and vesicle traffic dynamics and their interplay are coordinated by a variety of regulatory molecules. Among them, polarity regulators and membrane–cytoskeleton linkers are master controllers of this interplay. Here, we review the various ways the T cell plasma membrane, receptors, and their signaling machinery interplay with the actin and microtubule cytoskeleton and with intracellular vesicular compartments. We highlight the importance of this fine-tuned crosstalk in three key stages of T cell biology involving cell polarization: T cell migration in response to chemokines, immunological synapse formation in response to antigen cues, and effector functions. Finally, we discuss two examples of perturbation of this interplay in pathological settings, such as HIV-1 infection and mutation of the polarity regulator and tumor suppressor adenomatous polyposis coli (Apc) that leads to familial polyposis and colorectal cancer.https://www.frontiersin.org/articles/10.3389/fcell.2020.591348/fullTCRsignaling moleculesactinmicrotubulesmolecular transportHIV-1
spellingShingle Marta Mastrogiovanni
Marta Mastrogiovanni
Marie Juzans
Andrés Alcover
Vincenzo Di Bartolo
Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
Frontiers in Cell and Developmental Biology
TCR
signaling molecules
actin
microtubules
molecular transport
HIV-1
title Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
title_full Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
title_fullStr Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
title_full_unstemmed Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
title_short Coordinating Cytoskeleton and Molecular Traffic in T Cell Migration, Activation, and Effector Functions
title_sort coordinating cytoskeleton and molecular traffic in t cell migration activation and effector functions
topic TCR
signaling molecules
actin
microtubules
molecular transport
HIV-1
url https://www.frontiersin.org/articles/10.3389/fcell.2020.591348/full
work_keys_str_mv AT martamastrogiovanni coordinatingcytoskeletonandmoleculartrafficintcellmigrationactivationandeffectorfunctions
AT martamastrogiovanni coordinatingcytoskeletonandmoleculartrafficintcellmigrationactivationandeffectorfunctions
AT mariejuzans coordinatingcytoskeletonandmoleculartrafficintcellmigrationactivationandeffectorfunctions
AT andresalcover coordinatingcytoskeletonandmoleculartrafficintcellmigrationactivationandeffectorfunctions
AT vincenzodibartolo coordinatingcytoskeletonandmoleculartrafficintcellmigrationactivationandeffectorfunctions