Hippocampal structure and function are maintained despite severe innate peripheral inflammation

Brain, Behavior, and Immunity

Volumn 49, Issue , 2015, Pages 156-170

  Süß, Patrick ^a   Kalinichenko, Liubov ^a   Baum, Wolfgang ^a   Reichel, Martin ^a   Kornhuber, Johannes ^a   Loskarn, Sandra ^a   Ettle, Benjamin ^a   Distler, Jörg H W ^a   Schett, Georg ^a   Winkler, Jürgen ^a   Müller, Christian P ^a   Schlachetzki, Johannes C M ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Adult hippocampal neurogenesis; Anxiety; Depression; Locomotion; Neuroinflammation; Peripheral inflammation

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; AUTACOID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; ASTROCYTOSIS; BRAIN FUNCTION; BRAIN SIZE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DEPRESSION; DISEASE SEVERITY; FEMALE; GENE EXPRESSION REGULATION; GLIOSIS; HIPPOCAMPUS; IL 1BETA GENE; IL 6 GENE; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; MALE; MONOCYTOSIS; MOTOR DYSFUNCTION; MOUSE; NERVE CELL PLASTICITY; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SPLEEN; TRANSGENIC MOUSE; ANIMAL; BLOOD; C57BL MOUSE; COMPLICATION; DEPRESSIVE DISORDER; ENCEPHALITIS; GENETICS; HUMAN; IMMUNOLOGY; MOTOR ACTIVITY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT;

ANIMALS; ARTHRITIS; DEPRESSIVE DISORDER; ENCEPHALITIS; FEMALE; HIPPOCAMPUS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84940592528     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.05.011     Document Type: Article

References (78)

1. Balu D.T., Lucki I. Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci. Biobehav. Rev. 2009, 33(3):232-252.
2. Banks W.A. The blood-brain barrier in psychoneuroimmunology. Neurol. Clin. 2006, 24:413-419.
3. Banks W.A., Kastin A.J., Ehrensing C.A. Diurnal uptake of circulating interleukin-1alpha by brain, spinal cord, testis and muscle. Neuroimmunomodulation 1998, 5:36-41.
4. Baruch K., Schwartz M. CNS-specific T cells shape brain function via the choroid plexus. Brain Behav. Immun. 2013, 34:11-16.
5. Baruch K., Ron-Harel N., Gal H., Deczkowska A., Shifrut E., Ndifon W., et al. CNS-specific immunity at the choroid plexus shifts toward destructive Th2 inflammation in brain aging. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:2264-2269.
6. Belmaker R.H., Agam G. Major depressive disorder. N. Engl. J. Med. 2008, 358(1):55-68.
7. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol. Cell. Neurosci. 2003, 24:623-631.
8. Bluthe R.M., Pawlowski M., Suarez S., Parnet P., Pittman Q., Kelley K.W., et al. Synergy between tumor necrosis factor alpha and interleukin-1 in the induction of sickness behavior in mice. Psychoneuroendocrinology 1994, 19:197-207.
9. Bluthe R.M., Walter V., Parnet P., Laye S., Lestage J., Verrier D., et al. Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C. R. Acad. Sci. III 1994, 317:499-503.
10. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am. J. Psychiatry 2000, 157(1):115-118.
11. Brustolim D., Ribeiro-dos-Santos R., Kast R.E., Altschuler E.L., Soares M.B. A new chapter opens in anti-inflammatory treatments: the antidepressant bupropion lowers production of tumor necrosis factor-alpha and interferon-gamma in mice. Int. Immunopharmacol. 2006, 6(6):903-907.
12. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
13. Capuron L., Miller A.H. Cytokines and psychopathology: lessons from interferon-alpha. Biol. Psychiatry 2004, 56(11):819-824.
14. Chen X.X., Baum W., Dwyer D., Stock M., Schwabe K., Ke H.Z., et al. Sclerostin inhibition reverses systemic, periarticular and local bone loss in arthritis. Ann. Rheum. Dis. 2013, 72:1732-1736.
15. Couch Y., Alvarez-Erviti L., Sibson N.R., Wood M.J., Anthony D.C. The acute inflammatory response to intranigral α-synuclein differs significantly from intranigral lipopolysaccharide and is exacerbated by peripheral inflammation. J. Neuroinflamm. 2011, 8:166.
16. Covic T., Cumming S.R., Pallant J.F., Manolios N., Emery P., Conaghan P.G., et al. Depression and anxiety in patients with rheumatoid arthritis: prevalence rates based on a comparison of the Depression, Anxiety and Stress Scale (DASS) and the hospital, Anxiety and Depression Scale (HADS). BMC Psychiatry 2012, 12:6.
17. Crawley J., Goodwin F.K. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav. 1980, 13:167-170.
18. 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(1):46-56.
19. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., et al. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67(5):446-457.
20. Dranovsky A., Picchini A.M., Moadel T., Sisti A.C., Yamada A., Kimura S., et al. Experience dictates stem cell fate in the adult hippocampus. Neuron 2011, 70:908-923.
21. Easton A.C., Lucchesi W., Schumann G., Giese K.P., Müller C.P., Fernandes C. αCaMKII autophosphorylation controls exploratory activity to threatening novel stimuli. Neuropharmacology 2011, 61:1424-1431.
22. 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(23):13632-13637.
23. Gould E., Tanapat P., McEwen B.S., Flügge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3168-3171.
24. Hall C.S. Drive and emotionality: factors associated with adjustment in the rat. J. Comp. Psychol. 1934, 17:89-108.
25. Han Q.Q., Yu J. Inflammation: a mechanism of depression?. Neurosci. Bull. 2014, 30(3):515-523.
26. Hayward M.D., Jones B.K., Saparov A., Hain H.S., Trillat A.C., Bunzel M.M., et al. An extensive phenotypic characterization of the hTNFα transgenic mice. BMC Physiol. 2007, 7:13.
27. Hess A., Axmann R., Rech J., Finzel S., Heindl C., Kreitz S., et al. Blockade of TNF-α rapidly inhibits pain responses in the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3731-3736.
28. Himmerich H., Fulda S., Linseisen J., Seiler H., Wolfram G., Himmerich S., et al. Depression, comorbidities and the TNF-alpha system. Eur. Psychiatry 2008, 23(6):421-429.
29. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71(2):171-186.
30. Huang H.C., Yu H.R., Huang L.T., Huang H.C., Chen R.F., Lin I.C., et al. MiRNA-125b regulates TNF-α production in CD14+ neonatal monocytes via post-transcriptional regulation. J. Leukoc. Biol. 2012, 92:171-182.
31. 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.
32. Karrenbauer B.D., Müller C.P., Ho Y.J., Spanagel R., Huston J.P., Schwarting R.K.W., et al. Time-dependent in-vivo effects of interleukin-2 on neurotransmitters in various cortices: relationships with depressive-related and anxiety-like behaviour. J. Neuroimmunol. 2011, 237:23-32.
33. Keffer J., Probert L., Cazlaris H., Georgopoulos S., Kaslaris E., Kioussis D., et al. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J. 1991, 10:4025-4031.
34. Kontoyiannis D., Pasparakis M., Pizarro T.T., Cominelli F., Kollias G. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 1999, 10:387-398.
35. Kozlowski C., Weimer R.M. An automated method to quantify microglia morphology and application to monitor activation state longitudinally in vivo. PLoS ONE 2012, 7:e31814.
36. Kumar B., Kuhad A., Chopra K. Neuropsychopharmacological effect of sesamol in unpredictable chronic mild stress model of depression: behavioral and biochemical evidences. Psychopharmacology (Berl.) 2011, 214(4):819-828.
37. Lang V.R., Mielenz D., Neubert K., Bohm C., Schett G., Jack H.M., et al. The early marginal zone B cell-initiated T-independent type 2 response resists the proteasome inhibitor bortezomib. J. Immunol. 2010, 185:5637-5647.
38. Lanquillon S., Krieg J.C., Bening-Abu-Shach U., Vedder H. Cytokine production and treatment response in major depressive disorder. Neuropsychopharmacology 2000, 22(4):370-379.
39. Lee K.-J., Kim S.-J., Kim S.-W., Choi S.-H., Shin Y.-C., Park S.-H., et al. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 2006, 38:44-54.
40. Leuchtweis J., Boettger M.K., Niv F., Redecker C., Schaible H.G. Enhanced neurogenesis in the hippocampal dentate gyrus during antigen-induced arthritis in adult rat - a crucial role of immunization. PLoS ONE 2014, 9:e89258.
41. Lewis M., Tartaglia L.A., Lee A., Bennett G.L., Rice G.C., Wong G.H., et al. Cloning and expression of cDNAs for two distinct murine tumor necrosis factor receptors demonstrate one receptor is species specific. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:2830-2834.
42. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl.) 1987, 92:180-185.
43. Maseda D., Meister S., Neubert K., Herrmann M., Voll R.E. Proteasome inhibition drastically but reversibly impairs murine lymphocyte development. Cell Death Differ. 2008, 15:600-612.
44. Matcham F., Rayner L., Steer S., Hotopf M. The prevalence of depression in rheumatoid arthritis: a systematic review and meta-analysis. Rheumatology (Oxford) 2013, 52:2136-2148.
45. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302(5651):1760-1765.
46. Mutso A.A., Radzicki D., Baliki M.N., Huang L., Banisadr G., Centeno M.V., et al. Abnormalities in hippocampal functioning with persistent pain. J. Neurosci. 2012, 32:5747-5756.
47. Najjar S., Pearlman D.M., Alper K., Najjar A., Devinsky O. Neuroinflammation and psychiatric illness. J. Neuroinflamm. 2013, 10:43.
48. Paus M., Kohl Z., Ben Abdallah N.M., Galter D., Gillardon F., Winkler J. Enhanced dendritogenesis and axogenesis in hippocampal neuroblasts of LRRK2 knockout mice. Brain Res. 2013, 1497:85-100.
49. Peng D., Shi F., Shen T., Peng Z., Zhang C., Liu X., et al. Altered brain network modules induce helplessness in major depressive disorder. J. Affect. Disord. 2014, 168:21-29.
50. Perera T.D., Dwork A.J., Keegan K.A., Thirumangalakudi L., Lipira C.M., Joyce N., et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE 2011, 6:e17600.
51. Perry V.H., Holmes C. Microglial priming in neurodegenerative disease. Nat. Rev. Neurol. 2014, 10:217-224.
52. Pertsov S.S., Koplik E.V., Simbirtsev A.S., Kalinichenko L.S. Effect of interleukin-1beta on the behavior of rats during mild stress in the open-field test. Bull. Exp. Biol. Med. 2009, 148(5):735-737.
53. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 2003, 17:879-886.
54. Plumpe T., Ehninger D., Steiner B., Klempin F., Jessberger S., Brandt M. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 2006, 7:77.
55. Pollak Y., Yirmiya R. Cytokine-induced changes in mood and behaviour: implications for 'depression due to a general medical condition', immunotherapy and antidepressive treatment. Int. J. Neuropsychopharmacol. 2002, 5(4):389-399.
56. Polzer K., Neubert K., Meister S., Frey B., Baum W., Distler J.H., et al. Proteasome inhibition aggravates tumor necrosis factor-mediated bone resorption in a mouse model of inflammatory arthritis. Arthritis Rheum. 2011, 63:670-680.
57. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 1977 Oct, 229(2):327-336.
58. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
59. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006, 27(1):24-31.
60. Rathbun A.M., Reed G.W., Harrold L.R. The temporal relationship between depression and rheumatoid arthritis disease activity, treatment persistence and response: a systematic review. Rheumatology (Oxford) 2013, 52(10):1785-1794.
61. Schett G., Redlich K., Hayer S., Zwerina J., Bolon B., Dunstan C., et al. Osteoprotegerin protects against generalized bone loss in tumor necrosis factor-transgenic mice. Arthritis Rheum. 2003, 48:2042-2051.
62. Schiepers O.J., Wichers M.C., Maes M. Cytokines and major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29(2):201-217.
63. Schlachetzki J.C., Marxreiter F., Regensburger M., Kulinich A., Winner B., Winkler J. Increased tyrosine hydroxylase expression accompanied by glial changes within the non-lesioned hemisphere in the 6-hydroxydopamine model of Parkinson's disease. Restor. Neurol. Neurosci. 2014, 32:447-462.
64. Seguin J.A., Brennan J., Mangano E., Hayley S. Proinflammatory cytokines differentially influence adult hippocampal cell proliferation depending upon the route and chronicity of administration. Neuropsychiatr. Dis. Treat. 2009, 5(1):5-14.
65. Shin S.Y., Katz P., Wallhagen M., Julian L. Cognitive impairment in persons with rheumatoid arthritis. Arthritis Care Res. (Hoboken) 2012, 64:1144-1150.
66. Spalding K.L., Bergmann O., Alkass K., Bernard S., Salehpour M., Huttner H.B., et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 2013, 153:1219-1227.
67. Stamou P., Kontoyiannis D.L. Posttranscriptional regulation of TNF mRNA: a paradigm of signal-dependent mRNA utilization and its relevance to pathology. Curr. Dir. Autoimmun. 2010, 11:61-79.
68. Valliéres L., Campbell I.L., Gage F.H., Sawchenko P.E. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 2002, 22(2):486-492.
69. Van Bokhoven P., Oomen C.A., Hoogendijk W.J.G., Smit A.B., Lucassen P.J., Spijker S. Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur. J. Neurosci. 2011, 33:1833-1840.
70. van den Berg W.B., Joosten L.A., van Lent P.L. Murine antigen-induced arthritis. Methods Mol. Med. 2007, 136:243-253.
71. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 1999, 2:266-270.
72. Villeda S.A., Luo J., Mosher K.I., Zou B., Britschgi M., Bieri G., et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
73. Wolf S.A., Steiner B., Wengner A., Lipp M., Kammertoens T., Kempermann G. Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J. 2009, 23:3121-3128.
74. Wu M.D., Hein A.M., Moravan M.J., Shaftel S.S., Olschowka J.A., O'Banion M.K. Adult murine hippocampal neurogenesis is inhibited by sustained IL-1β and not rescued by voluntary running. Brain Behav. Immun. 2012, 26(2):292-300.
75. Wu M.V., Shamy J.L., Bedi G., Choi C.-W.J., Wall M.M., Arango V., et al. Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 2014, 10.1038/npp.2014.33.
76. Yang L., Lindholm K., Konishi Y., Li R., Shen Y. Target depletion of distinct tumor necrosis factor receptor subtypes reveals hippocampal neuron death and survival through different signal transduction pathways. J. Neurosci. 2002, 22:3025-3032.
77. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 2006, 9:268-275.
78. Zunszain P.A., Hepgul N., Pariante C.M. Inflammation and depression. Curr. Top. Behav. Neurosci. 2013, 14:135-151.