冷冻电镜技术的突破导致结构生物学发生革命性变化
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摘要
最近,冷冻电镜技术的突破引起结构生物学发生了革命。这一革命导致2017年诺贝尔化学奖授予对冷冻电镜技术发展做出开创性贡献的3位科学家Jacques Dubochet、Joachim Frank和Richard Henderson。本文将综述冷冻电镜的发展历程,导致结构生物学革命的冷冻电镜关键技术,包括电镜、图像记录装置和图像处理算法方面的突破,以及中国科学家应用冷冻电镜取得的重要科学成就,涵盖基因表达/调控、蛋白质合成/降解、膜蛋白、免疫、病毒等相关蛋白复合体。最后,对冷冻电镜的未来发展方向进行展望。
Recent technical breakthroughs in cryo-electron microscopy(cryo-EM) revolutionized structural biology,which led to the 2017 Nobel Prize in chemistry award to three scientists Jacques Dubochet, Joachim Frank and Richard Henderson, who had groundbreaking contribution to the development of cryo-EM. In this review,I will give a comprehensive review on the development history of cryo-EM,the technical aspects of the breakthroughs in cryo-EM leading to structural biology revolution,including electron microscope, image recording device and image processing algorithm, and major scientific achievements by Chinese scientists employing cryo-EM,covering protein complexes involved in or related to gene expression and regulation,protein synthesis and degradation,membrane proteins,immunity and viruses. Finally,I will give a perspective outlook on the development of cryo-EM in the future.
Recent technical breakthroughs in cryo-electron microscopy(cryo-EM) revolutionized structural biology,which led to the 2017 Nobel Prize in chemistry award to three scientists Jacques Dubochet, Joachim Frank and Richard Henderson, who had groundbreaking contribution to the development of cryo-EM. In this review,I will give a comprehensive review on the development history of cryo-EM,the technical aspects of the breakthroughs in cryo-EM leading to structural biology revolution,including electron microscope, image recording device and image processing algorithm, and major scientific achievements by Chinese scientists employing cryo-EM,covering protein complexes involved in or related to gene expression and regulation,protein synthesis and degradation,membrane proteins,immunity and viruses. Finally,I will give a perspective outlook on the development of cryo-EM in the future.
引文
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[43]Qian H,Zhao X,Cao P,et al.Structure of the Human Lipid Exporter ABCA1[J].Cell,2017,169(7):1228-1239.e10
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[45]Wu M,Gu J,Guo R,et al.Structure of Mammalian Respiratory Supercomplex I1III2IV1[J].Cell,2016,167(6):1598-1609.e10
[46]Guo R,Zong S,Wu M,et al.Architecture of Human Mitochondrial Respiratory Megacomplex I2III2IV2[J].Cell,2017,170(6):1247-1257.e12
[47]Gu J,Wu M,Guo R,et al.The architecture of the mammalian respirasome[J].Nature,2016,537(7622):639-643
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[49]Li M,Zhou X,Wang S,et al.Structure of a eukaryotic cyclicnucleotide-gated channel[J].Nature,2017,542(7639):60-65
[50]Yan Z,Yin M,Xu D,et al.Structural insights into the secretin translocation channel in the type II secretion system[J].Nat Struct Mol Biol,2017,24(2):177-183
[51]Wei X,Su X,Cao P,et al.Structure of spinach photosystem IILHCII supercomplex at 3.2resolution[J].Nature,2016,534(7605):69-74
[52]Su X,Ma J,Wei X,et al.Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex[J].Science,2017,357(6353):815-820
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[54]Sun S,Li L,Yang F,et al.Cryo-EM structures of the ATPbound Vps4E233Qhexamer and its complex with Vta1 at nearatomic resolution[J].Nat Commun,2017,8:16064
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[56]Hu Z,Zhou Q,Zhang C,et al.Structural and biochemical basis for induced self-propagation of NLRC4[J].Science,2015,350(6259):399-404
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[2]De Rosier DJ,Klug A.Reconstruction of three dimensional structures from electron micrographs[J].Nature,1968,217(5124):130-134
[3]Henderson R.Realizing the potential of electron cryo-microscopy[J].Q Rev Biophys,2004,37(1):3-13
[4]Mc Mullan G,Faruqi AR,Clare D,et al.Comparison of optimal performance at 300ke V of three direct electron detectors for use in low dose electron microscopy[J].Ultramicroscopy,2014,147:156-163
[5]Liao M,Cao E,Julius D,et al.Structure of the TRPV1 ion channel determined by electron cryo-microscopy[J].Nature,2013,504(7478):107-112
[6]Fernández IS,Bai XC,Hussain T,et al.Molecular architecture of a eukaryotic translational initiation complex[J].Science,2013,342(6160):1240585
[7]Yan C,Hang J,Wan R,et al.Structure of a yeast spliceosome at 3.6-angstrom resolution[J].Science,2015,349(6253):1182-1191
[8]Wan R,Yan C,Bai R,et al.The 3.8structure of the U4/U6.U5 tri-snRNP:Insights into spliceosome assembly and catalysis[J].Science,2016,351(6272):466-475
[9]Yan C,Wan R,Bai R,et al.Structure of a yeast activated spliceosome at 3.5resolution[J].Science,2016,353(6302):904-911
[10]Wan R,Yan C,Bai R,et al.Structure of a yeast catalytic step I spliceosome at 3.4resolution[J].Science,2016,353(6302):895-904
[11]Yan C,Wan R,Bai R,et al.Structure of a yeast step II catalytically activated spliceosome[J].Science,2017,355(6321):149-155
[12]Zhang X,Yan C,Hang J,et al.An Atomic Structure of the Human Spliceosome[J].Cell,2017,169(5):918-929.e14
[13]Wan R,Yan C,Bai R,et al.Structure of an Intron Lariat Spliceosome from Saccharomyces cerevisiae[J].Cell,2017,171(1):120-132.e12
[14]Bai R,Yan C,Wan R,et al.Structure of the Post-catalytic Spliceosome from Saccharomyces cerevisiae[J].Cell,2017.pii:S0092-8674(17)31264-3
[15]Song F,Chen P,Sun D,et al.Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units[J].Science,2014,344(6182):376-380
[16]Xu P,Li C,Chen Z,et al.The Nu A4 Core Complex Acetylates Nucleosomal Histone H4 through a Double Recognition Mechanism[J].Mol Cell,2016,63(6):965-975
[17]Liu X,Li M,Xia X,et al.Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure[J].Nature,2017,544(7651):440-445
[18]Wang X,Sun Q,Ding Z,et al.Redefining the modular organization of the core Mediator complex[J].Cell Res,2014,24(7):796-808
[19]Li N,Zhai Y,Zhang Y,et al.Structure of the eukaryotic MCM complex at 3.8[J].Nature,2015,524(7564):186-191
[20]Chang S,Sun D,Liang H,et al.Cryo-EM structure of influenza virus RNA polymerase complex at 4.3resolution[J].Mol Cell,2015,57(5):925-935
[21]Xu J,Zhao L,Xu Y,et al.Cryo-EM structures of human RAD51 recombinase filaments during catalysis of DNA-strand exchange[J].Nat Struct Mol Biol,2017,24(1):40-46
[22]Qu G,Kaushal PS,Wang J,et al.Structure of a group II intron in complex with its reverse transcriptase[J].Nat Struct Mol Biol,2016,23(6):549-557
[23]Yin X,Liu M,Tian Y,et al.Cryo-EM structure of human DNAPK holoenzyme[J].Cell Res,2017,27(11):1341-1350
[24]Liu JJ,Niu CY,Wu Y,et al.Cryo EM structure of yeast cytoplasmic exosome complex[J].Cell Res,2016,26(7):822-837
[25]Feng B,Mandava CS,Guo Q,et al.Structural and functional insights into the mode of action of a universally conserved Obg GTPase[J].PLo S Biol,2014,12(5):e1001866
[26]Wu S,Tutuncuoglu B,Yan K,et al.Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes[J].Nature,2016,534(7605):133-137
[27]Ma C,Kurita D,Li N,et al.Mechanistic insights into the alternative translation termination by Arf A and RF2[J].Nature,2017,541(7638):550-553
[28]Ma C,Wu S,Li N,et al.Structural snapshot of cytoplasmic pre-60S ribosomal particles bound by Nmd3,Lsg1,Tif6 and Reh1[J].Nat Struct Mol Biol,2017,24(3):214-220
[29]Li Z,Guo Q,Zheng L,et al.Cryo-EM structures of the 80S ribosomes from human parasites Trichomonas vaginalis and Toxoplasma gondii[J].Cell Res,2017,27(10):1275-1288
[30]Lu Y,Wu J,Dong Y,et al.Conformational Landscape of the p28-Bound Human Proteasome Regulatory Particle[J].Mol Cell,2017,67(2):322-333.e6
[31]Zhang L,Wang X,Fan F,et al.Cryo-EM structure of Nma111p,a unique Htr A protease composed of two protease domains and four PDZ domains[J].Cell Res,2017,27(4):582-585
[32]Lu P,Bai XC,Ma D,et al.Three-dimensional structure of humanγ-secretase[J].Nature,2014,512(7513):166-170
[33]Sun L,Zhao L,Yang G,et al.Structural basis of humanγ-secretase assembly[J].Proc Natl Acad Sci U S A,2015,112(19):6003-6008
[34]Bai XC,Yan C,Yang G,et al.An atomic structure of humanγ-secretase[J].Nature,2015,525(7568):212-217
[35]Shen H,Zhou Q,Pan X,et al.Structure of a eukaryotic voltagegated sodium channel at near-atomic resolution[J].Science,2017,355(6328).pii:eaal4326
[36]Yan Z,Zhou Q,Wang L,et al.Structure of the Nav1.4-β1Complex from Electric Eel[J].Cell,2017,170(3):470-482.e11
[37]Wu J,Yan Z,Li Z,et al.Structure of the voltage-gated calcium channel Cav1.1 complex[J].Science,2015,350(6267):aad2395
[38]Wu J,Yan Z,Li Z,et al.Structure of the voltage-gated calcium channel Ca(v)1.1 at 3.6resolution[J].Nature,2016,537(7619):191-196
[39]Yan Z,Bai X,Yan C,et al.Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution[J].Nature,2015,517(7532):50-55
[40]Peng W,Shen H,Wu J,et al.Structural basis for the gating mechanism of the type 2 ryanodine receptor RyR2[J].Science,2016,354(6310).pii:aah5324
[41]Bai XC,Yan Z,Wu J,et al.The Central domain of RyR1 is the transducer for long-range allosteric gating of channel opening[J].Cell Res,2016,26(9):995-1006
[42]Wei R,Wang X,Zhang Y,et al.Structural insights into Ca(2+)-activated long-range allosteric channel gating of RyR1[J].Cell Res,2016,26(9):977-994
[43]Qian H,Zhao X,Cao P,et al.Structure of the Human Lipid Exporter ABCA1[J].Cell,2017,169(7):1228-1239.e10
[44]Gong X,Qian H,Zhou X,et al.Structural Insights into the Niemann-Pick C1(NPC1)-Mediated Cholesterol Transfer and Ebola Infection[J].Cell,2016,165(6):1467-1478
[45]Wu M,Gu J,Guo R,et al.Structure of Mammalian Respiratory Supercomplex I1III2IV1[J].Cell,2016,167(6):1598-1609.e10
[46]Guo R,Zong S,Wu M,et al.Architecture of Human Mitochondrial Respiratory Megacomplex I2III2IV2[J].Cell,2017,170(6):1247-1257.e12
[47]Gu J,Wu M,Guo R,et al.The architecture of the mammalian respirasome[J].Nature,2016,537(7622):639-643
[48]Ge J,Li W,Zhao Q,et al.Architecture of the mammalian mechanosensitive Piezo1 channel[J].Nature,2015,527(7576):64-69
[49]Li M,Zhou X,Wang S,et al.Structure of a eukaryotic cyclicnucleotide-gated channel[J].Nature,2017,542(7639):60-65
[50]Yan Z,Yin M,Xu D,et al.Structural insights into the secretin translocation channel in the type II secretion system[J].Nat Struct Mol Biol,2017,24(2):177-183
[51]Wei X,Su X,Cao P,et al.Structure of spinach photosystem IILHCII supercomplex at 3.2resolution[J].Nature,2016,534(7605):69-74
[52]Su X,Ma J,Wei X,et al.Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex[J].Science,2017,357(6353):815-820
[53]Zhang J,Ma J,Liu D,et al.Structure of phycobilisome from the red alga Griffithsia pacifica[J].Nature,2017,551(7678):57-63
[54]Sun S,Li L,Yang F,et al.Cryo-EM structures of the ATPbound Vps4E233Qhexamer and its complex with Vta1 at nearatomic resolution[J].Nat Commun,2017,8:16064
[55]Zhou Q,Huang X,Sun S,et al.Cryo-EM structure of SNAPSNARE assembly in 20S particle[J].Cell Res,2015,25(5):551-560
[56]Hu Z,Zhou Q,Zhang C,et al.Structural and biochemical basis for induced self-propagation of NLRC4[J].Science,2015,350(6259):399-404
[57]Zhang L,Chen S,Ruan J,et al.Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization[J].Science,2015,350(6259):404-409
[58]Wang X,Li SH,Zhu L,et al.Near-atomic structure of Japanese encephalitis virus reveals critical determinants of virulence and stability[J].Nat Commun,2017,8(1):14
[59]Wang X,Zhu L,Dang M,et al.Potent neutralization of hepatitis A virus reveals a receptor mimic mechanism and the receptor recognition site[J].Proc Natl Acad Sci U S A,2017,114(4):770-775
[60]Zhu L,Wang X,Ren J,et al.Structure of human Aichi virus and implications for receptor binding[J].Nat Microbiol,2016,1(11):16150
[61]Zhu L,Wang X,Ren J,et al.Structure of Ljungan virus provides insight into genome packaging of this picornavirus[J].Nat Commun,2015,6:8316
[62]Yuan Y,Cao D,Zhang Y,et al.Cryo-EM structures of MERSCo V and SARS-Co V spike glycoproteins reveal the dynamic receptor binding domains[J].Nat Commun,2017,8:15092
[63]Gui M,Song W,Zhou H,et al.Cryo-electron microscopy structures of the SARS-Co V spike glycoprotein reveal a prerequisite conformational state for receptor binding[J].Cell Res,2017,27(1):119-129
[64]Misasi J,Gilman MS,Kanekiyo M,et al.Structural and molecular basis for Ebola virus neutralization by protective human antibodies[J].Science,2016,351(6279):1343-1346
[65]Liu H,Cheng L.Cryo-EM shows the polymerase structures and a nonspooled genome within a dsRNA virus[J].Science,2015,349(6254):1347-1350
[66]Wei DY,Yin CC.An optimized locally adaptive non-local means denoising filter for cryo-electron microscopy data[J].J Struct Biol,2010,172(3):211-218
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