Research

The function of molecular chaperones in the cell – Folding and remodeling of proteins

Proteins are dynamic macromolecules. In all living cells molecular chaperones play critical roles in remodeling protein structure — assisting de novo protein folding, preventing protein aggregation, facilitating assembly and disassembling of protein complexes and modulating protein:protein interactions. We focus on the most versatile of molecular chaperones – Hsp70. Unlike many molecular chaperones systems, components of Hsp70-based chaperone machines are encoded by sizeable multigene families. In particular, J-domain proteins, cochaperone partners of Hsp70, orchestrate the ability of Hsp70s to participate in a wide array of complex and diverse biological processes.

Cartoon of adenine nucleotide dependent cycle of Hsp70 interaction with substrate polypeptide.
Adenine nucleotide dependent cycle of Hsp70 interaction with substrate polypeptide.

Although the basic biochemical principles behind the cycle of interaction of Hsp70 with substrate are well established, how this machinery is optimized for productive interaction with diverse polypeptide substrates present in the cell remains largely unknown. Our goal is to understand how this remarkable functional diversity is achieved. We take a “mechanistic genetic approach – iterative use of genetic and biophysical/biochemical techniques – using Saccharomyces cerevisiae as a model system.

Two structurally similar, yet functionally distinct, J-domain proteins

Cartoon of Evolution of Hsp70 systems in cytosolic ribosome-associated protein folding and mitochondrial Fe/S cluster biogenesis.
Evolution of Hsp70 systems in cytosolic ribosome-associated protein folding and mitochondrial Fe/S cluster biogenesis. Specialized Hsp70s Ssb and Ssq1 function with single J-domain protein cochaperone.

The presence of two functionally distinct J-domain proteins partnering with the same Hsp70 in the same cellular compartment, provides a system for genetic and biochemical probing of the tuning of the Hsp70 cycle behind its accommodation of diverse substrates. We isolate and analyze suppressor variants that can overcome the absence of the essential Sis1 J-domain protein. Thus far, we have isolated suppressors of both Ydj1, a structurally related J-domain protein, and Hsp70 itself.

Conserved, yet specialized, Hsp70 chaperone systems

We exploit two specialized systems in which not only the J-domain protein, but also, due to an Hsp70 gene duplication during fungal evolution, the Hsp70 are highly specialized. These specialized systems allow us to not only probe Hsp70 chaperone system function in specific cellular functions, but uncover general principles of chaperone function and evolution.

Cartoon of Substitutions in substrate binding domain of Hsp70 allows growth in the absence of J-domain protein Sis1.
Substitutions in substrate binding domain of Hsp70 allows growth in the absence of J-domain protein Sis1. Suppressor substitutions R444 and K446 (blue) affect rate of lid closure.

Specialized ribosome-associated molecular chaperones: During their synthesis on ribosomes, proteins are particularly susceptible to aggregation, which prohibits their proper folding. We are studying ribosome-associated molecular chaperones that are tethered near the site from which the nascent chain exits the ribosome tunnel. Our goal is to determine how this chaperone and associated factors aid in folding of newly synthesized proteins and functionally integrate with other molecular chaperone systems.

Conserved system for assembly of Fe/S clusters and their insertion into proteins: Mitochondria contain a complex system for assembly of Fe/S metal centers and their insertion into proteins. A specialized J-protein/Hsp70 molecular chaperone pair is a critical part of this system, interacting specifically with the scaffold protein on which clusters are first built and facilitating cluster transfer. We aim to unravel the mechanism of action of this dedicated chaperone system and the regulation of expression of its components.