Maternal sucrose consumption alters steroid levels in the mother, placenta and fetus

in Journal of Endocrinology
Authors:
Désirée R Seib Department of Psychology and Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada

Search for other papers by Désirée R Seib in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0001-9953-8270
,
Minseon M Jung Department of Psychology and Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada
Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

Search for other papers by Minseon M Jung in
Current site
Google Scholar
PubMed Close
, and
Kiran K Soma Department of Psychology and Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada
Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

Search for other papers by Kiran K Soma in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0003-2169-8092

Correspondence should be addressed to D R Seib: dseib@upei.ca

(Present address: Department of Biology, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada)

DOI:
https://doi.org/10.1530/JOE-24-0238
Volume/Issue:
Volume 265: Issue 1
Article Type:
Research Article
Article ID:
e240238
Online Publication Date:
24 Feb 2025
Copyright:
© the author(s) 2025
Restricted access
Rent on DeepDyve

Sign up for journal news

Maternal diet has long-term effects on offspring brain development and behavior. Sucrose (table sugar) intake is high in modern diets, but it is not clear how a maternal high-sucrose diet (HSD) affects offspring. In rats, a maternal HSD (26% of calories from sucrose, which is human-relevant) alters maternal metabolism and brain and also alters adult offspring endocrinology and behavior in a sex-specific manner. Maternal sucrose intake increases corticosterone levels in adult female offspring and increases motivation for a sugar reward in adult male offspring. Here, to identify possible underlying mechanisms, we examined how a maternal HSD affects steroids in the dam, placenta and fetus at embryonic day 19.5 using liquid chromatography–tandem mass spectrometry. Maternal sucrose intake increased glucocorticoids (11-deoxycorticosterone and 11-dehydrocorticosterone) and tended to increase the mineralocorticoid aldosterone in maternal serum. In the placenta, maternal sucrose intake decreased androstenedione and testosterone. Maternal HSD increased aldosterone in the fetal blood. Similarly, in the fetal brain, maternal high sucrose intake increased aldosterone in the medial prefrontal cortex and nucleus accumbens, decreased testosterone in the nucleus accumbens and decreased corticosterone in the orbital cortex. In addition, the 11-dehydrocorticosterone/corticosterone and aldosterone/corticosterone ratios were increased in most examined brain regions. Finally, maternal HSD increased 11-dehydrocorticosterone and aldosterone in the amniotic fluid. In summary, we found dramatic and widespread changes in maternal, placental and fetal steroids that might mediate the long-term effects of maternal sucrose consumption on adult offspring neuroendocrinology and behavior.

Supplementary Materials

Journal of Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 57 57 33
PDF Downloads 59 59 39

 

  • Collapse
  • Expand
Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© the author(s) 2025
Article ID:
e240238
Article Type:
Research Article
Received Date:
12 Aug 2024
Rev-recd:
03 Dec 2024
Accepted Date:
28 Jan 2025
Print Publication Date:
01 Apr 2025
Online Publication Date:
24 Feb 2025
Keywords:
neurosteroid; steroid profiling; stress; estradiol; hippocampus

  • Adler A, Vescovo P, Robinson JK, et al. 1999 Gonadectomy in adult life increases tyrosine hydroxylase immunoreactivity in the prefrontal cortex and decreases open field activity in male rats. Neuroscience 89 939–954. (https://doi.org/10.1016/S0306-4522(98)00341-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Asghar ZA, Thompson A, Chi M, et al. 2016 Maternal fructose drives placental uric acid production leading to adverse fetal outcomes. Sci Rep 6 25091. (https://doi.org/10.1038/srep25091)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bast B-O, Rickert U, Schneppenheim J, et al. 2018 Aldosterone exerts anti-inflammatory effects on LPS stimulated microglia. Heliyon 4 e00826. (https://doi.org/10.1016/j.heliyon.2018.e00826)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bayard F, Ances IG, Tapper AJ, et al. 1970 Transplacental passage and fetal secretion of aldosterone. J Clin Invest 49 1389–1393. (https://doi.org/10.1172/JCI106356)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bordt EA, Moya HA, Jo YC, et al. 2024 Gonadal hormones impart male-biased behavioral vulnerabilities to immune activation via microglial mitochondrial function. Brain Behav Immun 115 680–695. (https://doi.org/10.1016/j.bbi.2023.11.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Briski KP, DiPasquale BM & Gillen E 1997 Induction of immediate–early gene expression in preoptic and hypothalamic neurons by the glucocorticoid receptor agonist, dexamethasone. Brain Res 768 185–196. (https://doi.org/10.1016/S0006-8993(97)00642-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brochu ML, Lehoux J-G & Picard S 1997 Effects of gestation on enzymes controlling aldosterone synthesis in the rat adrenal. Endocrinology 138 2354–2358. (https://doi.org/10.1210/endo.138.6.5198)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brunton PJ 2015 Programming the brain and behaviour by early-life stress: a focus on neuroactive steroids. J Neuroendocrinol 27 468–480. (https://doi.org/10.1111/jne.12265)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brunton PJ & Walker C-D 2024 Regulation of the hypothalamo-pituitary-adrenal axis in pregnancy and lactation. In Neuroendocrine Regulation of Mammalian Pregnancy and Lactation, pp 93–131. Eds PJ Brunton & DR Grattan. Cham: Springer International Publishing. (https://doi.org/10.1007/978-3-031-51138-7_4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chan SWC & Leathem JH 1975 Placental steroidogenesis in the rat: progesterone production by tissue of the basal zone. Endocrinology 96 298–303. (https://doi.org/10.1210/endo-96-2-298)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Connell JMC & Davies E 2005 The new biology of aldosterone. J Endocrinol 186 1–20. (https://doi.org/10.1677/joe.1.06017)

  • Cottrell EC, Seckl JR, Holmes MC, et al. 2014 Foetal and placental 11β‐HSD2: a hub for developmental programming. Acta Physiol 210 288–295. (https://doi.org/10.1111/apha.12187)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Crew RC, Mark PJ, Clarke MW, et al. 2016 Obesity disrupts the rhythmic profiles of maternal and fetal progesterone in rat pregnancy. Biol Reprod 95 55. (https://doi.org/10.1095/biolreprod.116.139451)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dhakal P & Soares MJ 2017 Single-step PCR-based genetic sex determination of rat tissues and cells. Biotechniques 62 232–233. (https://doi.org/10.2144/000114548)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Furukawa S, Tsuji N, Hayashi S, et al. 2022 Effects of testosterone on rat placental development. J Toxicol Pathol 35 37–44. (https://doi.org/10.1293/tox.2021-0035)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gennari-Moser C, Khankin EV, Schüller S, et al. 2011 Regulation of placental growth by aldosterone and cortisol. Endocrinology 152 263–271. (https://doi.org/10.1210/en.2010-0525)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • George G, Draycott SAV, Muir R, et al. 2019 The impact of exposure to cafeteria diet during pregnancy or lactation on offspring growth and adiposity before weaning. Sci Rep 9 14173. (https://doi.org/10.1038/s41598-019-50448-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gibson DA, Simitsidellis I & Saunders PTK 2016 Regulation of androgen action during establishment of pregnancy. J Mol Endocrinol 57 R35–R47. (https://doi.org/10.1530/JME-16-0027)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gildawie KR, Orso R, Peterzell S, et al. 2020 Sex differences in prefrontal cortex microglia morphology: impact of a two-hit model of adversity throughout development. Neurosci Lett 738 135381. (https://doi.org/10.1016/j.neulet.2020.135381)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hajnal A & Norgren R 2001 Accumbens dopamine mechanisms in sucrose intake. Brain Res 904 76–84. (https://doi.org/10.1016/S0006-8993(01)02451-9)

  • Hajnal A, Smith GP & Norgren R 2004 Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 286 R31–R37. (https://doi.org/10.1152/ajpregu.00282.2003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hamden JE, Gray KM, Salehzadeh M, et al. 2021 Steroid profiling of glucocorticoids in microdissected mouse brain across development. Developmental Neurobiol 81 189–206. (https://doi.org/10.1002/dneu.22808)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Handelsman DJ & Ly LP 2019 An accurate substitution method to minimize left censoring bias in serum steroid measurements. Endocrinology 160 2395–2400. (https://doi.org/10.1210/en.2019-00340)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Harrell CS, Zainaldin C, McFarlane D, et al. 2018 High-fructose diet during adolescent development increases neuroinflammation and depressive-like behavior without exacerbating outcomes after stroke. Brain Behav Immun 73 340–351. (https://doi.org/10.1016/j.bbi.2018.05.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Herman JP, Nawreen N, Smail MA, et al. 2020 Brain mechanisms of HPA axis regulation: neurocircuitry and feedback in context Richard Kvetnansky lecture. Stress 23 617–632. (https://doi.org/10.1080/10253890.2020.1859475)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hsu TM, Konanur VR, Taing L, et al. 2015 Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats: adolescent sugar intake impairs spatial memory. Hippocampus 25 227–239. (https://doi.org/10.1002/hipo.22368)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jacques A, Chaaya N, Beecher K, et al. 2019 The impact of sugar consumption on stress driven, emotional and addictive behaviors. Neurosci Biobehav Rev 103 178–199. (https://doi.org/10.1016/j.neubiorev.2019.05.021)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jalabert C, Ma C & Soma KK 2021 Profiling of systemic and brain steroids in male songbirds: seasonal changes in neurosteroids. J Neuroendocrinol 33 e12922. (https://doi.org/10.1111/jne.12922)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jiang P, Ren L, Zhi L, et al. 2021 Negative regulation of AMPK signaling by high glucose via E3 ubiquitin ligase MG53. Mol Cell 81 629–637.e5. (https://doi.org/10.1016/j.molcel.2020.12.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kendig MD 2014 Cognitive and behavioural effects of sugar consumption in rodents. A review. Appetite 80 41–54. (https://doi.org/10.1016/j.appet.2014.04.028)

  • Kinote A, Faria JA, Roman EA, et al. 2012 Fructose-induced hypothalamic AMPK activation stimulates hepatic PEPCK and gluconeogenesis due to increased corticosterone levels. Endocrinology 153 3633–3645. (https://doi.org/10.1210/en.2012-1341)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Klein-Flügge MC, Bongioanni A & Rushworth MFS 2022 Medial and orbital frontal cortex in decision-making and flexible behavior. Neuron 110 2743–2770. (https://doi.org/10.1016/j.neuron.2022.05.022)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kritzer MF 2003 Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-beta-hydroxylase-choline acetyltransferase- or serotonin-immunoreactive axons in the medial prefrontal cortices of adult male rats. Cereb Cortex 13 282–296. (https://doi.org/10.1093/cercor/13.3.282)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kubzansky LD & Adler GK 2010 Aldosterone: a forgotten mediator of the relationship between psychological stress and heart disease. Neurosci Biobehav Rev 34 80–86. (https://doi.org/10.1016/j.neubiorev.2009.07.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kumar S, Gordon GH, Abbott DH, et al. 2018 Androgens in maternal vascular and placental function: implications for preeclampsia pathogenesis. Reproduction 156 R155–R167. (https://doi.org/10.1530/REP-18-0278)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Legeza B, Marcolongo P, Gamberucci A, et al. 2017 Fructose, glucocorticoids and adipose tissue: implications for the metabolic syndrome. Nutrients 9 426. (https://doi.org/10.3390/nu9050426)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lien EL, Boyle FG, Wrenn JM, et al. 2001 Comparison of AIN-76A and AIN-93G diets: a 13-week study in rats. Food Chem Toxicol 39 385–392. (https://doi.org/10.1016/S0278-6915(00)00142-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • MacKenzie SM, Clark CJ, Fraser R, et al. 2000 Expression of 11beta-hydroxylase and aldosterone synthase genes in the rat brain. J Mol Endocrinol 24 321–328. (https://doi.org/10.1677/jme.0.0240321)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • MacKenzie SM, Lai M, Clark CJ, et al. 2002 11beta-hydroxylase and aldosterone synthase expression in fetal rat hippocampal neurons. J Mol Endocrinol 29 319–325. (https://doi.org/10.1677/jme.0.0290319)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mairesse J, Lesage J, Breton C, et al. 2007 Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab 292 E1526–E1533. (https://doi.org/10.1152/ajpendo.00574.2006.2006)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Martin CE, Cake MH, Hartmann PE, et al. 1977 Relationship between foetal corticosteroids, maternal progesterone and parturition in the rat. Acta Endocrinol 84 167–176. (https://doi.org/10.1530/acta.0.0840167)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matt DW & MacDonald GJ 1984 In vitro progesterone and testosterone production by the rat placenta during pregnancy. Endocrinology 115 741–747. (https://doi.org/10.1210/endo-115-2-741)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matt DW & MacDonald GJ 1985 Placental steroid production by the basal and labyrinth zones during the latter third of gestation in the rat. Biol Reprod 32 969–977. (https://doi.org/10.1095/biolreprod32.4.969)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mizera J, Kazek G, Niedzielska‐Andres E, et al. 2021 Maternal high‐sugar diet results in NMDA receptors abnormalities and cognitive impairment in rat offspring. FASEB J 35 e21547. (https://doi.org/10.1096/fj.202002691R)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mosili P, Mkhize BC, Ngubane P, et al. 2020 The dysregulation of the hypothalamic–pituitary–adrenal axis in diet-induced prediabetic male Sprague Dawley rats. Nutr Metab 17 104. (https://doi.org/10.1186/s12986-020-00532-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Munetsuna E, Yamada H, Yamazaki M, et al. 2019 Maternal high-fructose intake increases circulating corticosterone levels via decreased adrenal corticosterone clearance in adult offspring. J Nutr Biochem 67 44–50. (https://doi.org/10.1016/j.jnutbio.2019.01.016)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Murck H, Lehr L & Jezova D 2023 A viewpoint on aldosterone and BMI related brain morphology in relation to treatment outcome in patients with major depression. J Neuroendocrinol 35 e13219. (https://doi.org/10.1111/jne.13219)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nader N, Ng SSM, Lambrou GI, et al. 2010 AMPK regulates metabolic actions of glucocorticoids by phosphorylating the glucocorticoid receptor through p38 MAPK. Mol Endocrinol 24 1748–1764. (https://doi.org/10.1210/me.2010-0192)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Naef L, Srivastava L, Gratton A, et al. 2008 Maternal high fat diet during the perinatal period alters mesocorticolimbic dopamine in the adult rat offspring: reduction in the behavioral responses to repeated amphetamine administration. Psychopharmacology 197 83–94. (https://doi.org/10.1007/s00213-007-1008-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Newens KJ & Walton J 2016 A review of sugar consumption from nationally representative dietary surveys across the world. J Hum Nutr Diet 29 225–240. (https://doi.org/10.1111/jhn.12338)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nouchi Y, Munetsuna E, Yamada H, et al. 2023 Maternal high-fructose corn syrup intake impairs corticosterone clearance by reducing renal 11β-hsd2 activity via miR-27a-mediated mechanism in rat offspring. Nutrients 15 2122. (https://doi.org/10.3390/nu15092122)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Palkovits M 1973 Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59 449–450. (https://doi.org/10.1016/0006-8993(73)90290-4)

  • Parsons AM & Bouma GJ 2021 A potential role and contribution of androgens in placental development and pregnancy. Life 11 644. (https://doi.org/10.3390/life11070644)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Price HR, Jalabert C, Seib DR, et al. 2023 Measurement of steroids in the placenta, maternal serum, and fetal serum in humans, rats, and mice: a technical note. Separations 10 221. (https://doi.org/10.3390/separations10040221)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Reeves PG 1997 Components of the AIN-93 diets as improvements in the AIN-76a diet. J Nutr 127 838S–841S. (https://doi.org/10.1093/jn/127.5.838S)

  • Reichelt AC, Gibson GD, Abbott KN, et al. 2019 A high-fat high-sugar diet in adolescent rats impairs social memory and alters chemical markers characteristic of atypical neuroplasticity and parvalbumin interneuron depletion in the medial prefrontal cortex. Food Funct 10 1985–1998. (https://doi.org/10.1039/C8FO02118J)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ricciuto L, Fulgoni VL, Gaine PC, et al. 2021 Sources of added sugars intake among the U.S. population: analysis by selected sociodemographic factors using the national health and nutrition examination survey 2011–18. Front Nutr 8 687643. (https://doi.org/10.3389/fnut.2021.687643)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ruff JS, Suchy AK, Hugentobler SA, et al. 2013 Human-relevant levels of added sugar consumption increase female mortality and lower male fitness in mice. Nat Commun 4 2245. (https://doi.org/10.1038/ncomms3245)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Salehzadeh M, Hamden JE, Li MX, et al. 2022 Glucocorticoid production in lymphoid organs: acute effects of lipopolysaccharide in neonatal and adult mice. Endocrinology 163 bqab244. (https://doi.org/10.1210/endocr/bqab244)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schmidt MV 2019 Stress-hyporesponsive period. In Stress: Physiology, Biochemistry, and Pathology, pp 49–56. Elsevier. (https://doi.org/10.1016/B978-0-12-813146-6.00004-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Seib DR, Tobiansky DJ, Meitzen J, et al. 2023 Neurosteroids and the mesocorticolimbic system. Neurosci Biobehav Rev 153 105356. (https://doi.org/10.1016/j.neubiorev.2023.105356)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Smith SM & Vale WW. 2006 The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 8 383–395. (https://doi.org/10.31887/DCNS.2006.8.4/ssmith)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stanhope KL 2016 Sugar consumption, metabolic disease and obesity: the state of the controversy. Crit Rev Clin Lab Sci 53 52–67. (https://doi.org/10.3109/10408363.2015.1084990)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sullivan RM & Gratton A 2002 Prefrontal cortical regulation of hypothalamic–pituitary–adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 27 99–114. (https://doi.org/10.1016/S0306-4530(01)00038-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Taves MD, Ma C, Heimovics SA, et al. 2011 Measurement of steroid concentrations in brain tissue: methodological considerations. Front Endocrinol 2 39. (https://doi.org/10.3389/fendo.2011.00039)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Taves MD, Plumb AW, Sandkam BA, et al. 2015 Steroid profiling reveals widespread local regulation of glucocorticoid levels during mouse development. Endocrinology 156 511–522. (https://doi.org/10.1210/en.2013-1606)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tobiansky DJ, Korol AM, Ma C, et al. 2018 Testosterone and corticosterone in the mesocorticolimbic system of male rats: effects of gonadectomy and caloric restriction. Endocrinology 159 450–464. (https://doi.org/10.1210/en.2017-00704)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tobiansky DJ, Kachkovski GV, Enos RT, et al. 2020 Sucrose consumption alters steroid and dopamine signalling in the female rat brain. J Endocrinol 245 231–246. (https://doi.org/10.1530/JOE-19-0386)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tobiansky DJ, Kachkovski GV, Enos RT, et al. 2021 Maternal sucrose consumption alters behaviour and steroids in adult rat offspring. J Endocrinol 251 161–180. (https://doi.org/10.1530/JOE-21-0166)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tomm RJ, Seib DR, Kachkovski GV, et al. 2022 Androgen synthesis inhibition increases behavioural flexibility and mPFC tyrosine hydroxylase in gonadectomized male rats. J Neuroendocrinol 34 e13128. (https://doi.org/10.1111/jne.13128)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tsuneoka Y & Funato H 2021 Cellular composition of the preoptic area regulating sleep, parental, and sexual behavior. Front Neurosci 15 649159. (https://doi.org/10.3389/fnins.2021.649159)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vacher C-M, Lacaille H, O’Reilly JJ, et al. 2021 Placental endocrine function shapes cerebellar development and social behavior. Nat Neurosci 24 1392–1401. (https://doi.org/10.1038/s41593-021-00896-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vagnerová K, Jágr M, Mekadim C, et al. 2023 Profiling of adrenal corticosteroids in blood and local tissues of mice during chronic stress. Sci Rep 13 7278. (https://doi.org/10.1038/s41598-023-34395-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Varga J, Ferenczi S, Kovács KJ, et al. 2013 Comparison of stress-induced changes in adults and pups: is aldosterone the main adrenocortical stress hormone during the perinatal period in rats? PLoS One 8 e72313. (https://doi.org/10.1371/journal.pone.0072313)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Viau V & Meaney M 1996 The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci 16 1866–1876. (https://doi.org/10.1523/JNEUROSCI.16-05-01866.1996)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vickers MH, Clayton ZE, Yap C, et al. 2011 Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology 152 1378–1387. (https://doi.org/10.1210/en.2010-1093)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Villee DB 1979 Endocrine functions of the placenta. In Placenta, pp 74–83. Elsevier. (https://doi.org/10.1016/B978-0-08-024435-8.50014-6)

  • Vucetic Z, Kimmel J, Totoki K, et al. 2010 Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151 4756–4764. (https://doi.org/10.1210/en.2010-0505)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wallin-Miller K, Li G, Kelishani D, et al. 2016 Anabolic-androgenic steroids decrease dendritic spine density in the nucleus accumbens of male rats. Neuroscience 330 72–78. (https://doi.org/10.1016/j.neuroscience.2016.05.045)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ward IL, Ward OB, Affuso JD, et al. 2003 Fetal testosterone surge: specific modulations induced in male rats by maternal stress and/or alcohol consumption. Horm Behav 43 531–539. (https://doi.org/10.1016/S0018-506X(03)00061-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wei R, Wang J, Jia E, et al. 2018a GSimp: a Gibbs sampler based left-censored missing value imputation approach for metabolomics studies. PLoS Comput Biol 14 e1005973. (https://doi.org/10.1371/journal.pcbi.1005973)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wei R, Wang J, Su M, et al. 2018b Missing value imputation approach for mass spectrometry-based metabolomics data. Sci Rep 8 663. (https://doi.org/10.1038/s41598-017-19120-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wiss DA, Criscitelli K, Gold M, et al. 2017 Preclinical evidence for the addiction potential of highly palatable foods: current developments related to maternal influence. Appetite 115 19–27. (https://doi.org/10.1016/j.appet.2016.12.019)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wong A, Dogra VR & Reichelt AC 2017 High-sucrose diets in male rats disrupt aspects of decision making tasks, motivation and spatial memory, but not impulsivity measured by operant delay-discounting. Behav Brain Res 327 144–154. (https://doi.org/10.1016/j.bbr.2017.03.029)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wotus C, Levay-Young BK, Rogers LM, et al. 1998 Development of adrenal zonation in fetal rats defined by expression of aldosterone synthase and 11β-hydroxylase. Endocrinology 139 4397–4403. (https://doi.org/10.1210/endo.139.10.6230)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yamazaki M, Yamada H, Munetsuna E, et al. 2018 Excess maternal fructose consumption impairs hippocampal function in offspring via epigenetic modification of BDNF promoter. FASEB J 32 2549–2562. (https://doi.org/10.1096/fj.201700783RR)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yuan S-Y, Liu J, Zhou J, et al. 2016 AMPK mediates glucocorticoids stress-induced downregulation of the glucocorticoid receptor in cultured rat prefrontal cortical astrocytes. PLoS One 11 e0159513. (https://doi.org/10.1371/journal.pone.0159513)

    • PubMed
    • Search Google Scholar
    • Export Citation