Globotriaosyl Ceramide Modulates Interferon-alpha-induced Growth Inhibition and CD19 Expression in Burkitt's Lymphoma Cells

Overview

Journal Glycoconj J

Publisher Springer

Specialties Biochemistry
Endocrinology

Date 2001 Jan 2

PMID 11133022

Citations 5

Authors

M D Maloney

C A Lingwood

Affiliations

Soon will be listed here.

Abstract

Previous studies have indicated that globotriaosyl ceramide (Gb3 or CD77) plays a role in alpha-interferon signal transduction and CD19-mediated homotypic adhesion in B cell lines derived from Burkitt's lymphoma. These roles for Gb3 may involve the proteins IFNAR-1 (subunit 1 of the interferon-alpha receptor) and CD19, respectively, both of which have potential Gb3-binding sites in their extracellular domains which resemble those of the verotoxin (Shiga toxin and Shiga-like toxin) B subunit. The majority of this work was performed using wild-type Daudi cells and a single, Gb3-deficient mutant cell line, VT500. In the present investigations, these and additional Daudi-derived cells with varying degrees of sensitivity to interferon-alpha were examined for Gb3 expression, interferon-induced growth inhibition and CD19 expression. The degree of interferon-induced growth inhibition and CD19 expression correlated with Gb3 expression in the various cell lines tested. In addition, reconstitution of the VT500 cell line with Gb3 but not other glycolipids partially restored the sensitivity of cells to IFN-induced growth inhibition. The degree to which reconstitution restored sensitivity to growth inhibition was similar to the results of previous studies in which Gb3 reconstitution restored sensitivity to verotoxin-induced cytotoxicity. These results demonstrate that Gb3 is specifically required for IFN-induced growth inhibition in Daudi cells and provide further evidence of a role for Gb3 in CD19 expression and function in these cells.

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References

Khine A, Firtel M, Lingwood C . CD77-dependent retrograde transport of CD19 to the nuclear membrane: functional relationship between CD77 and CD19 during germinal center B-cell apoptosis. J Cell Physiol. 1998; 176(2):281-92. DOI: 10.1002/(SICI)1097-4652(199808)176:2<281::AID-JCP6>3.0.CO;2-K. View

Ling H, Boodhoo A, Hazes B, Cummings M, Armstrong G, Brunton J . Structure of the shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry. 1998; 37(7):1777-88. DOI: 10.1021/bi971806n. View

Murray L, Habeshaw J, Wiels J, Greaves M . Expression of Burkitt lymphoma-associated antigen (defined by the monoclonal antibody 38.13) on both normal and malignant germinal-centre B cells. Int J Cancer. 1985; 36(5):561-5. DOI: 10.1002/ijc.2910360508. View

Arab S, Lingwood C . Intracellular targeting of the endoplasmic reticulum/nuclear envelope by retrograde transport may determine cell hypersensitivity to verotoxin via globotriaosyl ceramide fatty acid isoform traffic. J Cell Physiol. 1999; 177(4):646-60. DOI: 10.1002/(SICI)1097-4652(199812)177:4<646::AID-JCP15>3.0.CO;2-B. View

Taga S, Carlier K, Mishal Z, Capoulade C, Mangeney M, Lecluse Y . Intracellular signaling events in CD77-mediated apoptosis of Burkitt's lymphoma cells. Blood. 1997; 90(7):2757-67. View

Lingwood C, Law H, Richardson S, Petric M, Brunton J, de Grandis S . Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro. J Biol Chem. 1987; 262(18):8834-9. View

Hakomori S . Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J Biol Chem. 1990; 265(31):18713-6. View

Smith S, Rigley K, Callard R . Activation of human B cells through the CD19 surface antigen results in homotypic adhesion by LFA-1-dependent and -independent mechanisms. Immunology. 1991; 73(3):293-7. PMC: 1384545. View

Liu Y, Arpin C, de Bouteiller O, Guret C, Banchereau J, Martinez-Valdez H . Sequential triggering of apoptosis, somatic mutation and isotype switch during germinal center development. Semin Immunol. 1996; 8(3):169-77. DOI: 10.1006/smim.1996.0021. View

10.

Lingwood C, Yiu S . Glycolipid modification of alpha 2 interferon binding. Sequence similarity between the alpha 2 interferon receptor and verotoxin (Shiga-like toxin) B-subunit. Biochem J. 1992; 283 ( Pt 1):25-6. PMC: 1130985. DOI: 10.1042/bj2830025. View

11.

Mazur E, Richtsmeier W, South K . Alpha-interferon: differential suppression of colony growth from human erythroid, myeloid, and megakaryocytic hematopoietic progenitor cells. J Interferon Res. 1986; 6(3):199-206. DOI: 10.1089/jir.1986.6.199. View

12.

Sandvig K, Garred O, Prydz K, Kozlov J, Hansen S, van Deurs B . Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature. 1992; 358(6386):510-2. DOI: 10.1038/358510a0. View

13.

Balana A, Wiels J, Tetaud C, Mishal Z, Tursz T . Induction of cell differentiation in Burkitt lymphoma lines. BLA: a glycolipid marker of B-cell differentiation. Int J Cancer. 1985; 36(4):453-60. DOI: 10.1002/ijc.2910360407. View

14.

Lingwood C . Verotoxin-binding in human renal sections. Nephron. 1994; 66(1):21-8. DOI: 10.1159/000187761. View

15.

Fearon D, Carter R . The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol. 1995; 13:127-49. DOI: 10.1146/annurev.iy.13.040195.001015. View

16.

Ilangumaran S, Briol A, Hoessli D . CD44 selectively associates with active Src family protein tyrosine kinases Lck and Fyn in glycosphingolipid-rich plasma membrane domains of human peripheral blood lymphocytes. Blood. 1998; 91(10):3901-8. View

17.

Behr S, Schriever F . Engaging CD19 or target of an antiproliferative antibody 1 on human B lymphocytes induces binding of B cells to the interfollicular stroma of human tonsils via integrin alpha 4/beta 1 and fibronectin. J Exp Med. 1995; 182(5):1191-9. PMC: 2192200. DOI: 10.1084/jem.182.5.1191. View

18.

Magnani J, Smith D, Ginsburg V . Detection of gangliosides that bind cholera toxin: direct binding of 125I-labeled toxin to thin-layer chromatograms. Anal Biochem. 1980; 109(2):399-402. DOI: 10.1016/0003-2697(80)90667-3. View

19.

Cheng P, Dykstra M, Mitchell R, Pierce S . A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J Exp Med. 1999; 190(11):1549-60. PMC: 2195743. DOI: 10.1084/jem.190.11.1549. View

20.

Lingwood C, Khine A, Arab S . Globotriaosyl ceramide (Gb3) expression in human tumour cells: intracellular trafficking defines a new retrograde transport pathway from the cell surface to the nucleus, which correlates with sensitivity to verotoxin. Acta Biochim Pol. 1998; 45(2):351-9. View