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Article ; Online: The spatio-temporal control of effector T cell migration.

Fowell, Deborah J / Kim, Minsoo

2021 Volume 21, Issue 9, Page(s) 582–596

Abstract: Effector T cells leave the lymph nodes armed with specialized functional attributes. Their antigenic targets may be located anywhere in the body, posing the ultimate challenge: how to efficiently identify the target tissue, navigate through a complex ... ...

Abstract	Effector T cells leave the lymph nodes armed with specialized functional attributes. Their antigenic targets may be located anywhere in the body, posing the ultimate challenge: how to efficiently identify the target tissue, navigate through a complex tissue matrix and, ultimately, locate the immunological insult. Recent advances in real-time in situ imaging of effector T cell migratory behaviour have revealed a great degree of mechanistic plasticity that enables effector T cells to push and squeeze their way through inflamed tissues. This process is shaped by an array of 'stop' and 'go' guidance signals including target antigens, chemokines, integrin ligands and the mechanical cues of the inflamed microenvironment. Effector T cells must sense and interpret these competing signals to correctly position themselves to mediate their effector functions for complete and durable responses in infectious disease and malignancy. Tuning T cell migration therapeutically will require a new understanding of this complex decision-making process.
MeSH term(s)	Animals ; Biomechanical Phenomena ; Cell Movement/immunology ; Cell Movement/physiology ; Computer Systems ; Humans ; Imaging, Three-Dimensional ; Inflammation/immunology ; Integrins/immunology ; Intravital Microscopy ; Ligands ; Models, Immunological ; Signal Transduction/immunology ; Spatio-Temporal Analysis ; T-Lymphocytes/immunology ; T-Lymphocytes/physiology
Chemical Substances	Integrins ; Ligands
Language	English
Publishing date	2021-02-24
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2062776-2
ISSN	1474-1741 ; 1474-1733
ISSN (online)	1474-1741
ISSN	1474-1733
DOI	10.1038/s41577-021-00507-0
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Article ; Online: CCR7 fuels and LFA-1 grips.

Oakes, Patrick W / Fowell, Deborah J

Nature immunology

2019 Volume 19, Issue 6, Page(s) 516–518

MeSH term(s)	Actins ; Chemokines ; Friction ; Lymphocyte Function-Associated Antigen-1 ; T-Lymphocytes
Chemical Substances	Actins ; Chemokines ; Lymphocyte Function-Associated Antigen-1
Language	English
Publishing date	2019-02-12
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-018-0118-y
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Zs.MG 42: Show issues

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Article: T cells Use Focal Adhesions to Pull Themselves Through Confined Environments.

Caillier, Alexia / Oleksyn, David / Fowell, Deborah J / Miller, Jim / Oakes, Patrick W

bioRxiv : the preprint server for biology

2023

Abstract: Immune cells are highly dynamic and able to migrate through environments with diverse biochemical and mechanical composition. Their migration has classically been defined as amoeboid under the assumption that it is integrin-independent. Here we show that ...

Abstract	Immune cells are highly dynamic and able to migrate through environments with diverse biochemical and mechanical composition. Their migration has classically been defined as amoeboid under the assumption that it is integrin-independent. Here we show that activated primary Th1 T cells require both confinement and extracellular matrix protein to migrate efficiently. This migration is mediated through small and dynamic focal adhesions that are composed of the same proteins associated with canonical mesenchymal focal adhesions, such as integrins, talin, and vinculin. These focal adhesions, furthermore, localize to sites of contractile traction stresses, enabling T cells to pull themselves through confined spaces. Finally, we show that Th1 T cell preferentially follows tracks of other T cells, suggesting that these adhesions are modifying the extracellular matrix to provide additional environmental guidance cues. These results demonstrate not only that the boundaries between amoeboid and mesenchymal migration modes are ambiguous, but that integrin-mediated adhesions play a key role in T cell motility.
Language	English
Publishing date	2023-10-19
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.16.562587
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Article ; Online: Ccr2+ Monocyte-Derived Macrophages Influence Trajectories of Acquired Therapy Resistance in Braf-Mutant Melanoma.

Kim, Dahihm / An, Luye / Moon, Jiwon / Maymi, Viviana I / McGurk, Alexander I / Rudd, Brian D / Fowell, Deborah J / White, Andrew C

Cancer research

2024 Volume 83, Issue 14, Page(s) 2328–2344

Abstract: Therapies targeting oncogene addiction have had a tremendous impact on tumor growth and patient outcome, but drug resistance continues to be problematic. One approach to deal with the challenge of resistance entails extending anticancer treatments beyond ...

Abstract	Therapies targeting oncogene addiction have had a tremendous impact on tumor growth and patient outcome, but drug resistance continues to be problematic. One approach to deal with the challenge of resistance entails extending anticancer treatments beyond targeting cancer cells by additionally altering the tumor microenvironment. Understanding how the tumor microenvironment contributes to the evolution of diverse resistance pathways could aid in the design of sequential treatments that can elicit and take advantage of a predictable resistance trajectory. Tumor-associated macrophages often support neoplastic growth and are frequently the most abundant immune cell found in tumors. Here, we used clinically relevant in vivo Braf-mutant melanoma models with fluorescent markers to track the stage-specific changes in macrophages under targeted therapy with Braf/Mek inhibitors and assessed the dynamic evolution of the macrophage population generated by therapy pressure-induced stress. During the onset of a drug-tolerant persister state, Ccr2+ monocyte-derived macrophage infiltration rose, suggesting that macrophage influx at this point could facilitate the onset of stable drug resistance that melanoma cells show after several weeks of treatment. Comparison of melanomas that develop in a Ccr2-proficient or -deficient microenvironment demonstrated that lack of melanoma infiltrating Ccr2+ macrophages delayed onset of resistance and shifted melanoma cell evolution towards unstable resistance. Unstable resistance was characterized by sensitivity to targeted therapy when factors from the microenvironment were lost. Importantly, this phenotype was reversed by coculturing melanoma cells with Ccr2+ macrophages. Overall, this study demonstrates that the development of resistance may be directed by altering the tumor microenvironment to improve treatment timing and the probability of relapse. Significance: Ccr2+ melanoma macrophages that are active in tumors during the drug-tolerant persister state following targeted therapy-induced regression are key contributors directing melanoma cell reprogramming toward specific therapeutic resistance trajectories.
MeSH term(s)	Humans ; Neoplasm Recurrence, Local ; Melanoma/drug therapy ; Melanoma/genetics ; Melanoma/pathology ; Immunotherapy ; Macrophages/metabolism ; Proto-Oncogene Proteins B-raf ; Drug Resistance, Neoplasm/genetics ; Protein Kinase Inhibitors/pharmacology ; Cell Line, Tumor ; Tumor Microenvironment
Chemical Substances	Proto-Oncogene Proteins B-raf (EC 2.7.11.1) ; Protein Kinase Inhibitors
Language	English
Publishing date	2024-01-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1432-1
ISSN	1538-7445 ; 0008-5472
ISSN (online)	1538-7445
ISSN	0008-5472
DOI	10.1158/0008-5472.CAN-22-2841
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Article ; Online: IL-17-Dependent Dysregulated Cutaneous Immune Homeostasis in the Absence of the Wiskott-Aldrich Syndrome Protein.

Herman, Katherine E / Yoshida, Takeshi / Hughson, Angela / Grier, Alex / Gill, Steven R / Beck, Lisa A / Fowell, Deborah J

Frontiers in immunology

2022 Volume 13, Page(s) 817427

Abstract: Wiskott-Aldrich Syndrome (WAS) is characterized by recurrent infections, thrombocytopenia, and eczema. Here, we show that WASp-deficient mice on a BALB/c background have dysregulated cutaneous immune homeostasis with increased leukocyte accumulation in ... ...

Abstract	Wiskott-Aldrich Syndrome (WAS) is characterized by recurrent infections, thrombocytopenia, and eczema. Here, we show that WASp-deficient mice on a BALB/c background have dysregulated cutaneous immune homeostasis with increased leukocyte accumulation in the skin, 1 week after birth. Increased cutaneous inflammation was associated with epithelial abnormalities, namely, altered keratinization, abnormal epidermal tight junctional morphology and increased trans-epidermal water loss; consistent with epidermal barrier dysfunction. Immune and physical barrier disruption was accompanied by progressive skin dysbiosis, highlighting the functional significance of the disrupted cutaneous homeostasis. Interestingly, the dysregulated immunity in the skin preceded the systemic elevation in IgE and lymphocytic infiltration of the colonic lamina propria associated with WASp deficiency. Mechanistically, the enhanced immune cell accumulation in the skin was lymphocyte dependent. Elevated levels of both Type 2 (IL-4, IL-5) and Type 17 (IL-17, IL-22, IL-23) cytokines were present in the skin, as well as the 'itch' factor IL-31. Unexpectedly, the canonical WAS-associated cytokine IL-4 did not play a role in the immune dysfunction. Instead, IL-17 was critical for skin immune infiltration and elevation of both Type 2 and Type 17 cytokines. Our findings reveal a previously unrecognized IL-17-dependent breakdown in immune homeostasis and cutaneous barrier integrity in the absence of WASp, targeting of which may provide new therapeutic possibilities for the treatment of skin pathologies in WAS patients.
MeSH term(s)	Animals ; Cytokines ; Homeostasis ; Interleukin-17 ; Interleukin-4 ; Mice ; Mice, Knockout ; Wiskott-Aldrich Syndrome/genetics ; Wiskott-Aldrich Syndrome Protein/genetics
Chemical Substances	Cytokines ; Il17a protein, mouse ; Interleukin-17 ; Wiskott-Aldrich Syndrome Protein ; Interleukin-4 (207137-56-2)
Language	English
Publishing date	2022-02-21
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.817427
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Article ; Online: Signals for the execution of Th2 effector function.

Fowell, Deborah J

Cytokine

2009 Volume 46, Issue 1, Page(s) 1–6

Abstract: Appropriate control of infection depends on the generation of lymphocytes armed with a particular array of cytokine and chemokine effector molecules. The differentiation of naïve T cells into functionally distinct effector subsets is regulated by signals ...

Abstract	Appropriate control of infection depends on the generation of lymphocytes armed with a particular array of cytokine and chemokine effector molecules. The differentiation of naïve T cells into functionally distinct effector subsets is regulated by signals from the T cell receptor (TCR) and cytokine receptors. Using gene knock-out approaches, the initiation of discrete effector programs appears differentially sensitive to the loss of individual TCR signaling components; likely due to differences in the transcription factors needed to activate individual cytokine genes. Less well understood however, are the signal requirements for the execution of effector function. With a focus on Th2 cells and the kinase ITK, we review recent observations that point to differences between the signals needed for the initiation and implementation of cytokine programs in CD4+ T cells. Indeed, Th2 effector cells signal differently from both their naïve counterparts and from Th1 effectors suggesting they may transduce activation signals differently or may be selectively receptive to different activation signals. Potential regulation points for effector function lie at the level of transcription and translation of cytokine genes. We also discuss how provision of these execution signals may be spatially segregated in vivo occurring at tissue sites of inflammation and subject to modulation by the pathogen itself.
MeSH term(s)	Animals ; CD4-Positive T-Lymphocytes/metabolism ; Cytokines/metabolism ; Humans ; Immune System ; Inflammation ; Interleukin-4/metabolism ; Ligands ; Lymph Nodes/pathology ; Models, Biological ; Signal Transduction ; Th2 Cells/cytology ; Th2 Cells/metabolism ; Transcription Factors/metabolism
Chemical Substances	Cytokines ; Ligands ; Transcription Factors ; Interleukin-4 (207137-56-2)
Language	English
Publishing date	2009-02-23
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1018055-2
ISSN	1096-0023 ; 1043-4666
ISSN (online)	1096-0023
ISSN	1043-4666
DOI	10.1016/j.cyto.2008.12.023
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Article ; Online: T cell activation niches-Optimizing T cell effector function in inflamed and infected tissues.

Bala, Noor / McGurk, Alexander I / Zilch, Tiago / Rup, Anastasia N / Carter, Evan M / Leddon, Scott A / Fowell, Deborah J

Immunological reviews

2021 Volume 306, Issue 1, Page(s) 164–180

Abstract: Successful immunity to infection, malignancy, and tissue damage requires the coordinated recruitment of numerous immune cell subsets to target tissues. Once within the target tissue, effector T cells rely on local chemotactic cues and structural cues ... ...

Abstract	Successful immunity to infection, malignancy, and tissue damage requires the coordinated recruitment of numerous immune cell subsets to target tissues. Once within the target tissue, effector T cells rely on local chemotactic cues and structural cues from the tissue matrix to navigate the tissue, interact with antigen-presenting cells, and release effector cytokines. This highly dynamic process has been "caught on camera" in situ by intravital multiphoton imaging. Initial studies revealed a surprising randomness to the pattern of T cell migration through inflamed tissues, behavior thought to facilitate chance encounters with rare antigen-bearing cells. Subsequent tissue-wide visualization has uncovered a high degree of spatial preference when it comes to T cell activation. Here, we discuss the basic tenants of a successful effector T cell activation niche, taking cues from the dynamics of Tfh positioning in the lymph node germinal center. In peripheral tissues, steady-state microanatomical organization may direct the location of "pop-up" de novo activation niches, often observed as perivascular clusters, that support early effector T cell activation. These perivascular activation niches appear to be regulated by site-specific chemokines that coordinate the recruitment of dendritic cells and other innate cells for local T cell activation, survival, and optimized effector function.
MeSH term(s)	Antigen-Presenting Cells ; Cell Movement ; Chemokines ; Cytokines ; Humans ; Lymphocyte Activation ; T-Lymphocytes
Chemical Substances	Chemokines ; Cytokines
Language	English
Publishing date	2021-12-02
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	391796-4
ISSN	1600-065X ; 0105-2896
ISSN (online)	1600-065X
ISSN	0105-2896
DOI	10.1111/imr.13047
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Article ; Online: Imaging CD4 T Cell Interstitial Migration in the Inflamed Dermis.

Gaylo, Alison / Overstreet, Michael G / Fowell, Deborah J

Journal of visualized experiments : JoVE

2016 , Issue 109, Page(s) e53585

Abstract: The ability of CD4 T cells to carry out effector functions is dependent upon the rapid and efficient migration of these cells in inflamed peripheral tissues through an as-yet undefined mechanism. The application of multiphoton microscopy to the study of ... ...

Abstract	The ability of CD4 T cells to carry out effector functions is dependent upon the rapid and efficient migration of these cells in inflamed peripheral tissues through an as-yet undefined mechanism. The application of multiphoton microscopy to the study of the immune system provides a tool to measure the dynamics of immune responses within intact tissues. Here we present a protocol for non-invasive intravital multiphoton imaging of CD4 T cells in the inflamed mouse ear dermis. Use of a custom imaging platform and a venous catheter allows for the visualization of CD4 T cell dynamics in the dermal interstitium, with the ability to interrogate these cells in real-time via the addition of blocking antibodies to key molecular components involved in motility. This system provides advantages over both in vitro models and surgically invasive imaging procedures. Understanding the pathways used by CD4 T cells for motility may ultimately provide insight into the basic function of CD4 T cells as well as the pathogenesis of both autoimmune diseases and pathology from chronic infections.
MeSH term(s)	Animals ; CD4-Positive T-Lymphocytes/immunology ; Cell Movement ; Dermis/immunology ; Dermis/pathology ; Ear/pathology ; Inflammation/immunology ; Intravital Microscopy/methods ; Mice ; Microscopy, Fluorescence, Multiphoton/methods
Language	English
Publishing date	2016-03-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/53585
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Article ; Online: CD4

Fernandes, Ninoshka R J / Reilly, Nicholas S / Schrock, Dillon C / Hocking, Denise C / Oakes, Patrick W / Fowell, Deborah J

Frontiers in immunology

2020 Volume 11, Page(s) 1501

Abstract: The extracellular matrix (ECM) is extensively remodeled during inflammation providing essential guidance cues for immune cell migration and signals for cell activation and survival. There is increasing interest in the therapeutic targeting of ECM to ... ...

Abstract	The extracellular matrix (ECM) is extensively remodeled during inflammation providing essential guidance cues for immune cell migration and signals for cell activation and survival. There is increasing interest in the therapeutic targeting of ECM to mitigate chronic inflammatory diseases and enhance access to the tumor microenvironment. T cells utilize the ECM as a scaffold for interstitial migration, dependent on T cell expression of matrix-binding integrins α
MeSH term(s)	Adoptive Transfer ; Animals ; CD4-Positive T-Lymphocytes/immunology ; Cell Movement ; Cells, Cultured ; Extracellular Matrix/immunology ; Extracellular Matrix/metabolism ; Fibronectins/chemistry ; Fibronectins/immunology ; Fibronectins/metabolism ; Inflammation ; Intestinal Mucosa/immunology ; Mice ; Mice, Inbred BALB C ; Mice, Transgenic ; Peptide Fragments/administration & dosage ; Polymerization ; Receptors, Antigen, T-Cell/genetics ; Skin/immunology
Chemical Substances	Fibronectins ; Peptide Fragments ; Receptors, Antigen, T-Cell ; pUR4 peptide
Language	English
Publishing date	2020-07-24
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2020.01501
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Article: Hyperspectral multiphoton microscopy for

Bares, Amanda J / Mejooli, Menansili A / Pender, Mitchell A / Leddon, Scott A / Tilley, Steven / Lin, Karen / Dong, Jingyuan / Kim, Minsoo / Fowell, Deborah J / Nishimura, Nozomi / Schaffer, Chris B

Optica

2021 Volume 7, Issue 11, Page(s) 1587–1601

Abstract: The insensitivity of multiphoton microscopy to optical scattering enables high-resolution, high-contrast imaging deep into tissue, including in live animals. Scattering does, however, severely limit the use of spectral dispersion techniques to improve ... ...

Abstract	The insensitivity of multiphoton microscopy to optical scattering enables high-resolution, high-contrast imaging deep into tissue, including in live animals. Scattering does, however, severely limit the use of spectral dispersion techniques to improve spectral resolution. In practice, this limited spectral resolution together with the need for multiple excitation wavelengths to excite different fluorophores limits multiphoton microscopy to imaging a few, spectrally-distinct fluorescent labels at a time, restricting the complexity of biological processes that can be studied. Here, we demonstrate a hyperspectral multiphoton microscope that utilizes three different wavelength excitation sources together with multiplexed fluorescence emission detection using angle-tuned bandpass filters. This microscope maintains scattering insensitivity, while providing high enough spectral resolution on the emitted fluorescence and capitalizing on the wavelength-dependent nonlinear excitation of fluorescent dyes to enable clean separation of multiple, spectrally overlapping labels,
Language	English
Publishing date	2021-04-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	2779175-0
ISSN	2334-2536
ISSN	2334-2536
DOI	10.1364/optica.389982
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