Preparation, crystallization, and preliminary crystallographic analysis of wild-type and mutant human TREM-2 ectodomains linked to neurodegenerative and inflammatory diseases

Protein Expression and Purification

Volumn 96, Issue , 2014, Pages 32-38

  Kober, Daniel L ^a   Wanhainen, Kelsey M ^a   Johnson, Britney M ^a   Randolph, David T ^a   Holtzman, Michael J ^a   Brett, Tom J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Crystallography; Inflammation; Innate immunity; Neurodegenerative disease; Parkinson's disease; Receptor

Indexed keywords

IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; TREM2 PROTEIN, HUMAN;

BIOSYNTHESIS; DEGENERATIVE DISEASE; GENE EXPRESSION; GENETICS; HUMAN; INFLAMMATION; MOLECULAR CLONING; MUTATION; PATHOLOGY; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION; HUMANS; INFLAMMATION; MEMBRANE GLYCOPROTEINS; MUTATION; NEURODEGENERATIVE DISEASES; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, IMMUNOLOGIC;

EID: 84894241018     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2014.01.015     Document Type: Article

References (45)

1. R. Guerreiro, A. Wojtas, J. Bras, M. Carrasquillo, E. Rogaeva, E. Majounie, C. Cruchaga, C. Sassi, J.S. Kauwe, S. Younkin, L. Hazrati, J. Collinge, J. Pocock, T. Lashley, J. Williams, J.C. Lambert, P. Amouyel, A. Goate, R. Rademakers, K. Morgan, J. Powell, P. St George-Hyslop, A. Singleton, and J. Hardy TREM2 variants in Alzheimer's disease N. Engl. J. Med. 368 2013 117 127
2. T. Jonsson, H. Stefansson, S. Steinberg, I. Jonsdottir, P.V. Jonsson, J. Snaedal, S. Bjornsson, J. Huttenlocher, A.I. Levey, J.J. Lah, D. Rujescu, H. Hampel, I. Giegling, O.A. Andreassen, K. Engedal, I. Ulstein, S. Djurovic, C. Ibrahim-Verbaas, A. Hofman, M.A. Ikram, C.M. van Duijn, U. Thorsteinsdottir, A. Kong, and K. Stefansson Variant of TREM2 associated with the risk of Alzheimer's disease N. Engl. J. Med. 368 2013 107 116
3. A.M. Saunders, W.J. Strittmatter, D. Schmechel, P.H. George-Hyslop, M.A. Pericak-Vance, S.H. Joo, B.L. Rosi, J.F. Gusella, D.R. Crapper-MacLachlan, and M.J. Alberts et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease Neurology 43 1993 1467 1472 (Pubitemid 23230526)
4. B.A. Benitez, B. Cooper, P. Pastor, S.C. Jin, E. Lorenzo, S. Cervantes, and C. Cruchaga TREM2 is associated with the risk of Alzheimer's disease in Spanish population Neurobiol. Aging 34 1711 2013 e1715 e1717
5. C. Pottier, D. Wallon, S. Rousseau, A. Rovelet-Lecrux, A.C. Richard, A. Rollin-Sillaire, T. Frebourg, D. Campion, and D. Hannequin TREM2 R47H variant as a risk factor for early-onset Alzheimer's disease J. Alzheimers Dis. 35 2013 45 49
6. B.A. Benitez, and C. Cruchaga TREM2 and neurodegenerative disease N. Engl. J. Med. 369 2013 1567 1568
7. S. Rayaprolu, B. Mullen, M. Baker, T. Lynch, E. Finger, W.W. Seeley, K.J. Hatanpaa, C. Lomen-Hoerth, A. Kertesz, E.H. Bigio, C. Lippa, K.A. Josephs, D.S. Knopman, C.L. White 3rd, R. Caselli, I.R. Mackenzie, B.L. Miller, M. Boczarska-Jedynak, G. Opala, A. Krygowska-Wajs, M. Barcikowska, S.G. Younkin, R.C. Petersen, N. Ertekin-Taner, R.J. Uitti, J.F. Meschia, K.B. Boylan, B.F. Boeve, N.R. Graff-Radford, Z.K. Wszolek, D.W. Dickson, R. Rademakers, and O.A. Ross TREM2 in neurodegeneration: evidence for association of the p. R47H variant with frontotemporal dementia and Parkinson's disease Mol. Neurodegener. 8 2013 19
8. R.J. Guerreiro, E. Lohmann, J.M. Bras, J.R. Gibbs, J.D. Rohrer, N. Gurunlian, B. Dursun, B. Bilgic, H. Hanagasi, H. Gurvit, M. Emre, A. Singleton, and J. Hardy Using exome sequencing to reveal mutations in TREM2 presenting as a frontotemporal dementia-like syndrome without bone involvement JAMA. Neurol. 70 2013 78 84
9. R. Guerreiro, B. Bilgic, G. Guven, J. Bras, J. Rohrer, E. Lohmann, H. Hanagasi, H. Gurvit, and M. Emre A novel compound heterozygous mutation in TREM2 found in a Turkish frontotemporal dementia-like family Neurobiol. Aging 34 2890 2013 e2891 2895
10. B. Borroni, F. Ferrari, D. Galimberti, B. Nacmias, C. Barone, S. Bagnoli, C. Fenoglio, I. Piaceri, S. Archetti, C. Bonvicini, M. Gennarelli, M. Turla, E. Scarpini, S. Sorbi, and A. Padovani Heterozygous TREM2 mutations in frontotemporal dementia Neurobiol. Aging 2013
11. E. Cuyvers, K. Bettens, S. Philtjens, T. Van Langenhove, I. Gijselinck, J. van der Zee, S. Engelborghs, M. Vandenbulcke, J. Van Dongen, N. Geerts, G. Maes, M. Mattheijssens, K. Peeters, P. Cras, R. Vandenberghe, P.P. De Deyn, C. Van Broeckhoven, M. Cruts, and K. Sleegers Investigating the role of rare heterozygous TREM2 variants in Alzheimer's disease and frontotemporal dementia Neurobiol. Aging 35 726 2014 e711 e729
12. T.E. Golde, W.J. Streit, and P. Chakrabarty Alzheimer's disease risk alleles in TREM2 illuminate innate immunity in Alzheimer's disease Alzheimers Res. Ther. 5 2013 24
13. J.W. Ford, and D.W. McVicar TREM and TREM-like receptors in inflammation and disease Curr. Opin. Immunol. 21 2009 38 46
14. A. Bouchon, C. Hernandez-Munain, M. Cella, and M. Colonna A DAP12-mediated pathway regulates expression of CC chemokine receptor 7 and maturation of human dendritic cells J. Exp. Med. 194 2001 1111 1122 (Pubitemid 32995781)
15. E.N. N'Diaye, C.S. Branda, S.S. Branda, L. Nevarez, M. Colonna, C. Lowell, J.A. Hamerman, and W.E. Seaman TREM-2 (triggering receptor expressed on myeloid cells 2) is a phagocytic receptor for bacteria J. Cell. Biol. 184 2009 215 223
16. C.L. Hsieh, M. Koike, S.C. Spusta, E.C. Niemi, M. Yenari, M.C. Nakamura, and W.E. Seaman A role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia J. Neurochem. 109 2009 1144 1156
17. N. Takegahara, H. Takamatsu, T. Toyofuku, T. Tsujimura, T. Okuno, K. Yukawa, M. Mizui, M. Yamamoto, D.V. Prasad, K. Suzuki, M. Ishii, K. Terai, M. Moriya, Y. Nakatsuji, S. Sakoda, S. Sato, S. Akira, K. Takeda, M. Inui, T. Takai, M. Ikawa, M. Okabe, A. Kumanogoh, and H. Kikutani Plexin-A1 and its interaction with DAP12 in immune responses and bone homeostasis Nat. Cell Biol. 8 2006 615 622 (Pubitemid 43827355)
18. L. Stefano, G. Racchetti, F. Bianco, N. Passini, R.S. Gupta, P. Panina Bordignon, and J. Meldolesi The surface-exposed chaperone, Hsp60, is an agonist of the microglial TREM2 receptor J. Neurochem. 110 2009 284 294
19. J. Paloneva, T. Manninen, G. Christman, K. Hovanes, J. Mandelin, R. Adolfsson, M. Bianchin, T. Bird, R. Miranda, A. Salmaggi, L. Tranebjaerg, Y. Konttinen, and L. Peltonen Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype Am. J. Hum. Genet. 71 2002 656 662 (Pubitemid 34970138)
20. A.R. Aricescu, W. Lu, and E.Y. Jones A time- and cost-efficient system for high-level protein production in mammalian cells Acta Crystallogr. D Biol. Crystallogr. 62 2006 1243 1250 (Pubitemid 44526216)
21. M.S. Kelker, E.W. Debler, and I.A. Wilson Crystal structure of mouse triggering receptor expressed on myeloid cells 1 (TREM-1) at 1.76 A J. Mol. Biol. 344 2004 1175 1181 (Pubitemid 39550471)
22. M.S. Kelker, T.R. Foss, W. Peti, L. Teyton, J.W. Kelly, K. Wuthrich, and I.A. Wilson Crystal structure of human triggering receptor expressed on myeloid cells 1 (TREM-1) at 1.47 A J. Mol. Biol. 342 2004 1237 1248 (Pubitemid 39207900)
23. S. Radaev, M. Kattah, B. Rostro, M. Colonna, and P.D. Sun Crystal structure of the human myeloid cell activating receptor TREM-1 Structure 11 2003 1527 1535 (Pubitemid 37510352)
24. J.L. Gattis, A.V. Washington, M.M. Chisholm, L. Quigley, A. Szyk, D.W. McVicar, and J. Lubkowski The structure of the extracellular domain of triggering receptor expressed on myeloid cells like transcript-1 and evidence for a naturally occurring soluble fragment J. Biol. Chem. 281 2006 13396 13403 (Pubitemid 43855251)
25. J.A. Marquez, E. Galfre, F. Dupeux, D. Flot, O. Moran, and N. Dimasi The crystal structure of the extracellular domain of the inhibitor receptor expressed on myeloid cells IREM-1 J. Mol. Biol. 367 2007 310 318
26. C. Cantoni, M. Ponassi, R. Biassoni, R. Conte, A. Spallarossa, A. Moretta, L. Moretta, M. Bolognesi, and D. Bordo The three-dimensional structure of the human NK cell receptor NKp44, a triggering partner in natural cytotoxicity Structure 11 2003 725 734 (Pubitemid 37281187)
27. C. Yang, W. Cheng, P.Y. Teo, A.C. Engler, D.J. Coady, J.L. Hedrick, and Y.Y. Yang Mitigated cytotoxicity and tremendously enhanced gene transfection efficiency of PEI through facile one-step carbamate modification Adv. Healthcare Mater. 2 2013 1304 1308
28. V.T. Chang, M. Crispin, A.R. Aricescu, D.J. Harvey, J.E. Nettleship, J.A. Fennelly, C. Yu, K.S. Boles, E.J. Evans, D.I. Stuart, R.A. Dwek, E.Y. Jones, R.J. Owens, and S.J. Davis Glycoprotein structural genomics: solving the glycosylation problem Structure 15 2007 267 273 (Pubitemid 46366717)
29. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326 (Pubitemid 27085611)
30. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
31. L. Tong, and M.G. Rossmann Rotation function calculations with GLRF program Methods Enzymol. 276 1997 594 611 (Pubitemid 27085625)
32. Z. Yurtsever, M. Sala-Rabanal, D.T. Randolph, S.M. Scheaffer, W.T. Roswit, Y.G. Alevy, A.C. Patel, R.F. Heier, A.G. Romero, C.G. Nichols, M.J. Holtzman, and T.J. Brett Self-cleavage of human CLCA1 protein by a novel internal metalloprotease domain controls calcium-activated chloride channel activation J. Biol. Chem. 287 2012 42138 42149
33. M.R. Sawaya Characterizing a crystal from an initial native dataset Methods Mol. Biol. 364 2007 95 120 (Pubitemid 350183133)
34. A. Paradowska-Gorycka, and M. Jurkowska Structure, expression pattern and biological activity of molecular complex TREM-2/DAP12 Hum. Immunol. 74 2013 730 737
35. L. Piccio, C. Buonsanti, M. Cella, I. Tassi, R.E. Schmidt, C. Fenoglio, J. Rinker 2nd, R.T. Naismith, P. Panina-Bordignon, N. Passini, D. Galimberti, E. Scarpini, M. Colonna, and A.H. Cross Identification of soluble TREM-2 in the cerebrospinal fluid and its association with multiple sclerosis and CNS inflammation Brain 131 2008 3081 3091
36. K. Takahashi, M. Prinz, M. Stagi, O. Chechneva, and H. Neumann TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis PLoS Med. 4 2007 e124
37. M.W. Sieber, N. Jaenisch, M. Brehm, M. Guenther, B. Linnartz-Gerlach, H. Neumann, O.W. Witte, and C. Frahm Attenuated inflammatory response in triggering receptor expressed on myeloid cells 2 (TREM2) knock-out mice following stroke PLoS One 8 2013 e52982
38. C. Correale, M. Genua, S. Vetrano, E. Mazzini, C. Martinoli, A. Spinelli, V. Arena, L. Peyrin-Biroulet, F. Caprioli, N. Passini, P. Panina-Bordignon, A. Repici, A. Malesci, S. Rutella, M. Rescigno, and S. Danese Bacterial sensor triggering receptor expressed on myeloid cells-2 regulates the mucosal inflammatory response Gastroenterology 144 2013 346 356.e3
39. S. Poliska, E. Csanky, A. Szanto, I. Szatmari, B. Mesko, L. Szeles, B. Dezso, B. Scholtz, J. Podani, I. Kilty, L. Takacs, and L. Nagy Chronic obstructive pulmonary disease-specific gene expression signatures of alveolar macrophages as well as peripheral blood monocytes overlap and correlate with lung function Respiration 81 2011 499 510
40. B. Heras, M.A. Edeling, K.A. Byriel, A. Jones, S. Raina, and J.L. Martin Dehydration converts DsbG crystal diffraction from low to high resolution Structure 11 2003 139 145 (Pubitemid 36183640)
41. B. Heras, and J.L. Martin Post-crystallization treatments for improving diffraction quality of protein crystals Acta Crystallogr. D Biol. Crystallogr. 61 2005 1173 1180 (Pubitemid 43961288)
42. C. Abergel Spectacular improvement of X-ray diffraction through fast desiccation of protein crystals Acta Crystallogr. D Biol. Crystallogr. 60 2004 1413 1416 (Pubitemid 41079738)
43. J.M. Harp, B.L. Hanson, D.E. Timm, and G.J. Bunick Macromolecular crystal annealing: evaluation of techniques and variables Acta Crystallogr. D Biol. Crystallogr. 55 1999 1329 1334 (Pubitemid 29350734)
44. J.M. Harp, D.E. Timm, and G.J. Bunick Macromolecular crystal annealing: overcoming increased mosaicity associated with cryocrystallography Acta Crystallogr. D Biol. Crystallogr. 54 1998 622 628 (Pubitemid 28343805)
45. J.I. Yeh, and W.G. Hol A flash-annealing technique to improve diffraction limits and lower mosaicity in crystals of glycerol kinase Acta Crystallogr. D Biol. Crystallogr. 54 1998 479 480 (Pubitemid 28235875)