Abstract
Pancreatic cancer is a highly malignant tumor of the digestive tract that is difficult to diagnose and treat. It is more common in developed countries and has become one of the main causes of death in some countries and regions. Currently, pancreatic cancer generally has a poor prognosis, partly due to the lack of symptoms in the early stages of pancreatic cancer. Therefore, most cases are diagnosed at advanced stage. With the continuous in-depth research of glycoproteomics in precision medical diagnosis, there have been some reports on quantitative analysis of cancer-related cells, plasma or tissues to find specific biomarkers for targeted therapy. This research is based on the developed complete N-linked glycopeptide database search engine GPSeeker, combined with liquid-mass spectrometry and stable diethyl isotope labeling, providing a benchmark of site- and structure-specific quantitative tissue N-glycoproteomics for discovery of potential N-glycoprotein markers. With spectrum-level FDR ≤1%, 20,038 intact N-Glycopeptides corresponding to 4518 peptide backbones, 228 N-glycan monosaccharide compositions 1026 N-glycan putative structures, 4460 N-glycosites and 3437 intact N-glycoproteins were identified. With the criteria of ≥1.5-fold change and p value<0.05, 52 differentially expressed intact N-glycopeptides (DEGPs) were found in pancreatic cancer tussues relative to control, where 38 up-regulated and 14 down-regulated, respectively.
Similar content being viewed by others
References
Blomme, B., Van Steenkiste, C., Callewaert, N., Van Vlierberghe, H.: Alteration of protein glycosylation in liver diseases. J. Hepatol. 50(3), 592–603 (2009). https://doi.org/10.1016/j.jhep.2008.12.010
Dennis, J., Laferte, S., Waghorne, C., Breitman, M., Kerbel, R.: Beta 1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science. 236(4801), 582–585 (1987). https://doi.org/10.1126/science.2953071
Kronewitter, S.R., de Leoz, M.L.A., Peacock, K.S., McBride, K.R., An, H.J., Miyamoto, S., Leiserowitz, G.S., Lebrilla, C.B.: Human serum processing and analysis methods for rapid and reproducible N-glycan mass profiling. J. Proteome Res. 9(10), 4952–4959 (2010). https://doi.org/10.1021/pr100202a
Lattová, E., Bryant, J., Skřičková, J., Zdráhal, Z., Popovič, M.: Efficient procedure for N-glycan analyses and detection of Endo H-like activity in human tumor specimens. J. Proteome Res. 15(8), 2777–2786 (2016). https://doi.org/10.1021/acs.jproteome.6b00346
Osumi, D., Takahashi, M., Miyoshi, E., Yokoe, S., Lee, S.H., Noda, K., Nakamori, S., Gu, J., Ikeda, Y., Kuroki, Y., Sengoku, K., Ishikawa, M., Taniguchi, N.: Core fucosylation of E-cadherin enhances cell–cell adhesion in human colon carcinoma WiDr cells. Cancer Sci. 100(5), 888–895 (2009). https://doi.org/10.1111/j.1349-7006.2009.01125.x
Pan, S., Brentnall, T.A., Chen, R.: Glycoproteins and glycoproteomics in pancreatic cancer. World J. Gastroenterol. 22(42), 9288–9299 (2016). https://doi.org/10.3748/wjg.v22.i42.9288
Pan, S., Chen, R., Aebersold, R., Brentnall, T.A.: Mass spectrometry based Glycoproteomics—from a proteomics perspective. Mol. Cell. Proteomics. 10(1), R110.003251 (2011). https://doi.org/10.1074/mcp.R110.003251
Ruhaak, L.R., Miyamoto, S., Lebrilla, C.B.: Developments in the identification of glycan biomarkers for the detection of Cancer. Mol. Cell. Proteomics. 12(4), 846–855 (2013). https://doi.org/10.1074/mcp.R112.026799
Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., Thun, M.J.: Cancer statistics, 2008. CA Cancer J. Clin. 58(2), 71–96 (2008). https://doi.org/10.3322/ca.2007.0010
Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Thun, M.J.: Cancer statistics, 2009. CA Cancer J. Clin. 59(4), 225–249 (2009). https://doi.org/10.3322/caac.20006
Ballehaninna, U.K., Chamberlain, R.S.: The clinical utility of serum CA 19-9 in the diagnosis, prognosis and management of pancreatic adenocarcinoma: An evidence based appraisal. J. Gastrointest. Oncol. 3(2), 105–119 (2011)
KIM, J.-E., LEE, K.T., LEE, J.K., PAIK, S.W., RHEE, J.C., CHOI, K.W.: Clinical usefulness of carbohydrate antigen 19-9 as a screening test for pancreatic cancer in an asymptomatic population. J. Gastroenterol. Hepatol. 19(2), 182–186 (2004). https://doi.org/10.1111/j.1440-1746.2004.03219.x
Zhao, J., Simeone, D.M., Heidt, D., Anderson, M.A., Lubman, D.M.: Comparative serum glycoproteomics using lectin selected sialic acid glycoproteins with mass spectrometric analysis: application to pancreatic cancer serum. J. Proteome Res. 5(7), 1792–1802 (2006). https://doi.org/10.1021/pr060034r
Sarrats, A., Saldova, R., Pla, E., Fort, E., Harvey, D.J., Struwe, W.B., de Llorens, R., Rudd, P.M., Peracaula, R.: Glycosylation of liver acute-phase proteins in pancreatic cancer and chronic pancreatitis. Proteomics: Clin. Appl. 4(4), 432–448 (2010). https://doi.org/10.1002/prca.200900150
Pan, S., Chen, R., Tamura, Y., Crispin, D.A., Lai, L.A., May, D.H., McIntosh, M.W., Goodlett, D.R., Brentnall, T.A.: Quantitative Glycoproteomics analysis reveals changes in N-glycosylation level associated with pancreatic ductal adenocarcinoma. J. Proteome Res. 13(3), 1293–1306 (2014). https://doi.org/10.1021/pr4010184
Park, H.-M., Hwang, M.P., Kim, Y.-W., Kim, K.-J., Jin, J.M., Kim, Y.H., Yang, Y.-H., Lee, K.H., Kim, Y.-G.: Mass spectrometry-based N-linked glycomic profiling as a means for tracking pancreatic cancer metastasis. Carbohydr. Res. 413, 5–11 (2015). https://doi.org/10.1016/j.carres.2015.04.019
Krishnan, S., Whitwell, H.J., Cuenco, J., Gentry-Maharaj, A., Menon, U., Pereira, S.P., Gaspari, M., Timms, J.F.: Evidence of altered glycosylation of serum proteins prior to pancreatic Cancer diagnosis. Int. J. Mol. Sci. 18(12), 2670 (2017)
Xiao, K., Tian, Z.: GPSeeker enables quantitative structural N-Glycoproteomics for site- and structure-specific characterization of differentially expressed N-glycosylation in hepatocellular carcinoma. J. Proteome Res. 18(7), 2885–2895 (2019). https://doi.org/10.1021/acs.jproteome.9b00191
Wang, Y., Xiao, K., Tian, Z.: Quantitative N-glycoproteomics using stable isotopic diethyl labeling. Talanta. 219, 121359 (2020). https://doi.org/10.1016/j.talanta.2020.121359
Xiao, K., Tian, Z.: Site- and structure-specific quantitative N-Glycoproteomics using RPLC-pentaHILIC separation and the intact N-Glycopeptide search engine GPSeeker. Curr. Protoc. Protein Sci. 97(1), e94 (2019). https://doi.org/10.1002/cpps.94
Wang, Y., Xu, F., Chen, Y., Tian, Z.: A quantitative N-glycoproteomics study of cell-surface N-glycoprotein markers of MCF-7/ADR cancer stem cells. Anal. Bioanal. Chem. 412(11), 2423–2432 (2020). https://doi.org/10.1007/s00216-020-02453-7
Wang, Y., Xu, F., Xiao, K., Chen, Y., Tian, Z.: Site- and structure-specific characterization of N-glycoprotein markers of MCF-7 cancer stem cells using isotopic-labelling quantitative N-glycoproteomics. Chem. Commun. 55(55), 7934–7937 (2019). https://doi.org/10.1039/C9CC04114A
Xu, F., Wang, Y., Xiao, K., Hu, Y., Tian, Z., Chen, Y.: Quantitative site- and structure-specific N-glycoproteomics characterization of differential N-glycosylation in MCF-7/ADR cancer stem cells. Clin. Proteomics. 17(1), 3 (2020). https://doi.org/10.1186/s12014-020-9268-7
Koehler, C.J., Arntzen, M.Ø., Thiede, B.: The impact of carbon-13 and deuterium on relative quantification of proteins using stable isotope diethyl labeling. Rapid Commun. Mass Spectrom. 29(9), 830–836 (2015). https://doi.org/10.1002/rcm.7170
Chen, Z., Yu, Q., Hao, L., Liu, F., Johnson, J., Tian, Z., Kao, W.J., Xu, W., Li, L.: Site-specific characterization and quantitation of N-glycopeptides in PKM2 knockout breast cancer cells using DiLeu isobaric tags enabled by electron-transfer/higher-energy collision dissociation (EThcD). Analyst. 143(11), 2508–2519 (2018). https://doi.org/10.1039/C8AN00216A
Miyauchi, E., Furuta, T., Ohtsuki, S., Tachikawa, M., Uchida, Y., Sabit, H., Obuchi, W., Baba, T., Watanabe, M., Terasaki, T., Nakada, M.: Identification of blood biomarkers in glioblastoma by SWATH mass spectrometry and quantitative targeted absolute proteomics. PLoS One. 13(3), e0193799 (2018). https://doi.org/10.1371/journal.pone.0193799
Zhou, Q., Andersson, R., Hu, D., Bauden, M., Kristl, T., Sasor, A., Pawłowski, K., Pla, I., Hilmersson, K.S., Zhou, M., Lu, F., Marko-Varga, G., Ansari, D.: Quantitative proteomics identifies brain acid soluble protein 1 (BASP1) as a prognostic biomarker candidate in pancreatic cancer tissue. EBioMedicine. 43, 282–294 (2019). https://doi.org/10.1016/j.ebiom.2019.04.008
Tralhão, J.G., Schaefer, L., Micegova, M., Evaristo, C., Schönherr, E., Kayal, S., Veiga-Fernandes, H., Danel, C., Iozzo, R.V., Kresse, H., Lemarchand, P.: In vivo selective and distant killing of cancer cells using adenovirus-mediated decorin gene transfer. FASEB J. 17(3), 464–466 (2003). https://doi.org/10.1096/fj.02-0534fje
Nash, M.A., Loercher, A.E., Freedman, R.S.: In vitro growth inhibition of ovarian Cancer cells by Decorin: synergism of action between Decorin and carboplatin. Cancer Res. 59(24), 6192–6196 (1999)
Jörg, K., Nathalia, A.G., Fabio, F.M., Pascal, B., Thomas, G., Irene, E., Max, G.B., Markus, W.B., Helmut, F.: Overexpressed Decorin in Pancreatic Cancer. Clin. Cancer. Res.10(14):4776-4783 (2004). https://doi.org/10.1158/1078-0432.CCR-1190-03
Johnson, M.D., Torri, J.A., Lippman, M.E., Dickson, R.B.: The role of cathepsin D in the invasiveness of human breast cancer cells. Cancer Res. 53(4), 873–877 (1993)
Cheng, A.-L., Huang, W.-G., Chen, Z.-C., Zhang, P.-F., Li, M.-Y., Li, F., Li, J.-L., Li, C., Yi, H., Peng, F., Duan, C.-J., Xiao, Z.-Q.: Identificating Cathepsin D as a biomarker for differentiation and prognosis of nasopharyngeal carcinoma by laser capture microdissection and proteomic analysis. J. Proteome Res. 7(6), 2415–2426 (2008). https://doi.org/10.1021/pr7008548
Roth, U., Razawi, H., Hommer, J., Engelmann, K., Schwientek, T., Müller, S., Baldus, S.E., Patsos, G., Corfield, A.P., Paraskeva, C., Hanisch, F.-G.: Differential expression proteomics of human colorectal cancer based on a syngeneic cellular model for the progression of adenoma to carcinoma. Proteomics. 10(2), 194–202 (2010). https://doi.org/10.1002/pmic.200900614
Selicharova, I., Sanda, M., Mladkova, J., Ohri, S.S., Vashishta, A., Fusek, M., Jiracek, J., Vetvicka, V.: 2-DE analysis of breast cancer cell lines 1833 and 4175 with distinct metastatic organ-specific potentials: comparison with parental cell line MDA-MB-231. Oncol. Rep. 19(5), 1237–1244 (2008). https://doi.org/10.3892/or.19.5.1237
Bossard, N., Descotes, F., Bremond, A.G., Bobin, Y., De Saint Hilaire, P., Golfier, F., Awada, A., Mathevet, P.M., Berrerd, L., Barbier, Y., Estève, J.: Keeping data continuous when analyzing the prognostic impact of a tumor marker: An example with Cathepsin D in breast Cancer. Breast Cancer Res. Treat. 82(1), 47–59 (2003). https://doi.org/10.1023/B:BREA.0000003919.75055.e8
Kirana, C., Shi, H., Laing, E., Hood, K., Miller, R., Bethwaite, P., Keating, J., Jordan, T.W., Hayes, M., Stubbs, R.: Cathepsin D expression in colorectal Cancer: from proteomic discovery through validation using Western blotting, immunohistochemistry, and tissue microarrays. Int J Proteomics. 2012, 245819–245819 (2012). https://doi.org/10.1155/2012/245819
Shin, I.Y., Sung, N.Y., Lee, Y.S., Kwon, T.S., Si, Y., Lee, Y.S., Oh, S.T., Lee, I.K.: The expression of multiple proteins as prognostic factors in colorectal cancer: cathepsin D, p53, COX-2, epidermal growth factor receptor, C-erbB-2, and Ki-67. Gut Liver. 8(1), 13–23 (2014). https://doi.org/10.5009/gnl.2014.8.1.13
Hui-juan, Z., Xiao-wei, Z., Ling, Q., Hong-chao, L., Wen-jing, C., Feng, L., Cai-yun, J.: Clinical significance and correlation with prognosis of novel glycosylation isoform of cathepsin D expression in lung cancer. Acta Anat Sin. 49(2), 191–197 (2018). https://doi.org/10.16098/j.issn.0529-1356.2018.02.009
Kang, J., Yu, Y., Jeong, S., Lee, H., Heo, H.J., Park, J.J., Na, H.S., Ko, D.S., Kim, Y.H.: Prognostic role of high cathepsin D expression in breast cancer: a systematic review and meta-analysis. Ther. Adv. Med. Oncol. 12, 1758835920927838–1758835920927838 (2020). https://doi.org/10.1177/1758835920927838
Whiteman, H.J., Weeks, M.E., Dowen, S.E., Barry, S., Timms, J.F., Lemoine, N.R., Crnogorac-Jurcevic, T.: The role of S100P in the invasion of pancreatic Cancer cells is mediated through cytoskeletal changes and regulation of Cathepsin D. cancer Res. 67(18), 8633–8642 (2007). https://doi.org/10.1158/0008-5472.can-07-0545
Dumartin, L., Whiteman, H.J., Weeks, M.E., Hariharan, D., Dmitrovic, B., Iacobuzio-Donahue, C.A., Brentnall, T.A., Bronner, M.P., Feakins, R.M., Timms, J.F., Brennan, C., Lemoine, N.R., Crnogorac-Jurcevic, T.: AGR2 is a novel surface antigen that promotes the dissemination of pancreatic cancer cells through regulation of cathepsins B and D. cancer Res. 71(22), 7091–7102 (2011). https://doi.org/10.1158/0008-5472.CAN-11-1367
Ivry, S.L., Knudsen, G.M., Caiazza, F., Sharib, J.M., Jaradeh, K., Ravalin, M., O’Donoghue, A.J., Kirkwood, K.S., Craik, C.S.: The lysosomal aminopeptidase tripeptidyl peptidase 1 displays increased activity in malignant pancreatic cysts. Biol. Chem. 400(12), 1629–1638 (2019). https://doi.org/10.1515/hsz-2019-0103
Nastase, M.V., Young, M.F., Schaefer, L.: Biglycan: a multivalent proteoglycan providing structure and signals. J. Histochem. Cytochem. 60(12), 963–975 (2012). https://doi.org/10.1369/0022155412456380
Hu, L., Zang, M.-D., Wang, H.-X., Li, J.-F., Su, L.-P., Yan, M., Li, C., Yang, Q.-M., Liu, B.-Y., Zhu, Z.-G.: Biglycan stimulates VEGF expression in endothelial cells by activating the TLR signaling pathway. Mol. Oncol. 10(9), 1473–1484 (2016). https://doi.org/10.1016/j.molonc.2016.08.002
Schaefer, L., Tredup, C., Gubbiotti, M.A., Iozzo, R.V.: Proteoglycan neofunctions: regulation of inflammation and autophagy in cancer biology. FASEB J. 284(1), 10–26 (2017). https://doi.org/10.1111/febs.13963
Xing, X., Gu, X., Ma, T., Ye, H.: Biglycan up-regulated vascular endothelial growth factor (VEGF) expression and promoted angiogenesis in colon cancer. Tumor Biol. 36(3), 1773–1780 (2015). https://doi.org/10.1007/s13277-014-2779-y
Gu, X., Ma, Y., Xiao, J., Zheng, H., Song, C., Gong, Y., Xing, X.: Up-regulated biglycan expression correlates with the malignancy in human colorectal cancers. Clin. Exp. Med. 12(3), 195–199 (2012). https://doi.org/10.1007/s10238-011-0155-4
Liu, Y., Li, W., Li, X., Tai, Y., Lü, Q., Yang, N., Jiang, J.: Expression and significance of biglycan in endometrial cancer. Arch. Gynecol. Obstet. 289(3), 649–655 (2014). https://doi.org/10.1007/s00404-013-3017-3
Niedworok, C., Röck, K., Kretschmer, I., Freudenberger, T., Nagy, N., Szarvas, T., vom Dorp, F., Reis, H., Rübben, H., Fischer, J.W.: Inhibitory Role of the Small Leucine-Rich Proteoglycan Biglycan in Bladder Cancer. PLoS One. 8(11), e80084 (2013). https://doi.org/10.1371/journal.pone.0080084
Wang, B., Li, G.-X., Zhang, S.-G., Wang, Q., Wen, Y.-G., Tang, H.-M., Zhou, C.-Z., Xing, A.-Y., Fan, J.-W., Yan, D.-W., Qiu, G.-Q., Yu, Z.-H., Peng, Z.-H.: Biglycan expression correlates with aggressiveness and poor prognosis of gastric cancer. Exp. Biol. Med. 236(11), 1247–1253 (2011). https://doi.org/10.1258/ebm.2011.011124
Zhao, S.F., Yin, X.J., Zhao, W.J., Liu, L.C., Wang, Z.P.: Biglycan as a potential diagnostic and prognostic biomarker in multiple human cancers. Oncol. Lett. 19(3), 1673–1682 (2020). https://doi.org/10.3892/ol.2020.11266
Yamamoto, K., Ohga, N., Hida, Y., Maishi, N., Kawamoto, T., Kitayama, K., Akiyama, K., Osawa, T., Kondoh, M., Matsuda, K., Onodera, Y., Fujie, M., Kaga, K., Hirano, S., Shinohara, N., Shindoh, M., Hida, K.: Biglycan is a specific marker and an autocrine angiogenic factor of tumour endothelial cells. Br. J. Cancer. 106(6), 1214–1223 (2012). https://doi.org/10.1038/bjc.2012.59
Weber, C.K., Sommer, G., Michl, P., Fensterer, H., Weimer, M., Gansauge, F., Leder, G., Adler, G., Gress, T.M.: Biglycan is overexpressed in pancreatic cancer and induces G1-arrest in pancreatic cancer cell lines. Gastroenterology. 121(3), 657–667 (2001). https://doi.org/10.1053/gast.2001.27222
Aprile, G., Avellini, C., Reni, M., Mazzer, M., Foltran, L., Rossi, D., Cereda, S., Iaiza, E., Fasola, G., Piga, A.: Biglycan expression and clinical outcome in patients with pancreatic adenocarcinoma. Tumor Biol. 34(1), 131–137 (2013). https://doi.org/10.1007/s13277-012-0520-2
Otterbein, H., Lehnert, H., Ungefroren, H.: Negative control of cell migration by Rac1b in highly metastatic pancreatic Cancer cells is mediated by sequential induction of nonactivated Smad3 and Biglycan. Cancers. 11(12), 1959 (2019). https://doi.org/10.3390/cancers11121959
Maliniemi, P., Carlsson, E., Kaukola, A., Ovaska, K., Niiranen, K., Saksela, O., Jeskanen, L., Hautaniemi, S., Ranki, A.: NAV3 copy number changes and target genes in basal and squamous cell cancers. Exp. Dermatol. 20(11), 926–931 (2011). https://doi.org/10.1111/j.1600-0625.2011.01358.x
Cohen-Dvashi, H., Ben-Chetrit, N., Russell, R., Carvalho, S., Lauriola, M., Nisani, S., Mancini, M., Nataraj, N., Kedmi, M., Roth, L., Köstler, W., Zeisel, A., Yitzhaky, A., Zylberg, J., Tarcic, G., Eilam, R., Wigelman, Y., Will, R., Lavi, S., Porat, Z., Wiemann, S., Ricardo, S., Schmitt, F., Caldas, C., Yarden, Y.: Navigator-3, a modulator of cell migration, may act as a suppressor of breast cancer progression. EMBO Mol. Med. 7(3), 299–314 (2015). https://doi.org/10.15252/emmm.201404134
Duarte, B.D.P., Bonatto, D.: The heat shock protein 47 as a potential biomarker and a therapeutic agent in cancer research. J. Cancer Res. Clin. Oncol. 144(12), 2319–2328 (2018). https://doi.org/10.1007/s00432-018-2739-9
Schwab, M.: Amplification of oncogenes in human cancer cells. Bioessays. 20(6), 473–479 (1998)
Zhu, J., Xiong, G., Fu, H., Evers, B.M., Zhou, B.P., Xu, R.: Chaperone Hsp47 drives malignant growth and invasion by modulating an ECM gene network. Cancer Res. 75(8), 1580–1591 (2015). https://doi.org/10.1158/0008-5472.can-14-1027
Poschmann, G., Sitek, B., Sipos, B., Ulrich, A., Wiese, S., Stephan, C., Warscheid, B., Klöppel, G., Vander Borght, A., Ramaekers, F.C.S., Meyer, H.E., Stühler, K.: Identification of proteomic differences between squamous cell carcinoma of the lung and bronchial epithelium. Mol. Cell. Proteomics. 8(5), 1105–1116 (2009). https://doi.org/10.1074/mcp.M800422-MCP200
Thierolf, M., Hagmann, M.-L., Pfeffer, M., Berntenis, N., Wild, N., Roeßler, M., Palme, S., Karl, J., Bodenmüller, H., Rüschoff, J., Rossol, S., Rohr, G., Rösch, W., Friess, H., Eickhoff, A., Jauch, K.-W., Langen, H., Zolg, W., Tacke, M.: Towards a comprehensive proteome of normal and malignant human colon tissue by 2-D-LC-ESI-MS and 2-DE proteomics and identification of S100A12 as potential cancer biomarker. Proteomics: Clin. Appl. 2(1), 11–22 (2008). https://doi.org/10.1002/prca.200780046
Yamamoto, N., Kinoshita, T., Nohata, N., Yoshino, H., Itesako, T., Fujimura, L., Mitsuhashi, A., Usui, H., Enokida, H., Nakagawa, M., Shozu, M., Seki, N.: Tumor-suppressive microRNA-29a inhibits cancer cell migration and invasion via targeting HSP47 in cervical squamous cell carcinoma. Int. J. Oncol. 43(6), 1855–1863 (2013). https://doi.org/10.3892/ijo.2013.2145
Zhang, X., Yang, J.-J., Kim, Y.S., Kim, K.-Y., Ahn, W.S., Yang, S.: An 8-gene signature, including methylated and down-regulated glutathione peroxidase 3, of gastric cancer. Int. J. Oncol. 36(2), 405–414 (2010). https://doi.org/10.3892/ijo_00000513
Maitra, A., Iacobuzio-Donahue, C., Rahman, A., Sohn, T.A., Argani, P., Meyer, R., Yeo, C.J., Cameron, J.L., Goggins, M., Kern, S.E., Ashfaq, R., Hruban, R.H., Wilentz, R.E.: Immunohistochemical validation of a novel epithelial and a novel stromal marker of pancreatic ductal adenocarcinoma identified by global expression microarrays: sea urchin Fascin homolog and heat shock protein 47. Am. J. Clin. Pathol. 118(1), 52–59 (2002). https://doi.org/10.1309/3pam-p5wl-2lv0-r4eg
Cao, D., Maitra, A., Saavedra, J.-A., Klimstra, D.S., Adsay, N.V., Hruban, R.H.: Expression of novel markers of pancreatic ductal adenocarcinoma in pancreatic nonductal neoplasms: additional evidence of different genetic pathways. Mod. Pathol. 18(6), 752–761 (2005). https://doi.org/10.1038/modpathol.3800363
Shimada, H., Kuboshima, M., Shiratori, T., Nabeya, Y., Takeuchi, A., Takagi, H., Nomura, F., Takiguchi, M., Ochiai, T., Hiwasa, T.: Serum anti-myomegalin antibodies in patients with esophageal squamous cell carcinoma. Int. J. Oncol. 30(1), 97–103 (2007). https://doi.org/10.3892/ijo.30.1.97
Sattar, M., Majid, A.: Lung Cancer classification models using discriminant information of mutated genes in protein amino acids sequences. Arabian J. Sci. Eng. 44(4), 3197–3211 (2019). https://doi.org/10.1007/s13369-018-3468-8
Ma, H., Song, B., Guo, S., Li, G., Jin, G.: Identification of germline and somatic mutations in pancreatic adenosquamous carcinoma using whole exome sequencing. Cancer Biomark. 27, 389–397 (2020). https://doi.org/10.3233/CBM-190236
Kasthuri, R.S., Taubman, M.B., Mackman, N.: Role of tissue factor in cancer. J. Clin. Oncol. 27(29), 4834–4838 (2009). https://doi.org/10.1200/JCO.2009.22.6324
van den Berg, Y.W., Osanto, S., Reitsma, P.H., Versteeg, H.H.: The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood. 119(4), 924–932 (2012). https://doi.org/10.1182/blood-2011-06-317685
Dammacco, F., Vacca, A., Procaccio, P., Ria, R., Marech, I., Racanelli, V.: Cancer-related coagulopathy (Trousseau’s syndrome): review of the literature and experience of a single center of internal medicine. Clin. Exp. Med. 13(2), 85–97 (2013). https://doi.org/10.1007/s10238-013-0230-0
Haas, S.L., Jesnowski, R., Steiner, M., Hummel, F., Ringel, J., Burstein, C., Nizze, H., Liebe, S., Löhr, J.M.: Expression of tissue factor in pancreatic adenocarcinoma is associated with activation of coagulation. World J. Gastroenterol. 12(30), 4843–4849 (2006). https://doi.org/10.3748/wjg.v12.i30.4843
Bieker, R., Kessler, T., Schwöppe, C., Padró, T., Persigehl, T., Bremer, C., Dreischalück, J., Kolkmeyer, A., Heindel, W., Mesters, R.M., Berdel, W.E.: Infarction of tumor vessels by NGR-peptide–directed targeting of tissue factor: experimental results and first-in-man experience. Blood. 113(20), 5019–5027 (2009). https://doi.org/10.1182/blood-2008-04-150318
Ferreira, C.A., Ehlerding, E.B., Rosenkrans, Z.T., Jiang, D., Sun, T., Aluicio-Sarduy, E., Engle, J.W., Ni, D., Cai, W.: 86/90Y-labeled monoclonal antibody targeting tissue factor for pancreatic Cancer Theranostics. Mol. Pharm. 17(5), 1697–1705 (2020). https://doi.org/10.1021/acs.molpharmaceut.0c00127
Jaffe, E.A., Ruggiero, J.T., Leung, L.K., Doyle, M.J., McKeown-Longo, P.J., Mosher, D.F.: Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix. Proc. Natl. Acad. Sci. U. S. A. 80(4), 998–1002 (1983). https://doi.org/10.1073/pnas.80.4.998
Phillips, D.R., Jennings, L.K., Prasanna, H.R.: Ca2+−mediated association of glycoprotein G (thrombinsensitive protein, thrombospondin) with human platelets. J. Biol. Chem. 255(24), 11629–11632 (1980)
Simantov, R., Febbraio, M., Crombie, R., Asch, A.S., Nachman, R.L., Silverstein, R.L.: Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. J. Clin. Invest. 107(1), 45–52 (2001). https://doi.org/10.1172/JCI9061
Pengfei, W., Zheng, Z., Caiji, L., Jiali, W., Wenwen, X., Wenqing, M., Qian, X., Huidi, L., Shu-Lin, L.: Thrombospondin-1 as a potential therapeutic target: multiple roles in cancers. Curr. Pharm. Des. 26(18), 2116–2136 (2020). https://doi.org/10.2174/1381612826666200128091506
Albo, D., Berger, D.H., Wang, T.N., Hu, X., Rothman, V., Tuszynski, G.P.: Thrombospondin-1 and transforming growth factor-betal promote breast tumor cell invasion through up-regulation of the plasminogen/plasmin system. Surgery. 122(2), 493–500 (1997). https://doi.org/10.1016/S0039-6060(97)90043-X
Bocci, G., Fioravanti, A., Orlandi, P., Di Desidero, T., Natale, G., Fanelli, G., Viacava, P., Naccarato, A.G., Francia, G., Danesi, R.: Metronomic ceramide analogs inhibit angiogenesis in pancreatic cancer through up-regulation of caveolin-1 and thrombospondin-1 and down-regulation of cyclin D1. Neoplasia (New York, N.Y.). 14(9), 833–845 (2012). https://doi.org/10.1593/neo.12772
Qian, X., Rothman, V.L., Nicosia, R.F., Tuszynski, G.P.: Expression of thrombospondin-1 in human pancreatic adenocarcinomas: role in matrix metalloproteinase-9 production. Pathol. Oncol. Res. 7(4), 251–259 (2001). https://doi.org/10.1007/BF03032381
Laklai, H., Laval, S., Dumartin, L., Rochaix, P., Hagedorn, M., Bikfalvi, A., Le Guellec, S., Delisle, M.-B., Schally, A.V., Susini, C., Pyronnet, S., Bousquet, C.: Thrombospondin-1 is a critical effector of oncosuppressive activity of sst2 somatostatin receptor on pancreatic cancer. Proc. Natl. Acad. Sci. U. S. A. 106(42), 17769–17774 (2009). https://doi.org/10.1073/pnas.0908674106
Zhang, X., Connolly, C., Duquette, M., Lawler, J., Parangi, S.: Continuous administration of the three thrombospondin-1 type 1 repeats recombinant protein improves the potency of therapy in an orthotopic human pancreatic cancer model. Cancer Lett. 247(1), 143–149 (2007). https://doi.org/10.1016/j.canlet.2006.04.003
Nie, S., Lo, A., Wu, J., Zhu, J., Tan, Z., Simeone, D.M., Anderson, M.A., Shedden, K.A., Ruffin, M.T., Lubman, D.M.: Glycoprotein biomarker panel for pancreatic Cancer discovered by quantitative proteomics analysis. J. Proteome Res. 13(4), 1873–1884 (2014). https://doi.org/10.1021/pr400967x
Choi, S.H., Tamura, K., Khajuria, R.K., Bhere, D., Nesterenko, I., Lawler, J., Shah, K.: Antiangiogenic variant of TSP-1 targets tumor cells in glioblastomas. Mol. Ther. 23(2), 235–243 (2015). https://doi.org/10.1038/mt.2014.214
Fu, X., Zhu, B.T.: Human pancreas-specific protein disulfide isomerase homolog (PDIp) is redox-regulated through formation of an inter-subunit disulfide bond. Arch. Biochem. Biophys. 485(1), 1–9 (2009). https://doi.org/10.1016/j.abb.2008.12.021
Fu, X.-M., Zhu, B.T.: Human pancreas-specific protein disulfide isomerase homolog (PDIp) is an intracellular estrogen-binding protein that modulates estrogen levels and actions in target cells. J. Steroid Biochem. Mol. Biol. 115(1–2), 20–29 (2009). https://doi.org/10.1016/j.jsbmb.2009.02.008
Fu, X.-M., Dai, X., Ding, J., Zhu, B.T.: Pancreas-specific protein disulfide isomerase has a cell type-specific expression in various mouse tissues and is absent in human pancreatic adenocarcinoma cells: implications for its functions. J. Mol. Histol. 40(3), 189–199 (2009). https://doi.org/10.1007/s10735-009-9230-5
Ozawa, K., Kuwabara, K., Tamatani, M., Takatsuji, K., Tsukamoto, Y., Kaneda, S., Yanagi, H., Stern, D.M., Eguchi, Y., Tsujimoto, Y., Ogawa, S., Tohyama, M.: 150-kDa oxygen-regulated protein (ORP150) suppresses hypoxia-induced apoptotic cell death. J. Biol. Chem. 274(10), 6397–6404 (1999). https://doi.org/10.1074/jbc.274.10.6397
Asahi, H., Koshida, K., Hori, O., Ogawa, S., Namiki, M.: Immunohistochemical detection of the 150-kDa oxygen-regulated protein in bladder cancer. BJU Int. 90, 462–466 (2002). https://doi.org/10.1046/j.1464-410X.2002.02915.x
Tsukamoto, Y., Kuwabara, K., Hirota, S., Kawano, K., Yoshikawa, K., Ozawa, K., Kobayashi, T., Yanagi, H., Stern, D.M., Tohyama, M., Kitamura, Y., Ogawa, S.: Expression of the 150-kd oxygen-regulated protein in human breast cancer. Lab. Investig. 78(6), 699–706 (1998)
Zhou, Q., Andersson, R., Hu, D., Bauden, M., Sasor, A., Bygott, T., PawŁowski, K., Pla, I., Marko-Varga, G., Ansari, D.: Alpha-1-acid glycoprotein 1 is upregulated in pancreatic ductal adenocarcinoma and confers a poor prognosis. Transl. Res. 212, 67–79 (2019). https://doi.org/10.1016/j.trsl.2019.06.003
Wang, Y., Wu, W., Zhu, M., Wang, C., Shen, W., Cheng, Y., Geng, L., Li, Z., Zhang, J., Dai, J., Ma, H., Chen, L., Hu, Z., Jin, G., Shen, H.: Integrating expression-related SNPs into genome-wide gene- and pathway-based analyses identified novel lung cancer susceptibility genes. Int. J. Cancer. 142(8), 1602–1610 (2018). https://doi.org/10.1002/ijc.31182
Castro-Piedras, I., Sharma, M., den Bakker, M., Molehin, D., Martinez, E.G., Vartak, D., Pruitt, W.M., Deitrick, J., Almodovar, S., Pruitt, K.: DVL1 and DVL3 differentially localize to CYP19A1 promoters and regulate aromatase mRNA in breast cancer cells. Oncotarget. 9(86), 35639–35654 (2018)
Chen, X.Q., Jiang, J., Wang, X.T., Zhang, C.L., Ji, A.Y., Chen, X.J.: Role and mechanism of Dvl3 in the esophageal squamous cell carcinoma. Eur. Rev. Med. Pharmacol. Sci. 22(22), 7716–7725 (2018). https://doi.org/10.26355/eurrev_201811_16393
Kafka, A., Tomas, D., Lechpammer, M., Gabud, T., Pažanin, L., Pećina-Šlaus, N.: Expression levels and localizations of DVL3 and sFRP3 in Glioblastoma. Dis. Markers. 2017(9253495), 1–10 (2017). https://doi.org/10.1155/2017/9253495
Barat, S., Chen, X., Cuong Bui, K., Bozko, P., Götze, J., Christgen, M., Krech, T., Malek, N.P., Plentz, R.R.: Gamma-Secretase inhibitor IX (GSI) impairs concomitant activation of notch and Wnt-Beta-catenin pathways in CD44+ gastric Cancer stem cells. Stem Cells Transl. Med. 6(3), 819–829 (2017). https://doi.org/10.1002/sctm.16-0335
Pai, V.C., Hsu, C.-C., Chan, T.-S., Liao, W.-Y., Chuu, C.-P., Chen, W.-Y., Li, C.-R., Lin, C.-Y., Huang, S.-P., Chen, L.-T., Tsai, K.K.: ASPM promotes prostate cancer stemness and progression by augmenting Wnt-Dvl-3-β-catenin signaling. Oncogene. 38(8), 1340–1353 (2019). https://doi.org/10.1038/s41388-018-0497-4
Rodriguez-Mora, O., LaHair, M.M., Howe, C.J., McCubrey, J.A., Franklin, R.A.: Calcium/calmodulin-dependent protein kinases as potential targets in cancer therapy. Expert Opin. Ther. Targets. 9(4), 791–808 (2005). https://doi.org/10.1517/14728222.9.4.791
Tadic, M., Stoos-Veic, T., Kujundzic, M., Turcic, P., Aralica, G., Boskoski, I.: Insulin-like growth factor 2 binding protein 3 expression on endoscopic ultrasound guided fine needle aspiration specimens in pancreatic ductal adenocarcinoma. Eur. J. Gastroenterol. Hepatol. 32(4), 496–500 (2020). https://doi.org/10.1097/meg.0000000000001696
Acknowledgments
This research was financially supported by National Natural Science Foundation of China (21775110, 22074105) and Shanghai Science and Technology Commission (14DZ2261100).
Availability of data and material
The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
This study was performed in compliance with the Helsinki Declaration on ethical principles for handling human tissue specimens, with all China national regulations and requirements. Written informed consent was obtained from participants. Ethical permission for the study was granted by the ethics committees at Tongji University (Shanghai, China) and Changhai Hospital (Shanghai, China).
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lu, H., Xiao, K. & Tian, Z. Benchmark of site- and structure-specific quantitative tissue N-glycoproteomics for discovery of potential N-glycoprotein markers: a case study of pancreatic cancer. Glycoconj J 38, 213–231 (2021). https://doi.org/10.1007/s10719-021-09994-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10719-021-09994-8