Age-related alterations in the dynamic behavior of microglia

Aging Cell

Volumn 10, Issue 2, 2011, Pages 263-276

  Damani, Mausam R ^a   Zhao, Lian ^a   Fontainhas, Aurora M ^a   Amaral, Juan ^a   Fariss, Robert N ^a   Wong, Wai T ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

Age related macular degeneration; Aging; Imaging; Laser; Microglia; Retina

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ANIMAL TISSUE; ARTICLE; CELL AGING; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; DEGENERATIVE DISEASE; DENDRITIC CELL; MICROGLIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TISSUE INJURY;

ADENOSINE TRIPHOSPHATE; AGING; ANIMALS; CELL MOVEMENT; MICE; MICE, TRANSGENIC; MICROGLIA; MICROSCOPY, CONFOCAL; RECEPTORS, CHEMOKINE; RETINA;

ANIMALIA;

EID: 79952610280     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00660.x     Document Type: Article

References (68)

1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 10, 1538-1543.
2. Amor S, Puentes F, Baker D, van der Valk P (2010) Inflammation in neurodegenerative diseases. Immunology 129, 154-169.
3. Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci. 30, 596-602.
4. Birch DG, Anderson JL (1992) Standardized full-field electroretinography. Normal values and their variation with age. Arch. Ophthalmol. 110, 1571-1576.
5. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, Hubbard WC, Calkins DJ, Horner PJ, Vetter ML (2008) Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest. Ophthalmol. Vis. Sci. 49, 1437-1446.
6. Chan-Ling T, Hughes S, Baxter L, Rosinova E, McGregor I, Morcos Y, van Nieuwenhuyzen P, Hu P (2007) Inflammation and breakdown of the blood-retinal barrier during "physiological aging" in the rat retina: a model for CNS aging. Microcirculation 14, 63-76.
7. Combadiere C, Feumi C, Raoul W, Keller N, Rodero M, Pezard A, Lavalette S, Houssier M, Jonet L, Picard E, Debre P, Sirinyan M, Deterre P, Ferroukhi T, Cohen SY, Chauvaud D, Jeanny JC, Chemtob S, Behar-Cohen F, Sennlaub F (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J. Clin. Invest. 117, 2920-2928.
8. Dailey ME, Waite M (1999) Confocal imaging of microglial cell dynamics in hippocampal slice cultures. Methods 18, 222-230.
9. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758.
10. Dorshkind K, Swain S (2009) Age-associated declines in immune system development and function: causes, consequences, and reversal. Curr. Opin. Immunol. 21, 404-407.
11. Eter N, Engel DR, Meyer L, Helb HM, Roth F, Maurer J, Holz FG, Kurts C (2008) In vivo visualization of dendritic cells, macrophages, and microglial cells responding to laser-induced damage in the fundus of the eye. Invest. Ophthalmol. Vis. Sci. 49, 3649-3658.
12. Fields RD, Stevens-Graham B (2002) New insights into neuron-glia communication. Science 298, 556-562.
13. Flanary BE, Sammons NW, Nguyen C, Walker D, Streit WJ (2007) Evidence that aging and amyloid promote microglial cell senescence. Rejuvenation Res. 10, 61-74.
14. Gresh J, Goletz PW, Crouch RK, Rohrer B (2003) Structure-function analysis of rods and cones in juvenile, adult, and aged C57bl/6 and Balb/c mice. Vis. Neurosci. 20, 211-220.
15. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp. Eye Res. 76, 463-471.
16. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9, 1512-1519.
17. Inamizu T, Chang MP, Makinodan T (1985) Influence of age on the production and regulation of interleukin-1 in mice. Immunology 55, 447-455.
18. Inoue K (2002) Microglial activation by purines and pyrimidines. Glia 40, 156-163.
19. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114.
20. Kaneko H, Nishiguchi KM, Nakamura M, Kachi S, Terasaki H (2008) Characteristics of bone marrow-derived microglia in the normal and injured retina. Invest. Ophthalmol. Vis. Sci. 49, 4162-4168.
21. Kezic J, Xu H, Chinnery HR, Murphy CC, McMenamin PG (2008) Retinal microglia and uveal tract dendritic cells and macrophages are not CX3CR1 dependent in their recruitment and distribution in the young mouse eye. Invest. Ophthalmol. Vis. Sci. 49, 1599-1608.
22. Kullberg S, Aldskogius H, Ulfhake B (2001) Microglial activation, emergence of ED1-expressing cells and clusterin upregulation in the aging rat CNS, with special reference to the spinal cord. Brain Res. 899, 169-186.
23. Lawson LJ, Perry VH, Gordon S (1992) Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48, 405-415.
24. Lee CK, Weindruch R, Prolla TA (2000) Gene-expression profile of the ageing brain in mice. Nat. Genet. 25, 294-297.
25. Lee JC, Cho GS, Choi BO, Kim HC, Kim YS, Kim WK (2006) Intracerebral hemorrhage-induced brain injury is aggravated in senescence-accelerated prone mice. Stroke 37, 216-222.
26. Lee JE, Liang KJ, Fariss RN, Wong WT (2008) Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest. Ophthalmol. Vis. Sci. 49, 4169-4176.
27. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest. Ophthalmol. Vis. Sci. 50, 4444-4451.
28. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891.
29. Luhmann UF, Robbie S, Munro PM, Barker SE, Duran Y, Luong V, Fitzke FW, Bainbridge JW, Ali RR, MacLaren RE (2009) The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest. Ophthalmol. Vis. Sci. 50, 5934-5943.
30. Luo XG, Ding JQ, Chen SD (2010) Microglia in the aging brain: relevance to neurodegeneration. Mol. Neurodegener. 5, 12.
31. Ma L, Morton AJ, Nicholson LF (2003) Microglia density decreases with age in a mouse model of Huntington's disease. Glia 43, 274-280.
32. Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454, 428-435.
33. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10, 1544-1553.
34. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969.
35. Neufeld AH (1999) Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch. Ophthalmol. 117, 1050-1056.
36. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318.
37. Njie EG, Boelen E, Stassen FR, Steinbusch HW, Borchelt DR, Streit WJ (2010) Ex vivo cultures of microglia from young and aged rodent brain reveal age-related changes in microglial function. Neurobiol. Aging (in press).
38. Ogura K, Ogawa M, Yoshida M (1994) Effects of ageing on microglia in the normal rat brain: immunohistochemical observations. Neuroreport 5, 1224-1226.
39. Ohsawa K, Irino Y, Sanagi T, Nakamura Y, Suzuki E, Inoue K, Kohsaka S (2010) P2Y12 receptor-mediated integrin-beta1 activation regulates microglial process extension induced by ATP. Glia 58, 790-801.
40. Paques M, Simonutti M, Augustin S, Goupille O, El Mathari B, Sahel JA (2010) In vivo observation of the locomotion of microglial cells in the retina. Glia 58, 1663-1668.
41. Perry VH, Matyszak MK, Fearn S (1993) Altered antigen expression of microglia in the aged rodent CNS. Glia 7, 60-67.
42. Perry VH, Nicoll JA, Holmes C (2010) Microglia in neurodegenerative disease. Nat. Rev. Neurol. 6, 193-201.
43. Petersen MA, Dailey ME (2004) Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices. Glia 46, 195-206.
44. Raivich G (2005) Like cops on the beat: the active role of resting microglia. Trends Neurosci. 28, 571-573.
45. Raivich G, Jones LL, Werner A, Bluthmann H, Doetschmann T, Kreutzberg GW (1999) Molecular signals for glial activation: pro- and anti-inflammatory cytokines in the injured brain. Acta Neurochir. Suppl. 73, 21-30.
46. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492.
47. Sandhir R, Onyszchuk G, Berman NE (2008) Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp. Neurol. 213, 372-380.
48. Santos AM, Calvente R, Tassi M, Carrasco MC, Martin-Oliva D, Marin-Teva JL, Navascues J, Cuadros MA (2008) Embryonic and postnatal development of microglial cells in the mouse retina. J. Comp. Neurol. 506, 224-239.
49. Sasaki Y, Hoshi M, Akazawa C, Nakamura Y, Tsuzuki H, Inoue K, Kohsaka S (2003) Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 44, 242-250.
50. Shaked I, Tchoresh D, Gersner R, Meiri G, Mordechai S, Xiao X, Hart RP, Schwartz M (2005) Protective autoimmunity: interferon-gamma enables microglia to remove glutamate without evoking inflammatory mediators. J. Neurochem. 92, 997-1009.
51. Sheffield LG, Berman NE (1998) Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol. Aging 19, 47-55.
52. Sheng JG, Mrak RE, Griffin WS (1998) Enlarged and phagocytic, but not primed, interleukin-1 alpha-immunoreactive microglia increase with age in normal human brain. Acta Neuropathol. 95, 229-234.
53. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K (2007) Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55, 412-424.
54. Stout RD, Suttles J (2005) Immunosenescence and macrophage functional plasticity: dysregulation of macrophage function by age-associated microenvironmental changes. Immunol. Rev. 205, 60-71.
55. Streit WJ, Sammons NW, Kuhns AJ, Sparks DL (2004) Dystrophic microglia in the aging human brain. Glia 45, 208-212.
56. Streit WJ, Miller KR, Lopes KO, Njie E (2008) Microglial degeneration in the aging brain - bad news for neurons? Front. Biosci. 13, 3423-3438.
57. Streit WJ, Braak H, Xue QS, Bechmann I (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathol. 118, 475-485.
58. Sugama S, Yang L, Cho BP, DeGiorgio LA, Lorenzl S, Albers DS, Beal MF, Volpe BT, Joh TH (2003) 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, 288-294.
59. Tuo J, Bojanowski CM, Zhou M, Shen D, Ross RJ, Rosenberg KI, Cameron DJ, Yin C, Kowalak JA, Zhuang Z, Zhang K, Chan CC (2007) Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 48, 3827-3836.
60. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974-3980.
61. Wasserman JK, Schlichter LC (2008) White matter injury in young and aged rats after intracerebral hemorrhage. Exp. Neurol. 214, 266-275.
62. Wasserman JK, Yang H, Schlichter LC (2008) Glial responses, neuron death and lesion resolution after intracerebral hemorrhage in young vs. aged rats. Eur. J. Neurosci. 28, 1316-1328.
63. Wynne AM, Henry CJ, Huang Y, Cleland A, Godbout JP (2010) Protracted downregulation of CX(3)CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav. Immun. 24, 1190-1201.
64. Xu H, Chen M, Mayer EJ, Forrester JV, Dick AD (2007) Turnover of resident retinal microglia in the normal adult mouse. Glia 55, 1189-1198.
65. Xu H, Chen M, Forrester JV (2009) Para-inflammation in the aging retina. Prog. Retin Eye Res. 28, 348-368.
66. Ye SM, Johnson RW (2001) An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 9, 183-192.
67. Yuan L, Neufeld AH (2001) Activated microglia in the human glaucomatous optic nerve head. J. Neurosci. Res. 64, 523-532.
68. Zimmermann H (1994) Signalling via ATP in the nervous system. Trends Neurosci. 17, 420-426.