(+)-Catechin mitigates impairment in insulin secretion and beta cell damage in methylglyoxal-induced pancreatic beta cells.

(+)-Catechin Advanced glycation end products Anti-glycation Diabetic complications Insulin secretion Methylglyoxal

Journal

Molecular biology reports

ISSN: 1573-4978

Titre abrégé: Mol Biol Rep

Pays: Netherlands

ID NLM: 0403234

Informations de publication

Date de publication:
23 Mar 2024

Historique:

received: 17 11 2023

accepted: 08 02 2024

medline: 23 3 2024

pubmed: 23 3 2024

entrez: 23 3 2024

Statut: epublish

Résumé

The formation of advanced glycation end products (AGEs) is the central process contributing to diabetic complications in diabetic individuals with sustained and inconsistent hyperglycemia. Methylglyoxal, a reactive carbonyl species, is found to be a major precursor of AGEs, and its levels are elevated in diabetic conditions. Dysfunction of pancreatic beta cells and impairment in insulin secretion are the hallmarks of diabetic progression. Exposure to methylglyoxal-induced AGEs alters the function and maintenance of pancreatic beta cells. Hence, trapping methylglyoxal could be an ideal approach to alleviate AGE formation and its influence on beta cell proliferation and insulin secretion, thereby curbing the progression of diabetes to its complications. In the present study, we have explored the mechanism of action of (+)-Catechin against methylglyoxal-induced disruption in pancreatic beta cells via molecular biology techniques, mainly western blot. Methylglyoxal treatment decreased insulin synthesis (41.5%) via downregulating the glucose-stimulated insulin secretion pathway (GSIS). This was restored upon co-treatment with (+)-Catechin (29.9%) in methylglyoxal-induced Beta-TC-6 cells. Also, methylglyoxal treatment affected the autocrine function of insulin by disrupting the IRS1/PI3k/Akt pathway. Methylglyoxal treatment suppresses Pdx-1 and Maf A levels, which are responsible for beta cell maintenance and cell proliferation. (+)-Catechin could significantly augment the levels of these transcription factors. This is the first study to examine the impact of a natural compound on methylglyoxal with the insulin-mediated autocrine and paracrine activities of pancreatic beta cells. The results indicate that (+)-Catechin exerts a protective effect against methylglyoxal exposure in pancreatic beta cells and can be considered a potential anti-glycation agent in further investigations on ameliorating diabetic complications.

Sections du résumé

BACKGROUND BACKGROUND

METHODS AND RESULTS RESULTS

In the present study, we have explored the mechanism of action of (+)-Catechin against methylglyoxal-induced disruption in pancreatic beta cells via molecular biology techniques, mainly western blot. Methylglyoxal treatment decreased insulin synthesis (41.5%) via downregulating the glucose-stimulated insulin secretion pathway (GSIS). This was restored upon co-treatment with (+)-Catechin (29.9%) in methylglyoxal-induced Beta-TC-6 cells. Also, methylglyoxal treatment affected the autocrine function of insulin by disrupting the IRS1/PI3k/Akt pathway. Methylglyoxal treatment suppresses Pdx-1 and Maf A levels, which are responsible for beta cell maintenance and cell proliferation. (+)-Catechin could significantly augment the levels of these transcription factors.

CONCLUSION CONCLUSIONS

This is the first study to examine the impact of a natural compound on methylglyoxal with the insulin-mediated autocrine and paracrine activities of pancreatic beta cells. The results indicate that (+)-Catechin exerts a protective effect against methylglyoxal exposure in pancreatic beta cells and can be considered a potential anti-glycation agent in further investigations on ameliorating diabetic complications.

Identifiants

DOI: 10.1007/s11033-024-09338-3 PMID: 38520585

pubmed: 38520585

doi: 10.1007/s11033-024-09338-3

pii: 10.1007/s11033-024-09338-3

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

434

Subventions

Organisme : Human Resource Development Centre, Council of Scientific And Industrial Research

ID : 31/038(0579)/2019-EMRI

Organisme : National Institute for Interdisciplinary Science and Technology

ID : OM-6/1/TD-HTC/2020-TMD-SeMI

Informations de copyright

Références

Kharroubi AT, Darwish HM (2015) Diabetes mellitus: the epidemic of the century. World J Diabetes 6:850–867. https://doi.org/10.4239/wjd.v6.i6.850

doi: 10.4239/wjd.v6.i6.850 pubmed: 26131326 pmcid: 4478580

Sun H, Saeedi P, Karuranga S et al (2022) IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 183:109119. https://doi.org/10.1016/j.diabres.2021.109119

doi: 10.1016/j.diabres.2021.109119 pubmed: 34879977

Kyrou I, Katsarou C, Skoufas E et al (2020) Sociodemographic and lifestyle-related risk factors for identifying vulnerable groups for type 2 diabetes: a narrative review with emphasis on data from Europe. BMC Endocr Disord 20:134. https://doi.org/10.1186/s12902-019-0463-3

doi: 10.1186/s12902-019-0463-3 pubmed: 32164656 pmcid: 7066728

Devendra D, Liu E, Eisenbarth GS (2004) Type 1 diabetes: recent developments. BMJ 328:750–754

doi: 10.1136/bmj.328.7442.750 pubmed: 15044291 pmcid: 381328

Westman EC (2021) Type 2 diabetes Mellitus: a pathophysiologic perspective. Front Nutr 8

García-Aguilar A, Guillén C (2022) Targeting pancreatic beta cell death in type 2 diabetes by polyphenols. Front Endocrinol 13

Matafome P, Rodrigues T, Sena C, Seiça R (2017) Methylglyoxal in metabolic disorders: facts, myths, and promises. Med Res Rev 37:368–403. https://doi.org/10.1002/med.21410

doi: 10.1002/med.21410 pubmed: 27636890

Khalid M, Petroianu G, Adem A (2022) Advanced Glycation End products and Diabetes Mellitus: mechanisms and perspectives. https://doi.org/10.3390/biom12040542 . Biomolecules 12:

Liu C, Huang Y, Zhang Y et al (2017) Intracellular methylglyoxal induces oxidative damage to pancreatic beta cell line INS-1 cell through Ire1 α -JNK and mitochondrial apoptotic pathway. 5762. https://doi.org/10.1080/10715762.2017.1289376

Ashraf JM, Ahmad S, Choi I et al (2015) Recent advances in detection of AGEs: Immunochemical, bioanalytical and biochemical approaches. IUBMB Life 67:897–913. https://doi.org/10.1002/iub.1450

doi: 10.1002/iub.1450 pubmed: 26597014

Lee EJ, Park JH (2013) Receptor for Advanced Glycation endproducts (RAGE), its ligands, and Soluble RAGE: potential biomarkers for diagnosis and therapeutic targets for Human Renal diseases. Genomics Inf 11:224. https://doi.org/10.5808/GI.2013.11.4.224

doi: 10.5808/GI.2013.11.4.224

Nedić O, Rattan SIS, Grune T, Trougakos IP (2013) Molecular effects of advanced glycation end products on cell signalling pathways, ageing and pathophysiology. Free Radic Res 47 Suppl 128–38. https://doi.org/10.3109/10715762.2013.806798

Lapolla A, Reitano R, Seraglia R et al (2005) Evaluation of advanced glycation end products and carbonyl compounds in patients with different conditions of oxidative stress. Mol Nutr Food Res 49:685–690. https://doi.org/10.1002/MNFR.200400093

doi: 10.1002/MNFR.200400093 pubmed: 15926142

Fiory F, Lombardi A, Miele C et al (2011) Methylglyoxal impairs insulin signalling and insulin action on glucose-induced insulin secretion in the pancreatic beta cell line INS-1E. Diabetologia 54:2941–2952. https://doi.org/10.1007/s00125-011-2280-8

doi: 10.1007/s00125-011-2280-8 pubmed: 21861178

Kalwat MA, Cobb MH (2017) Mechanisms of the amplifying pathway of insulin secretion in the β cell. Pharmacol Ther 179:17–30. https://doi.org/10.1016/j.pharmthera.2017.05.003

doi: 10.1016/j.pharmthera.2017.05.003 pubmed: 28527919 pmcid: 7269041

Elghazi L, Bernal-Mizrachi E (2009) Akt and PTEN: β-cell mass and pancreas plasticity. Trends Endocrinol Metab 20:243–251. https://doi.org/10.1016/j.tem.2009.03.002

doi: 10.1016/j.tem.2009.03.002 pubmed: 19541499 pmcid: 4456182

Fujimoto K, Polonsky KS (2009) Pdx1 and other factors that regulate pancreatic β-cell survival. Diabetes Obes Metab 11:30–37. https://doi.org/10.1111/j.1463-1326.2009.01121.x

doi: 10.1111/j.1463-1326.2009.01121.x pubmed: 19817786 pmcid: 2802270

Toprak C, Yigitaslan S (2019) Alagebrium and complications of Diabetes Mellitus. Eurasian J Med 51:285–292. https://doi.org/10.5152/eurasianjmed.2019.18434

doi: 10.5152/eurasianjmed.2019.18434 pubmed: 31692712 pmcid: 6812920

Salazar J, Navarro C, Ortega Á et al (2021) Advanced Glycation End products: New Clinical and Molecular perspectives. Int J Environ Res Public Health 18:7236. https://doi.org/10.3390/ijerph18147236

doi: 10.3390/ijerph18147236 pubmed: 34299683 pmcid: 8306599

Sadowska-Bartosz I, Bartosz G (2015) Prevention of protein glycation by natural compounds. Molecules 20:3309–3334. https://doi.org/10.3390/molecules20023309

doi: 10.3390/molecules20023309 pubmed: 25690291 pmcid: 6272653

Anaga N, Abraham DB B, et al (2020) Advanced glycation end-products (AGE) trapping agents: design and synthesis of nature inspired indeno[2,1-c]pyridinones. https://doi.org/10.1016/J.BIOORG.2020.104375 . Bioorganic Chem 105:

Chen Y, Tang S, Chen Y et al (2019) Structure-activity relationship of procyanidins on advanced glycation end products formation and corresponding mechanisms. Food Chem 272:679–687. https://doi.org/10.1016/j.foodchem.2018.08.090

doi: 10.1016/j.foodchem.2018.08.090 pubmed: 30309598

Fan F-Y, Sang L-X, Jiang M (2017) Catechins and their therapeutic benefits to inflammatory bowel disease. Mol J Synth Chem Nat Prod Chem 22:484. https://doi.org/10.3390/molecules22030484

doi: 10.3390/molecules22030484

Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. https://doi.org/10.1016/0022-1759(83)90303-4

doi: 10.1016/0022-1759(83)90303-4 pubmed: 6606682

Bo J, Xie S, Guo Y et al (2016) Methylglyoxal Impairs Insulin Secretion of Pancreatic β-Cells through Increased Production of ROS and Mitochondrial Dysfunction Mediated by Upregulation of UCP2 and MAPKs. J Diabetes Res 2016:2029854. https://doi.org/10.1155/2016/2029854

Zhu Y, Shu T, Lin Y et al (2011) Inhibition of the receptor for advanced glycation endproducts (RAGE) protects pancreatic β-cells. Biochem Biophys Res Commun 404:159–165. https://doi.org/10.1016/j.bbrc.2010.11.085

doi: 10.1016/j.bbrc.2010.11.085 pubmed: 21111711

Guillam MT, Dupraz P, Thorens B (2000) Glucose uptake, utilization, and signaling in GLUT2-null islets. Diabetes 49:1485–1491. https://doi.org/10.2337/diabetes.49.9.1485

doi: 10.2337/diabetes.49.9.1485 pubmed: 10969832

Dhar A, Dhar I, Jiang B et al (2011) Chronic Methylglyoxal infusion by Minipump causes pancreatic β-Cell dysfunction and induces type 2 diabetes in Sprague-Dawley rats. Diabetes 60:899–908. https://doi.org/10.2337/db10-0627

doi: 10.2337/db10-0627 pubmed: 21300844 pmcid: 3046851

Jung H, Joo J, Jeon Y et al (2011) Advanced glycation end products downregulate glucokinase in mice. Diabetes Metab Res Rev 27:557–563. https://doi.org/10.1002/dmrr.1208

doi: 10.1002/dmrr.1208 pubmed: 21538775

Yoo HJ, Hong CO, Ha SK, Lee KW (2020) Chebulic acid prevents methylglyoxal-induced mitochondrial dysfunction in ins-1 pancreatic β-cells. Antioxidants 9:1–16. https://doi.org/10.3390/antiox9090771

doi: 10.3390/antiox9090771

Kennedy RT, Kauri LM, Dahlgren GM, Jung S-K (2002) Metabolic oscillations in beta-cells. Diabetes 51 Suppl 1 https://doi.org/10.2337/diabetes.51.2007.s152 . :S152-161

Dadi PK, Vierra NC, Ustione A et al (2014) Inhibition of pancreatic β-Cell Ca2+/Calmodulin-dependent protein kinase II reduces glucose-stimulated calcium influx and insulin secretion, impairing glucose tolerance. J Biol Chem 289:12435–12445. https://doi.org/10.1074/jbc.M114.562587

doi: 10.1074/jbc.M114.562587 pubmed: 24627477 pmcid: 4007438

Wang H, Ai J, Shopit A et al (2022) Protection of pancreatic β-cell by phosphocreatine through mitochondrial improvement via the regulation of dual AKT/IRS-1/GSK-3β and STAT3/Cyp-D signaling pathways. Cell Biol Toxicol 38:531–551. https://doi.org/10.1007/s10565-021-09644-7

doi: 10.1007/s10565-021-09644-7 pubmed: 34455488

Otani K, Kulkarni RN, Baldwin AC et al (2004) Reduced beta-cell mass and altered glucose sensing impair insulin-secretory function in betaIRKO mice. Am J Physiol Endocrinol Metab 286:E41–49. https://doi.org/10.1152/ajpendo.00533.2001

doi: 10.1152/ajpendo.00533.2001 pubmed: 14519599

Liu Z, Tanabe K, Bernal-Mizrachi E, Permutt MA (2008) Mice with beta cell overexpression of glycogen synthase kinase-3beta have reduced beta cell mass and proliferation. Diabetologia 51:623–631. https://doi.org/10.1007/s00125-007-0914-7

doi: 10.1007/s00125-007-0914-7 pubmed: 18219478

Prudente S, Sesti G, Pandolfi A et al (2012) The mammalian Tribbles Homolog TRIB3, glucose homeostasis, and Cardiovascular diseases. Endocr Rev 33:526–546. https://doi.org/10.1210/er.2011-1042

doi: 10.1210/er.2011-1042 pubmed: 22577090 pmcid: 3410226

Wang M, Zhang W, Xu S et al (2017) TRB3 mediates advanced glycation end product-induced apoptosis of pancreatic β-cells through the protein kinase C β pathway. Int J Mol Med 40:130–136. https://doi.org/10.3892/ijmm.2017.2991

doi: 10.3892/ijmm.2017.2991 pubmed: 28534945 pmcid: 5466392

Holland AM, Hale MA, Kagami H et al (2002) Experimental control of pancreatic development and maintenance. Proc Natl Acad Sci 99:12236–12241. https://doi.org/10.1073/pnas.192255099

doi: 10.1073/pnas.192255099 pubmed: 12221286 pmcid: 129428

Lee B-H, Hsu W-H, Hsu Y-W, Pan T-M (2013) Dimerumic acid protects pancreas damage and elevates insulin production in methylglyoxal-treated pancreatic RINm5F cells. J Funct Foods 5:642–650. https://doi.org/10.1016/j.jff.2012.12.007

doi: 10.1016/j.jff.2012.12.007

Kaneto H, Xu G, Fujii N et al (2002) Involvement of c-Jun N-terminal kinase in oxidative stress-mediated suppression of insulin gene Expression*. J Biol Chem 277:30010–30018. https://doi.org/10.1074/jbc.M202066200

doi: 10.1074/jbc.M202066200 pubmed: 12011047

Zhang C, Moriguchi T, Kajihara M et al (2005) MafA is a Key Regulator of glucose-stimulated insulin secretion. Mol Cell Biol 25:4969. https://doi.org/10.1128/MCB.25.12.4969-4976.2005

doi: 10.1128/MCB.25.12.4969-4976.2005 pubmed: 15923615 pmcid: 1140590

Okauchi S, Shimoda M, Obata A et al (2016) Protective effects of SGLT2 inhibitor luseogliflozin on pancreatic β-cells in obese type 2 diabetic db/db mice. Biochem Biophys Res Commun 470:772–782. https://doi.org/10.1016/j.bbrc.2015.10.109

doi: 10.1016/j.bbrc.2015.10.109 pubmed: 26505796

Tanigawa T, Kanazawa S, Ichibori R et al (2014) (+)-Catechin protects dermal fibroblasts against oxidative stress-induced apoptosis. BMC Complement Altern Med 14:133. https://doi.org/10.1186/1472-6882-14-133

doi: 10.1186/1472-6882-14-133 pubmed: 24712558 pmcid: 4004505

Zhang P, Li Y, Guo R, Zang W (2018) Salidroside protects against Advanced Glycation End products-Induced Vascular endothelial dysfunction. Med Sci Monit Int Med J Exp Clin Res 24:2420–2428. https://doi.org/10.12659/MSM.906064

doi: 10.12659/MSM.906064

Zhu D, Wang L, Zhou Q et al (2014) (+)-Catechin ameliorates diabetic nephropathy by trapping methylglyoxal in type 2 diabetic mice. Mol Nutr Food Res 58:2249–2260. https://doi.org/10.1002/mnfr.201400533

doi: 10.1002/mnfr.201400533 pubmed: 25243815