Engineering a reversible, high-affinity system for efficient protein purification based on the cohesin-dockerin interaction

Journal of Molecular Recognition

Volumn 22, Issue 2, 2009, Pages 91-98

  Karpol, Alon ^a   Kantorovich, Lia ^a   Demishten, Alik ^a   Barak, Yoav ^a   Morag, Ely ^a   Lamed, Raphael ^b   Bayer, Edward A ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Affinity chromatography; Calcium dependence; Cellulosome; Cohesin; Dockerin

Indexed keywords

BACTERIA (MICROORGANISMS); CLOSTRIDIUM THERMOCELLUM;

CALCIUM; CELL CYCLE PROTEIN; CELLULOSE; COHESINS; EDETIC ACID; NONHISTONE PROTEIN; RECOMBINANT PROTEIN; XYLAN 1,4 BETA XYLOSIDASE;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CLOSTRIDIUM THERMOCELLUM; ENZYMOLOGY; GENETIC ENGINEERING; GENETICS; GEOBACILLUS STEAROTHERMOPHILUS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACILLUS STEAROTHERMOPHILUS; CALCIUM; CELL CYCLE PROTEINS; CELLULOSE; CHROMATOGRAPHY, AFFINITY; CHROMOSOMAL PROTEINS, NON-HISTONE; CLOSTRIDIUM THERMOCELLUM; EDETIC ACID; GENETIC ENGINEERING; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; XYLOSIDASES;

EID: 63449108277     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.926     Document Type: Article

References (56)

1. Barak Y, Handelsman T, Nakar D, Mechaly A, Lamed R, Shoham Y, Bayer EA, 2005, Matching fusion-protein systems for affinity analysis of two interacting families of proteins: The cohesin-dockerin interaction. J. Mol. Recogit. 18:491-501.
2. Bayer EA, Morag E, Lamed R. 1994. The cellulosome - A treasure-trove for biotechnology. Trends Biotechnol. 12: 378-386.
3. Bayer EA, Chanzy H, Lamed R, Shoham Y 1998a, Cellulose, cellulases and cellulosomes. Curr. Opirt. Struct. Biol. 8: 548-557.
4. Bayer EA, Shimon LJW, Lamed R, Shoham Y. 1998b. Cellulosomes: structure and ultrastructure. J. Struct. Biol. 124: 221-234.
5. rd edition (latest update release 3.7, September 2001). http://link.springer.de/link/service/books/10125/index.htm Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds.) Springer-Verlag, New York,
6. Bayer EA, Belaich J-P, Shoham Y, Lamed R. 2004, The cellulosomes: Multi-enzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. 58: 521-554.
7. Bhat MK. 1998, Clostridium thermocellum cellulosome: Dissociation, isolation and characterisation of subunits and the potential biotech-nological implications. Recent Res. Dev. Biotechnol. Bioeng. 1: 59-84.
8. Bhat KM, Wood TM, 1992, The cellulase of the anaerobic bacterium Clostridium thermocellum: Isolation, dissociation, and rassociation of the cellulosome. Carbohydr. Res. 227: 293-300.
9. Bhat S, Goodenough PW, Bhat MK, Owen E. 1994. Isolation of four major subunits from Clostridium thermocellum cellulosome and their synergism in the hydrolysis of crystalline cellulose. Int. J. Biol. Macromol. 16: 335-342.
10. Carvalho AL, Dias FM, Prates JA, Nagy T, Gilbert HJ, Davies GJ, Ferreira LM, Romäo MJ, Fontes CM. 2003. Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex. Proc. Natl. Acad. Sci. USA 100: 13809-13814.
11. Carvalho AL, Dias FMV, Nagy T, Prates JAM, Proctor MR, Smith N, Bayer EA, Davies GJ, Ferreira LMA, Ramäo Ml, Fortes CMGA, Gilbert HJ. 2007, Evidence for a dual binding mode of dockerin modules to cohesins. Proc. Natl. Acad. Sci. USA 104: 3089-3094.
12. Caspi J, Irwin D, Lamed R, Shoham Y, Fierobe H-P, Wilson DB, Bayer EA, 2006. Thermobifida fusca family-6 cellulases as potential designer cellulosome components. Biocat. Biotransform. 24: 3-12.
13. Caspi J, Irwin D, Lamed R, Fierobe H-P, Wilson DB, Bayer EA. 2008, Conversion of noncellulosomal Thermobifida fusca free exogluca-nases into cellulosomal components: Comparative impact on cellulose-degrading activity, J, Biotechnol.
14. Choi SK, Ljungdahl LG. 1996, Dissociation of the cellulosome of Clostridium thermocellum in the presence of ethylenediaminetetraacetic acid occurs with the formation of truncated polypeptides. Biochemistry 35: 4897-4905.
15. Chong S, Mersha FB, Comb DG, Scott ME, Landry D, Vence LM, Perler FB, Benner J, Kucera RB, Hirvonen CA, Pelletier JJ, Paulus H, Xu MQ. 1997, Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene 192:271-281.
16. Craig SJ, Foong FC, Nordon R. 2006. Engineered proteins containing the cohesin and dockerin domains from Clostridium thermocellum provides a reversible, high affinity interaction for biotechnology applications, J. Biotechnol. 121: 165-173.
17. Cuatrecasas P, Wilchek M, Anfinsen CB. 1968. Selective enzyme purification by affinity chromatography. Proc. Natl. Acad. Sci. USA 61: 636-643.
18. Demain AL, Newcomb M, Wu JH. 2005. Cellulase, Clostridia, and ethanol. Microbiol. Mol. Biol. Rev. 69: 124-154.
19. Doi RH, Kosugi A, 2004, Cellulosomes: Plant-cell-wall-degrading enzyme complexes. Nat. Rev. Microbiol. 2: 541-551.
20. Fierobe H-P, fvlechaly A, Tardif C, Belaich A, Lamed R, Shoham Y, Belaich J-P, 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.
21. Fierobe H-P, Bayer EA, Tardif C, Czjzek M, Mechaly A, Belaich A, Lamed R, Shoham Y, Belaich J-P. 2002. Degradation of cellulose substrates by cellulosome chimeras: Substrate targeting versus proximity of enzyme components. J. Biol. Chem. 277: 49621-49630.
22. Fierobe H-P, Mingardon F, Mechaly A, Belaich A, Rincon MT, Lamed R, Tardif C, Belaich J-P, Bayer EA. 2005. Action of designer cellulosomes on homogeneous versus complex substrates: Controlled incorporation of three distinct enzymes into a defined tri-functional scaffoldin. J. Biol. Chem. 280: 16325-16334.
23. Flint HJ, Bayer EA, Lamed R, White BA, 2008, Polysaccharide utilization by gut bacteria: Potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6: 121-131.
24. Gaberc-Porekar V, Menart V. 2001. Perspectives of immobilized-metal affinity chromatography. J. Biochem. Biophys. Methods 49: 335-360.
25. L-protein reveals an unusual degree of internal homology. Mol. Microbiol. 8: 325-334.
26. Greenwood JM, Ong E, Gilkes NR, Warren RAJ, Miller RCJ, Kilburn DG. 1992, Cellulose-binding domains: Potential for purification of complex proteins. Protein Eng. 5: 361-365.
27. Haimovitz R, Barak Y, Morag E, Voronov-Goldman M, Lamed R, Bayer EA. 2008, Cohesin-dockerin microarray: Diverse specificities between two complementary families of interacting protein modules. Proteomics 8: 968-979.
28. Handelsman T, Barak Y, Nakar D, Mechaly A, Lamed R, Shoham Y, Bayer EA. 2004, Cohesin-dockerin interaction in cellulosome assembly: A single Asp-to-Asn mutation disrupts high-affinity cohesin-dockerin binding. FEBS Lett. 572: 195-200.
29. Hjelm H, Hjelm K, Sjoquist J. 1972. Protein A from Staphylococcus aureus. Its isolation by affinity chromatography and its use as an immunosorbent for isolation of immunoglobulins. FEBS Lett. 28: 73-76.
30. Jarvis M. 2003. Chemistry: Cellulose stacks up. Nature 426: 611-612.
31. Jindou S, Kajino T, Inagaki M, Karita S, Beguin P, Kimura T, Sakka K, Ohmiya K. 2004a, Interaction between a type-II dockerin domain and a type-II cohesin domain from Clostridium thermocellum cellulosome. Biosci. Biotechnol. Biochem. 68: 924-926,
32. Jindou S, Souda A, Karita S, Kajino T, Beguin P, Wu D, Inagaki M, Kimura T, Sakka K, Ohmiya K. 2004b. Cohesin/dockerin interactions within and between Clostridium josui and Clostridium thermocellum: Binding selectivity between cognate dockerin and cohesin domains and species specificity. J. Biol. Chem. 279: 9867-9874.
33. Karpol A, Barak Y, Lamed R, Shoham Y, Bayer EA. 2008. Functional asymmetry in cohesin binding belies inherent symmetry of the dockerin module: Insight into cellulosome assembly revealed by systematic mutagenesis. Biochem. J. 410: 331-338.
34. Lamed R, Setter E, Kenig R, Bayer EA. 1983. The cellulosome - a discrete cell surface organelle of Clostridium thermocellum which exhibits separate antigenic, cellulose-binding and various cellulolytic activities. Biotechnol. Bioeng. Symp. 13: 163-181.
35. Lapidot A, Mechaly A, Shoham Y, 1996. Overexpression and single-step purification of a thermostable xylanase from Bacillus stearothermophilus T-6. J. Biotechnol. 51: 259-264.
36. Levy I, Shoseyov O. 2002. Cellulose-binding domains: Biotechnological applications. Biotechnol. Adv. 20: 191-213.
37. Lytle B, Myers C, Kruus K, Wu JHD. 1996. Interactions of the CelS binding ligand with various receptor domains of the Clostridium thermocellum cellulosomal scaffolding protein, CipA. J. Bacterial. 178: 1200-1203.
38. Lytle B, Volkman BF, Westler WM, Wu JHD, 2000, Secondary structure and calcium-induced folding of the Clostridium thermocellum dockerin domain determined by NMR spectroscopy. Arch. Biochem. Biophys. 379: 237-244.
39. Lytle BL, Volkman BF, Westler WM, Heckman MP, Wu JHD. 2001. Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J. Mol. Biol. 307: 745-753.
40. Mechaly A, Yaron S, Lamed R, Fierobe H-P, Belaich A, Belaich J-P, Shoham Y, Bayer EA. 2000. Cohesin-dockerin recognition in cellulosome assembly: Experiment versus hypothesis. Proteins 39: 170-177.
41. Mechaly A, Fierobe H-P, Belaich A, Belaich J-P, Lamed R, Shoham Y, Bayer EA. 2001. Cohesin-dockerin interaction in cellulosome assembly: A single hydroxyl group of a dockerin domain distinguishes between non-recognition and high-affinity recognition. J. Biol. Chem. 276: 9883-9888; Erratum 19678.
42. Mingardon F, Chantai A, Tardif C, Bayer EA, Fierobe H-P. 2007. Exploration of new geometries in cellulosome-like chimeras. Appl. Environ. Microbiol. 73: 7138-7149.
43. Morag E, Yaron S, Lamed R, Kenig R, Shoham Y, Bayer EA. 1996. Dissociation of the cellulosome of Clostridium thermocellum under nondenaturing conditions. J. Biotechnol. 51: 235-242.
44. Nakar D, Handelsman T, Shoham Y, Fierobe H-P, Belaich JP, Morag E, Lamed R, Bayer EA. 2004. Pinpoint mapping of recognition residues on the cohesin surface by progressive homologue swapping. J. Biol. Chem. 279:42881-42888.
45. Nilsson J, Larsson M, Stahl S, Nygren PA, Uhlen M. 1996. Multiple affinity domains for the detection, purification and immobilization of recombinant proteins. J. Mol. Recognit. 9: 585-594.
46. Ofir K, Berdichevsky Y, Benhar I, Azriel-Rosenfeld R, Lamed R, Barak Y, Bayer EA, Morag E. 2005. Versatile protein microarray based on carbohydrate-binding modules, Proteomics 5: 1806-1814.
47. Pagès S, Belaich A, Belaich J-P, Morag E, Lamed R, Shoham Y, Bayer EA. 1997. Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: Prediction of specificity determinants of the dockerin domain. Proteins 29: 517-527.
48. Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G, 2007, The molecular architecture of protein-protein binding sites. Curr. Opin. Struct. Biol. 17: 67-76.
49. Salamitou S, Raynaud O, Lemaire M, Coughlan M, Béguin P, Aubert J-P. 1994. Recognition specificity of the duplicated segments present in Clostridium thermocellum endoglucanase CelD and in the cellulosome-integrating protein CipA. J. Bacterial. 176: 2822-2827.
50. Schwarz WH. 2001. The cellulosome and cellulose degradation by anaerobic bacteria. Appl. Microbiol. Biotechnol. 56: 634-649.
51. Smith DB, Johnson KS. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67: 31-40.
52. Terpe K, 2003. Overview of tag protein fusions: From molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 60: 523-533.
53. s (CelS), a major cellulosome component. J. Bacterial. 175: 1293-1302.
54. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite, Nature 450; 560-565,
55. Wu J, Filutowicz M. 1999. Hexahistidine (His6)-tag dependent protein dimerization: a cautionary tale. Acta Biochim. Pol. 46: 591-599.
56. Yaron S, Morag E, Bayer EA, Lamed R, Shoham Y. 1995, Expression, purification and subunit-binding properties of cohesins 2 and 3 of the Clostridium thermocellum cellulosome. FEBS Lett. 360:121-124.