Structural insights into the Niemann-Pick C1 (NPC1)-mediated cholesterol transfer and ebola infection

Cell

Volumn 165, Issue 6, 2016, Pages 1467-1478

  Gong, Xin ^a,b   Qian, Hongwu ^a,b   Zhou, Xinhui ^a,b   Wu, Jianping ^a,b   Wan, Tao ^c   Cao, Pingping ^a,b   Huang, Weiyun ^a,b   Zhao, Xin ^a,b   Wang, Xudong ^c   Wang, Peiyi ^d   Shi, Yi ^c,e   Gao, George F ^c,e   Zhou, Qiang ^a,b   Yan, Nieng ^a,b  

^a TSINGHUA UNIVERSITY   (China)

^b Tsinghua University   (China)

^c INSTITUTE OF MICROBIOLOGY   (China)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; MEMBRANE PROTEIN; MONOMER; NIEMANN PICK C1 PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; CARRIER PROTEIN; ENVELOPE GLYCOPROTEIN, EBOLA VIRUS; GLYCOPROTEIN; NPC1 PROTEIN, HUMAN; NPC2 PROTEIN, HUMAN; VIRUS ENVELOPE PROTEIN;

ARTICLE; BIOCHEMICAL ANALYSIS; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; EBOLA HEMORRHAGIC FEVER; EBOLAVIRUS; HUMAN; LUMENAL DOMAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STEROL SENSING DOMAIN; AMINO ACID SEQUENCE; CHEMISTRY; METABOLISM; MOLECULAR MODEL; NIEMANN PICK DISEASE; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; VIROLOGY;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CHOLESTEROL; CRYOELECTRON MICROSCOPY; EBOLAVIRUS; GLYCOPROTEINS; HEMORRHAGIC FEVER, EBOLA; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; NIEMANN-PICK DISEASES; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL ENVELOPE PROTEINS;

EID: 84969961924     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.05.022     Document Type: Article

References (71)

1. S.W. Altmann, H.R. Davis Jr., L.J. Zhu, X. Yao, L.M. Hoos, G. Tetzloff, S.P.N. Iyer, M. Maguire, A. Golovko, M. Zeng, and et al. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption Science 303 2004 1201 1204
2. R. Burke, D. Nellen, M. Bellotto, E. Hafen, K.A. Senti, B.J. Dickson, and K. Basler Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells Cell 99 1999 803 815
3. J.E. Carette, M. Raaben, A.C. Wong, A.S. Herbert, G. Obernosterer, N. Mulherkar, A.I. Kuehne, P.J. Kranzusch, A.M. Griffin, G. Ruthel, and et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 Nature 477 2011 340 343
4. E.D. Carstea, J.A. Morris, K.G. Coleman, S.K. Loftus, D. Zhang, C. Cummings, J. Gu, M.A. Rosenfeld, W.J. Pavan, D.B. Krizman, and et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis Science 277 1997 228 231
5. K. Chandran, N.J. Sullivan, U. Felbor, S.P. Whelan, and J.M. Cunningham Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection Science 308 2005 1643 1645
6. S. Chen, G. McMullan, A.R. Faruqi, G.N. Murshudov, J.M. Short, S.H. Scheres, and R. Henderson High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy Ultramicroscopy 135 2013 24 35
7. M. Côté, J. Misasi, T. Ren, A. Bruchez, K. Lee, C.M. Filone, L. Hensley, Q. Li, D. Ory, K. Chandran, and J. Cunningham Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection Nature 477 2011 344 348
8. J.P. Davies, and Y.A. Ioannou Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein J. Biol. Chem. 275 2000 24367 24374
9. J.P. Davies, F.W. Chen, and Y.A. Ioannou Transmembrane molecular pump activity of Niemann-Pick C1 protein Science 290 2000 2295 2298
10. M.S. Deffieu, and S.R. Pfeffer Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding Proc. Natl. Acad. Sci. USA 108 2011 18932 18936
11. DeLano, W.L. (2002). The PyMOL Molecular Graphics System on World Wide Web http://www.pymol.org.
12. J.A. Delmar, C.C. Su, and E.W. Yu Bacterial multidrug efflux transporters Annu. Rev. Biophys. 43 2014 93 117
13. R. Doolman, G.S. Leichner, R. Avner, and J. Roitelman Ubiquitin is conjugated by membrane ubiquitin ligase to three sites, including the N terminus, in transmembrane region of mammalian 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for sterol-regulated enzyme degradation J. Biol. Chem. 279 2004 38184 38193
14. T. Eicher, M.A. Seeger, C. Anselmi, W. Zhou, L. Brandstätter, F. Verrey, K. Diederichs, J.D. Faraldo-Gómez, and K.M. Pos Coupling of remote alternating-access transport mechanisms for protons and substrates in the multidrug efflux pump AcrB eLife 3 2014 e03145
15. D. Elmlund, and H. Elmlund SIMPLE: Software for ab initio reconstruction of heterogeneous single-particles J. Struct. Biol. 180 2012 420 427
16. T. Grant, and N. Grigorieff Measuring the optimal exposure for single particle cryo-EM using a 2.6 Å reconstruction of rotavirus VP6 eLife 4 2015 e06980
17. H. Hofmann-Winkler, F. Kaup, and S. Pöhlmann Host cell factors in filovirus entry: novel players, new insights Viruses 4 2012 3336 3362
18. J.E. Hooper, and M.P. Scott The Drosophila patched gene encodes a putative membrane protein required for segmental patterning Cell 59 1989 751 765
19. X. Hua, A. Nohturfft, J.L. Goldstein, and M.S. Brown Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein Cell 87 1996 415 426
20. C.L. Hunt, N.J. Lennemann, and W. Maury Filovirus entry: a novelty in the viral fusion world Viruses 4 2012 258 275
21. R.E. Infante, M.L. Wang, A. Radhakrishnan, H.J. Kwon, M.S. Brown, and J.L. Goldstein NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes Proc. Natl. Acad. Sci. USA 105 2008 15287 15292
22. E.S. Istvan, M. Palnitkar, S.K. Buchanan, and J. Deisenhofer Crystal structure of the catalytic portion of human HMG-CoA reductase: insights into regulation of activity and catalysis EMBO J. 19 2000 819 830
23. A. Krishnan, E.H. Miller, A.S. Herbert, M. Ng, E. Ndungo, S.P. Whelan, J.M. Dye, and K. Chandran Niemann-Pick C1 (NPC1)/NPC1-like1 chimeras define sequences critical for NPC1's function as a flovirus entry receptor Viruses 4 2012 2471 2484
24. A. Kucukelbir, F.J. Sigworth, and H.D. Tagare Quantifying the local resolution of cryo-EM density maps Nat. Methods 11 2014 63 65
25. P.E. Kuwabara, and M. Labouesse The sterol-sensing domain: multiple families, a unique role? Trends Genet. 18 2002 193 201
26. H.J. Kwon, L. Abi-Mosleh, M.L. Wang, J. Deisenhofer, J.L. Goldstein, M.S. Brown, and R.E. Infante Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol Cell 137 2009 1213 1224
27. J.E. Lee, M.L. Fusco, A.J. Hessell, W.B. Oswald, D.R. Burton, and E.O. Saphire Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor Nature 454 2008 177 182
28. X. Li, P. Mooney, S. Zheng, C.R. Booth, M.B. Braunfeld, S. Gubbens, D.A. Agard, and Y. Cheng Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Nat. Methods 10 2013 584 590
29. J. Li, M.S. Deffieu, P.L. Lee, P. Saha, and S.R. Pfeffer Glycosylation inhibition reduces cholesterol accumulation in NPC1 protein-deficient cells Proc. Natl. Acad. Sci. USA 112 2015 14876 14881
30. S.K. Loftus, J.A. Morris, E.D. Carstea, J.Z. Gu, C. Cummings, A. Brown, J. Ellison, K. Ohno, M.A. Rosenfeld, D.A. Tagle, and et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene Science 277 1997 232 235
31. F. Long, C.C. Su, M.T. Zimmermann, S.E. Boyken, K.R. Rajashankar, R.L. Jernigan, and E.W. Yu Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport Nature 467 2010 484 488
32. G. Lu, Y. Hu, Q. Wang, J. Qi, F. Gao, Y. Li, Y. Zhang, W. Zhang, Y. Yuan, J. Bao, and et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26 Nature 500 2013 227 231
33. F. Lu, Q. Liang, L. Abi-Mosleh, A. Das, J.K. De Brabander, J.L. Goldstein, and M.S. Brown Identification of NPC1 as the target of U18666A, an inhibitor of lysosomal cholesterol export and Ebola infection eLife 4 2015 e12177
34. K.L. Luskey, and B. Stevens Human 3-hydroxy-3-methylglutaryl coenzyme A reductase. Conserved domains responsible for catalytic activity and sterol-regulated degradation J. Biol. Chem. 260 1985 10271 10277
35. K. Malathi, K. Higaki, A.H. Tinkelenberg, D.A. Balderes, D. Almanzar-Paramio, L.J. Wilcox, N. Erdeniz, F. Redican, M. Padamsee, Y. Liu, and et al. Mutagenesis of the putative sterol-sensing domain of yeast Niemann Pick C-related protein reveals a primordial role in subcellular sphingolipid distribution J. Cell Biol. 164 2004 547 556
36. V. Martín, G. Carrillo, C. Torroja, and I. Guerrero The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking Curr. Biol. 11 2001 601 607
37. E.E. Millard, S.E. Gale, N. Dudley, J. Zhang, J.E. Schaffer, and D.S. Ory The sterol-sensing domain of the Niemann-Pick C1 (NPC1) protein regulates trafficking of low density lipoprotein cholesterol J. Biol. Chem. 280 2005 28581 28590
38. G. Millat, C. Marçais, C. Tomasetto, K. Chikh, A.H. Fensom, K. Harzer, D.A. Wenger, K. Ohno, and M.T. Vanier Niemann-Pick C1 disease: correlations between NPC1 mutations, levels of NPC1 protein, and phenotypes emphasize the functional significance of the putative sterol-sensing domain and of the cysteine-rich luminal loop Am. J. Hum. Genet. 68 2001 1373 1385
39. E.H. Miller, G. Obernosterer, M. Raaben, A.S. Herbert, M.S. Deffieu, A. Krishnan, E. Ndungo, R.G. Sandesara, J.E. Carette, A.I. Kuehne, and et al. Ebola virus entry requires the host-programmed recognition of an intracellular receptor EMBO J. 31 2012 1947 1960
40. S. Murakami, R. Nakashima, E. Yamashita, and A. Yamaguchi Crystal structure of bacterial multidrug efflux transporter AcrB Nature 419 2002 587 593
41. Y. Nakano, I. Guerrero, A. Hidalgo, A. Taylor, J.R.S. Whittle, and P.W. Ingham A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched Nature 341 1989 508 513
42. S. Naureckiene, D.E. Sleat, H. Lackland, A. Fensom, M.T. Vanier, R. Wattiaux, M. Jadot, and P. Lobel Identification of HE1 as the second gene of Niemann-Pick C disease Science 290 2000 2298 2301
43. W.F. Neiss A coat of glycoconjugates on the inner surface of the lysosomal membrane in the rat kidney Histochemistry 80 1984 603 608
44. A. Nohturfft, M.S. Brown, and J.L. Goldstein Sterols regulate processing of carbohydrate chains of wild-type SREBP cleavage-activating protein (SCAP), but not sterol-resistant mutants Y298C or D443N Proc. Natl. Acad. Sci. USA 95 1998 12848 12853
45. N. Ohgami, D.C. Ko, M. Thomas, M.P. Scott, C.C.Y. Chang, and T.Y. Chang Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain Proc. Natl. Acad. Sci. USA 101 2004 12473 12478
46. J.E. Pak, E.N. Ekendé, E.G. Kifle, J.D. O'Connell 3rd, F. De Angelis, M.B. Tessema, K.M. Derfoufi, Y. Robles-Colmenares, R.A. Robbins, E. Goormaghtigh, and et al. Structures of intermediate transport states of ZneA, a Zn(II)/proton antiporter Proc. Natl. Acad. Sci. USA 110 2013 18484 18489
47. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
48. A. Radhakrishnan, L.P. Sun, H.J. Kwon, M.S. Brown, and J.L. Goldstein Direct binding of cholesterol to the purified membrane region of SCAP: mechanism for a sterol-sensing domain Mol. Cell 15 2004 259 268
49. S.H. Scheres A Bayesian view on cryo-EM structure determination J. Mol. Biol. 415 2012 406 418
50. S.H. Scheres RELION: implementation of a Bayesian approach to cryo-EM structure determination J. Struct. Biol. 180 2012 519 530
51. S.H. Scheres Semi-automated selection of cryo-EM particles in RELION-1.3 J. Struct. Biol. 189 2015 114 122
52. S.H. Scheres, and S. Chen Prevention of overfitting in cryo-EM structure determination Nat. Methods 9 2012 853 854
53. K. Schornberg, S. Matsuyama, K. Kabsch, S. Delos, A. Bouton, and J. White Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein J. Virol. 80 2006 4174 4178
54. C. Scott, and Y.A. Ioannou The NPC1 protein: structure implies function Biochim Biophys Acta. 1685 2004 8 13
55. G. Sennhauser, M.A. Bukowska, C. Briand, and M.G. Grütter Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa J. Mol. Biol. 389 2009 134 145
56. D.E. Sleat, J.A. Wiseman, M. El-Banna, S.M. Price, L. Verot, M.M. Shen, G.S. Tint, M.T. Vanier, S.U. Walkley, and P. Lobel Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport Proc. Natl. Acad. Sci. USA 101 2004 5886 5891
57. H. Strutt, C. Thomas, Y. Nakano, D. Stark, B. Neave, A.M. Taylor, and P.W. Ingham Mutations in the sterol-sensing domain of Patched suggest a role for vesicular trafficking in Smoothened regulation Curr. Biol. 11 2001 608 613
58. J. Taipale, M.K. Cooper, T. Maiti, and P.A. Beachy Patched acts catalytically to suppress the activity of Smoothened Nature 418 2002 892 897
59. T.T. Tseng, K.S. Gratwick, J. Kollman, D. Park, D.H. Nies, A. Goffeau, and M.H. Saier Jr. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins J. Mol. Microbiol. Biotechnol. 1 1999 107 125
60. M.T. Vanier Niemann-Pick disease type C Orphanet J. Rare Dis. 5 2010 16
61. M.T. Vanier Complex lipid trafficking in Niemann-Pick disease type C J. Inherit. Metab. Dis. 38 2015 187 199
62. M.T. Vanier, and G. Millat Niemann-Pick disease type C Clin. Genet. 64 2003 269 281
63. H. Venter, R. Mowla, T. Ohene-Agyei, and S. Ma RND-type drug efflux pumps from Gram-negative bacteria: molecular mechanism and inhibition Front Microbiol 6 2015 377
64. M.L. Wang, M. Motamed, R.E. Infante, L. Abi-Mosleh, H.J. Kwon, M.S. Brown, and J.L. Goldstein Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes Cell Metab. 12 2010 166 173
65. H. Wang, J. Qi, N. Liu, Y. Li, J. Gao, T. Zhang, Y. Chai, F. Gao, H. Zhang, X. Li, and et al. Crystal structures of human TIM members: Ebolavirus entry-enhancing receptors Chin. Sci. Bull. 60 2015 3438 3453
66. H. Wang, Y. Shi, J. Song, J. Qi, G. Lu, J. Yan, and G.F. Gao Ebola viral glycoprotein bound to its endosomal receptor Niemann-Pick C1 Cell 164 2016 258 268
67. J.M. White, and K.L. Schornberg A new player in the puzzle of filovirus entry Nat. Rev. Microbiol. 10 2012 317 322
68. D. Yabe, Z.P. Xia, C.M. Adams, and R.B. Rawson Three mutations in sterol-sensing domain of SCAP block interaction with insig and render SREBP cleavage insensitive to sterols Proc. Natl. Acad. Sci. USA 99 2002 16672 16677
69. A. Yamaguchi, R. Nakashima, and K. Sakurai Structural basis of RND-type multidrug exporters Front Microbiol 6 2015 327
70. K. Zhang Gctf: Real-time CTF determination and correction J. Struct. Biol. 193 2016 1 12
71. Y. Zhao, J. Ren, K. Harlos, and D.I. Stuart Structure of glycosylated NPC1 luminal domain C reveals insights into NPC2 and Ebola virus interactions FEBS Lett. 590 2016 605 612