Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-07-01T12:48:23.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of prenatal stress on metabolic abnormalities induced by postnatal intake of a high-fat diet in BALB/c mice

Published online by Cambridge University Press:  29 October 2020

Yamila Raquel Juárez ,
Sofía Quiroga ,
Andrés Prochnik ,
Miriam Wald ,
Mariana Lorena Tellechea ,
Ana María Genaro  and
Adriana Laura Burgueño Open the ORCID record for Adriana Laura Burgueño [Opens in a new window]
Yamila Raquel Juárez
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina
Sofía Quiroga
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina
Andrés Prochnik
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina
Miriam Wald
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina
Mariana Lorena Tellechea
Affiliation:
Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE), CONICET – FEI – División de Endocrinología, Hospital de Niños R. Gutiérrez, Gallo 1330, C1425EFDBuenos Aires, Argentina
Ana María Genaro
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina Departamento de Farmacología, Facultad de Medicina, Universidad de Buenos Aires. Paraguay 2151 Piso 15, Buenos AiresC1121ABG, Argentina
Adriana Laura Burgueño*
Affiliation:
Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Alicia Moreau de Justo 1600, Buenos AiresC1107AFF, Argentina
*
Address for correspondence: Burgueño Adriana Laura, Instituto de Investigaciones Biomédicas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Pontificia Universidad Católica Argentina, Av. Alicia Moreau de Justo 1600, Piso 3, Buenos AiresC1107AFF, Argentina. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Prenatal insults during fetal development result in increased likelihood of developing chronic disease. Obesity, the biggest risk factor for the development of metabolic disease, is affected by several genetic and environmental factors. High-fat diet (HFD) consumption is usually linked with the development of obesity. The main goal of this study was to analyze the impact of the exposure to a HFD in prenatally stressed animals. For this purpose, we subjected pregnant BALB/c mice to restraint stress for 2 h a day between gestational day (GD) 14 and GD 21. Prenatally stressed and control offspring of both sexes were postnatally exposed to a HFD for 24 weeks. We found that prenatal stress (PS) per se produced disturbances in males such as increased total blood cholesterol and triglycerides, with a decrease in mRNA expression of sirtuin-1. When these animals were fed a HFD, we observed a rise in glucose and insulin levels and an increase in visceral adipose tissue gene expression of leptin, resistin, and interleukin-1 beta. Although females proved to be more resilient to PS consequences, when they were fed a HFD, they showed significant metabolic impairment. In addition to the changes observed in males, females also presented an increase in body weight and adiposity and a rise in cholesterol levels.

Keywords

Prenatal stressobesitymetabolismgene expression
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 5 , October 2021 , pp. 721 - 730
Check for updates
Copyright
© The Author(s), 2020. 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.)

Footnotes

*

These authors contributed equally to this work.

References

Stevens, GA, Singh, GM, Lu, Y, et al. National, regional, and global trends in adult overweight and obesity prevalences. Popul Health Metr. 2012; 10, 22.CrossRefGoogle ScholarPubMed
Romieu, I, Dossus, L, Barquera, S, et al. Energy balance and obesity: what are the main drivers? Cancer Causes Control. 2017; 28, 247–258.CrossRefGoogle ScholarPubMed
Deng, Y, Scherer, PE. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N Y Acad Sci. 2010; 1212, E1–E19.CrossRefGoogle ScholarPubMed
Wajchenberg, BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev. 2000; 21, 697–738.CrossRefGoogle ScholarPubMed
Hajer, GR, van Haeften, TW, Visseren, FLJ. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J. 2008; 29, 2959–2971.CrossRefGoogle ScholarPubMed
Fontana, L, Eagon, JC, Trujillo, ME, Scherer, PE, Klein, S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007; 56, 1010–1013.CrossRefGoogle ScholarPubMed
Jensen, MD. Role of body fat distribution and the metabolic complications of obesity. J Clin Endocrinol Metab. 2008; 93, S57–63.CrossRefGoogle ScholarPubMed
Friend, DM, Devarakonda, K, O’Neal, TJ, et al. Basal ganglia dysfunction contributes to physical inactivity in obesity. Cell Metab. 2017; 25, 312–321.CrossRefGoogle ScholarPubMed
Spaeth, AM, Dinges, DF, Goel, N. Effects of experimental sleep restriction on weight gain, caloric intake, and meal timing in healthy adults. Sleep. 2013; 36, 981–990.CrossRefGoogle ScholarPubMed
Wang, Y, Carreras, A, Lee, S, et al. Chronic sleep fragmentation promotes obesity in young adult mice. Obesity (Silver Spring). 2014; 22, 758–762.CrossRefGoogle ScholarPubMed
Fonken, LK, Workman, JL, Walton, JC, et al. Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci USA. 2010; 107, 18664–18669.CrossRefGoogle ScholarPubMed
Albreiki, MS, Middleton, B, Hampton, SM. A single night light exposure acutely alters hormonal and metabolic responses in healthy participants. Endocr Connect. 2017; 6, 100–110.CrossRefGoogle ScholarPubMed
Bandín, C, Scheer, FAJL, Luque, AJ, et al. Meal timing affects glucose tolerance, substrate oxidation and circadian-related variables: a randomized, crossover trial. Int J Obes. 2015; 39, 828–833.CrossRefGoogle ScholarPubMed
Delezie, J, Challet, E. Interactions between metabolism and circadian clocks: reciprocal disturbances. Ann N Y Acad Sci. 2011; 1243, 30–46.CrossRefGoogle ScholarPubMed
Golay, A, Bobbioni, E. The role of dietary fat in obesity. Int J Obes Relat Metab Disord. 1997; 21 Suppl 3, S2–11.Google Scholar
Waterland, RA, Michels, KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007; 27, 363–388.CrossRefGoogle ScholarPubMed
Harris, A, Seckl, J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011; 59, 279–289.CrossRefGoogle ScholarPubMed
Maccari, S, Polese, D, Reynaert, M-L, Amici, T, Morley-Fletcher, S, Fagioli, F. Early-life experiences and the development of adult diseases with a focus on mental illness: the Human Birth Theory. Neuroscience. 2017; 342, 232–251.CrossRefGoogle ScholarPubMed
Seckl, JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001; 185, 61–71.CrossRefGoogle ScholarPubMed
Sandman, CA, Wadhwa, PD, Dunkel-Schetter, C, et al. Psychobiological influences of stress and HPA regulation on the human fetus and infant birth outcomes. Ann N Y Acad Sci. 1994; 739, 198–210.CrossRefGoogle ScholarPubMed
Nieuwenhuizen, AG, Rutters, F. The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol Behav. 2008; 94, 169–177.CrossRefGoogle ScholarPubMed
Burgueño, AL, Juarez, YR, Genaro, AM, Tellechea, ML. Systematic review and meta-analysis on the relationship between prenatal stress and metabolic syndrome intermediate phenotypes. Int J Obes. 2020; 44, 1–12.CrossRefGoogle ScholarPubMed
Boersma, GJ, Tamashiro, KL. Individual differences in the effects of prenatal stress exposure in rodents. Neurobiol Stress. 2015; 1, 100–108.CrossRefGoogle ScholarPubMed
Burgueño, AL, Juárez, YR, Genaro, AM, Tellechea, ML. Prenatal stress and later metabolic consequences: systematic review and meta-analysis in rodents. Psychoneuroendocrinology. 2019; 113, 104560.CrossRefGoogle ScholarPubMed
Frankenhaeuser, M, Dunne, E, Lundberg, U. Sex differences in sympathetic-adrenal medullary reactions induced by different stressors. Psychopharmacology. 1976; 47, 1–5.CrossRefGoogle ScholarPubMed
Taylor, SE, Klein, LC, Lewis, BP, Gruenewald, TL, Gurung, RA, Updegraff, JA. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev. 2000; 107, 411–429.CrossRefGoogle Scholar
Williams, DR, Carlsson, R, Bürkner, P-C. Between-litter variation in developmental studies of hormones and behavior: inflated false positives and diminished power. Front Neuroendocrinol. 2017; 47, 154–166.CrossRefGoogle ScholarPubMed
Bowman, RE, MacLusky, NJ, Sarmiento, Y, Frankfurt, M, Gordon, M, Luine, VN. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology. 2004; 145, 3778–3787.CrossRefGoogle ScholarPubMed
Pascuan, CG, Di Rosso, ME, Pivoz-Avedikian, JE, Wald, MR, Zorrilla Zubilete, MA, Genaro, AM. Alteration of neurotrophin and cytokine expression in lymphocytes as novel peripheral markers of spatial memory deficits induced by prenatal stress. Physiol Behav. 2017; 173, 144–155.CrossRefGoogle ScholarPubMed
Ward, IL, Weisz, J. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology. 1984; 114, 1635–1644.CrossRefGoogle ScholarPubMed
Igosheva, N, Klimova, O, Anishchenko, T, Glover, V. Prenatal stress alters cardiovascular responses in adult rats. J Physiol (Lond). 2004; 557, 273–285.CrossRefGoogle ScholarPubMed
Sternberg, WF, Ridgway, CG. Effects of gestational stress and neonatal handling on pain, analgesia, and stress behavior of adult mice. Physiol Behav. 2003; 78, 375–383.CrossRefGoogle ScholarPubMed
Szuran, TF, Pliska, V, Pokorny, J, Welzl, H. Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav. 2000; 71, 353–362.CrossRefGoogle ScholarPubMed
Nishikawa, S, Yasoshima, A, Doi, K, Nakayama, H, Uetsuka, K. Involvement of sex, strain and age factors in high fat diet-induced obesity in C57BL/6J and BALB/cA mice. Exp Anim. 2007; 56, 263–272.CrossRefGoogle ScholarPubMed
McGuinness, OP, Ayala, JE, Laughlin, MR, Wasserman, DH. NIH experiment in centralized mouse phenotyping: the Vanderbilt experience and recommendations for evaluating glucose homeostasis in the mouse. Am J Physiol Endocrinol Metab. 2009; 297, E849–E855.CrossRefGoogle ScholarPubMed
Liu, M, Liu, F. Transcriptional and post-translational regulation of adiponectin. Biochem J. 2009; 425, 41–52.CrossRefGoogle ScholarPubMed
Yoshizaki, T, Milne, JC, Imamura, T, et al. SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol Cell Biol. 2009; 29, 1363–1374.CrossRefGoogle ScholarPubMed
Yoshizaki, T, Schenk, S, Imamura, T, et al. SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am J Physiol Endocrinol Metab. 2010; 298, E419–E428.CrossRefGoogle ScholarPubMed
Tack, CJ, Stienstra, R, Joosten, LAB, Netea, MG. Inflammation links excess fat to insulin resistance: the role of the interleukin-1 family. Immunol Rev. 2012; 249, 239–252.CrossRefGoogle ScholarPubMed
Wen, H, Gris, D, Lei, Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011; 12, 408–415.CrossRefGoogle ScholarPubMed
Entringer, S, Buss, C, Swanson, JM, et al. Fetal programming of body composition, obesity, and metabolic function: the role of intrauterine stress and stress biology. J Nutr Metab. 2012; 2012, 632548.CrossRefGoogle ScholarPubMed
Reynolds, RM. Corticosteroid-mediated programming and the pathogenesis of obesity and diabetes. J Steroid Biochem Mol Biol. 2010; 122, 3–9.CrossRefGoogle ScholarPubMed
Yu, H-R, Tain, Y-L, Tiao, M-M, et al. Prenatal dexamethasone and postnatal high-fat diet have a synergistic effect of elevating blood pressure through a distinct programming mechanism of systemic and adipose renin-angiotensin systems. Lipids Health Dis. 2018; 17, 50.CrossRefGoogle ScholarPubMed
Drago, F, Di Leo, F, Giardina, L. Prenatal stress induces body weight deficit and behavioural alterations in rats: the effect of diazepam. Eur Neuropsychopharmacol. 1999; 9, 239–245.CrossRefGoogle ScholarPubMed
Lesage, J, Del-Favero, F, Leonhardt, M, et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol. 2004; 181, 291–296.CrossRefGoogle ScholarPubMed
Kelishadi, R, Haghdoost, AA, Jamshidi, F, Aliramezany, M, Moosazadeh, M. Low birthweight or rapid catch-up growth: which is more associated with cardiovascular disease and its risk factors in later life? A systematic review and cryptanalysis. Paediatr Int Child Health. 2015; 35, 110–123.CrossRefGoogle ScholarPubMed
Dulloo, AG, Jacquet, J, Seydoux, J, Montani, JP. The thrifty “catch-up fat” phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes. 2006; 30 Suppl 4, S23–S35.CrossRefGoogle Scholar
Berends, LM, Fernandez-Twinn, DS, Martin-Gronert, MS, Cripps, RL, Ozanne, SE. Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. Int J Obes. 2013; 37, 1051–1057.CrossRefGoogle ScholarPubMed
Salsberry, PJ, Reagan, PB. Dynamics of early childhood overweight. Pediatrics. 2005; 116, 1329–1338.CrossRefGoogle ScholarPubMed
Maccari, S, Darnaudery, M, Morley-Fletcher, S, Zuena, AR, Cinque, C, Van Reeth, O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev. 2003; 27, 119–127.CrossRefGoogle ScholarPubMed
Tamashiro, KLK, Terrillion, CE, Hyun, J, Koenig, JI, Moran, TH. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes. 2009; 58, 1116–1125.CrossRefGoogle ScholarPubMed
Tsai, C-C, Tiao, M-M, Sheen, J-M, et al. Obesity programmed by prenatal dexamethasone and postnatal high-fat diet leads to distinct alterations in nutrition sensory signals and circadian-clock genes in visceral adipose tissue. Lipids Health Dis. 2019; 18, 19.CrossRefGoogle ScholarPubMed
Baran, SE, Campbell, AM, Kleen, JK, et al. Combination of high fat diet and chronic stress retracts hippocampal dendrites. Neuroreport. 2005; 16, 39–43.CrossRefGoogle ScholarPubMed
Burkuš, J, Kačmarová, M, Kubandová, J, et al. Stress exposure during the preimplantation period affects blastocyst lineages and offspring development. J Reprod Dev. 2015; 61, 325–331.CrossRefGoogle ScholarPubMed
Bruder-Nascimento, T, Campos, DHS, Alves, C, Thomaz, S, Cicogna, AC, Cordellini, S. Effects of chronic stress and high-fat diet on metabolic and nutritional parameters in Wistar rats. Arq Bras Endocrinol Metabol. 2013; 57, 642–649.CrossRefGoogle ScholarPubMed
Panetta, P, Berry, A, Bellisario, V, et al. Long-term sex-dependent vulnerability to metabolic challenges in prenatally stressed rats. Front Behav Neurosci. 2017; 11, 113.CrossRefGoogle ScholarPubMed
Boersma, GJ, Moghadam, AA, Cordner, ZA, Tamashiro, KL. Prenatal stress and stress coping style interact to predict metabolic risk in male rats. Endocrinology. 2014; 155, 1302–1312.CrossRefGoogle ScholarPubMed
Abildgaard, A, Lund, S, Hougaard, KS. Chronic high-fat diet increases acute neuroendocrine stress response independently of prenatal dexamethasone treatment in male rats. Acta Neuropsychiatr. 2014; 26, 8–18.CrossRefGoogle ScholarPubMed
Sheen, J-M, Hsieh, C-S, Tain, Y-L, et al. Programming effects of prenatal glucocorticoid exposure with a postnatal high-fat diet in diabetes mellitus. Int J Mol Sci. 2016; 17, 533.CrossRefGoogle ScholarPubMed
Balasubramanian, P, Varde, PA, Abdallah, SL, Najjar, SM, Mohan Kumar, PS, Mohan Kumar, SMJ. Differential effects of prenatal stress on metabolic programming in diet-induced obese and dietary-resistant rats. Am J Physiol Endocrinol Metab. 2015; 309, E582–E588.CrossRefGoogle ScholarPubMed
Paternain, L, de la Garza, AL, Batlle, MA, Milagro, FI, Martínez, JA, Campión, J. Prenatal stress increases the obesogenic effects of a high-fat-sucrose diet in adult rats in a sex-specific manner. Stress. 2013; 16, 220–232.CrossRefGoogle Scholar
Sakoda, H, Ogihara, T, Anai, M, et al. Dexamethasone-induced insulin resistance in 3T3-L1 adipocytes is due to inhibition of glucose transport rather than insulin signal transduction. Diabetes. 2000; 49, 1700–1708.CrossRefGoogle ScholarPubMed
Haffner, SM, Valdez, RA, Hazuda, HP, Mitchell, BD, Morales, PA, Stern, MP. Prospective analysis of the insulin-resistance syndrome (syndrome X). Diabetes. 1992; 41, 715–722.CrossRefGoogle Scholar
Wyrwoll, CS, Mark, PJ, Mori, TA, Waddell, BJ. Developmental programming of adult hyperinsulinemia, increased proinflammatory cytokine production, and altered skeletal muscle expression of SLC2A4 (GLUT4) and uncoupling protein 3. J Endocrinol. 2008; 198, 571–579.CrossRefGoogle ScholarPubMed
D’mello, AP, Liu, Y. Effects of maternal immobilization stress on birth weight and glucose homeostasis in the offspring. Psychoneuroendocrinology. 2006; 31, 395–406.CrossRefGoogle ScholarPubMed
Othman, H, Ammari, M, Sakly, M, Abdelmelek, H. Effects of prenatal exposure to WIFI signal (2.45GHz) on postnatal development and behavior in rat: influence of maternal restraint. Behav Brain Res. 2017; 326, 291–302.CrossRefGoogle ScholarPubMed
Luft, C, Levices, IP, Pedrazza, L, de Oliveira, JR, Donadio, MVF. Sex-dependent metabolic effects of pregestational exercise on prenatally stressed mice. J Dev Orig Health Dis. 2020 May 14, 1–9.Google ScholarPubMed
Owecki, M, Miczke, A, Nikisch, E, Pupek-Musialik, D, Sowiński, J. Serum resistin concentrations are higher in human obesity but independent from insulin resistance. Exp Clin Endocrinol Diabetes. 2011; 119, 117–121.CrossRefGoogle ScholarPubMed
Könner, AC, Brüning, JC. Selective insulin and leptin resistance in metabolic disorders. Cell Metab. 2012; 16, 144–152.CrossRefGoogle ScholarPubMed
Barnes, KM, Miner, JL. Role of resistin in insulin sensitivity in rodents and humans. Curr Protein Pept Sci. 2009; 10, 96–107.CrossRefGoogle ScholarPubMed
Khalyfa, A, Carreras, A, Almendros, I, Hakim, F, Gozal, D. Sex dimorphism in late gestational sleep fragmentation and metabolic dysfunction in offspring mice. Sleep. 2015; 38(4), 545–557.CrossRefGoogle ScholarPubMed
Schug, TT, Li, X. Sirtuin 1 in lipid metabolism and obesity. Ann Med. 2011; 43, 198–211.CrossRefGoogle ScholarPubMed
Llorente, E, Brito, ML, Machado, P, González, MC. Effect of prenatal stress on the hormonal response to acute and chronic stress and on immune parameters in the offspring. J Physiol Biochem. 2002; 58, 143–149.CrossRefGoogle ScholarPubMed
Chalkiadaki, A, Guarente, L. High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab. 2012; 16, 180–188.CrossRefGoogle ScholarPubMed
Schuster, DP. Obesity and the development of type 2 diabetes: the effects of fatty tissue inflammation. Diabetes Metab Syndr Obes. 2010; 3, 253–262.CrossRefGoogle ScholarPubMed
Ellulu, MS, Patimah, I, Khaza’ai, H, Rahmat, A, Abed, Y. Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci. 2017; 13, 851–863.CrossRefGoogle ScholarPubMed
Emanuela, F, Grazia, M, Marco, DR, Maria Paola, L, Giorgio, F, Marco, B. Inflammation as a link between obesity and metabolic syndrome. J Nutr Metab. 2012; 2012, 476380.CrossRefGoogle ScholarPubMed
Mark, PJ, Wyrwoll, CS, Zulkafli, IS, Mori, TA, Waddell, BJ. Rescue of glucocorticoid-programmed adipocyte inflammation by omega-3 fatty acid supplementation in the rat. Reprod Biol Endocrinol. 2014; 12, 39.CrossRefGoogle ScholarPubMed
Ward, GR, Wainwright, PE. Reductions in maternal food and water intake account for prenatal stress effects on neurobehavioral development in B6D2F2 mice. Physiol Behav. 1988; 44, 781–786.CrossRefGoogle ScholarPubMed
Montgomery, MK, Fiveash, CE, Braude, JP, et al. Disparate metabolic response to fructose feeding between different mouse strains. Sci Rep. 2015; 5, 18474.CrossRefGoogle ScholarPubMed
Montgomery, MK, Hallahan, NL, Brown, SH, et al. Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia. 2013; 56, 1129–1139.CrossRefGoogle ScholarPubMed
Savignac, HM, Dinan, TG, Cryan, JF. Resistance to early-life stress in mice: effects of genetic background and stress duration. Front Behav Neurosci. 2011; 5, 13.CrossRefGoogle ScholarPubMed
Razzoli, M, Carboni, L, Andreoli, M, Ballottari, A, Arban, R. Different susceptibility to social defeat stress of BalbC and C57BL6/J mice. Behav Brain Res. 2011; 216, 100–108.CrossRefGoogle ScholarPubMed
Supplementary material: File

Juárez et al. supplementary material

Tables S1-S2 and Figures S1-S2

Download Juárez et al. supplementary material(File)
File 294 KB