Skip to main content
Top
Published in: Journal of Inflammation 1/2006

Open Access 01-12-2006 | Short Report

Heparan sulfate proteoglycan-dependent neutrophil chemotaxis toward PR-39 cathelicidin

Authors: Angela Djanani, Birgit Mosheimer, Nicole C Kaneider, Christopher R Ross, Giovanni Ricevuti, Josef R Patsch, Christian J Wiedermann

Published in: Journal of Inflammation | Issue 1/2006

Login to get access

Abstract

Cathelicidins are mammalian proteins containing a C-terminal cationic antimicrobial domain. Porcine PR-39 cathelicidin affects leukocyte biology. Mechanisms of action may involve alteration of heparan sulfate proteoglycan-dependent functions in inflammatory cells. It was tested whether PR-39 affects human neutrophil migration and if such effects involve heparan sulphate proteoglycans. Neutrophils were from forearm venous blood of healthy donors. Migration was tested in modified Boyden chamber assays. Involvement of heparan sulfate proteoglycans was tested by their chemical modification and by the use of specific antibodies. PR-39 induced migration in neutrophils in a concentration dependent manner. Modification of heparan sulfate proteoglycans with sodium chlorate inhibited migration whereas chemotaxis toward the chemoattractant formyl-Met-Leu-Phe was not affected. Removal of heparan sulfates or chondroitin sulfates from the surface of neutrophils by heparinase or chondroitinase inhibited migration toward PR-39. In conclusion, antimicrobial PR-39 stimulates human neutrophil chemotaxis in a heparan sulfate proteoglycan-dependent manner. Involvment of syndecans is likely as both heparinase and chondroitinase were abrogating. Data suggest active participation of heparan sulfate proteoglycans of neutrophils in cathelicidin peptide-mediated regulation of the antimicrobial host defense.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lehrer RI, Ganz T: Defensins of vertebrate animals. Curr Opin Immunol. 2002, 14: 96-102. 10.1016/S0952-7915(01)00303-X.PubMedCrossRef Lehrer RI, Ganz T: Defensins of vertebrate animals. Curr Opin Immunol. 2002, 14: 96-102. 10.1016/S0952-7915(01)00303-X.PubMedCrossRef
2.
go back to reference Lehrer RI, Ganz T: Cathelicidins: a family of endogenous antimicrobial peptides. Curr Opin Hematol. 2002, 9: 18-22. 10.1097/00062752-200201000-00004.PubMedCrossRef Lehrer RI, Ganz T: Cathelicidins: a family of endogenous antimicrobial peptides. Curr Opin Hematol. 2002, 9: 18-22. 10.1097/00062752-200201000-00004.PubMedCrossRef
3.
go back to reference Zaiou M, Gallo RL: Cathelicidins, essential gene-encoded mammalian antibiotics. J Mol Med. 2002, 80: 549-61. 10.1007/s00109-002-0350-6.PubMedCrossRef Zaiou M, Gallo RL: Cathelicidins, essential gene-encoded mammalian antibiotics. J Mol Med. 2002, 80: 549-61. 10.1007/s00109-002-0350-6.PubMedCrossRef
4.
go back to reference Zanetti M, Gennaro R, Romeo D: Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Lett. 1995, 374: 1-5. 10.1016/0014-5793(95)01050-O.PubMedCrossRef Zanetti M, Gennaro R, Romeo D: Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Lett. 1995, 374: 1-5. 10.1016/0014-5793(95)01050-O.PubMedCrossRef
5.
go back to reference Zanetti M, Del Sal G, Storici P, Schneider C, Romeo D: The cDNA of the neutrophil antibiotic Bac5 predicts a pro-sequence homologous to a cysteine proteinase inhibitor that is common to other neutrophil antibiotics. J Biol Chem. 1993, 268: 522-6.PubMed Zanetti M, Del Sal G, Storici P, Schneider C, Romeo D: The cDNA of the neutrophil antibiotic Bac5 predicts a pro-sequence homologous to a cysteine proteinase inhibitor that is common to other neutrophil antibiotics. J Biol Chem. 1993, 268: 522-6.PubMed
6.
go back to reference Bagella L, Scocchi M, Zanetti M: cDNA sequences of three sheep myeloid cathelicidins. FEBS Lett. 1995, 376: 225-8. 10.1016/0014-5793(95)01285-3.PubMedCrossRef Bagella L, Scocchi M, Zanetti M: cDNA sequences of three sheep myeloid cathelicidins. FEBS Lett. 1995, 376: 225-8. 10.1016/0014-5793(95)01285-3.PubMedCrossRef
7.
go back to reference Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R: Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem. 1977, 272: 13088-93. 10.1074/jbc.272.20.13088.CrossRef Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R: Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem. 1977, 272: 13088-93. 10.1074/jbc.272.20.13088.CrossRef
8.
go back to reference Agerberth B, Gunne H, Odeberg J, Kogner P, Boman HG, Gudmundsson GH: FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proc Natl Acad Sci USA. 1995, 92: 195-9. 10.1073/pnas.92.1.195.PubMedPubMedCentralCrossRef Agerberth B, Gunne H, Odeberg J, Kogner P, Boman HG, Gudmundsson GH: FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proc Natl Acad Sci USA. 1995, 92: 195-9. 10.1073/pnas.92.1.195.PubMedPubMedCentralCrossRef
9.
go back to reference Storici P, Scocchi M, Tossi A, Gennaro R, Zanetti M: Chemical synthesis and biological activity of a novel antibacterial peptide deduced from a pig myeloid cDNA. FEBS Lett. 1994, 337: 303-7. 10.1016/0014-5793(94)80214-9.PubMedCrossRef Storici P, Scocchi M, Tossi A, Gennaro R, Zanetti M: Chemical synthesis and biological activity of a novel antibacterial peptide deduced from a pig myeloid cDNA. FEBS Lett. 1994, 337: 303-7. 10.1016/0014-5793(94)80214-9.PubMedCrossRef
10.
go back to reference Tossi A, Scocchi M, Zanetti M, Storici P, Gennaro R: PMAP-37, a novel antibacterial peptide from pig myeloid cells. cDNA cloning, chemical synthesis and activity. Eur J Biochem. 1995, 228: 941-6. 10.1111/j.1432-1033.1995.tb20344.x.PubMedCrossRef Tossi A, Scocchi M, Zanetti M, Storici P, Gennaro R: PMAP-37, a novel antibacterial peptide from pig myeloid cells. cDNA cloning, chemical synthesis and activity. Eur J Biochem. 1995, 228: 941-6. 10.1111/j.1432-1033.1995.tb20344.x.PubMedCrossRef
11.
go back to reference Zanetti M, Litteri L, Gennaro R, Horstmann H, Romeo D: Bactenecins, defense polypeptides of bovine neutrophils, are generated from precursor molecules stored in the large granules. J Cell Biol. 1990, 111: 1363-71. 10.1083/jcb.111.4.1363.PubMedCrossRef Zanetti M, Litteri L, Gennaro R, Horstmann H, Romeo D: Bactenecins, defense polypeptides of bovine neutrophils, are generated from precursor molecules stored in the large granules. J Cell Biol. 1990, 111: 1363-71. 10.1083/jcb.111.4.1363.PubMedCrossRef
12.
go back to reference Gallo RL, Ono M, Povsic T, Page C, Eriksson E, Klagsbrun M, Bernfield M: Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc Natl Acad Sci USA. 1994, 91: 11035-9. 10.1073/pnas.91.23.11035.PubMedPubMedCentralCrossRef Gallo RL, Ono M, Povsic T, Page C, Eriksson E, Klagsbrun M, Bernfield M: Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc Natl Acad Sci USA. 1994, 91: 11035-9. 10.1073/pnas.91.23.11035.PubMedPubMedCentralCrossRef
13.
go back to reference Frohm NM, Sandstedt B, Sorensen O, Weber G, Borregaard N, Stahle-Backdahl M: The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect Immun. 1999, 67: 2561-6. Frohm NM, Sandstedt B, Sorensen O, Weber G, Borregaard N, Stahle-Backdahl M: The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect Immun. 1999, 67: 2561-6.
14.
go back to reference Sorensen O, Arnljots K, Cowland JB, Bainton DF, Borregaard N: The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils. Blood. 1997, 90: 2796-803.PubMed Sorensen O, Arnljots K, Cowland JB, Bainton DF, Borregaard N: The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils. Blood. 1997, 90: 2796-803.PubMed
15.
go back to reference Agerberth B, Lee JY, Bergman T, Carlquist M, Boman HG, Mutt V, Jornvall H: Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur J Biochem. 1991, 202: 849-54. 10.1111/j.1432-1033.1991.tb16442.x.PubMedCrossRef Agerberth B, Lee JY, Bergman T, Carlquist M, Boman HG, Mutt V, Jornvall H: Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur J Biochem. 1991, 202: 849-54. 10.1111/j.1432-1033.1991.tb16442.x.PubMedCrossRef
16.
go back to reference Shi J, Ross CR, Chengappa MM, Blecha F: Identification of a proline-arginine-rich antibacterial peptide from neutrophils that is analogous to PR-39, an antibacterial peptide from the small intestine. J Leukoc Biol. 1994, 56: 807-11.PubMed Shi J, Ross CR, Chengappa MM, Blecha F: Identification of a proline-arginine-rich antibacterial peptide from neutrophils that is analogous to PR-39, an antibacterial peptide from the small intestine. J Leukoc Biol. 1994, 56: 807-11.PubMed
17.
go back to reference Shi J, Ross CR, Chengappa MM, Sylte MJ, McVey DS, Blecha F: Antibacterial activity of a synthetic peptide (PR-26) derived from PR-39, a proline-arginine-rich neutrophil antimicrobial peptide. Antimicrob Agents Chemother. 1996, 40: 115-21.PubMedPubMedCentral Shi J, Ross CR, Chengappa MM, Sylte MJ, McVey DS, Blecha F: Antibacterial activity of a synthetic peptide (PR-26) derived from PR-39, a proline-arginine-rich neutrophil antimicrobial peptide. Antimicrob Agents Chemother. 1996, 40: 115-21.PubMedPubMedCentral
18.
go back to reference Boman HG, Agerberth B, Boman A: Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun. 1993, 61: 2978-84.PubMedPubMedCentral Boman HG, Agerberth B, Boman A: Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun. 1993, 61: 2978-84.PubMedPubMedCentral
19.
go back to reference Ohtake T, Fujimoto Y, Ikuta K, Saito H, Ohhira M, Ono M, Kohgo Y: Proline-rich antimicrobial peptide, PR-39 gene transduction altered invasive activity and actin structure in human hepatocellular carcinoma cells. Br J Cancer. 1999, 8: 393-403. 10.1038/sj.bjc.6690707.CrossRef Ohtake T, Fujimoto Y, Ikuta K, Saito H, Ohhira M, Ono M, Kohgo Y: Proline-rich antimicrobial peptide, PR-39 gene transduction altered invasive activity and actin structure in human hepatocellular carcinoma cells. Br J Cancer. 1999, 8: 393-403. 10.1038/sj.bjc.6690707.CrossRef
20.
go back to reference Li J, Post M, Volk R, Gao Y, Li M, Metais C, Sato K, Tsai J, Aird W, Rosenberg RD, Hampton TG, Sellke F, Carmeliet P, Simons M: PR39, a peptide regulator of angiogenesis. Nat Med. 2000, 6: 49-55. 10.1038/71527.PubMedCrossRef Li J, Post M, Volk R, Gao Y, Li M, Metais C, Sato K, Tsai J, Aird W, Rosenberg RD, Hampton TG, Sellke F, Carmeliet P, Simons M: PR39, a peptide regulator of angiogenesis. Nat Med. 2000, 6: 49-55. 10.1038/71527.PubMedCrossRef
21.
go back to reference Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A: Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest. 1998, 101: 877-89.PubMedPubMedCentralCrossRef Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A: Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest. 1998, 101: 877-89.PubMedPubMedCentralCrossRef
22.
go back to reference Parmley RT, Hurst RE, Takagi M, Spicer SS, Austin RL: Glycosaminoglycans in human neutrophils and leukemic myeloblasts: ultrastructural, cytochemical, immunologic, and biochemical characterization. Blood. 1983, 61: 257-66.PubMed Parmley RT, Hurst RE, Takagi M, Spicer SS, Austin RL: Glycosaminoglycans in human neutrophils and leukemic myeloblasts: ultrastructural, cytochemical, immunologic, and biochemical characterization. Blood. 1983, 61: 257-66.PubMed
23.
go back to reference Yeaman C, Rapraeger AC: Membrane-anchored proteoglycans of mouse macrophages: P388D1 cells express a syndecan-4-like heparan sulfate proteoglycan and a distinct chondroitin sulfate form. J Cell Physiol. 1993, 157: 413-25. 10.1002/jcp.1041570226.PubMedCrossRef Yeaman C, Rapraeger AC: Membrane-anchored proteoglycans of mouse macrophages: P388D1 cells express a syndecan-4-like heparan sulfate proteoglycan and a distinct chondroitin sulfate form. J Cell Physiol. 1993, 157: 413-25. 10.1002/jcp.1041570226.PubMedCrossRef
24.
go back to reference Yeaman C, Rapraeger AC: Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol. 1993, 122: 941-50. 10.1083/jcb.122.4.941.PubMedCrossRef Yeaman C, Rapraeger AC: Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol. 1993, 122: 941-50. 10.1083/jcb.122.4.941.PubMedCrossRef
25.
go back to reference Huang HJ, Ross CR, Blecha F: Chemoattractant properties of PR-39, a neutrophil antibacterial peptide. J Leukoc Biol. 1997, 61: 624-9.PubMed Huang HJ, Ross CR, Blecha F: Chemoattractant properties of PR-39, a neutrophil antibacterial peptide. J Leukoc Biol. 1997, 61: 624-9.PubMed
26.
go back to reference Dunzendorfer S, Kaneider N, Rabensteiner A, Meierhofer C, Reinisch C, Romisch J, Wiedermann CJ: Cell-surface heparan sulfate proteoglycan-mediated regulation of human neutrophil migration by the serpin antithrombin III. Blood. 2001, 97: 1079-85. 10.1182/blood.V97.4.1079.PubMedCrossRef Dunzendorfer S, Kaneider N, Rabensteiner A, Meierhofer C, Reinisch C, Romisch J, Wiedermann CJ: Cell-surface heparan sulfate proteoglycan-mediated regulation of human neutrophil migration by the serpin antithrombin III. Blood. 2001, 97: 1079-85. 10.1182/blood.V97.4.1079.PubMedCrossRef
27.
go back to reference Mertens G, Cassiman JJ, Van den Berghe H, Vermylen J, David G: Cell surface heparan sulfate proteoglycans from human vascular endothelial cells. Core protein characterization and antithrombin III binding properties. J Biol Chem. 1992, 267: 20435-43.PubMed Mertens G, Cassiman JJ, Van den Berghe H, Vermylen J, David G: Cell surface heparan sulfate proteoglycans from human vascular endothelial cells. Core protein characterization and antithrombin III binding properties. J Biol Chem. 1992, 267: 20435-43.PubMed
28.
go back to reference James PE, Madhani M, Ross C, Klei L, Barchowsky A, Swartz HM: Tissue hypoxia during bacterial sepsis is attenuated by PR-39, an antibacterial peptide. Adv Exp Med Biol. 2003, 530: 645-52.PubMedCrossRef James PE, Madhani M, Ross C, Klei L, Barchowsky A, Swartz HM: Tissue hypoxia during bacterial sepsis is attenuated by PR-39, an antibacterial peptide. Adv Exp Med Biol. 2003, 530: 645-52.PubMedCrossRef
29.
go back to reference Madhani M, Barchowsky A, Klei L, Ross CR, Jackson SK, Swartz HM, James PE: Antibacterial peptide PR-39 affects local nitric oxide and preserves tissue oxygenation in the liver during septic shock. Biochim Biophys Acta. 2002, 1588: 232-40.PubMedCrossRef Madhani M, Barchowsky A, Klei L, Ross CR, Jackson SK, Swartz HM, James PE: Antibacterial peptide PR-39 affects local nitric oxide and preserves tissue oxygenation in the liver during septic shock. Biochim Biophys Acta. 2002, 1588: 232-40.PubMedCrossRef
30.
go back to reference De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ, Chertov O: 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, 192: 1069-74. 10.1084/jem.192.7.1069.CrossRef De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ, Chertov O: 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, 192: 1069-74. 10.1084/jem.192.7.1069.CrossRef
31.
go back to reference Niyonsaba F, Iwabuchi K, Someya A, Hirata M, Matsuda H, Ogawa H, Nagaoka I: A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology. 2000, 106: 20-6. 10.1046/j.1365-2567.2002.01398.x.CrossRef Niyonsaba F, Iwabuchi K, Someya A, Hirata M, Matsuda H, Ogawa H, Nagaoka I: A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology. 2000, 106: 20-6. 10.1046/j.1365-2567.2002.01398.x.CrossRef
32.
go back to reference Kaneider NC, Egger P, Dunzendorfer S, Wiedermann CJ: Syndecan-4 as antithrombin receptor of human neutrophils. Biochem Biophys Res Commun. 2001, 287: 42-6. 10.1006/bbrc.2001.5534.PubMedCrossRef Kaneider NC, Egger P, Dunzendorfer S, Wiedermann CJ: Syndecan-4 as antithrombin receptor of human neutrophils. Biochem Biophys Res Commun. 2001, 287: 42-6. 10.1006/bbrc.2001.5534.PubMedCrossRef
33.
go back to reference Cardin AD, Weintraub HJ: Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 1989, 9: 21-32.PubMedCrossRef Cardin AD, Weintraub HJ: Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 1989, 9: 21-32.PubMedCrossRef
34.
go back to reference Andersson E, Rydengard V, Sonesson A, Morgelin M, Bjorck L, Schmidtchen A: Antimicrobial activities of heparin-binding peptides. Eur J Biochem. 2004, 271: 1219-26. 10.1111/j.1432-1033.2004.04035.x.PubMedCrossRef Andersson E, Rydengard V, Sonesson A, Morgelin M, Bjorck L, Schmidtchen A: Antimicrobial activities of heparin-binding peptides. Eur J Biochem. 2004, 271: 1219-26. 10.1111/j.1432-1033.2004.04035.x.PubMedCrossRef
35.
go back to reference Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M: Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999, 68: 729-77. 10.1146/annurev.biochem.68.1.729.PubMedCrossRef Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M: Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999, 68: 729-77. 10.1146/annurev.biochem.68.1.729.PubMedCrossRef
36.
go back to reference Wadstrom T, Ljungh A: Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J Med Microbiol. 1999, 48: 223-33.PubMedCrossRef Wadstrom T, Ljungh A: Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J Med Microbiol. 1999, 48: 223-33.PubMedCrossRef
37.
go back to reference Kjellen L, Lindahl U: Proteoglycans: structures and interactions. Annu Rev Biochem. 1991, 60: 443-75. 10.1146/annurev.bi.60.070191.002303.PubMedCrossRef Kjellen L, Lindahl U: Proteoglycans: structures and interactions. Annu Rev Biochem. 1991, 60: 443-75. 10.1146/annurev.bi.60.070191.002303.PubMedCrossRef
38.
go back to reference Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ: Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992, 8: 365-93. 10.1146/annurev.cb.08.110192.002053.PubMedCrossRef Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ: Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992, 8: 365-93. 10.1146/annurev.cb.08.110192.002053.PubMedCrossRef
39.
go back to reference Chan YR, Gallo RL: PR-39, a syndecan-inducing antimicrobial peptide, binds and affects p130(Cas). J Biol Chem. 1998, 273: 28978-85. 10.1074/jbc.273.44.28978.PubMedCrossRef Chan YR, Gallo RL: PR-39, a syndecan-inducing antimicrobial peptide, binds and affects p130(Cas). J Biol Chem. 1998, 273: 28978-85. 10.1074/jbc.273.44.28978.PubMedCrossRef
40.
go back to reference Honda H, Nakamoto T, Sakai R, Hirai H: p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem Biophys Res Commun. 1999, 262: 25-30. 10.1006/bbrc.1999.1162.PubMedCrossRef Honda H, Nakamoto T, Sakai R, Hirai H: p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem Biophys Res Commun. 1999, 262: 25-30. 10.1006/bbrc.1999.1162.PubMedCrossRef
41.
go back to reference Cary LA, Han DC, Polte TR, Hanks SK, Guan JL: Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol. 1998, 140: 211-21. 10.1083/jcb.140.1.211.PubMedPubMedCentralCrossRef Cary LA, Han DC, Polte TR, Hanks SK, Guan JL: Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol. 1998, 140: 211-21. 10.1083/jcb.140.1.211.PubMedPubMedCentralCrossRef
42.
go back to reference Wilcox-Adelman SA, Denhez F, Goetinck PF: Syndecan-4 modulates focal adhesion kinase phosphorylation. J Biol Chem. 2002, 277: 32970-7. 10.1074/jbc.M201283200.PubMedCrossRef Wilcox-Adelman SA, Denhez F, Goetinck PF: Syndecan-4 modulates focal adhesion kinase phosphorylation. J Biol Chem. 2002, 277: 32970-7. 10.1074/jbc.M201283200.PubMedCrossRef
Metadata
Title
Heparan sulfate proteoglycan-dependent neutrophil chemotaxis toward PR-39 cathelicidin
Authors
Angela Djanani
Birgit Mosheimer
Nicole C Kaneider
Christopher R Ross
Giovanni Ricevuti
Josef R Patsch
Christian J Wiedermann
Publication date
01-12-2006
Publisher
BioMed Central
Published in
Journal of Inflammation / Issue 1/2006
Electronic ISSN: 1476-9255
DOI
https://doi.org/10.1186/1476-9255-3-14

Other articles of this Issue 1/2006

Journal of Inflammation 1/2006 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.