TREM2 Maintains Microglial Metabolic Fitness in Alzheimer's Disease

Cell

Volumn 170, Issue 4, 2017, Pages 649-663.e13

  Ulland, Tyler K ^a   Song, Wilbur M ^a   Huang, Stanley Ching Cheng ^a   Ulrich, Jason D ^a   Sergushichev, Alexey ^b   Beatty, Wandy L ^a   Loboda, Alexander A ^b   Zhou, Yingyue ^a   Cairns, Nigel J ^a   Kambal, Amal ^a   Loginicheva, Ekaterina ^a   Gilfillan, Susan ^a   Cella, Marina ^a   Virgin, Herbert W ^a   Unanue, Emil R ^a   Wang, Yaming ^a   Artyomov, Maxim N ^a   Holtzman, David M ^a   Colonna, Marco ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ITMO UNIVERSITY   (Russian Federation)

Author keywords

Alzheimer's disease; immunity; metabolism; microglia; TREM2

Indexed keywords

DECTIN 1; MAMMALIAN TARGET OF RAPAMYCIN; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; CREATININE; CYCLOCREATINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN RECEPTOR; LECTIN; MEMBRANE PROTEIN; TARGET OF RAPAMYCIN KINASE; TREM2 PROTEIN, HUMAN; TREM2 PROTEIN, MOUSE;

ADULT; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL METABOLISM; CELL VACUOLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENERGY METABOLISM; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MALE; METABOLOMICS; MICROGLIA; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SIGNAL TRANSDUCTION; AMYLOID PLAQUE; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; NEURITE; PATHOLOGY;

ALZHEIMER DISEASE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CREATININE; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HUMANS; LECTINS, C-TYPE; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICROGLIA; NEURITES; PLAQUE, AMYLOID; RECEPTORS, IMMUNOLOGIC; TOR SERINE-THREONINE KINASES;

EID: 85027528978     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.07.023     Document Type: Article

References (55)

1. Ara, G., Gravelin, L.M., Kaddurah-Daouk, R., Teicher, B.A., Antitumor activity of creatine analogs produced by alterations in pancreatic hormones and glucose metabolism. In Vivo 12 (1998), 223–231.
2. Arase, H., Mocarski, E.S., Campbell, A.E., Hill, A.B., Lanier, L.L., Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296 (2002), 1323–1326.
3. Atagi, Y., Liu, C.C., Painter, M.M., Chen, X.F., Verbeeck, C., Zheng, H., Li, X., Rademakers, R., Kang, S.S., Xu, H., et al. Apolipoprotein E is a ligand for triggering receptor expressed on myeloid cells 2 (TREM2). J. Biol. Chem. 290 (2015), 26043–26050.
4. 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.
5. Cho, M.H., Cho, K., Kang, H.J., Jeon, E.Y., Kim, H.S., Kwon, H.J., Kim, H.M., Kim, D.H., Yoon, S.Y., Autophagy in microglia degrades extracellular β-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy 10 (2014), 1761–1775.
6. Dambuza, I.M., Brown, G.D., C-type lectins in immunity: recent developments. Curr. Opin. Immunol. 32 (2015), 21–27.
7. Ford, J.W., McVicar, D.W., TREM and TREM-like receptors in inflammation and disease. Curr. Opin. Immunol. 21 (2009), 38–46.
8. Freeman, L.C., Ting, J.P., The pathogenic role of the inflammasome in neurodegenerative diseases. J. Neurochem. 136:Suppl 1 (2016), 29–38.
9. Galluzzi, L., Pietrocola, F., Levine, B., Kroemer, G., Metabolic control of autophagy. Cell 159 (2014), 1263–1276.
10. Gold, M., El Khoury, J., β-amyloid, microglia, and the inflammasome in Alzheimer's disease. Semin. Immunopathol. 37 (2015), 607–611.
11. Guerreiro, R., Hardy, J., Genetics of Alzheimer's disease. Neurotherapeutics 11 (2014), 732–737.
12. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., Mizushima, N., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889.
13. Hedrick, S.M., Matis, L.A., Hecht, T.T., Samelson, L.E., Longo, D.L., Heber-Katz, E., Schwartz, R.H., The fine specificity of antigen and Ia determinant recognition by T cell hybridoma clones specific for pigeon cytochrome c. Cell 30 (1982), 141–152.
14. Heneka, M.T., Kummer, M.P., Stutz, A., Delekate, A., Schwartz, S., Vieira-Saecker, A., Griep, A., Axt, D., Remus, A., Tzeng, T.C., et al. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493 (2013), 674–678.
15. Heneka, M.T., Golenbock, D.T., Latz, E., Innate immunity in Alzheimer's disease. Nat. Immunol. 16 (2015), 229–236.
16. Holtzman, D.M., Morris, J.C., Goate, A.M., Alzheimer's disease: the challenge of the second century. Sci. Transl. Med., 3, 2011, 77sr1.
17. Hong, S., Beja-Glasser, V.F., Nfonoyim, B.M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K.M., Shi, Q., Rosenthal, A., Barres, B.A., et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science 352 (2016), 712–716.
18. Huang, Y., Mucke, L., Alzheimer mechanisms and therapeutic strategies. Cell 148 (2012), 1204–1222.
19. Jay, T.R., Hirsch, A.M., Broihier, M.L., Miller, C.M., Neilson, L.E., Ransohoff, R.M., Lamb, B.T., Landreth, G.E., Disease progression-dependent effects of TREM2 deficiency in a mouse model of Alzheimer's disease. J. Neurosci. 37 (2017), 637–647.
20. Kim, J., Kundu, M., Viollet, B., Guan, K.L., AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13 (2011), 132–141.
21. Klionsky, D.J., Abdelmohsen, K., Abe, A., Abedin, M.J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C.M., Adams, P.D., Adeli, K., et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12 (2016), 1–222.
22. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., Tanaka, K., Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006), 880–884.
23. Kroemer, G., Mariño, G., Levine, B., Autophagy and the integrated stress response. Mol. Cell 40 (2010), 280–293.
24. Kuiper, J.W., Pluk, H., Oerlemans, F., van Leeuwen, F.N., de Lange, F., Fransen, J., Wieringa, B., Creatine kinase-mediated ATP supply fuels actin-based events in phagocytosis. PLoS Biol., 6, 2008, e51.
25. Kurosawa, Y., Degrauw, T.J., Lindquist, D.M., Blanco, V.M., Pyne-Geithman, G.J., Daikoku, T., Chambers, J.B., Benoit, S.C., Clark, J.F., Cyclocreatine treatment improves cognition in mice with creatine transporter deficiency. J. Clin. Invest. 122 (2012), 2837–2846.
26. Laplante, M., Sabatini, D.M., mTOR signaling in growth control and disease. Cell 149 (2012), 274–293.
27. Lucin, K.M., O'Brien, C.E., Bieri, G., Czirr, E., Mosher, K.I., Abbey, R.J., Mastroeni, D.F., Rogers, J., Spencer, B., Masliah, E., Wyss-Coray, T., Microglial beclin 1 regulates retromer trafficking and phagocytosis and is impaired in Alzheimer's disease. Neuron 79 (2013), 873–886.
28. Masliah, E., Sisk, A., Mallory, M., Mucke, L., Schenk, D., Games, D., Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer's disease. J. Neurosci. 16 (1996), 5795–5811.
29. McLaughlin, A.C., Cohn, M., Kenyon, G.L., Specificity of creatine kinase for guanidino substrates. Kinetic and proton nuclear magnetic relaxation rate studies. J. Biol. Chem. 247 (1972), 4382–4388.
30. Meyer-Luehmann, M., Prinz, M., Myeloid cells in Alzheimer's disease: culprits, victims or innocent bystanders?. Trends Neurosci. 38 (2015), 659–668.
31. Netea-Maier, R.T., Plantinga, T.S., van de Veerdonk, F.L., Smit, J.W., Netea, M.G., Modulation of inflammation by autophagy: Consequences for human disease. Autophagy 12 (2016), 245–260.
32. Neumann, H., Takahashi, K., Essential role of the microglial triggering receptor expressed on myeloid cells-2 (TREM2) for central nervous tissue immune homeostasis. J. Neuroimmunol. 184 (2007), 92–99.
33. O'Neill, L.A., Pearce, E.J., Immunometabolism governs dendritic cell and macrophage function. J. Exp. Med. 213 (2016), 15–23.
34. Oakley, H., Cole, S.L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26 (2006), 10129–10140.
35. Orre, M., Kamphuis, W., Osborn, L.M., Jansen, A.H., Kooijman, L., Bossers, K., Hol, E.M., Isolation of glia from Alzheimer's mice reveals inflammation and dysfunction. Neurobiol. Aging 35 (2014), 2746–2760.
36. Peng, Q., Malhotra, S., Torchia, J.A., Kerr, W.G., Coggeshall, K.M., Humphrey, M.B., TREM2- and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci. Signal., 3, 2010, ra38.
37. Perry, V.H., Holmes, C., Microglial priming in neurodegenerative disease. Nat. Rev. Neurol. 10 (2014), 217–224.
38. Saxton, R.A., Sabatini, D.M., mTOR signaling in growth, metabolism, and disease. Cell 168 (2017), 960–976.
39. Sergushichev, A.A., Loboda, A.A., Jha, A.K., Vincent, E.E., Driggers, E.M., Jones, R.G., Pearce, E.J., Artyomov, M.N., GAM: a web-service for integrated transcriptional and metabolic network analysis. Nucleic Acids Res. 44:W1 (2016), W194–W200.
40. Shibuya, Y., Chang, C.C., Huang, L.H., Bryleva, E.Y., Chang, T.Y., Inhibiting ACAT1/SOAT1 in microglia stimulates autophagy-mediated lysosomal proteolysis and increases Aβ1-42 clearance. J. Neurosci. 34 (2014), 14484–14501.
41. Snow, R.J., Murphy, R.M., Creatine and the creatine transporter: a review. Mol. Cell. Biochem. 224 (2001), 169–181.
42. Tanzi, R.E., The genetics of Alzheimer disease. Cold Spring Harb. Perspect. Med., 2012, 10.1101/cshperspect.a006296 Published online July 14, 2017.
43. Tejera, D., Heneka, M.T., Microglia in Alzheimer's disease: the good, the bad and the ugly. Curr. Alzheimer Res. 13 (2016), 370–380.
44. Turnbull, I.R., Gilfillan, S., Cella, M., Aoshi, T., Miller, M., Piccio, L., Hernandez, M., Colonna, M., Cutting edge: TREM-2 attenuates macrophage activation. J. Immunol. 177 (2006), 3520–3524.
45. Ulrich, J.D., Finn, M.B., Wang, Y., Shen, A., Mahan, T.E., Jiang, H., Stewart, F.R., Piccio, L., Colonna, M., Holtzman, D.M., Altered microglial response to Aβ plaques in APPPS1-21 mice heterozygous for TREM2. Mol. Neurodegener., 9, 2014, 20.
46. Vincent, E.E., Sergushichev, A., Griss, T., Gingras, M.C., Samborska, B., Ntimbane, T., Coelho, P.P., Blagih, J., Raissi, T.C., Choinière, L., et al. Mitochondrial phosphoenolpyruvate carboxykinase regulates metabolic adaptation and enables glucose-independent tumor growth. Mol. Cell 60 (2015), 195–207.
47. Walker, J.B., Creatine: biosynthesis, regulation, and function. Adv. Enzymol. Relat. Areas Mol. Biol. 50 (1979), 177–242.
48. Wang, Y., Cella, M., Mallinson, K., Ulrich, J.D., Young, K.L., Robinette, M.L., Gilfillan, S., Krishnan, G.M., Sudhakar, S., Zinselmeyer, B.H., et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model. Cell 160 (2015), 1061–1071.
49. Wang, Y., Ulland, T.K., Ulrich, J.D., Song, W., Tzaferis, J.A., Hole, J.T., Yuan, P., Mahan, T.E., Shi, Y., Gilfillan, S., et al. TREM2-mediated early microglial response limits diffusion and toxicity of amyloid plaques. J. Exp. Med. 213 (2016), 667–675.
50. Werner, M., Hobeika, E., Jumaa, H., Role of PI3K in the generation and survival of B cells. Immunol. Rev. 237 (2010), 55–71.
51. Woznicki, D.T., Walker, J.B., Formation of a supplemental long time-constant reservoir of high energy phosphate by brain in vivo and in vitro and its reversible depletion by potassium depolarization. J. Neurochem. 33 (1979), 75–80.
52. Wyss, M., Kaddurah-Daouk, R., Creatine and creatinine metabolism. Physiol. Rev. 80 (2000), 1107–1213.
53. Yang, D.S., Stavrides, P., Mohan, P.S., Kaushik, S., Kumar, A., Ohno, M., Schmidt, S.D., Wesson, D., Bandyopadhyay, U., Jiang, Y., et al. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134 (2011), 258–277.
54. Yeh, F.L., Wang, Y., Tom, I., Gonzalez, L.C., Sheng, M., TREM2 binds to apolipoproteins, including APOE and CLU/APOJ, and thereby facilitates uptake of amyloid-beta by microglia. Neuron 91 (2016), 328–340.
55. Yuan, P., Condello, C., Keene, C.D., Wang, Y., Bird, T.D., Paul, S.M., Luo, W., Colonna, M., Baddeley, D., Grutzendler, J., TREM2 haplodeficiency in mice and humans impairs the microglia barrier function leading to decreased amyloid compaction and severe axonal dystrophy. Neuron 90 (2016), 724–739.