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Brain organic cation transporter 2 controls response and vulnerability to stress and GSK3β signaling

Molecular Psychiatry volume 20, pages 889–900 (2015)Cite this article

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Abstract

Interactions between genetic and environmental factors, like exposure to stress, have an important role in the pathogenesis of mood-related psychiatric disorders, such as major depressive disorder. The polyspecific organic cation transporters (OCTs) were shown previously to be sensitive to the stress hormone corticosterone in vitro, suggesting that these transporters might have a physiologic role in the response to stress. Here, we report that OCT2 is expressed in several stress-related circuits in the brain and along the hypothalamic-pituitary-adrenocortical (HPA) axis. Genetic deletion of OCT2 in mice enhanced hormonal response to acute stress and impaired HPA function without altering adrenal sensitivity to adrenocorticotropic hormone (ACTH). As a consequence, OCT2−/− mice were potently more sensitive to the action of unpredictable chronic mild stress (UCMS) on depression-related behaviors involving self-care, spatial memory, social interaction and stress-sensitive spontaneous behavior. The functional state of the glycogen synthase kinase-3β (GSK3β) signaling pathway, highly responsive to acute stress, was altered in the hippocampus of OCT2−/− mice. In vivo pharmacology and western blot experiments argue for increased serotonin tonus as a main mechanism for impaired GSK3β signaling in OCT2−/− mice brain during acute response to stress. Our findings identify OCT2 as an important determinant of the response to stress in the brain, suggesting that in humans OCT2 mutations or blockade by certain therapeutic drugs could interfere with HPA axis function and enhance vulnerability to repeated adverse events leading to stress-related disorders.

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References

  1. Wong ML, Licinio J . Research and treatment approaches to depression. Nat Rev Neurosci 2001; 2: 343–351.

    Article  CAS  PubMed  Google Scholar 

  2. Krishnan V, Nestler EJ . The molecular neurobiology of depression. Nature 2008; 455: 894–902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Caspi A, Hariri AR, Holmes A, Uher R, Moffitt TE . Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am J Psychiatry 2010; 167: 509–527.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mazure CM, Bruce ML, Maciejewski PK, Jacobs SC . Adverse life events and cognitive-personality characteristics in the prediction of major depression and antidepressant response. Am J Psychiatry 2000; 157: 896–903.

    Article  CAS  PubMed  Google Scholar 

  5. Lupien SJ, McEwen BS, Gunnar MR, Heim C . Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009; 10: 434–445.

    Article  CAS  PubMed  Google Scholar 

  6. Herbert J . Cortisol and depression: three questions for psychiatry. Psychol Med 2013; 43: 449–469.

    Article  CAS  PubMed  Google Scholar 

  7. Ulrich-Lai YM, Herman JP . Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009; 10: 397–409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ziegler DR, Herman JP . Neurocircuitry of stress integration: anatomical pathways regulating the hypothalamo-pituitary-adrenocortical axis of the rat. Integr Comp Biol 2002; 42: 541–551.

    Article  PubMed  Google Scholar 

  9. Kvetnansky R, Sabban EL, Palkovits M . Catecholaminergic systems in stress: structural and molecular genetic approaches. Physiol Rev 2009; 89: 535–606.

    Article  CAS  PubMed  Google Scholar 

  10. Vialou V, Balasse L, Callebert J, Launay JM, Giros B, Gautron S . Altered aminergic neurotransmission in the brain of organic cation transporter 3-deficient mice. J Neurochem 2008; 106: 1471–1482.

    CAS  PubMed  Google Scholar 

  11. Bacq A, Balasse L, Biala G, Guiard B, Gardier AM, Schinkel A, et al. Organic cation transporter 2 controls brain norepinephrine and serotonin clearance and antidepressant response. Mol Psychiatry 2012; 17: 926–939.

    Article  CAS  PubMed  Google Scholar 

  12. Horton RE, Apple DM, Owens WA, Baganz NL, Cano S, Mitchell NC, et al. Decynium-22 enhances SSRI-induced antidepressant-like effects in mice: uncovering novel targets to treat depression. J Neurosci 2013; 33: 10534–10543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Grundemann D, Schechinger B, Rappold GA, Schomig E . Molecular identification of the corticosterone-sensitive extraneuronal catecholamine transporter. Nat Neurosci 1998; 1: 349–351.

    Article  CAS  PubMed  Google Scholar 

  14. Hayer-Zillgen M, Bruss M, Bonisch H . Expression and pharmacological profile of the human organic cation transporters hOCT1, hOCT2 and hOCT3. Br J Pharmacol 2002; 136: 829–836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gasser PJ, Lowry CA, Orchinik M . Corticosterone-sensitive monoamine transport in the rat dorsomedial hypothalamus: potential role for organic cation transporter 3 in stress-induced modulation of monoaminergic neurotransmission. J Neurosci 2006; 26: 8758–8766.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Baganz N, Horton R, Martin K, Holmes A, Daws LC . Repeated swim impairs serotonin clearance via a corticosterone-sensitive mechanism: organic cation transporter 3, the smoking gun. J Neurosci 2010; 30: 15185–15195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Jonker JW, Wagenaar E, Van Eijl S, Schinkel AH . Deficiency in the organic cation transporters 1 and 2 (Oct1/Oct2 [Slc22a1/Slc22a2]) in mice abolishes renal secretion of organic cations. Mol Cell Biol 2003; 23: 7902–7908.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Nollet M, Le Guisquet AM, Belzung C . Models of depression: unpredictable chronic mild stress in mice. Curr Protoc Pharmacol 2013; Chapter 5: Unit 5 65.

    PubMed  Google Scholar 

  19. Surget A, Saxe M, Leman S, Ibarguen-Vargas Y, Chalon S, Griebel G, et al. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 2008; 64: 293–301.

    Article  CAS  PubMed  Google Scholar 

  20. Guiard BP, El Mansari M, Blier P . Cross-talk between dopaminergic and noradrenergic systems in the rat ventral tegmental area, locus ceruleus, and dorsal hippocampus. Mol Pharmacol 2008; 74: 1463–1475.

    Article  CAS  PubMed  Google Scholar 

  21. David DJ, Bourin M, Jego G, Przybylski C, Jolliet P, Gardier AM . Effects of acute treatment with paroxetine, citalopram and venlafaxine in vivo on noradrenaline and serotonin outflow: a microdialysis study in Swiss mice. Br J Pharmacol 2003; 140: 1128–1136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Meller E, Li H, Carr KD, Hiller JM . 5-Hydroxytryptamine(1A) receptor-stimulated [(35)S]GTPgammaS binding in rat brain: absence of regional differences in coupling efficiency. J Pharmacol Exp Ther 2000; 292: 684–691.

    CAS  PubMed  Google Scholar 

  23. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003; 24: 151–180.

    Article  CAS  PubMed  Google Scholar 

  24. Nussdorfer GG . Paracrine control of adrenal cortical function by medullary chromaffin cells. Pharmacol Rev 1996; 48: 495–530.

    CAS  PubMed  Google Scholar 

  25. Brede M, Nagy G, Philipp M, Sorensen JB, Lohse MJ, Hein L . Differential control of adrenal and sympathetic catecholamine release by alpha 2-adrenoceptor subtypes. Mol Endocrinol 2003; 17: 1640–1646.

    Article  CAS  PubMed  Google Scholar 

  26. Rush AJ, Giles DE, Schlesser MA, Orsulak PJ, Parker CR Jr., Weissenburger JE, et al. The dexamethasone suppression test in patients with mood disorders. J Clin Psychiatry 1996; 57: 470–484.

    Article  CAS  PubMed  Google Scholar 

  27. Gourley SL, Wu FJ, Kiraly DD, Ploski JE, Kedves AT, Duman RS, et al. Regionally specific regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 2008; 63: 353–359.

    Article  CAS  PubMed  Google Scholar 

  28. Denmark A, Tien D, Wong K, Chung A, Cachat J, Goodspeed J, et al. The effects of chronic social defeat stress on mouse self-grooming behavior and its patterning. Behav Brain Res 2010; 208: 553–559.

    Article  PubMed  Google Scholar 

  29. Bird CM, Burgess N . The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 2008; 9: 182–194.

    Article  CAS  PubMed  Google Scholar 

  30. Deacon RM . Assessing nest building in mice. Nat Protoc 2006; 1: 1117–1119.

    Article  PubMed  Google Scholar 

  31. Gobbi G, Murphy DL, Lesch K, Blier P . Modifications of the serotonergic system in mice lacking serotonin transporters: an in vivo electrophysiological study. J Pharmacol Exp Ther 2001; 296: 987–995.

    CAS  PubMed  Google Scholar 

  32. Cole AR . GSK3 as a sensor determining cell fate in the brain. Front Mol Neurosci 2012; 5: 4.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Beaulieu JM, Zhang X, Rodriguiz RM, Sotnikova TD, Cools MJ, Wetsel WC, et al. Role of GSK3 beta in behavioral abnormalities induced by serotonin deficiency. Proc Natl Acad Sci USA 2008; 105: 1333–1338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Beaulieu JM, Gainetdinov RR, Caron MG . Akt/GSK3 signaling in the action of psychotropic drugs. Annu Rev Pharmacol Toxicol 2009; 49: 327–347.

    Article  CAS  PubMed  Google Scholar 

  35. Li X, Zhu W, Roh MS, Friedman AB, Rosborough K, Jope RS . In vivo regulation of glycogen synthase kinase-3beta (GSK3beta) by serotonergic activity in mouse brain. Neuropsychopharmacology 2004; 29: 1426–1431.

    Article  CAS  PubMed  Google Scholar 

  36. Frame S, Cohen P, Biondi RM . A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 2001; 7: 1321–1327.

    Article  CAS  PubMed  Google Scholar 

  37. Segal RA . Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 2003; 26: 299–330.

    Article  CAS  PubMed  Google Scholar 

  38. Tanaka KF, Samuels BA, Hen R . Serotonin receptor expression along the dorsal-ventral axis of mouse hippocampus. Philos Trans R Soc Lond Ser B 2012; 367: 2395–2401.

    Article  CAS  Google Scholar 

  39. Pariante CM, Lightman SL . The HPA axis in major depression: classical theories and new developments. Trends Neurosci 2008; 31: 464–468.

    Article  CAS  PubMed  Google Scholar 

  40. Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW, et al. Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 2012; 13: 769–787.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Elliott E, Ezra-Nevo G, Regev L, Neufeld-Cohen A, Chen A . Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 2010; 13: 1351–1353.

    Article  CAS  PubMed  Google Scholar 

  42. Russo SJ, Murrough JW, Han MH, Charney DS, Nestler EJ . Neurobiology of resilience. Nat Neurosci 2012; 15: 1475–1484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Marazziti D, Consoli G, Picchetti M, Carlini M, Faravelli L . Cognitive impairment in major depression. Eur J Pharmacol 2010; 626: 83–86.

    Article  CAS  PubMed  Google Scholar 

  44. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM . Neurobiology of depression. Neuron 2002; 34: 13–25.

    Article  CAS  PubMed  Google Scholar 

  45. Nutt DJ . The psychobiology of posttraumatic stress disorder. J Clin Psychiatry 2000; 61 (Suppl 5):24–29; discussion 30-22.

    CAS  PubMed  Google Scholar 

  46. Bogdan R, Nikolova YS, Pizzagalli DA . Neurogenetics of depression: a focus on reward processing and stress sensitivity. Neurobiol Dis 2013; 52: 12–23.

    Article  PubMed  Google Scholar 

  47. Busch AE, Karbach U, Miska D, Gorboulev V, Akhoundova A, Volk C, et al. Human neurons express the polyspecific cation transporter hOCT2, which translocates monoamine neurotransmitters, amantadine, and memantine. Mol Pharmacol 1998; 54: 342–352.

    Article  CAS  PubMed  Google Scholar 

  48. Bangasser DA, Shors TJ . The hippocampus is necessary for enhancements and impairments of learning following stress. Nat Neurosci 2007; 10: 1401–1403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wagner KV, Hartmann J, Mangold K, Wang XD, Labermaier C, Liebl C, et al. Homer1 mediates acute stress-induced cognitive deficits in the dorsal hippocampus. J Neurosci 2013; 33: 3857–3864.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kaouane N, Porte Y, Vallee M, Brayda-Bruno L, Mons N, Calandreau L et al. Glucocorticoids can induce PTSD-like memory impairments in mice. Science 2012; 335: 1510–1513.

    Article  CAS  PubMed  Google Scholar 

  51. de Quervain DJ, Roozendaal B, McGaugh JL . Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998; 394: 787–790.

    Article  CAS  PubMed  Google Scholar 

  52. Herman JP, Cullinan WE . Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997; 20: 78–84.

    Article  CAS  PubMed  Google Scholar 

  53. Kaidanovich-Beilin O, Milman A, Weizman A, Pick CG, Eldar-Finkelman H . Rapid antidepressive-like activity of specific glycogen synthase kinase-3 inhibitor and its effect on beta-catenin in mouse hippocampus. Biol Psychiatry 2004; 55: 781–784.

    Article  CAS  PubMed  Google Scholar 

  54. Polter A, Beurel E, Yang S, Garner R, Song L, Miller CA, et al. Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 2010; 35: 1761–1774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. O'Brien WT, Harper AD, Jove F, Woodgett JR, Maretto S, Piccolo S, et al. Glycogen synthase kinase-3beta haploinsufficiency mimics the behavioral and molecular effects of lithium. J Neurosci 2004; 24: 6791–6798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Beaulieu JM, Marion S, Rodriguiz RM, Medvedev IO, Sotnikova TD, Ghisi V, et al. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 2008; 132: 125–136.

    Article  CAS  PubMed  Google Scholar 

  57. Polter AM, Li X . Glycogen synthase kinase-3 is an intermediate modulator of serotonin neurotransmission. Front Mol Neurosci 2011; 4: 31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tsuji M, Takeda H, Matsumiya T . Protective effects of 5-HT1A receptor agonists against emotional changes produced by stress stimuli are related to their neuroendocrine effects. Br J Pharmacol 2001; 134: 585–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mikkelsen JD, Hay-Schmidt A, Kiss A . Serotonergic stimulation of the rat hypothalamo-pituitary-adrenal axis: interaction between 5-HT1A and 5-HT2A receptors. Ann N Y Acad Sci 2004; 1018: 65–70.

    Article  CAS  PubMed  Google Scholar 

  60. Hong JG, Kim DH, Lee CH, Park SJ, Kim JM, Cai M, et al. GSK-3beta activity in the hippocampus is required for memory retrieval. Neurobiol Learn Mem 2012; 98: 122–129.

    Article  CAS  PubMed  Google Scholar 

  61. Kimura T, Yamashita S, Nakao S, Park JM, Murayama M, Mizoroki T, et al. GSK-3beta is required for memory reconsolidation in adult brain. PLoS One 2008; 3: e3540.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D et al. A critical role for IGF-II in memory consolidation and enhancement. Nature 2011; 469: 491–497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, et al. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 2007; 53: 703–717.

    Article  CAS  PubMed  Google Scholar 

  64. Ge Y, Dong Z, Bagot RC, Howland JG, Phillips AG, Wong TP, et al. Hippocampal long-term depression is required for the consolidation of spatial memory. Proc Natl Acad Sci USA 2010; 107: 16697–16702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Dong Z, Bai Y, Wu X, Li H, Gong B, Howland JG, et al. Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze. Neuropharmacology 2013; 64: 65–73.

    Article  CAS  PubMed  Google Scholar 

  66. Latapy C, Rioux V, Guitton MJ, Beaulieu JM . Selective deletion of forebrain glycogen synthase kinase 3beta reveals a central role in serotonin-sensitive anxiety and social behaviour. Philos Trans R Soc Lond Ser B 2012; 367: 2460–2474.

    Article  CAS  Google Scholar 

  67. Wilkinson MB, Dias C, Magida J, Mazei-Robison M, Lobo M, Kennedy P, et al. A novel role of the WNT-dishevelled-GSK3beta signaling cascade in the mouse nucleus accumbens in a social defeat model of depression. J Neurosci 2011; 31: 9084–9092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dahlhoff M, Siegmund A, Golub Y, Wolf E, Holsboer F, Wotjak CT . AKT/GSK-3beta/beta-catenin signalling within hippocampus and amygdala reflects genetically determined differences in posttraumatic stress disorder like symptoms. Neuroscience 2010; 169: 1216–1226.

    Article  CAS  PubMed  Google Scholar 

  69. Takeda M, Khamdang S, Narikawa S, Kimura H, Kobayashi Y, Yamamoto T, et al. Human organic anion transporters and human organic cation transporters mediate renal antiviral transport. J Pharmacol Exp Ther 2002; 300: 918–924.

    Article  CAS  PubMed  Google Scholar 

  70. Kimura N, Masuda S, Tanihara Y, Ueo H, Okuda M, Katsura T, et al. Metformin is a superior substrate for renal organic cation transporter OCT2 rather than hepatic OCT1. Drug Metab Pharmacokinet 2005; 20: 379–386.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank M Nosten-Bertrand for advice concerning behavior and statistics and F Machulka for expert assistance in animal care. TC, AB and LB were recipients of fellowships from the French Ministry for Research and the Société Française de Pharmacologie et Thérapeutique. This study was financially supported by the Institut National pour la Santé et la Recherche Médicale (INSERM), the Fondation de France and the Agence nationale de la recherche (ANR-13-SAMENTA-0003-01).

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  1. A Bacq

    Present address: 9Present address: Laboratory of Behavioral Genetics, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.,

Authors and Affiliations

  1. INSERM U1130, Paris, France

    T Couroussé, A Bacq, L Balasse, F Louis, B Giros & S Gautron

  2. CNRS UMR 8246, Paris, France

    T Couroussé, A Bacq, L Balasse, F Louis, B Giros & S Gautron

  3. Sorbonne Universités, UPMC Univ Paris 06, Paris, France

    T Couroussé, A Bacq, L Balasse, F Louis, B Giros & S Gautron

  4. Université Paris Descartes, Ecole Doctorale Médicament Toxicologie Chimie Environnement, Paris, France

    T Couroussé

  5. INSERM U930, Tours, France

    C Belzung & A-M Le Guisquet

  6. Laboratoire de Neuropharmacologie EA3544, Université Paris-Sud XI, Faculté de Pharmacie, Châtenay-Malabry, France

    B Guiard & A M Gardier

  7. Division of Molecular Biology, The Netherlands Cancer Institute, Amsterdam, The Netherlands

    A H Schinkel

  8. Department of Psychiatry, Douglas Hospital, McGill University, Montreal, QC, Canada,

    B Giros

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Couroussé, T., Bacq, A., Belzung, C. et al. Brain organic cation transporter 2 controls response and vulnerability to stress and GSK3β signaling. Mol Psychiatry 20, 889–900 (2015). https://doi.org/10.1038/mp.2014.86

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