Involvement of neuropeptide Y signaling in the antidepressant-like effect and hippocampal cell proliferation induced by Kososan, a Kampo medicine, in the stress-induced depression-like model mice

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 10, 2012, Pages 1775-1783

  Ito, Naoki ^a   Hori, Atsushi ^a   Yabe, Takeshi ^a   Nagai, Takayuki ^a   Oikawa, Tetsuro ^a   Yamada, Haruki ^a   Hanawa, Toshihiko ^a  

^a KITASATO UNIVERSITY   (Japan)

Author keywords

Antidepressant like effect; Cell proliferation; Kososan; Neuropeptide Y; Orexin A

Indexed keywords

KAMPO; KOSOSAN; N2 DIPHENYLACETYL N (4 UREIDOMETHYLBENZYL)ARGININAMIDE; NEUROPEPTIDE Y; NEUROPEPTIDE Y RECEPTOR ANTAGONIST; NEUROPEPTIDE Y1 RECEPTOR; OREXIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BLOOD LEVEL; BRAIN NERVE CELL; CELL PROLIFERATION; CONTROLLED STUDY; DEPRESSION; HIPPOCAMPUS; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; PHYSICALLY INDUCED STRESS; SIGNAL TRANSDUCTION; TREATMENT DURATION;

ANIMALS; ANTIDEPRESSIVE AGENTS; ARGININE; CELL PROLIFERATION; DEPRESSION; DISEASE MODELS, ANIMAL; DRUGS, CHINESE HERBAL; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEDICINE, KAMPO; MICE; NEUROPEPTIDE Y; NEUROPEPTIDES; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84867276420     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b12-00466     Document Type: Article

References (65)

1. Balasubramaniam AA. Neuropeptide Y family of hormones: receptor subtypes and antagonists. Peptides, 18, 445-457 (1997).
2. Stanley BG, Leibowitz SF. Neuropeptide Y injected in the paraventricular hypothalamus: a powerful stimulant of feeding behavior. Proc. Natl. Acad. Sci. U.S.A., 82, 3940-3943 (1985).
3. Marsh DJ, Hollopeter G, Kafer KE, Palmiter RD. Role of the Y5 neuropeptide Y receptor in feeding and obesity. Nat. Med., 4, 718-721 (1998).
4. Fujimiya M, Inui A. Peptidergic regulation of gastrointestinal motility in rodents. Peptides, 21, 1565-1582 (2000).
5. Albers HE, Ferris CF. Neuropeptide Y: role in light-dark cycle entrainment of hamster circadian rhythms. Neurosci. Lett., 50, 163-168 (1984).
6. Flood JF, Hernandez EN, Morley JE. Modulation of memory processing by neuropeptide Y. Brain Res., 421, 280-290 (1987).
7. Redrobe JP, Dumont Y, St-Pierre JA, Quirion R. Multiple receptors for neuropeptide Y in the hippocampus: putative roles in seizures and cognition. Brain Res., 848, 153-166 (1999).
8. Vezzani A, Sperk G, Colmers WF. Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci., 22, 25-30 (1999).
9. Sajdyk TJ, Vandergriff MG, Gehlert DR. Amygdalar neuropeptide Y Y1 receptors mediate the anxiolytic-like actions of neuropeptide Y in the social interaction test. Eur. J. Pharmacol., 368, 143-147 (1999).
10. Sparta DR, Fee JR, Knapp DJ, Breese GR, Thiele TE. Elevated anxiety-like behavior following ethanol exposure in mutant mice lacking neuropeptide Y (NPY). Drug Alcohol Depend., 90, 297-300 (2007).
11. Sergeyev V, Fetissov S, Mathé AA, Jimenez PA, Bartfai T, Mortas P, Gaudet L, Moreau JL, Hökfelt T. Neuropeptide expression in rats exposed to chronic mild stresses. Psychopharmacology (Berl.), 178, 115-124 (2005).
12. Ishida H, Shirayama Y, Iwata M, Kawahara R. Subchronic treatment with imipramine ameliorates the decreased number in neuropeptide Y-positive cells in the hippocampus of learned helplessness rats. Brain Res., 1046, 239-243 (2005).
13. Jiménez-Vasquez PA, Mathé AA, Thomas JD, Riley EP, Ehlers CL. Early maternal separation alters neuropeptide Y concentrations in selected brain regions in adult rats. Brain Res. Dev. Brain Res., 131, 149-152 (2001).
14. Husum H, Termeer E, Mathé AA, Bolwig TG, Ellenbroek BA. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology, 42, 798-806 (2002).
15. Caberlotto L, Fuxe K, Overstreet DH, Gerrard P, Hurd YL. Alterations in neuropeptide Y and Y1 receptor mRNA expression in brains from an animal model of depression: region specific adaptation after fluoxetine treatment. Brain Res. Mol. Brain Res., 59, 58-65 (1998).
16. Jiménez Vasquez PA, Salmi P, Ahlenius S, Mathé AA. Neuropeptide Y in brains of the Flinders Sensitive Line rat, a model of depression. Effects of electroconvulsive stimuli and D-amphetamine on peptide concentrations and locomotion. Behav. Brain Res., 111, 115-123 (2000).
17. Jiménez-Vasquez PA, Overstreet DH, Mathé AA. Neuropeptide Y in male and female brains of Flinders Sensitive Line, a rat model of depression. Effects of electroconvulsive stimuli. J. Psychiatr. Res., 34, 405-412 (2000).
18. Jiménez-Vasquez PA, Diaz-Cabiale Z, Caberlotto L, Bellido I, Overstreet D, Fuxe K, Mathé AA. Electroconvulsive stimuli selectively affect behavior and neuropeptide Y (NPY) and NPY Y(1) receptor gene expressions in hippocampus and hypothalamus of Flinders Sensitive Line rat model of depression. Eur. Neuropsychopharmacol., 17, 298-308 (2007).
19. Mathé AA, Jimenez PA, Theodorsson E, Stenfors C. Neuropeptide Y, neurokinin A and neurotensin in brain regions of Fawn Hooded "depressed," Wistar, and Sprague Dawley rats. Effects of electroconvulsive stimuli. Prog. Neuropsychopharmacol. Biol. Psychiatry, 22, 529-546 (1998).
20. Wörtwein G, Husum H, Andersson W, Bolwig TG, Mathé AA. Effects of maternal separation on neuropeptide Y and calcitonin gene-related peptide in "depressed" Flinders Sensitive Line rats: a study of gene-environment interactions. Prog. Neuropsychopharmacol. Biol. Psychiatry, 30, 684-693 (2006).
21. Husum H, Van Kammen D, Termeer E, Bolwig G, Mathé A. Topiramate normalizes hippocampal NPY-LI in flinders sensitive line 'depressed' rats and upregulates NPY, galanin, and CRH-LI in the hypothalamus: implications for mood-stabilizing and weight loss-inducing effects. Neuropsychopharmacology, 28, 1292-1299 (2003).
22. Bjørnebekk A, Mathé AA, Brené S. Running has differential effects on NPY, opiates, and cell proliferation in an animal model of depression and controls. Neuropsychopharmacology, 31, 256-264 (2006).
23. Redrobe JP, Dumont Y, Fournier A, Quirion R. The neuropeptide Y (NPY) Y1 receptor subtype mediates NPY-induced antidepressant-like activity in the mouse forced swimming test. Neuropsychopharmacology, 26, 615-624 (2002).
24. Ishida H, Shirayama Y, Iwata M, Katayama S, Yamamoto A, Kawahara R, Nakagome K. Infusion of neuropeptide Y into CA3 region of hippocampus produces antidepressant-like effect via Y1 receptor. Hippocampus, 17, 271-280 (2007).
25. Stogner KA, Holmes PV. Neuropeptide-Y exerts antidepressant-like effects in the forced swim test in rats. Eur. J. Pharmacol., 387, R9-R10 (2000).
26. Luo DD, An SC, Zhang X. Involvement of hippocampal serotonin and neuropeptide Y in depression induced by chronic unpredicted mild stress. Brain Res. Bull., 77, 8-12 (2008).
27. Hansel DE, Eipper BA, Ronnett GV. Neuropeptide Y functions as a neuroproliferative factor. Nature, 410, 940-944 (2001).
28. Howell OW, Scharfman HE, Herzog H, Sundstrom LE, Beck-Sickinger A, Gray WP. Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem., 86, 646-659 (2003).
29. Howell OW, Doyle K, Goodman JH, Scharfman HE, Herzog H, Pringle A, Beck-Sickinger AG, Gray WP. Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem., 93, 560-570 (2005).
30. Howell OW, Silva S, Scharfman HE, Sosunov AA, Zaben M, Shatya A, McKhann G 2nd, Herzog H, Laskowski A, Gray WP. Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol. Dis., 26, 174-188 (2007).
31. Decressac M, Wright B, David B, Tyers P, Jaber M, Barker RA, Gaillard A. Exogenous neuropeptide Y promotes in vivo hippocampal neurogenesis. Hippocampus, 21, 233-238 (2011).
32. Kendler KS, Karkowski LM, Prescott CA. Causal relationship between stressful life events and the onset of major depression. Am. J. Psychiatry, 156, 837-841 (1999).
33. Joëls M, Karst H, Alfarez D, Heine VM, Qin Y, van Riel E, Verkuyl M, Lucassen PJ, Krugers HJ. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress, 7, 221-231 (2004).
34. Widerlöv E, Lindström LH, Wahlestedt C, Ekman R. Neuropeptide Y and peptide YY as possible cerebrospinal fluid markers for major depression and schizophrenia, respectively. J. Psychiatr. Res., 22, 69-79 (1988).
35. Gjerris A, Widerlöv E, Werdelin L, Ekman R. Cerebrospinal fluid concentrations of neuropeptide Y in depressed patients and in controls. J. Psychiatry Neurosci., 17, 23-27 (1992).
36. Heilig M, Zachrisson O, Thorsell A, Ehnvall A, Mottagui-Tabar S, Sjögren M, Asberg M, Ekman R, Wahlestedt C, Agren H. Decreased cerebrospinal fluid neuropeptide Y (NPY) in patients with treatment refractory unipolar major depression: preliminary evidence for association with preproNPY gene polymorphism. J. Psychiatr. Res., 38, 113-121 (2004).
37. Hou C, Jia F, Liu Y, Li L. CSF serotonin, 5-hydroxyindolacetic acid and neuropeptide Y levels in severe major depressive disorder. Brain Res., 1095, 154-158 (2006).
38. Nikisch G, Mathé AA. CSF monoamine metabolites and neuropeptides in depressed patients before and after electroconvulsive therapy. Eur. Psychiatry, 23, 356-359 (2008).
39. Nikisch G, Agren H, Eap CB, Czernik A, Baumann P, Mathé AA. Neuropeptide Y and corticotropin-releasing hormone in CSF mark response to antidepressive treatment with citalopram. Int. J. Neuropsychopharmacol., 8, 403-410 (2005).
40. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell, 92, 573-585 (1998).
41. Allard JS, Tizabi Y, Shaffery JP, Trouth CO, Manaye K. Stereological analysis of the hypothalamic hypocretin/orexin neurons in an animal model of depression. Neuropeptides, 38, 311-315 (2004).
42. Brundin L, Petersén A, Björkqvist M, Träskman-Bendz L. Orexin and psychiatric symptoms in suicide attempters. J. Affect. Disord., 100, 259-263 (2007).
43. Brundin L, Björkqvist M, Petersén A, Träskman-Bendz L. Reduced orexin levels in the cerebrospinal fluid of suicidal patients with major depressive disorder. Eur. Neuropsychopharmacol., 17, 573-579 (2007).
44. Lutter M, Krishnan V, Russo SJ, Jung S, McClung CA, Nestler EJ. Orexin signaling mediates the antidepressant-like effect of calorie restriction. J. Neurosci., 28, 3071-3075 (2008).
45. Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky SA, Anderson JG, Jung S, Birnbaum S, Yanagisawa M, Elmquist JK, Nestler EJ, Zigman JM. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat. Neurosci., 11, 752-753 (2008).
46. Ito N, Yabe T, Gamo Y, Nagai T, Oikawa T, Yamada H, Hanawa T. I.c.v. administration of orexin-A induces an antidepressive-like effect through hippocampal cell proliferation. Neuroscience, 157, 720-732 (2008).
47. Hanawa T. Kososan and Hangekobokuto. Journal of Kampo Medicine, 42, 418-426 (1995).
48. Ito N, Nagai T, Yabe T, Nunome S, Hanawa T, Yamada H. Antidepressant-like activity of a Kampo (Japanese herbal) medicine, Koso-san (Xiang-Su-San), and its mode of action via the hypothalamic-pituitary-adrenal axis. Phytomedicine, 13, 658-667 (2006).
49. Nagai T, Narikawa T, Ito N, Takeda T, Hanawa T, Yamada H. Antidepressant-like effect of a Kampo (Japanese herbal) medicine, kososan, against the interferon-α-induced depressive-like model mice. J. Trad. Med., 25, 74-80 (2008).
50. Ito N, Yabe T, Nagai T, Oikawa T, Yamada H, Hanawa T. A possible mechanism underlying an antidepressive-like effect of Kososan, a Kampo medicine, via the hypothalamic orexinergic system in the stress-induced depression-like model mice. Biol. Pharm. Bull., 32, 1716-1722 (2009).
51. Porsolt RD, Bertin A, Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther., 229, 327-336 (1977).
52. Detke MJ, Johnson J, Lucki I. Acute and chronic antidepressant drug treatment in the rat forced swimming test model of depression. Exp. Clin. Psychopharmacol., 5, 107-112 (1997).
53. Solberg LC, Horton TH, Turek FW. Circadian rhythms and depression: effects of exercise in an animal model. Am. J. Physiol., 276, R152-R161 (1999).
54. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl.), 93, 358-364 (1987).
55. Higuchi H, Yang HY. Splanchnic nerve transection abolishes the age-dependent increase of neuropeptide Y-like immunoreactivity in rat adrenal gland. J. Neurochem., 46, 1658-1660 (1986).
56. Ekblad E, Håkanson R, Sundler F. VIP and PHI coexist with an NPY-like peptide in intramural neurones of the small intestine. Regul. Pept., 10, 47-55 (1984).
57. Chen H, Pandey GN, Dwivedi Y. Hippocampal cell proliferation regulation by repeated stress and antidepressants. Neuroreport, 17, 863-867 (2006).
58. Kastin AJ, Akerstrom V. Orexin A but not orexin B rapidly enters brain from blood by simple diffusion. J. Pharmacol. Exp. Ther., 289, 219-223 (1999).
59. Muroya S, Funahashi H, Yamanaka A, Kohno D, Uramura K, Nambu T, Shibahara M, Kuramochi M, Takigawa M, Yanagisawa M, Sakurai T, Shioda S, Yada T. Orexins (hypocretins) directly interact with neuropeptide Y, POMC and glucose-responsive neurons to regulate Ca2+ signaling in a reciprocal manner to leptin: orexigenic neuronal pathways in the mediobasal hypothalamus. Eur. J. Neurosci., 19, 1524-1534 (2004).
60. Kharlamov EA, Kharlamov A, Kelly KM. Changes in neuropeptide Y protein expression following photothrombotic brain infarction and epileptogenesis. Brain Res., 1127, 151-162 (2007).
61. Elias CF, Saper CB, Maratos-Flier E, Tritos NA, Lee C, Kelly J, Tatro JB, Hoffman GE, Ollmann MM, Barsh GS, Sakurai T, Yanagi sawa M, Elmquist JK. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J. Comp. Neurol., 402, 442-459 (1998).
62. Horvath TL, Peyron C, Diano S, Ivanov A, Aston-Jones G, Kilduff TS, van Den Pol AN. Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J. Comp. Neurol., 415, 145-159 (1999).
63. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature, 404, 661-671 (2000).
64. Saper CB, Chou TC, Elmquist JK. The need to feed: homeostatic and hedonic control of eating. Neuron, 36, 199-211 (2002).
65. Fu LY, Acuna-Goycolea C, van den Pol AN. Neuropeptide Y inhibits hypocretin/orexin neurons by multiple presynaptic and postsynaptic mechanisms: tonic depression of the hypothalamic arousal system. J. Neurosci., 24, 8741-8751 (2004).