Protein Homeostasis in Mitochondria: Chaperones and Proteases of the Mitochondrial Matrix Prof. Wolfgang Voos
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1 Protein Homeostasis in Mitochondria: Chaperones and Proteases of the Mitochondrial Matrix Institute for Biochemistry and Molecular Biology (IBMB) University of Bonn, Germany 1 Mitochondrial function: Principles of mitochondrial protein homeostasis Energy production (synthesis of ATP) Metabolic pathways (TCA cycle, β-oxidation) Biosynthesis (amino acids, heme, Fe/S) Cellular regulation (apoptosis) Biogenesis and propagation Maintenance of enzymatic functions 2 Cytosolic protein synthesis and subsequent import Protein quality control: folding, assembly and degradation Enzymatic mediators of mitochondrial protein homeostasis Protein folding Protein import Proteolysis Chaperones: Hsp100 (2x) Hsp90 Hsp70 (3x) Hsp60 Proteases: Pim1/LON ClpP AAA (2x) HtrA2 Assembly of protein complexes Protein biosynthesis 3 Reactivation of protein aggregates Stabilisation under stress conditions 1
2 Protein quality control in the matrix compartment 4 Situation in yeast (S. cerevisiae) Question and approaches How can mitochondria protect their functional integrity under normal and stress conditions? Hypothesis: to avoid accumulation of protein aggregates, inactive and/or denatured proteins have to be specifically recognized and removed by proteolysis 1. Which proteins are affected? Quantitative analysis of mitochondrial protein turnover 2. How are damaged polypeptides distinguished from intact enzymes? Biochemical characterization of proteolytic mechanisms 5 In organello degradation assay Import of urea-denatured preproteins into purified intact mitochondria Incubate at different experimental conditions to follow degradation kinetics Separate mitochondrial proteins by SDS-PAGE, detect and quantify reporter proteins Pim1/LON mediates the degradation of imported reporter proteins 6 2
3 The mitochondrial protease Pim1 Pim1 belongs to the AAA+ protein family (ATPases associated with a variety of cellular activities) Mammalian homolog is named LON Pim1 has an ATP-dependent serine protease activity 7 subunits of Pim1 form a large, ring-shaped protein complex with a pore in the center In addition to the proteolytic domain, Lon-type proteases contain also a N-terminal chaperone-like domain 7 from: Stahlberg et al., (1999) PNAS Degradation rates of imported reporter proteins 8 Fusion proteins with short N-terminal extensions can not be degraded completely by the Pim1 protease Resistant proteins prevent degradation of substrate proteins by a competitive inhibition mechanism Effect of the folding state on mitochondrial proteolysis Mitochondrial degradation assay: 9 Proteolysis of proteins with a folded C-terminal domain results in the formation of a proteolytic fragment of a characteristic size 3
4 Biochemical properties of the protease Pim1 Degradation of reporter protein with long N-terminal segment: 10 Destabilization of the folded DHFR domain allows complete degradation Pim1 has a low substrate unfolding activity Substrate selectivity of the mitochondrial protease Pim1 Native protein with folded domains Protein with exposed segment Unfolded (destabilized) conformation No degradation Partial degradation Complete degradation Unstructured segment of aa required for initiation of proteolysis 2. Absent or low intrinsic unfolding capacity 2D gel 12 4
5 Proteomic analysis of the mitochondrial protein turnover 13 WT pim1d Working hypothesis: endogenous substrate proteins have a higher abundance in protease-deficient mitochondria Quantitative analysis of protein spot pattern Differences in protein amount between WT and pim1δ mitochondria: 14 A specific subgroup of mitochondrial proteins is accumulating in protease-deficient mitochondria at normal temperature conditions (30 C) Proteolysis in organello 15 The proteins Lys4, Yjl200c, Ilv1 and Lsc1 are degraded by the protease Pim1 after import into the mitochondrial matrix 5
6 Pim1 substrates Protein/gene symbol Lys4/YDR234W Yjl200/YJL200C Lsc1/YOR142W Lsc2/YGR244C Ilv1/YER086W Biological function Homoaconitase Lysine biosynthesis Fe/S cluster as cofactor Aconitase/IPM isomerase family Aconitate hydratase activity Biological process unknown possible function in TCA cycle Fe/S cluster as cofactor Aconitase family Succinyl-CoA ligase, α chain TCA cycle Belongs to the succinate/malate CoA ligase α subunit family Succinyl-CoA ligase, β chain TCA cycle Belongs to the succinate/malate CoA ligase β subunit family Threonine deaminase Isoleucin biosynthesis Pyridoxal phosphate as cofactor Serine/threonine dehydratase family 16 Ilv2/YMR108W Acetolactate synthase Valine and isoleucine biosynhesis Thiamine pyrophoshate as cofactor TPP enzyme family Proteins with a complex tertiary structure (cofactors) are prone to proteolysis by Pim1 Degradation in Fe/S cluster assembly mutants Defects in mitochondrial Fe/S cluster assembly leads to enhanced degradation of Pim1 substrate proteins containing Fe/S cofactors 17 Proteomic analysis of mitochondrial protein dynamics under oxidative stress 1. Treatment of isolated intact mitochondria with different oxidative stressors 2. Separation of mitochondrial proteins by 2D-PAGE H 2O 2 Menadione (superoxide generation) Antimycin A (respiratory chain inhibitor) Quantitative spot pattern analysis reveals ROS-specific protein degradation 4. Identification of candidate substrates proteins by mass spectroscopy 100 kda 10 2D-PAGE ph
7 Protein degradation in ROS stressed mitochondria Untreated 19 ROS stress Quantitative changes in the mitochondrial proteome Oxididative phosphorylation: Metabolic enzymes: Chaperones/biogenesis: 20 House-keeping enzymes show only minor changes upon oxidative stress Proteins with Fe/S cluster cofactors Relative changes in protein abundance: Amounts of degraded polypeptides: Fe/S cofactor enzymes are particularly sensitive to ROS-induced proteolysis 21 Aco1: aconitase Ilv3: dihydroxy-acid dehydratase Lys4: homoaconitase Sdh2: succinate dehydrogenase 7
8 In organello degradation of imported Ilv3 ROS-sensitivity Pim1-dependence Ilv3 is degraded in mitochondrial matrix by the protease Pim1 22 Ilv3 (dihydroxyacid dehydratase): Catalyzes third step in the common pathway leading to biosynthesis of branched-chain amino acids localized in the matrix Deletion mutant is viable High homology to E. coli enzyme containing an Fe/S cluster ROS-protective enzymes Proteins with a high affinity to oxygen and related molecules are highly susceptible to modification and degradation 23 Ccp1: cytochrome c peroxidase Sod2: Mn-superoxide dismutase Yhb1: nitric oxide oxidoreductase Prx1: peroxiredoxin Prx1 (peroxiredoxin) Prx1(1-Cys Prx) : Thioredoxin peroxidase activity Role in reduction of hydroperoxides Localized in the matrix Deletion mutant viable In vitro degradation of imported Prx1: Prx1 2D spot analysis: 24 Mitochondrial Prx1 is quantitatively transformed into a overoxidised form by ROS-treatment 8
9 Effect of oxidative stress on protein aggregation Aggregated aconitase after 15 min heat shock: 25 The effects of heat and oxidative stress on aggregation rates of aconitase are additive Identification of mitochondrial proteins affected by aggregation 15 min heat shock treatment of isolated mitochondria: Kgd1: a-ketoglutarate dehydrogenase Aco1: Aconitase Pox1: Fatty-acyl coenzyme A oxidase Ssc1: mitochondrial Hsp70 Ilv2: Acetolactate synthase Leu4: a-isopropylmalate synthase Gut2: Glycerol-3-phosphate dehydrogenase Hsp60: mitochondrial Chaperonin Lat1: Dihydolipoylamide acetyltransferase Ald4: Aldehyde dehydrogenase Kgd2: Dihydrolipoyl transsuccinylase Atp1: F 1F o-atpase, subunit a Atp2: F 1F o-atpase, subunit b Lsc2: Succinyl-CoA ligase, subunit b Pda1: Pyruvate dehydrogenase, subunit a Pdb1: Pyruvate dehydrogenase, subunit b 26 Enzyme activities of affected proteins Aconitase: Ketoglutarate dehydrogenase: Pyruvate dehydrogenase (control): Kinetics of aconitase inactivation: The efficiency of the TCA cycle in mitochondria is strongly reduced by protein aggregation 27 9
10 Energy dependence of mitochondrial protein aggregation Aggregation of Ilv2: The amount of aggregated polypeptides is affected by the energetic state (ATP level) 28 Aggregated Ilv2: Protective effects of the mitochondrial chaperone system Co-sedimenting chaperones: 29 Chaperones only slightly decrease protein aggregation Highest protective effect at normal temperature range The AAA+ protease Pim1/LON protects against aggregation Aggregation rates of Ilv2: Aggregation rates of Aco1: The proteolytical activity of Pim1 strongly influences the amount of aggregated polypeptides 30 10
11 Chaperones of the Hsp100/ClpB family Properties of Hsp78: Hsp78 belongs to the AAA+ protein family; Homologs of Hsp78 exist in bacteria (ClpB) and in the eukaryotic cytosol (Hsp104) Members of the family can protect proteins against aggregation under stress conditions Activity and oligomerisation is regulated by ATP Hsp100 proteins form large ring-shaped protein complexes consisting of 6 subunits 31 (Hypothetical model) Reversal of protein aggregation 32 Proteins with a destabilized folding state are disaggregated by the Hsp78/mtHsp70 system The chaperone system closely cooperates with the Pim1 protease in the removal of misfolded polypeptides Resistance to oxidative stress in vivo Protein expression levels after stress: Growth inhibition by oxidative stress: Chaperones AAA-proteases 33 Increased levels of mitochondrial PQC components Pim1 and Hsp78 protect cells against toxic effects of reactive oxygen species 11
12 Flow diagram of the mitochondrial protein quality control reaction Folded Oxidative stress Misfolded Aggregated 34 Degraded Thanks to Tom Bender Former coworkers: Ilka Lewrenz Birgit von Janowsky Catherina Baitzel Claudia Leidhold Dorothea Becker Tamara Major Ursula Seibold Karin Knapp Judith Richter Martin Krayl Katja Baitzel Yanfeng Li Uschi Gerken Nicole Rietzschel Nicole Zufall Collaboration partners: Financial support: Prof. G. Auburger (Uniklinik Frankfurt/Main) DFG priority program 1138 Prof. J. A. Bárcena (University of Córdoba, Spanien) Proteolysis in prokaryots Dr. S. Franken (Universität Bonn) DFG project support Prof. W. Kunz (Universität Bonn) Analysis of mitochondrial protein aggregation Dr. M. P. Mayer (ZMBH, Heidelberg) 35 Prof. N. Pfanner (Universität Freiburg) 36 12
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