Sexually dimorphic effects of early life stress in rat pups on urinary bladder detrusor muscle contractility in adulthood

Springer Science and Business Media LLC - Tập 7 - Trang 1-10 - 2016
Ehsan Mohammadi1, Dawn K. Prusator1, Eleanor Healing1, Robert Hurst1,2, Rheal A. Towner1,3, Amy B. Wisniewski2, Beverley Greenwood-Van Meerveld4,5,1
1Oklahoma Center for Neuroscience, University of Oklahoma Health Science Center, Oklahoma City, USA
2Department of Urology, University of Oklahoma Health Science Center, Oklahoma City, USA
3Advanced Magnetic Resonance Center, Oklahoma Medical Research Foundation, Oklahoma City, USA
4VA Medical Center, Oklahoma City, USA
5Department of Physiology, University of Oklahoma Health Science Center, Oklahoma City, USA

Tóm tắt

Painful bladder syndrome/interstitial cystitis (PBS/IC) is a chronic disorder that is commonly seen in women who report a history of adversity in early life. Here, we test the hypothesis that early life stress (ELS) induces sexually dimorphic abnormalities in urinary bladder smooth muscle function in adulthood. Male and female rat pups were conditioned on postnatal (PN) days 8–12 with either a “predictable or “unpredictable” odor-shock, or odor only control treatment. In adulthood, urinary bladder function was assessed in vivo via urine spot analysis and in vitro via contractile responses to electrical field stimulation (EFS) and membrane depolarization with potassium chloride (KCl). In adulthood, we found that female rats exposed to unpredictable ELS showed a significant (p < 0.05) increase in urine voiding volume compared to predictable ELS or controls. We also found that detrusor muscle contractile responses to EFS were significantly (p < 0.001) decreased following unpredictable ELS in adult female rats compared to the predictable ELS or controls. In male rats exposed to ELS, there was no difference in voiding volume or EFS-induced contractility between groups. In adulthood, the myogenic smooth muscle response to KCl was not significantly different between groups. Histological analysis from adult female and male rats revealed no differences in the appearance of the urinary bladder in rats exposed to ELS. In summary, our findings provide evidence to support abnormalities in the nerve-mediated contractile responses of the detrusor smooth muscle in adult female rats following ELS. We speculate that these sexually dimorphic alterations in urinary bladder function may account, at least in part, for the female predominance of PBS/IC.

Tài liệu tham khảo

Chrysanthopoulou EL, Doumouchtsis SK. Challenges and current evidence on the management of bladder pain syndrome. Neurourol Urodyn. 2014;33:1193–201. Van de Merwe JP, Nordling J, Bouchelouche P, Bouchelouche K, Cervigni M, Daha LK, et al. Diagnostic criteria, classification, and nomenclature for painful bladder syndrome/interstitial cystitis: an ESSIC proposal. Eur Urol. 2008;53:60–7. McLennan MT. Interstitial cystitis: epidemiology, pathophysiology, and clinical presentation. Obstet Gynecol Clin North Am. 2014;41(3):385–95. Lai H, Gardner V, Vetter J, Andriole GL. Correlation between psychological stress levels and the severity of overactive bladder symptoms. BMC Urol. 2015;15:14. Hanno P, Nordling J, Fall M. Bladder pain syndrome. Med Clin North Am. 2011;95:55–73. Buffington CA. Comorbidity of interstitial cystitis with other unexplained clinical conditions. J Urol. 2004;172:1242–8. Chang A, Butler S, Sliwoski J, Valentino R, Canning D, Zderic S. Social stress in mice induces voiding dysfunction and bladder wall remodeling. Am J Physiol Renal Physiol. 2009;297:F1101–8. Mingin GC, Peterson A, Erickson CS, Nelson MT, Vizzard MA. Social stress induces changes in urinary bladder function, bladder NGF content, and generalized bladder inflammation in mice. Am J Physiol Regul Integr Comp Physiol. 2014;307:R893–900. McGonagle E, Smith A, Butler S, Sliwoski J, Valentino R, Canning D, et al. Water avoidance stress results in an altered voiding phenotype in male mice. Neurourol Urodyn. 2012;31:1185–9. Demir A, Onol FF, Ercan F, Tarcan T. Effect of cold-induced stress on rat bladder tissue contractility and histomorphology. Neurourol Urodyn. 2007;26:296–301. Nickel JC, Tripp DA, Pontari M, Moldwin R, Mayer R, Carr LK, et al. Childhood sexual trauma in women with interstitial cystitis/bladder pain syndrome: a case control study. Can Urol Assoc J. 2011;5:410–5. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptions to adverse early experience. Prog Brain Res. 2000;122:81–103. Ivy AS, Brunson KL, Sandman C, Baram TZ. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience. 2008;154:1132–42. Sullivan RM, Landers M, Yeaman B, Wilson DA. Good memories of bad events in infancy. Nature. 2000;407:38–9. Camp LL, Rudy JW. Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev Psychobiol. 1988;21:25–42. Roth TL, Sullivan RM. Endogenous opioids and their role in odor preference acquisition and consolidation following odor-shock conditioning in infant rats. Dev Psychobiol. 2001;39:188–98. Chaloner A, Greenwood-Van Meerveld B. Sexually dimorphic effects of unpredictable early life adversity on visceral pain behavior in a rodent model. J Pain. 2013;14:270–80. Tyler K, Moriceau S, Sullivan RM, Greenwood-Van Meerveld B. Long-term colonic hypersensitivity in adult rats induced by neonatal unpredictable vs predictable shock. Neurogastroenterol Motil. 2007;19:761–8. Moriceau S, Sullivan RM. Corticosterone influences on mammalian neonatal sensitive-period learning. Behav Neurosci. 2004;118:274–81. Kong XT, Deng FM, Hu P, Liang FX, Zhou G, Auerbach AB, et al. Roles of uroplakins in plaque formation, umbrella cell enlargement and urinary tract diseases. J Cell Biol. 2004;167:1195–204. Noronha R, Akbarali H, Malykhina A, Foreman RD, Greenwood-Van Meerveld B. Changes in urinary bladder smooth muscle function in response to colonic inflammation. Am J Physiol Renal Physiol. 2007;293:F1461–7. Gilles EE, Schultz L, Baram TZ. Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr Neurol. 1996;15:114–9. Alvarez P, Green PG, Levine JD. Stress in the adult rat exacerbates muscle pain induced by early-life stress. Biol Psychiatry. 2013;74:688–95. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to subsequent stressor. Metab Brain Dis. 2004;19:3–14. Ren TH, Wu J, Yew D, Ziea E, Lao L, Leung WK, et al. Effects of neonatal maternal separation on neurochemical and sensory response to colonic distension in a rat model of irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2007;292:G849–56. Yehuda R, Levengood RA, Schmeidler J, Wilson S, Guo LS, Gerber D. Increased pituitary activation following metyrapone administration in post-traumatic stress disorder. Psychoneuroendrocrinology. 1996;1:1–16. Johnson OL, Berkley KJ. Estrous influences on micturition thresholds of the female rat before and after bladder inflammation. Am J Physiol Regul Integr Comp Physiol. 2002;282:R289–94. Maggi CA, Santicioli P, Meli A. Postnatal development of micturition reflex in rats. Am J Physiol. 1986;250(5 Pt 2):R926–31. Crumley S, Ge Y, Zhou H, Shen SS, Ro JY. Interstitial cystitis: another IgG4-related inflammatory disease? Ann Diagn Pathol. 2013;17:403–7.