Abstract
The mast cell is one of the major effector cells in inflammatory reactions and can be found in most tissues throughout the body. During inflammation, an increase in the number of mast cells in the local milieu occurs, and such accumulation requires directed migration of this cell population. As it has previously been reported that the human cathelicidin-derived antibacterial peptide, LL-37, stimulates the degranulation of mast cells, we hypothesized that LL-37 could be a mast cell chemotaxin. The present study shows that LL-37 is a potent chemotactic factor for mast cells. The chemotactic response was dose-dependent and bell-shaped, reaching an optimal concentration of 5 microg/ml. In addition, checkerboard analysis showed that cell migration towards this peptide was chemotactic rather than chemokinetic. Moreover, Scatchard analysis using 125I-labelled LL-37-derived peptide revealed that LL-37 has at least two classes of receptors, namely high- and low-affinity receptors, on mast cells. Furthermore, the competitive binding assay suggested that LL-37 is unlikely to utilize formyl peptide receptor-like 1 (FPRL1), a functional LL-37 receptor for neutrophil and monocyte migration, on mast cells. In addition, the treatment of cells with pertussis toxin and phospholipase C inhibitor, U-73122, inhibited LL-37-mediated migration, indicating that LL-37 induces mast cell chemotaxis through a Gi protein-phospholipase C signalling pathway. These results show that besides its antibacterial activities, LL-37 may have the potential to recruit mast cells to inflammation foci.
MeSH Terms
Animals
Antimicrobial Cationic Peptides/immunology
Binding, Competitive/immunology
Calcium/metabolism
Cathelicidins
Chemotactic Factors/immunology
Chemotaxis/immunology
Dose-Response Relationship, Immunologic
Estrenes
Immune Sera/immunology
Male
Mast Cells/immunology,metabolism
Pertussis Toxin
Phosphodiesterase Inhibitors/pharmacology
Prodrugs/pharmacology
Pyrrolidinones
Rats
Rats, Sprague-Dawley
Signal Transduction/immunology
Virulence Factors, Bordetella/pharmacology
Chemicals
Antimicrobial Cationic Peptides
Cathelicidins
Chemotactic Factors
Estrenes
Immune Sera
Phosphodiesterase Inhibitors
Prodrugs
Pyrrolidinones
Virulence Factors, Bordetella
1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
ropocamptide
Pertussis Toxin
Calcium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Niyonsaba François
Department of Biochemistry, Juntendo University, School of Medicine, Tokyo, Japan.
Iwabuchi Kazuhisa
Someya Akimasa
Hirata Michimasa
Matsuda Hiroshi
Ogawa Hideoki
Nagaoka Isao
References (28)
28 references, click to expand
-
Evaluation of the expression of human CAP18 gene during neutrophil maturation in the bone marrow.
J Leukoc Biol. 1998 Dec;64(6):845-52
PMID: 9850169
-
Epithelial antimicrobial peptides: review and significance for oral applications.
Crit Rev Oral Biol Med. 1998;9(4):399-414
PMID: 9825219
-
Antimicrobial peptides in mammalian and insect host defence.
Curr Opin Immunol. 1999 Feb;11(1):23-7
PMID: 10047545
-
The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6.
Infect Immun. 1999 May;67(5):2561-6
PMID: 10225921
-
Synergistic actions of antibacterial neutrophil defensins and cathelicidins.
Inflamm Res. 2000 Feb;49(2):73-9
PMID: 10738945
-
Augmentation of innate host defense by expression of a cathelicidin antimicrobial peptide.
Infect Immun. 1999 Nov;67(11):6084-9
PMID: 10531270
-
Nerve growth factor functions as a chemoattractant for mast cells through both mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling pathways.
Blood. 2000 Mar 15;95(6):2052-8
PMID: 10706874
-
Human mast cell migration in response to members of the transforming growth factor-beta family.
J Leukoc Biol. 2000 Mar;67(3):350-6
PMID: 10733095
-
LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells.
J Exp Med. 2000 Oct 2;192(7):1069-74
PMID: 11015447
-
Evaluation of the effects of peptide antibiotics human beta-defensins-1/-2 and LL-37 on histamine release and prostaglandin D(2) production from mast cells.
Eur J Immunol. 2001 Apr;31(4):1066-75
PMID: 11298331
-
Cathelicidin family of antibacterial peptides CAP18 and CAP11 inhibit the expression of TNF-alpha by blocking the binding of LPS to CD14(+) cells.
J Immunol. 2001 Sep 15;167(6):3329-38
PMID: 11544322
-
Ligand: a versatile computerized approach for characterization of ligand-binding systems.
Anal Biochem. 1980 Sep 1;107(1):220-39
PMID: 6254391
-
Quantitation of human synovial mast cells in rheumatoid arthritis and other rheumatic diseases.
Arthritis Rheum. 1984 Aug;27(8):852-6
PMID: 6380504
-
Intraepithelial migration of nasal mucosal mast cells in hay fever.
Int Arch Allergy Appl Immunol. 1986;80(1):44-51
PMID: 3957446
-
The mast cell in health and disease.
J Am Acad Dermatol. 1990 Oct;23(4 Pt 1):615-24
PMID: 1699980
-
Intraepithelial mast cells in allergic and nonallergic asthma. Assessment using bronchial brushings.
Am Rev Respir Dis. 1993 Jul;148(1):80-6
PMID: 8317819
-
Isolation and characterization of the neutrophil-binding proteins for platelet-derived adherence-inhibiting factor.
Blood. 1993 Sep 15;82(6):1884-90
PMID: 8400239
-
A novel granulocyte-derived peptide with lipopolysaccharide-neutralizing activity.
J Immunol. 1994 Jan 1;152(1):231-40
PMID: 8254193
-
Stem cell factor is a chemotactic factor for human mast cells.
J Immunol. 1994 Oct 15;153(8):3717-23
PMID: 7523504
-
FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis.
Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):195-9
PMID: 7529412
-
Peptide antibiotics and their role in innate immunity.
Annu Rev Immunol. 1995;13:61-92
PMID: 7612236
-
hCAP-18, a cathelin/pro-bactenecin-like protein of human neutrophil specific granules.
FEBS Lett. 1995 Jul 10;368(1):173-6
PMID: 7615076
-
Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain.
FEBS Lett. 1995 Oct 23;374(1):1-5
PMID: 7589491
-
C3a and C5a are chemotaxins for human mast cells and act through distinct receptors via a pertussis toxin-sensitive signal transduction pathway.
J Immunol. 1996 Aug 15;157(4):1693-8
PMID: 8759757
-
The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratinocytes during inflammatory disorders.
J Biol Chem. 1997 Jun 13;272(24):15258-63
PMID: 9182550
-
Chemokines--chemotactic cytokines that mediate inflammation.
N Engl J Med. 1998 Feb 12;338(7):436-45
PMID: 9459648
-
The peptide antibiotic LL-37/hCAP-18 is expressed in epithelia of the human lung where it has broad antimicrobial activity at the airway surface.
Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9541-6
PMID: 9689116
-
Identification of surrogate agonists for the human FPRL-1 receptor by autocrine selection in yeast.
Nat Biotechnol. 1998 Dec;16(13):1334-7
PMID: 9853614