The APOE ε4 genotype modulates CSF YKL-40 levels and their structural brain correlates in the continuum of Alzheimer's disease but not those of sTREM2

Alzheimer's and Dementia: Diagnosis, Assessment and Disease Monitoring

Volumn 6, Issue , 2017, Pages 50-59

  Gispert, Juan Domingo ^a,b,c   Monté, Gemma C ^d   Suárez Calvet, Marc ^e,f   Falcon, Carles ^a,b   Tucholka, Alan ^a   Rojas, Santiago ^a,g   Rami, Lorena ^d   Sánchez Valle, Raquel ^d   Lladó, Albert ^d   Kleinberger, Gernot ^e,h   Haass, Christian ^e,f,h   Molinuevo, José Luis ^a,d  

^a Barcelonaßeta Brain Research Center   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d HOSPITAL CLÍNIC   (Spain)

^e UNIVERSITY OF MUNICH   (Germany)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^g UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^h Technische Universität München Munich Cluster for Systems Neurology   (Germany)

Author keywords

Astrogliosis; Glial biomarkers; Inflammation; Microgliosis; TREM2

Indexed keywords

APOLIPOPROTEIN E4; CHITINASE 3 LIKE PROTEIN 1; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; BRAIN SIZE; BRAIN STRUCTURE; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; GENETIC REGULATION; GENOTYPE; GLIA CELL; GRAY MATTER; HUMAN; IMAGE ANALYSIS; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NERVOUS SYSTEM PARAMETERS; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PROTEIN ANALYSIS; PROTEIN CEREBROSPINAL FLUID LEVEL;

EID: 85010433518     PISSN: None     EISSN: 23528729     Source Type: Journal    
DOI: 10.1016/j.dadm.2016.12.002     Document Type: Article

References (46)

1. [1] Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7 (2011), 270–279.
2. [2] Dubois, B., Feldman, H.H., Jacova, C., Hampel, H., Molinuevo, J.L., Blennow, K., et al. Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria. Lancet Neurol 13 (2014), 614–629.
3. [3] Sperling, R.A., Aisen, P.S., Beckett, L.A., Bennett, D.A., Craft, S., Fagan, A.M., et al. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7 (2011), 280–292.
4. [4] Verghese, P.B., Castellano, J.M., Holtzman, D.M., Apolipoprotein E in Alzheimer's disease and other neurological disorders. Lancet Neurol 10 (2011), 241–252.
5. [5] Liu, C.C., Kanekiyo, T., Xu, H., Bu, G., Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol 9 (2013), 106–118.
6. [6] Gispert, J.D., Rami, L., Sanchez-Benavides, G., Falcon, C., Tucholka, A., Rojas, S., et al. Nonlinear cerebral atrophy patterns across the Alzheimer's disease continuum: impact of APOE4 genotype. Neurobiol Aging 36 (2015), 2687–2701.
7. [7] Liu, Y., Yu, J.T., Wang, H.F., Han, P.R., Tan, C.C., Wang, C., et al. APOE genotype and neuroimaging markers of Alzheimer's disease: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 86 (2015), 127–134.
8. [8] Wolk, D.A., Dickerson, B.C., Alzheimer's Disease Neuroimaging Initiative. Apolipoprotein E (APOE) genotype has dissociable effects on memory and attentional-executive network function in Alzheimer's disease. Proc Natl Acad Sci U S A 107 (2010), 10256–10261.
9. [9] Xu, Q., Bernardo, A., Walker, D., Kanegawa, T., Mahley, R.W., Huang, Y., Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. J Neurosci 26 (2006), 4985–4994.
10. [10] Kim, J., Basak, J.M., Holtzman, D.M., The role of apolipoprotein E in Alzheimer's disease. Neuron 63 (2009), 287–303.
11. [11] Eikelenboom, P., Veerhuis, R., van Exel, E., Hoozemans, J.J., Rozemuller, A.J., van Gool, W.A., The early involvement of the innate immunity in the pathogenesis of late-onset Alzheimer's disease: neuropathological, epidemiological and genetic evidence. Curr Alzheimer Res 8 (2011), 142–150.
12. [12] Heneka, M.T., Carson, M.J., El Khoury, J., Landreth, G.E., Brosseron, F., Feinstein, D.L., et al. Neuroinflammation in Alzheimer's disease. Lancet Neurol 14 (2015), 388–405.
13. [13] Wyss-Coray, T., Loike, J.D., Brionne, T.C., Lu, E., Anankov, R., Yan, F., et al. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9 (2003), 453–457.
14. [14] Koistinaho, M., Lin, S., Wu, X., Esterman, M., Koger, D., Hanson, J., et al. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 10 (2004), 719–726.
15. [15] Atagi, Y., Liu, C.C., Painter, M.M., Chen, X.F., Verbeeck, C., Zheng, H., et al. Apolipoprotein E is a ligand for triggering receptor expressed on myeloid cells 2 (TREM2). J Biol Chem 290 (2015), 26043–26050.
16. [16] Mattsson, N., Tabatabaei, S., Johansson, P., Hansson, O., Andreasson, U., Mansson, J.E., et al. Cerebrospinal fluid microglial markers in Alzheimer's disease: elevated chitotriosidase activity but lack of diagnostic utility. Neuromolecular Med 13 (2011), 151–159.
17. [17] Bonneh-Barkay, D., Bissel, S.J., Kofler, J., Starkey, A., Wang, G., Wiley, C.A., Astrocyte and macrophage regulation of YKL-40 expression and cellular response in neuroinflammation. Brain Pathol 22 (2012), 530–546.
18. [18] Craig-Schapiro, R., Perrin, R.J., Roe, C.M., Xiong, C., Carter, D., Cairns, N.J., et al. YKL-40: a novel prognostic fluid biomarker for preclinical Alzheimer's disease. Biol Psychiatry 68 (2010), 903–912.
19. [19] Sutphen, C.L., Jasielec, M.S., Shah, A.R., Macy, E.M., Xiong, C., Vlassenko, A.G., et al. Longitudinal cerebrospinal fluid biomarker changes in preclinical Alzheimer disease during middle age. JAMA Neurol 72 (2015), 1029–1042.
20. [20] Alcolea, D., Vilaplana, E., Pegueroles, J., Montal, V., Sanchez-Juan, P., Gonzalez-Suarez, A., et al. Relationship between cortical thickness and cerebrospinal fluid YKL-40 in predementia stages of Alzheimer's disease. Neurobiol Aging 36 (2015), 2018–2023.
21. [21] Antonell, A., Mansilla, A., Rami, L., Llado, A., Iranzo, A., Olives, J., et al. Cerebrospinal fluid level of YKL-40 protein in preclinical and prodromal Alzheimer's disease. J Alzheimers Dis 42 (2014), 901–908.
22. [22] Hsieh, C.L., Koike, M., Spusta, S.C., Niemi, E.C., Yenari, M., Nakamura, M.C., et al. A role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia. J Neurochem 109 (2009), 1144–1156.
23. [23] Klesney-Tait, J., Turnbull, I.R., Colonna, M., The TREM receptor family and signal integration. Nat Immunol 7 (2006), 1266–1273.
24. [24] Takahashi, K., Rochford, C.D., Neumann, H., Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201 (2005), 647–657.
25. [25] Wang, Y., Cella, M., Mallinson, K., Ulrich, J.D., Young, K.L., Robinette, M.L., et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model. Cell 160 (2015), 1061–1071.
26. [26] Borroni, B., Ferrari, F., Galimberti, D., Nacmias, B., Barone, C., Bagnoli, S., et al. Heterozygous TREM2 mutations in frontotemporal dementia. Neurobiol Aging 35 (2014), 934.e7–934.e10.
27. [27] Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., et al. TREM2 variants in Alzheimer's disease. N Engl J Med 368 (2013), 117–127.
28. [28] Jonsson, T., Stefansson, H., Steinberg, S., Jonsdottir, I., Jonsson, P.V., Snaedal, J., et al. Variant of TREM2 associated with the risk of Alzheimer's disease. N Engl J Med 368 (2013), 107–116.
29. [29] Roussos, P., Katsel, P., Fam, P., Tan, W., Purohit, D.P., Haroutunian, V., The triggering receptor expressed on myeloid cells 2 (TREM2) is associated with enhanced inflammation, neuropathological lesions and increased risk for Alzheimer's dementia. Alzheimers Dement 11 (2015), 1163–1170.
30. [30] Kleinberger, G., Yamanishi, Y., Suarez-Calvet, M., Czirr, E., Lohmann, E., Cuyvers, E., et al. TREM2 mutations implicated in neurodegeneration impair cell surface transport and phagocytosis. Sci Transl Med, 6, 2014, 243ra86.
31. [31] Piccio, L., Buonsanti, C., Cella, M., Tassi, I., Schmidt, R.E., Fenoglio, C., et al. Identification of soluble TREM-2 in the cerebrospinal fluid and its association with multiple sclerosis and CNS inflammation. Brain 131 (2008), 3081–3091.
32. [32] Heslegrave, A., Heywood, W., Paterson, R., Magdalinou, N., Svensson, J., Johansson, P., et al. Increased cerebrospinal fluid soluble TREM2 concentration in Alzheimer's disease. Mol Neurodegener, 11, 2016, 3.
33. [33] Suarez-Calvet, M., Kleinberger, G., Araque Caballero, M.A., Brendel, M., Rominger, A., Alcolea, D., et al. 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 (2016), 466–476.
34. [34] Piccio, L., Deming, Y., Del-Aguila, J.L., Ghezzi, L., Holtzman, D.M., Fagan, A.M., et al. Cerebrospinal fluid soluble TREM2 is higher in Alzheimer disease and associated with mutation status. Acta Neuropathol 131 (2016), 925–933.
35. [35] Bailey, C.C., DeVaux, L.B., Farzan, M., The triggering receptor expressed on myeloid cells 2 binds Apolipoprotein E. J Biol Chem 290 (2015), 26033–26042.
36. [36] Li, X., Montine, K.S., Keene, C.D., Montine, T.J., Different mechanisms of apolipoprotein E isoform-dependent modulation of prostaglandin E2 production and triggering receptor expressed on myeloid cells 2 (TREM2) expression after innate immune activation of microglia. FASEB J 29 (2015), 1754–1762.
37. [37] Gispert, J.D., Monte, G.C., Falcon, C., Tucholka, A., Rojas, S., Sanchez-Valle, R., et al. CSF YKL-40 and pTau181 are related to different cerebral morphometric patterns in early AD. Neurobiol Aging 38 (2016), 47–55.
38. [38] Gispert, J.D., Suarez-Calvet, M., Monté, G.C., Tucholka, A., Falcon, C., Rojas, S., et al. Cerebrospinal fluid sTREM2 levels are associated with gray matter volume increases and reduced diffusivity in early Alzheimer's Disease. Alzheimers Dement 12 (2016), 1259–1272.
39. [39] Pena-Casanova, J., Aguilar, M., Santacruz, P., Bertran-Serra, I., Hernandez, G., Sol, J.M., et al. (Trans.) Adaptation and normalization of the Alzheimer's disease Assessment Scale for Spain (NORMACODEM) (II) Neurologia 12 (1997), 69–77.
40. [40] Blesa, R., Pujol, M., Aguilar, M., Santacruz, P., Bertran-Serra, I., Hernandez, G., et al. Clinical validity of the ‘mini-mental state’ for Spanish speaking communities. Neuropsychologia 39 (2001), 1150–1157.
41. [41] Sjogren, M., Vanderstichele, H., Agren, H., Zachrisson, O., Edsbagge, M., Wikkelso, C., et al. Tau and Abeta42 in cerebrospinal fluid from healthy adults 21-93 years of age: establishment of reference values. Clin Chem 47 (2001), 1776–1781.
42. [42] Jack, C.R. Jr., Albert, M.S., Knopman, D.S., McKhann, G.M., Sperling, R.A., Carrillo, M.C., et al. Introduction to the recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7 (2011), 257–262.
43. [43] Molinuevo, J.L., Gispert, J.D., Dubois, B., Heneka, M.T., Lleo, A., Engelborghs, S., et al. The AD-CSF-index discriminates Alzheimer's disease patients from healthy controls: a validation study. J Alzheimers Dis 36 (2013), 67–77.
44. [44] Alemán-Gómez Y, Melie-García L, Valdés-Hernandez P. IBASPM: toolbox for automatic parcellation of brain structures. 12th Annual Meeting of the Organization for Human Brain Mapping. Florence, Italy 2006.
45. [45] Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15 (2002), 273–289.
46. [46] Espeseth, T., Westlye, L.T., Fjell, A.M., Walhovd, K.B., Rootwelt, H., Reinvang, I., Accelerated age-related cortical thinning in healthy carriers of apolipoprotein E epsilon 4. Neurobiol Aging 29 (2008), 329–340.