Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury

Experimental Neurology

Volumn 213, Issue 2, 2008, Pages 372-380

  Sandhir, Rajat ^a,b   Onyszchuk, Gregory ^b   Berman, Nancy E J ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Astrocyte; CD11b; GFAP; Hippocampus; Iba1; Inflammation; Microglia; S100B; Traumatic brain injury

Indexed keywords

BIOLOGICAL MARKER; CD11B ANTIGEN; MESSENGER RNA; PROTEIN S100B;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL DEATH; COGNITIVE DEFECT; CONVALESCENCE; HIPPOCAMPUS; INFLAMMATION; MICROGLIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; TRAUMATIC BRAIN INJURY;

AGE FACTORS; AGING; ANIMALS; ASTROCYTES; BRAIN INJURIES; CEREBRAL CORTEX; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICROGLIA;

EID: 51549101179     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.06.013     Document Type: Article

References (62)

1. Ashcroft G.S., Mills S.J., and Ashworth J.J. Ageing and wound healing. Biogerontology 3 (2002) 337-345
2. Berman N.E., Marcario J.K., Yong C., Raghavan R., Raymond L.A., Joag S.V., Narayan O., and Cheney P.D. Microglial activation and neurological symptoms in the SIV model of NeuroAIDS: association of MHC-II and MMP-9 expression with behavioral deficits and evoked potential changes. Neurobiol. Dis. 6 (1999) 486-498
3. Bigler E.D., Anderson C.V., and Blatter D.D. Temporal lobe morphology in normal aging and traumatic brain injury. AJNR Am. J. Neuroradiol. 23 (2002) 255-266
4. Bramlett H.M., and Dietrich W.D. Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog. Brain Res. 161 (2007) 125-141
5. Brown A.W., Leibson C.L., Malec J.F., Perkins P.K., Diehl N.N., and Larson D.R. Long-term survival after traumatic brain injury: a population-based analysis. NeuroRehabilitation 19 (2004) 37-43
6. Chung J.H., Seo A.Y., Chung S.W., Kim M.K., Leeuwenburgh C., Yu B.P., and Chung H.Y. Molecular mechanism of PPAR in the regulation of age-related inflammation. Ageing Res. Rev. 7 (2008) 126-136
7. Conde J.R., and Streit W.J. Effect of aging on the microglial response to peripheral nerve injury. Neurobiol. Aging 27 (2006) 1451-1461
8. Conde J.R., and Streit W.J. Microglia in the aging brain. J. Neuropathol. Exp. Neurol. 65 (2006) 199-203
9. Coronado V.G., Thomas K.E., Sattin R.W., and Johnson R.L. The CDC traumatic brain injury surveillance system: characteristics of persons aged 65 years and older hospitalized with a TBI. J. Head Trauma Rehabil. 20 (2005) 215-228
10. Deng X.H., Bertini G., Xu Y.Z., Yan Z., and Bentivoglio M. Cytokine-induced activation of glial cells in the mouse brain is enhanced at an advanced age. Neuroscience 141 (2006) 645-661
11. Diamond M.S., Staunton D.E., Marlin S.D., and Springer T.A. Binding of the integrin Mac-1 (CD11b/CD18) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylation. Cell 65 (1991) 961-971
12. Felzien L.K., McDonald J.T., Gleason S.M., Berman N.E., and Klein R.M. Increased chemokine gene expression during aging in the murine brain. Brain Res. 890 (2001) 137-146
13. Ferrell R., and Tanev K. Traumatic brain injury in older adults. Curr. Psychiatry Rep. 4 (2002) 354-362
14. Floyd C.L., and Lyeth B.G. Astroglia: important mediators of traumatic brain injury. Prog. Brain Res. 161 (2007) 61-79
15. Francesco Amenta E.B.M.S.J.A.V. Astrocyte changes in aging cerebral cortex and hippocampus: a quantitative immunohistochemical study. Microsc. Res. Tech. (1998) 29-33
16. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., and Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19 (2005) 1329-1331
17. Goldstein F.C., and Levin H.S. Cognitive outcome after mild and moderate traumatic brain injury in older adults. J. Clin. Exp. Neuropsychol. 23 (2001) 739-753
18. Goss J.R., Finch C.E., and Morgan D.G. Age-related changes in glial fibrillary acidic protein mRNA in the mouse brain. Neurobiol. Aging 12 (1991) 165-170
19. Hauwel M., Furon E., Canova C., Griffiths M., Neal J., and Gasque P. Innate (inherent) control of brain infection, brain inflammation and brain repair: the role of microglia, astrocytes, "protective" glial stem cells and stromal ependymal cells. Brain Res. Brain Res. Rev. 48 (2005) 220-233
20. Hukkelhoven C.W., Steyerberg E.W., Rampen A.J., Farace E., Habbema J.D., Marshall L.F., Murray G.D., and Maas A.I. Patient age and outcome following severe traumatic brain injury: an analysis of 5600 patients. J. Neurosurg. 99 (2003) 666-673
21. Johnstone B., Childers M.K., and Hoerner J. The effects of normal ageing on neuropsychological functioning following traumatic brain injury. Brain Inj. 12 (1998) 569-576
22. Kim K.Y., Ju W.K., and Neufeld A.H. Neuronal susceptibility to damage: comparison of the retinas of young, old and old/caloric restricted rats before and after transient ischemia. Neurobiol. Aging 25 (2004) 491-500
23. Klein M., Houx P.J., and Jolles J. Long-term persisting cognitive sequelae of traumatic brain injury and the effect of age. J. Nerv. Ment. Dis. 184 (1996) 459-467
24. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996) 312-318
25. Kyrkanides S., O'Banion M.K., Whiteley P.E., Daeschner J.C., and Olschowka J.A. Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury. J. Neuroimmunol. 119 (2001) 269-277
26. Lee C.K., Weindruch R., and Prolla T.A. Gene-expression profile of the ageing brain in mice. Nat. Genet. 25 (2000) 294-297
27. Letarte P. The brain. In: Feliciano D., Nattox K.L., and Moore E.E. (Eds). Trauma (2006), McGraw Hill, New York 397-418
28. Liu B., Gao H.M., and Hong J.S. Parkinson's disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ. Health Perspect. 111 (2003) 1065-1073
29. Liu B., Gao H.M., Wang J.Y., Jeohn G.H., Cooper C.L., and Hong J.S. Role of nitric oxide in inflammation-mediated neurodegeneration. Ann. N.Y. Acad. Sci. 962 (2002) 318-331
30. Lucas S.M., Rothwell N.J., and Gibson R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 147 Suppl 1 (2006) S232-S240
31. Maeda J., Higuchi M., Inaji M., Ji B., Haneda E., Okauchi T., Zhang M.-R., Suzuki K., and Suhara T. Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res. 1157 (2007) 100-111
32. Mahesh V.B., Dhandapani K.M., and Brann D.W. Role of astrocytes in reproduction and neuroprotection. Mol. Cell Endocrinol. 246 (2006) 1-9
33. Major D.E., Kesslak J.P., Cotman C.W., Finch C.E., and Day J.R. Life-long dietary restriction attenuates age-related increases in hippocampal glial fibrillary acidic protein mRNA. Neurobiol. Aging 18 (1997) 523-526
34. Marchetti B., and Abbracchio M.P. To be or not to be (inflamed)-is that the question in anti-inflammatory drug therapy of neurodegenerative disorders?. Trends Pharmacol. Sci. 26 (2005) 517-525
35. Mohindra, S., Mukherjee, K.K., Gupta, R., Chhabra, R., Continuation of poor surgical outcome after elderly brain injury. Surg. Neurol. In Press, Corrected Proof.
36. Mrak R.E., and Griffin W.S. Glia and their cytokines in progression of neurodegeneration. Neurobiol. Aging 26 (2005) 349-354
37. Myer D.J., Gurkoff G.G., Lee S.M., Hovda D.A., and Sofroniew M.V. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 129 (2006) 2761-2772
38. Ohsawa K., Imai Y., Kanazawa H., Sasaki Y., and Kohsaka S. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J. Cell Sci. 113 Pt 17 (2000) 3073-3084
39. Onyszchuk G., Al-Hafez B., He Y.Y., Bilgen M., Berman N.E., and Brooks W.M. A mouse model of sensorimotor controlled cortical impact: characterization using longitudinal magnetic resonance imaging, behavioral assessments and histology. J. Neurosci. Methods 160 (2007) 187-196
40. Onyszchuk G., He Y.Y., Berman N.E., and Brooks W.M. Detrimental effects of aging on outcome from traumatic brain injury: a behavioral, magnetic resonance imaging, and histological study in mice. J. Neurotrauma 25 (2008) 153-171
41. Pelinka L.E., Kroepfl A., Leixnering M., Buchinger W., Raabe A., and Redl H. GFAP versus S100B in serum after traumatic brain injury: relationship to brain damage and outcome. J. Neurotrauma 21 (2004) 1553-1561
42. Pertusa M., Garcia-Matas S., Rodriguez-Farre E., Sanfeliu C., and Cristofol R. Astrocytes aged in vitro show a decreased neuroprotective capacity. J. Neurochem. (2007) 794-805
43. Petcu E.B., Sfredel V., Platt D., Herndon J.G., Kessler C., and Popa-Wagner A. Cellular and molecular events underlying the dysregulated response of the aged brain to stroke. Gerontology (2007)
44. Pfaffl M.W., Horgan G.W., and Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30 (2002) e36
45. Popa-Wagner A., Carmichael S.T., Kokaia Z., Kessler C., and Walker L.C. The response of the aged brain to stroke: too much, too soon?. Curr. Neurovasc. Res. 4 (2007) 216-227
46. Rapoport M.J., Herrmann N., Shammi P., Kiss A., Phillips A., and Feinstein A. Outcome after traumatic brain injury sustained in older adulthood: a one-year longitudinal study. Am. J. Geriatr. Psychiatry 14 (2006) 456-465
47. Rink A., Fung K.M., Trojanowski J.Q., Lee V.M., Neugebauer E., and McIntosh T.K. Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am. J. Pathol. 147 (1995) 1575-1583
48. Sandhir R., Puri V., Klein R.M., and Berman N.E. Differential expression of cytokines and chemokines during secondary neuron death following brain injury in old and young mice. Neurosci. Lett. 369 (2004) 28-32
49. Sawada M., Sawada H., and Nagatsu T. Effects of aging on neuroprotective and neurotoxic properties of microglia in neurodegenerative diseases. Neurodegener. Dis. 5 (2008) 254-256
50. Schmidt O., Infanger M., Heyde C., Ertel W., and Stahel P. The role of neuroinflammation in traumatic brain injury. Eur. J. Trauma 30 (2004) 135-149
51. Scholz J., Abele A., Marian C., Haussler A., Herbert T.A., Woolf C.J., and Tegeder I. Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats. Pain (2008)
52. Schwartz M., Butovsky O., Bruck W., and Hanisch U.K. Microglial phenotype: is the commitment reversible?. Trends Neurosci. 29 (2006) 68-74
53. Sheffield L.G., and Berman N.E. Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol. Aging 19 (1998) 47-55
54. Stolzing A., Sethe S., and Grune T. Chronically active: activation of microglial proteolysis in ageing and neurodegeneration. Redox. Rep. 10 (2005) 207-213
55. Streit W.J., Sammons N.W., Kuhns A.J., and Sparks D.L. Dystrophic microglia in the aging human brain. Glia 45 (2004) 208-212
56. Sugama S., Yang L., Cho B.P., DeGiorgio L.A., Lorenzl S., Albers D.S., Beal M.F., Volpe B.T., and Joh T.H. Age-related microglial activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurodegeneration in C57BL/6 mice. Brain Res. 964 (2003) 288-294
57. Topp K.S., Faddis B.T., and Vijayan V.K. Trauma-induced proliferation of astrocytes in the brains of young and aged rats. Glia 2 (1989) 201-211
58. White-Gbadebo D., and Hamm R.J. Chronic corticosterone treatment potentiates deficits following traumatic brain injury in rats: implications for aging. J. Neurotrauma 10 (1993) 297-306
59. Wilhelmsson U., Li L., Pekna M., Berthold C.H., Blom S., Eliasson C., Renner O., Bushong E., Ellisman M., Morgan T.E., and Pekny M. Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J. Neurosci. 24 (2004) 5016-5021
60. Wu D., Ren Z., Pae M., Guo W., Cui X., Merrill A.H., and Meydani S.N. Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. J. Immunol. 179 (2007) 4829-4839
61. Yoshida T., Goldsmith S.K., Morgan T.E., Stone D.J., and Finch C.E. Transcription supports age-related increases of GFAP gene expression in the male rat brain. Neurosci. Lett. 215 (1996) 107-110
62. Zhu W., Umegaki H., Shinkai T., Kurotani S., Suzuki Y., Endo H., and Iguchi A. Different glial reactions to hippocampal stab wounds in young adult and aged rats. J. Gerontol. A Biol. Sci. Med. Sci. 58 (2003) 117-122