Sulfation of O-glycans on mucin-type proteins from serous ovarian epithelial tumors (original) (raw)

Abstract

Ovarian cancer tissue contains highly sulfated O-glycoproteins. • Sulfation occurs on GlcNAc (6-position) and Gal (3-and 6-position). • Sulfation of Gal can be mimicked recombinantly with selected sulfotransferase. • The Gal3ST2 sulfotransferase level is lower in malignant cancer compared with benign.

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References (37)

  1. Lheureux, S., Gourley, C., Vergote, I., and Oza, A. M. (2019) Epithelial ovarian cancer. Lancet 393, 1240-1253
  2. Wu, A. M. (2019) Glycan structures and their recognition roles in the human blood group ABH/Ii, Lea, b, x, y and Sialyl Lea,x active cyst glycoproteins. Glycoconj. J. 36, 495-507
  3. Elzek, M. A., and Rodland, K. D. (2015) Proteomics of ovarian cancer: Functional insights and clinical applications. Cancer Metastasis Rev. 34, 83-96
  4. Kristjansdottir, B., Levan, K., Partheen, K., Carlsohn, E., and Sundfeldt, K. (2013) Potential tumor biomarkers identified in ovarian cyst fluid by quantitative proteomic analysis, iTRAQ. Clin. Proteomics 10, 4
  5. van Putten, J. P. M., and Strijbis, K. (2017) Transmembrane mucins: Signaling receptors at the intersection of inflammation and cancer. J. Innate Immun. 9, 281-299
  6. Christiansen, M. N., Chik, J., Lee, L., Anugraham, M., Abrahams, J. L., and Packer, N. H. (2014) Cell surface protein glycosylation in cancer. Prote- omics 14, 525-546
  7. Duarte, H. O., Freitas, D., Gomes, C., Gomes, J., Magalhães, A., and Reis, C. A. (2016) Mucin-type O-glycosylation in gastric carcinogenesis. Bio- molecules 6, 33
  8. Jabbar, K. S., Arike, L., Verbeke, C. S., Sadik, R., and Hansson, G. C. (2018) Highly accurate identification of cystic precursor lesions of pancreatic cancer through targeted mass spectrometry: A phase IIc diagnostic study. J. Clin. Oncol. 36, 367-375
  9. Yin, B. W., and Lloyd, K. O. (2001) Molecular cloning of the CA125 ovarian cancer antigen: Identification as a new mucin, MUC16. J. Biol. Chem. 276, 27371-27375
  10. Chen, K., Gentry-Maharaj, A., Burnell, M., Steentoft, C., Marcos-Silva, L., Mandel, U., Jacobs, I., Dawnay, A., Menon, U., and Blixt, O. (2013) Microarray glycoprofiling of CA125 improves differential diagnosis of ovarian cancer. J. Proteome Res. 12, 1408-1418
  11. Ricardo, S., Marcos-Silva, L., Valente, C., Coelho, R., Gomes, R., and Da- vid, L. (2016) Mucins MUC16 and MUC1 are major carriers of SLe(a) and SLe(x) in borderline and malignant serous ovarian tumors. Virchows Arch. 468, 715-722
  12. Ricardo, S., Marcos-Silva, L., Pereira, D., Pinto, R., Almeida, R., Soderberg, O., Mandel, U., Clausen, H., Felix, A., Lunet, N., and David, L. (2015) Detection of glyco-mucin profiles improves specificity of MUC16 and MUC1 biomarkers in ovarian serous tumours. Mol. Oncol. 9, 503-512
  13. Vallen, M. J. E., van der Steen, S. C. H. A., van Tilborg, A. A. G., Massuger, L. F. A. G., and van Kuppevelt, T. H. (2014) Sulfated sugars in the extracellular matrix orchestrate ovarian cancer development: 'When sweet turns sour'. Gynecol. Oncol. 135, 371-381
  14. Oliveira-Ferrer, L., Heßling, A., Trillsch, F., Mahner, S., and Milde-Langosch, K. (2015) Prognostic impact of chondroitin-4-sulfotransferase CHST11 in ovarian cancer. Tumour Biol. 36, 9023-9030
  15. Vitiazeva, V., Kattla, J. J., Flowers, S. A., Linden, S. K., Premaratne, P., Weijdegard, B., Sundfeldt, K., and Karlsson, N. G. (2015) The O-linked glycome and blood group antigens ABO on mucin-type glycoproteins in mucinous and serous epithelial ovarian tumors. PLoS One 10, e0130197
  16. Shibata, T. K., Matsumura, F., Wang, P., Yu, S., Chou, C. C., Khoo, K. H., Kitayama, K., Akama, T. O., Sugihara, K., Kanayama, N., Kojima-Aikawa, K., Seeberger, P. H., Fukuda, M., Suzuki, A., Aoki, D., et al. (2012) Iden- tification of mono-and disulfated N-acetyl-lactosaminyl oligosaccharide structures as epitopes specifically recognized by humanized monoclonal antibody HMOCC-1 raised against ovarian cancer. J. Biol. Chem. 287, 6592-6602
  17. Schulz, B. L., Packer, N. H., and Karlsson, N. G. (2002) Small-scale analysis of O-linked oligosaccharides from glycoproteins and mucins separated by gel electrophoresis. Anal. Chem. 74, 6088-6097
  18. Cherian, R. M., Jin, C., Liu, J., Karlsson, N. G., and Holgersson, J. (2015) A panel of recombinant mucins carrying a repertoire of sialylated O-gly- cans based on different core chains for studies of glycan binding pro- teins. Biomolecules 5, 1810-1831
  19. Liu, J., Jin, C., Cherian, R. M., Karlsson, N. G., and Holgersson, J. (2015) O- glycan repertoires on a mucin-type reporter protein expressed in CHO cell pools transiently transfected with O-glycan core enzyme cDNAs. J. Biotechnol. 199, 77-89
  20. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. (2008) GlycoWorkbench: A tool for the computer-assisted annotation of mass spectra of glycans. J. Proteome Res. 7, 1650-1659
  21. Barone, A., Linder, A., Mateoiu, C., Köster Larsen, R., Blixt, O., Teneberg, S., and Sundfeldt, K. (2020) Evaluation of sialyl-lactotetra as a marker for epithelial ovarian tumors. Front. Oncol. 10, 561888
  22. Thomsson, K. A., Karlsson, H., and Hansson, G. C. (2000) Sequencing of sulfated oligosaccharides from mucins by liquid chromatography and electrospray ionization tandem mass spectrometry. Anal. Chem. 72, 4543-4549
  23. Flowers, S. A., Ali, L., Lane, C. S., Olin, M., and Karlsson, N. G. (2013) Selected reaction monitoring to differentiate and relatively quantitate isomers of sulfated and unsulfated core 1 O-glycans from salivary MUC7 protein in rheumatoid arthritis. Mol. Cell. Proteomics 12, 921-931
  24. Langford, R., Hurrion, E., and Dawson, P. A. (2017) Genetics and patho- physiology of mammalian sulfate biology. J. Genet. Genomics 44, 7-20
  25. Uchimura, K., and Rosen, S. D. (2006) Sulfated L-selectin ligands as a therapeutic target in chronic inflammation. Trends Immunol. 27, 559-565
  26. Macauley, M. S., Crocker, P. R., and Paulson, J. C. (2014) Siglec-mediated regulation of immune cell function in disease. Nat. Rev. Immunol. 14, 653-666
  27. Al-Saedi, F., Vaz, D. P., Stones, D. H., and Krachler, A. M. (2017) 3- Sulfogalactosyl-dependent adhesion of Escherichia coli HS multivalent adhesion molecule is attenuated by sulfatase activity. J. Biol. Chem. 292, 19792-19803
  28. Benjdia, A., Martens, E. C., Gordon, J. I., and Berteau, O. (2011) Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J. Biol. Chem. 286, 25973-25982
  29. Fukuta, M., Inazawa, J., Torii, T., Tsuzuki, K., Shimada, E., and Habuchi, O. (1997) Molecular cloning and characterization of human keratan sulfate Gal-6-sulfotransferase. J. Biol. Chem. 272, 32321-32328
  30. Torii, T., Fukuta, M., and Habuchi, O. (2000) Sulfation of sialyl N-ace- tyllactosamine oligosaccharides and fetuin oligosaccharides by keratan sulfate Gal-6-sulfotransferase. Glycobiology 10, 203-211
  31. Bistrup, A., Bhakta, S., Lee, J. K., Belov, Y. Y., Gunn, M. D., Zuo, F. R., Huang, C. C., Kannagi, R., Rosen, S. D., and Hemmerich, S. (1999) Sulfotransferases of two specificities function in the reconstitution of high endothelial cell ligands for L-selectin. J. Cell Biol. 145, 899-910
  32. Honke, K., Tsuda, M., Koyota, S., Wada, Y., Iida-Tanaka, N., Ishizuka, I., Nakayama, J., and Taniguchi, N. (2001) Molecular cloning and charac- terization of a human beta-Gal-3'-sulfotransferase that acts on both type 1 and type 2 (Gal beta 1-3/1-4GlcNAc-R) oligosaccharides. J. Biol. Chem. 276, 267-274
  33. Löfling, J., and Holgersson, J. (2009) Core saccharide dependence of sialyl Lewis X biosynthesis. Glycoconj. J. 26, 33-40
  34. Seko, A., Hara-Kuge, S., and Yamashita, K. (2001) Molecular cloning and characterization of a novel human galactose 3-O-sulfotransferase that transfers sulfate to gal beta 1->3galNAc residue in O-glycans. J. Biol. Chem. 276, 25697-25704
  35. El-Fasakhany, F. M., Uchimura, K., Kannagi, R., and Muramatsu, T. (2001) A novel human gal-3-O-sulfotransferase: Molecular cloning, character- ization, and its implications in biosynthesis of (SO(4)-3)Galbeta1- 4(Fucalpha1-3)GlcNAc. J. Biol. Chem. 276, 26988-26994
  36. Varki, A., Cummings, R. D., Aebi, M., Packer, N. H., Seeberger, P. H., Esko, J. D., Stanley, P., Hart, G., Darvill, A., Kinoshita, T., Prestegard, J. J., Schnaar, R. L., Freeze, H. H., Marth, J. D., Bertozzi, C. R., et al. (2015) Symbol nomenclature for graphical representations of glycans. Glycobi- ology 25, 1323-1324
  37. Swerdlow, S. H., Campo, E., Harris, N. L., Jaffe, E. S., Pileri, S. A., Stein, H., Thiele, J., Vardiman, J. W., eds. (2008) WHO classification of tu- mours of haematopoietic and lymphoid tissues. WHO Press, Geneva, Switzerland