Combined effects of early life stress and prolonged exposure to western diet on emotional responses and gut microbiota

  1. Isabel López Taboada
  2. Silvia Arboleya Montes
  3. Saúl Sal Sarriá
  4. Miguel Gueimonde
  5. Héctor González Pardo
  6. Nélida María Conejo Jiménez
Revista:
Psicothema

ISSN: 0214-9915 1886-144X

Año de publicación: 2024

Volumen: 36

Número: 2

Páginas: 133-144

Tipo: Artículo

DOI: 10.7334/PSICOTHEMA2023.287 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Psicothema

Resumen

Background: Exposure to early life stress (ELS) and maternal consumption of a high-fat and high-sugar diet can have detrimental effects on adult emotional responses. The microbiota and gut-brain axis have been proposed as playing a mediating role in the regulation of stress and emotion. Method: Young male rats were exposed to maternal separation (MS) together with maternal and postnatal consumption of a HFS diet (45%kcal saturated fat, 17%kcal sucrose). Anxiety-like behaviour was evaluated using an elevated zero-maze, and depression-like behaviour using the forced-swim and sucrose preference tests. Microbiota composition and derived metabolites were also analysed in faecal samples using a gas chromatograph and mass spectrometry. Results: Combined exposure to MS and lifelong consumption of a HFS diet partially reversed the abnormal anxiety-like and depression-like behaviours in early adulthood caused by each adverse factor alone. Diet composition had a greater negative impact than ELS exposure on the gut microbiota, and both environmental factors interacted with microbiota composition partially counteracting their negative effects. Conclusions: The effects of exposure to early life stress and a HFS diet independently are partially reversed after the combination of both factors. These results suggest that ELS and diet interact to modulate adult stress response and gut microbiota.

Referencias bibliográficas

  • Abenavoli, L., Scarpellini, E., Colica, C., Boccuto, L., Salehi, B., Sharifi-Rad, J., Aiello, V., Romano, B., De Lorenzo, A., Izzo, A. A., & Capasso, R. (2019). Gut microbiota and obesity: A role for probiotics. Nutrients, 11(11), Article 2690. https://doi.org/10.3390/nu11112690
  • Adan, R.A.H., van der Beek, E.M., Buitelaar, J.K., Cryan, J.F., Hebebrand, J., Higgs, S., Schellekens, H., & Dickson, S.L., (2019). Nutritional psychiatry: Towards improving mental health by what you eat. European Neuropsychopharmacology, 29(12), 1321–1332. https://doi.org/10.1016/j.euroneuro.2019.10.011
  • Agorastos, A., Pervanidou, P., Chrousos, G.P., & Baker, D.G. (2019). Developmental trajectories of early life stress and trauma: A narrative review on neurobiological aspects beyond stress system dysregulation. Frontiers in Psychiatry, 10, Article 118. https://doi.org/10.3389/fpsyt.2019.00118
  • Anyan, J., & Amir, S. (2018). Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology, 43, 931–933. https://doi.org/10.1038/NPP.2017.260
  • Armario, A. (2021). The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neuroscience and Biobehavioral Reviews, 128, 74–86. https://doi.org/10.1016/j.neubiorev.2021.06.014
  • Aslani, S., Vieira, N., Marques, F., Costa, P.S., Sousa, N., & Palha, J.A. (2015). The effect of high-fat diet on rat’s mood, feeding behavior and response to stress. Translational Psychiatry, 5(11), Article e684. https://doi.org/10.1038/tp.2015.178
  • Bokulich, N.A., Subramanian, S., Faith, J.J., Gevers, D., Gordon, J.I., Knight, R., Mills, D.A., & Caporaso, J.G. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10, 57–59. https://doi.org/10.1038/nmeth.2276
  • Cao, B., Wang, J., Zhang, X., Yang, X., Poon, D.C.-H., Jelfs, B., Chan, R.H.M., Wu, J.C.-Y., & Li, Y., (2016). Impairment of decision making and disruption of synchrony between basolateral amygdala and anterior cingulate cortex in the maternally separated rat. Neurobiol. Learning & Memory, 136, 74–85. https://doi.org/10.1016/j.nlm.2016.09.015
  • Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pẽa, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., & Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336. https://doi.org/10.1038/nmeth.f.303
  • Chen, L.P., Murad, M.H., Paras, M.L., Colbenson, K.M., Sattler, A.L., Goranson, E.N., Elamin, M.B., Seime, R.J., Shinozaki, G., Prokop, L.J., & Zirakzadeh, A. (2010). Sexual abuse and lifetime diagnosis of psychiatric disorders: Systematic review and meta-analysis. Mayo Clinic Proceedings, 85, 618–629. https://doi.org/10.4065/mcp.2009.0583
  • Commons, K.G., Cholanians, A.B., Babb, J.A., & Ehlinger, D.G. (2017). The rodent forced swim test measures stress-coping strategy, not depressionlike behavior. ACS Chemical Neuroscience, 8(5), 955–960. https://doi.org/10.1021/acschemneuro.7b00042
  • Cryan, J.F., O’riordan, K.J., Cowan, C.S.M., Sandhu, K. V., Bastiaanssen, T.F.S., Boehme, M., Codagnone, M.G., Cussotto, S., Fulling, C., Golubeva, A. V., Guzzetta, K.E., Jaggar, M., Long-Smith, C.M., Lyte, J.M., Martin, J.A., Molinero-Perez, A., Moloney, G., Morelli, E., Morillas, E., O’connor, R., Cruz-Pereira, J.S., Peterson, V.L., Rea, K., Ritz, N.L., Sherwin, E., Spichak, S., Teichman, E.M., van de Wouw, M., Ventura-Silva, A.P., Wallace-Fitzsimons, S.E., Hyland, N., Clarke, G., & Dinan, T.G. (2019). The microbiota-gut-brain axis. Physiological Reviews, 99(4), 1877–2013. https://doi.org/10.1152/physrev.00018.2018
  • Daniels, W.M.U., Pietersen, C.Y., Carstens, M.E., & Stein, D.J. (2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolical Brain Disease, 19(1-2), 3–14. https://doi.org/10.1023/b:mebr.0000027412.19664.b3
  • de la Cuesta-Zuluaga, J., Mueller, N.T., Álvarez-Quintero, R., VelásquezMejía, E.P., Sierra, J.A., Corrales-Agudelo, V., Carmona, J.A., Abad, J.M., & Escobar, J.S. (2019). Higher fecal short-chain fatty acid levels are associated with gut microbiome dysbiosis, obesity, hypertension and cardiometabolic disease risk factors. Nutrients, 11(1), 51. https://doi.org/10.3390/nu11010051
  • Edgar, R.C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998. https://doi.org/10.1038/nmeth.2604
  • Enqi, W., Jingzhu, S., Lingpeng, P., & Yaqin, L. (2021). Comparison of the gut microbiota disturbance in rat models of irritable bowel syndrome induced by maternal separation and multiple early-life adversity. Frontiers in Cellular and Infection Microbiology, 10, Article 581974. https://doi.org/10.3389/fcimb.2020.581974
  • Fernandes, D.J., Spring, S., Roy, A.R., Qiu, L.R., Yee, Y., Nieman, B.J., Lerch, J.P., & Palmert, M.R. (2021). Exposure to maternal high-fat diet induces extensive changes in the brain of adult offspring. Translational Psychiatry, 11(1), Article 149. https://doi.org/10.1038/s41398-021-01274-1
  • Francis, H., & Stevenson, R. (2013). The longer-term impacts of Western diet on human cognition and the brain. Appetite, 63, 119-128. https://doi.org/10.1016/j.appet.2012.12.018
  • González-Pardo, H., Arias, J.L., Gómez-Lázaro, E., Taboada, I.L., & Conejo, N.M. (2020). Sex-specific effects of early life stress on brain mitochondrial function, monoamine levels and neuroinflammation. Brain Sciences, 10, 1–17. https://doi.org/10.3390/brainsci10070447
  • Haas, B.J., Gevers, D., Earl, A.M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S.K., Sodergren, E., Methé, B., DeSantis, T.Z., Petrosino, J.F., Knight, R., & Birren, B.W. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494–504. https://doi.org/10.1101/gr.112730.110
  • Johnson, S.A., Javurek, A.B., Painter, M.S., Murphy, C.R., Conard, C.M., Gant, K.L., Howald, E.C., Ellersieck, M.R., Wiedmeyer, C.E., VieiraPotter, V.J., & Rosenfeld, C.S. (2017). Effects of a maternal high-fat diet on offspring behavioral and metabolic parameters in a rodent model. Journal of Developmental Origins of Health and Disease, 8(1), 75–88. https://doi.org/10.1017/S2040174416000490
  • Karl, P.J., Hatch, A.M., Arcidiacono, S.M., Pearce, S.C., Pantoja-Feliciano, I.G., Doherty, L.A., & Soares, J.W. (2018). Effects of psychological, environmental and physical stressors on the gut microbiota. Frontiers in Microbiology, 9, Article 2013. https://doi.org/10.3389/fmicb.2018.02013
  • Lippmann, M., Bress, A., Nemeroff, C.B., Plotsky, P.M., & Monteggia, L.M. (2007). Long-term behavioural and molecular alterations associated with maternal separation in rats. European Journal of Neuroscience, 25, 30913098. https://doi.org/10.1111/j.1460-9568.2007.05522.x
  • Liu, R. T., Walsh, R. F. L., & Sheehan, A. E. (2019). Prebiotics and probiotics for depression and anxiety: A systematic review and meta-analysis of controlled clinical trials. Neuroscience and biobehavioral reviews, 102, 13–23. https://doi.org/10.1016/j.neubiorev.2019.03.023
  • López-Taboada, I., González-Pardo, H., & Conejo, N. M. (2020). Western diet: implications for brain function and behavior. Frontiers in Psychology, 11, Article 564413. https://doi.org/10.3389/fpsyg.2020.564413
  • Magoč, T., & Salzberg, S.L. (2011). FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27, 2957–2963. https://doi.org/10.1093/bioinformatics/btr507
  • Malesza, I.J., Malesza, M., Walkowiak, J., Mussin, N., Walkowiak, D., Aringazina, R., Bartkowiak-Wieczorek, J., & Mądry, E. (2021). Highfat, western-style diet, systemic inflammation, and gut microbiota: A narrative review. Cells, 10(11), Article 3164. https://doi.org/10.3390/cells10113164
  • Maniam, J., Antoniadis, C.P., Le, V., & Morris, M.J. (2016). A diet high in fat and sugar reverses anxiety-like behaviour induced by limited nesting in male rats: Impacts on hippocampal markers. Psychoneuroendocrinology, 68, 202–209. https://doi.org/10.1016/j.psyneuen.2016.03.007
  • Maniam, J., & Morris, M.J. (2010). Palatable cafeteria diet ameliorates anxiety and depression-like symptoms following an adverse early environment. Psychoneuroendocrinology, 35, 717–728. https://doi.org/10.1016/j.psyneuen.2009.10.013
  • Moris, G., Arboleya, S., Mancabelli, L., Milani, C., Ventura, M., de los ReyesGavilán, C.G., & Gueimonde, M. (2018). Fecal microbiota profile in a group of myasthenia gravis patients. Scientific Reports, 8(1), Article 14384. https://doi.org/10.1038/s41598-018-32700-y
  • Morris, M.J., Beilharz, J.E., Maniam, J., Reichelt, A.C., & Westbrook, R.F. (2015). Why is obesity such a problem in the 21st century? The intersection of palatable food, cues and reward pathways, stress, and cognition. Neuroscience and Biobehavioral Reviews, 58, 36–45. https://doi.org/10.1016/j.neubiorev.2014.12.002
  • Nemeroff, C.B. (2016). Paradise lost: The neurobiological and clinical consequences of child abuse and neglect. Neuron, 89, 892–909. https://doi.org/10.1016/j.neuron.2016.01.019
  • O’Mahony, S.M., McVey Neufeld, K.A., Waworuntu, R. V., Pusceddu, M.M., Manurung, S., Murphy, K., Strain, C., Laguna, M.C., Peterson, V.L., Stanton, C., Berg, B.M., Dinan, T.G., & Cryan, J.F. (2020). The enduring effects of early-life stress on the microbiota–gut–brain axis are buffered by dietary supplementation with milk fat globule membrane and a prebiotic blend. European Journal of Neuroscience, 51, 1042–1058. https://doi.org/10.1111/ejn.14514
  • Oriach, C.S., Robertson, R.C., Stanton, C., Cryan, J.F., & Dinan, T.G. (2016). Food for thought: The role of nutrition in the microbiota-gut-brain axis. Clinical Nutrition Experimental, 6, 25-35. https://doi.org/10.1016/j.yclnex.2016.01.003
  • Paulson, J.N., Colin Stine, O., Bravo, H.C., & Pop, M. (2013). Differential abundance analysis for microbial marker-gene surveys. Nature Methods, 10, 1200–1202. https://doi.org/10.1038/nmeth.2658
  • Pini, R.T.B., Ferreira do Vales, L.D.M., Braga Costa, T.M., & Almeida, S.S. (2017). Effects of cafeteria diet and high fat diet intake on anxiety, learning and memory in adult male rats. Nutritional Neuroscience, 20, 396–408. https://doi.org/10.1080/1028415x.2016.1149294
  • Porsolt, R.D., Bertin, A., & Jalfre, M. (1978). “Behavioural despair” in rats and mice: Strain differences and the effects of imipramine. European Journal of Pharmacology, 51, 291–294. https://doi.org/10.1016/00142999(78)90414-4
  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F.O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue), D590-D596. https://doi.org/10.1093/nar/gks1219
  • Rabasa, C., Winsa-Jörnulf, J., Vogel, H., Babaei, C.S., Askevik, K., & Dickson, S.L. (2016). Behavioral consequences of exposure to a high fat diet during the post-weaning period in rats. Hormones and Behavior, 85, 56–66. https://doi.org/10.1016/j.yhbeh.2016.07.008
  • Rincel, M., Aubert, P., Chevalier, J., Grohard, P.A., Basso, L., Monchaux de Oliveira, C., Helbling, J.C., Lévy, É., Chevalier, G., Leboyer, M., Eberl, G., Layé, S., Capuron, L., Vergnolle, N., Neunlist, M., Boudin, H., Lepage, P., & Darnaudéry, M. (2019). Multi-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner. Brain, Behavior, and Immunity, 80, 179–192. https://doi.org/10.1016/j.bbi.2019.03.006
  • Rincel, M., Lépinay, A.L., Delage, P., Fioramonti, J., Théodorou, V.S., Layé, S., & Darnaudéry, M. (2016). Maternal high-fat diet prevents developmental programming by early-life stress. Translational Psychiatry, 6(11), Article e966. https://doi.org/10.1038/tp.2016.235
  • Rincel, M., Lépinay, A.L., Janthakhin, Y., Soudain, G., Yvon, S., Da Silva, S., Joffre, C., Aubert, A., Séré, A., Layé, S., Theodorou, V., Ferreira, G., & Darnaudéry, M. (2018). Maternal high-fat diet and early life stress differentially modulate spine density and dendritic morphology in the medial prefrontal cortex of juvenile and adult rats. Brain Structure and Function, 223, 883–895. https://doi.org/10.1007/s00429-017-1526-8
  • Rincel, M., Olier, M., Minni, A., de Oliveira, C.M., Matime, Y., Gaultier, E., Grit, I., Helbling, J.C., Costa, A.M., Lépinay, A., Moisan, M.P., Layé, S., Ferrier, L., Parnet, P., Theodorou, V., & Darnaudéry, M. (2019). Pharmacological restoration of gut barrier function in stressed neonates partially reverses long-term alterations associated with maternal separation. Psychopharmacology (Berlin), 236, 1583–1596. https://doi.org/10.1007/s00213-019-05252-w
  • Romaní-Pérez, M., Lépinay, A.L., Alonso, L., Rincel, M., Xia, L., Fanet, H., Caillé, S., Cador, M., Layé, S., Vancassel, S., & Darnaudéry, M. (2017). Impact of perinatal exposure to high-fat diet and stress on responses to nutritional challenges, food-motivated behaviour and mesolimbic dopamine function. International Journal of Obesity, 41, 502–509. https://doi.org/10.1038/ijo.2016.236
  • Salazar, N., González, S., Nogacka, A.M., Rios-Covián, D., Arboleya, S., Gueimonde, M., & de los Reyes-Gavilán, C.G. (2019). Microbiome: Effects of ageing and diet. Current Issues in Molecular Biology, 36, 33–62. https://doi.org/10.21775/cimb.036.033
  • Sasaki, A., de Vega, W., Sivanathan, S., St-Cyr, S., & McGowan, P. (2014). Maternal high-fat diet alters anxiety behavior and glucocorticoid signaling in adolescent offspring. Neuroscience, 272, 92–101. https://doi.org/10.1016/j.neuroscience.2014.04.012
  • Sasaki, A., de Vega, W.C., St-Cyr, S., Pan, P., & McGowan, P.O. (2013). Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience, 240, 1–12. https://doi.org/10.1016/j.neuroscience.2013.02.044
  • Scheggi, S., De Montis, M.G., & Gambarana, C. (2018). Making sense of rodent models of anhedonia. The International Journal of Psychopharmacology, 21(11), 1049-1065 https://doi.org/10.1093/ijnp/pyy083
  • Shepherd, J.K., Grewal, S.S., Fletcher, A., Bill, D.J., & Dourish, C.T. (1994). Behavioural and pharmacological characterisation of the elevated “zeromaze” as an animal model of anxiety. Psychopharmacology (Berlin), 116, 56–64. https://doi.org/10.1007/BF02244871
  • Silva, Y.P., Bernardi, A., & Frozza, R.L. (2020). The role of short-chain fatty acids from gut microbiota in gut-brain communication. Frontiers in Endocrinology (Lausanne), 11, Article 25. https://doi.org/10.3389/fendo.2020.00025
  • Souto, T. dos S., Nakao, F.S.N., Giriko, C.Á., Dias, C.T., Cheberle, A.I. do P., Lambertucci, R.H., & Mendes-da-Silva, C. (2020). Lardrich and canola oil-rich high-fat diets during pregnancy promote rats’ offspring neurodevelopmental delay and behavioral disorders. Physiology & Behavior, 213, Article 112722. https://doi.org/10.1016/j.physbeh.2019.112722
  • Tsan, L., Décarie-Spain, L., Noble, E.E., & Kanoski, S.E. (2021). Western diet consumption during development: setting the stage for neurocognitive dysfunction. Frontiers in Neuroscience, 15, Article 632312. https://doi.org/10.3389/fnins.2021.632312
  • van Bodegom, M., Homberg, J.R., & Henckens, M.J.A.G. (2017). Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Frontiers in Cellular Neuroscience, 11, Article 87. https://doi.org/10.3389/fncel.2017.00087
  • van de Wouw, M., Boehme, M., Lyte, J.M., Wiley, N., Strain, C., O’Sullivan, O., Clarke, G., Stanton, C., Dinan, T.G., & Cryan, J.F. (2018). Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain–gut axis alterations. Journal of Physiology, 596, 4923–4944. https://doi.org/10.1113/JP276431
  • Wang, D., Levine, J.L.S., Avila-Quintero, V., Bloch, M., & Kaffman, A. (2020). Systematic review and meta-analysis: effects of maternal separation on anxiety-like behavior in rodents. Translational Psychiatry, 10(1), Article 174. https://doi.org/10.1038/s41398-020-0856-0
  • Wang, S., Huang, M., You, X., Zhao, J., Chen, L., Wang, L., Luo, Y., & Chen, Y. (2018). Gut microbiota mediates the anti-obesity effect of calorie restriction in mice. Scientific Reports, 8(1), Article 13037. https://doi.org/10.1038/s41598-018-31353-1
  • Winther, G., Elfving, B., Müller, H.K., Lund, S., & Wegener, G. (2018). Maternal high-fat diet programs offspring emotional behavior in adulthood. Neuroscience, neuroscience.2018.07.014 388, 87–101. https://doi.org/10.1016/j.
  • Yang, Y., Duan, C., Huang, L., Xia, X., Zhong, Z., Wang, B., Wang, Y., & Ding, W. (2020). Juvenile high–fat diet–induced senescent glial cells in the medial prefrontal cortex drives neuropsychiatric behavioral abnormalities in mice. Behavioural Brain Research, 395, Article 112838. https://doi.org/10.1016/j.bbr.2020.112838