Endogenous formation of Nε-(carboxymethyl)lysine is increased in fatty livers and induces inflammatory markers in an in vitro model of hepatic steatosis

Gaens, Katrien H.J.; Niessen, Petra M.G.; Rensen, Sander S.; Buurman, Wim A.; Greve, Jan Willem M.; Driessen, Ann; Wolfs, Marcel G.M.; Hofker, Marten H.; Bloemen, Johanne G.; Dejong, Cornelis H.; Stehouwer, Coen D.A.; Schalkwijk, Casper G.

doi:10.1016/j.jhep.2011.07.028

Cited by 110Liver Disease Diagnosis and TreatmentAdvanced Glycation End Products researchLiver physiology and pathology

Endogenous formation of Nε-(carboxymethyl)lysine is increased in fatty livers and induces inflammatory markers in an in vitro model of hepatic steatosis

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Gaens, Katrien H.J., Niessen, Petra M.G., Rensen, Sander S., Buurman, Wim A., Greve, Jan Willem M., Driessen, Ann, Wolfs, Marcel G.M., Hofker, Marten H. +4 more·2012·Journal of Hepatology

DOI 10.1016/j.jhep.2011.07.028

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Abstract

Background & aims Increased lipid peroxidation and inflammation are major factors in the pathogenesis of nonalcoholic fatty liver disease (NAFLD). A lipoxidation product that could play a role in the induction of hepatic inflammation is N(ε)-(carboxymethyl)lysine (CML). The aim of the present study was to investigate the relationship between steatosis and CML and to study the role of CML in hepatic inflammation.Methods We included 74 obese individuals, which were categorized into 3 groups according to the grade of hepatic steatosis. CML accumulation in liver biopsies was assessed by immunohistochemistry and plasma CML levels were measured by mass spectrometry. Plasma CML levels were also determined in the hepatic artery, portal, and hepatic vein of 22 individuals, and CML fluxes across the liver were calculated. Hepatocyte cell lines were used to study CML formation during intracellular lipid accumulation and the effect of CML on pro-inflammatory cytokine expression. Gene expression levels of the inflammatory markers were determined in liver biopsies of the obese individuals.Results CML accumulation was significantly associated with the grade of hepatic steatosis, the grade of hepatic inflammation, and gene expression levels of inflammatory markers PAI-1, IL-8, and CRP. Analysis of CML fluxes showed no release/uptake of CML by the liver. Lipid accumulation in hepatocytes, induced by incubation with fatty acids, was associated with increased CML formation and expression of the receptor for advanced glycation endproducts (RAGE), PAI-1, IL-8, IL-6, and CRP. Pyridoxamine and aminoguanidine inhibited the endogenous CML formation and the increased RAGE, PAI-1, IL-8, IL-6, and CRP expression. Incubation of hepatocytes with CML-albumin increased the expression of RAGE, PAI-1, and IL-6, which was inhibited by an antibody against RAGE.Conclusions Accumulation of CML and a CML-upregulated RAGE-dependent inflammatory response in steatotic livers may play an important role in hepatic steatosis and in the pathogenesis of NAFLD.

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Intracellular AGE accumulation is observed in animal models of hepatic steatosis and other advanced liver diseases, such as steatohepatitis and fibrosis/cirrhosis.
“Intracellular AGE accumulation is observed in animal models of hepatic steatosis and other advanced liver diseases, such as hepatic inflammation (steatohepatitis) and fibrosis/cirrhosis.”
From Advanced glycation end products (AGEs) and other adducts in aging-related diseases and alcohol-mediated tissue injury (2021) · cites this paper as [123]
Accumulated AGEs in hepatocytes stimulate apoptosis and inflammation, leading to cellular dysfunction, steatosis, and ultimately NAFLD.
“Accumulated AGEs in hepatocytes can stimulate apoptosis and inflammation, leading to cellular dysfunction, steatosis, and ultimately nonalcoholic fatty liver disease (NAFLD)121–123.”
From Advanced glycation end products (AGEs) and other adducts in aging-related diseases and alcohol-mediated tissue injury (2021) · cites this paper as [123]

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Lindera obtusiloba Blume Alleviates Non-Alcoholic Fatty Liver Disease Promoted by Nε-(carboxymethyl)lysine
Lee, J., Gu, M. J., Lee, Y. R., Kim, Y., Choi, I., Kim, D., & Ha, S. K. (2024) · Nutrients · doi:10.3390/nu16142330 · Cited by 2 · see citing works

Authors: Gaens, K. H. J., Niessen, P. M. G., Rensen, S. S., Buurman, W. A., Greve, J. W. M., Driessen, A., Wolfs, M. G. M., Hofker, M. H., Bloemen, J. G., Dejong, C. H., Stehouwer, C. D. A., & Schalkwijk, C. G.
Affiliations: Maastricht University Medical Centre (NL)
University Medical Center Groningen (NL)
Corresponding author: Schalkwijk, Casper G.
ORCID: Rensen, Sander S.
Buurman, Wim A.
Greve, Jan Willem M.
Driessen, Ann
Stehouwer, Coen D.A.
Schalkwijk, Casper G.
Venue: Journal of Hepatology
Publisher: Elsevier BV
Published: 2012-03
Volume: 56
Issue: 3
Pages: 647-655
ISSN: 0168-8278 (ISSN-L)
DOI: 10.1016/j.jhep.2011.07.028
OpenAlex: W1964714465
Cited by: 109
References: 36
Citations by year: 2026: 4 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 8 · 2021: 9 · 2020: 6 · 2019: 14 · 2018: 10 · 2017: 15 · 2016: 7 · 2015: 8 · 2014: 2 · 2013: 6 · 2012: 3
FWCI: 2.89
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Hepatology (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (submittedVersion, other-oa)
Funders: Universiteit Maastricht
Nierstichting (01C-104)
Diabetes Fonds (01C-104)
Maastricht Universitair Medisch Centrum
Center for Translational Molecular Medicine (01 C-104)
Transnationale Universiteit Limburg
SenterNovem
Topics: Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords: carboxymethyllysine, advanced glycation end products, non-alcoholic fatty liver disease, hepatic steatosis, liver inflammation, receptor for advanced glycation end products, lipid peroxidation, inflammatory cytokines, plasminogen activator inhibitor-1, interleukin-8, C-reactive protein, pyridoxamine, aminoguanidine, hepatocyte lipid accumulation, obesity
MeSH terms: Aged, Biopsy, Enzyme Inhibitors, Fatty Liver, Female, Guanidines, Humans, Liver, Lysine, Male, Middle Aged, Obesity, Pyridoxamine, Vitamin B Complex, Biomarkers, Gene Expression, Cytokines, Hepatocytes, Hep G2 Cells, Non-alcoholic Fatty Liver Disease, In Vitro Techniques

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Endogenous formation of Nε-(carboxymethyl)lysine is increased in fatty livers and induces inflammatory markers in an in vitro model of hepatic steatosis

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