Abstract
Replacement of wounded skin requires the initially florid cellular response to abate and even regress as the dermal layer returns to a relatively paucicellular state. The signals that direct this "stop and return" process have yet to be deciphered. CXCR3 chemokine receptor and its ligand CXCL11/IP-9/I-TAC are expressed by basal keratinocytes and CXCL10/IP-10 by keratinocytes and endothelial cells during wound healing in mice and humans. In vitro, these ligands limit motility in dermal fibroblasts and endothelial cells. To examine whether this signaling pathway contributes to wound healing in vivo, full-thickness excisional wounds were created on CXCR3 wild-type (+/+) or knockout (-/-) mice. Even at 90 days, long after wound closure, wounds in the CXCR3(-/-) mice remained hypercellular and presented immature matrix components. The CXCR3(-/-) mice also presented poor remodeling and reorganization of collagen, which resulted in a weakened healed dermis. This in vivo model substantiates our in vitro findings that CXCR3 signaling is necessary for inhibition of fibroblast and endothelial cell migration and subsequent redifferentiation of the fibroblasts to a contractile state. These studies establish a pathophysiologic role for CXCR3 and its ligand during wound repair.
MeSH Terms
Adult
Animals
Animals, Newborn
Apoptosis/genetics,physiology
Chemokine CXCL11
Chemokines, CXC/genetics,metabolism
Collagen/metabolism
Dermis/metabolism,pathology,physiopathology
Extracellular Matrix/metabolism
Female
Fibroblasts/cytology,drug effects,metabolism
Fibronectins/metabolism
Gene Expression
Humans
Intercellular Signaling Peptides and Proteins/pharmacology
Male
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Knockout
Neovascularization, Physiologic/genetics,physiology
Receptors, CXCR3
Receptors, Chemokine/deficiency,genetics,physiology
Signal Transduction/genetics,physiology
Skin/metabolism,pathology,physiopathology
Time Factors
Wound Healing/genetics,physiology
Chemicals
CXCL11 protein, human
CXCR3 protein, human
Chemokine CXCL11
Chemokines, CXC
Cxcl11 protein, mouse
Cxcr3 protein, mouse
Fibronectins
Intercellular Signaling Peptides and Proteins
Receptors, CXCR3
Receptors, Chemokine
Collagen
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Yates Cecelia C
Department of Pathology, University of Pittsburgh and Pittsburgh VAMC, Pittsburgh, Pennsylvania 15261, USA.
Whaley Diana
Kulasekeran Priya
Hancock Wayne W
Lu Bao
Bodnar Richard
Newsome Joseph
Hebda Patricia A
Wells Alan
References (31)
31 references, click to expand
-
Interferon-inducible protein 9 (CXCL11)-induced cell motility in keratinocytes requires calcium flux-dependent activation of mu-calpain.
Mol Cell Biol. 2005 Mar;25(5):1922-41
PMID: 15713646
-
The role of thrombospondin-1 in human disease.
J Surg Res. 2004 Nov;122(1):135-42
PMID: 15522326
-
Morphological evidence for the role of suprabasal keratinocytes in wound reepithelialization.
Wound Repair Regen. 2005 Sep-Oct;13(5):468-79
PMID: 16176455
-
CXCR3-mediated opposite effects of CXCL10 and CXCL4 on TH1 or TH2 cytokine production.
J Allergy Clin Immunol. 2005 Dec;116(6):1372-9
PMID: 16337473
-
IP-10 blocks vascular endothelial growth factor-induced endothelial cell motility and tube formation via inhibition of calpain.
Circ Res. 2006 Mar 17;98(5):617-25
PMID: 16484616
-
Multiple signaling pathways mediate compaction of collagen matrices by EGF-stimulated fibroblasts.
Exp Cell Res. 2006 Jul 1;312(11):1970-82
PMID: 16595133
-
Epidermal maturation arrest.
Dermatol Surg. 1999 Nov;25(11):900-3
PMID: 10594606
-
Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway.
J Biol Chem. 2000 Jan 28;275(4):2390-8
PMID: 10644690
-
Delayed wound healing in CXCR2 knockout mice.
J Invest Dermatol. 2000 Aug;115(2):234-44
PMID: 10951241
-
Requirement of the chemokine receptor CXCR3 for acute allograft rejection.
J Exp Med. 2000 Nov 20;192(10):1515-20
PMID: 11085753
-
Epidermal growth factor (EGF)-like repeats of human tenascin-C as ligands for EGF receptor.
J Cell Biol. 2001 Jul 23;154(2):459-68
PMID: 11470832
-
Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain.
Mol Cell Biol. 2002 Apr;22(8):2716-27
PMID: 11909964
-
Platelets, thrombospondin-1 and human dermal fibroblasts cooperate for stimulation of endothelial cell tubulogenesis through VEGF and PAI-1 regulation.
Exp Cell Res. 2007 Feb 1;313(3):486-99
PMID: 17126831
-
Epidermal growth factor induces acute matrix contraction and subsequent calpain-modulated relaxation.
Wound Repair Regen. 2002 Jan-Feb;10(1):67-76
PMID: 11983008
-
Tenascin-C modulates matrix contraction via focal adhesion kinase- and Rho-mediated signaling pathways.
Mol Biol Cell. 2002 Oct;13(10):3601-13
PMID: 12388760
-
Regeneration or scarring: an immunologic perspective.
Dev Dyn. 2003 Feb;226(2):268-79
PMID: 12557205
-
Dendritic fibroblasts in three-dimensional collagen matrices.
Mol Biol Cell. 2003 Feb;14(2):384-95
PMID: 12589041
-
Glu-Leu-Arg-negative CXC chemokine interferon gamma inducible protein-9 as a mediator of epidermal-dermal communication during wound repair.
J Invest Dermatol. 2003 Jun;120(6):1110-7
PMID: 12787142
-
Epithelial-mesenchymal networks in wounds: a hierarchical view.
J Invest Dermatol. 2003 Jun;120(6):ix-xi
PMID: 12787148
-
Absence of inhibition of cutaneous wound healing in mice by oral doxycycline.
Wound Repair Regen. 2003 Sep-Oct;11(5):373-9
PMID: 12950642
-
CXC chemokines: the regulatory link between inflammation and angiogenesis.
Trends Immunol. 2004 Apr;25(4):201-9
PMID: 15039047
-
Induction of tenascin in healing wounds.
J Cell Biol. 1988 Dec;107(6 Pt 2):2757-67
PMID: 2462568
-
Expression of integrins and basement membrane components by wound keratinocytes.
J Clin Invest. 1993 Sep;92(3):1425-35
PMID: 8376596
-
TGF-beta 1 induces the expression of type I collagen and SPARC, and enhances contraction of collagen gels, by fibroblasts from young and aged donors.
J Cell Physiol. 1994 Jan;158(1):169-79
PMID: 8263022
-
Fibroblasts, myofibroblasts, and wound contraction.
J Cell Biol. 1994 Feb;124(4):401-4
PMID: 8106541
-
Wound repair in the context of extracellular matrix.
Curr Opin Cell Biol. 1994 Oct;6(5):717-25
PMID: 7530463
-
Interferon gamma-inducible protein 10 (IP-10), a member of the C-X-C chemokine family, is an inhibitor of angiogenesis.
Biochem Biophys Res Commun. 1995 May 5;210(1):51-7
PMID: 7537965
-
The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation.
J Exp Med. 1995 Jul 1;182(1):219-31
PMID: 7790818
-
Differences in the regulation of fibroblast contraction of floating versus stressed collagen matrices.
J Biol Chem. 1999 Jan 8;274(2):918-23
PMID: 9873032
-
IP-10 inhibits epidermal growth factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity.
J Cell Biol. 1999 Jul 12;146(1):243-54
PMID: 10402474
-
Chemokine receptor CXCR3: an unexpected enigma.
Curr Top Dev Biol. 2005;68:149-81
PMID: 16124999