The Beneficial Impact of Antidepressant Drugs on Prenatal Stress-Evoked Malfunction of the Insulin-Like Growth Factor-1 (IGF-1) Protein Family in the Olfactory Bulbs of Adult Rats

Neurotoxicity Research

Volumn 29, Issue 2, 2016, Pages 288-298

  Trojan, Ewa ^a   Głombik, Katarzyna ^a   Ślusarczyk, Joanna ^a   Budziszewska, Bogusława ^a   Kubera, Marta ^a   Roman, Adam ^a   Lasoń, Władysław ^a   Basta Kaim, Agnieszka ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Antidepressant drugs; Insulin like growth factor 1 (IGF 1) family; Olfactory bulbs; Prenatal stress

Indexed keywords

ANTIDEPRESSANT AGENT; FLUOXETINE; IMIPRAMINE; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 6; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TIANEPTINE; INSULIN-LIKE GROWTH FACTOR-1, RAT; MESSENGER RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLIMBING; CONTROLLED STUDY; DEPRESSION; FEMALE; FORCED SWIM TEST; GENE EXPRESSION; IGF 1 GENE; IMMOBILITY; LONG TERM CARE; MALE; NONHUMAN; OLFACTORY BULB; PRENATAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SUBUNIT; RAT; SWIMMING; ANIMAL; COMPLICATION; DEPRESSIVE DISORDER; DISEASE MODEL; DRUG EFFECTS; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; FEMALE; INSULIN-LIKE GROWTH FACTOR I; MALE; MOTOR ACTIVITY; OLFACTORY BULB; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, IGF TYPE 1; RNA, MESSENGER; STRESS, PSYCHOLOGICAL;

EID: 84954397749     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-015-9575-3     Document Type: Article

References (57)

1. Ajo R, Cacicedo L, Navarro C, Sánchez-Franco F (2003) Growth hormone action on proliferation and differentiation of cerebral cortical cells from fetal rat. Endocrinology 144(3):1086–1097
2. Annuziata M, Granata R, Ghigo E (2011) The IGF system. Acta Diabetol 48(1):1–9
3. Ashpole NM, Sanders JE, Hodges EL, Yan H, Sonntag WE (2015) Growth hormone, insulin-like growth factor-1 and the aging brain. Exp Gerontol 68:76–81
4. Basta-Kaim A, Budziszewska B, Leśkiewicz M, Fijał K, Regulska M, Kubera M, Wędzony K, Lasoń W (2011) Hyperactivity of the hypothalamus-pituitary-adrenal axis in lipopolysaccharide-induced neurodevelopmental model of schizophrenia in rats: effects of antipsychotic drugs. Eur J Pharmacol 650(2–3):586–595
5. Basta-Kaim A, Szczesny E, Glombik K, Stachowicz K, Slusarczyk J, Nalepa I, Zelek-Molik A, Rafa-Zablocka K, Budziszewska B, Kubera M, Leskiewicz M, Lason W (2014) Prenatal stress affects insulin-like growth factor-1 (IGF-1) level and IGF-1 receptor phosphorylation in the brain of adult rats. Eur Neuropsychopharmacol 24(9):1546–1556
6. Bezchlibnyk YB, Wang JF, Shao L, Young LT (2006) Insulin-like growth factor binding protein-2 expression is decreased by lithium. NeuroReport 17(9):897–901
7. Bondy CA (1991) Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J Neurosci 11:3442–3455
8. Bourner MJ, Busby WH Jr, Siegel NR, Krivi GG, McCusker RH, Clemmons DR (1992) Cloning and sequence determination of bovine insulin-like growth factor binding protein-2 (IGFBP-2): comparison of its structural and functional properties with IGFBP-1. J Cell Biochem 48(2):215–226
9. Branchi I, Francia N, Alleva E (2004) Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behav Pharmacol 15:353–362
10. Bredt D, Furey ML, Chen G, Lovenberg T, Drevets WC, Manji HK (2015) Translating depression biomarkers for improved targeted therapies. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2015.09.013
11. Brooker GJ, Kalloniatis M, Russo VC, Murphy M, Werther GA, Bartlett PF (2000) Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells. J Neurosci Res 59:332–341
12. Budziszewska B, Szymanska M, Leskiewicz M, Basta-Kaim A, Jaworska-Feil L, Kubera M, Jantas D, Lason W (2010) The decrease in JNK- and p38-MAP kinase activity is accompanied by the enhancement of PP2A phosphate level in the brain of prenatally stressed rats. J Physiol Pharmacol 61(2):207–215
13. Bunn RC, King WD, Winkler MK, Fowlkes JL (2005) Early developmental changes in IGF-I, IGF-II, IGF binding protein-1, and IGF binding protein-3 concentration in the cerebrospinal fluid of children. Pediatr Res 58(1):89–93
14. Castren E (2004) Neurotrophic effects of antidepressant drugs. Curr Opin Pharmacol 4:58–64
15. Chesik D, De Keyser J, Wilczak N (2007) Insulin-like growth factor binding protein-2 as a regulator of IGF actions in CNS: implications in multiple sclerosis. Cytokine Growth Factor Rev 18(3–4):267–278
16. de Pablo F, de la Rosa EJ (1995) The developing CNS: a scenario for the action of proinsulin, insulin and insulin-like growth factors. Trends Neurosci 18(3):143–150
17. Detke MJ, Rickels M, Lucki I (1995) Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacol 121:66–72
18. Duman R (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med 5(1):11–25
19. Duman CH, Schlesinger L, Terwilliger R, Russell DS, Newton SS, Duman RS (2009) Peripheral insulin-like growth factor-I produces antidepressant-like behavior and contributes to the effect of exercise. Behav Brain Res 198(2):366–371
20. Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23:824–854
21. Freitas AE, Machado DG, Budni J, Neis VB, Balen GO, Lopes MW, de Souza LF, Dafre AL, Leal RB, Rodrigues AL (2013) Fluoxetine modulates hippocampal cell signaling pathways implicated in neuroplasticity in olfactory bulbectomized mice. Behav Brain Res 237:176–184
22. Grunbaum-Novak N, Taler M, Gil-Ad I, Weizman A, Cohen H, Weizman R (2008) Relationship between antidepressants and IGF-1 system in the brain: possible role in cognition. Eur Neuropsychopharmacol 18:431–438
23. Han VK, Matsell DG, Delhanty PJ, Hill DJ, Shimasaki S, Nygard K (1996) IGF-binding protein mRNAs in the human fetus: tissue and cellular distribution of developmental expression. Horm Res 45:160–166
24. Hoshaw BA, Malberg JE, Lucki I (2005) Central administration of IGF-I and BDNF leads to long-lasting antidepressant-like activity. Brain Res 1037(1–2):204–208
25. Hoshaw BA, Hill TI, Crowley JJ, Malberg JE, Khawaja X, Rosenzweig- Lipson S, Schechter LE, Lucki I (2008) Antidepressant-like behavioral effects of IGF-1 produced by enhanced serotonin transmission. Eur J Pharmacol 594(1–3):109–116
26. Hurtado-Chong A, Yusta-Boyo MJ, Vergaño-Vera E, Bulfone A, de Pablo F, Vicario-Abejón C (2009) IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci 30(5):742–755
27. Kalluri HS, Dempsey RJ (2011) IGFBP-3 inhibits the proliferation of neural progenitor cells. Neurochem Res 36(3):406–411
28. Kelly JP, Wrynn AS, Leonard BE (1997) The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 74:299–316
29. Khawaja X, Xu J, Liang JJ, Barrett JE (2004) Proteomic analysis of protein changes developing in rat hippocampus after chronic antidepressant treatment: implications for depressive disorders and future therapies. J Neurosci Res 75(4):451–460
30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
31. Machado DG, Cunha MP, Neis VB, Balen GO, Colla AR, Grando J, Brocardo PS, Bettio LE, Dalmarco JB, Rial D, Prediger RD, Pizzolatti MG, Rodrigues AL (2012) Rosmarinus officinalis L. hydroalcoholic extract, similar to fluoxetine, reverses depressive-like behavior without altering learning deficit in olfactory bulbectomized mice. J Ethnopharmacol 143(1):158–169
32. Matsui H, Noguchi T, Takakusaki K, Kashiwayanagi M (2014) Co-localization of TRPV2 and insulin-like growth factor-I receptor in olfactory neurons in adult and fetal mouse. Biol Pharm Bull 37(12):1907–1912
33. Mazerbourg S, Callebaut I, Zapf J, Mohan S, Overgaard M, Monget P (2004) Update on IGFBP-4: regulation of IGFBP-4 levels and functions, in vitro and in vivo. Growth Horm IGF Res 4(2):71–84
34. McEwen BS, Chattarji S, Diamond DM, Jay TM, Reagan LP, Svenningsson P, Fuchs E (2010) The neurobiological properties of tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation. Mol Psychiatry 15(3):237–249
35. Morley-Fletcher S, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S (2003) Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res 989(2):246–251
36. Morley-Fletcher S, Darnaudéry M, Mocaer E, Froger N, Lanfumey L, Laviola G, Casolini P, Zuena AR, Marzano L, Hamon M, Maccari S (2004) Chronic treatment with imipramine reverses immobility behaviour, hippocampal corticosteroid receptors and cortical 5-HT(1A) receptor mRNA in prenatally stressed rats. Neuropharmacology 47(6):841–847
37. Ning Y, Schuller AG, Conover CA, Pintar JE (2008) Insulin-like growth factor (IGF) binding protein-4 is both a positive and negative regulator of IGF activity in vivo. Mol Endocrinol 22(5):1213–1225
38. Ocrant I (1991) Insulin-like growth factor binding proteins in the nervous system. Adv Exp Med Biol 293:471–482
39. Ocrant I (1993) Insulin-like growth factor binding proteins in nervous-tissue-derived cells. Ann N Y Acad Sci 692:44–50
40. Pariante CM, Miller AH (2001) Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol Psychiatry 49(5):391–404
41. Pariante CM, Thomas SA, Lovestone S, Makoff A, Kerwin RW (2004) Do antidepressants regulate how cortisol affects the brain? Psychoneuroendocrinology 29(4):423–447
42. Paslakis G, Blum WF, Deuschle M (2012) Intranasal insulin-like growth factor I (IGF-I) as a plausible future treatment of depression. Med Hypotheses 79(2):222–225
43. Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391
44. Praveen Kumar VR, Sehgal P, Thota B, Patil S, Santosh V, Kondaiah P (2014) Insulin like growth factor binding protein 4 promotes GBM progression and regulates key factors involved in EMT and invasion. J Neurooncol 116(3):455–464
45. Rao U, McGinty DJ, Shinde A, McCracen JT, Poland RE (1999) Prenatal stress is associated with depression-related electroencephalographic sleep changes in adult males rats: a preliminary report. Prog Neuropsychopharmacol Biol Psychiatry 23:929–939
46. Russo VC, Bach LA, Fosang AJ, Baker NL, Werther GA (1997) Insulin-like growth factor binding protein-2 binds to cell surface proteoglycans in the rat brain olfactory bulb. Endocrinology 138:4858–4867
47. Russo VC, Gluckman PD, Feldman EL, Werther GA (2005) The insulin-like growth factor system and its pleiotropic functions in brain. Endocr Rev 6(7):916–943
48. Schilling C, Blum WF, Heuser I, Paslakis G, Deuschle M (2011) Treatment with antidepressants increases insulin-like growth factor-I in cerebrospinal fluid. J Clin Psychopharmacol 31:390–392
49. Song C, Leonard BE (2005) The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 29:627–647
50. Sowa J, Bobula B, Glombik K, Slusarczyk J, Basta-Kaim A, Hess G (2015) Prenatal stress enhances excitatory synaptic transmission and impairs long-term potentiation in the frontal cortex of adult offspring rats. PLoS One 10(3):e0119407
51. Szewczyk B, Kotarska K, Daigle M, Misztak P, Sowa-Kucma M, Rafalo A, Curzytek K, Kubera M, Basta-Kaim A, Nowak G, Albert PR (2014) Stress-induced alterations in 5-HT1A receptor transcriptional modulators NUDR and Freud-1. Int J Neuropsychopharmacol 17(11):1763–1775
52. Szymańska M, Budziszewska B, Jaworska-Feil L, Basta-Kaim A, Kubera M, Leśkiewicz M, Regulska M, Lasoń W (2009a) The effect of antidepressant drugs on the HPA axis activity, glucocorticoid receptor level and FKBP51 concentration in prenatally stressed rats. Psychoneuroendocrinology 34(6):822–832
53. Szymańska M, Suska A, Budziszewska B, Jaworska-Feil L, Basta-Kaim A, Leśkiewicz M, Kubera M, Gergont A, Kroczka S, Kaciński M, Lasoń W (2009b) Prenatal stress decreases glycogen synthase kinase-3 phosphorylation in the rat frontal cortex. Pharmacol Rep 61(4):612–620
54. Uzbekov MG (2009) Antidepressant action of tianeptine is connected with acceleration of serotonin turnover in the synapse: a hypothesis. Neuropsychopharmacol Hung 11(2):83–87
55. Werther GA, Russo V, Baker N, Butler G (1998) The role of the insulin-like growth factor system in the developing brain. Horm Res 49(1):37–40
56. Whitman MC, Greer CA (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89(2):162–175
57. Zueger M, Urani A, Chourbaji S, Zacher C, Roche M, Harkin A, Gass P (2005) Olfactory bulbectomy in mice induces alterations in exploratory behavior. Neurosci Lett 374(2):142–146