Higher Peripheral TREM2 mRNA Levels Relate to Cognitive Deficits and Hippocampal Atrophy in Alzheimer's Disease and Amnestic Mild Cognitive Impairment

Journal of Alzheimer's Disease

Volumn 58, Issue 2, 2017, Pages 413-423

  Tan, Yi Jayne ^a,b   Ng, Adeline S L ^b   Vipin, Ashwati ^a   Lim, Joseph K W ^a   Chander, Russell J ^b   Ji, Fang ^a   Qiu, Yingwei ^a   Ting, Simon K S ^c   Hameed, Shahul ^c   Lee, Tih Shih ^a   Zeng, Li ^b   Kandiah, Nagaendran ^b   Zhou, Juan ^a,d  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

^c SINGAPORE GENERAL HOSPITAL   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Alzheimer's disease; atrophy; blood based biomarkers; hippocampus; mild cognitive impairment; TREM2

Indexed keywords

APOLIPOPROTEIN E4; MESSENGER RNA; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; APOLIPOPROTEIN E; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; TREM2 PROTEIN, HUMAN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; EPISODIC MEMORY; FEMALE; GENOTYPE; GRAY MATTER; HIPPOCAMPUS; HUMAN; IMAGE PROCESSING; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; MONTREAL COGNITIVE ASSESSMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; VOXEL BASED MORPHOMETRY; ANALYSIS OF VARIANCE; ATROPHY; BLOOD; COHORT ANALYSIS; COMPLICATION; DIAGNOSTIC IMAGING; GENETICS; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; STATISTICS; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; APOLIPOPROTEINS E; ATROPHY; COGNITION DISORDERS; COHORT STUDIES; FEMALE; GENOTYPE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; STATISTICS AS TOPIC;

EID: 85019218273     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-161277     Document Type: Article

References (53)

1. Colonna M (2003) TREMs in the immune system and beyond. Nat Rev Immunol 3, 445-453.
2. Hsieh CL, Koike M, Spusta S, Niemi E, Yenari M, Nakamura MC, SeamanWE(2009) A role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia. J Neurochem 109, 1144-1156.
3. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JSK, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert J-C, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St George-Hyslop P, Singleton A, Hardy J, Alzheimer Genetic Analysis Group (2013) TREM2 variants in Alzheimer's disease. N Engl J Med 368, 117-127.
4. 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, 107-116.
5. Lue L-F, Schmitz CT, Serrano G, Sue LI, Beach TG, Walker DG (2015) TREM2 protein expression changes correlate with Alzheimer's disease neurodegenerative pathologies in post-mortem temporal cortices. Brain Pathol 25, 469-480.
6. Celarain N, Sánchez-Ruiz de Gordoa J, Zelaya MV, Roldán M, Larumbe R, Pulido L, Echavarri C, Mendioroz M (2016) TREM2 upregulation correlates with 5-hydroxymethycytosine enrichment in Alzheimer's disease hippocampus. Clin Epigenetics 8, 37.
7. Heslegrave A, Heywood W, Paterson R, Magdalinou N, Svensson J, Johansson P, Ohrfelt A, Blennow K, Hardy J, Schott J, Mills K, Zetterberg H (2016) Increased cerebrospinal fluid soluble TREM2 concentration in Alzheimer's disease. Mol Neurodegener 11, 3. doi: 10.1186/s13024-016-0071-x
8. Piccio L, Buonsanti C, Cella M, Tassi I, Schmidt RE, Fenoglio C, Rinker J, Naismith RT, Panina-Bordignon P, Passini N, Galimberti D, Scarpini E, Colonna M, Cross AH (2008) Identification of soluble TREM-2 in the cerebrospinal fluid and its association with multiple sclerosis and CNS inflammation. Brain 131, 3081-3091.
9. Baird AL, Westwood S, Lovestone S (2015) Blood-based proteomic biomarkers of Alzheimer's disease pathology. Front Neurol 6, 236.
10. Hu N, Tan M-S, Yu J-T, Sun L, Tan L, Wang Y-L, Jiang T, Tan L (2014) Increased expression of TREM2 in peripheral blood of Alzheimer's disease patients. J Alzheimers Dis 38, 497-501.
11. Mori Y, Yoshino Y, Ochi S, Yamazaki K, Kawabe K, Abe M, Kitano T, Ozaki Y, Yoshida T, Numata S, Mori T, Iga J, Kuroda N, Ohmori T, Ueno S-I (2015) TREM2 mRNA expression in leukocytes is increased in Alzheimer's disease and schizophrenia. PLoS One 10, e0136835.
12. Guedes JR, Santana I, Cunha C, Duro D, Almeida MR, Cardoso AM, de Lima MC, Cardoso AL (2016) MicroRNA deregulation and chemotaxis and phagocytosis impairment in Alzheimer's disease. Alzheimers Dement (Amst) 3, 7-17.
13. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (2011) The diagnosis of dementia 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, 263-269.
14. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol 56, 303-308.
15. FolsteinMF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
16. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA:Abrief screening tool for mild cognitive impairment. J Am Geriatr Soc 53, 695-699.
17. Mohs RC, CohenL(1988) Alzheimer's Disease Assessment Scale (ADAS). Psychopharmacol Bull 24, 627-628.
18. Hartman DE (2009) Wechsler Adult Intelligence Scale IV (WAIS IV): Return of the gold standard. Appl Neuropsychol 16, 85-87.
19. Dubois B, SlachevskyA, Litvan I, PillonB(2000) The FAB: A Frontal Assessment Battery at bedside. Neurology 55, 1621-1626.
20. Elia LF, Satz P, Uchiyama CL, Uchiyama CL, White T (1996) Color Trails Test: Professional Manual. Psychological Assessment Resources, Odessa, FL.
21. Cheung RW, Cheung M-C, Chan AS (2004) Confrontation naming in Chinese patients with left, right or bilateral brain damage. J Int Neuropsychol Soc 10, 46-53.
22. Dale AM, Fischl B, Sereno MI (1999) Cortical surfacebased analysis. I. Segmentation and surface reconstruction. Neuroimage 9, 179-194.
23. Fischl B, Sereno MI, Dale AM (1999) Cortical surfacebased analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195-207.
24. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355.
25. Fischl B, Salat DH, van der Kouwe AJ, Makris N, Segonne F, Quinn BT, Dale AM (2004) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23 (Suppl 1), S69-S84.
26. Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, Snyder AZ (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: Reliability and validation against manual measurement of total intracranial volume. Neuroimage 23, 724-738.
27. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14, 21-36.
28. Ng KK, Lo JC, Lim JK, CheeMW, Zhou J (2016) Reduced functional segregation between the default mode network and the executive control network in healthy older adults: A longitudinal study. Neuroimage 133, 321-330.
29. Chong JS, Ng GJ, Lee SC, Zhou J (2016) Salience network connectivity in the insula is associated with individual differences in interoceptive accuracy. Brain Struct Funct, 1-10. doi: 10.1007/s00429-016-1297-7
30. Firbank MJ, Minett T, O'Brien JT (2003) Changes in DWI and MRS associated with white matter hyperintensities in elderly subjects. Neurology 61, 950-954.
31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
32. Koch W, Ehrenhaft A, Griesser K, Pfeufer A, Müller J, Schömig A, Kastrati A (2002) TaqMan systems for genotyping of disease-related polymorphisms present in the gene encoding apolipoprotein E. Clin Chem Lab Med 40, 1123-1131.
33. Whitney AR, Diehn M, Popper SJ, Alizadeh AA, Boldrick JC, Relman DA, Brown PO (2003) Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci U S A 100, 1896-1901.
34. Eady JJ, Wortley GM, Wormstone YM, Hughes JC, Astley SB, Foxall RJ, Doleman JF, Elliott RM (2005) Variation in gene expression profiles of peripheral blood mononuclear cells from healthy volunteers. Physiol Genomics 22, 402-411.
35. Berchtold NC, Cribbs DH, Coleman PD, Rogers J, Head E, Kim R, Beach T, Miller C, Troncoso J, Trojanowski JQ, Zielke HR, Cotman CW (2008) Gene expression changes in the course of normal brain aging are sexually dimorphic. Proc Natl Acad Sci U S A 105, 15605-15610.
36. Spielman RS, Bastone LA, Burdick JT, Morley M, Ewens WJ, Cheung VG (2007) Common genetic variants account for differences in gene expression among ethnic groups. Nat Genet 39, 226-231.
37. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923.
38. Agosta F, Vossel KA, Miller BL, Migliaccio R, Bonasera SJ, Filippi M, Boxer AL, Karydas A, Possin KL, Gorno-TempiniML(2009) Apolipoprotein E epsilon4 is associated with disease-specific effects on brain atrophy in Alzheimer's disease and frontotemporal dementia. Proc Natl Acad Sci U S A 106, 2018-2022.
39. Pievani M, Galluzzi S, Thompson PM, Rasser PE, Bonetti M, Frisoni GB (2011) APOE4 is associated with greater atrophy of the hippocampal formation in Alzheimer's disease. Neuroimage 55, 909-919.
40. Caselli RJ, Reiman EM, Osborne D, Hentz JG, Baxter LC, Hernandez JL, Alexander GG (2004) Longitudinal changes in cognition and behavior in asymptomatic carriers of the APOE e4 allele. Neurology 62, 1990-1995.
41. Caselli RJ, Reiman EM, Locke DE, Hutton ML, Hentz JG, Hoffman-Snyder C, Woodruff BK, Alexander GE, Osborne D (2007) Cognitive domain decline in healthy apolipoprotein E epsilon4 homozygotes before the diagnosis of mild cognitive impairment. Arch Neurol 64, 1306-1311.
42. Susanto TA, Pua EP, Zhou J, Alzheimer's Disease Neuroimaging Initiative (2015) Cognition, brain atrophy, and cerebrospinal fluid biomarkers changes from preclinical to dementia stage of Alzheimer's disease and the influence of apolipoprotein E. J Alzheimers Dis 45, 253-268.
43. Trzepacz PT, Hochstetler H, Wang S, Walker B, Saykin AJ (2015) Relationship between the Montreal Cognitive Assessment and Mini-mental State Examination for assessment of mild cognitive impairment in older adults. BMC Geriatrics 15, 107.
44. Wang Y, Ulland TK, Ulrich JD, Song W, Tzaferis JA, Hole JT, Yuan P, Mahan TE, Shi Y, Gilfillan S, Cella M, Grutzendler J, DeMattos RB, Cirrito JR, Holtzman DM, ColonnaM(2016) TREM2-mediated early microglial response limits diffusion and toxicity of amyloid plaques. J Exp Med 213, 667-675.
45. Savage JC, Jay T, Goduni E, Quigley C, Mariani MM, Malm T, Ransohoff RM, Lamb BT, Landreth GE (2015) Nuclear receptors license phagocytosis by trem2+ myeloid cells in mouse models of Alzheimer's disease. J Neurosci 35, 6532-6543.
46. Frank S, Burbach GJ, Bonin M, Walter M, Streit W, Bechmann I, Deller T (2008)TREM2is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56, 1438-1447.
47. Varvel NH, Grathwohl SA, Baumann F, Liebig C, Bosch A, Brawek B, Thal DR, Charo IF, Heppner FL, Aguzzi A, Garaschuk O, Ransohoff RM, Jucker M (2012) Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc Natl Acad Sci U S A 109, 18150-18155.
48. Jay TR, Miller CM, Cheng PJ, Graham LC, Bemiller S, Broihier ML, Xu G, Margevicius D, Karlo JC, Sousa GL, Cotleur AC, Butovsky O, Bekris L, Staugaitis SM, Leverenz JB, Pimplikar SW, Landreth GE, Howell GR, Ransohoff RM, Lamb BT (2015) TREM2 deficiency eliminates TREM2+ inflammatory macrophages and ameliorates pathology in Alzheimer's disease mouse models. J Exp Med 212, 287-295.
49. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13, 432-438.
50. Naert G, Rivest S (2011) CC chemokine receptor 2 deficiency aggravates cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. J Neurosci 31, 6208-6220.
51. Naert G, Rivest S (2012) Hematopoietic CC-chemokine receptor 2 (CCR2) competent cells are protective for the cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. Mol Med 18, 297-313.
52. Maier T, Güell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583, 3966-3973.
53. Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13, 227-232.