Glycolaldehyde‐modified β‐lactoglobulin AGEs are unable to stimulate inflammatory signaling pathways in RAGE‐expressing human cell lines
Open accessAbstract
SCOPE: Advanced glycation endproducts (AGEs) are suspected to stimulate inflammatory signaling pathways in target tissues via activation of the receptor for AGEs. Endotoxins are generally recognized as potential contamination of AGE preparations and stimulate biological actions that are very similar as or identical to those induced by AGEs. METHODS AND RESULTS: In our study, we used glycolaldehyde-modified β-lactoglobulin preparations as model AGEs and employed two methods to remove endotoxin using either affinity columns or extraction with Triton X-114 (TX-114). Affinity column-purified AGEs retained their ability to stimulate inflammatory signaling as measured by mRNA expression of inflammatory cytokines in the human lung epithelial cell line Beas2b. However, glycolaldehyde-modified AGEs purified by extraction with TX-114 did not show any stimulation of mRNA expression of inflammatory cytokines. The presence of a cell stimulating endotoxin-like activity was demonstrated in the detergent phase after extraction with TX-114, thus indicating that not AGEs but a lipophilic contamination was responsible for the stimulation of inflammatory signaling. CONCLUSION: Our results demonstrate that glycolaldehyde-modified AGEs are unable to induce inflammatory signaling in receptor for AGE-expressing cells. The observed cell-activating activity can be ascribed to an endotoxin-like lipophilic contamination present in AGE preparations and affinity column purification was insufficient to remove this contamination.
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Elderly people have higher basal levels of inflammation independently of disease status.
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From Dietary factors and low-grade inflammation in relation to overweight and obesity (2011) · cites this paper as [228]
Cites
Phase separation of integral membrane proteins in Triton X-114 solution.
Bordier, C. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69848-0 · Cited by 3,324 · see citing works
The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses
Schmidt, A. M., Yan, S. D., Yan, S. F., & Stern, D. M. (2001) · Journal of Clinical Investigation · doi:10.1172/jci14002 · Cited by 1,256 · see citing works
The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses
Schmidt, A. M., Yan, S. D., Yan, S. F., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci200114002 · Cited by 1,039 · see citing works
Ramasamy, R., Vannucci, S. J., Yan, S. S. D., Herold, K., Yan, S. F., & Schmidt, A. M. (2005) · Glycobiology · doi:10.1093/glycob/cwi053 · Cited by 834 · see citing works
Brett, J., Schmidt, A. M., Yan, S. D., Zou, Y. S., Weidman, E., Pinsky, D. J., Nowygrod, R., Neeper, M. P., Przysiecki, C. T., & SHAW, A. R. (1993) · PubMed Central · Cited by 776 · see citing works
Thornalley, P. J., Battah, S., Ahmed, N., Karachalias, N., Agalou, S., Babaei‐Jadidi, R., & Dawnay, A. (2003) · Biochemical Journal · doi:10.1042/bj20030763 · Cited by 659 · see citing works
Removal of endotoxin from protein solutions by phase separation using triton X-114
Aida, Y., & Pabst, M. J. (1990) · Journal of Immunological Methods · doi:10.1016/0022-1759(90)90029-u · Cited by 602 · see citing works
Maillard reaction products in tissue proteins: New products and new perspectives
Thorpe, S. R., & Baynes, J. (2003) · Amino Acids · doi:10.1007/s00726-003-0017-9 · Cited by 543 · see citing works
Binding of S100 proteins to RAGE: An update
Leclerc, E., Fritz, G., Vetter, S. W., & Heizmann, C. W. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.11.016 · Cited by 490 · see citing works
Methods of endotoxin removal from biological preparations: a review.
Magalhães, P. O., Lopes, A. M., Mazzola, P. G., Rangel‐Yagui, C. D. O., Penna, T. C. V., & Pessoa, A. (2007) · PubMed · Cited by 402 · see citing works
Removal of Endotoxin from Recombinant Protein Preparations
Liu, S., Tobias, R. B., McClure, S., Styba, G., Shi, Q., & Jackowski, G. (1997) · Clinical Biochemistry · doi:10.1016/s0009-9120(97)00049-0 · Cited by 332 · see citing works
RAGE (receptor for advanced glycation end products): a central player in the inflammatory response
Chavakis, T., Bierhaus, A., & Nawroth, P. P. (2004) · Microbes and Infection · doi:10.1016/j.micinf.2004.08.004 · Cited by 301 · see citing works
Stern, D. M., Yan, S. D., Yan, S. F., & Schmidt, A. M. (2002) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(02)00160-6 · Cited by 281 · see citing works
Structural and functional insights into RAGE activation by multimeric S100B
Ostendorp, T., Leclerc, E., Galichet, A., Koch, M., Demling, N., Weigle, B., Heizmann, C., Kroneck, P., & Fritz, G. (2007) · EMBO Journal · doi:10.1038/sj.emboj.7601805 · Cited by 257 · see citing works
Structural Basis for Pattern Recognition by the Receptor for Advanced Glycation End Products (RAGE)
Xie, J., Reverdatto, S., Frolov, A., Hoffmann, R., Burz, D. S., & Shekhtman, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801622200 · Cited by 252 · see citing works
The receptor RAGE: Bridging inflammation and cancer
Riehl, A., Németh, J., Angel, P. E., & Heß, J. (2009) · Cell Communication and Signaling · doi:10.1186/1478-811x-7-12 · Cited by 236 · see citing works
Valencia, J., Weldon, S. C., Quinn, D. F., Kiers, G. H., DeGroot, J., TeKoppele, J. M., & Hughes, T. E. (2003) · Analytical Biochemistry · doi:10.1016/j.ab.2003.09.013 · Cited by 178 · see citing works
Amphoterin as an extracellular regulator of cell motility: from discovery to disease
Huttunen, H. J., & Rauvala, H. (2004) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2003.01301.x · Cited by 173 · see citing works
Single step protocol to purify recombinant proteins with low endotoxin contents
Reichelt, P., Schwarz, C., & Donzeau, M. (2005) · Protein Expression and Purification · doi:10.1016/j.pep.2005.09.027 · Cited by 166 · see citing works
Pathologies Involving the S100 Proteins and Rage
Heizmann, C. W., Ackermann, G. E., & Galichet, A. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6191-2_5 · Cited by 160 · see citing works
Site-Specific Blockade of RAGE-V<sub>d</sub>Prevents Amyloid-β Oligomer Neurotoxicity
Sturchler, E., Galichet, A., Weibel, M., Leclerc, E., & Heizmann, C. W. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4878-07.2008 · Cited by 136 · see citing works
Srikrishna, G., Huttunen, H. J., Johansson, L., Weigle, B., Yamaguchi, Y., Rauvala, H., & Freeze, H. H. (2002) · Journal of Neurochemistry · doi:10.1046/j.0022-3042.2002.00796.x · Cited by 130 · see citing works
Hegele, J., Buetler, T. M., & Delatour, T. (2008) · Analytica Chimica Acta · doi:10.1016/j.aca.2007.12.027 · Cited by 106 · see citing works
Global Analysis of a Macromolecular Interaction Measured on BIAcore
Roden, L. D., & Myszka, D. G. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1297 · Cited by 102 · see citing works
Mone, M. D., Koehne, C., Rediske, J. J., Hughes, T. E., & Valencia, J. (2004) · Diabetologia · doi:10.1007/s00125-004-1392-9 · Cited by 94 · see citing works
Buetler, T. M., Leclerc, E., Baumeyer, A., Latado, H., Newell, J. W., Adolfsson, O., Parisod, V., Richoz, J., Maurer, S., Foata, F., et al. (2008) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200700101 · Cited by 82 · see citing works
THE AGE/RAGE AXIS IN DIABETES‐ACCELERATED ATHEROSCLEROSIS
Jandeleit-Dahm, K. A. M., Watson, A. M. D., & Soro‐Paavonen, A. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04875.x · Cited by 80 · see citing works
Advanced glycation end products in uremia
Henle, T., & Miyata, T. (2003) · Advances in Renal Replacement Therapy · doi:10.1053/j.arrt.2003.08.006 · Cited by 65 · see citing works
A Nondegradative Route for the Removal of Endotoxin from Exopolysaccharides
Adam, O., Vercellone, A., Paul, F., MONSAN, P. F., & Puzo, G. (1995) · Analytical Biochemistry · doi:10.1006/abio.1995.1161 · Cited by 60 · see citing works
V domain of RAGE interacts with AGEs on prostate carcinoma cells
Allmen, E. U., Koch, M., Fritz, G., & Legler, D. F. (2008) · The Prostate · doi:10.1002/pros.20736 · Cited by 55 · see citing works
Reznikov, L. L., Waksman, J., Azam, T., Kim, S.-H., Bufler, P., Niwa, T., Werman, A., Zhang, X., Pischetsrieder, M., Shaldon, S., et al. (2004) · Clinical Nephrology · doi:10.5414/cnp61324 · Cited by 50 · cited 2× · see citing works
“[20] showing that strictly endotoxin-free AGEs were unable to stimulate cytokine production (TNF-a, IL-1b and IL-8) in peripheral blood monocytes of healthy donors.”
BackgroundMethodHui, Y. Y., McAmis, W., Baynes, J., Schaeffer, R. C., & Wolf, M. B. (2001) · Diabetologia · doi:10.1007/s001250100646 · Cited by 27 · see citing works
Spanneberg, R., Osswald, F., Kolesov, I. S., Anton, W., Radusch, H., & Glomb, M. A. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf9039827 · Cited by 25 · see citing works
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Dietary factors and low-grade inflammation in relation to overweight and obesity
Calder, P. C., Ahluwalia, N., Brouns, F., Buetler, T., Clement, K., Cunningham, K., Esposito, K., Jönsson, L. S., Kolb, H., Lansink, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114511005460 · Cited by 1,098 · see citing works
Advanced glycation endproducts in food and their effects on health
Poulsen, M. W., Hedegaard, R. V., Andersen, J. M., de Courten, B., Bügel, S., Nielsen, J., Skibsted, L. H., & Dragsted, L. O. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.06.052 · Cited by 751 · see citing works
Vascular effects of advanced glycation endproducts: Clinical effects and molecular mechanisms
Stirban, A. O., Gawlowski, T., & Roden, M. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.11.006 · Cited by 365 · see citing works
Teodorowicz, M., van Neerven, R. J. J., & Savelkoul, H. F. J. (2017) · Nutrients · doi:10.3390/nu9080835 · Cited by 211 · see citing works
Teodorowicz, M., Perdijk, O., Verhoek, I. C., Govers, C., Savelkoul, H. F. J., Tang, Y., Wichers, H. J., & Broersen, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173778 · Cited by 92 · see citing works
Dietary Advanced Glycation Endproducts Induce an Inflammatory Response in Human Macrophages in Vitro
van der Lugt, T., Weseler, A. R., Gebbink, W. A., Vrolijk, M. F., Opperhuizen, A., & Bast, A. (2018) · Nutrients · doi:10.3390/nu10121868 · Cited by 54 · see citing works
Klenovics, K. S., Boor, P., Somoza, V., Celec, P., Fogliano, V., & Šebeková, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053056 · Cited by 50 · see citing works
Chrysanthou, M., Estruch, I. M., Rietjens, I. M. C. M., Wichers, H. J., & Hoppenbrouwers, T. (2022) · Nutrients · doi:10.3390/nu14020363 · Cited by 29 · see citing works
Lopes, A. M., Molino, J. V. D., Santos‐Ebinuma, V. C., Pessoa, A., Valentini, S. R., & Pereira, J. F. B. (2018) · Separation and Purification Technology · doi:10.1016/j.seppur.2018.04.090 · Cited by 27 · see citing works
Stirban, A. O., Kotsi, P., Franke, K., Strijowski, U., Cai, W., Götting, C., & Tschoepe, D. (2012) · Diabetes Care · doi:10.2337/dc12-1489 · Cited by 25 · see citing works
Kim, D.-K., Choi, H., Nishida, H., Oh, J. Y., Gregory, C. A., Lee, R. H., Yu, J. M., Watanabe, J., An, S. Y., Bartosh, T. J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147553 · Cited by 22 · see citing works
Introduction to the Maillard Reaction
(2015) · CRC Press eBooks · doi:10.1201/b19207-3 · Cited by 2 · see citing works
Toxicological consequences of the Maillard reaction
Timme, V. D. L. (2020) · doi:10.26481/dis.20200918tl
- Authors
- Buetler, T. M., Latado, H., Leclerc, E., Weigle, B., Baumeyer, A., Heizmann, C. W., & Scholz, G.
- Affiliations
- Nestlé (Switzerland) (CH)
- North Dakota State University (US)
- University of Zurich (CH)
- Corresponding author
- Scholz, Gabriele
- Venue
- Molecular Nutrition & Food Research
- Publisher
- Wiley
- Published
- 2010-08-16
- Volume
- 55
- Issue
- 2
- Pages
- 291-299
- ISSN
- 1613-4125 (ISSN-L)
- 1613-4133
- OpenAlex
- W2107304339
- Cited by
- 13
- References
- 32
- Citations by year
- 2022: 1 · 2020: 1 · 2018: 2 · 2017: 2 · 2016: 1 · 2015: 1 · 2013: 3 · 2012: 1
- FWCI
- 1.00
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Molecular Nutrition & Food Research (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
- Life Sciences › Agricultural and Biological Sciences › Food Science › Potato Plant Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Keywords
- advanced glycation end products, receptor for advanced glycation end products, endotoxin contamination, inflammatory signaling, inflammatory cytokines, Triton X-114 extraction
- MeSH terms
- Receptor for Advanced Glycation End Products, Acetaldehyde, Cell Line, Detergents, Endotoxins, Humans, Inflammation, Lactoglobulins, Polyethylene Glycols, Receptors, Immunologic, RNA, Messenger, Reproducibility of Results, Signal Transduction, Cytokines, Glycation End Products, Advanced, Octoxynol
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