The Journal of Experimental Medicine
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Published online 5 June 2006 doi:10.1084/jem.20051210
Rockefeller University Press, 0022-1007 $8.00
JEM, Volume 203, Number 6, 1519-1532
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ARTICLE

 Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils

Shijun Wang1, Mathieu-Benoit Voisin1, Karen Y. Larbi1, John Dangerfield1, Christoph Scheiermann1, Maxine Tran2, Patrick H. Maxwell2, Lydia Sorokin3, and Sussan Nourshargh1

1 Cardiovascular Medicine Unit, National Heart and Lung Institute and 2 Renal Section, Division of Medicine, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London W12 ONN, England, UK
3 Institute of Physiological Chemistry and Pathobiochemistry Muenster, University Waldeyerstrasse, 15 48149 Muenster, Germany

CORRESPONDENCE Sussan Nourshargh: s.nourshargh{at}imperial.ac.uk

The mechanism of leukocyte migration through venular walls in vivo is largely unknown. By using immunofluorescence staining and confocal microscopy, the present study demonstrates the existence of regions within the walls of unstimulated murine cremasteric venules where expression of key vascular basement membrane (BM) constituents, laminin 10, collagen IV, and nidogen-2 (but not perlecan) are considerably lower (<60%) than the average expression detected in the same vessel. These sites were closely associated with gaps between pericytes and were preferentially used by migrating neutrophils during their passage through cytokine-stimulated venules. Although neutrophil transmigration did not alter the number/unit area of extracellular matrix protein low expression sites, the size of these regions was enlarged and their protein content was reduced in interleukin-1ß–stimulated venules. These effects were entirely dependent on the presence of neutrophils and appeared to involve neutrophil-derived serine proteases. Furthermore, evidence was obtained indicating that transmigrating neutrophils carry laminins on their cell surface in vivo. Collectively, through identification of regions of low extracellular matrix protein localization that define the preferred route for transmigrating neutrophils, we have identified a plausible mechanism by which neutrophils penetrate the vascular BM without causing a gross disruption to its intricate structure.

Abbreviations used: BM, basement membrane; LE, low expression; NE, neutrophil elastase; PF, paraformaldehyde.

S. Wang and M.-B. Voisin contributed equally to this work.


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