The increased density of p38 mitogen-activated protein kinase-immunoreactive microglia in the sensorimotor cortex of aged TgCRND8 mice is associated predominantly with smaller dense-core amyloid plaques

European Journal of Neuroscience

Volumn 33, Issue 8, 2011, Pages 1433-1444

  Chlan Fourney, J ^a   Zhao, T ^a,b   Walz, W ^b   Mousseau, D D ^a,b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Alzheimer's disease; Dementia; Macrophage 1(CD11b CD18); Microglia; P38 mitogen activated protein kinase; Stereology

Indexed keywords

CD11B ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38;

AMYLOID PLAQUE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; GENE MUTATION; IMMUNOREACTIVITY; MALE; MICROGLIA; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSORIMOTOR CORTEX; SIGNAL TRANSDUCTION;

AGING; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CEREBRAL CORTEX; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICROGLIA; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLAQUE, AMYLOID;

EID: 79954546312     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07597.x     Document Type: Article

References (52)

1. Bellucci, A., Rosi, M.C., Grossi, C., Fiorentini, A., Luccarini, I. & Casamenti, F. (2007) Abnormal processing of tau in the brain of aged TgCRND8 mice. Neurobiol. Dis., 27, 328-338.
2. Boissonneault, V., Filali, M., Lessard, M., Relton, J., Wong, G. & Rivest, S. (2009) Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain, 132, 1078-1092.
3. Bolmont, T., Haiss, F., Eicke, D., Radde, R., Mathis, C.A., Klunk, W.E., Kohsaka, S., Jucker, M. & Calhoun, M.E. (2008) Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J. Neurosci., 28, 4283-4292.
4. Bornemann, K.D., Wiederhold, K.H., Pauli, C., Ermini, F., Stalder, M., Schnell, L., Sommer, B., Jucker, M. & Staufenbiel, M. (2001) Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol., 158, 63-73.
5. Bu, X., Huang, P., Qi, Z., Zhang, N., Han, S., Fang, L. & Li, J. (2007) Cell type-specific activation of p38 MAPK in the brain regions of hypoxic preconditioned mice. Neurochem. Int., 51, 459-466.
6. Cao, X., Rui, L., Pennington, P.R., Chlan-Fourney, J., Jiang, Z., Wei, Z., Li, X.M., Edmondson, D.E. & Mousseau, D.D. (2009) Serine 209 resides within a putative p38(MAPK) consensus motif and regulates monoamine oxidase-A activity. J. Neurochem., 111, 101-110.
7. Chishti, M.A., Yang, D.S., Janus, C., Phinney, A.L., Horne, P., Pearson, J., Strome, R., Zuker, N., Loukides, J., French, J., Turner, S., Lozza, G., Grilli, M., Kunicki, S., Morissette, C., Paquette, J., Gervais, F., Bergeron, C., Fraser, P.E., Carlson, G.A., George-Hyslop, P.S. & Westaway, D. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem., 276, 21562-21570.
8. Choucair-Jaafar, N., Laporte, V., Levy, R., Poindron, P., Lombard, Y. & Gies, J.P. (2011) Complement receptor 3 (CD11b/CD18) is implicated in the elimination of beta-amyloid peptides. Fundam. Clin. Pharmacol., 25, 115-122.
9. Culbert, A.A., Skaper, S.D., Howlett, D.R., Evans, N.A., Facci, L., Soden, P.E., Seymour, Z.M., Guillot, F., Gaestel, M. & Richardson, J.C. (2006) MAPK-activated protein kinase 2 deficiency in microglia inhibits pro-inflammatory mediator release and resultant neurotoxicity. Relevance to neuroinflammation in a transgenic mouse model of Alzheimer disease. J. Biol. Chem., 281, 23658-23667.
10. D'Andrea, M.R. & Nagele, R.G. (2009) Morphologically distinct types of amyloid plaques point the way to a better understanding of Alzheimer's disease pathogenesis. Biotech. Histochem., 85, 133-147.
11. D'Andrea, M.R., Reiser, P.A., Gumula, N.A., Hertzog, B.M. & Andrade-Gordon, P. (2001) Application of triple immunohistochemistry to characterize amyloid plaque-associated inflammation in brains with Alzheimer's disease. Biotech. Histochem., 76, 97-106.
12. Davalos, D., Grutzendler, J., Yang, G., Kim, J.V., Zuo, Y., Jung, S., Littman, D.R., Dustin, M.L. & Gan, W.B. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci., 8, 752-758.
13. El Khoury, J., Toft, M., Hickman, S.E., Means, T.K., Terada, K., Geula, C. & Luster, A.D. (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat. Med., 13, 432-438.
14. Franklin, K. & Paxinos, G. (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
15. Frautschy, S.A., Yang, F., Irrizarry, M., Hyman, B., Saido, T.C., Hsiao, K. & Cole, G.M. (1998) Microglial response to amyloid plaques in APPsw transgenic mice. Am. J. Pathol., 152, 307-317.
16. Frisoni, G.B., Prestia, A., Rasser, P.E., Bonetti, M. & Thompson, P.M. (2009) In vivo mapping of incremental cortical atrophy from incipient to overt Alzheimer's disease. J. Neurol., 256, 916-924.
17. Giovannini, M.G., Cerbai, F., Bellucci, A., Melani, C., Grossi, C., Bartolozzi, C., Nosi, D. & Casamenti, F. (2008) Differential activation of mitogen-activated protein kinase signalling pathways in the hippocampus of CRND8 transgenic mouse, a model of Alzheimer's disease. Neuroscience, 153, 618-633.
18. Grathwohl, S.A., Kalin, R.E., Bolmont, T., Prokop, S., Winkelmann, G., Kaeser, S.A., Odenthal, J., Radde, R., Eldh, T., Gandy, S., Aguzzi, A., Staufenbiel, M., Mathews, P.M., Wolburg, H., Heppner, F.L. & Jucker, M. (2009) Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat. Neurosci., 12, 1361-1363.
19. Hanisch, U.K. & Kettenmann, H. (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci., 10, 1387-1394.
20. Hensley, K., Floyd, R.A., Zheng, N.Y., Nael, R., Robinson, K.A., Nguyen, X., Pye, Q.N., Stewart, C.A., Geddes, J., Markesbery, W.R., Patel, E., Johnson, G.V. & Bing, G. (1999) p38 kinase is activated in the Alzheimer's disease brain. J. Neurochem., 72, 2053-2058.
21. Honda, S., Sasaki, Y., Ohsawa, K., Imai, Y., Nakamura, Y., Inoue, K. & Kohsaka, S. (2001) Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci., 21, 1975-1982.
22. Hua, R. & Walz, W. (2006) Minocycline treatment prevents cavitation in rats after a cortical devascularizing lesion. Brain Res., 1090, 172-181.
23. Jin, S.X., Zhuang, Z.Y., Woolf, C.J. & Ji, R.R. (2003) p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J. Neurosci., 23, 4017-4022.
24. Juretic, N., Santibanez, J.F., Hurtado, C. & Martinez, J. (2001) ERK 1, 2 and p38 pathways are involved in the proliferative stimuli mediated by urokinase in osteoblastic SaOS-2 cell line. J. Cell. Biochem., 83, 92-98.
25. Koistinaho, M., Kettunen, M.I., Goldsteins, G., Keinanen, R., Salminen, A., Ort, M., Bures, J., Liu, D., Kauppinen, R.A., Higgins, L.S. & Koistinaho, J. (2002) Beta-amyloid precursor protein transgenic mice that harbor diffuse A beta deposits but do not form plaques show increased ischemic vulnerability: role of inflammation. Proc. Natl Acad. Sci. USA, 99, 1610-1615.
26. Lee, S.H., Park, J., Che, Y., Han, P.L. & Lee, J.K. (2000) Constitutive activity and differential localization of p38alpha and p38beta MAPKs in adult mouse brain. J. Neurosci. Res., 60, 623-631.
27. Maier, M., Peng, Y., Jiang, L., Seabrook, T.J., Carroll, M.C. & Lemere, C.A. (2008) Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. J. Neurosci., 28, 6333-6341.
28. Majumdar, A., Cruz, D., Asamoah, N., Buxbaum, A., Sohar, I., Lobel, P. & Maxfield, F.R. (2007) Activation of microglia acidifies lysosomes and leads to degradation of Alzheimer amyloid fibrils. Mol. Biol. Cell, 18, 1490-1496.
29. Malm, T., Koistinaho, M., Muona, A., Magga, J. & Koistinaho, J. (2010) The role and therapeutic potential of monocytic cells in Alzheimer's disease. Glia, 58, 889-900.
30. Morooka, T. & Nishida, E. (1998) Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J. Biol. Chem., 273, 24285-24288.
31. Naderi, J., Lopez, C. & Pandey, S. (2006) Chronically increased oxidative stress in fibroblasts from Alzheimer's disease patients causes early senescence and renders resistance to apoptosis by oxidative stress. Mech. Ageing Dev., 127, 25-35.
32. Neary, J.T., Rathbone, M.P., Cattabeni, F., Abbracchio, M.P. & Burnstock, G. (1996) Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci., 19, 13-18.
33. Nimmerjahn, A., Kirchhoff, F. & Helmchen, F. (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science, 308, 1314-1318.
34. Park, J.G., Yuk, Y., Rhim, H., Yi, S.Y. & Yoo, Y.S. (2002) Role of p38 MAPK in the regulation of apoptosis signaling induced by TNF-alpha in differentiated PC12 cells. J. Biochem. Mol. Biol., 35, 267-272.
35. Pearson, R.C., Esiri, M.M., Hiorns, R.W., Wilcock, G.K. & Powell, T.P. (1985) Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. Proc. Natl Acad. Sci. USA, 82, 4531-4534.
36. Pei, J.J., Braak, E., Braak, H., Grundke-Iqbal, I., Iqbal, K., Winblad, B. & Cowburn, R.F. (2001) Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration. J. Alzheimers Dis., 3, 41-48.
37. Premkumar, D.R., Smith, M.A., Richey, P.L., Petersen, R.B., Castellani, R., Kutty, R.K., Wiggert, B., Perry, G. & Kalaria, R.N. (1995) Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem., 65, 1399-1402.
38. Probst, A., Ulrich, J. & Heitz, P.U. (1982) Senile dementia of Alzheimer type: astroglial reaction to extracellular neurofibrillary tangles in the hippocampus. An immunocytochemical and electron-microscopic study. Acta Neuropathol., 57, 75-79.
39. Puig, B., Gomez-Isla, T., Ribe, E., Cuadrado, M., Torrejon-Escribano, B., Dalfo, E. & Ferrer, I. (2004) Expression of stress-activated kinases c-Jun N-terminal kinase (SAPK/JNK-P) and p38 kinase (p38-P), and tau hyperphosphorylation in neurites surrounding betaA plaques in APP Tg2576 mice. Neuropathol. Appl. Neurobiol., 30, 491-502.
40. Reed-Geaghan, E.G., Savage, J.C., Hise, A.G. & Landreth, G.E. (2009) CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J. Neurosci., 29, 11982-11992.
41. Savage, M.J., Lin, Y.G., Ciallella, J.R., Flood, D.G. & Scott, R.W. (2002) Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J. Neurosci., 22, 3376-3385.
42. Scheaffer, R.L., Mendenhall, W. & Ott, R.L. (1996) Systematic sampling (Ch. 7). Elementary Survey Sampling, 5th Edn. Duxbury Press, Boston.
43. Schmitz, C. & Hof, P.R. (2005) Design-based stereology in neuroscience. Neuroscience, 130, 813-831.
44. Simard, A.R. & Rivest, S. (2004) Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J., 18, 998-1000.
45. Simard, A.R., Soulet, D., Gowing, G., Julien, J.P. & Rivest, S. (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron, 49, 489-502.
46. Stalder, M., Phinney, A., Probst, A., Sommer, B., Staufenbiel, M. & Jucker, M. (1999) Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am. J. Pathol., 154, 1673-1684.
47. Wada, T. & Penninger, J.M. (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene, 23, 2838-2849.
48. Wood, C.D., Thornton, T.M., Sabio, G., Davis, R.A. & Rincon, M. (2009) Nuclear localization of p38 MAPK in response to DNA damage. Int. J. Biol. Sci., 5, 428-437.
49. Yakushev, I., Hammers, A., Fellgiebel, A., Schmidtmann, I., Scheurich, A., Buchholz, H.G., Peters, J., Bartenstein, P., Lieb, K. & Schreckenberger, M. (2009) SPM-based count normalization provides excellent discrimination of mild Alzheimer's disease and amnestic mild cognitive impairment from healthy aging. Neuroimage, 44, 43-50.
50. Yosimichi, G., Nakanishi, T., Nishida, T., Hattori, T., Takano-Yamamoto, T. & Takigawa, M. (2001) CTGF/Hcs24 induces chondrocyte differentiation through a p38 mitogen-activated protein kinase (p38MAPK), and proliferation through a p44/42 MAPK/extracellular-signal regulated kinase (ERK). Eur. J. Biochem., 268, 6058-6065.
51. Yune, T.Y., Lee, J.Y., Jung, G.Y., Kim, S.J., Jiang, M.H., Kim, Y.C., Oh, Y.J., Markelonis, G.J. & Oh, T.H. (2007) Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci., 27, 7751-7761.
52. Zhu, X., Raina, A.K., Lee, H.G., Chao, M., Nunomura, A., Tabaton, M., Petersen, R.B., Perry, G. & Smith, M.A. (2003) Oxidative stress and neuronal adaptation in Alzheimer disease: the role of SAPK pathways. Antioxid. Redox Signal., 5, 571-576.