Pseudo-T-even Bacteriophage RB49 Encodes CocO, a Cochaperonin for GroEL, Which Can Substitute for Escherichia coli's GroES and Bacteriophage T4's Gp31

Abstract

Bacteriophage T4-encoded Gp31 is a functional ortholog of the Escherichia coli GroES cochaperonin protein. Both of these proteins form transient, productive complexes with the GroEL chaperonin, required for protein folding and other related functions in the cell. However, Gp31 is specifically required, in conjunction with GroEL, for the correct folding of Gp23, the major capsid protein of T4. To better understand the interaction between GroEL and its cochaperonin cognates, we determined whether the so-called “pseudo-T-even bacteriophages” are dependent on host GroEL function and whether they also encode their own cochaperonin. Here, we report the isolation of an allele-specific mutation of bacteriophage RB49, called ε22, which permits growth on the E. coli groEL44 mutant but not on the isogenic wild type host. RB49 ε22 was used in marker rescue experiments to identify the corresponding wild type gene, which we have named cocO(cochaperonin cognate). CocO has extremely limited identity to GroES but is 34% identical and 55% similar at the protein sequence level to T4 Gp31, sharing all of the structural features of Gp31 that distinguish it from GroES. CocO can substitute for Gp31 in T4 growth and also suppresses the temperature-sensitive phenotype of the E. coli groES42 mutant. CocO's predicted mobile loop is one residue longer than that of Gp31, with the ε22 mutation resulting in a Q36R substitution in this extra residue. Both the CocO wild type and ε22 proteins have been purified and shownin vitro to assist GroEL in the refolding of denatured citrate synthase. Bacteriophage T4-encoded Gp31 is a functional ortholog of the Escherichia coli GroES cochaperonin protein. Both of these proteins form transient, productive complexes with the GroEL chaperonin, required for protein folding and other related functions in the cell. However, Gp31 is specifically required, in conjunction with GroEL, for the correct folding of Gp23, the major capsid protein of T4. To better understand the interaction between GroEL and its cochaperonin cognates, we determined whether the so-called “pseudo-T-even bacteriophages” are dependent on host GroEL function and whether they also encode their own cochaperonin. Here, we report the isolation of an allele-specific mutation of bacteriophage RB49, called ε22, which permits growth on the E. coli groEL44 mutant but not on the isogenic wild type host. RB49 ε22 was used in marker rescue experiments to identify the corresponding wild type gene, which we have named cocO(cochaperonin cognate). CocO has extremely limited identity to GroES but is 34% identical and 55% similar at the protein sequence level to T4 Gp31, sharing all of the structural features of Gp31 that distinguish it from GroES. CocO can substitute for Gp31 in T4 growth and also suppresses the temperature-sensitive phenotype of the E. coli groES42 mutant. CocO's predicted mobile loop is one residue longer than that of Gp31, with the ε22 mutation resulting in a Q36R substitution in this extra residue. Both the CocO wild type and ε22 proteins have been purified and shownin vitro to assist GroEL in the refolding of denatured citrate synthase. tetracycline-resistant high pressure liquid chromatography The Escherichia coli GroEL and GroES proteins form a complex, known as the GroE chaperone machine, that is crucial to the functions related to protein folding (reviewed in Refs. 1Georgopoulos C. Welch W.J. Annu. Rev. Cell Biol. 1993; 9: 601-635Crossref PubMed Scopus (1000) Google Scholar, 2Lorimer G. Nature. 1997; 388: 720-723Crossref PubMed Scopus (79) Google Scholar, 3Bukau B. Horwich A.L. Cell. 1998; 92: 351-366Abstract Full Text Full Text PDF PubMed Scopus (2423) Google Scholar, 4Sigler P.B. Xu Z. Rye H.S. Burston S.G. Fenton W.A. Horwich A.L. Annu. Rev. Biochem. 1998; 67: 581-608Crossref PubMed Scopus (476) Google Scholar). The GroEL and GroES proteins are often referred to as chaperonin and cochaperonin, respectively (5Ellis R.J. van der Vies S.M. Annu. Rev. Biochem. 1991; 60: 321-347Crossref PubMed Google Scholar). Both GroES and GroEL have been shown to be essential for E. coli viability under all conditions tested (6Fayet O. Ziegelhoffer T. Georgopoulos C. J. Bacteriol. 1989; 171: 1379-1385Crossref PubMed Scopus (542) Google Scholar). Extensive structural analysis has revealed that both proteins are organized into rings with a 7-fold rotational axis (7Braig K. Otwinowski Z. Hegde R. Boisvert D.C. Joachimiak A. Horwich A.L. Sigler P.B. Nature. 1994; 371: 578-586Crossref PubMed Scopus (1191) Google Scholar, 8Hunt J.F. Weaver A.J. Landry S.J. Gierasch L. Deisenhofer J. Nature. 1996; 379: 37-45Crossref PubMed Scopus (402) Google Scholar). GroEL is arranged in two head-to-head stacked rings of seven subunits in whose central cavities various substrate proteins can bind, primarily through hydrophobic interactions (Ref. 9Fenton W.A. Kashi Y. Furtak K. Horwich A.L. Nature. 1994; 371: 614-619Crossref PubMed Scopus (574) Google Scholar; reviewed in Refs. 2Lorimer G. Nature. 1997; 388: 720-723Crossref PubMed Scopus (79) Google Scholarand 4Sigler P.B. Xu Z. Rye H.S. Burston S.G. Fenton W.A. Horwich A.L. Annu. Rev. Biochem. 1998; 67: 581-608Crossref PubMed Scopus (476) Google Scholar). GroES is a heptameric ring of 10.5-kDa subunits from which mobile loops extend and interact with GroEL (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google Scholar, 11Xu Z. Horwich A.L. Sigler P.B. Nature. 1997; 388: 741-750Crossref PubMed Scopus (1038) Google Scholar). A typical GroEL substrate is first captured in either of the GroEL central cavities, and the subsequent binding of ATP and GroES to the same ring (referred to as the cis ring) results in the formation of a dome-like structure over the substrate, which is now released into the GroEL cis cavity. The subsequent binding of ATP and substrate (and potentially GroES as well) in thetrans GroEL ring results in the release of GroES from thecis ring (4Sigler P.B. Xu Z. Rye H.S. Burston S.G. Fenton W.A. Horwich A.L. Annu. Rev. Biochem. 1998; 67: 581-608Crossref PubMed Scopus (476) Google Scholar, 12Rye H.S. Roseman A.M. Chen S. Furtak K. Fenton W.A. Saibil H.R. Howich A.L. Cell. 1999; 97: 325-328Abstract Full Text Full Text PDF PubMed Scopus (285) Google Scholar). If the substrate in the cisring is properly folded, or in a form that no longer binds GroEL, it is released into the medium, and this GroEL ring will become the newtrans ring in a new GroEL folding cycle. Houry et al. (13Houry W.A. Frishman D. Eckerskorn C. Lottspeich F. Hartl F.U. Nature. 1999; 402: 147-154Crossref PubMed Scopus (434) Google Scholar) have shown, by using coimmunoprecipitation experiments, that ∼10% of E. coli's polypeptides bind transiently to GroEL. Some of these proteins are encoded by essential genes, in agreement with the genetic observation that the groES andgroEL genes are both essential for E. coli growth (6Fayet O. Ziegelhoffer T. Georgopoulos C. J. Bacteriol. 1989; 171: 1379-1385Crossref PubMed Scopus (542) Google Scholar). The bacteriophage T4, which is dependent on the host GroEL function for folding of its major capsid protein, Gp23, encodes its own GroES ortholog, termed Gp31. There is very little sequence similarity between GroES and Gp31 (14Keppel F. Lipinska B. Ang D. Georgopoulos C. Gene ( Amst. ). 1990; 90: 19-25Crossref Scopus (27) Google Scholar, 15Nivinskas R. Black L.W. Gene ( Amst. ). 1988; 73: 251-257Crossref PubMed Scopus (18) Google Scholar), although there is a limited conservation in certain regions, most notably the mobile loop that becomes immobilized upon binding to GroEL (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google Scholar, 16Koonin E.V. van der Vies S. Trends Biochem. Sci. 1995; 20: 14-15Abstract Full Text PDF PubMed Scopus (25) Google Scholar, 17Richardson A. Landry S.J. Georgopoulos C. Trends Biochem. Sci. 1998; 23: 138-143Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar). The functional importance of the mobile loop was first shown by sequencing mutations in groESthat blocked bacteriophage λ growth (λ requires both GroEL and GroES host functions for growth (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google Scholar, 18Tilly K. Murialdo H. Georgopoulos C. Proc. Natl. Acad. Sci. U. S. A. 1981; 78: 1629-1633Crossref PubMed Scopus (109) Google Scholar)). Similarly, T4 gene31 mutations, which allow T4 to propagate on coli also the Gp31 mobile loop (14Keppel F. Lipinska B. Ang D. Georgopoulos C. Gene ( Amst. ). 1990; 90: 19-25Crossref Scopus (27) Google S.J. A. Georgopoulos C. van der Vies S. Proc. Natl. Acad. Sci. U. S. A. 1996; PubMed Scopus Google Scholar, A. van der Vies S. F. A. Landry S.J. Georgopoulos C. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). of GroES and Gp31 have shown that Gp31 can substitute for the is not Gp31 can the temperature-sensitive phenotype of the E. coli groES42 mutant and can in the in of various but GroES is to substitute for Gp31 in T4 bacteriophage der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google Scholar). not be it is that Gp31 as a ortholog of GroES that specifically the is the by the under the of the (reviewed in Refs. 3Bukau B. Horwich A.L. Cell. 1998; 92: 351-366Abstract Full Text Full Text PDF PubMed Scopus (2423) Google and 4Sigler P.B. Xu Z. Rye H.S. Burston S.G. Fenton W.A. Horwich A.L. Annu. Rev. Biochem. 1998; 67: 581-608Crossref PubMed Scopus (476) Google Scholar). that the in the formation of a under the of the Gp31 to a longer mobile the of the loop in and of a which into the of GroES J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar, A. Georgopoulos C. 1999; Google Scholar). a of with have been to their sequence with the T4, and F. F. J. 1994; PubMed Scopus Google Scholar). The of these are very related to at the sequence However, a of have that and these have been termed “pseudo-T-even bacteriophages” C. F. F. J. Biol. 1997; PubMed Scopus Google Scholar). the of the to whether they a a of either GroES or Gp31. Here, we report on the bacteriophage RB49 which we have named The various and used in this are in and or S. J. Biol. Scopus Google Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google and Gene ( Amst. ). 1995; PubMed Scopus Google J. Fayet O. L. Georgopoulos C. J. Bacteriol. 1993; PubMed Google J. Fayet O. L. Georgopoulos C. J. Bacteriol. 1993; PubMed Google J. Fayet O. L. Georgopoulos C. J. Bacteriol. 1993; PubMed Google J. Fayet O. L. Georgopoulos C. J. Bacteriol. 1993; PubMed Google S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google groES42 S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google type mutation in A. E. E. R. A. on and of mutation in A. E. E. R. A. on and of on E. coli C. Biol. PubMed Scopus Google type C. F. F. J. Biol. 1997; PubMed Scopus Google mutation RB49 on E. coli RB49 Gene ( Amst. ). 1995; PubMed Scopus Google with Gene ( Amst. ). 1995; PubMed Scopus Google Gene ( Amst. ). 1995; PubMed Scopus Google L.M. D. J. J. Bacteriol. 1995; PubMed Scopus Google Scholar, D. from in a new in of of of or on of of of of was used for with and to the at of or was used for of bacteriophage and for bacteriophage of an RB49 was by T. J. A Scholar), by on a The bacteriophage was for in by two in of The bacteriophage was with by T. J. A Scholar). The was using and of purified from an The to the of Gene ( Amst. ). 1995; PubMed Scopus Google Scholar) in which by was used to the which been The was into and on at at a with the bacteriophage at a of of The at was to and the of all To for wild type of the was with of a and of and an The at to allow E. coli groES42 with either the or is a that the which has an mutation in The was from a T4 into the L.M. D. J. J. Bacteriol. 1995; PubMed Scopus Google for at two from in of of of and the on The at or and was using the and the on a sequencing The used for sequencing and are as and used to the from wild type RB49 The was into the and of the under the of the as Gene ( Amst. ). 1995; PubMed Scopus Google Scholar). The resulting was named The was in the same using RB49 as resulting in with in at of CocO was with for by and in and The was at and in A and by two through a at The are from the used for Gp31 der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google Scholar). of the by at by for at the was by a of The was by a CocO in the CocO was into and to a which binds of its CocO in the a CocO was and into and an to which a to was CocO at into by on a CocO at an of of the mutant protein was its from using the for the wild type protein. The for of citrate has been 1991; PubMed Scopus Google Scholar). citrate at was denatured in and for at citrate was to into a and various of the at for as under The refolding at in a of and citrate was The was by the in at to the of and the of Both and experiments with the bacteriophage RB49 that this bacteriophage has no gene31 with sequence similarity to the T4 not we determined RB49 growth is dependent on the host GroEL and GroES bacteriophage T4, bacteriophage RB49 is dependent on coli GroEL function for of its but is not dependent on GroES that wild type RB49, which with an of on the wild type not form on either the E. coli groEL44 or mutant but propagate on the bacteriophage T4 it that RB49 is to of this of various on various at and wild of the was in on of the bacteriophage and of was on The at or and the The of of bacteriophage on a host is shown by either a an of of or a an of of than in a new of the was in on of the bacteriophage and of was on The at or and the The of of bacteriophage on a host is shown by either a an of of or a an of of than with the isolation of the bacteriophage mutant A. Georgopoulos C. 1999; Google Scholar, C. Biol. PubMed Scopus Google Scholar), of RB49 can be at a of on groEL44 mutant RB49 ε22, wild on the E. coli groEL44 mutant host at was that RB49 ε22 form on either wild at it form on these same at we the T4 mutant T4 in which was as a on groEL44 C. Biol. PubMed Scopus Google Scholar). analysis has shown that the T4 mutation results in an substitution in the of the mobile loop of Gp31 (14Keppel F. Lipinska B. Ang D. Georgopoulos C. Gene ( Amst. ). 1990; 90: 19-25Crossref Scopus (27) Google Scholar, S.J. A. Georgopoulos C. van der Vies S. Proc. Natl. Acad. Sci. U. S. A. 1996; PubMed Scopus Google Scholar, A. Georgopoulos C. 1999; Google Scholar). for a Gp31 in RB49 by that the T4 the ε22 mutation bacteriophage RB49 ε22 growth on the E. coli wild type host at a both the E. coli and groES wild type genes not the ε22 mutation not results shown that of groES also not the der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google of Gp31 and CocO proteins to specifically the growth of bacteriophage or wild type E. coli was with either the T4 or the the to for a of the conditions and of The experiments at The that mutations to in a new The wild type E. coli was with either the T4 or the the to for a of the conditions and of The experiments at The that mutations to To identify the RB49 the ε22 mutation we an RB49 in the the of the RB49 was with the resulting was in of the of of the RB49 in E. the into the E. coli groEL44 which is for RB49 ε22 and used this in a marker rescue it was whether the wild type corresponding to ε22 be in RB49 we with an of groEL44 with purified from the of was into and to RB49 ε22 was on these of and of was on the mutant at to the of RB49 wild type or most of the than of from to The marker rescue was for two of these that the of wild type was not to of these was for by the marker rescue with of and we of RB49 wild type we to a a the RB49 wild type that to the ε22 mutation and which we have cognate). the to with the ε22 the experiments that the a the of both the T4 which an mutation in and mutant to propagate on their wild type which a we that suppresses the temperature-sensitive phenotype of the E. coli groES42 as was shown with the T4 der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google Scholar). the of the gene, it was into tested the resulting for a of RB49 that on the of on but not on the host. that of all the RB49 RB49 was of growth on the it was RB49 the growth of RB49 but of the wild type RB49 with that the the wild type that to the RB49 ε22 and The predicted sequence of the RB49 is shown in encodes a residue protein with a predicted of and a of is 34% identical and 55% similar at the sequence level to T4 Gp31 1999; PubMed Google Scholar). The ε22 mutation is a resulting in the of a to at Gp31 GroES have this residue in their mobile with Gp31, the predicted mobile loop of CocO is longer than that of GroES and the and the hydrophobic at in CocO to Gp31, CocO encodes the loop of in the at of both features the other GroES cochaperonin J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar, A. Georgopoulos C. 1999; Google Scholar). of T4 Gp31 has to the that these in a in the J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar). this a better of the capsid protein, which is at the of the by the of the Gp31, and CocO a of in between the two but in GroES and the of its cochaperonin the structure of Gp31, this an extra loop from the of the Gp31 J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar). of the RB49 mutation that it is in a to the corresponding protein be than wild type CocO in the host. The phenotype of this mutation that the of CocO are for its correct The CocO wild type protein was and purified from the for Similarly, the mutant protein was and purified from the Both proteins at as by of the purified protein by The of both proteins an of with their heptameric not To whether the purified CocO wild type and proteins are and of with their GroEL we in vitro folding with denatured citrate synthase. it was that the correct in vitro folding of citrate requires both the GroEL and GroES proteins J. R. R. T. 1991; PubMed Scopus Google Scholar, Landry S.J. Gierasch L.M. Sci. PubMed Scopus Google Scholar). shown in the CocO cochaperonin is of wild type GroEL in the folding of denatured citrate synthase. are the that the wild type CocO protein assist the mutant protein in citrate the in of bacteriophage RB49 to propagate on the groEL44 mutant host and the mutant protein the of the mutant protein to citrate in agreement with the in that the bacteriophage RB49 mutant on the groEL44 mutant host experiments have been using various with the same results not to bacteriophage phenotype the mutant protein was of the wild type GroEL protein in citrate is not bacteriophage RB49 can form on wild type at high interaction between GroEL wild type and at at high citrate although a substrate is is not as to as the RB49 major capsid protein. the of the GroEL chaperonin and its GroES cochaperonin have been both as a and as of their interaction with other and their are not G. Nature. 1997; 388: 720-723Crossref PubMed Scopus (79) Google Scholar, K. Otwinowski Z. Hegde R. Boisvert D.C. Joachimiak A. Horwich A.L. Sigler P.B. Nature. 1994; 371: 578-586Crossref PubMed Scopus (1191) Google Scholar, 8Hunt J.F. Weaver A.J. Landry S.J. Gierasch L. Deisenhofer J. Nature. 1996; 379: 37-45Crossref PubMed Scopus (402) Google Scholar, 11Xu Z. Horwich A.L. Sigler P.B. Nature. 1997; 388: 741-750Crossref PubMed Scopus (1038) Google Scholar). The that GroES with GroEL has been to a residue of GroES. so-called mobile although in a structure upon binding to GroEL (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google Scholar). the the that GroES with GroEL is with a hydrophobic in the of its mobile loop (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google Z. Horwich A.L. Sigler P.B. Nature. 1997; 388: 741-750Crossref PubMed Scopus (1038) Google Scholar). The of other to both the binding of GroES to GroEL and to the subsequent of the are that to be is whether GroES binding to the ring of GroEL can GroES is to the cis ring and whether binding be required for the release of from the cis ring of GroEL. and have the bacteriophage T4-encoded Gp31 protein of as essential for the correct folding of of the major bacteriophage capsid protein F. G. J. Biol. PubMed Scopus Google Scholar, Black L.W. J. Biol. Full Text PDF PubMed Google Scholar, B. J. PubMed Google Scholar, J. PubMed Google Scholar). the of a functional the capsid protein in on the E. coli F. G. J. Biol. PubMed Scopus Google Scholar). The that mutations of the bacteriophage T4 by with the of Gp31 to the that Gp31 as a of the correct folding of by GroEL (14Keppel F. Lipinska B. Ang D. Georgopoulos C. Gene ( Amst. ). 1990; 90: 19-25Crossref Scopus (27) Google Scholar, C. Ang D. K. A. Georgopoulos C. in and Scholar) the that the GroES and Gp31 proteins little sequence identity Refs. F. Lipinska B. Ang D. Georgopoulos C. Gene ( Amst. ). 1990; 90: 19-25Crossref Scopus (27) Google Scholar, 15Nivinskas R. Black L.W. Gene ( Amst. ). 1988; 73: 251-257Crossref PubMed Scopus (18) Google Scholar, 16Koonin E.V. van der Vies S. Trends Biochem. Sci. 1995; 20: 14-15Abstract Full Text PDF PubMed Scopus (25) Google Scholar). Gp31 is a cochaperonin for it for GroES in protein binds GroEL, and its as GroES and suppresses the temperature-sensitive phenotype mutations der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google Scholar). Gp31, and not can assist in folding in der Vies S.M. Georgopoulos C. Nature. 1994; PubMed Scopus Google Scholar, Black L. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar). is the of Gp31 that it from et al. J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar) structural features that distinguish Gp31 from GroES and all of the other mobile loop is longer with that of GroES (10Landry S.J. Zeilstra-Ryalls J. Fayet O. Georgopoulos C. Gierasch L.M. Nature. 1993; 364: 255-258Crossref PubMed Scopus (212) Google S.J. A. Georgopoulos C. van der Vies S. Proc. Natl. Acad. Sci. U. S. A. 1996; PubMed Scopus Google Scholar), this in the formation of a structure over GroEL. a in the better Gp23, a substrate at A mobile loop is also a of the CocO cochaperonin which is one longer than that of Gp31. The ε22 mutation that results in an interaction with the mutant chaperonin this extra residue in have shown that Gp31 and not form a in vitro A. van der Vies S. F. A. Landry S.J. Georgopoulos C. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). CocO and from a similar which is by the Q36R substitution of The of the wild type to interact in be vitro they are to citrate synthase. the of mutant proteins that functions in for bacteriophage RB49 also citrate in this it is that the mutation of bacteriophage T4 that is of interaction with is the T4 an substitution in mobile loop A. Georgopoulos C. 1999; Google Scholar). substitution results in a hydrophobic for in the first of the hydrophobic of Gp31. the Q36R substitution in CocO's mobile loop it to interact better with as by the that on groEL44 at but not at RB49 at both and The Q36R substitution is two to the hydrophobic and the by a than the substitution of Gp31. et al. J.F. van der Vies S.M. L. Deisenhofer J. Cell. 1997; 90: Full Text Full Text PDF PubMed Scopus Google Scholar) also the of a residue at in GroES and its residue into the central of GroES and the the for substrate is from the in both Gp31 and the CocO cochaperonin that both Gp31 and CocO from GroES and the other is the of a structure at the of the GroES this allow Gp31 and CocO to a substrate, as both Gp31 and CocO an extra loop at their that is in GroES and all other the Gp31 this extra loop is of the it is not it in Gp31 and CocO cochaperonin of this loop Gp31 for but not for its E. coli protein A. of Scholar). the various structural between the cochaperonin and the the that the of the cochaperonin to the capsid protein The an structure of subunits C. A. E. A. R. U. J. Biol. 1991; PubMed Scopus Google Scholar). If one a of bacteriophage subunits the at for to the capsid protein also has a to as by the formation of in the of Gp31 F. G. J. Biol. PubMed Scopus Google Scholar). of GroEL binding and release for its be that the folding is than that of the and of is that the cochaperonin can bind to the ring of GroEL than GroES in the release of from the cis the and of the be specifically for of these are and they all to the correct and of this between Gp31 and GroES it is that the cochaperonin is of folding all of E. coli's essential GroEL either Gp31 or CocO can substitute for GroES in and C. Gp31 all features for the correct folding of experiments are as experiments, to the Gp31 features that of this Here, we have the structure and function of the Gp31 protein of an bacteriophage and its with of the T4 and the E. coli There is extremely little sequence between bacteriophage T4 Gp31 and E. coli although their cochaperonin functions are very sequence is between GroES and RB49 CocO in the of these Gp31 are from we that their to the GroES protein will become an analysis of Gp31 also the and that are for function and and for their in the for and for of the