ATP induces large quaternary rearrangements in a cage-like chaperonin structure

Saibil, Helen R.; Dong, Zheng; Roseman, Alan M.; Hunter, Allison S.; Watson, G. M.; Chen, S.; Mauer, Arlene auf der; O'Hara, B.P.; Wood, Steve; Mann, Nicholas H.; Barnett, Leslie; Ellis, R. John

doi:10.1016/0960-9822(93)90176-o

Cited by 205 publications

(108 citation statements)

References 42 publications

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“…Our data support the notion that the role of ATP hydrolysis is to act as a switch between two conformational states (3,23): one (the ADP-bound form) has the ability to bind unfolded target proteins with high affinity (i.e., less than 0.1 rLM), while the other (the ATP-bound form) cannot. Structural differences between chaperonin forms have already been noted from electron microscopic analyses (16,41).…”

Section: Discussionmentioning

confidence: 97%

Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates.

Melki¹,

Cowan²

1994

Mol. Cell. Biol.

107

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In the cytoplasm of eukaryotes, the folding of actins and tubulins is facilitated via interaction with a heteromeric toroidal complex (cytoplasmic chaperonin). The folding reaction consists of the formation of a binary complex between the unfolded target protein and the chaperonin, followed by the ultimate release of the native polypeptide in an ATP-dependent reaction. Here we show that the mitochondrial chaperonin (cpn6O) and the cytoplasmic chaperonin both recognize a range of target proteins with different relative affinities; however, the cytoplasmic chaperonin shows the highest affinity for intermediates derived from unfolded tubulins and actins. These high-affinity actin and tubulin folding intermediates are distinct from the "molten globule" intermediates formed by noncytoskeletal target proteins in that they form relatively slowly. We show that the interaction between cytoplasmic chaperonin and unfolded target proteins depends on the chaperonin being in its ADP-bound state and that the release of the target protein occurs after a transition of the chaperonin to the ATP-bound state. Our data suggest a model in which ATP hydrolysis acts as a switch between conformational forms of the cytoplasmic chaperonin that interact either strongly or weakly with unfolded substrates.The biological function of most, if not all, proteins depends critically upon their three-dimensional structure. Although the information contained in the linear sequence of amino acids is thought to be sufficient. to specify this structure (2, 24), the correct folding of many proteins is not a spontaneous process under physiological conditions; rather, there is a requirement for interaction with a class of proteins or protein complexes known as molecular chaperones (reviewed in references 14, 18, and 39). In particular, one class of chaperones (typified by GroEL in prokaryotes) consist of multisubunit toroidal ring assemblies and are believed to function by providing a sequestered environment in which aberrant folding and aggregation are prevented; the correctly folded polypeptide is ultimately discharged in an Mg-ATP-dependent reaction. These toroidal structures are termed chaperonins (6,10,19,28,34,35,46). Actin and tubulin are the major soluble cytoplasmic proteins in eukaryotic cells and are the subunits from which actin filaments and microtubules are assembled. The folding of actins, tubulins, and actin-and tubulin-related proteins is facilitated by a chaperonin (15-17, 31, 49) that differs from its prokaryotic and mitochondrial homologs in that it is heteromeric: the multisubunit toroidal structure is assembled from eight different (though related) polypeptides (15, 38), one of which is the t-complex polypeptide TCP-1 (27, 42). As is the case for other chaperonins, the cytoplasmic chaperonin forms a stable binary complex with unfolded target polypeptides in the absence of Mg-ATP, and the hydrolysis of Mg-ATP is absolutely required for the generation of folded proteins (15-17). However, an important difference exists between the mecha...

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Section: Discussionmentioning

confidence: 97%

Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates.

Melki¹,

Cowan²

1994

Mol. Cell. Biol.

107

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“…The higher number of C-terminal Gly-Gly-Met repeats observed for sea anemone Hsp60 is intriguing. The structure and function of this motif is not fully elucidated (Gupta 1995;Sanchez et al 1999); however, it could potentially alter the internal cavity of the GroEL heptameric ring at the level of the equatorial domain (Saibil et al 1993;Thiyagarajan et al 1996). We also note the replacement of a conserved Tyr by His in one of the eight essential hydrophobic amino acids involved in polypeptide binding in sea anemone Hsp60.…”

Section: Discussionmentioning

confidence: 99%

Increased light intensity induces heat shock protein Hsp60 in coral species

Chow

Ferrier‐Pagés

Khalouei

et al. 2009

Cell Stress and Chaperones

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The effect of increased light intensity and heat stress on heat shock protein Hsp60 was examined in two coral species using a branched coral and a laminar coral, selected for their different resistance to environmental perturbation. Transient Hsp60 induction was observed in the laminar coral following either light or thermal stress. Sustained induction was observed when these stresses were combined. The branched coral exhibited comparatively weak transient Hsp60 induction after heat stress and no detectable induction following light stress, consistent with its susceptibility to bleaching in native environments compared to the laminar coral. Our observations also demonstrate that increased light intensity and heat stress exhibited a greater negative impact on the photosynthetic capacity of environmentally sensitive branched coral than the more resistant laminar coral. This supports a correlation between stress induction of Hsp60 and (a) ability to counter perturbation of photosynthetic capacity by light and heat stress and (b) resistance to environmentally induced coral bleaching.

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“…This interaction also induces a number of changes in the morphology of GroEL, some of them similar to those produced by the interaction of GroEL with ATP [29]. Electron microscopy of the complexes formed under the conditions of the functional assay described in Fig.…”

Section: Structure Of the Groelgroes Complexes Built Up In The Presenmentioning

confidence: 99%

The formation of symmetrical GroEL‐GroES complexes in the presence of ATP

et al. 1994

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The incubation of chaperonins cpn60 (GroEL) and cpnl0 (GroES) from E. coli in the presence of Mg-ATP and KC1 generates the formation, as revealed by electron microscopy, of GroEL-GroES complexes with a symmetrical shape in which one toroidal GroES oligomer is bound to each end of the tetradecameric GroEL aggregate (1: 2 GroEL : GroES oligomer molar ratio). The symmetrical complexes are not observed in the presence of ADP or the non-hydrolyzable ATP analog, ATPyS, where only asymmetrical complexes (1: 1 GroEL: GroES oligomer molar ratio) are formed.These results suggest that ATP hydrolysis is required for the formation of symmetrical complexes.

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ATP induces large quaternary rearrangements in a cage-like chaperonin structure

Cited by 205 publications

References 42 publications

Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates.

Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates.

Increased light intensity induces heat shock protein Hsp60 in coral species

The formation of symmetrical GroEL‐GroES complexes in the presence of ATP

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