Matrix metalloproteinases modulate ameboid-like migration of neutrophils through inflamed interstitial tissue

Lerchenberger, Maximilian; Uhl, Bernd; Stark, Konstantin; Zuchtriegel, Gabriele; Eckart, Annekathrin; Miller, Meike; Puhr‐Westerheide, Daniel; Praetner, Marc; Rehberg, Markus; Khandoga, Alexander G.; Lauber, Kirsten; Maßberg, Steffen; Krombach, Fritz; Reichel, Christoph

doi:10.1182/blood-2012-12-472944

Cited by 37 publications

(32 citation statements)

References 40 publications

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“…Recent advances in the use of multicolor fluorescence spinning disk and multiphoton confocal intravital microscopic imaging have shown that once the inflammatory phagocytes pierce the endothelial barrier and subendothelial matrix, they migrate along pericytes to exit the vascular wall at regions of low matrix deposition in the basement membrane that are also characterized by gaps between pericytes (594, 595, 644, 741). Once in the subendothelial space, neutrophils are guided by pericyte cues to enter and move through the interstitium by a mechanism dependent on actin polymerization and on matrix metalloproteinase (MMP)activity but without degradation of pericellular collagen (486). Reverse migration of neutrophils away from sites of injury and inflammation has also been described, but the pathophysiologic relevance of this response has not been evaluated in I/R (98, 596).…”

Section: Cell Types Involved In Postischemic Inflammationmentioning

confidence: 99%

Ischemia/Reperfusion

Kalogeris

Baines

Krenz

et al. 2016

Comprehensive Physiology

647

565

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Ischemic disorders, such as myocardial infarction, stroke, and peripheral vascular disease, are the most common causes of debilitating disease and death in westernized cultures. The extent of tissue injury relates directly to the extent of blood flow reduction and to the length of the ischemic period, which influence the levels to which cellular ATP and intracellular pH are reduced. By impairing ATPase-dependent ion transport, ischemia causes intracellular and mitochondrial calcium levels to increase (calcium overload). Cell volume regulatory mechanisms are also disrupted by the lack of ATP, which can induce lysis of organelle and plasma membranes. Reperfusion, although required to salvage oxygen-starved tissues, produces paradoxical tissue responses that fuel the production of reactive oxygen species (oxygen paradox), sequestration of proinflammatory immunocytes in ischemic tissues, endoplasmic reticulum stress, and development of postischemic capillary no-reflow, which amplify tissue injury. These pathologic events culminate in opening of mitochondrial permeability transition pores as a common end-effector of ischemia/reperfusion (I/R)-induced cell lysis and death. Emerging concepts include the influence of the intestinal microbiome, fetal programming, epigenetic changes, and microparticles in the pathogenesis of I/R. The overall goal of this review is to describe these and other mechanisms that contribute to I/R injury. Because so many different deleterious events participate in I/R, it is clear that therapeutic approaches will be effective only when multiple pathologic processes are targeted. In addition, the translational significance of I/R research will be enhanced by much wider use of animal models that incorporate the complicating effects of risk factors for cardiovascular disease.

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Section: Cell Types Involved In Postischemic Inflammationmentioning

confidence: 99%

Ischemia/Reperfusion

Kalogeris

Baines

Krenz

et al. 2016

Comprehensive Physiology

647

565

View full text Add to dashboard Cite

show abstract

“…A recent work described that neutrophils locomote in a tidy fashion toward an inflamed site showing an ameboid-like migration mediated by MMP and using the dense collagen network of the inflamed tissue as a guidance (Lerchenberger et al, 2013). Inhibition of MMP significantly impaired the migration of neutrophils by decreasing their directionality, velocity and distance traveled, suggesting these as important features of the full neutrophil functionality.…”

Section: Relevant Indices For Immune Cell Active/functional Statementioning

confidence: 99%

“…Inhibition of MMP significantly impaired the migration of neutrophils by decreasing their directionality, velocity and distance traveled, suggesting these as important features of the full neutrophil functionality. Furthermore, the directional migration required a morphological polarization that can be measured by the shape descriptor eccentricity (the cell long axis divided by the cell short axis), which decreased by application of the MMP inhibitor (Lerchenberger et al, 2013). Although this study applies 2-PM to a peripheral inflamed mouse organ -the cremaster muscle -it is conceivable that these motility descriptors would be useful to track neutrophil functional state in the CNS.…”

Section: Relevant Indices For Immune Cell Active/functional Statementioning

confidence: 99%

A close look at brain dynamics: Cells and vessels seen by in vivo two-photon microscopy

Fumagalli

Ortolano

Simoni

2014

Progress in Neurobiology

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“…While various results have been obtained about the roles of integrins [84, 85], actin polymerization [86], and myosin II function [86, 87] in neutrophil interstitial migration in vivo, the nature of the experiments leaves open questions about whether the manipulations employed acted directly on the studied leukocytes or indirectly via other tissue cells. On the other hand, numerous mouse knockout models for regulators of actin polymerization and actomyosin contraction have studied neutrophil function [88–96], but rarely addressed interstitial migration by direct in vivo imaging.…”

Section: Physiological Leukocyte Migrationmentioning

confidence: 99%

The multiple faces of leukocyte interstitial migration

2014

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Spatiotemporal control of leukocyte dynamics within tissues is critical for successful innate and adaptive immune responses. Homeostatic trafficking and coordinated infiltration into and within sites of inflammation and infection rely on signaling in response to extracellular cues that in turn controls a variety of intracellular protein networks regulating leukocyte motility, migration, chemotaxis, positioning, and cell–cell interaction. In contrast to mesenchymal cells, leukocytes migrate in an amoeboid fashion by rapid cycles of actin polymerization and actomyosin contraction, and their migration in tissues is generally referred to as low adhesive and nonproteolytic. The interplay of actin network expansion, contraction, and adhesion shapes the exact mode of amoeboid migration, and in this review, we explore how leukocyte subsets potentially harness the same basic biomechanical mechanisms in a cell-type-specific manner. Most of our detailed understanding of these processes derives from in vitro migration studies in three-dimensional gels and confined spaces that mimic geometrical aspects of physiological tissues. We summarize these in vitro results and then critically compare them to data from intravital imaging of leukocyte interstitial migration in mouse tissues. We outline the technical challenges of obtaining conclusive mechanistic results from intravital studies, discuss leukocyte migration strategies in vivo, and present examples of mode switching during physiological interstitial migration. These findings are also placed in the context of leukocyte migration defects in primary immunodeficiencies. This overview of both in vitro and in vivo studies highlights recent progress in understanding the molecular and biophysical mechanisms that shape robust leukocyte migration responses in physiologically complex and heterogeneous environments.

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Matrix metalloproteinases modulate ameboid-like migration of neutrophils through inflamed interstitial tissue

Abstract: Key Points The density of the interstitial collagen network increases in inflamed tissue, providing physical guidance to infiltrating neutrophils. Neutrophil interstitial migration does not require the pericellular degradation of collagen fibers, but it is modulated by MMPs.

Cited by 37 publications

References 40 publications

Ischemia/Reperfusion

Ischemia/Reperfusion

A close look at brain dynamics: Cells and vessels seen by in vivo two-photon microscopy

The multiple faces of leukocyte interstitial migration

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