Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-19T04:37:44.198Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of Leuconostoc SD23 intake in obese pregnant rats: benefits for maternal metabolism

Part of: DOHaD Research in Latin-American

Published online by Cambridge University Press:  19 May 2020

Diana C. Castro-Rodríguez Open the ORCID record for Diana C. Castro-Rodríguez [Opens in a new window] ,
Gimena Juárez-Pilares ,
Luz Cano-Cano ,
Mariana Pérez-Sánchez ,
Carlos A. Ibáñez Open the ORCID record for Carlos A. Ibáñez [Opens in a new window] ,
Luis A. Reyes-Castro Open the ORCID record for Luis A. Reyes-Castro [Opens in a new window] ,
Jorge Yáñez-Fernández Open the ORCID record for Jorge Yáñez-Fernández [Opens in a new window]  and
Elena Zambrano Open the ORCID record for Elena Zambrano [Opens in a new window]
Diana C. Castro-Rodríguez
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico CONACYT-Cátedras, Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición SZ, Mexico City, Mexico
Gimena Juárez-Pilares
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Luz Cano-Cano
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Mariana Pérez-Sánchez
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Carlos A. Ibáñez
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Luis A. Reyes-Castro
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Jorge Yáñez-Fernández
Affiliation:
Bioprocess Department, Unidad Profesional Interdisciplinaria de Biotecnología (UPIBI), Instituto Politécnico Nacional (IPN), Mexico City, Mexico
Elena Zambrano*
Affiliation:
Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
*
Address for correspondence: Elena Zambrano, Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Maternal obesity (MO) during pregnancy and lactation leads to maternal and offspring metabolic dysfunction. Recent research has suggested that probiotics might be a novel approach to counteract these unwanted MO effects. The aim of this research was to analyze the impact of Leuconostoc SD23, a probiotic isolated from aguamiel (traditional Mexican drink), on MO metabolism in rats at the end of lactation (21 days). From weaning through lactation, control female Wistar rats (C) ate chow (5% fat) or high-energy obesogenic diet (MO; 25% fat). Half the C and MO mothers received a daily dose (1 × 1010 CFU/ml) of probiotic orally, control with probiotic (CP) and MO with probiotic (MOP), 1 month before mating and through pregnancy and lactation. Histological analyses of the liver, white adipose tissue and small intestine, body composition, glucose, insulin, triglycerides, and leptin were determined in mothers at the end of lactation. Maternal weight during pregnancy was greater in MO than C mothers, but similar at the end of lactation. Probiotic intervention had no effect on maternal weight. However, at the end of lactation, percentage of body fat was higher in MO than C, CP, and MOP. Serum glucose, homeostasis model assessment of insulin resistance, and triglycerides were higher in MO versus C, CP, and MOP. MO small intestine villus height was higher versus MOP, C, and CP. Leuconostoc SD23 did not present adverse effects in C. Conclusions: maternal administration of Leuconostoc SD23 has beneficial effects on maternal metabolism, which holds possibilities for preventing adverse offspring metabolic programming.

Keywords

ProbioticsobesityprogrammingAgave salmianaaguamiel
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 5 , October 2020 , pp. 533 - 539
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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

Tain, Y-L, Hsu, C-N.Developmental origins of chronic kidney disease: should we focus on early life? Int J Mol Sci. 2017; 18, 381.CrossRefGoogle ScholarPubMed
Dickinson, H, Moss, T, Gatford, KL, et al.A review of fundamental principles for animal models of DOHaD research: an Australian perspective. J Dev Orig Health Dis. 2016; 7, 449–472.CrossRefGoogle Scholar
Briffa, JF, O’Dowd, R, Moritz, KM, et al.Uteroplacental insufficiency reduces rat plasma leptin concentrations and alters placental leptin transporters: ameliorated with enhanced milk intake and nutrition. J Physiol. 2017; 595, 3389–3407.CrossRefGoogle ScholarPubMed
Cuffe, J, Turton, E, Akison, L, et al.Prenatal corticosterone exposure programs sex-specific adrenal adaptations in mouse offspring. Int J Endocrinol. 2017; 232, 37–48.CrossRefGoogle ScholarPubMed
Rodríguez-Rodríguez, P, de Pablo, ALL, García-Prieto, CF, et al.Long term effects of fetal undernutrition on rat heart. Role of hypertension and oxidative stress. PLoS One. 2017; 12, e0171544.CrossRefGoogle ScholarPubMed
Entringer, S, Buss, C, Wadhwa, PD.Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings. Curr Opin Endocrinol Diabetes Obes. 2010; 17, 507.CrossRefGoogle ScholarPubMed
Ma, J, Prince, AL, Bader, D, et al.High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun. 2014; 5, 3889.CrossRefGoogle Scholar
Zambrano, E, Nathanielsz, PW.Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutr Rev. 2013; 71, S42–S54.CrossRefGoogle ScholarPubMed
Ginzberg, MB, Kafri, R, Kirschner, M.On being the right (cell) size. Science. 2015; 348, 1245075.CrossRefGoogle ScholarPubMed
Cano, PG, Santacruz, A, Trejo, FM, et al.Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet-fed mice. Obesity. 2013; 21, 2310–2321.CrossRefGoogle ScholarPubMed
Lim, S-M, Jeong, J-J, Woo, KH, et al.Lactobacillus sakei OK67 ameliorates high-fat diet–induced blood glucose intolerance and obesity in mice by inhibiting gut microbiota lipopolysaccharide production and inducing colon tight junction protein expression. Nutr Res. 2016; 36, 337–348.CrossRefGoogle ScholarPubMed
Kobyliak, N, Conte, C, Cammarota, G, et al.Probiotics in prevention and treatment of obesity: a critical view. Nutr Metabol. 2016; 13, 14.CrossRefGoogle ScholarPubMed
Hill, C, Guarner, F, Reid, G, et al.The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014; 11, 506–514.CrossRefGoogle ScholarPubMed
Argyri, AA, Zoumpopoulou, G, Karatzas, K-AG, et al.Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol. 2013; 33, 282–291.CrossRefGoogle ScholarPubMed
Melgar-Lalanne, G, Rivera-Espinoza, Y, Méndez, AIR, et al.In vitro evaluation of the probiotic potential of halotolerant lactobacilli isolated from a ripened tropical Mexican cheese. Probiotics Antimicrob Proteins. 2013; 5, 239–251.CrossRefGoogle ScholarPubMed
de Paula, AT, Jeronymo-Ceneviva, AB, Silva, LF, et al.Leuconostoc mesenteroides SJRP55: a potential probiotic strain isolated from Brazilian water buffalo mozzarella cheese. Ann Microbiol. 2015; 65, 899–910.CrossRefGoogle Scholar
Castro-Rodríguez, D, Hernández-Sánchez, H, Yáñez Fernández, J.Probiotic properties of Leuconostoc mesenteroides isolated from aguamiel of Agave salmiana. Probiotics Antimicrob Proteins. 2015; 7, 107–117.Google Scholar
Castro-Rodríguez, DC, Reyes-Castro, LA, Vega, CC, et al.Leuconostoc mesenteroides subsp. Mesenteroides SD23 prevents metabolic dysfunction associated with high-fat diet–induced obesity in male mice. Probiotics Antimicrob Proteins. 2019. doi: 10.1007/s12602-019-09556-3Google Scholar
Shokryazdan, P, Jahromi, MF, Liang, JB, et al.Safety assessment of two new Lactobacillus strains as probiotic for human using a rat model. PLoS One. 2016; 11.CrossRefGoogle ScholarPubMed
Rodríguez-González, GL, Reyes-Castro, LA, Bautista, CJ, et al.Maternal obesity accelerates rat offspring metabolic aging in a sex dependent manner. J Physiol. 2019; 597, 5549–5563.CrossRefGoogle Scholar
Zambrano, E, Bautista, C, Deas, M, et al.A low maternal protein diet during pregnancy and lactation has sex-and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571, 221–230.CrossRefGoogle ScholarPubMed
Vega, CC, Reyes-Castro, LA, Bautista, CJ, et al.Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes. 2015; 39, 712.CrossRefGoogle ScholarPubMed
Mah, AT, Van Landeghem, L, Gavin, HE, et al.Impact of diet-induced obesity on intestinal stem cells: hyperproliferation but impaired intrinsic function that requires insulin/IGF1. Endocrinology. 2014; 155, 3302–3314.CrossRefGoogle ScholarPubMed
Scott, DW.Sturges’ rule. Wiley Interdiscip Rev Comput Stat. 2009; 1, 303–306.CrossRefGoogle Scholar
Ibáñez, CA, Vázquez-Martínez, M, León-Contreras, JC, et al.Different statistical approaches to characterization of adipocyte size in offspring of obese rats: effects of maternal or offspring exercise intervention. Front Physiol. 2018; 9.Google ScholarPubMed
Rautava, S, Luoto, R, Salminen, S, et al.Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol. 2012; 9, 565.CrossRefGoogle ScholarPubMed
Angelakis, E, Armougom, F, Million, M, et al.The relationship between gut microbiota and weight gain in humans. Future Microbiol. 2012; 7, 91–109.CrossRefGoogle ScholarPubMed
Andersson, U, Bränning, C, Ahrné, S, et al.Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes. 2010; 1, 189–196.CrossRefGoogle ScholarPubMed
Boden, G, She, P, Mozzoli, M, et al.Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-κB pathway in rat liver. Diabetes. 2005; 54, 3458–3465.CrossRefGoogle ScholarPubMed
Ma, X, Hua, J, Li, Z.Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepat. 2008; 49, 821–830.CrossRefGoogle ScholarPubMed
Ipsen, DH, Lykkesfeldt, J, Tveden-Nyborg, P.Molecular mechanisms of hepatic lipid accumulation in non-alcoholic fatty liver disease. Cell Mol Life Sci. 2018; 75, 3313–3327.CrossRefGoogle ScholarPubMed
Dailey, MJ.Nutrient-induced intestinal adaption and its effect in obesity. Physiol Behav. 2014; 136, 74–78.CrossRefGoogle ScholarPubMed
Lam, YY, Ha, CW, Campbell, CR, et al.Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS One. 2012; 7, e34233.CrossRefGoogle ScholarPubMed
de La Serre, CB, Ellis, CL, Lee, J, et al.Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010; 299, G440–G448.CrossRefGoogle ScholarPubMed
Covasa, M.Deficits in gastrointestinal responses controlling food intake and body weight. Am J Physiol Gastrointest Liver Physiol. 2010; 299, R1423–R1439.Google ScholarPubMed
Mao, J, Hu, X, Xiao, Y, et al.Overnutrition stimulates intestinal epithelium proliferation through β-catenin signaling in obese mice. Diabetes. 2013; 62, 3736–3746.CrossRefGoogle ScholarPubMed
Baldassano, S, Amato, A, Cappello, F, et al.Glucagon-like peptide-2 and mouse intestinal adaptation to a high-fat diet. J Endocrinol. 2013; 217, 11–20.CrossRefGoogle ScholarPubMed
Esposito, E, Iacono, A, Bianco, G, et al.Probiotics reduce the inflammatory response induced by a high-fat diet in the liver of young rats. J Nutr. 2009; 139, 905–911.CrossRefGoogle ScholarPubMed
Wagner, M, Samdal Steinskog, ES, Wiig, H.Adipose tissue macrophages: the inflammatory link between obesity and cancer? Exp Opin Ther Targets. 2015; 19, 527–538.CrossRefGoogle ScholarPubMed
Garaulet, M, Hernandez-Morante, J, Lujan, J, et al.Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans. Int J Obes. 2006; 30, 899.CrossRefGoogle ScholarPubMed
Bjørndal, B, Burri, L, Staalesen, V, et al.Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes. 2011; 2011.Google ScholarPubMed
Fang, L, Guo, F, Zhou, L, et al.The cell size and distribution of adipocytes from subcutaneous and visceral fat is associated with type 2 diabetes mellitus in humans. Adipocyte. 2015; 4, 273–279.CrossRefGoogle ScholarPubMed
Faust, IM, Johnson, PR, Stern, JS, et al.Diet-induced adipocyte number increase in adult rats: a new model of obesity. Am J Physiol Endocrinol Metab. 1978; 235, E279.CrossRefGoogle ScholarPubMed
MacDougald, OA, Mandrup, S.Adipogenesis: forces that tip the scales. Trends Endocrinol Metab. 2002; 13, 5–11.CrossRefGoogle ScholarPubMed