The LIU LAB

Electron Tomography at Yale University

updated  on August 31, 2017

​Click on each publication in order to be directed to its link.

Other publications


10.      Liu J, Taylor DW, Krementsova EB, Trybus KM, Taylor KA: Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography, Nature 442:208-211, 2006.
11.     Liu J, Bartesaghi A, Borgnia M, Sapiro G, Subramaniam S: Molecular architecture of native HIV-1 gp120 trimers, Nature 455:109-113, 2008.

12.    Liu J, Wendt T, Taylor D, Taylor KA: Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. J Mol Biol 329:963-972, 2003.

13.    Zhu P, Chertova E, Bess J, Jr., Lifson JD, Arthur LO, Liu J, Taylor KA, Roux KH: Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci U S A 100:15812-15817, 2003.

14.    Liu J, Reedy MC, Goldman YE, Franzini-Armstrong C, Sasaki H, Tregear RT, Lucaveche C, Winkler H, Baumann BA, Squire JM, Irving TC, Reedy MK, Taylor KA: Electron tomography of fast frozen, stretched rigor fibers reveals elastic distortions in the myosin crossbridges. J Struct Biol 147:268-282, 2004.

15.    Liu J, Taylor DW, Taylor KA: A 3-D reconstruction of smooth muscle alpha-actinin by CryoEm reveals two different conformations at the actin-binding region. J Mol Biol 338:115-125, 2004.

16.    Tama F, Feig M, Liu J, Brooks CL, 3rd, Taylor KA: The requirement for mechanical coupling between head and S2 domains in smooth muscle myosin ATPase regulation and its implications for dimeric motor function. J Mol Biol 345:837-854, 2005.

17.     Liu J, Wu S, Reedy MC, Winkler H, Lucaveche C, Cheng Y, Reedy MK, Taylor KA: Electron tomography of swollen rigor fibers of insect flight muscle reveals a short and variably angled S2 domain. J Mol Biol 362:844-860, 2006.

18.     Zhu P, Liu J, Bess J, Jr., Chertova E, Lifson JD, Grise H, Ofek GA, Taylor KA, Roux KH: Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852, 2006.

19.     Bennett AE, Liu J, Van Ryk D, Bliss D, Arthos J, Henderson R M, Subramaniam S: Cryo electron tomographic analysis of an HIV neutralizing protein and its complex with native viral gp120. J Biol Chem 282(38): 27754-27759, 2007.

20.     Liu J, McBride MJ, Subramaniam S: Cell-surface filaments of the gliding bacterium Flavobacterium johnsoniae revealed by cryo-electron tomography. J Bacteriol 189: 7503-7506, 2007.

21.     Dai W, Jia Q, Bortz E, Shah S, Liu J, Atanasov I, Li X, Taylor KA, Sun R, Zhou ZH: Unique structures in a tumor herpesvirus revealed by cryo-electron tomography and microscopy. J Struct Biol 161:428-438, 2008.

22.    Bartesaghi A, Sprechmann P, Liu J, Randall G, Sapiro G, Subramaniam S: Classification and 3D averaging with missing wedge-correction in biological electron tomography. J Struct Biol 162(3):436-50, 2008.

23.    Miao L, Vanderlinde O, Liu J, Grant R, Wouterse A, Philipse A, Stewart M, Roberts TM: Filament packing constraints generate protrusive force on amoeboid cell motility. Proc Natl Acad Sci U S A 105:5390-5, 2008.

24.    Ye F, Liu J, Winkler H, Taylor KA: Integrin aIIbb3 in a membrane environment remains the same height after Mn2+ Activation when observed by cryo-electron tomography. J Mol Biol 378:976-86, 2008.

25.    Hampton CM, Liu J, Taylor DW, DeRosier DJ, Taylor KA: The 3D Structure of Villin as a Unique F-Actin Crosslinker. Structure 16(12):1882-91, 2008.

26.    Wu S, Liu J, Reedy MC, Winkler H, Reedy MK, Taylor KA: Methods for identifying and averaging variable molecular conformations in tomograms of actively contracting insect flight muscle. J Struct Biol 168(3):485-502, 2009.

27.    Sanabria H, Swulius MT, Kolodziej SJ, Liu J, Waxham NM: CaMKII Regulates Actin Assembly and Structure, J Biol Chem 284(15):9770-80, 2009.

28.    Winkler H, Zhu P, Liu J, Ye F, Roux KH, Taylor KA: Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J Struct Biol 165(2):64-77, 2009.

29.    Liu J, Wright ER, Winkler H: 3D visualization of HIV virions by cryoelectron tomography. Methods Enzymol 483:267-90, 2010.

30.    Liu J, Howell JK, Bradley SD, Zheng Y, Zhou ZH, Norris SJ: Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J Mol Biol 403(4):546-61, 2010.

31.    Wu S, Liu J, Reedy MC, Tregear RT, Winkler H, Franzini-Armstrong C, Sasaki H, Lucaveche C, Goldman YE, Reedy MK, Taylor KA: Electron tomography of cryofixed, isometrically contracting insect flight muscle reveals novel actin-myosin interactions. PLoS One 5(9):e12643, 2010.

32.    Fu X, Walter MH, Paredes A, Morais MC, Liu J: The mechanism of DNA ejection in the Bacillus anthracis spore-binding phage 8a reveaed by cryo-electron tomography. Virology 421(2):141-8, 2011.

33.    Sze CW, Morado DR, Liu J, Charon NW, Xu H, Li C: Carbon storage regulator A (CsrA(Bb)) is a repressor of Borrelia burgdorferi flagellin protein FlaB. Mol Microbiol 82(4):851-64, 2011.

34.    Liu J, Chen CY, Shiomi D, Niki H, Margolin W: Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli. Virology 417(2):304-11, 2011.

35.    Motaleb MA, Pitzer JE, Sultan SZ, Liu J: A novel gene inactivation system reveals altered periplasmic flagellar orientation in a Borrelia burgdorferi fliL mutant. J Bacteriol 193(13):3324-31, 2011.

36.    Xu H, Raddi G, Liu J, Charon NW, Li C: Chemoreceptors and flagellar motors are subterminally located in close proximity at the two cell poles in spirochetes. J Bacteriol 193(10):2652-6, 2011.

37.    Zhang K, Tong BA, Liu J, Li C: A single-domain FlgJ contributes to flagellar hook and filament formation in the Lyme disease spirochete Borrelia burgdorferi. J Bacteriol 194(4):866-74, 2012.

38.    Zhang K, Liu J, Tu Y, Xu H, Charon NW, Li C: Two CheW coupling proteins are essential in a chemosensory pathway of Borrelia burgdorferi. Mol Microbiol 85(4):782-94, 2012.

39.    Wu S, Liu J, Reedy MC, Perz-Edwards RJ, Tregear RT, Winkler H, Franzini-Armstrong C, Sasaki H, Lucaveche C, Goldman YE, Reedy MK, Taylor KA: Structural Changes in Isometrically Contracting Insect Flight Muscle Trapped following a Mechanical Perturbation. PLoS One 7(6):e39422, 2012.

40.    Raddi G, Morado DR, Yan J, Haake DA, Yang XF, Liu J: Three-dimensional structures of pathogenic and saprophytic Leptospira species revealed by cryo-electron tomography. J Bacteriol 194(6):1299-306, 2012.

41.    Li C, Kurniyati, Hu B, Bian J, Sun J, Zhang W, Liu J, Pan Y, Li C: Abrogation of neuraminidase reduces biofilm formation, capsule biosynthesis, and virulence of Porphyromonas gingivalis. Infect Immun. 80(1):3-13, 2012.

42.    Halford C, Gonzalez R, Campuzano S, Hu B, Babbitt JT, Liu J, Wang J, Churchill BM, Haake DA. Rapid Antimicrobial Susceptibility Testing by Sensitive Detection of Precursor Ribosomal RNA Using a Novel Electrochemical Biosensing Platform. Antimicrob Agents Chemother 57(2):936-43, 2013.

43.    Chen L, Xu Q, Tu J, Ge Y, Liu J, Liang FT: Increasing RpoS Expression Causes Cell Death in Borrelia burgdorferi. PLoS

One 8(12):e83276, 2013.

44.    Miller KA, Motaleb MA, Liu J, Hu B, Caimano MJ, Miller MR, Charon NW: Initial Characterization of the FlgE Hook High Molecular Weight Complex of Borrelia burgdorferi. PLoS One 9(5):e98338, 2014.

45.     Dutta M, Liu J, Roux KH, Taylor KA: Visualization of retroviral envelope spikes in complex with the V3 loop antibody 447-52D on intact viruses by cryo-electron tomography. J Virol. 2014 Nov;88(21):12265-75. PMCID: PMC4248906

46.    Zhao X, Norris SJ, Liu J: Molecular Architecture of Bacterial Flagellar Motor in Cells. Biochemistry. 2014 Apr 3. [Epub ahead of print]

47.    Lin T, Gao L, Zhao X, Liu J, Norris SJ, Mutations in the Borrelia burgdorferi Flagellar Type III Secretion System Genes fliH and fliI Profoundly Affect Spirochete Flagellar Assembly, Morphology, Motility, Structure, and Cell Division. MBio. 2015 May 12;6(3):e00579-15. doi: 10.1128/mBio.00579-15.
48.    
Sultan SZ, Sekar P, Zhao X, Manne A, Liu J, Wooten RM, Motaleb MA, Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts. Infect Immun. 2015 May;83(5):1765-77. doi: 10.1128/IAI.03097-14. Epub 2015 Feb 17.
49.   
Prüβ B, Liu J, Higgs P, Thompson L, Lessons in Fundamental Mechanisms and Diverse Adaptations from the 2015 BLAST (Bacterial Locomotion and Signal Transduction) Meeting, J Bacteriol, 2015 Oct 1;197(19):3028-40. 

50.    Yan R, Edwards TJ, Pankratz LM, Kuhn RJ, Lanman JK, Liu, J., and Jiang W: A fast cross- validation method for alignment of electron tomography images based on Beer-Lambert law. J Struct Biol. 2015 Oct 5. pii: S1047-8477(15)30082-4.
51.    Yan R, Edwards TJ, Pankratz LM, Kuhn RJ, Lanman JK, Liu, J., and Jiang W: Simultaneous determination of sample thickness, tilt, and electron mean free path using tomographic tilt images based on Beer-Lambert law. J Struct Biol. 2015 Oct 7. pii: S1047-8477(15)30074-5. 
52.    Morado DR, Hu B, Liu J, Using tomoauto – a protocol for high-throughput automated cryo-electron tomography, J Vis Exp, 2016

53.    Farley M, Hu B, Margolin W, Liu J,  Minicells, Back in Fashion, Journal of Bacteriology, 2016 Mar 31;198(8):1186-95.

54.    Yuan Z, Bai L, Sun J, Georgescu R, Liu J, O'Donnell ME, Li H: Structure of the eukaryotic replicative CMG helicase suggests a pumpjack motion for translocation. Nat Struct Mol Biol. 2016 Mar; 23(3):217-24.  
55.    Xu R, Zhang G, Mai J, Deng X, Segura-Ibarra V, Wu S, Shen J, Liu H, Hu Z, Chen L, Huang Y, Koay E, Huang Y, Liu J, Ensor JE, Blanco E, Liu X, Ferrari M, Shen H. An injectable nanoparticle generator enhances delivery of cancer therapeutics. Nat Biotechnol. 2016 Apr;34(4):414-8. Epub 2016 Mar 14. 
56.    Wunder EA, Figueira CP, Benaroudj N, Hu B, Tong BA, Trajtenberg F, Liu J, Reis MG, Charon NW, Buschiazzo A, Picardeau M, Ko AI. A novel flagellar sheath protein, FcpA, determines filament coiling, translational motility and virulence for the Leptospira spirochete. Mol Microbiol. 2016 Aug; 101(3): 457-70. 

​57.    Miller MR, Miller KA, Bian J, James ME, Zhang S, Lynch M, Callery PS, Hettick JM, Cockburn A, Liu J, Li C, Crane BR, Charon NW: Spirochaete flagella hook proteins self-catalyse a lysinoalanine covalent crosslink for motility, Nature Microbial, 2016 Aug 8;1(10):16134.
58.    Moon KH, Zhao X, Manne A, Wang J, Yu Z, Liu J, Motaleb MA: Spirochetes flagellar collar proteins have astounding effects in orientation of periplasmic flagella, bacterial shape, motility, and stability of motors in Borrelia burgdorferi. Mol Microbiol, 2016 Oct;102(2):336-348.
59.    Farley M, Tu J, Kearns DB, Molineux IJ, Liu J: Ultrastructural analysis of bacteriophage Φ29 during infection of Bacillus subtilis, J Struct Biol, 2016 Jul 29. pii: S1047-8477(16)30167-8.
60.   Kurniyati K, Kelly JF, Vinogradov E, Robotham A, Tu Y, Wang J, Liu J, Logan SM, Li C: A novel glycan modifies the flagellar filament proteins of the oral bacterium Treponema denticola, Mol Microbiol, 2016 Oct 1. doi: 10.1111/mmi.13544.
61.   Qin Z, Lin W, Zhu S, Franco AT, Liu J: Imaging the motility and chemotaxis machineries in Helicobacter pylori by cryo-electron tomography, J Bacteriol 2016 Nov 14. pii: JB.00695-16. [Epub ahead of print]

62.   Tu J, Park T, Morado DR, Hughes KT, Molineux IJ, Liu J: Dual host specificity of phage SP6 is facilitated by tailspike rotation. Virology. 2017 Jul;507:206-215. doi: 10.1016/j.virol.2017.04.017.

63.   Zhu S, Qin Z, Wang J, Morado DR, Liu J: In Situ Structural Analysis of the Spirochetal Flagellar Motor by Cryo-Electron Tomography. Methods Mol Biol. 2017;1593:229-242. doi: 10.1007/978-1-4939-6927-2_18.

64.   Siegel SD, Liu J, Ton-That H: Biogenesis of the Gram-positive bacterial cell envelope. Curr Opin Microbiol. 2016 Dec;34:31-37. doi: 10.1016/j.mib.2016.07.015. Epub 2016 Aug 4.

65.   Marcin Krupka, Veronica Rowlett, Dustin Morado, Heidi Vitrac, Kara Schoenemann, Jun Liu, and William Margolin: Escherichia coli FtsA forms lipid-bound minirings that antagonize lateral interactions between FtsZ protofilaments, Nature Communications, 2017 Jul 11;8:15957.




Selected publications


1.      Liu J, Lin T, Botkin DJ, McCrum E, Winkler H, Norris SJ:  Intact Flagellar Motor of Borrelia burgdorferi Revealed by Cryo-Electron Tomography: Evidence for Stator Ring Curvature and Rotor/C Ring Assembly Flexion, J Bacteriol 191(16):5026-36, 2009.

2.      Luther PK, Winkler H, Taylor K, Zoghbi ME, Craig R, Padrón R, Squire JM, Liu J: Direct visualization of myosin-binding protein C bridging myosin and actin filaments in intact muscle, Proc Natl Acad Sci U S A 108(28):11423-8, 2011.

3.      Liu J, Hu B, Morado DR, Jani S, Manson MD, Margolin W: Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells, Proc Natl Acad Sci U S A 109(23):E1481-8, 2012.

4.      Hu B, Margolin W, Molineux IJ, Liu J: The Bacteriophage T7 Virion Undergoes Extensive Structural Remodeling during infection, Science 339(6119):576-9, 2013.

5.      Zhao X, Zhang K, Boquoi T, Hu B, Motaleb MA, Miller K, James M, Charon NW, Manson MD, Norris SJ, Li C, Liu J: Cryo-Electron Tomography Reveals the Sequential Assembly of Bacterial Flagella in Borrelia burgdorferi, Proc Natl Acad Sci U S A, 110(35): 14390-5.

6.      Hu B, Morado DR, Margolin W, Rohde JR, Arizmendi O, Picking WL, Picking WD, Liu J: Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci U S A. 112(4):1047-52, 2015.

7.      Hu B, Margolin W, Molineux IJ, Liu J, Structural remodeling of bacteriophage T4 and host membranes during infection initiation, Proc Natl Acad Sci U S A,112(35):E4919-28, 2015.

8.      Hu B, Lara-Tejero M, Kong Q, Galán JE, Liu J: In situ molecular architecture of the Salmonella type III secretion machine, Cell 168(6):1065-1074.e10, 2017.

9.      Zhu S, Nishikino T, Hu B, Kojima S, Homma M, Liu J: Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus, Proc Natl Acad Sci U S A  in press.