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J Immunol. 2019 Jan 1;202(1):207-217. doi: 10.4049/jimmunol.1801255. Epub 2018 Nov 30.

Immature Neutrophils Released in Acute Inflammation Exhibit Efficient Migration despite Incomplete Segmentation of the Nucleus.

Author information

1
Department of Respiratory Medicine, University Medical Center Utrecht, 3508 AB Utrecht, the Netherlands.
2
Laboratory of Translational Immunology, University Medical Center Utrecht, 3508 AB Utrecht, the Netherlands.
3
Department of Tumor Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands; and.
4
Department of Cell Biology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands.
5
Department of Respiratory Medicine, University Medical Center Utrecht, 3508 AB Utrecht, the Netherlands; N.Vrisekoop@umcutrecht.nl.

Abstract

Acute inflammation recruits neutrophils with a band-shaped nucleus to the circulation. This neutrophil population was recently shown to have superior antibacterial capacity. Early recruitment of banded neutrophils to an infection site will likely improve the outcome of the immune response, yet it critically depends on efficient migration. However, the current dogma states that the segmentation of the mature neutrophil nucleus has evolved to favor migration through narrow pores as found between endothelial cells and in the interstitium. Therefore, we hypothesized that banded neutrophils migrate less efficiently than neutrophils with segmented nuclei, whereas recently described neutrophils with hypersegmented nuclei would in turn migrate more efficiently. Acute inflammation was evoked in a human model of experimental endotoxemia to recruit neutrophil subsets with different nuclear segmentation to the circulation. To simulate migration toward an infection site, migration of the subsets was studied in in vitro models of transendothelial migration or interstitial chemokinesis and chemotaxis. In both models, nuclear segmentation did not increase migration speed. In dense collagen matrices, the speed of the hypersegmented neutrophils was even reduced compared with the banded neutrophils. Fluorescence microscopy suggested that the hypersegmented neutrophils displayed reduced rear release and deposited more membrane vesicles. Vice versa, migration through narrow pores did not induce nuclear segmentation in the neutrophils. In conclusion, like neutrophils with a segmented nucleus, the banded subset exhibited efficient migration through narrow pores. These findings suggest that the nucleus does not preclude the banded subset from reaching an infection site.

PMID:
30504419
DOI:
10.4049/jimmunol.1801255
[Indexed for MEDLINE]
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