Galectin-4 and Sulfatides in Apical Membrane Trafficking in Enterocyte-like Cells

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2005 May 11

PMID 15883199

Citations 93

Authors

Delphine Delacour

Valerie Gouyer

Jean-Pierre Zanetta

Herve Drobecq

Emmanuelle Leteurtre

Georges Grard

Odile Moreau-Hannedouche

Emmanuel Maes

Alexandre Pons

Sabine Andre

Andre Le Bivic

Hans Joachim Gabius

Aki Manninen

Kai Simons

Guillemette Huet

Affiliations

Soon will be listed here.

Abstract

We have previously reported that 1-benzyl-2-acetamido-2-deoxy-alpha-D-galactopyranoside (GalNAc alpha-O-bn), an inhibitor of glycosylation, perturbed apical biosynthetic trafficking in polarized HT-29 cells suggesting an involvement of a lectin-based mechanism. Here, we have identified galectin-4 as one of the major components of detergent-resistant membranes (DRMs) isolated from HT-29 5M12 cells. Galectin-4 was also found in post-Golgi carrier vesicles. The functional role of galectin-4 in polarized trafficking in HT-29 5M12 cells was studied by using a retrovirus-mediated RNA interference. In galectin-4-depleted HT-29 5M12 cells apical membrane markers accumulated intracellularly. In contrast, basolateral membrane markers were not affected. Moreover, galectin-4 depletion altered the DRM association characteristics of apical proteins. Sulfatides with long chain-hydroxylated fatty acids, which were also enriched in DRMs, were identified as high-affinity ligands for galectin-4. Together, our data propose that interaction between galectin-4 and sulfatides plays a functional role in the clustering of lipid rafts for apical delivery.

Citing Articles

Intracellular galectin interactions in health and disease.

Jacob R, Gorek L Semin Immunopathol. 2024; 46(1-2):4.

PMID: 38990375 PMC: 11239732. DOI: 10.1007/s00281-024-01010-z.

Galectin-4 is associated with diabetes and obesity in a heart failure population.

Dieden A, Gudmundsson P, Korduner J, Molvin J, Zaghi A, Nezami Z Sci Rep. 2023; 13(1):20285.

PMID: 37985679 PMC: 10662206. DOI: 10.1038/s41598-023-47426-9.

Plasma Galectin-4 Levels Are Increased after Stroke in Mice and Humans.

Jujic A, Vieira J, Matuskova H, Nilsson P, Lindblad U, Olsen M Int J Mol Sci. 2023; 24(12).

PMID: 37373212 PMC: 10298636. DOI: 10.3390/ijms241210064.

Oligosaccharide Ligands of Galectin-4 and Its Subunits: Multivalency Scores Highly.

Slamova K, cerveny J, Meszaros Z, Friede T, Vrbata D, Kren V Molecules. 2023; 28(10).

PMID: 37241779 PMC: 10223884. DOI: 10.3390/molecules28104039.

Galectins-Potential Therapeutic Targets for Neurodegenerative Disorders.

Chaudhary S, Chaudhary S, Rawat S, Kulkarni A, Bilgrami A, Perveen A Int J Mol Sci. 2022; 23(19).

PMID: 36232314 PMC: 9569834. DOI: 10.3390/ijms231911012.

References

Nickel W . The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem. 2003; 270(10):2109-19. DOI: 10.1046/j.1432-1033.2003.03577.x. View

Nagy N, Legendre H, Engels O, Andre S, Kaltner H, Wasano K . Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin fingerprinting. Cancer. 2003; 97(8):1849-58. DOI: 10.1002/cncr.11268. View

Wice B, Gordon J . A strategy for isolation of cDNAs encoding proteins affecting human intestinal epithelial cell growth and differentiation: characterization of a novel gut-specific N-myristoylated annexin. J Cell Biol. 1992; 116(2):405-22. PMC: 2289284. DOI: 10.1083/jcb.116.2.405. View

Fullekrug J, Scheiffele P, Simons K . VIP36 localisation to the early secretory pathway. J Cell Sci. 1999; 112 ( Pt 17):2813-21. DOI: 10.1242/jcs.112.17.2813. View

Folsch H, Ohno H, Bonifacino J, Mellman I . A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell. 1999; 99(2):189-98. DOI: 10.1016/s0092-8674(00)81650-5. View

Gorvel J, Ferrero A, Chambraud L, Rigal A, Bonicel J, MAROUX S . Expression of sucrase-isomaltase and dipeptidylpeptidase IV in human small intestine and colon. Gastroenterology. 1991; 101(3):618-25. DOI: 10.1016/0016-5085(91)90517-o. View

Byrd J, Dahiya R, Huang J, Kim Y . Inhibition of mucin synthesis by benzyl-alpha-GalNAc in KATO III gastric cancer and Caco-2 colon cancer cells. Eur J Cancer. 1995; 31A(9):1498-505. DOI: 10.1016/0959-8049(95)00248-h. View

Ideo H, Seko A, Ohkura T, Matta K, Yamashita K . High-affinity binding of recombinant human galectin-4 to SO(3)(-)-->3Galbeta1-->3GalNAc pyranoside. Glycobiology. 2002; 12(3):199-208. DOI: 10.1093/glycob/12.3.199. View

Dunphy J, Barcham G, Bischof R, Young A, Nash A, Meeusen E . Isolation and characterization of a novel eosinophil-specific galectin released into the lungs in response to allergen challenge. J Biol Chem. 2002; 277(17):14916-24. DOI: 10.1074/jbc.M200214200. View

10.

Nelson W . Adaptation of core mechanisms to generate cell polarity. Nature. 2003; 422(6933):766-74. PMC: 3373010. DOI: 10.1038/nature01602. View

11.

Scheiffele P, Verkade P, Fra A, Virta H, Simons K, Ikonen E . Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J Cell Biol. 1998; 140(4):795-806. PMC: 2141752. DOI: 10.1083/jcb.140.4.795. View

12.

ISHIZUKA I . Complete 1H and 13C NMR assignment of mono-sulfated galactosylceramides with four types of ceramides from human kidney. Carbohydr Res. 2000; 324(3):218-22. DOI: 10.1016/s0008-6215(99)00291-8. View

13.

Scheiffele P, Peranen J, Simons K . N-glycans as apical sorting signals in epithelial cells. Nature. 1995; 378(6552):96-8. DOI: 10.1038/378096a0. View

14.

Fiedler K, Simons K . Characterization of VIP36, an animal lectin homologous to leguminous lectins. J Cell Sci. 1996; 109 ( Pt 1):271-6. DOI: 10.1242/jcs.109.1.271. View

15.

Mostov K, Verges M, Altschuler Y . Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol. 2000; 12(4):483-90. DOI: 10.1016/s0955-0674(00)00120-4. View

16.

Brewer C . Binding and cross-linking properties of galectins. Biochim Biophys Acta. 2002; 1572(2-3):255-62. DOI: 10.1016/s0304-4165(02)00312-4. View

17.

Gharahdaghi F, Weinberg C, Meagher D, Imai B, Mische S . Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis. 1999; 20(3):601-5. DOI: 10.1002/(SICI)1522-2683(19990301)20:3<601::AID-ELPS601>3.0.CO;2-6. View

18.

Monlauzeur L, Breuza L, Le Bivic A . Putative O-glycosylation sites and a membrane anchor are necessary for apical delivery of the human neurotrophin receptor in Caco-2 cells. J Biol Chem. 1998; 273(46):30263-70. DOI: 10.1074/jbc.273.46.30263. View

19.

Le Bivic A, Real F, Rodriguez-Boulan E . Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc Natl Acad Sci U S A. 1989; 86(23):9313-7. PMC: 298485. DOI: 10.1073/pnas.86.23.9313. View

20.

Danielsen E, van Deurs B . Galectin-4 and small intestinal brush border enzymes form clusters. Mol Biol Cell. 1997; 8(11):2241-51. PMC: 25705. DOI: 10.1091/mbc.8.11.2241. View