Home LiteratureArticle Details
PMID: 26623517 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Sampling the conformational space of the catalytic subunit of human γ-secretase.

eLife ·Vol. 4 ·2015-12-01

Bai XC, Rajendra E, Yang G, Shi Y, Scheres SH

Abstract

Human γ-secretase is an intra-membrane protease that cleaves many different substrates. Aberrant cleavage of Notch is implicated in cancer, while abnormalities in cutting amyloid precursor protein lead to Alzheimer's disease. Our previous cryo-EM structure of γ-secretase revealed considerable disorder in its catalytic subunit presenilin. Here, we describe an image classification procedure that characterizes molecular plasticity at the secondary structure level, and apply this method to identify three distinct conformations in our previous sample. In one of these conformations, an additional transmembrane helix is visible that cannot be attributed to the known components of γ-secretase. In addition, we present a γ-secretase structure in complex with the dipeptidic inhibitor N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester (DAPT). Our results reveal how conformational mobility in the second and sixth transmembrane helices of presenilin is greatly reduced upon binding of DAPT or the additional helix, and form the basis for a new model of how substrate enters the transmembrane domain.

Keywords
biophysics electron microscopy gamma-secretase human image analysis structural biology
MeSH Terms
Dipeptides/metabolism Humans Image Processing, Computer-Assisted Models, Molecular Presenilins/chemistry,metabolism Protein Structure, Secondary
Chemicals
Dipeptides N-(N-(3,5-difluorophenacetyl)alanyl)phenylglycine tert-butyl ester Presenilins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bai Xiao-chen
MRC Laboratory of Molecular Biology, Cambridge, United Kingdom.
Rajendra Eeson
MRC Laboratory of Molecular Biology, Cambridge, United Kingdom.
Yang Guanghui
Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Joint Center for Life Sciences, Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing, China.
Shi Yigong
Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Joint Center for Life Sciences, Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing, China.
Scheres Sjors H W ORCID
MRC Laboratory of Molecular Biology, Cambridge, United Kingdom.
References (54)
54 references, click to expand
  1. Structure of the yeast mitochondrial large ribosomal subunit.
    Science. 2014 Mar 28;343(6178):1485-9 PMID: 24675956
  2. CTFFIND4: Fast and accurate defocus estimation from electron micrographs.
    J Struct Biol. 2015 Nov;192(2):216-21 PMID: 26278980
  3. Cryo-EM structure of the Plasmodium falciparum 80S ribosome bound to the anti-protozoan drug emetine.
    Elife. 2014;3. doi: 10.7554/eLife.03080 PMID: 24913268
  4. A conserved GXXXG motif in APH-1 is critical for assembly and activity of the gamma-secretase complex.
    J Biol Chem. 2004 Feb 6;279(6):4144-52 PMID: 14627705
  5. Allosteric regulation of γ-secretase activity by a phenylimidazole-type γ-secretase modulator.
    Proc Natl Acad Sci U S A. 2014 Jul 22;111(29):10544-9 PMID: 25009180
  6. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search.
    Anal Chem. 2002 Oct 15;74(20):5383-92 PMID: 12403597
  7. Features and development of Coot.
    Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501 PMID: 20383002
  8. Structural analysis of viral nucleocapsids by subtraction of partial projections.
    J Struct Biol. 2007 Feb;157(2):356-64 PMID: 17064936
  9. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy.
    J Mol Biol. 2003 Oct 31;333(4):721-45 PMID: 14568533
  10. Structure of the SecY channel during initiation of protein translocation.
    Nature. 2014 Feb 6;506(7486):102-6 PMID: 24153188
  11. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective.
    Cell. 2005 Feb 25;120(4):545-55 PMID: 15734686
  12. Trajectories of the ribosome as a Brownian nanomachine.
    Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):17492-7 PMID: 25422471
  13. RELION: implementation of a Bayesian approach to cryo-EM structure determination.
    J Struct Biol. 2012 Dec;180(3):519-30 PMID: 23000701
  14. How cryo-EM is revolutionizing structural biology.
    Trends Biochem Sci. 2015 Jan;40(1):49-57 PMID: 25544475
  15. Analysis of the gamma-secretase interactome and validation of its association with tetraspanin-enriched microdomains.
    Nat Cell Biol. 2009 Nov;11(11):1340-6 PMID: 19838174
  16. In vitro characterization of the presenilin-dependent gamma-secretase complex using a novel affinity ligand.
    Biochemistry. 2003 Jul 15;42(27):8133-42 PMID: 12846562
  17. Complex relationships between substrate sequence and sensitivity to alterations in γ-secretase processivity induced by γ-secretase modulators.
    Biochemistry. 2014 Apr 1;53(12):1947-57 PMID: 24620716
  18. Presenilins and γ-secretase: structure, function, and role in Alzheimer Disease.
    Cold Spring Harb Perspect Med. 2012 Jan;2(1):a006304 PMID: 22315713
  19. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM.
    Nat Methods. 2013 Jun;10(6):584-90 PMID: 23644547
  20. Nicastrin functions as a gamma-secretase-substrate receptor.
    Cell. 2005 Aug 12;122(3):435-47 PMID: 16096062
  21. C-terminal fragment of presenilin is the molecular target of a dipeptidic gamma-secretase-specific inhibitor DAPT (N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester).
    J Biol Chem. 2006 May 26;281(21):14670-6 PMID: 16569643
  22. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins.
    Mol Cell. 2000 Sep;6(3):625-36 PMID: 11030342
  23. Localized reconstruction of subunits from electron cryomicroscopy images of macromolecular complexes.
    Nat Commun. 2015;6:8843 PMID: 26534841
  24. Lysine 624 of the amyloid precursor protein (APP) is a critical determinant of amyloid β peptide length: support for a sequential model of γ-secretase intramembrane proteolysis and regulation by the amyloid β precursor protein (APP) juxtamembrane region.
    J Biol Chem. 2011 Nov 18;286(46):39804-12 PMID: 21868378
  25. Contribution of the γ-secretase subunits to the formation of catalytic pore of presenilin 1 protein.
    J Biol Chem. 2012 Jul 27;287(31):25834-43 PMID: 22689582
  26. Processive proteolysis by γ-secretase and the mechanism of Alzheimer's disease.
    Biol Chem. 2012 Sep;393(9):899-905 PMID: 22944690
  27. C-terminal PAL motif of presenilin and presenilin homologues required for normal active site conformation.
    J Neurochem. 2006 Jan;96(1):218-27 PMID: 16305624
  28. Lessons from a failed γ-secretase Alzheimer trial.
    Cell. 2014 Nov 6;159(4):721-6 PMID: 25417150
  29. Conserved "PAL" sequence in presenilins is essential for gamma-secretase activity, but not required for formation or stabilization of gamma-secretase complexes.
    Neurobiol Dis. 2004 Apr;15(3):654-66 PMID: 15056474
  30. Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly.
    Nat Struct Biol. 2003 Jul;10(7):572-6 PMID: 12778115
  31. The architecture of the spliceosomal U4/U6.U5 tri-snRNP.
    Nature. 2015 Jul 2;523(7558):47-52 PMID: 26106855
  32. Differential effects of inhibitors on the gamma-secretase complex. Mechanistic implications.
    J Biol Chem. 2003 May 9;278(19):16470-3 PMID: 12644463
  33. Refinement of macromolecular structures by the maximum-likelihood method.
    Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55 PMID: 15299926
  34. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo.
    Neuron. 1996 Jul;17(1):181-90 PMID: 8755489
  35. EMAN2: an extensible image processing suite for electron microscopy.
    J Struct Biol. 2007 Jan;157(1):38-46 PMID: 16859925
  36. An atomic structure of human γ-secretase.
    Nature. 2015 Sep 10;525(7568):212-7 PMID: 26280335
  37. Activity-dependent isolation of the presenilin- gamma -secretase complex reveals nicastrin and a gamma substrate.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):2720-5 PMID: 11867728
  38. Three-dimensional structure of human γ-secretase.
    Nature. 2014 Aug 14;512(7513):166-70 PMID: 25043039
  39. Cryo-EM structure of SNAP-SNARE assembly in 20S particle.
    Cell Res. 2015 May;25(5):551-60 PMID: 25906996
  40. Semi-automated selection of cryo-EM particles in RELION-1.3.
    J Struct Biol. 2015 Feb;189(2):114-22 PMID: 25486611
  41. Prevention of overfitting in cryo-EM structure determination.
    Nat Methods. 2012 Sep;9(9):853-4 PMID: 22842542
  42. Probability-based protein identification by searching sequence databases using mass spectrometry data.
    Electrophoresis. 1999 Dec;20(18):3551-67 PMID: 10612281
  43. Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions.
    Acta Crystallogr D Biol Crystallogr. 2015 Jan 1;71(Pt 1):136-53 PMID: 25615868
  44. Designed helical peptides inhibit an intramembrane protease.
    J Am Chem Soc. 2003 Oct 1;125(39):11794-5 PMID: 14505382
  45. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity.
    Nature. 2006 Apr 27;440(7088):1208-12 PMID: 16641999
  46. Functional analysis of the transmembrane domains of presenilin 1: participation of transmembrane domains 2 and 6 in the formation of initial substrate-binding site of gamma-secretase.
    J Biol Chem. 2010 Jun 25;285(26):19738-46 PMID: 20418378
  47. Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2.
    Proc Natl Acad Sci U S A. 2003 May 27;100(11):6382-7 PMID: 12740439
  48. Beam-induced motion correction for sub-megadalton cryo-EM particles.
    Elife. 2014;3:e03665 PMID: 25122622
  49. Conformation-independent structural comparison of macromolecules with ProSMART.
    Acta Crystallogr D Biol Crystallogr. 2014 Sep;70(Pt 9):2487-99 PMID: 25195761
  50. Linear non-competitive inhibition of solubilized human gamma-secretase by pepstatin A methylester, L685458, sulfonamides, and benzodiazepines.
    J Biol Chem. 2002 Aug 30;277(35):31499-505 PMID: 12072428
  51. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy.
    Ultramicroscopy. 2013 Dec;135:24-35 PMID: 23872039
  52. Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex.
    Neuron. 2003 Apr 10;38(1):9-12 PMID: 12691659
  53. The initial substrate-binding site of gamma-secretase is located on presenilin near the active site.
    Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3230-5 PMID: 15722417
  54. Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain.
    J Neurochem. 2001 Jan;76(1):173-81 PMID: 11145990
Article Info
Journal
eLife
Abbr.
Elife
ISSN
2050-084X
Published
2015-12-01
Epub
2015-00-01
Language
English
Region
England
NLM ID
101579614
PMCID
PMC4718806
Subset
IM
Grants
Medical Research Council · MC_UP_A025_1013 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com