Concentrations of BDNF and neuropeptides in blood as potential biomarkers of behavioral impairments in rats with ultrasound prenatal stress experience

Ol'ga Vyacheslavovna Abramova; Yana Aleksandrovna Zorkina; Valeriya Mikhaylovna Ushakova; Evgeniy Andreevich Zubkov; Zinaida Ivanovna Storozheva; Ol'ga Ivanovna Gurina; Svetlana Vyacheslavovna Shport; Vladimir Pavlovich Chekhonin; Anna Yur'evna Morozova

doi:10.34757/1560-957X.2023.27.4.002

Concentrations of BDNF and neuropeptides in blood as potential biomarkers of behavioral impairments in rats with ultrasound prenatal stress experience

Full Text: Subscribers Only

Suggested citation:

Abramova OV, Zorkina YaA, Ushakova VM, et al. [Concentrations of BDNF and neuropeptides in blood as potential biomarkers of behavioral impairments in rats with ultrasound prenatal stress experience]. Rossiiskii psikhiatricheskii zhurnal [Russian Journal of Psychiatry]. 2023;(4):18-30. Russian

Abstract

In an experimental study, pregnant females were continuously exposed to ultrasound of variable frequency throughout the gestational period to evaluate the concentrations of BDNF, α-MSH, β-endorphin, neurotensin, oxytocin, and substance P in the blood plasma of rats with experience of ultrasound-induced prenatal stress and to identify the relationship of concentrations with rat behavior. We evaluated the behavior of the obtained offspring in the Open field, Elevated plus maze, Social interaction, anhedonia test and Forced swim test. Concentrations were analyzed by enzyme-linked immunosorbent assay and multiplex analysis. Ultrasound prenatal stress decreased motor and exploratory activity as well as normal social activity, increased anxiety and aggressive social behavior in rats (alterations were more pronounced in males), and increased plasma oxytocin concentrations in females. Differences between sexes were revealed: control males had lower concentration of α-MSH than control females, which was not observed in offspring with prenatal stress; the concentration of substance P was reduced in prenatal stress males compared to prenatal stress females, which was not observed in the control group. The data obtained can be used in the study of predictors of behavioral disorders in humans.

Keywords prenatal stress; neuropeptides; BDNF; rats; behavioral impairment; ultrasound exposure

References

1. Krontira AC, Cruceanu C, Binder EB. Glucocorticoids as Mediators of Adverse Outcomes of Prenatal Stress. Trends Neurosci. 2020;43(6):394–405. DOI: https://doi.org/10.1016/j.tins.2020.03.008 2. Miguel PM, Pereira LO, Silveira PP, Meaney MJ. Early environmental influences on the development of children's brain structure and function. Dev Med Child Neurol. 2019;61(10):1127–33. DOI: https://doi.org/10.1111/dmcn.14182 3. Haq SU, Bhat UA, Kumar A. Prenatal stress effects on offspring brain and behavior: Mediators, alterations and dysregulated epigenetic mechanisms. J Biosci. 2021;46:34. PMID: 33859069 4. Lautarescu A, Craig MC, Glover V. Prenatal stress: Effects on fetal and child brain development. Int Rev Neurobiol. 2020;150:17–40. DOI: https://doi.org/10.1016/bs.irn.2019.11.002 5. Abe H, Hidaka N, Kawagoe C, et al. Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis. Neurosci Res. 2007;59(2):145–51. DOI: https://doi.org/10.1016/j.neures.2007.06.1465 6. Meyer U, Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol. 2010;90(3):285–326. DOI: https://doi.org/10.1016/j.pneurobio.2009.10.018 7. Morozova AY, Zubkov EA, Storozheva ZI, et al. Effect of ultrasonic irradiation on the development of symptoms of depression and anxiety in rats. Bull Exp Biol Med. 2013;154(6):740–3. DOI: https://doi.org/10.1007/s10517-013-2044-1 8. Morozova AY, Zubkov EA, Storozheva ZI, et al. Behavioral patterns and expression of genes coding serotonin receptors in rats with ultrasound induced depression. Br J Med Med Res. 2013;3:2107–18. DOI: https://doi.org/10.13140/2.1.2928.8963 9. Morozova A, Zubkov E, Strekalova T, et al. Ultrasound of alternating frequencies and variable emotional impact evokes depressive syndrome in mice and rats. Prog Neuropsychopharmacol Biol Psychiatry. 2016;68:52–63. DOI: https://doi.org/10.1016/j.pnpbp.2016.03.003 10. Zorkina YA, Zubkov EA, Morozova AY, et al. The Comparison of a New Ultrasound-Induced Depression Model to the Chronic Mild Stress Paradigm. Front Behav Neurosci. 2019;13:146. DOI: https://doi.org/10.3389/fnbeh.2019.00146 11. Abramova O, Zorkina Y, Syunyakov T, et al. Brain Metabolic Profile after Intranasal vs. Intraperitoneal Clomipramine Treatment in Rats with Ultrasound Model of Depression. Int J Mol Sci. 2021;22(17):9598. DOI: https://doi.org/10.3390/ijms22179598 12. Abramova OV, Zubkov EA, Zorkina YA, et al. Social and Cognitive Impairments in Rat Offspring after Ultrasound-Induced Prenatal Stress. Bull Exp Biol Med. 2020;168(6):730–3. DOI: https://doi.org/10.1007/s10517-020-04790-0 13. Abramova O, Ushakova V, Zorkina Y, et al. The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress. Front Physiol. 2021;12:659366. DOI: https://doi.org/10.3389/fphys.2021.659366 14. Kupcova I, Danisovic L, Grgac I, Harsanyi S. Anxiety and Depression: What Do We Know of Neuropeptides? Behav Sci (Basel). 2022;12(8):262. DOI: https://doi.org/10.3390/bs12080262 15. Autry AE, Monteggia LM. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev. 2012;64(2):238–58. DOI: https://doi.org/10.1124/pr.111.005108 16. Hökfelt T, Barde S, Xu ZD, et al. Neuropeptide and Small Transmitter Coexistence: Fundamental Studies and Relevance to Mental Illness. Front Neural Circuits. 2018;12:106. DOI: https://doi.org/10.3389/fncir.2018.00106 17. Knight P, Chellian R, Wilson R, et al. Sex differences in the elevated plus-maze test and large open field test in adult Wistar rats. Pharmacol Biochem Behav. 2021;204:173168. DOI: https://doi.org/10.1016/j.pbb.2021.173168 18. Bopaiah CP, Pradhan N, Venkataram BS. Pharmacological study on antidepressant activity of 50% ethanol extract of a formulated ayurvedic product in rats. J Ethnopharmacol. 2000;72(3):411–9. DOI: https://doi.org/10.1016/s0378-8741(00)00232-4 19. Bourin M, Mocaër E, Porsolt R. Antidepressant-like activity of S 20098 (agomelatine) in the forced swimming test in rodents: involvement of melatonin and serotonin receptors. J Psychiatry Neurosci. 2004;29(2):126–33. PMID: 15069466 20. Vaneev AN, Gorelkin PV, Garanina AS, et al. In Vitro and In Vivo Electrochemical Measurement of Reactive Oxygen Species After Treatment with Anticancer Drugs. Anal Chem. 2020;92(12):8010–4. DOI: https://doi.org/10.1021/acs.analchem.0c01256 21. Vaneev AN, Timoshenko RV, Gorelkin PV, et al. Nano- and Microsensors for In Vivo Real-Time Electrochemical Analysis: Present and Future Perspectives. Nanomaterials (Basel). 2022;12(21):3736. DOI: https://doi.org/10.3390/nano12213736 22. Ni P, Tian Y, Gu X, et al. Plasma neuropeptides as circulating biomarkers of multifactorial schizophrenia. Compr Psychiatry. 2019;94:152114. DOI: https://doi.org/10.1016/j.comppsych.2019.152114 23. de Souza MA, Centenaro LA, Menegotto PR, et al. Prenatal stress produces social behavior deficits and alters the number of oxytocin and vasopressin neurons in adult rats. Neurochem Res. 2013;38(7):1479–89. DOI: https://doi.org/10.1007/s11064-013-1049-5 24. He F, Wang Z, Guo G. Postnatal separation prevents the development of prenatal stress-induced anxiety in association with changes in oestrogen receptor and oxytocin immunoreactivity in female mandarin vole (Microtus mandarinus) offspring. Eur J Neurosci. 2018;47(1):95–108. DOI: https://doi.org/10.1111/ejn.13788 25. Amani M, Houwing DJ, Homberg JR, Salari AA. Perinatal fluoxetine dose-dependently affects prenatal stress-induced neurobehavioural abnormalities, HPA-axis functioning and underlying brain alterations in rat dams and their offspring. Reprod Toxicol. 2021;104:27–43. DOI: https://doi.org/10.1016/j.reprotox.2021.06.014 26. Kajanoja J, Nolvi S, Kantojärvi K, et al. Oxytocin receptor genotype moderates the association between maternal prenatal stress and infant early self-regulation. Psychoneuroendocrinology. 2022;138:105669. DOI: https://doi.org/10.1016/j.psyneuen.2022.105669 27. Rijlaarsdam J, van IJzendoorn MH, Verhulst FC, et al. Prenatal stress exposure, oxytocin receptor gene (OXTR) methylation, and child autistic traits: The moderating role of OXTR rs53576 genotype. Autism Res. 2017;10(3):430–8. DOI: https://doi.org/10.1002/aur.1681 28. Murat Öztürk D, Sayiner FD, Polat Corumlu E, Ulupinar E. Behavioral and hormonal effects of prenatal and maternal separation stresses in postpartum rats. Women Health. 2022;62(7):633–43. DOI: https://doi.org/10.1080/03630242.2022.2100563 29. Onaka T, Takayanagi Y. Role of oxytocin in the control of stress and food intake. J Neuroendocrinol. 2019;31(3):e12700. DOI: https://doi.org/10.1111/jne.12700 30. Takayanagi Y, Onaka T. Roles of Oxytocin in Stress Responses, Allostasis and Resilience. Int J Mol Sci. 2021;23(1):150. DOI: https://doi.org/10.3390/ijms23010150 31. Carter DA, Saridaki E, Lightman SL. Sexual differentiation of oxytocin stress responsiveness: effect of neonatal androgenization, castration and a luteinizing hormone-releasing hormone antagonist. Acta Endocrinol (Copenh). 1988;117(4):525–30. DOI: https://doi.org/10.1530/acta.0.1170525 32. Wang Y, Zhao S, Liu X, et al. Oxytocin improves animal behaviors and ameliorates oxidative stress and inflammation in autistic mice. Biomed Pharmacother. 2018;107:262–9. DOI: https://doi.org/10.1016/j.biopha.2018.07.148 33. Rutigliano G, Rocchetti M, Paloyelis Y, et al. Peripheral oxytocin and vasopressin: Biomarkers of psychiatric disorders? A comprehensive systematic review and preliminary meta-analysis. Psychiatry Res. 2016;241:207–20. DOI: https://doi.org/10.1016/j.psychres.2016.04.117 34. Ferreira AC, Osório FL. Peripheral oxytocin concentrations in psychiatric disorders – A systematic review and methanalysis: Further evidence. Prog Neuropsychopharmacol Biol Psychiatry. 2022;117:110561. DOI: https://doi.org/10.1016/j.pnpbp.2022.110561 35. Conte-Devolx B, Giraud P, Castanas E, et al. Effect of neonatal treatment with monosodium glutamate on the secretion of alpha-MSH, beta-endorphin and ACTH in the rat. Neuroendocrinology. 1981;33(4):207–11. DOI: https://doi.org/10.1159/000123230 36. Thody AJ, Celis ME, Fisher C. Changes in plasma, pituitary and brain alpha-MSH content in rats from birth to sexual maturity. Peptides. 1980;1(2):125–9. DOI: https://doi.org/10.1016/0196-9781(80)90075-3 37. Donahoo WT, Hernandez TL, Costa JL, et al. Plasma alpha-melanocyte-stimulating hormone: sex differences and correlations with obesity. Metabolism. 2009;58(1):16–21. DOI: https://doi.org/10.1016/j.metabol.2008.07.028 38. Herpfer I, Lieb K. Substance P and Substance P receptor antagonists in the pathogenesis and treatment of affective disorders. World J Biol Psychiatry. 2003;4(2):56–63. DOI: https://doi.org/10.3109/15622970309167952 39. Kormos V, Gaszner B. Role of neuropeptides in anxiety, stress, and depression: from animals to humans. Neuropeptides. 2013;47(6):401–19. DOI: https://doi.org/10.1016/j.npep.2013.10.014 40. Li L, Gao X, Zhao J, et al. Plasma and cerebrospinal fluid substance P in post-stroke patients with depression. Psychiatry Clin Neurosci. 2009;63(3):298–304. DOI: https://doi.org/10.1111/j.1440-1819.2009.01936.x 41. Xie R, Xie H, Krewski D, He G. Plasma concentrations of neurotransmitters and postpartum depression. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2018;43(3):274–81. DOI: https://doi.org/10.11817/j.issn.1672-7347.2018.03.007 42. Jang MU, Park JW, Kho HS, et al. Plasma and saliva levels of nerve growth factor and neuropeptides in chronic migraine patients. Oral Dis. 2011;17(2):187–93. DOI: https://doi.org/10.1111/j.1601-0825.2010.01717.x 43. Won E, Kang J, Choi S, et al. The association between substance P and white matter integrity in medication-naive patients with major depressive disorder. Sci Rep. 2017;7(1):9707. DOI: https://doi.org/10.1038/s41598-017-10100-y

DOI: http://dx.doi.org/10.34757/1560-957X.2023.27.4.002

Article Metrics

Metrics Loading ...