Hippocampal neurogenesis dysfunction linked to depressive-like behaviors in a neuroinflammation induced model of depression

Physiology and Behavior

Volumn 161, Issue , 2016, Pages 166-173

  Tang, Ming ming ^a,b   Lin, Wen juan ^a   Pan, Yu qin ^a   Guan, Xi ting ^a,b   Li, Ying cong ^a  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Depressive like behavior; Lipopolysaccharide; Neurogenesis; Neuroinflammation; Pro inflammatory cytokine

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; SACCHARIN; TUMOR NECROSIS FACTOR ALPHA; BROXURIDINE; CYTOKINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM DISEASE; DEPRESSION; HIPPOCAMPAL NEUROGENESIS DYSFUNCTION; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NOVELTY SUPPRESSED FEEDING TEST; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; TAIL SUSPENSION TEST; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENCEPHALITIS; EXPLORATORY BEHAVIOR; FOOD PREFERENCE; HIPPOCAMPUS; IMMOBILIZATION; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; BROMODEOXYURIDINE; CELL PROLIFERATION; CYTOKINES; DEPRESSION; DISEASE MODELS, ANIMAL; ENCEPHALITIS; EXPLORATORY BEHAVIOR; FOOD PREFERENCES; HINDLIMB SUSPENSION; HIPPOCAMPUS; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; NEUROGENESIS; RATS; RATS, SPRAGUE-DAWLEY; SACCHARIN; TIME FACTORS;

EID: 84964413556     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2016.04.034     Document Type: Article

References (49)

1. Dantzer R., Kelley K.W. Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 2007, 21:153-160.
2. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
3. Dunn A.J., Swiergiel A.H. Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol. Biochem. Behav. 2005, 81:688-693.
4. Maes M. Evidence for an immune response in major depression: a review and hypothesis. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 1995, 19:11-38.
5. Yirmiya R., Weidenfeld J., Pollak Y., Morag M., Morag A., Avitsur R., et al. Cytokines, "depression due to a general medical condition," and antidepressant drugs. Cytokines, stress, and depression 1999, 283-316. Springer.
6. McNally L., Bhagwagar Z., Hannestad J. Inflammation, glutamate, and glia in depression: a literature review. CNS Spectr. 2008, 13:501-510.
7. O'Connor J.C., Lawson M.A., Andre C., Moreau M., Lestage J., Castanon N., et al. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2.3-dioxygenase activation in mice. Mol. Psychiatry 2009, 14:511-522.
8. Wang D., Lin W., Pan Y., Kuang X., Qi X., Sun H. Chronic blockade of glucocorticoid receptors by RU486 enhances lipopolysaccharide-induced depressive-like behaviour and cytokine production in rats. Brain Behav. Immun. 2011, 25:706-714.
9. Krishnadas R., Cavanagh J. Depression: an inflammatory illness?. J. Neurol. Neurosurg. Psychiatry 2012, 83:495-502.
10. Maes M., Yirmyia R., Noraberg J., Brene S., Hibbeln J., Perini G., et al. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis. 2009, 24:27-53.
11. Emsley J.G., Mitchell B.D., Kempermann G., Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 2005, 75:321-341.
12. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
13. Jacobs B.L., van Praag H., Gage F.H. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol. Psychiatry 2000, 5:262-269.
14. Kempermann G., Krebs J., Fabel K. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr. Opin. Psychiatry 2008, 21:290-295.
15. Samuels B.A., Hen R. Neurogenesis and affective disorders. Eur. J. Neurosci. 2011, 33:1152-1159.
16. Hanson N.D., Owens M.J., Nemeroff C.B. Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 2011, 36:2589-2602.
17. Kohman R.A., Rhodes J.S. Neurogenesis, inflammation and behavior. Brain Behav. Immun. 2013, 27:22-32.
18. Ekdahl C.T., Kokaia Z., Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009, 158:1021-1029.
19. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
20. Guan X., Lin W., Tang M. Comparison of stress-induced and LPS-induced depressive-like behaviours and the alterations of central pro-inflammatory cytokines mRNA in rats. PsyCh Journal. 2015, 4(3):113-122.
21. Bluthé R.-M., Castanon N., Pousset F., Bristow A., Ball C., Lestage J., et al. Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats. Psychoneuroendocrinology 1999, 24:301-311.
22. Pan Y., Lin W., Wang W., Qi X., Wang D., Tang M. The effects of central pro-and anti-inflammatory immune challenges on depressive-like behavior induced by chronic forced swim stress in rats. Behav. Brain Res. 2013, 247:232-240.
23. Tang M., Pan Y., Lin W. A new animal model of depression induced by repeated central lipopolysaccharide administration. Acta Psychol. Sin. 2014, 46:639-646.
24. Cifuentes M., Perez-Martin M., Grondona J.M., Lopez-Avalos M.D., Inagaki N., Granados-Duran P., et al. A comparative analysis of intraperitoneal versus intracerebroventricular administration of bromodeoxyuridine for the study of cell proliferation in the adult rat brain. J. Neurosci. Methods 2011, 201:307-314.
25. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
26. Wann B.P., Audet M.C., Gibb J., Anisman H. Anhedonia and altered cardiac atrial natriuretic peptide following chronic stressor and endotoxin treatment in mice. Psychoneuroendocrinology 2010, 35:233-240.
27. Maes M., Berk M., Goehler L., Song C., Anderson G., Galecki P., et al. Depression and sickness behavior are Janus-faced responses to shared inflammatory pathways. BMC medicine. 2012, 10:66.
28. Caliyurt O., Altiay G. Resting energy expenditure in manic episode. Bipolar Disord. 2009, 11:102-106.
29. Silverman M.N., Mukhopadhyay P., Belyavskaya E., Tonelli L.H., Revenis B.D., Doran J.H., et al. Glucocorticoid receptor dimerization is required for proper recovery of LPS-induced inflammation, sickness behavior and metabolism in mice. Mol. Psychiatry 2013, 18:1006-1017.
30. Frenois F., Moreau M., O'Connor J., Lawson M., Micon C., Lestage J., et al. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 2007, 32:516-531.
31. O'Connor J.C., Andre C., Wang Y., Lawson M.A., Szegedi S.S., Lestage J., et al. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2.3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin. J. Neurosci. 2009, 29:4200-4209.
32. David D.J., Samuels B.A., Rainer Q., Wang J.W., Marsteller D., Mendez I., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
33. Johnson E., Kan R. The acute phase response and soman-induced status epilepticus: temporal, regional and cellular changes in rat brain cytokine concentrations. J. Neuroinflammation 2010, 7:40.
34. Elsayed M., Banasr M., Duric V., Fournier N.M., Licznerski P., Duman R.S. Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol. Psychiatry 2012, 72:258-265.
35. Fujioka H., Akema T. Lipopolysaccharide acutely inhibits proliferation of neural precursor cells in the dentate gyrus in adult rats. Brain Res. 2010, 1352:35-42.
36. Kyritsis N., Kizil C., Zocher S., Kroehne V., Kaslin J., Freudenreich D., et al. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 2012, 338:1353-1356.
37. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates: Hard Cover Edition 2006, Academic Press.
38. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 1996, 711:163-174.
39. Engeland C.G., Kavaliers M., Ossenkopp K.P. Influence of the estrous cycle on tolerance development to LPS-induced sickness behaviors in rats. Psychoneuroendocrinology 2006, 31:510-525.
40. Franklin A.E., Engeland C.G., Kavaliers M., Ossenkopp K.-P. The rate of behavioral tolerance development to repeated lipopolysaccharide treatments depends upon the time of injection during the light-dark cycle: a multivariable examination of locomotor activity. Behav. Brain Res. 2007, 180:161-173.
41. Franklin A.E., Engeland C.G., Kavaliers M., Ossenkopp K.P. Lipopolysaccharide-induced hypoactivity and behavioral tolerance development are modulated by the light-dark cycle in male and female rats. Psychopharmacology 2003, 170:399-408.
42. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13632-13637.
43. Bastos G.N., Moriya T., Inui F., Katura T., Nakahata N. Involvement of cyclooxygenase-2 in lipopolysaccharide-induced impairment of the newborn cell survival in the adult mouse dentate gyrus. Neuroscience 2008, 155:454-462.
44. Ho Y.C., Wang S. Adult neurogenesis is reduced in the dorsal hippocampus of rats displaying learned helplessness behavior. Neuroscience 2010, 171:153-161.
45. Jayatissa M.N., Bisgaard C., Tingstrom A., Papp M., Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 2006, 31:2395-2404.
46. Jayatissa M.N., Henningsen K., Nikolajsen G., West M.J., Wiborg O. A reduced number of hippocampal granule cells does not associate with an anhedonia-like phenotype in a rat chronic mild stress model of depression. Stress 2010, 13:95-105.
47. Vollmayr B., Simonis C., Weber S., Gass P., Henn F. Reduced cell proliferation in the dentate gyrusis not correlated with the development of learned helplessness. Biol. Psychiatry 2003, 54:1035-1040.
48. Hanson N.D., Owens M.J., Boss-Williams K.A., Weiss J.M., Nemeroff C.B. Several stressors fail to reduce adult hippocampal neurogenesis. Psychoneuroendocrinology 2011, 36:1520-1529.
49. Süß P., Kalinichenko L., Baum W., Reichel M., Kornhuber J., Loskarn S., et al. Hippocampal structure and function are maintained despite severe innate peripheral inflammation. Brain Behav. Immun. 2015, 49:156-170.