The proteomic profile is altered but not repaired after bariatric surgery in type 2 diabetes pigs.
ALKBH proteins
DNA modifications
Diabetes
High energy diet
Pig model
Proteomic studies
Scopinaro bariatric surgery
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 May 2024
03 May 2024
Historique:
received:
14
11
2023
accepted:
17
04
2024
medline:
4
5
2024
pubmed:
4
5
2024
entrez:
3
5
2024
Statut:
epublish
Résumé
To reveal the sources of obesity and type 2 diabetes (T2D) in humans, animal models, mainly rodents, have been used. Here, we propose a pig model of T2D. Weaned piglets were fed high fat/high sugar diet suppling 150% of metabolizable energy. Measurements of weight gain, blood morphology, glucose plasma levels, cholesterol, and triglycerides, as well as glucose tolerance (oral glucose tolerance test, OGTT) were employed to observe T2D development. The histology and mass spectrometry analyses were made post mortem. Within 6 months, the high fat-high sugar (HFHS) fed pigs showed gradual and significant increase in plasma triglycerides and glucose levels in comparison to the controls. Using OGTT test, we found stable glucose intolerance in 10 out of 14 HFHS pigs. Mass spectrometry analysis indicated significant changes in 330 proteins in the intestine, liver, and pancreas of the HFHS pigs. These pigs showed also an increase in DNA base modifications and elevated level of the ALKBH proteins in the tissues. Six diabetic HFHS pigs underwent Scopinaro bariatric surgery restoring glycaemia one month after surgery. In conclusion, a high energy diet applied to piglets resulted in the development of hyperlipidaemia, hyperglycaemia, and type 2 diabetes being reversed by a bariatric procedure, excluding the proteomic profile utill one month after the surgery.
Identifiants
pubmed: 38702370
doi: 10.1038/s41598-024-60022-9
pii: 10.1038/s41598-024-60022-9
doi:
Substances chimiques
Blood Glucose
0
Proteome
0
Triglycerides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10235Subventions
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Ministerstwo Edukacji i Nauki
ID : SPUB/SP/530290/2022
Organisme : Polish-Norwegian Research Fund Grant
ID : POL-NOR/196258/59/2013
Organisme : Polish-Norwegian Research Fund Grant
ID : POL-NOR/196258/59/2013
Organisme : Polish-Norwegian Research Fund Grant
ID : POL-NOR/196258/59/2013
Organisme : Polish-Norwegian Research Fund Grant
ID : POL-NOR/196258/59/2013
Organisme : Polish-Norwegian Research Fund Grant
ID : POL-NOR/196258/59/2013
Organisme : Narodowym Centrum Nauki
ID : UMO-2017/25/B/NZ4/02668
Organisme : Narodowym Centrum Nauki
ID : UMO-2017/25/B/NZ4/02668
Organisme : Narodowym Centrum Nauki
ID : UMO-2017/25/B/NZ4/02668
Organisme : Narodowym Centrum Nauki
ID : UMO-2017/25/B/NZ4/02668
Organisme : Narodowym Centrum Nauki
ID : UMO-2017/25/B/NZ4/02668
Informations de copyright
© 2024. The Author(s).
Références
Bouchard, C. The biological predisposition to obesity: Beyond the thrifty genotype scenario. Int. J. Obes. 31 (2007).
Murri, M. et al. Changes in oxidative stress and insulin resistance in morbidly obese patients after bariatric surgery. Obes. Surg. 20, (2010).
Shabalala, S. C. et al. Detrimental Effects of Lipid Peroxidation in Type 2 Diabetes: Exploring the Neutralizing Influence of Antioxidants. Antioxidants 11, (2022).
Tangvarasittichai, S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J. Diabetes 6, (2015).
Ferenc, K. et al. Intracellular and tissue specific expression of FTO protein in pig: changes with age, energy intake and metabolic status. Sci. Rep. 10, (2020).
Rao, R. S., Yanagisawa, R. & Kini, S. Insulin resistance and bariatric surgery. Obes. Rev. 13, (2012).
Ferchak, C. V. & Meneghini, L. F. Obesity, bariatric surgery and type 2 diabetes - A systematic review. Diabetes Metab. Res. Rev. 20, (2004).
Buchwald, H. et al. Bariatric Surgery A Systematic Review and Meta-analysis. JAMA 13, (2004).
Rubino, F. et al. The early effect of the Roux-en-Y gastric bypass on hormones involved in body weight regulation and glucose metabolism. Ann. Surg. 240, (2004).
Dib, N. et al. Early-effect of bariatric surgery (Scopinaro method) on intestinal hormones and adipokines in insulin resistant wistar rat. J. Physiol. Pharmacol. 64, (2013).
Srinivasan, K. & Ramarao, P. Animal models in type 2 diabetes research: An overview. Indian J. Med. Res. 125, (2007).
Boissel, S. et al. Loss-of-function mutation in the dioxygenase-encoding FTO gene causes severe growth retardation and multiple malformations. Am. J. Hum. Genet. 85, (2009).
Hasler-Rapacz, J. et al. Effects of simvastatin on plasma lipids and apolipoproteins in familial hypercholesterolemic swine. Arterioscler. Thromb. Vasc. Biol. 16, (1996).
Bellinger, D. A., Merricks, E. P. & Nichols, T. C. Swine models of type 2 diabetes mellitus: Insulin resistance, glucose tolerance, and cardiovascular complications. ILAR J. (2006)
Larsen, M. O. & Rolin, B. Use of the Göttingen minipig as a model of diabetes, with special focus on type 1 diabetes research. ILAR J. 45, (2004).
Guilloteau, P., Zabielski, R., Hammon, H. M. & Metges, C. C. Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr. Res. Rev. (2010).
Ferenc, K. et al. Intrauterine growth retarded piglet as a model for humans - Studies on the perinatal development of the gut structure and function. Reprod. Biol. 14, (2014).
Badin, J. K. et al. Alloxan-induced diabetes exacerbates coronary atherosclerosis and calcification in Ossabaw miniature swine with metabolic syndrome. J. Transl. Med. 16, (2018).
Bassols, A. et al. The pig as an animal model for human pathologies: A proteomics perspective. Proteomics Clin. Appl. 8 (2014).
Obtułowicz, T. et al. Aberrant repair of etheno-DNA adducts in leukocytes and colon tissue of colon cancer patients. Free Radic. Biol. Med. 49, (2010).
Shoelson, S. E., Lee, J. & Goldfine, A. B. Inflammation and insulin resistance. J. Clin. Invest. 116, (2006).
Shin, G., Jang, K., Kim, M., Lee, J. H. & Yoo, H. J. Inflammatory Markers and Plasma Fatty Acids in Predicting WBC Level Alterations in Association With Glucose-Related Markers: A Cross-Sectional Study. Front. Immunol. 11, (2020).
Zatterale, F. et al. Chronic Adipose Tissue Inflammation Linking Obesity to Insulin Resistance and Type 2 Diabetes. Front. Physiol. 10, (2020).
Tagi, V. M., Giannini, C. & Chiarelli, F. Insulin resistance in children. Front. Endocrinol. 10, (2019).
King, A. J. F. The use of animal models in diabetes research. Brit. J. Pharmacol. 166, (2012).
Zuo, L. et al. Inflammaging and oxidative stress in human diseases: From molecular mechanisms to novel treatments. Int. J. Mol. Sci. 20, (2019).
Kasuga, M. Insulin resistance and pancreatic β cell failure. J. Clin. Invest. 116, (2006).
Hall, T. C., Pellen, M. G. C., Sedman, P. C. & Jain, P. K. Preoperative factors predicting remission of type 2 diabetes mellitus after Roux-en-Y Gastric bypass surgery for obesity. Obes. Surg. 20, (2010).
Pond, W. G. et al. Effect of dietary fat and cholesterol level on growing pigs selected for three generations for high or low serum cholesterol at age 56 days. J. Anim. Sci. 70, (1992).
Khalaf, K. I. & Taegtmeyer, H. Clues from bariatric surgery: Reversing insulin resistance to heal the heart. Curr. Diab. Rep. 13, (2013).
Stenberg, E. & Thorell, A. Insulin resistance in bariatric surgery. Curr. Opin. Clin. Nutr. Metab. Care 23, (2020).
Bensellam, M., Laybutt, D. R. & Jonas, J. C. The molecular mechanisms of pancreatic β-cell glucotoxicity: Recent findings and future research directions. Mol. Cell. Endocrinol. 364, (2012).
Klöppel, G., Löhr, M., Habich, K., Oberholzer, M. & Heitz, P.U. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv. Synth. Pathol. Res.4, (1985)
Mezza, T. et al. Insulin resistance alters islet morphology in nondiabetic humans. Diabetes 63, (2014)
Kehm, R. et al.. Age-related oxidative changes in pancreatic islets are predominantly located in the vascular system. Redox Biol. 15, (2018).
Jo, J. Choi, M.Y. & Koh, D.S. Size Distribution of Mouse Langerhans Islets. Biophys. J. 93, (2007).
Langie, S. A. S. et al. The effect of oxidative stress on nucleotide-excision repair in colon tissue of newborn piglets. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 695, (2010).
Langie, S. A. S. et al. Redox and epigenetic regulation of the APE1 gene in the hippocampus of piglets: The effect of early life exposures. DNA Repair (Amst). 18, (2014).
Hill, J. W., Hazra, T. K., Izumi, T. & Mitra, S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: Potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29, (2001).
Olinski, R. et al. DNA base modifications in chromatin of human cancerous tissues. FEBS Lett. 309, (1992).
Shigenaga, M. K., Gimeno, C. J. & Ames, B. N. Urinary 8-hydroxy-2’-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc. Natl. Acad. Sci. U. S. A. 86, (1989).
Halliwell, B. Can oxidative DNA damage be used as a biomarker of cancer risk in humans? Problems, resolutions and preliminary results from nutritional supplementation studies. Free Radic. Res. 29, (1998).
Arcidiacono, B. et al. Insulin resistance and cancer risk: An overview of the pathogenetic mechanisms. Exp. Diabetes Res. 2012 (2012).
Fraga, C. G., Shigenaga, M. K., Park, J. W., Degan, P. & Ames, B. N. Oxidative damage to DNA during aging: 8-Hydroxy-2’-deoxyguanosine in rat organ DNA and urine. Proc. Natl. Acad. Sci. U. S. A. 87, (1990).
Marnett, L. J. Oxyradicals and DNA damage. Carcinogenesis 21, (2000).
Kowalczyk, P. et al. Inflammation increases oxidative DNA damage repair and stimulates preneoplastic changes in colons of newborn rats. J Physiol. Pharmacol. 67, (2016).
Le Tran, N., Wang, Y. & Nie, G. Podocalyxin in normal tissue and epithelial cancer. Cancers 13, (2021).
Krupenko, S. A., & Oleinik, N. V. 10-Formyltetrahydrofolate dehydrogenase, one of the major folate enzymes, is down-regulated in tumor tissues and possesses suppressor effects on cancer cells. Cell Growth Differ. 13, (2002).
Musso, G., Gambino, R. & Cassader, M. Obesity, diabetes, and gut microbiota: The hygiene hypothesis expanded? Diabetes Care 33, (2010).
Krack, A., Sharma, R., Figulla, H. R. & Anker, S. D. The importance of the gastrointestinal system in the pathogenesis of heart failure. Eur. Heart J. 26, (2005).
Leustean, A. M. et al. Implications of the intestinal microbiota in diagnosing the progression of diabetes and the presence of cardiovascular complications. J. Diabetes Res. 2018, (2018).
Kitai, T. & Tang, W. H. W. Gut microbiota in cardiovascular disease and heart failure. Clin. Sci. 132, (2018).
Wang, C. et al. Small intestine proteomics coupled with serum metabolomics reveal disruption of amino acid metabolism in Chinese hamsters with type 2 diabetes mellitus. J. Proteomics 223, (2020).
Vilahur, G., Ben-Aicha, S. & Badimon, L. New insights into the role of adipose tissue in thrombosis. Cardiovasc. Res. 113, (2017).
Kaur, R., Kaur, M. & Singh, J. Endothelial dysfunction and platelet hyperactivity in type 2 diabetes mellitus: Molecular insights and therapeutic strategies. Cardiovasc. Diabetol. 17, (2018).
Chang, D. C., Xu, X., Ferrante, A. W. & Krakoff, J. Reduced plasma albumin predicts type 2 diabetes and is associated with greater adipose tissue macrophage content and activation. Diabetol. Metab. Syndr. 11, (2019).
Chen, Q., Lu, M., Monks, B. R. & Birnbaum, M. J. Insulin is required to maintain albumin expression by inhibiting forkhead box O1 protein. J. Biol. Chem. 291, (2016).
Hou, X. Z. et al. The negative association between serum albumin levels and coronary heart disease risk in adults over 45 years old: a cross-sectional survey. Sci. Rep. 13, (2023).
Aas, P. A. et al. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421, 859–863 (2003).
doi: 10.1038/nature01363
pubmed: 12594517
Duncan, T. et al. Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. U. S. A. (2002).
Falnes P, Øand Bjørås, M., Aas, P. A., Sundheim, O. & Seeberg, E. Substrate specificities of bacterial and human AlkB proteins. Nucleic Acids Res. 32, (2004).
Ringvoll, J. et al. AlkB homologue 2-mediated repair of ethenoadenine lesions in mammalian DNA. Cancer Res. 68, (2008).
Fu, D. & Samson, L. D. Direct repair of 3,N 4-ethenocytosine by the human ALKBH2 dioxygenase is blocked by the AAG/MPG glycosylase. DNA Repair (Amst) (2012).
Zdzalik, D. et al. Differential repair of etheno-DNA adducts by bacterial and human AlkB proteins. DNA Repair (Amst). (2015)
Bian, L., Meng, Y., Zhang, M. & Li, D. MRE11-RAD50-NBS1 complex alterations and DNA damage response: Implications for cancer treatment. Mol. Cancer 18, (2019).
Lee, M. Y., Leonardi, A., Begley, T. J. & Melendez, J. A. Loss of epitranscriptomic control of selenocysteine utilization engages senescence and mitochondrial reprogramming. Redox Biol. (2020).
Scheithauer, T. P. M. et al. Gut Microbiota as a Trigger for Metabolic Inflammation in Obesity and Type 2 Diabetes. Front. Immunol. 11, (2020).
Abudawood, M., Tabassum, H., Almaarik, B. & Aljohi, A. Interrelationship between oxidative stress, DNA damage and cancer risk in diabetes (Type 2) in Riyadh, KSA. Saudi J. Biol. Sci. 27, (2020).
Ahmed, S. A. H., Ansari, S. A., Mensah-Brown, E. P. K. & Emerald, B. S. The role of DNA methylation in the pathogenesis of type 2 diabetes mellitus. Clin. Epigen. 12, (2020).
Nicoletti, C. F. et al. DNA methylation screening after roux-en y gastric bypass reveals the epigenetic signature stems from genes related to the surgery per se. BMC Med. Genomics 12, (2019).
Liu, T., Zou, X., Ruze, R. & Xu, Q. Bariatric Surgery: Targeting pancreatic β cells to treat type II diabetes. Front. Endocrinol. 14, (2023).
Li, M.-M.M. et al. ALKBH4-dependent demethylation of actin regulates actomyosin dynamics. Nat. Commun. 4, 1832 (2013).
doi: 10.1038/ncomms2863
pubmed: 23673617
Hales, J., Moustsen, V. A., Nielsen, M. B. F. & Hansen, C. F. Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system. J. Anim. Sci. 91, (2013).
Scopinaro, N., Gianetta, E., Civalleri, D., Bonalumi, U. & Bachi, V. Bilio‐pancreatic bypass for obesity: II. Initial experience in man. Br. J. Surg. 66, (1979).
Olszewski, J. et al. Differences in intestinal barrier development between intrauterine growth restricted and normal birth weight piglets. Animals 11, (2021).
Szklarczyk, D. et al. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, (2019).
Eaton, S. L. et al. Total Protein Analysis as a Reliable Loading Control for Quantitative Fluorescent Western Blotting. PLoS One 8, (2013).
Pardela, M., Wiewióra, M., & Sitkiewicz, T. W. M. The progress in bariatric surgery. J. Physiol. Pharmacol. 56, (2005).