Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T11:17:19.877Z Has data issue: false hasContentIssue false
  • English
  • Français

Early postnatal exposure of rat pups to methylglyoxal induces oxidative stress, inflammation and dysmetabolism at adulthood

Published online by Cambridge University Press:  21 January 2022

Flávio A. Francisco ,
Lucas P. J. Saavedra Open the ORCID record for Lucas P. J. Saavedra [Opens in a new window] ,
Marcos D. Ferreira-Junior Open the ORCID record for Marcos D. Ferreira-Junior [Opens in a new window] ,
Keilah V. N. Cavalcante ,
Veridiana M. Moreira ,
Kelly V. Prates Open the ORCID record for Kelly V. Prates [Opens in a new window] ,
Stephanie C. Borges ,
Nilza C. Buttow ,
Tatiane A. Ribeiro  and
Gustavo R. Pedrino
...Show all authors
Flávio A. Francisco
Affiliation:
Department of Biotechnology, Genetics, and Cellular Biology, State University of Maringá, Maringá, Brazil
Lucas P. J. Saavedra
Affiliation:
Department of Biotechnology, Genetics, and Cellular Biology, State University of Maringá, Maringá, Brazil
Marcos D. Ferreira-Junior
Affiliation:
Department of Physiological Sciences, Federal University of Goiás, Goiânia, Brazil
Keilah V. N. Cavalcante
Affiliation:
Department of Physiological Sciences, Federal University of Goiás, Goiânia, Brazil
Veridiana M. Moreira
Affiliation:
Department of Biotechnology, Genetics, and Cellular Biology, State University of Maringá, Maringá, Brazil Department of Physiology, Federal University of Sergipe, São Cristóvão, Brazil
Kelly V. Prates
Affiliation:
Department of Biotechnology, Genetics, and Cellular Biology, State University of Maringá, Maringá, Brazil
Stephanie C. Borges
Affiliation:
Department of Morphological Sciences, State University of Maringá, Maringá, Brazil
Nilza C. Buttow
Affiliation:
Department of Morphological Sciences, State University of Maringá, Maringá, Brazil
Tatiane A. Ribeiro
Affiliation:
Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, ON, Canada
Gustavo R. Pedrino
Affiliation:
Department of Physiological Sciences, Federal University of Goiás, Goiânia, Brazil
Carlos H. Xavier
Affiliation:
Department of Physiological Sciences, Federal University of Goiás, Goiânia, Brazil
Paulo Matafome
Affiliation:
Coimbra Institute of Clinical and Biomedical Research (iCBR), Faculty of Medicine and Center for Innovative Biomedicine and Biotechnology (CIBB), University of Coimbra, Coimbra, Portugal Clinical Academic Center of Coimbra, Coimbra, Portugal Department of Complementary Sciences, Instituto Politécnico de Coimbra, Coimbra Health School (ESTeSC), Coimbra, Portugal
Paulo C. de Freitas Mathias
Affiliation:
Department of Biotechnology, Genetics, and Cellular Biology, State University of Maringá, Maringá, Brazil
Rodrigo M. Gomes*
Affiliation:
Department of Physiological Sciences, Federal University of Goiás, Goiânia, Brazil
*
Address for correspondence: Rodrigo M. Gomes, Laboratory of Endocrine Physiology and Metabolism (LabFEM), Department of Physiological Sciences (DCiF) – Biological Science Institute II (ICB-II), room 101, Federal University of Goiás (UFG) – Campus II, Esperança Avenue s/n, Goiânia, GO 74690-900, Brazil. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This work aimed to investigate the effects of early progeny exposure to methylglyoxal (MG), programming for metabolic dysfunction and diabetes-like complications later in life. At delivery (PN1), the animals were separated into two groups: control group (CO), treated with saline, and MG group, treated with MG (20 mg/kg of BW; i.p.) during the first 2 weeks of the lactation period. In vivo experiments and tissue collection were done at PN90. Early MG exposure decreased body weight, adipose tissue, liver and kidney weight at adulthood. On the other hand, MG group showed increased relative food intake, blood fructosamine, blood insulin and HOMA-IR, which is correlated with insulin resistance. Besides, MG-treated animals presented dyslipidaemia, increased oxidative stress and inflammation. Likewise, MG group showed steatosis and perivascular fibrosis in the liver, pancreatic islet hypertrophy, increased glomerular area and pericapsular fibrosis, but reduced capsular space. This study shows that early postnatal exposure to MG induces oxidative stress, inflammation and fibrosis markers in pancreas, liver and kidney, which are related to metabolic dysfunction features. Thus, nutritional disruptors during lactation period may be an important risk factor for metabolic alterations at adulthood.

Keywords

Metabolic programmingAGEsmethylglyoxaldyslipidaemialactation
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 5 , October 2022 , pp. 617 - 625
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Chen, H, Simar, D, Lambert, K, Mercier, J, Morris, MJ. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology. 2008; 149(11), 5348–5356.CrossRefGoogle ScholarPubMed
Melo, AM, Benatti, RO, Ignacio-Souza, LM, et al. Hypothalamic endoplasmic reticulum stress and insulin resistance in offspring of mice dams fed high-fat diet during pregnancy and lactation. Metab Clin Exp. 2014; 63(5), 682–692.CrossRefGoogle ScholarPubMed
Phillips, SA, Thornalley, PJ. The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal. Eur J Biochem. 1993; 212(1), 101–105.CrossRefGoogle ScholarPubMed
Miyata, T, Inagi, R, Asahi, K, et al. Generation of protein carbonyls by glycoxidation and lipoxidation reactions with autoxidation products of ascorbic acid and polyunsaturated fatty acids. FEBS Lett. 1998; 437(1-2), 24–28.CrossRefGoogle ScholarPubMed
Miyata, T, Van Ypersele de Strihou, C, Kurokawa, K, Baynes, JW. Alterations in nonenzymatic biochemistry in uremia: origin and significance of, carbonyl stress, in long-term uremic complications. Kidney Int. 1999; 55(2), 389–399.CrossRefGoogle ScholarPubMed
Matafome, P, Rodrigues, T, Sena, C, Seiça, R. Methylglyoxal in metabolic disorders: facts, myths, and promises. Med Res Rev. 2017; 37(2), 368–403.CrossRefGoogle ScholarPubMed
Uribarri, J, del Castillo, MD, de la Maza, MP, et al. Dietary advanced glycation end products and their role in health and disease. Adv Nut. 2015; 6(4), 461–473.CrossRefGoogle ScholarPubMed
Li, S, Yang, H. Relationship between advanced glycation end products and gestational diabetes mellitus. J Matern-Fetal Neonatal Med. 2019; 32(17), 2783–2789.CrossRefGoogle ScholarPubMed
Francisco, FA, Barella, LF, da Silveira, S, et al. Methylglyoxal treatment in lactating mothers leads to type 2 diabetes phenotype in male rat offspring at adulthood. Eur J Nutr. 2018; 57(2), 477–486.CrossRefGoogle ScholarPubMed
McLellan, AC, Phillips, SA, Thornalley, PJ. The assay of S-D-lactoylglutathione in biological systems. Anal Biochem. 1993; 211(1), 37–43.CrossRefGoogle ScholarPubMed
Dakin, HD, Dudley, HW. An enzyme concerned with the formation of hydroxy acids from ketonic aldehydes. J Biol Chem. 1913; 14(2), 155–157.CrossRefGoogle Scholar
Rabbani, N, Xue, M, Thornalley, PJ. Dicarbonyls and glyoxalase in disease mechanisms and clinical therapeutics. Glycoconj J. 2016; 33(4), 513–525.CrossRefGoogle ScholarPubMed
Monnier, VM, Taniguchi, N. Advanced glycation in diabetes, aging and age-related diseases: editorial and dedication. Glycoconj J. 2016; 33(4), 483–486.CrossRefGoogle ScholarPubMed
Moura, AS, Carpinelli, AR, Barbosa, FB, Gravena, C, De Freitas Mathias, PC. Undernutrition during early lactation as an alternative model to study the onset of diabetes mellitus type II. Res Commun Mol Pathol Pharmacol. 1996; 92, 73–84.Google Scholar
de Oliveira, JC, Scomparin, DX, Andreazzi, AE, et al. Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. J Neuroendocrinol. 2011; 23(2), 148–157.CrossRefGoogle ScholarPubMed
Hales, CN, Barker, DJP. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Int J Epidemiol. 2013; 42(5), 1215–1222.CrossRefGoogle ScholarPubMed
Desai, M, Jellyman, JK, Han, G, Beall, M, Lane, RH, Ross, MG. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am J Obstet Gynecol. 2014; 211(3), 237.e1–237.e13.CrossRefGoogle ScholarPubMed
Guarda, DS, Lisboa, PC, de Oliveira, E, Nogueira-Neto, JF, de Moura, EG, Figueiredo, MS. Flaxseed oil during lactation changes milk and body composition in male and female suckling pups rats. Food Chem Toxicol. 2014; 69, 69–75.CrossRefGoogle ScholarPubMed
Valério Prates, K, Ribeiro, TA, Pavanello, A, et al. Potential attenuation of early-life overfeeding-induced metabolic dysfunction by chronic maternal acetylcholinesterase inhibitor exposure. Toxicology. 2019; 425(4), 152250.CrossRefGoogle ScholarPubMed
Federico, G, Gori, M, Randazzo, E, Vierucci, F. Skin advanced glycation end-products evaluation in infants according to the type of feeding and mother’s smoking habits. SAGE Open Med. 2016; 4(11), 205031211668212.CrossRefGoogle Scholar
Kutlu, T. Dietary glycotoxins and infant formulas. Turk Pediatri Arsivi. 2016; 51, 179–185.CrossRefGoogle ScholarPubMed
Prosser, CG, Carpenter, EA, Hodgkinson, AJ. Nϵ-carboxymethyllysine in nutritional milk formulas for infants. Food Chem. 2019; 274(10–11), 886–890.CrossRefGoogle Scholar
Gomes, RM, Tófolo, LP, Rinaldi, W, et al. Moderate exercise restores pancreatic beta-cell function and autonomic nervous system activity in obese rats induced by high-fat diet. Cell Physiol Biochem. 2013; 32(2), 310–321.CrossRefGoogle ScholarPubMed
Berlanga, J, Cibrian, D, Guillén, I, et al. Methylglyoxal administration induces diabetes-like microvascular changes and perturbs the healing process of cutaneous wounds. Clin Sci. 2005; 109(1), 83–95.CrossRefGoogle ScholarPubMed
Antunes, LC, Elkfury, JL, Jornada, MN, Foletto, KC, Bertoluci, MC. Validation of HOMA-IR in a model of insulin-resistance induced by a high-fat diet in Wistar rats. Arch Endocrinol Metab. 2016; 60(2), 138–142.CrossRefGoogle Scholar
Borges, SC, Ferreira, PEB, da Silva, LM, et al. Evaluation of the treatment with resveratrol-loaded nanoparticles in intestinal injury model caused by ischemia and reperfusion. Toxicology. 2018; 396-397(1), 13–22.CrossRefGoogle ScholarPubMed
Prosser, CG, Carpenter, EA, Hodgkinson, AJ. Nϵ-carboxymethyllysine in nutritional milk formulas for infants. Food Chem. 2019; 274(10–11), 886–890.CrossRefGoogle Scholar
Milkovska-Stamenova, S, Hoffmann, R. Influence of storage and heating on protein glycation levels of processed lactose-free and regular bovine milk products. Food Chem. 2017; 221(19), 489–495.CrossRefGoogle ScholarPubMed
Dittrich, R, Hoffmann, I, Stahl, P, Müller, A, Beckmann, MW, Pischetsrieder, M. Concentrations of Nϵ-carboxymethyllysine in human breast milk, infant formulas, and urine of infants. J Agric Food Chem. 2006; 54(18), 6924–6928.CrossRefGoogle Scholar
Rodrigues, T, Matafome, P, Santos-Silva, D, Sena, C, Seiça, R. Reduction of methylglyoxal-induced glycation by pyridoxamine improves adipose tissue microvascular lesions. J Diabetes Res. 2013; 2013(8), 1–9.CrossRefGoogle ScholarPubMed
Rodrigues, T, Matafome, P, Sereno, J, et al. Methylglyoxal-induced glycation changes adipose tissue vascular architecture, flow and expansion, leading to insulin resistance. Sci Rep. 2017; 7(1), 1698.CrossRefGoogle ScholarPubMed
Hosogai, N, Fukuhara, A, Oshima, K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes. 2007; 56(4), 901–911.CrossRefGoogle ScholarPubMed
Rutkowski, JM, Davis, KE, Scherer, PE. Mechanisms of obesity and related pathologies: the macro- and microcirculation of adipose tissue. FEBS J. 2009; 276(20), 5738–5746.CrossRefGoogle ScholarPubMed
Biswas, UK, Kumar, A. Study on the changes of carbonic anhydrase activity in insulin resistance and the effect of methylglyoxal. J Pak Med Assoc. 2012; 62, 417–421.Google Scholar
Sheader, EA, Benson, RSP, Best, L. Cytotoxic action of methylglyoxal on insulin-secreting cells. Biochem Pharmacol. 2001; 61(11), 1381–1386.CrossRefGoogle ScholarPubMed
Riboulet-Chavey, A, Pierron, A, Durand, I, Murdaca, J, Giudicelli, J, Van Obberghen, E. Methylglyoxal impairs the insulin signaling pathways independently of the formation of intracellular reactive oxygen species. Diabetes. 2006; 55(5), 1289–1299.CrossRefGoogle ScholarPubMed
Franco, JG, Dias-Rocha, CP, Fernandes, TP, et al. Resveratrol treatment rescues hyperleptinemia and improves hypothalamic leptin signaling programmed by maternal high-fat diet in rats. Eur J Nutr. 2016; 55(2), 601–610.CrossRefGoogle ScholarPubMed
Meerwaldt, R, Links, T, Zeebregts, C, Tio, R, Hillebrands, J-L, Smit, A. The clinical relevance of assessing advanced glycation endproducts accumulation in diabetes. Cardiovasc Diabetol. 2008; 7(1), 29.CrossRefGoogle ScholarPubMed
da Silva Lima, N, de Moura, EG, Passos, MCF, et al. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr. 2011; 105(9), 1405–1413.CrossRefGoogle Scholar
Chen, C, Hosokawa, H, Bumbalo, LM, Leahy, JL. Mechanism of compensatory hyperinsulinemia in normoglycemic insulin- resistant spontaneously hypertensive rats. Augmented enzymatic activity of glucokinase in β-cells. J Clin Investig. 1994; 94(1), 399–404.CrossRefGoogle ScholarPubMed
Sechi, LA, Griffin, CA, Giacchetti, G, et al. Abnormalities of insulin receptors in spontaneously hypertensive rats. Hypertension. 1996; 27(4), 955–961.CrossRefGoogle ScholarPubMed
Wang, X, Desai, K, Chang, T, Wu, L. Vascular methylglyoxal metabolism and the development of hypertension. J Hypertens. 2005; 23(8), 1565–1573.CrossRefGoogle ScholarPubMed
Chang, T, Wang, R, Wu, L. Methylglyoxal-induced nitric oxide and peroxynitrite production in vascular smooth muscle cells. Free Radic Biol Med. 2005; 38(2), 286–293.CrossRefGoogle ScholarPubMed
Thornalley, PJ. Glutathione-dependent detoxification of α-oxoaldehydes by the glyoxalase system: involvement in disease mechanisms and antiproliferative activity of glyoxalase I inhibitors. Chem Biol Interact. 1998; 111-112, 137–151.CrossRefGoogle ScholarPubMed
Cha, SH, Hwang, Y, Heo, SJ, Jun, HS. Indole-4-carboxaldehyde isolated from seaweed, sargassum thunbergii, attenuates methylglyoxal-induced hepatic inflammation. Mar Drugs. 2019; 17(9), 486.CrossRefGoogle ScholarPubMed
Neves, C, Rodrigues, T, Sereno, J, et al. Dietary glycotoxins impair hepatic lipidemic profile in diet-induced obese rats causing hepatic oxidative stress and insulin resistance. Oxid Med Cell Longev. 2019; 2019(12), 1–14.Google ScholarPubMed
Gaens, KHJ, Niessen, PMG, Rensen, SS, et al. Endogenous formation of Nϵ-(carboxymethyl)lysine is increased in fatty livers and induces inflammatory markers in an in vitro model of hepatic steatosis. J Hepatol. 2012; 56(3), 647–655.CrossRefGoogle Scholar
Rodrigues, L, Matafome, P, Crisóstomo, J, et al. Advanced glycation end products and diabetic nephropathy: a comparative study using diabetic and normal rats with methylglyoxal-induced glycation. J Physiol Biochem. 2014; 70(1), 173–184.CrossRefGoogle ScholarPubMed
Markova, I, Hüttl, M, Oliyarnyk, O, et al. The effect of dicarbonyl stress on the development of kidney dysfunction in metabolic syndrome - A transcriptomic and proteomic approach. Nutr Metab. 2019; 16(1), 51.CrossRefGoogle ScholarPubMed
Vlassara, H. Advanced glycation in health and disease: role of the modern environment. Ann N Y Acad Sci. 2005; 1043(1), 452–460.CrossRefGoogle ScholarPubMed
Uribarri, J, Cai, W, Ramdas, M, et al. Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1. Diabetes Care. 2011; 34(7), 1610–1616.CrossRefGoogle ScholarPubMed
Mark, AB, Poulsen, MW, Andersen, S, et al. Consumption of a diet low in advanced glycation end products for 4 weeks improves insulin sensitivity in overweight women. Diabetes Care. 2014; 37(1), 88–95.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Francisco et al. supplementary material

Francisco et al. supplementary material

Download Francisco et al. supplementary material(Image)
Image 1.8 MB