The effects of forced exercise and zinc supplementation during pregnancy on prenatally stress-induced behavioral and neurobiological consequences in adolescent female rat offspring.


Journal

Developmental psychobiology
ISSN: 1098-2302
Titre abrégé: Dev Psychobiol
Pays: United States
ID NLM: 0164074

Informations de publication

Date de publication:
09 2023
Historique:
revised: 10 04 2023
received: 09 04 2022
accepted: 23 06 2023
medline: 24 8 2023
pubmed: 23 8 2023
entrez: 22 8 2023
Statut: ppublish

Résumé

Prenatal manipulations can lead to neurobehavioral changes in the offspring. In this study, individual and combined effects of forced exercise and zinc supplementation during pregnancy on prenatally restraint stress (PRS)-induced behavioral impairments, neuro-inflammatory responses, and oxidative stress have been investigated in adolescent female rat offspring. Pregnant rats were divided into five groups: control; restraint stress (RS); RS + exercise stress (RS + ES), RS + zinc supplementation (RS + Zn); and RS + ES + Zn. All the pregnant rats (except control) were exposed to RS from gestational days 15 to 19. Pregnant rats in ES groups were subjected to forced treadmill exercise (30 min/daily), and in Zn groups to zinc sulfate (30 mg/kg/orally), throughout the pregnancy. At postnatal days 25-27, anxiety-like and stress-coping behaviors were recorded, and the gene expressions of interleukin-1β (IL-1β) and tumor necrosis factor-α (TNF-α) and the concentration of total antioxidant capacity were measured in the prefrontal cortex. PRS significantly enhanced anxiety, generated passive coping behaviors, increased IL-1β and TNF-α expression, and decreased the antioxidant capacity. ES potentiated while zinc reversed PRS-induced behavioral impairments. Prenatal zinc also restored the anti-inflammatory and antioxidant capacity but had no effect on additive responses imposed by the combination of RS and ES. Suppression of PRS-induced behavioral and neurobiological impairments by zinc suggests the probable clinical importance of zinc on PRS-induced changes on child temperament.

Identifiants

pubmed: 37607889
doi: 10.1002/dev.22411
doi:

Substances chimiques

Zinc J41CSQ7QDS
Antioxidants 0
Tumor Necrosis Factor-alpha 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e22411

Informations de copyright

© 2023 Wiley Periodicals LLC.

Références

Ahmadzadeh, R., Saboory, E., Roshan-Milani, S., & Pilehvarian, A. A. (2011). Predator and restraint stress during gestation facilitates pilocarpine-induced seizures in prepubertal rats. Developmental Psychobiology, 53(8), 806-812.
Alizadeh, F., Davoodian, N., Kazemi, H., Ghasemi-Kasman, M., & Shaerzadeh, F. (2020). Prenatal zinc supplementation attenuates lipopolysaccharide-induced behavioral impairments in maternal immune activation model. Behavioural Brain Research, 377, 112247.
Asami, T., Yamasue, H., Hayano, F., Nakamura, M., Uehara, K., Otsuka, T., Roppongi, T., Nihashi, N., Inoue, T., & Hirayasu, Y. (2009). Sexually dimorphic gray matter volume reduction in patients with panic disorder. Psychiatry Research, 173(2), 128-134.
Azizi, N., Roshan-Milani, S., MahmoodKhani, M., Saboory, E., Gholinejad, Z., Abdollahzadeh, N., Sayyadi, H., & Chodari, L. (2019). Parental pre-conception stress status and risk for anxiety in rat offspring: Specific and sex-dependent maternal and paternal effects. Stress (Amsterdam, Netherlands), 22(5), 619-631.
Bagheri, M., Saboory, E., Nejatbakhsh, M., Roshan-Milani, S., Derafshpour, L., Sayyadi, H., & Rasmi, Y. (2020). Prenatal stress increased γ2 GABAA receptor subunit gene expression in hippocampus and potentiated pentylenetetrazol-induced seizure in rats. Iranian Journal of Basic Medical Sciences, 23(6), 724-729.
Bernhardt, L. K., Madhyastha, S., Bairy, L., & Kishore, A. (2017). Status of the brain antioxidant system at different growing periods after prenatal stress and N-acetyl cysteine administration. Folia Neuropathologica, 55(1), 38-48.
Boersma, G. J., Liang, N. C., Lee, R. S., Albertz, J. D., Kastelein, A., Moody, L. A., Aryal, S., Moran, T. H., & Tamashiro, K. L. (2016). Failure to upregulate Agrp and Orexin in response to activity based anorexia in weight loss vulnerable rats characterized by passive stress coping and prenatal stress experience. Psychoneuroendocrinology, 67, 171-181.
Brocardo, P. S., Boehme, F., Patten, A., Cox, A., Gil-Mohapel, J., & Christie, B. R. (2012). Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: Protective effects of voluntary physical exercise. Neuropharmacology, 62(4), 1607-1618.
Calcia, M. A., Bonsall, D. R., Bloomfield, P. S., Selvaraj, S., Barichello, T., & Howes, O. D. (2016). Stress and neuroinflammation: A systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology, 233(9), 1637-1650.
Cao, K., Zheng, A., Xu, J., Li, H., Liu, J., Peng, Y., Long, J., Zou, X., Li, Y., Chen, C., Liu, J., & Feng, Z. (2014). AMPK activation prevents prenatal stress-induced cognitive impairment: Modulation of mitochondrial content and oxidative stress. Free Radical Biology & Medicine, 75, 156-166.
Carey, L. C., Berbée, P. L., Coyle, P., Philcox, J. C., & Rofe, A. M. (2003). Zinc treatment prevents lipopolysaccharide-induced teratogenicity in mice. Birth Defects Research. Part A, Clinical and Molecular Teratology, 67(4), 240-245.
Cechetti, F., Worm, P. V., Elsner, V. R., Bertoldi, K., Sanches, E., Ben, J., Siqueira, I. R., & Netto, C. (2012). A Forced treadmill exercise prevents oxidative stress and memory deficits following chronic cerebral hypoperfusion in the rat. Neurobiology of Learning and Memory, 97(1), 90-96.
Cerqueira, É., Marinho, D. A., Neiva, H. P., & Lourenço, O. (2019). Inflammatory effects of high and moderate intensity exercise-A systematic review. Frontiers in Physiology, 10, 1550.
Chen, M. X., Liu, Q., Cheng, S., Lei, L., Lin, A. J., Wei, R., Hui, T. C. K., Li, Q., Ao, L. J., & Sham, P. C. (2020). Interleukin-18 levels in the hippocampus and behavior of adult rat offspring exposed to prenatal restraint stress during early and late pregnancy. Neural Regeneration Research, 15(9), 1748-1756.
Chen, Y. H., Zhao, M., Chen, X., Zhang, Y., Wang, H., Huang, Y. Y., Wang, Z., Zhang, Z. H., Zhang, C., & Xu, D. X. (2012). Zinc supplementation during pregnancy protects against lipopolysaccharide-induced fetal growth restriction and demise through its anti-inflammatory effect. Journal of Immunology, 189(1), 454-463.
Chua, J. S., Cowley, C. J., Manavis, J., Rofe, A. M., & Coyle, P. (2012). Prenatal exposure to lipopolysaccharide results in neurodevelopmental damage that is ameliorated by zinc in mice. Brain, Behavior, and Immunity, 26(2), 326-336.
Coyle, P., Tran, N., Fung, J. N., Summers, B. L., & Rofe, A. M. (2009). Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy. Behavioural Brain Research, 197(1), 210-218.
Darnaudéry, M., & Maccari, S. (2008). Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Research Reviews, 57(2), 571-585.
da Rocha, A. L., Pinto, A. P., Kohama, E. B., Pauli, J. R., de Moura, L. P., Cintra, D. E., Ropelle, E. R., & da Silva, A. S. R. (2019). The proinflammatory effects of chronic excessive exercise. Cytokine, 119, 57-61.
Davis, E. P., & Sandman, C. A. (2012). Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology, 37(8), 1224-1233.
de Barcellos, L. A. M., Gonçalves, W. A., Esteves de Oliveira, M. P., Guimarães, J. B., Queiroz-Junior, C. M., de Resende, C. B., Russo, R. C., Coimbra, C. C., Silva, A. N., Teixeira, M. M., Rezende, B. M., & Pinho, V. (2021). Effect of physical training on exercise-induced inflammation and performance in mice. Frontiers in Cell and Developmental Biology, 9, 625680.
de Kloet, E. R., & Molendijk, M. L. (2016). Coping with the forced swim stressor: Towards understanding an adaptive mechanism. Neural Plasticity, 2016, 6503162.
Dowell, J., Elser, B. A., Schroeder, R. E., & Stevens, H. E. (2019). Cellular stress mechanisms of prenatal maternal stress: Heat shock factors and oxidative stress. Neuroscience Letters, 709, 134368.
Dresler, T., Guhn, A., Tupak, S. V., Ehlis, A. C., Herrmann, M. J., Fallgatter, A. J., Deckert, J., & Domschke, K. (2013). Revise the revised? New dimensions of the neuroanatomical hypothesis of panic disorder. Journal of Neural Transmission (Vienna, Austria: 1996), 120(1), 3-29.
Fan, J. M., Chen, X. Q., & Du, J. Z. (2014). Prenatal stress, anxiety and depression: A mechanism involving CRH peptide family. Neuro Endocrinology Letters, 35(6), 429-439.
French, N. P., Hagan, R., Evans, S. F., Mullan, A., & Newnham, J. P. (2004). Repeated antenatal corticosteroids: Effects on cerebral palsy and childhood behavior. American Journal of Obstetrics and Gynecology, 190(3), 588-595.
Galvão, M. C., Chaves-Kirsten, G. P., Queiroz-Hazarbassanov, N., Carvalho, V. M., Bernardi, M. M., & Kirsten, T. B. (2015). Prenatal zinc reduces stress response in adult rat offspring exposed to lipopolysaccharide during gestation. Life Sciences, 120, 54-60.
Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017). Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain, Behavior, and Immunity, 64, 50-58.
Hagmeyer, S., Haderspeck, J. C., & Grabrucker, A. M. (2014). Behavioral impairments in animal models for zinc deficiency. Frontiers in Behavioral Neuroscience, 8, 443.
Hantsoo, L., Kornfield, S., Anguera, M. C., & Epperson, C. N. (2019). Inflammation: A proposed intermediary between maternal stress and offspring neuropsychiatric risk. Biological Psychiatry, 85, 97-106.
Hartman, S., Eilertsen, E. M., Ystrom, E., Belsky, J., & Gjerde, L. C. (2020). Does prenatal stress amplify effects of postnatal maternal depressive and anxiety symptoms on child problem behavior? Developmental Psychology, 56(1), 128-137.
Hashemi, P., Ebrahimi, L., Saboory, E., & Roshan-Milani, S. (2013). Effect of restraint stress during gestation on pentylenetetrazol-induced epileptic behaviors in rat offspring. Iranian Journal of Basic Medical Sciences, 16(9), 979-984.
Hashemi, P., Roshan-Milani, S., Saboory, E., Ebrahimi, L., & Soltanineghad, M. (2016). Interactive effects of prenatal exposure to restraint stress and alcohol on pentylenetetrazol-induced seizure behaviors in rat offspring. Alcohol, 56, 51-57.
Hong, H., Kim, C. J., Kim, J. D., & Seo, J. H. (2014). β-glucan reduces exercise-induced stress through downregulation of c-Fos and c-Jun expression in the brains of exhausted rats. Molecular Medicine Reports, 9(5), 1660-1666.
Jin, S., Zhao, Y., Jiang, Y., Wang, Y., Li, C., Zhang, D., Lian, B., Du, Z., Sun, H., & Sun, L. (2018). Anxiety-like behaviour assessments of adolescent rats after repeated maternal separation during early life. Neuroreport, 29(8), 643-649.
Kim, T. W., Shin, M. S., Park, J. K., Shin, M. A., Lee, H. H., & Lee, S. J. (2013). Treadmill exercise alleviates prenatal noise stress-induced impairment of spatial learning ability through enhancing hippocampal neurogenesis in rat pups. Journal of Exercise Rehabilitation, 9(5), 451-456.
Kullmann, J. S., Grigoleit, J. S., Lichte, P., Kobbe, P., Rosenberger, C., Banner, C., Wolf, O. T., Engler, H., Oberbeck, R., Elsenbruch, S., Bingel, U., Forsting, M., Gizewski, E. R., & Schedlowski, M. (2013). Neural response to emotional stimuli during experimental human endotoxemia. Human Brain Mapping, 34(9), 2217-2227.
Kwon, H. H., Lee, J. S., Park, H., Shin, J., Yin, Y., Shin, N., Shin, H. J., Hwang, J. A., Kim, D. W., & Kang, J. W. (2021). Vitamin E reduces spasms caused by prenatal stress by lowering calpain expression. Epilepsy & Behavior, 114(pt A), 107609.
Levenson, C. W., & Morris, D. (2011). Zinc and neurogenesis: Making new neurons from development to adulthood. Advances in Nutrition, 2(2), 96-100.
Lim, B. V., Jang, M. H., Shin, M. C., Kim, H. B., Kim, Y. J., Kim, Y. P., Chung, J. H., Kim, H., Shin, M. S., Kim, S. S., Kim, E. H., & Kim, C. J. (2001). Caffeine inhibits exercise-induced increase in tryptophan hydroxylase expression in dorsal and median raphe of Sprague-Dawley rats. Neuroscience Letters, 308(1), 25-28.
Lipton, L. R., Brunst, K. J., Kannan, S., Ni, Y. M., Ganguri, H. B., Wright, R. J., & Bosquet Enlow, M. (2017). Associations among prenatal stress, maternal antioxidant intakes in pregnancy, and child temperament at age 30 months. Journal of Developmental Origins of Health and Disease, 8(6), 638-648.
Liu, Y., Heron, J., Hickman, M., Zammit, S., & Wolke, D. (2021). Prenatal stress and offspring depression in adulthood: The mediating role of childhood trauma. Journal of Affective Disorders, 297, 45-52.
Lopim, G. M., Gutierre, R. C., da Silva, E. A., & Arida, R. M. (2020). Physical exercise during pregnancy minimizes PTZ-induced behavioral manifestations in prenatally stressed offspring. Developmental Psychobiology, 62(2), 240-249.
Luft, C., Haute, G. V., Wearick-Silva, L. E., Antunes, K. H., da Costa, M. S., de Oliveira, J. R., & Donadio, M. V. F. (2021). Prenatal stress and KCl-induced depolarization modulate cell death, hypothalamic-pituitary-adrenal axis genes, oxidative and inflammatory response in primary cortical neurons. Neurochemistry International, 147, 105053.
Madhyastha, S., Sahu, S. S., & Rao, G. (2014). Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons. Journal of Basic and Clinical Physiology and Pharmacology, 25(1), 63-72.
Mahmoodkhani, M., Saboory, E., Roshan-Milani, S., Azizi, N., Karimipour, M., Rasmi, Y., & Gholinejad, Z. (2018). Pregestational stress attenuated fertility rate in dams and increased seizure susceptibility in offspring. Epilepsy & Behavior, 79, 174-179.
Maxwell, S. D., Fineberg, A. M., Drabick, D. A., Murphy, S. K., & Ellman, L. M. (2018). Maternal prenatal stress and other developmental risk factors for adolescent depression: Spotlight on sex differences. Journal of Abnormal Child Psychology, 46(2), 381-397.
McClure, E. B., Monk, C. S., Nelson, E. E., Parrish, J. M., Adler, A., Blair, R. J., Fromm, S., Charney, D. S., Leibenluft, E., Ernst, M., & Pine, D. S. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64(1), 97-106.
McLean, M. A., Cobham, V. E., & Simcock, G. (2018). Prenatal maternal distress: A risk factor for child anxiety? Clinical Child and Family Psychology Review, 21(2), 203-223.
Molendijk, M. L., & de Kloet, E. R. (2015). Immobility in the forced swim test is adaptive and does not reflect depression. Psychoneuroendocrinology, 62, 389-391.
Monk, C. S., Telzer, E. H., Mogg, K., Bradley, B. P., Mai, X., Louro, H. M., Chen, G., McClure-Tone, E. B., Ernst, M., & Pine, D. S. (2008). Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Archives of General Psychiatry, 65(5), 568-576.
Mueller, B. R., & Bale, T. L. (2007). Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiology & Behavior, 91(1), 55-65.
Muscatell, K. A., Dedovic, K., Slavich, G. M., Jarcho, M. R., Breen, E. C., Bower, J. E., Irwin, M. R., & Eisenberger, N. I. (2015). Greater amygdala activity and dorsomedial prefrontal-amygdala coupling are associated with enhanced inflammatory responses to stress. Brain, Behavior, and Immunity, 43, 46-53.
Na, K. S., Ham, B. J., Lee, M. S., Kim, L., Kim, Y. K., Lee, H. J., & Yoon, H. K. (2013). Decreased gray matter volume of the medial orbitofrontal cortex in panic disorder with agoraphobia: A preliminary study. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 45, 195-200.
Nakhjiri, E., Saboory, E., Roshan-Milani, S., Rasmi, Y., & Khalafkhani, D. (2017). Effect of prenatal restraint stress and morphine co-administration on plasma vasopressin concentration and anxiety behaviors in adult rat offspring. Stress (Amsterdam, Netherlands), 20(2), 205-211.
Ostrowski, K., Rohde, T., Asp, S., Schjerling, P., & Pedersen, B. K. (1999). Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. The Journal of Physiology, 515(pt 1), 287-291.
Pallarés, M. E., Monteleone, M. C., Pastor, V., Grillo Balboa, J., Alzamendi, A., Brocco, M. A., & Antonelli, M. C. (2021). Early-life stress reprograms stress-coping abilities in male and female juvenile rats. Molecular Neurobiology, 58(11), 5837-5856.
Ramírez-Vélez, R., Romero, M., Echeverri, I., Ortega, J. G., Mosquera, M., Salazar, B., Girón, S. L., Saldarriaga, W., Aguilar de Plata, A. C., & Mateus, J. C. (2011). A factorial randomized controlled trial to evaluate the effect of micronutrients supplementation and regular aerobic exercise on maternal endothelium-dependent vasodilatation and oxidative stress of the newborn. Trials, 12, 60.
Rao, R. M., & Sadananda, M. (2016). Influence of state and/or trait anxieties of Wistar rats in an anxiety paradigm. Annals of Neurosciences, 23(1), 44-50.
Roshan-Milani, S., Seyyedabadi, B., Saboory, E., Parsamanesh, N., & Mehranfard, N. (2021). Prenatal stress and increased susceptibility to anxiety-like behaviors: Role of neuroinflammation and balance between GABAergic and glutamatergic transmission. Stress (Amsterdam, Netherlands), 24(5), 481-495.
Russo, A. J. (2011). Decreased zinc and increased copper in individuals with anxiety. Nutrition and Metabolic Insights, 4, 1-5.
Scott, H., Phillips, T. J., Sze, Y., Alfieri, A., Rogers, M. F., Volpato, V., Case, C. P., & Brunton, P. J. (2020). Maternal antioxidant treatment prevents the adverse effects of prenatal stress on the offspring's brain and behavior. Neurobiology of Stress, 13, 100281.
Seo, J. H., Sung, Y. H., Kim, K. J., Shin, M. S., Lee, E. K., & Kim, C. J. (2011). Effects of Phellinus linteus administration on serotonin synthesis in the brain and expression of monocarboxylate transporters in the muscle during exhaustive exercise in rats. Journal of Nutritional Science and Vitaminology, 57(1), 95-103.
Servatius, R. J., Salameh, G., Coyle, K. M., & Paré, W. P. (2007). Restraint stress. In G. Fink (Ed.), Encyclopedia of stress. Elsevier.
Sestakova, N., Puzserova, A., Kluknavsky, M., & Bernatova, I. (2013). Determination of motor activity and anxiety-related behaviour in rodents: Methodological aspects and role of nitric oxide. Interdisciplinary Toxicology, 6(3), 126-135.
Sirrieh, R. E., MacLean, D. M., & Jayaraman, V. (2013). Amino-terminal domain tetramer organization and structural effects of zinc binding in the N-methyl-D-aspartate (NMDA) receptor. Journal of Biological Chemistry, 288(31), 22555-22564.
Ślusarczyk, J., Trojan, E., Głombik, K., Budziszewska, B., Kubera, M., Lasoń, W., Popiołek-Barczyk, K., Mika, J., Wędzony, K., & Basta-Kaim, A. (2015). Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells. Frontiers in Cellular Neuroscience, 9, 82.
Ślusarczyk, J., Trojan, E., Wydra, K., Głombik, K., Chamera, K., Kucharczyk, M., Budziszewska, B., Kubera, M., Lasoń, W., Filip, M., & Basta-Kaim, A. (2016). Beneficial impact of intracerebroventricular fractalkine administration on behavioral and biochemical changes induced by prenatal stress in adult rats: Possible role of NLRP3 inflammasome pathway. Biochemical Pharmacology, 113, 45-56.
Sun, Q., Jia, N., Ren, F., & Li, X. (2021). Grape seed proanthocyanidins improves depression-like behavior by alleviating oxidative stress and NLRP3 activation in the hippocampus of prenatally-stressed female offspring rats. Journal of Histotechnology, 44(2), 90-98.
Surowka, P., Noworyta, K., Cieslik, A., & Rygula, R. (2022). Trait sensitivity to negative feedback determines the effects of chronic stress and chronic mirtazapine treatment on anxiety and stress-coping strategies in rats. Psychopharmacology, 239(12), 3975-3984.
Suzuki, K., Nakaji, S., Yamada, M., Totsuka, M., Sato, K., & Sugawara, K. (2002). Systemic inflammatory response to exhaustive exercise. Cytokine Kinetics. Exercise Immunology Review, 8, 6-48.
Tassabehji, N. M., Corniola, R. S., Alshingiti, A., & Levenson, C. W. (2008). Zinc deficiency induces depression-like symptoms in adult rats. Physiology & Behavior, 95(3), 365-369.
Trojan, E., Chamera, K., Bryniarska, N., Kotarska, K., Leśkiewicz, M., Regulska, M., & Basta-Kaim, A. (2019). Role of chronic administration of antidepressant drugs in the prenatal stress-evoked inflammatory response in the brain of adult offspring rats: Involvement of the NLRP3 inflammasome-related pathway. Molecular Neurobiology, 56(8), 5365-5380.
van den Bergh, B. R. H., Dahnke, R., & Mennes, M. (2018). Prenatal stress and the developing brain: Risks for neurodevelopmental disorders. Development and Psychopathology, 30(3), 743-762.
Weinstock, M. (2001). Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Progress in Neurobiology, 65(5), 427-451.
Weinstock, M. (2002). Can the behaviour abnormalities induced by gestational stress in rats be prevented or reversed? Stress (Amsterdam, Netherlands), 5(3), 167-176.
Weinstock, M. (2017). Prenatal stressors in rodents: Effects on behavior. Neurobiology of Stress, 6, 3-13.
Weissgerber, T. L., Wolfe, L. A., & Davies, G. A. (2004). The role of regular physical activity in preeclampsia prevention. Medicine and Science in Sports and Exercise, 36(12), 2024-2031.
Weissgerber, T. L., Wolfe, L. A., Davies, G. A., & Mottola, M. F. (2006). Exercise in the prevention and treatment of maternal-fetal disease: A review of the literature. Applied Physiology, Nutrition, and Metabolism, 31(6), 661-674.
Won, E., & Kim, Y. K. (2020). Neuroinflammation-associated alterations of the brain as potential neural biomarkers in anxiety disorders. International Journal of Molecular Sciences, 21(18), 6546.
Zhang, Y., Wang, R., Chen, R., & Wang, L. (2019). [Changes of Wnt/β-catenin signaling pathway in the hippocampus caused by prenatal stress induce depression- and anxiety-like behaviors in rats]. Nan Fang Yi Ke Da Xue Xue Bao, 39(2), 222-226.
Zheng, X., Cheng, Y., Chen, Y., Yue, Y., Li, Y., Xia, S., Li, Y., Deng, H., Zhang, J., & Cao, Y. (2019). Ferulic acid improves depressive-like behavior in prenatally-stressed offspring rats via anti-inflammatory activity and HPA axis. International Journal of Molecular Sciences, 20(3), 493.
Zhu, Z., Li, X., Chen, W., Zhao, Y., Li, H., Qing, C., Jia, N., Bai, Z., & Liu, J. (2004). Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. Journal of Neuroscience Research, 78(6), 837-844.

Auteurs

Parsa Sameei (P)

Student Research Committee, Urmia University of Medical Sciences, Urmia, Iran.

Sina Fatehfar (S)

Student Research Committee, Urmia University of Medical Sciences, Urmia, Iran.
School of Pharmacy, Urmia University of Medical Sciences, Urmia, Iran.
Cellular and Molecular Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences, Urmia, Iran.

Naseh Abdollahzadeh (N)

Neurophysiology Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences, Urmia, Iran.

Leila Chodari (L)

Neurophysiology Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences, Urmia, Iran.

Ehsan Saboory (E)

Zanjan Metabolic Diseases Research Center, Zanjan University of Medical Sciences, Zanjan, Iran.

Shiva Roshan-Milani (S)

Neurophysiology Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences, Urmia, Iran.
Department of Physiology, School of Medicine, Urmia University of Medical Sciences, Urmia, Iran.

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