Disease-related microglia heterogeneity in the hippocampus of Alzheimer’s disease, dementia with Lewy bodies, and hippocampal sclerosis of aging

Adam D. Bachstetter1, Linda J. Van Eldik1, Frederick A. Schmitt1, Janna H. Neltner1, Eseosa T. Ighodaro1, Scott J. Webster1, Ela Patel1, Erin L. Abner1, Richard J. Kryscio2, Peter T. Nelson3
1Sanders-Brown Center on Aging, University of Kentucky, 800 S. Limestone St, Lexington, KY, USA
2Department of Biostatistics, University of Kentucky, Lexington, KY, USA
3Department of Pathology and Laboratory Medicine, Division of Neuropathology, University of Kentucky, Lexington, KY, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Malik M, Simpson JF, Parikh I, Wilfred BR, Fardo DW, Nelson PT, Estus S (2013) CD33 Alzheimer's risk-altering polymorphism, CD33 expression, and exon 2 splicing. J Neurosci 33(33):13320–13325. doi:10.1523/JNEUROSCI.1224-13.2013

Griciuc A, Serrano-Pozo A, Parrado AR, Lesinski AN, Asselin CN, Mullin K, Hooli B, Choi SH, Hyman BT, Tanzi RE (2013) Alzheimer's disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron 78(4):631–643. doi:10.1016/j.neuron.2013.04.014

Jonsson T, Stefansson H, Steinberg S, Jonsdottir I, Jonsson PV, Snaedal J, Bjornsson S, Huttenlocher J, Levey AI, Lah JJ, Rujescu D, Hampel H, Giegling I, Andreassen OA, Engedal K, Ulstein I, Djurovic S, Ibrahim-Verbaas C, Hofman A, Ikram MA, van Duijn CM, Thorsteinsdottir U, Kong A, Stefansson K (2013) Variant of TREM2 associated with the risk of Alzheimer's disease. N Engl J Med 368(2):107–116. doi:10.1056/NEJMoa1211103

Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JS, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert JC, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St George-Hyslop P, Singleton A, Hardy J, Alzheimer Genetic Analysis G (2013) TREM2 variants in Alzheimer's disease. N Engl J Med 368(2):117–127. doi:10.1056/NEJMoa1211851

Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2):461–553. doi:10.1152/physrev.00011.2010

Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17(1):131–143. doi:10.1038/nn.3599

Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16(12):1896–1905. doi:10.1038/nn.3554

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(6):752–758. doi:10.1038/nn1472

Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318. doi:10.1126/science.1110647

Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, Cairns NJ, Castellani RJ, Crain BJ, Davies P, Del Tredici K, Duyckaerts C, Frosch MP, Haroutunian V, Hof PR, Hulette CM, Hyman BT, Iwatsubo T, Jellinger KA, Jicha GA, Kovari E, Kukull WA, Leverenz JB, Love S, Mackenzie IR, Mann DM, Masliah E, McKee AC, Montine TJ, Morris JC, Schneider JA, Sonnen JA, Thal DR, Trojanowski JQ, Troncoso JC, Wisniewski T, Woltjer RL, Beach TG (2012) Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 71(5):362–381. doi:10.1097/NEN.0b013e31825018f7

Nelson PT, Smith CD, Abner EL, Wilfred BJ, Wang WX, Neltner JH, Baker M, Fardo DW, Kryscio RJ, Scheff SW, Jicha GA, Jellinger KA, Van Eldik LJ, Schmitt FA (2013) Hippocampal sclerosis of aging, a prevalent and high-morbidity brain disease. Acta Neuropathol 126(2):161–177. doi:10.1007/s00401-013-1154-1

Kurushima H, Ramprasad M, Kondratenko N, Foster DM, Quehenberger O, Steinberg D (2000) Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. J Leukoc Biol 67(1):104–108

da Silva RP, Gordon S (1999) Phagocytosis stimulates alternative glycosylation of macrosialin (mouse CD68), a macrophage-specific endosomal protein. Biochem J 338(Pt 3):687–694

Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57(1):1–9

Schmitt FA, Nelson PT, Abner E, Scheff S, Jicha GA, Smith C, Cooper G, Mendiondo M, Danner DD, Van Eldik LJ, Caban-Holt A, Lovell MA, Kryscio RJ (2012) University of Kentucky Sanders-Brown healthy brain aging volunteers: donor characteristics, procedures and neuropathology. Curr Alzheimer Res 9(6):724–733

Bachstetter AD, Rowe RK, Kaneko M, Goulding D, Lifshitz J, Van Eldik LJ (2013) The p38alpha MAPK regulates microglial responsiveness to diffuse traumatic brain injury. J Neurosci 33(14):6143–6153. doi:10.1523/JNEUROSCI.5399-12.2013

Bachstetter AD, Norris CM, Sompol P, Wilcock DM, Goulding D, Neltner JH, St Clair D, Watterson DM, Van Eldik LJ (2012) Early stage drug treatment that normalizes proinflammatory cytokine production attenuates synaptic dysfunction in a mouse model that exhibits age-dependent progression of Alzheimer's disease-related pathology. J Neurosci 32(30):10201–10210. doi:10.1523/JNEUROSCI.1496-12.2012

Schmider E, Ziegler M, Danay E, Beyer L, Bühner M (2010) Is It Really Robust? Methodology: European Journal of Research Methods for the Behavioral and Social Sciences 6(4):147–151. doi:10.1027/1614-2241/a000016

Leverenz JB, Agustin CM, Tsuang D, Peskind ER, Edland SD, Nochlin D, DiGiacomo L, Bowen JD, McCormick WC, Teri L, Raskind MA, Kukull WA, Larson EB (2002) Clinical and neuropathological characteristics of hippocampal sclerosis - A community-based study. Arch Neurol 59(7):1099–1106. doi:10.1001/archneur.59.7.1099

Nelson PT, Schmitt FA, Lin YS, Abner EL, Jicha GA, Patel E, Thomason PC, Neltner JH, Smith CD, Santacruz KS, Sonnen JA, Poon LW, Gearing M, Green RC, Woodard JL, Van Eldik LJ, Kryscio RJ (2011) Hippocampal sclerosis in advanced age: clinical and pathological features. Brain 134:1506–1518. doi:10.1093/brain/awr053

Dickson DW, Davies P, Bevona C, Vanhoeven KH, Factor SM, Grober E, Aronson MK, Crystal HA (1994) Hippocampal sclerosis - a common pathological feature of dementia in very old (greater-than-or-equal-to-80 years of age) humans. Acta Neuropathol 88(3):212–221

West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14(4):275–285

Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134(Pt 2):127–136

Streit WJ (2006) Microglial senescence: does the brain's immune system have an expiration date? Trends Neurosci 29(9):506–510. doi:10.1016/j.tins.2006.07.001

Streit WJ, Xue QS, Tischer J, Bechmann I (2014) Microglial pathology. Acta Neuropathol Commun 2(1):142. doi:10.1186/s40478-014-0142-6

Boche D, Perry VH, Nicoll JA (2013) Review: activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol 39(1):3–18. doi:10.1111/nan.12011

Graeber MB (2010) Changing face of microglia. Science 330(6005):783–788. doi:10.1126/science.1190929

Mosher KI, Wyss-Coray T (2014) Microglial dysfunction in brain aging and Alzheimer's disease. Biochem Pharmacol 88(4):594–604. doi:10.1016/j.bcp.2014.01.008

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(4):475–485. doi:10.1007/s00401-009-0556-6

Xue QS, Streit WJ (2011) Microglial pathology in down syndrome. Acta Neuropathol 122(4):455–466. doi:10.1007/s00401-011-0864-5

Lopes KO, Sparks DL, Streit WJ (2008) Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 56(10):1048–1060. doi:10.1002/glia.20678

Streit WJ, Sammons NW, Kuhns AJ, Sparks DL (2004) Dystrophic microglia in the aging human brain. Glia 45(2):208–212. doi:10.1002/glia.10319

Smith AM, Dragunow M (2014) The human side of microglia. Trends Neurosci 37(3):125–135. doi:10.1016/j.tins.2013.12.001

Sudduth TL, Schmitt FA, Nelson PT, Wilcock DM (2013) Neuroinflammatory phenotype in early Alzheimer's disease. Neurobiol Aging 34(4):1051–1059. doi:10.1016/j.neurobiolaging.2012.09.012

Wirenfeldt M, Clare R, Tung S, Bottini A, Mathern GW, Vinters HV (2009) Increased activation of Iba1(+) microglia in pediatric epilepsy patients with Rasmussen's encephalitis compared with cortical dysplasia and tuberous sclerosis complex. Neurobiol Dis 34(3):432–440. doi:10.1016/j.nbd.2009.02.015

Taylor SE, Morganti-Kossmann C, Lifshitz J, Ziebell JM (2014) Rod microglia: a morphological definition. PLoS One 9(5), e97096. doi:10.1371/journal.pone.0097096

Ziebell JM, Taylor SE, Cao TX, Harrison JL, Lifshitz J (2012) Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury. J Neuroinflammation 9. doi:10.1186/1742-2094-9-247

Cao T, Thomas TC, Ziebell JM, Pauly JR, Lifshitz J (2012) Morphological and genetic activation of microglia after diffuse traumatic brain injury in the rat. Neuroscience 225:65–75. doi:10.1016/j.neuroscience.2012.08.058

Ackman JB, Siddiqi F, Walikonis RS, LoTurco JJ (2006) Fusion of microglia with pyramidal neurons after retroviral infection. J Neurosci 26(44):11413–11422. doi:10.1523/JNEUROSCI.3340-06.2006

Torres-Platas SG, Comeau S, Rachalski A, Dal Bo G, Cruceanu C, Turecki G, Giros B, Mechawar N (2014) Morphometric characterization of microglial phenotypes in human cerebral cortex. J Neuroinflammation 11. doi:10.1186/1742-2094-11-12

Beynon SB, Walker FR (2012) Microglial activation in the injured and healthy brain: What are we really tallkine about? Practical and theoretical issues associated with measurement of changes in microglia morphology. Neuroscience 225:162–171. doi:10.1016/j.neuroscience.2012.07.029

Nelson PT, Abner EL, Schmitt FA, Kryscio RJ, Jicha GA, Smith CD, Davis DG, Poduska JW, Patel E, Mendiondo MS, Markesbery WR (2010) Modeling the association between 43 different clinical and pathological variables and the severity of cognitive impairment in a large autopsy cohort of elderly persons. Brain Pathol 20(1):66–79. doi:10.1111/j.1750-3639.2008.00244.x