nach oben

14.05.2024 | Original Contribution

Effects of chronic exposure to a high fat diet, nutritive or non-nutritive sweeteners on hypothalamic-pituitary-adrenal (HPA) and -gonadal (HPG) axes of male Sprague-Dawley rats

verfasst von: Yiyuan Zhang, Chunyun Luo, Puxin Huang, Lu Chen, Yufang Ma, Hong Ding

Erschienen in: European Journal of Nutrition

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Diet-related factors are of great significance in the regulation of hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonad (HPG) axes. In this study, we aimed to investigate the effects of chronic exposure to a high fat diet (HFD), fructose or sucralose on the endocrine functions.

Methods

Male, Sprague-Dawley rats received a normal chow diet, HFD, 10% fructose or 0.02% sucralose for 10 weeks. Behavioral changes were assessed by open field (OFT) and elevated plus-maze (EPM) tests at week 8. H&E staining was used to observe pathological changes in adrenal cortex, testis and perirenal adipose tissue. Serum hormone concentrations were quantified via enzyme-linked immunosorbent assay (ELISA). The mRNA expression levels of genes along the HPA and HPG axes were determined using real-time PCR.

Results

All types of dietary interventions increased body weight and disturbed metabolic homeostasis, with anxiogenic phenotype in behavioral tests and damage to cell morphology of adrenal cortex and testis being observed. Along the HPA axis, significantly increased corticotropin releasing hormone (CRH), adrenocorticotropic hormone (ACTH) and corticosterone (CORT) concentrations were observed in the HFD or 0.02% sucralose group. For HPG axis, gonadotropin-releasing hormone (GnRH) and estradiol (E2) concentrations were significantly increased in all dietary intervention groups, while decreased concentrations of follicle-stimulating hormone (FSH) and testosterone (T) were also detected. Moreover, transcriptional profiles of genes involved in the synthesis of hormones and corresponding hormone receptors were significantly altered.

Conclusion

Long-term consumption of HFD, fructose or sucralose manifested deleterious effects on endocrine system and resulted in the dysregulation of HPA and HPG axes.

Nur mit Berechtigung zugänglich

Whittaker J (2023) Dietary trends and the decline in male reproductive health. Horm (Athens) 22:165–197. https://doi.org/10.1007/s42000-023-00431-zCrossRef

Lian CY, Zhai ZZ, Li ZF et al (2020) High fat diet-triggered non-alcoholic fatty liver disease: a review of proposed mechanisms. Chem Biol Interact 330:109199. https://doi.org/10.1016/j.cbi.2020.109199CrossRefPubMed

Moszak M, Szulinska M, Bogdanski P (2020) You are what you eat-the relationship between diet, microbiota, and metabolic disorders-a review. Nutrients 12. https://doi.org/10.3390/nu12041096

Wu T, Liu R, Zhang L et al (2022) Dietary intervention in depression - a review. Food Funct 13:12475–12486. https://doi.org/10.1039/d2fo02795jCrossRefPubMed

Varlamov O (2017) Western-style diet, sex steroids and metabolism. Biochim Biophys Acta Mol Basis Dis 1863:1147–1155. https://doi.org/10.1016/j.bbadis.2016.05.025CrossRefPubMed

Skoracka K, Eder P, Lykowska-Szuber L et al (2020) Diet and nutritional factors in male (in)fertility-underestimated factors. J Clin Med 9. https://doi.org/10.3390/jcm9051400

Neumann AM, Schmidt CX, Brockmann RM et al (2019) Circadian regulation of endocrine systems. Auton Neurosci 216:1–8. https://doi.org/10.1016/j.autneu.2018.10.001CrossRefPubMed

Feldt-Rasmussen U, Effraimidis G, Klose M (2021) The hypothalamus-pituitary-thyroid (hpt)-axis and its role in physiology and pathophysiology of other hypothalamus-pituitary functions. Mol Cell Endocrinol 525:111173. https://doi.org/10.1016/j.mce.2021.111173CrossRefPubMed

Hao S, Yang Y, Helmy M et al (2020) Neural regulation of feeding behavior. Adv Exp Med Biol 1284:23–33. https://doi.org/10.1007/978-981-15-7086-5_3CrossRefPubMed

10.

Asa SL, Ezzat S (2021) Hypothalamic hormone-producing tumors. Handb Clin Neurol 181:67–74. https://doi.org/10.1016/B978-0-12-820683-6.00006-3CrossRefPubMed

11.

Laporte E, Vankelecom H (2023) Organoid models of the pituitary gland in health and disease. Front Endocrinol (Lausanne) 14:1233714. https://doi.org/10.3389/fendo.2023.1233714CrossRefPubMed

12.

Dwyer JB, Aftab A, Radhakrishnan R et al (2020) Hormonal treatments for major depressive disorder: state of the art. Am J Psychiatry 177:686–705. https://doi.org/10.1176/appi.ajp.2020.19080848CrossRefPubMedPubMedCentral

13.

Acevedo-Rodriguez A, Kauffman AS, Cherrington BD et al (2018) Emerging insights into hypothalamic-pituitary-gonadal axis regulation and interaction with stress signalling. J Neuroendocrinol 30:11. https://doi.org/10.1111/jne.12590CrossRef

14.

Bruggemann M, Licht O, Fetter E et al (2018) Knotting nets: molecular junctions of interconnecting endocrine axes identified by application of the adverse outcome pathway concept. Environ Toxicol Chem 37:318–328. https://doi.org/10.1002/etc.3995CrossRefPubMed

15.

Chen L, Shi T, Wang YT et al (2021) Effects of acute exposure to microcystins on hypothalamic-pituitary-adrenal (hpa), -gonad (hpg) and -thyroid (hpt) axes of female rats. Sci Total Environ 778:145196. https://doi.org/10.1016/j.scitotenv.2021.145196CrossRefPubMed

16.

Boitard C, Parkes SL, Cavaroc A et al (2016) Switching adolescent high-fat diet to adult control diet restores neurocognitive alterations. Front Behav Neurosci 10:225. https://doi.org/10.3389/fnbeh.2016.00225CrossRefPubMedPubMedCentral

17.

Xu R, Feng J, Liang C et al (2022) Effects of high-fat diet and treadmill running on the hypothalamic kiss-1-gpr54 signaling pathway in male growing rats. Horm (Athens) 21:641–652. https://doi.org/10.1007/s42000-022-00389-4CrossRef

18.

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 (Lond) 17:104. https://doi.org/10.1186/s12986-020-00532-1CrossRefPubMed

19.

Lie ME, Overgaard A, Mikkelsen JD (2013) Effect of a postnatal high-fat diet exposure on puberty onset, estrous cycle regularity, and kisspeptin expression in female rats. Reprod Biol 13:298–308. https://doi.org/10.1016/j.repbio.2013.08.001CrossRefPubMed

20.

Liu L, Yang J, Qian F et al (2017) Hypothalamic-pituitary-adrenal axis hypersensitivity in female rats on a post-weaning high-fat diet after chronic mild stress. Exp Ther Med 14:439–446. https://doi.org/10.3892/etm.2017.4498CrossRefPubMedPubMedCentral

21.

Harrell CS, Burgado J, Kelly SD et al (2015) High-fructose diet during periadolescent development increases depressive-like behavior and remodels the hypothalamic transcriptome in male rats. Psychoneuroendocrinology 62:252–264. https://doi.org/10.1016/j.psyneuen.2015.08.025CrossRefPubMedPubMedCentral

22.

Hsia SM, Chiang YF, Chen HY et al (2022) Effect of high-fructose diet-induced metabolic syndrome on the pituitary-gonadal axis in male rats. Biomedicines 10. https://doi.org/10.3390/biomedicines10123009

23.

Jung S, Bae H, Song WS et al (2022) Dietary fructose and fructose-induced pathologies. Annu Rev Nutr 42:45–66. https://doi.org/10.1146/annurev-nutr-062220-025831CrossRefPubMedPubMedCentral

24.

Wu L, Zhang C, Long Y et al (2022) Food additives: from functions to analytical methods. Crit Rev Food Sci Nutr 62:8497–8517. https://doi.org/10.1080/10408398.2021.1929823CrossRefPubMed

25.

Risdon S, Battault S, Romo-Romo A et al (2021) Sucralose and cardiometabolic health: current understanding from receptors to clinical investigations. Adv Nutr 12:1500–1513. https://doi.org/10.1093/advances/nmaa185CrossRefPubMedPubMedCentral

26.

Walbolt J, Koh Y (2020) Non-nutritive sweeteners and their associations with obesity and type 2 diabetes. J Obes Metab Syndr 29:114–123. https://doi.org/10.7570/jomes19079CrossRefPubMedPubMedCentral

27.

Zhang Y, Chen L, Gao J et al (2023) Nutritive/non-nutritive sweeteners and high fat diet contribute to dysregulation of sweet taste receptors and metabolic derangements in oral, intestinal and central nervous tissues. Eur J Nutr 62:3149–3159. https://doi.org/10.1007/s00394-023-03187-9CrossRefPubMed

28.

Tang M, Liu Y, Wang L et al (2018) An omega-3 fatty acid-deficient diet during gestation induces depressive-like behavior in rats: the role of the hypothalamo-pituitary-adrenal (hpa) system. Food Funct 9:3481–3488. https://doi.org/10.1039/c7fo01714fCrossRefPubMed

29.

Raymond J, Morin A, Plamondon H (2022) Delivery method matters: omega-3 supplementation by restricted feeding period and oral gavage has a distinct impact on corticosterone secretion and anxious behavior in adolescent rats. Nutr Neurosci 25:11. https://doi.org/10.1080/1028415X.2020.1733813CrossRef

30.

Pentkowski NS, Rogge-Obando KK, Donaldson TN et al (2021) Anxiety and alzheimer’s disease: behavioral analysis and neural basis in rodent models of Alzheimer’s-related neuropathology. Neurosci Biobehav Rev 127:647–658. https://doi.org/10.1016/j.neubiorev.2021.05.005CrossRefPubMedPubMedCentral

31.

Roerink S, Wagenmakers M, Langenhuijsen JF et al (2017) Increased adipocyte size, macrophage infiltration, and adverse local adipokine profile in perirenal fat in cushing’s syndrome. Obes (Silver Spring) 25:1369–1374. https://doi.org/10.1002/oby.21887CrossRef

32.

Thaler JP, Yi CX, Schur EA et al (2012) Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 122:153–162. https://doi.org/10.1172/JCI59660CrossRefPubMed

33.

Seong J, Kang JY, Sun JS et al (2019) Hypothalamic inflammation and obesity: a mechanistic review. Arch Pharm Res 42:383–392. https://doi.org/10.1007/s12272-019-01138-9CrossRefPubMed

34.

Wang X, Younis S, Cen J et al (2021) Zbed6 counteracts high-fat diet-induced glucose intolerance by maintaining beta cell area and reducing excess mitochondrial activation. Diabetologia 64:2292–2305. https://doi.org/10.1007/s00125-021-05517-0CrossRefPubMedPubMedCentral

35.

Gu L, Ding X, Wang Y et al (2019) Spexin alleviates insulin resistance and inhibits hepatic gluconeogenesis via the foxo1/pgc-1alpha pathway in high-fat-diet-induced rats and insulin resistant cells. Int J Biol Sci 15:2815–2829. https://doi.org/10.7150/ijbs.31781CrossRefPubMedPubMedCentral

36.

Joung H, Chu J, Kim BK et al (2021) Probiotics ameliorate chronic low-grade inflammation and fat accumulation with gut microbiota composition change in diet-induced obese mice models. Appl Microbiol Biotechnol 105:1203–1213. https://doi.org/10.1007/s00253-020-11060-6CrossRefPubMed

37.

Eng JM, Estall JL (2021) Diet-induced models of non-alcoholic fatty liver disease: food for thought on sugar, fat, and cholesterol. Cells 10. https://doi.org/10.3390/cells10071805

38.

Bornemann V, Werness SC, Buslinger L et al (2018) Intestinal metabolism and bioaccumulation of sucralose in adipose tissue in the rat. J Toxicol Environ Health A 81:913–923. https://doi.org/10.1080/15287394.2018.1502560CrossRefPubMed

39.

Wu X, Cui L, Wang H et al (2023) Impact of dietary sucralose and sucrose-sweetened water intake on lipid and glucose metabolism in male mice. Eur J Nutr 62:199–211. https://doi.org/10.1007/s00394-022-02980-2CrossRefPubMed

40.

Shi Q, Zhu X, Deng S (2021) Sweet taste receptor expression and its activation by sucralose to regulate glucose absorption in mouse duodenum. J Food Sci 86:540–545. https://doi.org/10.1111/1750-3841.14586CrossRefPubMed

41.

Lin HQ, Wu JY, Chen ML et al (2019) Prevalence of dyslipidemia and prediction of 10-year cvd risk among older adults living in southeast coastal regions in China: a cross-sectional study. Clin Interv Aging 14

42.

Berman AN, Blankstein R (2019) Optimizing dyslipidemia management for the prevention of cardiovascular disease: a focus on risk assessment and therapeutic options. Curr Cardiol Rep 21:110. https://doi.org/10.1007/s11886-019-1175-zCrossRefPubMed

43.

Tsigos C, Kyrou I, Kassi E et al (2000) Stress: endocrine physiology and pathophysiology

44.

Leistner C, Menke A (2020) Hypothalamic-pituitary-adrenal axis and stress. Handb Clin Neurol 175:55–64. https://doi.org/10.1016/B978-0-444-64123-6.00004-7CrossRefPubMed

45.

Packard AE, Egan AE, Ulrich-Lai YM (2016) Hpa axis interactions with behavioral systems. Compr Physiol 6:1897–1934. https://doi.org/10.1002/cphy.c150042CrossRefPubMedPubMedCentral

46.

Sasaki A, de Vega WC, St-Cyr S et al (2013) Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience 240:1–12. https://doi.org/10.1016/j.neuroscience.2013.02.044CrossRefPubMed

47.

Shin AC, Balasubramanian P, Suryadevara P et al (2021) Metformin effectively restores the hpa axis function in diet-induced obese rats. Int J Obes (Lond) 45:383–395. https://doi.org/10.1038/s41366-020-00688-zCrossRefPubMed

48.

Abreu AP, Kaiser UB (2016) Pubertal development and regulation. Lancet Diabetes Endocrinol 4:254–264. https://doi.org/10.1016/S2213-8587(15)00418-0CrossRefPubMedPubMedCentral

49.

de Oliveira JC, de Moura EG, Miranda RA et al (2018) Low-protein diet in puberty impairs testosterone output and energy metabolism in male rats. J Endocrinol 237:243–254. https://doi.org/10.1530/JOE-17-0606CrossRefPubMed

50.

Teerds KJ, de Rooij DG, Keijer J (2011) Functional relationship between obesity and male reproduction: from humans to animal models. Hum Reprod Update 17:667–683. https://doi.org/10.1093/humupd/dmr017CrossRefPubMed

51.

Uenoyama Y, Inoue N, Nakamura S et al (2019) Central mechanism controlling pubertal onset in mammals: a triggering role of kisspeptin. Front Endocrinol (Lausanne) 10:312. https://doi.org/10.3389/fendo.2019.00312CrossRefPubMed

52.

Sanchez-Garrido MA, Ruiz-Pino F, Manfredi-Lozano M et al (2014) Obesity-induced hypogonadism in the male: premature reproductive neuroendocrine senescence and contribution of kiss1-mediated mechanisms. Endocrinology 155:1067–1079. https://doi.org/10.1210/en.2013-1584CrossRefPubMed

53.

Wang W, Mu Q, Feng X et al (2023) Sweet taste receptor t1r3 expressed in leydig cells is closely related to homeostasis of the steroid hormone metabolism profile. J Agric Food Chem 71:7791–7802. https://doi.org/10.1021/acs.jafc.3c01110CrossRefPubMed

54.

Ngekure MXK, Jiang J, Enayatullah H et al (2019) Sweet taste receptor agonists alter ovarian functions and ovarian cycles in aged mice. Reprod Biol 19:230–236. https://doi.org/10.1016/j.repbio.2019.07.007CrossRef

55.

Gong T, Wei QW, Mao DG et al (2016) Effects of daily exposure to saccharin and sucrose on testicular biologic functions in mice. Biol Reprod 95:116. https://doi.org/10.1095/biolreprod.116.140889CrossRefPubMed

Titel: Effects of chronic exposure to a high fat diet, nutritive or non-nutritive sweeteners on hypothalamic-pituitary-adrenal (HPA) and -gonadal (HPG) axes of male Sprague-Dawley rats
verfasst von: Yiyuan Zhang
Chunyun Luo
Puxin Huang
Lu Chen
Yufang Ma
Hong Ding
Publikationsdatum: 14.05.2024
Verlag: Springer Berlin Heidelberg
Erschienen in: European Journal of Nutrition
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-024-03427-6

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Effects of chronic exposure to a high fat diet, nutritive or non-nutritive sweeteners on hypothalamic-pituitary-adrenal (HPA) and -gonadal (HPG) axes of male Sprague-Dawley rats

Abstract

Purpose

Methods

Results

Conclusion

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Ist Fasten vor Koronarinterventionen wirklich nötig?

Typ-2-Diabetes: Ernährungsunsicherheit vervierfacht Risiko für schwere Hypoglykämien

Mehr Brustkrebs, aber weniger andere gynäkologische Tumoren mit Levonorgestrel-IUS

GLP-1-Agonist Semaglutid wirkt kardio- und nephroprotektiv

Update Innere Medizin

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Abstract

Purpose

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Ist Fasten vor Koronarinterventionen wirklich nötig?

Typ-2-Diabetes: Ernährungsunsicherheit vervierfacht Risiko für schwere Hypoglykämien

Mehr Brustkrebs, aber weniger andere gynäkologische Tumoren mit Levonorgestrel-IUS

GLP-1-Agonist Semaglutid wirkt kardio- und nephroprotektiv

Update Innere Medizin