Glycomic analysis of gastric carcinoma cells discloses glycans as modulators of RON receptor tyrosine kinase activation in cancer

Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLeX). SLeX overexpression is associated with tumor aggressive phenotype and patients' poor prognosis. MKN45 gastric carcinoma cells...

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Published inBiochimica et biophysica acta Vol. 1860; no. 8; pp. 1795 - 1808
Main Authors Mereiter, Stefan, Magalhães, Ana, Adamczyk, Barbara, Jin, Chunsheng, Almeida, Andreia, Drici, Lylia, Ibáñez-Vea, Maria, Gomes, Catarina, Ferreira, José A., Afonso, Luis P., Santos, Lúcio L., Larsen, Martin R., Kolarich, Daniel, Karlsson, Niclas G., Reis, Celso A.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.08.2016
Subjects
Biochemistry & Molecular Biology
Biofysik
Biophysics
biosynthesis
breast-cancer
c-met
colorectal-cancer
epitopes
Gastric cancer
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Neoplastic
gene overexpression
Glycome
Glycomics
glycosylation
Humans
in-vivo
insulin receptors
integrins
invasive growth
Lewis X Antigen - biosynthesis
Lewis X Antigen - genetics
linked
liquid chromatography
mass spectrometry
medicine
Molecular Biology
Molekylärbiologi
n-acetylglucosaminyltransferase-iii
neoplasm cells
Neoplasm Proteins - biosynthesis
Neoplasm Proteins - genetics
next-generation
oligosaccharides
patients
personalized medicine
phenotype
polysaccharides
Polysaccharides - biosynthesis
Polysaccharides - genetics
Receptor Protein-Tyrosine Kinases - genetics
Receptor Protein-Tyrosine Kinases - metabolism
RON
Sialome
Sialyl Lewis X (SLeX)
Sialyltransferases - biosynthesis
Sialyltransferases - genetics
ST3GAL4
stomach neoplasms
Stomach Neoplasms - genetics
Stomach Neoplasms - metabolism
structural-analysis
HILIC-FLD-UPLC
PLA
IHC
Glycome
PTM
RTK
SLeX
RON
Sialyl Lewis X (SLeX)
SLea
ST3GAL4
GC
Gastric cancer
Sialome
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Abstract Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLeX). SLeX overexpression is associated with tumor aggressive phenotype and patients' poor prognosis. MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors. Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLeX and the concomitant activation. SLeX and RON co-expression was validated in gastric tumors. The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation. This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc. •Expression of ST3GAL4 modulates sialylation and glycan size in cancer cells.•Modulation of sialylation impacts N-glycan branched structures.•47 increased sialylated proteins were identified in ST3GAL4 overexpressing cells.•Gastric cancer cells showed activation of aberrantly glycosylated RON receptor.•Aberrant RON glycosylation with SLeX was validated in human gastric tumors.
AbstractList Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLeX). SLeX overexpression is associated with tumor aggressive phenotype and patients' poor prognosis.MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors.Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLeX and the concomitant activation. SLeX and RON co-expression was validated in gastric tumors.The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation.This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc.
Background: Terminal alpha 2-3 and alpha 2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLe(X)). SLe(X) overexpression is associated with tumor aggressive phenotype and patients' poor prognosis. Methods: MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors. Results: Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from alpha 2-6 towards alpha 2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLe(X) and the concomitant activation. SLe(X) and RON co-expression was validated in gastric tumors. Conclusion: The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation. General significance: This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc.
Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLeX). SLeX overexpression is associated with tumor aggressive phenotype and patients' poor prognosis. MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors. Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLeX and the concomitant activation. SLeX and RON co-expression was validated in gastric tumors. The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation. This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc. •Expression of ST3GAL4 modulates sialylation and glycan size in cancer cells.•Modulation of sialylation impacts N-glycan branched structures.•47 increased sialylated proteins were identified in ST3GAL4 overexpressing cells.•Gastric cancer cells showed activation of aberrantly glycosylated RON receptor.•Aberrant RON glycosylation with SLeX was validated in human gastric tumors.
Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLe(X)). SLe(X) overexpression is associated with tumor aggressive phenotype and patients' poor prognosis.BACKGROUNDTerminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLe(X)). SLe(X) overexpression is associated with tumor aggressive phenotype and patients' poor prognosis.MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors.METHODSMKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors.Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLe(X) and the concomitant activation. SLe(X) and RON co-expression was validated in gastric tumors.RESULTSOur results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLe(X) and the concomitant activation. SLe(X) and RON co-expression was validated in gastric tumors.The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation.CONCLUSIONThe overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation.This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc.GENERAL SIGNIFICANCEThis study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc.
Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis X (SLe(X)). SLe(X) overexpression is associated with tumor aggressive phenotype and patients' poor prognosis. MKN45 gastric carcinoma cells transfected with the sialyltransferase ST3GAL4 were established as a model overexpressing sialylated terminal glycans. We have evaluated at the structural level the glycome and the sialoproteome of this gastric cancer cell line applying liquid chromatography and mass spectrometry. We further validated an identified target expression by proximity ligation assay in gastric tumors. Our results showed that ST3GAL4 overexpression leads to several glycosylation alterations, including reduced O-glycan extension and decreased bisected and increased branched N-glycans. A shift from α2-6 towards α2-3 linked sialylated N-glycans was also observed. Sialoproteomic analysis further identified 47 proteins with significantly increased sialylated N-glycans. These included integrins, insulin receptor, carcinoembryonic antigens and RON receptor tyrosine kinase, which are proteins known to be key players in malignancy. Further analysis of RON confirmed its modification with SLe(X) and the concomitant activation. SLe(X) and RON co-expression was validated in gastric tumors. The overexpression of ST3GAL4 interferes with the overall glycophenotype of cancer cells affecting a multitude of key proteins involved in malignancy. Aberrant glycosylation of the RON receptor was shown as an alternative mechanism of oncogenic activation. This study provides novel targets and points to an integrative tumor glycomic/proteomic-profiling for gastric cancer patients' stratification. This article is part of a Special Issue entitled "Glycans in personalised medicine" Guest Editor: Professor Gordan Lauc.
Author Mereiter, Stefan
Almeida, Andreia
Reis, Celso A.
Gomes, Catarina
Afonso, Luis P.
Magalhães, Ana
Karlsson, Niclas G.
Larsen, Martin R.
Kolarich, Daniel
Jin, Chunsheng
Drici, Lylia
Santos, Lúcio L.
Ibáñez-Vea, Maria
Ferreira, José A.
Adamczyk, Barbara
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  organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark
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  fullname: Ibáñez-Vea, Maria
  organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark
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  fullname: Gomes, Catarina
  organization: I3S — Instituto de Investigação e Inovação em Saúde, University of Porto, Portugal
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  givenname: José A.
  surname: Ferreira
  fullname: Ferreira, José A.
  organization: I3S — Instituto de Investigação e Inovação em Saúde, University of Porto, Portugal
– sequence: 10
  givenname: Luis P.
  surname: Afonso
  fullname: Afonso, Luis P.
  organization: Department of Pathology, Portuguese Institute of Oncology of Porto, Portugal
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  givenname: Lúcio L.
  surname: Santos
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  organization: Experimental Pathology and Therapeutics Group, Portuguese Institute of Oncology of Porto, Portugal
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  givenname: Martin R.
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  fullname: Kolarich, Daniel
  organization: Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
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  surname: Karlsson
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  surname: Reis
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  organization: I3S — Instituto de Investigação e Inovação em Saúde, University of Porto, Portugal
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Issue 8
Keywords HILIC-FLD-UPLC
PLA
IHC
Glycome
PTM
RTK
SLeX
RON
Sialyl Lewis X (SLeX)
SLea
ST3GAL4
GC
Gastric cancer
Sialome
Language English
License Copyright © 2015 Elsevier B.V. All rights reserved.
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Snippet Terminal α2-3 and α2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes such as sialyl-Lewis...
Background: Terminal alpha 2-3 and alpha 2-6 sialylation of glycans precludes further chain elongation, leading to the biosynthesis of cancer relevant epitopes...
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SubjectTerms Biochemistry & Molecular Biology
Biofysik
Biophysics
biosynthesis
breast-cancer
c-met
colorectal-cancer
epitopes
Gastric cancer
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Neoplastic
gene overexpression
Glycome
Glycomics
glycosylation
Humans
in-vivo
insulin receptors
integrins
invasive growth
Lewis X Antigen - biosynthesis
Lewis X Antigen - genetics
linked
liquid chromatography
mass spectrometry
medicine
Molecular Biology
Molekylärbiologi
n-acetylglucosaminyltransferase-iii
neoplasm cells
Neoplasm Proteins - biosynthesis
Neoplasm Proteins - genetics
next-generation
oligosaccharides
patients
personalized medicine
phenotype
polysaccharides
Polysaccharides - biosynthesis
Polysaccharides - genetics
Receptor Protein-Tyrosine Kinases - genetics
Receptor Protein-Tyrosine Kinases - metabolism
RON
Sialome
Sialyl Lewis X (SLeX)
Sialyltransferases - biosynthesis
Sialyltransferases - genetics
ST3GAL4
stomach neoplasms
Stomach Neoplasms - genetics
Stomach Neoplasms - metabolism
structural-analysis
Title Glycomic analysis of gastric carcinoma cells discloses glycans as modulators of RON receptor tyrosine kinase activation in cancer
URI https://dx.doi.org/10.1016/j.bbagen.2015.12.016
https://www.ncbi.nlm.nih.gov/pubmed/26721331
https://www.proquest.com/docview/1797232156
https://www.proquest.com/docview/2000204189
https://gup.ub.gu.se/publication/239781
Volume 1860
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