Abstract
Cell migration plays important roles in embryonic development and inflammation, and this process is highly regulated to ensure tissue homeostasis. A number of barriers exist to prevent the inappropriate migration of leukocytes into healthy peripheral tissues, including retention of these cells in the inactive state and maintenance of the integrity and charge of the vascular endothelium. However, active signals also are likely to exist that can repulse cells or abolish existing cell migration. One such paradigm exists in the developing nervous system, where neuronal migration is mediated by a balance between chemoattractive and chemorepulsive signals. The ability of the guidance molecule netrin-1 to repulse or abolish attraction of neuronal cells expressing the UNC5b receptor makes it an attractive candidate for the regulation of inflammatory cell migration. Here, we show that netrin-1 is expressed on vascular endothelium, where it is regulated by infection and inflammatory cytokines. The netrin-1 receptor UNC5b is strongly expressed by leukocytes, upon which netrin-1 acts as a potent inhibitor of migration to different chemotactic stimuli both in vivo and in vitro. These data suggest that endothelial expression of netrin-1 may inhibit basal cell migration into tissues and that its down-regulation with the onset of sepsis/inflammation may facilitate leukocyte recruitment.
MeSH Terms
Animals
Blotting, Western
Cell Movement/immunology
Cells, Cultured
Chemotaxis/immunology
DNA Primers
Endothelial Cells/immunology,metabolism
Female
Humans
Inflammation/immunology
Leukocytes/metabolism
Mice
Mice, Inbred C57BL
Nerve Growth Factors/immunology,metabolism
Netrin Receptors
Netrin-1
Receptors, Cell Surface/metabolism
Reverse Transcriptase Polymerase Chain Reaction
Superoxides/metabolism
Tumor Suppressor Proteins/immunology,metabolism
Chemicals
DNA Primers
NTN1 protein, human
Nerve Growth Factors
Netrin Receptors
Ntn1 protein, mouse
Receptors, Cell Surface
Tumor Suppressor Proteins
Superoxides
Netrin-1
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ly Ngoc P
Laboratory of Developmental Immunology, Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, GRJ 1414, Boston, MA 02114, USA.
Komatsuzaki Katsumi
Fraser Iain P
Tseng Anita A
Prodhan Parthak
Moore Kathryn J
Kinane T Bernard
References (22)
22 references, click to expand
-
Netrin 1 is required for semicircular canal formation in the mouse inner ear.
Development. 2000 Jan;127(1):13-22
PMID: 10654596
-
Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord.
Cell. 1994 Aug 12;78(3):425-35
PMID: 8062385
-
Chemokines in pathology and medicine.
J Intern Med. 2001 Aug;250(2):91-104
PMID: 11489059
-
Dynamic regulation of axon guidance.
Nat Neurosci. 2001 Nov;4 Suppl:1169-76
PMID: 11687826
-
Short- and long-range repulsion by the Drosophila Unc5 netrin receptor.
Neuron. 2001 Nov 20;32(4):605-17
PMID: 11719202
-
Modulation of G(ialpha(2)) signaling by the axonal guidance molecule UNC5H2.
Biochem Biophys Res Commun. 2002 Oct 4;297(4):898-905
PMID: 12359238
-
Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis.
Dev Cell. 2003 Mar;4(3):371-82
PMID: 12636918
-
Expression of Netrin-1 and its two receptors DCC and UNC5H2 in the developing mouse lung.
Gene Expr Patterns. 2003 Jun;3(3):279-83
PMID: 12799072
-
CD36 mediates the innate host response to beta-amyloid.
J Exp Med. 2003 Jun 16;197(12):1657-66
PMID: 12796468
-
Neuronal repellent Slit2 inhibits dendritic cell migration and the development of immune responses.
J Immunol. 2003 Dec 15;171(12):6519-26
PMID: 14662852
-
Slit protein-mediated inhibition of CXCR4-induced chemotactic and chemoinvasive signaling pathways in breast cancer cells.
J Biol Chem. 2004 Mar 5;279(10):9115-24
PMID: 14645233
-
Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis.
Curr Biol. 2004 May 25;14(10):897-905
PMID: 15186747
-
Retinoic acid decreases fetal lung mesenchymal cell proliferation in vivo and in vitro.
Dev Growth Differ. 2004 Jun;46(3):275-82
PMID: 15206958
-
Modulation of inflammation by slit protein in vivo in experimental crescentic glomerulonephritis.
Am J Pathol. 2004 Jul;165(1):341-52
PMID: 15215188
-
The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6.
Cell. 1994 Aug 12;78(3):409-24
PMID: 8062384
-
The molecular biology of axon guidance.
Science. 1996 Nov 15;274(5290):1123-33
PMID: 8895455
-
Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors.
Nature. 1997 Apr 24;386(6627):833-8
PMID: 9126742
-
Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary.
Development. 1998 Jan;125(1):41-50
PMID: 9389662
-
A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion.
Cell. 1999 Jun 25;97(7):927-41
PMID: 10399920
-
Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1.
Nature. 1999 Sep 2;401(6748):69-73
PMID: 10485706
-
Cutting edge: bone morphogenetic protein antagonists Drm/Gremlin and Dan interact with Slits and act as negative regulators of monocyte chemotaxis.
J Immunol. 2004 Nov 15;173(10):5914-7
PMID: 15528323
-
The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors.
Nature. 2001 Apr 19;410(6831):948-52
PMID: 11309622