Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T18:47:57.798Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential plastic changes in synthesis and binding in the mouse somatostatin system after electroconvulsive stimulation

Published online by Cambridge University Press:  21 March 2018

Mikkel Vestergaard Olesen ,
Casper René Gøtzsche ,
Søren Hofman Christiansen  and
David Paul Drucker Woldbye
Mikkel Vestergaard Olesen
Affiliation:
Laboratory of Neural Plasticity, Center for Neuroscience, University of Copenhagen, Copenhagen, Denmark Research Laboratory for Stereology and Neuroscience, Bispebjerg-Frederiksberg Hospital, Copenhagen University Hospital, Denmark
Casper René Gøtzsche
Affiliation:
Laboratory of Neural Plasticity, Center for Neuroscience, University of Copenhagen, Copenhagen, Denmark
Søren Hofman Christiansen
Affiliation:
Laboratory of Neural Plasticity, Center for Neuroscience, University of Copenhagen, Copenhagen, Denmark
David Paul Drucker Woldbye*
Affiliation:
Laboratory of Neural Plasticity, Center for Neuroscience, University of Copenhagen, Copenhagen, Denmark
*
Assoc. Prof. David P.D. Woldbye, MD, PhD, Laboratory of Neural Plasticity, Center for Neuroscience, University of Copenhagen, 3 Blegdamsvej, Panum Institute, Maersk Tower 5th floor, DK-2200 N Copenhagen, Denmark. Tel: +45 40156389 Fax: +45 35360116 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

Electroconvulsive therapy (ECT) is regularly used to treat patients with severe major depression, but the mechanisms underlying the beneficial effects remain uncertain. Electroconvulsive stimulation (ECS) regulates diverse neurotransmitter systems and induces anticonvulsant effects, properties implicated in mediating therapeutic effects of ECT. Somatostatin (SST) is a candidate for mediating these effects because it is upregulated by ECS and exerts seizure-suppressant effects. However, little is known about how ECS might affect the SST receptor system. The present study examined effects of single and repeated ECS on the synthesis of SST receptors (SSTR1–4) and SST, and SST receptor binding ([125I]LTT-SST28) in mouse hippocampal regions and piriform/parietal cortices.

Results

A complex pattern of plastic changes was observed. In the dentate gyrus, SST and SSTR1 expression and the number of hilar SST immunoreactive cells were significantly increased at 1 week after repeated ECS while SSTR2 expression was downregulated by single ECS, and SSTR3 mRNA and SST binding were elevated 24 h after repeated ECS. In hippocampal CA1 and parietal/piriform cortices, we found elevated SST mRNA levels 1 week after repeated ECS and elevated SST binding after single ECS and 24 h after repeated ECS. In hippocampal CA3, repeated ECS increased SST expression 1 week after and SST binding 24 h after. In the parietal cortex, SSTR2 mRNA expression was downregulated after single ECS while SSTR4 mRNA expression was upregulated 24 h after repeated ECS.

Conclusion

Considering the known anticonvulsant effects of SST, it is likely that these ECS-induced neuroplastic changes in the SST system could participate in modulating neuronal excitability and potentially contribute to therapeutic effects of ECT.

Keywords

electroconvulsive seizuremRNA and protein expressionreceptor bindingsomatostatin receptorssomatostatin
Type
Original Article
Information
Acta Neuropsychiatrica , Volume 30 , Issue 4 , August 2018 , pp. 192 - 202
Copyright
© Scandinavian College of Neuropsychopharmacology 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Weiner, R, Krystal, A. Electroconvulsive therapy. In Gabbard GO, and Rush AJ, editors. Treatment of psychiatric disorders. Washington, DC: American Psychiatric Press Inc, 2001:1267–1293.Google Scholar
2. Mathé, AA. Neuropeptides and electroconvulsive treatment. J ECT 1999;15:60–75.Google Scholar
3. Nemeroff, CB, Bissette, G, Akil, H, Fink, M. Neuropeptide concentrations in the cerebrospinal fluid of depressed patients treated with electroconvulsive therapy. Corticotrophin-releasing factor, beta-endorphin and somatostatin. Br J Psychiatry 1991;158:59–63.Google Scholar
4. Nikisch, G, Mathé, AA. CSF monoamine metabolites and neuropeptides in depressed patients before and after electroconvulsive therapy. Eur Psychiatry 2008;23:356–359.Google Scholar
5. Mikkelsen, JD, Woldbye, DP. Accumulated increase in neuropeptide Y and somatostatin gene expression of the rat in response to repeated electroconvulsive stimulation. J Psychiatr Res 2006;40:153–159.Google Scholar
6. Sackeim, HA, Decina, P, Prohovnik, I, Malitz, S, Resor, SR. Anticonvulsant and antidepressant properties of electroconvulsive therapy: a proposed mechanism of action. Biol Psychiatry 1983;18:1301–1310.Google Scholar
7. Sackeim, HA, Luber, B, katzman, GP et al. The effects of electroconvulsive therapy on quantitative electroencephalograms. Relationship to clinical outcome. Arch Gen Psychiatry 1996;53:814–824.Google Scholar
8. Sackeim, HA. The anticonvulsant hypothesis of the mechanisms of action of ECT: current status. J ECT 1999;15:5–26.Google Scholar
9. Bolwig, TG, Woldbye, DPD, Mikkelsen, JD. Electroconvulsive therapy as an anticonvulsant: a possible role of neuropeptide Y (NPY). J Electroconv Ther 1999;15:93–101.Google Scholar
10. Christiansen, SH, Woldbye, DPD. Regulation of the galanin system by repeated electroconvulsive seizures in mice. J Neurosci Res 2010;88:3635–3643.Google Scholar
11. Mathé, AA, Husum, H, El Khoury, A et al. Search for biological correlates of depression and mechanisms of action of antidepressant treatment modalities. Do neuropeptides play a role? Physiol Behav 2007;92:226–231.Google Scholar
12. Post, RM, Putnam, F, Uhde, TW, Weiss, SR. Electroconvulsive therapy as an anticonvulsant. Implications for its mechanism of action in affective illness. Ann N Y Acad Sci 1986;462:376–388.Google Scholar
13. Sattin, A. The role of TRH and related peptides in the mechanism of action of ECT. J ECT 1999;15:76–92.Google Scholar
14. Veronesi, MC, Aldouby, Y, Domb, AJ, Kubek, MJ. Thyrotropin-releasing hormone d,l polylactide nanoparticles (TRH-NPs) protect against glutamate toxicity in vitro and kindling development in vivo. Brain Res 2009;1303:151–160.Google Scholar
15. Binaschi, A, Bregola, G, Simonato, M. On the role of somatostatin in seizure control: clues from the hippocampus. Rev Neurosci 2003;14:285–301.Google Scholar
16. Buckmaster, PS, Otero-Corchón, V, Rubinstein, M, Low, MJ. Heightened seizure severity in somatostatin knockout mice. Epilepsy Res 2002;48:43–56.Google Scholar
17. Tallent, MK. QIU C. Somatostatin: an endogenous antiepileptic. Mol Cell Endocrinol 2008;286:96–103.Google Scholar
18. Tallent, MK, Siggins, GR. Somatostatin acts in CA1 and CA3 to reduce hippocampal epileptiform activity. J Neurophysiol 1999;81:1626–1635.Google Scholar
19. Vezzani, A, Hoyer, D. Brain somatostatin: a candidate inhibitory role in seizures and epileptogenesis. Eur J Neurosci 1999;11:3767–3776.Google Scholar
20. Bissette, G, Widerlöv, E, Walléus, H et al. Alterations in cerebrospinal fluid concentrations of somatostatinlike immunoreactivity in neuropsychiatric disorders. Arch Gen Psychiatry 1986;43:1148–1151.Google Scholar
21. Gerner, RH, Yamada, T. Altered neuropeptide concentrations in cerebrospinal fluid of psychiatric patients. Brain Res 1982;238:298–302.Google Scholar
22. Mathé, AA, Rudorfer, M, Stenfors, C, Manji, H, Potter, W, Theodorsson, E. Effects of electroconvulsive treatment on somatostatin, neuropeptide Y, endothelin, and neurokinin A concentrations in cerebrospinal fluid of depressed patients: a pilot study. Depression 1996;3:250–256.Google Scholar
23. Post, RM, Rubinow, DR, Kling, MA, Berrettini, W, Gold, PW. Neuroactive substances in cerebrospinal fluid. Normal and pathological regulatory mechanisms. Ann N Y Acad Sci 1988;531:15–28.Google Scholar
24. Rubinow, DR, Gold, PW, Post, RM et al. CSF somatostatin in affective illness. Arch Gen Psychiatry 1983;40:409–412.Google Scholar
25. Vecsei, L, Widerlöv, E. Brain and CSF somatostatin concentrations in patients with psychiatric or neurological illness. An overview. Acta Psychiatr Scand 1988;78:657–667.Google Scholar
26. Woldbye, DPD, Greisen, MH, Bolwig, TG, Larsen, PJ, Mikkelsen, JD. Prolonged induction of c-fos in neuropeptide Y- and somatostatin-immunoreactive neurons of the rat dentate gyrus after electroconvulsive stimulation. Brain Res 1996;720:111–119.Google Scholar
27. Dalby, NO, Tønder, N, Woldbye, DPD, West, M, Finsen, BR, Bolwig, TG. No loss of hippocampal hilar somatostatinergic neurons after repeated electroconvulsive shock: a combined stereological and in situ hybridization study. Biol Psychiatry 1996;40:54–60.Google Scholar
28. Kragh, J, Tønder, N, Finsen, BR, Zimmer, J, Bolwig, TG. Repeated electroconvulsive shocks cause transient changes in rat hippocampal somatostatin and neuropeptide Y immunoreactivity and mRNA in situ hybridization signals. Exp Brain Res 1994;98:305–313.Google Scholar
29. Orzi, F, Zoli, M, Passarelli, F, ferraguti, F, Fieschi, C, Agnati, LF. Repeated electroconvulsive shock increases glial fibrillary acidic protein, ornithine decarboxylase, somatostatin and cholecystokinin immunoreactivity in the hippocampal formation of the rat. Brain Res 1990;533:223–231.Google Scholar
30. Passarelli, F, Orzi, F. Somatostatin mRNA in the hippocampal formation following electroconvulsive shock in the rat. Neurosci Lett 1993;153:197–201.Google Scholar
31. Zachrisson, O, Mathé, AA, Stenfors, C, Lindefors, N. Limbic effects of repeated electroconvulsive stimulation on neuropeptide Y and somatostatin mRNA expression in the rat brain. Mol Brain Res 1995;31:71–85.Google Scholar
32. Engin, E, Stellbrink, J, Treit, D, Dickson, CT. Anxiolytic and antidepressant effects of intracerebroventricular administered somatostatin: behavioral and neuropsychological evidence. Neuroscience 2008;157:666–676.Google Scholar
33. Funch, T, Jefferson, SJ, Hopper, A, Yee, P-HP, Maguire, J, Luscher, B. Disinhibition of somatostatin-positive GABAergic interneurons results in an anxiolytic and antidepressant-like brain state. Mol Psychiatry 2017;22:920–930.Google Scholar
34. Ristori, C, Cammalleri, M, Martini, D et al. Involvement of the cAMP-dependent pathway in the reduction of epileptiform bursting caused by somatostatin in the mouse hippocampus. Naunyn Schmiedebergs Arch Pharmacol 2008;378:563–577.Google Scholar
35. Cammalleri, M, Cervia, D, Langenegger, D et al. Somatostatin receptors differentially affect spontaneous epileptiform activity in mouse hippocampal slices. Eur J Neurosci 2004;20:2711–2721.Google Scholar
36. Fehlmann, D, Langenegger, D, Schuebach, E, Siehler, S, Feuerbach, D, Hoyer, D. Distribution and characterisation of somatostatin receptor mRNA and binding sites in the brain and periphery. J Physiol Paris 2000;94:265–281.Google Scholar
37. Hannon, JP, Petrucci, C, Fehlmann, D, Viollet, C, Epelbaum, J, Hoyer, D. Somatostatin SST2 receptor knock-out mice: localization of SST1-5 receptor mRNA and binding in mouse brain by semi-quantitative RT-PCR, in situ hybridization histochemistry and receptor auroradiography. Neuropharmacology 2002;42:396–413.Google Scholar
38. Gale, K. Subcortical structures and pathways involved in convulsive seizure generation. J Clin Neurophysiol 1992;9:264–277.Google Scholar
39. Löscher, W, Ebert, U. The role of the piriform cortex in kindling. Prog Neurobiol 1996;50:427–481.Google Scholar
40. Aourz, N, DE Bundel, D, Stragier, B et al. Rat hippocampal somatostatin sst3 and sst4 receptors mediate anticonvulsive effects in vivo: indications of functional interaction with SST2 receptors. Neuropharmacology 2011;61:1327–1333.Google Scholar
41. Cammalleri, M, Martini, D, Timperio, AM, Bagnoli, P. Functional effects of somatostatin receptor 1 activation on synaptic transmission in the mouse hippocampus. J Neurochem 2009;111:1466–1477.Google Scholar
42. Moneta, D, Richichi, C, Aliprandi, M et al. Somatostatin receptor subtypes 2 and 4 affect seizure susceptibility and hippocampal excitatory neurotransmission in mice. Eur J Neurosci 2002;16:843–849.Google Scholar
43. Qiu, C, Zeyda, T, Johnson, B, Hochgeschwender, U, De Lecea, L, Tallent, MK. Somatostatin receptor subtype 4 couples to the M-current to regulate seizures. J Neurosci 2008;28:3567–3576.Google Scholar
44. Engin, E, Treit, D. Anxiolytic and antidepressant actions of somatostatin: the role of sst2 and SST3 receptors. Psychopharmacol (Berl) 2009;206:281–289.Google Scholar
45. Scheich, B, Gaszner, B, Kormos, V et al. Somatostatin receptor subtype 4 is involved in anxiety and depression-like behavior in mouse models. Psychopharmacol 2016;101:204–215.Google Scholar
46. Paxinos, G, Franklin, B. The mouse brain in stereotaxic coordinates. San Diego: Academic Press, 2001.Google Scholar
47. Christensen, DZ, Olesen, MV, Kristiansen, H, Mikkelsen, JD, Woldbye, DPD. Unaltered neuropeptide Y (NPY)-stimulated [35S]GTPgammaS binding suggests a net increase in NPY signalling after repeated electroconvulsive seizures in mice. J Neurosci Res 2006;84:1282–1291.Google Scholar
48. Woldbye, DPD, Nanobashvili, A, Sørensen, AT et al. Differential suppression of seizures via Y2 and Y5 neuropeptide Y receptors. Neurobiol Dis 2005;20:760–772.Google Scholar
49. Pannell, C, Simonian, SX, Gillies, GE, Luscher, B, Herbison, AE. Hypothalamic somatostatin and growth hormone-releasing hormone mRNA expression depend upon GABA(A) receptor expression in the developing mouse. Neuroendocrinology 2002;76:93–98.Google Scholar
50. Bates, CM, Kegg, H, Petrevski, C, Grady, S. Expression of somatostatin receptors 3, 4, and 5 in mouse kidney proximal tubules. Kidney Int 2003;63:53–63.Google Scholar
51. Hundahl, CA, Fahrenkrug, J, Hannibal, J. Neurochemical phenotype of cytoglobin-expressing neurons in the rat hippocampus. Biomed Reports 2014;2:620–627.Google Scholar
52. Drexel, M, Kirchmair, E, Wieselthaler-Hölzl, A, Preidt, AP, Sperk, G. Somatostatin and neuropeptide Y neurons undergo different plasticity in parahippocampal regions in kainic acid-induced epilepsy. J Neuropathol Exp Neurol 2012;71:312–329.Google Scholar
53. Pérez, J, Vezzani, G, Tutka, P, Rizzi, M, Schüpbach, E, Hoyer, D. Functional effects of D-Phe-c(Cys-Tyr-D-Trp-Lys-Val-Cys)-Trp-NH2 and differential changes in somatostatin receptor messenger RNAs, binding sites and somatostatin release in kainic acid-treated rats. Neuroscience 1995;65:1087–1097.Google Scholar
Supplementary material: File

Olesen et al. supplementary material

Olesen et al. supplementary material 1

Download Olesen et al. supplementary material(File)
File 22.8 KB