The Impact of Adolescent Stress on Nicotine Use and Affective Disorders in Rodent Models

Overview

Journal Eur J Neurosci

Specialty Neurology

Date 2021 Aug 17

PMID 34402112

Authors

Sean M Mooney-Leber

Michael J Caruso

Thomas J Gould

Sonia A Cavigelli

Helen M Kamens

Affiliations

Soon will be listed here.

Abstract

Recent findings indicate that stress exposure during adolescence contributes to the development of both nicotine use and affective disorders, suggesting a potential shared biological pathway. One key system that may mediate the association between adolescent stress and nicotine or affective outcomes is the hypothalamic-pituitary-adrenal (HPA) axis. Here we reviewed evidence regarding the effects of adolescent stress on nicotine responses and affective phenotypes and the role of the HPA-axis in these relationships. Literature indicates that stress, possibly via HPA-axis dysfunction, is a risk factor for both nicotine use and affective disorders. In rodent models, adolescent stress modulates behavioural responses to nicotine and increases the likelihood of affective disorders. The exact role that the HPA-axis plays in altering nicotine sensitivity and affective disorder development after adolescent stress remains unclear. However, it appears likely that adolescent stress-induced nicotine use and affective disorders are precipitated by repetitive activation of a hyperactive HPA-axis. Together, these preclinical studies indicate that adolescent stress is a risk factor for nicotine use and anxiety/depression phenotypes. The findings summarized here suggest that the HPA-axis mediates this relationship. Future studies that pharmacologically manipulate the HPA-axis during and after adolescent stress are critical to elucidate the exact role that the HPA-axis plays in the development of nicotine use and affective disorders following adolescent stress.

References

Booker C, Unger J, Azen S, Baezconde-Garbanati L, Lickel B, Johnson C . A longitudinal analysis of stressful life events, smoking behaviors, and gender differences in a multicultural sample of adolescents. Subst Use Misuse. 2008; 43(11):1521-43. DOI: 10.1080/10826080802238009. View

Buczek Y, Le A, Wang A, Stewart J, Shaham Y . Stress reinstates nicotine seeking but not sucrose solution seeking in rats. Psychopharmacology (Berl). 1999; 144(2):183-8. DOI: 10.1007/s002130050992. View

Iniguez S, Warren B, Parise E, Alcantara L, Schuh B, Maffeo M . Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology. 2008; 34(6):1609-24. PMC: 2692426. DOI: 10.1038/npp.2008.220. View

Keresztes A, Bender A, Bodammer N, Lindenberger U, Lee Shing Y, Werkle-Bergner M . Hippocampal maturity promotes memory distinctiveness in childhood and adolescence. Proc Natl Acad Sci U S A. 2017; 114(34):9212-9217. PMC: 5576837. DOI: 10.1073/pnas.1710654114. View

Neumann I, Wegener G, Homberg J, Cohen H, Slattery D, Zohar J . Animal models of depression and anxiety: What do they tell us about human condition?. Prog Neuropsychopharmacol Biol Psychiatry. 2010; 35(6):1357-75. DOI: 10.1016/j.pnpbp.2010.11.028. View

Gillespie C, Phifer J, Bradley B, Ressler K . Risk and resilience: genetic and environmental influences on development of the stress response. Depress Anxiety. 2009; 26(11):984-92. PMC: 2852579. DOI: 10.1002/da.20605. View

McCormick C, Robarts D, Gleason E, Kelsey J . Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats. Horm Behav. 2004; 46(4):458-66. DOI: 10.1016/j.yhbeh.2004.05.004. View

Iniguez S, Aubry A, Riggs L, Alipio J, Zanca R, Flores-Ramirez F . Social defeat stress induces depression-like behavior and alters spine morphology in the hippocampus of adolescent male C57BL/6 mice. Neurobiol Stress. 2016; 5():54-64. PMC: 5154707. DOI: 10.1016/j.ynstr.2016.07.001. View

Richards J, Stipelman B, Bornovalova M, Daughters S, Sinha R, Lejuez C . Biological mechanisms underlying the relationship between stress and smoking: state of the science and directions for future work. Biol Psychol. 2011; 88(1):1-12. PMC: 3171592. DOI: 10.1016/j.biopsycho.2011.06.009. View

10.

Bremner J, Narayan M, Anderson E, Staib L, Miller H, Charney D . Hippocampal volume reduction in major depression. Am J Psychiatry. 2000; 157(1):115-8. DOI: 10.1176/ajp.157.1.115. View

11.

Cotella E, Gomez A, Lemen P, Chen C, Fernandez G, Hansen C . Long-term impact of chronic variable stress in adolescence versus adulthood. Prog Neuropsychopharmacol Biol Psychiatry. 2018; 88:303-310. PMC: 6165677. DOI: 10.1016/j.pnpbp.2018.08.003. View

12.

Romeo R . The Teenage Brain: The Stress Response and the Adolescent Brain. Curr Dir Psychol Sci. 2014; 22(2):140-145. PMC: 4274618. DOI: 10.1177/0963721413475445. View

13.

Romeo R, Bellani R, Karatsoreos I, Chhua N, Vernov M, Conrad C . Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology. 2006; 147(4):1664-74. DOI: 10.1210/en.2005-1432. View

14.

Schmidt M, Scharf S, Liebl C, Harbich D, Mayer B, Holsboer F . A novel chronic social stress paradigm in female mice. Horm Behav. 2010; 57(4-5):415-20. DOI: 10.1016/j.yhbeh.2010.01.010. View

15.

Brielmaier J, Mcdonald C, Smith R . Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors. Psychopharmacology (Berl). 2011; 219(1):73-82. DOI: 10.1007/s00213-011-2378-1. View

16.

Romeo R, Minhas S, Svirsky S, Hall B, Savenkova M, Karatsoreos I . Pubertal shifts in adrenal responsiveness to stress and adrenocorticotropic hormone in male rats. Psychoneuroendocrinology. 2014; 42:146-52. PMC: 3959666. DOI: 10.1016/j.psyneuen.2014.01.016. View

17.

Ulrich-Lai Y, Herman J . Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci. 2009; 10(6):397-409. PMC: 4240627. DOI: 10.1038/nrn2647. View

18.

Victoria N, Karom M, Eichenbaum H, Murphy A . Neonatal injury rapidly alters markers of pain and stress in rat pups. Dev Neurobiol. 2013; 74(1):42-51. DOI: 10.1002/dneu.22129. View

19.

Gomes F, Grace A . Prefrontal Cortex Dysfunction Increases Susceptibility to Schizophrenia-Like Changes Induced by Adolescent Stress Exposure. Schizophr Bull. 2016; 43(3):592-600. PMC: 5464092. DOI: 10.1093/schbul/sbw156. View

20.

Gunnar M, Wewerka S, Frenn K, Long J, Griggs C . Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev Psychopathol. 2009; 21(1):69-85. PMC: 3933029. DOI: 10.1017/S0954579409000054. View