Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
May-2019 Volume 19 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
May-2019 Volume 19 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article Open Access

Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus

  • Authors:
    • Chong Zhang
    • Si‑Jing Fan
    • An‑Bang Sun
    • Zhen‑Zhen Liu
    • Lian Liu
  • View Affiliations / Copyright

    Affiliations: Department of Pharmacy, Xiangyang No. 1 People's Hospital, Hubei University of Medicine, Xiangyang, Hubei 441000, P.R. China, Department of Pharmacology, Medical School of Yangtze University, Jingzhou, Hubei 434023, P.R. China, Laboratory of Neuronal and Brain Disease Modulation, Yangtze University, Jingzhou, Hubei 434023, P.R. China
    Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 4185-4194
    |
    Published online on: March 29, 2019
       https://doi.org/10.3892/mmr.2019.10105
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Prenatal nicotine exposure (PNE) is closely related to depression in offspring. However, the underlying mechanism is still unclear. We hypothesized that neurosteroid in the hippocampus may mediate PNE‑induced depression‑like behaviors. Nicotine was subcutaneously administered (1.0 mg/kg) to pregnant rats twice daily from gestational day (GD) 9 to 20. In adolescent offspring, PNE significantly increased immobility time and decreased the sucrose preference in female rats. The numbers of hippocampal neurons declined in the CA3 and DG regions. Steroidogenic acute regulatory protein (StAR) expression was suppressed in female rats. In fetal offspring, the neuronal numbers of CA3 regions in PNE female fetal hippocampal were significantly decreased, accompanied by the enhanced content of corticosterone and StAR expression. These data indicated that PNE induced depression‑like behavior in adolescent female rats via the regulation of neurosteroid levels in the hippocampus.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

View References

1 

Organization WH, . Integrating mental health into primary care. A global perspective. 2008.

2 

Liu Q, Cai H, Yang LH, Xiang YB, Yang G, Li H, Gao YT, Zheng W, Susser E and Shu XO: Depressive symptoms and their association with social determinants and chronic diseases in middle-aged and elderly Chinese people. Sci Rep. 8:38412018. View Article : Google Scholar : PubMed/NCBI

3 

Capra L, Tezza G, Mazzei F and Boner AL: The origins of health and disease: The influence of maternal diseases and lifestyle during gestation. Ital J Pediatr. 39:72013. View Article : Google Scholar : PubMed/NCBI

4 

Pierrefiche O: Long term depression in rat hippocampus and the effect of ethanol during fetal life. Brain Sci. 7:E1572017. View Article : Google Scholar : PubMed/NCBI

5 

Belluscio LM, Alberca CD, Pregi N and Canepa ET: Altered gene expression in hippocampus and depressive-like behavior in young adult female mice by early protein malnutrition. Genes Brain Behav. 15:741–749. 2016. View Article : Google Scholar : PubMed/NCBI

6 

Tong VT, Dietz PM, Morrow B, D'Angelo DV, Farr SL, Rockhill KM and England LJ; Centers for Disease Control and Prevention (CDC), : Trends in smoking before, during, and after pregnancy-Pregnancy Risk Assessment Monitoring System, United States, 40 sites, 2000–2010. MMWR Surveill Sum. 62:1–19. 2013.

7 

Maughan B, Taylor A, Caspi A and Moffitt TE: Prenatal smoking and early childhood conduct problems: Testing genetic and environmental explanations of the association. Arch Gen Psychiatry. 61:836–843. 2004. View Article : Google Scholar : PubMed/NCBI

8 

Fergusson DM, Woodward LJ and Horwood LJ: Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. Arch Gen Psychiatry. 55:721–727. 1998. View Article : Google Scholar : PubMed/NCBI

9 

Stene-Larsen K, Borge AI and Vollrath ME: Maternal smoking in pregnancy and externalizing behavior in 18-month-old children: Results from a population-based prospective study. J Am Acad Child Adolesc Psychiatry. 48:283–289. 2009. View Article : Google Scholar : PubMed/NCBI

10 

Girdler SS and Klatzkin R: Neurosteroids in the context of stress: Implications for depressive disorders. Pharmacol Ther. 116:125–139. 2007. View Article : Google Scholar : PubMed/NCBI

11 

Jukic MM, Opel N, Strom J, Carrillo-Roa T, Miksys S, Novalen M, Renblom A, Sim SC, Peñas-Lledó EM, Courtet P, et al: Elevated CYP2C19 expression is associated with depressive symptoms and hippocampal homeostasis impairment. Mol Psychiatry. 22:12242017. View Article : Google Scholar : PubMed/NCBI

12 

Reddy DS: Neurosteroids: Endogenous role in the human brain and therapeutic potentials. Prog Brain Res. 186:113–137. 2010. View Article : Google Scholar : PubMed/NCBI

13 

Baulieu EE: Neurosteroids: A novel function of the brain. Psychoneuroendocrinology. 23:963–987. 1998. View Article : Google Scholar : PubMed/NCBI

14 

Izumi Y, O'Dell KA and Zorumski CF: Corticosterone enhances the potency of ethanol against hippocampal long-term potentiation via local neurosteroid synthesis. Front Cell Neurosci. 9:2542015. View Article : Google Scholar : PubMed/NCBI

15 

Tokuda K, Izumi Y and Zorumski CF: Ethanol enhances neurosteroidogenesis in hippocampal pyramidal neurons by paradoxical NMDA receptor activation. J Neurosci. 31:9905–9909. 2011. View Article : Google Scholar : PubMed/NCBI

16 

Slotkin TA: If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? Neurotoxicol Teratol. 30:1–19. 2008. View Article : Google Scholar : PubMed/NCBI

17 

Hellström-Lindahl E and Nordberg A: Smoking during pregnancy: A way to transfer the addiction to the next generation? Respiration. 69:289–293. 2002. View Article : Google Scholar : PubMed/NCBI

18 

Roy TS, Seidler FJ and Slotkin TA: Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther. 300:124–133. 2002. View Article : Google Scholar : PubMed/NCBI

19 

Li J, Bo L, Zhang P, Gao Q, Li L, Tang J, Wu C, Li D, Xiao J, Chen J, et al: Exposure to nicotine during pregnancy and altered learning and memory in the rat offspring. Nicotine Tob Res. 17:661–666. 2015. View Article : Google Scholar : PubMed/NCBI

20 

Kalejaiye OO and Gondre-Lewis MC: Enhanced susceptibility of CA3 hippocampus to prenatal nicotine exposure. J Dev Orig Health Dis. 8:155–160. 2017. View Article : Google Scholar : PubMed/NCBI

21 

Yan YE, Liu L, Wang JF, Liu F, Li XH, Qin HQ and Wang H: Prenatal nicotinic exposure suppresses fetal adrenal steroidogenesis via steroidogenic factor 1 (SF-1) deacetylation. Toxicol Appl Pharmacol. 277:231–241. 2014. View Article : Google Scholar : PubMed/NCBI

22 

Liu L, Wang JF, Fan J, Rao YS, Liu F, Yan YE and Wang H: Nicotine suppressed fetal adrenal StAR expression via YY1 mediated-histone deacetylation modification mechanism. Int J Mol Sci. 17:E14772016. View Article : Google Scholar : PubMed/NCBI

23 

Rice D and Barone S Jr: Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect. 108 (Suppl 3):S511–S533. 2000. View Article : Google Scholar

24 

Semple BD, Blomgren K, Gimlin K, Ferriero DM and Noble-Haeusslein LJ: Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol. 106-107:1–16. 2013. View Article : Google Scholar : PubMed/NCBI

25 

Bayer SA: Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J Comp Neurol. 190:115–134. 1980. View Article : Google Scholar : PubMed/NCBI

26 

Schaefer TL, Skelton MR, Herring NR, Gudelsky GA, Vorhees CV and Williams MT: Short- and long-term effects of (+)-methamphetamine and (+/-)-3,4-methylenedioxymethamphetamine on monoamine and corticosterone levels in the neonatal rat following multiple days of treatment. J Neurochem. 104:1674–1685. 2008. View Article : Google Scholar : PubMed/NCBI

27 

Zhang Y, Zhu X, Bai M, Zhang L, Xue L and Yi J: Maternal deprivation enhances behavioral vulnerability to stress associated with miR-504 expression in nucleus accumbens of rats. PLoS One. 8:e699342013. View Article : Google Scholar : PubMed/NCBI

28 

Bowen MT, Peters ST, Absalom N, Chebib M, Neumann ID and McGregor IS: Oxytocin prevents ethanol actions at delta subunit-containing GABAA receptors and attenuates ethanol-induced motor impairment in rats. Proc Natl Acad Sci USA. 112:3104–3109. 2015. View Article : Google Scholar : PubMed/NCBI

29 

Gao J, Wang H, Liu Y, Li YY, Chen C, Liu LM, Wu YM, Li S and Yang C: Glutamate and GABA imbalance promotes neuronal apoptosis in hippocampus after stress. Med Sci Monit. 20:499–512. 2014. View Article : Google Scholar : PubMed/NCBI

30 

Pan M and Zhang C: Stimulatory effect of gonadal hormones on fetal rat hippocampal neural proliferation requires neurotrophin receptor activation in vitro. Neurosci Lett. 546:1–5. 2013. View Article : Google Scholar : PubMed/NCBI

31 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI

32 

Sierra A: Neurosteroids: The StAR protein in the brain. J Neuroendocrinol. 16:787–793. 2004. View Article : Google Scholar : PubMed/NCBI

33 

Teicher MH and Samson JA: Annual research review: Enduring neurobiological effects of childhood abuse and neglect. J Child Psychol Psychiatry. 57:241–266. 2016. View Article : Google Scholar : PubMed/NCBI

34 

Lv J, Mao C, Zhu L, Hong Zhang, Hui Pengpeng, Feichao Xu, Yujuan Liu, Lubo Zhang and Zhice Xu: The effect of prenatal nicotine on expression of nicotine receptor subunits in the fetal brain. Neurotoxicology. 29:722–726. 2008. View Article : Google Scholar : PubMed/NCBI

35 

Krugers HJ, Arp JM, Xiong H, Kanatsou S, Lesuis SL, Korosi A, Joels M and Lucassen PJ: Early life adversity: Lasting consequences for emotional learning. Neurobiol Stress. 6:14–21. 2017. View Article : Google Scholar : PubMed/NCBI

36 

Chudal R, Brown AS, Gissler M, Suominen A and Sourander A: Is maternal smoking during pregnancy associated with bipolar disorder in offspring? J Affect Disord. 171:132–136. 2015. View Article : Google Scholar : PubMed/NCBI

37 

Martinez EJ, Kolb BL, Bell A, Savage DD and Allan AM: Moderate perinatal arsenic exposure alters neuroendocrine markers associated with depression and increases depressive-like behaviors in adult mouse offspring. Neurotoxicology. 29:647–655. 2008. View Article : Google Scholar : PubMed/NCBI

38 

Sobrian SK, Marr L and Ressman K: Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats. Prog Neuropsychopharmacol Biol Psychiatry. 27:501–518. 2003. View Article : Google Scholar : PubMed/NCBI

39 

Menezes AM, Murray J, Laszlo M, Wehrmeister FC, Hallal PC, Gonçalves H, Assunção MC, Menezes CB and Barros FC: Happiness and depression in adolescence after maternal smoking during pregnancy: Birth cohort study. PLoS One. 8:e803702013. View Article : Google Scholar : PubMed/NCBI

40 

Elmasry H, Goodwin RD, Terry MB and Tehranifar P: Early life exposure to cigarette smoke and depressive symptoms among women in midlife. Nicotine Tob Res. 16:1298–1306. 2014. View Article : Google Scholar : PubMed/NCBI

41 

Xu D, Liang G, Yan YE, He WW, Liu YS, Chen LB, Magdalou J and Wang H: Nicotine-induced over-exposure to maternal glucocorticoid and activated glucocorticoid metabolism causes hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic alterations in fetal rats. Toxicol Lett. 209:282–290. 2012. View Article : Google Scholar : PubMed/NCBI

42 

Silveira VM and Horta BL: Birth weight and metabolic syndrome in adults: Meta-analysis. Rev Saude Publica. 42:10–18. 2008.(In Portuguese). View Article : Google Scholar : PubMed/NCBI

43 

McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG, Karatsoreos IN and Nasca C: Mechanisms of stress in the brain. Nat Neurosci. 18:1353–1363. 2015. View Article : Google Scholar : PubMed/NCBI

44 

Naeff B, Schlumpf M and Lichtensteiger W: Pre- and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: An autoradiographic study. Brain Res Dev Brain Res. 68:163–174. 1992. View Article : Google Scholar : PubMed/NCBI

45 

Bayer SA, Altman J, Russo RJ and Zhang X: Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 14:83–144. 1993.PubMed/NCBI

46 

Quinn R: Comparing rat's to human's age: How old is my rat in people years? Nutrition. 21:775–777. 2005. View Article : Google Scholar : PubMed/NCBI

47 

Radic T, Friess L, Vijikumar A, Jungenitz T, Deller T and Schwarzacher SW: Differential postnatal expression of neuronal maturation markers in the dentate gyrus of mice and rats. Front Neuroanat. 11:1042017. View Article : Google Scholar : PubMed/NCBI

48 

Slotkin TA, Greer N, Faust J, Cho H and Seidler FJ: Effects of maternal nicotine injections on brain development in the rat: Ornithine decarboxylase activity, nucleic acids and proteins in discrete brain regions. Brain Res Bull. 17:41–50. 1986. View Article : Google Scholar : PubMed/NCBI

49 

Laudenbach V, Medja F, Zoli M, Rossi FM, Evrard P, Changeux JP and Gressens P: Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries. FASEB J. 16:423–425. 2002. View Article : Google Scholar : PubMed/NCBI

50 

Roy TS and Sabherwal U: Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol. 20:465–473. 1998. View Article : Google Scholar : PubMed/NCBI

51 

Wang H and Gondre-Lewis MC: Prenatal nicotine and maternal deprivation stress de-regulate the development of CA1, CA3, and dentate gyrus neurons in hippocampus of infant rats. PLoS One. 8:e655172013. View Article : Google Scholar : PubMed/NCBI

52 

Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas CA, Kempermann G, Taylor V and Giachino C: Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell. 6:445–456. 2010. View Article : Google Scholar : PubMed/NCBI

53 

Shruster A, Melamed E and Offen D: Neurogenesis in the aged and neurodegenerative brain. Apoptosis. 15:1415–1421. 2010. View Article : Google Scholar : PubMed/NCBI

54 

Fry JP, Li KY, Devall AJ, Cockcroft S, Honour JW and Lovick TA: Fluoxetine elevates allopregnanolone in female rat brain but inhibits a steroid microsomal dehydrogenase rather than activating an aldo-keto reductase. Br J Pharmacol. 171:5870–5880. 2014. View Article : Google Scholar : PubMed/NCBI

55 

Khisti RT and Chopde CT: Serotonergic agents modulate antidepressant-like effect of the neurosteroid 3alpha-hydroxy-5alpha-pregnan-20-one in mice. Brain Res. 865:291–300. 2000. View Article : Google Scholar : PubMed/NCBI

56 

Li L, Wang W, Zhang LM, Jiang XY, Sun SZ, Sun LJ, Guo Y, Gong J, Zhang YZ, Wang HL and Li YF: Overexpression of the 18 kDa translocator protein (TSPO) in the hippocampal dentate gyrus produced anxiolytic and antidepressant-like behavioural effects. Neuropharmacology. 125:117–128. 2017. View Article : Google Scholar : PubMed/NCBI

57 

Higo S, Hojo Y, Ishii H, Komatsuzaki Y, Ooishi Y, Murakami G, Mukai H, Yamazaki T, Nakahara D, Barron A, et al: Endogenous synthesis of corticosteroids in the hippocampus. PLoS One. 6:e216312011. View Article : Google Scholar : PubMed/NCBI

58 

Tsutsui K, Ukena K, Usui M, Sakamoto H and Takase M: Novel brain function: Biosynthesis and actions of neurosteroids in neurons. Neurosci Res. 36:261–273. 2000. View Article : Google Scholar : PubMed/NCBI

59 

Manna PR and Stocco DM: Regulation of the steroidogenic acute regulatory protein expression: Functional and physiological consequences. Curr Drug Targets Immune Endocr Metabol Disord. 5:93–108. 2005. View Article : Google Scholar : PubMed/NCBI

60 

Solomon MB and Herman JP: Sex differences in psychopathology: Of gonads, adrenals and mental illness. Physiol Behav. 97:250–258. 2009. View Article : Google Scholar : PubMed/NCBI

61 

Xu Y, Ma L, Jiang W, Li Y, Wang G and Li R: Study of sex differences in duloxetine efficacy for depression in transgenic mouse models. Front Cell Neurosci. 11:3442017. View Article : Google Scholar : PubMed/NCBI

62 

Autry AE, Adachi M, Cheng P and Monteggia LM: Gender-specific impact of brain-derived neurotrophic factor signaling on stress-induced depression-like behavior. Biol Psychiatry. 66:84–90. 2009. View Article : Google Scholar : PubMed/NCBI

63 

Cross SJ, Linker KE and Leslie FM: Sex-dependent effects of nicotine on the developing brain. J Neurosci Res. 95:422–436. 2017. View Article : Google Scholar : PubMed/NCBI

64 

Worly BL, Gur TL and Schaffir J: The relationship between progestin hormonal contraception and depression: A systematic review. Contraception. 97:478–489. 2018. View Article : Google Scholar : PubMed/NCBI

65 

O'Dell LE and Torres OV: A mechanistic hypothesis of the factors that enhance vulnerability to nicotine use in females. Neuropharmacology. 76:566–580. 2014. View Article : Google Scholar : PubMed/NCBI

66 

Lee CH, Chang YC, Chen CS, Tu SH, Wang YJ, Chen LC, Chang YJ, Wei PL, Chang HW, Chang CH, et al: Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces alpha9-nicotinic acetylcholine receptor expression in human breast cancer cells. Breast Cancer Res Treat. 129:331–345. 2011. View Article : Google Scholar : PubMed/NCBI

67 

el-Mas MM, el-Gowilly SM, Gohar EY, Ghazal AR and Abdel-Rahman AA: Estrogen dependence of the renal vasodilatory effect of nicotine in rats: Role of alpha7 nicotinic cholinergic receptor/eNOS signaling. Life Sci. 88:187–193. 2011. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Zhang C, Fan SJ, Sun AB, Liu ZZ and Liu L: Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus. Mol Med Rep 19: 4185-4194, 2019.
APA
Zhang, C., Fan, S., Sun, A., Liu, Z., & Liu, L. (2019). Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus. Molecular Medicine Reports, 19, 4185-4194. https://doi.org/10.3892/mmr.2019.10105
MLA
Zhang, C., Fan, S., Sun, A., Liu, Z., Liu, L."Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus". Molecular Medicine Reports 19.5 (2019): 4185-4194.
Chicago
Zhang, C., Fan, S., Sun, A., Liu, Z., Liu, L."Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus". Molecular Medicine Reports 19, no. 5 (2019): 4185-4194. https://doi.org/10.3892/mmr.2019.10105
Copy and paste a formatted citation
x
Spandidos Publications style
Zhang C, Fan SJ, Sun AB, Liu ZZ and Liu L: Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus. Mol Med Rep 19: 4185-4194, 2019.
APA
Zhang, C., Fan, S., Sun, A., Liu, Z., & Liu, L. (2019). Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus. Molecular Medicine Reports, 19, 4185-4194. https://doi.org/10.3892/mmr.2019.10105
MLA
Zhang, C., Fan, S., Sun, A., Liu, Z., Liu, L."Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus". Molecular Medicine Reports 19.5 (2019): 4185-4194.
Chicago
Zhang, C., Fan, S., Sun, A., Liu, Z., Liu, L."Prenatal nicotine exposure induces depression‑like behavior in adolescent female rats via modulating neurosteroid in the hippocampus". Molecular Medicine Reports 19, no. 5 (2019): 4185-4194. https://doi.org/10.3892/mmr.2019.10105
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team