Finding of widespread viral and bacterial revolution dsDNA translocation motors distinct from rotation motors by channel chirality and size

Cell & Bioscience

Peixuan Guo³  Farzin Haque²  Hui Zhang²  Oleg V Tsodikov¹  Chad Schwartz²  Lisa P Huang⁴  Shaoying Wang²  Zhengyi Zhao²  Gian Marco De-Donatis² 

[1] Department of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, KY, USA;Markey Cancer Center, University of Kentucky, Lexington, KY, USA;William Farish Endowed Chair in Nanobiotechnology, School of Pharmacy, University of Kentucky, 565 Biopharmaceutical Complex, 789 S. Limestone Street, Lexington, KY 40536, USA;Current address: Institute for Biomarker Research, Medical Diagnostic Laboratories, L.L.C., Hamilton, NJ 08690, USA

关键词: Nanomotor;    RecA;    FtsK;    Phi29;    Revolution force;    DNA helicase;    Bacteriophage;    Viral assembly;    Viral DNA packaging motor;    DsDNA viruses;    DNA translocase;   

Others  :  790487
DOI  :  10.1186/2045-3701-4-30

 received in 2014-04-14, accepted in 2014-05-16,  发布年份 2014

【 摘 要 】

Background

Double-stranded DNA translocation is ubiquitous in living systems. Cell mitosis, bacterial binary fission, DNA replication or repair, homologous recombination, Holliday junction resolution, viral genome packaging and cell entry all involve biomotor-driven dsDNA translocation. Previously, biomotors have been primarily classified into linear and rotational motors. We recently discovered a third class of dsDNA translocation motors in Phi29 utilizing revolution mechanism without rotation. Analogically, the Earth rotates around its own axis every 24 hours, but revolves around the Sun every 365 days.

Results

Single-channel DNA translocation conductance assay combined with structure inspections of motor channels on bacteriophages P22, SPP1, HK97, T7, T4, Phi29, and other dsDNA translocation motors such as bacterial FtsK and eukaryotic mimiviruses or vaccinia viruses showed that revolution motor is widespread. The force generation mechanism for revolution motors is elucidated. Revolution motors can be differentiated from rotation motors by their channel size and chirality. Crystal structure inspection revealed that revolution motors commonly exhibit channel diameters larger than 3 nm, while rotation motors that rotate around one of the two separated DNA strands feature a diameter smaller than 2 nm. Phi29 revolution motor translocated double- and tetra-stranded DNA that occupied 32% and 64% of the narrowest channel cross-section, respectively, evidencing that revolution motors exhibit channel diameters significantly wider than the dsDNA. Left-handed oriented channels found in revolution motors drive the right-handed dsDNA via anti-chiral interaction, while right-handed channels observed in rotation motors drive the right-handed dsDNA via parallel threads. Tethering both the motor and the dsDNA distal-end of the revolution motor does not block DNA packaging, indicating that no rotation is required for motors of dsDNA phages, while a small-angle left-handed twist of dsDNA that is aligned with the channel could occur due to the conformational change of the phage motor channels from a left-handed configuration for DNA entry to a right-handed configuration for DNA ejection for host cell infection.

Conclusions

The revolution motor is widespread among biological systems, and can be distinguished from rotation motors by channel size and chirality. The revolution mechanism renders dsDNA void of coiling and torque during translocation of the lengthy helical chromosome, thus resulting in more efficient motor energy conversion.

【 授权许可】

   
2014 De-Donatis et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]Snider J, Houry WA: AAA + proteins: diversity in function, similarity in structure. Biochem Soc Trans 2008, 36:72-77.
• [2]Ammelburg M, Frickey T, Lupas AN: Classification of AAA + proteins. J Struct Biol 2006, 156:2-11.
• [3]White SR, Lauring B: AAA + ATPases: Achieving diversity of function with conserved machinery. Traffic 2007, 8:1657-1667.
• [4]Chen YJ, Yu X, Egelman EH: The hexameric ring structure of the Escherichia coli RuvB branch migration protein. J Mol Biol 2002, 319:587-591.
• [5]Singleton MR, Dillingham MS, Wigley DB: Structure and mechanism of helicases and nucleic acid translocases. Ann Rev Biochem 2007, 76:23-50.
• [6]Kainov DE, Tuma R, Mancini EJ: Hexameric molecular motors: P4 packaging ATPase unravels the mechanism. Cell Mol Life Sci 2006, 63(10):1095-1105.
• [7]Hanson PI, Whiteheart SW: AAA + proteins: have engine, will work. Nat Rev Mol Cell Biol 2005, 6:519-529.
• [8]Schwartz C, Fang H, Huang L, Guo P: Sequential action of ATPase, ATP, ADP, Pi and dsDNA in procapsid-free system to enlighten mechanism in viral dsDNA packaging. Nucleic Acids Res 2012, 40:2577-2586.
• [9]Guo P, Schwartz C, Haak J, Zhao Z: Discovery of a new motion mechanism of biomotors similar to the earth revolving around the sun without rotation. Virology 2013, 446:133-143.
• [10]Guo P, Zhao Z, Haak J, Wang S, Weitao T: Common mechanisms of DNA translocation motors in bacteria and viruses using one-way revolution mechanism without rotation. Biotechnol Adv 2014. In Press
• [11]Zhang YB, Yuan FH, Presnell SR, Tian KL, Gao Y, Tomkinson AE, Gu LY, Li GM: Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 2005, 122:693-705.
• [12]Binzel DW, Khisamutdinov EF, Guo P: Entropy-Driven One-Step Formation of Phi29 pRNA 3WJ from Three RNA Fragments. Biochemistry 2014, 53:2221-2231.
• [13]Khisamutdinov EF, Jasinski DL, Guo P: RNA as a Boiling-Resistant Anionic Polymer Material To Build Robust Structures with Defined Shape and Stoichiometry. ACS Nano 2014. In press. DOI: 10.1021/nn5006254
• [14]Fang H, Zhang P, Huang LP, Zhao Z, Pi F, Montemagno C, Guo P: Binomial distribution for quantification of protein subunits in biological nanoassemblies and functional nanomachines. Nanomedicine 2014. In press. DOI: 10.1016/j.nano.2014.03.005
• [15]Zhang H, Guo P: Single molecule photobleaching (SMPB) technology for counting of RNA, DNA, protein and other molecules in nanoparticles and biological complexes by TIRF instrumentation. Methods 2014, 67(2):169-176.
• [16]Zhang H, Endrizzi JA, Shu Y, Haque F, Sauter C, Shlyakhtenko LS, Lyubchenko Y, Guo P, Chi YI: Crystal structure of 3WJ core revealing divalent Ion-promoted thermostability and assembly of the Phi29 Hexameric motor pRNA. RNA 2013, 19:1226-1237.
• [17]Shu Y, Shu D, Haque F, Guo P: Fabrication of pRNA nanoparticles to deliver therapeutic RNAs and bioactive compounds into tumor cells. Nat Protoc 2013, 8:1635-1659.
• [18]Xiao F, Zhang H, Guo P: Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging. Nucleic Acids Res 2008, 36:6620-6632.
• [19]Xiao F, Sun J, Coban O, Schoen P, Wang JC, Cheng RH, Guo P: Fabrication of massive sheets of single layer patterned arrays using lipid directed reengineered Phi29 motor Dodecamer. ACS Nano 2009, 3:100-107.
• [20]Xiao F, Demeler B, Guo P: Assembly mechanism of the sixty-subunit nanoparticles via interaction of RNA with the reengineered protein connector of phi29 DNA-packaging motor. ACS Nano 2010, 4:3293-3301.
• [21]Mehta A: Myosin learns to walk. J Cell Sci 2001, 114:1981-1998.
• [22]Visscher K, Schnitzer MJ, Block SM: Single kinesin molecules studied with a molecular force clamp. Nature 1999, 400:184-189.
• [23]Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, Yanagida T: Direct observation of single kinesin molecules moving along microtubules. Nature 1996, 380:451-453.
• [24]Harada Y, Ohara O, Takatsuki A, Itoh H, Shimamoto N, Kinosita K Jr: Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase. Nature 2001, 409:113-115.
• [25]Doering C, Ermentrout B, Oster G: Rotary DNA motors. Biophys J 1998, 69:2256-2267.
• [26]Ariga T, Masaike T, Noji H, Yoshida M: Stepping rotation of F(1)-ATPase with one, two, or three altered catalytic sites that bind ATP only slowly. J Biol Chem 2002, 277:24870-24874.
• [27]Casjens SR: The DNA-packaging nanomotor of tailed bacteriophages. Nat Rev Microbiol 2011, 9:647-657.
• [28]Roos WH, Ivanovska IL, Evilevitch A, Wuite GJL: Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell Mol Life Sci 2007, 64:1484-1497.
• [29]Catalano CE: The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. Cell Mol Life Sci 2000, 57:128-148.
• [30]Hendrix RW: Bacteriophage DNA packaging: RNA gears in a DNA transport machine (Minireview). Cell 1998, 94:147-150.
• [31]Guo PX, Lee TJ: Viral nanomotors for packaging of dsDNA and dsRNA. Mol Microbiol 2007, 64:886-903.
• [32]Zhang H, Schwartz C, De Donatis GM, Guo P: “Push Through One-Way Valve” mechanism of viral DNA packaging. Adv Virus Res 2012, 83:415-465.
• [33]Serwer P: A hypothesis for bacteriophage DNA packaging motors. Viruses 2010, 2:1821-1843.
• [34]Guo P, Peterson C, Anderson D: Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi29. J Mol Biol 1987, 197:229-236.
• [35]Sabanayagam CR, Oram M, Lakowicz JR, Black LW: Viral DNA packaging studied by fluorescence correlation spectroscopy. Biophys J 2007, 93:L17-L19.
• [36]Hwang JS, Bogner E: ATPase activity of the terminase subunit pUL56 of human cytomegalovirus. J Biol Chem 2002, 277:6943-6948.
• [37]Gual A, Camacho AG, Alonso JC: Functional analysis of the terminase large subunit, G2P, of Bacillus subtilis bacteriophage SPP1. J Biol Chem 2000, 275:35311-35319.
• [38]Hang JQ, Tack BF, Feiss M: ATPase center of bacteriophage lambda terminase involved in post- cleavage stages of DNA packaging: identification of ATP-interactive amino acids. J Mol Biol 2000, 302:777-795.
• [39]Hwang Y, Catalano CE, Feiss M: Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage lambda. Biochemistry 1996, 35:2796-2803.
• [40]Rubinchik S, Parris W, Gold M: The in-vitro atpases of bacteriophage-lambda terminase and its large subunit, gene product A. The relationship with their DNA helicase and packaging activities. J Biol Chem 1994, 269:13586-13593.
• [41]Morita M, Tasaka M, Fujisawa H: DNA packaging ATPase of bacteriophage T3. Virology 1993, 193:748-752.
• [42]Koonin EV, Senkevich TG, Chernos VI: Gene-A32 product of vaccinia virus may be an ATPase involved in viral-DNA packaging as indicated by seuqnce compareisons with other putative viral ATPases. Virus Genes 1993, 7:89-94.
• [43]Hendrix RW: Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci U S A 1978, 75:4779-4783.
• [44]Valpuesta JM, Carrascosa J: Structure of viral connectors and their funciton in bacteriophage assembly and DNA packaging. Q Rev Biophys 1994, 27:107-155.
• [45]Olia AS, Prevelige PE, Johnson JE, Cingolani G: Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 2011, 18:597-603.
• [46]Guasch A, Pous J, Ibarra B, Gomis-Ruth FX, Valpuesta JM, Sousa N, Carrascosa JL, Coll M: Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J Mol Biol 2002, 315:663-676.
• [47]Baumann RG, Mullaney J, Black LW: Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 2006, 61:16-32.
• [48]Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S, Walter JM, Faik W, Anderson DL, Bustamante C: Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PloS Biol 2007, 5:558-567.
• [49]Chang C, Zhang H, Shu D, Guo P, Savran C: Bright-field analysis of phi29 DNA packaging motor using a magnetomechanical system. Appl Phys Lett 2008, 93:153902-153903.
• [50]Schwartz C, De Donatis GM, Zhang H, Fang H, Guo P: Revolution rather than rotation of AAA + hexameric phi29 nanomotor for viral dsDNA packaging without coiling. Virology 2013, 443:28-39.
• [51]Shu D, Zhang H, Jin J, Guo P: Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. EMBO J 2007, 26:527-537.
• [52]Jing P, Haque F, Shu D, Montemagno C, Guo P: One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett 2010, 10:3620-3627.
• [53]Schwartz C, De Donatis GM, Fang H, Guo P: The ATPase of the phi29 DNA-packaging motor is a member of the hexameric AAA + superfamily. Virology 2013, 443:20-27.
• [54]Zhao Z, Khisamutdinov E, Schwartz C, Guo P: Mechanism of one-way traffic of hexameric phi29 DNA packaging motor with four electropositive relaying layers facilitating anti-parallel revolution. ACS Nano 2013, 7:4082-4092.
• [55]Guo P: Biophysical studies reveal new evidence for one-way revolution mechanism of bacteriophage varphi29 DNA packaging motor. Biophys J 2014, 106:1837-1838.
• [56]Demarre G, Galli E, Barre FX: The FtsK family of DNA pumps. Adv Exp Med Biol 2013, 767:245-262.
• [57]Barre FX: FtsK and SpoIIIE: the tale of the conserved tails. Mol Microbiol 2007, 66:1051-1055.
• [58]Crozat E, Grainge I: FtsK DNA translocase: the fast motor that knows where it’s going. Chembiochem 2010, 11:2232-2243.
• [59]Bath J, Wu LJ, Errington J, Wang JC: Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 2000, 290:995-997.
• [60]Massey TH, Mercogliano CP, Yates J, Sherratt DJ, Lowe J: Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 2006, 23:457-469.
• [61]Pease PJ, Levy O, Cost GJ, Gore J, Ptacin JL, Sherratt D, Bustamante C, Cozzarelli NR: Sequence-directed DNA translocation by purified FtsK. Science 2005, 307:586-590.
• [62]Saleh OA, Bigot S, Barre FX, Allemand JF: Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking. Nat Struct Mol Biol 2005, 12:436-440.
• [63]Iyer LM, Makarova KS, Koonin EV, Aravind L: Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 2004, 32:5260-5279.
• [64]Bianco P, Kowalczykowski S: Translocation step size and mechanism of the RecBC DNA helicase. Nature 2000, 405:368-372.
• [65]Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA: Structural framework for DNA translocation via the viral portal protein. EMBO J 2007, 26:1984-1994.
• [66]Sun S, Kondabagil K, Draper B, Alam TI, Bowman VD, Zhang Z, Hegde S, Fokine A, Rossmann MG, Rao VB: The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 2008, 135:1251-1262.
• [67]Enemark EJ, Joshua-Tor L: On helicases and other motor proteins. Curr Opin Struct Biol 2008, 18:243-257.
• [68]Patel SS, Picha KM: Structure and function of hexameric helicases. Annu Rev Biochem 2000, 69:651-697.
• [69]Itsathitphaisarn O, Wing RA, Eliason WK, Wang J, Steitz TA: The hexameric helicase DnaB adopts a nonplanar conformation during translocation. Cell 2012, 151:267-277.
• [70]Hacker KJ, Johnson KA: A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding. Biochemistry 1997, 36:14080-14087.
• [71]Dittrich M, Schulten K: PcrA helicase, a prototype ATP-driven molecular motor. Structure 2006, 14:1345-1353.
• [72]Phelps C, Lee W, Jose D, von Hippel PH, Marcus AH: Single-molecule FRET and linear dichroism studies of DNA breathing and helicase binding at replication fork junctions. Proc Natl Acad Sci U S A 2013, 110:17320-17325.
• [73]Fei J, Ha T: Watching DNA breath one molecule at a time. Proc Natl Acad Sci U S A 2013, 110:17173-17174.
• [74]Lee W, Jose D, Phelps C, Marcus AH, von Hippel PH: A single-molecule view of the assembly pathway, subunit stoichiometry, and unwinding activity of the bacteriophage T4 primosome (helicase-primase) complex. Biochemistry 2013, 52:3157-3170.
• [75]Agirrezabala X, Martin-Benito J, Valle M, Gonzalez JM, Valencia A, Valpuesta JM, Carrascosa JL: Structure of the connector of bacteriophage T7 at 8A resolution: structural homologies of a basic component of a DNA translocating machinery. J Mol Biol 2005, 347:895-902.
• [76]Xing X, Bell CE: Crystal structures of Escherichia coli RecA in a compressed helical filament. J Mol Biol 2004, 342:1471-1485.
• [77]Pascal JM, Tsodikov OV, Hura GL, Song W, Cotner EA, Classen S, Tomkinson AE, Tainer JA, Ellenberger T: A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol Cell 2006, 24:279-291.
• [78]Bailey S, Eliason WK, Steitz TA: Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 2007, 318:459-463.
• [79]Enemark EJ, Joshua-Tor L: Mechanism of DNA translocation in a replicative hexameric helicase. Nature 2006, 442:270-275.
• [80]Gomis-Ruth FX, Coll M: Structure of TrwB, a gatekeeper in bacterial conjugation. Int J Biochem Cell Biol 2001, 33:839-843.
• [81]Burroughs AM, Iyer LM, Aravind L: Comparative genomics and evolutionary trajectories of viral atp dependent DNA-packaging systems. Genome Dyn 2007, 3:48-65.
• [82]Chelikani V, Ranjan T, Zade A, Shukla A, Kondabagil K: Genome segregation and packaging machinery in acanthamoeba polyphaga mimivirus is reminiscent of bacterial apparatus. J Virol 2014, 88:6069-6075.
• [83]Guo F, Liu Z, Vago F, Ren Y, Wu W, Wright ET, Serwer P, Jiang W: Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7. Proc Natl Acad Sci U S A 2013, 110:6811-6816.
• [84]Pearson RK, Fox MS: Effects of DNA heterologies on bacteriophage lambda packaging. Genetics 1988, 118:5-12.
• [85]Moll W-D, Guo P: Translocation of nicked but not gapped DNA by the packaging motor of bacteriophage phi29. J Mol Biol 2005, 351:100-107.
• [86]Aathavan K, Politzer AT, Kaplan A, Moffitt JR, Chemla YR, Grimes S, Jardine PJ, Anderson DL, Bustamante C: Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 2009, 461:669-673.
• [87]Oram M, Sabanayagam C, Black LW: Modulation of the packaging reaction of bacteriophage T4 terminase by DNA structure. J Mol Biol 2008, 381:61-72.
• [88]Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS, Rossmann MG: Structure of the bacteriophage phi29 DNA packaging motor. Nature 2000, 408:745-750.
• [89]Fang H, Jing P, Haque F, Guo P: Role of channel Lysines and “Push Through a One-way Valve” mechanism of viral DNA packaging motor. Biophys J 2012, 102:127-135.
• [90]Grimes S, Ma S, Gao J, Atz R, Jardine PJ: Role of phi29 connector channel loops in late-stage DNA packaging. J Mol Biol 2011, 410:50-59.
• [91]Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, Poliakov A, Potter CS, Carragher B, Johnson JE: The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 2006, 312:1791-1795.
• [92]Molineux IJ, Panja D: Popping the cork: mechanisms of phage genome ejection. Nat Rev Microbiol 2013, 11:194-204.
• [93]Petrov AS, Harvey SC: Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys J 2008, 95:497-502.
• [94]Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W: Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 2006, 439:612-616.
• [95]Tang JH, Olson N, Jardine PJ, Girimes S, Anderson DL, Baker TS: DNA poised for release in bacteriophage phi29. Structure 2008, 16:935-943.
• [96]Geng J, Fang H, Haque F, Zhang L, Guo P: Three reversible and controllable discrete steps of channel gating of a viral DNA packaging motor. Biomaterials 2011, 32:8234-8242.
• [97]Liu S, Chistol G, Hetherington CL, Tafoya S, Aathavan K, Schnitzbauer J, Grimes S, Jardine PJ, Bustamante C: A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills. Cell 2014, 157:702-713.
• [98]Ray K, Ma J, Oram M, Lakowicz JR, Black LW: Single-molecule and FRET fluorescence correlation spectroscopy analyses of phage DNA packaging: colocalization of packaged phage T4 DNA ends within the capsid. J Mol Biol 2010, 395:1102-1113.
• [99]Wendell D, Jing P, Geng J, Subramaniam V, Lee TJ, Montemagno C, Guo P: Translocation of double-stranded DNA through membrane-adapted phi29 motor protein nanopores. Nat Nanotechnol 2009, 4:765-772.
• [100]Li X, Yang X, Qi J, Seeman N: Antiparallel DNA double crossover molecules as components for nanoconstruction. J Am Chem Soc 1996, 118:6131-6140.
• [101]Shu D, Guo P: Only one pRNA hexamer but multiple copies of the DNA-packaging protein gp16 are needed for the motor to package bacterial virus phi29 genomic DNA. Virology 2003, 309(1):108-113.