Running has differential effects on NPY, opiates, and cell proliferation in an animal model of depression and controls

Neuropsychopharmacology

Volumn 31, Issue 2, 2006, Pages 256-264

  Bjørnebekk, Astrid ^b   Mathé, Aleksander A ^a   Brené, Stefan ^a,b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Depression; Flinders Sensitive Line; Hippocampus; Neuropeptide Y; Opioid peptides; Physical activity

Indexed keywords

BROXURIDINE; DYNORPHIN; ENKEPHALIN; MESSENGER RNA; NEUROPEPTIDE Y; OPIATE PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORRELATION ANALYSIS; DENTATE GYRUS; DEPRESSION; HIPPOCAMPUS; MALE; NEUROTRANSMISSION; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RAT; REWARD; RUNNING; TREADMILL;

ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; DEPRESSION; DISEASE MODELS, ANIMAL; DYNORPHINS; ENKEPHALINS; EXERCISE THERAPY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEUROPEPTIDE Y; RATS; RATS, INBRED STRAINS; RUNNING;

EID: 30944440688     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300820     Document Type: Article

References (79)

1. Altman J (1962). Are new neurons formed in the brains of adult mammals? Science 135: 1127-1128.
2. Babyak M, Blumenthal JA, Herman S, Khatri P, Doraiswamy M, Moore K et al (2000). Exercise treatment for major depression: maintenance of therapeutic benefit at 10 months. Psychosom Med 62: 633-638.
3. Belke TW (1997). Running and responding reinforced by the opportunity to run: effect of reinforcer duration. J Exp Anal Behav 67: 337-351.
4. Bellmann R, Sperk G (1993). Effects of antidepressant drug treatment on levels of NPY or prepro-NPY-mRNA in the rat brain. Neurochem Int 22: 183-187.
5. Berrettini WH, Doran AR, Kelsoe J, Roy A, Pickar D (1987). Cerebrospinal fluid neuropeptide Y in depression and schizophrenia. Neuropsychopharmacology 1: 81-83.
6. Bjørnebekk A, Mathé AA, Brené S (2005). The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int J Neuropsychopharmacol Mar 15: 1-12 [Epub ahead of print].
7. Blumenthal JA, Babyak MA, Moore KA, Craighead WE, Herman S, Khatri P et al (1999). Effects of exercise training on older patients with major depression. Arch Intern Med 159: 2349-2356.
8. Bramham CR, Milgram NW, Srebro B (1991). Delta opioid receptor activation is required to induce LTP of synaptic transmission in the lateral perforant path in vivo. Brain Res 567: 42-50.
9. Britton KT, Southerland S, Van Uden E, Kirby D, Rivier J, Koob G (1997). Anxiolytic activity of NPY receptor agonists in the conflict test. Psychopharmacology (Berl) 132: 6-13.
10. Broom DC, Jutkiewicz EM, Folk JE, Traynor JR, Rice KC, Woods JH (2002). Nonpeptidic delta-opioid receptor agonists reduce immobility in the forced swim assay in rats. Neuropsychopharmacology 26: 744-755.
11. Buckland PR, Hoogendoorn B, Guy CA, Coleman SL, Smith SK, Buxbaum JD et al (2004). A high proportion of polymorphisms in the promoters of brain expressed genes influences transcriptional activity. Biochim Biophys Acta 1690: 238-249.
12. Caberlotto L, Jiménez P, Hurd YL, Mathé AA, Fuxe K (1999). Alterations in neuropeptide Y levels and Y1 binding sites in the Flinders Sensitive Line rats, a genetic animal model of depression. Neurosci Lett 265: 191-194.
13. Cole RL, Konradi C, Douglass J, Hyman SE (1995). Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 14: 813-823.
14. Douglass J, McMurray CT, Garrett JE, Adelman JP, Calavetta L (1989). Characterization of the rat prodynorphin gene. Mol Endocrinol 3: 2070-2078.
15. Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ et al (2003). VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18: 2803-2812.
16. Filliol D, Ghozland S, Chluba J, Martin M, Matthes HW, Simonin F et al (2000). Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat Genet 25: 195-200.
17. Gjerris A, Widerlöv E, Werdelin L, Ekman R (1992). Cerebrospinal fluid concentrations of neuropeptide Y in depressed patients and in controls. J Psychiatry Neurosci 17: 23-27.
18. Gross CG (2000). Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1: 67-73.
19. Hansel DE, Eipper BA, Ronnett GV (2001a). Neuropeptide Y functions as a neuroproliferative factor. Nature 410: 940-944.
20. Hansel DE, Eipper BA, Ronnett GV (2001b). Regulation of olfactory neurogenesis by amidated neuropeptides. J Neurosci Res 66: 1-7.
21. Heilig M, Söderpalm B, Engel JA, Widerlöv E (1989). Centrally administered neuropeptide Y (NPY) produces anxiolytic-like effects in animal anxiety models. Psychopharmacology (Berl) 98: 524-529.
22. Heilig M, Wahlestedt C, Ekman R, Widerlöv E (1988). Antidepressant drugs increase the concentration of neuropeptide Y (NPY)-like immunoreactivity in the rat brain. Eur J Pharmacol 147: 465-467.
23. Heilig M, Zachrisson O, Thorsell A, Ehnvall A, Mottagui-Tabar S, Sjogren M et al (2004). 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.
24. Husum H, Mathé AA (2002). Early life stress changes concentrations of neuropeptide Y and corticotropin-releasing hormone in adult rat brain. Lithium treatment modifies these changes. Neuropsychopharmacology 27: 756-764.
25. Husum H, Mikkelsen JD, Hogg S, Mathe AA, Mork A (2000). Involvement of hippocampal neuropeptide Y in mediating the chronic actions of lithium, electroconvulsive stimulation and citalopram. Neuropharmacology 39: 1463-1473.
26. Husum H, Termeer E, Mathé AA, Bolwig TG, Ellenbroek BA (2002). Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology 42: 798-806.
27. Husum H, Vasquez PA, Mathe AA (2001). Changed concentrations of tachykinins and neuropeptide Y in brain of a rat model of depression: lithium treatment normalizes tachykinins. Neuropsychopharmacology 24: 183-191.
28. Iversen IH (1993). Techniques for establishing schedules with wheel running as reinforcement in rats. J Exp Anal Behav 60: 219-238.
29. Jalava A, Mai S (1994). Fos and Jun form cell specific protein complexes at the neuropeptide tyrosine promoter. Oncogene 9: 2369-2375.
30. Jiménez Vasquez PA, Salmi P, Ahlenius S, Mathé AA (2000a). 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.
31. Jiménez-Vasquez PA, Mathé AA, Thomas JD, Riley EP, Ehlers CL (2001). Early maternal separation alters neuropeptide Y concentrations in selected brain regions in adult rats. Brain Res Dev Brain Res 131: 149-152.
32. Jiménez-Vasquez PA, Overstreet DH, Mathé AA (2000b). 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.
33. Larhammar D, Ericsson A, Persson H (1987). Structure and expression of the rat neuropeptide Y gene. Proc Natl Acad Sci USA 84: 2068-2072.
34. Lett BT, Grant VL, Koh MT (2001). Naloxone attenuates the conditioned place preference induced by wheel running in rats. Physiol Behav 72: 355-358.
35. Li BS, Kramer PR, Zhao W, Ma W, Stenger DA, Zhang L (2000). Molecular cloning, expression, and characterization of rat homolog of human AP-2alpha that stimulates neuropeptide Y transcription activity in response to nerve growth factor. Mol Endocrinol 14: 837-847.
36. Magni P, Beretta E, Scaccianoce E, Motta M (2000). Retinoic acid negatively regulates neuropeptide Y expression in human neuroblastoma cells. Neuropharmacology 39: 1628-1636.
37. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110.
38. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1988). Anatomy of CNS opioid receptors. Trends Neurosci 11: 308-314.
39. Martinsen EW (1990). Benefits of exercise for the treatment of depression. Sports Med 9: 380-389.
40. Martinsen EW, Hoffart A, Solberg O (1989). Comparing aerobic with nonaerobic forms of exercise in the treatment of clinical depression: a randomized trial. Comp Psychiatry 30: 324-331.
41. Martinsen EW, Medhus A, Sandvik L (1985). Effects of aerobic exercise on depression: a controlled study. Br Med J (Clin Res Edn) 291: 109.
42. Mathé AA (1999). Neuropeptides and electroconvulsive treatment. J ECT 15: 60-75.
43. Mathé AA, Andersson W, Angelucci F, El Khoury A, Gruber SHM, Husum H et al (2005). Search for biological correlates of depression and mechanisms of action of antidepressant treatment modalities. Do neuropeptides play a role? Physiol Behav, in press.
44. Mathé AA, Gruber S (2004). Neuropeptide Y has marked antidepressant properties in a rat model of depression. Neuropsychopharmacology 29(Suppl): 154.
45. Mathé AA, Gruber S, Jiménez PA, Theodorsson E, Stenfors C (1997). Effects of electroconvulsive stimuli and MK-801 on neuropeptide Y, neurokinin A, and calcitonin gene-related peptide in rat brain. Neurochem Res 22: 629-636.
46. Mathé AA, Jimenéz PA, Theodorsson E, Stenfors C (1998). 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.
47. Mathé AA, Jousisto-Hanson J, Stenfors C, Theodorsson E (1990). Effect of lithium on tachykinins, calcitonin-gene-related peptide, and neuropeptide Y in rat brain. J Neurosci Res 26: 233-237.
48. Mathé AA, Norstedt Wikner B, Stenfors C, Theodorsson E (1994). Effects of lithium on neuropeptide Y, neurokinin A and substance P in brain and peripheral tissues of rat. Lithium 5: 241-247.
49. Mathé AA, Rudorfer MV, Stenfors C, Manji HK, Potter WC, Theodorsson E (1996). Effects of electroconvulsive treatment on somatostatin, neuropeptide Y, endothelin and neurokinin. A concentration in cerebrospinal fluid of depressed patients. Depression 3: 250-256.
50. Mikkelsen JD, Woldbye D, Kragh J, Larsen PJ, Bolwig TG (1994). Electroconvulsive shocks increase the expression of neuropeptide Y (NPY) mRNA in the piriform cortex and the dentate gyrus. Brain Res Mol Brain Res 23: 317-322.
51. Nikisch G, Ågren H, Chin B, Czernik A, Baumann P, Mathé AA (2005). Neuropeptide Y and corticotropin-releasing hormone in CSF mark response to antidepressant treatment with citalopram. Int J Neuropsychopharmacol Mar 23: 1-8 [Epub ahead of print].
52. Nilsson C, Karlsson G, Blennow K, Heilig M, Ekman R (1996). Differences in the neuropeptide Y-like immunoreactivity of the plasma and platelets of human volunteers and depressed patients. Peptides 17: 359-362.
53. Overstreet DH (1993). The Flinders sensitive line rats: a genetic animal model of depression. Neurosci Biobehav Rev 17: 51-68.
54. Overstreet DH, Pucilowski O, Rezvani AH, Janowsky DS (1995). Administration of antidepressants, diazepam and psychomotor stimulants further confirms the utility of Flinders Sensitive Line rats as an animal model of depression. Psychopharmacology (Berl) 121: 27-37.
55. Overstreet DH, Russell RW, Helps SC, Messenger M (1979). Selective breeding for sensitivity to the anticholinesterase DFP. Psychopharmacology (Berl) 65: 15-20.
56. Persson AI, Thorlin T, Bull C, Zarnegar P, Ekman R, Terenius L et al (2003). Mu- and delta-opioid receptor antagonists decrease proliferation and increase neurogenesis in cultures of rat adult hippocampal progenitors. Eur J Neurosci 17: 1159-1172.
57. Pfeiffer A, Brantl V, Herz A, Emrich HM (1986). Psychotomimesis mediated by kappa opiate receptors. Science 233: 774-776.
58. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA (2001). Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21: 7397-7403.
59. Pucilowski O, Overstreet DH, Rezvani AH, Janowsky DS (1993). Chronic mild stress-induced anhedonia: greater effect in a genetic rat model of depression. Physiol Behav 54: 1215-1220.
60. Russell RW, Overstreet DH, Messenger M, Helps SC (1982). Selective breeding for sensitivity to DFP: generalization of effects beyond criterion variables. Pharmacol Biochem Behav 17: 885-891.
61. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809.
62. Shirayama Y, Ishida H, Iwata M, Hazama GI, Kawahara R, Duman RS (2004). Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem 90: 1258-1268.
63. Spanagel R, Herz A, Shippenberg TS (1992). Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci USA 89: 2046-2050.
64. Stenfors C, Theodorsson E, Mathé AA (1989). Effect of repeated electroconvulsive treatment on regional concentrations of tachykinins, neurotensin, vasoactive intestinal polypeptide, neuropeptide Y, and galanin in rat brain. J Neurosci Res 24: 445-450.
65. Stogner KA, Holmes PV (2000). Neuropeptide-Y exerts antidepressant-like effects in the forced swim test in rats. Eur J Pharmacol 387: R9-10.
66. Strawbridge WJ, Deleger S, Roberts RE, Kaplan GA (2002). Physical activity reduces the risk of subsequent depression for older adults. Am J Epidemiol 156: 328-334.
67. Tejedor-Real P, Mico JA, Smadja C, Maldonado R, Roques BP, Gilbert-Rahola J (1998). Involvement of delta-opioid receptors in the effects induced by endogenous enkephalins on learned helplessness model. Eur J Pharmacol 354: 1-7.
68. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96: 13427-13431.
69. Wagner JJ, Terman GW, Chavkin C (1993). Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363: 451-454.
70. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ et al (2002). Delta FosB regulates wheel running. J Neurosci 22: 8133-8138.
71. Werme M, Thoren P, Olson L, Brené S (1999). Addiction-prone Lewis but not Fischer rats develop compulsive running that coincides with downregulation of nerve growth factor inducible-B and neuron-derived orphan receptor 1. J Neurosci 19: 6169-6174.
72. Werme M, Thoren P, Olson L, Brené S (2000). Running and cocaine both upregulate dynorphin mRNA in medial caudate putamen. Eur J Neurosci 12: 2967-2974.
73. Wernersson J, Johansson I, Larsson U, Minth-Worby C, Pahlman S, Andersson G (1998). Activated transcription of the human neuropeptide Y gene in differentiating SH-SY5Y neuroblastoma cells is dependent on transcription factors AP-1, AP-2alpha, and NGFI. J Neurochem 70: 1887-1897.
74. West MJ, Slomianka L, Gundersen HJ (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
75. Widdowson PS, Ordway GA, Halaris AE (1992). Reduced neuropeptide Y concentrations in suicide brain. J Neurochem 59: 73-80.
76. Widerlov E, Lindstrom LH, Wahlestedt C, Ekman R (1988). Neuropeptide Y and peptide YY as possible cerebrospinal fluid markers for major depression and schizophrenia, respectively. J Psychiatr Res 22: 69-79.
77. Woldbye DP, Nanobashvili A, Husum H, Bolwig TG, Kokaia M (2002). Neuropeptide Y inhibits in vitro epileptiform activity in the entorhinal cortex of mice. Neurosci Lett 333: 127-130.
78. Zachrisson O, Mathé AA, Stenfors C, Lindefors N (1995). Limbic effects of repeated electroconvulsive stimulation on neuropeptide Y and somatostatin mRNA expression in the rat brain. Brain Res Mol Brain Res 31: 71-85.
79. Zurawski G, Benedik M, Kamb BJ, Abrams JS, Zurawski SM, Lee FD (1986). Activation of mouse T-helper cells induces abundant preproenkephalin mRNA synthesis. Science 232: 772-775.