Increase of TREM2 during aging of an Alzheimer's disease mouse model is paralleled by microglial activation and amyloidosis

Frontiers in Aging Neuroscience

Volumn 9, Issue JAN, 2017, Pages

  Brendel, Matthias ^a   Kleinberger, Gernot ^a   Probst, Federico ^a   Jaworska, Anna ^b,c   Overhoff, Felix ^a   Blume, Tanja ^a   Albert, Nathalie L ^a   Carlsen, Janette ^a   Lindner, Simon ^a   Gildehaus, Franz Josef ^a   Ozmen, Laurence ^d   Suárez Calvet, Marc ^a,b   Bartenstein, Peter ^a   Baumann, Karlheinz ^d   Ewers, Michael ^b   Herms, Jochen ^a,b   Haass, Christian ^a,b   Rominger, Axel ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Alzheimer's disease; Amyloid PET; Neuroinflammation; TREM2; TSPO PET

Indexed keywords

AMYLOID PROTEIN; BIOLOGICAL MARKER; FLORBETABEN; FLUTRICICLAMIDE F 18; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2;

AGING; ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL ACTIVATION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; DISEASE COURSE; HISTOPATHOLOGY; MICROGLIA; MOUSE; MOUSE MODEL; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION;

EID: 85012165835     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2017.00008     Document Type: Article

References (46)

1. Bateman, R. J., Xiong, C., Benzinger, T. L., Fagan, A. M., Goate, A., Fox, N. C., et al. (2012). Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N. Engl. J. Med. 367, 795-804. doi: 10.1056/NEJMoa1202753
2. Birch, A. M., Katsouri, L., and Sastre, M. (2014). Modulation of inflammation in transgenic models of Alzheimer's disease. J. Neuroinflammation 11:25. doi: 10.1186/1742-2094-11-25
3. Brendel, M., Högenauer, M., Delker, A., Sauerbeck, J., Bartenstein, P., Seibyl, J., et al. (2015). Improved longitudinal [18F]-AV45 amyloid PET by white matter reference and VOI-based partial volume effect correction. Neuroimage 108, 450-459. doi: 10.1016/j.neuroimage.2014.11.055
4. Brendel, M., Jaworska, A., Grießinger, E., Rötzer, C., Burgold, S., Gildehaus, F. J., et al. (2015). Cross-sectional comparison of small animal [18F]-florbetaben amyloid-PET between transgenic AD mouse models. PLoS One 10:e0116678. doi: 10.1371/journal.pone.0116678
5. Brendel, M., Jaworska, A., Herms, J., Trambauer, J., Rotzer, C., Gildehaus, F. J., et al. (2015). Amyloid-PET predicts inhibition of de novo plaque formation upon chronic γ-secretase modulator treatment. Mol. Psychiatry 20, 1179-1187. doi: 10.1038/mp.2015.74
6. Brendel, M., Probst, F., Jaworska, A., Overhoff, F., Korzhova, V., Albert, N., et al. (2016). Glial activation and glucose metabolism in a transgenic amyloid mouse model: a triple tracer PET study. J. Nucl. Med. 57, 954-960. doi: 10.2967/jnumed.115.167858
7. Dickens, A. M., Vainio, S., Marjamäki, P., Johansson, J., Lehtiniemi, P., Rokka, J., et al. (2014). Detection of microglial activation in an acute model of neuroinflammation using PET and radiotracers 11C-(R)-PK11195 and 18F-GE-180. J. Nucl. Med. 55, 466-472. doi: 10.2967/jnumed.113.125625
8. Dorr, A., Sled, J. G., and Kabani, N. (2007). Three-dimensional cerebral vasculature of the CBA mouse brain: a magnetic resonance imaging and micro computed tomography study. Neuroimage 35, 1409-1423. doi: 10.1016/j.neuroimage.2006.12.040
9. Duyckaerts, C., Delatour, B., and Potier, M. C. (2009). Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 118, 5-36. doi: 10.1007/s00401-009-0532-1
10. Förster, S., Grimmer, T., Miederer, I., Henriksen, G., Yousefi, B. H., Graner, P., et al. (2012). Regional expansion of hypometabolism in Alzheimer's disease follows amyloid deposition with temporal delay. Biol. Psychiatry 71, 792-797. doi: 10.1016/j.biopsych.2011.04.023
11. Frank, S., Burbach, G. J., Bonin, M., Walter, M., Streit, W., Bechmann, I., et al. (2008). TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56, 1438-1447. doi: 10.1002/glia.20710
12. Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., et al. (2013). TREM2 variants in Alzheimer's disease. N. Engl. J. Med. 368, 117-127. doi: 10.1056/NEJMoa1211851
13. Hall, A. M., and Roberson, E. D. (2012). Mouse models of Alzheimer's disease. Brain Res. Bull. 88, 3-12. doi: 10.1016/j.brainresbull.2011.11.017
14. Heneka, M. T., Carson, M. J., El Khoury, J., Landreth, G. E., Brosseron, F., Feinstein, D. L., et al. (2015). Neuroinflammation in Alzheimer's disease. Lancet Neurol. 14, 388-405. doi: 10.1016/S1474-4422(15)70016-5
15. Heslegrave, A., Heywood, W., Paterson, R., Magdalinou, N., Svensson, J., Johansson, P., et al. (2016). Increased cerebrospinal fluid soluble TREM2 concentration in Alzheimer's disease. Mol. Neurodegener. 11:3. doi: 10.1186/s13024-016-0071-x
16. Jonsson, T., Stefansson, H., Steinberg, S., Jonsdottir, I., Jonsson, P. V., Snaedal, J., et al. (2013). Variant of TREM2 associated with the risk of Alzheimer's disease. N. Engl. J. Med. 368, 107-116. doi: 10.1056/NEJMoa1211103
17. Kleinberger, G., Yamanishi, Y., Suárez-Calvet, M., Czirr, E., Lohmann, E., Cuyvers, E., et al. (2014). TREM2 mutations implicated in neurodegeneration impair cell surface transport and phagocytosis. Sci. Transl. Med. 6:243ra86. doi: 10.1126/scitranslmed.3009093
18. Liu, B., Le, K. X., Park, M. A., Wang, S., Belanger, A. P., Dubey, S., et al. (2015). In vivo detection of age-and disease-related increases in neuroinflammation by 18F-GE180 TSPO MicroPET imaging in wild-type and Alzheimer's transgenic mice. J. Neurosci. 35, 15716-15730. doi: 10.1523/JNEUROSCI.0996-15.2015
19. Manook, A., Yousefi, B. H., Willuweit, A., Platzer, S., Reder, S., Voss, A., et al. (2012). Small-animal PET imaging of amyloid-beta plaques with [11C]PiB and its multi-modal validation in an APP/PS1 mouse model of Alzheimer's disease. PLoS One 7:e31310. doi: 10.1371/journal.pone.0031310
20. Matarin, M., Salih, D. A., Yasvoina, M., Cummings, D. M., Guelfi, S., Liu, W., et al. (2015). A genome-wide gene-expression analysis and database in transgenic mice during development of amyloid or tau pathology. Cell Rep. 10, 633-644. doi: 10.1016/j.celrep.2014.12.041
21. Minter, M. R., Main, B. S., Brody, K. M., Zhang, M., Taylor, J. M., and Crack, P. J. (2015). Soluble amyloid triggers a myeloid differentiation factor 88 and interferon regulatory factor 7 dependent neuronal type-1 interferon response in vitro. J. Neuroinflammation 12:71. doi: 10.1186/s12974-015-0263-2
22. Mirzaei, N., Tang, S. P., Ashworth, S., Coello, C., Plisson, C., Passchier, J., et al. (2016). In vivo imaging of microglial activation by positron emission tomography with [11C]PBR28 in the 5XFAD model of Alzheimer's disease. Glia 64, 993-1006. doi: 10.1002/glia.22978
23. Overhoff, F., Brendel, M., Jaworska, A., Korzhova, V., Delker, A., Probst, F., et al. (2016). Automated spatial brain normalization and hindbrain white matter reference tissue give improved [18F]-Florbetaben PET quantitation in Alzheimer's model mice. Front. Neurosci. 10:45. doi: 10.3389/fnins.2016.00045
24. Ozmen, L., Albientz, A., Czech, C., and Jacobsen, H. (2009). Expression of transgenic APP mRNA is the key determinant for beta-amyloid deposition in PS2APP transgenic mice. Neurodegener. Dis. 6, 29-36. doi: 10.1159/000170884
25. Piccio, L., Buonsanti, C., Cella, M., Tassi, I., Schmidt, R. E., Fenoglio, C., et al. (2008). Identification of soluble TREM-2 in the cerebrospinal fluid and its association with multiple sclerosis and CNS inflammation. Brain 131, 3081-3091. doi: 10.1093/brain/awn217
26. Piccio, L., Deming, Y., Del-águila, J. L., Ghezzi, L., Holtzman, D. M., Fagan, A. M., et al. (2016). Cerebrospinal fluid soluble TREM2 is higher in Alzheimer disease and associated with mutation status. Acta Neuropathol. 131, 925-933. doi: 10.1007/s00401-016-1533-5
27. Price, J. C., Klunk, W. E., Lopresti, B. J., Lu, X., Hoge, J. A., Ziolko, S. K., et al. (2005). Kinetic modeling of amyloid binding in humans using PET imaging and Pittsburgh Compound-B. J. Cereb. Blood Flow Metab. 25, 1528-1547. doi: 10.1038/sj.jcbfm.9600146
28. Richards, J. G., Higgins, G. A., Ouagazzal, A. M., Ozmen, L., Kew, J. N., Bohrmann, B., et al. (2003). PS2APP transgenic mice, coexpressing hPS2mut and hAPPswe, show age-related cognitive deficits associated with discrete brain amyloid deposition and inflammation. J. Neurosci. 23, 8989-9003.
29. Rodriguez-Vieitez, E., Ni, R., Gulyás, B., Tóth, M., Häggkvist, J., Halldin, C., et al. (2015). Astrocytosis precedes amyloid plaque deposition in Alzheimer APPswe transgenic mouse brain: a correlative positron emission tomography and in vitro imaging study. Eur. J. Nucl. Med. Mol. Imaging 42, 1119-1132. doi: 10.1007/s00259-015-3047-0
30. Rominger, A., Mille, E., Zhang, S., Böning, G., Förster, S., Nowak, S., et al. (2010). Validation of the octamouse for simultaneous 18F-fallypride small-animal PET recordings from 8 mice. J. Nucl. Med. 51, 1576-1583. doi: 10.2967/jnumed.110.078451
31. Rominger, A., Brendel, M., Burgold, S., Keppler, K., Baumann, K., Xiong, G., et al. (2013). Longitudinal assessment of cerebral β-amyloid deposition in mice overexpressing swedish mutant β-amyloid precursor protein using 18F-florbetaben PET. J. Nucl. Med. 54, 1127-1134. doi: 10.2967/jnumed.112.114660
32. Sawiak, S. J., Wood, N. I., Williams, G. B., Morton, A. J., and Carpenter, T. A. (2009). Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol. Dis. 33, 20-27. doi: 10.1016/j.nbd.2008.09.016
33. Suárez-Calvet, M., Araque Caballero, M. á., Kleinberger, G., Bateman, R. J., Fagan, A. M., Morris, C. M., et al. (2016). Early changes of CSF sTREM2 in dominantly inherited Alzheimer's disease follow markers of amyloid deposition and neuronal injury. Sci. Transl. Med. 8:369ra178. doi: 10.1126/scitranslmed.aag1767
34. Suárez-Calvet, M., Kleinberger, G., Araque Caballero, M. á., Brendel, M., Rominger, A., Alcolea, D., et al. (2016). sTREM2 cerebrospinal fluid levels are a potential biomarker for microglia activity in early-stage Alzheimer's disease and associate with neuronal injury markers. EMBO Mol. Med. 8, 466-476. doi: 10.15252/emmm.201506123
35. Tanzi, R. E. (2015). TREM2 and risk of Alzheimer's disease-friend or foe? N. Engl. J. Med. 372, 2564-2565. doi: 10.1056/NEJMcibr1503954
36. Teipel, S. J., Buchert, R., Thome, J., Hampel, H., and Pahnke, J. (2011). Development of Alzheimer-disease neuroimaging-biomarkers using mouse models with amyloid-precursor protein-transgene expression. Prog. Neurobiol. 95, 547-556. doi: 10.1016/j.pneurobio.2011.05.004
37. Villemagne, V. L., Burnham, S., Bourgeat, P., Brown, B., Ellis, K. A., Salvado, O., et al. (2013). Amyloid β deposition, neurodegeneration and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol. 12, 357-367. doi: 10.1016/S1474-4422(13)70044-9
38. Virdee, K., Cumming, P., Caprioli, D., Jupp, B., Rominger, A., Aigbirhio, F. I., et al. (2012). Applications of positron emission tomography in animal models of neurological and neuropsychiatric disorders. Neurosci. Biobehav. Rev. 36, 1188-1216. doi: 10.1016/j.neubiorev.2012.01.009
39. Wang, Y., Cella, M., Mallinson, K., Ulrich, J. D., Young, K. L., Robinette, M. L., et al. (2015). TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model. Cell 160, 1061-1071. doi: 10.1016/j.cell.2015.01.049
40. Wang, Y., Ulland, T. K., Ulrich, J. D., Song, W., Tzaferis, J. A., Hole, J. T., et al. (2016). TREM2-mediated early microglial response limits diffusion and toxicity of amyloid plaques. J. Exp. Med. 213, 667-675. doi: 10.1084/jem.20151948
41. Weiner, M. W., Veitch, D. P., Aisen, P. S., Beckett, L. A., Cairns, N. J., Green, R. C., et al. (2012). The Alzheimer's disease neuroimaging initiative: a review of papers published since its inception. Alzheimers Dement. 8, S1-S68. doi: 10.1016/j.jalz.2011.09.172
42. Wickstrøm, T., Clarke, A., Gausemel, I., Horn, E., Jørgensen, K., Khan, I., et al. (2014). The development of an automated and GMP compliant FASTlab Synthesis of [18F]GE-180; a radiotracer for imaging translocator protein (TSPO). J. Labelled Comp. Radiopharm. 57, 42-48. doi: 10.1002/jlcr.3112
43. Wunderlich, P., Glebov, K., Kemmerling, N., Tien, N. T., Neumann, H., and Walter, J. (2013). Sequential proteolytic processing of the triggering receptor expressed on myeloid cells-2 (TREM2) protein by ectodomain shedding and gamma-secretase-dependent intramembranous cleavage. J. Biol. Chem. 288, 33027-33036. doi: 10.1074/jbc.M113.517540
44. Xiang, X., Werner, G., Bohrmann, B., Liesz, A., Mazaheri, F., Capell, A., et al. (2016). TREM2 deficiency reduces the efficacy of immunotherapeutic amyloid clearance. EMBO Mol. Med. 8, 992-1004. doi: 10.15252/emmm.201606370
45. Ziegler-Graham, K., Brookmeyer, R., Johnson, E., and Arrighi, H. M. (2008). Worldwide variation in the doubling time of Alzheimer's disease incidence rates. Alzheimers Dement. 4, 316-323. doi: 10.1016/j.jalz.2008.05.2479
46. Zimmer, E. R., Parent, M. J., Cuello, A. C., Gauthier, S., and Rosa-Neto, P. (2014). MicroPET imaging and transgenic models: a blueprint for Alzheimer's disease clinical research. Trends Neurosci. 37, 629-641. doi: 10.1016/j.tins.2014.07.002