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Stress
The International Journal on the Biology of Stress
Volume 27, 2024 - Issue 1
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Research Article

Adolescent high fat diet alters the transcriptional response of microglia in the prefrontal cortex in response to stressors in both male and female mice

ORCID Icon, , ORCID Icon, & ORCID Icon
Article: 2365864 | Received 31 Oct 2023, Accepted 28 May 2024, Published online: 24 Jun 2024

References

  • Alexaki, V. I. (2021). The impact of obesity on microglial function: Immune, metabolic and endocrine perspectives. Cells, 10(7), 1. https://doi.org/10.3390/cells10071584
  • Andersen, C. L., Jensen, J. L., & Ørntoft, T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research, 64(15), 5245–14. https://doi.org/10.1158/0008-5472.CAN-04-0496
  • Astrup, A., Dyerberg, J., Selleck, M., & Stender, S. (2008). Nutrition transition and its relationship to the development of obesity and related chronic diseases. Obesity Reviews, 9 Suppl 1, 48–52. https://doi.org/10.1111/j.1467-789X.2007.00438.x
  • Beilharz, J. E., Maniam, J., & Morris, M. J. (2015). Diet-induced cognitive deficits: The role of fat and sugar, potential mechanisms and nutritional interventions. Nutrients, 7(8), 6719–6738. https://doi.org/10.3390/nu7085307
  • Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Layé, S., & Ferreira, G. (2014). Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain, Behavior, and Immunity, 40, 9–17. https://doi.org/10.1016/j.bbi.2014.03.005
  • Boitard, C., Etchamendy, N., Sauvant, J., Aubert, A., Tronel, S., Marighetto, A., Layé, S., & Ferreira, G. (2012). Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice. Hippocampus, 22(11), 2095–2100. https://doi.org/10.1002/hipo.22032
  • Bollinger, J. L., & Wohleb, E. S. (2019). The formative role of microglia in stress-induced synaptic deficits and associated behavioral consequences. Neuroscience Letters, 711, 134369. https://doi.org/10.1016/j.neulet.2019.134369
  • Bollinger, J. L., Horchar, M. J., & Wohleb, E. S. (2020). Diazepam limits microglia-mediated neuronal remodeling in the prefrontal cortex and associated behavioral consequences following chronic unpredictable stress. Neuropsychopharmacology, 45(10), 1766–1776. https://doi.org/10.1038/s41386-020-0720-1
  • Bollinger, J. L., Horchar, M. J., & Wohleb, E. S. (2024). Repeated activation of pyramidal neurons in the prefrontal cortex alters microglial phenotype in male mice. The Journal of Pharmacology and Experimental Therapeutics, 388(2), 715–723. https://doi.org/10.1124/jpet.123.001759
  • Butler, M. J. (2021). The role of Western diets and obesity in peripheral immune cell recruitment and inflammation in the central nervous system. Brain, Behavior, and Immunity-Health, 16, 100298. https://doi.org/10.1016/j.bbih.2021.100298
  • Butler, M. J., Cole, R. M., Deems, N. P., Belury, M. A., & Barrientos, R. M. (2020). Fatty food, fatty acids, and microglial priming in the adult and aged hippocampus and amygdala. Brain, Behavior, and Immunity, 89, 145–158. https://doi.org/10.1016/j.bbi.2020.06.010
  • Butler, M. J., Perrini, A. A., & Eckel, L. A. (2020). Estradiol treatment attenuates high fat diet-induced microgliosis in ovariectomized rats. Hormones and Behavior, 120, 104675. https://doi.org/10.1016/j.yhbeh.2020.104675
  • Caballero, A., Granberg, R., & Tseng, K. Y. (2016). Mechanisms contributing to prefrontal cortex maturation during adolescence. Neuroscience and Biobehavioral Reviews, 70, 4–12. https://doi.org/10.1016/j.neubiorev.2016.05.013
  • Cai, G., Dinan, T., Barwood, J. M., De Luca, S. N., Soch, A., Ziko, I., Chan, S. M. H., Zeng, X.-Y., Li, S., Molero, J., & Spencer, S. J. (2014). Neonatal overfeeding attenuates acute central pro-inflammatory effects of short-term high fat diet. Frontiers in Neuroscience, 8, 446. https://doi.org/10.3389/fnins.2014.00446
  • Carlin, J. L., McKee, S. E., Hill-Smith, T., Grissom, N. M., George, R., Lucki, I., & Reyes, T. M. (2016). Removal of high-fat diet after chronic exposure drives binge behavior and dopaminergic dysregulation in female mice. Neuroscience, 326, 170–179. https://doi.org/10.1016/j.neuroscience.2016.04.002
  • Carrillo-de Sauvage, M. Á., Maatouk, L., Arnoux, I., Pasco, M., Sanz Diez, A., Delahaye, M., Herrero, M. T., Newman, T. A., Calvo, C. F., Audinat, E., Tronche, F., & Vyas, S. (2013). Potent and multiple regulatory actions of microglial glucocorticoid receptors during CNS inflammation. Cell Death and Differentiation, 20(11), 1546–1557. https://doi.org/10.1038/cdd.2013.108
  • Dantzer, R., O’Connor, J. C., Freund, G. G., Johnson, R. W., & Kelley, K. W. (2008). From inflammation to sickness and depression: When the immune system subjugates the brain. Nature Reviews. Neuroscience, 9(1), 46–56. https://doi.org/10.1038/nrn2297
  • Dayas, C. V., Buller, K. M., Crane, J. W., Xu, Y., & Day, T. A. (2001). Stressor categorization: Acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. The European Journal of Neuroscience, 14(7), 1143–1152. https://doi.org/10.1046/j.0953-816x.2001.01733.x
  • Deczkowska, A., Keren-Shaul, H., Weiner, A., Colonna, M., Schwartz, M., & Amit, I. (2018). Disease-associated microglia: A universal immune sensor of neurodegeneration. Cell, 173(5), 1073–1081. https://doi.org/10.1016/j.cell.2018.05.003
  • Doremus-Fitzwater, T. L., Gano, A., Paniccia, J. E., & Deak, T. (2015). Male adolescent rats display blunted cytokine responses in the CNS after acute ethanol or lipopolysaccharide exposure. Physiology & Behavior, 148, 131–144. https://doi.org/10.1016/j.physbeh.2015.02.032
  • Fakih, W., Zeitoun, R., AlZaim, I., Eid, A. H., Kobeissy, F., Abd-Elrahman, K. S., & El-Yazbi, A. F. (2022). Early metabolic impairment as a contributor to neurodegenerative disease: Mechanisms and potential pharmacological intervention. Obesity, 30(5), 982–993. https://doi.org/10.1002/oby.23400
  • Gądek-Michalska, A., Tadeusz, J., Rachwalska, P., Spyrka, J., & Bugajski, J. (2011). Effect of prior stress on interleukin-1β and HPA axis responses to acute stress. Pharmacological Reports, 63(6), 1393–1403. https://doi.org/10.1016/s1734-1140(11)70703-4
  • Gao, Y., Vidal-Itriago, A., Kalsbeek, M. J., Layritz, C., García-Cáceres, C., Tom, R. Z., Eichmann, T. O., Vaz, F. M., Houtkooper, R. H., van der Wel, N., Verhoeven, A. J., Yan, J., Kalsbeek, A., Eckel, R. H., Hofmann, S. M., & Yi, C.-X. (2017). Lipoprotein lipase maintains microglial innate immunity in obesity. Cell Reports, 20(13), 3034–3042. https://doi.org/10.1016/j.celrep.2017.09.008
  • Gibb, J., Hayley, S., Gandhi, R., Poulter, M. O., & Anisman, H. (2008). Synergistic and additive actions of a psychosocial stressor and endotoxin challenge: Circulating and brain cytokines, plasma corticosterone and behavioral changes in mice. Brain, Behavior, and Immunity, 22(4), 573–589. https://doi.org/10.1016/j.bbi.2007.12.001
  • Guneykaya, D., Ivanov, A., Hernandez, D. P., Haage, V., Wojtas, B., Meyer, N., Maricos, M., Jordan, P., Buonfiglioli, A., Gielniewski, B., Ochocka, N., Cömert, C., Friedrich, C., Artiles, L. S., Kaminska, B., Mertins, P., Beule, D., Kettenmann, H., & Wolf, S. A. (2018). Transcriptional and translational differences of microglia from male and female brains. Cell Reports, 24(10), 2773–2783.e6. https://doi.org/10.1016/j.celrep.2018.08.001
  • Herman, J. P., & Cullinan, W. E. (1997). Neurocircuitry of stress: Central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neurosciences, 20(2), 78–84. https://doi.org/10.1016/s0166-2236(96)10069-2
  • Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L-C., Means, T. K., & El Khoury, J. (2013). The microglial sensome revealed by direct RNA sequencing. Nature Neuroscience, 16(12), 1896–1905. https://doi.org/10.1038/nn.3554
  • Hirbec, H., Marmai, C., Duroux-Richard, I., Roubert, C., Esclangon, A., Croze, S., Lachuer, J., Peyroutou, R., & Rassendren, F. (2018). The microglial reaction signature revealed by RNAseq from individual mice. Glia, 66(5), 971–986. https://doi.org/10.1002/glia.23295
  • Horchar, M. J., & Wohleb, E. S. (2019). Glucocorticoid receptor antagonism prevents microglia-mediated neuronal remodeling and behavioral despair following chronic unpredictable stress. Brain, Behavior, and Immunity, 81, 329–340. https://doi.org/10.1016/j.bbi.2019.06.030
  • Ishii, Y., Yamaizumi, A., Kawakami, A., Islam, A., Choudhury, M. E., Takahashi, H., Yano, H., & Tanaka, J. (2015). Anti-inflammatory effects of noradrenaline on LPS-treated microglial cells: Suppression of NFκB nuclear translocation and subsequent STAT1 phosphorylation. Neurochemistry International, 90, 56–66. https://doi.org/10.1016/j.neuint.2015.07.010
  • Iwata, M., Ota, K. T., Li, X.-Y., Sakaue, F., Li, N., Dutheil, S., Banasr, M., Duric, V., Yamanashi, T., Kaneko, K., Rasmussen, K., Glasebrook, A., Koester, A., Song, D., Jones, K. A., Zorn, S., Smagin, G., & Duman, R. S. (2016). Psychological stress activates the inflammasome via release of adenosine triphosphate and stimulation of the purinergic type 2X7 receptor. Biological Psychiatry, 80(1), 12–22. https://doi.org/10.1016/j.biopsych.2015.11.026
  • Johnson, J. D., Zimomra, Z. R., & Stewart, L. T. (2012). Beta-adrenergic receptor activation primes microglia cytokine production. Journal of Neuroimmunology, 254(1–2), 161–164. https://doi.org/10.1016/j.jneuroim.2012.08.007
  • Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., Itzkovitz, S., Colonna, M., Schwartz, M., & Amit, I. (2017). A unique microglia type associated with restricting development of Alzheimer’s disease. Cell, 169(7), 1276–1290.e17. https://doi.org/10.1016/j.cell.2017.05.018
  • Kim, J. D., Yoon, N. A., Jin, S., & Diano, S. (2019). Microglial UCP2 mediates inflammation and obesity induced by high-fat feeding. Cell Metabolism, 30(5), 952–962.e5. https://doi.org/10.1016/j.cmet.2019.08.010
  • Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., Greco, D. J., Smith, S. T., Tweet, G., Humulock, Z., Zrzavy, T., Conde-Sanroman, P., Gacias, M., Weng, Z., Chen, H., … Butovsky, O. (2017). The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity, 47(3), 566–581.e9. https://doi.org/10.1016/j.immuni.2017.08.008
  • Lasselin, J., Schedlowski, M., Karshikoff, B., Engler, H., Lekander, M., & Konsman, J. P. (2020). Comparison of bacterial lipopolysaccharide-induced sickness behavior in rodents and humans: Relevance for symptoms of anxiety and depression. Neuroscience and Biobehavioral Reviews, 115, 15–24. https://doi.org/10.1016/j.neubiorev.2020.05.001
  • Lovelock, D. F., & Deak, T. (2018). Neuroendocrine and neuroimmune adaptation to chronic escalating distress (CED): A novel model of chronic stress. Neurobiology of Stress, 9, 74–83. https://doi.org/10.1016/j.ynstr.2018.08.007
  • Makinson, R., Lloyd, K., Rayasam, A., McKee, S., Brown, A., Barila, G., Grissom, N., George, R., Marini, M., Fabry, Z., Elovitz, M., & Reyes, T. M. (2017). Intrauterine inflammation induces sex-specific effects on neuroinflammation, white matter, and behavior. Brain, Behavior, and Immunity, 66, 277–288. https://doi.org/10.1016/j.bbi.2017.07.016
  • Marsh, S. E., Walker, A. J., Kamath, T., Dissing-Olesen, L., Hammond, T. R., de Soysa, T. Y., Young, A. M. H., Murphy, S., Abdulraouf, A., Nadaf, N., Dufort, C., Walker, A. C., Lucca, L. E., Kozareva, V., Vanderburg, C., Hong, S., Bulstrode, H., Hutchinson, P. J., Gaffney, D. J., … Stevens, B. (2022). Dissection of artifactual and confounding glial signatures by single-cell sequencing of mouse and human brain. Nature Neuroscience, 25(3), 306–316. https://doi.org/10.1038/s41593-022-01022-8
  • McWhirt, J., Sathyanesan, M., Sampath, D., & Newton, S. S. (2019). Effects of restraint stress on the regulation of hippocampal glutamate receptor and inflammation genes in female C57BL/6 and BALB/c mice. Neurobiology of Stress, 10, 100169. https://doi.org/10.1016/j.ynstr.2019.100169
  • Milanova, I. V., Kalsbeek, M. J. T., Wang, X.-L., Korpel, N. L., Stenvers, D. J., Wolff, S. E. C., de Goede, P., Heijboer, A. C., Fliers, E., la Fleur, S. E., Kalsbeek, A., & Yi, C.-X. (2019). Diet-induced obesity disturbs microglial immunometabolism in a time-of-day manner. Frontiers in Endocrinology, 10, 424. https://doi.org/10.3389/fendo.2019.00424
  • Ocañas, S. R., Pham, K. D., Blankenship, H. E., Machalinski, A. H., Chucair-Elliott, A. J., & Freeman, W. M. (2022). Minimizing the ex vivo confounds of cell-isolation techniques on transcriptomic and translatomic profiles of purified microglia. eNeuro, 9(2), ENEURO.0348-21.2022. https://doi.org/10.1523/ENEURO.0348-21.2022
  • Osborne, B. F., Caulfield, J. I., Solomotis, S. A., & Schwarz, J. M. (2017). Neonatal infection produces significant changes in immune function with no associated learning deficits in juvenile rats. Developmental Neurobiology, 77(10), 1221–1236. https://doi.org/10.1002/dneu.22512
  • Paolicelli, R. C., & Angiari, S. (2019). Microglia immunometabolism: From metabolic disorders to single cell metabolism. Seminars in Cell & Developmental Biology, 94, 129–137. https://doi.org/10.1016/j.semcdb.2019.03.012
  • Picard, K., Bisht, K., Poggini, S., Garofalo, S., Golia, M. T., Basilico, B., Abdallah, F., Ciano Albanese, N., Amrein, I., Vernoux, N., Sharma, K., Hui, C. W., C Savage, J., Limatola, C., Ragozzino, D., Maggi, L., Branchi, I., & Tremblay, M.-È. (2021). Microglial-glucocorticoid receptor depletion alters the response of hippocampal microglia and neurons in a chronic unpredictable mild stress paradigm in female mice. Brain, Behavior, and Immunity, 97, 423–439.
  • Porterfield, V. M., Zimomra, Z. R., Caldwell, E. A., Camp, R. M., Gabella, K. M., & Johnson, J. D. (2011). Rat strain differences in restraint stress-induced brain cytokines. Neuroscience, 188, 48–54. https://doi.org/10.1016/j.neuroscience.2011.05.023
  • Ramirez, K., Fornaguera-Trías, J., & Sheridan, J. F. (2017). Stress-induced microglia activation and monocyte trafficking to the brain underlie the development of anxiety and depression. Current Topics in Behavioral Neurosciences, 31, 155–172. https://doi.org/10.1007/7854_2016_25.
  • Reyes, T. M., Walker, J. R., DeCino, C., Hogenesch, J. B., & Sawchenko, P. E. (2003). Categorically distinct acute stressors elicit dissimilar transcriptional profiles in the paraventricular nucleus of the hypothalamus. The Journal of Neuroscience, 23(13), 5607–5616. https://doi.org/10.1523/JNEUROSCI.23-13-05607.2003
  • Sárvári, M., Hrabovszky, E., Kalló, I., Solymosi, N., Likó, I., Berchtold, N., Cotman, C., & Liposits, Z. (2012). Menopause leads to elevated expression of macrophage-associated genes in the aging frontal cortex: Rat and human studies identify strikingly similar changes. Journal of Neuroinflammation, 9(1), 264. https://doi.org/10.1186/1742-2094-9-264
  • Sathyanesan, M., Haiar, J. M., Watt, M. J., & Newton, S. S. (2017). Restraint stress differentially regulates inflammation and glutamate receptor gene expression in the hippocampus of C57BL/6 and BALB/c mice. Stress, 20(2), 197–204. https://doi.org/10.1080/10253890.2017.1298587
  • Sawchenko, P. E., Brown, E. R., Chan, R. K. W., Ericsson, A., Li, H.-Y., Roland, B. L., & Kovács, K. J. (1996). Chapter 12: The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. In G. Holstege, R. Bandler, & C. B. Saper (Eds.), Progress in brain research (Vol. 107, pp. 201–222). Elsevier.
  • Sawchenko, P. E., Li, H.-Y., & Ericsson, A. (2000). Chapter 6 – Circuits and mechanisms governing hypothalamic responses to stress: A tale of two paradigms. In E. A. Mayer & C. B. Saper (Eds.), Progress in brain research (Vol. 122, pp. 61–78). Elsevier.
  • Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron, 74(4), 691–705. https://doi.org/10.1016/j.neuron.2012.03.026
  • Schwarz, J. M., Sholar, P. W., & Bilbo, S. D. (2012). Sex differences in microglial colonization of the developing rat brain. Journal of Neurochemistry, 120(6), 948–963. https://doi.org/10.1111/j.1471-4159.2011.07630.x
  • Sobesky, J. L., D’Angelo, H. M., Weber, M. D., Anderson, N. D., Frank, M. G., Watkins, L. R., Maier, S. F., & Barrientos, R. M. (2016). Glucocorticoids mediate short-term high-fat diet induction of neuroinflammatory priming, the NLRP3 inflammasome, and the danger signal HMGB1. eNeuro, 3(4), ENEURO.0113-16.2016. https://doi.org/10.1523/ENEURO.0113-16.2016
  • Spencer, S. J., D’Angelo, H., Soch, A., Watkins, L. R., Maier, S. F., & Barrientos, R. M. (2017). High-fat diet and aging interact to produce neuroinflammation and impair hippocampal- and amygdalar-dependent memory. Neurobiology of Aging, 58, 88–101. https://doi.org/10.1016/j.neurobiolaging.2017.06.014
  • Sugama, S., Takenouchi, T., Hashimoto, M., Ohata, H., Takenaka, Y., & Kakinuma, Y. (2019). Stress-induced microglial activation occurs through β-adrenergic receptor: Noradrenaline as a key neurotransmitter in microglial activation. Journal of Neuroinflammation, 16(1), 266. https://doi.org/10.1186/s12974-019-1632-z
  • Tanaka, K. F., Kashima, H., Suzuki, H., Ono, K., & Sawada, M. (2002). Existence of functional β1- and β2-adrenergic receptors on microglia. Journal of Neuroscience Research, 70(2), 232–237. https://doi.org/10.1002/jnr.10399
  • VanRyzin, J. W., Marquardt, A. E., Pickett, L. A., & McCarthy, M. M. (2020). Microglia and sexual differentiation of the developing brain: A focus on extrinsic factors. Glia, 68(6), 1100–1113. https://doi.org/10.1002/glia.23740
  • Vegeto, E., Belcredito, S., Ghisletti, S., Meda, C., Etteri, S., & Maggi, A. (2006). The endogenous estrogen status regulates microglia reactivity in animal models of neuroinflammation. Endocrinology, 147(5), 2263–2272. https://doi.org/10.1210/en.2005-1330
  • Vinuesa, A., Pomilio, C., Menafra, M., Bonaventura, M. M., Garay, L., Mercogliano, M. F., Schillaci, R., Lux Lantos, V., Brites, F., Beauquis, J., & Saravia, F. (2016). Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity. Psychoneuroendocrinology, 72, 22–33. https://doi.org/10.1016/j.psyneuen.2016.06.004
  • Wang, J., Li, J., Sheng, X., Zhao, H., Cao, X.-D., Wang, Y.-Q., & Wu, G.-C. (2010). β-adrenoceptor mediated surgery-induced production of pro-inflammatory cytokines in rat microglia cells. Journal of Neuroimmunology, 223, 77–83.
  • Wohleb, E. S., Fenn, A. M., Pacenta, A. M., Powell, N. D., Sheridan, J. F., & Godbout, J. P. (2012). Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice. Psychoneuroendocrinology, 37(9), 1491–1505. https://doi.org/10.1016/j.psyneuen.2012.02.003
  • Wohleb, E. S., Terwilliger, R., Duman, C. H., & Duman, R. S. (2018). Stress-induced neuronal colony stimulating factor 1 provokes microglia-mediated neuronal remodeling and depressive-like behavior. Biological Psychiatry, 83(1), 38–49. https://doi.org/10.1016/j.biopsych.2017.05.026
  • Xu, H., Rajsombath, M. M., Weikop, P., & Selkoe, D. J. (2018). Enriched environment enhances β-adrenergic signaling to prevent microglia inflammation by amyloid-β. EMBO Molecular Medicine, 10. https://doi.org/10.15252/emmm.201808931.
  • 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, 112838. https://doi.org/10.1016/j.bbr.2020.112838