Abstract
Directed cell migration is a prerequisite not only for the development of the central nervous system, but also for topically restricted, appropriate immune responses. This is crucial for host defense and immune surveillance. Attracting environmental cues guiding leukocyte cell traffic are likely to be complemented by repulsive cues, which actively abolish cell migration. One such a paradigm exists in the developing nervous system, where neuronal migration and axonal path finding is balanced by chemoattractive and chemorepulsive cues, such as the neuronal repulsive guidance molecule-A (RGM-A). As expressed at the inflammatory site, the role of RGM-A within the immune response remains unclear. Here we report that RGM-A (i) is expressed by epithelium and leukocytes (granulocytes, monocytes, and T/B lymphocytes); (ii) inhibits leukocyte migration by contact repulsion and chemorepulsion, depending on dosage, through its receptor neogenin; and (iii) suppresses the inflammatory response in a model of zymosan-A-induced peritonitis. Systemic application of RGM-A attenuates the humoral proinflammatory response (TNF-α, IL-6, and macrophage inflammatory protein 1α), infiltration of inflammatory cell traffic, and edema formation. In contrast, the demonstrated anti-inflammatory effect of RGM-A is absent in mice homozygous for a gene trap mutation in the neo1 locus (encoding neogenin). Thus, our results suggest that RGM-A is a unique endogenous inhibitor of leukocyte chemotaxis that limits inflammatory leukocyte traffic and creates opportunities to better understand and treat pathologies caused by exacerbated or misdirected inflammatory responses.
MeSH Terms
Animals
Caco-2 Cells
Chemotaxis/drug effects,genetics,immunology
Cytokines/biosynthesis,genetics,immunology
Epithelium/immunology,metabolism
GPI-Linked Proteins/biosynthesis,genetics,immunology
Gene Expression Regulation/drug effects,genetics,immunology
Humans
Inflammation/chemically induced,genetics,immunology,metabolism
Leukocytes/immunology,metabolism
Mice
Mice, Knockout
Nerve Tissue Proteins/biosynthesis,genetics,immunology
Organ Specificity/drug effects,genetics,immunology
Peritonitis/chemically induced,genetics,immunology,metabolism
Zymosan/toxicity
Chemicals
Cytokines
GPI-Linked Proteins
Nerve Tissue Proteins
RGMA protein, human
Rgma protein, mouse
Zymosan
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Mirakaj Valbona
Department of Anesthesiology and Intensive Care Medicine, Tübingen University Hospital, 72076 Tübingen, Germany.
Brown Sebastian
Laucher Stefanie
Steinl Carolin
Klein Gerd
Köhler David
Skutella Thomas
Meisel Christian
Brommer Benedikt
Rosenberger Peter
Schwab Jan M
References (33)
33 references, click to expand
-
RGMA and IL21R show association with experimental inflammation and multiple sclerosis.
Genes Immun. 2010 Jun;11(4):279-93
PMID: 20072140
-
Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin.
Nature. 2007 Apr 5;446(7136):680-4
PMID: 17377534
-
Repulsive guidance molecule (RGMa), a DRAGON homologue, is a bone morphogenetic protein co-receptor.
J Biol Chem. 2005 Aug 19;280(33):29820-7
PMID: 15975920
-
Chemokines and leukocyte traffic.
Nature. 1998 Apr 9;392(6676):565-8
PMID: 9560152
-
Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm.
Cell. 1994 Jan 28;76(2):301-14
PMID: 7507411
-
RGM and its receptor neogenin regulate neuronal survival.
Nat Cell Biol. 2004 Aug;6(8):749-55
PMID: 15258591
-
Chemokines--chemotactic cytokines that mediate inflammation.
N Engl J Med. 1998 Feb 12;338(7):436-45
PMID: 9459648
-
Central nervous system injury-induced repulsive guidance molecule expression in the adult human brain.
Arch Neurol. 2005 Oct;62(10):1561-8
PMID: 16216939
-
Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury.
Annu Rev Pathol. 2007;2:111-43
PMID: 18039095
-
The molecular biology of axon guidance.
Science. 1996 Nov 15;274(5290):1123-33
PMID: 8895455
-
The role of repulsive guidance molecules in the embryonic and adult vertebrate central nervous system.
Philos Trans R Soc Lond B Biol Sci. 2006 Sep 29;361(1473):1513-29
PMID: 16939972
-
Resolvin E1 and protectin D1 activate inflammation-resolution programmes.
Nature. 2007 Jun 14;447(7146):869-74
PMID: 17568749
-
Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia.
Nat Immunol. 2009 Feb;10(2):195-202
PMID: 19122655
-
Anti-inflammatory lipid mediators and insights into the resolution of inflammation.
Nat Rev Immunol. 2002 Oct;2(10):787-95
PMID: 12360216
-
DRAGON, a bone morphogenetic protein co-receptor.
J Biol Chem. 2005 Apr 8;280(14):14122-9
PMID: 15671031
-
Defining brain wiring patterns and mechanisms through gene trapping in mice.
Nature. 2001 Mar 8;410(6825):174-9
PMID: 11242070
-
Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza.
Sci Transl Med. 2010 Mar 17;2(23):23ra19
PMID: 20375003
-
RGMa inhibition promotes axonal growth and recovery after spinal cord injury.
J Cell Biol. 2006 Apr 10;173(1):47-58
PMID: 16585268
-
The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors.
Nature. 2001 Apr 19;410(6831):948-52
PMID: 11309622
-
Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons.
Neuron. 1999 Apr;22(4):731-42
PMID: 10230793
-
Neuronal migration and molecular conservation with leukocyte chemotaxis.
Genes Dev. 2002 Dec 1;16(23):2973-84
PMID: 12464628
-
Biochemical characterization of a putative axonal guidance molecule of the chick visual system.
Neuron. 1990 Nov;5(5):735-43
PMID: 2171592
-
Nonresolving inflammation.
Cell. 2010 Mar 19;140(6):871-82
PMID: 20303877
-
Cell migration: integrating signals from front to back.
Science. 2003 Dec 5;302(5651):1704-9
PMID: 14657486
-
Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system.
J Neurosci. 2004 Jan 28;24(4):808-18
PMID: 14749425
-
Semaphorins command cells to move.
Nat Rev Mol Cell Biol. 2005 Oct;6(10):789-800
PMID: 16314868
-
RGM is a repulsive guidance molecule for retinal axons.
Nature. 2002 Sep 26;419(6905):392-5
PMID: 12353034
-
Netrin-1 inhibits leukocyte migration in vitro and in vivo.
Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14729-34
PMID: 16203981
-
Collagen type VI in the human bone marrow microenvironment: a strong cytoadhesive component.
Blood. 1995 Sep 1;86(5):1740-8
PMID: 7655006
-
Epithelial decision makers: in search of the 'epimmunome'.
Nat Immunol. 2010 Aug;11(8):656-65
PMID: 20644571
-
Repulsive guidance molecule plays multiple roles in neuronal differentiation and axon guidance.
J Neurosci. 2006 May 31;26(22):6082-8
PMID: 16738252
-
Neogenin mediates the action of repulsive guidance molecule.
Nat Cell Biol. 2004 Aug;6(8):756-62
PMID: 15258590
-
Repulsive guidance molecule/neogenin: a novel ligand-receptor system playing multiple roles in neural development.
Dev Growth Differ. 2004 Dec;46(6):481-6
PMID: 15610137