Variable expression of microglial DAP12 and TREM2 genes in Nasu-Hakola disease

Neurogenetics

Volumn 16, Issue 4, 2015, Pages 265-276

  Sasaki, Atsushi ^a   Kakita, Akiyoshi ^b   Yoshida, Kunihiro ^c   Konno, Takuya ^b   Ikeuchi, Takeshi ^b   Hayashi, Shintaro ^d   Matsuo, Hidenori ^e   Shioda, Kei ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d Mishima Hospital   (Japan)

^e Nagasaki Kawatana Medical Center   (Japan)

Author keywords

DAP12; Macrophage; Microglia; Nasu Hakola disease; PLOSL; TREM2

Indexed keywords

MESSENGER RNA; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TREM2 PROTEIN, HUMAN; TYROBP PROTEIN, HUMAN;

ADULT; ARTICLE; BRAIN DISEASE; DNAX ACTIVATION PROTEIN 12 GENE; FEMALE; FRAMESHIFT MUTATION; GENE; GENE EXPRESSION; GENE SEQUENCE; GENETIC SCREENING; GENOTYPE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MIDDLE AGED; MISSENSE MUTATION; MOLECULAR CLONING; NASU HAKOLA DISEASE; NUCLEIC ACID BASE SUBSTITUTION; PHENOTYPE; PRESENILE DEMENTIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE DISTRIBUTION; TRANSLATION INITIATION; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2 GENE; WESTERN BLOTTING; WHITE MATTER; BRAIN; CHONDRODYSPLASIA; GENETICS; LIPODYSTROPHY; METABOLISM; SUBACUTE SCLEROSING PANENCEPHALITIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; BRAIN; FEMALE; GENOTYPE; HUMANS; LIPODYSTROPHY; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROGLIA; MIDDLE AGED; OSTEOCHONDRODYSPLASIAS; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; SUBACUTE SCLEROSING PANENCEPHALITIS;

EID: 84942198698     PISSN: 13646745     EISSN: 13646753     Source Type: Journal    
DOI: 10.1007/s10048-015-0451-3     Document Type: Article

References (47)

1. Hakola HPA (1972) Neuropsychiatric and genetic aspects of a new hereditary disease characterized by progressive dementia and lipomembranous polycystic osteodysplasia. Acta Psychiatr Scand 232(suppl):1–17
2. Nasu T, Tsukahara Y, Terayama K (1973) A lipid metabolic disease—“membranous lipodystrophy”—an autopsy case demonstrating numerous peculiar membrane structures composed of compound lipid in bone and bone marrow and various adipose tissues. Acta Pathol Jpn 23:539–559
3. Pekkarinen P, Hovatta I, Hakola P, Jarvi O, Kestila M, Lenkkeri U, Adolfsson R, Holmgren G, Nylander PO, Tranebjaerg L et al (1998) Assignment of the locus for PLOSL, a frontal-lobe dementia with bone cysts, to 19q13. Am J Hum Genet 62:362–372
4. Kaneko M, Sano K, Nakayama J, Amano N (2010) Nasu-Hakola disease: the first case reported by Nasu and review. Neuropathology 30:463–470
5. Roumier A, Bechade C, Poncer JC, Smalla KH, Tomasello E, Vivier E, Gundelfinger ED, Triller A, Bessis A (2004) Impaired synaptic function in the microglial KARAP/DAP12-deficient mouse. J Neurosci 24:11421–11428
6. Thrash JC, Torbett BE, Carson MJ (2009) Developmental regulation of TREM2 and DAP12 expression in the murine CNS: implications for Nasu-Hakola disease. Neurochem Res 34:38–45
7. Graeber MB, Streit WJ (2010) Microglia: biology and pathology. Acta Neuropathol 119:89–105
8. Kettenmann K, Kirchhoff F, Verkhratsky A (2013) Microglia: new roles for the synaptic stripper. Neuron 77:10–18
9. Saijo K, Glass CK (2011) Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 11:775–787
10. Imai Y, Ibata I, Ito D, Ohsawa K, Kosaka S (1996) A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224:855–862
11. Paulus W, Roggendorf W, Kirchner T (1992) Ki-M1P as a marker for microglia and brain macrophages in routinely processed human tissues. Acta Neuropathol 84:538–844
12. Sasaki A, Nakazato Y (1992) The identity of cells expressing MHC class II antigens in normal and pathological human brain. Neuropathol Appl Neurobiol 18:13–26
13. Husemann J, Loike JD, Anankov R, Febbraio M, Silverstein SC (2002) Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system. Glia 40:195–205
14. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495
15. Minagawa M, Maeshiro H, Shioda K, Hirano A (1985) Membranous lipodystrophy (Nasu disease): clinical and neuropathological study of a case. Clin Neuropathol 4:38–45
16. Kondo T, Takahashi K, Kohara N, Takahashi Y, Hayashi S, Takahashi H, Matsuo H, Yamazaki M, Inoue K, Miyamoto K et al (2002) Heterogeneity of presenile dementia with bone cysts (Nasu-Hakola disease). Neurology 59:1105–1107
17. Paloneva J, Kestila M, Wu J, Salminen A, Bohling T, Ruotsalainen V, Hakola P, Bakker AB, Phillips JH, Pekkarinen P et al (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25:357–361
18. Numasawa Y, Yamamura C, Ishihara S, Shintani S, Yamazaki M, Tabunoki H, Satoh J-I (2010) Nasu-Hakola disease with a splicing mutation of TREM2 in a Japanese family. Eur J Neurol 18:1179–1183
19. Konno T, Tada M, Tada M, Koyama A, Nozaki H, Harigaya Y, Nishimiya J, Matsunaga A, Yoshikura N, Ishihara K et al (2013) Haploinsufficiency of CSF-1R and clinicopathologic characterization in patients with HDLS. Neurology 82:139–148
20. Lanier LL, Corliss B, Wu J, Phillips JH (1998) Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 8:693–701
21. Humpherey MB, Lanier LL, Nakamura MC (2005) Role of ITAM-containing adapter proteins and their receptors in the immune system and bone. Immunol Rev 208:50–65
22. Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH (1998) Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391:703–707
23. Kiialainen A, Hovanes K, Paloneva J, Kopra O, Peltonen L (2005) Dap12 and Trem2, molecules involved in innate immunity and neurodegeneration, are co-expressed in the CNS. Neurobiol Dis 18:314–322
24. Wakselman S, Bechade C, Roomier A, Bernard D, Triller A, Bessis A (2008) Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J Neurosci 28:8138–8143
25. Otero K, Turnbull IR, Poliani PL, Vermi W, Cerutti E, Aoshi T, Tassi I, Takai T, Stanley SL, Miller M et al (2009) Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and b-catenin. Nat Immunol 10:734–744
26. Mehdi H, Ono E, Gupta KC (1990) Initiation of translation at CUG, GUG, and ACG codons in mammalian cells. Gene 91:173–178
27. Arai H, Miyamoto K, Taketani Y, Yamamoto H, Iemori Y, Morita K et al (1997) A vitamin D receptor gene polymorphism in the translation initiation codon: effect on protein activity and relation to bone mineral density in Japanese women. J Bone Miner Res 12:915–921
28. Montalbetti L, Ratti MT, Greco B, Aprile C, Moglia A, Soragna D (2005) Neuropsychological tests and functional nuclear neuroimaging provide evidence of subclinical impairment in Nasu-Hakola disease heterozygotes. Funct Neurol 20:71–75
29. Chouery E, Delague V, Bergougnoux A, Koussa S, Serre JL, Megarbane A (2008) Mutations in TREM2 lead to pure early-onset dementia without bone cysts. Hum Mutat 29:E194–E204
30. Verloes A, Maguet P, Sadzot B, Vivario M, Thiry A, Franck G (1997) Nasu-Hakola syndrome: polycystic lipomembranous osteodysplasia with sclerosing leucoencephalopathy and presenile dementia. J Med Genet 34:753–757
31. Paloneva J, Autti T, Raininko R, Partanen J, Salonen O, Puranen M, Hakola P, Haltia M (2001) CNS manifestations of Nasu-Hakola disease: a frontal dementia with bone cysts. Neurology 56:1552–1558
32. Bianchin MM, Capella HM, Chaves DL, Steindel M, Grisard EC, Ganev GG, da Silva Junior JP, Neto Evaldo S, Poffo MA, Walz R et al (2004) Nasu-Hakola disease (polycystic lipomembranous osteodysplasia with sclerosing leukoencephalopathy-PLOSL): a dementia associated with bone cystic lesions. From clinical to genetic and molecular aspects. Cell Mol Neurobiol 24:1–24
33. Satoh J, Tabunoki H, Ishida T, Yagishita S, Jinnai K, Futamura N, Kobayashi M, Toyoshima I, Yoshioka T, Enomoto K et al (2011) Immunohistochemical characterization of microglia in Nasu-Hakola disease brains. Neuropathology 31:363–375
34. Peri F, Nusslein-Volhard C (2008) Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133:916–927
35. Trapp BD, Wujek JR, Criste GA, Jalabi W, Yin X, Kidd GJ et al (2007) Evidence for synaptic stripping by cortical microglia. Glia 55(4):360–368. doi:10.1002/glia.20462
36. Aoki N, Tsuchiya K, Togo T, Kobayashi Z, Uchikado H, Katsuse O et al (2011) Gray matter lesions in Nasu-Hakola disease: a report on three autopsy cases. Neuropathology 31:135–143
37. Lue L-F, Schmitz C, Walker DG (2014) What happens to microglial TREM2 in Alzheimer’s disease: immunoregulatory turned into immunopathogenic? Neuroscience. doi:10.1016/j.neuroscience.2014.09.050
38. Guerreiro (2013) TREM2 variants in Alzheimer’s disease. N Engl J Med 368:117–127
39. Lue LF, Schmitz CT, Serrano G, Sue LI, Beach TG, Walker DG (2014) TREM2 protein expression changes correlate with Alzheimer’s disease neurodegenerative pathologies in post-mortem temporal cortices. Brain Pathol. doi:10.1111/bpa.12190
40. Neumann H, Daly MJ (2013) Variant TREM2 as risk factor for Alzheimer’s disease. N Eng J Med 368:182–183
41. Sierra A, Abiega O, Shahraz A, Neumann H (2013) Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6. doi:10.3389/fncel.2013.00006
42. Kaifu T, Nakahara J, Inui M, Mishima K, Momiyama T, Kaji M et al (2003) Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J Clin Invest 111:323–332
43. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR III, Lafaille JJ et al (2013) Microglia promote learning dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609
44. Kielar C, Wishart TM, Palmer A, Dihanich S, Wong AM, Macauley SL et al (2009) Molecular correlates of axonal and synaptic pathology in mouse models of Batten disease. Hum Mol Genet 18:4066–4408
45. Giuliano S, Agresta AM, De Palma A, Viglio S, Mauri P, Fumagalli M et al (2014) Proteomic analysis of lymphoblastoid cells from Nasu-Hakola patients: a step forward in our understanding of this neurodegenerative disorder. PLoS One 9, e11073
46. Chen S-K, Tvrdik P, Peden E, Cho S, Wu S, Spangrude MR (2010) Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 141:775–785
47. Naj AC, Jun G, Beecham GW, Wang LS, Vardarajan BN, Buros J et al (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer’s disease. Nat Genet 43:436–441