De novo design of signal sequences to localize cargo to the 1,2-propanediol utilization microcompartment

Protein Science

Volumn 26, Issue 5, 2017, Pages 1086-1092

  Jakobson, Christopher M ^a,c   Slininger Lee, Marilyn F ^a,b   Tullman Ercek, Danielle ^a  

^a Northwestern University   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

bacterial microcompartments; nanoreactor; Salmonella; signal sequence

Indexed keywords

PROPYLENE GLYCOL; SIGNAL PEPTIDE; BACTERIAL PROTEIN; LEUCINE ZIPPER PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL MICROCOMPARTMENT; BASIC LEUCINE ZIPPER MOTIF; CARBOXY TERMINAL SEQUENCE; CELL ORGANELLE; FLUORESCENCE MICROSCOPY; NONHUMAN; PEPTIDE LIBRARY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; WESTERN BLOTTING; GENETICS; METABOLISM; PROTEIN ENGINEERING; PROTEIN TRANSPORT;

BACTERIAL PROTEINS; LEUCINE ZIPPERS; PROPYLENE GLYCOL; PROTEIN ENGINEERING; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM;

EID: 85018819393     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.3144     Document Type: Article

References (28)

1. Kim E, Tullman-Ercek D (2012) Engineering nanoscale protein compartments for synthetic organelles. Curr Opin Biotechnol 4:627–632.
2. Kerfeld CA, Erbilgin O (2015) Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol 23:22–34.
3. Chowdhury C, Sinha S, Chun S, Yeates TO, Bobik TA (2014) Diverse bacterial microcompartment organelles. Microbiol Mol Biol Rev 78:438–468.
4. Giessen TW, Silver PA (2015) Encapsulation as a strategy for the design of biological compartmentalization. J Mol Biol 428:916–927.
5. Chessher A, Breitling R, Takano E (2015) Bacterial microcompartments: biomaterials for synthetic biology-based compartmentalization strategies. ACS Biomater Sci Eng 1:345–351.
6. Fan C, Cheng S, Liu Y, Escobar CM, Crowley CS, Jefferson RE, Yeates TO, Bobik TA (2010) Short N-terminal sequences package proteins into bacterial microcompartments. Proc Natl Acad Sci USA 107:7509–7514.
7. Fan C, Bobik TA (2011) The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. J Bacteriol 193:5623–5628.
8. 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 USA 109:14995–15000.
9. Choudhary S, Quin MB, Sanders MA, Johnson ET, Schmidt-Dannert C (2012) Engineered protein nano-compartments for targeted enzyme localization. PloS One 7:e33342.
10. Bobik TA, Havemann GD, Busch RJ, Williams DS, Aldrich HC (1999) The propanediol utilization (pdu) operon of Salmonella enterica Serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B12-dependent 1,2-propanediol degradation. J Bacteriol 181:5967–5975.
11. Kofoid E, Rappleye C, Stojiljkovic I, Roth J (1999) The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. J Bacteriol 181:5317–5329.
12. Erbilgin O, McDonald KL, Kerfeld CA (2014) Characterization of a planctomycetal organelle: A novel bacterial microcompartment for the aerobic degradation of plant saccharides. Appl Environ Microbiol 80:2193–2205.
13. Sampson EM, Bobik TA (2008) Microcompartments for B12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J Bacteriol 190:2966–2971.
14. Cheng S, Bobik TA (2012) The PduQ enzyme is an alcohol dehydrogenase used to recycle NAD+ internally within the Pdu microcompartment of Salmonella enterica. PLoS ONE 10:e47144.
15. Huseby DL, Roth JR (2013) Evidence that a metabolic microcompartment contains and recycles private cofactor pools. J Bacteriol 195:2864–2879.
16. Jakobson CM, Slininger MF, Tullman-Ercek D, Mangan NM (2016) A systems-level model reveals that 1,2-propanediol utilization microcompartments enhance pathway flux through intermediate sequestration. bioRxiv 69542.
17. Lawrence AD, Frank S, Newnham S, Lee MJ, Brown IR, Xue W-F, Rowe ML, Mulvihill DP, Prentice MB, Howard MJ, Warren MJ (2014) Solution structure of a bacterial microcompartment targeting peptide and its application in the construction of an ethanol bioreactor. ACS Synth Biol 3:454–465.
18. Jakobson CM, Chen Y, Slininger MF, Valdivia E, Kim EY, Tullman-Ercek D (2016) Tuning the catalytic activity of subcellular nanoreactors. J Mol Biol 428:2989–2996.
19. Wagner HJ, Capitain CC, Richter K, Nessling M, Mampel J (2017) Engineering bacterial microcompartments with heterologous enzyme cargos. Eng Life Sci 17:36–46.
20. Aussignargues C, Paasch BC, Gonzalez-Esquer R, Erbilgin O, Kerfeld CA (2015) Bacterial microcompartment assembly: The key role of encapsulation peptides. Commun Integr Biol 8:e1039755.
21. Jakobson CM, Kim EY, Slininger MF, Chien A, Tullman-Ercek D (2015) Localization of proteins to the 1,2-propanediol utilization microcompartment by non-native signal sequences is mediated by a common hydrophobic motif. J Biol Chem 290:24519–24533.
22. Kim E, Tullman-Ercek D (2014) A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments. Biotechnol J 9:348–354.
23. Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3:e3647.
24. DeGrado WF, Regan L, Ho SP (1987) The design of a four-helix bundle protein. Cold Spring Harb Symp Quant Biol 52:521–526.
25. Regan L, DeGrado WF (1988) Characterization of a helical protein designed from first principles. Science 241:976–978.
26. Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27:946–950.
27. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
28. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207–234.