Building spatial synthetic biology with compartments, scaffolds, and communities

Cold Spring Harbor Perspectives in Biology

Volumn 8, Issue 8, 2016, Pages

  Polka, Jessica K ^a,b   Hays, Stephanie G ^a,b   Silver, Pamela A ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

CELL FRACTIONATION; METABOLISM; SYNTHETIC BIOLOGY;

PROTEINS; SUBCELLULAR FRACTIONS; SYNTHETIC BIOLOGY;

EID: 84982851778     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a024018     Document Type: Article

References (133)

1. Agapakis CM, Niederholtmeyer H, Noche RR, Lieberman TD, Megason SG, Way JC, Silver PA. 2011. Towards a synthetic chloroplast. PLoS ONE 6: e18877.
2. Alfano EF, Lentz EM, Bellido D, Dus Santos MJ, Goldbaum FA, Wigdorovitz A, Bravo-Almonacid FF. 2015. Expression of the multimeric and highly immunogenic Brucella spp. lumazine synthase fused to bovine rotavirus VP8d as a scaffold for antigen production in tobacco chloroplasts. Front Plant Sci 6: 1170.
3. Avalos JL, Fink GR, Stephanopoulos G. 2013. Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat Biotechnol 31: 335-341.
4. Avila-Calderón ED, Araiza-Villanueva MG, Cancino-Diaz JC, López-Villegas EO, Sriranganathan N, Boyle SM, Contreras-Rodríguez A. 2015. Roles of bacterial membrane vesicles. Arch Microbiol 197: 1-10.
5. Baldi PC, Velikovsky CA, Braden BC, Giambartolomei GH, Fossati CA, Goldbaum FA. 2000. Structural, functional and immunological studies on a polymeric bacterial protein. Braz J Med Biol Res 33: 741-747.
6. Beck T, Tetter S, Kunzle M, Hilvert D. 2014. Construction of Matryoshka-type structures from supercharged protein nanocages. Angew Chem Int Ed Engl 54: 937-940.
7. Blobel G, Sabatini DD. 1971. Ribosome-membrane interaction in eukaryotic cells. In Biomembranes (ed. Manson LA), pp. 193-195. Springer, Berlin.
8. Bonacci W, Teng PK, Afonso B, Niederholtmeyer H, Grob P, Silver PA, Savage DF. 2012. Modularity of a carbon-fixing protein organelle. Proc Natl Acad Sci 109: 478-483.
9. Brenner K, Karig DK, Weiss R, Arnold FH. 2007. Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc Natl Acad Sci 104: 17300-17304.
10. Buehler DC, Marsden MD, Shen S, Toso DB, Wu X, Loo JA, Zhou ZH, Kickhoefer VA, Wender PA, Zack JA, et al. 2014. Bioengineered vaults: Self-assembling protein shell-lipophilic core nanoparticles for drug delivery. ACS Nano 8: 7723-7732.
11. Byrne JM, Coker VS, Moise S, Wincott PL, Vaughan DJ, Tuna F, Arenholz E, van der Laan G, Pattrick RAD, Lloyd JR, et al. 2013. Controlled cobalt doping in biogenic magnetite nanoparticles. J R Soc Interface R Soc 10: 20130134.
12. Cai F, Sutter M, Bernstein SL, Kinney JN, Kerfeld CA. 2014. Engineering bacterial microcompartment shells: Chimeric shell proteins and chimeric carboxysome shells. ACS Synth Biol 4: 444-453.
13. Cai F, Bernstein SL, Wilson SC, Kerfeld CA. 2016. Production and characterization of synthetic carboxysome shells with incorporated luminal proteins. Plant Physiol 170: 1868-1877.
14. Carpenter EJ, Montoya JP, Burns J, Mulholland MR, Subramaniam A, Capone DG. 1999. Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Mar Ecol Prog Ser 185: 273-283.
15. Chen DJ, Osterrieder N, Metzger SM, Buckles E, Doody AM, DeLisa MP, Putnam D. 2010. Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc Natl Acad Sci 107: 3099-3104.
16. Chen AH, Robinson-Mosher A, Savage DF, Silver PA, Polka JK. 2013. The bacterial carbon-fixing organelle is formed by shell envelopment of preassembled cargo. PloS ONE 8: e76127.
17. Chen AY, Deng Z, Billings AN, Seker UOS, Lu MY, Citorik RJ, Zakeri B, Lu TK. 2014. Synthesis and patterning of tunable multiscale materials with engineered cells. Nat Mater 13: 515-523.
18. Chen Y, Kim JK, Hirning AJ, Josic´ K, Bennett MR. 2015. Emergent genetic oscillations in a synthetic microbial consortium. Science 349: 986-989.
19. Choudhary S, Quin MB, Sanders MA, Johnson ET, Schmidt-Dannert C. 2012. Engineered protein nano-compartments for targeted enzyme localization. PLoS ONE 7: e33342.
20. Conrado RJ, Wu GC, Boock JT, Xu H, Chen SY, Lebar T, Turnšek J, Tomšič N, Avbelj M, Gaber R, et al. 2012. DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency. Nucleic Acids Res 40: 1879-1889.
21. Danese PN, Silhavy TJ. 1998. Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu Rev Genet 32: 59-94.
22. Delebecque CJ, Silver PA, Lindner AB. 2012. Designing and using RNA scaffolds to assemble proteins in vivo. Nat Protoc 7: 1797-1807.
23. Do Nascimento M, Dublan Mde L, Ortiz-Marquez JC, Curatti L. 2013. High lipid productivity of an Ankistrodesmus-Rhizobium artificial consortium. Bioresour Technol 146: 400-407.
24. Du ZQ, Wang JY. 2015. A novel lumazine synthase molecule from Brucella significantly promotes the immune-stimulation effects of antigenic protein. Genet Mol Res 14: 13084-13095.
25. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KLJ, Keasling JD. 2009. Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27: 753-759.
26. Eriksson HM, Wessman P, Ge C, Edwards K, Wieslander A. 2009. Massive formation of intracellular membrane vesicles in Escherichia coli by a monotopic membrane-bound lipid glycosyltransferase. J Biol Chem 284: 33904-33914.
27. Fan C, Bobik TA. 2011. The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu micro-compartment. J Bacteriol 193: 5623-5628.
28. Fan C, Cheng S, Sinha S, Bobik TA. 2012. Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments. Proc Natl Acad Sci 109: 14995-15000.
29. Fassel TA, Buchholz LA, Collins ML, Remsen CC. 1992. Localization of methanol dehydrogenase in two strains of methylotrophic bacteria detected by immunogold labeling. Appl Environ Microbiol 58: 2302-2307.
30. Fierobe HP, Mechaly A, Tardif C, Belaich A, Lamed R, Shoham Y, Belaich JP, Bayer EA. 2001. Design and production of active cellulosome chimeras selective incorporation of dockerin-containing enzymes into defined functional complexes. J Biol Chem 276: 21257-21261.
31. Frostl J, Overmann J. 1998. Physiology and tactic response of the phototrophic consortium “Chlorochromatium aggregatum.” Arch Microbiol 169: 129-135.
32. Fu J, Liu M, Liu Y, Woodbury NW, Yan H. 2012. Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures. J Am Chem Soc 134: 5516-5519.
33. Galloway JM, Bramble JP, Rawlings AE, Burnell G, Evans SD, Staniland SS. 2012. Biotemplated magnetic nanoparticle arrays. Small 8: 204-208.
34. Ginet N, Pardoux R, Adryanczyk G, Garcia D, Brutesco C, Pignol D. 2011. Single-step production of a recyclable nano-biocatalyst for organophosphate pesticides biodegradation using functionalized bacterial magnetosomes. PLoS ONE 6: e21442.
35. Goldsmith LE, Pupols M, Kickhoefer VA, Rome LH, Monbouquette HG. 2009. Utilization of a protein “shuttle” to load vault nanocapsules with gold probes and proteins. ACS Nano 3: 3175-3183.
36. Gong FC, Giddings TH, Meehl JB, Staehelin LA, Galbraith DW. 1996. Z-membranes: Artificial organelles for over-expressing recombinant integral membrane proteins. Proc Natl Acad Sci 93: 2219-2223.
37. Goodman BS, Derr ND, Reck-Peterson SL. 2012. Engineered, harnessed, and hijacked: Synthetic uses for cytoskeletal systems. Trends Cell Biol 22: 644-652.
38. Han M, Kickhoefer VA, Nemerow GR, Rome LH. 2011. Targeted vault nanoparticles engineered with an endosomolytic peptide deliver biomolecules to the cytoplasm. ACS Nano 5: 6128-6137.
39. Hansen AK, Moran NA. 2011. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci 108: 2849-2854.
40. Honda T, Tanaka T, Yoshino T. 2015. Stoichiometrically controlled immobilization of multiple enzymes on magnetic nanoparticles by the magnetosome display system for efficient cellulose hydrolysis. Biomacromolecules 16: 3863-3868.
41. Jorda J, Lopez D, Wheatley NM, Yeates TO. 2013. Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria. Protein Sci Publ Protein Soc 22: 179-195.
42. Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, MacKintosh FC, Hoogenraad CC. 2010a. Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol 20: 290-299.
43. Kapitein LC, Schlager MA, van der Zwan WA, Wulf PS, Keijzer N, Hoogenraad CC. 2010b. Probing intracellular motor protein activity using an inducible cargo trafficking assay. Biophys J 99: 2143-2152.
44. Kedersha NL, Rome LH. 1986. Isolation and characterization of a novel ribonucleoprotein particle: Large structures contain a single species of small RNA. J Cell Biol 103: 699-709.
45. Kickhoefer VA, Searles RP, Kedersha NL, Garber ME, Johnson DL, Rome LH. 1993. Vault ribonucleoprotein particles from rat and bullfrog contain a related small RNA that is transcribed by RNA polymerase III. J Biol Chem 268: 7868-7873.
46. Kickhoefer VA, Siva AC, Kedersha NL, Inman EM, Ruland C, Streuli M, Rome LH. 1999. The 193-Kd vault protein, Vparp, is a novel poly(Adp-ribose) polymerase. J Cell Biol 146: 917.
47. Kickhoefer VA, Garcia Y, Mikyas Y, Johansson E, Zhou JC, Raval-Fernandes S, Minoofar P, Zink JI, Dunn B, Stewart PL, et al. 2005. Engineering of vault nanocapsules with enzymatic and fluorescent properties. Proc Natl Acad Sci 102: 4348-4352.
48. Kinney JN, Salmeen A, Cai F, Kerfeld CA. 2012. Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J Biol Chem 287: 17729-17736.
49. Kolinko I, Lohße A, Borg S, Raschdorf O, Jogler C, Tu Q, Pósfai M, Tompa É, Plitzko JM, Brachmann A, et al. 2014. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat Nanotechnol 9: 193-197.
50. Komeili A, Li Z, Newman DK, Jensen GJ. 2006. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311: 242-245.
51. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325: 477-481.
52. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184.
53. Ladenstein R, Ritsert K, Huber R, Richter G, Bacher A. 1994. The lumazine synthase/riboflavin synthase complex of Bacillus subtilis. Eur J Biochem 223: 1007-1017.
54. Lassila JK, Bernstein SL, Kinney JN, Axen SD, Kerfeld CA. 2014. Assembly of robust bacterial microcompartment shells using building blocks from an organelle of unknown function. J Mol Biol 426: 2217-2228.
55. Lavieu G, Zheng H, Rothman JE. 2013. Stapled Golgi cisternae remain in place as cargo passes through the stack. eLife 2: e00558.
56. Lawrence AD, Frank S, Newnham S, Lee MJ, Brown IR, Xue WF, Rowe ML, Mulvihill DP, Prentice MB, Howard MJ, et al. 2014. Solution structure of a bacterial microcosmpartment targeting peptide and its application in the construction of an ethanol bioreactor. ACS Synth Biol 3: 454-465.
57. Lee LA, Hoewyk DV, Orr-Weaver TL. 2003. The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions. Genes Dev 17: 2979-2991.
58. Levskaya A, Weiner OD, Lim WA, Voigt CA. 2009. Spatiotemporal control of cell signalling using a light-switch-able protein interaction. Nature 461: 997-1001.
59. Li N, Cannon MC. 1998. Gas vesicle genes identified in Bacillus megaterium and functional expression in Escherichia coli. J Bacteriol 180: 2450-2458.
60. Lin MT, Occhialini A, Andralojc PJ, Devonshire J, Hines KM, Parry MAJ, Hanson MR. 2014a. b-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts. Plant J Cell Mol Biol 79: 1-12.
61. Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR. 2014b. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513: 547-550.
62. Lingwood D, Schuck S, Ferguson C, Gerl MJ, Simons K. 2009. Generation of cubic membranes by controlled homotypic interaction of membrane proteins in the endoplasmic reticulum. J Biol Chem 284: 12041-12048.
63. Long BM, Badger MR, Whitney SM, Price GD. 2007. Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282: 29323-29335.
64. Long BM, Tucker L, Badger MR, Price GD. 2010. Functional cyanobacterial b-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153: 285-293.
65. Marcus ME, Leonard JN. 2013. FedExosomes: Engineering therapeutic biological nanoparticles that truly deliver. Pharm Basel Switz 6: 659-680.
66. McGrath JM, Long SP. 2014. Can the cyanobacterial carbonconcentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164: 2247-2261.
67. McHugh CA, Fontana J, Nemecek D, Cheng N, Aksyuk AA, Heymann JB, Winkler DC, Lam AS, Wall JS, Steven AC, et al. 2014. A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. EMBO J 33: 1896-1911.
68. Meining W, Mortl S, Fischer M, Cushman M, Bacher A, Ladenstein R. 2000. The atomic structure of pentameric lumazine synthase from Saccharomyces cerevisiae at 1.85 ˚ resolution reveals the binding mode of a phosphonate intermediate analogue. J Mol Biol 299: 181-197.
69. Minty JJ, Singer ME, Scholz SA, Bae CH, Ahn JH, Foster CE, Liao JC, Lin XN. 2013. Design and characterization of synthetic fungal-bacterial consortia for direct production of isobutanol from cellulosic biomass. Proc Natl Acad Sci 110: 14592-14597.
70. Moon H, Lee J, Min J, Kang S. 2014. Developing genetically engineered encapsulin protein cage nanoparticles as a targeted delivery nanoplatform. Biomacromolecules 15: 3794-3801.
71. Muller MJI, Neugeboren BI, Nelson DR, Murray AW. 2014. Genetic drift opposes mutualism during spatial population expansion. Proc Natl Acad Sci 111: 1037-1042.
72. Namba K, Hagiwara K, Tanaka H, Nakaishi Y, Chong KT, Yamashita E, Armah GE, Ono Y, Ishino Y, Omura T, et al. 2005. Expression and molecular characterization of spherical particles derived from the genome of the hyperthermophilic euryarchaeote Pyrococcus furiosus. J Biochem (Tokyo) 138: 193-199.
73. Naughton LM, Mandel MJ. 2012. Colonization of Euprymna scolopes squid by Vibrio fischeri. J Vis Exp 2012: e3758.
74. Nguyen PQ, Botyanszki Z, Tay PKR, Joshi NS. 2014. Programmable biofilm-based materials from engineered curli nanofibres. Nat Commun 5: 4945.
75. Niedziela-Majka A, Rymarczyk G, Kochman M, Ozyhar A. 1998. GST-Induced dimerization of DNA-binding domains alters characteristics of their interaction with DNA. Protein Expr Purif 14: 208-220.
76. Nishida K, Silver PA. 2012. Induction of biogenic magnetization and redox control by a component of the target of rapamycin complex 1 signaling pathway. PLoS Biol 10: e1001269.
77. Ortiz-Marquez JCF, Do Nascimento M, Dublan Mde A, Curatti L. 2012. Association with an ammonium-excreting bacterium allows diazotrophic culture of oil-rich eukaryotic microalgae. Appl Environ Microbiol 78: 2345-2352.
78. Overmann J. 2010. The phototrophic consortium “Chlorochromatium aggregatum”—A model for bacterial heterologous multicellularity. Adv Exp Med Biol 675: 15-29.
79. Parker MW, Bello ML, Federici G. 1990. Crystallization of glutathione S-transferase from human placenta. J Mol Biol 213: 221-222.
80. Parsons JB, Dinesh SD, Deery E, Leech HK, Brindley AA, Heldt D, Frank S, Smales CM, Lunsdorf H, Rambach A, et al. 2008. Biochemical and structural insights into bacterial organelle form and biogenesis. J Biol Chem 283: 14366-14375.
81. Parsons JB, Frank S, Bhella D, Liang M, Prentice MB, Mulvihill DP, Warren MJ. 2010. Synthesis of empty bacterial microcompartments, directed organelle protein incorporation, and evidence of filament-associated organelle movement. Mol Cell 38: 305-315.
82. Pasotti L, Zucca S, Lupotto M, Cusella De Angelis MG, Magni P. 2011. Characterization of a synthetic bacterial self-destruction device for programmed cell death and for recombinant proteins release. J Biol Eng 5: 8.
83. Pfeifer F. 2012. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol 10: 705-715.
84. Poderycki MJ, Kickhoefer VA, Kaddis CS, Raval-Fernandes S, Johansson E, Zink JI, Loo JA, Rome LH. 2006. The vault exterior shell is a dynamic structure that allows incorporation of vault-associated proteins into its interior. Biochemistry (Mosc) 45: 12184-12193.
85. Polka JK, Silver PA. 2016. A tunable protein piston that breaks membranes to release encapsulated cargo. ACS Synth Biol doi: 10.1021/acssynbio.5b00237.
86. Pollithy A, Romer T, Lang C, Muller FD, Helma J, Leonhardt H, Rothbauer U, Schuler D. 2011. Magnetosome expression of functional camelid antibody fragments (nanobodies) in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 77: 6165-6171.
87. Pond FR, Gibson I, Lalucat J, Quackenbush RL. 1989. R-body-producing bacteria. Microbiol Rev 53: 25-67.
88. 2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77: 357-379.
89. Rahmanpour R, Bugg TDH. 2013. Assembly in vitro of Rhodococcus jostii RHA1 encapsulin and peroxidase DypB to form a nanocompartment. FEBS J 280: 2097-2104.
90. Rapaport D. 2003. Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep 4: 948-952.
91. Rice KC, Bayles KW. 2008. Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72: 85-109.
92. Rivera VM, Wang X, Wardwell S, Courage NL, Volchuk A, Keenan T, Holt DA, Gilman M, Orci L, Cerasoli F, et al. 2000. Regulation of protein secretion through controlled aggregation in the endoplasmic reticulum. Science 287: 826-830.
93. Rizzo R, Parashuraman S, Mirabelli P, Puri C, Lucocq J, Luini A. 2013. The dynamics of engineered resident proteins in the mammalian Golgi complex relies on cisternal maturation. J Cell Biol 201: 1027-1036.
94. Rollins CT, Rivera VM, Woolfson DN, Keenan T, Hatada M, Adams SE, Andrade LJ, Yaeger D, van Schravendijk MR, Holt DA, et al. 2000. A ligand-reversible dimerization system for controlling protein-protein interactions. Proc Natl Acad Sci 97: 7096-7101.
95. Roth MS. 2014. The engine of the reef: Photobiology of the coral-algal symbiosis. Front Microbiol 5: 422.
96. Sargent F, Davidson FA, Kelly CL, Binny R, Christodoulides N, Gibson D, Johansson E, Kozyrska K, Lado LL, MacCallum J, et al. 2013. A synthetic system for expression of components of a bacterial microcompartment. Microbiology 159: 2427-2436.
97. Savage DF, Afonso B, Chen AH, Silver PA. 2010. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327: 1258-1261.
98. Schmid MF, Paredes AM, Khant HA, Soyer F, Aldrich HC, Chiu W, Shively JM. 2006. Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography. J Mol Biol 364: 526-535.
99. Schouten S, Villareal TA, Hopmans EC, Mets A, Swanson KM, Sinninghe Damsté JS. 2013. Endosymbiotic heterocystous cyanobacteria synthesize different heterocyst glycolipids than free-living heterocystous cyanobacteria. Phytochemistry 85: 115-121.
100. Seebeck FP, Woycechowsky KJ, Zhuang W, Rabe JP, Hilvert D. 2006. A simple tagging system for protein encapsulation. J Am Chem Soc 128: 4516-4517.
101. Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS, Schaffer DV, Conolly SM. 2014. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol 9: 311-316.
102. Shou W, Ram S, Vilar JMG. 2007. Synthetic cooperation in engineered yeast populations. Proc Natl Acad Sci 104: 1877-1882.
103. Silver PA, Keegan LP, Ptashne M. 1984. Amino terminus of the yeast GAL4 gene product is sufficient for nuclear localization. Proc Natl Acad Sci 81: 5951-5955.
104. Smith S. 1994. The animal fatty acid synthase: One gene, one polypeptide, seven enzymes. FASEB J 8: 1248-1259.
105. Snapp EL, Hegde RS, Francolini M, Lombardo F, Colombo S, Pedrazzini E, Borgese N, Lippincott-Schwartz J. 2003. Formation of stacked ER cisternae by low affinity protein interactions. J Cell Biol 163: 257-269.
106. Song Y, Kang YJ, Jung H, Kim H, Kang S, Cho H. 2015. Lumazine synthase protein nanoparticle-Gd(III)-DOTA conjugate as a T1 contrast agent for high-field MRI. Sci Rep 5: 15656.
107. Stal LJ, van Gemerden H, Krumbein WE. 1985. Structure and development of a benthic marine microbial mat. FEMS Microbiol Lett 31: 111-125.
108. Stephen AG, Raval-Fernandes S, Huynh T, Torres M, Kickhoefer VA, Rome LH. 2001. Assembly of vault-like particles in insect cells expressing only the major vault protein. J Biol Chem 276: 23217-23220.
109. Straight PD, Fischbach MA, Walsh CT, Rudner DZ, Kolter R. 2007. A singular enzymatic megacomplex from Bacillus subtilis. Proc Natl Acad Sci 104: 305-310.
110. Stuart ES, Morshed F, Sremac M, DasSarma S. 2001. Antigen presentation using novel particulate organelles from halophilic archaea. J Biotechnol 88: 119-128.
111. Sun F, Zhang WB, Mahdavi A, Arnold FH, Tirrell DA. 2014. Synthesis of bioactive protein hydrogels by genetically encoded SpyTag-SpyCatcher chemistry. Proc Natl Acad Sci 111: 11269-11274.
112. Sundararajan A, Ju LK. 2006. Use of cyanobacterial gas vesicles as oxygen carriers in cell culture. Cytotechnology 52: 139-149.
113. Sutter M, Boehringer D, Gutmann S, Günther S, Prangishvili D, Loessner MJ, Stetter KO, Weber-Ban E, Ban N. 2008. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15: 939-947.
114. Tamura A, Fukutani Y, Takami T, Fujii M, Nakaguchi Y, Murakami Y, Noguchi K, Yohda M, Odaka M. 2015. Packaging guest proteins into the encapsulin nanocompartment from Rhodococcus erythropolis N771. Biotechnol Bioeng 112: 13-20.
115. Tian L, Okita TW. 2014. mRNA-based protein targeting to the endoplasmic reticulum and chloroplasts in plant cells. Curr Opin Plant Biol 22C: 77-85.
116. Toledo MAS, Janissen R, Favaro MTP, Cotta MA, Monteiro GA, Prazeres DMF, Souza AP, Azzoni AR. 2012. Development of a recombinant fusion protein based on the dynein light chain LC8 for non-viral gene delivery. J Control Release 159: 222-231.
117. Uratani Y, Hoshino T. 1984. Pyocin R1 inhibits active transport in Pseudomonas aeruginosa and depolarizes membrane potential. J Bacteriol 157: 632-636.
118. Voges MJ, Silver PA, Way JC, Mattozzi MD. 2013. Targeting a heterologous protein to multiple plant organelles via rationally designed 50 mRNA tags. J Biol Eng 7: 20.
119. Walser PJ, Ariotti N, Howes M, Ferguson C, Webb R, Schwudke D, Leneva N, Cho KJ, Cooper L, Rae J, et al. 2012. Constitutive formation of caveolae in a bacterium. Cell 150: 752-763.
120. Wang M, Abad D, Kickhoefer VA, Rome LH, Mahendra S. 2015. Vault nanoparticles packaged with enzymes as an efficient pollutant biodegradation technology. ACS Nano 9: 10931-10940.
121. Washida H, Sugino A, Kaneko S, Crofts N, Sakulsingharoj C, Kim D, Choi SB, Hamada S, Ogawa M, Wang C, et al. 2009. Identification of cis-localization elements of the maize 10-kDa d-zein and their use in targeting RNAs to specific cortical endoplasmic reticulum subdomains. Plant J Cell Mol Biol 60: 146-155.
122. Weber W, Baba MDE, Fussenegger M. 2007. Synthetic ecosystems based on airborne interand intrakingdom communication. Proc Natl Acad Sci 104: 10435-10440.
123. Williams SR, Gebhart D, Martin DW, Scholl D. 2008. Retargeting R-type pyocins to generate novel bactericidal protein complexes. Appl Environ Microbiol 74: 3868-3876.
124. Wintermute EH, Silver PA. 2010. Emergent cooperation in microbial metabolism. Mol Syst Biol 6: 407.
125. Wörsdörfer B, Pianowski Z, Hilvert D. 2011a. Efficient in vitro encapsulation of protein cargo by an engineered protein container. J Am Chem Soc 134: 909-911.
126. Wörsdörfer B, Woycechowsky KJ, Hilvert D. 2011b. Directed evolution of a protein container. Science 331: 589-592.
127. Yamamoto A, Masaki R, Tashiro Y. 1996. Formation of crystalloid endoplasmic reticulum in COS cells upon overexpression of microsomal aldehyde dehydrogenase by cDNA transfection. J Cell Sci 109: 1727-1738.
128. Yang J, Kickhoefer VA, Ng BC, Gopal A, Bentolila LA, John S, Tolbert SH, Rome LH. 2010. Vaults are dynamically unconstrained cytoplasmic nanoparticles capable of half vault exchange. ACS Nano 4: 7229-7240.
129. Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U, Moy VT, Howarth M. 2012. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc Natl Acad Sci 109: E690-E697.
130. Zhang X, Meining W, Fischer M, Bacher A, Ladenstein R. 2001. X-ray structure analysis and crystallographic refinement of lumazine synthase from the hyperthermophile Aquifex aeolicus at 1.6 ˚ resolution: Determinants of thermostability revealed from structural comparisons. J Mol Biol 306: 1099-1114.
131. Zhang X, Konarev PV, Petoukhov MV, Svergun DI, Xing L, Cheng RH, Haase I, Fischer M, Bacher A, Ladenstein R, et al. 2006a. Multiple assembly states of lumazine synthase: A model relating catalytic function and molecular assembly. J Mol Biol 362: 753-770.
132. Zhang Y, Li SZ, Li J, Pan X, Cahoon RE, Jaworski JG, Wang X, Jez JM, Chen F, Yu O. 2006b. Using unnatural protein fusions to engineer resveratrol biosynthesis in yeast and mammalian cells. J Am Chem Soc 128: 13030-13031.
133. Zhu Y, Jiang J, Said-Sadier N, Boxx G, Champion C, Tetlow A, Kickhoefer VA, Rome LH, Ojcius DM, Kelly KA. 2014. Activation of the NLRP3 inflammasome by vault nanoparticles expressing a chlamydial epitope. Vaccine 33: 298-306.