Exposure to chronic early-life stress lastingly alters the adipose tissue, the leptin system and changes the vulnerability to western-style diet later in life in mice
Open accessAbstract
Early-life stress (ES) increases the vulnerability to develop psychopathologies and cognitive decline in adulthood. Interestingly, this is often comorbid with metabolic disorders, such as obesity. However, it is unclear whether ES leads to lasting metabolic changes and to what extent this is associated with the ES-induced cognitive impairments. Here, we used an established chronic ES mouse model (from postnatal day (P) 2 to P9) to investigate the short- and long-term effects of ES exposure on parameters of the adipose tissue and the leptin system (i.e. circulating levels and gene expression of leptin and its receptor) in both sexes. Immediately following ES, the offspring exhibited reductions in white adipose tissue (WAT) mass, plasma leptin levels and in leptin mRNA expression in WAT. Furthermore, ES exposure led to increased brown adipose tissue and browning of WAT, which was evident by a drastic increase in uncoupling protein 1 mRNA expression in the inguinal WAT at P9. Notably, the ES-induced reductions in WAT mass, plasma leptin and leptin expression in WAT were sustained into adulthood and were accompanied by changes in body fat distribution, such as a higher ratio between mesenteric WAT and other WATs. Interestingly, while ES exposure increased leptin receptor mRNA expression in the choroid plexus, it was unaltered in the hippocampus. This suggests an adaptation to maintain central leptin homeostasis following ES exposure. In addition, chronic ES exposure resulted in the well-established cognitive impairment in object recognition performance during adulthood, which correlated positively with reductions in WAT mass observed in male, but not in female mice. Finally, to assess if ES leads to a different metabolic phenotype in a moderate obesogenic environment, we measured body fat accumulation of control and ES-exposed mice in response to a moderate western-style diet (WSD) that was provided during adulthood. ES-exposed mice subjected to WSD exhibit a higher increase in adiposity when compared to controls, suggesting that ES exposure might result in a higher vulnerability to develop obesity in a moderate obesogenic environment. To conclude, chronic ES exposure alters parameters of the adipose tissue, leads to central adaptations in leptin regulation and results in higher fat accumulations when exposed to a WSD challenge later in life. A better understanding of these metabolic effects induced by ES might open up new avenues for therapeutic (e.g. nutritional) interventions.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ELS/CT programming effect on adipose tissue leads for example to alterations in adipokine regulation and higher fat accumulations in mice.
“leading for example to alterations in adipokine regulation and higher fat accumulations in mice (300).”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [300]
The Discussion (section 4) reports altered leptin regulation and greater fat accumulation in early-life-stressed mice, but specifies that the greater accumulation occurred under a moderate western-style diet. The Results (section 3.5) also report lower body fat before that diet challenge and no difference in absolute fat mass at its end. The citing sentence omits this condition and could imply generally higher fat mass. (LLM, conf=0.89)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
A transgenic model of visceral obesity and the metabolic syndrome
Masuzaki, H., Paterson, J., Shinyama, H., Morton, N. M., Mullins, J. J., Seckl, J. R., & Flier, J. S. (2001) · Science · doi:10.1126/science.1066285 · Cited by 1,766 · see citing works
The link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704 · see citing works
The sexual dimorphism of obesity
Palmer, B. F., & Clegg, D. J. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.11.029 · Cited by 919 · see citing works
Adaptive thermogenesis in adipocytes: Is beige the new brown?
Wu, J., Cohen, P., & Spiegelman, B. M. (2013) · Genes & Development · doi:10.1101/gad.211649.112 · Cited by 828 · see citing works
Childhood maltreatment and obesity: systematic review and meta-analysis
Danese, A., & Tan, M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.54 · Cited by 709 · cited 1× · see citing works
“…the developmental trajectory of these circuitries Interest-ingly, both clinical and pre-clinical evidence suggests that ES does reduce leptin levels early (Salzmann et al., 2004; Schmidt et al., 2006) and later in life (Danese and Tan 2014; Viveros et al., 2010; Llorente-Berzal et al., 2011 .”
BackgroundAhima, R. S., Prabakaran, D., & Flier, J. S. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1176 · Cited by 627 · see citing works
Assessing rodent hippocampal involvement in the novel object recognition task. A review
Cohen, S. J., & Stackman, R. W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.002 · Cited by 592 · see citing works
Chugani, H. T., Behen, M. E., Muzik, O., Juhász, C., Nagy, F. T., & Chugani, D. C. (2001) · NeuroImage · doi:10.1006/nimg.2001.0917 · Cited by 577 · see citing works
The effects of glucocorticoids on adipose tissue lipid metabolism
Peckett, A. J., Wright, D. C., & Riddell, M. C. (2011) · Metabolism · doi:10.1016/j.metabol.2011.06.012 · Cited by 548 · see citing works
A Novel Mouse Model for Acute and Long-Lasting Consequences of Early Life Stress
Rice, C. J., Sandman, C. A., Lenjavi, M. R., & Baram, T. Z. (2008) · Endocrinology · doi:10.1210/en.2008-0633 · Cited by 521 · see citing works
Leptin targets in the mouse brain
Scott, M. M., Lachey, J. L., Sternson, S. M., Lee, C. E., Elias, C. F., Friedman, J. M., & Elmquist, J. K. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.22025 · Cited by 484 · see citing works
Browning of Subcutaneous White Adipose Tissue in Humans after Severe Adrenergic Stress
Sidossis, L. S., Porter, C. C., Saraf, M. K., Børsheim, E., Radhakrishnan, R. S., Chao, T., Ali, A., Chondronikola, M., Mlcak, R. P., Finnerty, C. C., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.06.022 · Cited by 394 · see citing works
Obesity and Hypertriglyceridemia Produce Cognitive Impairment
Farr, S. A., Yamada, K. A., Butterfield, D. A., Abdul, H. M., Xu, L., Miller, N. E., Banks, W. A., & Morley, J. E. (2008) · Endocrinology · doi:10.1210/en.2007-1722 · Cited by 382 · see citing works
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.007 · Cited by 368 · see citing works
Zakrzewska, K. E., Cusin, I., Sainsbury, A., Rohner‐Jeanrenaud, F., & Jeanrenaud, B. (1997) · Diabetes · doi:10.2337/diab.46.4.717 · Cited by 313 · see citing works
Naninck, E. F. G., Hoeijmakers, L., Kakava-Georgiadou, N., Meesters, A., Lazic, S. E., Lucassen, P. J., & Kőrösi, A. (2014) · Hippocampus · doi:10.1002/hipo.22374 · Cited by 281 · see citing works
Self-citationThe Neurobiological Toll of Child Abuse and Neglect
Neigh, G. N., Gillespie, C. F., & Nemeroff, C. B. (2009) · Trauma Violence & Abuse · doi:10.1177/1524838009339758 · Cited by 240 · see citing works
Developmental programming of hypothalamic feeding circuits
Bouret, S., & Simerly, R. (2006) · Clinical Genetics · doi:10.1111/j.1399-0004.2006.00684.x · Cited by 227 · see citing works
Milaneschi, Y., Lamers, F., Bot, M., Drent, M. L., & Penninx, B. W. J. H. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.023 · Cited by 209 · see citing works
Leptin and its role in hippocampal synaptic plasticity
HARVEY, J., SOLOVYOVA, N., & IRVING, A. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.03.001 · Cited by 202 · see citing works
Perinatal environment and its influences on metabolic programming of offspring
Tamashiro, K. L., & Moran, T. H. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.04.008 · Cited by 195 · see citing works
Lucassen, P. J., Naninck, E. F. G., van Goudoever, J. B., Fitzsimons, C. P., Joëls, M., & Kőrösi, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.08.002 · Cited by 173 · see citing works
Self-citationZloković, B. V., Jovanovic, S. S., Miao, W., Samara, S., Verma, S. P., & Farrell, C. L. (2000) · Endocrinology · doi:10.1210/endo.141.4.7435 · Cited by 170 · see citing works
Sex differences in adipose tissue
Fuente-Martín, E., Argente-Arizón, P., Ros, P., Argente, J., & Chowen, J. A. (2013) · Adipocyte · doi:10.4161/adip.24075 · Cited by 161 · see citing works
Molecular mapping of mouse brain regions innervated by leptin receptor-expressing cells
Patterson, C. M., Leshan, R. L., Jones, J. C., & Myers, M. G. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.010 · Cited by 150 · see citing works
Farr, O. M., Tsoukas, M. A., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.07.004 · Cited by 146 · see citing works
Avishai‐Eliner, S., Gilles, E. E., Eghbal‐Ahmadi, M., Bar‐El, Y., & Baram, T. Z. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00698.x · Cited by 139 · see citing works
Nousen, E. K., Franco, J. G., & Sullivan, E. L. (2013) · Neuroendocrinology · doi:10.1159/000355632 · Cited by 123 · see citing works
Leptin regulation of hippocampal synaptic function in health and disease
Irving, A. J., & Harvey, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0155 · Cited by 123 · see citing works
Vázquez, D. M., van Oers, H. J. J., Levine, S. D., & Akil, H. (1996) · Brain Research · doi:10.1016/0006-8993(96)00465-9 · Cited by 122 · see citing works
Nutritional manipulations in the perinatal period program adipose tissue in offspring
Lukaszewski, M., Eberlé, D., Vieau, D., & Breton, C. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00231.2013 · Cited by 122 · see citing works
Effects of early-life stress on cognitive function and hippocampal structure in female rodents.
Loi, M., Mossink, J. C. L., Meerhoff, G. F., Den Blaauwen, J. L., Lucassen, P. J., & Joëls, M. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.024 · Cited by 109 · see citing works
Self-citationSelective deletion of leptin receptors in adult hippocampus induces depression-related behaviours
Guo, M., Huang, T.-Y., Garza, J. C., Chua, S. C., & Lu, X. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000703 · Cited by 101 · see citing works
Schmidt, M. V., Levine, S. D., Alam, S., Harbich, D., Sterlemann, V., Ganea, K., de Kloet, E. R., Holsboer, F., & Müller, M. B. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01482.x · Cited by 93 · see citing works
Reduced serum levels of adiponectin in elderly patients with major depression
Diniz, B. S., Teixeira, A. L., Campos, A. C., de Miranda, A. S., Rocha, N. P., Talib, L. L., Gattaz, W. F., & Forlenza, O. V. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.04.028 · Cited by 91 · see citing works
Llorente‐Berzal, A., Fuentes, S., Gagliano, H., López‐Gallardo, M., Armario, A., Viveros, M., & Nadal, R. A. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00318.x · Cited by 88 · see citing works
Catalano, K. J., Stefanovski, D., & Bergman, R. N. (2010) · Diabetes · doi:10.2337/db08-0675 · Cited by 84 · see citing works
Salzmann, C., Otis, M., Long, H., Roberge, C., Gallo‐Payet, N., & Walker, C. (2003) · Endocrinology · doi:10.1210/en.2003-1514 · Cited by 72 · see citing works
Mitchell, S. E., Nogueiras, R., Morris, A. C., Tovar, S. A., Grant, C., Cruickshank, M., Rayner, D. V., Diéguez, C., & Williams, L. M. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.173328 · Cited by 65 · see citing works
Phenotypic effects of an induced mutation of the ObRa isoform of the leptin receptor
Li, Z., Ceccarini, G., Eisenstein, M., Tan, K., & Friedman, J. M. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.07.007 · Cited by 55 · see citing works
Viveros, M., Llorente, R., Díaz, F., Romero‐Zerbo, S., Bermúdez‐Silva, F. J., de Fonseca, F. R., Argente, J., & Chowen, J. A. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.08.003 · Cited by 46 · see citing works
Adipocyte glucocorticoid receptors mediate fat-to-brain signaling
de Kloet, A. D., Krause, E. G., Solomon, M. B., Flak, J. N., Scott, K. A., Kim, D. H., Myers, B., Ulrich‐Lai, Y. M., Woods, S. C., Seeley, R. J., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.03.008 · Cited by 46 · see citing works
Childhood maltreatment increases the risk for visceral obesity
Li, L., Chassan, R. A., Bruer, E. H., Gower, B. A., & Shelton, R. C. (2015) · Obesity · doi:10.1002/oby.21143 · Cited by 41 · see citing works
Increased vulnerability to ethanol consumption in adolescent maternal separated mice
García‐Gutiérrez, M. S., Navarrete, F., Aracil-Fernández, A., Bartoll, A., Martínez‐Gras, I., Lanciego, J. L., Rubio, G., & Manzanares, J. (2015) · Addiction Biology · doi:10.1111/adb.12266 · Cited by 40 · see citing works
Postnatal maternal separation modifies the response to an obesogenic diet in adulthood
Paternain, L., Martisova, E., Milagro, F. I., Ramírez, M. J., Martínez, J. A., & Campión, J. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009043 · Cited by 39 · see citing works
Kohda, K., Jinde, S., Iwamoto, K., Bundo, M., Kato, N., & Kato, T. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705005857 · Cited by 26 · see citing works
Maniam, J., Antoniadis, C. P., Wang, K. W., & Morris, M. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00138 · Cited by 24 · see citing works
Choosing an Adipose Tissue Depot for Sampling
Casteilla, L., Pénicaud, L., Cousin, B., & Calise, D. (2003) · Humana Press eBooks · doi:10.1385/1-59259-231-7:001 · Cited by 15 · see citing works
The role of adiposity in the relationship between serum leptin and severe major depressive episode
Ubani, C. C., & Zhang, J. (2015) · Psychiatry Research · doi:10.1016/j.psychres.2015.05.009 · Cited by 9 · see citing works
Barbero (2014) · doi:10.1016/j · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 402 · see citing works
Self-citationAgorastos, A., Pervanidou, P., Chrousos, G. P., & Baker, D. G. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00118 · Cited by 385 · see citing works
“On the other hand, there is also evidence that ELS/CT can exert a programming effect on the adipose tissue and alter the highly sensitive process of adipogenesis (282), leading for example to alterations in adipokine regulation and higher fat accumulations in mice (300).”
BackgroundFood for thought: how nutrition impacts cognition and emotion
Spencer, S. J., Kőrösi, A., Layé, S., Shukitt‐Hale, B., & Barrientos, R. M. (2017) · npj Science of Food · doi:10.1038/s41538-017-0008-y · Cited by 279 · see citing works
Obesity as a Risk Factor for Dementia and Alzheimer’s Disease: The Role of Leptin
Flores-Cordero, J. A., Pérez-Pérez, A., Jiménez-Cortegana, C., Alba, G., Flores-Barragán, A., & Sánchez-Margalet, V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23095202 · Cited by 212 · see citing works
Kronman, H., Torres-Berrío, A., Sidoli, S., Issler, O., Godino, A., Ramakrishnan, A., Mews, P., Lardner, C. K., Parise, E. M., Walker, D. M., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00814-8 · Cited by 108 · see citing works
Guadagno, A., Wong, T. P., & Walker, C. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.09.025 · Cited by 107 · see citing works
Bolton, J. L., Ruiz, C. M., Rismanchi, N., Sanchez, G. A., Castillo, E., Huang, J. J., Cross, C., Baram, T. Z., & Mahler, S. V. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.01.002 · Cited by 91 · see citing works
Manzano-Nieves, G., Bravo, M., Baskoylu, S. N., & Bath, K. (2020) · eLife · doi:10.7554/elife.55263 · Cited by 88 · see citing works
Social Origins of Developmental Risk for Mental and Physical Illness
Cameron, J. L., Eagleson, K. L., Fox, N. A., Hensch, T. K., & Levitt, P. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1822-17.2017 · Cited by 81 · see citing works
Obesity-induced chronic low-grade inflammation in adipose tissue: A pathway to Alzheimer’s disease
Zhai, W., Meng, Z., Chunxiao, W., Lingjie, M., Anguo, Z., Zhang, Y., Xinran, C., Yanjiao, X., & Li, S. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102402 · Cited by 64 · see citing works
Choroid Plexus Blood-CSF Barrier: Major Player in Brain Disease Modeling and Neuromedicine
Johanson, C. E. (2018) · Journal of Neurology and Neuromedicine · doi:10.29245/2572.942x/2018/4.1194 · Cited by 62 · see citing works
Hoeijmakers, L., Lesuis, S. L., Krugers, H. J., Lucassen, P. J., & Kőrösi, A. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.02.003 · Cited by 63 · see citing works
Self-citationMorató, L., Astori, S., Zalachoras, I., Rodrigues, J., Ghosal, S., Huang, W., de Suduiraut, I. G., Grosse, J., Zanoletti, O., Cao, L., et al. (2022) · Science Advances · doi:10.1126/sciadv.abj9109 · Cited by 51 · see citing works
Eck, S. R., Ardekani, C. S., Salvatore, M., Luz, S., Kim, E. D., Rogers, C. M., Hall, A., Lee, D. E., Famularo, S. T., Bhatnagar, S., et al. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14609 · Cited by 52 · see citing works
de Lima, R. M. S., Bento, L. V. D. S., Lugon, M. D. M. V., Baraúna, V. G., Bittencourt, A. S., Dalmaz, C., & Bittencourt, A. P. S. D. V. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112399 · Cited by 50 · see citing works
Yam, K., Schipper, L., Reemst, K., Ruigrok, S. R., Abbink, M. R., Hoeijmakers, L., Naninck, E. F. G., Zarekiani, P., Oosting, A., van der Beek, E. M., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201802297r · Cited by 49 · see citing works
Self-citationYam, K., Ruigrok, S. R., Ziko, I., Luca, S. N. D., Lucassen, P. J., Spencer, S. J., & Kőrösi, A. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.09.006 · Cited by 45 · see citing works
Self-citationLeigh, S.-J., Lee, F., & Morris, M. J. (2018) · Current Obesity Reports · doi:10.1007/s13679-018-0292-0 · Cited by 43 · see citing works
Lesuis, S. L., Kaplick, P. M., Lucassen, P. J., & Krugers, H. J. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.02.023 · Cited by 40 · see citing works
Self-citationZhou, L., Xiao, X., Zhang, Q., Zheng, J., Li, M., Wang, X., Deng, M., Zhai, X., & Liu, J. Y. (2019) · Food & Function · doi:10.1039/c9fo01046g · Cited by 42 · see citing works
Effects of early-life stress on peripheral and central mitochondria in male mice across ages
Ruigrok, S. R., Yim, K., Emmerzaal, T. L., Geenen, B., Stöberl, N., den Blaauwen, J. L., Abbink, M. R., Kiliaan, A. J., van Schothorst, E. M., Kozicz, T., et al. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105346 · Cited by 37 · see citing works
Self-citationHormonal and nutritional regulation of postnatal hypothalamic development
Sominsky, L., Jasoni, C. L., Twigg, H., & Spencer, S. J. (2018) · Journal of Endocrinology · doi:10.1530/joe-17-0722 · Cited by 34 · see citing works
Méquinion, M., Foldi, C. J., & Andrews, Z. B. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00190 · Cited by 34 · see citing works
Strzelewicz, A. R., Sanchez, E. O., Rondón-Ortiz, A. N., Raneri, A., Famularo, S. T., Bangasser, D. A., & Kentner, A. C. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.01.003 · Cited by 28 · see citing works
Eller, O. C., Morris, E. M., Thyfault, J. P., & Christianson, J. A. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113000 · Cited by 28 · see citing works
Luo, Q., Zhang, L., Huang, C.-C., Zheng, Y., Kanen, J. W., Zhao, Q., Yao, Y., Quinlan, E. B., Jia, T., Banaschewski, T., et al. (2020) · BMC Medicine · doi:10.1186/s12916-020-01743-2 · Cited by 26 · see citing works
Reemst, K., Ruigrok, S. R., Bleker, L. S., Naninck, E. F. G., Ernst, T. R., Kotah, J. M., Lucassen, P. J., Roseboom, T. J., Pollux, B. J. A., de Rooij, S. R., et al. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104627 · Cited by 26 · see citing works
Self-citationLesuis, S. L., van Hoek, B. A. C. E., Lucassen, P. J., & Krugers, H. J. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.05.016 · Cited by 27 · see citing works
Self-citationBielefeld, P., Abbink, M. R., Davidson, A. R., Reijner, N., Abiega, O., Lucassen, P. J., Kőrösi, A., & Fitzsimons, C. P. (2021) · Stress · doi:10.1080/10253890.2021.1879787 · Cited by 24 · see citing works
Self-citationShupe, E. A., & Clinton, S. M. (2021) · Developmental Psychobiology · doi:10.1002/dev.22144 · Cited by 24 · see citing works
Proteomic and mitochondrial adaptations to early-life stress are distinct in juveniles and adults
Eagleson, K. L., Villaneuva, M., Southern, R. M., & Levitt, P. R. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100251 · Cited by 24 · see citing works
Ruigrok, S. R., Abbink, M. R., Geertsema, J., Kuindersma, J. E., Stöberl, N., van der Beek, E. M., Lucassen, P. J., Schipper, L., & Kőrösi, A. (2021) · Nutrients · doi:10.3390/nu13020288 · Cited by 23 · see citing works
Self-citationAssociations of early life stress with leptin and ghrelin in healthy young adults
Daniels, T. E., Mathis, K. J., Gobin, A. P., Angeles, W. W. L.-D. L., Smith, E. M., Chanthrakumar, P., de la Monte, S. M., & Tyrka, A. R. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.106007 · Cited by 22 · see citing works
Early life stress and metabolism
Malik, S., & Spencer, S. J. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.01.016 · Cited by 21 · see citing works
Reemst, K., Broos, J. Y., Abbink, M. R., Cimetti, C., Giera, M. A., Kooij, G., & Kőrösi, A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.967437 · Cited by 22 · see citing works
Self-citationSinghaarachchi, P. H., Antal, P., Calon, F., Culmsee, C., Delpech, J.-C., Feldotto, M., Geertsema, J., Hoeksema, E. E., Kőrösi, A., Layé, S., et al. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105724 · Cited by 18 · see citing works
Abbink, M. R., Schipper, L., Naninck, E. F. G., de Vos, C. M. H., Meier, R. T., van der Beek, E. M., Lucassen, P. J., & Kőrösi, A. (2020) · Nutrients · doi:10.3390/nu12020570 · Cited by 19 · see citing works
Self-citationReemst, K., Tims, S., Yam, K., Mischke, M., Knol, J., Brul, S., Schipper, L., & Kőrösi, A. (2022) · mSystems · doi:10.1128/msystems.00180-22 · Cited by 17 · see citing works
Self-citationModulation of the Hypothalamic Nutrient Sensing Pathways by Sex and Early-Life Stress
Ruigrok, S. R., Stöberl, N., Yam, K., de Lucia, C., Lucassen, P. J., Thuret, S., & Kőrösi, A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.695367 · Cited by 16 · see citing works
Self-citationKim, C., Schilder, N., Adolphus, K., Berry, A., Musillo, C., Dye, L., Cirulli, F., Kőrösi, A., & Thuret, S. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104072 · Cited by 16 · see citing works
Early Life Stress, Brain Development, and Obesity Risk: Is Oxytocin the Missing Link?
Colleluori, G., Galli, C., Severi, I., Perugini, J., & Giordano, A. (2022) · Cells · doi:10.3390/cells11040623 · Cited by 15 · see citing works
Knop, J., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Joëls, M., & van der Veen, R. (2020) · Genes Brain & Behavior · doi:10.1111/gbb.12655 · Cited by 15 · see citing works
Kotah, J. M., Kater, M. S. J., Brosens, N., Lesuis, S. L., Tandari, R., Blok, T. M., Marchetto, L., Yusaf, E., Koopmans, F., Smit, A. B., et al. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13569 · Cited by 14 · see citing works
Self-citationLapp, H. E., Mueller, I., & Moore, C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112957 · Cited by 14 · see citing works
Ruigrok, S. R., Kotah, J. M., Kuindersma, J. E., Speijer, E., van Irsen, A. A. S., la Fleur, S. E., & Kőrösi, A. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100360 · Cited by 15 · see citing works
Alshagga, M. A., Mohamed, Z., Seyedan, A., Ebling, F. J. P., & Alshawsh, M. A. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.113187 · Cited by 13 · see citing works
Sepers, B., Verhoeven, K. J. F., & van Oers, K. (2024) · Evolutionary Applications · doi:10.1111/eva.13664 · Cited by 11 · see citing works
Lesuis, S. L., Lucassen, P. J., & Krugers, H. J. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.012 · Cited by 13 · see citing works
Self-citationYun, L., Wu, T., Li, W., & Zhang, M. (2020) · Food & Function · doi:10.1039/d0fo02754e · Cited by 11 · see citing works
Maturation of White Adipose Tissue Function in C57BL/6j Mice From Weaning to Young Adulthood
Kodde, A., Engels, E., Oosting, A., van Limpt, K., van der Beek, E. M., & Keijer, J. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00836 · Cited by 11 · see citing works
Self-citationRen, Z., Su, B., Du, Y., Zhou, T., Zheng, X., & Liu, J. (2023) · General Psychiatry · doi:10.1136/gpsych-2023-101092 · Cited by 8 · see citing works
Reemst, K., Lopizzo, N., Abbink, M. R., Engelenburg, H. J., Cattaneo, A., & Kőrösi, A. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.01.011 · Cited by 8 · see citing works
Self-citationBarbour‐Tuck, E., Boyes, N. G., Tomczak, C. R., Lahti, D. S., Baril, C. L., Pockett, C. R., Runalls, S., Kakadekar, A. P., Pharis, S., Bradley, T. J., et al. (2020) · BMC Cardiovascular Disorders · doi:10.1186/s12872-020-01508-y · Cited by 8 · see citing works
Kotah, J. M., Hoeijmakers, L., Nutma, E., Lucassen, P. J., & Kőrösi, A. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100379 · Cited by 7 · see citing works
Self-citationThe relevance of a rodent cohort in the Consortium on Individual Development
van der Veen, R., Bonapersona, V., & Joëls, M. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100846 · Cited by 6 · see citing works
Is there a hypothalamic basis for anorexia nervosa?
Tolle, V., Ramoz, N., & Epelbaum, J. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820683-6.00030-0 · Cited by 6 · see citing works
Xiao, Y., Wang, J., Siegel, P. B., Cline, M. A., & Gilbert, E. R. (2020) · Life · doi:10.3390/life10050051 · Cited by 5 · see citing works
Cadney, M. D., de Albuquerque, R. L., Schwartz, N. E., McNamara, M. P., Castro, A. A., Schmill, M. P., Hillis, D. A., & Garland, T. (2022) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s204017442200054x · Cited by 5 · see citing works
Sallam, N. A., Peterson, C. S., Kamar, S. S., Saenz, C., Visser, F., & Borgland, S. L. (2025) · British Journal of Pharmacology · doi:10.1111/bph.17447 · Cited by 4 · see citing works
Life-course effects of early life adversity exposure on eating behavior and metabolism
de Lima, R. M. S., Barth, B., Arcego, D. M., Krolow, R., Silveira, P. P., & Dalmaz, C. (2021) · Advances in food and nutrition research · doi:10.1016/bs.afnr.2021.02.003 · Cited by 4 · see citing works
Ige, S., Alaoui, K., Al‐Dibouni, A., Dallas, M. L., Cagampang, F. R. A., Sellayah, D., Chantler, P. D., & Boateng, S. Y. (2023) · The FASEB Journal · doi:10.1096/fj.202300269rrr · Cited by 4 · see citing works
Schneider, S. C. S., de Andrade, B. Z., Paz, E. D. R., Amaral, A. C., Bronczek, G. A., Lubaczeuski, C., Grassiolli, S., Koehler‐Santos, P., de Oliveira, J. R., Donadio, M. V. F., et al. (2018) · Experimental Physiology · doi:10.1113/ep087171 · Cited by 3 · see citing works
Snowden, S. G., Koulman, A., Christian Gaser, B., la Fleur, S. E., Roseboom, T. J., Kőrösi, A., & de Rooij, S. R. (2024) · npj Aging · doi:10.1038/s41514-024-00169-x · Cited by 3 · see citing works
Adverse Childhood Experiences Influence Longitudinal Changes in Leptin But Not Adiponectin
Matovic, S., Rummel, C. D., Neumann, E., McGrath, J. J., & Gouin, J. (2025) · Psychosomatic Medicine · doi:10.1097/psy.0000000000001366 · Cited by 2 · see citing works
ALZHEIMER HASTALIĞI, RİSK FAKTÖRLERİ VE TEDAVİ
Yıldırım, N., & Eke, B. C. (2024) · Ankara Universitesi Eczacilik Fakultesi Dergisi · doi:10.33483/jfpau.1441827 · Cited by 2 · see citing works
Cruz-Carrillo, G., Herrejón, K., Ruiz‐González, R., Roque, A. P., Zamudio-Flores, J., & Lajud, N. (2026) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174425100433 · Cited by 1 · see citing works
Chd8 haploinsufficiency impacts rearing experience in C57BL/6 mice
Tabbaa, M., & Levitt, P. R. (2024) · Genes Brain & Behavior · doi:10.1111/gbb.12892 · Cited by 1 · see citing works
Programming of metabolic functions by early-life stress: Relevance for vulnerability to obesity
Ruigrok, S. R., Yam, K., Abbink, M. R., Kroon, J., la Fleur, S. E., Lucassen, P. J., & Kőrösi, A. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.11.776
Self-citationEarly life stress decreases the proliferation and numbers of adult hypothalamic neural stem cellsPreprint
Bielefeld, P., Abbink, M. R., Davidson, A. R., Lucassen, P. J., Kőrösi, A., & Fitzsimons, C. P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/831446
Self-citationNieves, G. M., Bravo, M., & Bath, K. (2020) · bioRxiv · doi:10.1101/2020.01.07.892687
Schneider, S. C. S., Paz, E. D. R., de Andrade, B. Z., Amaral, A. C., Bronczek, G. A., Koehler‐Santos, P., de Oliveira, J. R., Franci, C. R., Donadio, M. V. F., Holman, P. J., et al. (2025) · PLoS ONE · doi:10.1371/journal.pone.0313103
Maternal stress shapes offspring innate immunity via milk leptinPreprint
Sommer, E. L., Valtakari, N. V., Holleman, M., Peters, C. S. D., Linsen, S. A. M., Zegelaar, M., Markus, N., Mackaaij, C., Thijssen, S., Perdijk, O., et al. (2026) · Research Square · doi:10.21203/rs.3.rs-9587229/v1
Navarrete, J., V, & Vásquez, B. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27115056
Holt, N. C., Nguyen, B. D., Reitman, T., Polly Campbell, A., Samuk, K., & Malone, M. (2026) · Integrative and Comparative Biology · doi:10.1093/icb/icag114
Effects of early life adversity on acute metabolic outcomes during neonatal development
Lapp, H. E., Salazar, M. G., Deveraux, E., Misztal, P. K., & Champagne, F. A. (2026) · Neurobiology of Stress · doi:10.1016/j.ynstr.2026.100835
Crino, O. L., Friesen, C. R., Hill, G. E., Leibold, D. C., Recio, P., Salin, K., Wild, K. H., & Noble, D. W. A. (2026) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1002/brv.70199
Early life stress affects the transcription and chromatin accessibility of spermatogonial cellsPreprint
Arzate‐Mejía, R. G., Schöpp, T., Uzel, K., Lazar-Contes, I., & Mansuy, I. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.20.745941
- Authors
- Yam, K. Y., Naninck, E. F. G., Abbink, M. R., la Fleur, S. E., Schipper, L., van den Beukel, J. C., Grefhorst, A., Oosting, A., van der Beek, E. M., Lucassen, P. J., & Korosi, A.
- Affiliations
- University of Amsterdam (NL)
- Nutricia Research (Netherlands) (NL)
- Erasmus MC (NL)
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2017-03
- Volume
- 77
- Pages
- 186-195
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2562701561
- Cited by
- 78
- References
- 50
- Citations by year
- 2026: 7 · 2025: 3 · 2024: 9 · 2023: 3 · 2022: 8 · 2021: 10 · 2020: 14 · 2019: 12 · 2018: 6 · 2017: 6
- FWCI
- 5.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Alzheimer Nederland
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- early life stress, chronic stress, white adipose tissue, brown adipose tissue, brown adipose tissue browning, leptin, leptin receptor, UCP1, body fat distribution, cognitive impairment, object recognition memory, Western diet, sex differences, choroid plexus, hippocampus
- MeSH terms
- Uncoupling Protein 1, Adipose Tissue, Animals, Disease Models, Animal, Feeding Behavior, Obesity, Stress, Psychological, Leptin, Mice, Diet, Western
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
