Advanced glycation endproducts and polysialylation affect the turnover of the neural cell adhesion molecule (NCAM) and the receptor for advanced glycation endproducts (RAGE)
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Franziska Frank
Abstract
The balance between protein synthesis and degradation regulates the amount of expressed proteins. This protein turnover is usually quantified as the protein half-life time. Several studies suggest that protein degradation decreases with age and leads to increased deposits of damaged and non-functional proteins. Glycation is an age-dependent, non-enzymatic process leading to posttranslational modifications, so-called advanced glycation endproducts (AGE), which usually damage proteins and lead to protein aggregation. AGE are formed by the Maillard reaction, where carbonyls of carbohydrates or metabolites react with amino groups of proteins. In this study, we quantified the half-life time of two important receptors of the immunoglobulin superfamily, the neural cell adhesion molecule (NCAM) and the receptor for advanced glycation end products (RAGE) before and after glycation. We found, that in two rat PC12 cell lines glycation leads to increased turnover, meaning that glycated, AGE-modified proteins are degraded faster than non-glycated proteins. NCAM is the most prominent carrier of a unique enzymatic posttranslational modification, the polysialylation. Using two PC12 cell lines (a non-polysialylated and a polysialylated one), we could additionally demonstrate, that polysialylation of NCAM has an impact on its turnover and that it significantly increases its half-life time.
Acknowledgement
This work was supported by the Deutsche Forschungsgemeinschaft, Funder Id: 10.13039/501100001659 (RTG 2155, ProMoAge).
References
Ahmed, N., Battah, S., Karachalias, N., Babaei-Jadidi, R., Horányi, M., Baróti, K., Hollan, S., and Thornalley, P.J. (2003). Increased formation of methylglyoxal and protein glycation, oxidation and nitrosation in triosephosphate isomerase deficiency. Biochim. Biophys. Acta 1639, 121–132.10.1016/j.bbadis.2003.08.002Suche in Google Scholar
Antecol, M.H., Darveau, A., Sonenberg, N., and Mukherjee, B.B. (1986). Altered biochemical properties of actin in normal skin fibroblasts from individuals predisposed to dominantly inherited cancers. Cancer Res. 46, 1867–1873.Suche in Google Scholar
Bennmann, D., Horstkorte, R., Hofmann, B., Jacobs, K., Navarrete-Santos, A., Simm, A., Bork, K., and Gnanapragassam, V.S. (2014). Advanced glycation endproducts interfere with adhesion and neurite outgrowth. PLoS One 9, e112115.10.1371/journal.pone.0112115Suche in Google Scholar
Bierhaus, A., Humpert, P.M., Morcos, M., Wendt, T., Chavakis, T., Arnold, B., Stern, D.M., and Nawroth, P.P. (2005). Understanding RAGE, the receptor for advanced glycation end products. J. Mol. Med. 83, 876–886.10.1007/s00109-005-0688-7Suche in Google Scholar
Chiu, F.C. and Goldman, J.E. (1984). Synthesis and turnover of cytoskeletal proteins in cultured astrocytes. J. Neurochem. 42, 166–174.10.1111/j.1471-4159.1984.tb09713.xSuche in Google Scholar
Cunningham, B.A., Hemperly, J.J., Murray, B.A., Prediger, E.A., Brackenbury, R., and Edelman, G.M. (1987). Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236, 799–806.10.1126/science.3576199Suche in Google Scholar
Diestel, S., Schaefer, D., Cremer, H., and Schmitz, B. (2007). NCAM is ubiquitylated, endocytosed and recycled in neurons. J. Cell Sci. 120, 4035–4049.10.1242/jcs.019729Suche in Google Scholar
Eckhardt, M., Mühlenhoff, M., Bethe, A., Koopman, J., Frosch, M., and Gerardy-Schahn, R. (1995). Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373, 715–718.10.1038/373715a0Suche in Google Scholar
Finne, J., Finne, U., Deagostini-Bazin, H., and Goridis, C. (1983). Occurrence of α2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochem. Biophys. Res. Commun. 112, 482–487.10.1016/0006-291X(83)91490-0Suche in Google Scholar
Gasser, A. and Forbes, J.M. (2008). Advanced glycation: implications in tissue damage and disease. Protein Pept. Lett. 15, 385–391.10.2174/092986608784246515Suche in Google Scholar PubMed
Gkogkolou, P. and Böhm, M. (2012). Advanced glycation end products. Dermatoendocrinology 4, 259–270.10.4161/derm.22028Suche in Google Scholar PubMed PubMed Central
Hinsby, A.M., Berezin, V., and Bock, E. (2004). Molecular mechanisms of NCAM function. Front. Biosci. 9, 2227–2244.10.2741/1393Suche in Google Scholar PubMed
Horstkorte, R., Leßner, N., Gerardy-Schahn, R., Lucka, L., Danker, K., and Reutter, W. (1999). Expression of the polysialyltransferase ST8SiaIV: polysialylation interferes with adhesion of PC12 cells in vitro. Exp. Cell Res. 246, 122–128.10.1006/excr.1998.4255Suche in Google Scholar PubMed
John, W.G. and Lamb, E.J. (1993). The maillard or browning reaction in diabetes. Eye 7, 230–237.10.1038/eye.1993.55Suche in Google Scholar PubMed
Kalapos, M.P. (2008). Methylglyoxal and glucose metabolism: a historical perspective and future avenues for research. Drug Metabol. Drug Interact. 23, 69–91.10.1515/DMDI.2008.23.1-2.69Suche in Google Scholar
Kao, S.H., Wang, W.L., Chen, C.Y., Chang, Y.L., Wu, Y.Y., Wang, Y.-T., Wang, S.-P., Nesvizhskii, A.I., Chen, Y.-J., Hong, T.-M., et al. (2015). Analysis of protein stability by the cyclohexemide chase assay. Bio-Protocl. 5.10.21769/BioProtoc.1374Suche in Google Scholar PubMed PubMed Central
Lapolla, A., Flamini, R., Vedova, A.D., Senesi, A., Reitano, R., Fedele, D., Basso, E., Seraglia, R., and Traldi, P. (2003). Glyoxal and methylglyoxal levels in diabetic patients: quantitative determination by a new GC/MS method. Clin. Chem. Lab. Med. 41, 1166–1173.10.1515/CCLM.2003.180Suche in Google Scholar PubMed
Nakayama, J., Fukuda, M.N., Fredette, B., Ranscht, B., and Fukuda, M. (1995). Expression cloning of a human polysialyltransferase that form polysialylated neural cell adhesion molecule present in embryonic brain. Proc. Natl. Acad. Sci. USA 92, 7031–7035.10.1073/pnas.92.15.7031Suche in Google Scholar PubMed PubMed Central
Park, T.U., Lucka, L., Reutter, W., and Horstkorte, R. (1997). Turnover studies of the neural cell adhesion molecule NCAM: degradation of NCAM in PC12 cells depends on the presence of NGF. Biochem. Biophys. Res. Commun. 234, 686–689.10.1006/bbrc.1997.6700Suche in Google Scholar PubMed
Schalkwijk, C.G. and Miyata, T. (2012). Early- and advanced non-enzymatic glycation in diabetic vascular complications: the search for therapeutics. Amino Acids 42, 1193–1204.10.1007/s00726-010-0779-9Suche in Google Scholar PubMed PubMed Central
Schmidt, A.M., Yan, S.D., Yan, S.F., and Stern, D.M. (2001). The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest. 108, 949–955.10.1172/JCI200114002Suche in Google Scholar
Shafer, T.J. and Atchison, W.D. (1991). Transmitter, ion channel and receptor properties of pheochromocytoma (PC12) cells: a model for neurotoxicological studies. Neurotoxicology 12, 473–492.Suche in Google Scholar
Singh, R., Barden, A., Mori, T., and Beilin, L. (2001). Advanced glycation end-products: a review. Diabetologia 44, 129–146.10.1007/s001250051591Suche in Google Scholar
Tauber, R., Park, C.S., and Reutter, W. (1983). Intramolecular heterogeneity of degradation in plasma membrane glycoproteins: evidence for a general characteristic. Proc. Natl. Acad. Sci. USA 80, 4026–4029.10.1073/pnas.80.13.4026Suche in Google Scholar
Thiery, J.P., Brackenbury, R., Rutishauser, U., and Edelman, G.M. (1977). Adhesion among neural cells of the chick embryo. II. Purification and characterization of a cell adhesion molecule from neural retina. J. Biol. Chem. 252, 6841–6845.10.1016/S0021-9258(17)39926-XSuche in Google Scholar
Tischler, A.S. and Greene, L.A. (1978). Morphologic and cytochemical properties of a clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Lab. Invest. 39, 77–89.Suche in Google Scholar
Vistoli, G., De Maddis, D., Cipak, A., Zarkovic, N., Carini, M., and Aldini, G. (2013). Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic. Res. 47 (Supppl 1), 3–27.10.3109/10715762.2013.815348Suche in Google Scholar PubMed
©2019 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Mitochondria, Apoptosis and Cancer (MAC) 2017
- Transglutaminase type 2 in the regulation of proteostasis
- Mitochondria-driven elimination of cancer and senescent cells
- Comparative study of the differential cell death protecting effect of various ROS scavengers
- Involvement of mitophagy in cisplatin-induced cell death regulation
- Differential involvement of TAK1, RIPK1 and NF-κB signaling in Smac mimetic-induced cell death in breast cancer cells
- Selective BH3-mimetics targeting BCL-2, BCL-XL or MCL-1 induce severe mitochondrial perturbations
- BNIP3 contributes to the glutamine-driven aggressive behavior of melanoma cells
- Review
- Multiple binding sites in organic cation transporters require sophisticated procedures to identify interactions of novel drugs
- Research Articles/Short Communications
- Membranes, Lipids, Glycobiology
- Characterization of the cholesterol efflux of apolipoprotein E-containing high-density lipoprotein in THP-1 cells
- Advanced glycation endproducts and polysialylation affect the turnover of the neural cell adhesion molecule (NCAM) and the receptor for advanced glycation endproducts (RAGE)
- Cell Biology and Signaling
- miR-34a-5p aggravates hypoxia-induced apoptosis by targeting ZEB1 in cardiomyocytes
- MicroRNA-1225-5p acts as a tumor-suppressor in laryngeal cancer via targeting CDC14B
- Novel Techniques
- Tandem DNAzyme for double digestion: a new tool for circRNA suppression
Artikel in diesem Heft
- Frontmatter
- Mitochondria, Apoptosis and Cancer (MAC) 2017
- Transglutaminase type 2 in the regulation of proteostasis
- Mitochondria-driven elimination of cancer and senescent cells
- Comparative study of the differential cell death protecting effect of various ROS scavengers
- Involvement of mitophagy in cisplatin-induced cell death regulation
- Differential involvement of TAK1, RIPK1 and NF-κB signaling in Smac mimetic-induced cell death in breast cancer cells
- Selective BH3-mimetics targeting BCL-2, BCL-XL or MCL-1 induce severe mitochondrial perturbations
- BNIP3 contributes to the glutamine-driven aggressive behavior of melanoma cells
- Review
- Multiple binding sites in organic cation transporters require sophisticated procedures to identify interactions of novel drugs
- Research Articles/Short Communications
- Membranes, Lipids, Glycobiology
- Characterization of the cholesterol efflux of apolipoprotein E-containing high-density lipoprotein in THP-1 cells
- Advanced glycation endproducts and polysialylation affect the turnover of the neural cell adhesion molecule (NCAM) and the receptor for advanced glycation endproducts (RAGE)
- Cell Biology and Signaling
- miR-34a-5p aggravates hypoxia-induced apoptosis by targeting ZEB1 in cardiomyocytes
- MicroRNA-1225-5p acts as a tumor-suppressor in laryngeal cancer via targeting CDC14B
- Novel Techniques
- Tandem DNAzyme for double digestion: a new tool for circRNA suppression