Modification of P-selectin Glycoprotein Ligand-1 with a Natural Killer Cell-restricted Sulfated Lactosamine Creates an Alternate Ligand for L-selectin

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2000 Mar 22

PMID 10725346

Citations 21

Authors

P Andre

O Spertini

S Guia

P Rihet

F Dignat-George

H Brailly

J Sampol

P J Anderson

E Vivier

Affiliations

Soon will be listed here.

Abstract

Natural killer (NK) cells are components of the innate immune system that can recognize and kill virally infected cells, tumor cells, and allogeneic cells without prior sensitization. NK cells also elaborate cytokines (e.g., interferon-gamma and tumor necrosis factor-alpha) and chemokines (e.g., macrophage inflammatory protein-1alpha) that promote the acquisition of antigen-specific immunity. NK cell differentiation is accompanied by the cell surface expression of a mucin-like glycoprotein bearing an NK cell-restricted keratan sulfate-related lactosamine carbohydrate, the PEN5 epitope. Here, we report that PEN5 is a post-translational modification of P-selectin glycoprotein ligand-1 (PSGL-1). The PEN5 epitope creates on PSGL-1 a unique binding site for L-selectin, which is independent of PSGL-1 tyrosine sulfation. On the surface of NK cells, the expression of PEN5 is coordinated with the disappearance of L-selectin and the up-regulation of Killer cell Ig-like Receptors (KIR). These results indicate that NK cell differentiation is accompanied by the acquisition of a unique carbohydrate, PEN5, that can serve as part of a combination code to deliver KIR(+) NK cells to specific tissues.

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References

Frey M, Packianathan N, Fehniger T, Ross M, Wang W, Stewart C . Differential expression and function of L-selectin on CD56bright and CD56dim natural killer cell subsets. J Immunol. 1998; 161(1):400-8. View

Biron C, Nguyen K, Pien G, Cousens L, Salazar-Mather T . Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol. 1999; 17:189-220. DOI: 10.1146/annurev.immunol.17.1.189. View

McEver R, Moore K, Cummings R . Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem. 1995; 270(19):11025-8. DOI: 10.1074/jbc.270.19.11025. View

McIntyre K, Welsh R . Accumulation of natural killer and cytotoxic T large granular lymphocytes in the liver during virus infection. J Exp Med. 1986; 164(5):1667-81. PMC: 2188440. DOI: 10.1084/jem.164.5.1667. View

Snapp K, Ding H, Atkins K, Warnke R, Luscinskas F, Kansas G . A novel P-selectin glycoprotein ligand-1 monoclonal antibody recognizes an epitope within the tyrosine sulfate motif of human PSGL-1 and blocks recognition of both P- and L-selectin. Blood. 1998; 91(1):154-64. View

Walcheck B, Moore K, McEver R, Kishimoto T . Neutrophil-neutrophil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1. A mechanism that amplifies initial leukocyte accumulation of P-selectin in vitro. J Clin Invest. 1996; 98(5):1081-7. PMC: 507527. DOI: 10.1172/JCI118888. View

Borges E, Pendl G, Eytner R, Steegmaier M, Zollner O, Vestweber D . The binding of T cell-expressed P-selectin glycoprotein ligand-1 to E- and P-selectin is differentially regulated. J Biol Chem. 1997; 272(45):28786-92. DOI: 10.1074/jbc.272.45.28786. View

Long E . Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999; 17:875-904. DOI: 10.1146/annurev.immunol.17.1.875. View

Baume D, Robertson M, Levine H, Manley T, Schow P, Ritz J . Differential responses to interleukin 2 define functionally distinct subsets of human natural killer cells. Eur J Immunol. 1992; 22(1):1-6. DOI: 10.1002/eji.1830220102. View

10.

Tu L, Chen A, Delahunty M, Moore K, Watson S, McEver R . L-selectin binds to P-selectin glycoprotein ligand-1 on leukocytes: interactions between the lectin, epidermal growth factor, and consensus repeat domains of the selectins determine ligand binding specificity. J Immunol. 1996; 157(9):3995-4004. View

11.

Bianchi G, Sironi M, Ghibaudi E, Selvaggini C, Elices M, Allavena P . Migration of natural killer cells across endothelial cell monolayers. J Immunol. 1993; 151(10):5135-44. View

12.

Vivier E, Sorrell J, Ackerly M, Robertson M, Rasmussen R, Levine H . Developmental regulation of a mucinlike glycoprotein selectively expressed on natural killer cells. J Exp Med. 1993; 178(6):2023-33. PMC: 2191265. DOI: 10.1084/jem.178.6.2023. View

13.

Ohmori K, Takada A, Yoneda T, Buma Y, Hirashima K, Tsuyuoka K . Differentiation-dependent expression of sialyl stage-specific embryonic antigen-1 and I-antigens on human lymphoid cells and its implications for carbohydrate-mediated adhesion to vascular endothelium. Blood. 1993; 81(1):101-11. View

14.

Baumheter S, Singer M, Henzel W, Hemmerich S, Renz M, Rosen S . Binding of L-selectin to the vascular sialomucin CD34. Science. 1993; 262(5132):436-8. DOI: 10.1126/science.7692600. View

15.

De Luca M, Dunlop L, Andrews R, Flannery Jr J, Ettling R, Cumming D . A novel cobra venom metalloproteinase, mocarhagin, cleaves a 10-amino acid peptide from the mature N terminus of P-selectin glycoprotein ligand receptor, PSGL-1, and abolishes P-selectin binding. J Biol Chem. 1995; 270(45):26734-7. DOI: 10.1074/jbc.270.45.26734. View

16.

Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari M . Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol. 1996; 14:619-48. DOI: 10.1146/annurev.immunol.14.1.619. View

17.

Berman M, Xie Y, Muller W . Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation. J Immunol. 1996; 156(4):1515-24. View

18.

Sako D, Comess K, Barone K, Camphausen R, Cumming D, Shaw G . A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell. 1995; 83(2):323-31. DOI: 10.1016/0092-8674(95)90173-6. View

19.

Springer T . Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994; 76(2):301-14. DOI: 10.1016/0092-8674(94)90337-9. View

20.

Berg E, McEvoy L, Berlin C, Bargatze R, Butcher E . L-selectin-mediated lymphocyte rolling on MAdCAM-1. Nature. 1993; 366(6456):695-8. DOI: 10.1038/366695a0. View