Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1994 Nov;94(5):1968–1973. doi: 10.1172/JCI117548

Role of the GRO family of chemokines in monocyte adhesion to MM-LDL-stimulated endothelium.

D Schwartz 1, A Andalibi 1, L Chaverri-Almada 1, J A Berliner 1, T Kirchgessner 1, Z T Fang 1, P Tekamp-Olson 1, A J Lusis 1, C Gallegos 1, A M Fogelman 1, et al.
PMCID: PMC294616  PMID: 7962543

Abstract

We have previously shown that treatment of endothelial cells with minimally modified LDL (MM-LDL) induces the binding of monocytes to unknown endothelial receptor molecules. We now report that a member of the GRO family of chemokines plays a role in MM-LDL-induced monocyte binding. A cDNA library made from rabbit aortic endothelial cells (RAEC) treated with MM-LDL was expression screened for molecules inducing binding of a human monocyte cell line (THP-1). A cDNA was isolated with 75% homology to GRO. GRO mRNA levels were significantly elevated after exposure of RAEC or human aortic endothelial cells (HAEC) to MM-LDL. HAEC treated with MM-LDL displayed an increase in a surface-associated protein that bound to antibody against GRO despite low levels of GRO in the medium. Antibody to GRO significantly inhibited the binding of monocytes to MM-LDL-treated RAEC and HAEC. The increase in GRO expression and monocyte binding were reduced by incubating MM-LDL-treated endothelial cells with heparin (in a method that releases heparan sulfate bound molecules from the cell surface). These results suggest that GRO related chemokines are bound to the surface of MM-LDL-treated endothelial cells and may contribute to the monocyte adhesion induced by MM-LDL.

Full text

PDF
1968

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aruffo A., Seed B. Molecular cloning of a CD28 cDNA by a high-efficiency COS cell expression system. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8573–8577. doi: 10.1073/pnas.84.23.8573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berliner J. A., Schwartz D. S., Territo M. C., Andalibi A., Almada L., Lusis A. J., Quismorio D., Fang Z. P., Fogelman A. M. Induction of chemotactic cytokines by minimally oxidized LDL. Adv Exp Med Biol. 1993;351:13–18. doi: 10.1007/978-1-4615-2952-1_2. [DOI] [PubMed] [Google Scholar]
  3. Berliner J. A., Territo M. C., Sevanian A., Ramin S., Kim J. A., Bamshad B., Esterson M., Fogelman A. M. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J Clin Invest. 1990 Apr;85(4):1260–1266. doi: 10.1172/JCI114562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berliner J. A., Territo M., Almada L., Carter A., Shafonsky E., Fogelman A. M. Monocyte chemotactic factor produced by large vessel endothelial cells in vitro. Arteriosclerosis. 1986 May-Jun;6(3):254–258. doi: 10.1161/01.atv.6.3.254. [DOI] [PubMed] [Google Scholar]
  5. Bork R. W., Svenson K. L., Mehrabian M., Lusis A. J., Fogelman A. M., Edwards P. A. Mechanisms controlling competence gene expression in murine fibroblasts stimulated with minimally modified LDL. Arterioscler Thromb. 1992 Jul;12(7):800–806. doi: 10.1161/01.atv.12.7.800. [DOI] [PubMed] [Google Scholar]
  6. Busch C., Dawes J., Pepper D. S., Wasteson A. Binding of platelet factor 4 to cultured human umbilical vein endothelial cells. Thromb Res. 1980 Jul 1;19(1-2):129–137. doi: 10.1016/0049-3848(80)90412-0. [DOI] [PubMed] [Google Scholar]
  7. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  8. Cheng Q. C., Han J. H., Thomas H. G., Balentien E., Richmond A. The melanoma growth stimulatory activity receptor consists of two proteins. Ligand binding results in enhanced tyrosine phosphorylation. J Immunol. 1992 Jan 15;148(2):451–456. [PubMed] [Google Scholar]
  9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  10. Clore G. M., Appella E., Yamada M., Matsushima K., Gronenborn A. M. Determination of the secondary structure of interleukin-8 by nuclear magnetic resonance spectroscopy. J Biol Chem. 1989 Nov 15;264(32):18907–18911. [PubMed] [Google Scholar]
  11. Clore G. M., Appella E., Yamada M., Matsushima K., Gronenborn A. M. Three-dimensional structure of interleukin 8 in solution. Biochemistry. 1990 Feb 20;29(7):1689–1696. doi: 10.1021/bi00459a004. [DOI] [PubMed] [Google Scholar]
  12. Cushing S. D., Berliner J. A., Valente A. J., Territo M. C., Navab M., Parhami F., Gerrity R., Schwartz C. J., Fogelman A. M. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5134–5138. doi: 10.1073/pnas.87.13.5134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cushing S. D., Fogelman A. M. Monocytes may amplify their recruitment into inflammatory lesions by inducing monocyte chemotactic protein. Arterioscler Thromb. 1992 Jan;12(1):78–82. doi: 10.1161/01.atv.12.1.78. [DOI] [PubMed] [Google Scholar]
  14. Fogelman A. M., Elahi F., Sykes K., Van Lenten B. J., Territo M. C., Berliner J. A. Modification of the Recalde method for the isolation of human monocytes. J Lipid Res. 1988 Sep;29(9):1243–1247. [PubMed] [Google Scholar]
  15. Gallagher J. T., Lyon M., Steward W. P. Structure and function of heparan sulphate proteoglycans. Biochem J. 1986 Jun 1;236(2):313–325. doi: 10.1042/bj2360313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Haskill S., Peace A., Morris J., Sporn S. A., Anisowicz A., Lee S. W., Smith T., Martin G., Ralph P., Sager R. Identification of three related human GRO genes encoding cytokine functions. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7732–7736. doi: 10.1073/pnas.87.19.7732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hession C., Osborn L., Goff D., Chi-Rosso G., Vassallo C., Pasek M., Pittack C., Tizard R., Goelz S., McCarthy K. Endothelial leukocyte adhesion molecule 1: direct expression cloning and functional interactions. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1673–1677. doi: 10.1073/pnas.87.5.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iida N., Grotendorst G. R. Cloning and sequencing of a new gro transcript from activated human monocytes: expression in leukocytes and wound tissue. Mol Cell Biol. 1990 Oct;10(10):5596–5599. doi: 10.1128/mcb.10.10.5596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jackson R. L., Busch S. J., Cardin A. D. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev. 1991 Apr;71(2):481–539. doi: 10.1152/physrev.1991.71.2.481. [DOI] [PubMed] [Google Scholar]
  20. Jose P. J., Collins P. D., Perkins J. A., Beaubien B. C., Totty N. F., Waterfield M. D., Hsuan J., Williams T. J. Identification of a second neutrophil-chemoattractant cytokine generated during an inflammatory reaction in the rabbit peritoneal cavity in vivo. Purification, partial amino acid sequence and structural relationship to melanoma-growth-stimulatory activity. Biochem J. 1991 Sep 1;278(Pt 2):493–497. doi: 10.1042/bj2780493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Loscalzo J., Melnick B., Handin R. I. The interaction of platelet factor four and glycosaminoglycans. Arch Biochem Biophys. 1985 Jul;240(1):446–455. doi: 10.1016/0003-9861(85)90049-9. [DOI] [PubMed] [Google Scholar]
  22. Loscalzo J., Melnick B., Handin R. I. The interaction of platelet factor four and glycosaminoglycans. Arch Biochem Biophys. 1985 Jul;240(1):446–455. doi: 10.1016/0003-9861(85)90049-9. [DOI] [PubMed] [Google Scholar]
  23. Moser B., Clark-Lewis I., Zwahlen R., Baggiolini M. Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med. 1990 May 1;171(5):1797–1802. doi: 10.1084/jem.171.5.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moser B., Schumacher C., von Tscharner V., Clark-Lewis I., Baggiolini M. Neutrophil-activating peptide 2 and gro/melanoma growth-stimulatory activity interact with neutrophil-activating peptide 1/interleukin 8 receptors on human neutrophils. J Biol Chem. 1991 Jun 5;266(16):10666–10671. [PubMed] [Google Scholar]
  25. Mukaida N., Hishinuma A., Zachariae C. O., Oppenheim J. J., Matsushima K. Regulation of human interleukin 8 gene expression and binding of several other members of the intercrine family to receptors for interleukin-8. Adv Exp Med Biol. 1991;305:31–38. doi: 10.1007/978-1-4684-6009-4_4. [DOI] [PubMed] [Google Scholar]
  26. Oppenheim J. J., Zachariae C. O., Mukaida N., Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617–648. doi: 10.1146/annurev.iy.09.040191.003153. [DOI] [PubMed] [Google Scholar]
  27. Parhami F., Fang Z. T., Fogelman A. M., Andalibi A., Territo M. C., Berliner J. A. Minimally modified low density lipoprotein-induced inflammatory responses in endothelial cells are mediated by cyclic adenosine monophosphate. J Clin Invest. 1993 Jul;92(1):471–478. doi: 10.1172/JCI116590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raines E. W., Ross R. Compartmentalization of PDGF on extracellular binding sites dependent on exon-6-encoded sequences. J Cell Biol. 1992 Jan;116(2):533–543. doi: 10.1083/jcb.116.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rajavashisth T. B., Andalibi A., Territo M. C., Berliner J. A., Navab M., Fogelman A. M., Lusis A. J. Induction of endothelial cell expression of granulocyte and macrophage colony-stimulating factors by modified low-density lipoproteins. Nature. 1990 Mar 15;344(6263):254–257. doi: 10.1038/344254a0. [DOI] [PubMed] [Google Scholar]
  30. Richmond A., Lawson D. H., Nixon D. W., Stevens J. S., Chawla R. K. Extraction of a melanoma growth-stimulatory activity from culture medium conditioned by the Hs0294 human melanoma cell line. Cancer Res. 1983 May;43(5):2106–2112. [PubMed] [Google Scholar]
  31. Rot A. Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol Today. 1992 Aug;13(8):291–294. doi: 10.1016/0167-5699(92)90039-A. [DOI] [PubMed] [Google Scholar]
  32. Rot A. Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur J Immunol. 1993 Jan;23(1):303–306. doi: 10.1002/eji.1830230150. [DOI] [PubMed] [Google Scholar]
  33. Sager R., Haskill S., Anisowicz A., Trask D., Pike M. C. GRO: a novel chemotactic cytokine. Adv Exp Med Biol. 1991;305:73–77. doi: 10.1007/978-1-4684-6009-4_9. [DOI] [PubMed] [Google Scholar]
  34. Schiffer M., Edmundson A. B. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys J. 1967 Mar;7(2):121–135. doi: 10.1016/S0006-3495(67)86579-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schröder J. M., Persoon N. L., Christophers E. Lipopolysaccharide-stimulated human monocytes secrete, apart from neutrophil-activating peptide 1/interleukin 8, a second neutrophil-activating protein. NH2-terminal amino acid sequence identity with melanoma growth stimulatory activity. J Exp Med. 1990 Apr 1;171(4):1091–1100. doi: 10.1084/jem.171.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shimada K., Gill P. J., Silbert J. E., Douglas W. H., Fanburg B. L. Involvement of cell surface heparin sulfate in the binding of lipoprotein lipase to cultured bovine endothelial cells. J Clin Invest. 1981 Oct;68(4):995–1002. doi: 10.1172/JCI110354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sparrow C. P., Parthasarathy S., Steinberg D. Enzymatic modification of low density lipoprotein by purified lipoxygenase plus phospholipase A2 mimics cell-mediated oxidative modification. J Lipid Res. 1988 Jun;29(6):745–753. [PubMed] [Google Scholar]
  38. St Charles R., Walz D. A., Edwards B. F. The three-dimensional structure of bovine platelet factor 4 at 3.0-A resolution. J Biol Chem. 1989 Feb 5;264(4):2092–2099. [PubMed] [Google Scholar]
  39. Takeya M., Yoshimura T., Leonard E. J., Kato T., Okabe H., Takahashi K. Production of monocyte chemoattractant protein-1 by malignant fibrous histiocytoma: relation to the origin of histiocyte-like cells. Exp Mol Pathol. 1991 Feb;54(1):61–71. doi: 10.1016/0014-4800(91)90044-x. [DOI] [PubMed] [Google Scholar]
  40. Tanaka Y., Adams D. H., Hubscher S., Hirano H., Siebenlist U., Shaw S. T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1 beta. Nature. 1993 Jan 7;361(6407):79–82. doi: 10.1038/361079a0. [DOI] [PubMed] [Google Scholar]
  41. Tekamp-Olson P., Gallegos C., Bauer D., McClain J., Sherry B., Fabre M., van Deventer S., Cerami A. Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J Exp Med. 1990 Sep 1;172(3):911–919. doi: 10.1084/jem.172.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Walz A., Meloni F., Clark-Lewis I., von Tscharner V., Baggiolini M. [Ca2+]i changes and respiratory burst in human neutrophils and monocytes induced by NAP-1/interleukin-8, NAP-2, and gro/MGSA. J Leukoc Biol. 1991 Sep;50(3):279–286. doi: 10.1002/jlb.50.3.279. [DOI] [PubMed] [Google Scholar]
  43. Watanabe K., Konishi K., Fujioka M., Kinoshita S., Nakagawa H. The neutrophil chemoattractant produced by the rat kidney epithelioid cell line NRK-52E is a protein related to the KC/gro protein. J Biol Chem. 1989 Nov 25;264(33):19559–19563. [PubMed] [Google Scholar]
  44. Webb L. M., Ehrengruber M. U., Clark-Lewis I., Baggiolini M., Rot A. Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7158–7162. doi: 10.1073/pnas.90.15.7158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wen D. Z., Rowland A., Derynck R. Expression and secretion of gro/MGSA by stimulated human endothelial cells. EMBO J. 1989 Jun;8(6):1761–1766. doi: 10.1002/j.1460-2075.1989.tb03569.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wolpe S. D., Cerami A. Macrophage inflammatory proteins 1 and 2: members of a novel superfamily of cytokines. FASEB J. 1989 Dec;3(14):2565–2573. doi: 10.1096/fasebj.3.14.2687068. [DOI] [PubMed] [Google Scholar]
  47. Zimmerman G. A., McIntyre T. M., Mehra M., Prescott S. M. Endothelial cell-associated platelet-activating factor: a novel mechanism for signaling intercellular adhesion. J Cell Biol. 1990 Feb;110(2):529–540. doi: 10.1083/jcb.110.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES