Age and duration of inflammatory environment differentially affect the neuroimmune response and catecholaminergic neurons in the midbrain and brainstem

Neurobiology of Aging

Volumn 35, Issue 5, 2014, Pages 1065-1073

  Bardou, Isabelle ^a   Kaercher, Roxanne M ^a   Brothers, Holly M ^a   Hopp, Sarah C ^a   Royer, Sarah ^a   Wenk, Gary L ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Aging; Alzheimer's disease; Cytokines; Locus coeruleus; Microglia; Neuroinflammation; Parkinson's disease; Rat; Substantia nigra

Indexed keywords

AGING; ALZHEIMER'S DISEASE; CYTOKINES; LOCUS COERULEUS; MICROGLIA; NEUROINFLAMMATION; PARKINSON'S DISEASE; RAT; SUBSTANTIA NIGRA;

AGING; ANIMALS; CATECHOLAMINES; GENE EXPRESSION; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; LOCUS COERULEUS; MALE; MICROGLIA; NEURODEGENERATIVE DISEASES; NEUROIMMUNOMODULATION; NEURONS; PEPTIDE FRAGMENTS; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 84893719111     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.11.006     Document Type: Article

References (68)

1. Aarsland D., Andersen K., Larsen J.P., Lolk A., Nielsen H., Kragh-Sorensen P. Risk of dementia in Parkinson's disease: a community based, prospective study. Neurology 2001, 56:730-736.
2. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Landreth G., McGeer P.L., Mrak R., MacKenzie I., O'Banion K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray A. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
3. Bardou I., Brothers H.M., Kaercher R.M., Hopp S.C., Wenk G.L. Differential effects of duration and age upon the consequences of neuroinflammation in the hippocampus. Neurobiol. Aging 2013, 34:2293-2301.
4. Bartels A.L., Leenders K.L. Neuroinflammation in the pathophysiology of Parkinson's disease: evidence from animal models to human invivo studies with [11C] PK11195 PET. Mov. Disord. 2005, 22:1852-1856.
5. Bilbo S.D. Early-life infection is a vulnerability factor for aging-related glial alterations and cognitive decline. Neurobiol. Learn Mem. 2010, 94:57-64.
6. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76:77-98.
7. Braak H., Del Tredici K., Rub U., DeVos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
8. Brothers, H.M., Bardou, I., Hopp, S.C., Marchalant, Y., Kaercher, R.M., Turner, S.M., Mitchem, M.R., Kigerl, K., Wenk, G.L., 2013a, Time-dependent compensatory responses to chronic neuroinflammation in hippocampus and brainstem: the potential role of glutamate neurotransmission. J. Alz. Dis. Parkin, in press.
9. Brothers H.M., Bardou I., Hopp S.C., Kaercher R.M., Wynne-Corona A., Fenn A.M., Godbout J.P., Wenk G.L. Riluzole partially rescues age-associated, but not LPS-induced, loss of glutamate transporters and spatial memory impairment. J. Neuroimmune Pharmacol. 2013, 8:1098-1105.
10. Cacheaux L.P., Ivens S., David Y., Lakhter A.J., Bar-Klein G., Shapira M., Heinemann U., Friedman A., Kaufer D. Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J.Neurosci. 2009, 29:8927-8935.
11. Cagnin A., Kassiou M., Meikle S.R., Banati R.B. Invivo evidence for microglial activation in neurodegenerative dementia. Acta Neurol. Scand. Suppl. 2006, 114:107-114.
12. Castano A., Herrera A.J., Cano J., Machado A. The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-alpha, IL-1beta and IFN-gamma. J.Neurochem. 2002, 81:150-157.
13. Chen Y.L., Huang Y.L., Lin N.Y., Chen H.C., Chiu W.C., Change C.J. Differential regulation of ARE-mediated TNFα and IL-1β mRNA stability by lipopolysaccharide in RAW264.7 cells. Biochem. Biophys. Res. Commun. 2006, 346:160-168.
14. Colton C.A., Wilcock D.M. Assessing activation states in microglia. CNS Neurol. Disord. Drug Targets 2010, 9:174-191.
15. Cribbs D.H., Berchtold N.C., Perreau V., Coleman P.D., Rogers J., Tenner A.J., Cotman C.W. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J.Neuroinflammation 2012, 9:179.
16. Dame J.B., Christensen R.D., Juul S.E. The distribution of granulocyte-macrophage colony-stimulating factor and its receptor in the developing human fetus. Pediatr. Res. 1999, 46:358-366.
17. Eikelenboom P., van Exel E., Hoozemans J.J.M., Veerhuis R., Rosemuller A.J.M., van Gool W.A. Neuroinflammation - an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis. 2010, 7:38-41.
18. Feinstein D.L., Heneka M.T., Gavrilyuk V., Dello Russo C., Weinberg G., Galea E. Noradrenergic regulation of inflammatory gene expression in brain. Neurochem. Int. 2002, 41:357-365.
19. Gasbarri A., Packard M.G., Campana E., Pacitti C. Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res. Bull. 1994, 33:445-452.
20. Gerhard A., Pavese N., Hotton G., Turkheimer F., Es M., Hammers A., Eggert K., Oertel W., Banati R.B., Brooks D.J. Invivo imaging of microglial activation with [C-11](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol. Dis. 2006, 21:404-412.
21. Gozlan H., Daval G., Verge D., Spampinato U., Fattaccini C.M., Gallissot M.C., Elmestikawy S., Hamon M. Aging associated changes in serotoninergic and dopaminergic pre- and postsynaptic neurochemical markers in the rat brain. Neurobiol. Aging 1990, 11:437-449.
22. Griffin W.S., Stanley L.C., Ling C., White L., MacLeod V., Perrot L.J., White C.L., Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A 1989, 86:7611-7615.
23. Grudzien A., Shaw P., Weintraub S., Bigio E., Mash D.C., Mesulam M.M. Locus coeruleus neurofibrillary degeneration in aging, mild cognitive impairment and early Alzheimer's Disease. Neurobiol. Aging 2007, 28:327-335.
24. Halliday G.M., Del Tredici K., Braak H. Critical appraisal of brain pathology staging related to presymptomatic and symptomatic cases of sporadic Parkinson's disease. J.Neural Trans. Suppl. 2006, 70:99-103.
25. Harry G.J. Microglia during development and aging. Pharmacol. Ther. 2013, 139:313-326.
26. Hauss-Wegrzyniak B., Dobrzanski P., Stoehr J.D., Wenk G.L. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer's disease. Brain Res. 1998, 780:294-303.
27. Heneka M.T., O'Banion M.K., Terwel D., Kummer M.P. Neuroinflammatory processes in Alzheimer's disease. J.Neural Trans. 2010, 117:919-947.
28. Herrera A.J., Castano A., Venero J.L., Cano J., Machado A. The single intranigral injection of LPS as a new model for studying the selective effects ofinflammatory reactions on dopaminergic system. Neurobiol. Dis. 2000, 7:429-447.
29. Herrup K. Reimagining Alzheimer's disease- an age-based hypothesis. J.Neurosci. 2010, 30:16755-16762.
30. Hobson P., Meara J. Risk and incidence of dementia in a cohort of older subjects with Parkinson's disease in the United Kingdom. Mov. Disord. 2004, 19:1043-1049.
31. Hughes T.A., Ross H.F., Musa S., Bhattacherjee S., Nathan R.N., Mindham R.H., Spokes E.G. A10-year study of the incidence of and factors predicting dementia in Parkinson's disease. Neurology 2000, 54:1596-1602.
32. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003, 106:518.
33. Jackman N.A., Uliasz T.F., Hewett J.A., Hewett S.J. Regulation of system x(c)(-) activity and expression in astrocytes by interleukin-1 beta: implications for hypoxic neuronal injury. Glia 2010, 58:1806-1815.
34. Kim Y.S., Joh T.H. Matrix metalloproteinases, new insights into the understanding of neurodegenerative disorders. Biomol. Ther. 2012, 20:133-143.
35. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J.Neurosci. 2000, 20:6309-6316.
36. Koprich J.B., Reske-Nielsen C., Mithal P., Isacson O. Neuroinflammation mediated by IL-1β increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J.Neuroinflammation 2008, 5:8.
37. Liu L., Aboud O., Jones R.A., Mrak R.E., Griffin W.S.T., Barger S.W. Apolipoprotein E expression is elevated by interleukin 1 and other interleukin 1-induced factors. J.Neuroinflammation 2011, 8:175.
38. Manaye K.F., Mouton P.R., Xu G., Drew A., Lei D.-L., Sharma Y., Rebeck G.W., Turner S. Age-related loss of noradrenergic neurons in the brains of triple transgenic mice. Age 2013, 35:139-147.
39. Mannari C., Origlia N., Scatena A., Del Debbio A., Catena M., Dell'agnello G., Barraco A., Giovannini L., Dell'osso L., Domenici L., Piccinni A. BDNF level in the rat prefrontal cortex increases following chronic but not acute treatment with duloxetine, a dual acting inhibitor of noradrenaline and serotonin re-uptake. Cell Mol. Neurobiol. 2008, 28:457-468.
40. Marchalant Y., Brothers H.M., Norman G.J., Karolina K., DeVries C., Wenk G.L. Cannabinoids attenuate the effects of aging upon neuroinflammation and neurogenesis. Neurobiol. Dis. 2009, 34:300-307.
41. Marchalant Y., Rosi S., Wenk G.L. Anti-inflammatory property of the cannabinoid agonist WIN-55212-2 in a rodent model of chronic brain inflammation. Neuroscience 2007, 144:1516-1522.
42. Masuda T., Nakagawa S., Boku S., Nishikawa H., Takamura N., Kato A., Inoue T., Koyama T. Noradrenaline increases neural precursor cells derived from middle-aged rat dentate gyrus through beta2 receptor. Prog. Neuropsychopharmacol. Biol. Psychiatary 2012, 36:44-51.
43. Miguez J.M., Aldegunde M., Paz-Valinas L., Recio J., Sanchez-Barcelo E. Selective changes in the contents of noradrenaline, dopamine and serotonin in rat brain areas during aging. J.Neural. Transm. 1999, 106:1089-1098.
44. Mouton P.R., Kelly-Bell B., Tweedie D., Spangler E.L., Perez E., Carlson O.D., Short R.G., deCabo R., Chang J., Ingram D.K., Li Y., Greig N.H. The effects of age and lipopolysaccharide (LPS)-mediated peripheral inflammation on numbers of central catecholaminergic neurons. Neurobiol. Aging 2012, 33:423-427.
45. Parajuli B., Sonobe Y., Kawanokuchi J., Doi Y., Noda M., Takeuchi H., Mizuno T., Suzumura A. GM-CSF increases LPS-induced production of proinflammatory mediators via upregulation of TLR4 and CD14 in murine microglia. J.Neuroinflammation 2012, 9:268.
46. Pierson E., Simmons S.B., Castelli L., Goverman J.M. Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol. Rev. 2012, 248:205-215.
47. Prow N.A., Irani D.N. The inflammatory cytokine, interleukin-1 beta, mediates loss of astroglial glutamate transport and drives excitotoxic motor neuron injury in the spinal cord during acute viral encephalomyelitis. J.Neurochem. 2008, 105:1276-1286.
48. Rosi S., Ramirez-Amaya V., Hauss-Wegrzyniak B., Wenk G.L. Chronic brain inflammation leads to a decline in hippocampal NMDA R1 receptors. J.Neuroinflammation 2004, 1:12-18.
49. Rudow G., O'Brien R., Savonenko A.V., Resnick S.M., Zonderman A.B., Pletnikova O., Marsh L., Dawson T.M., Crain B.J., West M.J., Troncoso J.C. Morphometry of the human substantia nigra in ageing and Parkinson's disease. Acta Neuropathol. 2008, 115:461-470.
50. Shi N., Kawano Y., Tateishi T., Kikuchi H., Osoegawa M., Ohyagi Y., Kira J. Increased IL-13-producing T cells in ALS: positive correlations with disease severity and progression rate. J.Neuroimmunol. 2007, 182:232-235.
51. Sitcheran R., Gupta P., Fisher P.B., Baldwin A.S. Positive and negative regulation of EAAT2 by NF-kappaB: a role for N-myc in TNFalpha-controlled repression. EMBO J. 2005, 24:510-520.
52. Smith J.A., Das A., Ray S.K., Banik N.L. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull. 2012, 87:10-20.
53. Swardfager W., LanctÔt K., Rothenburg L., Wong A., Cappell J., Herrmann N. Ameta-analysis of cytokines in Alzheimer's disease. Biol. Psychiatry 2010, 68:930-941.
54. Szot P., White S.S., Greenup J.L., Leverenz J.B., Peskind E.R., Raskind M.A. Compensatory changes in the noradrenergic nervous system in the locus ceruleus and hippocampus of postmortem subjects with Alzheimer's disease and dementia with Lewy bodies. J.Neurosci. 2006, 26:467-478.
55. Takaki J., Fujimori K., Miura M., Suzuki T., Sekino Y., Sato K. L-glutamate released from activated microglia downregulates astrocytic L-glutamate transporter expression in neuroinflammation: the "collusion" hypothesis for increased extracellular L-glutamate concentration in neuroinflammation. J.Neuroinflammation 2012, 9:275.
56. Takeuchi H., Jin S.J., Wang J.Y., Zhang G.Q., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., Suzumura A. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J.Biol. Chem. 2006, 281:21362-21368.
57. Taylor D.L., Jones F., Kubota E.S., Pocock J.M. Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor alpha-induced neurotoxicity in concert with microglial-derived Fas ligand. J.Neurosci. 2005, 25:2952-2964.
58. Tome C.M.L., Tyson T., Rey N.L., Grathwohl S., Britschgi M., Brundin P. Inflammation and alpha-synuclein's prion-like behavior in Parkinson's disease-is there a link?. Mol. Neurobiol. 2013, 47:561-574.
59. Tong L., Balazs R., Soiampornkul R., Thangnipon W., Cotman C.W. Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol. Aging 2008, 29:1380-1393.
60. Trotti D., Danbolt N.C., Volterra A. Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration?. Trends Pharmacol Sci. 1998, 19:328-334.
61. Von Bohlen und Halbach O., Minichiello L. Neurotrophin receptor heterozygosity causes deficits in catecholaminergic innervation of amygdala and hippocampus in aged mice. J.Neural Transm. 2006, 113:1829-1836.
62. Wang J., Song N., Jiang H., Wang J., Xie J.X. Pro-inflammatory cytokines modulate iron regulatory protein 1 expression and iron transportation through reactive oxygen/nitrogen species production in ventral mesencephalic neurons. Biochim. Biophys. Acta Mol. Basis Dis. 2013, 1832:618-625.
63. Wenk G.L., Hauss-Wegrzyniak B. Animal Models of Chronic Neuroinflammation as a Model of Alzheimer's Disease. Inflammatory Events in Neurodegeneration 2001, 83-87. Prominent Press, Scottsdale, AZ. S. Bondy, A. Campbell (Eds.).
64. Wenk G.L., McGann K., Hauss-Wegrzyniak B., Rosi S. The toxicity of tumor necrosis factor-α upon cholinergic neurons within the nucleus basalis and the role of norepinephrine in the regulation of inflammation: implications for Alzheimer's disease. Neuroscience 2003, 121:719-729.
65. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 2007, 150:963-976.
66. Willard L.B., Hauss-Wegrzyniak B., Wenk G.L. Pathological and biochemical consequences of acute and chronic neuroinflammation within the basal forebrain cholinergic system of rats. Neuroscience 1999, 88:193-200.
67. Wynne A.M., Henry C.J., Huang Y., Cleland A., Godbout J.P. Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav. Immun. 2010, 24:1190-1201.
68. Ye S.M., Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. J.Neuroimmunol. 1999, 93:139-148.