Analysis of Shear Flow-induced Migration of Murine Marginal Zone B Cells In Vitro

Tedford, Kerry; Tech, Laura; Steiner, Michael; Korthals, Mark; Fischer, Klaus–Dieter

doi:10.3791/58759

Cited by 2 publications

(4 citation statements)

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“…Although the individual steps of the leukocyte adhesion cascade have been studied extensively (1,2,42-44), we have been intrigued by the recent discovery that several immune cell subsets and tumor cells are able to crawl efficiently against the direction of shear slow. Our laboratory and others have demonstrated that both murine and human T lymphocytes (17,45), human HSPCs (23), and murine marginal zone B cells (21,22) are able to efficiently crawl against the direction of shear flow on ICAM-1 surfaces and surfaces coated with mixtures of ICAM-1 and VCAM-1 but maintain a preference for downstream migration on VCAM-1 surfaces (20,45). In all immune cells that show upstream migration, migration against the direction of shear flow was is dependent on LFA-1/ICAM-1 interactions (16,17,(19)(20)(21)23).…”

Section: Discussionmentioning

confidence: 97%

“…The biological function of upstream migration is still unknown, but we have some clues as to its function from other types of cells displaying this mode of motility. Marginal zone B cells will crawl upstream on ICAM-1, against the blood flow that goes from the follicle to the red pulp in the spleen, when leaving the marginal zone to enter the follicle for further maturation (21,22). Furthermore, human breast cancer cells are able to migrate against direction of interstitial shear flow in a three-dimensional collagen gel to escape into the leaky vasculature and metastasize further (51,52).…”

Section: Discussionmentioning

confidence: 99%

“…The Theodoly laboratory and our laboratory established that CD4 þ T lymphocytes crawl upstream on ICAM-1 surfaces and downstream on VCAM-1 surfaces and our laboratory demonstrated that T cells crawling upstream are able transmigrate faster through the endothelium (16)(17)(18)(19)(20). It has since been shown that marginal zone B cells will crawl upstream on ICAM-1, against the blood flow, to leave the marginal zone and enter the follicle in the spleen (21,22). Our laboratory recently showed that hematopoietic stem and progenitor cells (HSPCs), although homing to the bone marrow post-transplantation, can migrate upstream on pure ICAM-1 surfaces, mixtures of ICAM-1 and VCAM-1, and stimulated human umbilical vein endothelial cells (HUVECs), but crawl primarily downstream on surfaces of VCAM-1 only (23).…”

Section: Introductionmentioning

confidence: 93%

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Human Neutrophils Will Crawl Upstream on ICAM-1 If Mac-1 Is Blocked

Buffone

Anderson

Hammer

2019

Biophysical Journal

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The recruitment of neutrophils to sites of inflammatory insult is a hallmark of the innate immune response. Neutrophil recruitment is regulated by a multistep process that includes cell rolling, activation, adhesion, and transmigration through the endothelium commonly referred to as the leukocyte adhesion cascade. After selectin-mediated braking, neutrophils migrate along the activated vascular endothelium on which ligands, including intercellular adhesion molecule-1 (ICAM-1) and vascular cell adhesion molecule-1 (VCAM-1), are expressed. Previous studies have shown that two cells that commonly home from blood vessel to tissue-T cells and hematopoietic stem and progenitor cells-use the integrin lymphocyte functional antigen-1 (LFA-1) to migrate against the direction of shear flow once adherent on ICAM-1 surfaces. Like T cells and hematopoietic stem and progenitor cells, neutrophils express LFA-1, but they also express macrophage-1 antigen (Mac-1), which binds to ICAM-1. Previous reports have shown that neutrophils will not migrate against the direction of flow on ICAM-1, but we hypothesized this was due to the influence of Mac-1. Here, we report that both the HL-60 neutrophil-like cell line and primary human neutrophils can migrate against the direction of fluid flow on ICAM-1 surfaces via LFA-1 if Mac-1 is blocked; otherwise, they migrate downstream. We demonstrate this both on ICAM-1 surfaces and on activated endothelium. In sum, both LFA-1 and Mac-1 binding ICAM-1 play a critical role in determining the direction of neutrophil migration along the endothelium, and their interaction may play an important role in controlling neutrophil trafficking during inflammation.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 93%

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Human Neutrophils Will Crawl Upstream on ICAM-1 If Mac-1 Is Blocked

Buffone

Anderson

Hammer

2019

Biophysical Journal

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“…Splenic endothelial cells express both ICAM-1 and VCAM-1 (Ulyanova et al, 2005), and the shear flow acts as a mechanotransducer to activate both LFA-1 and VLA-4 on the MZBs. MZBs crawl upstream on ICAM-1 and mixed ICAM-1/ VCAM-1 surfaces and downstream on VCAM-1 surfaces (Tedford et al, 2017;Tedford et al, 2018). The expression of CXCL13 and Mucosal Vascular Addressin Cellular Adhesion Molecule (MAdCAM-1) in blood vessels retards the upstream migration.…”

Section: Upstream Migration Observed In Other Cell Typesmentioning

confidence: 99%

Not all (cells) who wander are lost: Upstream migration as a pervasive mode of amoeboid cell motility

Buffone,

Hammer,

Kim

et al. 2023

Front. Cell Dev. Biol.

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Leukocytes possess the ability to migrate upstream—against the direction of flow—on surfaces of specific chemistry. Upstream migration was first characterized in vitro for T-cells on surfaces comprised of intracellular adhesion molecule-1 (ICAM-1). Upstream migration occurs when the integrin receptor αLβ2 (also known as lymphocyte function-associated antigen-1, or LFA-1) binds to ICAM-1. LFA-1/ICAM-1 interactions are ubiquitous and are widely found in leukocyte trafficking. Upstream migration would be employed after cells come to arrest on the apical surface of the endothelium and might confer an advantage for both trans-endothelial migration and tissue surveillance. It has now been shown that several other motile amoeboid cells which have the responsibility of trafficking from blood vessels into tissues, such as Marginal zone B cells, hematopoietic stem cells, and neutrophils (when macrophage-1 antigen, Mac-1, is blocked), can also migrate upstream on ICAM-1 surfaces. This review will summarize what is known about the basic mechanisms of upstream migration, which cells have displayed this phenomenon, and the possible role of upstream migration in physiology and tissue homeostasis.

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Analysis of Shear Flow-induced Migration of Murine Marginal Zone B Cells In Vitro

Cited by 2 publications

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Human Neutrophils Will Crawl Upstream on ICAM-1 If Mac-1 Is Blocked

Human Neutrophils Will Crawl Upstream on ICAM-1 If Mac-1 Is Blocked

Not all (cells) who wander are lost: Upstream migration as a pervasive mode of amoeboid cell motility

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